Regulation of fertilization-initiated [Ca2+]i oscillations in mammalian eggs: A multi-pronged approach

Seminars in Cell and Developmental Biology

Volumn 17, Issue 2, 2006, Pages 274-284

  Lee, Bora ^a   Yoon, Sook Young ^a   Fissore, Rafael A ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

Calcium; Cell cycle; Fertilization; Inositol 1,4,5 trisphosphate receptor type 1 (IP3R 1); Phospholipase (PLC )

Indexed keywords

INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; PHOSPHOLIPASE C; PHOSPHOLIPASE C ZETA; PROTEIN; RECEPTOR SUBTYPE; SPERM FACTOR; UNCLASSIFIED DRUG;

CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL CYCLE M PHASE; CELLULAR DISTRIBUTION; EGG; ENZYME ACTIVITY; FERTILIZATION; HUMAN; MAMMAL; NONHUMAN; OOCYTE MATURATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVIEW; ZYGOTE;

MAMMALIA;

EID: 33745876224     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcdb.2006.02.011     Document Type: Review

References (124)

1. Berridge M.J., Lipp P., and Bootman M.D. The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1 (2000) 11-21
2. Berridge M.J., Bootman M.D., and Roderick H.L. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4 (2003) 517-529
3. Patterson R.L., Boehning D., and Snyder S.H. Inositol 1,4,5-trisphosphate receptors as signal integrators. Annu Rev Biochem 73 (2004) 437-465
4. 2+ oscillations at fertilization of mammalian eggs. Dev Biol 158 (1993) 62-78
5. Stricker S.A. Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev Biol 211 (1999) 157-176
6. Whitaker M. Calcium at fertilization and in early development. Physiol Rev 86 (2006) 25-88
7. Schultz R.M., and Kopf G.S. Molecular basis of mammalian egg activation. Curr Topics Dev Biol 30 (1995) 21-62
8. 2+ oscillation number. Dev Biol 250 (2002) 280-291
9. 2+ oscillations and egg activation in mammals is a novel phospholipase C: PLC zeta. Reproduction 127 (2004) 431-439
10. Kline D., and Kline J.T. Thapsigargin activates a calcium influx pathway in the unfertilized mouse egg and suppresses repetitive calcium transients in the fertilized egg. J Biol Chem 267 (1992) 17624-17630
11. Miyazaki S. Inositol 1,4,5-trisphosphate-induced calcium release and guanine nucleotide-binding protein-mediated periodic calcium rises in golden hamster eggs. J Cell Biol 106 (1988) 345-353
12. 2+ oscillation by antibody to the inositol 1,4,5-trisphosphate receptor in fertilized hamster eggs. Science 257 (1992) 251-255
13. Fissore R.A., Longo F.J., Anderson E., Parys J.B., and Ducibella T. Differential distribution of inositol trisphosphate receptor isoforms in mouse oocytes. Biol Reprod 60 (1999) 49-57
14. Jellerette T., He C.L., Wu H., Parys J.B., and Fissore R.A. Down-regulation of the inositol 1,4,5-trisphosphate receptor in mouse eggs following fertilization or parthenogenetic activation. Dev Biol 223 (2000) 238-250
15. Parrington J., Brind S., De Smedt H., Gangeswaran R., Lai F.A., Wojcikiewicz R., et al. Expression of inositol 1,4,5-trisphosphate receptors in mouse oocytes and early embryos: the type I isoform is upregulated in oocytes and downregulated after fertilization. Dev Biol 203 (1998) 451-461
16. 2+ oscillations in fertilized mouse eggs. Dev Biol 218 (2000) 299-313
17. Kurokawa M., and Fissore R.A. ICSI-generated mouse zygotes exhibit altered calcium oscillations, inositol 1,4,5-trisphosphate receptor-1 down-regulation, and embryo development. Mol Hum Reprod 9 (2003) 523-533
18. 2+ elevations in rabbit eggs. Dev Biol 159 (1993) 122-130
19. 2+ responses during fertilization of bovine eggs. J Reprod Dev 41 (1995) 77-84
20. 2+ transients in mouse oocytes are cell cycle dependent. Development 121 (1995) 3259-3266
21. 2+ spiking in the mouse zygote. Cell Calcium 28 (2000) 47-54
22. 2+ oscillations at fertilization in mammals are regulated by the formation of pronuclei. Development 130 (2003) 1461-1472
