SPE-44 implements sperm cell fate

PLoS Genetics

Volumn 8, Issue 4, 2012, Pages

  Kulkarni, Madhura ^a,d   Shakes, Diane C ^b   Guevel, Katie ^b   Smith, Harold E ^c  

^a University of Maryland   (United States)

^b William and Mary   (United States)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; SPE 44 PROTEIN; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; SPE 44 PROTEIN,C ELEGANS; SPE-44 PROTEIN,C ELEGANS;

ARTICLE; AUTOSOME; CAENORHABDITIS ELEGANS; CELL CYCLE PROGRESSION; CELL DAMAGE; CELL FATE; CELL ORGANELLE; CONTROLLED STUDY; CYTOKINESIS; GENE CONTROL; GENE DELETION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENETIC CONSERVATION; NONHUMAN; PROTEIN LOCALIZATION; REGULATOR GENE; SEX DETERMINATION; SPE 44 GENE; SPERM; SPERMATOGENESIS; TRANSCRIPTION REGULATION; X CHROMOSOME; ANIMAL; CELL CYCLE CHECKPOINT; CELL DIFFERENTIATION; CELL LINEAGE; CHROMATIN; CYTOLOGY; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; SEX DETERMINATION PROCESS; SIGNAL TRANSDUCTION; SPERMATOZOON; STEM CELL;

CAENORHABDITIS; CAENORHABDITIS ELEGANS;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL CYCLE CHECKPOINTS; CELL DIFFERENTIATION; CELL LINEAGE; CHROMATIN; CYTOKINESIS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; SEX DETERMINATION PROCESSES; SIGNAL TRANSDUCTION; SPERMATOGENESIS; SPERMATOZOA; STEM CELLS; TRANSCRIPTION, GENETIC;

EID: 84860594312     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002678     Document Type: Article

References (81)

1. Tapscott SJ, Davis RL, Thayer MJ, Cheng PF, Weintraub H, et al. (1988) MyoD1: a nuclear phosphoprotein requiring a Myc homology region to convert fibroblasts to myoblasts. Science 242: 405-411.
2. Kimble J, Crittenden SL, (2007) Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans. Ann Rev Cell Dev Biol 23: 405-433.
3. Morgan CT, Lee MH, Kimble J, (2010) Chemical reprogramming of Caenorhabditis elegans germ cell fate. Nat Chem Biol 6: 102-104.
4. Tursun B, Patel T, Kratsios P, Hobert O, (2011) Direct conversion of C. elegans germ cells into specific neuron types. Science 331: 304-308.
5. Zarkower D, (2006) Somatic sex determination. WormBook Feb 10: 1-12.
6. Hodgkin J, (1993) Molecular cloning and duplication of the nematode sex-determining gene tra-1. Genetics 133: 543-560.
7. Zarkower D, Hodgkin J, (1992) Molecular analysis of the C. elegans sex-determining gene tra-1: a gene encoding two zinc finger proteins. Cell 70: 237-249.
8. Yi W, Ross JM, Zarkower D, (2000) Mab-3 is a direct tra-1 target gene regulating diverse aspects of C. elegans male sexual development and behavior. Development 127: 4469-4480.
9. Conradt B, Horvitz HR, (1999) The TRA-1 sex determination protein of C. elegans regulates sexually dimorphic cell deaths by repressing the egl-1 cell death activator gene. Cell 98: 317-327.
10. Peden E, Kimberly E, Gengyo-Ando K, Mitani S, Xue D, (2007) Control of sex-specific apoptosis in C. elegans by the BarH homeodomain protein CEH-30 and the transcriptional repressor UNC-37/Groucho. Genes Dev 21: 3195-3207.
11. Schwartz HT, Horvitz HR, (2007) The C. elegans protein CEH-30 protects male-specific neurons from apoptosis independently of the Bcl-2 homolog CED-9. Genes Dev 21: 181-194.
12. Szabo E, Hargitai B, Regos A, Tihanyi B, Barna J, et al. (2009) TRA-1/GLI controls the expression of the Hox gene lin-39 during C. elegans vulval development. Dev Biol 330: 339-348.
13. Mason DA, Rabinowitz JS, Portman DS, (2008) dmd-3, a doublesex-related gene regulated by tra-1, governs sex-specific morphogenesis in C. elegans. Development 135: 2373-2382.
14. Spence AM, Coulson A, Hodgkin J, (1990) The product of fem-1, a nematode sex-determining gene, contains a motif found in cell cycle control proteins and receptors for cell-cell interactions. Cell 60: 981-990.
15. Pilgrim D, McGregor A, Jackle P, Johnson T, Hansen D, (1995) The C. elegans sex-determining gene fem-2 encodes a putative protein phosphatase. Mol Biol Cell 6: 1159-1171.
16. 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.
17. Starostina NG, Lim JM, Schvarzstein M, Wells L, Spence AM, et al. (2007) A CUL-2 ubiquitin ligase containing the three FEM proteins degrades TRA-1 to regulate C. elegans sex determination. Dev Cell 13: 127-139.
18. Luitjens C, Gallegos M, Kraemer B, Kimble J, Wickens M, (2000) CPEB proteins control two key steps in spermatogenesis in C. elegans. Genes Dev 14: 2596-2609.
19. Chen PJ, Singal A, Kimble J, Ellis RE, (2000) A novel member of the tob family of proteins controls sexual fate in Caenorhabditis elegans germ cells. Dev Biol 217: 77-90.
20. Winkler GS, (2010) The mammalian anti-proliferative BTG/Tob protein family. J Cell Physiol 222: 66-72.
21. Lee MH, Won Kim K, Morgan CT, Morgan DE, Kimble H, (2011) Phosphorylation state of a Tob/BTG protein, FOG-3, regulates initiation and maintenance of the Caenorhabditis elegans sperm fate program. Proc Natl Acad Sci USA 108: 9125-2130.
22. Reinke V, Smith HE, Nance J, Wang J, Van Doren C, et al. (2000) A global profile of germline gene expression in C. elegans. Mol Cell 6: 605-616.
23. Reinke V, Gil IS, Ward S, Kazmer K, (2004) Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 131: 311-323.
24. Nishimura H, L'Hernault SW, (2010) Spermatogenesis-defective (spe) mutants of the nematode Caenorhabditis elegans provide clues to solve the puzzle of male germline functions during reproduction. Dev Dyn 239: 1502-1514.
25. Merritt C, Rasoloson D, Ko D, Seydoux G, (2008) 3′ UTRs are the primary regulators of gene expression in the C. elegans germline. Curr Biol 18: 1476-1482.
26. Hodgkin J, (1987) A genetic analysis of the sex-determining gene, tra-1, in the nematode Caenorhabditis elegans. Genes Dev 1: 731-745.
27. Schedl T, Graham PL, Barton MK, Kimble J, (1989) Analysis of the role of tra-1 in germline sex determination in the nematode Caenorhabditis elegans. Genetics 123: 755-769.
28. 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.
