Identification of potential oviductal factors responsible for zona pellucida hardening and monospermy during fertilization in mammals

Biology of Reproduction

Volumn 89, Issue 3, 2013, Pages

  Mondéjar, Irene ^a,c   Martínez Martínez, Irene ^a   Avilés, Manuel ^b   Coy, Pilar ^a,c  

^a UNIVERSITY OF MURCIA   (Spain)

^b UNIVERSITY OF MURCIA   (Spain)

^c Murcia Biomedical Research Institute (IMIB)   (Spain)

Author keywords

Enzymatic hardening; In vitro fertilization; Oviductal fluid; Polyspermy; Zona pellucida

Indexed keywords

HEAT SHOCK PROTEIN; HEPARIN; PROTEIN DISULFIDE ISOMERASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; COW; ELECTROPHORESIS; EMBRYO DEVELOPMENT; FEMALE; FERTILIZATION; FERTILIZATION IN VITRO; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MALE GENITAL SYSTEM FUNCTION; MONOSPERMY; MUSCLE; NONHUMAN; OOCYTE; OVIDUCT; POLYSPERMY; PRIORITY JOURNAL; PRONUCLEUS; PROTEIN PURIFICATION; SPERMATOZOON; SWINE; ZONA PELLUCIDA;

ENZYMATIC HARDENING; IN VITRO FERTILIZATION; OVIDUCTAL FLUID; POLYSPERMY; ZONA PELLUCIDA;

ANIMALS; BODY FLUIDS; CATTLE; CELLS, CULTURED; FALLOPIAN TUBES; FEMALE; FERTILIZATION; FERTILIZATION IN VITRO; HARDNESS; IN VITRO OOCYTE MATURATION TECHNIQUES; MALE; PROTEINS; SPERM-OVUM INTERACTIONS; SWINE; ZONA PELLUCIDA;

EID: 84889576573     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.111385     Document Type: Article

References (41)

