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Journal of Cellular and Molecular Medicine logoLink to Journal of Cellular and Molecular Medicine
. 2007 May 1;8(1):144–152. doi: 10.1111/j.1582-4934.2004.tb00270.x

Redox regulation of angiotensin II siganling in the heart

Dipak K Das 1,, Nilanjana Maulik 1, Rjichard M Engelam 1
PMCID: PMC6740106  PMID: 15090271

Abstract

A large number of studies have demonstrated the role of angiotensin II in cardiac preconditioning against ischemic reperfusion injury. Generally, angiotensin II is a detrimental factor for the heart, and its inhibition with an ACE inhibitor provides cardioprotection. This review provides an explanation for such paradoxical behavior of angiotensin II. Angiotensin II can potentiate the induction of the expression of a variety of redox‐sensitive factors including p38 MAPK, JNK and Akt, IGF‐IR, EGF‐R, and HO‐1 as well as redox‐regulated genes and transcription factors such as NF??B. It becomes increasingly apparent that during the earlier phase, the heart attempts to adapt itself against the detrimental effects of angiotensin II by upregulating several cardioprotective genes and proteins. These genes and proteins are redox‐regulated and the antioxidants or ROS scavengers block their expressions. Interestingly, an identical pattern of cardioprotective proteins and genes are expressed in the preconditioned heart, which are also inhibited with ROS scavengers. It is tempting to speculate that the induction of the expression of the redox‐sensitive cardioprotective proteins is the results of adaptation of the heart against the oxidative stress resulting from angiotensin II; and preconditioning is the net result of harnessing its own protection during ischemic and/or oxidative stress through its ability to trigger redox signaling.

Keywords: angiotnsin II, redox sigaling, preecoditioning, reactive oxygen species, oxidative strees, gene expression, adaptation

References

  • 1. Irani K., Oxidant signaling in vascular cell growth, death, and survival: a review of the roles of reactive oxygen species in smooth muscle and endothelial cell mitogenic and apoptotic signaling, Circ. Res., 87: 179–183, 2000. [DOI] [PubMed] [Google Scholar]
  • 2. Berk B.C., Redox signals that regulate the vascular response to injury, Thromb. Hoemost., 82: 810–817, 1999. [PubMed] [Google Scholar]
  • 3. Lesnefsky E.J., Gudz T.I., Migita C.T., Ikeda‐Saito M., Hassan M.O., Turkaly P.J., Hoppel C.L., Ischemic injury to mitochondrial electron transport in the aging heart: damage to the iron‐sulfur protein subunit of electron transport complex III, Arch. Biochem. Biophys., 385: 117–128, 2001. [DOI] [PubMed] [Google Scholar]
  • 4. Sun J.S., Lu F.J., Huang W.C., Hou S.M., Tsuang Y.H., Hang Y.S., Antioxidant status following acute ischemic limb injury: a rabbit model, Free Radical Res., 31: 9–21, 1999. [DOI] [PubMed] [Google Scholar]
  • 5. Yamashita N., Hoshida S., Otsu K., Asahi M., Kuzuya T., Hori M., Exercise provides direct biphasic cardioprotection via manganese superoxide dismutase activation, J. Exp. Med., 189: 1699–1706, 1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6. Paradies G., Petrosillo G., Pistolese M., Di Venosa N., Federici A., Ruggiero F.M., Decrease in mitochondrial complex I activity in ischemic/reperfused rat heart: involvement of reactive oxygen species and cardiolipin, Circ. Res., 94: 53–59, 2004. [DOI] [PubMed] [Google Scholar]
