Changes of the zona pellucida patterns during oocyte maturation, fertilization and embryo development in mammals: mini-review

1. Dunbar BS, Prasad SV, Timmons TM. Comparative structure and function of mammalian zonae pellucidae. In Dunbar BS & O’Rand MG, eds. A Comparative Overview of Mammalian Fertilization. Boston. MA: Springer. 1991;97–114.10.1007/978-1-4757-8982-9_6 Search in Google Scholar

2. Dunbar BS, Avery S, Lee V, Prasad S, Schwahn D, Schwoebel E, Skinner S, Wilkins B. The mammalian zona pellucida: its biochemistry, immunochemistry, molecular biology, and developmental expression. Reprod Fertil Dev. 1994;6:331–347; DOI:10.1071/rd9940331.10.1071/RD9940331 Search in Google Scholar

3. Epifano O, Dean J. Biology and structure of the zona pellucida: a target for immunocontraception. Reprod Fertil Dev. 1994;6:319–330; DOI:10.1071/rd9940319.10.1071/RD9940319 Search in Google Scholar

4. Kaji K, Kudo A. The mechanism of sperm-oocyte fusion in mammals. Reproduction. 2004;127:423–429; DOI:10.1530/rep.1.00163.10.1530/rep.1.0016315047933 Search in Google Scholar

5. Wassarman PM. Zona pellucida glycoproteins. Annu Rev Biochem. 1988;57:415–442; DOI:10.1146/annurev.bi.57.070188.002215.10.1146/annurev.bi.57.070188.0022153052278 Search in Google Scholar

6. Yanagimachi R. Mammalian fertilization in physiology of reproduction. In: Knobil E, Neill JD, eds. New York: Raven Press. 1994;189–317. Search in Google Scholar

7. Tulsiani DR, Yoshida-Komiya H, Araki Y. Mammalian fertilization: a carbohydrate-mediated event. Biol Reprod. 1997;57:487–494; DOI:10.1095/biolreprod57.3.487.10.1095/biolreprod57.3.4879282981 Search in Google Scholar

8. Santos P, Chaveiro A, Simoes N, Moreira da Silva F. Bovine oocyte quality in relation to ultrastructural characteristics of zona pellucida, polyspermic penetration and developmental competence. Reprod Domest Anim. 2008;43:685–689; DOI:10.1111/j.1439-0531.2007.00970.x.10.1111/j.1439-0531.2007.00970.x18484959 Search in Google Scholar

9. Vanroose G, Nauwynck H, Van Soom A, Ysebaert MT, Charlier G, Van Oostveldt P, de Kruif A. Structural aspects of the zona pellucida of in vitro-produced bovine embryos: a scanning electron and confocal laser scanning microscopic study. Biol Reprod. 2000;62:463–469; DOI:10.1095/biolreprod62.2.463.10.1095/biolreprod62.2.46310642588 Search in Google Scholar

10. Topfer-Petersen E, Ekhlasi-Hundrieser M, Tsolova M. Glycobiology of fertilization in the pig. Int J Dev Biol. 2008;52:717–736; DOI:10.1387/ijdb.072536et.10.1387/ijdb.072536et18649284 Search in Google Scholar

11. Wiesak T, Wasielak M, Złotkowska A, Milewski R. Effect of vitrification on the zona pellucida hardening and follistatin and cathepsin B genes expression and developmental competence of in vitro matured bovine oocytes. Cryobiology. 2017;76: 18–23; DOI:10.1016/j.cryobiol.2017.05.001.10.1016/j.cryobiol.2017.05.00128487134 Search in Google Scholar

12. Gupta SK. Human zona pellucida glycoproteins: binding characteristics with human spermatozoa and induction of acrosome reaction. Front Cell Dev Biol. 2021;9: 619868; DOI:10.3389/fcell.2021.619868.10.3389/fcell.2021.619868 Search in Google Scholar

13. Michelmann HW, Rath D, Topfer-Petersen E, Schwartz P. Structural and functional events on the porcine zona pellucida during maturation, fertilization and embryonic development: a scanning electron microscopy analysis. Reprod Domest Anim. 2007;42:594–602; DOI:10.1111/j.1439-0531.2006.00829.x.10.1111/j.1439-0531.2006.00829.x Search in Google Scholar

14. Nikas G, Paraschos T, Psychoyos A, Handyside AH. The zona reaction in human oocytes as seen with scanning electron microscopy. Hum Reprod. 1994;9:2135–2138; DOI:10.1093/oxfordjournals.humrep.a138405.10.1093/oxfordjournals.humrep.a138405 Search in Google Scholar

15. Anonymous. Recommendations for the sanitary handling of embryos. In: Stringfellow DA, Seidel SM (eds.). Manual of the International Embryo Transfer Society, 3th ed. Champaign, IL: International Embryo Transfer Society. 1998;26. Search in Google Scholar

16. Yudin AI, Cherr GN, Katz DF. Structure of the cumulus matrix and zona pellucida in the golden hamster: a new view of sperm interaction with oocyte-associated extracellular matrices, Cell Tissue Res. 1988;251: 555–564; DOI:10.1007/BF00214003.10.1007/BF00214003 Search in Google Scholar

17. Goudet G, Mugnier S, Callebaut I, Monget P. Phylogenetic analysis and identification of pseudogenes reveal a progressive loss of zona pellucida genes during evolution of vertebrates. Biol Reprod. 2008;78:796–806; DOI:10.1095/biolreprod.107.064568.10.1095/biolreprod.107.064568 Search in Google Scholar

18. Noguchi S, Yonezawa N, Katsumata T, Hashizume K, Kuwayama M, Hamano S, Watanabe S, Nakano M. Characterization of the zona pellucida glycoproteins from bovine ovarian and fertilized eggs. Biochim Biophys Acta. 1994;1201:7–14; DOI:10.1016/0304-4165(94)90143-0.10.1016/0304-4165(94)90143-0 Search in Google Scholar

19. Izquierdo-Rico MJ, Jimenez-Movilla M, Llop E, Perez-Oliva AB, Ballesta J, Gutierrez-Gallego R, Jimenez-Cervantes C, Aviles M. Hamster zona pellucida is formed by four glycoproteins: ZP1, ZP2, ZP3, and ZP4. J Proteome Res. 2009;8:926–941; DOI:10.1021/pr800568x.10.1021/pr800568x Search in Google Scholar

20. Stetson I, Aviles M, Moros C, Garcia-Vazquez FA, Gimeno L, Torrecillas A, Aliaga C, Bernardo-Pisa MV, Ballesta J, Izquierdo-Rico MJ. Four glycoproteins are expressed in the cat zona pellucida. Theriogenology. 2015;83:1162–1173; DOI:10.1016/j.theriogenology.2014.12.019.10.1016/j.theriogenology.2014.12.019 Search in Google Scholar

21. Wassarman PM. Mammalian fertilization: molecular aspects of gamete adhesion, exocytosis, and fusion. Cell. 1999;96:175–183; DOI:10.1016/s0092-8674(00)80558-9.10.1016/S0092-8674(00)80558-9 Search in Google Scholar

22. Wassarman PM, Jovine L, Litscher ES. A profile of fertilization in mammals. Nat Cell Biol. 2001;3:59–64; DOI:10.1038/35055178.10.1038/3505517811175768 Search in Google Scholar

23. Bleil JD, Greve JM, Wassarman PM. 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. 1988;128:376–385; DOI:10.1016/0012-1606(88)90299-0.10.1016/0012-1606(88)90299-0 Search in Google Scholar

24. Greve JM, Wassarman PM. Mouse egg extracellular coat is a matrix of interconnected filaments possessing a structural repeat. J Mol Biol. 1985;181:253–264; DOI:10.1016/0022-2836(85)90089-0.10.1016/0022-2836(85)90089-0 Search in Google Scholar

25. Litscher ES, Wassarman PM. A guide to zona pellucida domain proteins. Hoboken: John Wiley & Sons. 2015.10.1002/9781119044765 Search in Google Scholar

26. Bokhove M, Jovine L. Structure of zona pellucida module proteins. Curr Top Dev Biol. 2018;130:413–442; DOI:10.1016/bs.ctdb.2018.02.007.10.1016/bs.ctdb.2018.02.00729853186 Search in Google Scholar

27. Jovine L, Darie CC, Litscher ES, Wassarman PM. Zona pellucida domain proteins. Annu Rev Biochem. 2005;74:83–114; DOI:10.1146/annurev.biochem.74.082803.133039.10.1146/annurev.biochem.74.082803.13303915952882 Search in Google Scholar

28. Litscher ES, Janssen WG, Darie CC, Wassarman PM. Purified mouse egg zona pellucida glycoproteins polymerize into homomeric fibrils under non-denaturing conditions. J Cell Physiol. 2008;214:153–157; DOI:10.1002/jcp.21174.10.1002/jcp.2117417559063 Search in Google Scholar

29. Litscher ES, Wassarman PM. Zona pellucida proteins, fibrils, and matrix. Annu Rev Biochem. 2020;89:695-715; DOI:10.1146/annurev-biochem-011520-105310.10.1146/annurev-biochem-011520-10531032569527 Search in Google Scholar

30. Baez F, Camargo AA, Gastal GDA. Ultrastructural imaging analysis of the zona pellucida surface in bovine oocytes. Microsc Microanal. 2019;25:1032–1036; DOI:10.1017/S1431927619000692.10.1017/S143192761900069231134876 Search in Google Scholar

31. Suzuki H, Yang X, Foote RH. Surface alterations of the bovine oocyte and its investments during and after maturation and fertilization in vitro. Mol Reprod Dev. 1994;38:421–430; DOI:10.1002/mrd.1080380410.10.1002/mrd.10803804107980951 Search in Google Scholar

32. Allworth A, Albertini D. Meiotic maturation in cultured bovine oocytes is accompanied by remodeling of the cumulus cell cytoskeleton. Dev Biol. 1993;158: 101–121; DOI:10.1006/dbio.1993.1171.10.1006/dbio.1993.11718330667 Search in Google Scholar

33. Motta PM, Familiari G, Nottola SA, Micara G, Aragona C. Microstructural events of human egg investments during in vitro fertilization. Ultra-structure of the zona pellucida and cumulus oophorus. Bull Assoc Anat. 1991;75:89–91. Search in Google Scholar

34. Familiari G, Nottola SA, Macchiarelli G, Micara G, Aragona C, Motta PM. Human zona pellucida during in vitro fertilization: an ultrastructural study using saponin, ruthenium red, and osmium-thiocarbohydrazide. Mol Reprod Dev. 1992; 32 :51–61; DOI:10.1002/mrd.1080320109.10.1002/mrd.1080320109 Search in Google Scholar

35. Mugnier S, Dell’Aquila ME, Pelaez J, Douet C, Ambruosi B, De Santis T, Lacalandra GM, Lebos C, Sizaret P-Y, Delaleu B, Monget P, Mermillod P, Magistrini M, Meyers SA, Goudet G. New insights into the mechanisms of fertilization: comparison of the fertilization steps, composition, and structure of the zona pellucida between horses and pigs. Biol Reprod. 2009;81:856–870; DOI:10.1095/biolreprod.109.077651.10.1095/biolreprod.109.077651 Search in Google Scholar

36. Sutovsky P. Review: Sperm–oocyte interactions and their implications for bull fertility, with emphasis on the ubiquitin–proteasome system. Animal. 2018;12:121–132; DOI:10.1017/S1751731118000253.10.1017/S1751731118000253 Search in Google Scholar

37. Howes L, Jones R. Interactions between zona pellucida glycoproteins and sperm proacrosin/acrosin during fertilization. J Reprod Immunol. 2002;53:181–192; DOI:10.1016/s0165-0378(01)00101-2.10.1016/S0165-0378(01)00101-2 Search in Google Scholar

38. Zigo M, Dorosh A, Pohlova A, Jonakova V, Sulc M, Manaskova-Postlerova P. Panel of monoclonal antibodies to sperm surface proteins as a tool for monitoring localization and identification of sperm-zona pellucida receptors. Cell Tissue Res. 2015;359:895–908; DOI:10.1007/s00441-014-2072-9.10.1007/s00441-014-2072-9 Search in Google Scholar

39. Hatanaka Y, Nagai T, Tobita T, Nakano M. Changes in the properties and composition of zona pellucida pigs during fertilization in vitro. J Reprod Fertil. 1992;95:431–440; DOI:10.1530/jrf.0.0950431.10.1530/jrf.0.0950431 Search in Google Scholar

40. Legge M. Oocyte and zygote zona pellucida permeability to macromolecules. J Exp Zool. 1995;271:145–150; DOI:10.1002/jez.1402710210.10.1002/jez.1402710210 Search in Google Scholar

41. Hoodbhoy T, Dean J. Insights into the molecular basis of sperm–egg recognition in mammals. Reproduction. 2004;127:417–422; DOI:10.1530/rep.1.00181.10.1530/rep.1.00181 Search in Google Scholar

42. Wassarman PM. Regulation of mammalian fertilization by zona pellucida glycoproteins. J Reprod Fertil. 1990;42:79–87. Search in Google Scholar

43. Abbott AL, Ducibella T. Calcium and the control of mammalian cortical granule exocytosis. Front Biosci. 2001;6:792–806; DOI:10.2741/abbott.10.2741/Abbott Search in Google Scholar

44. Bleil JD, Wassarman PM. Mammalian sperm-egg interaction: Fertilization of mouse eggs triggers modification of the major zona pellucida glycoprotein, ZP2. Dev Biol. 1981;86:189–197; DOI:10.1016/0012-1606(81)90329-8.10.1016/0012-1606(81)90329-8 Search in Google Scholar

45. Gahley G, Gauthier L, Baibakov B, Epifano O, Dean J. Gamete recognition in mice depends on the cleavage status of an egg‘s zona pellucida protein. Science. 2010;329:216–219; DOI:10.1126/science.1188178.10.1126/science.1188178327226520616279 Search in Google Scholar

46. Burkart AD, Xiong B, Baibakov B, Jimenez-Movilla M, Dean J. Ovastacin, a cortical granule protease, cleaves ZP2 in the zona pellucida to prevent polyspermy. J Cell Biol. 2012;197:37–44; DOI:10.1083/jcb.201112094.10.1083/jcb.201112094331780322472438 Search in Google Scholar

47. Fahrenkamp E, Algarra B, Jovine L. Mammalian egg coat modifications and the block to polyspermy. Mol Reprod Dev. 2020;87:326–340; DOI:10.1002/mrd.23320.10.1002/mrd.23320715502832003503 Search in Google Scholar

48. Evans JP. Preventing polyspermy in mammalian eggs. Contributions of the membrane block and other mechanisms. Mol Reprod Dev. 2020;87:341–349; DOI:10.1002/mrd.23331.10.1002/mrd.2333132219915 Search in Google Scholar

49. Kopf GS. Zona pellucida-mediated signal transduction in mammalian spermatozoa. J Reprod Fertil. 1990;42:33–49. Search in Google Scholar

50. Green DP. Three-dimensional structure of the zona pellucida. Rev Re-prod. 1997;2:147–156; DOI:10.1530/ror.0.0020147.10.1530/ror.0.00201479414478 Search in Google Scholar

51. Talbot P. Hyaluronidase dissolves a component in the hamster zona pellucida. J Exp Zool. 1984;229:309–316; DOI:10.1002/jez.1402290216.10.1002/jez.14022902166736889 Search in Google Scholar

52. Dandekar P, Aggeler J, Talbot P. Structure, distribution and composition of the extracellular matrix of human oocytes and cumulus masses. Hum Reprod. 1992;7: 391–398; DOI:10.1093/oxfordjournals.humrep.a137656.10.1093/oxfordjournals.humrep.a1376561375234 Search in Google Scholar

53. Salustri A, Campagnolo L, Klinger FG, Camaioni A. Molecular organization and mechanical properties of the hyaluronan matrix surrounding the mammalian oocyte. Matrix Biol. 2019;78–79:11–23; DOI:10.1016/j.matbio.2018.02.002.10.1016/j.matbio.2018.02.00229408277 Search in Google Scholar

54. Taniyama A, Watanabe Y, Nishino Y, Inoue T. Assisted hatching of poor-quality bovine embryos increases pregnancy. J Reprod Dev. 2011;57:543–546; DOI:10.1262/jrd.10-096t.10.1262/jrd.10-096T21606632 Search in Google Scholar

55. Cole RJ. Cinemicrographic observations on the trophoblast and zona pellucida of the mouse blastocyst. J Embryol Exp Morphol. 1967;17:481–490; DOI:10.1242/dev.17.3.481.10.1242/dev.17.3.481 Search in Google Scholar

56. Massip A, Mulnard J. Time-lapse cinematographic analysis of hatching of normal and frozen-thawed cow blastocysts. J Reprod Fertil. 1980;58:475–478; DOI:10.1530/jrf.0.0580475.10.1530/jrf.0.0580475 Search in Google Scholar

57. Massip A, Mulnard J, Vanderzwalmen P, Hanzen C, Ectors F. The behaviour of cow blastocyst in vitro: cinematographic and morphometric analysis. J Anat. 1982;134:399–405. Search in Google Scholar

58. Sawada H, Yamazaki K, Hoshi M. Trypsin-like hatching protease from mouse embryos: evidence for the presence in culture medium and its enzymatic properties. J Exp Zool. 1990;254:83–87; DOI:10.1002/jez.1402540112.10.1002/jez.1402540112 Search in Google Scholar

59. Berg DA, Menino AR Jr. Bovine embryos produce urokinase-type plasmogen activator. Mol Reprod Dev. 1992;31:14–19 DOI:10.1002/mrd.1080310104.10.1002/mrd.1080310104 Search in Google Scholar

60. Mishra A, Seshagiri PB. Evidence for the involvement of a species-specific embryonic protease in zona escape of hamster blastocysts. Mol Hum Reprod. 2000;6: 1005–1012; DOI:10.1093/molehr/6.11.1005.10.1093/molehr/6.11.1005 Search in Google Scholar

61. Gonzales DS, Jones JM, Pinyopummintr T, Carnevale EM, Ginther OJ, Shapiro SS, Bavister BD. Implantation: Trophectoderm projections: a potential means for locomotion, attachment and implantation of bovine, equine and human blastocysts. Hum Reprod. 1996;11:2739–2745; DOI:10.1093/oxfordjournals.humrep.a019201.10.1093/oxfordjournals.humrep.a019201 Search in Google Scholar

62. Seshagiri PB, Sen Roy S, Sireesha G, Rao RP. Cellular and molecular regulation of mammalian blastocyst hatching. J Reprod Immunol. 2009;83:79–84; DOI:10.1016/j.jri.2009.06.264.10.1016/j.jri.2009.06.264 Search in Google Scholar

63. Perona RM, Wassarman PM. Mouse blastocysts hatch in vitro by using a trypsin-like proteinase associated with cells of mural trophectoderm. Dev Biol. 1986;114:42–52; DOI:10.1016/0012-1606(86)90382-9.10.1016/0012-1606(86)90382-9 Search in Google Scholar

64. O’Sullivan CM, Rancourt SL, Liu SY, Rancourt DE. A novel murine tryptase involved in blastocyst hatching and outgrowth. Reproduction. 2001;122:61–71; DOI:10.1530/rep.0.1220061.10.1530/rep.0.1220061 Search in Google Scholar

65. Coates AA, Menino AR. Effects of blastocoelic expansion and plasminogen activator activity on hatching and zona pellucida solubility in bovine embryos in vitro. J Anim Sci. 1994;72:2936–2942; DOI:10.2527/1994.72112936x.10.2527/1994.72112936x Search in Google Scholar

66. Sathananthan H, Menezes J, Gunasheela S. Mechanics of human blastocyst hatching in vitro. Reprod Biomed Online. 2003;7:228–234; DOI:10.1016/s1472-6483(10)61757-9.10.1016/S1472-6483(10)61757-9 Search in Google Scholar

67. Gonzales DS, Bavister BD. Zona pellucida escape by hamster blastocysts in vitro is delayed and morphologically different compared with zona escape in vivo. Biol Reprod. 1995;52:470–480; DOI:10.1095/biolreprod52.2.470.10.1095/biolreprod52.2.470 Search in Google Scholar

68. Betteridge KJ, Flechon JE. The anatomy and physiology of preattachement bovine embryos. Theriogenology. 1988;29:155–187; DOI:10.1016/0093-691X(88)90038-6.10.1016/0093-691X(88)90038-6 Search in Google Scholar

69. Negron-Perez VM, Hansen PJ. The bovine embryo hatches from the zona pellucida through either the embryonic or abembryonic pole. J Assist Reprod Genet. 2017;34: 725–731; DOI:10.1007/s10815-017-0933-3.10.1007/s10815-017-0933-3544505828466234 Search in Google Scholar

70. Niimura S, Ogata T, Okimura A, Sato T, Uchiyama Y, Seta T, Nakagawa H, Nakagawa K, Tamura Y. Time-lapse videomicrographic observations of blastocyst hatching in cattle. J Reprod Dev. 2010;56:649–654; DOI:10.1262/jrd.10-069h.10.1262/jrd.10-069H Search in Google Scholar