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International Journal of Hypertension
Volume 2013 (2013), Article ID 136028, 8 pages
The Brain Renin-Angiotensin System and Mitochondrial Function: Influence on Blood Pressure and Baroreflex in Transgenic Rat Strains
1Hypertension and Vascular Research Center, Wake Forest University School of Medicine, Medical Center Boulevard, Winston-Salem, NC 27157-1032, USA
2Department of General Surgery, Wake Forest University School of Medicine, Medical Center Boulevard, Winston-Salem, NC 27157-1032, USA
Received 2 October 2012; Accepted 23 December 2012
Academic Editor: Robert C. Speth
Copyright © 2013 Manisha Nautiyal et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- D. B. Averill and D. I. Diz, “Angiotensin peptides and baroreflex control of sympathetic outflow: pathways and mechanisms of the medulla oblongata,” Brain Research Bulletin, vol. 51, no. 2, pp. 119–128, 2000.
- M. J. Campagnole-Santos, S. B. Heringer, E. N. Batista, M. C. Khosla, and R. A. S. Santos, “Differential baroreceptor reflex modulation by centrally infused angiotensin peptides,” American Journal of Physiology, vol. 263, no. 1, part 2, pp. R89–R94, 1992.
- D. I. Diz, J. A. Jessup, B. M. Westwood et al., “Angiotensin peptides as neurotransmitters/neuromodulators in the dorsomedial medulla,” Clinical and Experimental Pharmacology and Physiology, vol. 29, no. 5-6, pp. 473–482, 2002.
- D. I. Diz, A. C. Arnold, M. Nautiyal, K. Isa, H. A. Shaltout, and E. A. Tallant, “Angiotensin peptides and central autonomic regulation,” Current Opinion in Pharmacology, vol. 11, no. 2, pp. 131–137, 2011.
- A. C. Arnold, A. Sakima, D. Ganten, C. M. Ferrario, and D. I. Diz, “Modulation of reflex function by endogenous angiotensins in older transgenic rats with low glial angiotensinogen,” Hypertension, vol. 51, no. 5, pp. 1326–1331, 2008.
- A. Sakima, D. B. Averill, P. E. Gallagher et al., “Impaired heart rate baroreflex in older rats: Role of endogenous angiotensin-(1–7) at the nucleus tractus solitarii,” Hypertension, vol. 46, no. 2, pp. 333–340, 2005.
- E. M. de Cavanagh, B. Piotrkowski, N. Basso et al., “Enalapril and losartan attenuate mitochondrial dysfunction in aged rats,” The FASEB Journal, vol. 17, no. 9, pp. 1096–1098, 2003.
- E. M. V. de Cavanagh, J. E. Toblli, L. Ferder et al., “Angiotensin II blockade improves mitochondrial function in spontaneouslyhypertensive rats,” Cellular and Molecular Biology, vol. 51, no. 6, pp. 573–578, 2005.
- E. M. V. de Cavanagh, J. E. Toblli, L. Ferder, B. Piotrkowski, I. Stella, and F. Inserra, “Renal mitochondrial dysfunction in spontaneously hypertensive rats is attenuated by losartan but not by amlodipine,” American Journal of Physiology, vol. 290, no. 6, pp. R1616–R1625, 2006.
- E. M. V. de Cavanagh, L. Ferder, J. E. Toblli et al., “Renal mitochondrial impairment is attenuated by AT1 blockade in experimental type I diabetes,” American Journal of Physiology, vol. 294, no. 1, pp. H456–H465, 2008.
- I. F. Benter, M. H. M. Yousif, F. M. Al-Saleh, R. Raghupathy, M. C. Chappell, and D. I. Diz, “Angiotensin-(1–7) blockade attenuates captopril- or hydralazine-induced cardiovascular protection in spontaneously hypertensive rats treated with NG-nitro-l-arginine methyl ester,” Journal of Cardiovascular Pharmacology, vol. 57, no. 5, pp. 559–567, 2011.
- H. A. Shaltout, J. C. Rose, M. C. Chappell, and D. I. Diz, “Angiotensin-(1–7) deficiency and baroreflex impairment precede the antenatal Betamethasone exposure-induced elevation in blood pressure,” Hypertension, vol. 59, no. 2, pp. 453–458, 2012.
- S. Sriramula, J. P. Cardinale, E. Lazartigues, and J. Francis, “ACE2 overexpression in the paraventricular nucleus attenuates angiotensin II-induced hypertension,” Cardiovascular Research, vol. 92, no. 3, pp. 401–408, 2011.
- T. M. Gwathmey, K. D. Pendergrass, S. D. Reid, J. C. Rose, D. I. Diz, and M. C. Chappell, “Angiotensin-(1–7)-angiotensin-converting enzyme 2 attenuates reactive oxygen species formation to angiotensin ii within the cell nucleus,” Hypertension, vol. 55, no. 1, pp. 166–171, 2010.