  • 7. Masini E., Pierpaoli S., Marzocca C., Mannaioni P.F., Pietrangeli P., Mateescu M.A., Zelli M., Federico R., Mondovi B., Protective effects of a plant histaminase in myocardial ischaemia and reperfusion injury in vivo , Biochem. Biophys. Res. Commun., 309: 432–439, 2003. [DOI] [PubMed] [Google Scholar]
  • 8. Novalija E., Kevin L.G., Camara A.K., Bosnjak Z.J., Kampine J.P, Stowe D.F., Reactive oxygen species precede the epsilon isoform of protein kinase C in the anesthetic preconditioning signaling cascade, Anesthesiology, 99: 421–428, 2003. [DOI] [PubMed] [Google Scholar]
  • 9. Turoczi T., Jun L., Cordis G., Morris J.E., Maulik N., Stevens R.G., Das D.K., HFE mutation and dietary iron content interact to increase ischemia/reperfusion injury of the heart in mice, Circ. Res., 92: 1240–1246, 2003. [DOI] [PubMed] [Google Scholar]
  • 10. Halmosi R., Berente Z., Osz E., Toth K., Literati‐Nagy P., Sumegi B., Effect of poly(ADP‐ribose) polymerase inhibitors on the ischemia‐reperfusion‐induced oxidative cell damage and mitochondrial metabolism in Langendorff heart perfusion system, Mol. Pharmacol. 59: 1497–1505, 2001. [DOI] [PubMed] [Google Scholar]
  • 11. Grisham M.B., Jourd'heuil D., Wink D.A., Chronic inflammation and reactive oxygen and nitrogen metabolism: implications in DNA damage and mutagenesis, Aliment. Pharmacol. Therap., 14(suppl 1): 3–9, 2000. [DOI] [PubMed] [Google Scholar]
  • 12. Mates J.M., Perez‐Gomez C., Nunez I., Antioxidant enzymes and human diseases, Clin. Biochem., 32: 595–603, 1999. [DOI] [PubMed] [Google Scholar]
  • 13. Zalba G.J., Beaumont G., San Jose A., Vascular oxidant stress: molecular mechanisms and pathophysiological implications, J. Physiol Biochem., 56: 57–64, 2000. [DOI] [PubMed] [Google Scholar]
  • 14. Yaguchi Y., Satoh H., Wakahara N., Katoh H., Uehara A., Terada H., Fujise Y., Hayashi H., Protective effects of hydrogen peroxide against ischemia/reperfusion injury in perfused rat hearts, Circ. J., 67: 253–258, 2003. [DOI] [PubMed] [Google Scholar]
  • 15. Berges A., Van Nassauw L., Bosmans J., Timmermans J.P., Vrints C., Role of nitric oxide and oxidative stress in ischaemic myocardial injury and preconditioning, Acta Cardiologica, 58: 119–132, 2003. [DOI] [PubMed] [Google Scholar]
  • 16. Novalija E., Varadarajan S.G., Camara A.K., An J., Chen Q., Riess M.L., Hogg N., Stowe D.F., Anesthetic preconditioning: triggering role of reactive oxygen and nitrogen species in isolated hearts, Am. J. Physiol - Heart & Circulatory Physiol., 283: H44–H52, 2002. [DOI] [PubMed] [Google Scholar]
  • 17. Yamamura T., Otani H., Nakao Y., Hattori R., Osako M., Imamura H., Das D.K., Dual involvement of coenzyme Q10 in redox signaling and inhibition of death signaling in the rat heart mitochondria, Antioxidants Redox Signal., 3: 103–112, 2001. [DOI] [PubMed] [Google Scholar]
  • 18. Laderoute K.R., Webster K.A., Hypoxia/reoxygenation stimulates Jun kinase activity through redox signaling in cardiac myocytes, Circ. Res., 80: 336–344, 1997. [DOI] [PubMed] [Google Scholar]
