Clinical and Experimental Reproductive Medicine

  • 제48권1호
  • /
  • Pages.50-60
  • /
  • 2021
  • /
  • 2233-8233(pISSN)
  • /
  • 2233-8241(eISSN)
대한생식의학회 (The Korean Society for Reproductive Medicine)
권호 표지
DOI QR코드

DOI QR Code

High mRNA expression of GABA receptors in human sperm with oligoasthenoteratozoospermia and teratozoospermia and its association with sperm parameters and intracytoplasmic sperm injection outcomes

  • Kaewman, Paweena (Department of Anatomy, Faculty of Medical Science, Naresuan University) ;
  • Nudmamud-Thanoi, Sutisa (Department of Anatomy, Faculty of Medical Science, Naresuan University) ;
  • Amatyakul, Patcharada (Department of Obstetrics and Gynecology, Faculty of Medicine, Naresuan University) ;
  • Thanoi, Samur (Department of Anatomy, Faculty of Medical Science, Naresuan University)
  • 투고 : 2020.08.01
  • 심사 : 2020.10.17
  • 발행 : 2021.03.31
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Objective: This study investigated the mRNA expression of gamma-aminobutyric acid (GABA) receptors in the sperm of oligoasthenoteratozoospermic (OAT) and teratozoospermic (TER) men compared to normozoospermic (NOR) men, as well as the relationships between GABA receptor expression and sperm parameters, fertilization rate, and embryo quality. Methods: The mRNA expression of GABA A-α1 and GABA B-R2 receptors in sperm was examined using reverse transcription-polymerase chain reaction in three groups of patients: NOR (n=32), OAT (n=22), and TER (n=45). The fertilization rate and embryo quality were assessed in 35 patients undergoing intracytoplasmic sperm injection (ICSI; 10 NOR, 10 OAT, and 15 TER men). Results: OAT men had significantly higher mRNA expression of GABA A-α1 and GABA B-R2 receptors in sperm than NOR men; however, the difference between TER and NOR men was not significant. High levels of these receptors were significantly correlated with low sperm concentration, motility, and morphology, as well as the rate of good-quality embryos (GQEs) at the cleavage stage after ICSI. Patients whose female partners had a >50% GQE rate at the cleavage stage had significantly lower levels of GABA A-α1 receptor expression than those whose partners had a ≤50% GQE rate. Conclusion: Our findings indicate that mRNA levels of GABA receptors in human sperm are correlated with poor sperm quality and associated with embryo development after ICSI treatment. The GABA A-α1 receptor in sperm has a stronger relationship with embryo quality at the cleavage stage than the GABA B-R2 receptor.

키워드

과제정보

We appreciate the facilities support from Naresuan University and the helpful comments from the Naresuan Infertility Centre. We would like to thank all patients for their participation.

