SPE-44 Implements Sperm Cell Fate
The sperm/oocyte decision in the hermaphrodite germline of Caenorhabditis elegans provides a powerful model for the characterization of stem cell fate specification and differentiation. The germline sex determination program that governs gamete fate has been well studied, but direct mediators of cell-type-specific transcription are largely unknown. We report the identification of spe-44 as a critical regulator of sperm gene expression. Deletion of spe-44 causes sperm-specific defects in cytokinesis, cell cycle progression, and organelle assembly resulting in sterility. Expression of spe-44 correlates precisely with spermatogenesis and is regulated by the germline sex determination pathway. spe-44 is required for the appropriate expression of several hundred sperm-enriched genes. The SPE-44 protein is restricted to the sperm-producing germline, where it localizes to the autosomes (which contain sperm genes) but is excluded from the transcriptionally silent X chromosome (which does not). The orthologous gene in other Caenorhabditis species is similarly expressed in a sex-biased manner, and the protein likewise exhibits autosome-specific localization in developing sperm, strongly suggestive of an evolutionarily conserved role in sperm gene expression. Our analysis represents the first identification of a transcriptional regulator whose primary function is the control of gamete-type-specific transcription in this system.
Vyšlo v časopise:
SPE-44 Implements Sperm Cell Fate. PLoS Genet 8(4): e32767. doi:10.1371/journal.pgen.1002678
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002678
Souhrn
The sperm/oocyte decision in the hermaphrodite germline of Caenorhabditis elegans provides a powerful model for the characterization of stem cell fate specification and differentiation. The germline sex determination program that governs gamete fate has been well studied, but direct mediators of cell-type-specific transcription are largely unknown. We report the identification of spe-44 as a critical regulator of sperm gene expression. Deletion of spe-44 causes sperm-specific defects in cytokinesis, cell cycle progression, and organelle assembly resulting in sterility. Expression of spe-44 correlates precisely with spermatogenesis and is regulated by the germline sex determination pathway. spe-44 is required for the appropriate expression of several hundred sperm-enriched genes. The SPE-44 protein is restricted to the sperm-producing germline, where it localizes to the autosomes (which contain sperm genes) but is excluded from the transcriptionally silent X chromosome (which does not). The orthologous gene in other Caenorhabditis species is similarly expressed in a sex-biased manner, and the protein likewise exhibits autosome-specific localization in developing sperm, strongly suggestive of an evolutionarily conserved role in sperm gene expression. Our analysis represents the first identification of a transcriptional regulator whose primary function is the control of gamete-type-specific transcription in this system.
Zdroje
1. TapscottSJDavisRLThayerMJChengPFWeintraubH 1988 MyoD1: a nuclear phosphoprotein requiring a Myc homology region to convert fibroblasts to myoblasts. Science 242 405 411
2. KimbleJCrittendenSL 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. MorganCTLeeMHKimbleJ 2010 Chemical reprogramming of Caenorhabditis elegans germ cell fate. Nat Chem Biol 6 102 104
4. TursunBPatelTKratsiosPHobertO 2011 Direct conversion of C. elegans germ cells into specific neuron types. Science 331 304 308
5. ZarkowerD 2006 Somatic sex determination. WormBook Feb 10 1 12
6. HodgkinJ 1993 Molecular cloning and duplication of the nematode sex-determining gene tra-1. Genetics 133 543 560
7. ZarkowerDHodgkinJ 1992 Molecular analysis of the C. elegans sex-determining gene tra-1: a gene encoding two zinc finger proteins. Cell 70 237 249
8. YiWRossJMZarkowerD 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. ConradtBHorvitzHR 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. PedenEKimberlyEGengyo-AndoKMitaniSXueD 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. SchwartzHTHorvitzHR 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. SzaboEHargitaiBRegosATihanyiBBarnaJ 2009 TRA-1/GLI controls the expression of the Hox gene lin-39 during C. elegans vulval development. Dev Biol 330 339 348
13. MasonDARabinowitzJSPortmanDS 2008 dmd-3, a doublesex-related gene regulated by tra-1, governs sex-specific morphogenesis in C. elegans. Development 135 2373 2382