23. Igusa Y., and Miyazaki S. Periodic increase of cytoplasmic free calcium in fertilized hamster eggs measured with calcium-sensitive electrodes. J Physiol 377 (1986) 193-205
24. 2+ concentrations in fertilized bovine eggs. Biol Reprod 47 (1992) 960-969
25. Taylor C.T., Lawrence Y.M., Kingsland C.R., Biljan M.M., and Cuthbertson K.S. Oscillations in intracellular free calcium induced by spermatozoa in human oocytes at fertilization. Hum Reprod 8 (1993) 2174-2179
26. cyt signal in the mouse. Dev Biol 282 (2005) 39-54
27. 2+ signal regime on development. Development 128 (2001) 917-928
28. Stith B.J., Goalstone M., Silva S., and Jaynes C. Inositol 1,4,5-trisphosphate mass changes from fertilization through first cleavage in Xenopus laevis. Mol Biol Cell 4 (1993) 435-443
29. Turner P.R., Sheetz M.P., and Jaffe L.A. Fertilization increases the polyphosphoinositide content of sea urchin eggs. Nature 310 (1984) 414-415
30. 2+ spiking. Biochem J 316 (1996) 583-591
31. Rebecchi M.J., and Pentyala S.N. Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol Rev 80 (2000) 1291-1335
32. Rhee S.G. Regulation of phosphoinositide-specific phospholipase C. Annu Rev Biochem 70 (2001) 281-312
33. Williams C.J., Schultz R.M., and Kopf G.S. Role of G proteins in mouse egg activation: stimulatory effects of acetylcholine on the ZP2 to ZP2f conversion and pronuclear formation in eggs expressing a functional m1 muscarinic receptor. Dev Biol 151 (1992) 288-296
34. Williams C.J., Mehlmann L.M., Jaffe L.A., Kopf G.S., and Schultz R.M. Evidence that Gq family G proteins do not function in mouse egg activation at fertilization. Dev Biol 198 (1998) 116-127
35. 2+ release at fertilization of mouse eggs. Dev Biol 203 (1998) 221-232
36. 2+ release at fertilization in mouse eggs. Dev Biol 236 (2001) 492-501
37. i oscillations in mouse eggs. Reproduction 127 (2004) 441-454
38. McDougall A., and Levasseur M. Sperm-triggered calcium oscillations during meiosis in ascidian oocytes first pause, restart, then stop: correlations with cell cycle kinase activity. Development 125 (1998) 4451-4459
39. 2+ release by the same pathway as fertilization. Development 127 (2000) 3227-3236
40. Sato K., Tokmakov A.A., and Fukami Y. Fertilization signalling and protein-tyrosine kinases. Comp Biochem Physiol B Biochem Mol Biol 126 (2000) 129-148
41. Swann K. A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs. Development 110 (1990) 1295-1302
42. Wu H., He C.L., and Fissore R.A. Injection of a porcine sperm factor triggers calcium oscillations in mouse oocytes and bovine eggs. Mol Reprod Dev 46 (1997) 176-189
43. Nakano Y., Shirakawa H., Mitsuhashi N., Kuwabara Y., and Miyazaki S. Spatiotemporal dynamics of intracellular calcium in the mouse egg injected with a spermatozoon. Mol Hum Reprod 3 (1997) 1087-1093
44. 2+ and fluorescent markers between the sperm and egg after fusion in the mouse. Development 125 (1998) 4627-4635
45. 2+ release in sea urchin egg homogenates. FEBS Lett 437 (1998) 297-300
46. 2 associated with intracellular organelles. Dev Biol 228 (2000) 125-135
47. 2+ ion concentrations. Biochem J 327 (1997) 545-552
48. 2+ oscillations in eggs and embryo development. Development 129 (2002) 3533-3544
49. 2+ oscillation-inducing phospholipase C zeta expressed in mouse eggs is accumulated to the pronucleus during egg activation. Dev Biol 268 (2004) 245-257
50. 2+ oscillations in mouse embryos are regulated by nuclear targeting of PLC zeta. J Cell Sci 117 (2004) 2513-2521
51. Kono T., Carroll J., Swann K., and Whittingham D.G. Nuclei from fertilized mouse embryos have calcium-releasing activity. Development 121 (1995) 1123-1128
52. 2+ release in activated and aging mouse oocytes. Dev Biol 178 (1996) 229-237
53. i oscillations in mouse zygotes and function of the inositol 1,4,5-trisphosphate receptor-1. Dev Biol 274 (2004) 94-109
