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HO-1/HSP32 and Cardiac Stress Signaling

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Heat Shock Proteins in Signaling Pathways

Part of the book series: Heat Shock Proteins ((HESP,volume 17))

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Abstract

In recent years, increased attention has been gained in elucidating the therapeutic potential of heme oxygenase-1 (HO-1), a rate limiting enzyme involved in the heme metabolism and their pathophysiology of various cardiovascular diseases and heart failure models. HO-1 exhibits multi-faceted role in the systemic regulation of redox, energy homeostasis and boosts the survival and vascular function in various cardiomyopathies. Induction of HO-1 has been known to modulate vascular cell proliferation, inflammation, endothelialization, oxidative damages, apoptosis, fibrosis, ischemic/perfusion injuries, neovascularization and prevent atherosclerotic lesion formation in the pathophysiology of experimental cardiomyopathies. The present chapter summarizes the cardioprotective mechanism of HO-1 and their molecular regulations, potential interaction/cross talk with myocardial cell survival and death signaling cascade. This chapter further reveals the genetic ablation of HO-1, overexpression of transgenic mutants and ascertains the role of HO-1 in cardiac stem cell therapy and xenograft survival in ischemic hearts. Eventually, we examined the pharmacological modulators of HO-1 from the natural and dietary therapeutic polyphenols and their mode of cardioprotection in both in vivo and in vitro models. In this context, the present chapter will append the existing knowledge of HO-1 and their regulation in the cardiac stress signaling cascades.

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Abbreviations

AP-1:

activator protein-1

AP-2:

activator protein-2

Bach1:

broad-complex, tramtrack and bric-a-brac and cap’n’collar homology 1

CAM:

cell adhesion molecule

CaMKKb:

Ca2+/calmodulin-dependent protein kinase

CO:

carbon monoxide

CREB1:

cAMP response element-binding protein 1

CTGF:

connective tissue growth factor

DCM:

diabetic cardiomyopathy

EBP:

emopamil-binding protein

ER:

endoplasmic reticulum

HO-1:

heme oxygenase-1

Hsp32:

heat shock protein 32

ICAM1:

intracellular adhesion molecule 1

IL:

interleukin

MAPK:

mitogen activated protein kinase

NF-κB:

nuclear factor-κB

Nrf2:

nuclear factor erythroid 2-related factor 2

PKC1:

protein kinase C1

SDF:

stromal cell-derived factor

SER:

smooth endoplasmic reticulum

STATx:

signal transducers and activators of transcription x

TNF-α:

tumor necrosis factor-α

VCAM1:

vascular cell adhesion molecule 1

References

  • Abraham NG, Lin JH, Schwartzman ML, Levere RD, Shibahara S (1988) The physiological significance of heme oxygenase. Int J Biochem 20:543–558

    Article  CAS  PubMed  Google Scholar 

  • Abraham NG, Rezzani R, Rodella L, Kruger A, Taller D, Li Volti G, Goodman AI, Kappas A (2004) Overexpression of human heme oxygenase-1 attenuates endothelial cell sloughing in experimental diabetes. Am J Physiol Heart Circ Physiol 287:H2468–H2477

    Article  CAS  PubMed  Google Scholar 

  • Abuarqoub H, Green CJ, Foresti R, Motterlini R (2007) Curcumin reduces cold storage-induced damage in human cardiac myoblasts. Exp Mol Med 39:139–148

    Article  CAS  PubMed  Google Scholar 

  • Agarwal A, Nick HS (2000) Renal response to tissue injury: lessons from heme oxygenase-1 gene ablation and expression. J Am Soc Nephrol 11:965–973

    CAS  PubMed  Google Scholar 

  • Aggeli IKS, Gaitanaki C, Beis I (2006) Involvement of JNKs and p38-MAPK/MSK1 pathways in H202-induced upregulation of heme oxygenase-1 mRNA in H9c2 cells. Cell Signal 18(10):1801–1812

    Article  CAS  PubMed  Google Scholar 

  • Bai Y, Chen Q, Sun YP, Wang X, Lv L, Zhang LP, Liu JS, Zhao S, Wang XL (2017) Sulforaphane protection against the development of doxorubicin-induced chronic heart failure is associated with Nrf2 upregulation. Cardiovasc Ther 35. https://doi.org/10.1111/1755-5922.12277

    Article  CAS  Google Scholar 

  • Barbagallo I, Galvano F, Frigiola A, Cappello F, Riccioni G, Murabito P, D’Orazio N, Torella M, Gazzolo D, Li Volti G (2013) Potential therapeutic effects of natural heme oxygenase-1 inducers in cardiovascular diseases. Antioxid Redox Signal 18:507–521

    Article  CAS  PubMed  Google Scholar 

  • Brunt KR, Fenrich KK, Kiani G, Tse MY, Pang SC, Ward CA, Melo LG (2006) Protection of human vascular smooth muscle cells from H2O2-induced apoptosis through functional codependence between HO-1 and AKT. Arterioscler Thromb Vasc Biol 26:2017–2034

    Article  CAS  Google Scholar 

  • Brunt KR, Tsuji MR, Lai JH, Kinobe RT, Durante W, Claycomb WC, Ward CA, Melo LG (2009) Heme oxygenase-1 inhibits pro-oxidant induced hypertrophy in HL-1 cardiomyocytes. Exp Biol Med (Maywood) 234:582–594

