Scott W. Knight, Brenda L. Bass^*

An early event in RNA interference (RNAi) is the cleavage of the initiating double-stranded RNA (dsRNA) to short pieces, 21 to 23 nucleotides in length. Here we describe a null mutation in dicer-1 (dcr-1), a gene proposed to encode the enzyme that generates these short RNAs. We find that dcr-1(/) animals have defects in RNAi under some, but not all, conditions. Mutant animals have germ line defects that lead to sterility, suggesting that cleavage of dsRNA to short pieces is a requisite event in normal development.

Department of Biochemistry and Howard Hughes Medical Institute, University of Utah, 50 North Medical Drive, Room 211, Salt Lake City, UT 84132, USA.
^*   To whom correspondence should be addressed. E-mail: bbass{at}howard.genetics.utah.edu

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The slicing activity of miRNA-specific Argonautes is essential for the miRNA pathway in C. elegans.

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M. B. Warf, B. A. Shepherd, W. E. Johnson, and B. L. Bass (2012)
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Functional parameters of Dicer-independent microRNA biogenesis.

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The RDE-10/RDE-11 complex triggers RNAi-induced mRNA degradation by association with target mRNA in C. elegans.

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Improved annotation of C. elegans microRNAs by deep sequencing reveals structures associated with processing by Drosha and Dicer.

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Dicer's helicase domain is required for accumulation of some, but not all, C. elegans endogenous siRNAs.

N. C. Welker, D. M. Pavelec, D. A. Nix, T. F. Duchaine, S. Kennedy, and B. L. Bass (2010)
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Caspase-Dependent Conversion of Dicer Ribonuclease into a Death-Promoting Deoxyribonuclease.

A. Nakagawa, Y. Shi, E. Kage-Nakadai, S. Mitani, and D. Xue (2010)
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Requirement for the ERI/DICER Complex in Endogenous RNA Interference and Sperm Development in Caenorhabditis elegans.

D. M. Pavelec, J. Lachowiec, T. F. Duchaine, H. E. Smith, and S. Kennedy (2009)
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A Caenorhabditis elegans RNA-Directed RNA Polymerase in Sperm Development and Endogenous RNA Interference.

J. I. Gent, M. Schvarzstein, A. M. Villeneuve, S. G. Gu, V. Jantsch, A. Z. Fire, and A. Baudrimont (2009)
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26G endo-siRNAs regulate spermatogenic and zygotic gene expression in Caenorhabditis elegans.

T. Han, A. P. Manoharan, T. T. Harkins, P. Bouffard, C. Fitzpatrick, D. S. Chu, D. Thierry-Mieg, J. Thierry-Mieg, and J. K. Kim (2009)
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Systematic analysis of dynamic miRNA-target interactions during C. elegans development.

L. Zhang, M. Hammell, B. A. Kudlow, V. Ambros, and M. Han (2009)
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Functional Association of the Microprocessor Complex with the Spliceosome.

N. Kataoka, M. Fujita, and M. Ohno (2009)
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Human Dicer Binds Short Single-strand and Double-strand RNA with High Affinity and Interacts with Different Regions of the Nucleic Acids.

W. F. Lima, H. Murray, J. G. Nichols, H. Wu, H. Sun, T. P. Prakash, A. R. Berdeja, H. J. Gaus, and S. T. Crooke (2009)
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A Novel Mechanism of Late Gene Silencing Drives SV40 Transformation of Human Mesothelial Cells.

M. Carbone, A. Pannuti, L. Zhang, J. R. Testa, and M. Bocchetta (2008)
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Dicer1 Is Required for Differentiation of the Mouse Male Germline.

D. M. Maatouk, K. L. Loveland, M. T. McManus, K. Moore, and B. D. Harfe (2008)
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A starvation-induced noncoding RNA modulates expression of Dicer-regulated genes.

S. Hellwig and B. L. Bass (2008)
PNAS 105, 12897-12902
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The RNAseIII enzyme Drosha is critical in T cells for preventing lethal inflammatory disease.

M. M.W. Chong, J. P. Rasmussen, A. Y. Rudensky, and D. R. Littman (2008)
J. Exp. Med. 205, 2005-2017
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Protection of specific maternal messenger RNAs by the P body protein CGH-1 (Dhh1/RCK) during Caenorhabditis elegans oogenesis.

P. R. Boag, A. Atalay, S. Robida, V. Reinke, and T. K. Blackwell (2008)
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Conditional Loss of Dicer Disrupts Cellular and Tissue Morphogenesis in the Cortex and Hippocampus.

T. H. Davis, T. L. Cuellar, S. M. Koch, A. J. Barker, B. D. Harfe, M. T. McManus, and E. M. Ullian (2008)
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The Caenorhabditis elegans rsd-2 and rsd-6 Genes Are Required for Chromosome Functions During Exposure to Unfavorable Environments.