54. 2+ release in early and late events of mouse egg activation. Development 120 (1994) 1851-1859
55. Mehlmann L.M., and Kline D. 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 (1994) 1088-1098
56. 2+ release increase during meiotic maturation of mouse oocytes. J Biol Chem 270 (1995) 6671-6677
57. 2+ release in mouse oocytes and embryos. Mol Biol Cell 14 (2003) 288-301
58. Patel S., Joseph S.K., and Thomas A.P. Molecular properties of inositol 1,4,5-trisphosphate receptors. Cell Calcium 25 (1999) 247-264
59. 2+ signals by differential expression of IP3 receptor subtypes. EMBO J 18 (1999) 1303-1308
60. 3 receptor. EMBO J 10 (1991) 3199-3206
61. Uchida K., Miyauchi H., Furuichi T., Michikawa T., and Mikoshiba K. Critical regions for activation gating of the inositol 1,45-trisphosphate receptor. J Biol Chem 278 (2003) 16551-16560
62. Bosanac I., Alattia J.R., Mal T.K., Chan J., Talarico S., Tong F.K., et al. Structure of the inositol 1,4,5-trisphosphate receptor binding core in complex with its ligand. Nature 420 (2002) 696-700
63. 2+-release channel function. Biochem J 337 (1999) 345-361
64. Sayers L.G., Miyawaki A., Muto A., Takeshita H., Yamamoto A., Michikawa T., et al. Intracellular targeting and homotetramer formation of a truncated inositol 1,4,5-trisphosphate receptor-green fluorescent protein chimera in Xenopus laevis oocytes: evidence for the involvement of the transmembrane spanning domain in endoplasmic reticulum targeting and homotetramer complex formation. Biochem J 323 (1997) 273-280
65. Ramos-Franco J., Galvan D., Mignery G.A., and Fill M. Location of the permeation pathway in the recombinant type 1 inositol 1,4,5-trisphosphate receptor. J Gen Physiol 114 (1999) 243-250
66. 2+ entry, and proliferation of A7r5 vascular smooth muscle cells. Circ Res 88 (2001) 202-209
67. Zhu C.C., Furuichi T., Mikoshiba K., and Wojcikiewicz R.J. Inositol 1,4,5-trisphosphate receptor down-regulation is activated directly by inositol 1,4,5-trisphosphate binding. Studies with binding-defective mutant receptors. J Biol Chem 274 (1999) 3476-3484
68. Wojcikiewicz R.J., Furuichi T., Nakade S., Mikoshiba K., and Nahorski S.R. Muscarinic receptor activation down-regulates the type I inositol 1,4,5-trisphosphate receptor by accelerating its degradation. J Biol Chem 269 (1994) 7963-7969
69. 2+. J Biol Chem 278 (2003) 38238-38246
70. Wojcikiewicz R.J., Xu Q., Webster J.M., Alzayady K., and Gao C. Ubiquitination and proteasomal degradation of endogenous and exogenous inositol 1,4,5-trisphosphate receptors in alpha T3-1 anterior pituitary cells. J Biol Chem 278 (2003) 940-947
71. Wojcikiewicz R.J. Regulated ubiquitination of proteins in GPCR-initiated signaling pathways. Trends Pharmacol Sci 25 (2004) 35-41
72. 2+ or egg activation. Dev Biol 223 (2000) 251-265
73. 3)-induced calcium release in type-1 inositol 1,4,5-trisphosphate receptor down-regulated bovine eggs. Biol Reprod 73 (2005) 2-13
74. 2+ oscillatory behavior in mouse eggs. Dev Biol 254 (2003) 163-171
75. Malathi K., Kohyama S., Ho M., Soghoian D., Li X., Silane M., et al. Inositol 1,4,5-trisphosphate receptor (type 1) phosphorylation and modulation by Cdc2. J Cell Biochem 90 (2003) 1186-1196
76. Winston N., McGuinness O., Johnson M.H., and Maro B. The exit of mouse oocytes from meiotic M-phase requires an intact spindle during intracellular calcium release. J Cell Sci 108 (1995) 143-151
77. 2+ signalling and cortical re-organisation during the transition from meiosis to mitosis in mammalian oocytes. Eur J Obstet Gynecol Reprod Biol 115 (2004) S61-S67
78. Krizanova O., and Ondrias K. The inositol 1,4,5-trisphosphate receptor-transcriptional regulation and modulation by phosphorylation. Gen Physiol Biophys 22 (2003) 295-311