    Article  CAS  PubMed Central  Google Scholar 

  • Cao J, Sodhi K, Puri N, Monu SR, Rezzani R, Abraham NG (2011) High fat diet enhances cardiac abnormalities in SHR rats: protective role of heme oxygenase-adiponectin axis. Diabetol Metab Syndr 37:1–13

    Google Scholar 

  • Cao J, Tsenovoy PL, Thompson EA, Falck JR, Touchon R, Sodhi K, Rezzani R, Shapiro JI, Abraham NG (2015) Agonists of epoxyeicosatrienoic acids reduce infarct size and ameliorate cardiac dysfunction via activation of HO-1 and Wnt1 canonical pathway. Prostaglandins Other Lipid Mediat 116:76–86

    Article  PubMed  CAS  Google Scholar 

  • Chen S, Kapturczak MH, Wasserfall C, Glushakova OY, Campbell-Thompson M, Deshane JS, Joseph R, Cruz PE, Hauswirth WW, Madsen KM, Croker BP, Berns KI, Atkinson MA, Flotte TR, Tisher CC, Agarwal A (2005) Interleukin 10 attenuates neointimal proliferation and inflammation in arotic allografts by a heme oxygenase-dependent pathway. Proc Natl Acad Sci U S A 102:7521–7526

    Google Scholar 

  • Chen SY, Hsiao G, Hwang HR, Cheng PY, Lee YM (2006) Tetramethylpyrazine induces heme oxygenase-1 expression and attenuates myocardial ischemia/reperfusion injury in rats. J Biomed Sci 13:731–740

    Article  CAS  PubMed  Google Scholar 

  • Chen HG, Xie KL, Han HZ, Wang WN, Liu DQ, Wang GL, Yu YH (2013) Heme oxygenase-1 mediates the anti-inflammatory effect of molecular hydrogen in LPS-stimulated RAW 264.7 macrophages. Int J Surg 11:1060–1066

    Article  PubMed  Google Scholar 

  • Choi HC, Lee KY, Lee DH, Kang YJ (2009) Heme oxygenase-1 induced by aprotinin inhibits vascular smooth muscle cell proliferation through cell cycle arrest in hypertensive rats. Korean J Physiol Pharmacol 13:309–313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Collino M, Pini A, Mugelli N, Mastroianni R, Bani D, Fantozzi R, Papucci L, Fazi M, Masini E (2013) Beneficial effect of prolonged heme oxygenase 1 activation in a rat model of chronic heart failure. Dis Model Mech 6:1012–1020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Csonka C, Varga E, Kovacs P, Ferdinandy P, Blasig IE, Szilvassy Z, Tosaki A (1999) Heme oxygenase and cardiac function in ischemic/reperfused rat hearts. Free Radic Biol Med 27:119–126

    Article  CAS  PubMed  Google Scholar 

  • Dai M, Wu L, He Z, Zhang S, Chen C, Xu X, Wang P, Gruzdev A, Zeldin DC, Wang DW (2015) Epoxyeicosatrienoic acids regulate macrophage polarization and prevent LPS-induced cardiac dysfunction. J Cell Physiol 230:2108–2119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng YM, Wu BJ, Witting PK, Stocker R (2004) Probucol protects against smooth muscle cell proliferation by upregulating heme oxygenase-1. Circulation 110:1855–1860

    Article  CAS  PubMed  Google Scholar 

  • Deng C, Sun Z, Tong G, Yi W, Ma L, Zhao B, Cheng L, Zhang J, Cao F, Yi D (2013) α-Lipoic acid reduces infarct size and preserves cardiac function in rat myocardial ischemia/reperfusion injury through activation of PI3K/Akt/Nrf2 pathway. PLoS One 8:e58371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deramaudt BM, Braunstein S, Remy P, Abraham NG (1998) Gene transfer of human heme oxygenase into coronary endothelial cells potentially promotes angiogenesis. J Cell Biochem 68:121–127

    Article  CAS  PubMed  Google Scholar 

  • Eyssen-Hernandez R, Ladoux A, Frelin C (1996) Differential regulation of cardiac heme oxygenase-1 and vascular endothelial growth factor mRNA expressions by hemin, heavy metals, heat shock and anoxia. FEBS Lett 382:229–233

    Article  CAS  PubMed  Google Scholar 

  • Fan Z, Han Y, Ye Y, Liu C, Cai H (2017) L-carnitine preserves cardiac function by activating p38 MAPK/Nrf2 signalling in hearts exposed to irradiation. Eur J Pharmacol 804:7–12

    Article  CAS  PubMed  Google Scholar 

  • Farhangkhoee H, Khan ZA, Mukherjee S, Cukiernik M, Barbin YP, Karmazyn M, Chakrabarti S (2003) Heme oxygenase in diabetes-induced oxidative stress in the heart. J Mol Cell Cardiol 35:1439–1448

    Article  CAS  PubMed  Google Scholar 

  • Gajos-Draus A, Duda M, Beresewicz A (2017) Cardiac and renal upregulation of Nox2 and NF-Ò¡B and repression of Nox4 and Nrf2 in season- and diabetes-mediated models of vascular oxidative stress in guinea-pig and rat. Physiol Rep 5:e13474

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gomez-Hurtado I, Zapater P, Bellot P, Pascual S, Perez-Mateo J, Such J, Frances R (2011) Interleukin-10-mediated heme oxygenase 1-induced underlying mechanism in inflammatory down-regulation by norfloxacin in cirrhosis. Hepatology 53:935–944

    Article  CAS  PubMed  Google Scholar 

  • Gu J, Song ZP, Gui DM, Hu W, Chen YG, Zhang DD (2012) Resveratrol attenuates doxorubicin-induced cardiomyocyte apoptosis in lymphoma nude mice by heme oxygenase-1 induction. Cardiovasc Toxicol 12:341–349

    Article  CAS  PubMed  Google Scholar 

  • Guo N, Zhang N, Yan L, Cao X, Wang J, Wang Y (2017) Correlation between genetic polymorphisms within the MAPK1/HIF-1/HO-1 signaling pathway and risk or prognosis of perimenopausal coronary artery disease. Clin Cardiol 40:597–604

    Article  PubMed  PubMed Central  Google Scholar 

  • Han F, Guo Y, Xu L, Hou N, Han F, Sun X (2015) Induction of haemeoxygenase-1 directly improves endothelial function in isolated aortas from obese rats through the Ampk-Pi3k/Akt-Enos pathway. Cell Physiol Biochem 36:1480–1490

    Article  CAS  PubMed  Google Scholar 

  • He M, Siow RC, Sugden D, Gao L, Cheng X, Mann GE (2011) Induction of HO-1 and redox signaling in endothelial cells by advanced glycation end products: a role for Nrf2 in vascular protection in diabetes. Nutr Metab Cardiovasc Dis 21:277–285

    CAS  PubMed  Google Scholar 

  • Hinkel R, Lange P, Petersen B, Gottlieg E, Ng JK, Finger S, Horstkotte J, Lee S, Thormann M, Knorr M, El-Aouni C, Boekstegers P, Reichart B, Wenzel P, Niemann H, Kupatt C (2015) Heme oxygenase-1 gene therapy provides cardioprotection via control of post-ischemic inflammation: an experimental study in a pre-clinical pig model. J Am Coll Cardiol 66:154–165

    Article  CAS  PubMed  Google Scholar 

  • Hoshida S, Nishida M, Yamashita N, Igarashi J, Aoki K, Hori M, Kuzuya T, Tada M (1996) Heme oxygenase-1 expression and its relation to oxidative stress during primary culture of cardiomyocytes. J Mol Cell Cardiol 28:1845–1855

    Article  CAS  PubMed  Google Scholar 

  • Hua W, Chen Q, Gong F, Xie C, Zhou S, Gao L (2013) Cardioprotection of H2S by downregulating iNOS and upregulating HO-1 expression in mice with CVB3-induced myocarditis. Life Sci 93:949–954

    Article  CAS  PubMed  Google Scholar 

  • Hwa JS, Jin YC, Lee YS, Ko YS, Kim YM, Shi LY, Kim HJ, Lee JH, Ngoc TM, Bae KH, Kim YS, Chang KC (2012) 2-methoxycinnamaldehyde from Cinnamomum cassia reduces rat myocardial ischemia and reperfusion injury in vivo due to HO-1 induction. J Ethnopharmacol 139:605–615

    Article  CAS  PubMed  Google Scholar 

  • Issan Y, Kornowski R, Aravot D, Shainberg A, Laniado-Schwartzman M, Sodhi K, Abraham NG, Hochhauser E (2014) Heme oxygenase-1 induction improves cardiac function following myocardial ischemia by reducing oxidative stress. PLoS One 9:e92246

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jancsó G, Cserepes B, Gasz B, Benkó L, Borsiczky B, Ferenc A, Kürthy M, Rácz B, Lantos J, Gál J, Arató E, Sínayc L, Wéber G, Róth E (2007) Expression and protective role of heme oxygenase-1 in delayed myocardial preconditioning. Ann N Y Acad Sci 1095:251–261

    Article  PubMed  CAS  Google Scholar 

  • Jeney V, Balla J, Yachie A, Varga Z, Vercellotti GM, Eaton JW, Balla G (2002) Pro-oxidant and cytotoxic effects of circulating heme. Blood 100:879–887

    Article  CAS  PubMed  Google Scholar 

  • Jin X, Xu Z, Cao J, Yan R, Xu R, Ran R, Ma Y, Cai W, Fan R, Zhang Y, Zhou X, Li Y (2017a) HO-1/EBP interaction alleviates cholesterol-induced hypoxia through the activation of the AKT and Nrf2/mTOR pathways and inhibition of carbohydrate metabolism in cardiomyocytes. Int J Mol Med 39:1409–1420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin X, Xu Z, Fan R, Wang C, Ji W, Ma Y, Cai W, Zhang Y, Yang N, Zou S, Zhou X, Li Y (2017b) HO-1 alleviates cholesterol-induced oxidative stress through activation of Nrf2/ERK and inhibition of PI3K/AKT pathways in endothelial cells. Mol Med Rep 16:3519–3527

    Article  CAS  PubMed  Google Scholar 

  • Kietzmann T, Samoylenko A, Immenschuh S (2003) Transcriptional regulation of heme oxygenase-1 gene expression by MAP kinases of the JNK and p38 pathways in primary cultures of rat hepatocytes. J Biol Chem 278:17927–17936

    Article  CAS  PubMed  Google Scholar 

  • Kim YM, Ha YM, Jin YC, Shi LY, Lee YS, Kim HJ, Seo HG, Choi JS, Kim YS, Kang SS, Lee JH, Chang KC (2009) Palmatine from Coptidis rhizoma reduces ischemia-reperfusion-mediated acute myocardial injury in the rat. Food Chem Toxicol 47:2097–2102

