Effect of Estrogenic Xonibiotics on Boar Sperm Motility and Motion Kinematics

Estrogenic Xenobiotics가 돼지 정자의 운동성 및 운동역학에 미치는 영향

  • Oh, Shin-Ae (Department of Animal Science and Technology, School of Bioresource & Bioscience, Chung-Ang University) ;
  • Park, Yoo-Jin (Department of Animal Science and Technology, School of Bioresource & Bioscience, Chung-Ang University) ;
  • Song, Won-Hee (Department of Animal Science and Technology, School of Bioresource & Bioscience, Chung-Ang University) ;
  • Mohamed, El-Sayed A. (Department of Animal Science and Technology, School of Bioresource & Bioscience, Chung-Ang University) ;
  • Pang, Myung-Geol (Department of Animal Science and Technology, School of Bioresource & Bioscience, Chung-Ang University)
  • 오신애 (중앙대학교 생명자원공학부 동물생명공학) ;
  • 박유진 (중앙대학교 생명자원공학부 동물생명공학) ;
  • 송원희 (중앙대학교 생명자원공학부 동물생명공학) ;
  • ;
  • 방명걸 (중앙대학교 생명자원공학부 동물생명공학)
  • Received : 2011.02.21
  • Accepted : 2011.02.28
  • Published : 2011.03.31

Abstract

Endocrine disruptors bind to hormone receptors on sperm membrane, therefore spermatozoa are potentially a useful model for examining estrogenic activities of endocrine disruptors. The objective of this study was to compare the effects of two xenoestrogenic compounds [genistein (Gen) and 4-tert-octylphenol (OP)] to those of two steroids [estrogen ($E_2$) and progesterone ($P_4$)] on boar sperm % motility and motion kinematics of in vitro. Porcine spermatozoa were incubated with various concentrations ($0.001{\sim}100\;{\mu}M$) of each chemical for 15 or 30 min, and then assessed % motility and sperm motion kinematics using computer assisted sperm analyzer (CASA). Each chemical decreased sperm % motility, and OP decreased VSL and VAP compared with untreated control(p<0.05). $E_2$ stimulated the motion kinematic changes except VCL. Moreover, Gen had effects on VCL and VAP alterations after 30 min incubation. In summary, since all chemicals studied effectively altered sperm % motility and motion kinematics, it was concluded that porcine spermatozoa could be a useful model for in vitro screening of potential endocrine disruptors.

