Egg activation in physiological polyspermy

Reproduction

Volumn 144, Issue 1, 2012, Pages 11-22

  Iwao, Yasuhiro ^a  

^a YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CITRATE SYNTHASE; SPERM SPECIFIC CITRATE SYNTHASE; UNCLASSIFIED DRUG;

AMPHIBIA; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL ACTIVATION; EMBRYO CELL; ENZYME ACTIVITY; FERTILIZATION; MITOCHONDRION; NONHUMAN; POLYSPERMY; PRIORITY JOURNAL; REPRODUCTION; REVIEW; ZYGOTE;

ANIMALS; CALCIUM; CELL NUCLEUS; CITRATE (SI)-SYNTHASE; FERTILIZATION; MITOCHONDRIA; OVUM; SALAMANDRIDAE; ZYGOTE;

AMPHIBIA; ANIMALIA; SALAMANDRIDAE; VERTEBRATA;

EID: 84863216187     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-12-0104     Document Type: Review

References (103)

1. Aarabi M, Qin Z, Xu W, Mewburn J & Oko R 2010 Sperm-borne protein, PAWP, initiates zygotic development in Xenopus laevis by eliciting intracellular calcium release. Molecular Reproduction and Development 77 249-256.
2. Aimar C & Labrousse J-P 1975 DNA synthesis and evolution, in presence of a somatic nucleus, of the female pronucleus after experimental activation of the egg of Pleurodeles waltlii. Development, Growth & Differentiation 17 197-207. (doi:10.1111/j.1440-169X.1975.00197.x)
3. Bonilla F, Ajmat MT, Sanchez Toranzo G, Zelarayan L, Oterino J & Buhler MI 2008 Activation of amphibian oocytes by sperm extracts. Zygote 16 303-308. (doi:10.1017/S0967199408004814)
4. Breed WG & Leigh CM 1990 Morphological changes in the oocyte and its surrounding vestments during in vivo fertilization in the dasyurid marsupial Sminthopsis crassicaudata. Journal of Morphology 204 177-196. (doi:10.1002/jmor.1052040207)
5. Carré D & Sardet C 1984 Fertilization and early development in Beroe ovata. Developmental Biology 105 188-195. (doi:10.1016/0012-1606 (84)90274-4)
6. Charbonneau M & Picheral B 1983 Early events in anuran amphibian fertilization: an ultrastructural study of changes occurring in the course of monospermic fertilization and artificial activation. Development, Growth & Differentiation 25 23-37. (doi:10.1111/j.1440-169X.1983.00023.x)
7. Charbonneau M, Moreau M, Picheral B, Vilain JP & Guerrier P 1983 Fertilization of amphibian eggs: a comparison of electrical responses between anurans and urodeles. Developmental Biology 98 304-318. (doi:10.1016/0012- 1606(83)90361-5)
8. Coward K, Campos-Mendoza A, Larman M, Hibbitt O, McAndrew B, Bromage N & Parrington J 2003 Teleost fish spermatozoa contain a cytosolic protein factor that induces calcium release in sea urchin egg homogenates and triggers calcium oscillations when injected into mouse oocytes. Biochemical and Biophysical Research Communications 305 299-304. (doi:10.1016/S0006-291X(03) 00753-8)
9. Coward K, Ponting CP, Chang HY, Hibbitt O, Savolainen P, Jones KT & Parrington J 2005 Phospholipase Cz, the trigger of egg activation in mammals, is present in a non-mammalian species. Reproduction 130 157-163. (doi:10.1530/rep.1.00707)
10. Coward K, Ponting CP, Zhang N, Young C, Huang CJ, Chou CM, Kashir J, Fissore RA & Parrington J 2011 Identification and functional analysis of an ovarian form of the egg activation factor phospholipase Cζ (PLCζ) in pufferfish. Molecular Reproduction and Development 78 48-56. (doi:10.1002/mrd.21262)
11. Cross NL & Elinson RP 1980 A fast block to polyspermy in frogs mediated by changes in the membrane potential. Developmental Biology 75 187-198. (doi:10.1016/0012-1606(80)90154-2)
12. Dong JB, Tang TS & Sun FZ 2000 Xenopus and chicken sperm contain a cytosolic soluble protein factor which can trigger calcium oscillations in mouse eggs. Biochemical and Biophysical Research Communications 268 947-951. (doi:10.1006/bbrc.2000.2218)
