Translational Significance of Heme Oxygenase in Obesity and Metabolic Syndrome

Trends in Pharmacological Sciences

Volumn 37, Issue 1, 2016, Pages 17-36

  Abraham, Nader G ^a,b   Junge, Joshua M ^a   Drummond, George S ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

^b MARSHALL UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BILIRUBIN; BILIVERDIN REDUCTASE; CARBON MONOXIDE; EPOXYICOSATRIENOIC ACID; FERRITIN; HEME; HEME OXYGENASE 1; HEME OXYGENASE 2; OXIDOREDUCTASE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; HEME OXYGENASE;

ADIPOCYTE; ADIPOGENESIS; APOPTOSIS; ATHEROSCLEROSIS; CARDIOVASCULAR RISK; CELL DIFFERENTIATION; CEREBROVASCULAR ACCIDENT; ENZYME ACTIVITY; GENETIC POLYMORPHISM; HEALTH STATUS; HEME SYNTHESIS; HUMAN; HYPERTENSION; INFLAMMATION; METABOLIC SYNDROME X; NONHUMAN; OBESITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; ENZYMOLOGY; METABOLISM;

ANIMALS; HEME OXYGENASE (DECYCLIZING); HUMANS; METABOLIC SYNDROME X; OBESITY;

EID: 84951838388     PISSN: 01656147     EISSN: 18733735     Source Type: Journal    
DOI: 10.1016/j.tips.2015.09.003     Document Type: Review

References (252)

1. J.E. Hall The kidney, hypertension, and obesity Hypertension 41 2003 625 633
2. C.L. Ogden, and et al. Prevalence of overweight and obesity in the United States, 1999-2004 JAMA 295 2006 1549 1555
3. L. Fontana, and et al. Visceral fat adipokine secretion is associated with systemic inflammation in obese humans Diabetes 56 2007 1010 1013
4. M. Li, and et al. Treatment of obese diabetic mice with a heme oxygenase inducer reduces visceral and subcutaneous adiposity, increases adiponectin levels, and improves insulin sensitivity and glucose tolerance Diabetes 57 2008 1526 1535
5. D.B. Briggs, and et al. Disulfide-dependent self-assembly of adiponectin octadecamers from trimers and presence of stable octadecameric adiponectin lacking disulfide bonds in vitro Biochemistry (Mosc.) 48 2009 12345 12357
6. Z.V. Wang, and P.E. Scherer Adiponectin, cardiovascular function, and hypertension Hypertension 51 2008 8 14
7. A.A. Elmarakby, and J.D. Imig Obesity is the major contributor to vascular dysfunction and inflammation in high fat diet hypertensive rats Clin. Sci. (Lond.) 118 2010 291 301
8. M.H. Wang, and et al. Downregulation of renal CYP-derived eicosanoid synthesis in rats with diet-induced hypertension Hypertension 42 2003 594 599
9. Y. Lin, and et al. The hyperglycemia-induced inflammatory response in adipocytes: the role of reactive oxygen species J. Biol. Chem. 280 2005 4617 4626
10. N.G. Abraham, and et al. Heme oxygenase-1 attenuates glucose-mediated cell growth arrest and apoptosis in human microvessel endothelial cells Circ. Res. 93 2003 507 514
11. N.G. Abraham, and et al. Overexpression of human heme oxygenase-1 attenuates endothelial cell sloughing in experimental diabetes Am. J Physiol. Heart Circ. Physiol. 287 2004 H2468 H2477
12. J.J. Chen, and I.M. London Hemin enhances the differentiation of mouse 3T3 cells to adipocytes Cell 26 1981 117 122
13. N. Kumar, and et al. Regulation of adipogenesis by natural and synthetic REV-ERB ligands Endocrinology 151 2010 3015 3025
14. N.G. Abraham, and A. Kappas Pharmacological and clinical aspects of heme oxygenase Pharmacol. Rev. 60 2008 79 127
15. L.A. Cassis, and et al. Local adipose tissue renin-angiotensin system Curr. Hypertens. Rep. 10 2008 93 98
16. C.M. Boustany, and et al. Activation of the systemic and adipose renin-angiotensin system in rats with diet-induced obesity and hypertension Am. J. Physiol. Regul. Integr. Comp. Physiol. 287 2004 R943 R949
17. S.H. Chang, and et al. Glucose deprivation induces heme oxygenase-1 gene expression by a pathway independent of the unfolded protein response J. Biol. Chem. 277 2002 1933 1940
18. S.H. Chang, and et al. Haem oxygenase 1 gene induction by glucose deprivation is mediated by reactive oxygen species via the mitochondrial electron-transport chain Biochem. J. 371 2003 877 885
19. S. Quan, and et al. Heme oxygenase-1 prevents superoxide anion-associated endothelial cell sloughing in diabetic rats Biochem. Biophys. Res. Commun. 315 2004 509 516
20. A.L. Kruger, and et al. Up-regulation of heme oxygenase provides vascular protection in an animal model of diabetes through its antioxidant and antiapoptotic effects J. Pharmacol. Exp. Ther. 319 2006 1144 1152
21. R. Kinobe, and et al. Peroxynitrite-mediated inactivation of heme oxygenases BMC Pharmacol. 4 2004 26
22. T.D. Hinds Jr, and et al. Increased HO-1 levels ameliorate fatty liver development through a reduction of heme and recruitment of FGF21 Obesity 22 2014 705 712
23. N.G. Abraham, and et al. Heme oxygenase: a target gene for anti-diabetic and obesity Curr. Pharm. Des. 14 2008 412 421
24. J.F. Ndisang Role of heme oxygenase in inflammation, insulin-signalling, diabetes and obesity Mediators Inflamm. 2010 2010 359732
25. N.G. Abraham, and et al. The biological significance and physiological role of heme oxygenase Cell. Physiol. Biochem. 6 1996 129 168
26. J. Kapitulnik, and M.D. Maines Pleiotropic functions of biliverdin reductase: cellular signaling and generation of cytoprotective and cytotoxic bilirubin Trends Pharmacol. Sci. 30 2009 129 137
27. Z. Ahmad, and et al. Human biliverdin reductase is a leucine zipper-like DNA-binding protein and functions in transcriptional activation of heme oxygenase-1 by oxidative stress J. Biol. Chem. 277 2002 9226 9232
28. K.D. Poss, and S. Tonegawa Heme oxygenase 1 is required for mammalian iron reutilization Proc. Natl. Acad. Sci. U.S.A. 94 1997 10919 10924
29. A.L. True, and et al. Heme oxygenase-1 deficiency accelerates formation of arterial thrombosis through oxidative damage to the endothelium, which is rescued by inhaled carbon monoxide Circ. Res. 101 2007 893 901
30. H.J. Duckers, and et al. Heme oxygenase-1 protects against vascular constriction and proliferation Nat. Med. 7 2001 693 698
31. D. Willis, and et al. Heme oxygenase: a novel target for the modulation of the inflammatory response Nat. Med. 2 1996 87 90
