Skip to main content Accessibility help
Hostname: page-component-684899dbb8-v9xhf Total loading time: 1.136 Render date: 2022-05-20T18:25:01.468Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "useRatesEcommerce": false, "useNewApi": true }

11 - Sperm-Specific WW-Domain-Binding Proteins

Published online by Cambridge University Press:  25 May 2017

Christopher J. De Jonge
University of Minnesota
Christopher L. R. Barratt
University of Dundee
Ryuzo Yanagimachi
University of Hawaii, Manoa
Get access


Image of the first page of this content. For PDF version, please use the ‘Save PDF’ preceeding this image.'
The Sperm Cell
Production, Maturation, Fertilization, Regeneration
, pp. 157 - 176
Publisher: Cambridge University Press
Print publication year: 2017

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)


Oko, R, Maravei, D. Distribution and possible role of perinuclear theca proteins during bovine spermiogenesis. Microsc Res Technol 1995; 32: 520–32.CrossRefGoogle ScholarPubMed
Yu, Y, Xu, W, Yi, YJ, Sutovsky, P, Oko, R. The extracellular protein coat of the inner acrosomal membrane is involved in zona pellucida binding and penetration during fertilization: Characterization of its most prominent polypeptide (IAM38). Dev Biol 2006; 290: 3243.CrossRefGoogle Scholar
Sutovsky, P, Manandhar, G, Wu, A, Oko, R. Interactions of sperm perinuclear theca with the oocyte: Implications for oocyte activation, anti-polyspermy defense, and assisted reproduction. Microsc Res Technol; 2003; 61: 362–78.CrossRefGoogle ScholarPubMed
Oko, R, Sutovsky, P. Biogenesis of sperm perinuclear theca and its role in sperm functional competence and fertilization. J Reprod Immunol 2009; 83: 27.CrossRefGoogle ScholarPubMed
Tran, MH, Aul, RB, Xu, W, van der Hoorn, FA, Oko, R. Involvement of classical bipartite/karyopherin nuclear import pathway components in acrosomal trafficking and assembly during bovine and murid spermiogenesis. Biol Reprod 2012; 86: 84.CrossRefGoogle ScholarPubMed
Kierszenbaum, AL, Rivkin, E, Tres, LL. Acroplaxome, an F-actin-keratin-containing plate, anchors the acrosome to the nucleus during shaping of the spermatid head. Mol Biol Cell 2003; 14: 4,628–40.CrossRefGoogle ScholarPubMed
Ito, C, Suzuki-Toyota, F, Maekawa, M, Toyama, Y, Yao, R, Noda, T, Toshimori, K. Failure to assemble the peri-nuclear structures in GOPC deficient spermatids as found in round-headed spermatozoa. Arch Histol Cytol 2004; 67: 349–60.CrossRefGoogle ScholarPubMed
Kierszenbaum, AL, Tres, L, Rivki, E, Kang-Decker, N, van Deursen, JM. The acroplaxome is the docking site of Golgi-derived myosin Va/Rab27a/b- containing proacrosomal vesicles in wild-type and Hrb mutant mouse spermatids. Biol Reprod 2004; 70: 1,400–10.CrossRefGoogle ScholarPubMed
Ito, C, Yamatoya, K, Yoshida, K, Kyono, K, Yao, R, Noda, T, Toshimori, K. Appearance of an oocyte activation-related substance during spermatogenesis in mice and humans. Hum Reprod 2010; 25: 2,734–44.CrossRefGoogle ScholarPubMed
Tovich, PR, Sutovsky, P, Oko, RJ. Novel aspect of perinuclear theca assembly revealed by immunolocalization of non-nuclear somatic histones during bovine spermiogenesis. Biol Reprod 2004; 71: 1,182–94.CrossRefGoogle ScholarPubMed
Wu, AT, Sutovsky, P, Xu, W, van der Spoel, AC, Platt, FM, Oko, R. The postacrosomal assembly of sperm head protein, PAWP, is independent of acrosome formation and dependent on microtubular manchette transport. Dev Biol 2007; 312: 471–83.CrossRefGoogle ScholarPubMed
Ito, C, Akutsu, H, Yao, R, Kyono, K, Suzuki-Toyota, F, Toyama, Y, Maekawa, M, Noda, T, Toshimori, K. Oocyte activation ability correlates with head flatness and presence of perinuclear theca substance in human and mouse sperm. Hum Reprod 2009; 24: 2,588–95.CrossRefGoogle ScholarPubMed
Oko, R, Morales, CR. A novel testicular protein, with sequence similarities to a family of lipid binding proteins, is a major component of the rat sperm perinuclear theca. Dev Biol 1994; 166: 235–45.CrossRefGoogle ScholarPubMed
Aul, RB, Oko, RJ. The major subacrosomal occupant of bull spermatozoa is a novel histone H2B variant associated with the forming acrosome during spermiogenesis. Dev Biol 2002; 242: 376–87.CrossRefGoogle ScholarPubMed
Mountjoy, JR, Xu, W, McLeod, D, Hyndman, D, Oko, R. RAB2A: A major subacrosomal protein of bovine spermatozoa implicated in acrosomal biogenesis. Biol Reprod 2008; 79: 223–32.CrossRefGoogle Scholar
Oko, R, Aul, RB, Wu, A. The spermhead cytoskeleton. In: Robaire, B (Ed.), Andrology in the 21st Century. Medical Publications, 2001: 3745.Google Scholar
Hamilton, LE, Acteau, G, Wei Xu, W, Sutovsky, P, Oko, RJ. The developmental origin and compartmentalization of glutathione-S-transferase omega 2 isoforms in the perinuclear theca of Eutherian spermatozoa. 2016; in preparation.
