Angiotensin II induces interleukin-6 expression in astrocytes: Role of reactive oxygen species and NF-κB

Molecular and Cellular Endocrinology

Volumn 437, Issue , 2016, Pages 130-141

  Gowrisankar, Yugandhar V ^a   Clark, Michelle A ^a  

^a NOVA SOUTHEASTERN UNIVERSITY   (United States)

Author keywords

Angiotensin II; Astrocytes; Interleukin 6; NF B; Reactive oxygen species

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN II; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; 1 (4 DIMETHYLAMINO 3 METHYLBENZYL) 5 DIPHENYLACETYL 4,5,6,7 TETRAHYDRO 1H IMIDAZO[4,5 C]PYRIDINE 6 CARBOXYLIC ACID; HYDRAZONE DERIVATIVE; IMIDAZOLE DERIVATIVE; LOSARTAN; NITROIMIDAZOLE DERIVATIVE; PYRIDINE DERIVATIVE; YCG 063;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN LEVEL; BRAIN STEM; CELL LEVEL; CEREBELLUM; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FEMALE; GENE EXPRESSION; HYPERTENSION; IL 6 GENE; IMMUNOMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; ANIMAL; BRAIN; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SECRETION (PROCESS); SPONTANEOUSLY HYPERTENSIVE RAT; TIME FACTOR; WISTAR RAT;

ANGIOTENSIN II; ANIMALS; ASTROCYTES; BRAIN; FEMALE; GENE EXPRESSION REGULATION; HYDRAZONES; IMIDAZOLES; INTERLEUKIN-6; LOSARTAN; NF-KAPPA B; NITROIMIDAZOLES; PYRIDINES; RATS, INBRED SHR; RATS, WISTAR; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; TIME FACTORS;

EID: 84983085429     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2016.08.013     Document Type: Article

References (111)

1. Abeywardena, M.Y., Leifert, W.R., Warnes, K.E., Varghese, J.N., Head, R.J., Cardiovascular biology of interleukin-6. Curr. Pharm. Des. 15 (2009), 1809–1821.
2. Akira, S., NF-IL6 and gene regulation. Res. Immunol. 143 (1992), 734–736.
3. Akira, S., Kishimoto, T., IL-6 and NF-IL6 in acute-phase response and viral infection. Immunol. Rev. 127 (1992), 25–50.
4. Alarcon, R., Fuenzalida, C., Santibanez, M., von Bernhardi, R., Expression of scavenger receptors in glial cells. Comparing the adhesion of astrocytes and microglia from neonatal rats to surface-bound beta-amyloid. J. Biol. Chem. 280 (2005), 30406–30415.
5. Baldi, P., Long, A.D., A Bayesian framework for the analysis of microarray expression data: regularized t -test and statistical inferences of gene changes. Bioinformatics 17 (2001), 509–519.
6. Baltatu, O., Bader, M., Brain renin-angiotensin system. Lessons from functional genomics. Neuroendocrinology 78 (2003), 253–259.
7. Bayir, H., Reactive oxygen species. Crit. Care Med. 33 (2005), S498–S501.
8. Beasley, D., Phorbol ester and interleukin-1 induce interleukin-6 gene expression in vascular smooth muscle cells via independent pathways. J. Cardiovasc Pharmacol. 29 (1997), 323–330.
9. Benigni, A., Cassis, P., Remuzzi, G., Angiotensin II revisited: new roles in inflammation, immunology and aging. EMBO Mol. Med. 2 (2010), 247–257.
10. Blume, A., Herdegen, T., Unger, T., Angiotensin peptides and inducible transcription factors. J. Mol. Med. (Berl) 77 (1999), 339–357.
11. Brands, M.W., Banes-Berceli, A.K., Inscho, E.W., Al-Azawi, H., Allen, A.J., Labazi, H., Interleukin 6 knockout prevents angiotensin II hypertension: role of renal vasoconstriction and janus kinase 2/signal transducer and activator of transcription 3 activation. Hypertension 56 (2010), 879–884.
12. Brasier, A.R., The NF-kappaB regulatory network. Cardiovasc Toxicol. 6 (2006), 111–130.
13. Chae, C.U., Lee, R.T., Rifai, N., Ridker, P.M., Blood pressure and inflammation in apparently healthy men. Hypertension 38 (2001), 399–403.
14. Chan, J.Y., Wang, L.L., Lee, H.Y., Chan, S.H., Augmented upregulation by c-fos of angiotensin subtype 1 receptor in nucleus tractus solitarii of spontaneously hypertensive rats. Hypertension 40 (2002), 335–341.
15. Cheng, Z.J., Vapaatalo, H., Mervaala, E., Angiotensin II and vascular inflammation. Med. Sci. Monit. 11 (2005), RA194–205.
16. Clark, M.A., Gonzalez, N., Angiotensin II stimulates rat astrocyte mitogen-activated protein kinase activity and growth through EGF and PDGF receptor transactivation. Regul. Pept. 144 (2007), 115–122.
17. Clark, M.A., Gonzalez, N., Src and Pyk2 mediate angiotensin II effects in cultured rat astrocytes. Regul. Pept. 143 (2007), 47–55.
18. Clark, M.A., Guillaume, G., Pierre-Louis, H.C., Angiotensin II induces proliferation of cultured rat astrocytes through c-Jun N-terminal kinase. Brain Res. Bull. 75 (2008), 101–106.
19. Constantinescu, C.S., Tani, M., Ransohoff, R.M., Wysocka, M., Hilliard, B., Fujioka, T., Murphy, S., Tighe, P.J., Das Sarma, J., Trinchieri, G., Rostami, A., Astrocytes as antigen-presenting cells: expression of IL-12/IL-23. J. Neurochem. 95 (2005), 331–340.
20. Dalton, T.P., Shertzer, H.G., Puga, A., Regulation of gene expression by reactive oxygen. Annu. Rev. Pharmacol. Toxicol. 39 (1999), 67–101.
21. Delaney, J., Chiarello, R., Villar, D., Kandalam, U., Castejon, A.M., Clark, M.A., Regulation of c-fos, c-jun and c-myc gene expression by angiotensin II in primary cultured rat astrocytes: role of ERK1/2 MAP kinases. Neurochem. Res. 33 (2008), 545–550.
22. Deng, H.X., Hentati, A., Tainer, J.A., Iqbal, Z., Cayabyab, A., Hung, W.Y., Getzoff, E.D., Hu, P., Herzfeldt, B., Roos, R.P., et al. Amyotrophic lateral sclerosis and structural defects in Cu,Zn superoxide dismutase. Science 261 (1993), 1047–1051.
23. Dhalla, N.S., Temsah, R.M., Netticadan, T., Role of oxidative stress in cardiovascular diseases. J. Hypertens. 18 (2000), 655–673.
24. Dikalov, S., Griendling, K.K., Harrison, D.G., Measurement of reactive oxygen species in cardiovascular studies. Hypertension 49 (2007), 717–727.
25. Ding, G., Zhang, A., Huang, S., Pan, X., Zhen, G., Chen, R., Yang, T., ANG II induces c-Jun NH2-terminal kinase activation and proliferation of human mesangial cells via redox-sensitive transactivation of the EGFR. Am. J. Physiol. Ren. Physiol. 293 (2007), F1889–F1897.
26. Ershler, W.B., Sun, W.H., Binkley, N., The role of interleukin-6 in certain age-related diseases. Drugs Aging 5 (1994), 358–365.
27. Fawcett, J.W., Asher, R.A., The glial scar and central nervous system repair. Brain Res. Bull. 49 (1999), 377–391.
28. Fliser, D., Buchholz, K., Haller, H., Olmesartan, E.U.T.o., Pravastatin in, I., Atherosclerosis, I., Antiinflammatory effects of angiotensin II subtype 1 receptor blockade in hypertensive patients with microinflammation. Circulation 110 (2004), 1103–1107.
29. Fontana, A., Fierz, W., Wekerle, H., Astrocytes present myelin basic protein to encephalitogenic T-cell lines. Nature 307 (1984), 273–276.
30. Funakoshi, Y., Ichiki, T., Ito, K., Takeshita, A., Induction of interleukin-6 expression by angiotensin II in rat vascular smooth muscle cells. Hypertension 34 (1999), 118–125.
31. Gilmore, T.D., Introduction to NF-kappaB: players, pathways, perspectives. Oncogene 25 (2006), 6680–6684.
32. Greenbaum, D., Colangelo, C., Williams, K., Gerstein, M., Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol., 4, 2003, 117.
33. Greenwood, F.C., Hunter, W.M., Glover, J.S., The preparation of I-131-Labelled human growth hormone of high specific radioactivity. Biochem. J. 89 (1963), 114–123.
34. Griendling, K.K., Ushio-Fukai, M., Lassegue, B., Alexander, R.W., Angiotensin II signaling in vascular smooth muscle. New concepts. Hypertension 29 (1997), 366–373.
35. Gupta, S., Young, D., Sen, S., Inhibition of NF-kappaB induces regression of cardiac hypertrophy, independent of blood pressure control, in spontaneously hypertensive rats. Am. J. Physiol. Heart Circ. Physiol. 289 (2005), H20–H29.
36. Han, Y., Runge, M.S., Brasier, A.R., Angiotensin II induces interleukin-6 transcription in vascular smooth muscle cells through pleiotropic activation of nuclear factor-kappa B transcription factors. Circ. Res. 84 (1999), 695–703.
37. Harrap, S.B., Van der Merwe, W.M., Griffin, S.A., Macpherson, F., Lever, A.F., Brief angiotensin converting enzyme inhibitor treatment in young spontaneously hypertensive rats reduces blood pressure long-term. Hypertension 16 (1990), 603–614.
38. Harrison, D.G., Endothelial function and oxidant stress. Clin. Cardiol., 20, 1997 II-11–7.
39. Hu, H.M., Baer, M., Williams, S.C., Johnson, P.F., Schwartz, R.C., Redundancy of C/EBP alpha, -beta, and -delta in supporting the lipopolysaccharide-induced transcription of IL-6 and monocyte chemoattractant protein-1. J. Immunol. 160 (1998), 2334–2342.
40. Hull, M., Muksch, B., Akundi, R.S., Waschbisch, A., Hoozemans, J.J., Veerhuis, R., Fiebich, B.L., Amyloid beta peptide (25-35) activates protein kinase C leading to cyclooxygenase-2 induction and prostaglandin E2 release in primary midbrain astrocytes. Neurochem. Int. 48 (2006), 663–672.
41. Hunyady, L., Catt, K.J., Pleiotropic AT1 receptor signaling pathways mediating physiological and pathogenic actions of angiotensin II. Mol. Endocrinol. 20 (2006), 953–970.
42. Ishikawa, M., Stokes, K.Y., Zhang, J.H., Nanda, A., Granger, D.N., Cerebral microvascular responses to hypercholesterolemia: roles of NADPH oxidase and P-selectin. Circ. Res. 94 (2004), 239–244.
43. Jaimes, E.A., Galceran, J.M., Raij, L., Angiotensin II induces superoxide anion production by mesangial cells. Kidney Int. 54 (1998), 775–784.
44. Kambayashi, Y., Bardhan, S., Takahashi, K., Tsuzuki, S., Inui, H., Hamakubo, T., Inagami, T., Molecular cloning of a novel angiotensin II receptor isoform involved in phosphotyrosine phosphatase inhibition. J. Biol. Chem. 268 (1993), 24543–24546.
45. Kandalam, U., Clark, M.A., Angiotensin II activates JAK2/STAT3 pathway and induces interleukin-6 production in cultured rat brainstem astrocytes. Regul. Pept. 159 (2010), 110–116.
46. Kandalam, U., Palanisamy, M., Clark, M.A., Angiotensin II induces cell growth and IL-6 mRNA expression through the JAK2-STAT3 pathway in rat cerebellar astrocytes. JAKSTAT 1 (2012), 83–89.