W. Han, P. Sundaram, H. Kenjale, J. Grantham, and L. Timmons (2008)
Genetics 178, 1875-1893
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Targets of Small Interfering RNA Restriction during Human Immunodeficiency Virus Type 1 Replication.

Y. Gao, M. A. Lobritz, J. Roth, M. Abreha, K. N. Nelson, I. Nankya, D. M. Moore-Dudley, A. Abraha, S. L. Gerson, and E. J. Arts (2008)
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A-to-I editing sites are a genomically encoded G: Implications for the evolutionary significance and identification of novel editing sites.

N. Tian, X. Wu, Y. Zhang, and Y. Jin (2008)
RNA 14, 211-216
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A Slicer-independent role for Argonaute 2 in hematopoiesis and the microRNA pathway.

D. O'Carroll, I. Mecklenbrauker, P. P. Das, A. Santana, U. Koenig, A. J. Enright, E. A. Miska, and A. Tarakhovsky (2007)
Genes & Dev. 21, 1999-2004
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Genes misregulated in C. elegans deficient in Dicer, RDE-4, or RDE-1 are enriched for innate immunity genes.

N. C. Welker, J. W. Habig, and B. L. Bass (2007)
RNA 13, 1090-1102
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Carbodiimide-mediated cross-linking of RNA to nylon membranes improves the detection of siRNA, miRNA and piRNA by northern blot.

G. S. Pall, C. Codony-Servat, J. Byrne, L. Ritchie, and A. Hamilton (2007)
Nucleic Acids Res. 35, e60
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Critical roles for Dicer in the female germline.

E. P. Murchison, P. Stein, Z. Xuan, H. Pan, M. Q. Zhang, R. M. Schultz, and G. J. Hannon (2007)
Genes & Dev. 21, 682-693
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Characterization of DGCR8/Pasha, the essential cofactor for Drosha in primary miRNA processing.

K.-H. Yeom, Y. Lee, J. Han, M. R. Suh, and V. N. Kim (2006)
Nucleic Acids Res. 34, 4622-4629
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A genomewide screen for components of the RNAi pathway in Drosophila cultured cells.

S. Dorner, L. Lum, M. Kim, R. Paro, P. A. Beachy, and R. Green (2006)
PNAS 103, 11880-11885
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ATP-binding Cassette Transporters Are Required for Efficient RNA Interference in Caenorhabditis elegans.

P. Sundaram, B. Echalier, W. Han, D. Hull, and L. Timmons (2006)
Mol. Biol. Cell 17, 3678-3688
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Comprehensive thermodynamic analysis of 3' double-nucleotide overhangs neighboring Watson-Crick terminal base pairs.

A. S. O'Toole, S. Miller, N. Haines, M. C. Zink, and M. J. Serra (2006)
Nucleic Acids Res. 34, 3338-3344
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Characterization of a Novel Protein Kinase D: CAENORHABDITIS ELEGANS DKF-1 IS ACTIVATED BY TRANSLOCATION-PHOSPHORYLATION AND REGULATES MOVEMENT AND GROWTH IN VIVO.

H. Feng, M. Ren, S.-L. Wu, D. H. Hall, and C. S. Rubin (2006)
J. Biol. Chem. 281, 17801-17814
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Drosha in Primary MicroRNA Processing.

Y. LEE, J. HAN, K.-H. YEOM, H. JIN, and V.N. KIM (2006)
Cold Spring Harb Symp Quant Biol 71, 51-57
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MicroRNA Function and Mechanism: Insights from Zebra Fish.

A.F. SCHIER and A.J. GIRALDEZ (2006)
Cold Spring Harb Symp Quant Biol 71, 195-203
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How Does RNA Editing Affect dsRNA-mediated Gene Silencing?.

B.L. BASS (2006)
Cold Spring Harb Symp Quant Biol 71, 285-292
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The Expanding Universe of Noncoding RNAs.

G.J. HANNON, F.V. RIVAS, E.P. MURCHISON, and J.A. STEITZ (2006)
Cold Spring Harb Symp Quant Biol 71, 551-564
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An antiviral role for the RNA interference machinery in Caenorhabditis elegans.

D. H. Schott, D. K. Cureton, S. P. Whelan, and C. P. Hunter (2005)
PNAS 102, 18420-18424
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A human, ATP-independent, RISC assembly machine fueled by pre-miRNA.

E. Maniataki and Z. Mourelatos (2005)
Genes & Dev. 19, 2979-2990
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Slicer function of Drosophila Argonautes and its involvement in RISC formation.

