In sexual reproduction, two gamete cells (i.e., egg and sperm) fuse (fertilization) to create a newborn with a genetic identity distinct from those of the parents. In the course of these developmental processes, a variety of signal transduction events occur simultaneously in each of the two gametes, as well as in the fertilized egg/zygote/early embryo. In particular, a growing body of knowledge suggests that the tyrosine kinase Src and/or other protein-tyrosine kinases are important elements that facilitate successful implementation of the aforementioned processes in many animal species. In this paper, we summarize recent findings on the roles of protein-tyrosine phosphorylation in many sperm-related processes (from spermatogenesis to epididymal maturation, capacitation, acrosomal exocytosis, and fertilization). 1. Introduction Protein-tyrosine kinase (PTK) activity and tyrosine phosphorylation of cellular protein were initially discovered by Hunter and colleagues [1–3]; they analyzed the protein kinase activity associated with the protein complex of polyoma virus middle T antigen and viral Src gene product, a cellular counterpart of which is the cellular Src protein. At that time, phosphorylation events on amino acids other than tyrosine (i.e., serine and threonine residues) were already known as posttranslational modifications of physiological importance. However, the discovery of tyrosine phosphorylation for the first time opened a window to understand the relationship between protein phosphorylation (including serine/threonine phosphorylation) and malignant cell transformation (e.g., development of cancer) [4]. In addition, a growing body of evidence has demonstrated that tyrosine phosphorylation catalyzed by cellular Src and other PTKs expressed in normal cells and tissues regulates a variety of cellular functions such as developmental processes, disorder of normal cell functions, immunological responses, neuronal differentiation and transmission, pathological infection, and senescence. Thus, protein-tyrosine phosphorylation has emerged as a signal transduction mechanism of fundamental importance in all eukaryotic cells and, in some cases, prokaryotic cell behavior [5–7]. In the sexual reproduction system, two different kinds of gamete cell: egg and sperm, interact and fuse with each other to accomplish fertilization that gives rise to a newborn [8]. In this fundamental biological event, both egg and sperm undergo a number of biochemical and cell biological reactions that culminate in successful embryogenesis and early development. Especially in
References
[1]
T. Hunter, “Tyrosine phosphorylation: thirty years and counting,” Current Opinion in Cell Biology, vol. 21, no. 2, pp. 140–146, 2009.
[2]
T. Hunter and B. M. Sefton, “Transforming gene product of Rous sarcoma virus phosphorylates tyrosine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 77, no. 3 I, pp. 1311–1315, 1980.
[3]
W. Eckhart, M. A. Hutchinson, and T. Hunter, “An activity phosphorylating tyrosine in polyoma T antigen immunoprecipitates,” Cell, vol. 18, no. 4, pp. 925–933, 1979.
[4]
J. M. Bishop, “Molecular themes in oncogenesis,” Cell, vol. 64, no. 2, pp. 235–248, 1991.
[5]
C. Grangeasse, A. J. Cozzone, J. Deutscher, and I. Mijakovic, “Tyrosine phosphorylation: an emerging regulatory device of bacterial physiology,” Trends in Biochemical Sciences, vol. 32, no. 2, pp. 86–94, 2007.
[6]
D. Pincus, I. Letunic, P. Bork, and W. A. Lim, “Evolution of the phospho-tyrosine signaling machinery in premetazoan lineages,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 28, pp. 9680–9684, 2008.
[7]
S. M. Thomas and J. S. Brugge, “Cellular functions regulated by SRC family kinases,” Annual Review of Cell and Developmental Biology, vol. 13, pp. 513–609, 1997.
[8]
R. Yanagimachi, “Mammalian fertilization,” in The Physiology of Reproduction, E. Knobil and J. D. Neil, Eds., pp. 189–317, Raven Press, New York, NY, USA, 1994.
[9]
G. Wei and A. P. Mahowald, “The germline: familiar and newly uncovered properties,” Annual Review of Genetics, vol. 28, pp. 309–324, 1994.
[10]
A. Darszon, T. Nishigaki, C. Beltran, and C. L. Trevi？o, “Calcium channels in the development, maturation, and function of spermatozoa,” Physiological Reviews, vol. 91, no. 4, pp. 1305–1355, 2011.
[11]
K. Toshimori, “Dynamics of the mammalian sperm head: modifications and maturation events from spermatogenesis to egg activation,” Advances in Anatomy, Embryology, and Cell Biology, vol. 204, pp. 5–94, 2009.
[12]
E. Voronina and G. M. Wessel, “The regulation of oocyte maturation,” Current Topics in Developmental Biology, vol. 58, pp. 53–110, 2003.
[13]
B. Ciapa and S. Chiri, “Egg activation: upstream of the fertilization calcium signal,” Biology of the Cell, vol. 92, no. 3-4, pp. 215–233, 2000.
[14]
A. M. Hasan, Y. Fukami, and K. I. Sato, “Gamete membrane microdomains and their associated molecules in fertilization signaling,” Molecular Reproduction and Development, vol. 78, no. 10-11, pp. 814–830, 2011.
[15]
W. H. Kinsey, “Tyrosine kinase signaling at fertilization,” Biochemical and Biophysical Research Communications, vol. 240, no. 3, pp. 519–522, 1997.
[16]
L. K. Mcginnis, D. J. Carroll, and W. H. Kinsey, “Protein tyrosine kinase signaling during oocyte maturation and fertilization,” Molecular Reproduction and Development, vol. 78, no. 10-11, pp. 831–845, 2011.
[17]
L. L. Runft, L. A. Jaffe, and L. M. Mehlmann, “Egg activation at fertilization: where it all begins,” Developmental Biology, vol. 245, no. 2, pp. 237–254, 2002.
[18]
K. I. Sato, T. Iwasaki, S. Hirahara, Y. Nishihira, and Y. Fukami, “Molecular dissection of egg fertilization signaling with the aid of tyrosine kinase-specific inhibitor and activator strategies,” Biochimica et Biophysica Acta, vol. 1697, no. 1-2, pp. 103–121, 2004.
[19]
M. Whitaker, “Calcium at fertilization and in early development,” Physiological Reviews, vol. 86, no. 1, pp. 25–88, 2006.
[20]
M. A. Handel, “Genetic control of spermatogenesis in mice,” Results and Problems in Cell Differentiation, vol. 15, pp. 1–62, 1987.
[21]
D. G. de Rooij, “Stem cells in the testis,” International Journal of Experimental Pathology, vol. 79, no. 2, pp. 67–80, 1998.
[22]
G. S. Roeder, “Meiotic chromosomes: it takes two to tango,” Genes and Development, vol. 11, no. 20, pp. 2600–2621, 1997.
[23]
K. Toshimori, “Biology of spermatozoa maturation: an overview with an introduction to this issue,” Microscopy Research and Technique, vol. 61, no. 1, pp. 1–6, 2003.
[24]
E. M. Eddy, K. Toshimori, and D. A. O'Brien, “Fibrous sheath of mammalian spermatozoa,” Microscopy Research and Technique, vol. 61, no. 1, pp. 103–115, 2003.
[25]
K. Steger, “Transcriptional and translational regulation of gene expression in haploid spermatids,” Anatomy and Embryology, vol. 199, no. 6, pp. 471–487, 1999.
[26]
E. M. Eddy, “Male germ cell gene expression,” Recent Progress in Hormone Research, vol. 57, pp. 103–128, 2002.
[27]
B. Senthilkumaran, “Recent advances in meiotic maturation and ovulation: comparing mammals and pisces,” Frontiers in Bioscience, vol. 16, no. 5, pp. 1898–1914, 2011.
[28]
M. Yamashita, “Molecular mechanisms of meiotic maturation and arrest in fish and amphibian oocytes,” Seminars in Cell and Developmental Biology, vol. 9, no. 5, pp. 569–579, 1998.
[29]
J. Deng, L. Carbajal, K. Evaul, M. Rasar, M. Jamnongjit, and S. R. Hammes, “Nongenomic steroid-triggered oocyte maturation: of mice and frogs,” Steroids, vol. 74, no. 7, pp. 595–601, 2009.
[30]
G. A. Cornwall, “New insights into epididymal biology and function,” Human Reproduction Update, vol. 15, no. 2, pp. 213–227, 2009.
[31]
X. Deng, K. Czymmek, and P. A. Martin-DeLeon, “Biochemical maturation of Spam1 (PH-20) during epididymal transit of mouse sperm involves modifications of N-linked oligosaccharides,” Molecular Reproduction and Development, vol. 52, no. 2, pp. 196–206, 1999.
[32]
G. Morin, C. Lalancette, R. Sullivan, and P. Leclerc, “Identification of the bull sperm p80 protein as a PH-20 ortholog and its modification during the epididymal transit,” Molecular Reproduction and Development, vol. 71, no. 4, pp. 523–534, 2005.
[33]
M. Nikolopoulou, D. A. Soucek, and J. C. Vary, “Changes in the lipid content of boar sperm plasma membranes during epididymal maturation,” Biochimica et Biophysica Acta, vol. 815, no. 3, pp. 486–498, 1985.
[34]
E. O. Hernández-González, C. L. Trevi？o, L. E. Castellano et al., “Involvement of cystic fibrosis transmembrane conductance regulator in mouse sperm capacitation,” Journal of Biological Chemistry, vol. 282, no. 33, pp. 24397–24406, 2007.
[35]
D. R. White and R. J. Aitken, “Influence of epididymal maturation on cyclic AMP levels in hamster spermatozoa,” International Journal of Andrology, vol. 12, no. 1, pp. 29–43, 1989.
[36]
R. Yanagimachi, Y. D. Noda, M. Fujimoto, and G. L. Nicolson, “The distribution of negative surface charges on mammalian spermatozoa,” American Journal of Anatomy, vol. 135, no. 4, pp. 497–519, 1972.
[37]
B. Lewis and R. J. Aitken, “Impact of epididymal maturation on the tyrosine phosphorylation patterns exhibited by rat spermatozoa,” Biology of Reproduction, vol. 64, no. 5, pp. 1545–1556.
[38]
C. R. Austin, “Observations on the penetration of the sperm in the mammalian egg,” Australian Journal of Scientific Research B, vol. 4, no. 4, pp. 581–596, 1951.
[39]
M. C. Chang, “Fertilizing capacity of spermatozoa deposited into the fallopian tubes,” Nature, vol. 168, no. 4277, pp. 697–698, 1951.
[40]
R. Yanagimachi and M. C. Chang, “Fertilization of hamster eggs in vitro,” Nature, vol. 200, no. 4903, pp. 281–282, 1963.
[41]
E. O. Hernández-González, J. Sosnik, J. Edwards et al., “Sodium and epithelial sodium channels participate in the regulation of the capacitation-associated hyperpolarization in mouse sperm,” Journal of Biological Chemistry, vol. 281, no. 9, pp. 5623–5633, 2006.
[42]
E. Arcelay, A. M. Salicioni, E. Wertheimer, and P. E. Visconti, “Identification of proteins undergoing tyrosine phosphorylation during mouse sperm capacitation,” International Journal of Developmental Biology, vol. 52, no. 5-6, pp. 463–472, 2008.
[43]
M. Eisenbach and L. C. Giojalas, “Sperm guidance in mammals—an unpaved road to the egg,” Nature Reviews Molecular Cell Biology, vol. 7, no. 4, pp. 276–285, 2006.
[44]
M. Yoshida, N. Kawano, and K. Yoshida, “Control of sperm motility and fertility: diverse factors and common mechanisms,” Cellular and Molecular Life Sciences, vol. 65, no. 21, pp. 3446–3457, 2008.
[45]
L. A. Burnett, X. Xiang, A. L. Bieber, and D. E. Chandler, “Crisp proteins and sperm chemotaxis: discovery in amphibians and explorations in mammals,” International Journal of Developmental Biology, vol. 52, no. 5-6, pp. 489–501, 2008.
[46]
M. Jin, E. Fujiwara, Y. Kakiuchi et al., “Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 12, pp. 4892–4896, 2011.
[47]
N. Inoue, M. Ikawa, A. Isotani, and M. Okabe, “The immunoglobulin superfamily protein Izumo is required for sperm to fuse with eggs,” Nature, vol. 434, no. 7030, pp. 234–238, 2005.
[48]
K. Kaji, S. Oda, T. Shikano et al., “The gamete fusion process is defective in eggs of Cd9-deficient mice,” Nature Genetics, vol. 24, no. 3, pp. 279–282, 2000.
[49]
C. Boucheix, “Severely reduced female fertility in CD9-deficient mice,” Science, vol. 287, no. 5451, pp. 319–321, 2000.
[50]
K. Miyado, G. Yamada, S. Yamada et al., “Requirement of CD9 on the egg plasma membrane for fertilization,” Science, vol. 287, no. 5451, pp. 321–324, 2000.
[51]
T. Ducibella and R. Fissore, “The roles of Ca2+, downstream protein kinases, and oscillatory signaling in regulating fertilization and the activation of development,” Developmental Biology, vol. 315, no. 2, pp. 257–279, 2008.
[52]
S. A. Stricker, “Comparative biology of calcium signaling during fertilization and egg activation in animals,” Developmental Biology, vol. 211, no. 2, pp. 157–176, 1999.
[53]
M. Nomikos, K. Swann, and F. A. Lai, “Starting a new life: sperm PLC-zeta mobilizes the Ca 2+ signal that induces egg activation and embryo development: an essential phospholipase C with implications for male infertility,” BioEssays, vol. 34, no. 2, pp. 126–134, 2012.
[54]
Y. Harada, T. Matsumoto, S. Hirahara et al., “Characterization of a sperm factor for egg activation at fertilization of the newt Cynops pyrrhogaster,” Developmental Biology, vol. 306, no. 2, pp. 797–808, 2007.
[55]
M. A. Baker, N. D. Smith, L. Hetherington et al., “Label-free quantitation of phosphopeptide changes during rat sperm capacitation,” Journal of Proteome Research, vol. 9, no. 2, pp. 718–729, 2010.
[56]
M. A. Baker, G. Reeves, L. Hetherington, and R. J. Aitken, “Analysis of proteomic changes associated with sperm capacitation through the combined use of IPG-strip prefractionation followed by RP chromatography LC-MS/ MS analysis,” Proteomics, vol. 10, no. 3, pp. 482–495, 2010.