13. 2+ oscillation number. Developmental Biology 250 280-291. (doi:10.1006/dbio.2002.0788)
14. Dumollard R, Carroll J, Dupont G & Sardet C 2002 Calcium wave pacemakers in eggs. Journal of Cell Science 115 3557-3564. (doi:10.1242/jcs. 00056)
15. Elinson RP 1986 Fertilization in amphibians: the ancestry of the block to polyspermy. International Review of Cytology 101 59-100. (Pubitemid 16118439)
16. Fankhauser G 1948 The organization of the amphibian egg during fertilization and cleavage. Annals of the New York Academy of Sciences 49 684-708. (doi:10.1111/j.1749-6632.1948.tb30961.x)
17. Feller AE & Hedges SB 1998 Molecular evidence for the early history of living amphibians. Molecular Phylogenetics and Evolution 9 509-516. (doi:10.1006/mpev.1998.0500)
18. Fontanilla RA & Nuccitelli R 1998 Characterization of the sperm-induced calcium wave in Xenopus eggs using confocal microscopy. Biophysical Journal 75 2079-2087. (doi:10.1016/S0006-3495(98)77650-7)
19. Gardner AJ, Williams CJ & Evans JP 2007 Establishment of the mammalian membrane block to polyspermy: evidence for calcium-dependent and -independent regulation. Reproduction 133 383-393. (doi:10.1530/REP-06-0304)
20. Gatenby JB & Hill JP 1924 On an ovum of Ornithorhynchus exhibiting polar bodies and polyspermy. Journal of Cell Science s2-68 229-238.
21. Gianaroli L, Tosti E, Magli C, Iaccarino M, Ferraretti AP & Dale B 1994 Fertilization current in the human oocyte. Molecular Reproduction and Development 38 209-214. (doi:10.1002/mrd.1080380212)
22. Gilkey JC, Jaffe LF, Ridgway EB & Reynolds GT 1978 A free calcium wave traverses the activating egg of themedaka, Oryzias latipes. Journal of Cell Biology 76 448-466. (doi:10.1083/jcb.76.2.448)
23. Goudeau M & Goudeau H 1993 Successive electrical responses to insemination and concurrent sperm entries in the polyspermic egg of the ctenophore Beroe ovata. Developmental Biology 156 537-551. (doi:10.1006/dbio. 1993.1100)
24. 2+ changes during physiological polyspermy in amphibian eggs. Development 114 617-624.
25. Harada Y, Matsumoto T, Hirahara S, Nakashima A, Ueno S, Oda S, Miyazaki S & Iwao Y 2007 Characterization of a sperm factor for egg activation at fertilization of the newt Cynops pyrrhogaster. Developmental Biology 306 797-808. (doi:10.1016/j.ydbio.2007.04.019)
26. 2+ increase by the sperm factor in physiologically polyspermic newt fertilization: its signaling mechanism in egg cytoplasm and the species-specificity. Developmental Biology 351 266-276. (doi:10.1016/j.ydbio.2011.01.003)
27. Harper EH 1904 The fertilization and early development of the pigeon's egg. American Journal of Anatomy 3 349-386. (doi:10.1002/aja.1000030402)
28. Hart NH 1990 Fertilization in teleost fishes: mechanisms of sperm-egg interactions. International Review of Cytology 121 1-66. (Pubitemid 20195569)
29. Hedrick JL 2008 Anuran and pig egg zona pellucida glycoproteins in fertilization and early development. International Journal of Developmental Biology 52 683-701. (doi:10.1387/ijdb.082580jh)
30. Houliston E, Carre D, Johnston JA & Sardet C 1993 Axis establishment and microtubule-mediated waves prior to first cleavage in Beroe ovata. Development 117 75-87. (Pubitemid 23094158)
31. Hughes RL & Hall LS 1998 Early development and embryology of the platypus. Philosophical Transactions of the Royal Society of London. Series B, Biological sciences 353 1101-1114. (doi:10.1098/rstb.1998.0269)
32. Iwamatsu T 2000 Fertilization in fishes. In Fertilization in Protozoa and Metazoan Animal, pp 89-146. Eds JJ Tarín& A Cano. Berlin: Springer.