32. D. Morse, and A.M. Choi Heme oxygenase-1: from bench to bedside Am. J. Respir. Crit. Care Med. 172 2005 660 670
33. D.M. Lundvig, and et al. Heme oxygenase, inflammation, and fibrosis: the good, the bad, and the ugly? Front. Pharmacol. 3 2012 81
34. A. Yachie, and et al. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency J. Clin. Invest. 103 1999 129 135
35. J.H. Kie, and et al. Heme oxygenase-1 deficiency promotes epithelial-mesenchymal transition and renal fibrosis J. Am. Soc. Nephrol. 19 2008 1681 1691
36. M.H. Kapturczak, and et al. Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse Am. J. Pathol. 165 2004 1045 1053
37. I.W. Asterholm, and P.E. Scherer Enhanced metabolic flexibility associated with elevated adiponectin levels Am. J. Pathol. 176 2010 1364 1376
38. P.A. Dennery, and et al. Oxygen toxicity and iron accumulation in the lungs of mice lacking heme oxygenase-2 J. Clin. Invest. 101 1998 1001 1011
39. A.I. Goodman, and et al. Heme oxygenase-2 deficiency contributes to diabetes-mediated increase in superoxide anion and renal dysfunction J. Am. Soc. Nephrol. 17 2006 1073 1081
40. K. Sodhi, and et al. Epoxyeicosatrienoic acid agonist rescues the metabolic syndrome phenotype of HO-2-null mice J. Pharmacol. Exp. Ther. 331 2009 906 916
41. C.K. Roberts, and et al. Oxidative stress and dysregulation of NAD(P)H oxidase and antioxidant enzymes in diet-induced metabolic syndrome Metabolism 55 2006 928 934
42. A. Kappas, and G. Drummond Control of heme metabolism with synthetic metalloporphyrins J. Clin. Invest. 77 1986 335 339
43. A. Kappas A method for interdicting the development of severe jaundice in newborns by inhibiting the production of bilirubin Pediatrics 113 2004 119 123
44. G.S. Drummond, and A. Kappas Chemoprevention of neonatal jaundice: potency of tin-protoporphyrin in an animal model Science 217 1982 1250 1252
45. J.H. Lin, and et al. Regulation of heme oxygenase gene expression by cobalt in rat liver and kidney Eur. J. Biochem. 192 1990 577 582
46. A. Jazwa, and et al. HIF-regulated HO-1 gene transfer improves the post-ischemic limb recovery and diminishes TLR-triggered immune responses - effects modified by concomitant VEGF overexpression Vasc. Pharmacol. 71 2015 127 138
47. Q. Li, and et al. Gene transfer as a strategy to achieve permanent cardioprotection II: rAAV-mediated gene therapy with heme oxygenase-1 limits infarct size 1 year later without adverse functional consequences Basic Res. Cardiol. 106 2011 1367 1377
48. D. Du, and et al. Adenovirus-mediated heme oxygenase transfer inhibits graft arteriosclerosis in rat aortic transplants Transplant. Proc. 39 2007 3446 3448
49. X. Liu, and et al. Preemptive heme oxygenase-1 gene delivery reveals reduced mortality and preservation of left ventricular function 1 yr after acute myocardial infarction Am. J. Physiol. Heart Circ. Physiol. 293 2007 H48 H59
50. W. Chen, and et al. CYP2J2 and EETs protect against lung ischemia/reperfusion injury via anti-inflammatory effects in vivo and in vitro Cell. Physiol. Biochem. 35 2015 2043 2054
51. J. Cao, and et al. Heme oxygenase gene targeting to adipocytes attenuates adiposity and vascular dysfunction in mice fed a high-fat diet Hypertension 60 2012 467 475
52. R. Stocker, and et al. Bilirubin is an antioxidant of possible physiological importance Science 235 1987 1043 1046
53. P.N. Hopkins, and et al. Higher serum bilirubin is associated with decreased risk for early familial coronary artery disease Arterioscler. Thromb. Vasc. Biol. 16 1996 250 255
54. A. Verma, and et al. Carbon monoxide: a putative neural messenger Science 259 1993 381 384
55. L.E. Otterbein, and A.M. Choi Heme oxygenase: colors of defense against cellular stress Am. J. Physiol. Lung Cell. Mol. Physiol. 279 2000 L1029 L1037
56. Y. Zhan, and et al. Role of JNK, p38, and ERK in platelet-derived growth factor-induced vascular proliferation, migration, and gene expression Arterioscler. Thromb. Vasc. Biol. 23 2003 795 801
57. L.E. Otterbein, and et al. Heme oxygenase-1: unleashing the protective properties of heme Trends Immunol. 24 2003 449 455
58. H.P. Kim, and et al. CO as a cellular signaling molecule Annu. Rev. Pharmacol. Toxicol. 46 2006 411 449
59. S.W. Ryter, and et al. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications Physiol. Rev. 86 2006 583 650
60. T. Kushida, and et al. TNF-alpha-mediated cell death is attenuated by retrovirus delivery of human heme oxygenase-1 gene into human microvessel endothelial cells Transplant. Proc. 34 2002 2973 2978
61. C. Fondevila, and et al. Biliverdin therapy protects rat livers from ischemia and reperfusion injury Hepatology 40 2004 1333 1341
62. S.S. Lee, and et al. Heme oxygenase-1, carbon monoxide, and bilirubin induce tolerance in recipients toward islet allografts by modulating T regulatory cells FASEB J. 21 2007 3450 3457