[57]
M. D. Piatt, A. M. Salicioni, D. F. Hunt, and P. E. Visconti, “Use of differential isotopic labeling and mass spectrometry to analyze capacitation-associated changes in the phosphorylation status of mouse sperm proteins,” Journal of Proteome Research, vol. 8, no. 3, pp. 1431–1440, 2009.
[58]
S. Goupil, S. La Salle, J. M. Trasler, L. J. Bordeleau, and P. Leclerc, “Developmental expression of Src-related tyrosine kinases in the mouse testis,” Journal of Andrology, vol. 32, no. 1, pp. 95–110, 2011.
[59]
C. Lawson, S. Goupil, and P. Leclerc, “Increased activity of the human sperm tyrosine kinase SRC by the cAMP-dependent pathway in the presence of calcium,” Biology of Reproduction, vol. 79, no. 4, pp. 657–666, 2008.
[60]
S. Lev, Y. Yarden, and D. Givol, “Dimerization and activation of the kit receptor by monovalent and bivalent binding of the stem cell factor,” Journal of Biological Chemistry, vol. 267, no. 22, pp. 15970–15977, 1992.
[61]
I. Godin, R. Deed, J. Cooke, K. Zsebo, M. Dexter, and C. C. Wylie, “Effects of the steel gene product on mouse primordial germ cells in culture,” Nature, vol. 352, no. 6338, pp. 807–809, 1991.
[62]
D. Farini, G. La Sala, M. Tedesco, and M. De Felici, “Chemoattractant action and molecular signaling pathways of Kit ligand on mouse primordial germ cells,” Developmental Biology, vol. 306, no. 2, pp. 572–583, 2007.
[63]
K. Yoshinaga, S. Nishikawa, M. Ogawa et al., “Role of c-kit in mouse spermatogenesis: identification of spermatogonia as a specific site of c-kit expression and function,” Development, vol. 113, no. 2, pp. 689–699, 1991.
[64]
J. M. Oatley, M. R. Avarbock, and R. L. Brinster, “Glial cell line-derived neurotrophic factor regulation of genes essential for self-renewal of mouse spermatogonial stem cells is dependent on Src family kinase signaling,” Journal of Biological Chemistry, vol. 282, no. 35, pp. 25842–25851, 2007.
[65]
H. Morimoto, M. Kanatsu-Shinohara, S. Takashima et al., “Phenotypic plasticity of mouse spermatogonial stem cells,” PLoS ONE, vol. 4, no. 11, Article ID e7909, 2009.
[66]
A. Navon, Y. Schwarz, B. Hazan, Y. Kassir, and U. Nir, “Meiosis-dependent tyrosine phosphorylation of a yeast protein related to the mouse p51(ferT),” Molecular and General Genetics, vol. 244, no. 2, pp. 160–167, 1994.
[67]
S. Vincent, D. Segretain, S. Nishikawa et al., “Stage-specific expression of the Kit receptor and its ligand (KL) during male gametogenesis in the mouse: a Kit-KL interaction critical for meiosis,” Development, vol. 125, no. 22, pp. 4585–4593, 1998.
[68]
M. Pellegrini, D. Filipponi, M. Gori et al., “ATRA and KL promote differentiation toward the meiotic program of male germ cells,” Cell Cycle, vol. 7, no. 24, pp. 3878–3888, 2008.
[69]
C. Lalancette, L. J. Bordeleau, R. L. Faure, and P. Leclerc, “Bull testicular haploid germ cells express a messenger encoding for a truncated form of the protein tyrosine kinase HCK,” Molecular Reproduction and Development, vol. 73, no. 4, pp. 520–530, 2006.
[70]
A. L. Kierszenbaum, E. Rivkin, A. Talmor-Cohen, R. Shalgi, and L. L. Tres, “Expression of full-length and truncated fyn tyrosine kinase transcripts and encoded proteins during spermatogenesis and localization during acrosome biogenesis and fertilization,” Molecular Reproduction and Development, vol. 76, no. 9, pp. 832–843, 2009.
[71]
L. J. Bordeleau and P. Leclerc, “Expression of hck-tr, a truncated form of the src-related tyrosine kinase hck, in bovine spermatozoa and testis,” Molecular Reproduction and Development, vol. 75, no. 5, pp. 828–837, 2008.
[72]
C. Albanesi, R. Geremia, M. Giorgio, S. Dolci, C. Sette, and P. Rossi, “A cell- and developmental stage-specific promoter drives the expression of a truncated c-kit protein during mouse spermatid elongation,” Development, vol. 122, no. 4, pp. 1291–1302, 1996.
[73]
P. Rossi, G. Marziali, C. Albanesi, A. Charlesworth, R. Geremia, and V. Sorrentino, “A novel c-kit transcript, potentially encoding a truncated receptor, originates within a kit gene intron in mouse spermatids,” Developmental Biology, vol. 152, no. 1, pp. 203–207, 1992.
[74]
M. P. Paronetto, J. P. Venables, D. J. Elliott, R. Geremia, P. Rossi, and C. Sette, “Tr-kit promotes the formation of a multimolecular complex composed by Fyn, PLCγ1 and Sam68,” Oncogene, vol. 22, no. 54, pp. 8707–8715, 2003.
[75]
B. Muciaccia, C. Sette, M. P. Paronetto et al., “Expression of a truncated form of KIT tyrosine kinase in human spermatozoa correlates with sperm DNA integrity,” Human Reproduction, vol. 25, no. 9, pp. 2188–2202, 2010.
[76]
M. K. Y. Siu, D. D. Mruk, W. M. Lee, and C. Y. Cheng, “Adhering junction dynamics in the testis are regulated by an interplay of β1-integrin and focal adhesion complex-associated proteins,” Endocrinology, vol. 144, no. 5, pp. 2141–2163, 2003.
[77]
Y. M. Chen, N. P. Y. Lee, D. D. Mruk, W. M. Lee, and C. Y. Cheng, “Fer kinase/FerT and adherens junction dynamics in the testis: an in vitro and in vivo study,” Biology of Reproduction, vol. 69, no. 2, pp. 656–672, 2003.
[78]
M. Maekawa, Y. Toyama, M. Yasuda, T. Yagi, and S. Yuasa, “Fyn tyrosine kinase in sertoli cells is involved in mouse spermatogenesis,” Biology of Reproduction, vol. 66, no. 1, pp. 211–221, 2002.
[79]
M. K. Y. Siu, C. H. Wong, W. M. Lee, and C. Y. Cheng, “Sertoli-germ cell anchoring junction dynamics in the testis are regulated by an interplay of lipid and protein kinases,” Journal of Biological Chemistry, vol. 280, no. 26, pp. 25029–25047, 2005.
[80]
M. Rassoulzadegan, V. Paquis-Flucklinger, B. Bertino et al., “Transmeiotic differentiation of male germ cells in culture,” Cell, vol. 75, no. 5, pp. 997–1006, 1993.
[81]
M. C. Hofmann, R. A. Hess, E. Goldberg, and J. L. Millán, “Immortalized germ cells undergo meiosis in vitro,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 12, pp. 5533–5537, 1994.
[82]
T. Sato, K. Katagiri, A. Gohbara et al., “In vitro production of functional sperm in cultured neonatal mouse testes,” Nature, vol. 471, no. 7339, pp. 504–507, 2011.
[83]
K. Miki, W. Qu, E. H. Goulding et al., “Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 47, pp. 16501–16506, 2004.
[84]
M. Nakamura, S. Okinaga, and K. Arai, “Metabolism of round spermatids: evidence that lactate is preferred substrate,” The American journal of physiology, vol. 247, no. 2, pp. E234–E242, 1984.
[85]
M. Nakamura, S. Okinaga, and K. Arai, “Metabolism of pachytene primary spermatocytes from rat testes: pyruvate maintenance of adenosine triphosphate level,” Biology of Reproduction, vol. 30, no. 5, pp. 1187–1197, 1984.
[86]
B. T. Storey and F. J. Kayne, “Energy metabolism of spermatozoa. V. The Embden Myerhof pathway of glycolysis: activities of pathway enzymes in hypotonically treated rabbit epididymal spermatozoa,” Fertility and Sterility, vol. 26, no. 12, pp. 1257–1265, 1975.
[87]
H. I. Calvin and J. M. Bedford, “Formation of disulphide bonds in the nucleus and accessory structures of mammalian spermatozoa during maturation in the epididymis,” Journal of reproduction and fertility. Supplement, vol. 13, supplement 13, pp. 65–75, 1971.
[88]
G. A. Cornwall, D. Vindivich, S. Tillman, and T. S. Chang, “The effect of sulfhydryl oxidation on the morphology of immature hamster epididymal spermatozoa induced to acquire motility in vitro,” Biology of Reproduction, vol. 39, no. 1, pp. 141–155, 1988.
[89]
J. Seligman, Y. Zipser, and N. S. Kosower, “Tyrosine phosphorylation, thiol status, and protein tyrosine phosphatase in rat epididymal spermatozoa,” Biology of Reproduction, vol. 71, no. 3, pp. 1009–1015, 2004.
[90]
K. U. Devi, M. B. Ahmad, and S. Shivaji, “A maturation-related differential phosphorylation of the plasma membrane proteins of the epididymal spermatozoa of the hamster by endogenous protein kinases,” Molecular Reproduction and Development, vol. 47, no. 3, pp. 341–350, 1997.
[91]
A. Fàbrega, M. Puigmulé, M. Yeste, I. Casas, S. Bonet, and E. Pinart, “Impact of epididymal maturation, ejaculation and in vitro capacitation on tyrosine phosphorylation patterns exhibited of boar (Sus domesticus) spermatozoa,” Theriogenology, vol. 76, no. 7, pp. 1356–1366, 2011.
[92]
R. Jones, P. S. James, D. Oxley, J. Coadwell, F. Suzuki-Toyota, and E. A. Howes, “The equatorial subsegment in mammalian spermatozoa is enriched in tyrosine phosphorylated proteins,” Biology of Reproduction, vol. 79, no. 3, pp. 421–431, 2008.
[93]
B. Lewis and R. J. Aitken, “A redox-regulated tyrosine phosphorylation cascade in rat spermatozoa,” Journal of Andrology, vol. 22, no. 4, pp. 611–622, 2001.
[94]
M. Lin, H. L. Yun, W. Xu, M. A. Baker, and R. J. Aitken, “Ontogeny of tyrosine phosphorylation-signaling pathways during spermatogenesis and epididymal maturation in the mouse,” Biology of Reproduction, vol. 75, no. 4, pp. 588–597, 2006.
[95]
H. Ecroyd, K. L. Asquith, R. C. Jones, and R. J. Aitken, “The development of signal transduction pathways during epididymal maturation is calcium dependent,” Developmental Biology, vol. 268, no. 1, pp. 53–63, 2004.
[96]
M. A. Baker, R. Witherdin, L. Hetherington, K. Cunningham-Smith, and R. J. Aitken, “Identification of post-translational modifications that occur during sperm maturation using difference in two-dimensional gel electrophoresis,” Proteomics, vol. 5, no. 4, pp. 1003–1012, 2005.
[97]
M. A. Baker, N. D. Smith, L. Hetherington, M. Pelzing, M. R. Condina, and R. J. Aitken, “Use of titanium dioxide to find phosphopeptide and total protein changes during epididymal sperm maturation,” Journal of Proteome Research, vol. 10, no. 3, pp. 1004–1017, 2011.
[98]
E. Sonnenberg-Riethmacher, B. Walter, D. Riethmacher, S. G？decke, and C. Birchmeier, “The c-ros tyrosine kinase receptor controls regionalization and differentiation of epithelial cells in the epididymis,” Genes and Development, vol. 10, no. 10, pp. 1184–1193, 1996.
[99]
H. Keilhack, M. Müller, S. A. B？hmer et al., “Negative regulation of Ros receptor tyrosine kinase signaling: an epithelial function of the SH2 domain protein tyrosine phosphatase SHP-1,” Journal of Cell Biology, vol. 152, no. 2, pp. 325–334, 2001.
[100]
P. Syntin, F. Dacheux, X. Druart, J. L. Gatti, N. Okamura, and J. L. Dacheux, “Characterization and identification of proteins secreted in the various regions of the adult boar epididymis,” Biology of Reproduction, vol. 55, no. 5, pp. 956–974, 1996.
[101]
J. L. Dacheux, M. Belghazi, Y. Lanson, and F. Dacheux, “Human epididymal secretome and proteome,” Molecular and Cellular Endocrinology, vol. 250, no. 1-2, pp. 36–42, 2006.
[102]
D. Krapf, Y. Chun Ruan, E. V. Wertheimer et al., “cSrc is necessary for epididymal development and is incorporated into sperm during epididymal transit,” Developmental Biology, vol. 369, no. 1, pp. 43–53, 2012.
[103]
A. E. Duncan and L. R. Fraser, “Cyclic AMP-dependent phosphorylation of epididymal mouse sperm proteins during capacitation in vitro: identification of an M(r) 95, 000 phosphotyrosine-containing protein,” Journal of Reproduction and Fertility, vol. 97, no. 1, pp. 287–299, 1993.
[104]
P. E. Visconti, J. L. Bailey, G. D. Moore, D. Pan, P. Olds-Clarke, and G. S. Kopf, “Capacitation of mouse spermatozoa. 1. Correlation between the capacitation state and protein tyrosine phosphorylation,” Development, vol. 121, no. 4, pp. 1129–1137, 1995.
[105]
P. E. Visconti, G. D. Moore, J. L. Bailey et al., “Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway,” Development, vol. 121, no. 4, pp. 1139–1150, 1995.
[106]
E. Baldi, M. Luconi, L. Bonaccorsi, C. Krausz, and G. Forti, “Human sperm activation during capacitation and acrosome reaction: role of calcium, protein phosphorylation and lipid remodelling pathways,” Frontiers in Bioscience, vol. 1, pp. d189–d205, 1996.
[107]
B. S. Pukazhenthi, D. E. Wildt, M. A. Ottinger, and J. Howard, “Compromised sperm protein phosphorylation after capacitation, swim-up, and zona pellucida exposure in teratospermic domestic cats,” Journal of Andrology, vol. 17, no. 4, pp. 409–419, 1996.
[108]
B. S. Pukazhenthi, J. A. Long, D. E. Wildt, M. A. Ottinger, D. L. Armstrong, and J. Howard, “Regulation of sperm function by protein tyrosine phosphorylation in diverse wild felid species,” Journal of Andrology, vol. 19, no. 6, pp. 675–685, 1998.
[109]
A. Carrera, J. Moos, X. P. Ning et al., “Regulation of protein tyrosine phosphorylation in human sperm by a calcium/calmodulin-dependent mechanism: identification of A kinase anchor proteins as major substrates for tyrosine phosphorylation,” Developmental Biology, vol. 180, no. 1, pp. 284–296, 1996.
[110]
A. Mandal, S. Naaby-Hansen, M. J. Wolkowicz et al., “FSP95, a testis-specific 95-kilodalton fibrous sheath antigen that undergoes tyrosine phosphorylation in capacitated human spermatozoa,” Biology of Reproduction, vol. 61, no. 5, pp. 1184–1197, 1999.
[111]
P. E. Visconti, L. R. Johnson, M. Oyaski et al., “Regulation, localization, and anchoring of protein kinase a subunits during mouse sperm capacitation,” Developmental Biology, vol. 192, no. 2, pp. 351–363, 1997.
[112]
R. K. Naz, “c-abl proto-oncoprotein is expressed and tyrosine phosphorylated in human sperm cell,” Molecular Reproduction and Development, vol. 51, no. 2, pp. 210–217, 1998.
[113]
P. E. Visconti, X. Ning, M. W. Fornés et al., “Cholesterol efflux-mediated signal transduction in mammalian sperm: cholesterol release signals an increase in protein tyrosine phosphorylation during mouse sperm capacitation,” Developmental Biology, vol. 214, no. 2, pp. 429–443, 1999.
[114]
P. E. Visconti, H. Galantino-Homer, X. Ning et al., “Cholesterol efflux-mediated signal transduction in mammalian sperm: β-cyclodextrins initiate transmembrane signaling leading to an increase in protein tyrosine phosphorylation and capacitation,” Journal of Biological Chemistry, vol. 274, no. 5, pp. 3235–3242, 1999.
[115]
J. E. Osheroff, P. E. Visconti, J. P. Valenzuela, A. J. Travis, J. Alvarez, and G. S. Kopf, “Regulation of human sperm capacitation by a cholesterol efflux-stimulated signal transduction pathway leading to protein kinase A-mediated up-regulation of protein tyrosine phosphorylation,” Molecular Human Reproduction, vol. 5, no. 11, pp. 1017–1026, 1999.
[116]
Y. Si and P. Olds-Clarke, “Evidence for the involvement of calmodulin in mouse sperm capacitation,” Biology of Reproduction, vol. 62, no. 5, pp. 1231–1239, 2000.
[117]
H. T. Zeng and D. R. P. Tulsiani, “Calmodulin antagonists differentially affect capacitation-associated protein tyrosine phosphorylation of mouse sperm components,” Journal of Cell Science, vol. 116, no. 10, pp. 1981–1989, 2003.
[118]
Y. H. Huang, S. T. Chu, and Y. H. Chen, “A seminal vesicle autoantigen of mouse is able to suppress sperm capacitation-related events stimulated by serum albumin,” Biology of Reproduction, vol. 63, no. 5, pp. 1562–1566, 2000.
[119]
Y. H. Huang, S. P. Kuo, M. H. Lin et al., “Signals of seminal vesicle autoantigen suppresses bovine serum albumin-induced capacitation in mouse sperm,” Biochemical and Biophysical Research Communications, vol. 338, no. 3, pp. 1564–1571, 2005.
[120]
S. A. Adeoya-Osiguwa and L. R. Fraser, “Fertilization promoting peptide and adenosine, acting as first messengers, regulate cAMP production and consequent protein tyrosine phosphorylation in a capacitation-dependent manner,” Molecular Reproduction and Development, vol. 57, no. 4, pp. 384–392, 2000.
[121]
H. Funahashi, A. Asano, T. Fujiwara, T. Nagai, K. Niwa, and L. R. Fraser, “Both fertilization promoting peptide and adenosine stimulate capacitation but inhibit spontaneous acrosome loss in ejaculated boar spermatozoa in vitro,” Molecular Reproduction and Development, vol. 55, no. 1, pp. 117–124, 2000.
[122]
F. Urner, G. Leppens-Luisier, and D. Sakkas, “Protein tyrosine phosphorylation in sperm during gamete interaction in the mouse: the influence of glucose,” Biology of Reproduction, vol. 64, no. 5, pp. 1350–1357, 2001.
[123]
I. A. Demarco, F. Espinosa, J. Edwards et al., “Involvement of a Na+/HCO？3 cotransporter in mouse sperm capacitation,” Journal of Biological Chemistry, vol. 278, no. 9, pp. 7001–7009, 2003.
[124]
E. Brener, S. Rubinstein, G. Cohen, K. Shternall, J. Rivlin, and H. Breitbart, “Remodeling of the actin cytoskeleton during mammalian sperm capacitation and acrosome reaction,” Biology of Reproduction, vol. 68, no. 3, pp. 837–845, 2003.
[125]
M. G. Buffone, T. W. Ijiri, W. Cao, T. Merdiushev, H. K. Aghajanian, and G. L. Gerton, “Heads or tails? Structural events and molecular mechanisms that promote mammalian sperm acrosomal exocytosis and motility,” Molecular Reproduction and Development, vol. 79, no. 1, pp. 4–18, 2012.
[126]
H. W. Ecroyd, R. C. Jones, and R. J. Aitken, “Endogenous redox activity in mouse spermatozoa and its role in regulating the tyrosine phosphorylation events associated with sperm capacitation,” Biology of Reproduction, vol. 69, no. 1, pp. 347–354, 2003.
[127]
R. J. Aitken and M. A. Baker, “Oxidative stress and male reproductive biology,” Reproduction, Fertility and Development, vol. 16, no. 5, pp. 581–588, 2004.
[128]
H. Ecroyd, R. C. Jones, and R. J. Aitken, “Tyrosine phosphorylation of HSP-90 during mammalian sperm capacitation,” Biology of Reproduction, vol. 69, no. 6, pp. 1801–1807, 2003.
[129]
K. L. Asquith, R. M. Baleato, E. A. McLaughlin, B. Nixon, and R. J. Aitken, “Tyrosine phosphorylation activates surface chaperones facilitating sperm-zona recognition,” Journal of Cell Science, vol. 117, pp. 3645–3657, 2004.
[130]
L. A. Mitchell, B. Nixon, and R. J. Aitken, “Analysis of chaperone proteins associated with human spermatozoa during capacitation,” Molecular Human Reproduction, vol. 13, no. 9, pp. 605–613, 2007.
[131]
T. A. Quill, S. A. Sugden, K. L. Rossi, L. K. Doolittle, R. E. Hammer, and D. L. Garbers, “Hyperactivated sperm motility driven by CatSper2 is required for fertilization,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 25, pp. 14869–14874, 2003.
[132]
M. A. Baker, L. Hetherington, H. Ecroyd, S. D. Roman, and R. J. Aitken, “Analysis of the mechanism by which calcium negatively regulates the tyrosine phosphorylation cascade associated with sperm capacitation,” Journal of Cell Science, vol. 117, pp. 211–222, 2004.
[133]
C. Rodeheffer and B. D. Shur, “Sperm from β1,4-galactosyltransferase l-null mice exhibit precocious capacitation,” Development, vol. 131, no. 3, pp. 491–501, 2004.