Wu, ATH, Sutovsky, P, Manandhar, G, Xu, W, Katayama, M, Day, BN, Park, KW, Yi, YJ, Xi, YW, Prather, RS, Oko, R. PAWP, a sperm-specific WW domain-binding protein, promotes meiotic resumption and pronuclear development during fertilization. J Biol Chem 2007; 282: 12,164–75.Google ScholarPubMed
Tovich, PR, Oko, RJ. Somatic histones are components of the perinuclear theca in bovine spermatozoa. J Biol Chem 2003; 278: 32,431–8.CrossRefGoogle ScholarPubMed
Hess, H, Heid, H, Franke, WW. Molecular characterization of mammalian cylicin, a basic protein of the sperm head cytoskeleton. J Cell Biol 1993; 122: 1,043–52.CrossRefGoogle ScholarPubMed
Hess, H, Heid, H, Zimbelmann, R, Franke, WW. The protein complexity of the cytoskeleton of bovine and human sperm heads: The identification and characterization of cylicin II. Exp Cell Res 1995; 218: 174–82.CrossRefGoogle ScholarPubMed
Von Bulow, M, Heid, H, Hess, H, Franke, WW. Molecular nature of calicin, a major basic protein of the mammalian sperm head cytoskeleton. Exp Cell Res 1995; 219: 407–13.CrossRefGoogle Scholar
Von Bulow, M, Rackwitz, HR, Zimbelmann, R, Franke, WW. CP beta3, a novel isoform of an actin-binding protein, is a component of the cytoskeletal calyx of the mammalian sperm head. Exp Cell Res 1997; 233: 216–24.Google ScholarPubMed
Heid, H, Figge, U, Winter, S, Kuhn, C, Zimbelmann, R, Franke, W. Novel actin-related proteins Arp-T1 and Arp-T2 as components of the cytoskeletal calyx of the mammalian sperm head. Exp Cell Res 2002; 279: 177–87.CrossRefGoogle ScholarPubMed
Leclerc, P, Goupil, S. Regulation of the human sperm tyrosine kinase c-yes. Activation by cyclic adenosine 3',5'-monophosphate and inhibition by Ca(2+). Biol Reprod 2002; 67: 301–7.CrossRefGoogle Scholar
Muciaccia, B, Sette, C, Paronetto, MP, Barchi, M, Pensini, S, DʼAgostino, A, Gandini, L, Geremia, R, Stefanini, M, Rossi, P. Expression of a truncated form of KIT tyrosine kinase in human spermatozoa correlates with sperm DNA integrity. Hum Reprod 2010; 25: 2,188202.CrossRefGoogle ScholarPubMed
Manandhar, G, Toshimori, K. Fate of postacrosomal perinuclear theca recognized by monoclonal antibody MN13 after sperm head microinjection and its role in oocyte activation in mice. Biol Reprod 2003; 68(2): 655–63.CrossRefGoogle ScholarPubMed
Herrada, G, Wolgemuth, DJ. The mouse transcription factor Stat4 is expressed in haploid male germ cells and is present in the perinuclear theca of spermatozoa. J Cell Sci 1997; 110(14): 1,543–53.Google ScholarPubMed
Lachance, C, Leclerc, P. Mediators of the Jak/STAT signaling pathway in human spermatozoa. Biol Reprod 2011; 85: 1,222–31.CrossRefGoogle ScholarPubMed
Kitamura, K, Iguchi, N, Kaneko, Y, Tanaka, H, Nishimune, Y. Characterization of a novel postacrosomal perinuclear theca-specific protein, CYPT1. Biol Reprod 2004; 71: 1,927–35.CrossRefGoogle ScholarPubMed
Liu, YQ, Bai, G, Zhang, H, Su, D, Tao, DC, Yang, Y, Ma, YX, Zhang, SZ. Human RING finger protein ZNF645 is a novel testis-specific E3 ubiquitin ligase. Asian J Androl 2010; 12(5): 658–66.CrossRefGoogle ScholarPubMed
Francou, MM, Hombrebueno, JR, De Juan, J. Identification and cellular location of glutamine synthetase in human sperm. Cell Tissue Res 2012; 350: 183–7.CrossRefGoogle ScholarPubMed
Hernandez-Gonzalez, EO, Martinez-Rojas, D, Mornet, D, Rendon, A, Mujica, A. Comparative distribution of short dystrophin superfamily products in various guinea pig spermatozoa domains. Eur J Cell Biol 2001; 80: 792–8.Google ScholarPubMed
Oko, RJ. Developmental expression and possible role of perinuclear theca proteins in mammalian spermatozoa. Reprod Fertil Dev 1995; 7: 777–97.CrossRefGoogle ScholarPubMed