1. Coy P, García-Vázquez FA, Visconti PE, Avilés M. Roles of the oviduct in mammalian fertilization. Reproduction 2012; 144:649-660.
2. Hunter RH. The Fallopian Tubes: Their Role in Fertility and Infertility. Berlin: Springer; 1988.
3. Avilés M, Gutiérrez-Adán A, Coy P. Oviductal secretions: will they be key factors for the future ARTs? Mol Hum Reprod 2010; 16:896-906.
4. Coy P, Cánovas S, Mondéjar I, Saavedra MD, Romar R, Grullón L, Matás C, Avilés M. Oviduct-specific glycoprotein and heparin modulate spermzona pellucida interaction during fertilization and contribute to the control of polyspermy. Proc Natl Acad Sci U S A 2008; 105:15809-15814.
5. Hunter RH. The effects of delayed insemination on fertilization and early cleavage in the pig. J Reprod Fertil 1967; 13:133-147.
6. Coy P, Avilés M. What controls polyspermy in mammals, the oviduct or the oocyte? Biol Rev Camb Philos Soc 2010; 85:593-605.
7. Kolbe T, Holtz W. Differences in proteinase digestibility of the zona pellucida of in vivo and in vitro derived porcine oocytes and embryos. Theriogenology 2005; 63:1695-1705.
8. Coy P, Gadea J, Romar R, Matás C, García E. Effect of in vitro fertilization medium on the acrosome reaction, cortical reaction, zona pellucida hardening and in vitro development in pigs. Reproduction 2002; 124:279-288.
9. Pursel VG, Johnson LA. Freezing of boar spermatozoa: fertilizing capacity with concentrated semen and a new thawing procedure. J Anim Sci 1975; 40:99-102.
10. Carrasco LC, Romar R, Avilés M, Gadea J, Coy P. Determination of glycosidase activity in porcine oviductal fluid at the different phases of the estrous cycle. Reproduction 2008; 136:833-842.
11. Orsi NM, Gopichandran N, Leese HJ, Picton HM, Harris SE. Fluctuations in bovine ovarian follicular fluid composition throughout the oestrous cycle. Reproduction 2005; 129:219-228.
12. Nagai T, Funahashi H, Yoshioka K, Kikuchi K. Update of in vitro production of porcine embryos. Front Biosci 2006; 11:2565-2573.
13. Sano H, Matsuura K, Naruse K, Funahashi H. Application of a microfluidic sperm sorter to the in-vitro fertilization of porcine oocytes reduced the incidence of polyspermic penetration. Theriogenology 2010; 74:863-870.
14. Ekhlasi-Hundrieser M, Gohr K, Wagner A, Tsolova M, Petrunkina A, Töpfer-Petersen E. Spermadhesin AQN1 is a candidate receptor molecule involved in the formation of the oviductal sperm reservoir in the pig. Biol Reprod 2005; 73:536-545.
15. Flechon JE, Hunter RHF. Distribution of spermatozoa in the utero-tubal junction and isthmus of pigs, and their relationship with the luminal epithelium after mating: a scanning electron microscope study. Tissue Cell 1981; 13:127-139.
16. Conley AJ, Howard HJ, Slanger WD, Ford JJ. Steroidogenesis in the preovulatory porcine follicle. Biol Reprod 1994; 51:655-661.
17. Hunter RH. Local action of progesterone leading to polyspermic fertilization in pigs. J Reprod Fertil 1972; 31:433-444.
18. Buhi WC, Alvarez IM, Choi I, Cleaver BD, Simmen FA. Molecular cloning and characterization of an estrogen-dependent porcine oviductal secretory glycoprotein. Biol Reprod 1996; 55:1305-1314.
19. Buhi WC. Characterization and biological roles of oviduct-specific, oestrogen-dependent glycoprotein. Reproduction 2002; 123:355-362.
20. Kouba AJ, Abeydeera LR, Alvarez IM, Day BN, Buhi WC. Effects of the porcine oviduct-specific glycoprotein on fertilization, polyspermy, and embryonic development in vitro. Biol Reprod 2000; 63:242-250.
21. Neuer A, Spandorfer SD, Giraldo P, Dieterle S, Rosenwaks Z, Witkin SS. The role of heat shock proteins in reproduction. Hum Reprod Update 2000; 6:149-159.
22. Ellis J. Proteins as molecular chaperones. Nature 1987; 328:378-379.
23. Hansen LK, O'Leary JJ, Skubitz AP, Furcht LT, McCarthy JB. Identification of a homologous heparin binding peptide sequence present in fibronectin and the 70 kDa family of heat-shock proteins. Biochim Biophys Acta 1995; 1252:135-145.
24. Hubbard MJ, Mangum JE, McHugh NJ. Purification and biochemical characterization of native ERp29 from rat liver. Biochem J 2004; 383: 589-597.
25. Bauersachs S, Rehfeld S, Ulbrich SE, Mallok S, Prelle K, Wenigerkind H, Einspanier R, Blum H, Wolf E. Monitoring gene expression changes in bovine oviduct epithelial cells during the oestrous cycle. J Mol Endocrinol 2004; 32:449-466.
26. Campanella C, Bucchieri F, Merendino AM, Fucarino A, Burgio G, Corona DF, Barbieri G, David S, Farina F, Zummo G, de Macario EC, Macario AJ, et al. The odyssey of Hsp60 from tumor cells to other destinations includes plasma membrane-associated stages and Golgi and exosomal protein-trafficking modalities. PLoS One 2012; 7:e42008.
27. Elliott RM, Lloyd RE, Fazeli A, Sostaric E, Georgiou AS, Satake N, Watson PF, Holt WV. Effects of HSPA8, an evolutionarily conserved oviductal protein, on boar and bull spermatozoa. Reproduction 2009; 137: 191-203.
28. Lloyd RE, Elliott RM, Fazeli A, Watson PF, Holt WV. Effects of oviductal proteins, including heat shock 70 kDa protein 8, on survival of ram spermatozoa over 48 h in vitro. Reprod Fertil Dev 2009; 21:408-418.
29. Sostaric E, Georgiou AS, Wong CH, Watson PF, Holt WV, Fazeli A. Global profiling of surface plasma membrane proteome of oviductal epithelial cells. J Proteome Res 2006; 5:3029-3037.
30. Topfer-Petersen E, Ekhlasi-Hundrieser M, Tsolova M. Glycobiology of fertilization in the pig. Int J Dev Biol 2008; 52:717-736.
31. Seytanoglu A, Georgiou AS, Sostaric E, Watson PF, Holt WV, Fazeli A. Oviductal cell proteome alterations during the reproductive cycle in pigs. J Proteome Res 2008; 7:2825-2833.
32. Marín-Briggiler CI, González-Echeverría MF, Munuce MJ, Ghersevich S, Caille AM, Hellman U, Corrigall VM, Vazquez-Levin MH. Glucoseregulated protein 78 (Grp78/BiP) is secreted by human oviduct epithelial cells and the recombinant protein modulates sperm-zona pellucida binding. Fertil Steril 2010; 93:1574-1584.
33. Boilard M, Reyes-Moreno C, Lachance C, Massicotte L, Bailey J, Sirard M, Leclerc P. Localization of the chaperone proteins GRP78 and HSP60 on the luminal surface of bovine oviduct epithelial cells and their association with spermatozoa. Biol Reprod 2004; 71:1879-1889.
34. Lachance C, Bailey JL, Leclerc P. Expression of Hsp60 and Grp78 in the human endometrium and oviduct, and their effect on sperm functions. Hum Reprod 2007; 22:2606-2614.
35. Appenzeller-Herzog C, Ellgaard L. The human PDI family: versatility packed into a single fold. Biochim Biophys Acta 2008; 1783:535-548.
36. Ellerman DA, Myles DG, Primakoff P. A role for sperm surface protein disulfide isomerase activity in gamete fusion: evidence for the participation of ERp57. Dev Cell 2006; 10:831-837.
37. Walsh A, Whelan D, Bielanowicz A, Skinner B, Aitken RJ, O'Bryan MK, Nixon B. Identification of the molecular chaperone, heat shock protein 1 (chaperonin 10), in the reproductive tract and in capacitating spermatozoa in the male mouse. Biol Reprod 2008; 78:983-993.
38. Redgrove KA, Nixon B, Baker MA, Hetherington L, Baker G, Liu DY, 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.
39. Turano C, Coppari S, Altieri F, Ferraro A. Proteins of the PDI family: unpredicted non-ER locations and functions. J Cell Physiol 2002; 193: 154-163.
40. Meunier L, Usherwood YK, Chung KT, Hendershot LM. A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Mol Biol Cell 2002; 13: 4456-4469.
41. Iwamoto K, Ikeda K, Yonezawa N, Noguchi S, Kudo K, Hamano S, Kuwayama M, Nakano M. Disulfide formation in bovine zona pellucida glycoproteins during fertilization: evidence for the involvement of cystine cross-linkages in hardening of the zona pellucida. J Reprod Fertil 1999; 117:395-402.