14. SpenceAMCoulsonAHodgkinJ 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. PilgrimDMcGregorAJacklePJohnsonTHansenD 1995 The C. elegans sex-determining gene fem-2 encodes a putative protein phosphatase. Mol Biol Cell 6 1159 1171
16. RosenquistTAKimbleJ 1988 Molecular cloning and transcript analysis of fem-3, a sex-determination gene in Caenorhabditis elegans. Genes Dev 2 606 616
17. StarostinaNGLimJMSchvarzsteinMWellsLSpenceAM 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. LuitjensCGallegosMKraemerBKimbleJWickensM 2000 CPEB proteins control two key steps in spermatogenesis in C. elegans. Genes Dev 14 2596 2609
19. ChenPJSingalAKimbleJEllisRE 2000 A novel member of the tob family of proteins controls sexual fate in Caenorhabditis elegans germ cells. Dev Biol 217 77 90
20. WinklerGS 2010 The mammalian anti-proliferative BTG/Tob protein family. J Cell Physiol 222 66 72
21. LeeMHWon KimKMorganCTMorganDEKimbleH 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. ReinkeVSmithHENanceJWangJVan DorenC 2000 A global profile of germline gene expression in C. elegans. Mol Cell 6 605 616
23. ReinkeVGilISWardSKazmerK 2004 Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 131 311 323
24. NishimuraHL'HernaultSW 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. MerrittCRasolosonDKoDSeydouxG 2008 3′ UTRs are the primary regulators of gene expression in the C. elegans germline. Curr Biol 18 1476 1482
26. HodgkinJ 1987 A genetic analysis of the sex-determining gene, tra-1, in the nematode Caenorhabditis elegans. Genes Dev 1 731 745
27. SchedlTGrahamPLBartonMKKimbleJ 1989 Analysis of the role of tra-1 in germline sex determination in the nematode Caenorhabditis elegans. Genetics 123 755 769
28. BartonMKKimbleJ 1990 fog-1, a regulatory gene required for specification of spermatogenesis in the germ line of Caenorhabditis elegans. Genetics 125 29 39
29. EllisREKimbleJ 1995 The fog-3 gene and regulation of cell fate in the germ line of Caenorhabditis elegans. Genetics 139 561 577
30. ChenPEllisRE 2000 TRA-1A regulates transcription of fog-3, which controls germ cell fate in C. elegans. Development 127 3119 3129
31. DoniachTHodgkinJ 1984 A sex-determining gene, fem-1, required for both male and hermaphrodite development in Caenorhabditis elegans. Dev Biol 106 223 235
32. HodgkinJ 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-OlivaresAKulkarniMSmithHE 2009 Regulation of sperm gene expression by the GATA factor ELT-1. Dev Biol 333 397 408
34. PageBDZhangWStewardKBlumenthalTPriessJR 1997 ELT-1, a GATA-like transcription factor, is required for epidermal cell fates in Caenorhabditis elegans. Genes Dev 11 1651 1661
35. SmithJAMcGarrPGilleardJS 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. GibsonTJRamuCGemundCAaslandR 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. ZengHJacksonDAOshimaHSimonsSSJr 1998 Cloning and characterization of a novel binding factor (GMEB-2) of the glucocorticoid modulatory element. J Biol Chem 273 17756 17762
38. TheriaultJRCharetteSJLambertHLandryJ 1999 Cloning and characterization of hGMEB1, a novel glucocorticoid modulatory element binding protein. FEBS Lett 452 170 176
39. OshimaHSzaparyDSimonsSSJr 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. GrossCTMcGinnisW 1996 DEAF-1, a novel protein that binds an essential region in a Deformed response element. EMBO J 15 1961 1970
41. BottomleyMJCollardMWHuggenvikJILiuZGibsonTJ 2001 The SAND domain structure defines a novel DNA-binding fold in transcriptional regulation. Nat Struct Biol 8 626 633
42. SurdoPLBottomleyMJSattlerMScheffzekK 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. MoermanDGBarsteadRJ 2008 Towards a mutation in every gene in Caenorhabditis elegans. Brief Funct Genomic Proteomic 7 195 204
44. WolfNHirshDMcIntoshJR 1978 Spermatogenesis in males of the free-living nematode, Caenorhabditis elegans. J Ultrastruct Res 63 155 169
45. WardSArgonYNelsonGA 1981 Sperm morphogenesis in wild-type and fertilization-defective mutants of Caenorhabditis elegans. J Cell Biol 91 26 44
46. ShakesDCWuJCSadlerPLLapradeKMooreLL 2009 Spermatogenesis-specific features of the meiotic program in Caenorhabditis elegans. PLoS Genet 5 e1000611 doi:10.1371/journal.pgen.1000611
47. CrosioCFimiaGMLouryRKimuraMOkanoY 2002 Mitotic phosphorylation of histone H3: spatio-temporal regulation by mammalian Aurora kinases. Mol Cell Biol 22 874 885
48. DavisFMTsaoTYFowlerSKRaoPN 1983 Monoclonal antibodies to mitotic cells. Proc Natl Acad Sci USA 80 2926 2930
49. OkamotoHThomsonJN 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. BurkeDJWardS 1983 Identification of a large multigene family encoding the major sperm protein of Caenorhabditis elegans. J Mol Biol 171 1 29
