Investigation of the mechanisms by which the molecular chaperone HSPA2 regulates the expression of sperm surface receptors involved in human sperm-oocyte recognition

Molecular Human Reproduction

Volumn 19, Issue 3, 2013, Pages 120-135

  Redgrove, Kate A ^a   Anderson, Amanda L ^a   McLaughlin, Eileen A ^a   O'Bryan, Moira K ^a,b   Aitken, R John ^a   Nixon, Brett ^a  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Capacitation; Hspa2; Molecular chaperone; Spermatozoa; Zona pellucida

Indexed keywords

CELL ADHESION MOLECULE; CEREBROSIDE SULFATASE; CHAPERONE; CHOLESTEROL; CYCLIC AMP DEPENDENT PROTEIN KINASE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 2; PROTEIN TYROSINE KINASE INHIBITOR; SPERM ADHESION MOLECULE 1; UNCLASSIFIED DRUG;

ARTICLE; BIOCHEMISTRY; BIOPHYSICS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CUMULUS CELL; CYTOARCHITECTURE; EJACULATION; FEMALE GENITAL SYSTEM; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMUNOLOCALIZATION; MALE; MEMBRANE FLUIDITY; OOCYTE; OOCYTE DEVELOPMENT; OVULATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN ENGINEERING; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SPERM; SPERMATOZOON; SPERMATOZOON CAPACITATION; SPERMATOZOON HEAD; SURFACE PROPERTY;

CELL ADHESION MOLECULES; CELLS, CULTURED; CEREBROSIDE-SULFATASE; CHOLESTEROL; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HSP70 HEAT-SHOCK PROTEINS; HUMANS; HYALURONOGLUCOSAMINIDASE; MALE; MEMBRANE MICRODOMAINS; OOCYTES; PROTEIN KINASE INHIBITORS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SPERM CAPACITATION; SPERM HEAD; SPERM-OVUM INTERACTIONS; ZONA PELLUCIDA;

MAMMALIA;

EID: 84876460101     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gas064     Document Type: Article

References (98)

