Differential expression and functions of cortical myosin IIa and IIb isotypes during meiotic maturation, fertilization, and mitosis in mouse oocytes and embryos

Molecular Biology of the Cell

Volumn 9, Issue 9, 1998, Pages 2509-2525

  Simerly, Calvin ^a,b   Nowak, Grzegorz ^c   De Lanerolle, Primal ^c   Schatten, Gerald ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEMECOLCINE; MYOSIN; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN LIGHT CHAIN; POLYCLONAL ANTIBODY;

ANIMAL CELL; ARTICLE; CELL POLARITY; CONTROLLED STUDY; CYTOKINESIS; EMBRYO; EMBRYO DEVELOPMENT; FERTILIZATION IN VITRO; MEIOSIS; MICROFILAMENT; MITOSIS; MITOSIS SPINDLE; MOUSE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; SPERM;

ANIMALIA; MURINAE;

EID: 0031720373     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.9.9.2509     Document Type: Article

References (69)

1. Alexandre, H., Van Cauwenberge, A., and Mulnard, J. (1989). Involvement of microtubules and microfilaments in the control of the nuclear movement during maturation of mouse oocyte. Dev. Biol. 136, 311-320.
2. Amsterdam, A., Lindner, A.R., and Groschel-Stewart, U. (1976). Localization of actin and myosin in the rat oocyte and follicular wall by immunofluorescence. Anat. Rec. 187, 311-328.
3. Battaglia, D.E., and Gaddum-Rosse P. (1986). The distribution of polymerized actin in the rat egg and its sensitivity to cytochalasin B during fertilization. J. Exp. Zool. 237, 97-105.
4. Bavister, B.D. (1989). A consistently successful procedure for in vitro fertilization of golden hamster eggs. Gamete Res. 23, 139-158.
5. Campanella, C., Gabbiani, G., Baccetti, B., Burrini, A.G and Pallini, V. (1979). Actin and myosin in the vertebrate acrosomal region. J. Submicrosc. Cytol. 11, 53-71.
6. Cheng, T.P., Murakami, N., and Elzinga, M. (1992). Localization of myosin-IIB at the leading-edge of growth cones from rat dorsal-root ganglionic cells. FEBS Lett. 311, 91-94.
7. Craig, R., Smith, R., and Kendrick-Jones, J. (1983). Light-chain phosphorylation controls the conformation of vertebrate non-muscle and smooth muscle myosin molecules. Nature 302, 436-439.
8. Damjanov, I., Damjanov, A., Lehto, V.P., and Virtanen, I. (1986). Spectrin in mouse gametogenesis and embryogenesis. Dev. Biol. 114, 132-140.
9. de Lanerolle, P., Gogas, G., Li, X., and Schluns, K. (1993). Myosin light chain phosphorylation does not increase during yeast phagocytosis by macrophages. J. Biol. Chem. 268, 16883-16886.
10. De Martino, C., Capanna, E., Nicotra, M.R., and Natali, P.G. (1980). Immunochemical localization of contractile proteins in mammalian meiotic chromosomes. Cell Tissue Res. 213, 159-178.
11. Ducibella, T., Duffy, P., Reindollar, R., and Su, B. (1990). Changes in the distribution of mouse oocyte cortical granules and the ability to undergo the cortical reaction during gonadotropin-stimulated meiotic maturation and aging in vivo. Biol. Reprod. 43, 870-876.
12. Fishkind, D.J., Cao, L.-G., and Wang, Y.-L. (1991). Microinjection of the catalytic fragment of myosin light chain kinase into dividing cells: effects on mitosis and cytokinesis. J. Cell Biol. 114, 967-975.
13. Flaherty, S.P., Winfrey, V.P., and Olson, G.E. (1986). Localization of actin in mammalian spermatozoa: a comparison of eight species. Anat. Rec. 216, 504-515.
14. Fujiwara, K., and Pollard, T.D. (1976). Fluorescent antibody localization of myosin in the cytoplasm, cleavage furrow and mitotic spindle of human cells. J. Cell Biol. 71, 848-875.
15. Gandhi, S., Lorimer, D.D., and de Lanerolle, P. (1997). Expression of a mutant myosin light chain that cannot be phosphorylated increases paracellular permeability. Am J. Physiol. 272, F214-F221.
16. Holzapfel, G., Wehland, J., and Weber, K. (1983). Calcium control of actin-myosin based contraction in Triton models of mouse 3T3 fibroblasts is mediated by the myosin light chain kinase (MLCK)-calmodulin complex. Exp. Cell Res. 148, 117-126.
17. Katsuragawa, Y., Yanagisawa, M, Inoue, A., and Masaki, T. (1989). Two distinct nonmuscle myosin-heavy chain mRNA's are differentially expressed in various chicken tissues: identification of a novel gene family of vertebrate non-sarcomeric myosin heavy chains. Eur. J. Biochem. 184, 611-616.
18. Kaufman, M.H. (1983). Early Mammalian Development: Parthenogenetic Studies, 1st ed., Cambridge: Cambridge University Press.
19. cdc2 kinase during meiosis. J. Biol. Chem. 270, 1395-1401.
20. Kelley, C.A., Sellers, J.R., Adelstein, R.S., and Baines, I.C. (1995). Xenopus nonmuscle myosin isoforms have different enzymatic activities and subcellular localizations. Mol. Biol. Cell 6, 26a.
21. Kiehart, D.P., et al. (1990). Contractile proteins in Drosophila development. Ann. N.Y. Acad. Sci. 528, 233-251.
22. Kiehart, D.P., Mabuchi, I., and Inoue, S. (1982). Evidence that myosin does not contribute to force production in chromosome movement. J. Cell Biol. 94, 165-178.
23. Longo, F.J. (1989). Egg cortical architecture. In:. The Cell Biology of Fertilization, ed. H. Schatten and G. Schatten, San Diego: Academic Press, 105-138.
24. Longo, F.J., and Chen, D.Y. (1985). Development of cortical polarity in mouse eggs: involvement of the meiotic apparatus. Dev. Biol. 107, 382-394.
25. Mabuchi, I. (1986). Biochemical aspects of cytokinesis. Int. Rev. Cytol. 101, 175-213.
26. Maro, B., Johnson, M.H., Pickering, S.J., and Flach, G. (1984). Changes in actin distribution during fertilization of the mouse egg. J. Embryol. Exp. Morphol. 81, 211-237.
27. Maro, B., Johnson, M.H., Webb, M., and Flach, G. (1986). Mechanism of polar body formation in the mouse oocyte: an interaction between the chromosomes, the cytoskeleton, and the plasma membrane. J. Embryol. Exp. Morphol. 92, 11-32.
28. Maupin, P., Phillips, C.L., Adelstein, R.S., and Pollard, T.D. (1994). Differential localization of myosin-II isozymes in human cultured cells and blood cells. J. Cell Sci. 107, 3077-3090.
29. Mazia, D., Schatten, G., and Sale, W. (1975). Adhesion of cells to surfaces coated with polylysine. J. Cell Biol. 66, 198-200.
30. Miller, M., Bower, E., Levitt, P., Li, D., and Chantler, P.D. (1992). Myosin II distribution in neurons is consistent with a role in growth cone motility but not synaptic vesicle mobilization. Neuron 8, 25-44.
31. Murakami, N., and Elzinga, M. (1992). Immunohistochemical studies on distribution of cellular myosin II isoforms in brain and aorta. Cell Motil. Cytoskeleton 22, 281-295.
32. Nicosia, S.V., Wolf, D.P., and Inoue, M. (1977). Cortical granule distribution and cell surface characteristics in mouse eggs. Dev. Biol. 57, 56-74.
33. Nicosia, S.V., Wolf, D.P., and Mastroianni, L. (1978). Surface topography of mouse eggs before and after insemination. Gamete Res. 1, 145-155.
