Understanding fertilization through intracytoplasmic sperm injection (ICSI)

Cell Calcium

Volumn 55, Issue 1, 2014, Pages 24-37

  Neri, Queenie V ^a   Lee, Bora ^a   Rosenwaks, Zev ^a   Machaca, Khaled ^b   Palermo, Gianpiero D ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (Qatar)

Author keywords

Assisted oocyte activation; Calcium influx; Failed fertilization; ICSI; Oocyte activation; PLC ; Sperm cytosolic factor

Indexed keywords

BIOLOGICAL FACTOR; CALCIUM ION; OOCYTE ACTIVATING FACTOR; OSCILLIN; PHOSPHOLIPASE C; PHOSPHOLIPASE C ZETA; STREPTOLYSIN O; UNCLASSIFIED DRUG;

ASSISTED OOCYTE ACTIVATION; CALCIUM TRANSPORT; CELL INTERACTION; CELL ULTRASTRUCTURE; ELECTROSTIMULATION; FERTILIZATION; FERTILIZATION FAILURE; GAMETE; GLOBOZOOSPERMIA; HUMAN; INFERTILITY; INFERTILITY THERAPY; INTRACYTOPLASMIC SPERM INJECTION; MOLECULAR DYNAMICS; MOUSE OOCYTE ACTIVATION TEST; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE MATURATION; PARTIAL ZONA DISSECTION; PATIENT SAFETY; PRIORITY JOURNAL; PROCEDURES CONCERNING CELLS; REVIEW; SEMEN ABNORMALITY; SPERMATOZOON; SUBZONAL SPERM INJECTION; TREATMENT FAILURE; ZONA DRILLING; CELL ACTIVATION; CELL ASSAY; CELL FUNCTION; CELL STRUCTURE; CELL VIABILITY; CELLULAR DISTRIBUTION; DISEASE ASSOCIATION; FERTILIZATION IN VITRO; OUTCOME ASSESSMENT; SEMEN ANALYSIS; SIGNAL TRANSDUCTION; SPERMATOZOON MOTILITY; TREATMENT RESPONSE;

ASSISTED OOCYTE ACTIVATION; CALCIUM INFLUX; FAILED FERTILIZATION; ICSI; OOCYTE ACTIVATION; PLCΖ; SPERM CYTOSOLIC FACTOR;

CALCIUM; FEMALE; FERTILIZATION; FERTILIZATION IN VITRO; HUMANS; MALE; OOCYTES; SPERM INJECTIONS, INTRACYTOPLASMIC; SPERMATOZOA;

EID: 84896729408     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2013.10.006     Document Type: Review

References (194)

1. Hardy K., Wright C., Rice S., Tachataki M., Roberts R., Morgan D., Spanos S., Taylor D. Future developments in assisted reproduction in humans. Reproduction 2002, 123:171-183.
2. Nomikos M., Elgmati K., Theodoridou M., Calver B.L., Nounesis G., Swann K., Lai F.A. Phospholipase Czeta binding to PtdIns(4 5)P2 requires the XY-linker region. Journal of Cell Science 2011, 124:2582-2590.
3. Sutovsky P. Sperm-egg adhesion and fusion in mammals. Expert Reviews in Molecular Medicine 2009, 11:e11.
4. Wassarman P.M., Jovine L., Qi H., Williams Z., Darie C., Litscher E.S. Recent aspects of mammalian fertilization research. Molecular and Cellular Endocrinology 2005, 234:95-103.
5. 2+increase at fertilization in the mouse. Development 1997, 124:233-241.
6. Swann K. The soluble sperm oscillogen hypothesis. Zygote 1993, 1:273-276.
7. Jaffe L.A., Cross N.L., Picheral B. Studies of the voltage-dependent polyspermy block using cross-species fertilization of amphibians. Developmental Biology 1983, 98:319-326.
8. Sun D.S., Lo S.J., Lin C.H., Yu M.S., Huang C.Y., Chen Y.F., Chang H.H. Calcium oscillation and phosphatidylinositol 3-kinase positively regulate integrin alpha(IIb)beta3-mediated outside-in signaling. Journal of Biomedical Science 2005, 12:321-333.
9. 2+ oscillations at fertilization of mammalian eggs. Developmental Biology 1993, 158:62-78.
10. Swann K., Whitaker M.J. Second messengers at fertilization in sea-urchin eggs. Journal of Reproduction and Fertility 1990, 42(Suppl.):141-153.
11. Dale B., DeFelice L.J., Ehrenstein G. Injection of a soluble sperm fraction into sea-urchin eggs triggers the cortical reaction. Experientia 1985, 41:1068-1070.
12. Berridge M.J. Inositol trisphosphate and calcium signalling. Nature 1993, 361:315-325.
13. 2+ entry during mammalian meiosis is required for the egg-to-embryo transition. Journal of Cell Science 2013, 126:1672-1681.
14. Runft L.L., Jaffe L.A., Mehlmann L.M. Egg activation at fertilization: where it all begins. Developmental Biology 2002, 245:237-254.
15. Stricker S.A. Comparative biology of calcium signaling during fertilization and egg activation in animals. Developmental Biology 1999, 211:157-176.
16. Parrington J., Swann K., Shevchenko V.I., Sesay A.K., Lai F.A. Calcium oscillations in mammalian eggs triggered by a soluble sperm protein. Nature 1996, 379:364-368.
17. Stice S.L., Robl J.M. Activation of mammalian oocytes by a factor obtained from rabbit sperm. Molecular Reproduction and Development 1990, 25:272-280.
18. Swann K. A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs. Development 1990, 110:1295-1302.
19. 2+ release in mammalian oocytes. Molecular Reproduction and Development 1999, 52:277-287.
20. Dale B., Marino M., Wilding M. Sperm-induced calcium oscillations. Soluble factor, factors or receptors?. Molecular Human Reproduction 1999, 5:1-4.
21. Jones K.T. Protein kinase C action at fertilization: overstated or undervalued?. Reviews of Reproduction 1998, 3:7-12.
22. Rice A., Parrington J., Jones K.T., Swann K. Mammalian sperm contain a Ca(2+)-sensitive phospholipase C activity that can generate InsP(3) from PIP(2) associated with intracellular organelles. Developmental Biology 2000, 228:125-135.
23. 2+ release in eggs. Reproduction 2002, 123:31-39.
24. Wu H., Smyth J., Luzzi V., Fukami K., Takenawa T., Black S.L., Allbritton N.L., Fissore R.A. Sperm factor induces intracellular free calcium oscillations by stimulating the phosphoinositide pathway. Biology of Reproduction 2001, 64:1338-1349.
25. Saunders C.M., Larman M.G., Parrington J., Cox L.J., Royse J., Blayney L.M., Swann K., Lai F.A. PLC zeta: a sperm-specific trigger of Ca(2+) oscillations in eggs and embryo development. Development 2002, 129:3533-3544.
26. 2+ oscillations, activation and development of mouse oocytes. Reproduction 2002, 124:611-623.
27. Aarabi M., Yu Y., Xu W., Tse M.Y., Pang S.C., Yi Y.J., Sutovsky P., Oko R. The testicular and epididymal expression profile of PLC zeta in mouse and human does not support its role as a sperm-borne oocyte activating factor. PLoS ONE 2012, 7:e33496. 1-12.
28. Colombero L.T., Moomjy M., Sills E.S., Rosenwaks Z., Palermo G.D. The role of structural integrity of the fertilising spermatozoon in early human embryogenesis. Zygote 1999, 7:157-163.
29. Grasa P., Coward K., Young C., Parrington J. The pattern of localization of the putative oocyte activation factor, phospholipase Czeta, in uncapacitated, capacitated, and ionophore-treated human spermatozoa. Human Reproduction 2008, 23:2513-2522.
30. Kuretake S., Kimura Y., Hoshi K., Yanagimachi R. Fertilization and development of mouse oocytes injected with isolated sperm heads. Biology of Reproduction 1996, 55:789-795.
31. Meng L., Wolf D.P. Sperm-induced oocyte activation in the rhesus monkey: nuclear and cytoplasmic changes following intracytoplasmic sperm injection. Human Reproduction 1997, 12:1062-1068.
32. Kimura Y., Yanagimachi R., Kuretake S., Bortkiewicz H., Perry A.C., Yanagimachi H. Analysis of mouse oocyte activation suggests the involvement of sperm perinuclear material. Biology of Reproduction 1998, 58:1407-1415.
33. Colombero L.T., Takeuchi T., Sills E.S., Breed W.G., Rosenwaks Z., Palermo G.D. A comparison of human spermatozoa immunolabeling features using xenogenic reagents for centrosomal proteins. Clinical and Experimental Obstetrics & Gynecology 1999, 26:141-146.
34. Palermo G., Munne S., Cohen J. The human zygote inherits its mitotic potential from the male gamete. Human Reproduction 1994, 9:1220-1225.
35. R.H.CDC Assisted Reproductive Technology Success Rates. National Summary and Fertility Clinic Reports 2008, National Center for Chronic Disease and Prevention and Health Promotion.
36. Cohen J., Edwards R.G., Fehilly C.B., Fishel S.B., Hewitt J., Rowland G., Steptoe P.C., Webster J. Treatment of male infertility by in vitro fertilization: factors affecting fertilization and pregnancy. Acta Europaea Fertilitatis 1984, 15:455-465.
37. Gordon J.W., Talansky B.E. Assisted fertilization by zona drilling: a mouse model for correction of oligospermia. Journal of Experimental Zoology 1986, 239:347-354.
38. Tsunoda Y., Yasui T., Nakamura K., Uchida T., Sugie T. Effect of cutting the zona-pellucida on the pronuclear transplantation in the mouse. Journal of Experimental Zoology 1986, 240:119-125.
39. Odawara Y., Lopata A. A zona opening procedure for improving in vitro fertilization at low sperm concentrations: a mouse model. Fertility and Sterility 1989, 51:699-704.
40. Gordon J.W., Grunfeld L., Garrisi G.J., Talansky B.E., Richards C., Laufer N. Fertilization of human oocytes by sperm from infertile males after zona pellucida drilling. Fertility and Sterility 1988, 50:68-73.
41. Cohen J., Malter H., Fehilly C., Wright G., Elsner C., Kort H., Massey J. Implantation of embryos after partial opening of oocyte zona pellucida to facilitate sperm penetration. Lancet 1988, 2. 162-162.
42. Antinori S., Versaci C., Fuhrberg P., Panci C., Caffa B., Gholami G.H. Seventeen live births after the use of an erbium-yytrium aluminum garnet laser in the treatment of male factor infertility. Human Reproduction 1994, 9:1891-1896.
43. Feichtinger W., Strohmer H., Fuhrberg P., Radivojevic K., Antinori S., Pepe G., Versaci C. Photoablation of oocyte zona pellucida by erbium-YAG laser for in-vitro fertilisation in severe male infertility. Lancet 1992, 339:811.
44. Laws-King A., Trounson A., Sathananthan H., Kola I. Fertilization of human oocytes by microinjection of a single spermatozoon under the zona pellucida. Fertility and Sterility 1987, 48:637-642.
45. Palermo G., Joris H., Devroey P., Van Steirteghem A.C. Induction of acrosome reaction in human spermatozoa used for subzonal insemination. Human Reproduction 1992, 7:248-254.
46. Palermo G., Van Steirteghem A. Enhancement of acrosome reaction and subzonal insemination of a single spermatozoon in mouse eggs. Molecular Reproduction and Development 1991, 30:339-345.
47. Palermo G., Joris H., Devroey P., Van Steirteghem A.C. Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet 1992, 340:17-18.
48. Hiramoto Y. Microinjection of the live spermatozoa into sea urchin eggs. Experimental Cell Research 1962, 27:416-426.
49. Lin T.P. Microinjection of mouse eggs. Science 1966, 151:333-337.
50. Uehara T., Yanagimachi R. Microsurgical injection of spermatozoa into hamster eggs with subsequent transformation of sperm nuclei into male pronuclei. Biology of Reproduction 1976, 15:467-470.
51. Naish S.J., Perreault S.D., Foehner A.L., Zirkin B.R. DNA synthesis in the fertilizing hamster sperm nucleus: sperm template availability and egg cytoplasmic control. Biology of Reproduction 1987, 36:245-253.
52. Perreault S.D., Wolff R.A., Zirkin B.R. The role of disulfide bond reduction during mammalian sperm nuclear decondensation in vivo. Developmental Biology 1984, 101:160-167.
53. Laufer N., Pratt B.M., DeCherney A.H., Naftolin F., Merino M., Markert C.L. The in vivo and in vitro effects of clomiphene citrate on ovulation, fertilization, and development of cultured mouse oocytes. American Journal of Obstetrics and Gynecology 1983, 147:633-639.
54. Thadani V.M. Injection of sperm heads into immature rat oocytes. Journal of Experimental Zoology 1979, 210:161-168.
55. Iritani A., Utsumi K., Miyake M., Hosoi Y., Saeki K. In vitro fertilization by a routine method and by micromanipulation. Annals of the New York Academy of Sciences 1988, 541:583-590.
56. Goto K., Kinoshita A., Takuma Y., Ogawa K. Fertilization of bovine oocytes by the injection of immobilized, killed spermatozoa. Veterinary Record 1990, 127:517-520.
57. Lanzendorf S.E., Maloney M.K., Veeck L.L., Slusser J., Hodgen G.D., Rosenwaks Z. A preclinical evaluation of pronuclear formation by microinjection of human spermatozoa into human oocytes. Fertility and Sterility 1988, 49:835-842.
58. Nakano Y., Shirakawa H., Mitsuhashi N., Kuwabara Y., Miyazaki S. Spatiotemporal dynamics of intracellular calcium in the mouse egg injected with a spermatozoon. Molecular Human Reproduction 1997, 3:1087-1093.
59. 2+]i rises in mouse eggs after intracytoplasmic sperm injection (ICSI). Cell Calcium 1999, 26:49-58.
60. Tesarik J., Sousa M., Testart J. Human oocyte activation after intracytoplasmic sperm injection. Human Reproduction 1994, 9:511-518.
61. Kimura Y., Yanagimachi R. Intracytoplasmic sperm injection in the mouse. Biology of Reproduction 1995, 52:709-720.
62. Van Steirteghem A.C., Liu J., Joris H., Nagy Z., Janssenswillen C., Tournaye H., Derde M.P., Van Assche E., Devroey P. Higher success rate by intracytoplasmic sperm injection than by subzonal insemination. Report of a second series of 300 consecutive treatment cycles. Human Reproduction 1993, 8:1055-1060.
63. Kimura Y., Yanagimachi R. Mouse oocytes injected with testicular spermatozoa or round spermatids can develop into normal offspring. Development 1995, 121:2397-2405.
64. Kimura Y., Yanagimachi R. Development of normal mice from oocytes injected with secondary spermatocyte nuclei. Biology of Reproduction 1995, 53:855-862.
65. 2+ oscillation-inducing sperm factor. Molecular Human Reproduction 1999, 5:132-138.
66. Sato Y., Miyazaki S., Shikano T., Mitsuhashi N., Takeuchi H., Mikoshiba K., Kuwabara Y. Adenophostin, a potent agonist of the inositol 1,4,5-trisphosphate receptor, is useful for fertilization of mouse oocytes injected with round spermatids leading to normal offspring. Biology of Reproduction 1998, 58:867-873.
67. Sousa M., Mendoza C., Barros A., Tesarik J. Calcium responses of human oocytes after intracytoplasmic injection of leukocytes, spermatocytes and round spermatids. Molecular Human Reproduction 1996, 2:853-857.
68. Tesarik J. Oocyte activation after intracytoplasmic injection of mature and immature sperm cells. Human Reproduction 1998, 13(Suppl. 1):117-127.
69. Ogura A., Matsuda J., Yanagimachi R. Birth of normal young after electrofusion of mouse oocytes with round spermatids. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:7460-7462.
70. Dozortsev D., Rybouchkin A., De Sutter P., Qian C., Dhont M. Human oocyte activation following intracytoplasmic injection: the role of the sperm cell. Human Reproduction 1995, 10:403-407.
71. Leybaert L., Depypere H.T., Dhont M., de Hemptinne A. Changes of intracellular free calcium during intracytoplasmic sperm injection. Molecular Reproduction and Development 1996, 43:256-260.
72. 2+ oscillations and overcomes activation failure of mammalian oocytes. Molecular Human Reproduction 1997, 3:367-374.
73. Harton G., Braude P., Lashwood A., Schmutzler A., Traeger-Synodinos J., Wilton L., Harper J.C. ESHRE PGD consortium best practice guidelines for organization of a PGD centre for PGD/preimplantation genetic screening. Human Reproduction 2011, 26:14-24.
74. Palermo G.D., Neri Q.V., Monahan D., Rosenwaks Z. Micromanipulation: Intracytoplasmic Sperm Injection and Assisted Hatching 2012, Springer, New York.
75. Bartoov B., Berkovitz A., Eltes F. Selection of spermatozoa with normal nuclei to improve the pregnancy rate with intracytoplasmic sperm injection. New England Journal of Medicine 2001, 345:1067-1068.
76. Bartoov B., Berkovitz A., Eltes F., Kogosowski A., Menezo Y., Barak Y. Real-time fine morphology of motile human sperm cells is associated with IVF-ICSI outcome. Journal of Andrology 2002, 23:1-8.
77. Antinori M., Licata E., Dani G., Cerusico F., Versaci C., d'Angelo D., Antinori S. Intracytoplasmic morphologically selected sperm injection: a prospective randomized trial. Reproductive Biomedicine Online 2008, 16:835-841.
78. Bartoov B., Berkovitz A., Eltes F., Kogosovsky A., Yagoda A., Lederman H., Artzi S., Gross M., Barak Y. Pregnancy rates are higher with intracytoplasmic morphologically selected sperm injection than with conventional intracytoplasmic injection. Fertility and Sterility 2003, 80:1413-1419.
79. Berkovitz A., Eltes F., Yaari S., Katz N., Barr I., Fishman A., Bartoov B. The morphological normalcy of the sperm nucleus and pregnancy rate of intracytoplasmic injection with morphologically selected sperm. Human Reproduction 2005, 20:185-190.
80. Hazout A., Dumont-Hassan M., Junca A.M., Cohen Bacrie P., Tesarik J. High-magnification ICSI overcomes paternal effect resistant to conventional ICSI. Reproductive Biomedicine Online 2006, 12:19-25.
81. Zamboni L. The ultrastructural pathology of the spermatozoon as a cause of infertility: the role of electron microscopy in the evaluation of semen quality. Fertility and Sterility 1987, 48:711-734.
82. Fawcett D.W., Ito S. Observations on the cytoplasmic membranes of testicular cells, examined by phase contrast and electron microscopy. Journal of Biophysical and Biochemical Cytology 1958, 4:135-142.
83. Baccetti B., Burrini A.G., Collodel G., Magnano A.R., Piomboni P., Renieri T., Sensini C. Crater defect in human spermatozoa. Gamete Research 1989, 22:249-255.
84. Kacem O., Sifer C., Barraud-Lange V., Ducot B., De Ziegler D., Poirot C., Wolf J. Sperm nuclear vacuoles, as assessed by motile sperm organellar morphological examination, are mostly of acrosomal origin. Reproductive Biomedicine Online 2010, 20:132-137.
85. Peer S., Eltes F., Berkovitz A., Yehuda R., Itsykson P., Bartoov B. Is fine morphology of the human sperm nuclei affected by in vitro incubation at 37 degrees C?. Fertility and Sterility 2007, 88:1589-1594.
86. Tanaka A., Nagayoshi M., Awata S., Tanaka I., Kusunoki H., Watanabe S. Are crater defects in human sperm heads physiological changes during spermiogenesis?. Fertility and Sterility 2009, 92:S165.
87. Watanabe S., Tanaka A., Fujii S., Misunuma H. No relationship between chromosome aberrations and vacuole-like structures on human sperm head. Human Reproduction 2009, 24:i94-i96.
88. Palermo G.D., Hu J.C.Y., Rienzi L., Maggiulli R., Takeuchi T., Yoshida A., Tanaka A., Kusunoki H., Watanabe S., Neri Q.V., Rosenwaks Z. Thoughts on IMSI 2011, Springer, New York.
89. Palermo G.D., Neri Q.V., Takeuchi T., Rosenwaks Z. ICSI: where we have been and where we are going. Seminars in Reproductive Medicine 2009, 27:191-201.
90. Esfandiari N., Faved M.H., Gotlieb L., Casper R.F. Complete failed fertilization after intracytoplasmic sperm injection - analysis of 10 years' data. International Journal of Fertility and Women's Medicine 2005, 50:187-192.
91. Devroey P., Liu J., Nagy Z., Goossens A., Tournaye H., Camus M., Van Steirteghem A., Silber S. Pregnancies after testicular sperm extraction and intracytoplasmic sperm injection in non-obstructive azoospermia. Human Reproduction 1995, 10:1457-1460.
92. Flaherty S.P., Payne D., Swann N.J., Mattews C.D. Aetiology of failed and abnormal fertilization after intracytoplasmic sperm injection. Human Reproduction 1995, 10:2623-2629.
93. Palermo G.D., Schlegel P.N., Colombero L.T., Zaninovic N., Moy F., Rosenwaks Z. Aggressive sperm immobilization prior to intracytoplasmic sperm injection with immature spermatozoa improves fertilization and pregnancy rates. Human Reproduction 1996, 11:1023-1029.
94. Sousa M., Tesarik J. Ultrastructural analysis of fertilization failure after intracytoplasmic sperm injection. Human Reproduction 1994, 9:2374-2380.
95. Yanagida K. Complete fertilization failure in ICSI. Human Cell 2004, 17:187-193.
96. Moomjy M., Colombero L.T., Veeck L.L., Rosenwaks Z., Palermo G.D. Sperm integrity is critical for normal mitotic division and early embryonic development. Molecular Human Reproduction 1999, 5:836-844.
97. Kang H., Neri Q.V., Takeuchi T., Moy F., Rosenwaks Z., Palermo G.D. Investigating unexpected complete fertilization failure with ICSI. Fertility and Sterility 2005, 84:S257.
98. Kocent J., Monahan D., Neri Q.V., Rosenwaks Z., Palermo G.D. Untimely cumulus removal affects ooplasmic competence. Fertility and Sterility 2010, 94:S252.
99. Palermo G.D., Neri Q.V., Monahan D., Kocent J., Rosenwaks Z. Development and current applications of assisted fertilization. Fertility and Sterility 2012, 97:248-259.