79. Tang T.S., Tu H., Wang Z., and Bezprozvanny I. Modulation of type 1 inositol (1,4,5)-trisphosphate receptor function by protein kinase a and protein phosphatase 1alpha. J Neurosci 23 (2003) 403-415
80. DeSouza N., Reiken S., Ondrias K., Yang Y.M., Matkovich S., and Marks A.R. Protein kinase A and two phosphatases are components of the inositol 1,4,5-trisphosphate receptor macromolecular signaling complex. J Biol Chem 277 (2002) 39397-39400
81. 2+ oscillations at fertilization in mouse eggs. J Cell Biol 164 (2004) 1033-1044
82. Markoulaki S., Matson S., Abbott A.L., and Ducibella T. Oscillatory CaMKII activity in mouse egg activation. Dev Biol 258 (2003) 464-474
83. Swann K., Igusa Y., and Miyazaki S. Evidence for an inhibitory effect of protein kinase C on G-protein-mediated repetitive calcium transients in hamster eggs. EMBO J 8 (1989) 3711-3718
84. Carroll J., and Swann K. Spontaneous cytosolic calcium oscillations driven by inositol trisphosphate occur during in vitro maturation of mouse oocytes. J Biol Chem 267 (1992) 11196-11201
85. Fujiwara T., Nakada K., Shirakawa H., and Miyazaki S. Development of inositol trisphosphate-induced calcium release mechanism during maturation of hamster oocytes. Dev Biol 156 (1993) 69-79
86. 2+/calmodulin-dependent protein kinase II antagonism. J Biol Chem 277 (2002) 35061-35070
87. 2+ transients in mouse embryos during the first mitotic division. J Cell Biol 132 (1996) 915-923
88. Tokmakov A.A., Sato K.I., and Fukami Y. Calcium oscillations in Xenopus egg cycling extracts. J Cell Biochem 82 (2001) 89-97
89. Russo G.L., Tosto M., Mupo A., Castellano I., Cuomo A., and Tosti E. Biochemical and functional characterization of protein kinase CK2 in ascidian Ciona intestinalis oocytes at fertilization. Cloning and sequence analysis of cDNA for alpha and beta subunits. J Biol Chem 279 (2004) 33012-33023
90. 2+ signals in pancreatic acinar cells. J Cell Sci 118 (2005) 971-980
91. Kline D., Mehlmann L., Fox C., and Terasaki M. The cortical endoplasmic reticulum (ER) of the mouse egg: localization of ER clusters in relation to the generation of repetitive calcium waves. Dev Biol 215 (1999) 431-442
92. Vermassen E., Van Acker K., Annaert W.G., Himpens B., Callewaert G., Missiaen L., et al. Microtubule-dependent redistribution of the type-1 inositol 1,4,5-trisphosphate receptor in A7r5 smooth muscle cells. J Cell Sci 116 (2003) 1269-1277
93. Vermassen E., Parys J.B., and Mauger J.P. Subcellular distribution of the inositol 1,4,5-trisphosphate receptors: functional relevance and molecular determinants. Biol Cell 96 (2004) 3-17
94. Wilson B.S., Pfeiffer J.R., Smith A.J., Oliver J.M., Oberdorf J.A., and Wojcikiewicz R.J. Calcium-dependent clustering of inositol 1,4,5-trisphosphate receptors. Mol Biol Cell 9 (1998) 1465-1478
95. Tateishi Y., Hattori M., Nakayama T., Iwai M., Bannai H., Nakamura T., et al. Cluster formation of inositol 1,4,5-trisphosphate receptor requires its transition to open state. J Biol Chem 280 (2005) 6816-6822
96. 2+ release during maturation of hamster oocytes. Dev Biol 170 (1995) 594-606
97. Kume S., Muto A., Okano H., and Mikoshiba K. Developmental expression of the inositol 1,4,5-trisphosphate receptor and localization of inositol 1,4,5-trisphosphate during early embryogenesis in Xenopus laevis. Mech Dev 66 (1997) 157-168
98. Mehlmann L.M., Mikoshiba K., and Kline D. Redistribution and increase in cortical inositol 1,4,5-trisphosphate receptors after meiotic maturation of the mouse oocyte. Dev Biol 180 (1996) 489-498
99. 2+ release events during oocyte maturation. Dev Biol 275 (2004) 170-182
100. 3 receptor activity is differentially regulated in endoplasmic reticulum subdomains during oocyte maturation. Curr Biol 15 (2005) 765-770
101. Terasaki M., Runft L.L., and Hand A.R. Changes in organization of the endoplasmic reticulum during Xenopus oocyte maturation and activation. Mol Biol Cell 12 (2001) 1103-1116