Keywords

References

  1. Adeoya-Osiguwa SA, Markoulaki S, Pocock V, Milligan SR, Fraser LR (2003): 17beta-estradiol and environmental estrogens significantly affect mammalian sperm function. Hum Reprod 18:100-107. https://doi.org/10.1093/humrep/deg037
  2. Akingbemi BT, Hardy MP (2001): Oestrogenic and antiandrogenic chemicals in the environment: effects on male reproductive health. Ann Med 33:391-403. https://doi.org/10.3109/07853890108995952
  3. Aydogan M, Barlas N (2006): Effect of maternal 4-tert-octylphenol exposure on the reproductive tract of male rats and adulthood. Reprod Toxicology 22:455-460. https://doi.org/10.1016/j.reprotox.2006.01.004
  4. Couse JF, Korach KS (1999): Estrogen receptor null mice: what have we learned and where will they lead us? Endocr Rev 20:358-417. https://doi.org/10.1210/er.20.3.358
  5. Ded L, Dostalova P, Dorosh A, Dvorakova-Hortova K, Peknicova J (2010): Effect of estrogens on boar sperm capacitation in vitro. Reprod BioI Endocrinol 13:87-97.
  6. Dixon RA (2004): Phytoestrogens. Annu Rev Plant BioI. 55:225-261. https://doi.org/10.1146/annurev.arplant.55.031903.141729
  7. Durkee TJ, Mueller M Zinaman M (1998): Identification of estrogen receptor protein and messenger ribonucleic acid in human spermatozoa. Am J Obstet GynecoI. 178:1288-1297. https://doi.org/10.1016/S0002-9378(98)70335-7
  8. Durkee TJ, Mueller M, Zinaman M (1998): Identification of estrogen receptor protein and messenger ribonucleic acid in human spermatozoa. Am J Obstet Gynecol 178:1288-1297. https://doi.org/10.1016/S0002-9378(98)70335-7
  9. Fraser LR, Beyret E, Milligan SR, Adeoya-Osiguwa SA (2006): Effects of estrogenic xenobiotics on human and mouse spermatozoa. Hum Reprod 21:1184-1193. https://doi.org/10.1093/humrep/dei486
  10. Kim JC, Li Y, Lee S, Yi YJ, Park CS, Woo SH (2008): Effects of cryopreservation on $Ca^{2+}$ signals induced by membrane depolarization, caffeine, thapsigargin and progesterone in boar spermatozoa. Mol Cells 26(6):558-565.
  11. Kuiper GGJM, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson JA (1998): Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138:863-870.
  12. Libersky EA, Boatman DE (1995): Progesterone concentrations in serum, follicular fluid, and oviductal fluid of the golden hamster during periovulatory period. BioI Reprod 53:477-482. https://doi.org/10.1095/biolreprod53.3.477
  13. Luconi M, Bonaccorsi L, Forti G, Baldi E (2001): Effects of estrogenic compounds on human spermatozoa: evidence for interaction with a nongenomic receptor for estrogen on hmnan sperm membrane. Mol Cell Endocrinol 178:39-45. https://doi.org/10.1016/S0303-7207(01)00416-6
  14. Luconi M, Francavilla F, Porazzi I, Macerola B, Forti G, Baldi E (2004): Human spermatozoa as a model for studying membrane receptors mediating rapid nongenomic effects of progesterone and estrogens. Steroids 69:553-559. https://doi.org/10.1016/j.steroids.2004.05.013
  15. Luconi M, Muratori M, Forti G, Baldi E (1999): Identification and characterization of a novel functional estrogen receptor on human sperm membrane that interferes with progesterone effects. J Clin EndocrinoI Metab 84:1670-1678. https://doi.org/10.1210/jc.84.5.1670
  16. Milligan SR, Kalita JC, Heyerick A, Rong H, De Cooman L, De Keukeleire D (1999): Identification of a potent phytoestrogen in hops (Humulus lupulus L.) and beer. J Clin Endocrinol Metab 83:2249-2252.
  17. Milligan SR, Kalita JC, Pocock V, Van de Kauter V, Stevens JF, Deinzer ML, Rong H, De Keukeleire D (2000): The endocrine activities of 8-prenylnaringenin and related hop (Humulus lupulus L.) flavonoids. J Clin Endocrinol Metab 85:4912-4915.
  18. Misao R, Niwa K, Morishita S, Fujimoto J, Nakanishi Y, Tamaya T (1997): Immunohistochemical detection of estrogen and progesterone receptors in spermatozoa of infertile men. Int J Fertil 42:421-425.
  19. Mohamed ES, Park YJ, Song WH, Shin DB, You YA, Ryu BY, Pang MG (2011): Xenoestrogenic compounds promote capacitation and an acrosome reaction in porcine sperm. Theriogenology 75(6):1161-9. https://doi.org/10.1016/j.theriogenology.2010.11.028
