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. 1996 Jul 1;494(Pt 1):29–40. doi: 10.1113/jphysiol.1996.sp021473

Spatiotemporal analysis of calcium dynamics in the nucleus of hamster oocytes.

H Shirakawa 1, S Miyazaki 1
PMCID: PMC1160612  PMID: 8814604

Abstract

1. Subcellular Ca2+ dynamics inside and around the nucleus of immature hamster oocytes were analysed with confocal Ca2+ imaging. 2. The ratio value between emission intensity of two injected fluorescent Ca2+ indicators, Calcium Green and Fura Red, was almost uniform over the entire oocyte, suggesting that nucleoplasmic Ca2+ concentration ([Ca2+]n) is comparable to cytoplasmic Ca2+ concentration ([Ca2+]c) at the resting state. 3. When Ca2+ was iontophoretically injected into the nucleoplasm or the perinuclear cytoplasm, it diffused across the nuclear envelope (NE), and perinuclear [Ca2+]c and [Ca2+]n reached the same level within 2 s, although the NE worked as a weak but detectable barrier for Ca2+ diffusion. 4. Inositol 1,4,5-trisphosphate (IP3)-induced Ca2+ release from the NE through the inner membrane was not detected, even when a large amount of IP3 was delivered in close proximity to the inner nuclear membrane. 5. When an oocyte was uniformly stimulated by photolysis of caged IP3, a Ca2+ rise was initiated in the perinuclear cytoplasm. The [Ca2+]n rise was always delayed with respect to, but rapidly equilibrated with, the [Ca2+]c rise. 6. Clusters of the endoplasmic reticulum were located in the perinuclear cytoplasm and served as the trigger zone of IP3-induced Ca2+ release. 7. The results indicate that the [Ca2+]n rise occurs as the consequence of the influx of Ca2+ which was released in the perinuclear cytoplasm, not Ca2+ release from NE to the nucleoplasm.

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Selected References

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  1. Baitinger C., Alderton J., Poenie M., Schulman H., Steinhardt R. A. Multifunctional Ca2+/calmodulin-dependent protein kinase is necessary for nuclear envelope breakdown. J Cell Biol. 1990 Nov;111(5 Pt 1):1763–1773. doi: 10.1083/jcb.111.5.1763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Boynton A. L., Whitfield J. F., MacManus J. P. Calmodulin stimulates DNA synthesis by rat liver cells. Biochem Biophys Res Commun. 1980 Jul 31;95(2):745–749. doi: 10.1016/0006-291x(80)90849-9. [DOI] [PubMed] [Google Scholar]
  3. Carroll J., Swann K. Spontaneous cytosolic calcium oscillations driven by inositol trisphosphate occur during in vitro maturation of mouse oocytes. J Biol Chem. 1992 Jun 5;267(16):11196–11201. [PubMed] [Google Scholar]
  4. Carroll J., Swann K., Whittingham D., Whitaker M. Spatiotemporal dynamics of intracellular [Ca2+]i oscillations during the growth and meiotic maturation of mouse oocytes. Development. 1994 Dec;120(12):3507–3517. doi: 10.1242/dev.120.12.3507. [DOI] [PubMed] [Google Scholar]
  5. Divecha N., Rhee S. G., Letcher A. J., Irvine R. F. Phosphoinositide signalling enzymes in rat liver nuclei: phosphoinositidase C isoform beta 1 is specifically, but not predominantly, located in the nucleus. Biochem J. 1993 Feb 1;289(Pt 3):617–620. doi: 10.1042/bj2890617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Franke W. W., Scheer U., Krohne G., Jarasch E. D. The nuclear envelope and the architecture of the nuclear periphery. J Cell Biol. 1981 Dec;91(3 Pt 2):39s–50s. doi: 10.1083/jcb.91.3.39s. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fujiwara T., Nakada K., Shirakawa H., Miyazaki S. Development of inositol trisphosphate-induced calcium release mechanism during maturation of hamster oocytes. Dev Biol. 1993 Mar;156(1):69–79. doi: 10.1006/dbio.1993.1059. [DOI] [PubMed] [Google Scholar]
  8. Furuno T., Hamano T., Nakanishi M. Receptor-mediated calcium signal playing a nuclear third messenger in the activation of antigen-specific B cells. Biophys J. 1993 Mar;64(3):665–669. doi: 10.1016/S0006-3495(93)81425-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gerasimenko O. V., Gerasimenko J. V., Tepikin A. V., Petersen O. H. ATP-dependent accumulation and inositol trisphosphate- or cyclic ADP-ribose-mediated release of Ca2+ from the nuclear envelope. Cell. 1995 Feb 10;80(3):439–444. doi: 10.1016/0092-8674(95)90494-8. [DOI] [PubMed] [Google Scholar]
  10. Gillot I., Whitaker M. Calcium signals in and around the nucleus in sea urchin eggs. Cell Calcium. 1994 Oct;16(4):269–278. doi: 10.1016/0143-4160(94)90090-6. [DOI] [PubMed] [Google Scholar]
  11. Giovannardi S., Cesare P., Peres A. Rapid synchrony of nuclear and cytosolic Ca2+ signals activated by muscarinic stimulation in the human tumour line TE671/RD. Cell Calcium. 1994 Dec;16(6):491–499. doi: 10.1016/0143-4160(94)90079-5. [DOI] [PubMed] [Google Scholar]
  12. Hennager D. J., Welsh M. J., DeLisle S. Changes in either cytosolic or nucleoplasmic inositol 1,4,5-trisphosphate levels can control nuclear Ca2+ concentration. J Biol Chem. 1995 Mar 10;270(10):4959–4962. doi: 10.1074/jbc.270.10.4959. [DOI] [PubMed] [Google Scholar]
  13. Himpens B., De Smedt H., Casteels R. Relationship between [Ca2+] changes in nucleus and cytosol. Cell Calcium. 1994 Oct;16(4):239–246. doi: 10.1016/0143-4160(94)90087-6. [DOI] [PubMed] [Google Scholar]
  14. Homa S. T. Neomycin, an inhibitor of phosphoinositide hydrolysis, inhibits the resumption of bovine oocyte spontaneous meiotic maturation. J Exp Zool. 1991 Apr;258(1):95–103. doi: 10.1002/jez.1402580111. [DOI] [PubMed] [Google Scholar]
  15. Horowitz S. B. The permeability of the amphibian oocyte nucleus, in situ. J Cell Biol. 1972 Sep;54(3):609–625. doi: 10.1083/jcb.54.3.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Iino M., Endo M. Calcium-dependent immediate feedback control of inositol 1,4,5-triphosphate-induced Ca2+ release. Nature. 1992 Nov 5;360(6399):76–78. doi: 10.1038/360076a0. [DOI] [PubMed] [Google Scholar]
  17. Katagiri S., Takamatsu T., Minamikawa T., Fujita S. Secretagogue-induced calcium wave shows higher and prolonged transients of nuclear calcium concentration in mast cells. FEBS Lett. 1993 Nov 22;334(3):343–346. doi: 10.1016/0014-5793(93)80708-3. [DOI] [PubMed] [Google Scholar]
  18. Kaufman M. L., Homa S. T. Defining a role for calcium in the resumption and progression of meiosis in the pig oocyte. J Exp Zool. 1993 Jan 1;265(1):69–76. doi: 10.1002/jez.1402650110. [DOI] [PubMed] [Google Scholar]
  19. Lanini L., Bachs O., Carafoli E. The calcium pump of the liver nuclear membrane is identical to that of endoplasmic reticulum. J Biol Chem. 1992 Jun 5;267(16):11548–11552. [PubMed] [Google Scholar]
  20. Lefèvre B., Pesty A., Testart J. Cytoplasmic and nucleic calcium oscillations in immature mouse oocytes: evidence of wave polarization by confocal imaging. Exp Cell Res. 1995 May;218(1):166–173. doi: 10.1006/excr.1995.1144. [DOI] [PubMed] [Google Scholar]
