Clinical and Experimental Reproductive Medicine

The Korean Society for Reproductive Medicine (대한생식의학회)
권호 표지
DOI QR코드

DOI QR Code

Effect of thymectomy on the female reproductive cycle in neonatal guinea pigs

  • Murali, P. (Department of Anatomy, SRM Medical College Hospital and Research Centre) ;
  • Radhika, J. (SRM Medical College Hospital and Research Centre) ;
  • Alwin, D. (Central Animal House, SRM Medical College Hospital and Research Centre)
  • Received : 2019.04.30
  • Accepted : 2019.09.24
  • Published : 2020.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: The appropriate function of the hypothalamic-pituitary-gonadal axis is essential for maintaining proper reproductive function. In female mammals, the hypothalamic-pituitary-gonadal axis regulates reproductive changes that take place in the estrus cycle and are necessary for successful reproduction. This study was conducted to investigate the effect of thymectomy on the estrus cycle in neonatally thymectomized guinea pigs. Methods: In this study, 12 female guinea pigs, six thymectomized and six sham-operated, were studied. The effects of neonatal thymectomy at 5-7 days of age on parameters of the reproductive axis were examined in female guinea pigs. Gonadotropin and 17β-estradiol levels were assessed at regular intervals (days 0, 3, 6, 9, 12, and 15) of the estrus cycle, and the time of vaginal opening in the thymectomized and shamoperated guinea pigs was determined. Results: Significant reductions in gonadotropins and 17β-estradiol levels during estrus cycle were found in neonatally thymectomized female guinea pigs compared to sham-operated guinea pigs. Conclusion: The results of this study underscore the importance of the thymus in the neonatal period for normal female reproductive function.

Keywords

References

  1. Sarraj MA, Drummond AE. Mammalian foetal ovarian development: consequences for health and disease. Reproduction 2012;143:151-63. https://doi.org/10.1530/REP-11-0247
  2. Everett JW, Sawyer CH, Markee JE. A neurogenic timing factor in control of the ovulatory discharge of luteinizing hormone in the cyclic rat. Endocrinology 1949;44:234-50. https://doi.org/10.1210/endo-44-3-234
  3. Gonzalez-Martinez D, De Mees C, Douhard Q, Szpirer C, Bakker J. Absence of gonadotropin-releasing hormone 1 and Kiss1 activation in alpha-fetoprotein knockout mice: prenatal estrogens defeminize the potential to show preovulatory luteinizing hormone surges. Endocrinology 2008;149:2333-40. https://doi.org/10.1210/en.2007-1422
  4. King JC, Tai DW, Hanna IK, Pfeiffer A, Haas P, Ronsheim PM, et al. A subgroup of LHRH neurons in guinea pigs with progestin receptors is centrally positioned within the total population of LHRH neurons. Neuroendocrinology 1995;61:265-75. https://doi.org/10.1159/000126848
  5. Espey LL, Richards JS. Ovulation. In: Plant TM, Zeleznik AJ, editors. Knobil and Neill's physiology of reproduction. 4th ed. Cambridge, MA: Academic Press; 2006. p. 425-74.
  6. Karsch FJ, Legan SJ, Ryan KD, Foster DL. Importance of estradiol and progesterone in regulating LH secretion and estrous behavior during the sheep estrous cycle. Biol Reprod 1980;23:404-13. https://doi.org/10.1095/biolreprod23.2.404
  7. Fabre-Nys C, Martin GB. Roles of progesterone and oestradiol in determining the temporal sequence and quantitative expression of sexual receptivity and the preovulatory LH surge in the ewe. J Endocrinol 1991;130:367-79. https://doi.org/10.1677/joe.0.1300367
  8. Caraty A, Skinner DC. Progesterone priming is essential for the full expression of the positive feedback effect of estradiol in inducing the preovulatory gonadotropin-releasing hormone surge in the ewe. Endocrinology 1999;140:165-70. https://doi.org/10.1210/endo.140.1.6444
  9. Balthazart J, Cornil CA, Charlier TD, Taziaux M, Ball GF. Estradiol, a key endocrine signal in the sexual differentiation and activation of reproductive behavior in quail. J Exp Zool A Ecol Genet Physiol 2009;311:323-45.
  10. Trainor BC, Kyomen HH, Marler CA. Estrogenic encounters: how interactions between aromatase and the environment modulate aggression. Front Neuroendocrinol 2006;27:170-9. https://doi.org/10.1016/j.yfrne.2005.11.001
  11. Cui J, Shen Y, Li R. Estrogen synthesis and signaling pathways during aging: from periphery to brain. Trends Mol Med 2013;19:197-209. https://doi.org/10.1016/j.molmed.2012.12.007
  12. Richards JS. Maturation of ovarian follicles: actions and interactions of pituitary and ovarian hormones on follicular cell differentiation. Physiol Rev 1980;60:51-89. https://doi.org/10.1152/physrev.1980.60.1.51
  13. Kelly MJ, Moss RL, Dudley CA. Differential sensitivity of preopticseptal neurons to microelectrophoresed estrogen during the estrous cycle. Brain Res 1976;114:152-7. https://doi.org/10.1016/0006-8993(76)91017-9
  14. Kenealy BP, Kapoor A, Guerriero KA, Keen KL, Garcia JP, Kurian JR, et al. Neuroestradiol in the hypothalamus contributes to the regulation of gonadotropin releasing hormone release. J Neurosci 2013;33:19051-9. https://doi.org/10.1523/JNEUROSCI.3878-13.2013
  15. Plant TM. 60 Years of neuroendocrinology: the hypothalamo-pituitary-gonadal axis. J Endocrinol 2015;226:T41-54. https://doi.org/10.1530/JOE-15-0113
  16. Terasawa E, Fernandez DL. Neurobiological mechanisms of the onset of puberty in primates. Endocr Rev 2001;22:111-51. https://doi.org/10.1210/er.22.1.111
  17. Abreu AP, Kaiser UB. Pubertal development and regulation. Lancet Diabetes Endocrinol 2016;4:254-64. https://doi.org/10.1016/S2213-8587(15)00418-0
  18. Calzolari A. Recherches experimentales sur un rapport probable entre la function du thymus et celle des testicules. Arch Ital Biol 1898;30:71-7.
  19. Lintern-Moore S. Effect of athymia on the initiation of follicular growth in the rat ovary. Biol Reprod 1977;17:155-61. https://doi.org/10.1095/biolreprod17.2.155
  20. Safieh B, Kendall MD, Norman JC, Metreau E, Dardenne M, Bach JF, et al. A new radioimmunoassay for the thymic peptide thymulin, and its application for measuring thymulin in blood samples. J Immunol Methods 1990;127:255-62. https://doi.org/10.1016/0022-1759(90)90076-8
  21. Markovic L. Interaction involving the thymus and the hypothalamus-pituitary axis, immunomodulation by hormones. Srp Arh Celok Lek 2004;132:187-93. https://doi.org/10.2298/SARH0406187M
  22. Dabrowski MP, Dabrowski MI, Stankiewicz W. The thymus in neuro-endocrine-immune network. Centr Eur J Immunol 2011;36:188-92.
  23. Wise T. In vitro and in vivo effects of thymulin on rat testicular steroid synthesis. J Steroid Biochem Mol Biol 1998;66:129-35. https://doi.org/10.1016/S0960-0760(98)00045-4
