US20040259247A1 - Rna interference mediating small rna molecules - Google Patents

Rna interference mediating small rna molecules Download PDF

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Publication number
US20040259247A1
US20040259247A1 US10/433,050 US43305004A US2004259247A1 US 20040259247 A1 US20040259247 A1 US 20040259247A1 US 43305004 A US43305004 A US 43305004A US 2004259247 A1 US2004259247 A1 US 2004259247A1
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Prior art keywords
target
rna
gene
cell
sirna
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US10/433,050
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English (en)
Inventor
Thomas Tuschl
Sayda Elbashir
Winfried Lendeckel
Matthias Wilm
Reinhard Luhrmann
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Max Planck Gesellschaft zur Foerderung der Wissenschaften eV
University of Massachusetts UMass
Whitehead Institute for Biomedical Research
Massachusetts Institute of Technology
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First worldwide family litigation filed litigation Critical https://patents.darts-ip.com/?family=40529293&utm_source=google_patent&utm_medium=platform_link&utm_campaign=public_patent_search&patent=US20040259247(A1) "Global patent litigation dataset” by Darts-ip is licensed under a Creative Commons Attribution 4.0 International License.
Priority claimed from PCT/US2001/010188 external-priority patent/WO2001075164A2/en
Application filed by Individual filed Critical Individual
Priority to US10/433,050 priority Critical patent/US20040259247A1/en
Assigned to MAX-PLANCK-GESELLSCHAFT ZUR FORDERUNG DER WISSENSCHAFTEN E. V., EUROPAISCHES LABORATORIUM FUR MOLEKULARBIOLOGIE (EMBL) reassignment MAX-PLANCK-GESELLSCHAFT ZUR FORDERUNG DER WISSENSCHAFTEN E. V. ASSIGNMENT OF ASSIGNORS INTEREST (SEE DOCUMENT FOR DETAILS). Assignors: TUSCHL, THOMAS, WILM, MATTHIAS, LUHRMANN, REINHARD
Priority to US10/832,257 priority patent/US20050026278A1/en
Publication of US20040259247A1 publication Critical patent/US20040259247A1/en
Priority to US11/142,866 priority patent/US20050234007A1/en
Priority to US11/142,865 priority patent/US20050234006A1/en
Priority to US11/634,138 priority patent/US20080269147A1/en
Priority to US11/634,129 priority patent/US20070093445A1/en
Priority to US12/260,443 priority patent/US20090155174A1/en
Assigned to MAX-PLANCK-GESELLSCHAFT ZUR FOERDERUNG DER WISSENSCHAFTEN. E.V. reassignment MAX-PLANCK-GESELLSCHAFT ZUR FOERDERUNG DER WISSENSCHAFTEN. E.V. ASSIGNMENT OF ASSIGNORS INTEREST (SEE DOCUMENT FOR DETAILS). Assignors: ELBASHIR, SAYDA, LENDECKEL, WINFRIED
Priority to US12/537,602 priority patent/US8372968B2/en
Priority to US12/537,632 priority patent/US20100010207A1/en
Assigned to MAX-PLANCK-GESELLSCHAFT ZUR FOERDERUNG DER WISSENSCHAFTEN E.V. reassignment MAX-PLANCK-GESELLSCHAFT ZUR FOERDERUNG DER WISSENSCHAFTEN E.V. ASSIGNMENT OF ASSIGNORS INTEREST (SEE DOCUMENT FOR DETAILS). Assignors: EUROPAEISCHES LABORATORIUM FUER MOLEKULARBIOLOGIE (EMBL)
Priority to US12/591,829 priority patent/US8853384B2/en
Priority to US12/683,070 priority patent/US8933044B2/en
Priority to US12/683,081 priority patent/US8362231B2/en
Priority to US12/794,071 priority patent/US8765930B2/en
Priority to US12/819,444 priority patent/US8796016B2/en
Priority to US12/834,311 priority patent/US8445237B2/en
Priority to US12/835,086 priority patent/US8778902B2/en
Priority to US12/838,786 priority patent/US8329463B2/en
Priority to US12/879,300 priority patent/US8993745B2/en
Priority to US12/897,374 priority patent/US8895718B2/en
Assigned to UNIVERSITY OF MASSACHUSETTS, MASSACHUSETTS INSTITUTE OF TECHNOLOGY, WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH reassignment UNIVERSITY OF MASSACHUSETTS ASSIGNMENT OF ASSIGNORS INTEREST (SEE DOCUMENT FOR DETAILS). Assignors: MAX-PLANCK-GESELLSCHAFT ZUR FORDERUNG DER WISSENSCHAFTEN E.V.
Assigned to UNIVERSITY OF MASSACHUSETTS, MAX-PLANCK-GESELLSCHAFT ZUR FORDERUNG DER WISSENSCHAFTEN E.V., WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH, MASSACHUSETTS INSTITUTE OF TECHNOLOGY reassignment UNIVERSITY OF MASSACHUSETTS CORRECTIVE ASSIGNMENT TO CORRECT THE OMISSION OF ASSIGNEE, MAX-PLANCK-GESELLSCHAFT ZUR FORDERUNG DER WISSENSCHAFTEN E.V., PREVIOUSLY RECORDED ON REEL 026583 FRAME 0614. ASSIGNOR(S) HEREBY CONFIRMS THE ASSIGNMENT. Assignors: MAX-PLANCK-GESELLSCHAFT ZUR FORDERUNG DER WISSENSCHAFTEN E.V.
Priority to US13/725,262 priority patent/US8895721B2/en
Priority to US14/476,465 priority patent/US9567582B2/en
Priority to US15/388,681 priority patent/US10633656B2/en
Priority to US16/805,072 priority patent/US20200299693A1/en
Abandoned legal-status Critical Current

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Definitions

  • RNA interference was coined after the discovery that injection of dsRNA into the nematode C. elegans leads to specific silencing of genes highly homologous in sequence to the delivered dsRNA (Fire et al., 1998). RNAi was subsequently also observed in insects, frogs (Oelgeschlager et al., 2000), and other animals including mice (Svoboda et al., 2000; Wianny and Zernicka-Goetz, 2000) and is likely to also exist in human.
  • RNAi is closely linked to the post-transcriptional gene-silencing (PTGS) mechanism of co-suppression in plants and quelling in fungi (Catalanotto et al., 2000; Cogoni and Macino, 1999; Dalmay et al., 2000; Ketting and Plasterk, 2000; Mourrain et al., 2000; Smardon et al., 2000) and some components of the RNAi machinery are also necessary for post-transcriptional silencing by co-suppression (Catalanotto et al., 2000; Dernburg et al., 2000; Ketting and Plasterk, 2000).
  • PTGS post-transcriptional gene-silencing
  • transgenes can also lead to transcriptional gene silencing via RNA-directed DNA methylation of cytosines (see references in Wassenegger, 2000). Genomic targets as short as 30 bp are methylated in plants in an RNA-directed manner (Pelissier, 2000). DNA methylation is also present in mammals.
  • RNAi and co-suppression appear to be protection of the genome against invasion by mobile genetic elements such as retro-transposons and viruses which produce aberrant RNA or dsRNA in the host cell when they become active (Jensen et al, 1999; Ketting et al., 1999; Ratcliff et al., 1999; Tabara et al., 1999).
  • Specific mRNA degradation prevents transposon and virus replication although some viruses are able to overcome or prevent this process by expressing proteins that suppress PTGS (Lucy et al., 2000; Voinnet et al., 2000).
  • RNA molecules of similar size also accumulate in plant tissue that exhibits PTGS (Hamilton and Baulcombe, 1999).
  • siRNAs short interfering RNAs
  • the siRNAs may also be important tools for transcriptional modulating, e.g. silencing of mammalian genes by guiding DNA methylation.
