1932

Abstract

The zona pellucida (ZP) is an extracellular matrix that surrounds all mammalian oocytes, eggs, and early embryos and plays vital roles during oogenesis, fertilization, and preimplantation development. The ZP is composed of three or four glycosylated proteins, ZP1–4, that are synthesized, processed, secreted, and assembled into long, cross-linked fibrils by growing oocytes. ZP proteins have an immunoglobulin-like three-dimensional structure and a ZP domain that consists of two subdomains, ZP-N and ZP-C, with ZP-N of ZP2 and ZP3 required for fibril assembly. A ZP2–ZP3 dimer is located periodically along ZP fibrils that are cross-linked by ZP1, a protein with a proline-rich N terminus. Fibrils in the inner and outer regions of the ZP are oriented perpendicular and parallel to the oolemma, respectively, giving the ZP a multilayered appearance. Upon fertilization of eggs, modification of ZP2 and ZP3 results in changes in the ZP's physical and biological properties that have important consequences. Certain structural features of ZP proteins suggest that they may be amyloid-like proteins.

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2020-06-20
2024-06-22
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Literature Cited

  1. 1. 
    von Baer KE. 1827. De ovi mammalium et hominis genesi [On the Genesis of the Ovum of Mammals and of Man] Leipzig, Ger: Leopold Voss http://embryo.asu.edu/handle/10776/11405
    [Google Scholar]
  2. 2. 
    Litscher ES, Wassarman PM. 2015. A Guide to Zona Pellucida Domain Proteins Hoboken, NJ: Wiley
    [Google Scholar]
  3. 3. 
    Wassarman PM, Albertini DF. 1994. The mammalian ovum. The Physiology of Reproduction E Knobil, JD Neill 79–122 New York: Raves, 2nd ed..
    [Google Scholar]
  4. 4. 
    Wassarman PM, Mortillo S. 1991. Structure of the mouse egg extracellular coat, the zona pellucida. Int. Rev. Cytol. 130:85–110
    [Google Scholar]
  5. 5. 
    Gwatkin RBL. 1977. Fertilization Mechanisms in Man and Mammals New York: Plenum
    [Google Scholar]
  6. 6. 
    Litscher ES, Wassarman PM. 2014. Evolution, structure, and synthesis of vertebrate egg-coat proteins. Trends Dev. Biol. 8:65–76
    [Google Scholar]
  7. 7. 
    Wassarman PM, Litscher ES. 2018. The mouse egg's zona pellucida. Curr. Top. Dev. Biol. 130:331–56
    [Google Scholar]
  8. 8. 
    Thim L. 1997. Trefoil peptides: from structure to function. Cell. Mol. Life Sci. 53:888–903
    [Google Scholar]
  9. 9. 
    Qi H, Williams Z, Wassarman PM 2002. Secretion and assembly of zona pellucida glycoproteins by growing mouse oocytes microinjected with epitope-tagged cDNAs for mZP2 and mZP3. Mol. Biol. Cell 13:530–41
    [Google Scholar]
  10. 10. 
    Chothia C, Gough J, Vogel C, Teichmann SA 2003. Evolution of the protein repertoire. Science 300:1701–3
    [Google Scholar]
  11. 11. 
    Liang L, Dean J. 1993. Conservation of mammalian secondary sperm receptor genes enables the promoter of the human gene to function in mouse oocytes. Dev. Biol. 156:399–408
    [Google Scholar]
  12. 12. 
    Epifano O, Liang LF, Dean J 1995. Mouse Zp1 encodes a zona pellucida protein homologous to egg envelope proteins in mammals and fish. J. Biol. Chem. 270:27254–58
    [Google Scholar]
  13. 13. 
    Liu C, Litscher ES, Mortillo S, Sakai Y, Kinloch RA et al. 1996. Targeted disruption of the mZP3 gene results in production of eggs lacking a zona pellucida and infertility in female mice. PNAS 93:5431–36
    [Google Scholar]
  14. 14. 
    Rankin T, Familiari M, Lee E, Ginsburg A, Dwyer N et al. 1996. Mice homozygous for an insertional mutation in the ZP3 gene lack a zona pellucida and are infertile. Development 122:2903–10
    [Google Scholar]
  15. 15. 
    Rankin T, O'Brien M, Lee E, Wigglesworth K, Eppig J et al. 2001. Defective zonae pellucidae in Zp2-null mice disrupt folliculogenesis, fertility, and development. Development 128:1119–26
    [Google Scholar]
  16. 16. 
    Litscher ES, Janssen WG, Darie CC, Wassarman PM 2008. Purified mouse egg zona pellucida glycoproteins polymerize into homomeric fibrils under non-denaturing conditions. J. Cell. Physiol. 214:153–57
    [Google Scholar]
  17. 17. 
    Wassarman PM, Qi H, Litscher ES 1997. Mutant female mice carrying a single mZP3 allele produce eggs with a thin zona pellucida, but reproduce normally. Proc. R. Soc. B 264:323–28
    [Google Scholar]
  18. 18. 
    Rankin T, Talbot P, Lee E, Dean J 1999. Abnormal zonae pellucidae in mice lacking ZP1 result in early embryonic loss. Development 126:3847–55
    [Google Scholar]
  19. 19. 
    Bork P, Sander C. 1992. A large domain common to sperm receptors (Zp2 and Zp3) and TGF-β type III receptor. FEBS Lett 300:237–40
    [Google Scholar]
  20. 20. 
    Wilburn DB, Swanson WJ. 2017. The “ZP domain” is not one, but likely two independent domains. Mol. Reprod. Dev. 84:284–85
    [Google Scholar]
  21. 21. 
    Jovine L, Darie CC, Litscher ES, Wassarman PM 2005. Zona pellucida domain proteins. Annu. Rev. Biochem. 74:83–114
    [Google Scholar]
  22. 22. 
    Callebaut I, Mornon JP, Monget P 2007. Isolated ZP-N domains constitute the N-terminal extensions of zona pellucida proteins. Bioinformatics 23:1871–74
    [Google Scholar]
  23. 23. 
    Jovine L, Janssen WG, Litscher ES, Wassarman PM 2006. The PLAC1-homology region of the ZP domain is sufficient for protein polymerisation. BMC Biochem 7:11
    [Google Scholar]
  24. 24. 
    Jovine L, Qi H, Williams Z, Litscher ES, Wassarman PM 2002. The ZP domain is a conserved module for polymerization of extracellular proteins. Nat. Cell Biol. 4:457–61
    [Google Scholar]
  25. 25. 
    Jovine L, Qi H, Williams Z, Litscher ES, Wassarman PM 2004. A duplicated motif controls assembly of zona pellucida domain proteins. PNAS 101:5922–27
    [Google Scholar]
  26. 26. 
    Jimenez-Movilla M, Dean J. 2011. ZP2 and ZP3 cytoplasmic tails prevent premature interactions and ensure incorporation into the zona pellucida. J. Cell Sci. 124:940–50
    [Google Scholar]
  27. 27. 
    Qi H, Wassarman PM. 1999. Secretion of zona pellucida glycoprotein mZP2 by growing oocytes from mZP3+/+ and mZP3−/− mice. Dev. Genet. 25:95–102
    [Google Scholar]
  28. 28. 
    Morgan AA, Rubenstein E. 2013. Proline: the distribution, frequency, positioning, and common functional roles of proline and polyproline sequences in the human proteome. PLOS ONE 8:e53785
    [Google Scholar]
  29. 29. 
    Adzhubei AA, Sternberg MJE, Makarov AA 2013. Polyproline-II helix in proteins: structure and function. J. Mol. Biol. 425:2100–32
    [Google Scholar]
  30. 30. 
    Darnell G, Orgel JP, Pahl R, Meredith SC 2007. Flanking polyproline sequences inhibit β-sheet structure in polyglutamine segments by inducing PPII-like helix structure. J. Mol. Biol. 374:688–704
    [Google Scholar]
  31. 31. 
    Darnell GD, Derryberry JM, Kurutz JW, Meredith SC 2009. Mechanism of cis-inhibition of polyQ fibrillation by polyP: PPII oligomers and the hydrophobic effect. Biophys. J. 97:2295–305
    [Google Scholar]
  32. 32. 
    Harris JD, Hibler DW, Fontenot GK, Hsu KT, Yurewicz EC et al. 1994. Cloning and characterization of zona pellucida genes and cDNAs from a variety of mammalian species: the ZPA, ZPB, and ZPC gene families. DNA Seq 4:361–93
    [Google Scholar]
  33. 33. 
