The sperm-oocyte switch in the C. elegans hermaphrodite is controlled through steady-state levels of the fem-3 mRNA

RNA

Volumn 18, Issue 7, 2012, Pages 1385-1394

  Zanetti, Simone ^a   Grinschgl, Sonja ^a   Meola, Marco ^a   Belfiore, Marco ^a   Rey, Samantha ^a   Bianchi, Pamela ^a   Puoti, Alessandro ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

Author keywords

Caenorhabditis elegans; Fem 3; Germline; RNA; Sex determination

Indexed keywords

FEM 3 MESSENGER RNA; MESSENGER RNA; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; GAIN OF FUNCTION MUTATION; GERM CELL; HERMAPHRODITIC SPECIES; NONHUMAN; OOCYTE; POLYSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPERMATOCYTE; SPERMATOGENESIS; STEADY STATE;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, SWITCH; HERMAPHRODITIC ORGANISMS; HETEROZYGOTE; MALE; OOCYTES; OOGENESIS; PROTEIN BINDING; RNA, MESSENGER; RNA-BINDING PROTEINS; SPERMATOGENESIS; SPERMATOZOA;

EID: 84862562510     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.031237.111     Document Type: Article

References (54)

1. Ahringer J, Kimble J. 1991. Control of the sperm-oocyte switch in Caenorhabditis elegans hermaphrodites by the fem-3 3′ untranslated region. Nature 349: 346-348.
2. Ahringer J, Rosenquist TA, Lawson DN, Kimble J. 1992. The Caenorhabditis elegans sex determining gene fem-3 is regulated post-transcriptionally. EMBO J 11: 2303-2310.
3. Arur S, OhmachiM, Berkseth M, Nayak S, Hansen D, Zarkower D, Schedl T. 2011. MPK-1 ERK controls membrane organization in C. elegans oogenesis via a sex-determination module. Dev Cell 20: 677-688.
4. Barker DD, Wang C, Moore J, Dickinson LK, Lehmann R. 1992. Pumilio is essential for function but not for distribution of the Drosophila abdominal determinant Nanos. Genes Dev 6: 2312-2326.
5. Barton MK, Kimble J. 1990. fog-1, a regulatory gene required for specification of spermatogenesis in the germ line of Caenorhabditis elegans. Genetics 125: 29-39.
6. Barton MK, Schedl TB, Kimble J. 1987. Gain-of-function mutations of fem-3, a sex-determination gene in Caenorhabditis elegans. Genetics 115: 107-119.
7. Belfiore M, Pugnale P, Saudan Z, Puoti A. 2004. Roles of the C. elegans cyclophilin-like protein MOG-6 in MEP-1 binding and germline fates. Development 131: 2935-2945.
8. Bernstein P, Ross J. 1989. Poly(a), Poly(a) binding-protein and the regulation of messenger-RNA stability. Trends Biochem Sci 14: 373-377.
9. Bernstein D, Hook B, Hajarnavis A, Opperman L, Wickens M. 2005. Binding specificity and mRNA targets of a C. elegans PUF protein, FBF-1. RNA 11: 447-458.
10. Bettinger JC, Lee K, Rougvie AE. 1996. Stage-specific accumulation of the terminal differentiation factor LIN-29 during Caenorhabditis elegans development. Development 122: 2517-2527.
11. Brengues M, Teixeira D, Parker R. 2005. Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310: 486-489.
12. Crittenden SL, Bernstein DS, Bachorik JL, Thompson BE, Gallegos M, Petcherski AG, Moulder G, Barstead R, Wickens M, Kimble J. 2002. A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417: 660-663.
13. Decker CJ, Parker R. 1993. A turnover pathway for both stable and unstable mRNAs in yeast: Evidence for a requirement for deadenylation. Genes Dev 7: 1632-1643.
14. Ding XC, Grosshans H. 2009. Repression of C. elegans microRNA targets at the initiation level of translation requires GW182 proteins. EMBO J 28: 213-222.