47. Kannel, W.B., Wolf, P.A., Castelli, W.P., D'Agostino, R.B., Fibrinogen and risk of cardiovascular disease. The Framingham Study. JAMA 258 (1987), 1183–1186.
48. Kazama, K., Anrather, J., Zhou, P., Girouard, H., Frys, K., Milner, T.A., Iadecola, C., Angiotensin II impairs neurovascular coupling in neocortex through NADPH oxidase-derived radicals. Circ. Res. 95 (2004), 1019–1026.
49. Kiechl, S., Egger, G., Mayr, M., Wiedermann, C.J., Bonora, E., Oberhollenzer, F., Muggeo, M., Xu, Q., Wick, G., Poewe, W., Willeit, J., Chronic infections and the risk of carotid atherosclerosis: prospective results from a large population study. Circulation 103 (2001), 1064–1070.
50. Kishi, T., Hirooka, Y., Kimura, Y., Ito, K., Shimokawa, H., Takeshita, A., Increased reactive oxygen species in rostral ventrolateral medulla contribute to neural mechanisms of hypertension in stroke-prone spontaneously hypertensive rats. Circulation 109 (2004), 2357–2362.
51. Kuller, L.H., Eichner, J.E., Orchard, T.J., Grandits, G.A., McCallum, L., Tracy, R.P., The relation between serum albumin levels and risk of coronary heart disease in the Multiple Risk Factor Intervention Trial. Am. J. Epidemiol. 134 (1991), 1266–1277.
52. Kuller, L.H., Tracy, R.P., Shaten, J., Meilahn, E.N., Relation of C-reactive protein and coronary heart disease in the MRFIT nested case-control study. Multiple Risk Factor Intervention Trial. Am. J. Epidemiol. 144 (1996), 537–547.
53. Laursen, J.B., Rajagopalan, S., Galis, Z., Tarpey, M., Freeman, B.A., Harrison, D.G., Role of superoxide in angiotensin II-induced but not catecholamine-induced hypertension. Circulation 95 (1997), 588–593.
54. Lee, M.C., Shoji, H., Miyazaki, H., Yoshino, F., Hori, N., Toyoda, M., Ikeda, Y., Anzai, K., Ikota, N., Ozawa, T., Assessment of oxidative stress in the spontaneously hypertensive rat brain using electron spin resonance (ESR) imaging and in vivo L-Band ESR. Hypertens. Res. 27 (2004), 485–492.
55. Lee, D.L., Sturgis, L.C., Labazi, H., Osborne, J.B. Jr., Fleming, C., Pollock, J.S., Manhiani, M., Imig, J.D., Brands, M.W., Angiotensin II hypertension is attenuated in interleukin-6 knockout mice. Am. J. Physiol. Heart Circ. Physiol. 290 (2006), H935–H940.
56. Lenkei, Z., Palkovits, M., Corvol, P., Llorens-Cortes, C., Distribution of angiotensin II type-2 receptor (AT2) mRNA expression in the adult rat brain. J. Comp. Neurol. 373 (1996), 322–339.
57. Lindenau, J., Noack, H., Possel, H., Asayama, K., Wolf, G., Cellular distribution of superoxide dismutases in the rat CNS. Glia 29 (2000), 25–34.
58. Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 (2001), 402–408.
59. Loppnow, H., Libby, P., Proliferating or interleukin 1-activated human vascular smooth muscle cells secrete copious interleukin 6. J. Clin. Invest. 85 (1990), 731–738.
60. Matsukawa, S., Keil, L.C., Reid, I.A., Role of endogenous angiotensin II in the control of vasopressin secretion during hypovolemia and hypotension in conscious rabbits. Endocrinology 128 (1991), 204–210.
61. Mattson, M.P., Camandola, S., NF-kappaB in neuronal plasticity and neurodegenerative disorders. J. Clin. Invest. 107 (2001), 247–254.
62. Mehta, P.K., Griendling, K.K., Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am. J. Physiol. Cell Physiol. 292 (2007), C82–C97.