33. Iwamatsu T & Ohta I 1974 Cleavage initiating activities of sperm fractions injected into the egg of the medaka, Oryzias latipes. Journal of Experimental Zoology 187 3-15. (doi:10.1002/jez.1401870103)
34. Iwao Y 1985 The membrane potential changes of amphibian eggs during species- and cross-fertilization. Developmental Biology 111 26-34. (doi:10.1016/0012-1606(85)90431-2)
35. Iwao Y 1989 An electrically mediated block to polyspermy in the primitive urodele Hynobius nebulosus and phylogenetic comparison with other amphibians. Developmental Biology 134 438-445. (doi:10.1016/0012-1606(89)90116-4)
36. Iwao Y 2000a Fertilization in amphibians. In Fertilization in Protozoa and Metazoan Animal, pp 147-191. Eds JJ Tarín& A Cano. Berlin: Springer.
37. Iwao Y 2000b Mechanisms of egg activation and polyspermy block in amphibians and comparative aspects with fertilization in other vertebrates. Zoological Science 17 699-709. (doi:10.2108/zsj.17.699)
38. Iwao Y & Jaffe LA 1989 Evidence that the voltage-dependent component in the fertilization process is contributed by the sperm. Developmental Biology 134 446-451. (doi:10.1016/0012-1606(89)90117-6)
39. Iwao Y & Elinson RP 1990 Control of sperm nuclear behavior in physiologically polyspermic newt eggs: possible involvement of MPF. Developmental Biology 142 301-312. (doi:10.1016/0012-1606(90)90351-I)
40. 2O. Development, Growth & Differentiation 37 641-651. (doi:10.1046/j.1440-169X. 1995.t01-5-00003.x)
41. 2+ release. Developmental Biology 177 558-567. (doi:10.1006/dbio.1996.0185)
42. Iwao Y, Yamasaki H & Katagiri C 1985 Experiments pertaining to the suppression of accessory sperm in fertilized newt eggs. Development, Growth & Differentiation 27 323-331. (doi:10.1111/j.1440-169X.1985.00323.x)
43. Iwao Y, Sakamoto N, Takahara K, Yamashita M & Nagahama Y 1993 The egg nucleus regulates the behavior of sperm nuclei as well as cycling of MPF in physiologically polyspermic newt eggs. Developmental Biology 160 15-27. (doi:10.1006/dbio.1993.1282)
44. Iwao Y, Miki A, Kobayashi M & Onitake K 1994 Activation of Xenopus eggs by an extract of Cynops sperm. Development, Growth & Differentiation 36 469-479. (doi:10.1111/j.1440-169X.1994.00469.x)
45. Iwao Y, Yasumitsu K, Narihira M, Jiang J & Nagahama Y 1997 Changes in microtubule structures during the first cell cycle of physiologically polyspermic newt eggs. Molecular Reproduction and Development 47 210-221. (doi:10.1002/(SICI)1098-2795(199706)47:2 〈210::AID-MRD13〉 3.0.CO;2-3)
46. Iwao Y, Murakawa T, Yamaguchi J & Yamashita M 2002 Localization of γ-tubulin and cyclin B during early cleavage in physiologically polyspermic newt eggs. Development, Growth & Differentiation 44 489-499. (doi:10.1046/j.1440-169X.2002.00661.x)
47. Jaffe LA, Sharp AP & Wolf DP 1983 Absence of an electrical polyspermy block in the mouse. Developmental Biology 96 317-323. (doi:10.1016/0012- 1606(83)90168-9)
48. Kim ST & Gye MC 2003 Activation of mouse oocytes following intracytoplasmic injection of chicken sperm extract. Reproduction in Domestic Animals 38 401-404. (doi:10.1046/j.1439-0531.2003.00455.x)
49. Kline D & Nuccitelli R 1985 The wave of activation current in the Xenopus egg. Developmental Biology 111 471-487. (doi:10.1016/0012-1606 (85)90499-3)
50. Kline D & Stewart-Savage J 1994 The timing of cortical granule fusion, content dispersal, and endocytosis during fertilization of the hamster egg: an electrophysiological and histochemical study. Developmental Biology 162 277-287. (doi:10.1006/dbio.1994.1085)
51. Kobayashi W, Baba Y, Shimozawa T & Yamamoto TS 1994 The fertilization potential provides a fast block to polyspermy in lamprey eggs. Developmental Biology 161 552-562. (doi:10.1006/dbio.1994.1053)
52. Kojima H & Numata O 2002 Enzymatic form and cytoskeletal form of bifunctional Tetrahymena 49 kDa protein is regulated by phosphorylation. Zoological Science 19 37-42. (doi:10.2108/zsj.19.37)
53. 2+ oscillations in mouse eggs. Journal of Biological Chemistry 279 10408-10412. (doi:10.1074/jbc.M313801200)
54. Kubo H, Shiga K, Harada Y & Iwao Y 2010 Analysis of a sperm surface molecule that binds to a vitelline envelope component of Xenopus laevis eggs. Molecular Reproduction and Development 77 728-735. (doi:10.1002/mrd.21211)
55. 2+ movement. FEBS Letters 331 35-37. (doi:10.1016/0014-5793(93)80292-3)
56. Mahbub Hasan AK, Sato K, Sakakibara K, Ou Z, Iwasaki T, Ueda Y &Fukami Y 2005 Uroplakin III, a novel Src substrate in Xenopus egg rafts, is a target for sperm protease essential for fertilization. Developmental Biology 286 483-492. (doi:10.1016/j.ydbio.2005.08.020)
57. Mahbub Hasan AK, Ou Z, Sakakibara K, Hirahara S, Iwasaki T, Sato K & Fukami Y 2007 Characterization of Xenopus egg membrane microdomains containing uroplakin Ib/III complex: roles of their molecular interactions for subcellular localization and signal transduction. Genes to Cells 12 251-267. (doi:10.1111/j.1365-2443.2007.01048.x)
58. Missiaen L, Parys JB, Smedt HD, Sienaert I, Sipma H, Vanlingen S, Maes K & Casteels R 1997 Effect of adenine nucleotides on myo-inositol-1,4, 5-trisphosphate-induced calcium release. Biochemical Journal 325 (Pt 3) 661-666. (Pubitemid 27367755)
59. Mizote A, Okamoto S & Iwao Y 1999 Activation of Xenopus eggs by proteases: possible involvement of a sperm protease in fertilization. Developmental Biology 208 79-92. (doi:10.1006/dbio.1999.9195)
60. Mizushima S, Takagi S, Ono T, Atsumi Y, Tsukada A, Saito N & Shimada K 2007 Possible role of calcium on oocyte development after intracytoplasmic sperm injection in quail (Coturnix japonica). Journal of Experimental Zoology. Part A, Ecological Genetics and Physiology 307 647-653. (doi:10.1002/jez.a.418)
61. Mizushima S, Takagi S, Ono T, Atsumi Y, Tsukada A, Saito N & Shimada K 2009 Phospholipase Cζ mRNA expression and its potency during spermatogenesis for activation of quail oocyte as a sperm factor. Molecular Reproduction and Development 76 1200-1207. (doi:10.1002/mrd.21097)
62. Nagai K, Ishida T, Hashimoto T, Harada Y, Ueno S, Ueda Y, Kubo H & Iwao Y 2009 The sperm-surface glycoprotein, SGP, is necessary for fertilization in the frog, Xenopus laevis. Development, Growth & Differentiation 51 499-510. (doi:10.1111/j.1440-169X.2009.01112.x)
63. Nishiyama T, Yoshizaki N, Kishimoto T & Ohsumi K 2007 Transient activation of calcineurin is essential to initiate embryonic development in Xenopus laevis. Nature 449 341-345. (doi:10.1038/nature06136)
64. 2C signal that induces egg activation and embryo development: an essential phospholipase C with implications for male infertility. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology 34 126-134. (doi:10.1002/bies.201100127)
65. Nuccitelli R 1980 The fertilization potential is not necessary for the block to polyspermy or the activation of development in the medaka egg. Developmental Biology 76 499-504. (doi:10.1016/0012-1606(80)90397-8)
66. Nuccitelli R, Kline D, Busa WB, Talevi R & Campanella C 1988 A highly localized activation current yet widespread intracellular calcium increase in the egg of the frog, Discoglossus pictus. Developmental Biology 130 120-132. (doi:10.1016/0012-1606(88)90419-8)
67. 2C wave following fertilization of the Xenopus egg requires the production of Ins(1, 4, 5)P3. Developmental Biology 158 200-212. (doi:10.1006/dbio.1993.1179)
68. Numata O 1996 Multifunctional proteins in Tetrahymena: 14-nm filament protein/citrate synthase and translation elongation factor-1 alpha. International Review of Cytology 164 1-35. (doi:10.1016/S0074-7696(08)62383-9)
69. Numata O, Sugai T & Watanabe Y 1985 Control of germ cell nuclear behaviour at fertilization by Tetrahymena intermediate filament protein. Nature 314 192-194. (doi:10.1038/314192a0)
70. 2C wave from the cortex mediated by the inositol 1,4,5-trisphosphate receptor. Developmental Biology 209 172-185. (doi:10.1006/dbio.1999.9233)
71. Ozil JP 1990 The parthenogenetic development of rabbit oocytes after repetitive pulsatile electrical stimulation. Development 109 117-127.
72. Parrington J, Swann K, Shevchenko VI, Sesay AK & Lai FA 1996 Calcium oscillations in mammalian eggs triggered by a soluble sperm protein. Nature 379 364-368. (doi:10.1038/379364a0)
73. Pelczar H, Caulet S, Thibier C, Aubet G, Poulhe R, Vallianou I, Yamashita M & Andeol Y 2007 Characterization and expression of a maternal axolotl cyclin B1 during oogenesis and early development. Development, Growth & Differentiation 49 407-419. (doi:10.1111/j. 1440-169X.2007.00934.x)
74. Perry MM 1987 Nuclear events from fertilisation to the early cleavage stages in the domestic fowl (Gallus domesticus). Journal of Anatomy 150 99-109. (Pubitemid 17020209)
75. Picheral B 1977 La fecondation chez le triton pleurodele. II. La penetration des spermatozoides et la reaction locale de l'oeuf. Journal of Ultra-structure Research 60 181-202. (doi:10.1016/S0022-5320(77)80064-6)
76. Rouvière C, Houliston E, Carré D, Chang P & Sardet C 1994 Characteristics of pronuclear migration in Beroe ovata. Cell Motility and the Cytoskeleton 29 301-311. (doi:10.1002/cm.970290403)
77. Sakakibara K, Sato K, Yoshino K, Oshiro N, Hirahara S, Mahbub Hasan AK, Iwasaki T, Ueda Y, Iwao Y, Yonezawa K et al. 2005 Molecular identification and characterization of Xenopus egg uroplakin III, an egg raft-associated transmembrane protein that is tyrosine-phosphorylated upon fertilization. Journal of Biological Chemistry 280 15029-15037. (doi:10.1074/jbc.M410538200)
78. Sakamoto I, Takahara K, Yamashita M & Iwao Y 1998 Changes in cyclin B during oocyte maturation and early embryonic cell cycle in the newt, Cynops pyrrhogaster: requirement of germinal vesicle for MPF activation. Developmental Biology 195 60-69. (doi:10.1006/dbio.1997.8835)
79. Sato K, Iwao Y, Fujimura T, Tamaki I, Ogawa K, Iwasaki T, Tokmakov AA, Hatano O & Fukami Y 1999 Evidence for the involvement of a Src-related tyrosine kinase in Xenopus egg activation. Developmental Biology 209 308-320. (doi:10.1006/dbio.1999.9255)
80. Sato K, Tokmakov AA, He CL, Kurokawa M, Iwasaki T, Shirouzu M, Fissore RA, Yokoyama S & Fukami Y 2003 Reconstitution of Src-dependent phospholipase Cg phosphorylation and transient calcium release by using membrane rafts and cell-free extracts from Xenopus eggs. Journal of Biological Chemistry 278 38413-38420. (doi:10.1074/jbc.M302617200)
81. 2C oscillations in eggs and embryo development. Development 129 3533-3544.
82. Shilling FM, Magie CR & Nuccitelli R 1998 Voltage-dependent activation of frog eggs by a sperm surface disintegrin peptide. Developmental Biology 202 113-124. (doi:10.1006/dbio.1998.8982)
83. Snook RR, Hosken DJ & Karr TL 2011 The biology and evolution of polyspermy: insights from cellular and functional studies of sperm and centrosomal behavior in the fertilized egg. Reproduction 142 779-792. (doi:10.1530/REP-11-0255)
84. Srere PA 1992 The molecular physiology of citrate. Current Topics in Cellular Regulation 33 261-275.
85. Stricker SA 1999 Comparative biology of calcium signaling during fertilization and egg activation in animals. Developmental Biology 211 157-176. (doi:10.1006/dbio.1999.9340)
86. Swann K 1990 A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs. Development 110 1295-1302. (Pubitemid 120009498)
87. 2C oscillations and egg activation in mammals. Seminars in Cell & Developmental Biology 17 264-273. (doi:10.1016/j.semcdb.2006.03.009)
88. Takeda T, Yoshihama I & Numata O 2001 Identification of Tetrahymena hsp60 as a 14-nm filament protein/citrate synthase-binding protein and its possible involvement in the oral apparatus formation. Genes to Cells 6 139-149. (doi:10.1046/j.1365-2443.2001.00400.x)
89. Talevi R 1989 Polyspermic eggs in the anuran Discoglossus pictus develop normally. Development 105 343-349. (Pubitemid 19053281)
90. Talevi R & Campanella C 1988 Fertilization in Discoglossus pictus (Anura). I. Sperm-egg interactions in distinct regions of the dimple and occurrence of a late stage of sperm penetration. Developmental Biology 130 524-535. (doi:10.1016/0012-1606(88)90347-8)
91. Talevi R, Dale B & Campanella C 1985 Fertilization and activation potentials in Discoglossus pictus (Anura) eggs: a delayed response to activation by pricking. Developmental Biology 111 316-323. (doi:10.1016/0012-1606(85) 90486-5)
92. Tomarev SI & Piatigorsky J 1996 Lens crystallins of invertebrates - diversity and recruitment from detoxification enzymes and novel proteins. European Journal of Biochemistry 235 449-465. (doi:10.1111/j.1432-1033.1996. 00449.x)
93. Vaur S, Poulhe R, Maton G, Andeol Y & Jessus C 2004 Activation of Cdc2 kinase during meiotic maturation of axolotl oocyte. Developmental Biology 267 265-278. (doi:10.1016/j.ydbio.2003.12.002)
94. Waddington D, Gribbin C, Sterling RJ, Sang HM & Perry MM 1998 Chronology of events in the first cell cycle of the polyspermic egg of the domestic fowl (Gallus domesticus). International Journal of Developmental Biology 42 625-628. (Pubitemid 28307869)
95. Wakimoto BT 1979 DNA synthesis after polyspermic fertilization in the axolotl. Journal of Embryology and Experimental Morphology 52 39-48. (Pubitemid 9250099)
96. Whitaker M 2006 Calcium at fertilization and in early development. Physiological Reviews 86 25-88. (doi:10.1152/physrev.00023.2005)
97. Wistow GJ, Mulders JW & de Jong WW 1987 The enzyme lactate dehydrogenase as a structural protein in avian and crocodilian lenses. Nature 326 622-624. (doi:10.1038/326622a0)
98. Wong JL & Wessel GM 2006 Defending the zygote: search for the ancestral animal block to polyspermy. Current Topics in Developmental Biology 72 1-151. (Pubitemid 43574747)
99. 2C level causes the decrease of cyclin B1 and Mos in the newt eggs at fertilization. Molecular Reproduction and Development 53 341-349. (doi:10.1002/(SICI)1098-2795(199907)53:3〈341::AID-MRD10〉3.0.CO;2-E)
100. Yamamoto S, Kubota HY, Yoshimoto Y & Iwao Y 2001 Injection of a sperm extract triggers egg activation in the newt Cynops pyrrhogaster. Developmental Biology 230 89-99. (doi:10.1006/dbio.2000.9949)
101. 2C oscillation-inducing phospholipase C zeta expressed in mouse eggs is accumulated to the pronucleus during egg activation. Developmental Biology 268 245-257. (doi:10.1016/j.ydbio.2003.12.028)
102. 2C with aequorin luminescence. International Review of Cytology 129 45-73.
103. 2C oscillations in mouse eggs by targeting intracellular and not plasma membrane PI(4,5)P2. Molecular Biology of the Cell 23 371-380. (doi:10.1091/mbc.E11-08-0687)