The C. elegans adult male germline: Stem cells and sexual dimorphism

Developmental Biology

Volumn 346, Issue 2, 2010, Pages 204-214

  Morgan, Dyan E ^a   Crittenden, Sarah L ^a   Kimble, Judith ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Cell cycle; Germline sex determination; Sexual dimorphism; Sexual identity; Stem cell; Stem cell niche

Indexed keywords

ARTICLE; CAENORHABDITIS ELEGANS; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL RENEWAL; CONTROLLED STUDY; GAMETE; GENDER IDENTITY; GERM LINE; HERMAPHRODITISM; MALE; MATHEMATICAL MODEL; METAPHASE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROGENY; SEX DIFFERENCE; SPERMATOGENESIS; STEM CELL; TRANSGENE; ANIMAL; ANIMAL EMBRYO; CELL DIFFERENTIATION; CELL DIVISION; CYTOLOGY; EMBRYOLOGY; GERM CELL; METABOLISM; OOCYTE; SEXUAL DEVELOPMENT;

CAENORHABDITIS ELEGANS;

ANIMALS; CAENORHABDITIS ELEGANS; CELL CYCLE; CELL DIFFERENTIATION; CELL DIVISION; EMBRYO, NONMAMMALIAN; GERM CELLS; MALE; OOCYTES; SEX CHARACTERISTICS; STEM CELLS;

EID: 77956873635     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.07.022     Document Type: Article

References (73)

