Fertility and Sterility
Volume 92, Issue 3 , Pages 971-978 , September 2009

Cumulus cells and their extracellular matrix affect the quality of the spermatozoa penetrating the cumulus mass

  • Shun-Jia Hong, Ph.D.

      Affiliations

    • Department of Obstetrics and Gynecology, Second Affiliated Hospital, Sun Yat-sen University, Guangdong, China
  • ,
  • Philip Chi-Ngong Chiu, Ph.D.

      Affiliations

    • Department of Obstetrics and Gynecology, University of Hong Kong, Queen Mary Hospital, Pokfulam, Hong Kong, China
  • ,
  • Kai-Fai Lee, Ph.D.

      Affiliations

    • Department of Obstetrics and Gynecology, University of Hong Kong, Queen Mary Hospital, Pokfulam, Hong Kong, China
  • ,
  • Jenny Yin-Mei Tse, Ph.D.

      Affiliations

    • Innovation and Technology Commission, Wanchai, Hong Kong, China
  • ,
  • Pak-Chung Ho, M.D.

      Affiliations

    • Department of Obstetrics and Gynecology, University of Hong Kong, Queen Mary Hospital, Pokfulam, Hong Kong, China
  • ,
  • William Shu-Biu Yeung, Ph.D.

      Affiliations

    • Department of Obstetrics and Gynecology, University of Hong Kong, Queen Mary Hospital, Pokfulam, Hong Kong, China
    • Corresponding Author InformationReprint requests: Dr. W. S.-B. Yeung, Department of Obstetrics and Gynaecology, University of Hong Kong, Queen Mary Hospital, Hong Kong, China (FAX: 852-28550947).

Received 19 May 2008 ,Revised 11 July 2008 ,Accepted 11 July 2008.