참고문헌

  1. Gladkevich A, Korf J, Hakobyan VP, Melkonyan KV. The peripheral GABAergic system as a target in endocrine disorders. Auton Neurosci 2006;124:1-8. https://doi.org/10.1016/j.autneu.2005.11.002
  2. Hu JH, He XB, Wu Q, Yan YC, Koide SS. Subunit composition and function of GABAA receptors of rat spermatozoa. Neurochem Res 2002;27:195-9. https://doi.org/10.1023/A:1014876303062
  3. Li SF, Hu JH, Yan YC, Chen YG, Koide SS, Li YP. Identification and characterization of a novel splice variant of beta3 subunit of GABA(A) receptor in rat testis and spermatozoa. Int J Biochem Cell Biol 2005;37:350-60. https://doi.org/10.1016/j.biocel.2004.07.008
  4. Li S, Zhang Y, Liu H, Yan Y, Li Y. Identification and expression of GABAC receptor in rat testis and spermatozoa. Acta Biochim Biophys Sin (Shanghai) 2008;40:761-7. https://doi.org/10.1111/j.1745-7270.2008.00453.x
  5. He XB, Hu JH, Wu Q, Yan YC, Koide SS. Identification of GABA(B) receptor in rat testis and sperm. Biochem Biophys Res Commun 2001;283:243-7. https://doi.org/10.1006/bbrc.2001.4732
  6. He X, Zhang Y, Yan Y, Li Y, Koide SS. Identification of GABABR2 in rat testis and sperm. J Reprod Dev 2003;49:397-402. https://doi.org/10.1262/jrd.49.397
  7. Kurata S, Hiradate Y, Umezu K, Hara K, Tanemura K. Capacitation of mouse sperm is modulated by gamma-aminobutyric acid (GABA) concentration. J Reprod Dev 2019;65:327-34. https://doi.org/10.1262/jrd.2019-008
  8. Wistrom CA, Meizel S. Evidence suggesting involvement of a unique human sperm steroid receptor/Cl- channel complex in the progesterone-initiated acrosome reaction. Dev Biol 1993;159:679-90. https://doi.org/10.1006/dbio.1993.1274
  9. Calogero AE, Hall J, Fishel S, Green S, Hunter A, D'Agata R. Effects of gamma-aminobutyric acid on human sperm motility and hyperactivation. Mol Hum Reprod 1996;2:733-8. https://doi.org/10.1093/molehr/2.10.733
  10. Ritta MN, Bas DE, Tartaglione CM. In vitro effect of gamma-aminobutyric acid on bovine spermatozoa capacitation. Mol Reprod Dev 2004;67:478-86. https://doi.org/10.1002/mrd.20038
  11. Jin JY, Chen WY, Zhou CX, Chen ZH, Yu-Ying Y, Ni Y, et al. Activation of GABAA receptor/Cl- channel and capacitation in rat spermatozoa: HCO3- and Cl- are essential. Syst Biol Reprod Med 2009;55: 97-108. https://doi.org/10.1080/19396360802626648
  12. Ritta MN, Calamera JC, Bas DE. Occurrence of GABA and GABA receptors in human spermatozoa. Mol Hum Reprod 1998;4:769-73. https://doi.org/10.1093/molehr/4.8.769
  13. Binh NT, Van Thuan N, Miyake M. Effects of liquid preservation of sperm on their ability to activate oocytes and initiate preimplantational development after intracytoplasmic sperm injection in the pig. Theriogenology 2009;71:1440-50. https://doi.org/10.1016/j.theriogenology.2009.01.018
  14. Kon H, Takei GL, Fujinoki M, Shinoda M. Suppression of progesterone-enhanced hyperactivation in hamster spermatozoa by γ-aminobutyric acid. J Reprod Dev 2014;60:202-9. https://doi.org/10.1262/jrd.2013-076
  15. Calogero AE, Burrello N, Ferrara E, Hall J, Fishel S, D'Agata R. Gamma-aminobutyric acid (GABA) A and B receptors mediate the stimulatory effects of GABA on the human sperm acrosome reaction: interaction with progesterone. Fertil Steril 1999;71:930-6. https://doi.org/10.1016/S0015-0282(99)00063-1
  16. Burrello N, Vicari E, D'Amico L, Satta A, D'Agata R, Calogero AE. Human follicular fluid stimulates the sperm acrosome reaction by interacting with the gamma-aminobutyric acid receptors. Fertil Steril 2004;82 Suppl 3:1086-90. https://doi.org/10.1016/j.fertnstert.2004.04.028
  17. Puente MA, Tartaglione CM, Ritta MN. Bull sperm acrosome reaction induced by gamma-aminobutyric acid (GABA) is mediated by GABAergic receptors type A. Anim Reprod Sci 2011;127:31-7. https://doi.org/10.1016/j.anireprosci.2011.07.001
  18. Gramajo-Buhler MC, Zelarayan L, Lopez Luis A, Sanchez-Toranzo G. Acrosome reaction in the epididymal sperm of Chinchilla lanigera: effect of progesterone, A23187 and stimulation of a GABAA-like receptor. J Exp Zool A Ecol Genet Physiol 2012;317:259-65. https://doi.org/10.1002/jez.1718
