Development and Reproduction (한국발생생물학회지:발생과생식)

The Korean Society of Developmental Biology (한국발생생물학회)
권호 표지
DOI QR코드

DOI QR Code

Role of Type 1 Inositol 1,4,5-triphosphate Receptors in Mammalian Oocytes

  • Yoon, Sook Young (Fertility Center of CHA Gangnam Medical Center, CHA University)
  • Received : 2019.01.10
  • Accepted : 2019.02.27
  • Published : 2019.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

The ability of oocytes to undergo normal fertilization and embryo development is acquired during oocyte maturation which is transition from the germinal vesicle stage (GV), germinal vesicle breakdown (GVBD) to metaphase of meiosis II (MII). Part of this process includes redistribution of inositol 1, 4, 5-triphosphate receptor (IP3R), a predominant $Ca^{2+}$ channel on the endoplasmic reticulum membrane. Type 1 IP3R (IP3R1) is expressed in mouse oocytes dominantly. At GV stage, IP3R1 are arranged as a network throughout the cytoplasm with minute accumulation around the nucleus. At MII stage, IP3R1 diffuses to the entire cytoplasm in a more reticular manner, and obvious clusters of IP3R1 are observed at the cortex of the egg. This structural reorganization provides acquisition of $[Ca^{2+}]_i$ oscillatory activity during fertilization. In this review, general properties of IP3R1 in somatic cells and mammalian oocyte are introduced.

Keywords

References

  1. Ajduk A, Malagocki A, Maleszewski M (2008) Cytoplasmic maturation of mammalian oocytes: Development of a mechanism responsible for sperm-induced $Ca^{2+}$ oscillations. Reprod Biol 8:3-22. https://doi.org/10.1016/S1642-431X(12)60001-1
  2. Alzayady KJ, Wojcikiewicz RJH (2005) The role of $Ca^{2+}$ in triggering inositol 1,4,5-trisphosphate receptor ubiquitination. Biochem J 392:601-606. https://doi.org/10.1042/BJ20050949
  3. Aromolaran AAS, Blatter LA (2005) Modulation of intracellular $Ca^{2+}$ release and capacitative $Ca^{2+}$ entry by CaMKII inhibitors in bovine vascular endothelial cells. Am J Physiol Cell Physiol 289:C1426-C1436. https://doi.org/10.1152/ajpcell.00262.2005
  4. Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: Dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4:517-529. https://doi.org/10.1038/nrm1155
  5. Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1:11-21. https://doi.org/10.1038/35036035
  6. Brind S, Swann K, Carroll J (2000) Inositol 1,4,5-trisphosphate receptors are downregulated in mouse oocytes in response to sperm or adenophostin A but not to increases in intracellular $Ca^{2+}$ or egg activation. Dev Biol 223:251-265. https://doi.org/10.1006/dbio.2000.9728
  7. Cameron AM, Steiner JP, Roskams AJ, Ali SM, Ronnett GV, Snyder SH (1995) Calcineurin associated with the inositol 1,4,5-trisphosphate receptor-FKBP12 complex modulates $Ca^{2+}$ flux. Cell 83:463-472. https://doi.org/10.1016/0092-8674(95)90124-8
  8. Cui J, Matkovich SJ, deSouza N, Li S, Rosemblit N, Marks AR (2004) Regulation of the type 1 inositol 1, 4,5-trisphosphate receptor by phosphorylation at tyrosine 353. J Biol Chem 279:16311-16316. https://doi.org/10.1074/jbc.M400206200
  9. Dupont G, Goldbeter A (1998) CaM kinase II as frequency decoder of $Ca^{2+}$ oscillations. Bioessays 20:607-610. https://doi.org/10.1002/(SICI)1521-1878(199808)20:8<607::AID-BIES2>3.0.CO;2-F
  10. Fissore RA, Dobrinsky JR, Balise JJ, Duby RT, Robl JM (1992) Patterns of intracellular $Ca^{2+}$ concentrations in fertilized bovine eggs. Biol Reprod 47:960-969. https://doi.org/10.1095/biolreprod47.6.960
  11. Fissore RA, Longo FJ, Anderson E, Parys JB, Ducibella T (1999) Differential distribution of inositol trisphosphate receptor isoforms in mouse oocytes. Biol Reprod 60:49-57. https://doi.org/10.1095/biolreprod60.1.49
  12. Fukatsu K, Bannai H, Zhang S, Nakamura H, Inoue T, Mikoshiba K (2004) Lateral diffusion of inositol 1,4,5-trisphosphate receptor type 1 is regulated by actin filaments and 4.1N in neuronal dendrites. J Biol Chem 279:48976-48982. https://doi.org/10.1074/jbc.M408364200
  13. Greenberg EF, Lavik AR, Distelhorst CW (2014) Bcl-2 regulation of the inositol 1,4,5-trisphosphate receptor and calcium signaling in normal and malignant lymphocytes: Potential new target for cancer treatment. Biochim Biophys Acta 1843:2205-2210. https://doi.org/10.1016/j.bbamcr.2014.03.008
  14. Hamada K, Miyata T, Mayanagi K, Hirota J, Mikoshiba K (2002) Two-state conformational changes in inositol 1,4,5-trisphosphate receptor regulated by calcium. J Biol Chem 277:21115-21118. https://doi.org/10.1074/jbc.C200244200
  15. Hamada K, Terauchi A, Mikoshiba K (2003) Three-dimensional rearrangements within inositol 1,4,5-trisphosphate receptor by calcium. J Biol Chem 278:52881-52889. https://doi.org/10.1074/jbc.M309743200
  16. He CL, Damiani P, Ducibella T, Takahashi M, Tanzawa K, Parys JB, Fissore RA (1999) Isoforms of the inositol 1,4,5-trisphosphate receptor are expressed in bovine oocytes and ovaries: The type-1 isoform is down-regulated by fertilization and by injection of adenophostin A. Biol Reprod 61:935-943. https://doi.org/10.1095/biolreprod61.4.935
  17. Ito J, Yoon SY, Lee B, Vanderheyden V, Vermassen E, Wojcikiewicz R, Alfandari D, De Smedt H, Parys JB, Fissore RA (2008) Inositol 1,4,5-trisphosphate receptor 1, a widespread $Ca^{2+}$ channel, is a novel substrate of polo-like kinase 1 in eggs. Dev Biol 320:402-413. https://doi.org/10.1016/j.ydbio.2008.05.548
  18. Jayaraman T, Ondrias K, Ondria E, Marks AR (1996) Regulation of the inositol 1,4,5-trisphosphate receptor by tyrosine phosphorylation. Science 272:1492-1494. https://doi.org/10.1126/science.272.5267.1492
  19. Jellerette T, He CL, Wu H, Parys JB, Fissore RA (2000) Down-regulation of the inositol 1,4,5-trisphosphate receptor in mouse eggs following fertilization or parthenogenetic activation. Dev Biol 223:238-250. https://doi.org/10.1006/dbio.2000.9675
  20. Jellerette T, Kurokawa M, Lee B, Malcuit C, Yoon SY, Smyth J, Vermassen E, De Smedt H, Parys JB, Fissore RA (2004) Cell cycle-coupled $[Ca^{2+}](i)$ oscillations in mouse zygotes and function of the inositol 1,4,5-trisphosphate receptor-1. Dev Biol 274:94-109. https://doi.org/10.1016/j.ydbio.2004.06.020
  21. Jones KT (2005) Mammalian egg activation: From $Ca^{2+}$ spiking to cell cycle progression. Reproduction 130:813-823. https://doi.org/10.1530/rep.1.00710
  22. Jones KT, Carroll J, Merriman JA, Whittingham DG, Kono T (1995a) Repetitive sperm-induced $Ca^{2+}$ transients in mouse oocytes are cell cycle dependent. Development 121:3259-3266. https://doi.org/10.1242/dev.121.10.3259
  23. Jones KT, Carroll J, Whittingham DG (1995b) Ionomycin, thapsigargin, ryanodine, and sperm induced $Ca^{2+}$ release increase during meiotic maturation of mouse oocytes. J Biol Chem 270:6671-6677. https://doi.org/10.1074/jbc.270.12.6671
  24. Joseph SK, Hajnoczky G (2007) IP3 receptors in cell survival and apoptosis: $Ca^{2+}$ release and beyond. Apoptosis 12:951-968. https://doi.org/10.1007/s10495-007-0719-7
  25. Lee B, Vermassen E, Yoon SY, Vanderheyden V, Ito J, Alfandari D, De Smedt H, Parys JB, Fissore RA (2006a) Phosphorylation of IP3R1 and the regulation of $[Ca^{2+}]_{i}$ responses at fertilization: A role for the MAP kinase pathway. Development 133:4355-4365. https://doi.org/10.1242/dev.02624
  26. Lee B, Yoon SY, Fissore RA (2006b) Regulation of fertilization-initiated $[Ca^{2+}]_{i}$ oscillations in mammalian eggs: A multi-pronged approach. Semin Cell Dev Biol 17:274-284. https://doi.org/10.1016/j.semcdb.2006.02.011
  27. Lee B, Yoon SY, Malcuit C, Parys JB, Fissore RA (2010) Inositol 1,4,5-trisphosphate receptor 1 degradation in mouse eggs and impact on $[Ca^{2+}]_{i}$ oscillations. J Cell Physiol 222:238-247. https://doi.org/10.1002/jcp.21945
  28. Machaca K (2004) Increased sensitivity and clustering of elementary $Ca^{2+}$ release events during oocyte maturation. Dev Biol 275:170-182. https://doi.org/10.1016/j.ydbio.2004.08.004
  29. Machaca K (2007) $Ca^{2+}$ signaling differentiation during oocyte maturation. J Cell Physiol 213:331-340. https://doi.org/10.1002/jcp.21194
  30. Mak DOD, McBride SMJ, Petrenko NB, Foskett JK (2003) Novel regulation of calcium inhibition of the inositol 1,4,5-trisphosphate receptor calcium-release channel. J Gen Physiol 122:569-581. https://doi.org/10.1085/jgp.200308808
  31. Malcuit C, Knott JG, He C, Wainwright T, Parys JB, Robl JM, Fissore RA (2005) Fertilization and inositol 1,4,5-trisphosphate (IP3)-induced calcium release in type-1 inositol 1,4,5-trisphosphate receptor down-regulated bovine eggs. Biol Reprod 73:2-13. https://doi.org/10.1095/biolreprod.104.037333
  32. Malcuit C, Kurokawa M, Fissore RA (2006) Calcium oscillations and mammalian egg activation. J Cell Physiol 206:565-573. https://doi.org/10.1002/jcp.20471
  33. Marks AR (1997) Intracellular calcium-release channels: Regulators of cell life and death. Am J Physiol 272:H597-H605.
  34. Mehlmann LM, Kline D (1994) Regulation of intracellular calcium in the mouse egg: Calcium release in response to sperm or inositol trisphosphate is enhanced after meiotic maturation. Biol Reprod 51:1088-1098. https://doi.org/10.1095/biolreprod51.6.1088
  35. Mehlmann LM, Mikoshiba K, Kline D (1996) Redistribution and increase in cortical inositol 1,4,5-trisphosphate receptors after meiotic maturation of the mouse oocyte. Dev Biol 180:489-498. https://doi.org/10.1006/dbio.1996.0322
  36. Miyazaki S, Shirakawa H, Nakada K, Honda Y (1993) Essential role of the inositol 1,4,5-trisphosphate receptor/$Ca^{2+}$ release channel in $Ca^{2+}$ waves and $Ca^{2+}$ oscillations at fertilization of mammalian eggs. Dev Biol 158:62-78. https://doi.org/10.1006/dbio.1993.1168
  37. Miyazaki S, Yuzaki M, Nakada K, Shirakawa H, Nakanishi S, Nakade S, Mikoshiba K (1992) Block of $Ca^{2+}$ wave and $Ca^{2+}$ oscillation by antibody to the inositol 1,4,5-trisphosphate receptor in fertilized hamster eggs. Science 257:251-255. https://doi.org/10.1126/science.1321497
  38. Polanski Z, Homer H, Kubiak JZ (2012) Cyclin B in mouse oocytes and embryos: Importance for human reproduction and aneuploidy. Results Probl Cell Differ 55:69-91. https://doi.org/10.1007/978-3-642-30406-4_4