  20. Neild DN, Gadella BM, Aguero A, Stout TAE, Colenbrander B (2005): Capacitation, acrosome finction and chromatin structure in stallion sperm. Anim Reprod Sci 89:47-56. https://doi.org/10.1016/j.anireprosci.2005.06.017
  21. Rago V, Aquila S, Panza R, Carpino A (2007): Cytochrome $P_{450}arom$, androgen and estrogen receptors in pig sperm. Reprod BioI Endocrinol 2007;5:23-28. https://doi.org/10.1186/1477-7827-5-23
  22. Rathi R, Colenbrander B, Stout TAE, Bevers MM, Gadella BM (2003): Progesterone induces acrosome reaction in stallion spermatozoa via a protein tyrosine kinase dependent pathway. Mol Reprod Dev 64:120-128. https://doi.org/10.1002/mrd.10216
  23. Rochira V, Granata AR, Madeo B, Zirilli L, Rossi G Carani C (2005): Estrogens in males: what have we learned in the last 10 years. Asian J Androl 7:3-20. https://doi.org/10.1111/j.1745-7262.2005.00018.x
  24. Saaranen MJ, Calvo L, Dennison L, Banks S, Bustillon AD, Dorfmann M, Goldstein M, Thorsell L, Schulmann JD, Sherins RJ (1993): Acrosome reaction inducing activity in follicular fluids correlates with progesterone concentration but not with oocyte maturity or fertilizability. Hum Reprod 8:1448-1454.
  25. Saberwal GS, Sharma MK, Balasinor N, Choudhary J, Juneja HS (2002): Estrogen receptor, calcium mobilization and rat sperm motility. Mol Cell Biochem 237:11-20. https://doi.org/10.1023/A:1016549922439
  26. Saberwal GS, Sharma MK, Balasinor N, Choudhary J, Juneja HS (2002): Estrogen receptor, calcium mobilization and rat sperm motility. Mol Cell Biochem 237:11-20. https://doi.org/10.1023/A:1016549922439
  27. Sharpe RM (2001): Hormones and testis development and the possible adverse effects of environmental chemicals. Toxicol Lett 120:221-232. https://doi.org/10.1016/S0378-4274(01)00298-3
  28. Sirianni R, Chimento A, Ruggiero C, De Luca A, Lappano R, Ando S, Maggiolini M, Pezzi V (2008): The novel estrogen receptor, G protein-coupled receptor 30, mediates the proliferative effects induced by 17 beta-estradiol on mouse spermatogonial GC-1 cell line. Endocrinology 149:5043-51. https://doi.org/10.1210/en.2007-1593
  29. Sirivaidyapong S, Bevers MM, Gadella BM, Colenbrander B (2001): Induction of the acrosome reaction in dog sperm cells is dependent on epididymal maturation: the generation of a functional progesterone receptor is involved. Mol Reprod Dev 58:451-459. https://doi.org/10.1002/1098-2795(20010401)58:4<451::AID-MRD14>3.0.CO;2-K
  30. Skakkebaek NE, Rajpert-De Meyts E, Main KM (2001): Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod 16:972-978. https://doi.org/10.1093/humrep/16.5.972
  31. Sohoni P, Sumpter JP (1998): Several environmental oestrogens are also anti-androgens. J Endocrinol 158:327-339. https://doi.org/10.1677/joe.0.1580327
  32. Stormshak F, Bishop CV (2008): Estrogen and progesterone signaling: genomic and nongenomic actions in domestic ruminants. J Anim Sci 86:299-315. https://doi.org/10.2527/jas.2007-0489
  33. Tubbs C, Thomas P (2008): Functional characteristics of membrane progestin receptor (mPR) subtypes: a review with new data showing mPR expression in seatrout sperm and its association with sperm motility. Steroids 73:935-941. https://doi.org/10.1016/j.steroids.2007.12.022
  34. Tubbs C, Thomas P (2009): Progestin signaling through an olfactory G protein and membrane progestin receptor-alpha in Atlantic croaker sperm: potential role in induction of sperm hypermotility. Endocrinology. 150:473-484.
  35. Uhler ML, Leung A, Chan SYW, Wang C (1992): Direct effects of progesterone and antiprogesterone on human sperm hyperactivated motility and acrosome reaction. FertiI Steril 58:1191-1198.
  36. Watson CE, Gauthier SY, Davies PL (1999): Structure and expression of the highly repetitive hustine H1-related sperm chromatin proteins from winter flounder. J Bio Chem 262:258-267.
  37. Watson CE, Gauthier SY, Davies PL (1999): Structure and expression of the highly repetitive hustine H1- related sperm chromatin proteins from winter flounder. J Bio Chem 262:258-267.
  38. Yanagimachi R (1994): Mammalian fertilization. In: Knobil E, Neill JD, editors. The Physiology of Eproduction. New York: Raven Press. pp 189-317.