  19. da Silva MC, Wessler LB, Madeira K, da Silva CC. Male infertility profile in an assisted human reproduction clinic from the south of Santa Catarina, Brazil, from 2012 to 2014. Reprod Climaterio 2017; 32:90-6. https://doi.org/10.1016/j.recli.2017.03.001
  20. Vander Borght M, Wyns C. Fertility and infertility: definition and epidemiology. Clin Biochem 2018;62:2-10. https://doi.org/10.1016/j.clinbiochem.2018.03.012
  21. Babakhanzadeh E, Nazari M, Ghasemifar S, Khodadadian A. Some of the factors involved in male infertility: a prospective review. Int J Gen Med 2020;13:29-41. https://doi.org/10.2147/IJGM.S241099
  22. Fainberg J, Kashanian JA. Recent advances in understanding and managing male infertility. F1000Res 2019;8:F1000 Faculty Rev-670.
  23. Neri QV, Lee B, Rosenwaks Z, Machaca K, Palermo GD. Understanding fertilization through intracytoplasmic sperm injection (ICSI). Cell Calcium 2014;55:24-37. https://doi.org/10.1016/j.ceca.2013.10.006
  24. Bhilawadikar R, Zaveri K, Mukadam L, Naik S, Kamble K, Modi D, et al. Levels of Tektin 2 and CatSper 2 in normozoospermic and oligoasthenozoospermic men and its association with motility, fertilization rate, embryo quality and pregnancy rate. J Assist Reprod Genet 2013;30:513-23. https://doi.org/10.1007/s10815-013-9972-6
  25. Anifandis G, Messini CI, Dafopoulos K, Daponte A, Messinis IE. Sperm contributions to oocyte activation: more that meets the eye. J Assist Reprod Genet 2016;33:313-6. https://doi.org/10.1007/s10815-016-0653-0
  26. Morozumi K, Shikano T, Miyazaki S, Yanagimachi R. Simultaneous removal of sperm plasma membrane and acrosome before intracytoplasmic sperm injection improves oocyte activation/embryonic development. Proc Natl Acad Sci U S A 2006;103:17661-6. https://doi.org/10.1073/pnas.0608183103
  27. Takeuchi T, Colombero LT, Neri QV, Rosenwaks Z, Palermo GD. Does ICSI require acrosomal disruption? An ultrastructural study. Hum Reprod 2004;19:114-7. https://doi.org/10.1093/humrep/deg511
  28. Seita Y, Ito J, Kashiwazaki N. Removal of acrosomal membrane from sperm head improves development of rat zygotes derived from intracytoplasmic sperm injection. J Reprod Dev 2009;55: 475-9. https://doi.org/10.1262/jrd.20216
  29. Katayama M, Sutovsky P, Yang BS, Cantley T, Rieke A, Farwell R, et al. Increased disruption of sperm plasma membrane at sperm immobilization promotes dissociation of perinuclear theca from sperm chromatin after intracytoplasmic sperm injection in pigs. Reproduction 2005;130:907-16. https://doi.org/10.1530/rep.1.0680
  30. World Health Organization. WHO laboratory manual for the examination and processing of human semen. Geneva: World Health Organization; 2010.
  31. Chen ZA, Bao MY, Xu YF, Zha RP, Shi HB, Chen TY, et al. Suppression of human liver cancer cell migration and invasion via the GABAA receptor. Cancer Biol Med 2012;9:90-8. https://doi.org/10.3969/j.issn.2095-3941.2012.02.002
  32. Plummer PN, Colson NJ, Lewohl JM, MacKay RK, Fernandez F, Haupt LM, et al. Significant differences in gene expression of GABA receptors in peripheral blood leukocytes of migraineurs. Gene 2011;490:32-6. https://doi.org/10.1016/j.gene.2011.08.031
  33. Yang L, Yu SJ, Hong Q, Yang Y, Shao ZM. Reduced expression of TET1, TET2, TET3 and TDG mRNAs are associated with poor prognosis of patients with early breast cancer. PLoS One 2015;10:e0133896. https://doi.org/10.1371/journal.pone.0133896
  34. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25:402-8. https://doi.org/10.1006/meth.2001.1262
  35. SHRE Working Group on Ultrasound in ART; D'Angelo A, Panayotidis C, Amso N, Marci R, Matorras R, et al. Recommendations for good practice in ultrasound: oocyte pick up. Hum Reprod Open 2019;2019:hoz025. https://doi.org/10.1093/hropen/hoz025