1. Aherne W.A., Camplejohn R.S., Wright N.A. An Introduction to Cell Population Kinetics 1977, Edward Arnold Ltd, London.
2. Anderson E.L., Baltus A.E., Roepers-Gajadien H.L., Hassold T.J., de Rooij D.G., van Pelt A.M.M., Page D.C. Stra8 and its inducer, retinoic acid, regulate meiotic initiation in both spermatogenesis and oogenesis in mice. Proc. Natl Acad. Sci. USA 2008, 105:14976-14980.
3. Angelo G., Van Gilst M. Starvation protects germline stem cells and extends reproductive longevity in C. elegans. Science 2009, 326:954-958.
4. Austin J., Kimble J. glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell 1987, 51:589-599.
5. Baltus A.E., Menke D.B., Hu Y.C., Goodheart M.L., Carpenter A.E., de Rooij D.G., Page D.C. In germ cells of mouse embryonic ovaries, the decision to enter meiosis precedes premeiotic DNA replication. Nat. Genet. 2006, 38:1430-1434.
6. Bargmann C.I., Avery L. Laser killing of cells in Caenorhabditis elegans. Caenorhabditis elegans: Modern Biological Analysis of an Organism 1995, 225-250. Academic Press, Inc., San Diego. H.F. Epstein, D.C. Shakes (Eds.).
7. Barton M.K., Kimble J. fog-1, a regulatory gene required for specification of spermatogenesis in the germ line of Caenorhabditis elegans. Genetics 1990, 125:29-39.
8. Barton M.K., Schedl T.B., Kimble J. Gain-of-function mutations of fem-3, a sex-determination gene in Caenorhabditis elegans. Genetics 1987, 115:107-119.
9. Bowles J., Koopman P. Retinoic acid, meiosis and germ cell fate in mammals. Development 2007, 134:3401-3411.
10. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
11. Casper A., Van Doren M. The control of sexual identity in the Drosophila germline. Development 2006, 133:2783-2791.
12. Casper A.L., Van Doren M. The establishment of sexual identity in the Drosophila germline. Development 2009, 136:3821-3830.
13. Chen P.-J., Singal A., Kimble J., Ellis R.E. A novel member of the Tob family of proteins controls sexual fate in Caenorhabditis elegans germ cells. Dev. Biol. 2000, 217:77-90.
14. Chesney M.A., Lam N., Morgan D.E., Phillips B.T., Kimble J. C. elegans HLH-2/E/Daughterless controls key regulatory cells during gonadogenesis. Dev. Biol. 2009, 331:14-25.
15. Cinquin O., Crittenden S.L., Morgan D.E., Kimble J. Progression from a stem cell-like state to early differentiation in the C. elegans germ line. Proc. Natl Acad. Sci. USA 2010, 107:2048-2053.
16. Crittenden S.L., Kimble J. Analysis of the C. elegans germline stem cell region. Germline Stem Cell Protocols 2008, vol. 450:27-44. The Humana Press, Inc, Totowa, NJ. S. Hou, S.R. Singh (Eds.).
17. Crittenden S.L., Leonhard K.A., Byrd D.T., Kimble J. Cellular analyses of the mitotic region in the Caenorhabditis elegans adult germ line. Mol. Biol. Cell 2006, 17:3051-3061.
18. Crittenden S.L., Troemel E.R., Evans T.C., Kimble J. GLP-1 is localized to the mitotic region of the C. elegans germ line. Development 1994, 120:2901-2911.
19. DeFalco T., Capel B. Gonad morphogenesis in vertebrates: divergent means to a convergent end. Annu. Rev. Cell Dev. Biol. 2009, 25:457-482.
20. Dernburg A.F., McDonald K., Moulder G., Barstead R., Dresser M., Villeneuve A.M. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 1998, 94:387-398.
21. Ellis, R., Schedl, T., 2007. Sex determination in the germ line, in: The C. elegans Research Community (Ed.), WormBook. WormBook. , 10.1895/wormbook.1.82.2. (March 5, 2007). http://www.wormbook.org.
22. Francis R., Barton M.K., Kimble J., Schedl T. gld-1, a tumor suppressor gene required for oocyte development in Caenorhabditis elegans. Genetics 1995, 139:579-606.
23. Gumienny T.L., Lambie E., Hartwieg E., Horvitz H.R., Hengartner M.O. Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 1999, 126:1011-1022.
24. Hansen D., Hubbard E.J.A., Schedl T. Multi-pathway control of the proliferation versus meiotic development decision in the Caenorhabditis elegans germline. Dev. Biol. 2004, 268:342-357.
25. Hempel L.U., Kalamegham R., Smith J.E., Oliver B. Drosophila germline sex determination: integration of germline autonomous cues and somatic signals. Curr. Top. Dev. Biol. 2008, 83:109-150.
26. Henderson S.T., Gao D., Lambie E.J., Kimble J. lag-2 may encode a signaling ligand for the GLP-1 and LIN-12 receptors of C. elegans. Development 1994, 120:2913-2924.
27. Hendzel M.J., Wei Y., Mancini M.A., Van Hooser A., Ranalli T., Brinkley B.R., Bazett-Jones D.P., Allis C.D. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 1997, 106:348-360.
28. Hodgkin J. A genetic analysis of the sex determining gene, tra-1, in the nematode Caenorhabditis elegans. Genes Dev. 1987, 1:731-745.
29. Hodgkin J., Horvitz H.R., Brenner S. Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics 1979, 91:67-94.
30. Hodgkin J., Kondo K., Waterston R.H. Suppression in the nematode Caenorhabditis elegans. Trends Genet. 1987, 3:325-329.
31. Hubbard E.J.A., Greenstein D. The Caenorhabditis elegans gonad: a test tube for cell and developmental biology. Dev. Dyn. 2000, 218:2-22.
32. Jaramillo-Lambert A., Ellefson M., Villeneuve A.M., Engebrecht J. Differential timing of S phases, X chomosome replication, and meiotic prophase in the C. elegans germ line. Dev. Biol. 2007, 308:206-221.
33. Jaramillo-Lambert A., Engebrecht J. A single unpaired and transcriptionally silenced X chromosome locally precludes checkpoint signaling in the Caenorhabditis elegans germ line. Genetics 2010, 184:613-628.
34. Jin S.W., Arno N., Cohen A., Shah A., Xu Q., Chen N., Ellis R.E. In Caenorhabditis elegans, the RNA-binding domains of the cytoplasmic polyadenylation element binding protein FOG-1 are needed to regulate germ cell fates. Genetics 2001, 159:1617-1630.
35. Jones A.R., Francis R., Schedl T. GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage- and sex-specific expression during Caenorhabditis elegans germline development. Dev. Biol. 1996, 180:165-183.
36. Kadyk L.C., Kimble J. Genetic regulation of entry into meiosis in Caenorhabditis elegans. Development 1998, 125:1803-1813.