102. 3 receptor: structure, function, and localization in oocytes and eggs. Cell 73 (1993) 555-570
103. 2+ signaling in maturing and fertilized oocytes of marine protostome worms: the roles of MAPKs and MPF. Development 130 (2003) 2867-2879
104. Pieper A.A., Brat D.J., O'Hearn E., Krug D.K., Kaplin A.I., Takahashi K., et al. Differential neuronal localizations and dynamics of phosphorylated and unphosphorylated type 1 inositol 1,4,5-trisphosphate receptors. Neuroscience 102 (2001) 433-444
105. Miyakawa-Naito A., Uhlen P., Lal M., Aizman O., Mikoshiba K., Brismar H., et al. Cell signaling microdomain with Na,K-ATPase and inositol 1,4,5-trisphosphate receptor generates calcium oscillations. J Biol Chem 278 (2003) 50355-50361
106. 2+ stores with inositol 1,4,5-trisphosphate receptor to the cleavage furrow in a microtubule-dependent manner. Int J Dev Biol 45 (2001) 861-868
107. Fukatsu K., Bannai H., Zhang S., Nakamura H., Inoue T., and Mikoshiba K. Lateral diffusion of inositol 1,4,5-trisphosphate receptor type 1 is regulated by actin filaments and 4.1 N in neuronal dendrites. J Biol Chem 279 (2004) 48976-48982
108. Wang Y., Mattson M.P., and Furukawa K. Endoplasmic reticulum calcium release is modulated by actin polymerization. J Neurochem 82 (2002) 945-952
109. Sugiyama T., Matsuda Y., and Mikoshiba K. Inositol 1,4,5-trisphosphate receptor associated with focal contact cytoskeletal proteins. FEBS Lett 466 (2000) 29-34
110. Joseph S.K., and Samanta S. Detergent solubility of the inositol trisphosphate receptor in rat brain membranes. Evidence for association of the receptor with ankyrin. J Biol Chem 268 (1993) 6477-6486
111. Wollert T., Weiss D.G., Gerdes H.H., and Kuznetsov S.A. Activation of myosin V-based motility and F-actin-dependent network formation of endoplasmic reticulum during mitosis. J Cell Biol 159 (2002) 571-577
112. 3 signaling in C. elegans. Curr Biol 12 (2002) 951-956
113. Vincent C., Cheek T., and Johnson M. Cell cycle progression of parthenogenetically activated mouse oocytes to interphase is dependent on the level of internal calcium. J Cell Sci 103 (1992) 389-396
114. 2+ oscillations induced by a cytosolic sperm protein factor are mediated by a maternal machinery that functions only once in mammalian eggs. Development 127 (2000) 1141-1150
115. Higo T., Hattori M., Nakamura T., Natsume T., Michikawa T., and Mikoshiba K. Subtype-specific and ER lumenal environment-dependent regulation of inositol 1,4,5-trisphosphate receptor type 1 by ERp44. Cell 120 (2005) 85-98
116. 2+ oscillations in mouse eggs injected with sperm extract. Cell Calcium 29 (2001) 311-325
117. Cheek T.R., McGuinness O.M., Vincent C., Moreton R.B., Berridge M.J., and Johnson M.H. Fertilisation and thimerosal stimulate similar calcium spiking patterns in mouse oocytes but by separate mechanisms. Development 119 (1993) 179-189
118. Putney Jr. J.W., Broad L.M., Braun F.J., Lievremont J.P., and Bird G.S. Mechanisms of capacitative calcium entry. J Cell Sci 114 (2001) 2223-2229
119. McGuinness O.M., Moreton R.B., Johnson M.H., and Berridge M.J. A direct measurement of increased divalent cation influx in fertilised mouse oocytes. Development 122 (1996) 2199-2206
120. Montell C., Birnbaumer L., and Flockerzi V. The TRP channels, a remarkably functional family. Cell 108 (2002) 595-598
121. Machaty Z., Ramsoondar J.J., Bonk A.J., Bondioli K.R., and Prather R.S. Capacitative calcium entry mechanism in porcine oocytes. Biol Reprod 66 (2002) 667-674
122. Spassova M.A., Soboloff J., He L.P., Hewavitharana T., Xu W., Venkatachalam K., et al. Calcium entry mediated by SOCs and TRP channels: variations and enigma. Biochem Biophys Acta 1742 (2004) 9-20
123. 2+ entry. J Cell Biol 156 (2002) 75-85
124. 2+ current. J Biol Chem 278 (2003) 33730-33737