Extracellular signal-regulated kinase mediates gonadotropin subunit gene expression and LH release responses to endogenous gonadotropin-releasing hormones in goldfish

General and Comparative Endocrinology

Volumn 158, Issue 1, 2008, Pages 36-46

  Klausen, Christian ^a   Booth, Morgan ^b   Habibi, Hamid R ^a   Chang, John P ^b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

ERK; GnRH; Goldfish; Gonadotropin gene expression; Pituitary

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; FOLLITROPIN BETA SUBUNIT; GONADORELIN; GONADOTROPIN; LUTEINIZING HORMONE; LUTEINIZING HORMONE BETA SUBUNIT; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CELL CULTURE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FEMALE; GENE EXPRESSION; GOLDFISH; HELA CELL; HORMONE SYNTHESIS; HYPOPHYSIS CELL; IMMUNOREACTIVITY; LIVER; LUTEINIZING HORMONE RELEASE; MALE; MUSCLE TISSUE; NEUROENDOCRINE SYSTEM; NONHUMAN; NORTHERN BLOTTING; OVARY; PRIORITY JOURNAL; TESTIS; WESTERN BLOTTING;

EID: 47749109048     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2008.05.003     Document Type: Article

References (64)

1. Adams B.A., Vickers E.D., Warby C., Park M., Fischer W.H., Craig A.G., Rivier J.E., and Sherwood N.M. Three forms of gonadotropin-releasing hormone, including a novel form, in a basal salmonid, Coregonus clupeaformis. Biol. Reprod. 67 (2002) 232-239
2. Adams B.A., Tello J.A., Erchegyi J., Warby C., Hong D.J., Akinsanya K.O., Mackie G.O., Vale W., Rivier J.E., and Sherwood N.M. Six novel gonadotropin-releasing hormones are encoded as triplets on each of two genes in the protochordate, Ciona intestinalis. Endocrinology 144 (2003) 1907-1919
3. Alessi D.R., Cuenda A., Cohen P., Dudley D.T., and Saltiel A.R. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J. Biol. Chem. 270 (1995) 27489-27494
4. Ando H., Hew C.L., and Urano A. Signal transduction pathways and transcription factors involved in the gonadotropin-releasing hormone-stimulated gonadotropin subunit gene expression. Comp. Biochem. Physiol. B 129 (2001) 525-532
5. Benard O., Naor Z., and Seger R. Role of dynamin, Src, and Ras in the protein kinase C-mediated activation of ERK by gonadotropin-releasing hormone. J. Biol. Chem. 276 (2001) 4554-4563
6. Blumberg P.M. In vitro studies on the mode of action of the phorbol esters, potent tumor promoters, part 2. Crit. Rev. Toxicol. 8 (1981) 199-234
7. Bonfil D., Chunderland D., Kraus S., Shahbazian D., Friedberg I., Seger R., and Naor Z. 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 145 (2004) 2228-2244
8. Call G.B., and Wolfe M.W. Gonadotropin-releasing hormone activates the equine luteinizing hormone β promoter through a protein kinase C/mitogen-activated protein kinase pathway. Biol. Reprod. 61 (1999) 715-723
9. Caunt C.J., Finch A.R., Sedgley K.R., and McArdle C.A. GnRH receptor signalling to ERK: kinetics and compartmentalization. Trends Endocrinol. Metab. 17 (2006) 308-313
10. Caunt C.J., Finch A.R., Sedgley K.R., Oakley L., Luttrell L.M., and McArdle C.A. Arrestin-mediated ERK activation by gonadotropin-releasing hormone receptors: receptor-specific activation mechanisms and compartmentalization. J. Biol. Chem. 281 (2006) 2701-2710
11. Chang J.P., Cook H., Freedman G.L., Wiggs A.J., Somoza G.M., de Leeuw R., and Peter R.E. Use of a pituitary cell dispersion method and primary culture system for the studies of gonadotropin-releasing hormone action in the goldfish, Carassius auratus: I. Initial morphological, static, and cell column perifusion studies. Gen. Comp. Endocrinol. 77 (1990) 256-273
12. Chang J.P., Freedman G.L., and de Leeuw R. Use of a pituitary cell dispersion method and primary culture system for the studies of gonadotropin-releasing hormone action in the goldfish, Carassius auratus: II. Extracellular calcium dependence and dopaminergic inhibition of gonadotropin responses. Gen. Comp. Endocrinol. 77 (1990) 274-282