  24. Allen LS, McClure JE, Goldstein AL, Barkley MS, Michael SD. Estrogen and thymic hormone interactions in the female mouse. J Reprod Immunol 1984;6:25-37. https://doi.org/10.1016/0165-0378(84)90039-1
  25. Kawashima I, Sakabe K, Seiki K, Fujii-Hanamoto H, Akatsuka A, Tsukamoto H. Localization of sex steroid receptor cells, with special reference to thymulin (FTS)-producing cells in female rat thymus. Thymus 1991;18:79-93.
  26. Garcia L, Hinojosa L, Dominguez R, Chavira R, Rosas P. Effects of infantile thymectomy on ovarian functions and gonadotrophininduced ovulation in prepubertal mice: role of thymulin. J Endocrinol 2000;166:381-7. https://doi.org/10.1677/joe.0.1660381
  27. Dullaart J, Kent J, Ryle M. Serum gonadotrophin concentrations in infantile female mice. J Reprod Fert 1975;43:189-92. https://doi.org/10.1530/jrf.0.0430189
  28. Rebar RW, Morandini IC, Benirschke K, Petze JE. Reduced gonadotropins in athymic mice: prevention by thymic transplantation. Endocrinology 1980;107:2130-2. https://doi.org/10.1210/endo-107-6-2130
  29. Sakakura T, Nishizuka Y. Thymic control mechanism in ovarian development: reconstitution of ovarian dysgenesis in thymectomized mice by replacement with thymic and other lymphoid tissues. Endocrinology 1972;90:431-7. https://doi.org/10.1210/endo-90-2-431
  30. Kosiewicz MM, Michael SD. Neonatal thymectomy affects follicle populations before the onset of autoimmune oophoritis in B6A mice. J Reprod Fertil 1990;88:427-40. https://doi.org/10.1530/jrf.0.0880427
  31. Adams DB. The effect of thymectomy in guinea pigs on the lymphocyte content of central lymph. Aust J Exp Biol Med Sci 1977;55:49-57. https://doi.org/10.1038/icb.1977.5
  32. Kohutova S, Jekl V, Knotek Z, Hauptman K. The effect of deslorelin acetate on the oestrous cycle of female guinea pigs. Vet Med 2015;60:155-60.
  33. Jadarmkunti UC, Kaliwal BB. Effect of dicofol formulation on estrous cycle and follicular dynamics in albino rats. J Basic Clin Physiol Pharmacol 1999;10:305-14. https://doi.org/10.1515/JBCPP.1999.10.4.305
  34. Lilley KG, Epping RJ, Hafner LM. The guinea pig estrous cycle: correlation of vaginal impedance measurements with vaginal cytologic findings. Lab Anim Sci 1997;47:632-7.
  35. Itoh M, Hiramine C, Mukasa A, Tokunaga Y, Fukui Y, Takeuchi Y, et al. Establishment of an experimental model of autoimmune epididymo-orchitis induced by the transfer of a T-cell line in mice. Int J Androl 1992;15:170-81.
  36. Sisk DB. Physiology. In: Wagner JE, Manning PJ, editors. The biology of the guinea pig. New York: Academic Press; 1976. p. 63-98.
  37. Michael SD, Taguchi O, Nishizuka Y, MC Clure JE, Gold Stein AL, Barkley MS. The effect of neonatal thymectomy on early follicular loss and circulating level of carticosterone, progesterone, estradiol and thymosin ${\alpha}1$. In: Hunzicker-Dunn M, Schwartz NB, eds. Dynamics of ovarian function. New York: Raven Press; 1981. p. 279-84.
  38. Besedovsky HO, Sorkin E. Thymus involvement in female sexual maturation. Nature 1974;249:356-8. https://doi.org/10.1038/249356a0
  39. Michael SD, Taguchi O, Nishizuka Y. Effect of neonatal thymectomy on ovarian development and plasma LH, FSH, GH and PRL in the mouse. Biol Reprod 1980;22:343-50. https://doi.org/10.1093/biolreprod/22.2.343
  40. Farookhi R, Wesolowski E, Trasler JM, Robaire B. Modulation by neonatal thymectomy of the reproductive axis in male and female rats during development. Biol Reprod 1988;38:91-9. https://doi.org/10.1095/biolreprod38.1.91
  41. Michael SD. The role of the endocrine thymus in female reproduction. Arthritis Rheum 1979;22:1241-5. https://doi.org/10.1002/art.1780221111
  42. Pierpaoli W, Besedovsky HO. Role of the thymus in programming of neuroendocrine functions. Clin Exp Immunol 1975;20:323-38.
  43. Rebar RW, Miyake A, Low TL, Goldstein AL. Thymosin stimulates secretion of luteinizing hormone-releasing factor. Science 1981;214:669-71. https://doi.org/10.1126/science.7027442
  44. Goya RG, Console G, Herenu C, Brown O, Rimoldi OJ. Thymus and aging: potential of gene therapy for restoration of endocrine thymic function in thymus-deficient animal models. Gerontology 2002;48:325-8. https://doi.org/10.1159/000065258
  45. Hareramadas B, Rai U. Cellular mechanism of estrogen-induced thymic involution in wall lizard: caspase-dependent action. J Exp Zool A Comp Exp Biol 2006;305:396-409. https://doi.org/10.1002/jez.a.260
  46. Rebar RW, Morandini IC, Erickson GF, Petze JE. The hormonal basis of reproductive defects in athymic mice: diminished gonadotropin concentrations in prepubertal females. Endocrinology 1981;108:120-6. https://doi.org/10.1210/endo-108-1-120
  47. Huang TS, Wang YH, Lai JS, Chang CC, Lien IN. The hypothalamus-pituitary-ovary and hypothalamus-pituitary-thyroid axes in spinal cord-injured women. Metabolism 1996;45:718-22. https://doi.org/10.1016/S0026-0495(96)90137-7
  48. Eppig JJ. Oocyte control of ovarian follicular development and function in mammals. Reproduction 2001;122:829-38. https://doi.org/10.1530/rep.0.1220829