- M. C. Chappell, “Emerging evidence for a functional angiotensin-converting enzyme 2-angiotensin-(1–7)-Mas receptor axis: more than regulation of blood pressure?” Hypertension, vol. 50, no. 4, pp. 596–599, 2007.
- R. A. S. Santos, A. J. Ferreira, and A. C. Simões e Silva, “Recent advances in the angiotensin-converting enzyme 2-angiotensin(1–7)-Mas axis,” Experimental Physiology, vol. 93, no. 5, pp. 519–527, 2008.
- J. J. Mullins, J. Peters, and D. Ganten, “Fulminant hypertension in transgenic rats harbouring the mouse Ren-2 gene,” Nature, vol. 344, no. 6266, pp. 541–544, 1990.
- J. J. Mullins and D. Ganten, “Transgenic animals: new approaches to hypertension research,” Journal of Hypertension, vol. 8, no. 7, pp. S35–S37, 1990.
- M. Schinke, M. Bohm, G. Bricca, A. Lippoldt, M. Bader, and D. Ganten, “Antisense RNA expression modulates angiotensinogen synthesis in cell culture and in the brain of transgenic rats,” Hypertension, vol. 26, no. 3, pp. 547–546, 1995.
- M. Schinke, O. Baltatu, M. Böhm et al., “Blood pressure reduction and diabetes insipidus in transgenic rats deficient in brain angiotensinogen,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 7, pp. 3975–3980, 1999.
- A. C. Arnold, A. Sakima, S. O. Kasper, S. Vinsant, M. A. Garcia-Espinosa, and D. I. Diz, “The brain renin-angiotensin system and cardiovascular responses to stress: insights from transgenic rats with low brain angiotensinogen,” Journal of Applied Physiology, vol. 113, no. 12, pp. 1929–1936, 2012.
- A. Sakima, D. B. Averill, S. O. Kasper et al., “Baroreceptor reflex regulation in anesthetized transgenic rats with low glia-derived angiotensinogen,” American Journal of Physiology, vol. 292, no. 3, pp. H1412–H1419, 2007.
- A. C. Arnold, M. Nautiyal, and D. I. Diz, “Protein phosphatase 1b in the solitary tract nucleus is necessary for normal baroreflex function,” Journal of Cardiovascular Pharmacology, vol. 59, no. 5, pp. 472–478, 2012.
- K. K. Griendling and M. Ushio-Fukai, “Reactive oxygen species as mediators of angiotensin II signaling,” Regulatory Peptides, vol. 91, no. 1–3, pp. 21–27, 2000.
- S. R. Datla and K. K. Griendling, “Reactive oxygen species, NADPH oxidases, and hypertension,” Hypertension, vol. 56, no. 3, pp. 325–330, 2010.
- M. C. Zimmerman, E. Lazartigues, J. A. Lang et al., “Superoxide mediates the actions of angiotensin II in the central nervous system,” Circulation Research, vol. 91, no. 11, pp. 1038–1045, 2002.
- M. C. Zimmerman, R. P. Dunlay, E. Lazartigues et al., “Requirement for Rac1-dependent NADPH oxidase in the cardiovascular and dipsogenic actions of angiotensin II in the brain,” Circulation Research, vol. 95, no. 5, pp. 532–539, 2004.
- G. Wang, J. Anrather, J. Huang, R. C. Speth, V. M. Pickel, and C. Iadecola, “NADPH oxidase contributes to angiotensin II signaling in the nucleus tractus solitarius,” Journal of Neuroscience, vol. 24, no. 24, pp. 5516–5524, 2004.
- E. M. V. de Cavanagh, F. Inserra, M. Ferder, and L. Ferder, “From mitochondria to disease: role of the renin-angiotensin system,” American Journal of Nephrology, vol. 27, no. 6, pp. 545–553, 2007.
- S. I. Dikalov, W. Li, A. K. Doughan, R. R. Blanco, and A. M. Zafari, “Mitochondrial reactive oxygen species and calcium uptake regulate activation of phagocytic NADPH oxidase,” American Journal of Physiology, vol. 302, no. 10, pp. R1134–R1142, 2012.
- A. K. Doughan, D. G. Harrison, and S. I. Dikalov, “Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction,” Circulation Research, vol. 102, no. 4, pp. 488–496, 2008.
- S. Kimura, G. X. Zhang, A. Nishiyama et al., “Mitochondria-derived reactive oxygen species and vascular MAP kinases: comparison of angiotensin II and diazoxide,” Hypertension, vol. 45, no. 3, pp. 438–444, 2005.