  • 19. Wang Y., De Keulenaer G.W., Lee R.T., Vitamin D(3)‐up‐regulated protein‐1 is a stress‐responsive gene that regulates cardiomyocyte viability through interaction with thioredoxin, J. Biol. Chem., 277: 26496–26500, 2002. [DOI] [PubMed] [Google Scholar]
  • 20. Torres M., Forman H.J., Redox signaling and the MAP kinase pathways, Biofactors, 17: 287–96, 2003. [DOI] [PubMed] [Google Scholar]
  • 21. Patel R.P., Moellering D., Murphy‐Ullrich J., Cell signaling by reactive nitrogen and oxygen species in atherosclerosis, Free Rad. Biol. Med., 28: 1780–1794, 2000. [DOI] [PubMed] [Google Scholar]
  • 22. Berk B.C., Redox signals that regulate the vascular response to injury, Thromb. Hoemost., 82: 810–817, 1999. [PubMed] [Google Scholar]
  • 23. Sundaresan M., Zu‐Xi Y., Ferrans V.J., Irani K., Finkrl T., Requirement for generation of H2O2 for platelet‐derived growth factor signal transduction, Science, 270: 296–299, 1995. [DOI] [PubMed] [Google Scholar]
  • 24. Griendling K.K., Sorescu D., Lassegue B., Ushio‐Fukai M., Modulation of protein kinase activity and gene expression by reactive oxygen species and their role in vascular physiology and pathophysiology, Arterioscler. Thromb. Vasc. Biol., 20: 2175–2183, 2000. [DOI] [PubMed] [Google Scholar]
  • 25. Timmermans P.B., Wong P.C., Chiu A.T., Angiotensin II receptors and angiotensin II receptor antagonists, Pharmacol. Rev., 45: 205–251, 1993. [PubMed] [Google Scholar]
  • 26. Sharma A., Singh M., Possible mechanism of cardioprotective effect of angiotensin preconditioning in isolated rat heart, Eur. J. Pharmacol., 406: 85–92, 2000. [DOI] [PubMed] [Google Scholar]
  • 27. Nakano A., Miura T., Ura N., Suzuki K., Shimamoto K., Role of angiotensin II type I receptor in preconditioning against infarction, Coronary Artery Dis., 8: 343–350, 1997. [DOI] [PubMed] [Google Scholar]
  • 28. Diaz R.J., Wilson G.J., Selective blockade of AT1 angiotensin II receptors abolishes ischemic preconditioning in isolated rabbit hearts, J. Mol. Cell. Cardiol., 29: 129–139, 1997. [DOI] [PubMed] [Google Scholar]
  • 29. Egido J., Vasoactive hormones and renal sclerosis. Kidney Int 49: 578–597, 1996. [DOI] [PubMed] [Google Scholar]
  • 30. Krejcy K., Eichler H.G., Jilma B., Kapiotis S., Wolzt M., Zanaschka G., Gasic S., Schutz W., Wagner O., Influence of angiotensin II on circulating adhesion molecules and blood leukocyte count in vivo , Can. J. Physiol. Pharmacol., 74: 9–14, 1996. [PubMed] [Google Scholar]
  • 31. Kunert‐Radek J., Stepien H., Komorowski J., Pawlikowski M., Stimulatory effect of angiotensin II on the proliferation of mouse spleen lymphocytes in vitro is mediated via both types of angiotensin II receptors, Biochem. Biophys. Res. Commun., 198: 1034–1039, 1994. [DOI] [PubMed] [Google Scholar]
  • 32. Matsubara H., Pathophysiological role of angiotensin II type 2 receptor in cardiovascular and renal diseases, Circ. Res., 83: 1182–1191, 1998. [DOI] [PubMed] [Google Scholar]
  • 33. Pratt R.E., Angiotensin II and the control of cardiovascular structures, J. Am. Soc. Nephrol., 10: 120–128, 1999. [PubMed] [Google Scholar]
  • 34. Matsubara H., Pathophysiological role of angiotensin II type 2 receptor in cardiovascular and renal diseases, Circ. Res., 83: 1182–1191, 1998. [DOI] [PubMed] [Google Scholar]
  • 35. Sadoshima J., Cytokine actions of angiotensin II, Circ. Res., 86: 1187–1189, 2000. [DOI] [PubMed] [Google Scholar]
  • 36. Ruiz‐Ortega M., Lorenzo O., Suzuki Y., Ruperez M., Egido J., Proinflammatory actions of angiotensin II, Curr. Opin. Nephrol. Hypertens., 10: 321–329, 2001. [DOI] [PubMed] [Google Scholar]
  • 37. Irani K., Angiotensin II‐stimulated vascular remodeling: the search for the culprit oxidase, Circ. Res., 88: 858–860, 2001. [DOI] [PubMed] [Google Scholar]
  • 38. Wolf G., Burns K., Harris R., Stahl R.A.K., Thaiss F., Angiotensin II activates the NFkB pathway through AT2 receptors, J. Am. Soc. Nephrol., 11: 430, 2000. [Google Scholar]
  • 39. Morrissey J.J., Klahr S., Differential effects of ACE and AT1 receptor inhibition on chemoattractant and adhesion molecule synthesis, Am. J. Physiol., 274: F580–F586, 1998. [DOI] [PubMed] [Google Scholar]
  • 40. Kim S., Iwao H., Molecular and cellular mechanisms of angiotensin II‐mediated cardiovascular and renal diseases, Pharmacol. Rev., 52: 11–34, 2001. [PubMed] [Google Scholar]
  • 41. Sato M., Engelman R.M., Otani H., Maulik N., Rousou J.A., Flack J.E. III, Deaton D.W., Das D.K., Myocardial Protection by Preconditioning of Heart With Losartan, an Angiotensin II Type 1‐Receptor Blocker: Implication of Bradykinin‐Dependent and Bradykinin‐Independent Mechanisms, Circulation, 102: 346–351, 2000. [DOI] [PubMed] [Google Scholar]
  • 42. Engelman R.M., Rousou J.A., Iyengar J., Das D.K., Captopril, an ACE inhibitor, for optimizing reperfusion after acute myocardial infarction, Ann. Thoracic Surg., 52: 918–926, 1991. [DOI] [PubMed] [Google Scholar]
  • 43. Vegh A., Papp J.G., Parratt J., Attenuation of the antiar‐rhythmic effects of ischemic preconditioning by blockade of bradykinin B2 receptors, Br. J. Pharmacol., 113: 1167–1172, 1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44. Jin Z.‐Q., Chen X., Bradykinin mediates myocardial ischemic preconditioning against free radical injury in guinea‐pig isolated heart, Clin. Exp. Pharmacol. Physiol., 25: 932–935, 1998. [DOI] [PubMed] [Google Scholar]
  • 45. Miki T., Miura T., Ura N., Ogawa T., Suzuki K., Shimamoto K., Ilmira O., Captopril potentiates the myocardial infarct size‐limiting effect of ischemic preconditioning through bradykinin B2 receptor activation, J. Am. Coll. Cardiol., 28: 1616–1622, 1996. [DOI] [PubMed] [Google Scholar]
  • 46. Schwarz E.R., Montino H., Fleischhauer J., Klues H.G., Dahl J.V., Hanrath P., Angiotensin II receptor antagonist EXP 3174 reduces infarct size comparable with enalaprilat and augments preconditioning in the pig heart, Cardiovasc. Drug. Therap., 11: 687–695, 1997. [DOI] [PubMed] [Google Scholar]
  • 47. Engelman R.M., Rousou J.A., Iyengar J., Das D.K., Captopril, an ACE inhibitor, for optimizing reperfusion after acute myocardial infarction, Ann. Thoracic Surg., 52: 918–926, 1991. [DOI] [PubMed] [Google Scholar]
  • 48. Steinberg M.I., Weist S.A., Palkowitz A.D., Non‐peptide Ang II receptor antagonists, Cardiovasc. Drug. Rev., 11: 312–358, 1993. [Google Scholar]
  • 49. Feolde E., Vigne P., Frelin C., Ang II receptor subtypes and biological responses in the rat heart, J. Mol. Cell. Cardiol., 25: 1359–1367, 1993. [DOI] [PubMed] [Google Scholar]
  • 50. Capponi A.M., Distribution and signal transduction of angiotensin II AT1 and AT2 receptors, Blood Press Suppl., 2: 41–46, 1996. [PubMed] [Google Scholar]
  • 51. Miki T., Miura T., Ura N., Ogawa T., Suzuki K., Shimamoto K., Limura O., Captopril potentiates the myocardial infarct size‐limiting effect of ischemic preconditioning through bradykinin B2 receptor activation, J. Am. Coll. Cardiol., 28: 1616–1622, 1996. [DOI] [PubMed] [Google Scholar]
  • 52. Zhu P., Zaugg C.E., Hornstein P.S., Allegrini P.R., Buser P.T., Bradykinin‐dependent cardioprotective effects of losartan against ischemia reperfusion in rat hearts, J. Cardiuovasc. Pharmacol., 33: 785–790, 1999. [DOI] [PubMed] [Google Scholar]
  • 53. Sharma A., Singh M., Effect of ethylisopropyl amiloride, a Na+‐H+ exchange inhibitor, on cardioprotective effect of ischemic and angiotensin preconditioning, Mol. Cell. Biochem., 214: 31–38, 2000. [DOI] [PubMed] [Google Scholar]
  • 54. Nakano A., Miura T., Ura N., Suzuki K., Shimamoto K., Role of angiotensin II type I receptor in preconditioning against infarction, Coronary Artery Dis., 8: 343–350, 1997. [DOI] [PubMed] [Google Scholar]
  • 55. Diaz R.J., Wilson G.J., Selective blockade of AT1 angiotensin II receptors abolishes ischemic preconditioning in isolated rabbit hearts, J. Mol. Cell. Cardiol., 29: 129–139, 1997. [DOI] [PubMed] [Google Scholar]
  • 56. Morris S.D., Yellon D.M., Angiotensin‐converting enzyme inhibitors potentiate preconditioning through bradykinin B2 receptor activation in human heart, J. Am. Coll. Cardiol., 29: 1599–1606, 1997. [DOI] [PubMed] [Google Scholar]
  • 57. Liu Y., Tsuchida A., Cohen M.V., Downey J.M., Pretreatment with angiotensin II activates protein kinase C and limits myocardial infarction in isolated rabbit hearts, J. Mol. Cell. Cardiol., 27: 883–892, 1995. [DOI] [PubMed] [Google Scholar]
  • 58. Vegh A., Papp J.G., Parratt J., Attenuation of the antiarrhythmic effects of ischemic preconditioning by blockade of bradykinin B2 receptors, Br. J. Pharmacol., 113: 1167–1172, 1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59. Miki T., Miura T., Ura N., Ogawa T., Suzuki K., Shimamoto K., Limura O., Captopril potentiates the myocardial infarct size‐limiting effect of ischemic preconditioning through bradykinin B2 receptor activation, J. Am. Coll. Cardiol., 28: 1616–1622, 1996. [DOI] [PubMed] [Google Scholar]
  • 60. Zhu P., Zaugg C.E., Hornstein P.S., Allegrini P.R., Buser P.T., Bradykinin‐dependent cardioprotective effects of losartan against ischemia reperfusion in rathearts, J. Cardiovasc. Pharmacol., 33: 785–790, 1999. [DOI] [PubMed] [Google Scholar]
  • 61. Schwarz E.R., Montino H., Fleischhauer J., Kleus H.G., vom Dahl J., Hanrath P., Angiotensin II receptor antagonist EXP 3174 reduces infarct size comparable with enalaprilat and augments preconditioning in the pig heart, Cardiovasc. Drug Therapy, 11: 687–695, 1997. [DOI] [PubMed] [Google Scholar]
  • 62. Rey F.E., Cifuentes M.E., Kiarash A., Quinn M.T., Pagano P.J., Novel competitive inhibitor of NADPH oxidase assembly attenuates vascular O2‐ and systolic blood pressure in mice, Circ. Res., 89: 408–414, 2001. [DOI] [PubMed] [Google Scholar]
  • 63. Griendling K.K., Sorescu D., Ushio‐Fukai M., NADPH oxidase: role in cardiovascular biology and disease, Circ. Res., 86: 494–501, 2000. [DOI] [PubMed] [Google Scholar]
  • 64. Griendling K.K., Minieri C.A., Ollerenshaw J.D., Alexander R.W., Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells, Circ Res., 74: 1141–1148, 1994. [DOI] [PubMed] [Google Scholar]
  • 65. Rajagopalan S., Kurz S., Munzel T., Tarpey M., Freeman B.A., Griendling K.K., Angiotensin II‐mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation, J. Clin. Invest., 97: 1916–1923, 1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 66. Griendling K., Ollerenshaw J.D., Minieri C.A., Alexander R.W., Angiotensin II stimulates NADH and NADPH activity in cultured vascular smooth muscle cells, Circ. Res., 74: 1141–1148, 1994. [DOI] [PubMed] [Google Scholar]
  • 67. Pagano P.J., Ito Y., Tornheim K., Gallop P.M., Tauber A.I., Cohen R.A., A NADPHoxidase superoxide‐generating system in the rabbit aorta, Am. J. Physiol., 268: H2274–H2280, 1995. [DOI] [PubMed] [Google Scholar]
  • 68. Suh Y., Arnold R.S., Lassegue B., Shi J., Xu X., Sorescu D., Chung A.B., Griendling K.K., Lambeth J.D., Cell transformation by the superoxide‐generating oxidase mox1, Nature, 401: 79–82, 1999. [DOI] [PubMed] [Google Scholar]
  • 69. Lassegue B., Sorescu D., Szocs K., Yin Q.Q., Akers M., Zhang Y., Grant S.L., Lambeth J.D., Griendling K.K., Novel gp91phox homologues in vascular smooth muscle cells nox1 mediates angiotensin II‐induced superoxide formation and redox‐sensitive signaling pathways, Circ. Res., 88: 888–894, 2001. [DOI] [PubMed] [Google Scholar]
  • 70. Das D.K., Maulik N., Preconditioning potentiates redox signaling and converts death signal into survival signal, Arch. Biochem. Biophys., 420: 305–311, 2003. [DOI] [PubMed] [Google Scholar]
  • 71. Das D.K., Maulik N., Evaluation of antioxidant effectiveness in ischemia reperfusion tissue injury, Methods Enzymol., 233: 601–610, 1994. [DOI] [PubMed] [Google Scholar]
  • 72. Maulik N., Goswami S., Galang N., Das D.K., Differential regulation of Bcl‐2, AP‐1 and NFkB on cardiomyocyte apoptosis during myocardial ischemic stress adaptation, FEBS Lett., 443: 331–336, 1999. [DOI] [PubMed] [Google Scholar]
  • 73. Maulik N., Engelman R.M., Flack J.E., Rousou J.A., Deaton D., Das D.K., Ischemic preconditioning reduces apoptosis by upregulating anti‐death gene Bcl‐2, Circulation, 100: II369–II375, 1999. [DOI] [PubMed] [Google Scholar]
  • 74. Das D.K., Maulik N., Sato M., Ray P., Reactive oxygen species function as second messengers during ischemic preconditioning of heart, Mol. Cell Biochem., 196: 59–67, 1999. [PubMed] [Google Scholar]
  • 75. Bass A.S., Berk B.C., ROS can directly activate JNK, Circ. Res., 77: 29–36, 1995. [DOI] [PubMed] [Google Scholar]
  • 76. Abe J.‐I., Kusuhara M., Ulevitch R., Berk B.C., Lee J.‐D., Big mitogen‐activated protein kinase 1 (BMK1) is a redoxsensitive kinase, J. Biol. Chem., 271: 16586–16590, 1996. [DOI] [PubMed] [Google Scholar]
  • 77. Ushio‐Fukai M., Alexander R.W., Akers M., Griendling K.K., P38 Mitogen‐activated protein kinase is a critical component of the redox‐sensitive signaling pathways activated by angiotensin II, J. Biol. Chem., 273: 15022–15029, 1998. [DOI] [PubMed] [Google Scholar]
  • 78. Bekay R.E., Alvarez M., Monteseirin J., Alba G., Chacon P., Vega A., Martin‐Nieto J., Jimenez J., Pintado E., Bedoya F.J., Sobrino F., Oxidative stress is a critical mediator of the angiotensin II signal in human neutrophils: involvement of mitogen‐activated protein kinase, calcineurin, and the transcription factor NFkB, Blood, 102: 662–671, 2003. [DOI] [PubMed] [Google Scholar]
  • 79. Wenzel S., Taimor G., Piper H.M., Schlueter K.‐D., Redox‐sensitive intermediates mediate angiotensin IIinduced p38 MAP kinase activation, AP‐1 binding activity, and TGFβ expression in adult ventricular cardiomyocytes, FASEB J., 15: 2291–2293, 2001. [DOI] [PubMed] [Google Scholar]
  • 80. Ushio‐Fukai M., Alexander R.W., Akers M., Yin Q.Q., Fujio Y., Walsh K., Griendling K.K., Reactive oxygen species mediate the activation of Akt/protein kinase B by angiotensin II in vascular smooth muscle cells, J. Biol. Chem., 274: 22699–22704, 1999. [DOI] [PubMed] [Google Scholar]
  • 81. Gorin Y., Kim N.‐H., Feliers D., Bhandari B., Ghosh‐Choudhury G., Abboud H.A., Angiotensin II activates Akt/protein kinase B by an arachidonic acid/redox‐dependent pathway and independent of phosphoinositide 3 kinase, FASEB J., 15: 1909–1920, 2001. [DOI] [PubMed] [Google Scholar]
  • 82. Du J., Peng T., Scheidegger K.J., Delafontaine P., Angiotensin II activation of insulin‐like growth factor‐1 receptor transcription is mediated by a tyrosine kinasedependent redox‐sensitive mechanism, Arterioscler. Thromb. Vasc. Biol., 19: 2119–2126, 1999. [DOI] [PubMed] [Google Scholar]
  • 83. Ushio‐Fukai M., Griendling K.K., Becker P.L., Hilenski L., Halleran S., Alexander R.W., Epidermal growth factor receptor transactivation by angiotensin II requires reactive oxygen species in vascular smooth muscle cells, Arterioscler. Thromb. Vasc. Biol., 21: 489–495, 2001. [DOI] [PubMed] [Google Scholar]
  • 84. Mueller C., Baudler S., Welzel H., Bohm M., Nickenig G., Identification of a novel redox‐sensitive gene Id3, which mediates angiotensin II‐induced cell growth, Circulation, 105: 2423–2428, 2002. [DOI] [PubMed] [Google Scholar]
  • 85. Aizawa T., Ishizaka N., Taguchi J., Kimura S., Kurokawa K., Ohno M., Balloon injury does not induce heme oxygenase 1 expression, but administration of hemin inhibits neointimal formation in balloon‐injured rat carotid artery, Biochem. Biophys. Res. Commun., 261: 302–307, 1999. [DOI] [PubMed] [Google Scholar]
  • 86. Ishizaka N., Griedling K.K., Heme oxygenase 2 is regulated by angiotensin II in rat vascular smooth muscle cells, Hypertension, 29: 790–795, 1997. [DOI] [PubMed] [Google Scholar]
  • 87. Maulik N., Das D.K., Potentiation of angiogenic response by ischemic and hypoxic preconditioning of the heart, J. Cell. Mol. Med., 6: 13–24, 2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 88. Cuevas P., Carceller F., Gimenez‐Gallego G., Fibroblast growth factors in myocardial ischemia / reperfusion injury and ischemic preconditioning, J. Cell. Mol. Med., 5: 132–142, 2001. [DOI] [PMC free article] [PubMed] [Google Scholar]

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