    Hyllner SJ, Westerlund L, Olsson PE, Schopen A 2001. Cloning of rainbow trout egg envelope proteins: members of a unique group of structural proteins. Biol. Reprod. 64:805–11
    [Google Scholar]
  34. 34. 
    Lefièvre L, Conner SJ, Salpekar A, Olufowobi O, Ashton P et al. 2004. Four zona pellucida glycoproteins are expressed in the human. Hum. Reprod. 19:1580–86
    [Google Scholar]
  35. 35. 
    Litscher ES, Wassarman PM. 2018. The fish egg's zona pellucida. Curr. Top. Dev. Biol. 130:275–305
    [Google Scholar]
  36. 36. 
    Rath A, Davidson AR, Deber CM 2005. The structure of “unstructured” regions in peptides and proteins: role of the polyproline II helix in protein folding and recognition. Biopolymers 80:179–85
    [Google Scholar]
  37. 37. 
    Bochicchio B, Tamburro AM. 2002. Polyproline II structure in proteins: identification by chiroptical spectroscopies, stability, and functions. Chirality 14:782–92
    [Google Scholar]
  38. 38. 
    Ruggiero MT, Sibik J, Orlando R, Zeitler JA, Korter TM 2016. Measuring the elasticity of poly-l-proline helices with terahertz spectroscopy. Angew. Chem. Int. Ed. 55:6877–81
    [Google Scholar]
  39. 39. 
    Sexton OJ, Bramble JE, Heisler IL, Phillips CA, Cox DL 2005. Eggshell composition of squamate reptiles: relationship between eggshell permeability and amino acid distribution. J. Chem. Ecol. 31:2391–401
    [Google Scholar]
  40. 40. 
    Bausek N, Waclawek M, Schneider WJ, Wohlrab F 2000. The major chicken egg envelope protein ZP1 is different from ZPB and is synthesized in the liver. J. Biol. Chem. 275:28866–72
    [Google Scholar]
  41. 41. 
    Vonk FJ, Casewell NR, Henkel CV, Heimberg AM, Jansen HJ et al. 2013. The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system. PNAS 110:20651–56
    [Google Scholar]
  42. 42. 
    Venkatesh B, Lee AP, Ravi V, Maurya AK, Lian MM et al. 2014. Elephant shark genome provides unique insights into gnathostome evolution. Nature 505:174–79
    [Google Scholar]
  43. 43. 
    Venkatesh B, Tay A, Dandona N, Patil JG, Brenner S 2005. A compact cartilaginous fish model genome. Curr. Biol. 15:R82–83
    [Google Scholar]
  44. 44. 
    Monné M, Han L, Schwend T, Burendahl S, Jovine L 2008. Crystal structure of the ZP-N domain of ZP3 reveals the core fold of animal egg coats. Nature 456:653–57
    [Google Scholar]
  45. 45. 
    Han L, Monné M, Okumura H, Schwend T, Cherry AL et al. 2010. Insights into egg-coat assembly and egg–sperm interaction from the X-ray structure of full-length ZP3. Cell 143:404–15
    [Google Scholar]
  46. 46. 
    Lin SJ, Hu Y, Zhu J, Woodruff TK, Jardetzky TS 2011. Structure of β-glycan zona pellucida (ZP)-C domain provides insights into ZP-mediated protein polymerization and TGF-β binding. PNAS 108:5232–36
    [Google Scholar]
  47. 47. 
    Diestel U, Resch M, Meinhardt K, Weiler S, Hellmann TV et al. 2013. Identification of a novel TGF-β-binding site in the zona pellucida C-terminal (ZP-C) domain of TGF-β receptor 3 (TGFR-3). PLOS ONE 8:e67214
    [Google Scholar]
  48. 48. 
    Bokhove M, Nishimura K, Brunati M, Han L, de Sanctis D et al. 2016. A structured interdomain linker directs self-polymerization of human uromodulin. PNAS 113:1552–57
    [Google Scholar]
  49. 49. 
    Raj I, Sadat Al Hosseini H, Dioguardi E, Nishimura K, Han L et al. 2017. Structural basis of egg coat–sperm recognition at fertilization. Cell 169:1315–26
    [Google Scholar]
  50. 50. 
    Saito T, Bokhove M, Croci R, Zamora-Caballero S, Han L et al. 2017. Structural basis of the human endoglin-BMP9 interaction: insights into BMP signaling and HHT1. Cell Rep 19:1917–28
    [Google Scholar]
  51. 51. 
    Nishimura K, Dioguardi E, Nishio S, Villa A, Han L et al. 2019. Molecular basis of egg coat cross-linking sheds light on ZP1-associated female infertility. Nat. Commun. 10:3086
    [Google Scholar]
  52. 52. 
    Bokhove M, Jovine L. 2018. Structure of zona pellucida module proteins. Curr. Top. Dev. Biol. 130:413–42
    [Google Scholar]
  53. 53. 
    Hutchinson EG, Thornton JM. 1993. The Greek key motif: extraction, classification and analysis. Protein Eng 6:233–45
    [Google Scholar]
  54. 54. 
    Tilson MD, Rzhetsky A. 2000. A novel hypothesis regarding the evolutionary origins of the immunoglobulin fold. Curr. Med. Res. Opin. 16:88–93
    [Google Scholar]
  55. 55. 
    Williams AF, Barclay AN. 1988. The immunoglobulin superfamily—domains for cell surface recognition. Annu. Rev. Immunol. 6:381–405
    [Google Scholar]
  56. 56. 
    Barclay AN. 2003. Membrane proteins with immunoglobulin-like domains—a master superfamily of interaction molecules. Semin. Immunol. 15:215–23
    [Google Scholar]
  57. 57. 
    Legan PK, Lukashkina VA, Goodyear RJ, Lukashkin AN, Verhoeven K et al. 2005. A deafness mutation isolates a second role for the tectorial membrane in hearing. Nat. Neurosci. 8:1035–42
    [Google Scholar]
  58. 58. 
    Greve JM, Wassarman PM. 1985. Mouse egg extracellular coat is a matrix of interconnected filaments possessing a structural repeat. J. Mol. Biol. 181:253–64
    [Google Scholar]
  59. 59. 
    Phillips DM, Shalgi RM. 1980. Surface properties of the zona pellucida. J. Ultrastruct. Res. 72:1–12
    [Google Scholar]
  60. 60. 
    Familiari G, Relucenti M, Heyn R, Micara G, Correr S 2006. Three-dimensional structure of the zona pellucida at ovulation. Microsc. Res. Tech. 69:415–26
    [Google Scholar]
  61. 61. 
    Keefe D, Tran P, Pellegrini C, Oldenbourg R 1997. Polarized light microscopy and digital image processing identify a multilaminar structure of hamster zona pellucida. Hum. Reprod. 12:1250–52
    [Google Scholar]
  62. 62. 
    Pelletier C, Keefe DL, Trimarchi JR 2004. Noninvasive polarized light microscopy quantitatively distinguishes the multilaminar structure of the zona pellucida of living human eggs and embryos. Fertil. Steril. 81:850–56
    [Google Scholar]
  63. 63. 
    Liu M. 2011. The biology and dynamics of mammalian cortical granules. Reprod. Biol. Endocrinol. 9:149–66
    [Google Scholar]
  64. 64. 
    de Paola M, Bello OD, Michaut MA 2015. Cortical granule exocytosis is mediated by α-SNAP and N-ethilmaleimide sensitive factor in mouse oocytes. PLOS ONE 10:e0135679
    [Google Scholar]
  65. 65. 
    Bleil JD, Beall CF, Wassarman PM 1981. Mammalian sperm-egg interaction: Fertilization of mouse eggs triggers modification of the major zona pellucida glycoprotein, ZP2. Dev. Biol. 86:189–97
    [Google Scholar]
  66. 66. 
    Moller CC, Wassarman PM. 1989. Characterization of a proteinase that cleaves zona pellucida glycoprotein ZP2 following activation of mouse eggs. Dev. Biol. 132:103–12
    [Google Scholar]
  67. 67. 
    Que EL, Bleher R, Duncan FE, Kong BY, Gleber SC et al. 2015. Quantitative mapping of zinc fluxes in the mammalian egg reveals the origin of fertilization-induced zinc sparks. Nat. Chem. 7:130–39
    [Google Scholar]
  68. 68. 
    Que EL, Duncan FE, Bayer AR, Philips SJ, Roth EW et al. 2017. Zinc sparks induce physiochemical changes in the egg zona pellucida that prevent polyspermy. Integr. Biol. 9:135–44
    [Google Scholar]
  69. 69. 
    Burkart AD, Xiong B, Baibakov B, Jimenez-Movilla M, Dean J 2012. Ovastacin, a cortical granule protease, cleaves ZP2 in the zona pellucida to prevent polyspermy. J. Cell Biol. 197:37–44
    [Google Scholar]
  70. 70. 
    Tokuhiro K, Dean J. 2018. Glycan-independent gamete recognition triggers egg zinc sparks and ZP2 cleavage to prevent polyspermy. Dev. Cell 46:627–40
    [Google Scholar]
  71. 71. 
    Murayama Y, Constantinou CE, Omata S 2004. Micro-mechanical sensing platform for the characterization of the elastic properties of the ovum via uniaxial measurement. J. Biomech. 37:67–72
    [Google Scholar]
  72. 72. 
    Papi M, Brunelli R, Sylla L, Parasassi T, Monaci M et al. 2010. Mechanical properties of zona pellucida hardening. Eur. Biophys. J. 39:987–92
    [Google Scholar]
  73. 73. 
    Boccaccio A, Lamberti L, Papi M, De Spirito M, Douet C et al. 2014. A hybrid characterization framework to determine the visco-hyperelastic properties of a porcine zona pellucida. Interface Focus 4:20130066
    [Google Scholar]
  74. 74. 
    Andolfi L, Masiero E, Giolo E, Martinelli M, Luppi S et al. 2016. Investigating the mechanical properties of zona pellucida of whole human oocytes by atomic force spectroscopy. Integr. Biol. 8:886–93
    [Google Scholar]
  75. 75. 
    Kim J, Kim J. 2013. Viscoelastic characterization of mouse zona pellucida. IEEE Trans. Biomed. Eng. 60:569–75
    [Google Scholar]
  76. 76. 
    Fowler DM, Koulov AV, Balch WE, Kelly JW 2007. Functional amyloid—from bacteria to humans. Trends Biochem. Sci. 32:217–24
    [Google Scholar]
  77. 77. 
    Jackson MP, Hewitt EW. 2017. Why are functional amyloids non-toxic in humans?. Biomolecules 7:e71
    [Google Scholar]
  78. 78. 
    Fändrich M. 2007. On the structural definition of amyloid fibrils and other polypeptide aggregates. Cell. Mol. Life Sci. 64:2066–78
    [Google Scholar]
  79. 79. 
    Jahn TR, Makin OS, Morris KL, Marshall KE, Tian P et al. 2010. The common architecture of cross-β amyloid. J. Mol. Biol. 395:717–27
    [Google Scholar]
  80. 80. 
    Eisenberg DS, Sawaya MR. 2017. Structural studies of amyloid proteins at the molecular level. Annu. Rev. Biochem. 86:69–95
    [Google Scholar]
  81. 81. 
    Tsolis AC, Papandreou NC, Iconomidou VA, Hamodrakas SJ 2013. A consensus method for the prediction of “aggregation-prone” peptides in globular proteins. PLOS ONE 8:e54175
    [Google Scholar]
  82. 82. 
    Louros NN, Iconomidou VA, Giannelou P, Hamodrakas SJ 2013. Structural analysis of peptide-analogues of human zona pellucida ZP1 protein with amyloidogenic properties: insights into mammalian zona pellucida formation. PLOS ONE 8:e73258
    [Google Scholar]
  83. 83. 
    Egge N, Muthusubramanian A, Cornwall GA 2015. Amyloid properties of the mouse egg zona pellucida. PLOS ONE 10:e0129907
    [Google Scholar]
  84. 84. 
    Morris KL, Serpell LC. 2012. X-ray fibre diffraction studies of amyloid fibrils. Methods Mol. Biol. 849:121–35
    [Google Scholar]
  85. 85. 
    Goldschmidt L, Teng PK, Riek R, Eisenberg D 2010. Identifying the amylome, proteins capable of forming amyloid-like fibrils. PNAS 107:3487–92
    [Google Scholar]
  86. 86. 
    Louros NN, Chrysina ED, Baltatzis GE, Patsouris ES, Hamodrakas SJ et al. 2016. A common “aggregation prone” interface possibly participates in the self-assembly of human zona pellucida proteins. FEBS Lett 590:619–30
    [Google Scholar]
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