K. Miyoshi, H. Tsukumo, T. Nagami, H. Siomi, and M. C. Siomi (2005)
Genes & Dev. 19, 2837-2848
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microPrimer: the biogenesis and function of microRNA.

T. Du and P. D. Zamore (2005)
Development 132, 4645-4652
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MicroRNA functions in animal development and human disease.

I. Alvarez-Garcia and E. A. Miska (2005)
Development 132, 4653-4662
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Ectopic DICER-LIKE1 Expression in P1/HC-Pro Arabidopsis Rescues Phenotypic Anomalies but Not Defects in MicroRNA and Silencing Pathways.

S. Mlotshwa, S. E. Schauer, T. H. Smith, A. C. Mallory, J.M. Herr Jr., B. Roth, D. S. Merchant, A. Ray, L. H. Bowman, and V. B. Vance (2005)
PLANT CELL 17, 2873-2885
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Ribo-gnome: The Big World of Small RNAs.

P. D. Zamore and B. Haley (2005)
Science 309, 1519-1524
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Biochemical and genomic analysis of substrate recognition by the double-stranded RNA binding domain of yeast RNase III.

A. K. HENRAS, M. SAM, S. L. HILEY, H. WU, T. R. HUGHES, J. FEIGON, and G. F. CHANFREAU (2005)
RNA 11, 1225-1237
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RNA Silencing of Single and Multiple Members in a Gene Family of Rice.

D. Miki, R. Itoh, and K. Shimamoto (2005)
Plant Physiology 138, 1903-1913
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RNA interference in biology and disease.

C. A. Sledz and B. R. G. Williams (2005)
Blood 106, 787-794
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A potential link between transgene silencing and poly(A) tails.

M. C. SIOMI, H. TSUKUMO, A. ISHIZUKA, T. NAGAMI, and H. SIOMI (2005)
RNA 11, 1004-1011
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EGO-1, a Putative RNA-Directed RNA Polymerase, Promotes Germline Proliferation in Parallel With GLP-1/Notch Signaling and Regulates the Spatial Organization of Nuclear Pore Complexes and Germline P Granules in Caenorhabditis elegans.

V. E. Vought, M. Ohmachi, M.-H. Lee, and E. M. Maine (2005)
Genetics 170, 1121-1132
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Human microRNA prediction through a probabilistic co-learning model of sequence and structure.

J.-W. Nam, K.-R. Shin, J. Han, Y. Lee, V. N. Kim, and B.-T. Zhang (2005)
Nucleic Acids Res. 33, 3570-3581
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Efficiency of RNA Interference in the Mouse Hematopoietic System Varies between Cell Types and Developmental Stages.

P. Oberdoerffer, C. Kanellopoulou, V. Heissmeyer, C. Paeper, C. Borowski, I. Aifantis, A. Rao, and K. Rajewsky (2005)
Mol. Cell. Biol. 25, 3896-3905
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Depletion of Human Micro-RNA miR-125b Reveals That It Is Critical for the Proliferation of Differentiated Cells but Not for the Down-regulation of Putative Targets during Differentiation.

Y. S. Lee, H. K. Kim, S. Chung, K.-S. Kim, and A. Dutta (2005)
J. Biol. Chem. 280, 16635-16641
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Transcriptional silencing of a transgene by RNAi in the soma of C. elegans.

A. Grishok, J. L. Sinskey, and P. A. Sharp (2005)
Genes & Dev. 19, 683-696
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Perspective: machines for RNAi.

Y. Tomari and P. D. Zamore (2005)
Genes & Dev. 19, 517-529
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Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing.

C. Kanellopoulou, S. A. Muljo, A. L. Kung, S. Ganesan, R. Drapkin, T. Jenuwein, D. M. Livingston, and K. Rajewsky (2005)
Genes & Dev. 19, 489-501
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RDE-2 interacts with MUT-7 to mediate RNA interference in Caenorhabditis elegans.

B. B. J. Tops, H. Tabara, T. Sijen, F. Simmer, C. C. Mello, R. H. A. Plasterk, and R. F. Ketting (2005)
Nucleic Acids Res. 33, 347-355
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The Drosha-DGCR8 complex in primary microRNA processing.

J. Han, Y. Lee, K.-H. Yeom, Y.-K. Kim, H. Jin, and V. N. Kim (2004)
Genes & Dev. 18, 3016-3027
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Identification and validation of cell surface antigens for antibody targeting in oncology.

P. Carter, L. Smith, and M. Ryan (2004)
Endocr. Relat. Cancer 11, 659-687
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Inhibition of Epstein-Barr Virus (EBV) Reactivation by Short Interfering RNAs Targeting p38 Mitogen-Activated Protein Kinase or c-myc in EBV-Positive Epithelial Cells.

