Argonautes ALG-3 and ALG-4 are required for spermatogenesis-specific 26G-RNAs and thermotolerant sperm in Caenorhabditis elegans

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 8, 2010, Pages 3588-3593

  Conine, Colin C ^a   Batista, Pedro J ^a   Gu, Weifeng ^a   Claycomb, Julie M ^a,b   Chaves, Daniel A ^a,c   Shirayama, Masaki ^a   Mello, Craig C ^a,b  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^c INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

Author keywords

Gene expression; Germline; P granules; RNAi; Spermiogenesis

Indexed keywords

ARGONAUTE PROTEIN; ARGONAUTE PROTEIN 3; ARGONAUTE PROTEIN 4; BINDING PROTEIN; GUANOSINE PHOSPHATE; MESSENGER RNA; PIWI PROTEIN; RNA; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; DOWN REGULATION; FEMALE; FERTILITY; GAMETOGENESIS; GENE EXPRESSION; GERM LINE; HEAT TOLERANCE; MALE; MALE FERTILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PACHYTENE; PRIORITY JOURNAL; SPERM; SPERMATOGENESIS; TEMPERATURE;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; FERTILITY; HOT TEMPERATURE; MALE; MUTATION; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; SPERMATOGENESIS; SPERMATOZOA;

CAENORHABDITIS ELEGANS; METAZOA;

EID: 77649254581     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0911685107     Document Type: Article

References (33)

1. Hutvagner G, Simard MJ (2008) Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol 9:22-32.
2. Tolia NH, Joshua-Tor L (2007) Slicer and the argonautes. Nat Chem Biol 3:36-43.
3. Yigit E, et al. (2006) Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi. Cell 127:747-757.
4. Grishok A, et al. (2001) Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 106:23-34.
5. Claycomb JM, et al. (2009) The Argonaute CSR-1 and its 22G-RNA cofactors are required for holocentric chromosome segregation. Cell 139:123-134.
6. Batista PJ, et al. (2008) PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. Mol Cell 31:67-78.
7. Das PP, et al. (2008) Piwi and piRNAs act upstream of an endogenous siRNA pathway to suppressTc3 transposon mobility in the Caenorhabditiselegansgermline.MolCell31:79-90.
8. Wang G, Reinke V (2008) A C. elegans Piwi, PRG-1, regulates 21U-RNAs during spermatogenesis. Curr Biol 18:861-867.
9. Gu W, et al. (2009) Distinct argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline. Mol Cell 36:231-244.
10. Ruby JG, et al. (2006) Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 127:1193-1207.
11. Duchaine TF, et al. (2006) Functional proteomics reveals the biochemical niche of C. elegans DCR-1 in multiple small-RNA-mediated pathways. Cell 124:343-354.
12. Gent JI, et al. (2009) A Caenorhabditis elegans RNA-directed RNA polymerase in sperm development and endogenous RNA interference. Genetics 183:1297-1314.
13. Pavelec DM, Lachowiec J, Duchaine TF, Smith HE, Kennedy S (2009) Requirement for ERI/DICER complex in endogenous RNAi and sperm development in Caenorhabditis elegans. Genetics 183:1283-1295.
14. Vasale JJ, et al. (2010) Sequential rounds of RNA-dependent RNA transcription drive endogenous small RNA biogenesis in the ERGO-1 argonaute pathway. Proc Natl Acad Sci USA.
15. Schedl T, Kimble J (1988) fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics 119:43-61.
16. Ward S, Miwa J (1978) Characterization of temperature-sensitive, fertilization-defective mutants of the nematode Caenorhabditis elegans. Genetics 88:285-303.
17. Shakes DC, et al. (2009) Spermatogenesis-specific features of the meiotic program in Caenorhabditis elegans. PLoS Genet 5:e1000611.
18. Kawasaki I, et al. (1998) PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. elegans. Cell 94:635-645.
19. Shakes DC, Ward S (1989) Initiation of spermiogenesis in C. elegans: a pharmacological and genetic analysis. Dev Biol 134:189-200.
20. L'Hernault SW (2006) Spermatogenesis. WormBook 20:1-14.
21. Reinke V, Gil IS, Ward S, Kazmer K (2004) Genome-wide germline-enriched and sexbiased expression profiles in Caenorhabditis elegans. Development 131:311-323.
22. Aravin AA, Hannon GJ, Brennecke J (2007) The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318:761-764.
23. Han T, et al. (2009) 26G endo-siRNAs regulate spermatogenic and zygotic gene expression in Caenorhabditis elegans. Proc Natl Acad Sci USA 106:18674-18679.
24. Altun ZF, Herndon LA, Crocker C, Lints R, HallDH(eds) 2002-2009. http://www.wormatlas.org.
25. Kuznicki KA, et al. (2000) Combinatorial RNA interference indicates GLH-4 can compensate for GLH-1; these two P granule components are critical for fertility in C. elegans. Development 127:2907-2916.
26. Anderson P, Kedersha N (2009) RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat Rev Mol Cell Biol 10:430-436.
27. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281-297.
28. Bushati N, Cohen SM (2007) microRNA functions. Annu Rev Cell Dev Biol 23:175-205.
29. Werdelin L, Nilsonne A (1999) The evolution of the scrotum and testicular descent in mammals: a phylogenetic view. J Theor Biol 196:61-72.
30. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71-94.
31. Praitis V, Casey E, Collar D, Austin J (2001) Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157:1217-1226.
32. Frøkjaer-Jensen C, et al. (2008) Single-copy insertion of transgenes in Caenorhabditis elegans. Nat Genet 40:1375-1383.
33. Miller MA (2006) Sperm and oocyte isolation methods for biochemical and proteomic analysis. Methods Mol Biol 351:193-201.