GnRH regulates gonadotropin gene expression through NADPH/dual oxidase-derived reactive oxygen species

Endocrinology

Volumn 156, Issue 6, 2015, Pages 2185-2199

  Kim, Taeshin ^a   Lawson, Mark A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FOLLITROPIN; GONADORELIN; GONADOTROPIN; LUTEINIZING HORMONE; MITOGEN ACTIVATED PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SHORT HAIRPIN RNA;

ANIMAL CELL; ARTICLE; CELL STRESS; DOWN REGULATION; FEMALE; GENE EXPRESSION; HYPOPHYSIS CELL; IMMUNOFLUORESCENCE; LUTEINIZING HORMONE RELEASE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECOND MESSENGER; WESTERN BLOTTING; ANIMAL; CELL LINE; DRUG EFFECTS; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; FOLLICLE STIMULATING HORMONE; GONADOTROPIN-RELEASING HORMONE; GONADOTROPINS; LUTEINIZING HORMONE; MALE; MICE; NADPH OXIDASE; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84930467990     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1709     Document Type: Article

References (73)

1. Gharib SD, Wierman ME, Shupnik MA, Chin WW. Molecular biology of the pituitary gonadotropins. Endocr Rev. 1990;11:177-199.
2. Shacham S, Harris D, Ben-Shlomo H, et al. Mechanism of GnRH receptor signaling on gonadotropin release and gene expression in pituitary gonadotrophs. Vitam Horm. 2001;63:63-90.
3. 2+ and protein kinase C. Front Neuroendocrinol. 1998;19:1-19.
4. Gur G, Bonfil D, Safarian H, Naor Z, Yaron Z. GnRH receptor signaling in tilapia pituitary cells: role of mitogen-activated protein kinase (MAPK). Comp Biochem Physiol B Biochem Mol Biol. 2001;129:517-524.
5. Liu F, Austin DA, Mellon PL, Olefsky JM, Webster NJ. GnRH activates ERK1/2 leading to the induction of c-fos and LHβ protein expression in LβT2 cells. Mol Endocrinol. 2002;16:419-434.
6. Shah BH, Farshori MP, Jambusaria A, Catt KJ. Roles of Src and epidermal growth factor receptor transactivation in transient and sustained ERK1/2 responses to gonadotropin-releasing hormone receptor activation. J Biol Chem. 2003;278:19118-19126.
7. Rubinfeld H, Seger R. The ERK cascade: a prototype of MAPK signaling. Mol Biotechnol. 2005;31:151-174.
8. Rubinfeld H, Seger R. The ERK cascade as a prototype of MAPK signaling pathways. Methods Mol Biol. 2004;250:1-28.
9. Sarker KP, Biswas KK, Yamakuchi M, et al. ASK1-p38 MAPK/JNK signaling cascade mediates anandamide-induced PC12 cell death. J Neurochem. 2003;85:50-61.
10. Seger R, Krebs EG. The MAPK signaling cascade. FASEB J. 1995; 9:726-735.
11. Son Y, Cheong YK, Kim NH, Chung HT, Kang DG, Pae HO. Mitogen-activated protein kinases and reactive oxygen species: how can ROS activate MAPK pathways? J Signal Transduct. 2011;2011:792639.
12. Binder AK, Grammer JC, Herndon MK, Stanton JD, Nilson JH. GnRH regulation of Jun and Atf3 requires calcium, calcineurin, and NFAT. Mol Endocrinol. 2012;26:873-886.
13. Coss D, Jacobs SB, Bender CE, Mellon PL. A novel AP-1 site is critical for maximal induction of the follicle-stimulating hormone beta gene by gonadotropin-releasing hormone. J Biol Chem. 2004;279:152-162.
14. Ding M, Li JJ, Leonard SS, et al. Vanadate-induced activation of activator protein-1: role of reactive oxygen species. Carcinogenesis. 1999;20:663-668.
15. Aggeli IK, Beis I, Gaitanaki C. ERKs and JNKs mediate hydrogen peroxide-induced Egr-1 expression and nuclear accumulation in H9c2 cells. Physiol Res. 2010;59:443-454.
16. Tremblay JJ, Drouin J. Egr-1 is a downstream effector of GnRH and synergizes by direct interaction with Ptx1 and SF-1 to enhance luteinizing hormone beta gene transcription. Mol Cell Biol. 1999;19:2567-2576.
17. Xie J, Bliss SP, Nett TM, Ebersole BJ, Sealfon SC, Roberson MS. Transcript profiling of immediate early genes reveals a unique role for activating transcription factor 3 in mediating activation of the glycoprotein hormone α-subunit promoter by gonadotropin-releasing hormone. Mol Endocrinol. 2005;19:2624-2638.
18. Lu D, Chen J, Hai T. The regulation of ATF3 gene expression by mitogen-activated protein kinases. Biochem J. 2007;401:559-567.
19. Allen RG, Tresini M. Oxidative stress and gene regulation. Free Radic Biol Med. 2000;28:463-499.
20. Poli G, Leonarduzzi G, Biasi F, Chiarpotto E. Oxidative stress and cell signalling. Curr Med Chem. 2004;11:1163-1182.
21. Wang X, Martindale JL, Liu Y, Holbrook NJ. The cellular response to oxidative stress: influences of mitogen-activated protein kinase signalling pathways on cell survival. Biochem J. 1998;333(Pt 2):291-300.
22. Bedard K, Krause KH. The NOX family of ROS-generating NA-DPH oxidases: physiology and pathophysiology. Physiol Rev. 2007;87:245-313.
23. Jiang F, Zhang Y, Dusting GJ. NADPH oxidase-mediated redox signaling: roles in cellular stress response, stress tolerance, and tissue repair. Pharmacol Rev. 2011;63:218-242.
24. Kuroda J, Nakagawa K, Yamasaki T, et al. The superoxide-producing NAD(P)H oxidase Nox4 in the nucleus of human vascular endothelial cells. Genes Cells. 2005;10:1139-1151.
25. 2 generation in the thyroid: investigation of the control of dual oxidases (DUOX) activity in intact ex vivo thyroid tissue and cell lines. Mol Cell Endocrinol. 2011;343:32-44.
26. Lacroix L, Nocera M, Mian C, et al. Expression of nicotinamide adenine dinucleotide phosphate oxidase flavoprotein DUOX genes and proteins in human papillary and follicular thyroid carcinomas. Thyroid. 2001;11:1017-1023.
27. Milenkovic M, De Deken X, Jin L, et al. Duox expression and related H2O2 measurement in mouse thyroid: onset in embryonic development and regulation by TSH in adult. J Endocrinol. 2007;192:615-626.
28. Rizzo A, Roscino MT, Binetti F, Sciorsci RL. Roles of reactive oxygen species in female reproduction. Reprod Domest Anim. 2012;47:344-352.
29. Aitken RJ, Clarkson JS, Fishel S. Generation of reactive oxygen species, lipid peroxidation, and human sperm function. Biol Reprod. 1989;41:183-197.
30. Baker MA, Aitken RJ. The importance of redox regulated pathways in sperm cell biology. Mol Cell Endocrinol. 2004;216:47-54.
31. Kato H, Sugino N, Takiguchi S, Kashida S, Nakamura Y. Roles of reactive oxygen species in the regulation of luteal function. Rev Reprod. 1997;2:81-83.
32. Do MH, Santos SJ, Lawson MA. GNRH induces the unfolded protein response in the LβT2 pituitary gonadotrope cell line. Mol Endocrinol. 2009;23:100-112.
33. -ΔΔCT method. Methods. 2001;25:402-408.
34. Breen KM, Thackray VG, Coss D, Mellon PL. Runt-related transcription factors impair activin induction of the follicle-stimulating hormone β-subunit gene. Endocrinology. 2010;151:2669-2680.
35. Nguyen KA, Intriago RE, Upadhyay HC, Santos SJ, Webster NJ, Lawson MA. Modulation of gonadotropin-releasing hormone-induced extracellular signal-regulated kinase activation by dual-specificity protein phosphatase 1 in LβT2 gonadotropes. Endocrinology. 2010;151:4882-4893.
36. Lawson MA, Tsutsumi R, Zhang H, et al. Pulse sensitivity of the luteinizing hormone β promoter is determined by a negative feedback loop involving early growth response-1 and Ngfi-A binding protein 1 and 2. Mol Endocrinol. 2007;21:1175-1191.
37. Dobkin-Bekman M, Rahamin-Ben Navi L, Shterntal B, et al. Differential role of PKC isoforms in GnRH and phorbol 12-myristate 13-acetate activation of extracellular signal-regulated kinase and Jun N-terminal kinase. Endocrinology. 2010;151:4894-4907.
38. Naor Z, Shacham S, Harris D, Seger R, Reiss N. Signal transduction of the gonadotropin releasing hormone (GnRH) receptor: cross-talk of calcium, protein kinase C (PKC), and arachidonic acid. Cell Mol Neurobiol. 1995;15:527-544.
39. Shah BH, Soh JW, Catt KJ. Dependence of gonadotropin-releasing hormone-induced neuronal MAPK signaling on epidermal growth factor receptor transactivation. J Biol Chem. 2003;278:2866-2875.
40. 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.
41. Sosnowski R, Mellon PL, Lawson MA. Activation of translation in pituitary gonadotrope cells by gonadotropin-releasing hormone. Mol Endocrinol. 2000;14:1811-1819.
42. Larivière S, Garrel G, Simon V, et al. Gonadotropin-releasing hormone couples to 3′,5′-cyclic adenosine-5′-monophosphate pathway through novel protein kinase Cδ and -∈ in LβT2 gonadotrope cells. Endocrinology. 2007;148:1099-1107.
43. 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.
44. Do MH, Kim T, He F, et al. Polyribosome and ribonucleoprotein complex redistribution of mRNA induced by GnRH involves both EIF2AK3 and MAPK signaling. Mol Cell Endocrinol. 2014;382:346-357.
45. Kim T, Do MH, Lawson MA. Translational control of gene expression in the gonadotrope. Mol Cell Endocrinol. 2014;385:78-87.
46. 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.
47. Thackray VG, Mellon PL, Coss D. Hormones in synergy: regulation of the pituitary gonadotropin genes. Mol Cell Endocrinol. 2010;314:192-203.
48. Bliss SP, Miller A, Navratil AM, et al. ERK signaling in the pituitary is required for female but not male fertility. Mol Endocrinol. 2009;23:1092-1101.
49. Mistry DS, Tsutsumi R, Fernandez M, et al. Gonadotropin-releasing hormone pulse sensitivity of follicle-stimulating hormone-beta gene is mediated by differential expression of positive regulatory activator protein 1 factors and corepressors SKIL and TGIF1. Mol Endocrinol. 2011;25:1387-1403.
50. Tsaneva-Atanasova K, Mina P, Caunt CJ, Armstrong SP, McArdle CA. Decoding GnRH neurohormone pulse frequency by convergent signalling modules. J R Soc Interface. 2012;9:170-182.
51. Pal L, Chu HP, Shu J, Topalli I, Santoro N, Karkanias G. In vitro evidence of glucose-induced toxicity in GnRH secreting neurons: high glucose concentrations influence GnRH secretion, impair cell viability, and induce apoptosis in the GT1-1 neuronal cell line. Fertil Steril. 2007;88:1143-1149.
52. Lawson MA, Jain S, Sun S, Patel K, Malcolm PJ, Chang RJ. Evidence for insulin suppression of baseline luteinizing hormone in women with polycystic ovarian syndrome and normal women. J Clin Endocrinol Metab. 2008;93:2089-2096.
53. Sharma S, Morinaga H, Hwang V, et al. Free fatty acids induce Lhb mRNA but suppress Fshb mRNA in pituitary LβT2 gonadotropes and diet-induced obesity reduces FSH levels in male mice and disrupts the proestrous LH/FSH surge in female mice. Endocrinology. 2013;154:2188-2199.
54. Navratil AM, Song H, Hernandez JB, et al. Insulin augments gonadotropin-releasing hormone induction of translation in LβT2 cells. Mol Cell Endocrinol. 2009;311:47-54.
55. Zhen S, Zakaria M, Wolfe A, Radovick S. Regulation of gonadotropin-releasing hormone (GnRH) gene expression by insulin-like growth factor I in a cultured GnRH-expressing neuronal cell line. Mol Endocrinol. 1997;11:1145-1155.
56. Bonfil D, Chuderland D, Kraus S, 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 beta-subunit promoter. Endocrinology. 2004;145:2228-2244.
57. Benard O, Naor Z, Seger R. Role of dynamin, Src, and Ras in the protein kinase C-mediated activation of ERK by gonadotropin-releasing hormone. J Biol Chem. 2001;276:4554-4563.
58. Chopra I, Li HF, Wang H, Webster KA. Phosphorylation of the insulin receptor by AMP-activated protein kinase (AMPK) promotes ligand-independent activation of the insulin signalling pathway in rodent muscle. Diabetologia. 2012;55:783-794.
59. Naor Z, Jabbour HN, Naidich M, et al. Reciprocal cross talk between gonadotropin-releasing hormone (GnRH) and prostaglandin receptors regulates GnRH receptor expression and differential gonadotropin secretion. Mol Endocrinol. 2007;21:524-537.
60. D'Autréaux B, Toledano MB. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol. 2007;8:813-824.
61. McCubrey JA, Lahair MM, Franklin RA. Reactive oxygen species-induced activation of the MAP kinase signaling pathways. Antioxid Redox Signal. 2006;8:1775-1789.
62. Forteza R, Salathe M, Miot F, Conner GE. Regulated hydrogen peroxide production by Duox in human airway epithelial cells. Am J Respir Cell Mol Biol. 2005;32:462-469.
63. Stefanska J, Pawliczak R. Apocynin: molecular aptitudes. Mediators Inflamm. 2008;2008:106507.
64. 2+ pump. Br J Pharmacol. 2009;158:790-796.
65. Tai P, Ascoli M. Reactive oxygen species (ROS) play a critical role in the cAMP-induced activation of Ras and the phosphorylation of ERK1/2 in Leydig cells. Mol Endocrinol. 2011;25:885-893.
66. + hematopoietic progenitor cells. Blood. 2010;115:1238-1246.
67. Armstrong J, Childs GV. Changes in expression of epidermal growth factor receptors by anterior pituitary cells during the estrous cycle: cyclic expression by gonadotropes. Endocrinology. 1997;138:1903-1908.
68. Fowkes RC, Burch J, Burrin JM. Stimulation of extracellular signal-regulated kinase by pituitary adenylate cyclase-activating polypeptide in αT3-1 gonadotrophs. J Endocrinol. 2001;171:R5-R10.
69. Kamata H, Honda S, Maeda S, Chang L, Hirata H, Karin M. Reactive oxygen species promote TNFα-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell. 2005;120:649-661.
70. Armstrong SP, Caunt CJ, McArdle CA. Gonadotropin-releasing hormone and protein kinase C signaling to ERK: spatiotemporal regulation of ERK by docking domains and dual-specificity phosphatases. Mol Endocrinol. 2009;23:510-519.
71. Choi SG, Ruf-Zamojski F, Pincas H, Roysam B, Sealfon SC. Characterization of a MAPK scaffolding protein logic gate in gonadotropes. Mol Endocrinol. 2011;25:1027-1039.
72. Perrett RM, Voliotis M, Armstrong SP, et al. Pulsatile hormonal signaling to extracellular signal-regulated kinase: exploring system sensitivity to gonadotropin-releasing hormone pulse frequency and width. J Biol Chem. 2014;289:7873-7883.
73. Ruf F, Hayot F, Park MJ, et al. Noise propagation and scaling in regulation of gonadotrope biosynthesis. Biophys J. 2007;93:4474-4480.