X. Gao, H. Wang, and T. Sairenji (2004)
J. Virol. 78, 11798-11806
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Structural Features of MicroRNA (miRNA) Precursors and Their Relevance to miRNA Biogenesis and Small Interfering RNA/Short Hairpin RNA Design.

J. Krol, K. Sobczak, U. Wilczynska, M. Drath, A. Jasinska, D. Kaczynska, and W. J. Krzyzosiak (2004)
J. Biol. Chem. 279, 42230-42239
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A single Argonaute protein mediates both transcriptional and posttranscriptional silencing in Schizosaccharomyces pombe.

A. Sigova, N. Rhind, and P. D. Zamore (2004)
Genes & Dev. 18, 2359-2367
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Inducible Silencing of KILLER/DR5 In vivo Promotes Bioluminescent Colon Tumor Xenograft Growth and Confers Resistance to Chemotherapeutic Agent 5-Fluorouracil.

S. Wang and W. S. El-Deiry (2004)
Cancer Res. 64, 6666-6672
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Effects of Length and Location on the Cellular Response to Double-Stranded RNA.

Q. Wang and G. G. Carmichael (2004)
Microbiol. Mol. Biol. Rev. 68, 432-452
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Distinct roles for Argonaute proteins in small RNA-directed RNA cleavage pathways.

K. Okamura, A. Ishizuka, H. Siomi, and M. C. Siomi (2004)
Genes & Dev. 18, 1655-1666
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Cell Cycle-dependent Nuclear Localization of Yeast RNase III Is Required for Efficient Cell Division.

M. Catala, B. Lamontagne, S. Larose, G. Ghazal, and S. A. Elela (2004)
Mol. Biol. Cell 15, 3015-3030
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Structural basis for recognition of the AGNN tetraloop RNA fold by the double-stranded RNA-binding domain of Rnt1p RNase III.

H. Wu, A. Henras, G. Chanfreau, and J. Feigon (2004)
PNAS 101, 8307-8312
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A combined computational-experimental approach predicts human microRNA targets.

M. Kiriakidou, P. T. Nelson, A. Kouranov, P. Fitziev, C. Bouyioukos, Z. Mourelatos, and A. Hatzigeorgiou (2004)
Genes & Dev. 18, 1165-1178
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Redundancy of the Two Dicer Genes in Transgene-Induced Posttranscriptional Gene Silencing in Neurospora crassa.

C. Catalanotto, M. Pallotta, P. ReFalo, M. S. Sachs, L. Vayssie, G. Macino, and C. Cogoni (2004)
Mol. Cell. Biol. 24, 2536-2545
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miRNP:mRNA association in polyribosomes in a human neuronal cell line.

P. T. NELSON, A. G. HATZIGEORGIOU, and Z. MOURELATOS (2004)
RNA 10, 387-394
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Specificity of microRNA target selection in translational repression.

J. G. Doench and P. A. Sharp (2004)
Genes & Dev. 18, 504-511
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Ago1 and Dcr1, Two Core Components of the RNA Interference Pathway, Functionally Diverge from Rdp1 in Regulating Cell Cycle Events in Schizosaccharomyces pombe.

J. B. Carmichael, P. Provost, K. Ekwall, and T. C. Hobman (2004)
Mol. Biol. Cell 15, 1425-1435
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The 5'-3' exoribonuclease xrn-1 is essential for ventral epithelial enclosure during C. elegans embryogenesis.

S. NEWBURY and A. WOOLLARD (2004)
RNA 10, 59-65
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RNA Interference: Biology, Mechanism, and Applications.

N. Agrawal, P. V. N. Dasaradhi, A. Mohmmed, P. Malhotra, R. K. Bhatnagar, and S. K. Mukherjee (2003)
Microbiol. Mol. Biol. Rev. 67, 657-685
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MicroRNAs and small interfering RNAs can inhibit mRNA expression by similar mechanisms.

Y. Zeng, R. Yi, and B. R. Cullen (2003)
PNAS 100, 9779-9784
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Double-stranded RNA-mediated gene silencing in fission yeast.

M. Raponi and G. M. Arndt (2003)
Nucleic Acids Res. 31, 4481-4489
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Inducible Systemic RNA Silencing in Caenorhabditis elegans.

L. Timmons, H. Tabara, C. C. Mello, and A. Z. Fire (2003)
Mol. Biol. Cell 14, 2972-2983
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The specifics of small interfering RNA specificity.

A. Dillin (2003)
PNAS 100, 6289-6291
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From Genes to Integrative Physiology: Ion Channel and Transporter Biology in Caenorhabditis elegans.

K. Strange (2003)
Physiol Rev 83, 377-415
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