References 

  1. Pereda J, Coppo M. An electron microscopic study of sperm penetration into the human egg investments. Anat Embryol (Berl). 1985;173:247–252
  2. Cummins JM, Yanagimachi R. Development of ability to penetrate the cumulus oophorus by hamster spermatozoa capacitated in vitro, in relation to the timing of acrosome reaction. Gamete Res. 1986;15:187–212
  3. Tsuiki A, Hoshiai H, Takahashi K, Suzuki M, Hoshi K. Sperm-egg interactions observed by scanning electron microscopy. Arch Androl. 1986;16:35–47
  4. 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
  5. Chen C, Sathananthan AH. Early penetration of human sperm through the vestments of human eggs in vitro. Arch Androl. 1986;16:183–197
  6. Cherr GN, Lambert H, Meizel S, Katz DF. In vitro studies of the golden hamster sperm acrosome reaction: completion on the zona pellucida and induction by homologous soluble zonae pellucidae. Dev Biol. 1986;114:119–131
  7. Corselli J, Talbot P. In vitro penetration of hamster oocyte-cumulus complexes using physiological numbers of sperm. Dev Biol. 1987;122:227–242
  8. Hizaki H, Segi E, Sugimoto Y, Hirose M, Saji T, Ushikubi F, et al. Abortive expansion of the cumulus and impaired fertility in mice lacking the prostaglandin E receptor subtype EP(2). Proc Natl Acad Sci U S A. 1999;96:10501–10506
  9. Zhuo L, Yoneda M, Zhao M, Yingsung W, Yoshida N, Kitagawa Y, et al. Defect in SHAP-hyaluronan complex causes severe female infertility. A study by inactivation of the bikunin gene in mice. J Biol Chem. 2001;276:7693–7696
  10. Fulop C, Szanto S, Mukhopadhyay D, Bardos T, Kamath RV, Rugg MS, et al. Impaired cumulus mucification and female sterility in tumor necrosis factor–induced protein-6 deficient mice. Development. 2003;130:2253–2261
  11. Sullivan R, Duchesne C, Fahmy N, Morin N, Dionne P. Protein synthesis and acrosome reaction–inducing activity of human cumulus cells. Hum Reprod. 1990;5:830–834
  12. Bastias MC, Kamijo H, Osteen KG. Assessment of human sperm functional changes after in-vitro coincubation with cells retrieved from the human female reproductive tract. Hum Reprod. 1993;8:1670–1677
  13. Fetterolf PM, Jurisicova A, Tyson JE, Casper RF. Conditioned medium from human cumulus oophorus cells stimulates human sperm velocity. Biol Reprod. 1994;51:184–192
  14. Mansour RT, Aboulghar MA, Serour GI, Abbas AM, Elattar I. The life span of sperm motility and pattern in cumulus coculture. Fertil Steril. 1995;63:660–662
  15. Hossain AM, Rizk B, Huff C, Helvacioglu A, Thorneycroft IH. Human sperm bioassay has potential in evaluating the quality of cumulus-oocyte complexes. Arch Androl. 1996;37:7–10
  16. Yao Y, Ho P, Yeung WS. Effects of human follicular fluid on spermatozoa that have been cocultured with human oviductal cells. Fertil Steril. 1999;72:1079–1084
  17. Hong SJ, Chiu PC, Lee KF, Tse JMY, Ho PC, Yeung WSB. Establishment of a capillary-cumulus model to study the selection of sperm for fertilization by cumulus oophorus. Hum Reprod. 2004;19:1562–1569
  18. Chiu PC, Chung MK, Koistinen R, Koistinen H, Seppala M, Ho PC, et al. Cumulus oophorus-associated glycodelin-C displaces sperm-bound glycodelin-A and -F and stimulates spermatozoa-zona pellucida binding. J Biol Chem. 2007;282:5378–5388
  19. Hong SJ, Tse JY, Ho PC, Yeung WS. Cumulus cells reduce the spermatozoa-zona binding inhibitory activity of human follicular fluid. Fertil Steril. 2003;79(Suppl 1):802–807
  20. Bains R, Miles DM, Carson RJ, Adeghe J. Hyaluronic acid increases motility/intracellular CA2+ concentration in human sperm in vitro. Arch Androl. 2001;47:119–125
  21. Sun F, Bahat A, Gakamsky A, Girsh E, Katz N, Giojalas LC, et al. Human sperm chemotaxis: both the oocyte and its surrounding cumulus cells secrete sperm chemoattractants. Hum Reprod. 2005;20:761–767
  22. Salustri A, Yanagishita M, Hascall VC. Synthesis and accumulation of hyaluronic acid and proteoglycans in the mouse cumulus cell–oocyte complex during follicle-stimulating hormone–induced mucification. J Biol Chem. 1989;264:13840–13847
  23. Talbot P. Hyaluronidase dissolves a component in the hamster zona pellucida. J Exp Zool. 1984;229:309–316
  24. Camaioni A, Hascall VC, Yanagishita M, Salustri A. Effects of exogenous hyaluronic acid and serum on matrix organization and stability in the mouse cumulus cell–oocyte complex. J Biol Chem. 1993;268:20473–20481
  25. Chen L, Russell PT, Larsen WJ. Functional significance of cumulus expansion in the mouse: roles for the preovulatory synthesis of hyaluronic acid within the cumulus mass. Mol Reprod Dev. 1993;34:87–93
  26. Zhuo L, Kimata K. Cumulus oophorus extracellular matrix: its construction and regulation. Cell Struct Funct. 2001;26:189–196
  27. Sabeur K, Cherr GN, Yudin AI, Overstreet JW. Hyaluronic acid enhances induction of the acrosome reaction of human sperm through interaction with the PH-20 protein. Zygote. 1998;6:103–111
  28. World Health Organization. Laboratory manual for the examination of human semen and semen–cervical mucus interaction. New York: Cambridge University Press; 1999;
  29. Ng EH, Yeung WS, Yee LL, So WW, Ho PC. High serum oestradiol concentrations in fresh IVF cycles do not impair implantation and pregnancy rates in subsequent frozen-thawed embryo transfer cycles. Hum Reprod. 2000;15:250–255
