The PI3K signaling-mediated nitric oxide contributes to cardiovascular effects of angiotensin-(1-7) in the nucleus tractus solitarii of rats

Nitric Oxide - Biology and Chemistry

Volumn 52, Issue , 2016, Pages 56-65

  Wu, Zhao Tang ^a   Ren, Chang Zhen ^a   Yang, Ya Hong ^a   Zhang, Ru Wen ^a   Sun, Jia Cen ^a   Wang, Yang Kai ^a   Su, Ding Feng ^a   Wang, Wei Zhong ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Angiotensin 1 7; Nitric oxide; Nucleus tractus solitarii; PI3K signaling; shRNA

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ANGIOTENSIN[1-7]; ANGIOTENSIN[1-7][7 DEXTRO ALANINE]; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SHORT HAIRPIN RNA; TRICIRIBINE; ANGIOTENSIN I; ANGIOTENSIN I (1-7); ENDOTHELIAL NITRIC OXIDE SYNTHASE; NEURONAL NITRIC OXIDE SYNTHASE; PEPTIDE FRAGMENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR EFFECT; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE SILENCING; IN VIVO STUDY; LENTIVIRINAE; MALE; MICROINJECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SOLITARY TRACT NUCLEUS; WESTERN BLOTTING; ANIMAL; CARDIOVASCULAR SYSTEM; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANGIOTENSIN I; ANIMALS; CARDIOVASCULAR SYSTEM; MALE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE III; PEPTIDE FRAGMENTS; PHOSPHATIDYLINOSITOL 3-KINASES; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SOLITARY NUCLEUS;

EID: 84954519152     PISSN: 10898603     EISSN: 10898611     Source Type: Journal    
DOI: 10.1016/j.niox.2015.12.002     Document Type: Article

References (52)

1. R.A. Santos, A.J. Ferreira, S.V. Pinheiro, W.O. Sampaio, R. Touyz, and M.J. Campagnole-Santos Angiotensin-(1-7) and its receptor as a potential targets for new cardiovascular drugs Expert. Opin. Investig. Drugs 14 2005 1019 1031
2. M.C. Chappell, J.G. Modrall, D.I. Diz, and C.M. Ferrario Novel aspects of the renal renin-angiotensin system: angiotensin-(1-7), ACE2 and blood pressure regulation Contrib. Nephrol. 143 2004 77 89
3. B. Langeveld, W.H. van Gilst, R.A. Tio, F. Zijlstra, and A.J. Roks Angiotensin-(1-7) attenuates neointimal formation after stent implantation in the rat Hypertension 45 2005 138 141
4. E.A. Tallant, and M.A. Clark Molecular mechanisms of inhibition of vascular growth by angiotensin-(1-7) Hypertension 42 2003 574 579
5. C.M. Ferrario, K.L. Barnes, C.H. Block, K.B. Brosnihan, D.I. Diz, M.C. Khosla, and R.A. Santos Pathways of angiotensin formation and function in the brain Hypertension 15 1990 I13 I19
6. Y. Feng, H. Xia, Y. Cai, C.M. Halabi, L.K. Becker, R.A. Santos, R.C. Speth, C.D. Sigmund, and E. Lazartigues Brain-selective overexpression of human Angiotensin-converting enzyme type 2 attenuates neurogenic hypertension Circ. Res. 106 2010 373 382
7. S. Sriramula, J.P. Cardinale, E. Lazartigues, and J. Francis ACE2 overexpression in the paraventricular nucleus attenuates angiotensin II-induced hypertension Cardiovasc. Res. 92 2011 401 408
8. G.Z. Chaves, S.M. Caligiorne, R.A. Santos, M.C. Khosla, and M.J. Campagnole-Santos 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 2000 1841 1848
9. M. Yamazato, Y. Yamazato, C. Sun, C. Diez-Freire, and M.K. Raizada Overexpression of angiotensin-converting enzyme 2 in the rostral ventrolateral medulla causes long-term decrease in blood pressure in the spontaneously hypertensive rats Hypertension 49 2007 926 931
10. S. Kar, L. Gao, and I.H. Zucker Exercise training normalizes ACE and ACE2 in the brain of rabbits with pacing-induced heart failure J. Appl. Physiol. 108 2010 923 932
11. A.J. Lawrence, and B. Jarrott Neurochemical modulation of cardiovascular control in the nucleus tractus solitarius Prog. Neurobiol. 48 1996 21 53
12. J.L. Seagard, C. Dean, and F.A. Hopp Neurochemical transmission of baroreceptor input in the nucleus tractus solitarius Brain Res. Bull. 51 2000 111 118
13. M.F. Doobay, L.S. Talman, T.D. Obr, X. Tian, R.L. Davisson, and E. Lazartigues Differential expression of neuronal ACE2 in transgenic mice with overexpression of the brain renin-angiotensin system Am. J. Physiol. Regul. Integr. Comp. Physiol. 292 2007 R373 R381
14. L.K. Becker, G.M. Etelvino, T. Walther, R.A. Santos, and M.J. Campagnole-Santos Immunofluorescence localization of the receptor Mas in cardiovascular-related areas of the rat brain Am. J. Physiol. Heart Circ. Physiol. 293 2007 H1416 H1424
15. D.I. Diz, M.A. Garcia-Espinosa, P.E. Gallagher, D. Ganten, C.M. Ferrario, and D.B. Averill Angiotensin-(1-7) and baroreflex function in nucleus tractus solitarii of (mRen2)27 transgenic rats J. Cardiovasc. Pharmacol. 51 2008 542 548
16. D.I. Diz, M.A. Garcia-Espinosa, S. Gegick, E.N. Tommasi, C.M. Ferrario, T.E. Ann, M.C. Chappell, and P.E. Gallagher 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 2008 694 700
17. K.P. Patel, and H.D. Schultz Angiotensin peptides and nitric oxide in cardiovascular disease Antioxid. Redox. Signal. 19 2013 1121 1132
18. H. Zheng, X. Liu, and K.P. Patel Angiotensin-converting enzyme 2 overexpression improves central nitric oxide-mediated sympathetic outflow in chronic heart failure Am. J. Physiol. Heart Circ. Physiol. 301 2011 H2402 H2412
19. A.B. Knott, and E. Bossy-Wetzel Nitric oxide in health and disease of the nervous system Antioxid. Redox. Signal. 11 2009 541 554
20. J. Garthwaite, and C.L. Boulton Nitric oxide signaling in the central nervous system Annu. Rev. Physiol. 57 1995 683 706
21. A.C. Dias, M. Vitela, E. Colombari, and S.W. Mifflin Nitric oxide modulation of glutamatergic, baroreflex, and cardiopulmonary transmission in the nucleus of the solitary tract Am. J. Physiol. Heart Circ. Physiol. 288 2005 H256 H262
22. I. Matsuo, Y. Hirooka, K. Hironaga, K. Eshima, H. Shigematsu, M. Shihara, K. Sakai, and A. Takeshita Glutamate release via NO production evoked by NMDA in the NTS enhances hypotension and bradycardia in vivo Am. J. Physiol. Regul. Integr. Comp. Physiol. 280 2001 R1285 R1291
23. C.J. Tseng, H.Y. Liu, H.C. Lin, L.P. Ger, C.S. Tung, and M.H. Yen Cardiovascular effects of nitric oxide in the brain stem nuclei of rats Hypertension 27 1996 36 42
24. W.T. Talman, D.N. Dragon, H. Ohta, and L.H. Lin Nitroxidergic influences on cardiovascular control by NTS: a link with glutamate Ann. N. Y. Acad. Sci. 940 2001 169 178
25. S. Wang, A.G. Teschemacher, J.F. Paton, and S. Kasparov Mechanism of nitric oxide action on inhibitory GABAergic signaling within the nucleus tractus solitarii FASEB J. 20 2006 1537 1539
26. R.F. Yang, J.X. Yin, Y.L. Li, M.C. Zimmerman, and H.D. Schultz Angiotensin-(1-7) increases neuronal potassium current via a nitric oxide-dependent mechanism Am. J. Physiol. Cell Physiol. 300 2011 C58 C64
27. C. Sun, J. Zubcevic, J.W. Polson, J.T. Potts, C. ez-Freire, Q. Zhang, J.F. Paton, and M.K. Raizada Shift to an involvement of phosphatidylinositol 3-kinase in angiotensin II actions on nucleus tractus solitarii neurons of the spontaneously hypertensive rat Circ. Res. 105 2009 1248 1255
28. J. Zubcevic, H. Waki, C. Diez-Freire, A. Gampel, M.K. Raizada, and J.F. Paton Chronic blockade of phosphatidylinositol 3-kinase in the nucleus tractus solitarii is prohypertensive in the spontaneously hypertensive rat Hypertension 53 2009 97 103
29. M. Hsiao, P.J. Lu, H.N. Huang, W.C. Lo, W.Y. Ho, T.C. Lai, H.T. Chiang, and C.J. Tseng Defective phosphatidylinositol 3-kinase signaling in central control of cardiovascular effects in the nucleus tractus solitarii of spontaneously hypertensive rats Hypertens. Res. 31 2008 1209 1218
30. M.M. El-Mas, M. Fan, and A.A. bdel-Rahman Facilitation of myocardial PI3K/Akt/nNOS signaling contributes to ethanol-evoked hypotension in female rats Alcohol. Clin. Exp. Res. 33 2009 1158 1168
31. W.H. Cheng, P.J. Lu, M. Hsiao, C.H. Hsiao, W.Y. Ho, P.W. Cheng, C.T. Lin, L.Z. Hong, and C.J. Tseng Renin activates PI3K-Akt-eNOS signalling through the angiotensin AT(1) and Mas receptors to modulate central blood pressure control in the nucleus tractus solitarii Br. J. Pharmacol. 166 2012 2024 2035
32. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates third ed. 1998 Academic Press New York
33. J. Peng, Y.K. Wang, L.G. Wang, W.J. Yuan, D.F. Su, X. Ni, X.M. Deng, and W.Z. Wang Sympathoinhibitory mechanism of moxonidine: role of the inducible nitric oxide synthase in the rostral ventrolateral medulla Cardiovasc. Res. 84 2009 283 291
34. J.F. Peng, Z.T. Wu, Y.K. Wang, W.J. Yuan, T. Sun, X. Ni, D.F. Su, W. Wang, M.J. Xu, and W.Z. Wang GABAergic mechanism in the rostral ventrolateral medulla contributes to the hypotension of moxonidine Cardiovasc. Res. 89 2011 473 481
35. Y.P. Zha, Y.K. Wang, Y. Deng, R.W. Zhang, X. Tan, W.J. Yuan, X.M. Deng, and W.Z. Wang Exercise training lowers the enhanced tonically active glutamatergic input to the rostral ventrolateral medulla in hypertensive rats, CNS Neurosci. Ther. 19 2013 244 251
36. J.M. Guo, A.J. Liu, P. Zang, W.Z. Dong, L. Ying, W. Wang, P. Xu, X.R. Song, J. Cai, S.Q. Zhang, J.L. Duan, J.L. Mehta, and D.F. Su ALDH2 protects against stroke by clearing 4-HNE Cell Res. 23 2013 915 930
37. K. Sakai, Y. Hirooka, I. Matsuo, K. Eshima, H. Shigematsu, H. Shimokawa, and A. Takeshita Overexpression of eNOS in NTS causes hypotension and bradycardia in vivo Hypertension 36 2000 1023 1028
38. Y.K. Wang, D. Shen, Q. Hao, Q. Yu, Z.T. Wu, Y. Deng, Y.F. Chen, W.J. Yuan, Q.K. Hu, D.F. Su, and W.Z. Wang Overexpression of angiotensin-converting enzyme 2 attenuates tonically active glutamatergic input to the rostral ventrolateral medulla in hypertensive rats Am. J. Physiol. Heart Circ. Physiol. 307 2014 H182 H190
39. W.Z. Wang, L. Gao, Y.X. Pan, I.H. Zucker, and W. Wang AT1 receptors in the nucleus tractus solitarii mediate the interaction between the baroreflex and the cardiac sympathetic afferent reflex in anesthetized rats Am. J. Physiol. Regul. Integr. Comp. Physiol. 292 2007 R1137 R1145
40. W.Z. Wang, L. Gao, H.J. Wang, I.H. Zucker, and W. Wang Interaction between cardiac sympathetic afferent reflex and chemoreflex is mediated by the NTS AT1 receptors in heart failure Am. J. Physiol. Heart Circ. Physiol. 295 2008 H1216 H1226
41. W.C. Lo, C.R. Jan, S.N. Wu, and C.J. Tseng Cardiovascular effects of nitric oxide and adenosine in the nucleus tractus solitarii of rats Hypertension 32 1998 1034 1038
42. J. Staschewski, C. Kulisch, and D. Albrecht Different isoforms of nitric oxide synthase are involved in Angiotensin-(1-7)-mediated plasticity changes in the amygdala in a gender-dependent manner Neuroendocrinology 94 2011 191 199
43. Y. Zhang, J. Lu, J. Shi, X. Lin, J. Dong, S. Zhang, Y. Liu, and Q. Tong 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 2008 593 600
44. W.T. Talman, and D.N. Dragon Transmission of arterial baroreflex signals depends on neuronal nitric oxide synthase Hypertension 43 2004 820 824
45. W.T. Talman NO and central cardiovascular control: a simple molecule with a complex story Hypertension 48 2006 552 554
46. L.H. Lin, and W.T. Talman Colocalization of GluR1 and neuronal nitric oxide synthase in rat nucleus tractus solitarii neurons Neuroscience 106 2001 801 809
47. T. Kishi, Y. Hirooka, Y. Kimura, K. Sakai, K. Ito, H. Shimokawa, and A. Takeshita Overexpression of eNOS in RVLM improves impaired baroreflex control of heart rate in SHRSP Hypertension 41 2003 255 260
48. H. Waki, D. Murphy, S.T. Yao, S. Kasparov, and J.F. Paton Endothelial NO synthase activity in nucleus tractus solitarii contributes to hypertension in spontaneously hypertensive rats Hypertension 48 2006 644 650
49. M.F. as-Peixoto, R.A. Santos, E.R. Gomes, M.N. Alves, P.W. Almeida, L. Greco, M. Rosa, B. Fauler, M. Bader, N. Alenina, and S. Guatimosim Molecular mechanisms involved in the angiotensin-(1-7)/mas signaling pathway in cardiomyocytes Hypertension 52 2008 542 548
50. W.O. Sampaio, R.A. Souza dos Santos, R. Faria-Silva, L.T. da Mata Machado, E.L. Schiffrin, and R.M. Touyz Angiotensin-(1-7) through receptor Mas mediates endothelial nitric oxide synthase activation via Akt-dependent pathways Hypertension 49 2007 185 192
51. H.T. Chiang, W.H. Cheng, P.J. Lu, H.N. Huang, W.C. Lo, Y.C. Tseng, J.L. Wang, M. Hsiao, and C.J. Tseng Neuronal nitric oxide synthase activation is involved in insulin-mediated cardiovascular effects in the nucleus tractus solitarii of rats Neuroscience 159 2009 727 734
52. W.H. Cheng, W.Y. Ho, C.F. Chang, P.J. Lu, P.W. Cheng, T.C. Yeh, L.Z. Hong, G.C. Sun, M. Hsiao, and C.J. Tseng Simvastatin induces a central hypotensive effect via Ras-mediated signalling to cause eNOS up-regulation Br. J. Pharmacol. 170 2013 847 858