Regulation of intracellular signaling cascades by GNRH pulse frequency in the rat pituitary: Roles for CaMK II, ERK, and JNK activation

Biology of Reproduction

Volumn 79, Issue 5, 2008, Pages 947-953

  Burger, Laura L ^a,b   Haisenleder, Daniel J ^a   Aylor, Kevin W ^a   Marshall, John C ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

Author keywords

CaMKII; ERK; Follicle stimulating hormone; Follistatin; GNRH; Gonadotropin releasing hormone; Gonadotropins; JNK; Luteinizing hormone; Signal transduction

Indexed keywords

CALCIUM CALMODULIN DEPENDENT KINASE II; FOLLITROPIN; GONADORELIN; LUTEINIZING HORMONE; MEMBRANE ENZYME; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 9; SIGNAL PEPTIDE; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME REGULATION; GENETIC TRANSCRIPTION; HYPOPHYSIS; IN VIVO STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; PULSE RATE; RAT; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

RATTUS;

EID: 55549118270     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.108.070987     Document Type: Article

References (40)

1. Gharib SD, Wierman ME, Shupnik MA, Chin WW. Molecular biology of the pituitary gonadotropins. Endocrine Rev 1990; 11:177-199.
2. Burger LL, Haisenleder DJ, Dalkin AC, Marshall JC. Regulation of gonadotropin subunit gene transcription. J Mol Endocrinol 2004; 33:559-584.
3. Millar RP, Lu ZL, Pawson AJ, Flanagan CA, Morgan K, Maudsley SR. Gonadotropin-releasing hormone receptors. Endocrine Rev 2004; 25:235-275.
4. Kaiser UB, Conn PM, Chin WW. Studies of GnRH action using GnRH receptor-expressing pituitary cell lines. Endocrine Rev 1997; 18:46-70.
5. Grosse R, Schmid A, Schoneberg T, Herrlich A, Muhn P, Schultz G, Gudermann T. Gonadotropin-releasing hormone receptor initiates multiple signaling pathways by exclusively coupling to G(q/11) proteins. J Biol Chem 2000; 275:9193-2000.
6. Liu F, Usui I, Evans LG, Austin DA, Mellon PL, Olefsky JM, Webster NJ. Involvement of both Gq/11 and Gs proteins in gonadotropin-releasing hormone receptor-mediated signaling in LβT2 cells. J Biol Chem 2002; 277:32099-32108.
7. Stojilkovic SS, Catt KJ. Novel aspects of GnRH-induced intracellular signaling and secretion in pituitary gonadotrophs. J Neuroendocrinol 1995; 7:739-757.
8. Ando H, Hew CL, Urano A. Signal transduction pathways and transcription factors involved in the gonadotropin-releasing hormone-stimulated gonadotropin subunit gene expression. Comp Biochem Physiol B Biochem Mol Biol 2001; 129:525-532.
9. Naor Z. Signal transduction mechanisms of Ca2+ mobilizing hormones: the case of gonadotropin-releasing hormone. Endocrine Rev 1990; 11:326-353.
10. Haisenleder DJ, Yasin M, Marshall JC. The regulation of prolactin, thyrotropin and gonadotropin subunit gene expression by pulsatile or continuous calcium signals. Endocrinology 1993; 133:2055-2061.
11. Weck J, Fallest PC, Pitt LK, Shupnik MA. Differential gonadotropin-releasing hormone stimulation of rat luteinizing hormone subunit gene transcription by calcium influx and mitogen-activated protein kinase-signaling pathways. Mol Endocrinol 1998; 12:451-457.
12. Haisenleder DJ, Yasin M, Marshall JC. Gonadotropin subunit and gonadotropin-releasing hormone receptor gene expression are regulated by alterations in the frequency of calcium pulsatile signals. Endocrinology 1997; 138:5227-5230.
13. Haisenleder DJ, Workman LJ, Burger LL, Aylor KW, Dalkin AC, Marshall JC. Gonadotropin subunit transcriptional responses to calcium signals in the rat: evidence for regulation by pulse frequency. Biol Reprod 2001; 65:1789-1793.
14. Hudmon A, Schulman H. Structure-function of the multifunctional Ca2+/calmodulin-dependent protein kinase II. Biochem J 2002; 364(pt 3):593-611.
15. De Koninck P, Schulman H. Sensitivity of CaM kinase II to the frequency of calcium oscillations. Science 1998; 279:227-230.
16. Haisenleder DJ, Burger LL, Aylor KW, Dalkin AC, Marshall JC. GnRH stimulation of gonadotropin subunit transcription: evidence for the involvement of calcium/calmodulin-dependent kinase II activation in rat pituitaries. Endocrinology 2003; 144:2768-2774.
17. Haisenleder DJ, Ferris HA, Shupnik MA. The calcium component of GnRH-stimulated LH subunit gene transcription is mediated by calcium/calmodulin-dependent protein kinase type II. Endocrinology 2003; 144:2409-2416.
18. Dobkin-Bekman M, Naidich M, Pawson AJ, Millar RP, Seger R, Naor Z. Activation of mitogen-activated protein kinase (MAPK) by GnRH is cell-context dependent. Mol Cell Endocrinol 2006; 252:184-190.
19. Haisenleder DJ, Cox ME, Parsons SJ, Marshall JC. Gonadotropin-releasing hormone pulses are required to maintain activation of mitogen-activated protein kinase: role in stimulation of gonadotrope gene expression. Endocrinology 1998; 139:3104-3111.
20. Harris D, Bonfil D, Chuderland D, Kraus S, Seger R, Naor Z. Activation of MAPK cascades by GnRH: ERK and JNK are involved in basal and GnRH-stimulated activity of the glycoprotein hormone LHβ-subunit promoter. Endocrinology 2002; 143:1018-1025.
21. Mulvaney JM, Roberson MS. Divergent signaling pathways requiring discrete calcium signals mediate concurrent activation of two mitogen-activated protein kinases by gonadotropin-releasing hormone. J Biol Chem 2000; 275:14182-14189.
22. Xie J, Bliss SP, Nett TM, Eersole BJ, Sealfon SC, Roberson MS. Transcript profiling of immediate early genes reveals a unique role of ATF-3 in mediating activation of the glycoprotein hormone alpha-subunit promoter by GnRH. Mol Endocrinol 2005; 19:2624-2638.
23. Haisenleder DJ, Burger LL, Walsh HE, Stevens J, Aylor KW, Shupnik MA, Marshall JC. Pulsatile gonadotropin-releasing hormone stimulation of gonadotropin subunit transcription in rat pituitaries: evidence for the involvement of Jun N-terminal kinase but not p38. Endocrinology 2008; 149:139-145.
24. Burger LL, Dalkin AC, Aylor KW, Haisenleder DJ, Marshall JC. 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 2002; 143:3243-3249.
25. Dalkin AC, Burger LL, Aylor KW, Haisenleder DJ, Workman LJ, Cho S, Marshall JC. Regulation of gonadotropin subunit gene transcription by gonadotropin-releasing hormone: measurement of primary transcript ribonucleic acids by quantitative reverse transcription-polymerase chain reaction assays. Endocrinology 2001; 142:139-146.
26. Chomczynski P, Sacchi N. Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162:156-159.
27. Burger LL, Haisenleder DJ, Wotton GM, Aylor KW, Dalkin AC, Marshall JC. The regulation of FSHb transcription by gonadal steroids: testosterone and estradiol modulation of the activin intracellular signaling pathway. Am J Physiol Endocrinol Metab 2007; 293:E277-E285.
28. Kirk SE, Dalkin AC, Yasin M, Haisenleder DJ, Marshall JC. Gonadotropin-releasing hormone pulse frequency regulates expression of pituitary follistatin messenger ribonucleic acid: a mechanism for differential gonadotrope function. Endocrinology 1994; 135:876-880.
29. Cui ZJ, Gorelick FS, Dannies PS. Calcium/calmodulin-dependent protein kinase-II activation in rat pituitary cells in the presence of thyrotropin-releasing hormone and dopamine. Endocrinology 1994; 134:2245-2250.
30. Cui ZJ, Hidaka H, Dannies PS. KN-62, a calcium/calmodulin-dependent protein kinase II inhibitor, inhibits high potassium-stimulated prolactin secretion and intracellular calcium increases in anterior pituitary cells. Biochim Biophys Acta 1996; 1310:343-347.
31. Means AR. Regulatory cascades involving calmodulin-dependent protein kinases. Mol Endocrinol 2000; 14:4-13.
32. Duan WR, Ito M, Park Y, Maizels ET, Hunzicker-Dunn M, Jameson JL. GnRH regulates early growth response protein 1 transcription through multiple promoter elements. Mol Endocrinol 2002; 16:221-233.
33. Reiss N, Llevi LN, Shacham S, Harris D, Seger R, Naor Z. Mechanism of mitogen-activated protein kinase activation by gonadotropin-releasing hormone in the pituitary of αT3-1 cell line: differential roles of calcium and protein kinase C. Endocrinology 1997; 138:1673-1682.
34. Bonfil D, Chuderland D, Kraus S, Shahbazian D, Friedberg I, Seger R, 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 2004; 145:2228-2244.
35. Kanasaki H, Bedecarrats GY, Kam KY, Xu S, Kaiser UB. Gonadotropin- releasing hormone pulse frequency-dependent activation of extracellular signal-regulated kinase pathways in perifused LβT2 cells. Endocrinology 2005; 146:5503-5513.
36. Yokoi T, Ohmichi M, Tasaka K, Kimura A, Kanda Y, Hayakawa J, Tahara M, Hisamoto K, Kurachi H, Murata Y. Activation of the luteinizing hormone beta promoter by gonadotropin- releasing hormone requires c-Jun NH2-terminal protein kinase. J Biol Chem 2000; 275:21639-21647.
37. Lui F, Austin DA, Mellon PL, Olefsky JM, Webster NJG. GnRH activates ERK 1 and 2 leading to the induction of c-fos and LHβ protein expression in Lβ-T2 cells. Mol Endocrinol 2002; 16:419-434.
38. Vasilyev VV, Lawson MA, Dipaolo D, Webster NJ, Mellon PL. Different signaling pathways control acute induction versus long-term repression of LHβ transcription by GnRH. Endocrinology 2002; 143:3414-3426.
39. Nguyen KA, Santos SJ, Kreidel MK, Diaz AL, Rey R, Lawson MA. Acute regulation of translation initiation by gonadotropin-releasing hormone in the gonadotrope cell line LβT2. Mol Endocrinol 2004; 18:1301-1312.
40. Roberson MS, Zhang T, Li HL, Mulvaney JM. Activation of the p38 mitogen-activated protein kinase pathway by gonadotropin-releasing hormone. Endocrinology 1999; 140:1310-1318.