- A. E. Dikalova, A. T. Bikineyeva, K. Budzyn et al., “Therapeutic targeting of mitochondrial superoxide in hypertension,” Circulation Research, vol. 107, no. 1, pp. 106–116, 2010.
- S. I. Dikalov and R. R. Nazarewicz, “Angiotensin II-induced production of mitochondrial reactive oxygen species: potential mechanisms and relevance for cardiovascular disease,” Antioxidants and Redox Signaling. In press.
- K. Block, Y. Gorin, and H. E. Abboud, “Subcellular localization of Nox4 and regulation in diabetes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 34, pp. 14385–14390, 2009.
- S. M. Kim, Y. G. Kim, K. H. Jeong et al., “Angiotensin II-induced mitochondrial Nox4 is a major endogenous source of oxidative stress in kidney tubular cells,” PLoS ONE, vol. 7, no. 7, Article ID e39739, 2012.
- J. Kuroda, T. Ago, S. Matsushima, P. Zhai, M. D. Schneider, and J. Sadoshima, “NADPH oxidase 4 (Nox4) is a major source of oxidative stress in the failing heart,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 35, pp. 15565–15570, 2010.
- I. F. Benter, M. H. M. Yousif, G. S. Dhaunsi, J. Kaur, M. C. Chappell, and D. I. Diz, “Angiotensin-(1–7) prevents activation of NADPH oxidase and renal vascular dysfunction in diabetic hypertensive rats,” American Journal of Nephrology, vol. 28, no. 1, pp. 25–33, 2007.
- G. S. Dhaunsi, M. H. M. Yousif, S. Akhtar, M. C. Chappell, D. I. Diz, and I. F. Benter, “Angiotensin-(1–7) prevents diabetes-induced attenuation in PPAR-γ and catalase activities,” European Journal of Pharmacology, vol. 638, no. 1–3, pp. 108–114, 2010.
- M. Nautiyal, P. V. Katakam, D. W. Busija et al., “Differences in oxidative stress status and expression of MKP-1 in dorsal medulla of transgenic rats with altered brain renin-angiotensin system,” American Journal of Physiology, vol. 303, no. 8, pp. R799–R806, 2012.
- M. H. Yousif, G. S. Dhaunsi, B. M. Makki, B. A. Qabazard, S. Akhtar, and I. F. Benter, “Characterization of Angiotensin-(1–7) effects on the cardiovascular system in an experimental model of type-1 diabetes,” Pharmacological Research, vol. 66, no. 3, pp. 269–275, 2012.
- Y. Hirooka, “Role of reactive oxygen species in brainstem in neural mechanisms of hypertension,” Autonomic Neuroscience: Basic and Clinical, vol. 142, no. 1-2, pp. 20–24, 2008.
- J. R. Peterson, R. V. Sharma, and R. L. Davisson, “Reactive oxygen species in the neuropathogenesis of hypertension,” Current Hypertension Reports, vol. 8, no. 3, pp. 232–241, 2006.
- S. H. H. Chan, K. L. H. Wu, A. Y. W. Chang, M. H. Tai, and J. Y. H. Chan, “Oxidative impairment of mitochondrial electron transport chain complexes in rostral ventrolateral medulla contributes to neurogenic hypertension,” Hypertension, vol. 53, no. 2, pp. 217–227, 2009.
- M. Nozoe, Y. Hirooka, Y. Koga et al., “Mitochondria-derived reactive oxygen species mediate sympathoexcitation induced by angiotensin II in the rostral ventrolateral medulla,” Journal of Hypertension, vol. 26, no. 11, pp. 2176–2184, 2008.
- J. Y. Jun, J. Zubcevic, Y. Qi, and M. K. Raizada, “Scavenging of mitochondrial ros in the brain prevents neurogenic hypertension,” in Proceedings of the 25th International Symposium on Cerebral Blood Flow, Metabolism and Function, 2011.
- K. Ogawa, Y. Hirooka, K. Shinohara, T. Kishi, and K. Sunagawa, “Inhibition of oxidative stress in rostral ventrolateral medulla improves impaired baroreflex sensitivity in stroke-prone spontaneously hypertensive rats,” International Heart Journal, vol. 53, no. 3, pp. 193–198, 2012.
- V. A. Braga, E. Colombari, and M. G. Jovita, “Angiotensin II-derived reactive oxygen species underpinning the processing of the cardiovascular reflexes in the medulla oblongata,” Neuroscience Bulletin, vol. 27, no. 4, pp. 269–274, 2011.
- M. Nautiyal, H. A. Shaltout, D. C. de Lima, N. K. do, M. C. Chappell, and D. I. Diz, “Central angiotensin-(1–7) improves vagal function independent of blood pressure in hypertensive (mRen2)27 rats,” Hypertension, vol. 60, no. 5, pp. 1257–1265, 2012.
- J. D. Malhotra and R. J. Kaufman, “ER stress and its functional link to mitochondria: role in cell survival and death,” Cold Spring Harbor Perspectives in Biology, vol. 3, no. 9, Article ID a004424, 2011.
- C. N. Young, X. Cao, M. R. Guruju et al., “ER stress in the brain subfornical organ mediates angiotensin-dependent hypertension.,” Journal of Clinical Investigation, vol. 122, no. 11, pp. 3960–3964, 2012.
- S. H. H. Chan, K. S. Hsu, C. C. Huang, L. L. Wang, C. C. Ou, and J. Y. H. Chan, “NADPH oxidase-derived superoxide anion mediates angiotensin II-induced pressor effect via activation of p38 mitogen-activated protein kinase in the rostral ventrolateral medulla,” Circulation Research, vol. 97, no. 8, pp. 772–780, 2005.
- S. H. H. Chan, L. L. Wang, H. L. Tseng, and J. Y. H. Chan, “Upregulation of AT1 receptor gene on activation of protein kinase Cβ/nicotinamide adenine dinucleotide diphosphate oxidase/ERK1/2/c-fos signaling cascade mediates long-term pressor effect of angiotensin II in rostral ventrolateral medulla,” Journal of Hypertension, vol. 25, no. 9, pp. 1845–1861, 2007.
- T. Kishi, Y. Hirooka, S. Konno, K. Ogawa, and K. Sunagawa, “Angiotensin II type 1 receptor-activated caspase-3 through ras/mitogen-activated protein kinase/extracellular signal-regulated kinase in the rostral ventrolateral medulla is involved in sympathoexcitation in stroke-prone spontaneously hypertensive rats,” Hypertension, vol. 55, no. 2, pp. 291–297, 2010.
- E. M. Logan, A. A. Aileru, H. A. Shaltout, D. B. Averill, and D. I. Diz, “The functional role of PI3K in maintenance of blood pressure and baroreflex suppression in (mRen2)27 and mRen2.Lewis rat,” Journal of Cardiovascular Pharmacology, vol. 58, no. 4, pp. 367–373, 2011.
- M. Soulsby and A. M. Bennett, “Physiological signaling specificity by protein tyrosine phosphatases,” Physiology, vol. 24, no. 5, pp. 281–289, 2009.
- R. J. R. Flach and A. M. Bennett, “Mitogen-activated protein kinase phosphatase-1—a potential therapeutic target in metabolic disease,” Expert Opinion on Therapeutic Targets, vol. 14, no. 12, pp. 1323–1332, 2010.
- R. C. Tsou and K. K. Bence, “The genetics of PTPN1 and obesity: insights from mouse models of tissue-specific PTP1B deficiency,” Journal of Obesity, vol. 2012, Article ID 926857, 8 pages, 2012.
- M. Elchebly, P. Payette, E. Michaliszyn et al., “Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene,” Science, vol. 283, no. 5407, pp. 1544–1548, 1999.
- J. J. Wu, R. J. Roth, E. J. Anderson et al., “Mice lacking MAP kinase phosphatase-1 have enhanced MAP kinase activity and resistance to diet-induced obesity,” Cell Metabolism, vol. 4, no. 1, pp. 61–73, 2006.
- R. J. Roth, A. M. Le, L. Zhang et al., “MAPK phosphatase-1 facilitates the loss of oxidative myofibers associated with obesity in mice,” Journal of Clinical Investigation, vol. 119, no. 12, pp. 3817–3829, 2009.
- S. O. Kasper, C. S. Carter, C. M. Ferrario et al., “Growth, metabolism, and blood pressure disturbances during aging in transgenic rats with altered brain renin-angiotensin systems,” Physiological Genomics, vol. 23, no. 3, pp. 311–317, 2005.
- S. O. Kasper, C. M. Ferrario, D. Ganten, and D. I. Diz, “Rats with low brain angiotensinogen do not exhibit insulin resistance during early aging,” Endocrine, vol. 30, no. 2, pp. 167–174, 2006.
- D. I. Diz, S. O. Kasper, A. Sakima, and C. M. Ferrario, “Aging and the brain renin-angiotensin system: insights from studies in transgenic rats,” Cleveland Clinic Journal of Medicine, vol. 74, supplement 1, pp. S95–S98, 2007.
- R. Bergeron, J. M. Ren, K. S. Cadman et al., “Chronic activation of AMP kinase results in NRF-1 activation and mitochondrial biogenesis,” American Journal of Physiology, vol. 281, no. 6, pp. E1340–E1346, 2001.
- L. H. Young, J. Li, S. J. Baron, and R. R. Russell, “AMP-activated protein kinase: a key stress signaling pathway in the heart,” Trends in Cardiovascular Medicine, vol. 15, no. 3, pp. 110–118, 2005.