[134]
S. Mededovic and L. R. Fraser, “Angiotensin II stimulates cAMP production and protein tyrosine phosphorylation in mouse spermatozoa,” Reproduction, vol. 127, no. 5, pp. 601–612, 2004.
[135]
K. C. Hess, B. H. Jones, B. Marquez et al., “The “soluble” adenylyl cyclase in sperm mediates multiple signaling events required for fertilization,” Developmental Cell, vol. 9, no. 2, pp. 249–259, 2005.
[136]
F. Xie, M. A. Garcia, A. E. Carlson et al., “Soluble adenylyl cyclase (sAC) is indispensable for sperm function and fertilization,” Developmental Biology, vol. 296, no. 2, pp. 353–362, 2006.
[137]
B. Nixon, D. A. MacIntyre, L. A. Mitchell, G. M. Gibbs, M. O'Bryan, and R. J. Aitken, “The identification of mouse sperm-surface-associated proteins and characterization of their ability to act as decapacitation factors,” Biology of Reproduction, vol. 74, no. 2, pp. 275–287, 2006.
[138]
J. C. Thundathil, M. Anzar, and M. M. Buhr, “Na+/K+ ATPase as a signaling molecule during bovine sperm capacitation,” Biology of Reproduction, vol. 75, no. 3, pp. 308–317, 2006.
[139]
J. B. Tang and Y. H. Chen, “Identification of a tyrosine-phosphorylated CCCTC-binding nuclear factor in capacitated mouse spermatozoa,” Proteomics, vol. 6, no. 17, pp. 4800–4807, 2006.
[140]
N. Kawano and M. Yoshida, “Semen-coagulating protein, SVS2, in mouse seminal plasma controls sperm fertility,” Biology of Reproduction, vol. 76, no. 3, pp. 353–361, 2007.
[141]
W. Cao, H. K. Aghajanian, L. A. Haig-Ladewig, and G. L. Gerton, “Sorbitol can fuel mouse sperm motility and protein tyrosine phosphorylation via sorbitol dehydrogenase,” Biology of Reproduction, vol. 80, no. 1, pp. 124–133, 2009.
[142]
E. V. Wertheimer, A. M. Salicioni, W. Liu et al., “Chloride is essential for capacitation and for the capacitation-associated increase in tyrosine phosphorylation,” Journal of Biological Chemistry, vol. 283, no. 51, pp. 35539–35550, 2008.
[143]
V. Kota, V. M. Dhople, and S. Shivaji, “Tyrosine phosphoproteome of hamster spermatozoa: role of glycerol-3-phosphate dehydrogenase 2 in sperm capacitation,” Proteomics, vol. 9, no. 7, pp. 1809–1826, 2009.
[144]
V. Kota, P. Rai, J. M. Weitzel, R. Middendorff, S. S. Bhande, and S. Shivaji, “Role of glycerol-3-phosphate dehydrogenase 2 in mouse sperm capacitation,” Molecular Reproduction and Development, vol. 77, no. 9, pp. 773–783, 2010.
[145]
C. Gyamera-Acheampong, J. Vasilescu, D. Figeys, and M. Mbikay, “PCSK4-null sperm display enhanced protein tyrosine phosphorylation and ADAM2 proteolytic processing during in vitro capacitation,” Fertility and Sterility, vol. 93, no. 4, pp. 1112–1123, 2010.
[146]
B. Nixon, A. Bielanowicz, A. L. Anderson et al., “Elucidation of the signaling pathways that underpin capacitation-associated surface phosphotyrosine expression in mouse spermatozoa,” Journal of Cellular Physiology, vol. 224, no. 1, pp. 71–83, 2010.
[147]
M. Shimada, Y. Yanai, T. Okazaki et al., “Hyaluronan fragments generated by sperm-secreted hyaluronidase stimulate cytokine/chemokine production via the TLR2 and TLR4 pathway in cumulus cells of ovulated COCs, which may enhance fertilization,” Development, vol. 135, no. 11, pp. 2001–2011, 2008.
[148]
V. G. Da Ros, J. A. Maldera, W. D. Willis et al., “Impaired sperm fertilizing ability in mice lacking Cysteine-RIch Secretory Protein 1 (CRISP1),” Developmental Biology, vol. 320, no. 1, pp. 12–18, 2008.
[149]
M. A. Baker, L. Hetherington, and R. J. Aitken, “Identification of SRC as a key PKA-stimulated tyrosine kinase involved in the capacitation-associated hyperactivation of murine spermatozoa,” Journal of Cell Science, vol. 119, pp. 3182–3192, 2006.
[150]
L. A. Mitchel, B. Nixon, M. A. Baker, and R. J. Aitken, “Investigation of the role of SRC in capacitation-associated tyrosine phosphorylation of human spermatozoa,” Molecular Human Reproduction, vol. 14, no. 4, pp. 235–243, 2008.
[151]
D. Krapf, E. Arcelay, E. V. Wertheimer et al., “Inhibition of Ser/Thr phosphatases induces capacitation-associated signaling in the presence of Src kinase inhibitors,” Journal of Biological Chemistry, vol. 285, no. 11, pp. 7977–7985, 2010.
[152]
L. Cotton, G. M. Gibbs, L. G. Sanchez-Partida, J. R. Morrison, D. M. de Kretser, and M. K. O'Bryan, “Erratum: FGFR-1 signaling is involved in spermiogenesis and sperm capacitation,” Journal of Cell Science, vol. 119, pp. 75–84, 2006.
[153]
M. A. Baker, L. Hetherington, B. Curry, and R. J. Aitken, “Phosphorylation and consequent stimulation of the tyrosine kinase c-Abl by PKA in mouse spermatozoa; its implications during capacitation,” Developmental Biology, vol. 333, no. 1, pp. 57–66, 2009.
[154]
L. Leyton and P. Saling, “95？kd sperm protein binds ZP3 and serve as tyrosine kinase substrates in response to zona binding,” Cell, vol. 57, no. 7, pp. 1123–1130, 1989.
[155]
L. Leyton, P. LeGuen, D. Bunch, and P. M. Saling, “Regulation of mouse gamete interaction by a sperm tyrosine kinase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 24, pp. 11692–11695, 1992.
[156]
R. K. Naz, C. Morte, K. Ahmad, and P. Martinez, “Hexokinase present in human sperm is not tyrosine phosphorylated but its antibodies affect fertilizing capacity,” Journal of Andrology, vol. 17, no. 2, pp. 143–150, 1996.
[157]
A. J. Travis, J. A. Foster, N. A. Rosenbaum et al., “Targeting of a germ cell-specific type 1 hexokinase lacking a porin- binding domain to the mitochondria as well as to the head and fibrous sheath of murine spermatozoa,” Molecular Biology of the Cell, vol. 9, no. 2, pp. 263–276, 1998.
[158]
S. Benoff, “Modelling human sperm-egg interactions in vitro: signal transduction pathways regulating the acrosome reaction,” Molecular Human Reproduction, vol. 4, no. 5, pp. 453–471, 1998.
[159]
G. Berruti and E. Martegani, “Identification of proteins cross-reactive to phosphotyrosine antibodies and of a tyrosine kinase activity in boar spermatozoa,” Journal of Cell Science, vol. 93, pp. 667–674, 1989.
[160]
R. K. Naz, “Protein tyrosine phosphorylation and signal transduction during capacitation-acrosome reaction and zona pellucida binding in human sperm,” Systems Biology in Reproductive Medicine, vol. 37, no. 1, pp. 47–55, 1996.
[161]
R. K. Naz and P. B. Rajesh, “Role of tyrosine phosphorylation in sperm capacitation/acrosome reaction,” Reproductive Biology and Endocrinology, vol. 2, article 75, 2004.
[162]
C. N. Tomes, C. R. Mcmaster, and P. M. Saling, “Activation of mouse sperm phosphatidylinositol-4,5 bisphosphate-phospholipase C by zona pellucida is modulated by tyrosine phosphorylation,” Molecular Reproduction and Development, vol. 43, no. 2, pp. 196–204, 1996.
[163]
K. Fukami, M. Yoshida, T. Inoue et al., “Phospholipase Cδ4 is required for Ca2+ mobilization essential for acrosome reaction in sperm,” Journal of Cell Biology, vol. 161, no. 1, pp. 79–88, 2003.
[164]
K. Fukami, K. Nakao, T. Inoue et al., “Requirement of phospholipase Cδ4 for the zona pellucida-induced acrosome reaction,” Science, vol. 292, no. 5518, pp. 920–923, 2001.
[165]
H. M. Fisher, I. A. Brewis, C. L. R. Barratt, I. D. Cooke, and H. D. M. Moore, “Phosphoinositide 3-kinase is involved in the induction of the human sperm acrosome reaction downstream of tyrosine phosphorylation,” Molecular Human Reproduction, vol. 4, no. 9, pp. 849–855, 1998.
[166]
H. Breitbart, T. Rotman, S. Rubinstein, and N. Etkovitz, “Role and regulation of PI3K in sperm capacitation and the acrosome reaction,” Molecular and Cellular Endocrinology, vol. 314, no. 2, pp. 234–238, 2010.
[167]
M. Luconi, L. Bonaccorsi, C. Krausz, G. Gervasi, G. Forti, and E. Baldi, “Stimulation of protein tyrosine phosphorylation by platelet-activating factor and progesterone in human spermatozoa,” Molecular and Cellular Endocrinology, vol. 108, no. 1-2, pp. 35–42, 1995.
[168]
L. Bonaccorsi, M. Luconi, G. Forti, and E. Baldi, “Tyrosine kinase inhibition reduces the plateau phase of the calcium increase in response to progesterone in human sperm,” FEBS Letters, vol. 364, no. 1, pp. 83–86, 1995.
[169]
S. Meizel and K. O. Turner, “Chloride efflux during the progesterone-initiated human sperm acrosome reaction is inhibited by lavendustin A, a tyrosine kinase inhibitor,” Journal of Andrology, vol. 17, no. 4, pp. 327–330, 1996.
[170]
B. S. Pukazhenthi, D. E. Wildt, M. A. Ottinger, and J. Howard, “Inhibition of domestic cat spermatozoa acrosome reaction and zona pellucida penetration by tyrosine kinase inhibitors,” Molecular Reproduction and Development, vol. 49, no. 1, pp. 48–57, 1998.
[171]
V. Dorval, M. Dufour, and P. Leclerc, “Role of protein tyrosine phosphorylation in the thapsigargin-induced intracellular Ca2+ store depletion during human sperm acrosome reaction,” Molecular Human Reproduction, vol. 9, no. 3, pp. 125–131, 2003.
[172]
C. Morte, A. Iborra, and P. Martínez, “Phosphorylation of Shc proteins in human sperm in response to capacitation and progesterone treatment,” Molecular Reproduction and Development, vol. 50, no. 1, pp. 113–120, 1998.
[173]
C. Picherit-Marchenay, S. Bréchard, D. Boucher, and G. Grizard, “Correlation between tyrosine phosphorylation intensity of a 107？kDa protein band and A23187-induced acrosome reaction in human spermatozoa,” Andrologia, vol. 36, no. 6, pp. 370–377, 2004.
[174]
V. Mor, T. Das, M. Bhattacharjee, and T. Chatterjee, “Protein tyrosine phosphorylation of a heparin-binding sperm membrane mitogen (HBSM) is associated with capacitation and acrosome reaction,” Biochemical and Biophysical Research Communications, vol. 352, no. 2, pp. 404–409, 2007.
[175]
C. N. Tomes, C. M. Roggero, G. De Blas, P. M. Saling, and L. S. Mayorga, “Requirement of protein tyrosine kinase and phosphatase activities for human sperm exocytosis,” Developmental Biology, vol. 265, no. 2, pp. 399–415, 2004.
[176]
V. E. P. Zarelli, M. C. Ruete, C. M. Roggero, L. S. Mayorga, and C. N. Tomes, “PTP1B dephosphorylates N-ethylmaleimide-sensitive factor and elicits SNARE complex disassembly during human sperm exocytosis,” Journal of Biological Chemistry, vol. 284, no. 16, pp. 10491–10503, 2009.
[177]
M. Finkelstein, N. Etkovitz, and H. Breitbart, “Role and regulation of sperm gelsolin prior to fertilization,” Journal of Biological Chemistry, vol. 285, no. 51, pp. 39702–39709, 2010.
[178]
Y. Lax, S. Rubinstein, and H. Breitbart, “Epidermal growth factor induces acrosomal exocytosis in bovine sperm,” FEBS Letters, vol. 339, no. 3, pp. 234–238, 1994.
[179]
N. Etkovitz, Y. Tirosh, R. Chazan et al., “Bovine sperm acrosome reaction induced by G protein-coupled receptor agonists is mediated by epidermal growth factor receptor transactivation,” Developmental Biology, vol. 334, no. 2, pp. 447–457, 2009.
[180]
L. Daniel, N. Etkovitz, S. R. Weiss, S. Rubinstein, D. Ickowicz, and H. Breitbart, “Regulation of the sperm EGF receptor by ouabain leads to initiation of the acrosome reaction,” Developmental Biology, vol. 344, no. 2, pp. 650–657, 2010.
[181]
K. I. Sato, A. Sato, M. Aoto, and Y. Fukami, “C-SRC phosphorylates epidermal growth factor receptor on tyrosine 845,” Biochemical and Biophysical Research Communications, vol. 215, no. 3, pp. 1078–1087, 1995.
[182]
D. A. Tice, J. S. Biscardi, A. L. Nickles, and S. J. Parsons, “Mechanism of biological synergy between cellular Src and epidermal growth factor receptor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 4, pp. 1415–1420, 1999.
[183]
J. S. Biscardi, M. C. Maa, D. A. Tice, M. E. Cox, T. H. Leu, and S. J. Parsons, “C-Src-mediated phosphorylation of the epidermal growth factor receptor on Tyr845 and Tyr1101 is associated with modulation of receptor function,” Journal of Biological Chemistry, vol. 274, no. 12, pp. 8335–8343, 1999.
[184]
G. Varano, A. Lombardi, G. Cantini, G. Forti, E. Baldi, and M. Luconi, “Src activation triggers capacitation and acrosome reaction but not motility in human spermatozoa,” Human Reproduction, vol. 23, no. 12, pp. 2652–2662, 2008.
[185]
S. Tapia, M. Rojas, P. Morales, M. A. Ramirez, and E. S. Diaz, “The laminin-induced acrosome reaction in human sperm is mediated by src kinases and the proteasome,” Biology of Reproduction, vol. 85, no. 2, pp. 357–366, 2011.
[186]
H. Feng, J. I. Sandlow, and A. Sandra, “The c-kit receptor and its possible signaling transduction pathway in mouse spermatozoa,” Molecular Reproduction and Development, vol. 49, no. 3, pp. 317–326, 1998.
[187]
D. Krapf, P. E. Visconti, S. E. Arranz, and M. O. Cabada, “Egg water from the amphibian Bufo arenarum induces capacitation-like changes in homologous spermatozoa,” Developmental Biology, vol. 306, no. 2, pp. 516–524, 2007.
[188]
B. Baibakov, L. Gauthier, P. Talbot, T. L. Rankin, and J. Dean, “Sperm binding to the zona pellucida is not sufficient to induce acrosome exocytosis,” Development, vol. 134, no. 5, pp. 933–943, 2007.
[189]
J. M. Teijeiro, M. O. Cabada, and P. E. Marini, “Sperm binding glycoprotein (SBG) produces calcium and bicarbonate dependent alteration of acrosome morphology and protein tyrosine phosphorylation on boar sperm,” Journal of Cellular Biochemistry, vol. 103, no. 5, pp. 1413–1423, 2008.
[190]
E. S. Diaz, M. Kong, and P. Morales, “Effect of fibronectin on proteasome activity, acrosome reaction, tyrosine phosphorylation and intracellular calcium concentrations of human sperm,” Human Reproduction, vol. 22, no. 5, pp. 1420–1430, 2007.
[191]
M. C. Gye, “Changes in sperm phosphotyrosine proteins by human follicular fluid in mice,” Archives of Andrology, vol. 49, no. 6, pp. 417–422, 2003.
[192]
I. K. Townley, E. Schuyler, M. Parker-Gür, and K. R. Foltz, “Expression of multiple Src family kinases in sea urchin eggs and their function in Ca2+ release at fertilization,” Developmental Biology, vol. 327, no. 2, pp. 465–477, 2009.
[193]
A. F. Giusti, D. J. Carroll, Y. A. Abassi, M. Terasaki, K. R. Foltz, and L. A. Jaffef, “Requirement of a Src family kinase for initiating calcium release at fertilization in starfish eggs,” Journal of Biological Chemistry, vol. 274, no. 41, pp. 29318–29322, 1999.
[194]
L. L. Runft and L. A. Jaffe, “Sperm extract injection into ascidian eggs signals Ca2+ release by the same pathway as fertilization,” Development, vol. 127, no. 15, pp. 3227–3236, 2000.
[195]
K. I. Sato, A. A. Tokmakov, T. Iwasaki, and Y. Fukami, “Tyrosine kinase-dependent activation of phospholipase Cγ is required for calcium transient in Xenopus egg fertilization,” Developmental Biology, vol. 224, no. 2, pp. 453–469, 2000.
[196]
L. K. McGinnis, D. F. Albertini, and W. H. Kinsey, “Localized activation of Src-family protein kinases in the mouse egg,” Developmental Biology, vol. 306, no. 1, pp. 241–254, 2007.
[197]
M. Levi, B. Maro, and R. Shalgi, “Fyn kinase is involved in cleavage furrow ingression during meiosis and mitosis,” Reproduction, vol. 140, no. 6, pp. 827–834, 2010.
[198]
C. Sette, A. Bevilacqua, A. Bianchini, F. Mangia, R. Geremia, and P. Rossi, “Parthenogenetic activation of mouse eggs by microinjection of a truncated c-kit tyrosine kinase present in spermatozoa,” Development, vol. 124, no. 11, pp. 2267–2274, 1997.
[199]
C. Sette, A. Bevilacqua, R. Geremia, and P. Rossi, “Involvement of phospholipase Cγ1 in mouse egg activation induced by a truncated form of the c-kit tyrosine kinase present in spermatozoa,” Journal of Cell Biology, vol. 142, no. 4, pp. 1063–1074, 1998.
[200]
C. Sette, M. P. Paronetto, M. Barchi, A. Bevilacqua, R. Geremia, and P. Rossi, “Tr-kit-induced resumption of the cell cycle in mouse eggs requires activation of a Src-like kinase,” The EMBO Journal, vol. 21, no. 20, pp. 5386–5395, 2002.
[201]
A. T. H. Wu, P. Sutovsky, G. Manandhar et al., “PAWP, a sperm-specific WW domain-binding protein, promotes meiotic resumption and pronuclear development during fertilization,” Journal of Biological Chemistry, vol. 282, no. 16, pp. 12164–12175, 2007.
[202]
K. Simons and D. Toomre, “Lipid rafts and signal transduction,” Nature Reviews Molecular Cell Biology, vol. 1, no. 1, pp. 31–39, 2000.
[203]
L. J. Pike, “Rafts defined: a report on the Keystone symposium on lipid rafts and cell function,” Journal of Lipid Research, vol. 47, no. 7, pp. 1597–1598, 2006.
[204]
R. J. Belton Jr., N. L. Adams, and K. R. Foltz, “Isolation and characterization of sea urchin egg lipid rafts and their possible function during fertilization,” Molecular Reproduction and Development, vol. 59, no. 3, pp. 294–305, 2001.
[205]
K. I. Sato, T. Iwasaki, K. Ogawa, M. Konishi, A. A. Tokmakov, and Y. Fukami, “Low density detergent-insoluble membrane of Xenopus eggs: subcellular microdomain for tyrosine kinase signaling in fertilization,” Development, vol. 129, no. 4, pp. 885–896, 2002.
[206]
A. Luria, V. Vegelyte-Avery, B. Stith et al., “Detergent-free domain isolated from Xenopus egg plasma membrane with properties similar to those of detergent-resistant membranes,” Biochemistry, vol. 41, no. 44, pp. 13189–13197, 2002.
[207]
M. Comiskey and C. M. Warner, “Spatio-temporal localization of membrane lipid rafts in mouse oocytes and cleaving preimplantation embryos,” Developmental Biology, vol. 303, no. 2, pp. 727–739, 2007.
[208]
B. Sato, Y. U. Katagiri, K. Miyado et al., “Lipid rafts enriched in monosialylGb5Cer carrying the stage-specific embryonic antigen-4 epitope are involved in development of mouse preimplantation embryos at cleavage stage,” BMC Developmental Biology, vol. 11, article 22, 2011.
[209]
A. K. M. Hasan, Z. Ou, K. Sakakibara et al., “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, vol. 12, no. 2, pp. 251–267, 2007.
[210]
A. K. M. Hasan, K. I. Sato, K. Sakakibara et al., “Uroplakin III, a novel Src substrate in Xenopus egg rafts, is a target for sperm protease essential for fertilization,” Developmental Biology, vol. 286, no. 2, pp. 483–492, 2005.
[211]
K. Sakakibara, K. I. Sato, K. I. Yoshino et al., “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, vol. 280, no. 15, pp. 15029–15037, 2005.
[212]
K. I. Sato, A. A. Tokmakov, C. L. He et al., “Reconstitution of Src-dependent phospholipase Cγ phosphorylation and transient calcium release by using membrane rafts and cell-free extracts from Xenopus eggs,” Journal of Biological Chemistry, vol. 278, no. 40, pp. 38413–38420, 2003.