  30. Ling JY, Kienzle TE, Stroop WG. An improved rapid method for purification of herpes simplex virus DNA using cesium trifluoroacetate. J Virol Methods. 1996;58:193–198
  31. Huszar G, Celik-Ozenci C, Cayli S, Kovacs T, Vigue L, Kovanci E. Semen characteristics after overnight shipping: preservation of sperm concentrations, HspA2 ratios, CK activity, cytoplasmic retention, chromatin maturity, DNA integrity, and sperm shape. J Androl. 2004;25:593–604
  32. Menkveld R, Stander FS, Kotze TJ, Kruger TF, van Zyl JA. The evaluation of morphological characteristics of human spermatozoa according to stricter criteria. Hum Reprod. 1990;5:586–592
  33. Chiu PC, Chung MK, Tsang HY, Koistinen R, Koistinen H, Seppala M, et al. Glycodelin-S in human seminal plasma reduces cholesterol efflux and inhibits capacitation of spermatozoa. J Biol Chem. 2005;280:25580–25589
  34. Chiu PC, Ho PC, Ng EH, Yeung WS. Comparative study of the biological activity of spermatozoa–zona pellucida binding inhibitory factors from human follicular fluid on various sperm function parameters. Mol Reprod Dev. 2002;61:205–212
  35. Chiu PC, Koistinen R, Koistinen H, Seppala M, Lee KF, Yeung WS. Binding of zona binding inhibitory factor-1 (ZIF-1) from human follicular fluid on spermatozoa. J Biol Chem. 2003;278:13570–13577
  36. Tanghe S, Van Soom A, Nauwynck H, Coryn M, de Kruif A. Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev. 2002;61:414–424
  37. Rodgers RJ, Irving-Rodgers HF, Russell DL. Extracellular matrix of the developing ovarian follicle. Reproduction. 2003;126:415–424
  38. Suarez SS, Pacey AA. Sperm transport in the female reproductive tract. Hum Reprod Update. 2006;12:23–37
  39. Jones AR. Metabolism of lactate by mature boar spermatozoa. Reprod Fertil Dev. 1997;9:227–232
  40. O'Flaherty CM, Beorlegui NB, Beconi MT. Lactate dehydrogenase-C4 is involved in heparin- and NADH-dependent bovine sperm capacitation. Andrologia. 2002;34:91–97
  41. Goldberg E. Molecular basis for multiple forms of LDH-X. J Exp Zool. 1973;186:273–278
  42. Gerez dBN, Burgos C, Coronel CE, Bertarelli DC, Pigini T, Blanco A. Correlation of lactate dehydrogenase isoenzyme C4 activity with the count and motility of human spermatozoa. J Reprod Fertil. 1979;55:107–111
  43. Gavella M, Cvitkovic P. Semen LDH-X deficiency and male infertility. Arch Androl. 1985;15:173–176
  44. Gardner DK, Lane M, Calderon I, Leeton J. Environment of the preimplantation human embryo in vivo: metabolite analysis of oviduct and uterine fluids and metabolism of cumulus cells. Fertil Steril. 1996;65:349–353
  45. Gardner DK, Leese HJ. Concentrations of nutrients in mouse oviduct fluid and their effects on embryo development and metabolism in vitro. J Reprod Fertil. 1990;88:361–368
  46. Baker MA, Aitken RJ. The importance of redox regulated pathways in sperm cell biology. Mol Cell Endocrinol. 2004;216:47–54
  47. de Lamirande E, Jiang H, Zini A, Kodama H, Gagnon C. Reactive oxygen species and sperm physiology. Rev Reprod. 1997;2:48–54
  48. Baker MA, Aitken RJ. Reactive oxygen species in spermatozoa: methods for monitoring and significance for the origins of genetic disease and infertility. Reprod Biol Endocrinol. 2005;29:67
  49. Tatemoto H, Sakurai N, Muto N. Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during In vitro maturation: role of cumulus cells. Biol Reprod. 2000;63:805–810
  50. Tesarik J, Mendoza OC, Testart J. Effect of the human cumulus oophorus on movement characteristics of human capacitated spermatozoa. J Reprod Fertil. 1990;88:665–675
  51. Kornovski BS, McCoshen J, Kredentser J, Turley E. The regulation of sperm motility by a novel hyaluronan receptor. Fertil Steril. 1994;61:935–940
  52. Ranganathan S, Ganguly AK, Datta K. Evidence for presence of hyaluronan binding protein on spermatozoa and its possible involvement in sperm function. Mol Reprod Dev. 1994;38:69–76
  53. Dirnfeld M, Goldman S, Gonen Y, Koifman M, Lissak A, Kraiem Z, et al. Functional differentiation in progesterone secretion by granulosa versus cumulus cells in the human preovulatory follicle and the effect of different induction of ovulation protocols. Fertil Steril. 1993;60:1025–1030
  54. Chian RC, Ao A, Clarke HJ, Tulandi T, Tan SL. Production of steroids from human cumulus cells treated with different concentrations of gonadotropins during culture in vitro. Fertil Steril. 1999;71:61–66
  55. Luconi M, Francavilla F, Porazzi I, Macerola B, Forti G, Baldi E. Human spermatozoa as a model for studying membrane receptors mediating rapid nongenomic effects of progesterone and estrogens. Steroids. 2004;69:553–559
  56. Huszar G, Willetts M, Corrales M. Hyaluronic acid (Sperm Select) improves retention of sperm motility and velocity in normospermic and oligospermic specimens. Fertil Steril. 1990;54:1127–1134
  57. Ohta N, Saito H, Kuzumaki T, Takahashi T, Ito MM, Saito T, et al. Expression of CD44 in human cumulus and mural granulosa cells of individual patients in in-vitro fertilization programmes. Mol Hum Reprod. 1999;5:22–28

 S.-J. H. has nothing to disclose. P. C.-C. has nothing to disclose. K.-F. L. has nothing to disclose. J.Y.-M. T. has nothing to disclose. P.-C. H. has nothing to disclose. W.S.-B. Y. has nothing to disclose.

 Supported by grants from the Research Grant Council, Hong Kong (HKU 7408/03M).

PII: S0015-0282(08)03283-4

doi: 10.1016/j.fertnstert.2008.07.1760

Fertility and Sterility
Volume 92, Issue 3 , Pages 971-978 , September 2009