Biparental inheritance of γ-tubulin during human fertilization: Molecular reconstitution of functional zygotic centrosomes in inseminated human oocytes and in cell-free extracts nucleated by human sperm

Molecular Biology of the Cell

Volumn 10, Issue 9, 1999, Pages 2955-2969

  Simerly, Calvin ^a   Zoran, Sara S ^a   Payne, Chris ^a   Dominko, Tanja ^a   Sutovsky, Peter ^a   Navara, Christopher S ^a   Salisbury, Jeffery L ^b   Schatten, Gerald ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CENTRIN; TUBULIN;

ANIMAL CELL; ARTICLE; CELL FREE SYSTEM; CENTROSOME; DISULFIDE BOND; DNA TEMPLATE; FERTILIZATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MICROTUBULE ASSEMBLY; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SPERM; SPERMATOZOON; XENOPUS LAEVIS; ZYGOTE;

ANIMALIA; ASTER; MAMMALIA; XENOPUS LAEVIS;

EID: 0032880088     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.10.9.2955     Document Type: Article

References (77)

1. Baron, A.T., Greenwood, T.M., Bazinet, C.W., and Salisbury, J.L. (1992). Centrin is a component of the pericentriolar lattice. Biol. Cell 76, 383-388.
2. Baron, A.T., Suman V.J., Nemeth, E., and Salisbury, J.L. (1994). The pericentriolar lattice of PtK2 cells exhibits temperature and calcium-modulated behavior. J. Cell Sei. 107, 2993-3003.
3. 2+-binding proteins. Proc. Natl. Acad. Sci. USA 83, 5512-5516.
4. Bellvé, A.R., Zheng, W., and Martinova, Y.S. (1993). Recovery, capacitation, acrosome reaction, and fractionation of sperm. Methods Enzymol. 225, 113-136.
5. Biggins, S., and Rose, M.D. (1994). Direct interaction between yeast spindle pole body components: Karlp is required for Cdc31p localization to the spindle pole body. J. Cell Biol. 125, 843-852.
6. Bornens, M., Paintrand, M., Berges, J., Marty, M.C., and Karsenti, E. (1987). Structural and chemical characterization of isolated centro-somes. Cell Motil. Cytoskeleton 8, 238-249.
7. Boveri, T. (1901). Zellen-Studien: Uber die Natur der Centrosomen, vol IV, Jena, Germany: Fisher.
8. Brinkley, B.R., Cox, S.M., and Fistel, S. (1980). Organizing centers for cell processes. Neurosci. Res. Program Bull. 19, 108-124.
9. Brown, D.B., Blake, E.J., Wolgemuth, D.J., Gordon, K., and Ruddle, F.H. (1987). Chromatin decondensarion and DNA synthesis in human sperm activated in vitro by using Xenopus laevis egg extracts. J. Exp. Zool. 242, 215-231.
10. Calvin, H.I., Yu, C.C., and Bedford, J.M. (1973). Effects of epididymal maturation, zinc (II) and copper (II) on the reactive sulfhydryl content of structural elements in rat spermatozoa. Exp. Cell Res. 81, 333-341.
11. cdc2 protein kinase activity in meiotic and mitotic cell cycles in mouse oocytes and embryos. Development 113, 789-795.
12. Davis, F.M., Tsao, T.Y., Fowler, S.K., and Rao, P.N. (1983). Monoclonal antibodies to mitotic cells. Proc. Natl. Acad. Sci. USA 80, 2926-2930.
13. Davis, T.N. (1997). The centrosome on center stage. Trends Cell Biol. 7, 508-510.
14. Doxsey, S. (1998). The centrosome: a tiny organelle with big potential. Nat. Genet. 20, 104-106.
15. Doxsey, S.J., Stein, P., Evans, L., Calarco, P.D., and Kirschner, M. (1994) Pericentrin, a highly conserved centrosome protein involved in microtubule organization. Cell 76, 639-650.
16. Errabolu, R., Sanders, M.A., and Salisbury, J.L. (1994). Cloning of a cDNA encoding human centrin, an EF-hand protein of centrosomes and mitotic spindle poles. J. Cell Sci. 107, 9-16.