15. Doniach T. 1986. Activity of the sex-determining gene tra-2 is modulated to allow spermatogenesis in the C. elegans hermaphrodite. Genetics 114: 53-76.
16. Epstein HF, Shakes DC. 1995. Caenorhabditis elegans: Modern biological analysis of an organism. Academic Press, Waltham, MA.
17. Evans TC, Crittenden SL, Kodoyianni V, Kimble J. 1994. Translational control of maternal glp-1 mRNA establishes an asymmetry in the C. elegans embryo. Cell 77: 183-194.
18. Gallegos M, Ahringer J, Crittenden S, Kimble J. 1998. Repression by the 3′ UTR of fem-3, a sex-determining gene, relies on a ubiquitous mog-dependent control in Caenorhabditis elegans. EMBO J 17: 6337-6347.
19. Goodwin EB, Okkema PG, Evans TC, Kimble J. 1993. Translational regulation of tra-2 by its 3′ untranslated region controls sexual identity in C. elegans. Cell 75: 329-339.
20. Graham PL, Kimble J. 1993. The mog-1 gene is required for the switch from spermatogenesis to oogenesis in Caenorhabditis elegans. Genetics 133: 919-931.
21. Graham PL, Schedl T, Kimble J. 1993. More mog genes that influence the switch from spermatogenesis to oogenesis in the hermaphrodite germ line of Caenorhabditis elegans. Dev Genet 14: 471-484.
22. Grant B, Hirsh D. 1999. Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol Biol Cell 10: 4311-4326.
23. Haag ES, Wang S, Kimble J. 2002. Rapid coevolution of the nematode sex-determining genes fem-3 and tra-2. Curr Biol 12: 2035-2041.
24. Hodgkin J. 1986. Sex determination in the nematode C. elegans: Analysis of tra-3 suppressors and characterization of fem genes. Genetics 114: 15-52.
25. Jones AR, Francis R, Schedl T. 1996. GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage- and sex-specific expression during Caenorhabditis elegans germline development. Dev Biol 180: 165-183.
26. Kasturi P, Zanetti S, Passannante M, Saudan Z, Muller F, Puoti A. 2010. The C. elegans sex determination protein MOG-3 functions in meiosis and binds to the CSL co-repressor CIR-1. Dev Biol 344: 593-602.
27. Kim KW, Nykamp K, Suh N, Bachorik JL, Wang L, Kimble J. 2009. Antagonism between GLD-2 binding partners controls gamete sex. Dev Cell 16: 723-733.
28. Kretsinger RH, Manner G, Gould BS, Rich A. 1964. Synthesis of collagen on polyribosomes. Nature 202: 438-441.
29. Lamont LB, Crittenden SL, Bernstein D, Wickens M, Kimble J. 2004. FBF-1 and FBF-2 regulate the size of the mitotic region in the C. elegans germline. Dev Cell 7: 697-707.
30. Lee MH, Hook B, Lamont LB, Wickens M, Kimble J. 2006. LIP-1 phosphatase controls the extent of germline proliferation in Caenorhabditis elegans. EMBO J 25: 88-96.
31. Macdonald PM. 1992. The Drosophila pumilio gene: An unusually long transcription unit and an unusual protein. Development 114: 221-232.
32. Marin VA, Evans TC. 2003. Translational repression of a C. elegans Notch mRNA by the STAR/KH domain protein GLD-1. Development 130: 2623-2632.
33. Noble SC, Allen BL, Goh LK, Nordick K, Evans TC. 2008. Maternal mRNAs are regulated by diverse P body-related mRNP granules during early Caenorhabditis elegans development. J Cell Biol 182: 559-572.
34. Nykamp K, Lee MH, Kimble J. 2008. C. elegans La-related protein, LARP-1, localizes to germline P bodies and attenuates Ras-MAPK signaling during oogenesis. RNA 14: 1378-1389.
35. Olivas W, Parker R. 2000. The Puf3 protein is a transcript-specific regulator of mRNA degradation in yeast. EMBO J 19: 6602-6611.
