Ultrastructural features of the adult hermaphrodite gonad of Caenorhabditis elegans: Relations between the germ line and soma

Developmental Biology

Volumn 212, Issue 1, 1999, Pages 101-123

  Hall, David H ^a   Winfrey, Virginia P ^b   Blaeuer, Gareth ^b   Hoffman, Loren H ^b   Furuta, Tokiko ^b   Rose, Kimberly L ^b   Hobert, Oliver ^c   Greenstein, David ^b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Caenorhabditis elegans; Cell cell interaction; Electron microscopy; Gap junction; Germ line; Meiosis; Oocyte

Indexed keywords

GREEN FLUORESCENT PROTEIN; YOLK PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CELL INTERACTION; CONTROLLED STUDY; EGG YOLK; ENDOCYTOSIS; FLUORESCENCE MICROSCOPY; GAP JUNCTION; GERM CELL; GONAD; HERMAPHRODITISM; MEIOSIS; MITOSIS; NONHUMAN; OOCYTE; OVULATION; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; SOMATIC CELL; ULTRASTRUCTURE;

EID: 0033179299     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1999.9356     Document Type: Article

References (76)

1. Abi-Rached M., Brun J. L. 'Etude ultrastructurale des relations entre ovocytes et rachis au cours de l'ovogenese du nematode C. elegans. Nematologica. 21:1975;151-162.
2. Albertson D. G., Thomson J. N. The pharynx of Caenorhabditis elegans. Philos. Trans. Royal Soc. 275B:1976;299-325.
3. Anderson E., Albertini D. F. Gap junctions between the oocyte and companion follicle cells in mammalian ovary. J. Cell Biol. 71:1976;680-686.
4. Artavanis-Tsakonas S., Rand M. D., Lake R. J. Notch signaling: Cell fate control and signal integration in development. Science. 284:1999;770-776.
5. 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. 51:1987;589-599.
6. Barnes T. M., Hekimi S. The Caenorhabditis elegans avermectin resistance and anesthetic response gene unc-9 encodes a member of a protein family implicated in electrical coupling of excitable cells. J. Neurochem. 69:1997;2251-2260.
7. Berry L. W., Westlund B., Schedl T. Germ-line tumor formation caused by activation of glp-1, a Caenorhabditis elegans member of the Notch family of receptors. Development. 124:1997;925-936.
8. Buechner, M, Hall, D. H, Bhatt, H, and, Hedgecock, E. M. 1999, Cystic canal mutants in C. elegans are defective in the apical membrane domain of the renal (excretory) cell. Submitted.
9. Chou R. G., Stromer M. H., Robson R. M., Huiatt T. W. Assembly of contractile and cytoskeletal elements in developing smooth muscle cells. Dev. Biol. 149:1992;339-348.
10. Church D. L., Guan K.-L., Lambie E. J. Three genes of the MAP kinase cascade, mek-2, mpk-1/sur-1 and let-60 ras, are required for meiotic cell cycle progression in Caenorhabditis elegans. Development. 121:1995;2525-2535.
11. Cines D. B., Pollak E. S., Buck C. A., Loscalzo J., Zimmerman G. A., McEver R. P., Pober J. S., Wick T. M., Konkle B. A., Schwartz B. S., Barnathan E. S., McCrae K. R., Hug B. A., Schmidt A.-M., Stern D. M. Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood. 91:1998;3527-3661.
12. Clandinin T. R., DeModena J. A., Sternberg P. W. Inositol triphosphate mediates a RAS-independent response to LET-23 receptor tyrosine kinase activation in C. elegans. Cell. 92:1998;523-533.
13. Crittenden S. L., Troeml E. R., Evans T. C., Kimble J. GLP-1 is localized to the mitotic region of the C. elegans germ line. Development. 120:1994;2901-2911.
14. Dolci S., Williams D. E., Ernst M. K., Resnick J. L., Braman C. I., Fock L. F., Lyman S. D., Boswell S. H., Donovan P. J. Requirements for mast cell growth factor for primordial germ cell survival in culture. Nature. 352:1991;809-811.
15. Dolci S., Pesce M., De Felici M. Combined action of stem cell factor, leukemia inhibitory factor, and cAMP on in vitro proliferation of mouse primordial germ cells. Mol. Reprod. Dev. 35:1993;134-139.
16. Doniach T., Hodgkin J. A sex-determining gene, fem-1, required for both male and hermaphrodite development in Caenorhabditis elegans. Dev. Biol. 106:1984;223-235.
17. Finbow M. E. Vetebrate and invertebrate gap junctions: A common molecular basis. Cell Biol. Int. 21:1997;329-331.
18. Fire A., Xu S., Montgomery M. K., Kostas S. A., Driver S. E., Mello C. C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 391:1998;806-811.
19. Fitzgerald K., Wilkinson H., Greenwald I. glp-1 can substitute for lin-12 in specifying cell fate decisions in C. elegans. Development. 119:1993;1019-1027.
20. Fitzgerald K., Greenwald I. Interchangeability of Caenorhabditis elegans DSL proteins and intrinsic signalling activity of their extracellular domains in vivo. Development. 121:1995;4275-4282.
21. Fleischman R. A. From white spots to stem cells: The role of the Kit receptor in mammalian development. Trends Genet. 9:1993;285-290.
22. Francis G. R., Waterston R. H. Muscle organization in Caenorhabditis elegans: Localization of proteins implicated in thin filament attachment and I-band organization. J. Cell Biol. 101:1985;1532-1549.
23. Francis R., Barton M. K., Kimble J., Schedl T. gld-1, a tumor suppressor gene required for oocyte development in Caenorhabditis elegans. Genetics. 139:1995;579-606.
24. Gettner S. N., Kenyon D., Reichardt L. F. Characterization of beta-pat-3 heterodimers, a family of essential integrin receptors in C. elegans. J. Cell Biol. 129:1995;1127-1141.
25. Gilchrist E. J., Moerman D. G. Mutations in the sup-38 gene of Caenorhabditis elegans suppress muscle-attachment defects in unc-52 mutants. Genetics. 132:1992;431-442.
26. Goodenough D. A., Goliger J. A., Paul D. L. Connexins, connexons, and intercellular communication. Annu. Rev. Biochem. 65:1996;475-502.
27. Greenstein D., Hird S., Plasterk R. H. A., Andachi Y., Kohara Y., Wang B., Finney M., Ruvkun G. Targeted mutations in the Caenorhabditis elegans POU homeobox gene ceh-18 cause defects in oocyte cell cycle arrest, gonad migration, and epidermal differentiation. Genes Dev. 8:1994;1935-1948.
28. Hall D. H. Freeze fracture and freeze etch studies of the nematode, Caenorhabditis elegans. Ann. N. Y. Acad. Sci. 494:1987;215-217.
29. Hall D. Electron microscopy and three-dimensional image reconstruction. Epstein H. F., Shakes D. C. Caenorhabditis elegans: Modern Biological Analysis of an Organism, Methods in Cell Biology. 1995;395-436 Academic Press, San Diego.
30. Heitzler P., Simpson P. The choice of cell fate in the epidermis of Drosophila. Cell. 64:1991;1083-1092.
31. 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. 120:1994;2913-2924.
32. Henderson S. T., Gao D., Christensen S., Kimble J. Functional domains of LAG-2, a putative signaling ligand for LIN-12 and GLP-1 receptors in Caenorhabditis elegans. Mol. Biol. Cell. 8:1997;1751-1762.
33. Hirsh D., Oppenheim D., Klass M. Development of the reproductive system of Caenorhabditis elegans. Dev. Biol. 49:1976;200-219.
34. Iwasaki K., McCarter J., Francis R., Schedl T. emo-1, a Caenorhabditis elegans Sec61p gamma homologue, is required for oocyte development and ovulation. J. Cell Biol. 134:1996;699-714.