34. Nowak, G., Pestic-Dragovich, L., Hozak, P., Philimonenko, A., Simerly, C., Schatten, G., and de Lanerolle, P. (1997). Evidence for the presence of myosin I in the nucleus. J. Biol. Chem. 272, 17176-17181.
35. Olson, G.E., Winfrey, V.P., and Flaherty, S.P. (1987). Cytoskeletal assemblies of mammalian spermatozoa. Ann. NY Acad. Sci. 513, 222-246.
36. Phillips, C.L., Yamakawa, K., and Adelstein, R.S. (1995). Cloning of the cDNA encoding human nonmuscle myosin heavy chain-B and analysis of human tissues with isoform-specific antibodies. J. Muscle Res. Cell Motil. 16, 379-389.
37. Reima, I., and Lehtonen, E. (1985). Localization of nonerythroid spectrin and actin in mouse oocytes and preimplantation embryos. Differentiation 30, 68-75.
38. Rochlin, M.W., Itoh, K., Adelstein, R.S., and Bridgman, P.C. (1995). Localization of myosin IIA and B isoforms in cultured neurons. J. Cell Sci. 108, 3661-3670.
39. Saez, C.G., Myers, J.C., Shows, T.B., and Leinwand, L.A. (1990). Human nonmuscle myosin heavy chain mRNA: generation of diversity through alternative polyadenylation. Proc. Natl. Acad. Sci. USA 87, 1164-1168.
40. Sanger, J.M., Mittal, B., Dome, J.S., and Sanger, J.W. (1989). Analysis of cell division using fluorescently labeled actin and myosin in living PtK2 cells. Cell Motil. Cytoskeleton 14, 201-219.
41. cdc2: a mechanism for the timing of cytokinesis. J. Cell Biol. 118, 595-605.
42. Sauman, I., and Berry, S.J. (1994). An actin infrastructure is associated with eukaryotic chromosomes: structural and functional significance. Eur. J. Cell Biol. 64, 348-356.
43. Schatten, G., Schatten, H., Spector, I., Cline, C., Paweletz, N., Simerly, C., and Petzelt, C. (1986a). Latrunculin inhibits the microfilament-mediated processes during fertilization, cleavage, and early development in sea urchins and mice. Exp. Cell Res. 166, 191-208.
44. Schatten, G., Simerly, C., Asai, D.J., Szöke, E., Cooke, P., and Schatten, H. (1988). Acetylated α-tubulin in microtubules during mouse fertilization and early development. Dev. Biol. 130, 74-86.
45. Schatten, G., and Schatten, H. (1987). Cytoskeletal alterations and nuclear architectural changes during mammalian fertilization. Curr. Top. Dev. Biol. 23, 23-54.
46. Schatten, H., Cheney, R., Balczon, R., Willard, M., Cline, C., Simerly, C., and Schatten, G. (1986b). Localization of fodrin during fertilization and early development of sea urchins and mice. Dev. Biol. 118, 457-466.
47. Sellers, J.R. (1991). Regulation of cytoplasmic and smooth muscle myosin. Curr. Opin. Cell Biol. 3, 98-104.
48. Shalgi, R., Phillips, D.M., and Kraicer, P.F. (1978). Observation on the incorporation cone in the rat. Gamete Res. 1, 27-37.
49. Simerly, C., Balczon, R., Brinkley, B.R., and Schatten, G. (1990). Microinjected kinetochore antibodies interfere with chromosome movement in meiotic and mitotic mouse oocytes. J. Cell Biol. 111, 1491-1504.
50. Simerly, C., Hecht, N., Goldberg, E., and Schatten, G. (1993). Tracing the incorporation of the sperm tail in the mouse zygote and early embryo using an anti-testicular α-tubulin antibody. Dev. Biol. 158, 536-548.
51. Simerly, C., Navara, C., Wu, G.-J., and Schatten, G. (1995). Cytoskeletal organization and dynamics in mammalian oocytes during maturation and fertilization. In: Cambridge Reviews in Human Reproduction. Gametes: The Oocyte, ed. J.G. Grudzinskas and J.L. Yovich, Cambridge: Cambridge University Press, 54-94.
52. Simerly, C., and Schatten, G. (1994). Techniques for the localization of specific molecules in oocytes and embryos. In: Methods in Enzymology, Vol. 225, ed. P.M. Wassarman and M. L. DePamphila, San Diego: Academic Press, 516-553.
53. Slager, H.G., Good, M.J., Schaart, G., Groenewoud, J.S., and Mummery, C.L. (1992). Organization of non-muscle myosin during early murine embryonic differentiation. Differentiation 50, 47-56.
54. Sobel, J.S. (1983a). Localization of myosin in the preimplantation mouse embryo. Dev. Biol. 95, 227-231.
55. Sobel, J.S. (1983b). Cell-cell contact modulation of myosin organization in the early mouse embryo. Dev. Biol. 100, 207-213.
56. Sobel, J.S. (1984). Myosin rings and spreading in mouse blastomeres. J. Cell Biol. 99, 1145-1150.
57. Sobel, J.S., and Allegro, M.A. (1985). Changes in the distribution of spectrin-like protein during development of the preimplantation mouse embryo. J. Cell Biol,.100, 333-336.
58. Sun, W., and Chantler, P.D. (1991). A unique cellular myosin II exhibiting differential expression in the cerebral cortex. Biochem. Biophys. Res. Commun. 175, 244-249.
59. Tamblyn, T.M. (1981). Evidence for non-muscle myosin in bovine ejaculated spermatozoa. Gamete Res. 4, 499-506.
60. Toothaker, L..E., Gonzalez, D.A., Tung, N., Lemons, R.S., Le Beau, M.M., Arnaout, M.A., Clayton, L.K., and Jenen, D.G. (1991). Cellular myosin heavy chain in human leukocytes: isolation of 5′ cDNA clones, characterization of the protein, chromosomal localization, and up-regulation during myeloid differentiation. Blood 78, 1826-1833.
61. Van Blerkom, J., and Bell, H. (1986). Regulation of development in the fully grown mouse oocyte: chromosome-mediated temporal and spatial differentiation of the cytoplasm and plasma membrane. J. Embryol. Exp. Morphol. 93, 213-238.
62. Virtanen, I., Badley, R.A., Paasivuo, R., and Lehto, V.P. (1984). Distinct cytoskeletal domains revealed in sperm cells. J. Cell Biol. 99, 1083-1091.
63. Walt, H., Saremaslani, P., Heizmann, C.W., and Hedinger, C. (1982). Myosin in early spermatids of the rat. Virchows Arch. B Cell Pathol. Inc. Mol. Pathol. 38, 307-310.
64. Wassarman, P.M., Josefowicz, W.J., Letourneau, G.E. (1976). Meiotic maturation of mouse oocytes in vitro: inhibition of maturation at specific stages of nuclear progression. J. Cell Sci. 22, 531-545.
65. Webb, M., Howlett, S.K., and Maro, B. (1986). Parthenogenesis and cytoskeleton organization in aging mouse oocytes. J. Embryol. Exp. Morphol. 95, 131-145.
66. Wilson, A.K., Gongas, G., Clampool, W.D., and de Lanerolle, P. (1991). An increase or a decrease in myosin II phosphorylation inhibits macrophage motility. J. Cell Biol. 114, 277-283.
67. Yoshihiko, Y., Yamashiro, S., and Matsumura, F. (1994). In vivo phosphorylation of regulatory light chain of myosin II during mitosis of cultured cells. J. Cell Biol. 124, 129-137.
68. Yumura, S., and Uyeda, T.Q.P. (1997). Myosin II can be localized to the cleavage furrow and to the posterior region of Dictyostelium amoebae without control by phosphorylation of myosin heavy and light chains. Cell Motil. Cytoskeleton 36, 313-322.
69. Zurek, B., Sanger, J.M., Sanger, J.W., and Jockusch, B.M. (1990). Differential effects of myosin-antibody complexes on contractile rings and circumferential belts in epithelioid cells. J. Cell Sci. 97, 297-306.