    Article  CAS  PubMed  Google Scholar 

  • Kim JE, Sung JY, Woo CH, Kang YJ, Lee KY, Kim HS, Kwun WH, Choi HC (2011) Cilostazol inhibits vascular smooth muscle cell proliferation and reactive oxygen species production through activation of AMP-activated protein kinase induced by heme oxygenase-1. Korean J Physiol Pharmacol 15:203–210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Konrad FM, Knausberg U, Hone R, Ngamsri KC, Reutershan J (2016) Tissue heme oxygenase-1 exerts anti-inflammatory effects of LPS-induced pulmonary inflammation. Mucosal Immunol 9:98–111

    Article  CAS  PubMed  Google Scholar 

  • Ku HC, Lee SY, Yang KC, Kuo YH, Su MJ (2016) Modification of caffeic acid with pyrrolidine enhances antioxidant ability by activating AKT/HO-1 pathway in heart. PLoS One 11:e0148545

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kusmic C, L’abbate A, Sambuceti G, Drummond G, Barsanti C, Matteucci M, Cao J, Piccolomini F, Cheng J, Abraham NG (2010) Improved myocardial perfusion in chronic diabetic mice by the up-regulation of pLKB1 and AMPK signaling. J Cell Biochem 109:1033–1044

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kusmic C, Barsanti C, Matteucci M, Vesentini N, Pelosi G, Abraham NG, L’Abbate A (2014) Up-regulation of heme oxygenase-1 after infarct initiation reduces mortality, infarct size and left ventricular remodeling: experimental evidence and proof of concept. J Transl Med 12:89

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuvin JT, Dave DM, Sliney KA, Mooney P, Patel AR, Kimmelstiel CD, Karas RH (2006) Effects of extended-release niacin on lipoprotein particle size, distribution, and inflammatory markers in patients with coronary artery disease. Am J Cardiol 98:743–745

    Article  CAS  PubMed  Google Scholar 

  • L’Abbate A, Neglia D, Vecoli C, Novelli M, Ottaviano V, Baldi S, Barsachhi R, Paolicchi A, Masiello P, Drummond GS, McClung JA, Abraham NG (2007) Beneficial effect of heme oxygenase-1 expression on myocardial ischemia-reperfusion involves an increase in adiponectin in mildly diabetic rats. Am J Physiol Heart Circ Physiol 293:H3532–H3541

    Article  PubMed  CAS  Google Scholar 

  • Lakkisto P, Palojoki E, Bäcklund T, Saraste A, Tikkanen I, Voipio-Pulkki LM, Pulkki K (2002) Expression of heme oxygenase-1 in response to myocardial infarction in rats. J Mol Cell Cardiol 34:1357–1365

    Article  CAS  PubMed  Google Scholar 

  • Lakkisto P, Siren JM, Kytö V, Forsten H, Laine M, Pulkki K, Tikkanen I (2011) Heme oxygenase-1 induction protects the heart and modulates cellular and extracellular remodelling after myocardial infarction in rats. Exp Biol Med (Maywood) 236:1437–1448

    Article  CAS  Google Scholar 

  • Lee TS, Chau LY (2002) Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med 8:240–246

    Article  CAS  PubMed  Google Scholar 

  • Lee YS, Kang YJ, Kim HJ, Park MK, Seo HG, Lee JH, Yun-Choi HS, Chang KC (2006) Higenamine reduces apoptotic cell death by induction of heme oxygenase-1 in rat myocardial ischemia-reperfusion injury. Apoptosis 11:1091–1100

    Article  CAS  PubMed  Google Scholar 

  • Lee YM, Cheng PY, Chim LS, Kung CW, Ka SM, Chung MT, Sheu JR (2011) Baicalein, an active component of Scutellaria baicalensis, Georgi, improves cardiac contractile function in endotoxaemic rats via induction of heme oxygenase-1 and suppression of inflammatory responses. J Ethnopharmacol 135:179–185

    Article  CAS  PubMed  Google Scholar 

  • Lee TM, Lin SZ, Chang NC (2014) Antiarrhythmic effect of lithium in rats after myocardial infarction by activation of Nrf2/HO-1 signaling. Free Radic Biol Med 77:71–81

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Hulderman T, Salmen R, Chapman R, Leonard SS, Young SH, Shvedova A, Luster MI, Simeonova PP (2007) Cardiovascular effects of pulmonary exposure to single-wall carbon nanotubes. Environ Health Perspect 115:377–382

    Article  CAS  PubMed  Google Scholar 

  • Li FY, Lam KS, Tse HF, Chen C, Wang Y, Vanhoutte PM, Xu A (2012) Endothelium-selective activation of AMP-activated protein kinase prevents diabetes mellitus-induced impairment in vascular function and reendothelialization via induction of heme oxygenase-1 in mice. Circulation 126:1267–1277

    Article  CAS  PubMed  Google Scholar 

  • Liang J, Li L, Sun Y, He W, Wang X, Su Q (2017) The protective effect of activating Nrf2 / HO-1 signaling pathway on cardiomyocyte apoptosis after coronary microembolization in rats. BMC Cardiovasc Disord 17:272

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liao HH, Zhu JX, Feng H, Ni J, Zhang N, Chen S, Liu HJ, Yang Z, Deng W, Tang QZ (2017) Myricetin possesses potential protective effects on diabetic cardiomyopathy through inhibiting IÒ¡Bα/NFÒ¡B and enhancing Nrf2/HO-1. Oxidative Med Cell Longev 2017:8370593

