Neuromodulatory role of angiotensin-(1-7) in the central nervous system

Clinical Science

Volumn 125, Issue 2, 2013, Pages 57-65

  Gironacci, Mariela M ^a   Longo Carbajosa, Nadia A ^a   Goldstein, Jorge ^a   Cerrato, Bruno D ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Angiotensin (1 7); Hypertension; Mas receptor; Noradrenaline (norepinephrine); Synapse; Tyrosine hydroxylase

Indexed keywords

ANGIOTENSIN[1-7]; GLUTAMIC ACID; NORADRENALIN; SUBSTANCE P; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; ANGIOTENSIN I; ANGIOTENSIN I (1 7); ANGIOTENSIN I (1-7); G PROTEIN COUPLED RECEPTOR; ONCOPROTEIN; PEPTIDE FRAGMENT; PROTO ONCOGENE PROTEINS C MAS 1; PROTO-ONCOGENE PROTEINS C-MAS-1;

ARTICLE; BLOOD PRESSURE REGULATION; CARDIOVASCULAR EFFECT; CARDIOVASCULAR FUNCTION; CENTRAL NERVOUS SYSTEM; DRUG MECHANISM; HEART RATE; HUMAN; NEUROMODULATION; NEUROPROTECTION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPTIC TRANSMISSION; VASODILATATION; ANIMAL; METABOLISM; REVIEW; SYNAPSE;

ANGIOTENSIN I; ANIMALS; CENTRAL NERVOUS SYSTEM; HUMANS; NEUROTRANSMITTER AGENTS; PEPTIDE FRAGMENTS; PROTO-ONCOGENE PROTEINS; RECEPTORS, G-PROTEIN-COUPLED; SYNAPSES;

MLCS; MLOWN;

EID: 84878087757     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20120652     Document Type: Article

References (85)

1. Wright, J. W. and Harding, J. W. (2011) Brain renin-angiotensin: a new look at an old system. Prog. Neurobiol. 95, 49-67
2. Sigmund, C. D. (2012) Divergent mechanism regulating fluid intake and metabolism by the brain renin-angiotensin system. Am. J. Physiol. Regul. Integr. Comp. Physiol. 302, R313-R320
3. Saavedra, J. M. (2005) Brain angiotensin II: new developments, unanswered questions and therapeutic opportunities. Cell. Mol. Neurobiol. 25, 485-512
4. Westwood, B. M. and Chappell, M. C. (2012) Divergent pathways for the angiotensin-(1-12) metabolism in the rat circulation and kidney. Peptides 35, 190-195
5. Arakawa, H., Kawabe, K. and Sapru, H. N. (2013) Angiotensin-(1-12) in the rostral ventrolateral medullary pressor area of the rat elicits sympathoexcitatory responses. Exp. Physiol. 98, 94-108
6. Ohishi, M., Yamamoto, K. and Rakugi, H. (2012) Angiotensin (1-7) and other angiotensin peptide. Curr. Pharm. Des., in the press
7. Ferrario, C. M., Ahmad, S., Joyner, J. and Varagic, J. (2010) Advances in the renin angiotensin system focus on angiotensin-converting enzyme 2 and angiotensin-(1-7). Adv. Pharmacol. 59, 197-233
8. Ferreira, A. J., Santos, R. A. S., Bradford, C. N., Mecca, C. N., Sumners, C., Katovich, M. J. and Raizada, M. K. (2010) Therapeutic implications of the vasoprotective axis of the renin-angiotensin system in cardiovascular diseases. Hypertension 55, 207-213
9. Karamyan, V. T. and Speth, R. C. (2007) Enzymatic pathways of the brain renin-angiotensin system: unsolved problems and continuing challenges. Regul. Pept. 143, 15-27
10. Rice, G. I., Thomas, D. A., Grant, P. J., Turner, A. J. and Hooper, N. M. (2004) Evaluation of angiotensin-converting enzyme (ACE), its homologue ACE2 and neprilysin in angiotensin peptide metabolism. Biochem. J. 383, 45-51
11. Vickers, C., Hales, P., Kaushik, V., Dick, L., Gavin, J., Tang, J., Gosbouf, K., Parsons, T., Baronas, E., Hsieh, F. et al. (2002) Hydrolysis of biological peptides by human angiotensinconverting enzyme-related carboxypeptidase. J. Biol. Chem. 277, 14838-14843
12. Campagnole-Santos, M. J., Diz, D. I., Santos, R. A. S., Khosla, M. C., Brosnihan, K. B. and Ferrario, C. M. (1989) Cardiovascular effects of angiotensin-(1-7) injected into the dorsal medulla of rats. Am. J. Physiol. 257, H324-H329
13. Felix, D., Khosla, M. C., Barnes, K. L., Imboden, H., Montani, B. and Ferrario, C. M. (1991) Neurophysiological responses to angiotensin-(1-7). Hypertension 17, 1111-1114
14. Barnes, K. L., Knowles, W. D. and Ferrario, C. M. (1990) Angiotensin II and angiotensin-(1-7) excite neurons in the canine medulla in vitro. Brain Res. Bull. 24, 275-280
15. Schiavone, M. T., Santos, R. A. S., Brosnihan, K. B., Khosla, M. C. and Ferrario, C. M. (1988) Release of vasopressin from the rat hypothalamo-neurohypophysial system by angiotensin-(1-7) heptapeptide. Proc. Natl. Acad. Sci. U.S.A, 85, 4095-4098
16. Bomtempo, C. A. S., Santos, C. F. P., Santos, R. A. S. and Campagnole-Santos, M. J. (1998) Interaction of bradykinin and angiotensin-(1-7) in the central modulation of the baroreflex control of the heart rate. J. Hypertens. 16, 1797-1804
17. Chaves, G. Z., Caligiorne, S. M., Santos, R. A., Khosla, M. C. and Campagnole-Santos, M. J. (2000) 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
18. Kar, S., Gao, L., Belatti, D. A., Curry, P. L. and Zucker, I. H. (2011) Central angiotensin (1-7) enhances baroreflex gain in conscious rabbits with heart failure. Hypertension 58, 627-634
19. Sakima, A., Averill, D. B., Gallagher, P. E., Kasper, S. O., Tommasi, E. N., Ferrario, C. M. and Diz, D. I. (2005) Impaired heart rate baroreflex in older rats: role of endogenous angiotensin-(1-7) at the nucleus tractus solitarii. Hypertension 46, 333-340
20. Xiao, L., Gao, L., Lazartigues, E. and Zucker, I. H. (2011) Brain-selective overexpression of angiotensin-converting enzyme
21. attenuates sympathetic nerve activity and enhances baroreflex function in chronic heart failure. Hypertension 58, 1057-1065
22. Diz, D. I., Garcia-Espinosa, M. A., Gegick, S., Tommasi, E. N., Ferrario, C. M., Tallant, A. E., Chappell, M. C. and Gallagher, P. E. (2008) Injections of angiotensin-converting enzyme 2 inhibitor MLN4760 into nucleus tractus solitarii reduce baroreceptor reflex sensitivity for heart rate control in rats. Exp. Physiol. 93, 694-700
23. Heringer-Walther, S., Batista, E. N., Walther, T., Khosla, M. C., Santos, R. A. S. and Campagnole-Santos, M. J. (2001) Baroreflex improvement in SHR after ACE inhibition involves angiotensin-(1-7). Hypertension 37, 1309-1314
24. Britto, R. R., Santos, R. A. S., Fagundes-Moura, C. R., Khosla, M. C. and Campagnole-Santos, M. J. (1997) Role of angiotensin-(1-7) in the modulation of the baroreflex in renovascular hypertensive rats. Hypertension 30, 549-556
25. Guimaraes, P. S., Santiago, N. M., Xavier, C. H., Velloso, E. P., Fontes, M. A., Santos, R. A. and Campagnole-Santos, M. J. (2012) Chronic infusion of angiotensin-(1-7) into the lateral ventricle of the brain attenuates hypertension in DOCA-salt rats. Am. J. Physiol. Heart Circ. Physiol. 303, H393-H400
26. Silva, L. C. S., Fontes, M. A. P., Campagnole-Santos, M. J., Khosla, M. C., Campos, Jr, R. R., Guertzenstein, P. G. and Santos, R. A. S. (1993) Cardiovascular effects produced by micro-injection of angiotensin-(1-7) on vasopressor and vasodepressor sites of the ventrolateral medulla. Brain Res. 613, 321-325
27. Fontes, M. A. P., Silva, L. C. S., Campagnole-Santos, M. J., Khosla, M. C., Guertzenstein, P. G. and Santos, R. A. S. (1994) 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
28. Ferreira, P. M., Alzamora, A. C., Santos, R. A. and Campagnole-Santos, M. J. (2008) Hemodynamic effect produced by microinjection of angiotensins at the caudal ventrolateral medulla of spontaneously hypertensive rats. Neuroscience 151, 1208-1216
29. Ambuhl, P., Felix, D., Imboden, H., Khosla, M. C. and Ferrario, C. M. (1992) Effects of angiotensin analogues and angiotensin receptors antagonists on paraventricular neurons. Regul. Pept. 38, 111-120
30. Ambuhl, P., Felix, D. and Khosla, M. C. (1994) [7-D-Ala]-Angiotensin-(1-7): selective antagonism of angiotensin-(1-7) in the rat paraventricular nucleus. Brain Res. Bull. 35, 289-291
31. Gomez da Silva, A. Q., Santos, R. A. S. and Peliky Fontes, M. A. (2005) Blockade of endogenous angiotensin-(1-7) in the hypothalamic paraventricular nucleus reduces renal sympathetic tone. Hypertension 46, 341-348
32. Ḧocht, C., Gironacci, M. M., Mayer, M. A., Schuman, M., Bertera, F. M. and Taira, C. A. (2008) Involvement of angiotensin-(1-7) in the hypothalamic hypotensive effect of captopril in sinoaortic denervated rats. Regul. Pept. 146, 58-66
33. Silva, A. Q., Santos, R. A. and Fontes, M. A. (2005) Blockade of endogenous angiotensin-(1-7) in the hypothalamic paraventricular nucleus reduces renal sympathetic tone. Hypertension 46, 341-348
34. Gomes da Silva, A. Q., Xavier, C. H., Campagnole-Santos, M. J., Caligiorne, S. M., Baltatu, O. C., Bader, M., Santos, R. A. and Fontes, M. A. (2012) Cardiovascular responses evoked by activation or blockade of GABAA receptors in the hypothalamic PVN are attenuated in transgenic rats with low brain angiotensinogen. Brain Res. 1448, 101-110
35. Cerrato, B. D., Frasch, A. P., Nakagawa, P., Longo-Carbajosa, N., Pena, C., Ḧocht, C. and Gironacci, M. M. (2012) Angiotensin-(1-7) upregulates central nitric oxide synthase in spontaneously hypertensive rats. Brain Res. 1453, 1-7
36. Alzamora, A. C., Santos, R. A. and Campagnole-Santos, M. J. (2002) Hypotensive effect of ANGII and ANG-(1-7) at the caudal ventrolateral medulla involves different mechanisms. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283, R1187-R1195
37. Yang, R. F., Yin, J. X., Li, Y. L., Zimmerman, M. C. and Schultz, H. D. (2011) Angiotensin-(1-7) increases neuronal potassium current via a nitric oxide-dependent mechanism. Am. J. Physiol. Cell Physiol. 300, C58-C64
38. Feng, Y., Xia, H, Cai, Y., Halabi, C. M., Becker, L. K., Santos, R. A., Speth, R. C., Sigmund, C. D. and Lazartigues, E. (2010) Brain-selective overexpression of human angiotensin-converting enzyme type 2 attenuates neurogenic hypertension. Circ. Res. 106, 373-382
39. Zhou, L., Shi, Z., Gao, J., Han, Y., Yuan, N., Gao, X. and Zhu, G. (2010) Angiotensin-(1-7) and angiotensin II in the rostral ventrolateral medulla modulate the cardiac sympathetic afferent reflex and sympathetic activity in rats. Pflugers Arch. 459, 681-688
40. Nakagaki, T., Hirooka, Y., Ito, K., Kishi, T., Hoka, S. and Sunagawa, K. (2011) Role of angiotensin-(1-7) in rostral ventrolateral medulla in blood pressure regulation via sympathetic nerve activity in Wistar-Kyoto and spontaneous hypertensive rats. Clin. Exp. Hypertens. 33, 223-230
41. Potts, P. D., Horiuchi, J., Coleman, M. J. and Dampney, R. A. (2000) The cardiovascular effects of angiotensin-(1-7) in the rostral and caudal ventrolateral medulla of the rabbit. Brain Res. 877, 58-64
42. Jiang, T., Gao, L., Shi, J., Lu, J., Wang, Y. and Zhang, Y. (2012) Angiotensin-(1-7) modulates renin-angiotensin system associated with reducing oxidative stress and attenuating neuronal apoptosis in the brain of hypertensive rats. Pharmacol. Res. 67, 84-93
43. Ḧocht, C., Opezzo, J. A., Gironacci, M. M., Pena, C. and Taira, C. A. (2006) Hypothalamic cardiovascular effects of angiotensin-(1-7) in spontaneously hypertensive rats. Regul. Pept. 135, 39-44
44. Feng, Y., Yue, X., Xia, H., Bindom, S. M., Hickman, P. J., Filipeanu, C. M., Wu, G. and Lazartigues, E. (2008) Angiotensin-converting enzyme 2 overexpression in the subfornical organ prevents the angiotensin II-mediated pressor and drinking responses and is associated with angiotensin II type 1 receptor downregulation. Circ. Res. 102, 729-736
45. Mecca, A. P., Regenhardt, R. W., O'Connor, T. E., Joseph, J. P., Raizada, M. K., Katovich, M. J. and Sumners, C. (2011) Cerebroprotection by angiotensin-(1-7) in endothelin-1-induced ischaemic stroke. Exp. Physiol. 96, 1084-1096
46. O'Brien, A. D. and Kaper, J. B. (1998) Shiga toxin-producing Escherichia coli: yesterday, today, and tomorrow. In: Escherichia coli O157:H7 and Other ShigaToxin-Producing E. coli Strains (Kaper, J. B. and O'Brien, A. D., eds), pp. 1-11, American Society for Microbiology, Washington, DC.
47. Goldstein, J., Loidl, C. F., Creydt, V. P., Boccoli, J. and Ibarra, C. (2007) Intracerebroventricular administration of Shiga toxin type 2 induces striatal neuronal death and glial alterations: an ultrastructural study. Brain Res. 1161, 106-115
48. Hellner, K., Walther, T., Schubert, M. and Albrecht, D. (2005) Angiotensin-(1-7) enhances LTP in the hippocampus through the G-protein-coupled receptor Mas. Mol. Cell. Neurosci. 29, 427-435
49. Albrecht, D. (2007) Angiotensin-(1-7)-induced plasticity changes in the lateral amygdala are mediated by COX-2 and NO. Learn. Mem. 14, 177-184
50. Lazaroni, T. L., Raslan, A. C., Fontes, W. R., de Oliveira, M. L., Bader, M., Alenina, N., Moraes, M. F., Dos Santos, R. A. and Pereira, G. S. (2012) Angiotensin-(1-7)/Mas axis integrity is required for the expression of object recognition memory. Neurobiol. Learn. Mem. 97, 113-1223
51. Poyner, D. R., Hawkins, P. T., Benton, H. P. and Hanley, M. R. (1990) Changes in inositol lipids and phosphates after stimulation of the MAS-transfected NG115-401L-C3 cell line by mitogenic and non-mitogenic stimuli. Biochem. J. 271, 605-611
52. Santos, R. A. S., Simoes e Silva, A. C., Maric, C., Silva, D. M. R., Machado, R. P., de Buhr, I., Heringer-Walther, S., Pinheiro, S. V., Lopes, M. T., Bader, M. et al. (2003) Angiotensin-(1-7) is an endogenous ligand for the G protein-coupled receptor Mas. Proc. Natl. Acad. Sci. U.S.A. 100, 8258-8263
53. Becker, L. K., Etelvino, G. M., Walther, T., Santos, R. A. S. and Campagnole-Santos, M. J. (2007) Immunofluorescence localization of the receptor mas in cardiovascular-related areas of the rat brain. Am. J. Physiol. Heart Circ. Physiol. 293, H1416-H1424
54. Lopez Verrilli, M. A., Fermeṕi{dotless}n, M., Longo, N., Landa, S, Cerrato, B. D., Garći{dotless}a, S., Fernandez, B. E. and Gironacci, M. M. (2012) Angiotensin-(1-7) through Mas receptor upregulates neuronal norepinephrine transporter via Akt and Erk1/2-dependent pathways. J. Neurochem. 120, 46-55
55. Gironacci, M. M., Ferńandez-Toḿe, M. C., Speziale, E., Sterin-Speziale, N. and Pena, C. (2002) Angiotensin-(1-7) enhances phosphatidylcholine biosynthesis in the rat renal cortex. Biochem. Pharmacol. 63, 507-514
56. Muthalif, M. M., Benter, I. F., Uddin, M. R., Harper, J. L. and Malik, K. U. (1998) Signal transduction mechanisms involved in angiotensin-(1-7)-stimulated arachidonic acid release and prostanoid synthesis in rabbit aortic smooth muscle cells. J. Pharmacol. Exp. Ther. 284, 388-398
57. Gironacci, M. M., Adamo, H. P., Corradi, G., Santos, R. A. S., Ortiz, P. and Carretero, O. A. (2011) Angiotensin-(1-7) induces Mas receptor internalization. Hypertension 58, 176-81
58. Clark, M. A., Diz, D. I. and Tallant, E. A. (2001) Angiotensin-(1-7) downregulates the angiotensin II type 1 receptor in vascular smooth muscle cells. Hypertension 37, 1141-1146
59. Diz, D. I. and Ferrario, C. M. (1996) Angiotensin receptor heterogeneity in the dorsal medulla oblongata as defined by angiotensin-(1-7). In Recent Advances in Cellular and Molecular Aspects of Angiotensin Receptors (Raizada, M. K., ed.), pp. 225-235, Plenum Press, New York
60. Diz, D. I. and Ferrario, C. M. (1996) Angiotensin receptor heterogeneity in the dorsal medulla oblongata as defined by angiotensin-(1-7). Adv. Exp. Med. Biol. 396, 225-235
61. Jaiswal, N., Tallant, E. A., Diz, D. I., Khosla, M. C. and Ferrario, C. M. (1991) Subtype 2 angiotensin receptors mediate prostaglandin synthesis in human astrocytes. Hypertension 17, 1115-1120
62. Pereyra-Alfonso, S., Rodŕi{dotless}guez de Lores Arnaiz, G. and Pena, C. (2007) Phosphoinositide hydrolysis increase by angiotensin-(1-7) in neonatal rat brain. Regul. Pept. 140, 162-167
63. Gironacci, M. M., Vatta, M., Rodriguez-Fermepin, M., Fernandez, B. E. and Pena, C. (2000) Angiotensin-(1-7) reduces norepinephrine release through a nitric oxide mechanism in rat hypothalamus. Hypertension 35, 1248-1252
64. Gironacci, M. M., Valera, M. S., Yujnovsky, I. and Pena, C. (2004) Angiotensin-(1-7) inhibitory mechanism of norepinephrine release in hypertensive rats. Hypertension 44, 783-787
65. Lopez Verrilli, M. A., Pirola, C. J., Pascual, M. M., Dominici, F. P., Turyn, D. and Gironacci, M. M. (2009) Angiotensin-(1-7) through AT receptors mediates tyrosine hydroxylase degradation via the ubiquitin-proteasome pathway. J. Neurochem. 109, 326-335
66. Singewald, N. and Philippu, A. (1996) Involvement of biogenic amines and amino acids in the central regulation of cardiovascular homeostasis. Trends Pharmacol. Sci. 17, 356-363
67. De Wardener, H. E. (2001) The hypothalamus and hypertension. Physiol. Rev. 81, 1599-1658
68. Wyss, J. M. and Carlson, S. H. (1999) The role of the central nervous system in hypertension. Curr. Hypertens. Rep. 1, 246-53
69. Dampney, R. A. L., Horiuchi, H., Killinger, S., Sheriff, M. F., Tan, P. S. P. and McDowall, L. M. (2005) Long-term regulation of arterial blood pressure by hypothalamic nuclei: some critical questions. Clin. Exp. Pharmacol. Physiol. 32, 419-425
70. Veersingham, S. J. and Raizada, M. K. (2003) Brain reninangiotensin system in hypertension. Br. J. Pharmacol. 139, 191-202
71. Gironacci, M. M., Adler-Graschinsky, E., Pena, C. and Enero, M. A. (1994) Effects of angiotensin II and angiotensin-(1-7) on the release of [3H]norepinephrine from rat atria. Hypertension 24, 457-460
72. Gironacci, M. M., Lorenzo, P. and Adler-Graschinsky, E. (1997) Possible participation of nitric oxide in the increase of noradrenaline release caused by angiotensin peptides in rat atria. Hypertension 29, 1344-1350
73. Gironacci, M. M., Yujnovsky, I., Gorzalczany, S., Taira, C. and Pena, C. (2004) Angiotensin-(1-7) inhibits the angiotensin II-enhanced norepinephrine release in coarcted hypertensive rats. Regul. Pept. 118, 45-49
74. Feng, Y., Hans, C., McIlwain, E., Varner, K. J. and Lazartigues, E. (2012) Angiotensin-converting enzyme 2 over-expression in the central nervous system reduces angiotensin-II-mediated cardiac hypertrophy. PLoS ONE 7, e48910
75. Fujisawa, H. and Okuno, S. (2005) Regulatory mechanisms of tyrosine hydroxylase. Biochem. Biophys. Res. Comun. 338, 271-276
76. Kravtsova-Ivantsiv, Y. and Ciechanover, A. (2012) Non-canonical ubiquitin-based signals for proteasomal degradation. J. Cell Sci. 125, 539-548
77. Segref, A. and Hoppe, T. (2009) Think locally: control of ubiquitin-dependent protein degradation in neurons. EMBO Rep. 10, 44-50
78. B̈onisch, H. and Br̈uss, M. (2006) The norepinephrine transporter in physiology and disease. Handb. Exp. Pharmacol. 175, 485-524
79. Kvetnansky, R., Sabban, E. L. and Palkovits, M. (2009) Catecholaminergic systems in stress: structural and molecular genetic approaches. Physiol. Rev. 89, 535-606
80. Schlaich, M. P., Lambert, E., Kaye, D. M., Krozowski, Z., Campbell, D. J., Lambert, G., Hastings, J., Aggarwal, A. and Ester, M. D. (2004) Sympathetic augmentation in hypertension: role of nerve firing, norepinephrine reuptake, and angiotensin neuromodulation. Hypertension 43, 169-75
81. Helke, C. J., Goldman, W. and Jacobowitz, D. M. (1980) Demonstration of substance P in aortic nerve afferent fibers by combined use of fluorescent retrograde neuronal labeling and immunohistochemistry. Peptides 1, 359-364
82. Diz, D. I., Jessup, J. A., Westwood, B. M., Bosch, S. M., Vinsant, S., Gallagher, P. E. and Averill, D. B. (2002) Angiotensin peptides as neurotransmitters/neuromodulators in the dorsomedial medulla. Clin. Exp. Pharmacol. Physiol. 29, 473-482
83. Diz, D. I. and Pirro, N. T. (1992) Differential actions of angiotensin II and angiotensin-(1-7) on transmitter release. Hypertension 19 (Suppl. II), II-41-II-48
84. Kubo, T., Amano, M., Ishizuka, T. and Ozaki, S. (1993) Beta-alanine and taurine microinjected into the rat caudal ventrolateral medulla increase blood pressure. Clin. Exp. Hypertens. 15, 585-597
85. Wang, J., Peng, Y. J. and Zhu, D. N. (2005) Amino acids modulate the hypotensive effect of angiotensin-(1-7) at the caudal ventrolateral medulla in rats. Regul. Pept. 129, 1-7