The composition, protein genesis and significance of the inner acrosomal membrane of eutherian sperm

Cell and Tissue Research

Volumn 349, Issue 3, 2012, Pages 733-748

  Ferrer, Marvin ^a   Xu, Wei ^a   Oko, Richard ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

Acrosomal biogenesis; Fertilization; Inner acrosomal membrane; Spermatozoa; Spermiogenesis

Indexed keywords

GELATINASE A; INNER ACROSOMAL MEMBRANE PROTEIN; MEMBRANE PROTEIN; PROACROSIN; SPERM ACROSOME MEMBRANE PROTEIN 14; UNCLASSIFIED DRUG;

ACROSOME; ACROSOME REACTION; CELL FRACTIONATION; CELL NUCLEUS; CELL VACUOLE; FERTILIZATION; MALE; METAPHASE; NONHUMAN; OOCYTE; PLACENTAL MAMMALS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REVIEW; SPERMATOGENESIS; SPERMATOZOON; THECA CELL; ZONA PELLUCIDA;

ACROSOME REACTION; ANIMALS; FERTILIZATION; HUMANS; MALE; SPERMATIDS; SPERMATOGENESIS; SPERMATOZOA;

EUTHERIA;

EID: 84866386456     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-012-1433-5     Document Type: Review

References (56)

1. Adham IM, Nayernia K, Engel W (1997) Spermatozoa lacking acrosin protein show delayed fertilization. Mol Reprod Dev 46:370-376
2. Aul RB, Oko R (2002) The major subacrosomal occupant of bull spermatozoa is a novel histone H2B variant associated with the forming acrosome during spermiogenesis. Dev Biol 242:376-387
3. Baba T, Azuma S, Kashiwabara S, Toyoda Y (1994) Sperm from mice carrying a targeted mutation of the acrosin gene can penetrate the oocyte zona pellucida and effect fertilization. J Biol Chem 269:31845-31849
4. Barth AD, Oko R (1989) Normal bovine spermatogenesis and sperm maturation. In: Barth AD, Oko R (eds) Abnormal morphology of bovine spermatozoa. Iowa State University Press, Ames, pp 19-88
5. Bleil JD, Wassarman PM (1986) Autoradiographic visualization of the mouse egg's sperm receptor bound to sperm. J Cell Biol 102:1363-1371
6. Bleil JD, Greve JM, Wassarman PM (1988) Identification of a secondary sperm receptor in the mouse egg zona pellucida: role in maintenance of binding of acrosome-reacted sperm to eggs. Dev Biol 128:376-385
7. Bülow M von, Heid H, Hess H, Franke WW (1995) Molecular nature of calicin, a major basic protein of the mammalian sperm head cytoskeleton. Exp Cell Res 219:407-413
8. Bülow Mvon, Rackwitz HR, Zimbelmann R, Franke WW (1997) 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 233:216-224
9. Cingolani G, Petosa C, Weis K, Muller CW (1999) Structure of importin-beta bound to the IBB domain of importin-alpha. Nature 399:221-229
10. Ferrer M, Rodriguez H, Zara L, Yu Y, Xu W, Oko R (2012) MMP2 and acrosin are major proteinases of the inner acrosomal membrane and may cooperate in sperm penetration of the zona pellucida during fertilization. Cell Tissue Res (in press)
11. Fraser LR (1982) p-Aminobenzamidine, an acrosin inhibitor, inhibits mouse sperm penetration of the zona pellucida but not the acrosome reaction. J Reprod Fertil 65:185-194
12. Frohnert C, Schweizer S, Hoyer-Fender S (2011) SPAG4L/SPAG4L-2 are testis-specific SUN domain proteins restricted to the apical nuclear envelope of round spermatids facing the acrosome. Mol Hum Reprod 17:207-218
13. Gerton GL (2002) Function of the acrosome. In: Hardy EM (ed) Fertilization. Academic Press, New York, pp 265-302
14. Gorlich D, Henklein P, Laskey RA, Hartmann E (1996) A 41 amino acid motif in importin-alpha confers binding to importin-beta and hence transit into the nucleus. EMBO J 15:1810-1817
15. Hao Z, Wolkowicz MJ, Shetty J, Klotz K, Bolling L, Sen B, Westbrook VA, Coonrod S, Flickinger CJ, Herr JC (2002) SAMP32, a testis-specific, isoantigenic sperm acrosomal membrane-associated protein. Biol Reprod 66:735-744
16. Heid H, Figge U, Winter S, Kuhn C, Zimbelmann R, Franke W (2002) Novel actin-related proteins Arp-T1 and Arp-T2 as components of the cytoskeletal calyx of the mammalian sperm head. Exp Cell Res 279:177-187
17. Hess H, Heid H, Franke WW (1993) Molecular characterization of mammalian cylicin, a basic protein of the sperm head cytoskeleton. J Cell Biol 122:1043-1052
18. Hess H, Heid H, Zimbelmann R, Franke WW (1995) The protein complexity of the cytoskeleton of bovine and human sperm heads: the identification and characterization of cylicin II. Exp Cell Res 218:174-182
19. Huang TT Jr, Yanagimachi R (1985) Inner acrosomal membrane of mammalian spermatozoa: its properties and possible functions in fertilization. Am J Anat 174:249-268
20. Inoue N, Satouh Y, Ikawa M, Okabe M, Yanagimachi R (2011) Acrosome-reacted mouse spermatozoa recovered from the perivitelline space can fertilize other eggs. Proc Natl Acad Sci USA 108:20008-20011
21. Jin M, Fujiwara E, Kakiuchi Y, Okabe M, Satouh Y, Baba SA, Chiba K, Hirohashi N (2011) Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization. Proc Natl Acad Sci USA 108:4892-4896
22. Jones R, James PS, Oxley D, Coadwell J, Suzuki-Toyota F, Howes EA (2008) The equatorial subsegment in mammalian spermatozoa is enriched in tyrosine phosphorylated proteins. Biol Reprod 79:421-431
23. Kawano N, Kang W, Yamashita M, Koga Y, Yamazaki T, Hata T, Miyado K, Baba T (2010) Mice lacking two sperm serine proteases, ACR and PRSS21, are subfertile, but the mutant sperm are infertile in vitro. Biol Reprod 83:359-369
24. Kim KS, Foster JA, Kvasnicka KW, Gerton GL (2011) Transitional states of acrosomal exocytosis and proteolytic processing of the acrosomal matrix in guinea pig sperm. Mol Reprod Dev 78:930-941
25. Lin YN, Roy A, Yan W, Burns KH, Matzuk MM (2007) Loss of zona pellucida binding proteins in the acrosomal matrix disrupts acrosome biogenesis and sperm morphogenesis. Mol Cell Biol 27:6794-6805
26. Lindstad RI, Sylte I, Mikalsen SO, Seglen PO, Berg E, Winberg JO (2005) Pancreatic trypsin activates human promatrix metalloproteinase-2. J Mol Biol 350:682-698
27. Miyamoto H, Chang MC (1973) Effects of protease inhibitors on the fertilizing capacity of hamster spermatozoa. Biol Reprod 9:533-537
28. Monea S, Lehti K, Keski-Oja J, Mignatti P (2002) Plasmin activates promatrix metalloproteinase-2 with a membrane-type 1 matrix metalloproteinase- dependent mechanism. J Cell Physiol 192:160-170
29. Mori E, Baba T, Iwamatsu A, Mori T (1993) Purification and characterization of a 38-kDa protein, Sp38, with zona pellucida-binding property from porcine epididymal sperm. Biochem Biophys Res Commun 196:196-202
30. Mori E, Kashiwabara S, Baba T, Inagaki Y, Mori T (1995) Amino acid sequences of porcine Sp38 and proacrosin required for binding to the zona pellucida. Dev Biol 168:575-583
31. Mortillo S, Wassarman PM (1991) Differential binding of gold-labeled zona pellucida glycoproteins mZP2 and mZP3 to mouse sperm membrane compartments. Development 113:141-149
32. Mountjoy JR, Xu W, McLeod D, Hyndman D, Oko R (2008) RAB2A: a major subacrosomal protein of bovine spermatozoa implicated in acrosomal biogenesis. Biol Reprod 79:223-232
33. Oko R (1995) Developmental expression and possible role of perinuclear theca proteins in mammalian spermatozoa. Reprod Fertil Dev 7:777-797
34. Oko R (1998) Occurrence and formation of cytoskeletal proteins in mammalian spermatozoa. Andrologia 30:193-206
35. Oko R, Maravei D (1994) Protein composition of the perinuclear theca of bull spermatozoa. Biol Reprod 50:1000-1014
36. Oko R, Maravei D (1995) Distribution and possible role of perinuclear theca proteins during bovine spermiogenesis. Microsc Res Tech 32:520-532
37. Oko R, Morales CR (1994) 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 166:235-245
38. Oko R, Sutovsky P (2009) Biogenesis of sperm perinuclear theca and its role in sperm functional competence and fertilization. J Reprod Immunol 83:2-7
39. Oko R, Aul R, Wu A, Sutovsky P (2001) The sperm head skeleton. In: Robaire B, Chemes H, Morales CR (eds) Andrology in 21st Century. Medimond, Englewood, pp 37-51
40. Oko R, Donald A, Xu W, Spoel AC van der (2011) Fusion failure of dense-cored proacrosomal vesicles in an inducible mouse model of male infertility. Cell Tissue Res 346:119-134
41. Sa SJ, Rhee HH, Cheong HT, Yang BK, Park CK (2006) Effects of plasmin on sperm-oocyte interactions during in vitro fertilization in the pig. Anim Reprod Sci 95:273-282
42. Saling PM (1981) Involvement of trypsin-like activity in binding of mouse spermatozoa to zonae pellucidae. Proc Natl Acad Sci USA 78:6231-6235
43. Shetty J, Wolkowicz MJ, Digilio LC, Klotz KL, Jayes FL, Diekman AB, Westbrook VA, Farris EM, Hao Z, Coonrod SA, Flickinger CJ, Herr JC (2003) SAMP14, a novel, acrosomal membrane-associated, glycosylphosphatidylinositol- anchored member of the Ly-6/urokinase-type plasminogen activator receptor superfamily with a role in sperm-egg interaction. J Biol Chem 278:30506-30515
44. Smokovitis A, Kokolis N, Taitzoglou I, Rekkas C (1992) Plasminogen activator: the identification of an additional proteinase at the outer acrosomal membrane of human and boar spermatozoa. Int J Fertil 37:308-314
45. Sutovsky P (2011) Sperm proteasome and fertilization. Reproduction 142:1-14
46. Taitzoglou I, Kokolis N, Smokovitis A (1996) Release of plasminogen activator and plasminogen activator inhibitor from spermatozoa of man, bull, ram and boar during acrosome reaction. Mol Androl 8:187-197
47. Tesarik J, Drahorad J, Peknicova J (1988) Subcellular immunochemical localization of acrosin in human spermatozoa during the acrosome reaction and zona pellucida penetration. Fertil Steril 50:133-141
48. Tovich PR, Oko RJ (2003) Somatic histones are components of the perinuclear theca in bovine spermatozoa. J Biol Chem 278:32431-32438
49. Tovich PR, Sutovsky P, Oko RJ (2004) Novel aspect of perinuclear theca assembly revealed by immunolocalization of non-nuclear somatic histones during bovine spermiogenesis. Biol Reprod 71:1182-1194
50. Tran MH, Aul RB, Xu W, Hoorn FA van der, Oko R (2011) Involvement of classical bipartite/karyopherin nuclear import pathway components in acrosomal trafficking and assembly during bovine and murid spermiogenesis. Biol Reprod 86:84
51. Wu AT, Sutovsky P, Manandhar G, Xu W, Katayama M, Day BN, Park KW, Yi YJ, Xi YW, Prather RS, Oko R (2007a) PAWP, a sperm-specific WW domain-binding protein, promotes meiotic resumption and pronuclear development during fertilization. J Biol Chem 282:12164-12175
52. Wu AT, Sutovsky P, Xu W, Spoel AC van der, Platt FM, Oko R (2007b) The postacrosomal assembly of sperm head protein, PAWP, is independent of acrosome formation and dependent on microtubular manchette transport. Dev Biol 312:471-483
53. Yang WX, Sperry AO (2003) C-terminal kinesin motor KIFC1 participates in acrosome biogenesis and vesicle transport. Biol Reprod 69:1719-1729
54. Yi YJ, Manandhar G, Sutovsky M, Zimmerman SW, Jonakova V, Leeuwen FW van, Oko R, Park CS, Sutovsky P (2010) Interference with the 19S proteasomal regulatory complex subunit PSMD4 on the sperm surface inhibits sperm-zona pellucida penetration during porcine fertilization. Cell Tissue Res 341:325-340
55. Yu Y, Xu W, Yi YJ, Sutovsky P, Oko R (2006) 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 290:32-43
56. Yu Y, Vanhorne J, Oko R (2009) The origin and assembly of a zona pellucida binding protein, IAM38, during spermiogenesis. Microsc Res Tech 72:558-565