36. Puoti A, Kimble J. 1999. The Caenorhabditis elegans sex determination gene mog-1 encodes a member of the DEAH-Box protein family. Mol Cell Biol 19: 2189-2197.
37. Puoti A, Kimble J. 2000. The hermaphrodite sperm/oocyte switch requires the Caenorhabditis elegans homologs of PRP2 and PRP22. Proc Natl Acad Sci 97: 3276-3281.
38. Rosenquist TA, Kimble J. 1988. Molecular cloning and transcript analysis of fem-3, a sex-determination gene in Caenorhabditis elegans. Genes Dev 2: 606-616.
39. Sachs A. 2000. Physical and functional interactions between the mRNA cap structure and the poly(A) tail. In Translational control of gene expression (ed. N Sonenberg et al.), pp. 447-465. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. Salles FJ, Strickland S. 1995. Rapid and sensitive analysis of mRNA polyadenylation states by PCR. PCR Methods Appl 4: 317-321.
41. Sassi HE, Renihan S, Spence AM, Cooperstock RL. 2005. Gene CATCHR - gene cloning and tagging for Caenorhabditis elegans using yeast homologous recombination: A novel approach for the analysis of gene expression. Nucleic Acids Res 33: e163. doi: 10.1093/nar/gni164.
42. Schmid M, Kuchler B, Eckmann CR. 2009. Two conserved regulatory cytoplasmic poly(A) polymerases, GLD-4 and GLD-2, regulate meiotic progression in C. elegans. Genes Dev 23: 824-836.
43. Scott RB, Bell E. 1964. Protein synthesis during development - control through messenger RNA. Science 145: 711-714.
44. Stafford DW, Iverson RM, Sofer WH. 1964. Demonstration of polyribosomes after fertilization of sea urchin egg. Proc Natl Acad Sci 52: 313-316.
45. Starostina NG, Lim JM, Schvarzstein M, Wells L, Spence AM, Kipreos ET. 2007. A CUL-2 ubiquitin ligase containing three FEM proteins degrades TRA-1 to regulate C. elegans sex determination. Dev Cell 13: 127-139.
46. Tadauchi T, Matsumoto K, Herskowitz I, Irie K. 2001. Post-transcriptional regulation through the HO 3′-UTR by Mpt5, a yeast homolog of Pumilio and FBF. EMBO J 20: 552-561.
47. Ward S, Roberts TM, Strome S, Pavalko FM, Hogan E. 1986. Monoclonal antibodies that recognize a polypeptide antigenic determinant shared by multiple Caenorhabditis elegans sperm-specific proteins. J Cell Biol 102: 1778-1786.
48. Wharton RP, Sonoda J, Lee T, Patterson M, Murata Y. 1998. The Pumilio RNA-binding domain is also a translational regulator. Mol Cell 1: 863-872.
49. Wickens M, Goodwin EB, Kimble J, Strickland S, Hentze MW. 2000. Translational control of developmental decisions. In Translational control of gene expression (ed. N Sonenberg et al.), pp. 295-370. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
50. Wreden C, Verrotti AC, Schisa JA, Lieberfarb ME, Strickland S. 1997. Nanos and pumilio establish embryonic polarity in Drosophila by promoting posterior deadenylation of hunchback mRNA. Development 124: 3015-3023.
51. Zanetti S, Meola M, Bochud A, Puoti A. 2011. Role of the C. elegans U2 snRNP protein MOG-2 in sex determination, meiosis, and splice site selection. Dev Biol 354: 232-241.
52. Zanin E, Pacquelet A, Scheckel C, Ciosk R, Gotta M. 2010. LARP-1 promotes oogenesis by repressing fem-3 in the C. elegans germline. J Cell Sci 123: 2717-2724.
53. Zhang B, Gallegos M, Puoti A, Durkin E, Fields S, Kimble J, Wickens MP. 1997. A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line. Nature 390: 477-484.
54. Zhao S, Fernald RD. 2005. Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 12: 1047-1064.