29. Ellis RE, Kimble J, (1995) The fog-3 gene and regulation of cell fate in the germ line of Caenorhabditis elegans. Genetics 139: 561-577.
30. Chen P, Ellis RE, (2000) TRA-1A regulates transcription of fog-3, which controls germ cell fate in C. elegans. Development 127: 3119-3129.
31. Doniach T, Hodgkin J, (1984) A sex-determining gene, fem-1, required for both male and hermaphrodite development in Caenorhabditis elegans. Dev Biol 106: 223-235.
32. Hodgkin J, (1986) Sex determination in the nematode C. elegans: analysis of tra-3 suppressors and characterization of fem genes. Genetics 114: 15-52.
33. del Castillo-Olivares A, Kulkarni M, Smith HE, (2009) Regulation of sperm gene expression by the GATA factor ELT-1. Dev Biol 333: 397-408.
34. Page BD, Zhang W, Steward K, Blumenthal T, Priess JR, (1997) ELT-1, a GATA-like transcription factor, is required for epidermal cell fates in Caenorhabditis elegans. Genes Dev 11: 1651-1661.
35. Smith JA, McGarr P, Gilleard JS, (2005) The Caenorhabditis elegans GATA factor elt-1 is essential for differentiation and maintenance of hypodermal seam cells and for normal location. J Cell Sci 118: 5709-5719.
36. Gibson TJ, Ramu C, Gemund C, Aasland R, (1998) The APECED polyglandular autoimmune syndrome protein, AIRE-1, contains the SAND domain and is probably a transcription factor. Trends Biochem Sci 23: 242-244.
37. Zeng H, Jackson DA, Oshima H, Simons SS Jr, (1998) Cloning and characterization of a novel binding factor (GMEB-2) of the glucocorticoid modulatory element. J Biol Chem 273: 17756-17762.
38. Theriault JR, Charette SJ, Lambert H, Landry J, (1999) Cloning and characterization of hGMEB1, a novel glucocorticoid modulatory element binding protein. FEBS Lett 452: 170-176.
39. Oshima H, Szapary D, Simons SS Jr, (1995) The factor binding to the glucococorticoid modulatory element of the tyrosine aminotransferase gene is a novel and ubiquitous heteromeric complex. J Biol Chem 270: 21893-21901.
40. Gross CT, McGinnis W, (1996) DEAF-1, a novel protein that binds an essential region in a Deformed response element. EMBO J 15: 1961-1970.
41. Bottomley MJ, Collard MW, Huggenvik JI, Liu Z, Gibson TJ, et al. (2001) The SAND domain structure defines a novel DNA-binding fold in transcriptional regulation. Nat Struct Biol 8: 626-633.
42. Surdo PL, Bottomley MJ, Sattler M, Scheffzek K, (2003) Crystal structure and nuclear magnetic resonance analyses of the SAND domain from glucococorticoid modulatory element binding protein-1 reveal deoxyribonucleic acid and zinc binding regions. Mol Endocrinol 17: 1283-1295.
43. Moerman DG, Barstead RJ, (2008) Towards a mutation in every gene in Caenorhabditis elegans. Brief Funct Genomic Proteomic 7: 195-204.
44. Wolf N, Hirsh D, McIntosh JR, (1978) Spermatogenesis in males of the free-living nematode, Caenorhabditis elegans. J Ultrastruct Res 63: 155-169.
45. Ward S, Argon Y, Nelson GA, (1981) Sperm morphogenesis in wild-type and fertilization-defective mutants of Caenorhabditis elegans. J Cell Biol 91: 26-44.
46. Shakes DC, Wu JC, Sadler PL, Laprade K, Moore LL, et al. (2009) Spermatogenesis-specific features of the meiotic program in Caenorhabditis elegans. PLoS Genet 5: e1000611 doi:10.1371/journal.pgen.1000611.
47. Crosio C, Fimia GM, Loury R, Kimura M, Okano Y, et al. (2002) Mitotic phosphorylation of histone H3: spatio-temporal regulation by mammalian Aurora kinases. Mol Cell Biol 22: 874-885.
48. Davis FM, Tsao TY, Fowler SK, Rao PN, (1983) Monoclonal antibodies to mitotic cells. Proc Natl Acad Sci USA 80: 2926-2930.
49. Okamoto H, Thomson JN, (1985) Monoclonal antibodies which distinguish certain classes of neuronal and supporting cells in the nervous tissue of the nematode Caenorhabditis elegans. J Neurosci 5: 643-653.
50. Burke DJ, Ward S, (1983) Identification of a large multigene family encoding the major sperm protein of Caenorhabditis elegans. J Mol Biol 171: 1-29.
51. Sepsenwol S, Ris H, Roberts TM, (1989) A unique cytoskeleton associated with crawling in the amoeboid sperm of the nematode, Ascaris suum. J Cell Biol 108: 55-66.
52. Miller MA, Nguyen VQ, Lee MH, Kosinski M, Schedl T, et al. (2001) A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 291: 2144-2147.
53. Schormann N, Symersky J, Luo M, (2004) Structure of sperm-specific protein SSP-19 from Caenorhabditis elegans. Acta Crystallogr D Biol Crystallogr 60: 1840-1845.