35. Kadyk L. C., Kimble J. Genetic regulation of entry into meiosis in Caenorhabditis elegans. Development. 125:1998;1803-1813.
36. Keshet E., Lyman S. D., Williams D. E., Anderson D. M., Jenkins N. A., Copeland N. G., Parada L. F. Embryonic RNA expression patterns of the c-kit receptor and its cognate ligand suggest multiple functional roles in mouse development. EMBO J. 10:1991;2425-2435.
37. Kimble J., Hirsh D. The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans. Dev. Biol. 70:1979;396-417.
38. Kimble J., Sharrock W. J. Tissue-specific synthesis of yolk proteins in Caenorhabditis elegans. Dev. Biol. 96:1983;189-196.
39. Kimble J., White J. On the control of germ cell development in Caenorhabditis elegans. Dev. Biol. 81:1981;208-219.
40. Kramer J., French R. P., Park E., Johnson J. J. The Caenorhabditis elegans rol-6 gene, which interacts with the sqt-1 collagen gene to determine organismal morphology, encodes a collagen. Mol. Cell Biol. 10:1990;2081-2090.
41. Lambie E. J., Kimble J. Two homologous regulatory genes, lin-12 and glp-1, have overlapping functions. Development. 112:1991;231-240.
42. Lane N. J., Flores V. The role of cytoskeletal components in the maintenance of intercellular junctions in an insect. Cell Tissue Res. 262:1990;373-385.
43. L'Hernault S. W. Spermatogenesis. Riddle D. L., Blumenthal T., Meyer B. J., Priess J. R. C. elegans II. 1997;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
44. Marziali B., Lazzaro D., Sorrentino V. Binding of germ cells to mutant Sld Sertoli cells is defective and is rescued by expression of the transmembrane form of the c-kit ligand. Dev. Biol. 157:1993;182-190.
45. Matsui Y., Zsebo K. M., Hogan B. L. M. Embryonic expression of a haematopoietic growth factor encoded by the Sl locus and the ligand for c-kit. Nature. 347:1990;666-669.
46. McCarter J., Bartlett B., Dang T., Schedl T. Soma-germ cell interactions in Caenorhabditis elegans: Multiple events in germline development require the somatic sheath and spermathecal lineages. Dev. Biol. 181:1997;121-143.
47. McCarter J., Bartlett B., Dang T., Schedl T. On the control of oocyte meiotic maturation and ovulation in C. elegans. Dev. Biol. 205:1999;111-128.
48. Mello C., Fire A. DNA transformation. Epstein H. F., Shakes D. C. Caenorhabditis elegans: Modern Biological Analysis of an Organism, Methods in Cell Biology. 1995;395-436 Academic Press, San Diego.
49. Moerman D. G., Fire A. Muscle: Structure, function, and development. Riddle D. L., Blumenthal T., Meyer B. J., Priess J. R. C. elegans II. 1997;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
50. Mukherjee S., Ghosh R. N., Maxfield F. R. Endocytosis. Physiol. Rev. 77:1997;759-803.
51. Myers C. D., Goh P.-Y., Allen T. StC., Bucher E. A., Bogaert T. Developmental genetic analysis of Troponin T mutations in striated and nonstriated muscle cells of Caenorhabditis elegans. J. Cell Biol. 132:1996;1061-1077.
52. Nagato T., Yoshida H., Yoshida A., Uehara Y. A scanning electron microscope study of myoepithelial cells in exocrine glands. Cell Tissue Res. 209:1980;1-10.
53. Newman A. P., White J. G., Sternberg P. W. Morphogenesis of the C. elegans hermaphrodite uterus. Development. 122:1996;3617-3626.
54. Pesce M., Di Carlo A., De Felici M. The c-kit receptor is involved in the adhesion of mouse primordial germ cells to somatic cells in culture. Mech. Dev. 68:1997;37-44.
55. Pfenninger K. H., Friedman L. B. Sites of plasmalemmal expansion in growth cones. Dev. Brain Res. 71:1993;181-192.