37. Killian D.J., Hubbard E.J.A. Caenorhabditis elegans germline patterning requires coordinated development of the somatic gonadal sheath and the germ line. Dev. Biol. 2005, 279:322-335.
38. Kim K.W., Nykamp K., Suh N., Bachorik J.L., Wang L., Kimble J. Antagonism between GLD-2 binding partners controls gamete sex. Dev. Cell 2009, 16:723-733.
39. Kimble J., Crittenden S.L. Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans. Annu. Rev. Cell Dev. Biol. 2007, 23:405-433.
40. Kimble J., Hirsh D. The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans. Dev. Biol. 1979, 70:396-417.
41. Kimble J., Page D.C. The mysteries of sexual identity. The germ cell's perspective. Science 2007, 316:400-401.
42. Kimble J.E., White J.G. On the control of germ cell development in Caenorhabditis elegans. Dev. Biol. 1981, 81:208-219.
43. Kocer A., Reichmann J., Best D., Adams I.R. Germ cell sex determination in mammals. Mol. Hum. Reprod. 2009, 15:205-213.
44. Korta D.Z., Hubbard E.J. Soma-germline interactions that influence germline proliferation in Caenorhabditis elegans. Dev. Dyn. 2010, 239:1449-1459.
45. Kraemer B., Crittenden S., Gallegos M., Moulder G., Barstead R., Kimble J., Wickens M. NANOS-3 and FBF proteins physically interact to control the sperm-oocyte switch in Caenorhabditis elegans. Curr. Biol. 1999, 9:1009-1018.
46. Lambie E.J., Kimble J. Two homologous regulatory genes, lin-12 and glp-1, have overlapping functions. Development 1991, 112:231-240.
47. Li L., Xie T. Stem cell niche: structure and function. Annu. Rev. Cell Dev. Biol. 2005, 21:605-631.
48. Maciejowski J., Ugel N., Mishra B., Isopi M., Hubbard E.J.A. Quantitative analysis of germline mitosis in adult C. elegans. Dev. Biol. 2006, 292:142-151.
49. Madl J.E., Herman R.K. Polyploids and sex determination in Caenorhabditis elegans. Genetics 1979, 93:393-402.
50. Mathies L.D., Schvarzstein M., Morphy K.M., Blelloch R., Spence A.M., Kimble J. TRA-1/GLI controls development of somatic gonadal precursors in C. elegans. Development 2004, 131:4333-4343.
51. McCarter J., Bartlett B., Dang T., Schedl T. Soma-germ cell interactions in Caenorhabditis elegans: multiple events of hermaphrodite germline development require the somatic sheath and spermathecal lineages. Dev. Biol. 1997, 181:121-143.
52. McGovern M., Voutev R., Maciejowski J., Corsi A.K., Hubbard E.J. A "latent niche" mechanism for tumor initiation. Proc. Natl Acad. Sci. USA 2009, 106:11617-11622.
53. Meyer, B. J., 2005. X-Chromosome dosage compensation, in: The C. elegans Research Community (Ed.), WormBook. WormBook. , 10.1895/wormbook.1.8.1. (June 25, 2005). http://www.wormbook.org.
54. Morgan C.T., Lee M.H., Kimble J. Chemical reprogramming of Caenorhabditis elegans germ cell fate. Nat. Chem. Biol. 2010, 6:102-104.
55. Morrison S.J., Kimble J. Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 2006, 441:1068-1074.
56. Nadarajan S., Govindan J.A., McGovern M., Hubbard E.J.A., Greenstein D. MSP and GLP-1/Notch signaling coordinately regulate actomyosin-dependent cytoplasmic streaming and oocyte growth in C. elegans. Development 2009, 136:2223-2234.
57. Okkema P.G., Kimble J. Molecular analysis of tra-2, a sex determining gene in Caenorhabditis elegans. EMBO J. 1991, 10:171-176.
58. Otori M., Karashima T., Yamamoto M. The Caenorhabditis elegans homologue of Deleted in Azoospermia is involved in the sperm/oocyte switch. Mol. Biol. Cell 2006, 17:3147-3155.
59. Rasband, W. S., ImageJ. U.S. National Institutes of Health, Bethesda, Maryland, USA, 1997-2009.
60. Schedin P., Jonas P., Wood W.B. Function of the her-1 gene is required for maintenance of male differentiation in adult tissues of C. elegans. Dev. Genet. 1994, 15:231-239.
61. Schedl T., Graham P.L., Barton M.K., Kimble J. Analysis of the role of tra-1 in germline sex determination in the nematode Caneorhabditis elegans. Genetics 1989, 123:755-769.
62. Shakes D.C., Wu J.C., Sadler P.L., Laprade K., Moore L.L., Noritake A., Chu D.S. Spermatogenesis-specific features of the meiotic program in Caenorhabditis elegans. PLoS Genet. 2009, 5:e1000611.
63. Siegfried K., Kimble J. POP-1 controls axis formation during early gonadogenesis in C. elegans. Development 2002, 129:443-453.
64. Starostina N.G., Lim J.M., Schvarzstein M., Wells L., Spence A.M., Kipreos E.T. A CUL-2 ubiquitin ligase containing three FEM proteins degrades TRA-1 to regulate C. elegans sex determination. Dev. Cell 2007, 13:127-139.
65. Taupin P. BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res. Rev. 2007, 53:198-214.
66. Thompson B.E., Bernstein D.S., Bachorik J.L., Petcherski A.G., Wickens M., Kimble J. Dose-dependent control of proliferation and sperm specification by FOG-1/CPEB. Development 2005, 132:3471-3481.
67. Uhlenhaut N.H., Jakob S., Anlag K., Eisenberger T., Sekido R., Kress J., Treier A.C., Klugmann C., Klasen C., Holter N.I., Riethmacher D., Schutz G., Cooney A.J., Lovell-Badge R., Treier M. Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 2009, 139:1130-1142.
68. Wawersik M., Milutinovich A., Casper A.L., Matunis E., Williams B., Van Doren M. Somatic control of germline sexual development is mediated by the JAK/STAT pathway. Nature 2005, 436:563-567.
69. Wilkins A.S., Holliday R. The evolution of meiosis from mitosis. Genetics 2009, 181:3-12.
70. Williams T.M., Carroll S.B. Genetic and molecular insights into the development and evolution of sexual dimorphism. Nat. Rev. Genet. 2009, 10:797-804.
71. Wolff J.R., Zarkower D. Somatic sexual differentiation in Caenorhabditis elegans. Curr. Top. Dev. Biol. 2008, 83:1-39.
72. Yamashita Y.M., Fuller M.T. Asymmetric centrosome behavior and the mechanisms of stem cell division. J. Cell Biol. 2008, 180:261-266.
73. Zarkower, D., 2006. Somatic sex determination, in: The C. elegans Research Community (Ed.), WormBook. WormBook. , doi/10.1895/wormbook1.84.1. (February 10, 2006). http://www.wormbook.org.