  • the object underlying the present invention is to provide novel agents capable of mediating target-specific RNA interference or other target-specific nucleic acid modifications such as DNA methylation, said agents having an improved efficacy and safety compared to prior art agents.
  • each RNA strand has a length from 19-25, particularly from 19-23 nucleotides, wherein said RNA molecule is capable of mediating target-specific nucleic acid modifications, particularly RNA interference and/or DNA methylation.
  • at least one strand has a 3′-overhang from 1-5 nucleotides, more preferably from 1-3 nucleotides and most preferably 2 nucleotides.
  • the other strand may be blunt-ended or has up to 6 nucleotides 3′ overhang.
  • the RNA molecule is preferably a synthetic RNA molecule which is substantially free from contaminants occurring in cell extracts, e.g. from Drosophila embryos. Further, the RNA molecule is preferably substantially free from any non-target-specific contaminants, particularly non-target-specific RNA molecules e.g. from contaminants occuring in cell extracts.
  • the invention relates to the use of isolated double-stranded RNA molecules, wherein each RNA strand has a length from 19-25 nucleotides, for mediating, target-specific nucleic acid modifications, particularly RNAi, in mammalian cells, particularly in human cells.
  • each strand of the RNA molecule has a length from 20-22 nucleotides (or 20-25 nucleotides in mammalian cells), wherein the length of each strand may be the same or different.
  • the length of the 3′-overhang reaches from 1-3 nucleotides, wherein the length of the overhang may be the same or different for each strand.
  • the RNA-strands preferably have 3′-hydroxyl groups.
  • the 5′-terminus preferably comprises a phosphate, diphosphate, triphosphate or hydroxyl group.
  • the most effective dsRNAs are composed of two 21 nt strands which are paired such that 1-3, particularly 2 nt 3′ overhangs are present on both ends of the dsRNA.
  • the target RNA cleavage reaction guided by siRNAs is highly sequence-specific. However, not all positions of a siRNA contribute equally to target recognition. Mismatches in the center of the siRNA duplex are most critical and essentially abolish target RNA cleavage. In contrast, the 3′ nucleotide of the siRNA strand (e.g. position 21) that is complementary to the single-stranded target RNA, does not contribute to specificity of the target recognition. Further, the sequence of the unpaired 2-nt 3′ overhang of the siRNA strand with the same polarity as the target RNA is not critical for target RNA cleavage as only the antisense siRNA strand guides target recognition. Thus, from the single-stranded overhanging nucleotides only the penultimate position of the antisense siRNA (e.g. position 20) needs to match the targeted sense mRNA.
  • the double-stranded RNA molecules of the present invention exhibit a high in vivo stability in serum or in growth medium for cell cultures.
  • the 3′-overhangs may be stablized against degradation, e.g. they may be selected such that they consist of purine nucleotides, particularly adenosine or guanosine nucleotides.
  • substitution of pyrimidine nucleotides by modified analogues e.g. substitution of uridine 2 nt 3′ overhangs by 2′-deoxythymidine is tolerated and does not affect the efficiency of RNA interference.
  • the absence of a 2′ hydroxyl significantly enhances the nuclease resistance of the overhang in tissue culture medium.
  • the RNA molecule may contain at least one modified nucleotide analogue.
  • the nucleotide analogues may be located at positions where the target-specific activity, e.g. the RNAi mediating activity is not substantially effected, e.g. in a region at the 5′-end and/or the 3′-end of the double-stranded RNA molecule.
  • the overhangs may be stabilized by incorporating modified nucleotide analogues.
  • O- and N-alkylated nucleotides e.g. N6-methyl adenosine are suitable.
  • the 2′OH-group is replaced by a group selected from H, OR, R, halo, SH, SR, NH 2 , NHR, NR 2 or CN, wherein R is C 1 -C 6 alkyl, alkenyl or alkynyl and halo is F, Cl, Br or I.
  • R is C 1 -C 6 alkyl, alkenyl or alkynyl and halo is F, Cl, Br or I.
  • the phosphoester group connecting to adjacent ribonucleotides is replaced by a modified group, e.g. of phosphothioate group. It should be noted that the above modifications may be combined.
  • the sequence of the double-stranded RNA molecule of the present invention has to have a sufficient identity to a nucleic acid target molecule in order to mediate target-specific RNAi and/or DNA methylation.
  • the sequence has an identity of at least 50%, particularly of at least 70% to the desired target molecule in the double-stranded portion of the RNA molecule. More preferably, the identity is at least 85% and most preferably 100% in the double-stranded portion of the RNA molecule.
  • I is the identity in percent
  • n is the number of identical nucleotides in the double-stranded portion of the ds RNA and the target
  • L is the length of the sequence overlap of the double-stranded portion of the dsRNA and the target.
  • the identity of the double-stranded RNA molecule to the target sequence may also be defined including the 3′ overhang, particularly an overhang having a length from 1-3 nucleotides.
  • the sequence identity is preferably at least 50%, more preferably at least 70% and most preferably at least 85% to the target sequence.
  • the nucleotides from the 3′ overhang and up to 2 nucleotides from the 5′ and/or 3′ terminus of the double strand may be modified without significant loss of activity.
  • the double-stranded RNA molecule of the invention may be prepared by a method comprising the steps:
  • RNA molecules Methods of synthesizing RNA molecules are known in the art. In this context, it is particularly referred to chemical synthesis methods as described in Verma and Eckstein (1998).
  • the single-stranded RNAs can also be prepared by enzymatic transcription from synthetic DNA templates or from DNA plasmids isolated from recombinant bacteria.
  • phage RNA polymerases are used such as T7, T3 or SP6 RNA polymerase (Milligan and Uhlenbeck (1989)).
  • a further aspect of the present invention relates to a method of mediating target-specific nucleic acid modifications, particularly RNA interference and/or DNA methylation in a cell or an organism comprising the steps:
  • the contacting step (a) comprises introducing the double-stranded RNA molecule into a target cell, e.g. an isolated target cell, e.g. in cell culture, a unicellular microorganism or a target cell or a plurality of target cells within a multicellular organism.
  • a target cell e.g. an isolated target cell, e.g. in cell culture, a unicellular microorganism or a target cell or a plurality of target cells within a multicellular organism.
  • the introducing step comprises a carrier-mediated delivery, e.g. by liposomal carriers or by injection.
  • the method of the invention may be used for determining the function of a gene in a cell or an organism or even for modulating the function of a gene in a cell or an organism, being capable of mediating RNA interference.
  • the cell is preferably a eukaryotic cell or a cell line, e.g. a plant cell or an animal cell, such as a mammalian cell, e.g. an embryonic cell, a pluripotent stem cell, a tumor cell, e.g. a teratocarcinoma cell or a virus-infected cell.
  • the organism is preferably a eukaryotic organism, e.g. a plant or an animal, such as a mammal, particularly a human.
  • the target gene to which the RNA molecule of the invention is directed may be associated with a pathological condition.
  • the gene may be a pathogen-associated gene, e.g. a viral gene, a tumor-associated gene or an autoimmune disease-associated gene.
  • the target gene may also be a heterologous gene expressed in a recombinant cell or a genetically altered organism. By determinating or modulating, particularly, inhibiting the function of such a gene valuable information and therapeutic benefits in the agricultural field or in the medicine or veterinary medicine field may be obtained.
  • the dsRNA is usually administered as a pharmaceutical composition.
  • the administration may be carried out by known methods, wherein a nucleic acid is introduced into a desired target cell in vitro or in vivo.