  39. Prentki M, Wollheim CB, Lew PD (1984) $Ca^{2+}$ homeostasis in permeabilized human neutrophils. Characterization of $Ca^{2+}$-sequestering pools and the action of inositol 1,4,5-triphosphate. J Biol Chem 259:13777-13782. https://doi.org/10.1016/S0021-9258(18)89813-1
  40. Rahman T (2012) Dynamic clustering of IP3 receptors by IP3. Biochem Soc Trans 40:325-330. https://doi.org/10.1042/BST20110772
  41. Rahman TU, Skupin A, Falcke M, Taylor CW (2009) Clustering of InsP3 receptors by InsP3 retunes their regulation by InsP3 and $Ca^{2+}$. Nature 458:655-659. https://doi.org/10.1038/nature07763
  42. Schlossmann J, Ammendola A, Ashman K, Zong X, Huber A, Neubauer G, Wang GX, Allescher HD, Korth M, Wilm M, Hofmann F, Ruth P (2000) Regulation of intracellular calcium by a signalling complex of IRAG, IP3 receptor and cGMP kinase Ibeta. Nature 404:197-201. https://doi.org/10.1038/35004606
  43. Sun L, Yu F, Ullah A, Hubrack S, Daalis A, Jung P, Machaca K (2011) Endoplasmic reticulum remodeling tunes IP3-dependent $Ca^{2+}$ release sensitivity. PLOS ONE 6:e27928. https://doi.org/10.1371/journal.pone.0027928
  44. Supattapone S, Worley PF, Baraban JM, Snyder SH (1988) Solubilization, purification, and characterization of an inositol trisphosphate receptor. J Biol Chem 263:1530-1534. https://doi.org/10.1016/S0021-9258(19)57336-7
  45. Tang TS, Tu H, Wang Z, Bezprozvanny I (2003) Modulation of type 1 inositol (1,4,5)-trisphosphate receptor function by protein kinase a and protein phosphatase 1alpha. J Neurosci 23:403-415. https://doi.org/10.1523/JNEUROSCI.23-02-00403.2003
  46. Tateishi Y, Hattori M, Nakayama T, Iwai M, Bannai H, Nakamura T, Michikawa T, Inoue T, Mikoshiba K (2005) Cluster formation of inositol 1,4,5-trisphosphate receptor requires its transition to open state. J Biol Chem 280:6816-6822. https://doi.org/10.1074/jbc.M405469200
  47. Taylor CW, Tovey SC (2010) IP(3) receptors: Toward understanding their activation. Cold Spring Harb Perspect Biol 2:a004010. https://doi.org/10.1101/cshperspect.a004010
  48. Tu H, Tang TS, Wang Z, Bezprozvanny I (2004) Association of type 1 inositol 1,4,5-trisphosphate receptor with AKAP9 (Yotiao) and protein kinase A. J Biol Chem 279:19375-19382. https://doi.org/10.1074/jbc.M313476200
  49. Ullah G, Jung P, Machaca K (2007) Modeling $Ca^{2+}$ signaling differentiation during oocyte maturation. Cell Calcium 42:556-564. https://doi.org/10.1016/j.ceca.2007.01.010
  50. Vanderheyden V, Wakai T, Bultynck G, De Smedt H, Parys JB, Fissore RA (2009) Regulation of inositol 1,4,5-trisphosphate receptor type 1 function during oocyte maturation by MPM-2 phosphorylation. Cell Calcium 46:56-64. https://doi.org/10.1016/j.ceca.2009.04.004
  51. Vermassen E, Van Acker K, Annaert WG, Himpens B, Callewaert G, Missiaen L, De Smedt H, Parys JB (2003) Microtubule-dependent redistribution of the type-1 inositol 1,4,5-trisphosphate receptor in A7r5 smooth muscle cells. J Cell Sci 116:1269-1277. https://doi.org/10.1242/jcs.00354
  52. Wagner LE, Joseph SK, Yule DI (2008) Regulation of single inositol 1,4,5-trisphosphate receptor channel activity by protein kinase A phosphorylation. J Physiol 586:3577-3596. https://doi.org/10.1113/jphysiol.2008.152314
  53. Wakai T, Vanderheyden V, Yoon SY, Cheon B, Zhang N, Parys JB, Fissore RA (2012) Regulation of inositol 1,4,5-trisphosphate receptor function during mouse oocyte maturation. J Cell Physiol 227:705-717. https://doi.org/10.1002/jcp.22778
  54. Worley PF, Baraban JM, Colvin JS, Snyder SH (1987) Inositol trisphosphate receptor localization in brain: Variable stoichiometry with protein kinase C. Nature 325:159-161. https://doi.org/10.1038/325159a0
  55. Xu Z, Williams CJ, Kopf GS, Schultz RM (2003) Maturation-associated increase in IP3 receptor type 1: Role in conferring increased IP3 sensitivity and $Ca^{2+}$ oscillatory behavior in mouse eggs. Dev Biol 254:163-171. https://doi.org/10.1016/S0012-1606(02)00049-0
  56. Yoon SY, Kang DW (2011) Production of intracellular calcium oscillation by phospholipase C zeta activation in mammalian eggs. Dev Reprod 15:197-204.
  57. Zhang N, Yoon SY, Parys JB, Fissore RA (2015) Effect of M-phase kinase phosphorylations on type 1 inositol 1,4,5-trisphosphate receptor-mediated $Ca^{2+}$ responses in mouse eggs. Cell Calcium 58:476-488. https://doi.org/10.1016/j.ceca.2015.07.004
  58. Zima AV, Bare DJ, Mignery GA, Blatter LA (2007) IP3-dependent nuclear $Ca^{2+}$ signalling in the mammalian heart. J Physiol 584:601-611. https://doi.org/10.1113/jphysiol.2007.140731