Angiotensin-(1-7) increases neuronal potassium current via a nitric oxide-dependent mechanism

American Journal of Physiology - Cell Physiology

Volumn 300, Issue 1, 2011, Pages

  Yang, Rui Fang ^a   Yin, Jing Xiang ^a   Li, Yu Long ^a,b   Zimmerman, Matthew C ^a,c   Schultz, Harold D ^a,c  

^a NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

Autonomic nervous system; Differentiated catecholamine neurons; Mas receptor; Neuronal nitric oxide synthase

Indexed keywords

4 AMINO 5 METHYL AMINO 2', 7' DIFLUOROFLUORESCEIN DIACETATE; ANGIOTENSIN RECEPTOR; ANGIOTENSIN RECEPTOR MASR; ANGIOTENSIN[1-7]; ANGIOTENSIN[1-7][7 DEXTRO ALANINE]; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FLUORESCEIN DIACETATE; INHIBITORY NITRIC OXIDE SYNTHASE; L N 5 (1 IMINOETHYL) ORNITHINE; N [3 (AMINOMETHYL)BENZYL]ACETAMIDINE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; S METHYL LEVO THIOCITRULLINE; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL;

ARTICLE; CATECHOLAMINE NERVE CELL; CONTROLLED STUDY; HUMAN; HUMAN CELL; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANGIOTENSIN I; ANGIOTENSIN II; ANGIOTENSIN RECEPTOR ANTAGONISTS; ANIMALS; CELL LINE; GENE EXPRESSION REGULATION; MEMBRANE POTENTIALS; NEURONS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; PEPTIDE FRAGMENTS; POTASSIUM; PROTEIN ISOFORMS; RECEPTORS, ANGIOTENSIN; SIGNAL TRANSDUCTION;

EID: 78651375228     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00369.2010     Document Type: Article

References (45)

1. Alenina N, Bader M, Walther T. Imprinting of the murine MAS protooncogene is restricted to its antisense RNA. Biochem Biophys Res Commun 290: 1072-1078, 2002.
2. Becker LK, Etelvino GM, Walther T, Santos RA, Campagnole-Santos MJ. Immunofluorescence localization of the receptor Mas in cardiovascular-related areas of the rat brain. Am J Physiol Heart Circ Physiol 293: H1416-H1424, 2007.
3. Bolotina VM, Najibi S, Palacino JJ, Pagano PJ, Cohen RA. Nitric oxide directly activates calcium-dependent potassium channels in vascular smooth muscle. Nature 368: 850-853, 1994.
4. Campagnole-Santos MJ, Diz DI, Santos RA, Khosla MC, Brosnihan KB, Ferrario CM. Cardiovascular effects of angiotensin-(1-7) injected into the dorsal medulla of rats. Am J Physiol Heart Circ Physiol 257: H324-H329, 1989.
5. Chang AY, Chan JY, Chan SH. Differential distribution of nitric oxide synthase isoforms in the rostral ventrolateral medulla of the rat. J Biomed Sci 10: 285-291, 2003.
6. Chappell MC, Brosnihan KB, Diz DI, Ferrario CM. Identification of angiotensin-(1-7) in rat brain. Evidence for differential processing of angiotensin peptides. J Biol Chem 264: 16518-16523, 1989.
7. Chaves GZ, Caligiorne SM, Santos RA, Khosla MC, Campagnole-Santos MJ. Modulation of the baroreflex control of heart rate by angiotensin-(1-7) at the nucleus tractus solitarii of normotensive and spontaneously hypertensive rats. J Hypertens 18: 1841-1848, 2000.
8. da Costa Goncalves AC, Leite R, Fraga-Silva RA, Pinheiro SV, Reis AB, Reis FM, Touyz RM, Webb RC, Alenina N, Bader M, Santos RA. Evidence that the vasodilator angiotensin-(1-7)-Mas axis plays an important role in erectile function. Am J Physiol Heart Circ Physiol 293: H2588-H2596, 2007.
9. Feng Y, Xia H, Cai Y, Halabi CM, Becker LK, Santos RA, Speth RC, Sigmund CD, Lazartigues E. Brain-selective overexpression of human Angiotensin- converting enzyme type 2 attenuates neurogenic hypertension5. Circ Res 106: 373-382, 2010.
10. Fontes MA, Silva LC, Campagnole-Santos MJ, Khosla MC, Guertzenstein PG, Santos RA. Evidence that angiotensin-(1-7) plays a role in the central control of blood pressure at the ventro-lateral medulla acting through specific receptors. Brain Res 665: 175-180, 1994.
11. Forstermann U, Kleinert H, Gath I, Schwarz P, Closs EI, Dun NJ. Expression and expressional control of nitric oxide synthases in various cell types. Adv Pharmacol 34: 171-186, 1995.
12. Gao L, Wang W, Li YL, Schultz HD, Liu D, Cornish KG, Zucker IH. Sympathoexcitation by central ANG II: roles for AT1 receptor upregulation and NAD(P)H oxidase in RVLM. Am J Physiol Heart Circ Physiol 288: H2271-H2279, 2005.
13. Gironacci MM, Vatta M, Rodriguez-Fermepin M, Fernandez BE, Pena C. Angiotensin-(1-7) reduces norepinephrine release through a nitric oxide mechanism in rat hypothalamus. Hypertension 35: 1248-1252, 2000. (Pubitemid 30413659)
14. Gomes ER, Lara AA, Almeida PW, Guimaraes D, Resende RR, Campagnole-Santos MJ, Bader M, Santos RA, Guatimosim S. Angiotensin-(1-7) prevents cardiomyocyte pathological remodeling through a nitric oxide/guanosine 3′,5′- cyclic monophosphate-dependent pathway. Hypertension 55: 153-160, 2010.
15. Hermann A, Erxleben C. Nitric oxide activates voltage-dependent potassium currents of crustacean skeletal muscle. Nitric Oxide 5: 361-369, 2001. (Pubitemid 32735388)
16. Hirooka Y, Shigematsu H, Kishi T, Kimura Y, Ueta Y, Takeshita A. Reduced nitric oxide synthase in the brainstem contributes to enhanced sympathetic drive in rats with heart failure. J Cardiovasc Pharmacol 42, Suppl 1: S111-S115, 2003.
17. Hocht C, Gironacci MM, Mayer MA, Schuman M, Bertera FM, Taira CA. Involvement of angiotensin-(1-7) in the hypothalamic hypotensive effect of captopril in sinoaortic denervated rats. Regul Pept 146: 58-66, 2008.
18. Hocht C, Opezzo JA, Gironacci MM, Pena C, Taira CA. Hypothalamic cardiovascular effects of angiotensin-(1-7) in spontaneously hypertensive rats. Regul Pept 135: 39-44, 2006.
19. Kawano T, Zoga V, Kimura M, Liang MY, Wu HE, Gemes G, McCallum JB, Kwok WM, Hogan QH, Sarantopoulos CD. Nitric oxide activates ATP-sensitive potassium channels in mammalian sensory neurons: action by direct S-nitrosylation. Mol Pain 5: 12, 2009.
20. Kojima H, Nakatsubo N, Kikuchi K, Kawahara S, Kirino Y, Nagoshi H, Hirata Y, Nagano T. Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins. Anal Chem 70: 2446-2453, 1998.
21. Lazaroff M, Dunlap K, Chikaraishi DM. A CNS catecholaminergic cell line expresses voltage-gated currents. J Membr Biol 151: 279-291, 1996.
22. Li Y, Zhang W, Stern JE. Nitric oxide inhibits the firing activity of hypothalamic paraventricular neurons that innervate the medulla oblongata: role of GABA. Neuroscience 118: 585-601, 2003.
23. Ljubkovic M, Shi Y, Cheng Q, Bosnjak Z, Jiang MT. Cardiac mitochondrial ATP-sensitive potassium channel is activated by nitric oxide in vitro. FEBS Lett 581: 4255-4259, 2007.
24. Oliveira DR, Santos RA, Santos GF, Khosla M, Campagnole-Santos MJ. Changes in the baroreflex control of heart rate produced by central infusion of selective angiotensin antagonists in hypertensive rats. Hypertension 27: 1284-1290, 1996.
25. Patel KP, Zhang K, Zucker IH, Krukoff TL. Decreased gene expression of neuronal nitric oxide synthase in hypothalamus and brainstem of rats in heart failure. Brain Res 734: 109-115, 1996.
26. Qi Y, Wang JK, McMillian M, Chikaraishi DM. Characterization of a CNS cell line, CAD, in which morphological differentiation is initiated by serum deprivation. J Neurosci 17: 1217-1225, 1997.
27. Sakima A, Averill DB, Gallagher PE, Kasper SO, Tommasi EN, Ferrario CM, Diz DI. Impaired heart rate baroreflex in older rats: role of endogenous angiotensin-(1-7) at the nucleus tractus solitarii. Hypertension 46: 333-340, 2005.
28. Sampaio WO, Souza dos Santos RA, Faria-Silva R, da Mata Machado LT, Schiffrin EL, Touyz RM. Angiotensin-(1-7) through receptor Mas mediates endothelial nitric oxide synthase activation via Akt-dependent pathways. Hypertension 49: 185-192, 2007.
29. Santos RA, Campagnole-Santos MJ, Andrade SP. Angiotensin-(1-7): an update. Regul Pept 91: 45-62, 2000.
30. Santos RA, Ferreira AJ, Pinheiro SV, Sampaio WO, Touyz R, Campagnole-Santos MJ. Angiotensin-(1-7) and its receptor as a potential targets for new cardiovascular drugs. Expert Opin Investig Drugs 14: 1019-1031, 2005.
31. Santos RA, Frezard F, Ferreira AJ. Angiotensin-(1-7): blood, heart, and blood vessels. Curr Med Chem Cardiovasc Hematol Agents 3: 383-391, 2005.
32. Santos RA, Simoes e Silva AC, Maric C, Silva DM, Machado RP, de B, I, Heringer-Walther S, Pinheiro SV, Lopes MT, Bader M, Mendes EP, Lemos VS, Campagnole-Santos MJ, Schultheiss HP, Speth R, Walther T. Angiotensin-(1-7) is an endogenous ligand for the G protein-coupled receptor Mas. Proc Natl Acad Sci USA 100: 8258-8263, 2003.
33. Silva LC, Fontes MA, Campagnole-Santos MJ, Khosla MC, Campos RR, Jr, Guertzenstein PG, Santos RA. Cardiovascular effects produced by micro-injection of angiotensin-(1-7) on vasopressor and vasodepressor sites of the ventrolateral medulla. Brain Res 613: 321-325, 1993.
34. Sun C, Du J, Raizada MK, Sumners C. Modulation of delayed rectifier potassium current by angiotensin II in CATH.a cells. Biochem Biophys Res Commun 310: 710-714, 2003.
35. Suri C, Fung BP, Tischler AS, Chikaraishi DM. Catecholaminergic cell lines from the brain and adrenal glands of tyrosine hydroxylase-SV40 T antigen transgenic mice. J Neurosci 13: 1280-1291, 1993.
36. Thornbury KD, Ward SM, Dalziel HH, Carl A, Westfall DP, Sanders KM. Nitric oxide and nitrosocysteine mimic nonadrenergic, noncholinergic hyperpolarization in canine proximal colon. Am J Physiol Gastrointest Liver Physiol 261: G553-G557, 1991.
37. Tjong YW, Li M, Hung MW, Wang K, Fung ML. Nitric oxide deficit in chronic intermittent hypoxia impairs large conductance calcium-activated potassium channel activity in rat hippocampal neurons. Free Radic Biol Med 44: 547-557, 2008. (Pubitemid 351181263)
38. Tseng CJ, Liu HY, Lin HC, Ger LP, Tung CS, Yen MH. Cardiovascular effects of nitric oxide in the brain stem nuclei of rats. Hypertension 27: 36-42, 1996.
39. Veerasingham SJ, Raizada MK. Brain renin-angiotensin system dysfunction in hypertension: recent advances and perspectives. Br J Pharmacol 139: 191-202, 2003.
40. Xu P, Costa-Goncalves AC, Todiras M, Rabelo LA, Sampaio WO, Moura MM, Santos SS, Luft FC, Bader M, Gross V, Alenina N, Santos RA. Endothelial dysfunction and elevated blood pressure in MAS gene-deleted mice. Hypertension 51: 574-580, 2008.
41. Yang Q, Chen SR, Li DP, Pan HL. Kv1.1/1.2.channels are downstream effectors of nitric oxide on synaptic GABA release to preautonomic neurons in the paraventricular nucleus. Neuroscience 149: 315-327, 2007.
42. Yin JX, Yang RF, Li S, Renshaw AO, Li YL, Schultz HD, Zimmerman MC. Mitochondria-produced superoxide mediates angiotensin II-induced inhibition of neuronal potassium current. Am J Physiol Cell Physiol 298: C857-C865, 2010.
43. Young CN, Fisher JP, Gallagher KM, Whaley-Connell A, Chaudhary K, Victor RG, Thomas GD, Fadel PJ. Inhibition of nitric oxide synthase evokes central sympatho-excitation in healthy humans. J Physiol 587: 4977-4986, 2009.
44. Zhang Y, Lu J, Shi J, Lin X, Dong J, Zhang S, Liu Y, Tong Q. Central administration of angiotensin-(1-7) stimulates nitric oxide release and upregulates the endothelial nitric oxide synthase expression following focal cerebral ischemia/reperfusion in rats. Neuropeptides 42: 593-600, 2008.
45. Zucker IH. Novel mechanisms of sympathetic regulation in chronic heart failure. Hypertension 48: 1005-1011, 2006.