63. Min, K.J., Yang, M.S., Kim, S.U., Jou, I., Joe, E.H., Astrocytes induce hemeoxygenase-1 expression in microglia: a feasible mechanism for preventing excessive brain inflammation. J. Neurosci. 26 (2006), 1880–1887.
64. Morimoto, S., Sigmund, C.D., Angiotensin mutant mice: a focus on the brain renin-angiotensin system. Neuropeptides 36 (2002), 194–200.
65. Mukoyama, M., Nakajima, M., Horiuchi, M., Sasamura, H., Pratt, R.E., Dzau, V.J., Expression cloning of type 2 angiotensin II receptor reveals a unique class of seven-transmembrane receptors. J. Biol. Chem. 268 (1993), 24539–24542.
66. Murphy, T.J., Alexander, R.W., Griendling, K.K., Runge, M.S., Bernstein, K.E., Isolation of a cDNA encoding the vascular type-1 angiotensin II receptor. Nature 351 (1991), 233–236.
67. Nakazono, K., Watanabe, N., Matsuno, K., Sasaki, J., Sato, T., Inoue, M., Does superoxide underlie the pathogenesis of hypertension?. Proc. Natl. Acad. Sci. U. S. A. 88 (1991), 10045–10048.
68. Nookala, A.R., Kumar, A., Molecular mechanisms involved in HIV-1 Tat-mediated induction of IL-6 and IL-8 in astrocytes. J. Neuroinflammation, 11, 2014, 214.
69. Okamoto, K., Aoki, K., Development of a strain of spontaneously hypertensive rats. Jpn. Circ. J. 27 (1963), 282–293.
70. Pagano, P.J., Clark, J.K., Cifuentes-Pagano, M.E., Clark, S.M., Callis, G.M., Quinn, M.T., Localization of a constitutively active, phagocyte-like NADPH oxidase in rabbit aortic adventitia: enhancement by angiotensin II. Proc. Natl. Acad. Sci. U. S. A. 94 (1997), 14483–14488.
71. Parsons, K.K., Coffman, T.M., The renin-angiotensin system: it's all in your head. J. Clin. Invest. 117 (2007), 873–876.
72. Peterson, J.R., Sharma, R.V., Davisson, R.L., Reactive oxygen species in the neuropathogenesis of hypertension. Curr. Hypertens. Rep. 8 (2006), 232–241.
73. Polizio, A.H., Pena, C., Effects of angiotensin II type 1 receptor blockade on the oxidative stress in spontaneously hypertensive rat tissues. Regul. Pept. 128 (2005), 1–5.
74. Rajagopalan, S., Kurz, S., Munzel, T., Tarpey, M., Freeman, B.A., Griendling, K.K., Harrison, D.G., Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation. Contribution to alterations of vasomotor tone. J. Clin. Invest. 97 (1996), 1916–1923.
75. Reid, M.B., Andrade, F.H., Balke, C.W., Esser, K.A., Redox mechanisms of muscle dysfunction in inflammatory disease. Phys. Med. Rehabil. Clin. N. Am. 16 (2005), 925–949 ix.
76. Ridker, P.M., Cushman, M., Stampfer, M.J., Tracy, R.P., Hennekens, C.H., Inflammation, aspirin, and the risk of cardiovascular disease in apparently healthy men. N. Engl. J. Med. 336 (1997), 973–979.
77. Rodriguez-Iturbe, B., Ferrebuz, A., Vanegas, V., Quiroz, Y., Mezzano, S., Vaziri, N.D., Early and sustained inhibition of nuclear factor-kappaB prevents hypertension in spontaneously hypertensive rats. J. Pharmacol. Exp. Ther. 315 (2005), 51–57.
78. Ruiz-Ortega, M., Ruperez, M., Lorenzo, O., Esteban, V., Blanco, J., Mezzano, S., Egido, J., Angiotensin II regulates the synthesis of proinflammatory cytokines and chemokines in the kidney. Kidney Int. Suppl., 2002, S12–S22.
79. Saavedra, J.M., Brain angiotensin II: new developments, unanswered questions and therapeutic opportunities. Cell Mol. Neurobiol. 25 (2005), 485–512.
