Maturation-promoting factor induces nuclear envelope breakdown in cycloheximide-arrested embryos of Xenopus laevis

We have studied the effect of maturation-promoting factor (MPF) on embryonic nuclei during the early cleavage stage of Xenopus laevis development. When protein synthesis is inhibited by cycloheximide during this stage, the embryonic cell cycle arrests in an artificially produced G2 phase-like state, after completion of one additional round of DNA synthesis. Approximately 100 nuclei can be arrested in a common cytoplasm if cytokinesis is first inhibited by cytochalasin B. Within 5 min after injection of MPF into such embryos, the nuclear envelope surrounding each nucleus disperses, as determined histologically or by immunofluorescent staining of the nuclear lamina with antilamin antiserum. The breakdown of the nuclear envelope occurs at levels of MPF comparable to or slightly lower than those required for oocyte maturation. Amplification of MPF activity, however, does not occur in the arrested egg as it does in the oocyte. These results suggest that MPF can act to advance interphase nuclei into the first events of mitosis and show that the nuclear lamina responds rapidly to MPF.

[1]  M. Kirschner,et al.  A major developmental transition in early xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage , 1982, Cell.

[2]  J. Sedat,et al.  Fluorescence microscopy: reduced photobleaching of rhodamine and fluorescein protein conjugates by n-propyl gallate. , 1982, Science.

[3]  P. Cohen,et al.  The role of protein phosphorylation in neural and hormonal control of cellular activity , 1982, Nature.

[4]  G. Krohne,et al.  Immunological localization of the major architectural protein associated with the nuclear envelope of the Xenopus laevis oocyte. , 1982, Experimental cell research.

[5]  L. D. Smith,et al.  Calmodulin triggers the resumption of meiosis in amphibian oocytes , 1981, The Journal of cell biology.

[6]  W. N. Burnette,et al.  "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate--polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. , 1981, Analytical biochemistry.

[7]  R. Harland,et al.  Regulated replication of DNA microinjected into eggs of Xenopus laevis , 1980, Cell.

[8]  J. Gerhart,et al.  Partial purification and characterization of the maturation-promoting factor from eggs of Xenopus laevis. , 1980, Developmental biology.

[9]  G. Blobel,et al.  The nuclear envelope lamina is reversibly depolymerized during mitosis , 1980, Cell.

[10]  B. Vogelstein,et al.  Protein factor(s) from mitotic CHO cells induce meiotic maturation in Xenopus laevis oocytes , 1980, FEBS letters.

[11]  G. Blobel,et al.  Immunocytochemical localization of the major polypeptides of the nuclear pore complex-lamina fraction. Interphase and mitotic distribution , 1978, The Journal of cell biology.

[12]  S. Ely,et al.  Localization of a nuclear envelope-associated protein by indirect immunofluorescence microscopy using antibodies against a major polypeptide from rat liver fractions enriched in nuclear envelope-associated material. , 1978, Cytobiologie.

[13]  L. D. Smith,et al.  The cyclic behavior of a cytoplasmic factor controlling nuclear membrane breakdown , 1978, The Journal of cell biology.

[14]  R. Merriam,et al.  Diffusible and bound actin in nuclei of xenopus laevis oocytes , 1977, Cell.

[15]  S. Løvtrup,et al.  Deoxynucleoside inhibition of differentiation in cultured embryonic cells. , 1977, Experimental cell research.

[16]  J. Gerhart,et al.  Changes in protein phosphorylation accompanying maturation of Xenopus laevis oocytes. , 1977, Developmental biology.

[17]  E. Adamson,et al.  The synthesis and storage of histones during the oogenesis of Xenopus laevis. , 1977, Developmental biology.

[18]  E. Krebs,et al.  Progesterone-stimulated meiotic cell division in Xenopus oocytes. Induction by regulatory subunit and inhibition by catalytic subunit of adenosine 3':5'-monophosphate-dependent protein kinase. , 1977, The Journal of biological chemistry.

[19]  M. Zalokar.  Autoradiographic study of protein and RNA formation during early development of Drosophila eggs. , 1976, Developmental biology.

[20]  M. Kirschner,et al.  Aster formation in eggs of Xenopus laevis. Induction by isolated basal bodies , 1975, The Journal of cell biology.

[21]  R. Benbow,et al.  Cytoplasmic control of nuclear DNA synthesis during early development of Xenopus laevis: a cell-free assay. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Y. Masui,et al.  Effects of cyclohexamide on a cytoplasmic factor initiating meiotic naturation in Xenopus oocytes. , 1975, Experimental cell research.

[23]  R. Pestell.  Microtubule protein synthesis during oogenesis and early embryogenesis in Xenopus laevis. , 1975, The Biochemical journal.

[24]  F. Eckstein.  Investigation of enzyme mechanisms with nucleoside phosphorothioates. , 1975, Angewandte Chemie.

[25]  J. Reynhout,et al.  Studies on the appearance and nature of a maturation-inducing factor in the cytoplasm of amphibian oocytes exposed to progesterone. , 1974, Developmental biology.

[26]  M. Hammer,et al.  Cytochalasin B II: Selective Inhibition of Cytokinesis in Xenopus laevis Eggs , 1971, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[27]  L. D. Smith,et al.  Role of the oocyte nucleus in physiological maturation in Rana pipiens. , 1969, Developmental biology.

[28]  R. W. Morgan,et al.  Changes in the cell cycle during early amphibian development , 1966 .

[29]  H. Kondo,et al.  Generality of the action of various maturation-promoting factors. , 1982, Experimental cell research.

[30]  J. Gerhart.  Mechanisms Regulating Pattern Formation in the Amphibian Egg and Early Embryo , 1980 .

[31]  J. Gerhart,et al.  Spatial and Temporal Changes in Early Amphibian Development , 1980 .

[32]  K Hara,et al.  A cytoplasmic clock with the same period as the division cycle in Xenopus eggs. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[33]  P. Sunkara,et al.  Mitotic factors from mammalian cells: a preliminary characterization. , 1979, Journal of supramolecular structure.

[34]  D. Mazia,et al.  THE EFFECT OF EMETINE ON FIRST CLEAVAGE DIVISION IN THE SEA URCHIN, STRONGYLOCENTROTUS PURPURATUS , 1978 .

[35]  S. Blackburn,et al.  Enzyme structure and function , 1976 .

[36]  L.Dennis Smith.  MOLECULAR EVENTS DURING OOCYTE MATURATION , 1975 .

[37]  G. Giudice.  Developmental biology of the sea urchin embryo , 1973 .