17. Félix, M.A., Antony, C., Wright, M., and Maro, B. (1994). Centro-some assembly in vitro: role of y-tubulin recruitment in Xenopus sperm aster formation. J. Cell Biol. 124, 19-31.
18. Gard, D.L. (1994). γ-Tubulin is asymmetrically distributed in the cortex of Xenopus oocytes. Dev. Biol. 161, 131-140.
19. Harrouk, W., and Clarke H.J. (1993). Sperm chromatin acquires an activity that induces microtubule assembly during residence in the cytoplasm of metaphase oocytes of the mouse. Chromosoma 102, 279-286.
20. Heidermann, S.R., and Kirschner, M.W. (1975). Aster formation in egg of Xenopus laevis. J. Cell Biol. 67, 105-117.
21. Horio, T., Uzawa, S., Jung, M.K., Oakley, B.R., Tanaka, K., and Yanagida, M. (1991). The fission yeast γ-rubulin is essential for mitosis and is localized at microtubule organizing centers. J. Cell Sci. 99, 693-700.
22. Hulen, D., Baron, A., Salisbury, J., and Clarke, M. (1991). Production and specificity of monoclonal antibodies against calmodulin from Dictyostelium discoideum. Cell Motil. Cytoskeleton 18, 113-122.
23. Joshi, H.C., Palacios, M.J., McNamara, L., and Cleveland, D.W. (1992). γ-Tubulin is a centrosomal protein required for cell cycle-dependent microtubule nucleation. Nature 356, 80-83.
24. Karsenti, E., Newport, J., Bubble, R., and Kirschner, M. (1984). Interconversion of metaphase and interphase microtubule arrays as studied by the injection of centrosomes and nuclei into Xenopus eggs. J. Cell Biol. 98, 1730-1745.
25. Kosower, N.S., and Kosower, E.M. (1987). Thiol labeling with bromobimanes. Methods Enzymol. 143, 76-84.
26. Kuriyama, R., Borisy, G.G., and Masui, Y. (1986). Microtubule cycles in oocytes of the surf clam, Spisula solidissima: an immunofluorescence study. Dev. Biol. 114, 151-160.
27. Lee, V.D., and Huang, B. (1993). Molecular cloning and centrosomal localization of human caltracrin. Proc. Natl. Acad. Sci. USA 90, 11039-11043.
28. Lohka, M.J., and Maller, J.L. (1988). Induction of metaphase chromosome condensation in human sperm by Xenopus egg extracts. Exp. Cell Res. 179, 303-309.
29. Long, C.R., Suncan, R.P., and Robl, J.M. (1997). Isolation and characterization of MPM-2 reactive sperm proteins: homology to components of the outer dense fibers and segmented columns. Biol. Reprod. 57, 246-254.
30. Maller, J. Poceia, D., Nishioka, D., Gerhart, J., and Hartman, H. (1976). Spindle formation and cleavage in Xenopus eggs injected with centriole-containing fractions from sperm. Exp. Cell Res. 99, 285-294.
31. Manandhar, G., Sutovsky, P., Joshi, H.C., Stearns, T., and Schatten, G. (1998). Centrosome reduction during mouse spermiogenesis. Dev. Biol. 203, 424-434.
32. Mazia, D. (1961). Mitosis and the physiology of cell division. In: The Cell, vol. III, ed. J. Bracket and A.E. Mirsky, New York: Academic Press, 78-412.
33. Mazia, D., and Zimmerman, A.M. (1958). SH compounds in mitosis. II. The effect of mercaptoethanol on the structure of the mitotic apparatus in sea urchin eggs. Exp. Cell Res. 15, 138-153.
34. McIntosh, J.R., and Koonce M.P. (1989). Mitosis. Science 246, 622-628.
35. Mellon, M.G., and Rebhun, L.I. (1976). Sulfhydryls and the in vitro polymerization of tubulin. J. Cell Biol. 70, 226-238.
36. Middendorp, S., Paoletti, A., Schiebel, E., and Bornens, M. (1997). Identification of a new mammalian centrin gene, more closely related to Saccharomyces cerevisiae CDC31 gene. Proc. Natl. Acad. Sci. USA 94, 9141-9146.
