The calcineurin-nuclear factor of activated T cells signaling pathway mediates the effect of corticotropin releasing factor and urocortins on catecholamine synthesis

Journal of Cellular Physiology

Volumn 227, Issue 5, 2012, Pages 1861-1872

  Dermitzaki, Eirini ^a   Tsatsanis, Christos ^a   Gravanis, Achille ^a   Margioris, Andrew N ^a  

^a UNIVERSITY OF CRETE   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; CORTICOTROPIN RELEASING FACTOR RECEPTOR 2; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLOSPORIN A; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE P38; NORADRENALIN; PROTEIN KINASE B; PROTEIN KINASE C; TRANSCRIPTION FACTOR NFAT; UROCORTIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CATECHOLAMINE SYNTHESIS; CELL ACTIVITY; FEMALE; GENETIC TRANSFECTION; NONHUMAN; ONCOGENE H RAS; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION INITIATION;

ANIMALS; CALCINEURIN; CATECHOLAMINES; CORTICOTROPIN-RELEASING HORMONE; CYCLOSPORINE; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HUMANS; NFATC TRANSCRIPTION FACTORS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PC12 CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN ISOFORMS; RATS; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; RECOMBINANT FUSION PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; UROCORTINS;

RATTUS;

EID: 84856138052     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22914     Document Type: Article

References (80)