51. SepsenwolSRisHRobertsTM 1989 A unique cytoskeleton associated with crawling in the amoeboid sperm of the nematode, Ascaris suum. J Cell Biol 108 55 66
52. MillerMANguyenVQLeeMHKosinskiMSchedlT 2001 A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 291 2144 2147
53. SchormannNSymerskyJLuoM 2004 Structure of sperm-specific protein SSP-19 from Caenorhabditis elegans. Acta Crystallogr D Biol Crystallogr 60 1840 1845
54. YiKWangXEmmettMRMarshallAGStewartM 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. WardSMiwaJ 1978 Characterization of temperature-sensitive, fertilization-defective mutants of the nematode Caenorhabditis elegans. Genetics 88 285 303
56. ArgonYWardS 1980 Caenorhabditis elegans fertilization-defective mutants with abnormal sperm. Genetics 96 413 433
57. L'HernaultSWShakesDCWardS 1988 Developmental genetics of chromosome I spermatogenesis-defective mutants in the nematode Caenorhabditis elegans. Geletics 120 435 452
58. LiJJHerskowitzI 1993 Isolation of ORC6, a component of the yeast origin recognition complex by a one-hybrid system. Science 262 1970 1874
59. KellyWGSchanerCEDernbergAFLeeMHKimSK 2002 X-chromosome silencing in the germline of C. elegans. Development 129 479 492
60. ShakesDCWardS 1989 Mutations that disrupt the morphogenesis and localization of a sperm-specific organelle in Caenorhabditis elegans. Dev Biol 134 307 316
61. L'HernaultSWBenianGMEmmonsRB 1993 Genetic and molecular characterization of the Caenorhabditis elegans spermatogenesis-defective gene spe-17. Genetics 134 769 780
62. VisintinRCraigKHwangESPrinzSTyersM 1998 The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk-dependent phosphorylation. Mol Cell 2 709 718
63. KaulSBlackfordJAJrChenJOgryzkoVVSimonsSSJr 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. AbramsonJGiraudMBenoistCMathisD 2010 Aire's partners in the molecular control of immunological tolerance. Cell 140 123 145
65. LehmingNLe SauxASchullerPtashneM 1998 Chromatin components as part of a putative transcriptional repressing complex. Proc Natl Acad Sci USA 95 7322 7326
66. SeelerJSMarchioASitterlinDTransyCDejeanA 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. CarlesCCFletcherJC 2009 The SAND domain protein ULTRAPETALA1 acts as a trithorax group factor to regulate cell fate in plants. Genes Dev 23 2723 2728
68. ChoSJinSWCohenAEllisRE 2004 A phylogeny of Caenorhabditis reveals frequent loss of introns during nematode evolution. Genome Res 14 1207 1220
69. KiontkeKGavinNPRaynesYRoehrigCPianoF 2004 Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc Natl Acad Sci USA 101 9003 9008
70. NayakSGoreeJSchedlT 2005 fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis. PLoS Biol 3 e6 doi:10.1371/journal.pbio.0030006
71. GuoYLangSEllisRE 2009 Independent recruitment of F box genes to regulate hermaphrodite development during nematode evolution. Curr Biol 19 1853 1860
72. HillRCHaagES 2009 A sensitized genetic background reveals evolution near the terminus of the Caenorhabditis germline sex determination pathway. Evol Dev 11 333 342
73. ZarkowerDHodgkinJ 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. BrennerS 1974 The genetics of Caenorhabditis elegans. Genetics 77 71 94
75. MelloCCKramerJMStinchcombDAmbrosV 1991 Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10 3959 3970
76. KellyWGXuSMontgomeryMKFireA 1997 Distinct requirements for somatic and germline expression of a generally expressed Caernorhabditis elegans gene. Genetics 146 227 238
77. GyurisJGolemisEChertkovHBrentR 1993 Cdi1, a human G1 and S phase protein phosphatase that associates with Cdk2. Cell 75 791 803
78. L'HernaultSWArduengoPM 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. RoseMDWinstonFHieterP 1990 Methods in Yeast Genetics: A Laboratory Course Manual CSHL Press, Cold Spring Harbor, NY
80. LeeMHSchedlT WormBook, The C. elegans Research Community, editors 2006 RNA in situ hybridization of dissected gonads.
81. LarkinMABlackshieldsGBrownNPChennaRMcGettiganPA 2007 Clustal W and Clustal X version 2.0. Bioinformatics 23 2947 2948
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 4
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- A Coordinated Interdependent Protein Circuitry Stabilizes the Kinetochore Ensemble to Protect CENP-A in the Human Pathogenic Yeast
- Coordinate Regulation of Lipid Metabolism by Novel Nuclear Receptor Partnerships
- Defective Membrane Remodeling in Neuromuscular Diseases: Insights from Animal Models
- Formation of Rigid, Non-Flight Forewings (Elytra) of a Beetle Requires Two Major Cuticular Proteins