56. Phelan P., Bacon J. P., Davies J. A., Stebbings L. A., Todman M., Avery L., Baines R. A., Barnes T. M., Ford C., Hekimi S., Lee R., Shaw J. E., Starich T. A., Curtin K. D., Sun Y., Wyman R. J. Innexins: A family of invertebrate gap-junction proteins. Trends Genet. 14:1998a;348-349.
57. Phelan P., Stebbings L. A., Baines R. A., Bacon J. P., Davies J. A., Ford C. Drosophila Shaking-B protein forms gap junctions in paired Xenopus oocytes. Nature. 391:1998b;181-184.
58. Quick D. C., Johnson R. G. Gap junctions and rhombic particle arrays in planaria. J. Ultrastruct. Res. 60:1977;348-361.
59. Rogalski T. M., Williams B. D., Mullen G. P., Moerman D. G. Products of the unc-52 gene in Caenorhabditis elegans are homologous to the core protein of the mammalian basement membrane heparan sulfate proteoglycan. Genes Dev. 7:1993;1471-1484.
60. Rogalski T. M., Gilchrist E. J., Mullen G. P., Moerman D. G. Mutations in the unc-52 gene responsible for body wall muscle defects in adult are located in alternatively spliced exons. Genetics. 139:1995;159-169.
61. Rose K. L., Winfrey V. P., Hoffman L. H., Hall D. H., Furuta T., Greenstein D. The POU gene ceh-18 promotes gonadal sheath cell differentiation and function required for meiotic maturation and ovulation in Caenorhabditis elegans. Dev. Biol. 192:1997;59-77.
62. Schedl T. Developmental genetics of the germ line. Riddle D. L., Blumenthal T., Meyer B. J., Priess J. R. C. elegans II. 1997;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
63. Sharrock W. J. Yolk proteins of C. elegans. Dev. Biol. 96:1983;182-188.
64. Sharrock W. J. Cleavage of two yolk proteins from a precursor in C. elegans. J. Mol. Biol. 174:1984;419-431.
65. Shen M. M., Hodgkin J. mab-3, a gene required for sex-specific yolk protein expression and a male-specific lineage in C. elegans. Cell. 54:1988;1019-1031.
66. Simionescu, N., and Simionescu, M.The cardiovascular system. In Cell and Tissue Biology (L. Weiss, Ed.), 6th ed., pp. 353-400. Urban and Schwrzenberg, Baltimore, MD.
67. Simon A. M., Goodenough D. A., Li E., Paul D. L. Female infertility in mice lacking connexin 37. Nature. 385:1997;525-529.
68. Simon A. M., Goodenough D. A. Diverse functions of vertebrate gap junctions. Trends Cell Biol. 8:1998;477-483.
69. Starich T. A., Lee R. Y. N., Panzarella C., Avery L., Shaw J. E. eat-5 and unc-7 represent a multigene family in Caenorhabditis elegans involved in cell-cell coupling. J. Cell Biol. 134:1996;537-548.
70. Strome S. Fluorescence visualization of the distribution of microfilaments in gonads and early embryos of the nematode C. elegans. J. Cell Biol. 103:1986;2241-2252.
71. Tax F. E., Yeargers J. J., Thomas J. H. Sequence of C. elegans lag-2 reveals a cell-signalling domain shared with Delta and Serrate of Drosophila. Nature. 388:1994;150-154.
72. Tepass U., Hartenstein V. The development of cellular junctions in the Drosophila embryo. Dev. Biol. 161:1994;563-596.
73. Ward S., Carrel J. S. Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev. Biol. 73:1979;304-321.
74. White J. G. The anatomy. Wood W. B. The Nematode Caenorhabditis elegans. 1988;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
75. Wickramasinghe D., Albertini D. F. Cell cycle control during mammalian oogenesis. Curr. Top. Dev. Biol. 28:1993;125-153.
76. Yochem J., Greenwald I. glp-1 and lin-12, genes implicated in distinct cell-cell interactions in C. elegans, encode similar transmembrane proteins. Cell. 58:1989;553-563.