1. Ahuja KK, Gilbert DJ. Involvement of sperm sulphatases in early spermzona interactions in the hamster. J Cell Sci 1985;78:247-261.
2. Asquith KL, Baleato RM, McLaughlin EA, Nixon B, Aitken RJ. Tyrosine phosphorylation activates surface chaperones facilitating sperm-zona recognition. J Cell Sci 2004;117:3645-3657.
3. Austin CR. Observations on the penetration of the sperm in the mammalian egg. Aust J Sci Res 1951;4:581-596.
4. Baba D, Kashiwabara S, Honda A, Yamagata K, Wu Q, Ikawa M, Okabe M, Baba T. Mouse sperm lacking cell surface hyaluronidase PH-20 can pass through the layer of cumulus cells and fertilize the egg. J Biol Chem 2002;277:30310-30314.
5. Baker MA, Lane DJ, Ly JD, De Pinto V, Lawen A. VDAC1 is a transplasma membrane NADH-ferricyanide reductase. J Biol Chem 2004; 279:4811-4819.
6. Baker MA, Hetherington L, Aitken RJ. Identification of SRC as a key PKA-stimulated tyrosine kinase involved in the capacitation-associated hyperactivation of murine spermatozoa. J Cell Sci 2006;119:3182-3192.
7. Baker MA, Reeves G, Hetherington L, Aitken RJ. Analysis of proteomic changes associated with sperm capacitation through the combined use of IPG-strip pre-fractionation followed by RP chromatography LC-MS/ MS analysis. Proteomics 2010;10:482-495.
8. Baker MA, Nixon B, Naumovski N, Aitken RJ. Proteomic insights into the maturation and capacitation of mammalian spermatozoa. Syst Biol Reprod Med 2012;58:211-217.
9. Bhasin S. Approach to the infertile man. J Clin Endocrinol Metab 2007; 92:1995-2004.
10. Biggers JD, Whitten WK, Whittingham DG. The culture of mouse embryos in vitro. In: Daniel JCJ (ed.). Methods in Mammalian Embryology. San Francisco, CA: Freeman Press, 1971, 86-116.
11. Carmona E, Weerachatyanukul W, Soboloff T, Fluharty AL, White D, Promdee L, Ekker M, Berger T, Buhr M, Tanphaichitr N. Arylsulfatase a is present on the pig sperm surface and is involved in sperm-zona pellucida binding. Dev Biol 2002a;247:182-196.
12. Carmona E, Weerachatyanukul W, Xu H, Fluharty A, Anupriwan A, Shoushtarian A, Chakrabandhu K, Tanphaichitr N. Binding of arylsulfatase A to mouse sperm inhibits gamete interaction and induces the acrosome reaction. Biol Reprod 2002b;66:1820-1827.
13. Chang MC. Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature 1951;168:697-698.
14. Cherr GN, Meyers SA, Yudin AI, VandeVoort CA, Myles DG, Primakoff P, Overstreet JW. The PH-20 protein in cynomolgus macaque spermatozoa: identification of two different forms exhibiting hyaluronidase activity. Dev Bio 1996;175:142-153.
15. Cherr GN, Yudin AI, Overstreet JW. The dual functions of GPI-anchored PH-20: hyaluronidase and intracellular signaling. Matrix Biol 2001; 20:515-525.
16. Cho C, Bunch DO, Faure JE, Goulding EH, Eddy EM, Primakoff P, Myles DG. Fertilization defects in sperm from mice lacking fertilin beta. Science 1998;281:1857-1859.
17. Cooper TG. The Epididymis, Sperm Maturation and Fertilisation, 1st edn. Berlin, Germany: Springer-Verlag, 1986.
18. Cowan AE, Primakoff P, Myles DG. Sperm exocytosis increases the amount of PH-20 antigen on the surface of guinea pig sperm. J Cell Biol 1986;103:1289-1297.
19. Cross NL. Role of cholesterol in sperm capacitation. Biol Reprod 1998; 59:7-11.
20. Cross NL. Decrease in order of human sperm lipids during capacitation. Biol Reprod 2003;69:529-534.
21. Cross NL. Reorganization of lipid rafts during capacitation of human sperm. Biol Reprod 2004;71:1367-1373.
22. de Lamirande E, Leclerc P, Gagnon C. Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol Hum Reprod 1997;3:175-194.
23. de Vries KJ, Wiedmer T, Sims PJ, Gadella BM. Caspase-independent exposure of aminophospholipids and tyrosine phosphorylation in bicarbonate responsive human sperm cells. Biol Reprod 2003; 68:2122-2134.
24. Dudkiewicz AB. Purification of boar acrosomal arylsulfatase A and possible role in the penetration of cumulus cells. Biol Reprod 1984; 30:1005-1014.
25. Dun MD, Smith ND, Baker MA, Lin M, Aitken RJ, Nixon B. The chaperonin containing TCP1 complex (CCT/TRiC) is involved in mediating sperm- oocyte interaction. J Biol Chem 2011;286:36875-36887.
26. Eckhardt M. The role and metabolism of sulfatide in the nervous system. Mol Neurobiol 2008;37:93-103.
27. Ecroyd H, Jones RC, Aitken RJ. Tyrosine phosphorylation of HSP-90 during mammalian sperm capacitation. Biol Reprod 2003;69:1801-1807.
28. Ensslin MA, Shur BD. Identification of mouse sperm SED1, a bimotif EGF repeat and discoidin-domain protein involved in sperm-egg binding. Cell 2003;114:405-417.
29. Fenichel P, Cervoni F, Hofmann P, Deckert M, Emiliozzi C, Hsi BL, Rossi B. Expression of the complement regulatory protein CD59 on human spermatozoa: characterization and role in gametic interaction. Mol Reprod Dev 1994;38:338-346.
30. Gadella BM. The assembly of a zona pellucida binding protein complex in sperm. Reprod Dom Anim Zuch 2008a;43(Suppl. 5):12-19.
31. Gadella BM. Sperm membrane physiology and relevance for fertilization. Anim Reprod Sci 2008b;107:229-236.
32. Gadella BM, Tsai PS, Boerke A, Brewis IA. Sperm head membrane reorganisation during capacitation. Int J Dev Biol 2008;52:473-480.
33. Gmachl M, Sagan S, Ketter S, Kreil G. The human sperm protein PH-20 has hyaluronidase activity. FEBS Lett 1993;336:545-548.
34. Govin J, Caron C, Escoffier E, Ferro M, Kuhn L, Rousseaux S, Eddy EM, Garin J, Khochbin S. Post-meiotic shifts in HSPA2/HSP70.2 chaperone activity during mouse spermatogenesis. J Biol Chem 2006; 281:37888-37892.
35. Harrison RA. Rapid PKA-catalysed phosphorylation of boar sperm proteins induced by the capacitating agent bicarbonate. Mol Reprod Dev 2004;67:337-352.
36. Harrison RA, Gadella BM. Bicarbonate-induced membrane processing in sperm capacitation. Theriogenology 2005;63:342-351.
37. Harrison RA, Miller NG. cAMP-dependent protein kinase control of plasma membrane lipid architecture in boar sperm. Mol Reprod Dev 2000;55:220-228.
38. Harrison RA, Ashworth PJ, Miller NG. Bicarbonate/CO2, an effector of capacitation, induces a rapid and reversible change in the lipid architecture of boar sperm plasma membranes. Mol Reprod Dev 1996; 45:378-391.
39. Huang TT, Kosower NS, Yanagimachi R. Localization of thiol and disulfide groups in guinea pig spermatozoa during maturation and capacitation using bimane fluorescent labels. Biol Reprod 1984;31:797-809.
40. Hunnicutt GR, Primakoff P, Myles DG. Sperm surface protein PH-20 is bifunctional: one activity is a hyaluronidase and a second, distinct activity is required in secondary sperm-zona binding. Biol Reprod 1996;55:80-86.
41. Huszar G, Vigue L, Oehninger S. Creatine kinase immunocytochemistry of human sperm-hemizona complexes: selective binding of sperm with mature creatine kinase-staining pattern. Fert Steril 1994;61:136-142.
42. Huszar G, Sbracia M, Vigue L, Miller DJ, Shur BD. Sperm plasma membrane remodeling during spermiogenetic maturation in men: relationship among plasma membrane beta 1,4-galactosyltransferase, cytoplasmic creatine phosphokinase, and creatine phosphokinase isoform ratios. Biol Reprod 1997;56:1020-1024.
43. Huszar G, Ozkavukcu S, Jakab A, Celik-Ozenci C, Sati GL, Cayli S. Hyaluronic acid binding ability of human sperm reflects cellular maturity and fertilizing potential: selection of sperm for intracytoplasmic sperm injection. Curr Opin Obstet Gynecol 2006; 18:260-267.
44. Huszar G, Jakab A, Sakkas D, Ozenci CC, Cayli S, Delpiano E, Ozkavukcu S. Fertility testing and ICSI sperm selection by hyaluronic acid binding: clinical and genetic aspects. Reprod Biomed Online 2007; 14:650-663.
45. Jones R,Williams RM. Identification of zona- and fucoidan-binding proteins in guinea-pig spermatozoa and mechanism of recognition. Development 1990;109:41-50.
46. Jones R, Parry R, Lo Leggio L, Nickel P. Inhibition of sperm-zona binding by suramin, a potential 'lead' compound for design of new anti-fertility agents. Mol Hum Reprod 1996;2:597-605.
47. Jones R, Howes E, Dunne PD, James P, Bruckbauer A, Klenerman D. Tracking diffusion of GM1 gangliosides and zona pellucida binding molecules in sperm plasma membranes following cholesterol efflux. Dev Biol 2010;339:398-406.
48. KangW, Zhou C, Koga Y, Baba T. Hyaluronan-degrading activity of mouse sperm hyaluronidase is not required for fertilization J Reprod Dev 2010; 56:140-144.
49. Kimura M, Kim E, Kang W, Yamashita M, Saigo M, Yamazaki T, Nakanishi T, Kashiwabara S, Baba T. Functional roles of mouse sperm hyaluronidases, HYAL5 and SPAM1, in fertilization. Biol Reprod 2009; 81:939-947.
50. Lathrop WF, Carmichael EP, Myles DG, Primakoff P. cDNA cloning reveals the molecular structure of a sperm surface protein, PH-20, involved in sperm-egg adhesion and the wide distribution of its gene among mammals. J Cell Biol 1990;111:2939-2949.
51. Leclerc P, de Lamirande E, Gagnon C. Cyclic adenosine 3′,5′ monophosphate-dependent regulation of protein tyrosine phosphorylation in relation to human sperm capacitation and motility. Biol Reprod 1996;55:684-692.
52. Leclerc P, de Lamirande E, Gagnon C. Interaction between Ca2+, cyclic 3′,5′ adenosine monophosphate, the superoxide anion, and tyrosine phosphorylation pathways in the regulation of human sperm capacitation. J Androl 1998;19:434-443.
53. Lefievre L, Jha KN, de Lamirande E, Visconti PE, Gagnon C. Activation of protein kinase A during human sperm capacitation and acrosome reaction. J Androl 2002;23:709-716.
54. Liu DY, Baker HW. Defective sperm-zona pellucida interaction: a major cause of failure of fertilization in clinical in-vitro fertilization. Hum Reprod 2000;15:702-708.
55. Lu Q, Shur BD. Sperm from beta 1,4-galactosyltransferase-null mice are refractory to ZP3-induced acrosome reactions and penetrate the zona pellucida poorly. Development 1997;124:4121-4131.
56. McLachlan RI, de Kretser DM. Male infertility: the case for continued research. Med J Aust 2001;174:116-117.
57. Mehl E, Jatzkewitz H. Cerebroside 3-sulfate as a physiological substrate of arylsulfatase A. Biochim Biophys Acta 1968;151:619-627.
58. Mitchell LA, Nixon B, Aitken RJ. Analysis of chaperone proteins associated with human spermatozoa during capacitation. Mol Human Reprod 2007; 13:605-613.
59. Mitchell LA, Nixon B, Baker MA, Aitken RJ. Investigation of the role of SRC in capacitation-associated tyrosine phosphorylation of human spermatozoa. Mol Hum Reprod 2008;14:235-243.
60. Myles DG, Primakoff P. Localized surface antigens of guinea pig sperm migrate to new regions prior to fertilization. J Cell Biol 1984; 99:1634-1641.
61. Nishimura H, Cho C, Branciforte DR, Myles DG, Primakoff P. Analysis of loss of adhesive function in sperm lacking cyritestin or fertilin beta. Dev Biol 2001;233:204-213.
62. Nixon B, Aitken RJ, McLaughlin EA. New insights into the molecular mechanisms of sperm-egg interaction. Cell Mol Life Sci 2007; 64:1805-1823.
63. Nixon B, Bielanowicz A, McLaughlin EA, Tanphaichitr N, Ensslin MA, Aitken RJ. Composition and significance of detergent resistant membranes in mouse spermatozoa. J Cell Physiol 2009;218:122-134.
64. Nixon B, Mitchell LA, Anderson AL, McLaughlin EA, O'Bryan MK, Aitken RJ. Proteomic and functional analysis of human sperm detergent resistant membranes. J Cell Physiol 2011;226:2651-2665.
65. Nixon B, Paul JW, Spiller CM, Attwell-Heap AG, Ashman LK, Aitken RJ. Evidence for the involvement of PECAM-1 in a receptor mediated signal-transduction pathway regulating capacitation-associated tyrosine phosphorylation in human spermatozoa. J Cell Sci 2005;118: 4865-4877.
66. O'Rand MG, Widgren EE, Fisher SJ. Characterization of the rabbit sperm membrane autoantigen, RSA, as a lectin-like zona binding protein. Dev Biol 1988;129:231-240.
67. Osheroff JE, Visconti PE, Valenzuela JP, Travis AJ, Alvarez J, Kopf GS. 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. Mol Hum Reprod 1999;5:1017-1026.
68. Panaretou B, Siligardi G, Meyer P, Maloney A, Sullivan JK, Singh S, Millson SH, Clarke PA, Naaby-Hansen S, Stein R et al. Activation of the ATPase activity of hsp90 by the stress-regulated cochaperone aha1. Mol Cell 2002;10:1307-1318.
69. Phelps BM, Myles DG. The guinea pig sperm plasma membrane protein, PH-20, reaches the surface via two transport pathways and becomes localized to a domain after an initial uniform distribution. Dev Biol 1987;123:63-72.
70. Prasad SV, Skinner SM, Carino C, Wang N, Cartwright J, Dunbar BS. Structure and function of the proteins of the mammalian Zona pellucida. Cells Tissues Organs 2000;166:148-164.
71. Primakoff P, Hyatt H, Myles DG. A role for the migrating sperm surface antigen PH-20 in guinea pig sperm binding to the egg zona pellucida. J Cell Biol 1985;101:2239-2244.
72. Rahi H, Srivastava PN. Isolation and characterization of the pig endometrial arylsulphatase A. Biochem J 1983;211:649-659.
73. Rattanachaiyanont M, Weerachatyanukul W, Leveille MC, Taylor T, D'Amours D, Rivers D, Leader A, Tanphaichitr N. Anti-SLIP1-reactive proteins exist on human spermatozoa and are involved in zona pellucida binding. Mol Hum Reprod 2001;7:633-640.
74. Redgrove KA, Anderson AL, Dun MD, McLaughlin EA, O'Bryan MK, Aitken RJ, Nixon B. Involvement of multimeric protein complexes in mediating the capacitation-dependent binding of human spermatozoa to homologous zonae pellucidae. Dev Biol 2011;356:460-474.
75. Redgrove KA, Nixon B, Baker MA, Hetherington L, Baker G, De-Yi L, Aitken RJ. The molecular chaperone HSPA2 plays a key role in regulating the expression of sperm surface receptors that mediate sperm-egg recognition. PLoS One 2012;7:e50851.
76. Reid AT, Redgrove K, Aitken RJ, Nixon B. Cellular mechanisms regulating sperm-zona pellucida interaction. Asian J Androl 2010;13:88-96.
77. Sabeur K, Cherr GN, Yudin AI, Primakoff P, Li MW, Overstreet JW. The PH-20 protein in human spermatozoa. J Androl 1997;18:151-158.
78. Schenk M, Koppisetty CA, Santos DC, Carmona E, Bhatia S, Nyholm PG, Tanphaichitr N. Interaction of arylsulfatase-A (ASA) with its natural sulfoglycolipid substrates: a computational and site-directed mutagenesis study. Glycoconj J 2009;26:1029-1045.
79. Shadan S, James PS, Howes EA, Jones R. Cholesterol efflux alters lipid raft stability and distribution during capacitation of boar spermatozoa. Biol Reprod 2004;71:253-265.
80. Shamsadin R, Adham IM, Nayernia K, Heinlein UA, Oberwinkler H, Engel W. Male mice deficient for germ-cell cyritestin are infertile. Biol Reprod 1999;61:1445-1451.
81. Tanphaichitr N, Smith J, Kates M. Levels of sulfogalactosylglycerolipid in capacitated motile and immotile mouse spermatozoa. Biochem Cell Biol 1990;68:528-535.
82. Tanphaichitr N, Smith J, Mongkolsirikieart S, Gradil C, Lingwood CA. Role of a gamete-specific sulfoglycolipid immobilizing protein on mouse sperm-egg binding. Dev Biol 1993;156:164-175.
83. Tanphaichitr N, Moase C, Taylor T, Surewicz K, Hansen C, Namking M, Berube B, Kamolvarin N, Lingwood CA, Sullivan R et al. Isolation of antiSLIP1-reactive boar sperm P68/62 and its binding to mammalian zona pellucida. Mol Reprod Dev 1998;49:203-216.
84. Tantibhedhyangkul J,WeerachatyanukulW, Carmona E, Xu H, AnupriwanA, MichaudD, TanphaichitrN. Role of spermsurface arylsulfatase A inmouse sperm-zona pellucida binding. Biol Reprod 2002;67:212-219.
85. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 1979;76:4350-4354.
86. Travis AJ, Kopf GS. The role of cholesterol efflux in regulating the fertilization potential of mammalian spermatozoa. J Clin Invest 2002;110:731-736.
87. Visconti PE, Bailey JL, Moore GD, Pan D, Olds-Clarke P, Kopf GS. Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development 1995a;121:1129-1137.
88. Visconti PE, Moore GD, Bailey JL, Leclerc P, Connors SA, Pan D, Olds-Clarke P, Kopf GS. Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development 1995b;121:1139-1150.
89. Visconti PE, Ning X, Fornes MW, Alvarez JG, Stein P, Connors SA, Kopf GS. Cholesterol efflux-mediated signal transduction in mammalian sperm: cholesterol release signals an increase in protein tyrosine phosphorylation during mouse sperm capacitation. Dev Biol 1999;214:429-443.
90. Visconti PE, Westbrook VA, Chertihin O, Demarco I, Sleight S, Diekman AB. Novel signaling pathways involved in sperm acquisition of fertilizing capacity. J Reprod Immunol 2002;53:133-150.
91. Vos MJ, Hageman J, Carra S, Kampinga HH. Structural and functional diversities between members of the human HSPB, HSPH, HSPA, and DNAJ chaperone families. Biochemistry 2008;47:7001-7011.
92. Weerachatyanukul W, Rattanachaiyanont M, Carmona E, Furimsky A, Mai A, Shoushtarian A, Sirichotiyakul S, Ballakier H, Leader A, Tanphaichitr N. Sulfogalactosylglycerolipid is involved in human gamete interaction. Mol Reprod Dev 2001;60:569-578.
93. Weerachatyanukul W, Xu H, Anupriwan A, Carmona E, Wade M, Hermo L, da Silva SM, Rippstein P, Sobhon P, Sretarugsa P et al. Acquisition of arylsulfatase A onto the mouse sperm surface during epididymal transit. Biol Reprod 2003;69:1183-1192.
94. White D, Weerachatyanukul W, Gadella B, Kamolvarin N, Attar M, Tanphaichitr N. Role of sperm sulfogalactosylglycerolipid in mouse sperm-zona pellucida binding. Biol Reprod 2000;63:147-155.
95. Wu A, Anupriwan A, Iamsaard S, Chakrabandhu K, Santos DC, Rupar T, Tsang BK, Carmona E, Tanphaichitr N. Sperm surface arylsulfatase A can disperse the cumulus matrix of cumulus oocyte complexes. J Cell Physiol 2007;213:201-211.
96. Xu H, Liu F, Srakaew N, Koppisetty C, Nyholm PG, Carmona E, Tanphaichitr N. Sperm arylsulfatase A binds to mZP2 and mZP3 glycoproteins in a nonenzymatic manner. Reproduction 2012; 144:209-219.
97. Yanagimachi R. Fertility of mammalian spermatozoa: its development and relativity. Zygote 1994;2:371-372.
98. Yanagimachi R, Lopata A, Odom CB, Bronson RA, Mahi CA, Nicolson GL. Retention of biologic characteristics of zona pellucida in highly concentrated salt solution: the use of salt-stored eggs for assessing the fertilizing capacity of spermatozoa. Fert Steril 1979;31:562-574.