  • Commonly used gene transfer techniques include calcium phosphate, DEAE-dextran, electroporation and microinjection and viral methods (Graham, F. L. and van der Eb, A. J. (1973) Virol. 52, 456; McCutchan, J. H. and Pagano, J. S. (1968), J. Natl. Cancer Inst. 41, 351; Chu, G. et al (1987), Nucl. Acids Res. 15, 1311; Fraley, R. et al. (1980), J. Biol. Chem.
  • the invention also relates to a pharmaceutical composition containing as an active agent at least one double-stranded RNA molecule as described above and a pharmaceutical carrier.
  • the composition may be used for diagnostic and for therapeutic applications in human medicine or in veterinary medicine.
  • the composition may be in form of a solution, e.g. an injectable solution, a cream, ointment, tablet, suspension or the like.
  • the composition may be administered in any suitable way, e.g. by injection, by oral, topical, nasal, rectal application etc.
  • the carrier may be any suitable pharmaceutical carrier.
  • a carrier is used, which is capable of increasing the efficacy of the RNA molecules to enter the target-cells. Suitable examples of such carriers are liposomes, particularly cationic liposomes.
  • a further preferred administration method is injection.
  • a further subject matter of the invention is a eukaryotic cell or a eukaryotic non-human organism exhibiting a target gene-specific knockout phenotype comprising an at least partially deficient expression of at least one endogeneous target gene wherein said cell or organism is transfected with at least one double-stranded RNA molecule capable of inhibiting the expression of at least one endogeneous target gene or with a DNA encoding at least one double stranded RNA molecule capable of inhibiting the expression of at least one endogeneous target gene.
  • the present invention allows a target-specific knockout of several different endogeneous genes due to the specificity of RNAi.
  • RNAi based knockout technologies the expression of an endogeneous target gene may be inhibited in a target cell or a target organism.
  • the endogeneous gene may be complemented by an exogeneous target nucleic acid coding for the target protein or a variant or mutated form of the target protein, e.g. a gene or a cDNA, which may optionally be fused to a further nucleic acid sequence encoding a detectable peptide or polypeptide, e.g. an affinity tag, particularly a multiple affinity tag.
  • Variants or mutated forms of the target gene differ from the endogeneous target gene in that they encode a gene product which differs from the endogeneous gene product on the amino acid level by substitutions, insertions and/or deletions of single or multiple amino acids.
  • the variants or mutated forms may have the same biological activity as the endogeneous target gene.
  • the variant or mutated target gene may also have a biological activity, which differs from the biological activity of the endogeneous target gene, e.g. a partially deleted activity, a completely deleted activity, an enhanced activity etc.
  • the complementation may be accomplished by coexpressing the polypeptide encoded by the exogeneous nucleic acid, e.g. a fusion protein comprising the target protein and the affinity tag and the double stranded RNA molecule for knocking out the endogeneous gene in the target cell.
  • This coexpression may be accomplished by using a suitable expression vector expressing both the polypeptide encoded by the exogeneous nucleic acid, e.g. the tag-modified target protein and the double stranded RNA molecule or alternatively by using a combination of expression vectors. Proteins and protein complexes which are synthesized de novo in the target cell will contain the exogeneous gene product, e.g. the modified fusion protein.
  • the nucleotide sequence encoding the exogeneous nucleic acid may be altered on the DNA level (with or without causing mutations on the amino acid level) in the part of the sequence which is homologous to the double stranded RNA molecule.
  • the endogeneous target gene may be complemented by corresponding nucleotide sequences from other species, e.g. from mouse.
  • the method and cell of the invention are also suitable in a procedure for identifying and/or characterizing pharmacological agents, e.g. identifying new pharmacological agents from a collection of test substances and/or characterizing mechanisms of action and/or side effects of known pharmacological agents.
  • test substance or a collection of test substances wherein pharmacological properties of said test substance or said collection are to be identified and/or characterized.
  • the preparative method may be employed for the purification of high molecular weight protein complexes which preferably have a mass of ⁇ 150 kD and more preferably of ⁇ 500 kD and which optionally may contain nucleic acids such as RNA.
  • heterotrimeric protein complex consisting of the 20 kD, 60 kD and 90 kD proteins of the U4/U6 snRNP particle, the splicing factor SF3b from the 17S U2 snRNP consisting of 5 proteins having molecular weights of 14, 49, 1 20, 145 and 155 kD and the 25S U41U6/U5 tri-snRNP particle containing the U4, U5 and U6 snRNA molecules and about 30 proteins, which has a molecular weight of about 1.7 MD.
  • FIG. 2 A 29 bp dsRNA is no longer processed to 21-23 nt fragments.
  • FIG. 4 21 and 22 nt RNA fragments are generated by an RNase III-like mechanism.
  • RNAs were generated by incubation of internally radiolabeled 504 bp Pp-luc dsRNA in Drosophila lysate, gel-purified, and then digested to mononucleotides with nuclease P1 (top row) or ribonuclease T2 (bottom row).
  • the dsRNA was internally radiolabeled by transcription in the presence of one of the indicated ⁇ - 32 P nucleoside triphosphates. Radioactivity was detected by phosphorimaging.
  • Nucleoside 5′-monophosphates, nucleoside 3′-mono-phosphates, nucleoside 5′,3′-diphosphates, and inorganic phosphate are indicated as pN, Np, pNp, and p i , respectively.
  • Black circles indicate UV-absorbing spots from non-radioactive carrier nucleotides.
  • the 3′,5′-bis-phosphates (red circles) were identified by co-migration with radiolabeled standards prepared by 5′-phosphorylation of nucleoside 3′-mono-phosphates with T4 polynucleotide kinase and ⁇ - 32 P-ATP.
  • the sense strand of 21 and 22 nt short interfering RNAs (siRNAs) is shown blue, the antisense strand in red.
  • the sequences of the siRNAs were derived from the cloned fragments of 52 and 111 bp dsRNAs (FIG. 4A), except for the 22 nt antisense strand of duplex 5.
  • the siRNAs in duplex 6 and 7 were unique to the 111 bp dsRNA processing reaction.
  • the two 3′ overhanging nucleotides indicated in green are present in the sequence of the synthetic antisense strand of duplexes 1 and 3.
  • the stable 5′ cleavage products were resolved on the gel.
  • the cleavage sites are indicated in FIG. 5A.
  • the region targeted by the 52 bp dsRNA or the sense (s) or antisense (as) strands are indicated by the black bars to the side of the gel.
  • the cleavage sites are all located within the region of identity of the dsRNAs. For precise determination of the cleavage sites of the antisense strand, a lower percentage gel was used.
  • RNAi is predicted to begin with processing of dsRNA (sense strand in black, antisense strand in red) to predominantly 21 and 22 nt short interfering RNAs (siRNAs). Short overhanging 3′ nucleotides, if present on the dsRNA, may be beneficial for processing of short dsRNAs.
  • the dsRNA-processing proteins which remain to be characterized, are represented as green and blue ovals, and assembled on the dsRNA in asymmetric fashion. In our model, this is illustrated by binding of a hypothetical blue protein or protein domain with the siRNA strand in 3′ to 5′ direction while the hypothetical green protein or protein domain is always bound to the opposing siRNA strand.
  • siRNA duplex proteins remain associated with the siRNA duplex and preserve its orientation as determined by the direction of the dsRNA processing reaction. Only the siRNA sequence associated with the blue protein is able to guide target RNA cleavage.
  • the endonuclease complex is referred to as small interfering ribonucleoprotein complex or siRNP. It is presumed here, that the endonuclease that cleaves the dsRNA may also cleave the target RNA, probably by temporarily displacing the passive siRNA strand not used for target recognition. The target RNA is then cleaved in the center of the region recognized by the sequence-complementary guide siRNA.
  • FIG. 8 Reporter constructs and siRNA duplexes.
  • the region targeted by the siRNA duplexes is indicated as black bar below the coding region of the luciferase genes.
  • the sense (top) and antisense (bottom) sequences of the siRNA duplexes targeting GL2, GL3 and RL luciferase are shown.
  • the GL2 and GL3 siRNA duplexes differ by only 3 single nucleotide substitutions (boxed in gray).
  • a duplex with the inverted GL2 sequence, invGL2 was synthesized.
  • the 2 nt 3′ overhang of 2′-deoxythymidine is indicated as TT; uGL2 is similar to GL2 siRNA but contains ribo-uridine 3′ overhangs.
  • FIG. 9 RNA interference by siRNA duplexes.
  • Ratios of target control luciferase were normalized to a buffer control (bu, black bars); gray bars indicate ratios of Photinus pyralis (Pp-luc) GL2 or GL3 luciferase to Renilla reniformis (Rr-luc) RL luciferase (left axis), white bars indicate RL to GL2 or GL3 ratios (right axis).
  • Panels a, c, e, g and i describe experiments performed with the combination of pGL2-Control and pRL-TK reporter plasmids, panels b, d, f, h and j with pGL3-Control and pRL-TK reporter plasmids.
  • the cell line used for the interference experiment is indicated at the top of each plot.
  • the ratios of Pp-luc/Rr-luc for the buffer control (bu) varied between 0.5 and 10 for pGL2/pRL and between 0.03 and 1 for pGL3/pRL, respectively, before normalization and between the various cell lines tested.
  • the plotted data were averaged from three independent experiments ⁇ S.D.
  • FIG. 10 Effects of 21 nt siRNA, 50 bp and 500 bp dsRNAs on luciferase expression in HeLa cells.
  • the ratios of luciferase activity for siRNA duplexes were normalized to a buffer control (bu, black bars); the luminescence ratios for 50 or 500 bp dsRNAs were normalized to the respective ratios observed for 50 and 500 bp dsRNA from humanized GFP (hG, black bars). It should be noted that the overall differences in sequences between the 49 and 484 bp dsRNAs targeting GL2 and GL3 are not sufficient to confer specificity between GL2 and GL3 targets (43 nt uninterrupted identity in 49 bp segment, 239 nt longest uninterrupted identity in 484 bp segment).
  • FIG. 11 Variation of the 3′ overhang of duplexes of 21-nt siRNAs.
  • the luminescence ratios determined in the presence of dsRNA were normalized to the ratio obtained for a buffer control (bu, black bar). Normalized ratios less than 1 indicate specific interference.
  • C-J Normalized interference ratios for eight series of 21-nt siRNA duplexes. The sequences of siRNA duplexes are depicted above the bar graphs. Each panel shows the interference ratio for a set of duplexes formed with a given antisense guide siRNA and 5 different sense siRNAs. The number of overhanging nucleotides (3′ overhang, positive numbers; 5′ overhangs, negative numbers) is indicated on the x-axis. Data points were averaged from at least 3 independent experiments, error bars represent standard deviations.
  • FIG. 12 Variation of the length of the sense strand of siRNA duplexes.
  • FIG. 13 Variation of the length of siRNA duplexes with preserved 2-nt 3′ overhangs.
  • FIG. 11H or 12 C The siRNA duplexes were extended to the 3′ side of the sense siRNA (B) or the 5′ side of the sense siRNA (C). The siRNA duplex sequences and the respective interference ratios are indicated.
  • FIG. 14 Substitution of the 2′-hydroxyl groups of the siRNA ribose residues.
  • FIG. 15 Mapping of sense and antisense target RNA cleavage by 21-nt siRNA duplexes with 2-nt 3′ overhangs.
  • the antisense siRNA was the same in all siRNA duplexes, but the sense strand was varied between 18 to 25 nt by changing the 3′ end (A) or 18 to 23 nt by changing the 5′ end (B).
  • the position of sense and antisense target RNA cleavage is indicated by triangles on top and below the siRNA duplexes, respectively.
  • C, D Analysis of target RNA cleavage using cap-labelled sense (top panel) or antisense (bottom panel) target RNAs. Only the cap-labelled 5′ cleavage products are shown. The sequences of the siRNA duplexes are indicated, and the length of the sense siRNA strands is marked on top of the panel.
  • the control lane marked with a dash in panel (C) shows target RNA incubated in absence of siRNAs. Markers were as described in FIG. 15.
  • the arrows in (D), bottom panel, indicate the target RNA cleavage sites that differ by 1 nt.
  • FIG. 17 Sequence variation of the 3′ overhang of siRNA duplexes.
  • the 2-nt 3′ overhang (NN, in gray) was changed in sequence and composition as indicated (T, 2′-deoxythymidine, dG, 2′-deoxyguanosine; asterisk, wild-type siRNA duplex). Normalized interference ratios were determined as described in FIG. 11. The wild-type sequence is the same as depicted in FIG. 14.
  • FIG. 18 Sequence specificity of target recognition.
  • the sequences of the mismatched siRNA duplexes are shown, modified sequence segments or single nucleotides are underlayed in gray.
  • the reference duplex (ref) and the siRNA duplexes 1 to 7 contain 2′-deoxythymidine 2-nt overhangs.
  • the silencing efficiency of the thymidine-modified reference duplex was comparable to the wild-type sequence (FIG. 17). Normnalized interference ratios were determined as described in FIG. 11.
  • FIG. 19 Variation of the length of siRNA duplexes with preserved 2-nt 3′ overhangs.
  • siRNA duplexes were extended to the 3′ side of the sense siRNA (A) or the 5′ side of the sense siRNA (B).
  • the siRNA duplex sequences and the respective interference ratios are indicated.
  • siRNA duplexes (0.84 ⁇ g) targeting GL2 luciferase were transfected together with pGL2-Control and pRL-TK plasmids.
  • the in vitro RNAi activities of siRNA duplexes tested in D. melanogaster lysate are indicated.
  • RNAi translation assays were performed with dsRNA concentrations of 5 nM and an-extended pre-incubation period of 15 min at 25° C. prior to the addition of in vitro transcribed, capped and polyadenylated Pp-luc and Rr-luc reporter mRNAs. The incubation was continued for 1 h and the relative amount of Pp-luc and Rr-luc protein was analyzed using the dual luciferase assay (Promega) and a Monolight 3010C luminometer (PharMingen).
  • RNA was prepared using Expedite RNA phosphoramidites (Proligo).
  • the 3′ adapter oligonucleotide was synthesized using dimethoxytrityl-1,4-benzenedimethanol-succinyl-aminopropyl-CPG.
  • the oligoribonucleotides were deprotected in 3 ml of 32% ammonia/ethanol (3/1) for 4 h at 55° C. (Expedite RNA) or 16 h at 55° C.
  • RNA transcripts for dsRNA preparation including long 3′ overhangs were generated from PCR templates that contained a T7 promoter in sense and an SP6 promoter in antisense direction.
  • the transcription template for sense and antisense target RNA was PCR-amplified with GCG TAATACGACTCACTATA GAACAATTGCTTTTACAG (underlined, T7 promoter) as 5′ primer and ATTTAGGTGACACTATA GGCATAAAGAATTGAAGA (underlined, SP6 promoter) as 3′ primer and the linearized Pp-luc plasmid (pGEM-luc sequence) (Tuschl et al., 1999) as template; the T7-transcribed sense RNA was 177 nt long with the Pp-luc sequence between pos. 113-273 relative to the start codon and followed by 17 nt of the complement of the SP6 promoter sequence at the 3′ end. Transcripts for blunt-ended dsRNA formation were prepared by transcription from two different PCR products which only contained a single promoter sequence.
  • DsRNA annealing was carried out using a phenol/chloroform extraction.
  • Equimolar concentration of sense and antisense RNA 50 nM to 10 ⁇ M, depending on the length and amount available
  • 0.3 M NaOAc pH 6
  • the resulting dsRNA was precipitated by addition of 2.5-3 volumes of ethanol.
  • the pellet was dissolved in lysis buffer (100 mM KCl, 30 mM HEPES-KOH, pH 7.4, 2 mM Mg(OAc) 2 ) and the quality of the dsRNA was verified by standard agarose gel electrophoreses in 1 ⁇ TAE-buffer.
  • the 52 bp dsRNAs with the 17 nt and 20 nt 3′ overhangs (FIG. 6) were annealed by incubating for 1 min at 95 ° C., then rapidly cooled to 70° C. and followed by slow cooling to room temperature over a 3 h period (50 ⁇ l annealing reaction, 1 ⁇ M strand concentration, 300 mM NaCl, 10 mM Tris-HCl, pH 7.5).
  • the dsRNAs were then phenol/chloroform extracted, ethanol-precipitated and dissolved in lysis buffer.
  • RNA used for dsRNA preparation was performed using 1 mM ATP, CTP, GTP, 0.1 or 0.2 mM UTP, and 0.2-0.3 ⁇ M- 32 P-UTP (3000 Ci/mmol), or the respective ratio for radiolabeled nucleoside triphosphates other than UTP. Labeling of the cap of the target RNAs was performed as described previously. The target RNAs were gel-purified after cap-labeling.
  • RNAi reactions were performed by pre-incubating 10 nM dsRNA for 15 min followed by addition of 10 nM cap-labeled target RNA. The reaction was stopped after a further 2 h (FIG. 2A) or 2.5 h incubation (FIGS. 5B and 6B) by proteinase K treatment (Tuschl et al., 1999). The samples were then analyzed on 8 or 10% sequencing gels. The 21 and 22 nt synthetic RNA duplexes were used at 100 nM final concentration (FIG. 5B).
  • the 21 nt RNAs were produced by incubation of radiolabeled dsRNA in Drosophila lysate in absence of target RNA (200 ⁇ l reaction, 1 h incubation, 50 nM dsP111, or 100 nM dsP52 or dsP39).
  • the reaction mixture was subsequently treated with proteinase K (Tuschl et al., 1999) and the dsRNA-processing products were separated on a denaturing 15% polyacrylamide gel.
  • A-band including a size range of at least 18 to 24 nt, was excised, eluted into 0.3 M NaCl overnight at 4° C. and in siliconized tubes.
  • RNA was recovered by ethanol-precipitation and dephosphorylated (30 ⁇ l reaction, 30 min, 50° C., 10 U alkaline phosphatase, Roche). The reaction was stopped by phenol/chloroform extraction and the RNA was ethanol-precipitated.
  • the 3′ adapter oligonucleotide (pUUUaaccgcatccttctcx: uppercase, RNA; lowercase, DNA; p, phosphate; x, 4-hydroxymethylbenzyl) was then ligated to the dephosphorylated ⁇ 21 nt RNA (20 ⁇ l reaction, 30 min, 37° C., 5 ⁇ M 3′ adapter, 50 mM Tris-HCl, pH 7.6, 10 mM MgCl 2 , 0.2 mM ATP, 0.1 mg/ml acetylated BSA, 15% DMSO, 25 U T4 RNA ligase, Amersham-Pharmacia) (Pan and Uhlenbeck, 1992).
  • the ligation reaction was stopped by the addition of an equal volume of 8 M urea/50 mM EDTA stopmix and directly loaded on a 15% gel. Ligation yields were greater 50%.
  • the ligation product was recovered from the gel and 5′-phosphorylated (20 ⁇ l reaction, 30 min, 37° C., 2 mM ATP, 5 U T4 polynucleotide kinase, NEB).
  • the phosphorylation reaction was stopped by phenol/chloroform extraction and RNA was recovered by ethanol-precipitation.
  • the 5′ adapter (tactaatacgactcactAAA: uppercase, RNA; lowercase, DNA) was ligated to the phosphorylated ligation product as described above.
  • the new ligation product was gel-purified and eluted from the gel slice in the presence of reverse transcription primer (GACTAGCTGGAATTCAAGGATGCGGTTAAA: bold, Eco RI site) used as carrier.
  • Reverse transcription (15 ⁇ l reaction, 30 min, 42° C., 150 U Superscript 11 reverse transcriptase, Life Technologies) was followed by PCR using as 5′ primer CAGCCAACGGAATTCATACGACTCACTAAA (bold, Eco RI site) and the 3′ RT primer.
  • the PCR product was purified by phenol/chloroform extraction and ethanol-precipitated.
  • PCR product was then digested with Eco RI (NEB) and concatamerized using T4 DNA ligase (high conc., NEB). Concatamers of a size range of 200 to 800 bp were separated on a low-melt agarose gel, recovered from the gel by a standard melting and phenol extraction procedure, and ethanol-precipitated. The unpaired ends were filled in by incubation with Taq polymerase under standard conditions for 1 5 min at 72° C. and the DNA product was directly ligated into the pCR2.1-TOPO vector using the TOPO TA cloning kit (Invitrogen). Colonies were screened using PCR and M13-20 and M13 Reverse sequencing primers. PCR products were directly submitted for custom sequencing (Sequence Laboratories Göttingen GmbH, Germany). On average, four to five 21 mer sequences were obtained per clone.
  • Nuclease P1 digestion of radiolabeled, gel-purified siRNAs and 2D-TLC was carried out as described (Zamore et al., 2000). Nuclease T2 digestion was performed in 10 ⁇ l reactions for 3 h at 50° C. in 10 mM ammonium acetate (pH 4.5) using 2 ⁇ g/ ⁇ l carrier tRNA and 30 U ribonuclease T2 (Life Technologies). The migration of non-radioactive standards was determined by UV shadowing.
  • nucleoside-3′,5′-disphosphates The identity of nucleoside-3′,5′-disphosphates was confirmed by co-migration of the T2 digestion products with standards prepared by 5′- 32 P-phosphorylation of commercial nucleoside 3′-monophosphates using ⁇ -32P-ATP and T4 polynucleotide kinase (data not shown).
  • Lysate prepared from D. melanogaster syncytial embryos recapitulates RNAi in vitro providing a novel tool for biochemical analysis of the mechanism of RNAi (Tuschl et al., 1999; Zamore et al., 2000).
  • In vitro and in vivo analysis of the length requirements of dsRNA for RNAi has revealed that short dsRNA ( ⁇ 1 50 bp) are less effective than longer dsRNAs in degrading target mRNA (Caplen et al., 2000; Hammond et al., 2000; Ngo et al., 1998); Tuschl et al., 1999). The reasons for reduction in mRNA degrading efficiency are not understood.
  • 21-23 nt RNA fragments generated by processing of dsRNAs are the mediators of RNA interference and co-suppression (Hamilton and Baulcombe, 1999; Hammond et al., 2000; Zamore et al., 2000).
  • Formation of 21-23 nt fragments in Drosophila lysate (FIG. 2) was readily detectable for 39 to 501 bp long dsRNAs but was significantly delayed for the 29 bp dsRNA.
  • the 52 bp dsRNA which shares the same 5′ end with the 39 bp dsRNA, produces the same cleavage site on the sense target, located 10 nt from the 5′ end of the region of identity with the dsRNA, in addition to two weaker cleavage sites 23 and 24 nt downstream of the first site.
  • the antisense target was only cleaved once, again 10 nt from the 5′ end of the region covered by its respective dsRNA. Mapping of the cleavage sites for the 38 to 49 bp dsRNAs shown in FIG. 1 showed that the first and predominant cleavage site was always located 7 to 10 nt downstream of the region covered by the dsRNA (data not shown). This suggests that the point of target RNA cleavage is determined by the end of the dsRNA and could imply that processing to 21-23 mers starts from the ends of the duplex.
  • Cleavage sites on sense and antisense target for the longer 111 bp dsRNA were much more frequent than anticipated and most of them appear in clusters separated by 20 to 23 nt (FIGS. 3A and 3B).
  • the first cleavage site on the sense target is 10 nt from the 5′ end of the region spanned by the dsRNA
  • the first cleavage site on the antisense target is located 9 nt from the 5′ end of region covered by the dsRNA.
  • RNAi in transposon silencing.
  • 3′ nucleotides that are derived from untemplated addition of nucleotides during RNA synthesis using T7 RNA polymerase.
  • endogenous Drosophila ⁇ 21 nt RNAs were also cloned, some of them from LTR and non-LTR retrotransposons (data not shown). This is consistent with a possible role for RNAi in transposon silencing.
  • the ⁇ 21 nt RNAs appear in clustered groups (FIG. 4A) which cover the entire dsRNA sequences. Apparently, the processing reaction cuts the dsRNA by leaving staggered 3′ ends, another characteristic of RNase III cleavage. For the 39 bp dsRNA, two clusters of ⁇ 21 nt RNAs were found from each dsRNA-constituting strand including overhanging 3′ ends, yet only one cleavage site was detected on the sense and antisense target (FIGS. 3A and 3B).
  • ⁇ 21 nt fragments were present as single-stranded guide RNAs in a complex that mediates mRNA degradation, it could be assumed that at least two target cleavage sites exist, but this was not the case. This suggests that the ⁇ 21 nt RNAs may be present in double-stranded form in the endonuclease complex but that only one of the strands can be used for target RNA recognition and cleavage.
  • the use of only one of the ⁇ 21 nt strands for target cleavage may simply be determined by the orientation in which the ⁇ 21 nt duplex is bound to the nuclease complex. This orientation is defined by the direction in which the original dsRNA was processed.
  • the ⁇ 21 mer clusters for the 52 bp and 111 bp dsRNA are less well defined when compared to the 39 bp dsRNA.
  • the clusters are spread over regions of 25 to 30 nt most likely representing several distinct subpopulations of ⁇ 21 nt duplexes and therefore guiding target cleavage at several nearby sites. These cleavage regions are still predominantly separated by 20 to. 23 nt intervals.
  • the rules determining how regular dsRNA can be processed to ⁇ 21 nt fragments are not yet understood, but it was previously observed that the approx. 21-23 nt spacing of cleavage sites could be altered by a run of uridines (Zamore et al., 2000).
  • dsRNA cleavage by E. coli RNase III appears to be mainly controlled by antideterminants, i.e. excluding some specific base-pairs at given positions relative to the cleavage site (Zhang and Nicholson, 1997).
  • nucleoside 3′,5′-diphosphates All four nucleoside 3′,5′-diphosphates were detected and suggest that the internucleotidic linkage was cleaved with little or no sequence-specificity.
  • the ⁇ 21 nt fragments are unmodified and were generated from dsRNA such that 5′-monophosphates and 3′-hydroxyls were present at the 5′-end.
  • the 21 and 22 nt RNA duplexes were incubated at 100 nM concentrations in the lysate, a 10-fold higher concentrations-than the 52 bp control dsRNA. Under these conditions, target RNA cleavage is readily detectable. Reducing the concentration of 21 and 22 nt duplexes from 100 to 10 nM does still cause target RNA cleavage. Increasing the duplex concentration from 100 nM to 1000 nM however does not further increase target cleavage, probably due to a limiting protein factor within the lysate.
  • the 21 and 22 nt dsRNAs with overhanging 3′ ends of 2 to 4 nt mediated efficient degradation of target RNA (duplexes 1, 3, 4, 6, FIGS. 5A and 5B).
  • Blunt-ended 21 or 22 nt dsRNAs (duplexes 2, 5, and 7, FIGS. 5A and 5B) were reduced in their ability to degrade the target and indicate that overhanging 3′ ends are critical for reconstitution of the RNA-protein nuclease complex.
  • the single-stranded overhangs may be required for high affinity binding of the ⁇ 21 nt duplex to the protein components.
  • the target cleavage site is located 11 or 1 2 nt downstream of the first nucleotide that is complementary to the 21 or 22 nt guide sequence, i.e. the cleavage site is near center of the region covered by the 21 or 22 nt RNAs (FIGS. 4A and 4B).
  • Displacing the sense strand of a 22 nt duplex by two nucleotides (compare duplexes 1 and 3 in FIG. 5A) displaced the cleavage site of only the antisense target by two nucleotides.
  • Displacing both sense and antisense strand by two nucleotides shifted both cleavage sites by two nucleotides (compare duplexes 1 and 4).
  • siRNAs short interfering RNAs
  • siRNP small interfering ribonucleoprotein particle
  • long dsRNAs may also contain internal dsRNA-processing signals or may get processed cooperatively due to the association of multiple cleavage factors.
  • Double-stranded RNA is first processed to short RNA duplexes of predominantly 21 and 22 nt in length and with staggered 3′ ends similar to an RNase III-like reaction (Dunn, 1982; Nicholson, 1999; Robertson, 1982). Based on the 21-23 nt length of the processed RNA fragments it has already been speculated that an RNase III-like activity may be involved in RNAi (Bass, 2000).
  • RNase III homologs Little is known about the biochemistry of RNase III homologs from plants, animals or human.
  • Two families of RNase III enzymes have been identified predominantly by database-guided sequence analysis or cloning of cDNAs.
  • the first RNase-III family is represented by the 1327 amino acid long D. melanogaster protein drosha (Acc. AF116572).
  • the C-terminus is composed of two RNase III and one dsRNA-binding domain and the N-terminus is of unknown function. Close homologs are also found in C. elegans (Acc. AF160248) and human (Acc. AF18901 1) (Filippov et al., 2000; Wu et al., 2000).
  • the drosha-like human RNase III was recently cloned and characterized (Wu et al., 2000).
  • the gene is ubiquitously expressed in human tissues and cell lines, and the protein is localized in the nucleus and the nucleolus of the cell. Based on results inferred from antisense inhibition studies, a role of this protein for rRNA processing was suggested.
  • the second class is represented by the C. elegans gene K12H4.8 (Acc. S44849) coding for a 1822 amino acid long protein.
  • This protein has an N-terminal RNA helicase motif which is followed by 2 RNase III catalytic domains and a dsRNA-binding motif, similar to the drosha RNase III family. There are close homologs in S.
  • pombe (Acc. Q09884), A. thaliana (Acc. AF187317), D. melanogaster (Acc. AE003740), and human (Acc. AB028449) (Filippov et al., 2000; Jacobsen et al., 1 999; Matsuda et al., 2000). Possibly the K12H4.8 RNase III/helicase is the likely candidate to be involved in RNAi.
  • Processing to the siRNA duplexes appears to start from the ends of both blunt-ended dsRNAs or dsRNAs with short (1-5 nt) 3′ overhangs, and proceeds in approximately 21-23 nt steps.
  • Long ( ⁇ 20 nt) 3′ staggered ends on short dsRNAs suppress RNAi, possibly through interaction with single-stranded RNA-binding proteins.
  • the suppression of RNAi by single-stranded regions flanking short dsRNA and the lack of siRNA formation from short 30 bp dsRNAs may explain why structured regions frequently encountered in mRNAs do not lead to activation of RNAi.
  • siRNA duplexes guide cleavage of sense as well as antisense target RNA as they are able to associate with the protein components in either of the two possible orientation.
  • siRNA duplexes represent a new alternative to antisense or ribozyme therapeutics.
  • RNAs were chemically synthesized using Expedite RNA phosphoramidites and thymidine phosphoramidite (Proligo, Germany). Synthetic oligonucleotides were deprotected and gel-purified (Example 1), followed by Sep-Pak C18 cartridge (Waters, Milford, Mass., USA) purification (Tuschl, 1993).
  • the siRNA sequences targeting GL2 (Acc. X65324) and GL3 luciferase (Acc. U47296) corresponded to the coding regions 153-173 relative to the first nucleotide of the start codon, siRNAs targeting RL (Acc.
  • AF025846 corresponded to region 119-129 after the start codon.
  • Longer RNAs were transcribed with T7 RNA polymerase from PCR products, followed by gel and Sep-Pak purification.
  • the 49 and 484 bp GL2 or GL3 dsRNAs corresponded to position 113-161 and 113-596, respectively, relative to the start of translation; the 50 and 501 bp RL dsRNAs corresponded to position 118-167 and 118-618, respectively.
  • PCR templates for dsRNA synthesis targeting humanized GFP were amplified from pAD3 (Kehlenbach, 1998), whereby 50 and 501 bp hG dsRNA corresponded to position 118-167 and 118-618, respectively, to the start codon.
  • annealing buffer 100 mM potassium acetate, 30 mM HEPES-KOH at pH 7.4, 2 mM magnesium acetate
  • annealing buffer 100 mM potassium acetate, 30 mM HEPES-KOH at pH 7.4, 2 mM magnesium acetate
  • the 37° C. incubation step was extended overnight for the 50 and 500 bp dsRNAs and these annealing reactions were performed at 8.4 ⁇ M and 0.84 ⁇ M strand concentrations, respectively.
  • S2 cells were propagated in Schneider's Drosophila medium (Life Technologies) supplemented with 10% FBS, 100 units/ml penicillin and 100 ⁇ g/ml streptomycin at 25° C. 293, NIH/3T3, HeLa S3, COS-7 cells were grown at 37° C. in Dulbecco's modified Eagle's medium supplemented with 10% FBS, 100 units/ml penicillin and 100 ⁇ g/ml streptomycin. Cells were regularly passaged to maintain exponential growth. 24 h before transfection at approx.
  • mammalian cells were trypsinized and diluted 1:5 with fresh medium without antibiotics (1-3 ⁇ 10 5 cells/ml) and transferred to 24-well plates (500 ⁇ l/well). S2 cells were not trypsinized before splitting. Transfection was carried out with Lipofectamine 2000 reagent (Life Technologies) as described by the manufacturer for adherent cell lines. Per well, 1.0 ⁇ g pGL2-Control (Promega) or pGL3-Control (Promega), 0.1 ⁇ g pRL-TK (Promega) and 0.28 ⁇ g siRNA duplex or dsRNA, formulated into liposomes, were applied; the final volume was 600 ⁇ l per well.
  • siRNA duplexes were co-transfected with the reporter plasmid combinations pGL2/pRL or pGL3/pRL into D. melanogaster Schneider S2 cells or mammalian cells using cationic liposomes. Luciferase activities were determined 20 h after transfection.
  • FIG. 9 a - j In all cell lines tested, we observed specific reduction of the expression of the reporter genes in the presence of cognate siRNA duplexes (FIG. 9 a - j ). Remarkably, the absolute luciferase expression levels were unaffected by non-cognate siRNAs, indicating the absence of harmful side effects by 21 nt RNA duplexes (e.g. FIG. 10 a - d for HeLa cells). In D. melanogaster S2 cells (FIG. 9 a, b ), the specific inhibition of luciferases was complete. In mammalian cells, where the reporter genes were 50- to 100-fold stronger expressed, the specific suppression was less complete (FIG. 9 c - j ).
  • GL2 expression was reduced 3- to 12-fold, GL3 expression 9- to 25-fold and RL expression 1- to 3-fold, in response to the cognate siRNAs.
  • targeting of RL luciferase by RL siRNAs was ineffective, although GL2 and GL3 targets responded specifically (FIG. 9 i, j ).
  • the lack of reduction of RL expression in 293 cells may be due to its 5- to 20-fold higher expression compared to any other mammalian cell line tested and/or to limited accessibility of the target sequence due to RNA secondary structure or associated proteins. Nevertheless, specific targeting of GL2 and GL3 luciferase by the cognate siRNA duplexes indicated that RNAi is also functioning in 293 cells.
  • the thymidine overhang was chosen, because it is supposed to enhance nuclease resistance of siRNAs in the tissue culture medium and within transfected cells. Indeed, the thymidine-modified GL2 siRNA was slightly more potent than the unmodified uGL2 siRNA in all cell lines tested (FIG. 9 a, c, e, g, i ). It is conceivable that further modifications of the 3′ overhanging nucleotides may provide additional benefits to the delivery and stability of siRNA duplexes.
  • siRNA duplexes were used (FIG. 9, 10).
  • Increasing the siRNA concentration to 100 nM did not enhance the specific silencing effects, but started to affect transfection efficiencies due to competition for liposome encapsulation between plasmid DNA and siRNA (data not shown).
  • Decreasing the siRNA concentration to 1.5 nM did not reduce the specific silencing effect (data not shown), even though the siRNAs were now only 2- to 20-fold more concentrated than the DNA plasmids. This indicates that siRNAs are extraordinarily powerful reagents for mediating gene silencing and that siRNAs are effective at concentrations that are several orders of magnitude below the concentrations applied in conventional antisense or ribozyme gene targeting experiments.
  • dsRNAs In order to monitor the effect of longer dsRNAs on mammalian cells, 50 and 500 bp dsRNAs cognate to the reporter genes were prepared. As non-specific control, dsRNAs from humanized GFP (hG) (Kehlenbach, 1998) was used. When dsRNAs were co-transfected, in identical amounts (not concentrations) to the siRNA duplexes, the reporter gene expression was strongly and unspecifically reduced. This effect is illustrated for HeLa cells as a representative example (FIG. 10 a - d ).
  • the absolute luciferase activities were decreased unspecifically 10- to 20-fold by 50 bp dsRNA and 20- to 200-fold by 500 bp dsRNA co-transfection, respectively. Similar unspecific effects were observed for COS-7 and NIH/3T3 cells. For 293 cells, a 10- to 20-fold unspecific reduction was observed only for 500 bp dsRNAs. Unspecific reduction in reporter gene expression by dsRNA >30 bp was expected as part of the interferon response.
  • CHO-K1 cells appear to be deficient in the interferon response.
  • 293, NIH/3T3 and BHK-21 cells were tested for RNAi using luciferase/lacZ reporter combinations and 829 bp specific lacZ or 717 bp unspecific GFP dsRNA (Caplen, 2000).
  • the failure of detecting RNAi in this case may be due to the less sensitive luciferase/lacZ reporter assay and the length differences of target and control dsRNA.
  • our results indicate that RNAi is active in mammalian cells, but that the silencing effect is difficult to detect, if the interferon system is activated by dsRNA >30 bp.
  • siRNA-mediated gene silencing in mammalian cells.
  • the use of short siRNAs holds great promise for inactivation of gene function in human tissue culture and the development of gene-specific therapeutics.
  • RNA synthesis, annealing, and luciferase-based RNAi assays were performed as described in Examples 1 or 2 or in previous publications (Tuschl et al., 1999; Zamore et al., 2000). All siRNA duplexes were directed against firefly luciferase, and the luciferase mRNA sequence was derived from pGEM-luc (GenBank acc. X65316) as described (Tuschl et al., 1999). The siRNA duplexes were incubated in D. melanogaster RNAi/translation reaction for 15 min prior to addition of mRNAs. Translation-based RNAi assays were performed at least in triplicates.
  • mapping of sense target RNA cleavage a 177-nt transcript was generated, corresponding to the firefly luciferase sequence between positions 113-273 relative to the start codon, followed by the 17-nt complement of the SP6 promoter sequence.
  • mapping of antisense target RNA cleavage a 166-nt transcript was produced from a template, which was amplified from plasmid sequence by PCR using 5′ primer TAATACGACTCACTATAGA GCCCATATCGTTTCATA (T7 promoter underlined) and 3! primer AGAGGATGGAACCGCTGG.
  • the target sequence corresponds to the complement of the firefly luciferase sequence between positions 50-215 relative to the start codon.
  • Guanylyl transferase labelling was performed as previously described (Zamore et al., 2000).
  • 100 nM siRNA duplex was incubated with 5 to 10 nM target RNA in D. melanogaster embryo lysate under standard conditions (Zamore et al., 2000) for 2 h at 25° C.
  • the reaction was stopped by the addition of 8 volumes of proteinase K buffer (200 mM Tris-HCl pH 7.5, 25 mM EDTA, 300 mM NaCl, 2% w/v sodium dodecyl sulfate). Proteinase K (E.M.
  • siRNA duplexes As described above, 2 or 3 unpaired nucleotides at the 3′ end of siRNA duplexes were more efficient in target RNA degradation than the respective blunt-ended duplexes.
  • sense and antisense siRNAs eight series of siRNA duplexes with synthetic overhanging ends were generated covering a range of 7-nt 3′ overhang to 4-nt 5′ overhang.
  • siRNA duplexes The interference of siRNA duplexes was measured using the dual luciferase assay system (Tuschl et al., 1999; Zamore et al., 2000). siRNA duplexes were directed against firefly luciferase mRNA, and sea pansy luciferase mRNA was used as internal control. The luminescence ratio of target to control luciferase activity was determined in the presence of siRNA duplex and was normalized to the ratio observed in the absence of dsRNA. For comparison, the interference ratios of long dsRNAs (39 to 504 pb) are shown in FIG. 11B. The interference ratios were determined at concentrations of 5 nM for long dsRNAs (FIG.
  • FIG. 13A Two series of siRNA duplexes were prepared including the 21-nt siRNA duplex of FIG. 11H as reference. The length of the duplexes was varied between 20 to 25 bp by extending the base-paired segment at the 3′ end of the sense siRNA (FIG. 13B) or at the 3′ end of the antisense siRNA (FIG. 13C). Duplexes of 20 to 23 bp caused specific repression of target luciferase activity, but the 21-nt siRNA duplex was at least 8-fold more efficient than any of the other duplexes. 24- and 25-nt siRNA duplexes did not result in any detectable interference. Sequence-specific effects were minor as variations on both ends of the duplex produced similar effects.
  • siRNA ribose residues were examined (FIG. 14).
  • Substitution of the 2-nt 3′ overhangs by 2′-deoxy nucleotides had no effect, and even the replacement of two additional riboncleotides adjacent to the overhangs in the paired region, produced significantly active siRNAs.
  • 8 out of 42 nt of a siRNA duplex were replaced by DNA residues without loss of activity.
  • Complete substitution of one or both siRNA strands by 2′-deoxy residues abolished RNAi, as did substitution by 2′-O-methyl residues.
  • Target RNA cleavage positions were previously determined for 22-nt siRNA duplexes and for a 21-nt/22-nt duplex. It was found that the position of the target RNA cleavage was located in the centre of the region covered by the siRNA duplex, 11 or 12 nt downstream of the first nucleotide that was complementary to the 21- or 22-nt siRNA guide sequence.
  • Five distinct 21-nt siRNA duplexes with 2-nt 3′ overhang (FIG. 1 5 A) were incubated with 5′ cap-labelled sense or antisense target RNA in D. melanogaster lysate (Tuschl et al., 1999; Zamore et al., 2000).
  • the 5′ cleavage products were resolved on sequencing gels (FIG. 15B).
  • the amount of sense target RNA cleaved correlates with the efficiency of siRNA duplexes determined in the translation-based assay, and siRNA duplexes 1, 2 and 4 (FIGS. 15B and 11H, G, E) cleave target RNA faster than duplexes 3 and 5 (FIGS. 15B and 11F, D).
  • the sum of radioactivity of the 5′ cleavage product and the input target RNA were not constant over time, and the 5′ cleavage products did not accumulate.
  • the cleavage products, once released from the siRNA-endonuclease complex are rapidly degraded due to the lack of either of the poly(A) tail of the 5′-cap.
  • the cleavage sites for both, sense and antisense target RNAs were located in the middle of the region spanned by the siRNA duplexes.
  • the cleavage sites for each target produced by the 5 different duplexes varied by 1-nt according to the 1-nt displacement of the duplexes along the target sequences.
  • the targets were cleaved precisely 11 nt downstream of the target position complementary to the 3′-most nucleotide of the sequence-complementary guide siRNA (FIG. 15A, B).
  • a 2-nt 3′ overhang is preferred for siRNA function.
  • RISC or siRNP endonuclease complex
  • sequence changes were introduced by inverting short segments of 3- or 4-nt length or as point mutations (FIG. 18).
  • the sequence changes in one siRNA strand were compensated in the complementary siRNA strand to avoid pertubing the base-paired siRNA duplex structure.
  • the sequence of all 2-nt 3′ overhangs was TT (T, 2′-deoxythymidine) to reduce costs of synthesis.
  • the TT/TT reference siRNA duplex was comparable in RNAi to the wild-type siRNA duplex AA/UG (FIG. 17).
  • Efficiently silencing siRNA duplexes are preferably composed of 21-nt antisense siRNAs, and should be selected to form a 19 bp double helix with 2-nt 3′ overhanging ends.
  • 2′-deoxy substitutions of the 2-nt 3′ overhanging ribonucleotides do not affect RNAi, but help to reduce the costs of RNA synthesis and may enhance RNAse resistance of siRNA duplexes. More extensive 2′-deoxy or 2′-O-methyl modifications, however, reduce the ability of siRNAs to mediate RNAi, probably by interfering with protein association for siRNAP assembly.
  • Target recognition is a highly sequence-specific process, mediated by the siRNA complementary to the target.
  • the 3′-most nucleotide of the guide siRNA does not contribute to specificity of target recognition, while the penultimate nucleotide of the 3′ overhang affects target RNA cleavage, and a mismatch reduces RNAi 2- to 4-fold.
  • the 5′ end of a guide siRNA also appears more permissive for mismatched target RNA recognition when compared to the 3′ end.
  • Nucleotides in the centre of the siRNA, located opposite the target RNA cleavage site are important specificity determinants and even single nucleotide changes reduce RNAi to undetectable level. This suggests that siRNA duplexes may be able to discriminate mutant or polymorphic alleles in gene targeting experiments, which may become an important feature for future therapeutic developments.
  • siRNA sequences with identical 3′ overhanging sequences.
  • Asymmetry in reconstitution of sense and antisense-cleaving siRNPs could be (partially) responsible for the variation in RNAi efficiency observed for various 21-nt siRNA duplexes with 2-nt 3′ overhangs used in this study (FIG. 14).
  • the nucleotide sequence at the target site and/or the accessibility of the target RNA structure may be responsible for the variation in efficiency for these siRNA duplexes.
  • PKR a protein kinase regulated by double-stranded RNA. Int. J. Biochem. Cell Biol. 29, 945-949.
  • EGO-1 is related to RNA-directed RNA polymerase and functions in germ-line development and RNA interference in C. elegans. Curr. Biol. 10, 169-178.
  • RNAi Double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101, 25-33.

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