54. Yi K, Wang X, Emmett MR, Marshall AG, Stewart M, et al. (2009) Dephosphorylation of major sperm protein (MSP) fiber protein 3 by protein phosphatase 2A during cell body retraction in the MSP-based amoeboid motility of Ascaris sperm. Mol Biol Cell 20: 3200-3208.
55. Ward S, Miwa J, (1978) Characterization of temperature-sensitive, fertilization-defective mutants of the nematode Caenorhabditis elegans. Genetics 88: 285-303.
56. Argon Y, Ward S, (1980) Caenorhabditis elegans fertilization-defective mutants with abnormal sperm. Genetics 96: 413-433.
57. L'Hernault SW, Shakes DC, Ward S, (1988) Developmental genetics of chromosome I spermatogenesis-defective mutants in the nematode Caenorhabditis elegans. Geletics 120: 435-452.
58. Li JJ, Herskowitz I, (1993) Isolation of ORC6, a component of the yeast origin recognition complex by a one-hybrid system. Science 262: 1970-1874.
59. Kelly WG, Schaner CE, Dernberg AF, Lee MH, Kim SK, et al. (2002) X-chromosome silencing in the germline of C. elegans. Development 129: 479-492.
60. Shakes DC, Ward S, (1989) Mutations that disrupt the morphogenesis and localization of a sperm-specific organelle in Caenorhabditis elegans. Dev Biol 134: 307-316.
61. L'Hernault SW, Benian GM, Emmons RB, (1993) Genetic and molecular characterization of the Caenorhabditis elegans spermatogenesis-defective gene spe-17. Genetics 134: 769-780.
62. Visintin R, Craig K, Hwang ES, Prinz S, Tyers M, et al. (1998) The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk-dependent phosphorylation. Mol Cell 2: 709-718.
63. Kaul S, Blackford JA Jr, Chen J, Ogryzko VV, Simons SS Jr, (2000) Properties of the glucocorticoid modulatory element binding proteins GMEB-1 and-2: potential new modifiers of glucocorticoid receptor transactivation and members of the family of KDWK proteins. Mol Endocrinol 14: 1010-1027.
64. Abramson J, Giraud M, Benoist C, Mathis D, (2010) Aire's partners in the molecular control of immunological tolerance. Cell 140: 123-145.
65. Lehming N, Le Saux A, Schuller, Ptashne M, (1998) Chromatin components as part of a putative transcriptional repressing complex. Proc Natl Acad Sci USA 95: 7322-7326.
66. Seeler JS, Marchio A, Sitterlin D, Transy C, Dejean A, (1998) Interaction of SP100 with PH1 proteins: a link between the promyelocytic leukemia-associated nuclear bodies and the chromatin compartment. Proc Natl Acad Sci USA 95: 7316-7321.
67. Carles CC, Fletcher JC, (2009) The SAND domain protein ULTRAPETALA1 acts as a trithorax group factor to regulate cell fate in plants. Genes Dev 23: 2723-2728.
68. Cho S, Jin SW, Cohen A, Ellis RE, (2004) A phylogeny of Caenorhabditis reveals frequent loss of introns during nematode evolution. Genome Res 14: 1207-1220.
69. Kiontke K, Gavin NP, Raynes Y, Roehrig C, Piano F, et al. (2004) Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc Natl Acad Sci USA 101: 9003-9008.
70. Nayak S, Goree J, Schedl T, (2005) fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis. PLoS Biol 3: e6 doi:10.1371/journal.pbio.0030006.
71. Guo Y, Lang S, Ellis RE, (2009) Independent recruitment of F box genes to regulate hermaphrodite development during nematode evolution. Curr Biol 19: 1853-1860.
72. Hill RC, Haag ES, (2009) A sensitized genetic background reveals evolution near the terminus of the Caenorhabditis germline sex determination pathway. Evol Dev 11: 333-342.
73. Zarkower D, Hodgkin J, (1993) Zinc fingers in sex determination: only one of the two C. elegans TRA-1 proteins binds DNA in vitro. Nucleic Acids Res 21: 3691-3698.
74. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
75. Mello CC, Kramer JM, Stinchcomb D, Ambros V, (1991) Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10: 3959-3970.
76. Kelly WG, Xu S, Montgomery MK, Fire A, (1997) Distinct requirements for somatic and germline expression of a generally expressed Caernorhabditis elegans gene. Genetics 146: 227-238.
77. Gyuris J, Golemis E, Chertkov H, Brent R, (1993) Cdi1, a human G1 and S phase protein phosphatase that associates with Cdk2. Cell 75: 791-803.
78. L'Hernault SW, Arduengo PM, (1992) Mutation of a putative sperm membrane protein in Caenorhabditis elegans prevents sperm differentiation but not its associated meiotic divisions. J Cell Biol 119: 55-68.
79. Rose MD, Winston F, Hieter P, (1990) Methods in Yeast Genetics: A Laboratory Course Manual CSHL Press, Cold Spring Harbor, NY.
80. Lee MH, Schedl T, WormBook, The C. elegans Research Community, editors (2006) RNA in situ hybridization of dissected gonads.
81. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.