100. Sundstrom P., Nilsson B.O. Meiotic and cytoplasmic maturation of oocytes collected in stimulated cycles is asynchronous. Human Reproduction 1988, 3:613-619.
101. Kashir J., Heindryckx B., Jones C., De Sutter P., Parrington J., Coward K. Oocyte activation, phospholipase C zeta and human infertility. Human Reproduction Update 2010, 16:690-703.
102. 2+ oscillations and egg activation in mammals is a novel phospholipase C: PLC zeta. Reproduction 2004, 127:431-439.
103. Swain J.E., Pool T.B. ART failure: oocyte contributions to unsuccessful fertilization. Human Reproduction Update 2008, 14:431-446.
104. Rawe V.Y., Brugo Olmedo S., Nodar F.N., Vitullo A.D. Microtubules and parental genome organisation during abnormal fertilisation in humans. Zygote 2002, 10:223-228.
105. Rawe V.Y., Terada Y., Nakamura S., Chillik C.F., Olmedo S.B., Chemes H.E. A pathology of the sperm centriole responsible for defective sperm aster formation, syngamy and cleavage. Human Reproduction 2002, 17:2344-2349.
106. Kovacic B., Vlaisavljevic V. Configuration of maternal and paternal chromatin and pertaining microtubules in human oocytes failing to fertilize after intracytoplasmic sperm injection. Molecular Reproduction and Development 2000, 55:197-204.
107. Eldar-Geva T., Brooks B., Margalioth E.J., Zylber-Haran E., Gal M., Silber S.J. Successful pregnancy and delivery after calcium ionophore oocyte activation in a normozoospermic patient with previous repeated failed fertilization after intracytoplasmic sperm injection. Fertility and Sterility 2003, 79(Suppl. 3):1656-1658.
108. Heindryckx B., Van der Elst J., De Sutter P., Dhont M. Treatment option for sperm- or oocyte-related fertilization failure: assisted oocyte activation following diagnostic heterologous ICSI. Human Reproduction 2005, 20:2237-2241.
109. Murase Y., Araki Y., Mizuno S., Kawaguchi C., Naito M., Yoshizawa M., Araki Y. Pregnancy following chemical activation of oocytes in a couple with repeated failure of fertilization using ICSI: case report. Human Reproduction 2004, 19:1604-1607.
110. Yanagida K., Katayose H., Yazawa H., Kimura Y., Sato A., Yanagimachi H., Yanagimachi R. Successful fertilization and pregnancy following ICSI and electrical oocyte activation. Human Reproduction 1999, 14:1307-1311.
111. Van Wissen B., Eisenberg C., Debey P., Pennehouat G., Auger J., Bomsel-Helmreich O. In vitro DNA fluorescence after in vitro fertilization (IVF) failure. Journal of Assisted Reproduction and Genetics 1992, 9:564-571.
112. Racowsky C., Kaufman M.L., Dermer R.A., Homa S.T., Gunnala S. Chromosomal analysis of meiotic stages of human oocytes matured in vitro: benefits of protease treatment before fixation. Fertility and Sterility 1992, 57:1026-1033.
113. Rosenbusch B.E. Frequency and patterns of premature sperm chromosome condensation in oocytes failing to fertilize after intracytoplasmic sperm injection. Journal of Assisted Reproduction and Genetics 2000, 17:253-259.
114. Eichenlaub-Ritter U., Schmiady H., Kentenich H., Soewarto D. Recurrent failure in polar body formation and premature chromosome condensation in oocytes from a human patient: indicators of asynchrony in nuclear and cytoplasmic maturation. Human Reproduction 1995, 10:2343-2349.
115. Miyara F., Aubriot F.X., Glissant A., Nathan C., Douard S., Stanovici A., Herve F., Dumont-Hassan M., LeMeur A., Cohen-Bacrie P., Debey P. Multiparameter analysis of human oocytes at metaphase II stage after IVF failure in non-male infertility. Human Reproduction 2003, 18:1494-1503.
116. WHO WHO Laboratory Manual for the Examination and Processing of Human Semen 2010, Cambridge University Press, Cambridge. 5th ed.
117. Heytens E., Parrington J., Coward K., Young C., Lambrecht S., Yoon S.Y., Fissore R.A., Hamer R., Deane C.M., Ruas M., Grasa P., Soleimani R., Cuvelier C.A., Gerris J., Dhont M., Deforce D., Leybaert L., De Sutter P. Reduced amounts and abnormal forms of phospholipase C zeta (PLCzeta) in spermatozoa from infertile men. Human Reproduction 2009, 24:2417-2428.
118. Yoon S.Y., Jellerette T., Salicioni A.M., Lee H.C., Yoo M.S., Coward K., Parrington J., Grow D., Cibelli J.B., Visconti P.E., Mager J., Fissore R.A. Human sperm devoid of PLC, zeta 1 fail to induce Ca(2+) release and are unable to initiate the first step of embryo development. Journal of Clinical Investigation 2008, 118:3671-3681.
119. Neri Q.V., Monahan D., Kocent J., Hu J.C.Y., Rosenwaks Z., Palermo G.D. Assessing and restoring sperm fertilizing ability. Fertility and Sterility 2010, 94:S147.
120. Aghajanpour S., Ghaedi K., Salamian A., Deemeh M.R., Tavalaee M., Moshtaghian J., Parrington J., Nasr-Esfahani M.H. Quantitative expression of phospholipase C zeta, as an index to assess fertilization potential of a semen sample. Human Reproduction 2011, 26:2950-2956.
121. Kashir J., Jones C., Mounce G., Ramadan W.M., Lemmon B., Heindryckx B., de Sutter P., Parrington J., Turner K., Child T., McVeigh E., Coward K. Variance in total levels of phospholipase C zeta (PLC-zeta) in human sperm may limit the applicability of quantitative immunofluorescent analysis as a diagnostic indicator of oocyte activation capability. Fertility and Sterility 2013, 99:107-117.
122. Rybouchkin A., Dozortsev D., de Sutter P., Qian C., Dhont M. Intracytoplasmic injection of human spermatozoa into mouse oocytes: a useful model to investigate the oocyte-activating capacity and the karyotype of human spermatozoa. Human Reproduction 1995, 10:1130-1135.
123. Vanden Meerschaut F., Leybaert L., Nikiforaki D., Qian C., Heindryckx B., De Sutter P. Diagnostic and prognostic value of calcium oscillatory pattern analysis for patients with ICSI fertilization failure. Human Reproduction 2013, 28:87-98.
124. Holstein A.F., Schirren C.G., Schirren C., Mauss J. Round headed spermatozoa: a cause of male infertility. Deutsche Medizinische Wochenschrift 1973, 98:61-62.
125. Singh G. Ultrastructural features of round-headed human spermatozoa. International Journal of Fertility 1992, 37:99-102.
126. Dale B., Iaccarino M., Fortunato A., Gragnaniello G., Kyozuka K., Tosti E. A morphological and functional-study of fusibility in round-headed spermatozoa in the human. Fertility and Sterility 1994, 61:336-340.
127. Aitken R.J., Kerr L., Bolton V., Hargreave T. Analysis of sperm function in globozoospermia - implications for the mechanism of sperm-zona interaction. Fertility and Sterility 1990, 54:701-707.
128. Rybouchkin A., Dozortsev D., Pelinck M.J., De Sutter P., Dhont M. Analysis of the oocyte activating capacity and chromosomal complement of round-headed human spermatozoa by their injection into mouse oocytes. Human Reproduction 1996, 11:2170-2175.
129. Dam A.H., Feenstra I., Westphal J.R., Ramos L., van Golde R.J., Kremer J.A. Globozoospermia revisited. Human Reproduction Update 2007, 13:63-75.
130. Moretti E., Collodel G., Scapigliati G., Cosci I., Sartini B., Baccetti B. 'Round head' sperm defect. Ultrastructural and meiotic segregation study. Journal of Submicroscopic Cytology and Pathology 2005, 37:297-303.
131. Dam A.H., Koscinski I., Kremer J.A., Moutou C., Jaeger A.S., Oudakker A.R., Tournaye H., Charlet N., Lagier-Tourenne C., van Bokhoven H., Viville S. Homozygous mutation in SPATA16 is associated with male infertility in human globozoospermia. American Journal of Human Genetics 2007, 81:813-820.
132. Liu G., Shi Q.W., Lu G.X. A newly discovered mutation in PICK1 in a human with globozoospermia. Asian Journal of Andrology 2010, 12:556-560.
133. Taylor S.L., Yoon S.Y., Morshedi M.S., Lacey D.R., Jellerette T., Fissore R.A., Oehninger S. Complete globozoospermia associated with PLCzeta deficiency treated with calcium ionophore and ICSI results in pregnancy. Reproductive Biomedicine Online 2010, 20:559-564.
134. Kashir J., Sermondade N., Sifer C., Oo S.L., Jones C., Mounce G., Turner K., Child T., McVeigh E., Coward K. Motile sperm organelle morphology evaluation-selected globozoospermic human sperm with an acrosomal bud exhibits novel patterns and higher levels of phospholipase C zeta. Human Reproduction 2012, 27:3150-3160.
135. Heytens E., Schmitt-John T., Moser J.M., Jensen N.M., Soleimani R., Young C., Coward K., Parrington J., De Sutter P. Reduced fertilization after ICSI and abnormal phospholipase C zeta presence in spermatozoa from the wobbler mouse. Reproductive Biomedicine Online 2010, 21:742-749.
136. Neri Q.V. Tweaking Human Fertilization, in: Reproductive Medicince, Clinical & Translation Science Center 2010, 24. Weill Cornell Medical College, New York.
137. Albertini D.F., Sanfins A., Combelles C.M. Origins and manifestations of oocyte maturation competencies. Reproductive Biomedicine Online 2003, 6:410-415.
138. Eppig J.J., O'Brien M., Wigglesworth K. Mammalian oocyte growth and development in vitro. Molecular Reproduction and Development 1996, 44:260-273.
139. Moor R.M., Dai Y., Lee C., Fulka J. Oocyte maturation and embryonic failure. Human Reproduction Update 1998, 4:223-236.
140. Trounson A., Anderiesz C., Jones G. Maturation of human oocytes in vitro and their developmental competence. Reproduction 2001, 121:51-75.
141. Eppig J.J., Schultz R.M., O'Brien M., Chesnel F. Relationship between the developmental programs controlling nuclear and cytoplasmic maturation of mouse oocytes. Developmental Biology 1994, 164:1-9.
142. Sundstrom P., Nilsson O. Sequential changes in cytoplasmatic features during maturation of the human oocyte. Progress in Clinical and Biological Research 1989, 296:327-333.
143. De Santis L., Cino I., Rabellotti E., Calzi F., Persico P., Borini A., Coticchio G. Polar body morphology and spindle imaging as predictors of oocyte quality. Reproductive Biomedicine Online 2005, 11:36-42.
144. Rienzi L., Ubaldi F., Iacobelli M., Minasi M.G., Romano S., Greco E. Meiotic spindle visualization in living human oocytes. Reproductive Biomedicine Online 2005, 10:192-198.
145. Montag M., Schimming T., van der Ven H. Spindle imaging in human oocytes: the impact of the meiotic cell cycle. Reproductive Biomedicine Online 2006, 12:442-446.
146. Hyun C.S., Cha J.H., Son W.Y., Yoon S.H., Kim K.A., Lim J.H. Optimal ICSI timing after the first polar body extrusion in in vitro matured human oocytes. Human Reproduction 2007, 22:1991-1995.
147. Trounson A.O. The choice of the most appropriate microfertilization technique for human male factor infertility. Reproduction, Fertility, and Development 1994, 6:37-43.
148. Palermo G.D., Bedford J.M. Micromanipulation of Human Gametes, Zygotes, and Embryos 2000, CRC Press LLC, Boca Raton, Florida.
149. Palermo G., Joris H., Derde M.P., Camus M., Devroey P., Van Steirteghem A. Sperm characteristics and outcome of human assisted fertilization by subzonal insemination and intracytoplasmic sperm injection. Fertility and Sterility 1993, 59:826-835.
150. Palermo G.D., Cohen J., Alikani M., Adler A., Rosenwaks Z. Intracytoplasmic sperm injection: a novel treatment for all forms of male factor infertility. Fertility and Sterility 1995, 63:1231-1240.
151. Schlegel P.N. Nonobstructive azoospermia: a revolutionary surgical approach and results. Seminars in Reproductive Medicine 2009, 27:165-170.
152. Tournaye H., Devroey P., Liu J., Nagy Z., Lissens W., Van Steirteghem A. Microsurgical epididymal sperm aspiration and intracytoplasmic sperm injection: a new effective approach to infertility as a result of congenital bilateral absence of the vas deferens. Fertility and Sterility 1994, 61:1045-1051.
153. Maggiulli R., Neri Q.V., Monahan D., Hu J., Takeuchi T., Rosenwaks Z., Palermo G.D. What to do when ICSI fails. Systems Biology in Reproductive Medicine 2010, 56:376-387.
154. Bhattacharya S., Hamilton M.P., Shaaban M., Khalaf Y., Seddler M., Ghobara T., Braude P., Kennedy R., Rutherford A., Hartshorne G., Templeton A. Conventional in-vitro fertilisation versus intracytoplasmic sperm injection for the treatment of non-male-factor infertility: a randomised controlled trial. Lancet 2001, 357:2075-2079.
155. Heindryckx B., De Gheselle S., Gerris J., Dhont M., De Sutter P. Efficiency of assisted oocyte activation as a solution for failed intracytoplasmic sperm injection. Reproductive Biomedicine Online 2008, 17:662-668.
156. Zhang J., Wang C.W., Blaszcyzk A., Grifo J.A., Ozil J., Haberman E., Adler A., Krey L.C. Electrical activation and in vitro development of human oocytes that fail to fertilize after intracytoplasmic sperm injection. Fertility and Sterility 1999, 72:509-512.
157. Koo O.J., Jang G., Kwon D.K., Kang J.T., Kwon O.S., Park H.J., Kang S.K., Lee B.C. Electrical activation induces reactive oxygen species in porcine embryos. Theriogenology 2008, 70:1111-1118.
158. Nasr-Esfahani M.H., Deemeh M.R., Tavalaee M. Artificial oocyte activation and intracytoplasmic sperm injection. Fertility and Sterility 2010, 94:520-526.
159. Alberio R., Zakhartchenko V., Motlik J., Wolf E. Mammalian oocyte activation: lessons from the sperm and implications for nuclear transfer. International Journal of Developmental Biology 2001, 45:797-809.
160. Yamano S., Nakagawa K., Nakasaka H., Aono T. Fertilization failure and oocyte activation. Journal of Medical Investigation 2000, 47:1-8.
161. Check J.H., Levito M.C., Summers-Chase D., Marmar J., Barci H. A comparison of the efficacy of intracytoplasmic sperm injection (ICSI) using ejaculated sperm selected by high magnification versus ICSI with testicular sperm both followed by oocyte activation with calcium ionophore. Clinical and Experimental Obstetrics & Gynecology 2007, 34:111-112.
162. Tesarik J., Sousa M. More than 90% fertilization rates after intracytoplasmic sperm injection and artificial induction of oocyte activation with calcium ionophore. Fertility and Sterility 1995, 63:343-349.
163. Moaz M.N., Khattab S., Foutouh I.A., Mohsen E.A. Chemical activation of oocytes in different types of sperm abnormalities in cases of low or failed fertilization after ICSI: a prospective pilot study. Reproductive Biomedicine Online 2006, 13:791-794.
164. Nasr-Esfahani M.H., Razavi S., Javdan Z., Tavalaee M. Artificial oocyte activation in severe teratozoospermia undergoing intracytoplasmic sperm injection. Fertility and Sterility 2008, 90:2231-2237.
165. Mansour R., Fahmy I., Tawab N.A., Kamal A., El-Demery Y., Aboulghar M., Serour G. Electrical activation of oocytes after intracytoplasmic sperm injection: a controlled randomized study. Fertility and Sterility 2009, 91:133-139.
166. Fields T., Neri Q.V., Hu J.C.Y., Rosenwaks Z., Palermo G.D. A qualitative assay for sperm fertilization competence. Human Reproduction 2011, 19:i349.
167. Alouf J.E. Streptococcal toxins (streptolysin O, streptolysin S, erythrogenic toxin). Pharmacology & Therapeutics 1980, 11:661-717.
168. Buckingham L., Duncan J.L. Approximate dimensions of membrane lesions produced by streptolysin-S and streptolysin-O. Biochimica et Biophysica Acta 1983, 729:115-122.
169. Sullivan E.J., Kasinathan S., Kasinathan P., Robl J.M., Collas P. Cloned calves from chromatin remodeled in vitro. Biology of Reproduction 2004, 70:146-153.
170. 2+ oscillations and egg activation in mammals. Seminars in Cell & Developmental Biology 2006, 17:264-273.
171. Kouchi Z., Shikano T., Nakamura Y., Shirakawa H., Fukami K., Miyazaki S. The role of EF-hand domains and C2 domain in regulation of enzymatic activity of phospholipase Czeta. Journal of Biological Chemistry 2005, 280:21015-21021.
172. 2+ oscillations cause coincident cytoplasmic movements in human oocytes that failed to fertilize after intracytoplasmic sperm injection. Fertility and Sterility 2012, 97:742-747.
173. 2+ oscillations and parthenogenetic activation of human oocytes. Reproduction 2004, 128:697-702.
174. Spadafora C. Endogenous reverse transcriptase: a mediator of cell proliferation and differentiation. Cytogenetic and Genome Research 2004, 105:346-350.
175. Yoon S.Y., Eum J.H., Lee J.E., Lee H.C., Kim Y.S., Han J.E., Won H.J., Park S.H., Shim S.H., Lee W.S., Fissore R.A., Lee D.R., Yoon T.K. Recombinant human phospholipase C zeta 1 induces intracellular calcium oscillations and oocyte activation in mouse and human oocytes. Human Reproduction 2012, 27:1768-1780.
176. Miyazaki S., Ito M. Calcium signals for egg activation in mammals. Journal of Pharmacological Sciences 2006, 100:545-552.
177. Fissore R.A., Long C.R., Duncan R.P., Robl J.M. Initiation and organization of events during the first cell cycle in mammals: applications in cloning. Cloning 1999, 1:89-100.
178. Shirakawa H., Miyazaki S. Spatiotemporal analysis of calcium dynamics in the nucleus of hamster oocytes. Journal of Physiology 1996, 494(Pt 1):29-40.
179. Markert C.L. Fertilization of mammalian eggs by sperm injection. Journal of Experimental Zoology 1983, 228:195-201.
180. Neri Q.V., Kocent J., Rosenwaks Z., Palermo G.D. Attempts to revive non-motile spermatozoa resilient to motility enhancers. Fertility and Sterility 2010, 94:S15-S16.
181. 2+ oscillatory pattern in fertilized mouse eggs affects gene expression and development to term. Developmental Biology 2006, 300:534-544.
182. Ahmady A., Michael E. Successful pregnancy and delivery following intracytoplasmic injection of frozen-thawed nonviable testicular sperm and oocyte activation with calcium ionophore. Journal of Andrology 2007, 28:13-14.
183. Chi H.J., Koo J.J., Song S.J., Lee J.Y., Chang S.S. Successful fertilization and pregnancy after intracytoplasmic sperm injection and oocyte activation with calcium ionophore in a normozoospermic patient with extremely low fertilization rates in intracytoplasmic sperm injection cycles. Fertility and Sterility 2004, 82:475-477.
184. Dirican E.K., Isik A., Vicdan K., Sozen E., Suludere Z. Clinical pregnancies and livebirths achieved by intracytoplasmic injection of round headed acrosomeless spermatozoa with and without oocyte activation in familial globozoospermia: case report. Asian Journal of Andrology 2008, 10:332-336.
185. Egashira A., Murakami M., Haigo K., Horiuchi T., Kuramoto T. A successful pregnancy and live birth after intracytoplasmic sperm injection with globozoospermic sperm and electrical oocyte activation. Fertility and Sterility 2009, 92:e2035-e2039. 2037.
186. Kim S.T., Cha Y.B., Park J.M., Gye M.C. Successful pregnancy and delivery from frozen-thawed embryos after intracytoplasmic sperm injection using round-headed spermatozoa and assisted oocyte activation in a globozoospermic patient with mosaic Down syndrome. Fertility and Sterility 2001, 75:445-447.
187. Kyono K., Kumagai S., Nishinaka C., Nakajo Y., Uto H., Toya M., Sugawara J., Araki Y. Birth and follow-up of babies born following ICSI using SrCl2 oocyte activation. Reproductive Biomedicine Online 2008, 17:53-58.
188. Rybouchkin A.V., Van der Straeten F., Quatacker J., De Sutter P., Dhont M. Fertilization and pregnancy after assisted oocyte activation and intracytoplasmic sperm injection in a case of round-headed sperm associated with deficient oocyte activation capacity. Fertility and Sterility 1997, 68:1144-1147.
189. Kyono K., Takisawa T., Nakajo Y., Doshida M., Toya M. Birth and follow-up of babies born following ICSI with oocyte activation using strontium chloride or calcium ionophore A23187. Journal of Mammalian Ova Research 2012, 29:35-40.
190. Vanden Meerschaut F., D'Haeseleer E., Roeyers H., Oostra A., Van Lierde K., De Sutter P. Neonatal and developmental outcome of children born following assisted oocyte activation (AOA). Fertility and Sterility 2012, 98:S16.
191. Kashir J., Konstantinidis M., Jones C., Lemmon B., Lee H.C., Hamer R., Heindryckx B., Deane C.M., De Sutter P., Fissore R.A., Parrington J., Wells D., Coward K. A maternally inherited autosomal point mutation in human phospholipase C zeta (PLCzeta) leads to male infertility. Human Reproduction 2012, 27:222-231.
192. Swann K., Lai F.A. PLCzeta and the initiation of Ca(2+) oscillations in fertilizing mammalian eggs. Cell Calcium 2012, 53:55-62.
193. Nomikos M., Yu Y., Elgmati K., Theodoridou M., Campbell K., Vassilakopoulou V., Zikos C., Livaniou E., Amso N., Nounesis G., Swann K., Lai F.A. Phospholipase Czeta rescues failed oocyte activation in a prototype of male factor infertility. Fertility and Sterility 2013, 99:76-85.
194. Swann K., Lai F.A. PLCzeta and the initiation of Ca(2+) oscillations in fertilizing mammalian eggs. Cell Calcium 2013, 53:55-62.