37. Moritz, M., Braunfeld, M.B., Sedat, J.W., Alberts, B., and Agard, D.A. (1995). Microtubule nucleation by γ-tubulin-containing rings in the centrosome. Nature 378, 638-640.
38. Murray, A.W. (1991). Cell cycle extracts. Methods Cell Biol. 36, 581-595.
39. Murray, A.W., and Hunt, T. (1993). The Cell Cycle: An Introduction, New York: W.H. Freeman.
40. Navara, C.S., First, N.L., and Schatten, G. (1994). Microtubule organization in the cow during fertilization, polyspermy, parthenogenesis, and nuclear transfer: the role of the sperm aster. Dev. Biol. 162, 29-40.
41. Oakley, B.R. (1992). γ-Tubulin: the microtubule organizer. Trends Cell Biol. 2, 1-5.
42. Oakley, C.E., and Oakley, B.R. (1989). Identification of γ-tubulin, a new member of the tubulin superfamily encoded by mipA gene of Aspergillus nidulans. Nature 338, 662-664.
43. Ohsumi, K., Katagiri, C., and Yanagimachi, R. (1986). Development of pronuclei from human spermatozoa injected microsurgically into frog (Xenopus) eggs. J. Exp. Zool. 237, 319-325.
44. Oliver, J.M., Albertini, D.F., and Berlin, R.D. (1976). Effects of glutathione oxidizing agents on microtubule assembly and microtubule-dependent surface properties of human neutrophils. J. Cell Biol. 71, 921-932.
45. Palacios, M.J., Joshi, H.C., Simerly, C., and Schatten, G. (1993). Dynamic reorganization of γ-tubulin during murine fertilization. J. Cell Sci. 104, 383-389.
46. Paoletti, A., Moudjou, M., Paintrand, M., Salisbury, J.L., and Bornens, M. (1996). Most of centrin in animal cells is not centro-some-associated and centrosomal centrin is confined to the distal lumen of centrioles. J. Cell Sci. 109, 3089-3102.
47. Perreault, S.D., Naish, S.J., and Zirken, B.R. (1987). The timing of hamster sperm nuclear decondensation and male pronucleus formation is related to sperm nuclear disulfide bond content. Biol. Reprod. 36, 239-244.
48. Perreault, S.D., Wolf, R.A., and Zirken, B.R. (1984). The role of disulfide bond reduction during mammalian sperm nuclear decondensation in vivo. Dev. Biol. 101, 160-167.
49. Pinto-Correia, C., Poccia, D.L., Chang, T., and Robl, J.M. (1994). Dephosphorylation of sperm midpiece antigens initiates aster formation in rabbit oocytes. Proc. Natl. Acad. Sci. USA 91, 7894-7898.
50. Rodman, T.C., Pruslin, F.H., Hoffmann, H.P., and Allfrey, V.G. (1981). Turnover of basic chromosomal proteins in fertilized eggs: a cytoimmunochemical study of events in vivo. J. Cell Biol. 90, 351-361.
51. Rose, M.D., Biggins, S., and Satterwhite, L.L. (1993). Unravelling the tangled web at the microtubule-organizing center. Curr. Opin. Cell Biol. 5, 105-115.
52. Salisbury, J.L. (1995). Centrin, centrosomes, and mitotic spindle poles. Curr. Opin. Cell Biol. 7, 39-45.
53. Sanders, M.A., and Salisbury, J.L. (1989). Centrin-mediated microtubule severing during flagellar excision in Chlamydomonas reinhardtii. J. Cell Biol. 108, 1751-1760.
54. Sanders, M.A., and Salisbury, J.L. (1994). Centrin plays an essential role in microtubule severing during flagellar excision in Chlamydomonas reinhardtii. J. Cell Biol. 124, 795-805.
55. Schatten, G. (1994). Centrosome inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization. Dev. Biol. 165, 299-335.
56. Schatten, G., Simerly, C., and Schatten, H. (1991). Maternal inheritance of centrosomes in mammals? Studies on parthenogenesis and polyspermy in mice. Proc. Natl. Acad. Sci. USA 88, 6785-6789.
57. Schatten, H., Schatten, G., Mazia, D., Balczon, R., and Simerly, C. (1986). Behavior of centrosomes during fertilization and cell division in mouse oocytes and in sea urchin eggs. Proc. Natl. Acad. Sci. USA 83, 105-109.
58. Schliwa, M., Pryzwansky, K.B., and Euteneuer, U. (1982). Centro-some splitting in neutrophils: an unusual phenomenon related to cell activation and motility. Cell 31, 705-717.
59. Shalgi, R., Seligman, J., and Kosower, N.S. (1989). Dynamics of the thiol status of rat spermatozoa during maturation: analysis with the fluorescent labeling agent monobromobimane. Biol. Reprod. 40, 1037-1045.
60. Simerly, C., and Schatten, G. (1993). Techniques for localization of specific molecules in oocytes and embryos. Methods Enzymol. 225, 516-552.
61. Simerly, C., et al. (1995). The paternal inheritance of the centrosome, the cell's microtubule-organizing center, in humans, and the implications for infertility. Nat. Med. 1, 47-52.
62. Stearns, T. (1995). The form and the substance. Nat. Med. 1, 19-20.
63. Stearns, T., Evans, L., and Kirschner, M. (1991). γ-Tubulin is a highly conserved component of the centrosome. Cell 65, 825-836.
64. Stearns, T., and Kirschner, M. (1994). In vitro reconstitution of centrosome assembly and function: the central role of γ-tubulin. Cell 76, 623-637.
65. Stearns, T., and Winey, M. (1997). The cell center at 100. Cell 91, 303-309.
66. Steffen-Zoran, S., Simerly, C.R., and Schatten, G. (1993). Microtubule organization in mouse oocytes after microinjection of sea urchin sperm heads, midpieces and centrosomal complexes. Biol. Res. 26, 453-464.
67. Sutovsky, P., Fléchon, J.E., Fléchon, B., Motlík, J., Peynot, N., Chesné, P., and Heyman, Y. (1993). Dynamic changes of gap junctions and cytoskeleton during in vitro culture of cattle oocyte cumulus complexes. Biol. Reprod. 49, 1277-1287.
68. Vandré, D.D., Davis, P.M., Rao, P.N., and Borisy, G.G. (1986). Distribution of cytoskeletal proteins sharing a conserved phosphorylated epitope. Eur. J. Cell Biol. 41, 72-81.
69. Verde, F., Labbé, J.C., Dorée, M., and Karsenti, E. (1990). Regulation of microtubule dynamics by cdc2 protein kinase in cell-free extracts of Xenopus eggs. Nature 343, 233-238.
70. Verlhac, M-H., Kubiak, J.Z., Clarke, H.J., and Maro, B. (1994). Microtubule and chromatin behavior follow MAP kinase activity but not MPF activity during meiosis in mouse oocytes. Development 120, 1017-1025.
71. Ward, W.S., and Coffey, D.S. (1991). DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol. Reprod. 44, 569-574.
72. Whitaker, M., and Swann, K. (1993). Lighting the fuse at fertilization. Development 117, 1-12.
73. Xu, Y.-S., Overton, W.R., Marmar, J.L., Leonard, J.C., McCoy, J.P., Jr., Butler, G.H., and Li, H. (1998). Complete replication of human sperm genome in egg extracts from Xenopus laevis. Biol. Reprod. 58, 641-647.
74. Zamboni, L., and Stefanini, M. (1971). The fine structure of the neck of mammalian spermatozoa. Anat. Rec. 269, 155-172.
75. Zheng, Y., Jung, M.K., and Oakley, B.R. (1991). γ-Tubulin is present in Drosophita melanogaster and Homo sapiens and is associated with the centrosome. Cell 65, 817-823.
76. Zheng, Y., Wong, M.L., Alberts, B., and Mitchison, T. (1995). A γ-tubulin ring complex purified from the unfertilized egg of Xenopus laevis can nucleate microtubule assembly in vitro. Nature 378, 578-583.
77. Zimmerman, W., Sparks, C.A., and Doxsey, S.J. (1999). Amorphous no longer: the centrosome comes into focus. Curr. Opin. Cell Biol. 11, 122-128.