1. Bale TL, Vale WW. 2004. CRF and CRF receptors: Role in stress responsivity and other behaviors. Annu Rev Pharmacol Toxicol 44: 525-557.
2. Bellacosa A, Chan TO, Ahmed NN, Datta K, Malstrom S, Stokoe D, McCormick F, Feng J, Tsichlis P. 1998. Akt activation by growth factors is a multiple-step process: The role of the PH domain. Oncogene 17: 313-325.
3. Benedito AB, Lehtinen M, Massol R, Lopes UG, Kirchhausen T, Rao A, Bonni A. 2005. The transcription factor NFAT3 mediates neuronal survival. J Biol Chem 280: 2818-2825.
4. Boss V, Talpade DJ, Murphy TJ. 1996. Induction of NFAT-mediated transcription by Gq-coupled receptors in lymphoid and non-lymphoid cells. J Biol Chem 271: 10429-10432.
5. Cano E, Canellada A, Minami T, Iglesias T, Redondo JM. 2005. Depolarization of neural cells induces transcription of the Down syndrome critical region 1 isoform 4 via a calcineurin/nuclear factor of activated T cells-dependent pathway. J Biol Chem 280: 29435-29443.
6. Chatzaki E, Margioris AN, Gravanis A. 2002. Expression and regulation of corticotropin-releasing hormone binding protein (CRH-BP) in rat adrenals. J Neurochem 80: 81-90.
7. Chen L, Glover JN, Hogan PG, Rao A, Harrison SC. 1998. Structure of the DNA-binding domains from NFAT, Fos and Jun bound specifically to DNA. Nature 392: 42-48.
8. Chow CW, Davis RJ. 2000. Integration of calcium and cyclic AMP signaling pathways by 14-3-3. Mol Cell Biol 20: 702-712.
9. Christoforidou AV, Papadaki HA, Margioris AN, Eliopoulos GD, Tsatsanis C. 2004. Expression of the Tpl2/Cot oncogene in human T-cell neoplasias. Mol Cancer 3: 34.
10. Clipstone NA, Crabtree GR. 1992. Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature 357: 695-697.
11. Crabtree GR, Olson EN. 2002. NFAT signaling: Choreographing the social lives of cells. Cell 109: S67-S79.
12. Dautzenberg FM, Hauger RL. 2002. The CRF peptide family and their receptors: Yet more partners discovered. Trends Pharmacol Sci 23: 71-77.
13. Dave JR, Eiden LE, Lozovsky D, Waschek JA, Eskay RL. 1987. Calcium-independent and calcium-dependent mechanisms regulate corticotropin-releasing factor-stimulated proopiomelanocortin peptide secretion and messenger ribonucleic acid production. Endocrinology 120: 305-310.
14. Delgado M, Ganea D. 2001. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit expression of Fas ligand in activated T lymphocytes by regulating c-Myc, NF-kappa B, NF-AT, and early growth factors 2/3. J Immunol 166: 1028-1040.
15. Dermitzaki E, Gravanis A, Venihaki M, Stournaras C, Margioris AN. 2001. Opioids suppress basal and nicotine-induced catecholamine secretion via a stabilizing effect on actin filaments. Endocrinology 142: 2022-2031.
16. Dermitzaki I, Tsatsanis C, Alexaki VI, Castanas E, Margioris AN. 2004. Roles of protein kinase A (PKA) and PKC on corticotropin-releasing hormone (CRH)-induced elevation of cytosolic calcium from extra- and intra-cellular sources. Hormones (Athens) 3: 252-258.
17. Dermitzaki E, Tsatsanis C, Charalampopoulos I, Androulidaki A, Alexaki VI, Castanas E, Gravanis A, Margioris AN. 2005. Corticotropin-releasing hormone activates protein kinase C in an isoenzyme-specific manner. Biochem Biophys Res Commun 327: 828-836.
18. Dermitzaki E, Tsatsanis C, Minas V, Chatzaki E, Charalampopoulos I, Venihaki M, Androulidaki A, Lambropoulou M, Spiess J, Michalodimitrakis E, Gravanis A, Margioris AN. 2007. Corticotropin-releasing factor (CRF) and the urocortins differentially regulate catecholamine secretion in human and rat adrenals, in a CRF receptor type-specific manner. Endocrinology 148: 1524-1538.
19. Dunn AJ, Berridge CW. 1990. Physiological and behavioral responses to corticotropin-releasing factor administration: Is CRF a mediator of anxiety or stress responses? Brain Res Brain Res Rev 15: 71-100.
20. Emmel EA, Verweij CL, Durand DB, Higgins KM, Lacy E, Crabtree GR. 1989. Cyclosporin A specifically inhibits function of nuclear proteins involved in T cell activation. Science 246: 1617-1620.
21. Flanagan WM, Corthesy B, Bram RJ, Crabtree GR. 1991. Nuclear association of a T-cell transcription factor blocked by FK-506 and cyclosporin A. Nature 352: 803-807.
22. Frantz B, Nordby EC, Bren G, Steffan N, Paya CV, Kincaid RL, Tocci MJ, O'Keefe SJ, O'Neill EA. 1994. Calcineurin acts in synergy with PMA to inactivate I kappa B/MAD3, an inhibitor of NF-kappa B. EMBO J 13: 861-870.
23. Fung BP, Yoon SO, Chikaraishi DM. 1992. Sequences that direct rat tyrosine hydroxylase gene expression. J Neurochem 58: 2044-2052.
24. Ganea D, Delgado M. 2002. Vasoactive intestinal peptide (VIP) and pituitary adenylate cyclase-activating polypeptide (PACAP) as modulators of both innate and adaptive immunity. Crit Rev Oral Biol Med 13: 229-237.
25. Gelain DP, Moreira JC, Bevilaqua LR, Dickson PW, Dunkley PR. 2007. Retinol activates tyrosine hydroxylase acutely by increasing the phosphorylation of serine40 and then serine31 in bovine adrenal chromaffin cells. J Neurochem 103: 2369-2379.
26. Graef IA, Chen F, Crabtree GR. 2001. NFAT signaling in vertebrate development. Curr Opin Genet Dev 11: 505-512.
27. Graef IA, Wang F, Charron F, Chen L, Neilson J, Tessier-Lavigne M, Crabtree GR. 2003. Neurotrophins and netrins require calcineurin/NFAT signaling to stimulate outgrowth of embryonic axons. Cell 113: 657-670.
28. Guerineau N, Corcuff JB, Tabarin A, Mollard P. 1991. Spontaneous and corticotropin-releasing factor-induced cytosolic calcium transients in corticotrophs. Endocrinology 129: 409-420.
29. Haug T, Storm JF. 2000. Protein kinase A mediates the modulation of the slow Ca(2+)-dependent K(+) current, I(sAHP), by the neuropeptides CRF, VIP, and CGRP in hippocampal pyramidal neurons. J Neurophysiol 83: 2071-2079.
30. Hauger RL, Grigoriadis DE, Dallman MF, Plotsky PM, Vale WW, Dautzenberg FM. 2003. International Union of Pharmacology. XXXVI. Current status of the nomenclature for receptors for corticotropin-releasing factor and their ligands. Pharmacol Rev 55: 21-26.
31. Hermann-Kleiter N, Thuille N, Pfeifhofer C, Gruber T, Schafer M, Zitt C, Hatzelmann A, Schudt C, Leitges M, Baier G. 2006. PKCtheta and PKA are antagonistic partners in the NF-AT transactivation pathway of primary mouse CD3+ T lymphocytes. Blood 107: 4841-4848.
32. Jain J, McCaffrey PG, Miner Z, Kerppola TK, Lambert JN, Verdine GL, Curran T, Rao A. 1993. The T-cell transcription factor NFATp is a substrate for calcineurin and interacts with Fos and Jun. Nature 365: 352-355.
33. Jain J, Burgeon E, Badalian TM, Hogan PG, Rao A. 1995. A similar DNA-binding motif in NFAT family proteins and the Rel homology region. J Biol Chem 270: 4138-4145.
34. Jedema HP, Grace AA. 2004. Corticotropin-releasing hormone directly activates noradrenergic neurons of the locus ceruleus recorded in vitro. J Neurosci 24: 9703-9713.
35. Kane LP, Mollenauer MN, Xu Z, Turck CW, Weiss A. 2002. Akt-dependent phosphorylation specifically regulates Cot induction of NF-kappa B-dependent transcription. Mol Cell Biol 22: 5962-5974.
36. Kao SC, Wu H, Xie J, Chang CP, Ranish JA, Graef IA, Crabtree GR. 2009. Calcineurin/NFAT signaling is required for neuregulin-regulated Schwann cell differentiation. Science 323: 651-654.
37. Karpurapu M, Wang D, Singh NK, Li Q, Rao GN. 2008. NFATc1 targets cyclin A in the regulation of vascular smooth muscle cell multiplication during restenosis. J Biol Chem 283: 26577-26590.
38. Kim Y, Park MK, Uhm DY, Chung S. 2007. Modulation of T-type Ca2+ channels by corticotropin-releasing factor through protein kinase C pathway in MN9D dopaminergic cells. Biochem Biophys Res Commun 358: 796-801.
39. Klee CB, Ren H, Wang X. 1998. Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. J Biol Chem 273: 13367-13370.
40. Kumer SC, Vrana KE. 1996. Intricate regulation of tyrosine hydroxylase activity and gene expression. J Neurochem 67: 443-462.
41. Kuryshev YA, Haak L, Childs GV, Ritchie AK. 1997. Corticotropin releasing hormone inhibits an inwardly rectifying potassium current in rat corticotropes. J Physiol 502: 265-279.
42. Lavicky J, Dunn AJ. 1993. Corticotropin-releasing factor stimulates catecholamine release in hypothalamus and prefrontal cortex in freely moving rats as assessed by microdialysis. J Neurochem 60: 602-612.
43. Lee AK, Tse A. 1997. Mechanism underlying corticotropin-releasing hormone (CRH) triggered cytosolic Ca2+ rise in identified rat corticotrophs. J Physiol 504: 367-378.
44. Macian F. 2005. NFAT proteins: Key regulators of T-cell development and function. Nat Rev Immunol 5: 472-484.
45. Macian F, Lopez-Rodriguez C, Rao A. 2001. Partners in transcription: NFAT and AP-1. Oncogene 20: 2476-2489.
46. Mallet J. 1999. Tyrosine hydroxylase from cloning to neuropsychiatric disorders. Brain Res Bull 50: 381-382.
47. Meinhardt H. 2000. Olson EN, Williams RS. Remodeling muscles with calcineurin. Bioessays 2000;22:510-519. Bioessays 22: 1049.
48. Millet I, Phillips RJ, Sherwin RS, Ghosh S, Voll RE, Flavell RA, Vignery A, Rincon M. 2000. Inhibition of NF-kappaB activity and enhancement of apoptosis by the neuropeptide calcitonin gene-related peptide. J Biol Chem 275: 15114-15121.
49. Molkentin JD, Lu JR, Antos CL, Markham B, Richardson J, Robbins J, Grant SR, Olson EN. 1998. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93: 215-228.
50. Muramatsu T, Inoue K, Iwasaki S, Yamauchi T, Hayashi T, Kiriike N. 2006. Corticotropin-releasing factor receptor type 1, but not type 2, in the ventromedial hypothalamus modulates dopamine release in female rats. Pharmacol Biochem Behav 85: 435-440.
51. Nabhen SL, Perfume G, Battistone MA, Rossi A, Abramoff T, Bianciotti LG, Vatta MS. 2009. Short-term effects of endothelins on tyrosine hydroxylase activity and expression in the olfactory bulb of normotensive rats. Neurochem Res 34: 953-963.
52. Nakashima A, Ota A, Sabban EL. 2003. Interactions between Egr1 and AP1 factors in regulation of tyrosine hydroxylase transcription. Brain Res Mol Brain Res 112: 61-69.
53. Northrop JP, Ho SN, Chen L, Thomas DJ, Timmerman LA, Nolan GP, Admon A, Crabtree GR. 1994. NF-AT components define a family of transcription factors targeted in T-cell activation. Nature 369: 497-502.
54. Okamura H, Garcia-Rodriguez C, Martinson H, Qin J, Virshup DM, Rao A. 2004. A conserved docking motif for CK1 binding controls the nuclear localization of NFAT1. Mol Cell Biol 24: 4184-4195.
55. Owens MJ, Nemeroff CB. 1991. Physiology and pharmacology of corticotropin-releasing factor. Pharmacol Rev 43: 425-473.
56. Perry SJ, Junger S, Kohout TA, Hoare SR, Struthers RS, Grigoriadis DE, Maki RA. 2005. Distinct conformations of the corticotropin releasing factor type 1 receptor adopted following agonist and antagonist binding are differentially regulated. J Biol Chem 280: 11560-11568.
57. Plyte S, Boncristiano M, Fattori E, Galvagni F, Paccani SR, Majolini MB, Oliviero S, Ciliberto G, Telford JL, Baldari CT. 2001. Identification and characterization of a novel nuclear factor of activated T-cells-1 isoform expressed in mouse brain. J Biol Chem 276: 14350-14358.
58. Qiu DL, Chu CP, Shirasaka T, Tsukino H, Nakao H, Kato K, Kunitake T, Katoh T, Kannan H. 2005. Corticotrophin-releasing factor augments the I(H) in rat hypothalamic paraventricular nucleus parvocellular neurons in vitro. J Neurophysiol 94: 226-234.
59. Raingeaud J, Gupta S, Rogers JS, Dickens M, Han J, Ulevitch RJ, Davis RJ. 1995. Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J Biol Chem 270: 7420-7426.
60. Rao A, Luo C, Hogan PG. 1997. Transcription factors of the NFAT family: Regulation and function. Annu Rev Immunol 15: 707-747.
61. Rasmussen TN, Novak I, Nielsen SM. 2004. Internalization of the human CRF receptor 1 is independent of classical phosphorylation sites and of beta-arrestin 1 recruitment. Eur J Biochem 271: 4366-4374.
62. Reisine T. 1989. Phorbol esters and corticotropin releasing factor stimulate calcium influx in the anterior pituitary tumor cell line, AtT-20, through different intracellular sites of action. J Pharmacol Exp Ther 248: 984-990.
63. Reyes BA, Fox K, Valentino RJ, Van Bockstaele EJ. 2006. Agonist-induced internalization of corticotropin-releasing factor receptors in noradrenergic neurons of the rat locus coeruleus. Eur J Neurosci 23: 2991-2998.
64. Riegel AC, Williams JT. 2008. CRF facilitates calcium release from intracellular stores in midbrain dopamine neurons. Neuron 57: 559-570.
65. Sabban EL, Kvetnansky R. 2001. Stress-triggered activation of gene expression in catecholaminergic systems: Dynamics of transcriptional events. Trends Neurosci 24: 91-98.
66. Saygili E, Rana OR, Meyer C, Gemein C, Andrzejewski MG, Ludwig A, Weber C, Schotten U, Kruttgen A, Weis J, Schwinger RH, Mischke K, Rassaf T, Kelm M, Schauerte P. 2009. The angiotensin-calcineurin-NFAT pathway mediates stretch-induced up-regulation of matrix metalloproteinases-2/-9 in atrial myocytes. Basic Res Cardiol 104: 435-448.
67. Seybold VS, Coicou LG, Groth RD, Mermelstein PG. 2006. Substance P initiates NFAT-dependent gene expression in spinal neurons. J Neurochem 97: 397-407.
68. Tsao P, von Zastrow M. 2000. Downregulation of G protein-coupled receptors. Curr Opin Neurobiol 10: 365-369.
69. Tsatsanis C, Patriotis C, Bear SE, Tsichlis PN. 1998a. The Tpl-2 protooncoprotein activates the nuclear factor of activated T cells and induces interleukin 2 expression in T cell lines. Proc Natl Acad Sci USA 95: 3827-3832.
70. Tsatsanis C, Patriotis C, Tsichlis PN. 1998b. Tpl-2 induces IL-2 expression in T-cell lines by triggering multiple signaling pathways that activate NFAT and NF-kappaB. Oncogene 17: 2609-2618.
71. Vale W, Spiess J, Rivier C, Rivier J. 1981. Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin. Science 213: 1394-1397.
72. Venihaki M, Gravanis A, Margioris AN. 1997. Comparative study between normal rat chromaffin and PC12 rat pheochromocytoma cells: Production and effects of corticotropin-releasing hormone. Endocrinology 138: 698-704.
73. Venihaki M, Ain K, Dermitzaki E, Gravanis A, Margioris AN. 1998. KAT45, a noradrenergic human pheochromocytoma cell line producing corticotropin-releasing hormone. Endocrinology 139: 713-722.
74. Wallace RW, Tallant EA, Cheung WY. 1980. High levels of a heat-labile calmodulin-binding protein (CaM-BP80) in bovine neostriatum. Biochemistry 19: 1831-1837.
75. Wanat MJ, Hopf FW, Stuber GD, Phillips PE, Bonci A. 2008. Corticotropin-releasing factor increases mouse ventral tegmental area dopamine neuron firing through a protein kinase C-dependent enhancement of Ih. J Physiol 586: 2157-2170.
76. Wiesner B, Roloff B, Fechner K, Slominski A. 2003. Intracellular calcium measurements of single human skin cells after stimulation with corticotropin-releasing factor and urocortin using confocal laser scanning microscopy. J Cell Sci 116: 1261-1268.
77. Yang TT, Chow CW. 2003. Transcription cooperation by NFAT.C/EBP composite enhancer complex. J Biol Chem 278: 15874-15885.
78. Yang YJ, Lee HJ, Huang HS, Lee BK, Choi HS, Lim SC, Lee CK, Lee MK. 2009. Effects of scoparone on dopamine biosynthesis and L-DOPA-induced cytotoxicity in PC12 cells. J Neurosci Res 87: 1929-1937.
79. Yoshida T, Mishina M. 2005. Distinct roles of calcineurin-nuclear factor of activated T-cells and protein kinase A-cAMP response element-binding protein signaling in presynaptic differentiation. J Neurosci 25: 3067-3079.
80. Zhong H, Lee D, Robeva A, Minneman KP, Plyte S, Boncristiano M, Fattori E, Galvagni F, Paccani SR, Majolini MB, Oliviero S, Ciliberto G, Telford JL, Baldari CT, Berts A, Abbott KL, Murphy TJ, Boss V, Talpade DJ, Ho AM, Jain J, Rao A, Hogan PG, Sun G, Tomita H, Shakkottai VG, Gargus JJ. 2001. Signaling pathways activated by alpha1-adrenergic receptor subtypes in PC12 cells. Life Sci 68: 2269-2276.