Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1989 Oct 1;109(4):1439–1444. doi: 10.1083/jcb.109.4.1439

Protein transport from endoplasmic reticulum to the Golgi complex can occur during meiotic metaphase in Xenopus oocytes

PMCID: PMC2115785  PMID: 2793929

Abstract

We have previously shown that Xenopus oocytes arrested at second meiotic metaphase lost their characteristic multicisternal Golgi apparati and cannot secrete proteins into the surrounding medium. In this paper, we extend these studies to ask whether intracellular transport events affecting the movement of secretory proteins from the endoplasmic reticulum to the Golgi apparatus are also similarly inhibited in such oocytes. Using the acquisition of resistance to endoglycosidase H (endo H) as an assay for movement to the Golgi, we find that within 6 h, up to 66% of the influenza virus membrane protein, hemagglutinin (HA), synthesized from injected synthetic RNA, can move to the Golgi apparati in nonmatured oocytes; indeed after longer periods some correctly folded HA can be detected at the cell surface where it distributes in a nonpolarized fashion. In matured oocytes, up to 49% of the HA becomes endo H resistant in the same 6-h period. We conclude that movement from the endoplasmic reticulum to the Golgi can occur in matured oocytes despite the dramatic fragmentation of the Golgi apparati that we observe to occur on maturation. This observation of residual protein movement during meiotic metaphase contrasts with the situation at mitotic metabphase in cultured mammalian cells where all movement ceases, but resembles that in the budding yeast Saccharomyces cerevisiae where transport is unaffected.

Full Text

The Full Text of this article is available as a PDF (1.4 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Balch W. E., Dunphy W. G., Braell W. A., Rothman J. E. Reconstitution of the transport of protein between successive compartments of the Golgi measured by the coupled incorporation of N-acetylglucosamine. Cell. 1984 Dec;39(2 Pt 1):405–416. doi: 10.1016/0092-8674(84)90019-9. [DOI] [PubMed] [Google Scholar]
  2. Beckers C. J., Balch W. E. Calcium and GTP: essential components in vesicular trafficking between the endoplasmic reticulum and Golgi apparatus. J Cell Biol. 1989 Apr;108(4):1245–1256. doi: 10.1083/jcb.108.4.1245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berlin R. D., Oliver J. M. Surface functions during mitosis. II. Quantitation of pinocytosis and kinetic characterization of the mitotic cycle with a new fluorescence technique. J Cell Biol. 1980 Jun;85(3):660–671. doi: 10.1083/jcb.85.3.660. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berlin R. D., Oliver J. M., Walter R. J. Surface functions during Mitosis I: phagocytosis, pinocytosis and mobility of surface-bound Con A. Cell. 1978 Oct;15(2):327–341. doi: 10.1016/0092-8674(78)90002-8. [DOI] [PubMed] [Google Scholar]
  5. Campanella C., Andreuccetti P., Taddei C., Talevi R. The modifications of cortical endoplasmic reticulum during in vitro maturation of Xenopus laevis oocytes and its involvement in cortical granule exocytosis. J Exp Zool. 1984 Feb;229(2):283–293. doi: 10.1002/jez.1402290214. [DOI] [PubMed] [Google Scholar]
  6. Ceriotti A., Colman A. Binding to membrane proteins within the endoplasmic reticulum cannot explain the retention of the glucose-regulated protein GRP78 in Xenopus oocytes. EMBO J. 1988 Mar;7(3):633–638. doi: 10.1002/j.1460-2075.1988.tb02857.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Colman A., Cutler D., Krieg P., Valle G. The oocyte as a secretory cell. Ciba Found Symp. 1983;98:249–267. doi: 10.1002/9780470720790.ch14. [DOI] [PubMed] [Google Scholar]
  8. Colman A., Jones E. A., Heasman J. Meiotic maturation in Xenopus oocytes: a link between the cessation of protein secretion and the polarized disappearance of Golgi apparati. J Cell Biol. 1985 Jul;101(1):313–318. doi: 10.1083/jcb.101.1.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Copeland C. S., Zimmer K. P., Wagner K. R., Healey G. A., Mellman I., Helenius A. Folding, trimerization, and transport are sequential events in the biogenesis of influenza virus hemagglutinin. Cell. 1988 Apr 22;53(2):197–209. doi: 10.1016/0092-8674(88)90381-9. [DOI] [PubMed] [Google Scholar]
  10. Cork R. J., Cicirelli M. F., Robinson K. R. A rise in cytosolic calcium is not necessary for maturation of Xenopus laevis oocytes. Dev Biol. 1987 May;121(1):41–47. doi: 10.1016/0012-1606(87)90136-9. [DOI] [PubMed] [Google Scholar]
  11. Cutler D., Lane C., Colman A. Non-parallel kinetics and the role of tissue-specific factors in the secretion of chicken ovalbumin and lysozyme from Xenopus oocytes. J Mol Biol. 1981 Dec 25;153(4):917–931. doi: 10.1016/0022-2836(81)90459-9. [DOI] [PubMed] [Google Scholar]
  12. Dumont J. N. Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J Morphol. 1972 Feb;136(2):153–179. doi: 10.1002/jmor.1051360203. [DOI] [PubMed] [Google Scholar]
  13. Featherstone C., Griffiths G., Warren G. Newly synthesized G protein of vesicular stomatitis virus is not transported to the Golgi complex in mitotic cells. J Cell Biol. 1985 Dec;101(6):2036–2046. doi: 10.1083/jcb.101.6.2036. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gahmberg N., Pettersson R. F., Käriäinen L. Efficient transport of Semliki Forest virus glycoproteins through a Golgi complex morphologically altered by Uukuniemi virus glycoproteins. EMBO J. 1986 Dec 1;5(12):3111–3118. doi: 10.1002/j.1460-2075.1986.tb04617.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gething M. J., Bye J., Skehel J., Waterfield M. Cloning and DNA sequence of double-stranded copies of haemagglutinin genes from H2 and H3 strains elucidates antigenic shift and drift in human influenza virus. Nature. 1980 Sep 25;287(5780):301–306. doi: 10.1038/287301a0. [DOI] [PubMed] [Google Scholar]
  16. Gething M. J., McCammon K., Sambrook J. Expression of wild-type and mutant forms of influenza hemagglutinin: the role of folding in intracellular transport. Cell. 1986 Sep 12;46(6):939–950. doi: 10.1016/0092-8674(86)90076-0. [DOI] [PubMed] [Google Scholar]
  17. Kornfeld R., Kornfeld S. Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem. 1985;54:631–664. doi: 10.1146/annurev.bi.54.070185.003215. [DOI] [PubMed] [Google Scholar]
  18. Krieg P. A., Melton D. A. Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucleic Acids Res. 1984 Sep 25;12(18):7057–7070. doi: 10.1093/nar/12.18.7057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lucocq J. M., Pryde J. G., Berger E. G., Warren G. A mitotic form of the Golgi apparatus in HeLa cells. J Cell Biol. 1987 Apr;104(4):865–874. doi: 10.1083/jcb.104.4.865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lucocq J. M., Warren G. Fragmentation and partitioning of the Golgi apparatus during mitosis in HeLa cells. EMBO J. 1987 Nov;6(11):3239–3246. doi: 10.1002/j.1460-2075.1987.tb02641.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Makarow M. Secretion of invertase in mitotic yeast cells. EMBO J. 1988 May;7(5):1475–1482. doi: 10.1002/j.1460-2075.1988.tb02965.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Matlin K. S. The sorting of proteins to the plasma membrane in epithelial cells. J Cell Biol. 1986 Dec;103(6 Pt 2):2565–2568. doi: 10.1083/jcb.103.6.2565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Maul G. G., Brinkley B. R. The golgi apparatus during mitosis in human melanoma cells in vitro. Cancer Res. 1970 Sep;30(9):2326–2335. [PubMed] [Google Scholar]
  24. Poenie M., Alderton J., Steinhardt R., Tsien R. Calcium rises abruptly and briefly throughout the cell at the onset of anaphase. Science. 1986 Aug 22;233(4766):886–889. doi: 10.1126/science.3755550. [DOI] [PubMed] [Google Scholar]
  25. Rothman J. E., Miller R. L., Urbani L. J. Intercompartmental transport in the Golgi complex is a dissociative process: facile transfer of membrane protein between two Golgi populations. J Cell Biol. 1984 Jul;99(1 Pt 1):260–271. doi: 10.1083/jcb.99.1.260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Schmitt H. D., Puzicha M., Gallwitz D. Study of a temperature-sensitive mutant of the ras-related YPT1 gene product in yeast suggests a role in the regulation of intracellular calcium. Cell. 1988 May 20;53(4):635–647. doi: 10.1016/0092-8674(88)90579-x. [DOI] [PubMed] [Google Scholar]
  27. Warren G., Davoust J., Cockcroft A. Recycling of transferrin receptors in A431 cells is inhibited during mitosis. EMBO J. 1984 Oct;3(10):2217–2225. doi: 10.1002/j.1460-2075.1984.tb02119.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Warren G., Featherstone C., Griffiths G., Burke B. Newly synthesized G protein of vesicular stomatitis virus is not transported to the cell surface during mitosis. J Cell Biol. 1983 Nov;97(5 Pt 1):1623–1628. doi: 10.1083/jcb.97.5.1623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Zeligs J. D., Wollman S. H. Mitosis in rat thyroid epithelial cells in vivo. I. Ultrastructural changes in cytoplasmic organelles during the mitotic cycle. J Ultrastruct Res. 1979 Jan;66(1):53–77. doi: 10.1016/s0022-5320(79)80065-9. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES