Table of Contents
Journal of Signal Transduction
Volume 2012, Article ID 198527, 7 pages
http://dx.doi.org/10.1155/2012/198527
Review Article

Extracellular Signal-Regulated Kinase (ERK) Activation and Mitogen-Activated Protein Kinase Phosphatase 1 Induction by Pulsatile Gonadotropin-Releasing Hormone in Pituitary Gonadotrophs

Department of Obstetrics and Gynecology, Faculty of Medicine, Shimane University, Izumo 693-8501, Japan

Received 14 August 2011; Accepted 25 September 2011

Academic Editor: J. Adolfo García-Sáinz

Copyright © 2012 Haruhiko Kanasaki et al. 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. L. C. Layman, “Genetics of human hypogonadotropic hypogonadism,” American Journal of Medical Genetics, vol. 89, no. 4, pp. 240–248, 1999. View at Publisher · View at Google Scholar · View at Scopus
  2. J. G. Pierce and T. F. Parsons, “Glycoprotein hormones: structure and function,” Annual Review of Biochemistry, vol. 50, pp. 465–495, 1981. View at Google Scholar · View at Scopus
  3. S. D. Gharib, M. E. Wierman, M. A. Shupnik, and W. W. Chin, “Molecular biology of the pituitary gonadotropins,” Endocrine Reviews, vol. 11, no. 1, pp. 177–199, 1990. View at Google Scholar · View at Scopus
  4. W. F. Crowley Jr., M. Filicori, D. I. Spratt, and N. F. Santoro, “The physiology of gonadotropin-releasing hormone (GnRH) secretion in men and women,” Recent Progress in Hormone Research, vol. 41, pp. 473–531, 1985. View at Google Scholar · View at Scopus
  5. J. E. Levine and V. D. Ramirez, “Luteinizing hormone-releasing hormone release during the rat estrous cycle and after ovariectomy, as estimated with push-pull cannulae,” Endocrinology, vol. 111, no. 5, pp. 1439–1448, 1982. View at Google Scholar · View at Scopus
  6. E. Knobil, “The neuroendocrine control of the menstrual cycle,” Recent Progress in Hormone Research, vol. 36, pp. 53–88, 1980. View at Google Scholar · View at Scopus
  7. L. Wildt, A. Hausler, G. Marshall et al., “Frequency and amplitude of gonadotropin-releasing hormone stimulation and gonadotropin secretion in the rhesus monkey,” Endocrinology, vol. 109, no. 2, pp. 376–385, 1981. View at Google Scholar
  8. A. C. Dalkin, D. J. Haisenleder, G. A. Ortolano, T. R. Ellis, and J. C. Marshall, “The frequency of gonadotropin-releasing hormone stimulation differentially regulates gonadotropin subunit messenger ribonucleic acid expression,” Endocrinology, vol. 125, no. 2, pp. 917–924, 1989. View at Google Scholar · View at Scopus
  9. D. J. Haisenleder, A. C. Dalkin, G. A. Ortolano, J. C. Marshall, and M. A. Shupnik, “A pulsatile gonadotropin-releasing hormone stimulus is required to increase transcription of the gonadotropin subunit genes: evidence for differential regulation of transcription by pulse frequency in vivo,” Endocrinology, vol. 128, no. 1, pp. 509–517, 1991. View at Google Scholar · View at Scopus
  10. U. B. Kaiser, A. Jakubowiak, A. Steinberger, and W. W. Chin, “Differential effects of gonadotropin-releasing hormone (GnRH) pulse frequency on gonadotropin subunit and GnRH receptor messenger ribonucleic acid levels in vitro,” Endocrinology, vol. 138, no. 3, pp. 1224–1231, 1997. View at Publisher · View at Google Scholar · View at Scopus
  11. D. J. Haisenleder, S. Khoury, S. M. Zmeili et al., “The frequency of gonadotropin-releasing hormone secretion regulates expression of α and luteinizing hormone β-subunit messenger ribonucleic acids in male rats,” Molecular Endocrinology, vol. 1, no. 11, pp. 834–838, 1987. View at Google Scholar
  12. P. M. Conn, W. R. Huckle, W. V. Andrews, and C. A. McArdle, “The molecular mechanism of action of gonadotropin releasing hormone (GnRH) in the pituitary,” Recent Progress in Hormone Research, vol. 43, pp. 29–68, 1987. View at Google Scholar · View at Scopus
  13. S. Sundaresan, I. M. Colin, R. G. Pestell, and J. L. Jameson, “Stimulation of mitogen-activated protein kinase by gonadotropin-releasing hormone: evidence for the involvement of protein kinase C,” Endocrinology, vol. 137, no. 1, pp. 304–311, 1996. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Kraus, Z. Naor, and R. Seger, “Intracellular signaling pathways mediated by the gonadotropin-releasing hormone (GnRH) receptor,” Archives of Medical Research, vol. 32, no. 6, pp. 499–509, 2001. View at Publisher · View at Google Scholar · View at Scopus
  15. D. Bonfil, D. Chuderland, S. Kraus et al., “Extracellular signal-regulated kinase, Jun N-terminal kinase, p38, and c-Src are involved in gonadotropin-releasing hormone-stimulated activity of the glycoprotein hormone follicle-stimulating hormone β-subunit promoter,” Endocrinology, vol. 145, no. 5, pp. 2228–2244, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  16. G. B. Call and M. W. Wolfe, “Gonadotropin-releasing hormone activates the equine luteinizing hormone β promoter through a protein kinase C/mitogen-activated protein kinase pathway,” Biology of Reproduction, vol. 61, no. 3, pp. 715–723, 1999. View at Publisher · View at Google Scholar · View at Scopus
  17. L. M. Halvorson, U. B. Kaiser, and W. W. Chin, “The protein kinase C system acts through the early growth response protein 1 to increase LHβ gene expression in synergy with steroidogenic factor-1,” Molecular Endocrinology, vol. 13, no. 1, pp. 106–116, 1999. View at Publisher · View at Google Scholar · View at Scopus
  18. C. Klausen, M. Booth, H. R. Habibi, and J. P. Chang, “Extracellular signal-regulated kinase mediates gonadotropin subunit gene expression and LH release responses to endogenous gonadotropin-releasing hormones in goldfish,” General and Comparative Endocrinology, vol. 158, no. 1, pp. 36–46, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. J. Weck, P. C. Fallest, L. K. Pitt, and M. A. Shupnik, “Differential gonadotropin-releasing hormone stimulation of rat luteinizing hormone subunit gene transcription by calcium influx and mitogen-activated protein kinase-signaling pathways,” Molecular Endocrinology, vol. 12, no. 3, pp. 451–457, 1998. View at Google Scholar · View at Scopus
  20. R. J. Davis, “Signal transduction by the JNK group of MAP kinases,” Cell, vol. 103, no. 2, pp. 239–252, 2000. View at Google Scholar · View at Scopus
  21. J. Raingeaud, A. J. Whitmarsh, T. Barrett, B. Dérijard, and R. J. Davis, “MKK3- and MKK6-regulated gene expression is mediated by the p38 mitogen-activated protein kinase signal transduction pathway,” Molecular and Cellular Biology, vol. 16, no. 3, pp. 1247–1255, 1996. View at Google Scholar · View at Scopus
  22. D. J. Haisenleder, L. L. Burger, K. W. Aylor, A. C. Dalkin, and J. C. Marshall, “Gonadotropin-releasing hormone stimulation of gonadotropin subunit transcription: evidence for the involvement of calcium/calmodulin-dependent kinase II (Ca/CAMK II) activation in rat pituitaries,” Endocrinology, vol. 144, no. 7, pp. 2768–2774, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. D. J. Haisenleder, H. A. Ferris, and M. A. Shupnik, “The calcium component of gonadotropin-releasing hormone-stimulated luteinizing hormone subunit gene transcription is mediated by calcium/calmodulin-dependent protein kinase type II,” Endocrinology, vol. 144, no. 6, pp. 2409–2416, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. M. S. Roberson, S. P. Bliss, J. Xie et al., “Gonadotropin-releasing hormone induction of extracellular signal-regulated kinase is blocked by inhibition of calmodulin,” Molecular Endocrinology, vol. 19, no. 9, pp. 2412–2423, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. F. Liu, I. Usui, L. G. Evans et al., “Involvement of both Gq/11 and Gs proteins in gonadotropin-releasing hormone receptor-mediated signaling in LβT2 cells,” Journal of Biological Chemistry, vol. 277, no. 35, pp. 32099–32108, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  26. I. N. Purwana, H. Kanasaki, T. Mijiddorj, A. Oride, and K. Miyazaki, “Induction of dual-specificity phosphatase 1 (DUSP1) by pulsatile gonadotropin-releasing hormone stimulation: role for gonadotropin subunit expression in mouse pituitary LbetaT2 Cells1,” Biology of Reproduction, vol. 84, no. 5, pp. 996–1004, 2011. View at Publisher · View at Google Scholar · View at PubMed
  27. S. L. Asa, K. Kovacs, E. Horvath et al., “Human fetal adenohypophysis. Electron microscopic and ultrastructural immunocytochemical analysis,” Neuroendocrinology, vol. 48, no. 4, pp. 423–431, 1988. View at Google Scholar
  28. J. J. Windle, R. I. Weiner, and P. L. Mellon, “Cell lines of the pituitary gonadotrope lineage derived by targeted oncogenesis in transgenic mice,” Molecular Endocrinology, vol. 4, no. 4, pp. 597–603, 1990. View at Google Scholar
  29. H. Kanasaki, G. Y. Bedecarrats, K. Y. Kam, S. Xu, and U. B. Kaiser, “Gonadotropin-releasing hormone pulse frequency-dependent activation of extracellular signal-regulated kinase pathways in perifused LβT2 Cells,” Endocrinology, vol. 146, no. 12, pp. 5503–5513, 2005. View at Publisher · View at Google Scholar · View at PubMed
  30. I. N. Purwana, H. Kanasaki, A. Oride, and K. Miyazaki, “Induction of dual specificity phosphatase 1 (DUSP1) by gonadotropin-releasing hormone (GnRH) and the role for gonadotropin subunit gene expression in mouse pituitary gonadotroph L beta T2 cells,” Biology of Reproduction, vol. 82, no. 2, pp. 352–362, 2010. View at Publisher · View at Google Scholar · View at PubMed
  31. S. M. Keyse, “Protein phosphatases and the regulation of MAP kinase activity,” Seminars in Cell and Developmental Biology, vol. 9, no. 2, pp. 143–152, 1998. View at Google Scholar
  32. J. M. Brondello, A. Brunet, J. Pouysségur, and F. R. McKenzie, “The dual specificity mitogen-activated protein kinase phosphatase-1 and -2 are induced by the p42/p44(MAPK) cascade,” Journal of Biological Chemistry, vol. 272, no. 2, pp. 1368–1376, 1997. View at Publisher · View at Google Scholar
  33. K. Kondoh and E. Nishida, “Regulation of MAP kinases by MAP kinase phosphatases,” Biochimica et Biophysica Acta—Molecular Cell Research, vol. 1773, no. 8, pp. 1227–1237, 2007. View at Publisher · View at Google Scholar · View at PubMed
  34. C. C. Franklin and A. S. Kraft, “Conditional expression of the mitogen-activated protein kinase (MAPK) phosphatase MKP-1 preferentially inhibits p38 MAPK and stress-activated protein kinase in U937 cells,” Journal of Biological Chemistry, vol. 272, no. 27, pp. 16917–16923, 1997. View at Publisher · View at Google Scholar
  35. T. Zhang, J. M. Mulvaney, and M. S. Roberson, “Activation of mitogen-activated protein kinase phosphatase 2 by gonadotropin-releasing hormone,” Molecular and Cellular Endocrinology, vol. 172, no. 1-2, pp. 79–89, 2001. View at Publisher · View at Google Scholar
  36. T. Zhang and M. S. Roberson, “Role of MAP kinase phosphatases in GnRH-dependent activation of MAP kinases,” Journal of Molecular Endocrinology, vol. 36, no. 1, pp. 41–50, 2006. View at Publisher · View at Google Scholar · View at PubMed
  37. K. A. Nguyen, R. E. Intriago, H. C. Upadhyay, S. J. Santos, N. J. G. Webster, and M. A. Lawson, “Modulation of gonadotropin-releasing hormone-induced extracellular signal-regulated kinase activation by dual-specificity protein phosphatase 1 in LβT2 gonadotropes,” Endocrinology, vol. 151, no. 10, pp. 4882–4893, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. S. P. Armstrong, C. J. Caunt, R. C. Fowkes, K. Tsaneva-Atanasova, and C. A. McArdle, “Pulsatile and sustained gonadotropin-releasing hormone (GnRH) receptor signaling: does the ERK signaling pathway decode GnRH pulse frequency?” Journal of Biological Chemistry, vol. 285, no. 32, pp. 24360–24371, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. M. S. Roberson, A. Misra-Press, M. E. Laurance, P. J. S. Stork, and R. A. Maurer, “A role for mitogen-activated protein kinase in mediating activation of the glycoprotein hormone α-subunit promoter by gonadotropin-releasing hormone,” Molecular and Cellular Biology, vol. 15, no. 7, pp. 3531–3539, 1995. View at Google Scholar · View at Scopus
  40. D. Harris, D. Chuderland, D. Bonfil, S. Kraus, R. Seger, and Z. Naor, “Extracellular signal-regulated kinase and c-Src, but not Jun N-terminal kinase, are involved in basal and gonadotropin-releasing hormone-stimulated activity of the glycoprotein hormone α-subunit promoter,” Endocrinology, vol. 144, no. 2, pp. 612–622, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. F. Liu, D. A. Austin, P. L. Mellon, J. M. Olefsky, and N. J. G. Webster, “GnRH activates ERK1/2 leading to the induction of c-fos and LHβ protein expression in LβT2 cells,” Molecular Endocrinology, vol. 16, no. 3, pp. 419–434, 2002. View at Publisher · View at Google Scholar
  42. D. Harris, D. Bonfil, D. Chuderland, S. Kraus, R. Seger, and Z. Naor, “Activation of MAPK cascades by GnRH: ERK and Jun N-terminal kinase are involved in basal and Gnrh-stimulated activity of the glycoprotein hormone LHβ-subunit promoter,” Endocrinology, vol. 143, no. 3, pp. 1018–1025, 2002. View at Publisher · View at Google Scholar · View at Scopus
  43. V. V. Vasilyev, F. Pernasetti, S. B. Rosenberg et al., “Transcriptional activation of the ovine follicle-stimulating hormone-β gene by gonadotropin-releasing hormone involves multiple signal transduction pathways,” Endocrinology, vol. 143, no. 5, pp. 1651–1659, 2002. View at Publisher · View at Google Scholar · View at Scopus
  44. Y. Yamada, H. Yamamoto, T. Yonehara et al., “Differential activation of the luteinizing hormone β-subunit promoter by activin and gonadotropin-releasing hormone: a role for the mitogen-activated protein kinase signaling pathway in LβT2 gonadotrophs,” Biology of Reproduction, vol. 70, no. 1, pp. 236–243, 2004. View at Publisher · View at Google Scholar · View at PubMed
  45. D. J. Haisenleder, M. E. Cox, S. J. Parsons, and J. C. Marshall, “Gonadotropin-releasing hormone pulses are required to maintain activation of mitogen-activated protein kinase: role in stimulation of gonadotrope gene expression,” Endocrinology, vol. 139, no. 7, pp. 3104–3111, 1998. View at Publisher · View at Google Scholar · View at Scopus
  46. R. Mitchell, P. J. Sim, M. S. Johnson, and F. J. Thomson, “Activation of MAP kinase associated with the priming effect of LHRH,” Journal of Endocrinology, vol. 140, no. 2, pp. R15–R18, 1994. View at Google Scholar · View at Scopus
  47. H. A. Ferris and M. A. Shupnik, “Mechanisms for pulsatile regulation of the gonadotropin subunit genes by GNRH1,” Biology of Reproduction, vol. 74, no. 6, pp. 993–998, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  48. J. Weiss, M. J. Guendner, L. M. Halvorson, and J. L. Jameson, “Transcriptional activation of the follicle-stimulating hormone β-subunit gene by activin,” Endocrinology, vol. 136, no. 5, pp. 1885–1891, 1995. View at Google Scholar · View at Scopus
  49. M. Shimonaka, S. Inouye, S. Shimasaki, and N. Ling, “Follistatin binds to both activin and inhibin through the common beta-subunit,” Endocrinology, vol. 128, no. 6, pp. 3313–3315, 1991. View at Google Scholar · View at Scopus
  50. L. L. Burger, A. C. Dalkin, K. W. Aylor, D. J. Haisenleder, and J. C. Marshall, “GnRH pulse frequency modulation of gonadotropin subunit gene transcription in normal gonadotropes—Assessment by primary transcript assay provides evidence for roles of GnRH and follistatin,” Endocrinology, vol. 143, no. 9, pp. 3243–3249, 2002. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Mutiara, H. Kanasaki, A. Oride et al., “Follistatin gene expression by gonadotropin-releasing hormone: a role for cyclic AMP and mitogen-activated protein kinase signaling pathways in clonal gonadotroph LβT2 cells,” Molecular and Cellular Endocrinology, vol. 307, no. 1-2, pp. 125–132, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. H. Kanasaki, I. N. Purwana, T. Mijiddorj, A. Oride, and K. Miyazaki, “Possible involvement of PACAP and PACAP type 1 receptor in GnRH-induced FSH β-subunit gene expression,” Regulatory Peptides, vol. 167, no. 2-3, pp. 227–232, 2011. View at Publisher · View at Google Scholar · View at PubMed
  53. I. N. Purwana, H. Kanasaki, A. Oride et al., “GnRH-induced PACAP and PAC1 receptor expression in pituitary gonadotrophs: a possible role in the regulation of gonadotropin subunit gene expression,” Peptides, vol. 31, no. 9, pp. 1748–1755, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus