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International Journal of Endocrinology
Volume 2009, Article ID 687259, 13 pages
http://dx.doi.org/10.1155/2009/687259
Review Article

Prolactin and Male Fertility: The Long and Short Feedback Regulation

Department of Neuroendocrinology, National Institute for Research in Reproductive Health, Jehangir Merwanji Street, Parel, Mumbai 400 012, India

Received 24 May 2008; Accepted 5 August 2008

Academic Editor: Mario Maggi

Copyright © 2009 M. K. Gill-Sharma. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Singh, C. O'Neill, and D. J. Handelsman, “Induction of spermatogenesis by androgens in gonadotropin-deficient (hpg) mice,” Endocrinology, vol. 136, no. 12, pp. 5311–5321, 1995. View at Publisher · View at Google Scholar
  2. S. Bhasin, T. Fielder, N. Peacock, U. A. Sod-Mariah, and R. S. Swerdloff, “Dissociating antifertility effects of GnRH-antagonist from its adverse effects on mating behavior in male rats,” American Journal of Physiology, Endocrinology and Metabolism, vol. 254, no. 1, pp. E84–E91, 1988. View at Google Scholar
  3. L. P. Mangurian, R. J. Walsh, and B. I. Posner, “Prolactin enhancement of its own uptake at the choroids plexus,” Endocrinology, vol. 131, no. 2, pp. 698–702, 1992. View at Publisher · View at Google Scholar
  4. D. R. Grattan, “The actions of prolactin in the brain during pregnancy and lactation,” Progress in Brain Research, vol. 133, pp. 153–171, 2001. View at Publisher · View at Google Scholar
  5. C. Bole-Feysot, V. Goffin, M. Edery, N. Binart, and P. A. Kelly, “Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice,” Endocrine Reviews, vol. 19, no. 3, pp. 225–268, 1998. View at Publisher · View at Google Scholar
  6. B. D. Albertson, M. L. Sienkiewicz, D. Kimball, A. K. Munabi, F. Cassorla, and D. L. Loriaux, “New evidence for a direct effect of prolactin on rat adrenal steroidogenesis,” Endocrine Research, vol. 13, no. 3, pp. 317–333, 1987. View at Google Scholar
  7. A. Bartke, “Hyperprolactinemia and male reproduction,” in Andrology, Male Fertility and Sterility, J. D. Paulsen, A. Negro-Vilar, E. Lucina, and L. Martini, Eds., pp. 101–123, Academic Press, New York, NY, USA, 1986. View at Google Scholar
  8. D. D. Rasmussen, “The interaction between mediobasohypothalamic dopaminergic and endorphinergic neuronal systems as a key regulator of reproduction: an hypothesis,” Journal of Endocrinological Investigation, vol. 14, no. 4, pp. 323–352, 1991. View at Google Scholar
  9. N. Binart, N. Melaine, C. Pineau et al., “Male reproductive function is not affected in prolactin receptor-deficient mice,” Endocrinology, vol. 144, no. 9, pp. 3779–3782, 2003. View at Publisher · View at Google Scholar
  10. R. W. Steger, V. Chandrashekar, W. Zhao, A. Bartke, and N. D. Horseman, “Neuroendocrine and reproductive functions in male mice with targeted disruption of the prolactin gene,” Endocrinology, vol. 139, no. 9, pp. 3691–3695, 1998. View at Publisher · View at Google Scholar
  11. J. H. Krege, J. B. Hodgin, J. F. Couse et al., “Generation and reproductive phenotypes of mice lacking estrogen receptor ß,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 26, pp. 15677–15682, 1998. View at Publisher · View at Google Scholar
  12. D. N. Petersen, G. T. Tkalcevic, P. H. Koza-Taylor, T. G. Turi, and T. A. Brown, “Identification of estrogen receptor β2, a functional variant of estrogen receptor β expressed in normal rat tissues,” Endocrinology, vol. 139, no. 3, pp. 1082–1092, 1998. View at Publisher · View at Google Scholar
  13. H. Wennbo, J. Kindblom, O. G. P. Isaksson, and J. Törnell, “Transgenic mice overexpressing the prolactin gene develop dramatic enlargement of the prostate gland,” Endocrinology, vol. 138, no. 10, pp. 4410–4415, 1997. View at Publisher · View at Google Scholar
  14. M. A. Kelly, M. Rubinstein, S. L. Asa et al., “Pituitary lactotroph hyperplasia and chronic hyperprolactinemia in dopamine D2 receptor-deficient mice,” Neuron, vol. 19, no. 1, pp. 103–113, 1997. View at Publisher · View at Google Scholar
  15. K. E. Moore and K. T. Demarest, “Tuberoinfundibular and tuberohypophysial dopaminergic neurons,” in Frontiers in Neuroendocrinology, W. F. Ganong and L. Martini, Eds., vol. 7, pp. 161–190, Raven Press, New York, NY, USA, 1982. View at Google Scholar
  16. S. T. Anderson, J. L. Barclay, K. J. Fanning, D. H. L. Kusters, M. J. Waters, and J. D. Curlewis, “Mechanisms underlying the diminished sensitivity to prolactin negative feedback during lactation: reduced STAT5 signaling and up-regulation of cytokine-inducible SH2 domain-containing protein (CIS) expression in tuberoinfundibular dopaminergic neurons,” Endocrinology, vol. 147, no. 3, pp. 1195–1202, 2006. View at Publisher · View at Google Scholar
  17. J. L. Voogt, Y. Lee, S. Yang, and L. Arbogast, “Regulation of prolactin secretion during pregnancy and lactation,” Progress in Brain Research, vol. 133, pp. 173–185, 2001. View at Publisher · View at Google Scholar
  18. V. Raymond, M. Bealieu, J. Boissier, and F. Labrie, “Potent antidopaminergic activity of estradiol at the pituitary level on prolactin release,” Science, vol. 200, no. 4346, pp. 1173–1175, 1978. View at Publisher · View at Google Scholar
  19. M. Blum, B. S. McEwen, and J. L. Roberts, “Transcriptional analysis of tyrosine hydroxylase gene expression in the tuberoinfundibular dopaminergic neurons of the rat arcuate nucleus after estrogen treatment,” Journal of Biological Chemistry, vol. 262, no. 2, pp. 817–821, 1987. View at Google Scholar
  20. T. W. Toney, K. J. Lookingland, and K. E. Moore, “Role of testosterone in the regulation of tuberoinfundibular dopaminergic neurons in the male rat,” Neuroendocrinology, vol. 54, no. 1, pp. 23–29, 1991. View at Publisher · View at Google Scholar
  21. K. Purvis, O. P. F. Clausen, A. Olsen, E. Haug, and V. Hansson, “Prolactin and Leydig cell responsiveness to LH/hCG in the rat,” Archives of Andrology, vol. 3, no. 3, pp. 219–230, 1979. View at Publisher · View at Google Scholar
  22. U. Mathur, A. Bartke, and J. Weisz, “Effects of prolactin and LH on the activity of Δ5-3β hydroxy-steroid dehydrogenase, dihydro orotic dehydrogenase, β-hydroxybutyrate dehydrogenase and glucose 6 phosphate dehydrogenase in the testis of the dwarf mice,” Indian Journal of Physiology and Pharmacology, vol. 19, no. 2, pp. 58–64, 1975. View at Google Scholar
  23. H. S. Juneja, M. Motta, R. Massa, M. Zanisi, and L. Martini, “Feedback control of gonadotropin secretion in the male,” in Sperm Action, P. O. Hubunont, M. L. Hermite, and J. Schwers, Eds., Progress in Reproductive Biology, pp. 162–173, Karger, Basel, Switzerland, 1973. View at Google Scholar
  24. M. K. Gill, S. Karanth, A. Dutt, and H. S. Juneja, “Effect of castration and steroid treatment on the release of gonadotropins by the rat pituitary-hypothalamus complex in vitro,” Hormone and Metabolic Research, vol. 17, no. 3, pp. 141–146, 1985. View at Google Scholar
  25. M. E. Freeman, B. Kanyicska, A. Lerant, and G. Nagy, “Prolactin: structure, function, and regulation of secretion,” Physiological Reviews, vol. 80, no. 4, pp. 1523–1631, 2000. View at Google Scholar
  26. Z. B. Andrews and D. R. Grattan, “The roles of dopamine and the neurointermediate lobe of the pituitary in the regulation of prolactin secretion during late pregnancy in rats,” Journal of Neuroendocrinology, vol. 16, no. 10, pp. 859–865, 2004. View at Publisher · View at Google Scholar
  27. A. Dutt, M. Gill, S. Karanth, N. Lehri, and H. S. Juneja, “The choice of a model for studying the hypothalamus-pituitary interactions in vitro,” Molecular and Cellular Endocrinology, vol. 45, no. 1, pp. 21–26, 1986. View at Publisher · View at Google Scholar
  28. M. Quijada, P. Illner, L. Krulich, and S. M. McCann, “The effect of catecholamines on hormone release from anterior pituitaries and ventral hypothalami incubated in vitro,” Neuroendocrinology, vol. 13, no. 3, pp. 151–163, 1974. View at Publisher · View at Google Scholar
  29. W. H. Rotsztejn, J. L. Charli, E. Pattou, and C. Kordon, “Stimulation by dopamine of luteinizing hormone-releasing hormone (LHRH) release from the mediobasal hypothalamus in male rats,” Endocrinology, vol. 101, no. 5, pp. 1475–1483, 1977. View at Google Scholar
  30. T. Yeo, M. O. Thorner, A. Jones, P. J. Lowry, and G. M. Besser, “The effects of dopamine, bromocriptine, lergotrile and metoclopramide on prolactin release from continuously perfused columns of isolated rat pituitary cells,” Clinical Endocrinology (Oxf), vol. 10, no. 2, pp. 123–130, 1979. View at Publisher · View at Google Scholar
  31. E. Horvath, K. Kovacs, and C. Ezrin, “Junctional contact between lactotrophs and gonadotrophs in the rat pituitary,” IRCS Medical Science: Cell and Membrane Biology, vol. 5, no. 11, p. 511, 1977. View at Google Scholar
  32. I. M. Kramer and C. R. Hopkins, “Studies on the kinetics of dopamine-regulated prolactin secretion,” Molecular and Cellular Endocrinology, vol. 28, no. 2, pp. 191–198, 1982. View at Publisher · View at Google Scholar
  33. A. Dutt and H. S. Juneja, “Effect of reserpine on the inhibition of prolactin released from different pituitary constructs in vitro by dopamine, bromocriptine and apomorphine,” Endocrine Research, vol. 18, no. 4, pp. 307–320, 1992. View at Google Scholar
  34. N. Ben-Jonathan, “Catecholamines and pituitary prolactin release,” Journal of Reproduction and Fertility, vol. 58, no. 2, pp. 501–512, 1980. View at Google Scholar
  35. S. Karanth, A. Dutt, and H. S. Juneja, “Age-related release of prolactin by the pituitary and the pituitary-hypothalamic complex in vitro: an attempt to describe the development of the hypothalamic prolactin-inhibiting and -releasing activities in male rats,” Journal of Endocrinology, vol. 115, no. 3, pp. 405–409, 1987. View at Google Scholar
  36. J. P. Advis, J. W. Simpkins, J. Bennett, and J. Meites, “Serotonergic control of prolactin release in male rats,” Life Sciences, vol. 24, no. 4, pp. 359–365, 1979. View at Publisher · View at Google Scholar
  37. T. L. Garthwaite and T. C. Hagen, “Evidence that serotonin stimulates a prolactin-releasing factor in the rat,” Neuroendocrinology, vol. 29, no. 3, pp. 215–220, 1979. View at Publisher · View at Google Scholar
  38. A. V. Schally, T. W. Redding, A. Arimura, A. Dupont, and G. L. Linthicum, “Isolation of gamma amino butyric acid from pig hypothalami and demonstration of its prolactin release inhibiting (PIF) activity in vivo and in vitro,” Endocrinology, vol. 100, no. 3, pp. 681–691, 1977. View at Google Scholar
  39. D. A. Leong, L. S. Frawley, and J. D. Neill, “Neuroendocrine control of prolactin secretion,” Annual Review of Physiology, vol. 45, pp. 109–127, 1983. View at Publisher · View at Google Scholar
  40. S. Hinuma, Y. Habata, R. Fujii et al., “A prolactin-releasing peptide in the brain,” Nature, vol. 393, no. 6682, pp. 272–276, 1998. View at Publisher · View at Google Scholar
  41. A. Arimura and A. V. Schally, “Prolactin release inhibiting and stimulating factors in the hypothalamus,” in Hypothalamic Peptide Hormones and Pituitary Regulation, J. C. Porter, Ed., pp. 237–252, Raven Press, New York, NY, USA, 1977. View at Google Scholar
  42. J. D. Neill, “Neuroendocrine regulation of prolactin secretion,” in Frontiers in Neuroendocrinology, L. Martini and W. F. Ganong, Eds., vol. 6, pp. 129–155, Raven Press, New York, NY, USA, 1980. View at Google Scholar
  43. P. N. Catalano, M. M. Bonaventura, P. Silveyra, B. Bettler, C. Libertun, and V. A. Lux-Lantos, “GABAB1 knockout mice reveal alterations in prolactin levels, gonadotropic axis, and reproductive function,” Neuroendocrinology, vol. 82, no. 5-6, pp. 294–305, 2005. View at Publisher · View at Google Scholar
  44. A. Negro-Vilar, L. Krulich, and S. M. McCann, “Changes in serum prolactin and gonadotropins during sexual development of the male rat,” Endocrinology, vol. 93, no. 3, pp. 660–664, 1973. View at Google Scholar
  45. D. Becú and C. Libertun, “Comparative maturation of the regulation of prolactin and thyrotropin by serotonin and thyrotropin-releasing hormone in male and female rats,” Endocrinology, vol. 110, no. 6, pp. 1879–1884, 1982. View at Google Scholar
  46. O. Khorram, L. R. Depalatis, and S. M. McCann, “Hypothalamic control of prolactin secretion during the perinatal period in the rat,” Endocrinology, vol. 115, no. 5, pp. 1698–1704, 1984. View at Google Scholar
  47. L. Debeljuk, A. Arimura, and A. V. Schally, “Studies on the pituitary responsiveness to luteinizing hormone-releasing hormone (LHRH) in intact male rats of different ages,” Endocrinology, vol. 90, no. 2, pp. 585–588, 1972. View at Google Scholar
  48. A. De Lean, L. Ferland, J. Drouin, P. A. Kelly, and F. Labrie, “Modulation of pituitary thyrotropin releasing hormone receptor levels by estrogens and thyroid hormones,” Endocrinology, vol. 100, no. 6, pp. 1496–1504, 1977. View at Google Scholar
  49. D. D. Nansel, G. A. Gudelsky, M. J. Reymond, and J. C. Porter, “Estrogen alters the responsiveness of the anterior pituitary gland to the actions of dopamine on lysosomal enzyme activity and prolactin release,” Endocrinology, vol. 108, no. 3, pp. 903–907, 1981. View at Google Scholar
  50. S. J. Nazian, “Pituitary function during the sexual maturation of the male rat: inhibition of prolactin secretion by exogenous dopamine,” Biology of Reproduction, vol. 28, no. 3, pp. 645–651, 1983. View at Publisher · View at Google Scholar
  51. N. Matsushita, Y. Kato, A. Shimatsu, H. Katakami, N. Yanaihara, and H. Imura, “Effects of VIP, TRH, GABA and dopamine on prolactin release from superfused rat anterior pituitary cells,” Life Sciences, vol. 32, no. 11, pp. 1263–1269, 1983. View at Publisher · View at Google Scholar
  52. W. K. Samson, M. M. Taylor, and J. R. Baker, “Prolactin-releasing peptides,” Regulatory Peptides, vol. 114, no. 1, pp. 1–5, 2003. View at Publisher · View at Google Scholar
  53. M. C. Lagerström, R. Fredriksson, T. K. Bjarnadóttir et al., “Origin of the prolactin-releasing hormone (PRLH) receptors: evidence of coevolution between PRLH and a redundant neuropeptide Y receptor during vertebrate evolution,” Genomics, vol. 85, no. 6, pp. 688–703, 2005. View at Publisher · View at Google Scholar
  54. M. K. Gill-Sharma, N. Lehri-Balasinor, and H. S. Juneja, “Effect of prolonged incubation of male rat whole pituitary or pituitary-hypothalamus complex with testosterone on release of gonadotrophin and prolactin in vitro,” Indian Journal of Experimental Biology, vol. 30, no. 11, pp. 1084–1092, 1992. View at Google Scholar
  55. G. Morel, A. Ouhtit, and P. A. Kelly, “Prolactin receptor immunoreactivity in rat anterior pituitary,” Neuroendocrinology, vol. 59, no. 1, pp. 78–84, 1994. View at Publisher · View at Google Scholar
  56. K. A. Krown, Y.-F. Wang, T. W. C. Ho, P. A. Kelly, and A. M. Walker, “Prolactin isoform 2 as an autocrine growth factor for GH3 cells,” Endocrinology, vol. 131, no. 2, pp. 595–602, 1992. View at Publisher · View at Google Scholar
  57. M. E. Cruz-Soto, M. D. Scheiber, K. A. Gregerson, G. P. Boivin, and N. D. Horseman, “Pituitary tumorigenesis in prolactin gene-disrupted mice,” Endocrinology, vol. 143, no. 11, pp. 4429–4436, 2002. View at Publisher · View at Google Scholar
  58. O. V. Smirnova, O. M. Petraschuk, and P. A. Kelly, “Immunocytochemical localization of prolactin receptors in rat liver cells: I. Dependence on sex and sex steroids,” Molecular and Cellular Endocrinology, vol. 105, no. 1, pp. 77–81, 1994. View at Publisher · View at Google Scholar
  59. M. K. Gill-Sharma, S. D'Souza, V. Padwal et al., “Antifertility effects of estradiol in adult male rats,” Journal of Endocrinological Investigation, vol. 24, no. 8, pp. 598–607, 2001. View at Google Scholar
  60. L. Q. Gothard, J. C. Hibbard, and M. A. Seyfred, “Estrogen-mediated induction of rat prolactin gene transcription requires the formation of a chromatin loop between the distal enhancer and proximal promoter regions,” Molecular Endocrinology, vol. 10, no. 2, pp. 185–195, 1996. View at Publisher · View at Google Scholar
  61. M. Aleem, V. Padwal, J. Choudhary, N. Balasinor, and M. K. Gill-Sharma, “Sperm protamine levels as indicators of fertilising potential in sexually mature male rats,” Andrologia, vol. 40, no. 1, pp. 29–37, 2008. View at Google Scholar
  62. M. Aleem, V. Padwal, J. Choudhari, N. Balasinor, P. Parte, and M. K. Gill-Sharma, “Cyproterone acetate affects protamine gene expression in the testis of adult male rat,” Contraception, vol. 71, no. 5, pp. 379–391, 2005. View at Publisher · View at Google Scholar
  63. D. K. Sarkar, P. E. Gottschall, and J. Meites, “Decline of tuberoinfundibular dopaminergic function resulting from chronic hyperprolactinemia in rats,” Endocrinology, vol. 115, no. 4, pp. 1269–1274, 1984. View at Google Scholar
  64. C. Oliver, R. S. Mical, and J. C. Porter, “Hypothalamic pituitary vasculature: evidence for retrograde blood flow in the pituitary stalk,” Endocrinology, vol. 101, no. 2, pp. 598–604, 1977. View at Google Scholar
  65. W. F. Silverman and R. J. Walsh, “Prolactin causes increased turnover of dopamine in 10-day-old rat median eminence,” The Anatomical Record, vol. 217, no. 1, pp. 53–55, 1987. View at Publisher · View at Google Scholar
  66. N. Balasinor, M. K. Gill-Sharma, P. Parte, and H. S. Juneja, “Cerebrospinal fluid and blood concentrations of luteinizing hormone, follicle stimulating hormone and prolactin following castration of adult male rats,” Acta Endocrinologica (Copenh), vol. 127, no. 1, pp. 58–65, 1992. View at Google Scholar
  67. M. Aleem, V. Padwal, J. Choudhari, N. Balasinor, P. Parte, and M. K. Gill-Sharma, “Estradiol affects androgen-binding protein expression and fertilizing ability of spermatozoa in adult male rats,” Molecular and Cellular Endocrinology, vol. 253, no. 1-2, pp. 1–13, 2006. View at Publisher · View at Google Scholar
  68. M. K. Gill-Sharma, M. Aleem, G. Sethi et al., “Antifertility effects of fluphenazine in adult male rats,” Journal of Endocrinological Investigation, vol. 26, no. 4, pp. 316–326, 2003. View at Google Scholar
  69. D. R. Grattan, C. L. Jasoni, X. Liu, G. M. Anderson, and A. E. Herbison, “Prolactin regulation of gonadotropin-releasing hormone neurons to suppress luteinizing hormone secretion in mice,” Endocrinology, vol. 148, no. 9, pp. 4344–4351, 2007. View at Publisher · View at Google Scholar
  70. G. M. Anderson, D. C. Kieser, F. J. Steyn, and D. R. Grattan, “Hypothalamic prolactin receptor messenger ribonucleic acid levels, prolactin signaling, and hyperprolactinemic inhibition of pulsatile luteinizing hormone secretion are dependent on estradiol,” Endocrinology, vol. 149, no. 4, pp. 1562–1570, 2008. View at Publisher · View at Google Scholar
  71. L. Milenkovió, G. D'Angelo, P. A. Kelly, and R. I. Weiner, “Inhibition of gonadotropin hormone-releasing hormone release by prolactin from GT1 neuronal cell lines through prolactin receptors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 4, pp. 1244–1247, 1994. View at Publisher · View at Google Scholar
  72. A. Bartke, M. S. Smith, S. D. Michael, F. G. Peron, and S. Dalterio, “Effects of experimentally induced chronic hyperprolactinemia on testosterone and gonadotropin levels in male rats and mice,” Endocrinology, vol. 100, no. 1, pp. 182–186, 1977. View at Google Scholar
  73. C. Aragona, H. G. Bohnet, and H. G. Friesen, “Localization of prolactin binding in prostate and testis: the role of serum prolactin concentration on the testicular LH receptor,” Acta Endocrinologica (Copenh), vol. 84, no. 2, pp. 402–409, 1977. View at Google Scholar
  74. D. A. Jeyaraj, G. Grossman, and P. Petrusz, “Altered bioavailability of testosterone in androgen-binding protein-transgenic mice,” Steroids, vol. 70, no. 10, pp. 704–714, 2005. View at Publisher · View at Google Scholar
  75. M. Aleem, J. Choudhari, V. Padwal, N. Balasinor, P. Parte, and M. K. Gill-Sharma, “Hyperprolactinemia affects spermiogenesis in adult male rats,” Journal of Endocrinological Investigation, vol. 28, no. 1, pp. 39–48, 2005. View at Google Scholar
  76. H. S. Juneja, S. Karanth, A. Dutt, P. Parte, and P. Meherjee, “Diurnal variations and temporal coupling of bioactive and immunoactive luteinizing hormone, prolactin, testosterone and 17-β-estradiol in adult men,” Hormone Research, vol. 35, no. 3-4, pp. 89–94, 1991. View at Google Scholar
  77. N. Ben-Jonathan, C. R. LaPensee, and E. W. LaPensee, “What can we learn from rodents about prolactin in humans?” Endocrine Reviews, vol. 29, no. 1, pp. 1–41, 2008. View at Publisher · View at Google Scholar