Au, CE, Hermo, L, Byrne, E, Smirle, J, Fazel, A, Kearney, RE, Smith, CE, Vali, H, Fernandez-Rodriguez, J, Simon, PHG, Mandato, C, Nilsson, T, Bergeron, JJM. Compartmentalization of membrane trafficking, glucose transport, glycolysis, actin, tubulin and the proteasome in the cytoplasmic droplet/Hermes body of epididymal sperm. Open Biol 2015; 5: 150080.CrossRefGoogle ScholarPubMed
Ferrer, M, Xu, W, Oko, R. The composition, protein genesis and significance of the inner acrosomal membrane of eutherian sperm. Cell Tissue Res 2012; 349: 733–48.CrossRefGoogle ScholarPubMed
Oko, R. Occurrence and formation of cytoskeletal proteins in mammalian spermatozoa. Andrologia 1998; 30(4–5): 193206.CrossRefGoogle ScholarPubMed
Yan, W, Morozumi, K, Zhang, J, Ro, S, Park, C, Yanagimachi, R. Birth of mice after intracytoplasmic injection of single purified sperm nuclei and detection of messenger RNAs and MicroRNAs in the sperm nuclei. Biol Reprod 2008; 78(5): 896902.CrossRefGoogle ScholarPubMed
Morozumi, K, Shikano, T, Miyazaki, S, Yanagimachi, R. Simultaneous removal of sperm plasma membrane and acrosome before intracytoplasmic sperm injection improves oocyte activation/embryonic development. Proc Natl Acad Sci USA 2006; 103: 17,661–6.CrossRefGoogle ScholarPubMed
Aarabi, M, Yu, Y, Xu, W, Tse, MY, Pang, SC, Yi, YJ, Sutovsky, P, Oko, R. The testicular and epididymal expression profile of PLCzeta in mouse and human does not support its role as a sperm-borne oocyte activating factor. PLoS One 2012; 7: e33496.CrossRefGoogle Scholar
Aarabi, M, Balakier, H, Bashar, S, Moskovtsev, SI, Sutovsky, P, Librach, CL, Oko, R. Sperm-derived WW domain-binding protein, PAWP, elicits calcium oscillations and oocyte activation in humans and mice. FASEB J 2014; 28: 4,434–40.CrossRefGoogle ScholarPubMed
Longo, FJ, Krohne, G, Franke, WW. Basic proteins of the perinuclear theca of mammalian spermatozoa and spermatids: A novel class of cytoskeletal elements. J Cell Biol 1987; 105: 1,105–20.CrossRefGoogle ScholarPubMed
Paranko, J, Longo, F, Potts, J, Krohne, G, Franke, WW. Widespread occurrence of calicin, a basic cytoskeletal protein of sperm cells, in diverse mammalian species. Differentiation 1988; 38: 21–7.CrossRefGoogle ScholarPubMed
Rousseaux-Prevost, R, Lecuyer, C, Drobecq, H, Sergheraert, C, Dacheux, JL, Rousseaux, J. Characterization of boar sperm cytoskeletal cylicin II as an actin-binding protein. Biochem Biophys Res Commun 2003; 303: 182–9.CrossRefGoogle ScholarPubMed
Aul, RB, Oko, RJ. The major subacrosomal occupant of bull spermatozoa is a novel histone H2B variant associated with the forming acrosome during spermiogenesis. Dev Biol 2001; 239: 376–87.CrossRefGoogle ScholarPubMed
Breed, WG, Idriss, D, Oko, RJ. Protein composition of the ventral processes on the sperm head of Australian hydromyine rodents. Biol Reprod 2000; 63: 629–34.CrossRefGoogle ScholarPubMed
Farkhondeh, P, Tahereh, K, Mahmood, JT, Mojgan, B, Jamileh, G, Fatemeh, SN. A novel human lipid binding protein coding gene: PERF15, sequence and cloning. J Reprod Infertil 2009; 10: 199205.Google ScholarPubMed
Selvaraj, V, Asano, A, Page, JL, Nelson, JL, Kothapalli, KS, Foster, JA, Brenna, JT, Weiss, RS, Travis, AJ. Mice lacking FABP9/PERF15 develop sperm head abnormalities but are fertile. Dev Biol 2010; 348: 177–89.CrossRefGoogle ScholarPubMed
Sette, C, Bevilacqua, A, Geremia, R, Rossi, P. Involvement of phospholipase Cgamma1 in mouse egg activation induced by a truncated form of the C-kit tyrosine kinase present in spermatozoa. J Cell Biol 1998; 142: 1,063–74.CrossRefGoogle ScholarPubMed
Sette, C, Paronetto, MP, Barchi, M, Bevilacqua, A, Geremia, R, Rossi, P. Tr-kit-induced resumption of the cell cycle in mouse eggs requires activation of a Src-like kinase. EMBO J 2002; 21: 5,386–95.CrossRefGoogle ScholarPubMed
Sette, C, Bevilacqua, A, Bianchini, A, Mangia, F, Geremia, R, Rossi, P. Parthenogenetic activation of mouse eggs by microinjection of a truncated c-kit tyrosine kinase present in spermatozoa. Development 1997; 124: 2,267–74.Google ScholarPubMed
Albanesi, C, Geremia, R, Giorgio, M, Dolci, S, Sette, C, Rossi, P. A cell- and developmental stage-specific promoter drives the expression of a truncated c-kit protein during mouse spermatid elongation. Development 1996; 122: 1,291130.Google ScholarPubMed
Sutovsky, P, Oko, R, Hewitson, L, Schatten, G. The removal of the sperm perinuclear theca and its association with the bovine oocyte surface during fertilization. Dev Biol 1997; 188: 7584.CrossRefGoogle ScholarPubMed
Sutovsky, P, Navara, CS, Schatten, G. Fate of the sperm mitochondria, and the incorporation, conversion, and disassembly of the sperm tail structures during bovine fertilization. Biol Reprod 1996; 55: 1,195205.CrossRefGoogle ScholarPubMed
Sutovsky, P, Schatten, G. Depletion of glutathione during bovine oocyte maturation reversibly blocks the decondensation of the male pronucleus and pronuclear apposition during fertilization. Biol Reprod 1997; 56: 1,503–12.CrossRefGoogle ScholarPubMed
Perry, AC, Wakayama, T, Cooke, IM, Yanagimachi, R. Mammalian oocyte activation by the synergistic action of discrete sperm head components: Induction of calcium transients and involvement of proteolysis. Dev Biol 2000; 217: 386–93.CrossRefGoogle ScholarPubMed
Kimura, Y, Yanagimachi, R, Kuretake, S, Bortkiewicz, H, Perry, AC, Yanagimachi, H. Analysis of mouse oocyte activation suggests the involvement of sperm perinuclear material. Biol Reprod 1998; 58: 1,407–15.CrossRefGoogle ScholarPubMed
Katayama, M, Sutovsky, P, Yang, BS, Cantley, T, Rieke, A, Farwell, R, Oko, R, Day, BN. Increased disruption of sperm plasma membrane at sperm immobilization promotes dissociation of perinuclear theca from sperm chromatin after intracytoplasmic sperm injection in pigs. Reproduction 2005; 130: 907–16.CrossRefGoogle ScholarPubMed
Sutovsky, P, Hewitson, L, Simerly, CR, Tengowski, MW, Navara, CS, Haavisto, A, Schatten, G. Intracytoplasmic sperm injection for Rhesus monkey fertilization results in unusual chromatin, cytoskeletal, and membrane events, but eventually leads to pronuclear development and sperm aster assembly. Hum Reprod 1996; 11: 1,703–12.CrossRefGoogle ScholarPubMed
Sudol, M. Structure and function of the WW domain. Prog Biophys Mol Biol 1996; 65: 113–32.CrossRefGoogle ScholarPubMed
Sudol, M. The WW module competes with the SH3 domain? Trends Biochem Sci 1996; 21: 161–3.CrossRefGoogle ScholarPubMed
Macias, MJ, Wiesner, S, Sudol, M. WW and SH3 domains, two different scaffolds to recognize proline-rich ligands. FEBS Lett 2002; 513: 30–7.CrossRefGoogle ScholarPubMed
Sudol, M, Bork, P, Einbond, A, Kastury, K, Druck, T, Negrini, M, Huebner, K, Lehman, D. Characterization of the mammalian YAP (Yes-associated protein) gene and its role in defining a novel protein module, the WW domain. J Biol Chem 1995; 270: 14,733–41.CrossRefGoogle ScholarPubMed
Li, Y, Ozaki, T, Kikuchi, H, Yamamoto, H, Ohira, M, Nakagawara, A. A novel HECT-type E3 ubiquitin protein ligase NEDL1 enhances the p53-mediated apoptotic cell death in its catalytic activity-independent manner. Oncogene 2008; 27: 3,700–9.CrossRefGoogle ScholarPubMed
Miyazaki, K, Ozaki, T, Kato, C, Hanamoto, T, Fujita, T, Irino, S, Watanabe, K, Nakagawa, T, Nakagawara, A. A novel HECT-type E3 ubiquitin ligase, NEDL2, stabilizes p73 and enhances its transcriptional activity. Biochem Biophys Res Commun 2003; 308: 106–13.CrossRefGoogle ScholarPubMed
Lu, L, Hu, S, Wei, R, Qiu, X, Lu, K, Fu, Y, Li, H, Xing, G, Li, D, Peng, R, He, F, Zhang, L. The HECT type ubiquitin ligase NEDL2 is degraded by anaphase-promoting complex/cyclosome (APC/C)-Cdh1, and its tight regulation maintains the metaphase to anaphase transition. J Biol Chem 2013; 288: 35,637–50.CrossRefGoogle ScholarPubMed
Rivkin, E, Cullinan, EB, Tres, LL, Kierszenbaum, AL. A protein associated with the manchette during rat spermiogenesis is encoded by a gene of the TBP-1-like subfamily with highly conserved ATPase and protease domains. Mol Reprod Dev 1997; 48: 7789.3.0.CO;2-T>CrossRefGoogle ScholarPubMed
Chen, HI, Sudol, M. The WW domain of Yes-associated protein binds a proline-rich ligand that differs from the consensus established for Src homology 3-binding modules. Proc Natl Acad Sci USA 1995; 92: 7,819–23.CrossRefGoogle ScholarPubMed
Sudol, M, Chen, HI, Bougeret, C, Einbond, A, Bork, P. Characterization of a novel protein-binding module – The WW domain. FEBS Lett 1995; 369: 6771.CrossRefGoogle ScholarPubMed
Dhananjayan, SC, Ramamoorthy, S, Khan, OY, Ismail, A, Sun, J, Slingerland, J, O'Malley, BW, Nawaz, Z. WW domain binding protein-2, an E6-associated protein interacting protein, acts as a coactivator of estrogen and progesterone receptors. Mol Endocrinol 2006; 20: 2,343–54.CrossRefGoogle ScholarPubMed
Grusche, FA, Degoutin, JL, Richardson, HE, Harvey, KF. The Salvador/Warts/Hippo pathway controls regenerative tissue growth in Drosophila melanogaster. Dev Biol 2011; 350: 255–66.CrossRefGoogle ScholarPubMed
Zhang, X, Milton, CC, Poon, CL, Hong, W, Harvey, KF. Wbp2 cooperates with Yorkie to drive tissue growth downstream of the Salvador-Warts-Hippo pathway. Cell Death Differ 2011; 18: 1,346–55.CrossRefGoogle ScholarPubMed
McDonald, CB, McIntosh, SK, Mikles, DC, Bhat, V, Deegan, BJ, Seldeen, KL, Saeed, AM, Buffa, L, Sudol, M, Nawaz, Z, Farooq, A. Biophysical analysis of binding of WW domains of the YAP2 transcriptional regulator to PPXY motifs within WBP1 and WBP2 adaptors. Biochemistry 2011; 50: 9,616–27.CrossRefGoogle ScholarPubMed
Miyazaki, S. Repetitive calcium transients in hamster oocytes. Cell Calcium 1991; 12: 205–16.CrossRefGoogle ScholarPubMed
Machaty, Z. Signal transduction in mammalian oocytes during fertilization. Cell Tissue Res 2016; 363: 169–83.CrossRefGoogle ScholarPubMed
Heyers, S, Sousa, M, Cangir, O, Schmoll, F, Schellander, K, van der Ven, H, Montag, M. Activation of mouse oocytes requires multiple sperm factors but not sperm PLCgamma1. Mol Cell Endocrinol 2000; 166: 51–7.CrossRefGoogle Scholar
Sato, K. Transmembrane signal transduction in oocyte maturation and fertilization: Focusing on Xenopus laevis as a model animal. Int J Mol Sci 2015; 16: 114–34.Google Scholar
Aarabi, M, Qin, Z, Xu, W, Mewburn, J, Oko, R. Sperm-borne protein, PAWP, initiates zygotic development in Xenopus laevis by eliciting intracellular calcium release. Mol Reprod Dev 2010; 77: 249–56.Google ScholarPubMed
Nomikos, M, Sanders, JR, Kashir, J, Sanusi, R, Buntwal, L, Love, D, Ashley, P, Sanders, D, Knaggs, P, Bunkheila, A, Swann, K, Lai, FA. Functional disparity between human PAWP and PLCzeta in the generation of Ca2+ oscillations for oocyte activation. Mol Hum Reprod 2015; 21: 702–10.CrossRefGoogle ScholarPubMed
Satouh, Y, Nozawa, K, Ikawa, M. Sperm postacrosomal WW domain-binding protein is not required for mouse egg activation. Biol Reprod 2015; 115: 131441.Google Scholar
Kennedy, CE, Krieger, KB, Sutovsky, M, Xu, W, Vargovic, P, Didion, BA, Ellersieck, MR, Hennessy, ME, Verstegen, J, Oko, R, Sutovsky, P. Protein expression pattern of PAWP in bull spermatozoa is associated with sperm quality and fertility following artificial insemination. Mol Reprod Dev 2014; 81: 436–49.CrossRefGoogle ScholarPubMed
Kaya, A, Dogan, S, Vargovic, P, Govindaraju, A, Ross, P, Topper, E, Oko, R, van der Hoorn, F, Sutovsky, P, Memili, E. Identification of fertility-correlated protein biomarkers of bull sperm quality. 2015; submitted for publication.
Aarabi, M, Balakier, H, Bashar, S, Moskovtsev, SI, Sutovsky, P, Librach, CL, Oko, R. Sperm content of postacrosomal WW binding protein is related to fertilization outcomes in patients undergoing assisted reproductive technology. Fertil Steril 2014; 102: 440–7.CrossRefGoogle ScholarPubMed
Nikiforaki, D, Vanden Meerschaut, F, De Gheselle, S, Qian, C, Van den Abbeel, E, De Vos, WH, Deroo, T, De Sutter, P, Heindryckx, B. Sperm involved in recurrent partial hydatidiform moles cannot induce the normal pattern of calcium oscillations. Fertil Steril 2014; 102: 581–8 e1.CrossRefGoogle ScholarPubMed
Durban, M, Barragan, M, Colodron, M, Ferrer-Buitrago, M, De Sutter, P, Heindryckx, B, Vernaeve, V, Vassena, R. PLCzeta disruption with complete fertilization failure in normozoospermia. J Assist Reprod Genet 2015; 32: 879–86.Google ScholarPubMed
Kashir, J, Jones, C, Mounce, G, Ramadan, WM, 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. Fertil Steril 2012; 99: 107–17.Google ScholarPubMed
Yelumalai, S, Yeste, M, Jones, C, Amdani, SN, Kashir, J, Mounce, G, Da Silva, SJ, Barratt, CL, McVeigh, E, Coward, K. Total levels, localization patterns, and proportions of sperm exhibiting phospholipase C zeta are significantly correlated with fertilization rates after intracytoplasmic sperm injection. Fertil Steril 2015; 104: 561568 e4.CrossRefGoogle ScholarPubMed
Taylor, SL, Yoon, SY, Morshedi, MS, Lacey, DR, Jellerette, T, Fissore, RA, Oehninger, S. Complete globozoospermia associated with PLCzeta deficiency treated with calcium ionophore and ICSI results in pregnancy. Reprod Biomed Online 2010; 20: 559–64.CrossRefGoogle ScholarPubMed
Yoon, SY, Jellerette, T, Salicioni, AM, Lee, HC, Yoo, MS, Coward, K, Parrington, J, Grow, D, Cibelli, JB, Visconti, PE, Mager, J, Fissore, RA. Human sperm devoid of PLC, zeta 1 fail to induce Ca(2+) release and are unable to initiate the first step of embryo development. J Clin Invest 2008; 118: 3,671–81.CrossRefGoogle ScholarPubMed
Nourashrafeddin, S, Aarabi, M, Modarressi, MH, Rahmati, M, Nouri, M. The evaluation of WBP2NL-related genes expression in breast cancer. Pathol Oncol Res 2015; 21: 293300.CrossRefGoogle ScholarPubMed
Nourashrafeddin, S, Dianatpour, M, Aarabi, M, Mobasheri, MB, Kazemi-Oula, G, Modarressi, MH. Elevated expression of the testis-specific gene WBP2NL in breast cancer. Biomark Cancer 2015; 7: 1924.CrossRefGoogle ScholarPubMed
Wang, J, Figueroa, JD, Wallstrom, G, Barker, K, Park, JG, Demirkan, G, Lissowska, J, Anderson, KS, Qiu, J, LaBaer, J. Plasmaautoantibodies associated with basal-like breast cancers. Cancer Epidemiol Biomarkers Prev 2015; 24: 1,332–40.CrossRefGoogle ScholarPubMed
Aarabi, M, Modarressi, MH, Soltanghoraee, H, Behjati, R, Amirjannati, N, Akhondi, MM. Testicular expression of synaptonemal complex protein 3 (SYCP3) messenger ribonucleic acid in 110 patients with nonobstructive azoospermia. Fertil Steril 2006; 86: 325–31.CrossRefGoogle ScholarPubMed
Jungbluth, AA, Ely, S, DiLiberto, M, Niesvizky, R, Williamson, B, Frosina, D, Chen, YT, Bhardwaj, N, Chen-Kiang, S, Old, LJ, Cho, HJ. The cancer-testis antigens CT7 (MAGE-C1) and MAGE-A3/6 are commonly expressed in multiple myeloma and correlate with plasma-cell proliferation. Blood 2005; 106: 167–74.CrossRefGoogle ScholarPubMed
Mobasheri, MB, Jahanzad, I, Mohagheghi, MA, Aarabi, M, Farzan, S, Modarressi, MH. Expression of two testis-specific genes, TSGA10 and SYCP3, in different cancers regarding to their pathological features. Cancer Detect Prev 2007; 31: 296302.CrossRefGoogle ScholarPubMed
Gjerstorff, MF, Andersen, MH, Ditzel, HJ. Oncogenic cancer/testis antigens: Prime candidates for immunotherapy. Oncotarget 2015; 6(18): 15,772–87.CrossRefGoogle ScholarPubMed
Lim, SH, Zhang, Y, Zhang, J. Cancer–testis antigens: The current status on antigen regulation and potential clinical use. Am J Blood Res 2012; 2(1): 2935.Google ScholarPubMed
Chan, SW, Lim, CJ, Huang, C, Chong, YF, Gunaratne, HJ, Hogue, KA, Blackstock, WP, Harvey, KF, Hong, W. WW domain-mediated interaction with Wbp2 is important for the oncogenic property of TAZ. Oncogene 2010; 30: 600–10.Google ScholarPubMed
Li, J, Liu, J, Ren, Y, Liu, P. Roles of the WWOX in pathogenesis and endocrine therapy of breast cancer. Exp Biol Med (Maywood) 2014; 240: 324–8.Google ScholarPubMed
Saunders, CM, Larman, MG, Parrington, J, Cox, LJ, Royse, J, Blayney, LM, Swann, K, Lai, FA. PLC zeta: A sperm-specific trigger of Ca(2+) oscillations in eggs and embryo development. Development 2002; 129: 3,533–44.Google ScholarPubMed
Kaewmala, K, Uddin, MJ, Cinar, MU, Grosse-Brinkhaus, C, Jonas, E, Tesfaye, D, Phatsara, C, Tholen, E, Looft, C, Schellander, K. Investigation into association and expression of PLCz and COX-2 as candidate genes for boar sperm quality and fertility. Reprod Domest Anim 2012; 47: 213–23.CrossRefGoogle ScholarPubMed
Zhu, H, Zhu, JX, Lo, PS, Li, J, Leung, KM, Rowlands, DK, Tsang, LL, Yu, MK, Jiang, JL, Lam, SY, Chung, YW, Zhou, Z, Sha, J, Chan, HC. Rescue of defective pancreatic secretion in cystic-fibrosis cells by suppression of a novel isoform of phospholipase C. Lancet 2003; 362: 2,059–65.CrossRefGoogle ScholarPubMed
Igarashi, H, Knott, JG, Schultz, RM, Williams, CJ. Alterations of PLCbeta1 in mouse eggs change calcium oscillatory behavior following fertilization. Dev Biol 2007; 312: 321–30.CrossRefGoogle ScholarPubMed
Bedford-Guaus, SJ, McPartlin, LA, Xie, J, Westmiller, SL, Buffone, MG, Roberson, MS. Molecular cloning and characterization of phospholipase C zeta in equine sperm and testis reveals species-specific differences in expression of catalytically active protein. Biol Reprod 2011; 85: 7888.CrossRefGoogle ScholarPubMed
Young, C, Grasa, P, Coward, K, Davis, LC, Parrington, J. Phospholipase C zeta undergoes dynamic changes in its pattern of localization in sperm during capacitation and the acrosome reaction. Fertil Steril 2009; 91: 2,230–42.CrossRefGoogle ScholarPubMed
Bi, Y, Xu, WM, Wong, HY, Zhu, H, Zhou, ZM, Chan, HC, Sha, JH. NYD-SP27, a novel intrinsic decapacitation factor in sperm. Asian J Androl 2009; 11: 229–39.CrossRefGoogle ScholarPubMed
Amdani, SN, Yeste, M, Jones, C, Coward, K. Sperm factors and oocyte activation: Current controversies and considerations. Biol Reprod 2015; 93: 50.CrossRefGoogle ScholarPubMed
Ito, J, Nagaoka, K, Kuroda, K, Kawano, N, Yoshida, K. Arrest of spermatogenesis at round spermatids in PLCZ1-deficient mice. In 11th International Symposium on Spermatology. Okinawa, Japan, 2010.Google Scholar
Miao, YL, Williams, CJ. Calcium signaling in mammalian egg activation and embryo development: the influence of subcellular localization. Mol Reprod Dev 2012; 79: 742–56.CrossRefGoogle ScholarPubMed
Rogers, CS, Stoltz, DA, Meyerholz, DK, Ostedgaard, LS, Rokhlina, T, Taft, PJ, Rogan, MP, Pezzulo, AA, Karp, PH, Itani, OA, Kabel, AC, Wohlford-Lenane, CL, Davis, GJ, Hanfland, RA, Smith, TL, Samuel, M, Wax, D, Murphy, CN, Rieke, A, Whitworth, K, Uc, A, Starner, TD, Brogden, KA, Shilyansky, J, McCray, PB Jr., Zabner, J, Prather, RS, Welsh, MJ. Disruption of the CFTR gene produces a model of cystic fibrosis in newborn pigs. Science 2008; 321: 1,837–41.CrossRefGoogle ScholarPubMed
International Mouse Phenotyping Consortium. (2015). Available at
Chen, M, Wang, H, Li, X, Li, N, Xu, G, Meng, Q. PLIN1 deficiency affects testicular gene expression at the meiotic stage in the first wave of spermatogenesis. Gene 2014; 543: 212–9.CrossRefGoogle ScholarPubMed
Wang, H, Wang, C, Yang, K, Liu, J, Zhang, Y, Wang, Y, Xu, X, Michal, JJ, Jiang, Z, Liu, B. Genome wide distributions and functional characterization of copy number variations between Chinese and Western pigs. PLoS One 2015; 10: e0131522.CrossRefGoogle ScholarPubMed
Neri, QV, Lee, B, Rosenwaks, Z, Machaca, K, Palermo, GD. Understanding fertilization through intracytoplasmic sperm injection (ICSI). Cell Calcium 2014; 55: 2437.CrossRefGoogle Scholar
Yanagida, K. Complete fertilization failure in ICSI. Hum Cell 2004; 17: 187–93.Google ScholarPubMed
Yamano, S, Nakagawa, K, Nakasaka, H, Aono, T. Fertilization failure and oocyte activation. J Med Invest 2000; 47: 18.Google ScholarPubMed
Yeste, M, Jones, C, Amdani, SN, Patel, S, Coward, K. Oocyte activation deficiency: A role for an oocyte contribution? Hum Reprod Update 2016; 22(1): 2347.CrossRefGoogle ScholarPubMed
Hewitson, L, Dominko, T, Takahashi, D, Martinovich, C, Ramalho-Santos, J, Sutovsky, P, Fanton, J, Jacob, D, Monteith, D, Neuringer, M, Battaglia, D, Simerly, C, Schatten, G. Unique checkpoints during the first cell cycle of fertilization after intracytoplasmic sperm injection in rhesus monkeys. Nat Med 1999; 5: 431–3.Google ScholarPubMed
Terada, Y, Luetjens, CM, Sutovsky, P, Schatten, G. Atypical decondensation of the sperm nucleus, delayed replication of the male genome, and sex chromosome positioning following intracytoplasmic human sperm injection (ICSI) into golden hamster eggs: Does ICSI itself introduce chromosomal anomalies? Fertil Steril 2000; 74: 454–60.CrossRefGoogle ScholarPubMed
Huang, T, Kimura, Y, Yanagimachi, R. The use of piezo micromanipulation for intracytoplasmic sperm injection of human oocytes. J Assist Reprod Genet 1996; 13: 320–8.CrossRefGoogle Scholar
Kimura, Y, Yanagimachi, R. Intracytoplasmic sperm injection in the mouse. Biol Reprod 1995; 52: 709–20.CrossRefGoogle ScholarPubMed
Katayama, M, Rieke, A, Cantley, T, Murphy, C, Dowell, L, Sutovsky, P, Day, BN. Improved fertilization and embryo development resulting in birth of live piglets after intracytoplasmic sperm injection and in vitro culture in a cysteine-supplemented medium. Theriogenology 2007; 67: 835–47.CrossRefGoogle Scholar
Takeuchi, T, Colombero, LT, Neri, QV, Rosenwaks, Z, Palermo, GD. Does ICSI require acrosomal disruption? An ultrastructural study. Hum Reprod 2004; 19: 114–7.CrossRefGoogle ScholarPubMed
Cited by

Save book to Kindle

To save this book to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the or variations. ‘’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats