Regulation of catecholamine release and tyrosine hydroxylase in human adrenal chromaffin cells by interleukin-1β: Role of neuropeptide y and nitric oxide

Journal of Neurochemistry

Volumn 109, Issue 3, 2009, Pages 911-922

  Rosmaninho Salgado, Joana ^a   Araújo, Inês M ^a   Álvaro, Ana Rita ^a   Mendes, Alexandrina F ^a,b   Ferreira, Lígia ^a   Grouzmann, Eric ^c   Mota, Alfredo ^d   Duarte, Emília P ^a,e   Cavadas, Cláudia ^a,b  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^d Hospital Center Coimbra   (Portugal)

^e UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Catecholamine; Human chromaffin cells; Interleukin 1 ; Neuropeptide Y; Nitric oxide; Tyrosine hydroxylase

Indexed keywords

ADRENALIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYTOKINE; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE; NEUROPEPTIDE Y; NEUROPEPTIDE Y3 RECEPTOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NORADRENALIN; PROTEIN KINASE C; TYROSINE 3 MONOOXYGENASE;

ARTICLE; CATECHOLAMINE RELEASE; CATECHOLAMINE SYNTHESIS; CHROMAFFIN CELL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ADRENAL GLANDS; ANALYSIS OF VARIANCE; ANTIBODIES; CATECHOLAMINES; CELLS, CULTURED; CHROMAFFIN CELLS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; HUMANS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1BETA; NEUROPEPTIDE Y; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; SIGNAL TRANSDUCTION; TIME FACTORS; TYROSINE 3-MONOOXYGENASE;

EID: 64149092206     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06023.x     Document Type: Article

References (72)

1. Ait-Ali D., Turquier V., Grumolato L., Yon L., Jourdain M., Alexandre D., Eiden L. E., Vaudry H. Anouar Y. (2004) The proinflammatory cytokines tumor necrosis factor-alpha and interleukin-1 stimulate neuropeptide gene transcription and secretion in adrenochromaffin cells via activation of extracellularly regulated kinase 1/2 and p38 protein kinases, and activator protein-1 transcription factors. Mol. Endocrinol., 18, 1721 1739.
2. Albert K. A., Helmer-Matyjek E., Nairn A. C., Muller T. H., Haycock J. W., Greene L. A., Goldstein M. Greengard P. (1984) Calcium/phospholipid- dependent protein kinase (protein kinase C) phosphorylates and activates tyrosine hydroxylase. Proc. Natl. Acad. Sci. USA, 81, 7713 7717.
3. Alvaro A. R., Martins J., Araujo I. M., Rosmaninho-Salgado J., Ambrosio A. F. Cavadas C. (2008) Neuropeptide Y stimulates retinal neural cell proliferation - involvement of nitric oxide. J. Neurochem. 105, 2501 2510.
4. Andersson C., Svenson S. B., Van Deventer S., Cerami A. Bartfai T. (1992) Interleukin-1 alpha expression is inducible by cholinergic stimulation in the rat adrenal gland. Neuroscience, 47, 481 485.
5. Arend W. P. (1993) Interleukin-1 receptor antagonist. Adv. Immunol., 54, 167 227.
6. Arend W. P. (2002) The balance between IL-1 and IL-1Ra in disease. Cytokine Growth Factor Rev., 13, 323 340.
7. Arend W. P. Gabay C. (2000) Physiologic role of interleukin-1 receptor antagonist. Arthritis Res, 2, 245 248.
8. Barnea A., Roberts J., Keller P. Word R. A. (2001) Interleukin-1beta induces expression of neuropeptide Y in primary astrocyte cultures in a cytokine-specific manner: induction in human but not rat astrocytes. Brain Res., 896, 137 145.
9. Bobrovskaya L., Cheah T. B., Bunn S. J. Dunkley P. R. (1998) Tyrosine hydroxylase in bovine adrenal chromaffin cells: angiotensin II-stimulated activity and phosphorylation of Ser19, Ser31, and Ser40. J. Neurochem., 70, 2565 2573.
10. Bobrovskaya L., Odell A., Leal R. B. Dunkley P. R. (2001) Tyrosine hydroxylase phosphorylation in bovine adrenal chromaffin cells: the role of MAPKs after angiotensin II stimulation. J. Neurochem., 78, 490 498.
11. Bobrovskaya L., Dunkley P. R. Dickson P. W. (2004) Phosphorylation of Ser19 increases both Ser40 phosphorylation and enzyme activity of tyrosine hydroxylase in intact cells. J. Neurochem., 90, 857 864.
12. Bobrovskaya L., Gelain D. P., Gilligan C., Dickson P. W. Dunkley P. R. (2007) PACAP stimulates the sustained phosphorylation of tyrosine hydroxylase at serine 40. Cell. Signal., 19, 1141 1149.
13. Bradford M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248 254.
14. Bredt D. S., Hwang P. M. Snyder S. H. (1990) Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature, 347, 768 770.
15. Cahill A. L., Horwitz J. Perlman R. L. (1989) Phosphorylation of tyrosine hydroxylase in protein kinase C-deficient PC12 cells. Neuroscience, 30, 811 818.
16. Cammarota M., Bevilaqua L. R., Rostas J. A. Dunkley P. R. (2003) Histamine activates tyrosine hydroxylase in bovine adrenal chromaffin cells through a pathway that involves ERK1/2 but not p38 or JNK. J. Neurochem., 84, 453 458.
17. Cannon J. G., Tompkins R. G., Gelfand J. A. et al. (1990) Circulating interleukin-1 and tumor necrosis factor in septic shock and experimental endotoxin fever. J. Infect. Dis., 161, 79 84.
18. Cannon J. G., Friedberg J. S., Gelfand J. A., Tompkins R. G., Burke J. F. Dinarello C. A. (1992) Circulating interleukin-1 beta and tumor necrosis factor-alpha concentrations after burn injury in humans. Crit. Care Med., 20, 1414 1419.
19. Cavadas C., Silva A. P., Mosimann F., Cotrim M. D., Ribeiro C. A., Brunner H. R. Grouzmann E. (2001) NPY regulates catecholamine secretion from human adrenal chromaffin cells. J. Clin. Endocrinol. Metab., 86, 5956 5963.
20. Cavadas C., Cefai D., Rosmaninho-Salgado J. et al. (2006) Deletion of the NPY Y1 receptor gene reveals a regulatory role of neuropeptide Y on catecholamine synthesis and secretion. PNAS, 103, 10497 10502.
21. Chi D. S., Fitzgerald S. M., Pitts S., Cantor K., King E., Lee S. A., Huang S. K. Krishnaswamy G. (2004) MAPK-dependent regulation of IL-1- and beta-adrenoreceptor-induced inflammatory cytokine production from mast cells: implications for the stress response. BMC Immunol, 5, 22.
22. Corbitt J., Vivekananda J., Wang S. S. Strong R. (1998) Transcriptional and posttranscriptional control of tyrosine hydroxylase gene expression during persistent stimulation of pituitary adenylate cyclase-activating polypeptide receptors on PC12 cells: regulation by protein kinase A-dependent and protein kinase A-independent pathways. J. Neurochem., 71, 478 486.
23. Cox M. E. Parsons S. J. (1997) Roles for protein kinase C and mitogen-activated protein kinase in nicotine-induced secretion from bovine adrenal chromaffin cells. J. Neurochem., 69, 1119 1130.
24. Currie K. P., Zhou Z. Fox A. P. (2000) Evidence for paracrine signaling between macrophages and bovine adrenal chromaffin cell Ca(2+) channels. J. Neurophysiol., 83, 280 287.
25. Dinarello C. A. (1991) Interleukin-1 and interleukin-1 antagonism. Blood, 77, 1627 1652.
26. Dinarello C. A. (1995) Interleukin-1 and interleukin-1 receptor antagonist. Nutrition, 11, 492 494.
27. Dunkley P. R., Bobrovskaya L., Graham M. E., von Nagy-Felsobuki E. I. Dickson P. W. (2004) Tyrosine hydroxylase phosphorylation: regulation and consequences. J. Neurochem., 91, 1025 1043.
28. Eastgate J. A., Symons J. A., Wood N. C., Grinlinton F. M., di Giovine F. S. Duff G. W. (1988) Correlation of plasma interleukin 1 levels with disease activity in rheumatoid arthritis. Lancet, 2, 706 709.
29. Engelman K., Horwitz D., Jequier E. Sjoerdsma A. (1968a) Biochemical and pharmacologic effects of alpha-methyltyrosine in man. J. Clin. Invest., 47, 577 594.
30. Engelman K., Jequier E., Udenfriend S. Sjoerdsma A. (1968b) Metabolism of alpha-methyltyrosine in man: relationship to its potency as an inhibitor of catecholamine biosynthesis. J. Clin. Invest., 47, 568 576.
31. Ferrer M., Sanchez M., Martin Mdel C., Marquez-Rodas I., Alonso M. J., Salaices M. Balfagon G. (2004) Protein kinase A increases electrical stimulation-induced neuronal nitric oxide release in rat mesenteric artery. Eur. J. Pharmacol., 487, 167 173.
32. Gonzalez-Hernandez J. A., Bornstein S. R., Ehrhart-Bornstein M., Gschwend J. E., Gwosdow A., Jirikowski G. Scherbaum W. A. (1995) IL-1 is expressed in human adrenal gland in vivo. Possible role in a local immune-adrenal axis. Clin. Exp. Immunol., 99, 137 141.
33. Griffiths J. Marley P. D. (2001) Ca2+ -dependent activation of tyrosine hydroxylase involves MEK1. Neuroreport, 12, 2679 2683.
34. Grouzmann E., Aubert J. F., Waeber B. Brunner H. R. (1992a) A sensitive and specific two-site, sandwich-amplified enzyme immunoassay for neuropeptide Y. Peptides, 13, 1049 1054.
35. Grouzmann E., Comoy E., Walker P., Burnier M., Bohuon C., Waeber B. Brunner H. (1992b) Production and characterization of four anti-neuropeptide Y monoclonal antibodies. Hybridoma, 11, 409 424.
36. Haycock J. W. (1990) Phosphorylation of tyrosine hydroxylase in situ at serine 8, 19, 31, and 40. J. Biol. Chem., 265, 11682 11691.
37. Haycock J. W. (1993) Multiple signaling pathways in bovine chromaffin cells regulate tyrosine hydroxylase phosphorylation at Ser19, Ser31, and Ser40. Neurochem. Res., 18, 15 26.
38. Kim D., Choi H. J., Kim S. W., Cho S. W. Hwang O. (2003) Upregulation of catecholamine biosynthetic enzymes by nitric oxide. J. Neurosci. Res., 72, 98 104.
39. Kobayashi H., Yanagita T., Yokoo H. Wada A. (2003) Pathophysiological function of adrenomedullin and proadrenomedullin N-terminal peptides in adrenal chromaffin cells. Hypertens. Res., 26 (Suppl S71 S78.
40. Kumakura K., Sasakawa N., Murayama N. Ohara-Imaizumi M. (2004) Spatio-temporal regulation of neurotransmitter release by PKC; studies in adrenal chromaffin cells. Crit. Rev. Neurobiol., 16, 173 179.
41. Kumer S. C. Vrana K. E. (1996) Intricate regulation of tyrosine hydroxylase activity and gene expression. J. Neurochem., 67, 443 462.
42. Lehmann I. T., Bobrovskaya L., Gordon S. L., Dunkley P. R. Dickson P. W. (2006) Differential regulation of the human tyrosine hydroxylase isoforms via hierarchical phosphorylation. J. Biol. Chem., 281, 17644 17651.
43. Liu Y., Liu T., McCarron R. M., Spatz M., Feuerstein G., Hallenbeck J. M. Siren A. L. (1996) Evidence for activation of endothelium and monocytes in hypertensive rats. Am. J. Physiol., 270, H2125 H2131.
44. Machado J. D., Morales A., Gomez J. F. Borges R. (2001) cAmp modulates exocytotic kinetics and increases quantal size in chromaffin cells. Mol. Pharmacol., 60, 514 520.
45. Marley P. D., McLeod J., Anderson C. Thomson K. A. (1995) Nerves containing nitric oxide synthase and their possible function in the control of catecholamine secretion in the bovine adrenal medulla. J. Auton. Nerv. Syst., 54, 184 194.
46. McMahan C. J., Slack J. L., Mosley B. et al. (1991) A novel IL-1 receptor, cloned from B cells by mammalian expression, is expressed in many cell types. EMBO J., 10, 2821 2832.
47. McNeill B. Perry S. F. (2005) Nitric oxide and the control of catecholamine secretion in rainbow trout Oncorhynchus mykiss. J. Exp. Biol., 208, 2421 2431.
48. Michell B. J., Chen Z., Tiganis T., Stapleton D., Katsis F., Power D. A., Sim A. T. Kemp B. E. (2001) Coordinated control of endothelial nitric-oxide synthase phosphorylation by protein kinase C and the cAMP-dependent protein kinase. J. Biol. Chem., 276, 17625 17628.
49. Morita K., Dohi T., Kitayama S., Koyama Y. Tsujimoto A. (1987) Enhancement of stimulation-evoked catecholamine release from cultured bovine adrenal chromaffin cells by forskolin. J. Neurochem., 48, 243 247.
50. Nussdorfer G. G. Malendowicz L. K. (1998) Role of VIP, PACAP, and related peptides in the regulation of the hypothalamo-pituitary-adrenal axis. Peptides, 19, 1443 1467.
51. Ohlsson K., Bjork P., Bergenfeldt M., Hageman R. Thompson R. C. (1990) Interleukin-1 receptor antagonist reduces mortality from endotoxin shock. Nature, 348, 550 552.
52. Oset-Gasque M. J., Parramon M., Hortelano S., Bosca L. Gonzalez M. P. (1994) Nitric oxide implication in the control of neurosecretion by chromaffin cells. J. Neurochem., 63, 1693 1700.
53. Oset-Gasque M. J., Vicente S., Gonzalez M. P., Rosario L. M. Castro E. (1998) Segregation of nitric oxide synthase expression and calcium response to nitric oxide in adrenergic and noradrenergic bovine chromaffin cells. Neuroscience, 83, 271 280.
54. Ping P., Takano H., Zhang J. et al. (1999) Isoform-selective activation of protein kinase C by nitric oxide in the heart of conscious rabbits: a signaling mechanism for both nitric oxide-induced and ischemia-induced preconditioning. Circ. Res., 84, 587 604.
55. Prieto I., Jimenez F., Aller M. A., Nava M. P., Vara E., Garcia C. Arias J. (2005) Tumor necrosis factor-alpha, interleukin-1beta and nitric oxide: induction of liver megamitochondria in prehepatic portal hypertensive rats. World J. Surg., 29, 903 908.
56. Rodriguez-Pascual F., Ferrero R., Miras-Portugal M. T. Torres M. (1999) Phosphorylation of tyrosine hydroxylase by cGMP-dependent protein kinase in intact bovine chromaffin cells. Arch. Biochem. Biophys., 366, 207 214.
57. Rosmaninho-Salgado J., Alvaro A. R., Grouzmann E., Duarte E. P. Cavadas C. (2007a) Neuropeptide Y regulates catecholamine release evoked by interleukin-1beta in mouse chromaffin cells. Peptides, 28, 310 314.
58. Rosmaninho-Salgado J., Araujo I. M., Alvaro A. R., Duarte E. P. Cavadas C. (2007b) Intracellular signaling mechanisms mediating catecholamine release upon activation of NPY Y1 receptors in mouse chromaffin cells. J. Neurochem., 103, 896 903.
59. Saklatvala J., Rawlinson L. M., Marshall C. J. Kracht M. (1993) Interleukin 1 and tumour necrosis factor activate the mitogen-activated protein (MAP) kinase kinase in cultured cells. FEBS Lett., 334, 189 192.
60. Schultzberg M., Andersson C., Unden A., Troye-Blomberg M., Svenson S. B. Bartfai T. (1989) Interleukin-1 in adrenal chromaffin cells. Neuroscience, 30, 805 810.
61. Schwarz P. M., Rodriguez-Pascual F., Koesling D., Torres M. Forstermann U. (1998) Functional coupling of nitric oxide synthase and soluble guanylyl cyclase in controlling catecholamine secretion from bovine chromaffin cells. Neuroscience, 82, 255 265.
62. Tanaka K. Chiba T. (1996) Ultrastructural localization of nerve terminals containing nitric oxide synthase in rat adrenal gland. Neurosci. Lett., 204, 153 156.
63. Taylor S. C., Green K. N., Carpenter E. Peers C. (2000) Protein kinase C evokes quantal catecholamine release from PC12 cells via activation of L-type Ca2+ channels. J. Biol. Chem., 275, 26786 26791.
64. Terbush D. R. Holz R. W. (1990) Activation of protein kinase C is not required for exocytosis from bovine adrenal chromaffin cells. The effects of protein kinase C(19-31), Ca/CaM kinase II(291-317), and staurosporine. J. Biol. Chem., 265, 21179 21184.
65. Thomas G., Haavik J. Cohen P. (1997) Participation of a stress-activated protein kinase cascade in the activation of tyrosine hydroxylase in chromaffin cells. Eur. J. Biochem., 247, 1180 1189.
66. Torres M., Ceballos G. Rubio R. (1994) Possible role of nitric oxide in catecholamine secretion by chromaffin cells in the presence and absence of cultured endothelial cells. J. Neurochem., 63, 988 996.
67. Uciechowski P., Saklatvala J., von der Ohe J., Resch K., Szamel M. Kracht M. (1996) Interleukin 1 activates jun N-terminal kinases JNK1 and JNK2 but not extracellular regulated MAP kinase (ERK) in human glomerular mesangial cells. FEBS Lett., 394, 273 278.
68. Vicente S., Gonzalez M. P. Oset-Gasque M. J. (2002) Neuronal nitric oxide synthase modulates basal catecholamine secretion in bovine chromaffin cells. J. Neurosci. Res., 69, 327 340.
69. Vicente S., Figueroa S., Perez-Rodriguez R., Gonzalez M. P. Oset-Gasque M. J. (2005) Nitric oxide donors induce calcium-mobilisation from internal stores but do not stimulate catecholamine secretion by bovine chromaffin cells in resting conditions. Cell Calcium, 37, 163 172.
70. Virdis A. Schiffrin E. L. (2003) Vascular inflammation: a role in vascular disease in hypertension? Curr. Opin. Nephrol. Hypertens., 12, 181 187.
71. Yanagihara N., Minami K., Shirakawa F., Uezono Y., Kobayashi H., Eto S. Izumi F. (1994) Stimulatory effect of IL-1 beta on catecholamine secretion from cultured bovine adrenal medullary cells. Biochem. Biophys. Res. Commun., 198, 81 87.
72. Zhao Q., Ishibashi M., Hiasa K., Tan C., Takeshita A. Egashira K. (2004) Essential role of vascular endothelial growth factor in angiotensin II-induced vascular inflammation and remodeling. Hypertension, 44, 264 270.