    Article  CAS  Google Scholar 

  • Lin Q, Weis S, Yang G, Weng YH, Heiston R, Rish K, Smith A, Bordner J, Polte T, Gaunitz F, Dennery PA (2007) Heme oxygenase-1 protein localizes to the nucleus and activates transcription factors important in oxidative stress. J Biol Chem 282:20621–20633

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Wei J, Peng DH, Layne MD, Yet SF (2005) Absence of heme oxygenase-1 exacerbates myocardial ischemia/reperfusion injury in diabetic mice. Diabetes 54:778–784

    Article  CAS  PubMed  Google Scholar 

  • Liu XM, Peyton KJ, Ensenat D, Wang H, Hannink M, Alam J, Durante W (2007) Nitric oxide stimulates heme oxygenase-1 gene transcription via the Nrf2/ARE complex to promote vascular smooth muscle cell survival. Cardiovasc Res 75:381–389

    Article  CAS  PubMed  Google Scholar 

  • Liu XM, Peyton KJ, Shebib AR, Wang H, Korthuis RJ, Durante W (2011) Activation of AMPK stimulates heme oxygenase-1 gene expression and human endothelial cell survival. Am J Physiol Heart Circ Physiol 300:H84–H93

    Article  CAS  PubMed  Google Scholar 

  • Liu XM, Peyton KJ, Durante W (2017) Ammonia promotes endothelial cell survival via the heme oxygenase-1-mediated release of carbon monoxide. Free Radic Biol Med 102:37–46

    Article  CAS  PubMed  Google Scholar 

  • Lu R, Peng J, Xiao L, Deng HW, Li YJ (2002) Heme oxygenase-1 pathway is involved in delayed protection induced by heat stress against cardiac ischemia-reperfusion injury. Int J Cardiol 82:133–140

    Article  PubMed  Google Scholar 

  • Lu HH, Sheng ZQ, Wang Y, Zhang L (2010) Levels of soluble adhesion molecules in patients with various clinical presentations of coronary atherosclerosis. Chin Med J 123:3123–3126

    PubMed  Google Scholar 

  • Luo J, Weaver MS, Cao B, Dennis JE, Van Biber B, Laflamme MA, Allen MD (2014) Cobalt protoporphyrin pretreatment protects human embryonic stem cell-derived cardiomyocytes from hypoxia/reoxygenation injury in vitro and increases graft size and vascularization in vivo. Stem Cells Transl Med 3:734–744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Madamanchi NR, Vendrov A, Runge MS (2005) Oxidative stress and vascular disease. Aterioscler Thromb Vasc Biol 25:29–38

    Article  CAS  Google Scholar 

  • Maines MD, Kappas A (1974) Cobalt induction of hepatic heme oxygenase; with evidence that cytochrome P-450 is not essential for this enzyme activity. Proc Natl Acad Sci U S A 71:4293–4297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maines MD, Kappas A (1975) Cobalt stimulation of heme degradation in the liver. Dissociation of microsomal oxidation of heme from cytochrome P-450. J Biol Chem 250:4171–4177

    CAS  PubMed  Google Scholar 

  • Maines MD, Kappas A (1976) The induction of heme oxidation in various tissues by trace metals: evidence for the catabolism of endogenous heme by hepatic heme oxygenase. Ann Clin Res 17:39–46

    Google Scholar 

  • Maines MD, Trakshel GM, Kutty RK (1986) Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible. J Biol Chem 261:411–419

    CAS  PubMed  Google Scholar 

  • Man W, Ming D, Fang D, Chao L, Jing C (2014) Dimethyl sulfoxide attenuates hydrogen peroxide-induced injury in cardiomyocytes via heme oxygenase-1. J Cell Biochem 115:1159–1165

    Article  CAS  PubMed  Google Scholar 

  • Mao X, Wang T, Liu Y, Irwin MG, Ou JS, Liao XL, Gao X, Xu Y, Ng KF, Vanhoutte PM, Xia Z (2013) N-acetylcysteine and allopurinol confer synergy in attenuating myocardial ischemia injury via restoring HIF-1a/HO-1 signaling in diabetic rats. PLoS One 8:e68949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCoubrey WK Jr, Ewing JF, Maines MD (1992) Human heme oxygenase-2: characterization and expression of a full-length cDNA and evidence suggesting that the two HO-2 transcripts may differ by choice of polyadenylation signal. Arch Biochem Biophys 295:13–20

    Article  CAS  PubMed  Google Scholar 

  • McNally SJ, Harrison EM, Ross JA, Garden OJ, Wigmore SJ (2007) Curcumin induces heme oxygenase 1 through generation of reactive oxygen species, p38 activation and phosphatase inhibition. Int J Mol Med 19:165–172

    CAS  PubMed  Google Scholar 

  • Melo LG, Agrawal R, Zhang L, Rezvani M, Mangi AA, Ehsan A, Griese DP, Dell’Acqua G, Mann MJ, Oyama J, Yet SF, Layne MD, Perrella MA, Dzau VJ (2002) Gene therapy strategy for long-term myocardial protection using adeno-associated virus-mediated delivery of heme oxygenase gene. Circulation 105:602–607

    Article  CAS  PubMed  Google Scholar 

  • Meng D, Wang X, Chang Q, Hitron A, Zhang Z, Xu M, Chen G, Luo J, Jiang B, Fang J, Shi X (2010) Arsenic promotes angiogenesis in vitro via a heme oxygenase-1-dependent mechanism. Toxicol Appl Pharmacol 244:291–299

    Article  CAS  PubMed  Google Scholar 

  • Meyers CD, Kamanna VS, Kashyap ML (2004) Niacin therapy in atherosclerosis. Curr Opin Lipidol 15:659–665

    Article  CAS  PubMed  Google Scholar 

  • Montellano PR (2000) The mechanism of heme oxygenase. Curr Opin Chem Biol 4:221–227

    Article  CAS  PubMed  Google Scholar 

  • Motterlini R, Foresti R, Bassi R, Green CJ (2000) Curcumin, an antioxidant and anti-inflammatory agent, induces heme oxygenase-1 and protects endothelial cells against oxidative stress. Free Radic Biol Med 28:1303–1312

    Article  CAS  PubMed  Google Scholar 

  • Mylroie H, Dumont O, Bauer A, Thornton CC, Mackey J, Calay D, Hamdulay SS, Choo JR, Boyle JJ, Samarel AM, Randi AM, Evans PC, Mason JC (2015) PKCe-CREB-Nrf2 signalling induces HO-1 in the vascular endothelium and enhances resistance to inflammation and apoptosis. Cardiovasc Res 106:509–519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakashima Y, Raines EW, Plump AS, Breslow JL, Ross R (1998) Upregulation of VCAM-1 and ICAM-1 at atherosclerosis-prone sites on the endothelium in the ApoE-deficient mouse. Aterioscler Thromb Vasc Biol 18:842–851

    Article  CAS  Google Scholar 

  • Novo G, Cappello F, Rizzo M, Fazio G, Zambuto S, Tortorici E, Marino Gammazza A, Corrao S, Zummo G, De Macario EC, Macario AJ, Assennato P, Novo S, Li Volti G (2011) Hsp60 and heme oxygenase-1 (Hsp32) in acute myocardial infarction. Transl Res 157:285–292

    Article  CAS  PubMed  Google Scholar 

  • Ono K, Goto Y, Takagi S, Baba S, Tago N, Nonogi H, Iwai N (2004) A promoter variant of the heme oxygenase-1 gene may reduce the incidence of ischemic heart disease in Japanese. Atherosclerosis 173:315–319

    Article  CAS  PubMed  Google Scholar 

  • Otterbein LE, Soares MP, Yamashita K, Bach FH (2003) Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 24:449–455

    Article  CAS  PubMed  Google Scholar 

  • Pachori AS, Melo LG, Zhang L, Solomon SD, Dzau VJ (2006) Chronic recurrent myocardial ischemic injury is significantly attenuated by pre-emptive adeno-associated virus heme oxygenase-1 gene delivery. J Am Coll Cardiol 47:635–643

    Article  CAS  PubMed  Google Scholar 

  • Panneerselvam L, Raghunath A, Perumal E (2017) Differential expression of myocardial heat shock proteins in rats acutely exposed to fluoride. Cell Stress Chaperones 22:743–750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Posa A, Szabo R, Kupai K, Berko AM, Veszelka M, Szucs G, Borzsei D, Gyongyosi M, Pavo I, Deim Z, Szilvassy Z, Juhasz B, Varga C (2017) Cardioprotective effect of selective estrogen receptor modulator raloxifene are mediated by heme oxygenase in estrogen-deficient rat. Oxidative Med Cell Longev 2017:2176749

    Article  CAS  Google Scholar 

  • Pullikotil P, Chen H, Muniyappa R, Greenberg CC, Yang S, Reiter CE, Lee JW, Chung JH, Quon MJ (2012) Epigallocatechin gallate induces expression of heme oxygenase-1 in endothelial cells via p38 MAPK and Nrf2 that suppresses proinflammatory actions of TNFα. J Nutr Biochem 23:1134–1145

    Article  CAS  PubMed  Google Scholar 

  • Reichard JF, Motz GT, Puga A (2007) Heme oxygenase-1 induction by NRF2 requires inactivation of the transcriptional repressor BACH1. Nucleic Acids Res 35:7074–7086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roos TU, Heiss EH, Schwaiberger AV, Schachner D, Sroka IM, Oberan T, Vollmar AM, Dirsch VM (2011) Caffeic acid phenethyl ester inhibits PDGF-induced proliferation of vascular smooth muscle cells via activation of p38 MAPK, HIF-1α, and heme oxygenase-1. J Nat Prod 74:352–356

    Article  CAS  PubMed  Google Scholar 

  • Rucker M, Schafer T, Roesken F, Spitzer WJ, Bauer M, Menger MD (2001) Reduction of inflammatory response in composite flap transfer by local stress conditioning-induced heat-shock protein 32. Surgery 129:292–301

    Article  CAS  PubMed  Google Scholar 

  • Ryter SW, Alam J, Choi AM (2006) Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86:583–650

    Article  CAS  PubMed  Google Scholar 

  • Sambuceti G, Morbelli S, Vanella L, Kusmic C, Marini C, Massollo M, Augeri C, Corselli M, Ghersi C, Chiavarina B, Rodella LF, L’Abbate A, Drummond G, Abraham NG, Frassoni F (2009) Diabetes impairs the vascular recruitment of normal stem cells by oxidant damage, reversed by increases in pAMPK, heme oxygenase-1, and adiponectin. Stem Cells 27:399–407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma HS, Maulik N, Gho BC, Das DK, Verdouw PD (1996) Coordinated expression of heme oxygenase-1 and ubiquitin in the porcine heart subjected to ischemia and reperfusion. Mol Cell Biochem 157:111–116

    Article  CAS  PubMed  Google Scholar 

  • Shibahara S, Muller RM, Taguchi H (1987) Transcriptional control of rat heme oxygenase by heat shock. J Biol Chem 262:12889–12892

    CAS  PubMed  Google Scholar 

  • Soares MP, Lin Y, Anrather J, Csizmadia E, Takigami K, Sato K, Grey ST, Colvin RB, Choi AM, Poss KD, Bach FH (1998) Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nat Med 4:1073–1077

    Article  CAS  PubMed  Google Scholar 

  • Suliman HB, Keenan JE, Piantadosi CA (2017) Mitochondrial quality-control dysregulation in conditional HO-1−/− mice. JCI Insight 2:e89676

    Article  PubMed  PubMed Central  Google Scholar 

  • Tang YL, Tang Y, Zhang YC, Qian K, Shen L, Phillips MI (2005) Improved graft mesenchymal stem cell survival in ischemic heart with a hypoxia-regulated heme oxygenase-1 vector. J Am Coll Cardiol 45:1339–1350

    Article  CAS  Google Scholar 

  • Tenhunen R, Marver HS, Schmid R (1968) The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci U S A 61:748–755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tenhunen R, Marver H, Pimstone NR, Trager WF, Cooper DY, Schmid R (1972) Enzymatic degradation of heme. Oxygenative cleavage requiring cytochrome P-450. Biochemistry 11:1716–1720

    Article  CAS  PubMed  Google Scholar 

  • Thirunavukkarasu M, Penumathsa SV, Koneru S, Juhasz B, Zhan L, Otani H, Bagchi D, Das DK, Maulik N (2007) Resveratrol alleviates cardiac dysfunction in streptozotocin-induced diabetes: role of nitric oxide, thioredoxin, and heme oxygenase. Free Radic Biol Med 43:720–729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian S, Ge X, Wu K, Yang H, Liu Y (2014) Ramipril protects the endothelium from high glucose-induced dysfunction through CaMKKß/AMPK and heme oxygenase-1 activation. J Pharmacol Exp Ther 350:5–13

    Article  PubMed  CAS  Google Scholar 

  • Tomczyk M, Kraszewska I, Szade K, Bukowska-Strakova K, Meloni M, Jozkowicz A, Dulak J, Jazwa A (2017) Splenic Ly6Chi monocytes contribute to adverse late post-ischemic left ventricular remodeling in heme oxygenase-1 deficient mice. Basic Res Cardiol 112:39

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ueyama T, Kawabe T, Hano T, Tsuruo Y, Ueda K, Ichinose M, Kimura H, Yoshida K (2009) Upregulation of heme oxygenase-1 in an animal model of Takotsubo cardiomyopathy. Circ J 73:1141–1146

    Article  CAS  PubMed  Google Scholar 

  • Vecsernyes M, Szokol M, Bombicz M, Priksz D, Gesztelyi R, Fulop GA, Varga B, Juhasz B, Haines D, Tosaki A (2017) Alpha-melanocyte-stimulating hormone induces vasodilation and exerts cardioprotection through the heme-oxygenase pathway in rat hearts. J Cardiovasc Pharmacol 69:286–297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wagener FA, Feldman E, de Witte T, Abraham NG (1997) Heme induces the expression of adhesion molecules ICAM-1, VCAM-1, and E selectin in vascular endothelial cells. Proc Soc Exp Biol Med 216:456–463

    Article  CAS  PubMed  Google Scholar 

  • Wagener FA, da Silva JL, Farley T, de Witte T, Kappas A, Abraham NG (1999) Differential effects of heme oxygenase isoforms on heme mediation of endothelial intracellular adhesion molecule 1 expression. J Pharmacol Exp Ther 291:416–423

    CAS  PubMed  Google Scholar 

  • Wang J, Hu X, Xie J, Xu W, Jiang H (2015a) Beta-1-adrenergic receptors mediate Nrf2-HO-1-HMGB1 axis regulation to attenuate hypoxia/reoxygenation-induced cardiomyocytes injury in vitro. Cell Physiol Biochem 35:767–777

    Article  PubMed  Google Scholar 

  • Wang YL, Lam KK, Cheng PY, Lee YM (2015b) Celastrol prevents circulatory failure via induction of heme oxygenase-1 and heat shock protein 70 in endotoxemic rats. J Ethanophrmacol 162:168–175

    Article  CAS  Google Scholar 

  • Wei B, Li WW, Ji J, Hu QH, Ji H (2014) The cardioprotective effect of sodium tanshinone IIA sulfonate and the optimizing of therapeutic time window in myocardial ischemia/reperfusion injury in rats. Artheroscletrosis 235:318–327

    Article  CAS  Google Scholar 

  • Wei H, Li H, Wan SP, Zeng QT, Cheng LX, Jiang LL, Peng YD (2017) Cardioprotective effects of Malvidin against isoproterenol-induced myocardial infarction in rats: a mechanistic study. Med Sci Monit 23:2007–2016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wenzel P, Rossman H, Muller C, Kossmann S, Oeize M, Schultz A, Arnold N, Simsek C, Lagrange J, Klemz R, Schonfelder T, Brandt M, Karbach SH, Knorr M, Finger S, Neukirch C, Hauser F, Beutel ME, Kroller-Schon S, Schulz E, Schnabel RB, Lackner K, Wild PS, Zeller T, Daiber A, Blankenberg S, Munzel T (2015) Heme oxygenase-1 suppresses a pro-inflammatory phenotype in monocytes and determines endothelial function and arterial hypertension in mice and humans. Eur Heart J 36:3437–3446

    Article  CAS  PubMed  Google Scholar 

  • Wilks A (2002a) Heme oxygenase: evolution, structure, and mechanism. Antioxid Redox Signal 4:603–614

    Article  CAS  PubMed  Google Scholar 

  • Wilks A (2002b) Analysis of heme and hemoproteins. In: Smith AG, Witty M (eds) Heme, chlorophyll, and bilins. Humana Press, Totowa, pp 157–118

    Google Scholar 

  • Wu BJ, Chen K, Barter PJ, Rye KA (2012) Niacin inhibits vascular inflammation via the induction of heme oxygenase-1. Circulation 125:150–158

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Jiang H, Shi Y (2017) Upregulation of heme oxygenase-1 expression by curcumin conferring protection from hydrogen peroxide-induced apoptosis in H9c2 cardiomyoblasts. Cell Biosci 7:1–8

    Article  CAS  Google Scholar 

  • Yet SF, Perrella MA, Layne MD, Hsieh CM, Maemura K, Kobzik L, Wiesel P, Christou H, Kourembanas S, Lee ME (1999) Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice. J Clin Invest 103:R23–R29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida T, Takahashi S, Kikuchi G (1974) Partial purification and reconstitution of the heme oxygenase system form pig spleen microsomes. J Biochem 75:1187–1191

    Article  CAS  PubMed  Google Scholar 

  • Yu X, Tao W, Jiang F, Li C, Lin J, Liu C (2010) Celastrol attenuates hypertension-induced inflammation and oxidative stress in vascular smooth muscle cells via induction of heme oxygenase-1. Am J Hypertens 23:895–903

    Article  CAS  PubMed  Google Scholar 

  • Zabalgoitia J, Colston JT, Reddy SV, Holt JW, Regan RF, Stec DE, Rimoldi JM, Valente AJ, Chandrasekar B (2008) Carbon monoxide donors or heme oxygenase-1 (HO-1) overexpression blocks interleukin-18-mediated NKÒ¡B-PTEN-dependent human cardiac endothelial cell death. Free Radic Biol Med 44:284–298

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Zhang L, Qiao Y, Zhou X, Wu G, Wang L, Peng Y, Dong X, Huang H, Si L, Zhang X, Zhang L, Li J, Wang W, Zhou L, Gao X (2013) Heme oxygenase-1 prevents cardiac dysfunction in streptozotocin-diabetic mice by reducing inflammation, oxidative stress, apoptosis and enhancing autophagy. PLoS One 8:e75927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao M, Guo H, Chen J, Fujino M, Ito H, Takahashi K, Abe F, Nakajima M, Tanaka T, Wang J, Huang H, Zheng S, Hei M, Li J, Huang S, Li J, Ma X, Chen Y, Zhao L, Zhuang J, Zhu P, Li XK (2015) 5-aminolevulinic acid combined with sodium ferrous citrate ameliorates H2O2-induced cardiomyocyte hypertrophy via activation of the MAPK/Nrf2/HO-1 pathway. Am J Phys Cell Phys 308:C665–C672

    Article  CAS  Google Scholar 

  • Zhu H, Gao Y, Zhu S, Cui Q, Du J (2017) Klotho improves cardiac function by suppressing reactive oxygen species (ROS) mediated apoptosis by modulating mapks/Nrf2 signaling in doxorubicin-induced cardiotoxicity. Med Sci Monit 23:5283–5293

    Article  PubMed  PubMed Central  Google Scholar 

  • Zimmermann K, Baldinger J, Mayerhofer B, Atanasov AG, Dirsch VM, Heiss EH (2015) Activated AMPK boosts the Nrf2/HO-1 signaling axis – a role for the unfolded protein response. Free Radic Biol Med 88:417–426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zou MH, Wu Y (2008) AMP-activated protein kinase activation as a strategy for protecting vascular endothelial function. Clin Exp Pharmacol Physiol 35:535–545

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Azhwar Raghunath is the recipient of a University Grants Commission – Basic Scientific Research Senior Research Fellowship (UGC-BSR-SRF – No.F.7-25/2007) funded by UGC-BSR, New Delhi, India. We thank the Department of Science and Technology, Science and Engineering Board (EMR/2014/000600), and Empowerment and Equity Opportunities for Excellence in Science (SB/EMEQ-246/2014), New Delhi, for financial assistance. This work was also supported by the University Grants Commission – Special Assistance Programme (UGC-SAP-II:F-3-20/2013) and Department of Science and Technology, Fund for Improvement of Science and Technology infrastructure in universities and higher educational institutions (DST-FIST:SR/FST/LSI-618/2014), New Delhi, India.

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Panneerselvam, L., Raghunath, A., Sundarraj, K., Perumal, E. (2019). HO-1/HSP32 and Cardiac Stress Signaling. In: Asea, A., Kaur, P. (eds) Heat Shock Proteins in Signaling Pathways. Heat Shock Proteins, vol 17. Springer, Cham. https://doi.org/10.1007/978-3-030-03952-3_8

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