  21. Lin C., Hajnóczky G., Thomas A. P. Propagation of cytosolic calcium waves into the nuclei of hepatocytes. Cell Calcium. 1994 Oct;16(4):247–258. doi: 10.1016/0143-4160(94)90088-4. [DOI] [PubMed] [Google Scholar]
  22. Lipp P., Niggli E. Ratiometric confocal Ca(2+)-measurements with visible wavelength indicators in isolated cardiac myocytes. Cell Calcium. 1993 May;14(5):359–372. doi: 10.1016/0143-4160(93)90040-d. [DOI] [PubMed] [Google Scholar]
  23. Malviya A. N. The nuclear inositol 1,4,5-trisphosphate and inositol 1,3,4,5-tetrakisphosphate receptors. Cell Calcium. 1994 Oct;16(4):301–313. doi: 10.1016/0143-4160(94)90094-9. [DOI] [PubMed] [Google Scholar]
  24. McCray J. A., Trentham D. R. Properties and uses of photoreactive caged compounds. Annu Rev Biophys Biophys Chem. 1989;18:239–270. doi: 10.1146/annurev.bb.18.060189.001323. [DOI] [PubMed] [Google Scholar]
  25. Minamikawa T., Takahashi A., Fujita S. Differences in features of calcium transients between the nucleus and the cytosol in cultured heart muscle cells: analyzed by confocal microscopy. Cell Calcium. 1995 Mar;17(3):167–176. doi: 10.1016/0143-4160(95)90031-4. [DOI] [PubMed] [Google Scholar]
  26. Miyazaki S., Yuzaki M., Nakada K., Shirakawa H., Nakanishi S., Nakade S., Mikoshiba K. Block of Ca2+ wave and Ca2+ oscillation by antibody to the inositol 1,4,5-trisphosphate receptor in fertilized hamster eggs. Science. 1992 Jul 10;257(5067):251–255. doi: 10.1126/science.1321497. [DOI] [PubMed] [Google Scholar]
  27. Nicotera P., Orrenius S., Nilsson T., Berggren P. O. An inositol 1,4,5-trisphosphate-sensitive Ca2+ pool in liver nuclei. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6858–6862. doi: 10.1073/pnas.87.17.6858. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Nicotera P., Zhivotovsky B., Orrenius S. Nuclear calcium transport and the role of calcium in apoptosis. Cell Calcium. 1994 Oct;16(4):279–288. doi: 10.1016/0143-4160(94)90091-4. [DOI] [PubMed] [Google Scholar]
  29. O'Malley D. M. Calcium permeability of the neuronal nuclear envelope: evaluation using confocal volumes and intracellular perfusion. J Neurosci. 1994 Oct;14(10):5741–5758. doi: 10.1523/JNEUROSCI.14-10-05741.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Opas M., Dziak E., Fliegel L., Michalak M. Regulation of expression and intracellular distribution of calreticulin, a major calcium binding protein of nonmuscle cells. J Cell Physiol. 1991 Oct;149(1):160–171. doi: 10.1002/jcp.1041490120. [DOI] [PubMed] [Google Scholar]
  31. Roche E., Prentki M. Calcium regulation of immediate-early response genes. Cell Calcium. 1994 Oct;16(4):331–338. doi: 10.1016/0143-4160(94)90097-3. [DOI] [PubMed] [Google Scholar]
  32. Shen S. S., Buck W. R. Sources of calcium in sea urchin eggs during the fertilization response. Dev Biol. 1993 May;157(1):157–169. doi: 10.1006/dbio.1993.1120. [DOI] [PubMed] [Google Scholar]
  33. Shiraishi K., Okada A., Shirakawa H., Nakanishi S., Mikoshiba K., Miyazaki S. Developmental changes in the distribution of the endoplasmic reticulum and inositol 1,4,5-trisphosphate receptors and the spatial pattern of Ca2+ release during maturation of hamster oocytes. Dev Biol. 1995 Aug;170(2):594–606. doi: 10.1006/dbio.1995.1239. [DOI] [PubMed] [Google Scholar]
  34. Stricker S. A., Centonze V. E., Melendez R. F. Calcium dynamics during starfish oocyte maturation and fertilization. Dev Biol. 1994 Nov;166(1):34–58. doi: 10.1006/dbio.1994.1295. [DOI] [PubMed] [Google Scholar]
  35. Sullivan K. M., Busa W. B., Wilson K. L. Calcium mobilization is required for nuclear vesicle fusion in vitro: implications for membrane traffic and IP3 receptor function. Cell. 1993 Jul 2;73(7):1411–1422. doi: 10.1016/0092-8674(93)90366-x. [DOI] [PubMed] [Google Scholar]
  36. Terasaki M., Jaffe L. A. Organization of the sea urchin egg endoplasmic reticulum and its reorganization at fertilization. J Cell Biol. 1991 Sep;114(5):929–940. doi: 10.1083/jcb.114.5.929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Thastrup O., Cullen P. J., Drøbak B. K., Hanley M. R., Dawson A. P. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2466–2470. doi: 10.1073/pnas.87.7.2466. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Tombes R. M., Simerly C., Borisy G. G., Schatten G. Meiosis, egg activation, and nuclear envelope breakdown are differentially reliant on Ca2+, whereas germinal vesicle breakdown is Ca2+ independent in the mouse oocyte. J Cell Biol. 1992 May;117(4):799–811. doi: 10.1083/jcb.117.4.799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Whitaker M., Patel R. Calcium and cell cycle control. Development. 1990 Apr;108(4):525–542. doi: 10.1242/dev.108.4.525. [DOI] [PubMed] [Google Scholar]
  40. al-Mohanna F. A., Caddy K. W., Bolsover S. R. The nucleus is insulated from large cytosolic calcium ion changes. Nature. 1994 Feb 24;367(6465):745–750. doi: 10.1038/367745a0. [DOI] [PubMed] [Google Scholar]

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