  36. Alpha Scientists in Reproductive Medicine and ESHRE Special Interest Group of Embryology. The Istanbul consensus workshop on embryo assessment: proceedings of an expert meeting. Hum Reprod 2011;26:1270-83. https://doi.org/10.1093/humrep/der037
  37. Gardner DK, Lane M, Stevens J, Schlenker T, Schoolcraft WB. Blastocyst score affects implantation and pregnancy outcome: towards a single blastocyst transfer. Fertil Steril 2000;73:1155-8. https://doi.org/10.1016/S0015-0282(00)00518-5
  38. Kaewman P, Nudmamud-Thanoi S, Thanoi S. GABAergic alterations in the rat testis after methamphetamine exposure. Int J Med Sci 2018;15:1349-54. https://doi.org/10.7150/ijms.27609
  39. Geigerseder C, Doepner RF, Thalhammer A, Krieger A, Mayerhofer A. Stimulation of TM3 Leydig cell proliferation via GABA(A) receptors: a new role for testicular GABA. Reprod Biol Endocrinol 2004;2:13. https://doi.org/10.1186/1477-7827-2-13
  40. Hu JH, Zhang JF, Ma YH, Jiang J, Yang N, Li XB, et al. Impaired reproduction in transgenic mice overexpressing Gamma-aminobutyric acid transporter I (GAT1). Cell Res 2004;14:54-9. https://doi.org/10.1038/sj.cr.7290202
  41. Loutradi KE, Tarlatzis BC, Goulis DG, Zepiridis L, Pagou T, Chatziioannou E, et al. The effects of sperm quality on embryo development after intracytoplasmic sperm injection. J Assist Reprod Genet 2006;23:69-74. https://doi.org/10.1007/s10815-006-9022-8
  42. Li B, Ma Y, Huang J, Xiao X, Li L, Liu C, et al. Probing the effect of human normal sperm morphology rate on cycle outcomes and assisted reproductive methods selection. PLoS One 2014;9:e113392. https://doi.org/10.1371/journal.pone.0113392
  43. Sivanarayana T, Krishna ChR, Prakash GJ, Krishna KM, Madan K, Rani BS, et al. CASA derived human sperm abnormalities: correlation with chromatin packing and DNA fragmentation. J Assist Reprod Genet 2012;29:1327-34. https://doi.org/10.1007/s10815-012-9885-9
  44. Calogero AE, De Palma A, Grazioso C, Barone N, Romeo R, Rappazzo G, et al. Aneuploidy rate in spermatozoa of selected men with abnormal semen parameters. Hum Reprod 2001;16:1172-9. https://doi.org/10.1093/humrep/16.6.1172
  45. Huang CC, Lin DP, Tsao HM, Cheng TC, Liu CH, Lee MS. Sperm DNA fragmentation negatively correlates with velocity and fertilization rates but might not affect pregnancy rates. Fertil Steril 2005;84: 130-40. https://doi.org/10.1016/j.fertnstert.2004.08.042
  46. Komiya A, Kato T, Kawauchi Y, Watanabe A, Fuse H. Clinical factors associated with sperm DNA fragmentation in male patients with infertility. ScientificWorldJournal 2014;2014:868303.
  47. Sivanarayana T, Ravi Krishna C, Jaya Prakash G, Krishna KM, Madan K, Sudhakar G, et al. Sperm DNA fragmentation assay by sperm chromatin dispersion (SCD): correlation between DNA fragmentation and outcome of intracytoplasmic sperm injection. Reprod Med Biol 2013;13:87-94. https://doi.org/10.1007/s12522-013-0168-7
  48. Borges E Jr, Zanetti BF, Setti AS, Braga DP, Provenza RR, Iaconelli A Jr. Sperm DNA fragmentation is correlated with poor embryo development, lower implantation rate, and higher miscarriage rate in reproductive cycles of non-male factor infertility. Fertil Steril 2019;112:483-90. https://doi.org/10.1016/j.fertnstert.2019.04.029
  49. Kim GY. What should be done for men with sperm DNA fragmentation? Clin Exp Reprod Med 2018;45:101-9. https://doi.org/10.5653/cerm.2018.45.3.101
  50. Chi HJ, Kim SG, Kim YY, Park JY, Yoo CS, Park IH, et al. ICSI significantly improved the pregnancy rate of patients with a high sperm DNA fragmentation index. Clin Exp Reprod Med 2017;44: 132-40. https://doi.org/10.5653/cerm.2017.44.3.132
  51. Yanagimachi R. Intracytoplasmic injection of spermatozoa and spermatogenic cells: its biology and applications in humans and animals. Reprod Biomed Online 2005;10:247-88. https://doi.org/10.1016/S1472-6483(10)60947-9
  52. Kurokawa M, Fissore RA. ICSI-generated mouse zygotes exhibit altered calcium oscillations, inositol 1,4,5-trisphosphate receptor-1 down-regulation, and embryo development. Mol Hum Reprod 2003;9:523-33. https://doi.org/10.1093/molehr/gag072