13. Chang J.P., Wildman B., and Van Goor F. Lack of involvement of arachidonic acid metabolism in chicken GnRH-II stimulation of gonadotropin secretion in dispersed pituitary cells of goldfish, Carassius auratus. Identification of a major difference in salmon GnRH and chicken GnRH-II mechanisms of action. Mol. Cell. Endocrinol. 79 (1991) 75-83
14. Chang J.P., Wong A.O.L., Van Der Kraak G., and Van Goor F. Relationship between cyclic AMP-stimulated and native gonadotropin-releasing hormone-stimulated gonadotropin release in the goldfish. Gen. Comp. Endocrinol. 86 (1992) 359-377
15. Chang J.P., Johnson J.D., Van Goor F., Wong C.J.H., Yunker W.K., Uretsky A.D., Taylor D., Jobin R.M., Wong A.O.L., and Goldberg J.I. Signal transduction mechanisms mediating secretion in goldfish gonadotropes and somatotropes. Biochem. Cell Biol. 78 (2000) 139-153
16. Dobkin-Bekman M., Naidich M., Pawson A.J., Millar R.P., Seger R., and Naor Z. Activation of mitogen-activated protein kinase (MAPK) by GnRH is cell-context dependent. Mol. Cell. Endocrinol. 152 (2006) 184-190
17. Dudley D.T., Pang L., Decker S.J., Bridges A.J., and Saltiel A.R. A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA 92 (1995) 7686-7689
18. Fowkes R.C., King P., and Burrin J.M. Regulation of human glycoprotein hormone α-subunit gene transcription in LβT2 gonadotropes by protein kinase C and extracellular signal-regulated kinase 1/2. Biol. Reprod. 67 (2002) 725-734
19. Gharib S.D., Wierman M.E., Shupnik M.A., and Chin W.W. Molecular biology of the pituitary gonadotropins. Endocr. Rev. 11 (1990) 177-199
20. Guilgur L.G., Moncaut N.P., Canário A.V.M., and Somoza G.M. Evolution of GnRH ligands and receptors in gnathostomata. Comp. Biochem. Physiol. A 144 (2007) 272-283
21. Gur G., Bonfil D., Safarian H., Naor Z., and Yaron Z. GnRH receptor signaling in tilapia pituitary cells: role of mitogen-activated protein kinase (MAPK). Comp. Biochem. Physiol. B 129 (2001) 517-524
22. Gur G., Bonfil D., Safarian H., Naor Z., and Yaron Z. GnRH signaling pathways regulate differentially the tilapia gonadotropin subunit genes. Mol. Cell. Endocrinol. 189 (2002) 125-134
23. Haisenleder D.J., Cox M.E., Parsons S.J., and Marshall J.C. Gonadotropin-releasing hormone pulses are required to maintain activation of mitogen-activated protein kinase: role in stimulation of gonadotrope gene expression. Endocrinology 138 (1998) 3104-3111
24. Han X.B., and Conn P.M. The role of protein kinases A and C pathways in the regulation of mitogen-activated protein kinase activation in response to gonadotropin-releasing hormone receptor activation. Endocrinology 140 (1999) 2241-2251
25. Harris D., Bonfil D., Chunderland D., Kraus S., Seger R., and Naor Z. 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 143 (2002) 1018-1025
26. Harris D., Chunderland D., Bonfil D., Kraus S., Seger R., and Naor Z. 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 144 (2003) 612-622
27. Huggard D., Khakoo Z., Kassam G., Mahmoud S.S., and Habibi H.R. Effect of testosterone on maturational gonadotropin subunit mRNA levels in the goldfish pituitary. Biol. Reprod. 54 (1996) 1184-1191
28. Huggard-Nelson D.L., Nathwani P.S., Kermouni A., and Habibi H.R. Molecular characterization of LH-β and FSH-β subunits and their regulation by estrogen in the goldfish pituitary. Mol. Cell. Endocrinol. 188 (2002) 171-193
29. Illing N., Troskie B.E., Nahorniak C.S., Hapgood J.P., Peter R.E., and Millar R.P. Two gonadotropin-releasing hormone receptor subtypes with distinct ligand selectivity and differential distribution in brain and pituitary in the goldfish (Carassius auratus). Proc. Natl. Acad. Sci. USA 96 (1999) 2526-2531
30. Iwakoshi E., Takuwa-Kuroda K., Fujisawa Y., Hisada M., Ukena K., Tsutsui K., and Minakata H. Isolation and characterization of a GnRH-like peptide from Octopus vulgaris. Biochem. Biophys. Res. Commun. 291 (2002) 1187-1193
31. Johnson J.D., Van Goor F., Jobin R.M., Wong C.J.H., Goldberg J.I., and Chang J.P. Agonist-specific Ca2+ signaling systems, composed of multiple intracellular Ca2+ stores, regulate gonadotropin secretion. Mol. Cell. Endocrinol. 170 (2000) 15-29
32. Johnson J.D., and Chang J.P. Agonist-specific and sexual stage-dependent inhibition of gonadotropin-releasing hormone-stimulated gonadotropin and growth hormone release by ryanodine: relationship to sexual stage-dependent caffeine-sensitive hormone release. J. Neuroendocrinol. 14 (2002) 144-155
33. Johnson J.D., Klausen C., Habibi H.R., and Chang J.P. A gonadotropin-releasing hormone insensitive, thapsigargin-sensitive Ca2+ store reduces basal gonadotropin exocytosis and gene expression: comparison with agonist-sensitive Ca2+ stores. J. Neuroendocrinol. 15 (2003) 204-214
34. Kah O., Lethimonier C., Somoza G., Guilgur L.G., Vaillant C., and Lareyre J.J. GnRH and GnRH receptors in metazoa: a historical, comparative, and evolution perspective. Gen. Comp. Endocrinol. 153 (2007) 346-364
35. Kanasaki H., Bedecarrats G.Y., Kam K.Y., Xu S., and Kaiser U.B. Gonadotropin-releasing hormone pulse frequency-dependent activation of extracellular signal-regulated kinase pathways in perifused LβT2 cells. Endocrinology 146 (2005) 5503-5513
36. 2 receptor agonist in clonal mouse gonadotroph αT3-1 cells. Biol. Reprod. 67 (2002) 1218-1224
37. Kim M.H., Oka Y., Amano M., Kobayashi M., Okuzawa K., Hasegawa Y., Kawashima S., Suzuki Y., and Aida K. Immunocytochemical localization of sGnRH and cGnRH-II in the brain of goldfish, Carassius auratus. J. Comp. Neurol. 356 (1995) 72-82
38. Klausen C., Chang J.P., and Habibi H.R. Time- and dose-related effects of gonadotropin-releasing hormone on growth hormone and gonadotropin subunit gene expression in the goldfish pituitary. Can. J. Physiol. Pharmacol. 80 (2002) 915-924
39. Klausen C., Chang J.P., and Habibi H.R. Multiplicity of gonadotropin-releasing hormone signaling: a comparative perspective. In: Parhar I.S. (Ed). Progress in Brain Research, Gonadotropin-Releasing Hormone: Molecules and Receptors vol. 141 (2002), Elsevier Science B.V., Amsterdam, The Netherlands 111-128
40. Klausen C., Severson D.L., Chang J.P., and Habibi H.R. Role of protein kinase C in the regulation of gonadotropin subunit mRNA levels: interaction with two native forms of gonadotropin-releasing hormone. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289 (2005) R1634-R1643
41. Lewis T.S., Shapiro P.S., and Ahn N.G. Signal transduction through MAP kinase cascades. In: Vande Woude G.F., and Klein G. (Eds). Advances in Cancer Research vol. 74 (1998), Academic Press, San Diego, USA 49-139
42. Liu F., Austin D.A., Mellon P.L., Olefsky J.M., and Webster N.J.G. GnRH activates ERK1/2 leading to the induction of c-fos and LHβ protein expression in LβT2 cells. Mol. Endocrinol. 16 (2002) 419-434
43. Liu F., Ruiz M.S., Austin D.A., and Webster N.J. Constitutively active Gq impairs gonadotropin-releasing hormone-induced intracellular signaling and luteinizing hormone secretion in LbetaT2 cells. Mol. Endocrinol. 19 (2005) 2074-2085
44. Maudsley S., Naor Z., Bonfil D., Davidson L., Karali D., Pawson A.J., Larder R., Pope C., Nelson N., Millar R.P., and Brown P. Proline-rich tyrosine kinase 2 mediates gonadotropin-releasing hormone signaling to a specific extracellular regulated kinase-sensitive transcript locus in the luteinizing hormone beta-subunit gene. Mol. Endocrinol. 21 (2007) 1216-1233
45. Millar R.P., Lu Z.L., Pawson A.J., Flanagan C.A., Morgan K., and Maudsley S.R. Gonadotropin-releasing hormone receptors. Endocr. Rev. 25 (2004) 235-275
46. Naor Z., Benard O., and Seger R. Activation of MAPK cascades by G-protein-coupled receptors: the case of gonadotropin-releasing hormone receptor. Trends Endocrinol. Metab. 11 (2000) 91-99
47. Navratil A.M., Knoll J.G., Whitesell J.D., Tobet S.A., and Clay C.M. Neuroendocrine plasticity in the anterior pituitary: gonadotropin-releasing hormone-mediated movement in vitro and in vivo. Endocrinology 148 (2007) 1736-1744
48. Nguyen K.A., Santos S.J., Kreidel M.K., Diaz A.L., Rev R., and Lawson M.A. Acute regulation of translation initiation by gonadotropin-releasing hormone in the gonadotrope cell line LbetaT2. Mol. Endocrinol. 18 (2004) 1301-1312
49. Pearson G., Robinson F., Gibson T.B., Xu B.E., Karandikar M., Berman K., and Cobb M.H. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22 (2001) 153-183
50. Peter R.E., Nahorniak C.S., Chang J.P., and Crim L.W. Gonadotropin release from the pars distalis of goldfish, Carassius auratus, transplanted beside the brain or into brain ventricle: additional evidence for gonadotropin-release-inhibitory factor. Gen. Comp. Endocrinol. 55 (1984) 337-346
51. Reiss N., Llevi L.N., Shacham S., Harris D., Seger R., and Naor Z. Mechanism of mitogen-activated protein kinase activation by gonadotropin-releasing hormone in the pituitary αT3-1 cell line: differential roles of calcium and protein kinase C. Endocrinology 138 (1997) 1673-1682
52. Roberson M.S., Misra-Press A., Laurance M.E., Stork P.J.S., and Maurer R.A. A role for mitogen-activated protein kinase in mediating activation of the glycoprotein hormone α-subunit promoter by gonadotropin-releasing hormone. Mol. Cell. Biol. 15 (1995) 3531-3539
53. Roberson M.S., Bliss S.P., Xie J., Navratil A.M., Farmerie T.A., Wolfe M.W., and Clay C.M. Gonadotropin-releasing hormone induction of extracellular-signal regulated kinase is blocked by inhibition of calmodulin. Mol. Endocrinol. 19 (2005) 2412-2423
54. Sundaresan S., Colin I.M., Pestell R.G., and Jameson J.L. Stimulation of mitogen-activated protein kinase by gonadotropin-releasing hormone: evidence for the involvement of protein kinase C. Endocrinology 137 (1996) 304-311
55. Toullec D., Pianetti P., Coste H., Bellevergue P., Grand-Perret T., Ajakane M., Baudet V., Boissin P., Boursier E., Loriolle F., Duhamel L., Charon D., and Kirilovsky J. The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J. Biol. Chem. 266 (1991) 15771-15781
56. Vasilyev V.V., Lawson M.A., Dipaolo D., Webster N.J.G., and Mellon P.L. Different signaling pathways control acute induction versus long-term repression of LHβ transcription by GnRH. Endocrinology 143 (2002) 3414-3426
57. Weck J., Fallest P.C., Pitt L.K., and Shupnik M.A. Differential gonadotropin-releasing hormone stimulation of rat luteinizing hormone subunit gene transcription by calcium influx and mitogen-activated protein kinase-signaling pathways. Mol. Endocrinol. 12 (1998) 451-457
58. Wong A.O.L., Chang J.P., and Peter R.E. Dopamine stimulates growth hormone release from the pituitary of goldfish, Carassius auratus, through the dopamine D1 receptors. Endocrinology 130 (1992) 1201-1210
59. Yamada Y., Yamamoto H., Yonehara T., Kanasaki H., Nakanishi H., Miyamoto E., and Miyazaki K. 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. Biol. Reprod. 70 (2004) 236-243
60. Yang D., Caraty A., and Dupont J. Molecular mechanisms involved in LH release by the ovine pituitary cells. Domest. Anim. Endocrinol. 29 (2005) 488-507
61. Yaron Z., Gur G., Melamed P., Rosenfeld H., Elizur A., and Levavi-Sivan B. Regulation of fish gonadotropins. Int. Rev. Cytol. 225 (2003) 131-185
62. 2-terminal protein kinase. J. Biol. Chem. 275 (2000) 21639-21647
63. Yu K.L., He M.L., Chik C.C., Lin X.W., Chang J.P., and Peter R.E. mRNA expression of gonadotropin-releasing hormones (GnRHs) and GnRH receptor in goldfish. Gen. Comp. Endocrinol. 112 (1998) 303-311
64. Yu K.L., Sherwood N.M., and Peter R.E. Differential distribution of two molecular forms of gonadotropin-releasing hormone in discrete brain areas of goldfish (Carassius auratus). Peptides 9 (1988) 625-630