80. Sanz-Rosa, D., Oubina, M.P., Cediel, E., de Las Heras, N., Vegazo, O., Jimenez, J., Lahera, V., Cachofeiro, V., Effect of AT1 receptor antagonism on vascular and circulating inflammatory mediators in SHR: role of NF-kappaB/IkappaB system. Am. J. Physiol. Heart Circ. Physiol. 288 (2005), H111–H115.
81. Sayre, L.M., Smith, M.A., Perry, G., Chemistry and biochemistry of oxidative stress in neurodegenerative disease. Curr. Med. Chem. 8 (2001), 721–738.
82. Schieffer, B., Luchtefeld, M., Braun, S., Hilfiker, A., Hilfiker-Kleiner, D., Drexler, H., Role of NAD(P)H oxidase in angiotensin II-induced JAK/STAT signaling and cytokine induction. Circ. Res. 87 (2000), 1195–1201.
83. Schieffer, B., Bunte, C., Witte, J., Hoeper, K., Boger, R.H., Schwedhelm, E., Drexler, H., Comparative effects of AT1-antagonism and angiotensin-converting enzyme inhibition on markers of inflammation and platelet aggregation in patients with coronary artery disease. J. Am. Coll. Cardiol. 44 (2004), 362–368.
84. Schnackenberg, C.G., Wilcox, C.S., Two-week administration of tempol attenuates both hypertension and renal excretion of 8-Iso prostaglandin f2alpha. Hypertension 33 (1999), 424–428.
85. Schnackenberg, C.G., Welch, W.J., Wilcox, C.S., Normalization of blood pressure and renal vascular resistance in SHR with a membrane-permeable superoxide dismutase mimetic: role of nitric oxide. Hypertension 32 (1998), 59–64.
86. Schulz, J.B., Henshaw, D.R., Siwek, D., Jenkins, B.G., Ferrante, R.J., Cipolloni, P.B., Kowall, N.W., Rosen, B.R., Beal, M.F., Involvement of free radicals in excitotoxicity in vivo. J. Neurochem. 64 (1995), 2239–2247.
87. Shimohama, S., Tanino, H., Kawakami, N., Okamura, N., Kodama, H., Yamaguchi, T., Hayakawa, T., Nunomura, A., Chiba, S., Perry, G., Smith, M.A., Fujimoto, S., Activation of NADPH oxidase in Alzheimer's disease brains. Biochem. Biophys. Res. Commun. 273 (2000), 5–9.
88. Silver, J., Miller, J.H., Regeneration beyond the glial scar. Nat. Rev. Neurosci. 5 (2004), 146–156.
89. Smith, M.A., Richey Harris, P.L., Sayre, L.M., Beckman, J.S., Perry, G., Widespread peroxynitrite-mediated damage in Alzheimer's disease. J. Neurosci. 17 (1997), 2653–2657.
90. Suzuki, H., Swei, A., Zweifach, B.W., Schmid-Schonbein, G.W., In vivo evidence for microvascular oxidative stress in spontaneously hypertensive rats. Hydroethidine microfluorography. Hypertension 25 (1995), 1083–1089.
91. Suzuki, H., DeLano, F.A., Parks, D.A., Jamshidi, N., Granger, D.N., Ishii, H., Suematsu, M., Zweifach, B.W., Schmid-Schonbein, G.W., Xanthine oxidase activity associated with arterial blood pressure in spontaneously hypertensive rats. Proc. Natl. Acad. Sci. U. S. A. 95 (1998), 4754–4759.
92. Szallasi, Z., Genetic network analysis in light of massively parallel biological data acquisition. Pac Symp. Biocomput., 1999, 5–16.
93. Tai, M.H., Wang, L.L., Wu, K.L., Chan, J.Y., Increased superoxide anion in rostral ventrolateral medulla contributes to hypertension in spontaneously hypertensive rats via interactions with nitric oxide. Free Radic. Biol. Med. 38 (2005), 450–462.
94. Tallant, E.A., Higson, J.T., Angiotensin II activates distinct signal transduction pathways in astrocytes isolated from neonatal rat brain. Glia 19 (1997), 333–342.
95. Tallant, E.A., Jaiswal, N., Diz, D.I., Ferrario, C.M., Human astrocytes contain two distinct angiotensin receptor subtypes. Hypertension 18 (1991), 32–39.
96. Terreni, L., De Simoni, M.G., Role of the brain in interleukin-6 modulation. Neuroimmunomodulation 5 (1998), 214–219.
97. Thomas, W.G., Mendelsohn, F.A., Angiotensin receptors: form and function and distribution. Int. J. Biochem. Cell Biol. 35 (2003), 774–779.
98. Touyz, R.M., Reactive oxygen species, vascular oxidative stress, and redox signaling in hypertension: what is the clinical significance?. Hypertension 44 (2004), 248–252.
99. Touyz, R.M., Schiffrin, E.L., Ang II-stimulated superoxide production is mediated via phospholipase D in human vascular smooth muscle cells. Hypertension 34 (1999), 976–982.
100. Touyz, R.M., Schiffrin, E.L., Signal transduction mechanisms mediating the physiological and pathophysiological actions of angiotensin II in vascular smooth muscle cells. Pharmacol. Rev. 52 (2000), 639–672.
101. Tschudi, M.R., Mesaros, S., Luscher, T.F., Malinski, T., Direct in situ measurement of nitric oxide in mesenteric resistance arteries. Increased decomposition by superoxide in hypertension. Hypertension 27 (1996), 32–35.
102. Turpaev, K.T., Reactive oxygen species and regulation of gene expression. Biochem. (Mosc) 67 (2002), 281–292.
103. Valko, M., Leibfritz, D., Moncol, J., Cronin, M.T., Mazur, M., Telser, J., Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39 (2007), 44–84.
104. Van Wagoner, N.J., Oh, J.W., Repovic, P., Benveniste, E.N., Interleukin-6 (IL-6) production by astrocytes: autocrine regulation by IL-6 and the soluble IL-6 receptor. J. Neurosci. 19 (1999), 5236–5244.
105. Veerasingham, S.J., Raizada, M.K., Brain renin-angiotensin system dysfunction in hypertension: recent advances and perspectives. Br. J. Pharmacol. 139 (2003), 191–202.
106. Wu, J.N., Berecek, K.H., Prevention of genetic hypertension by early treatment of spontaneously hypertensive rats with the angiotensin converting enzyme inhibitor captopril. Hypertension 22 (1993), 139–146.
107. Wu, W.C., Hu, D.N., Gao, H.X., Chen, M., Wang, D., Rosen, R., McCormick, S.A., Subtoxic levels hydrogen peroxide-induced production of interleukin-6 by retinal pigment epithelial cells. Mol. Vis. 16 (2010), 1864–1873.
108. Yoshioka, M., Aoyama, K., Matsushita, T., Effects of ascorbic acid on blood pressure and ascorbic acid metabolism in spontaneously hypertensive rats (SH rats). Int. J. Vitam. Nutr. Res. 55 (1985), 301–307.
109. Yu, H., Huang, J., Wang, S., Zhao, G., Jiao, X., Zhu, L., Overexpression of Smad7 suppressed ROS/MMP9-dependent collagen synthesis through regulation of heme oxygenase-1. Mol. Biol. Rep. 40 (2013), 5307–5314.
110. Zhai, P., Yamamoto, M., Galeotti, J., Liu, J., Masurekar, M., Thaisz, J., Irie, K., Holle, E., Yu, X., Kupershmidt, S., Roden, D.M., Wagner, T., Yatani, A., Vatner, D.E., Vatner, S.F., Sadoshima, J., Cardiac-specific overexpression of AT1 receptor mutant lacking G alpha q/G alpha i coupling causes hypertrophy and bradycardia in transgenic mice. J. Clin. Invest. 115 (2005), 3045–3056.
111. Zimmerman, M.C., Davisson, R.L., Redox signaling in central neural regulation of cardiovascular function. Prog. Biophys. Mol. Biol. 84 (2004), 125–149.