63. H. Wang, and et al. Bilirubin can induce tolerance to islet allografts Endocrinology 147 2006 762 768
64. L. O'Brien, and et al. Biliverdin reductase isozymes in metabolism Trends Endocrinol. Metab. 26 2015 212 220
65. B. Ding, and et al. The coordinated increased expression of biliverdin reductase and heme oxygenase-2 promotes cardiomyocyte survival: a reductase-based peptide counters beta-adrenergic receptor ligand-mediated cardiac dysfunction FASEB J. 25 2011 301 313
66. J. Liu, and et al. Unconjugated bilirubin mediates heme oxygenase-1-induced vascular benefits in diabetic mice Diabetes 64 2014 1564 1575
67. T. Ito, and et al. Mesobiliverdin IXalpha enhances rat pancreatic islet yield and function Front. Pharmacol. 4 2013 50
68. H. Dong, and et al. Bilirubin increases insulin sensitivity in leptin-receptor deficient and diet-induced obese mice through suppression of ER stress and chronic inflammation Endocrinology 155 2014 818 828
69. J.E. Clark, and et al. Heme oxygenase-1-derived bilirubin ameliorates postischemic myocardial dysfunction Am. J. Physiol. Heart Circ. Physiol. 278 2000 H643 H651
70. N. Hill-Kapturczak, and et al. Heme oxygenase and the kidney DNA Cell Biol. 21 2002 307 321
71. N.G. Abraham, and A. Kappas Heme oxygenase and the cardiovascular-renal system Free Radic. Biol. Med. 39 2005 1 25
72. L. Vitek The role of bilirubin in diabetes, metabolic syndrome, and cardiovascular diseases Front. Pharmacol. 3 2012 55
73. J. Neuzil, and R. Stocker Free and albumin-bound bilirubin are efficient co-antioxidants for alpha-tocopherol, inhibiting plasma and low density lipoprotein lipid peroxidation J. Biol. Chem. 269 1994 16712 16719
74. L. Wu, and R. Wang Carbon monoxide: endogenous production, physiological functions, and pharmacological applications Pharmacol. Rev. 57 2005 585 630
75. T.D. Oury, and et al. Cold-induced brain edema in mice. Involvement of extracellular superoxide dismutase and nitric oxide J. Biol. Chem. 268 1993 15394 15398
76. S.A. Lipton, and et al. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds Nature 364 1993 626 632
77. A. Friebe, and D. Koesling Mechanism of YC-1-induced activation of soluble guanylyl cylase Mol. Pharmacol. 53 1998 123 127
78. R.F. Furchgott, and D. Jothianandan Endothelium-dependent and -independent vasodilation involving cyclic GMP: relaxation induced by nitric oxide, carbon monoxide and light Blood Vessels 28 1991 52 61
79. C.W. Leffler, and et al. Carbon monoxide and cerebral microvascular tone in newborn pigs Am. J. Physiol. 276 1999 H1641 H1646
80. G. Czibik, and et al. Heme oxygenase-1: an emerging therapeutic target to curb cardiac pathology Basic Res. Cardiol. 109 2014 450
81. R. Motterlini, and R. Foresti Heme oxygenase-1 as a target for drug discovery Antioxid. Redox. Signal. 20 2014 1810 1826
82. P.A. Hosick, and et al. Chronic carbon monoxide treatment attenuates development of obesity and remodels adipocytes in mice fed a high-fat diet Int. J. Obes. (Lond.) 38 2014 132 139
83. P.A. Hosick, and et al. Chronic treatment with a carbon monoxide releasing molecular revereses dietary induced obesity in mice Adipocyte 5 2016 1 10
84. 2+ signals between pancreatic beta-cells Am. J. Physiol. Endocrinol. Metab. 285 2003 E1055 E1063
85. S. Brouard, and et al. Heme oxygenase-1-derived carbon monoxide requires the activation of transcription factor NF-kappa B to protect endothelial cells from tumor necrosis factor-alpha-mediated apoptosis J. Biol. Chem. 277 2002 17950 17961
86. P.A. Hosick, and D.E. Stec Heme oxygenase, a novel target for the treatment of hypertension and obesity? Am. J. Physiol. Regul. Integr. Comp. Physiol. 302 2012 R207 R214
87. G. Balla, and et al. Exposure of endothelial cells to free heme potentiates damage mediated by granulocytes and toxic oxygen species Lab. Invest. 64 1991 648 654
88. M. Valko, and et al. Metals, toxicity and oxidative stress Curr. Med. Chem. 12 2005 1161 1208
89. E. Grunblatt, and et al. The link between iron, metabolic syndrome, and Alzheimer's disease J. Neural Transm. 118 2011 371 379
90. C.D. Ferris, and et al. Haem oxygenase-1 prevents cell death by regulating cellular iron Nat. Cell Biol. 1 1999 152 157
91. P. Ponka, and et al. Function and regulation of transferrin and ferritin Semin. Hematol. 35 1998 35 54
92. E. Nagababu, and J.M. Rifkind Heme degradation by reactive oxygen species Antioxid. Redox. Signal. 6 2004 967 978
93. J. Balla, and et al. Endothelial cell heme oxygenase and ferritin induction by heme proteins: a possible mechanism for limiting shock damage Trans. Assoc. Am. Phys. 105 1992 1 7
94. R.S. Eisenstein, and et al. Regulation of ferritin and heme oxygenase synthesis in rat fibroblasts by different forms of iron Proc. Natl. Acad. Sci. U.S.A. 88 1991 688 692
95. Y.H. Chen, and et al. Serum bilirubin and ferritin levels link heme oxygenase-1 gene promoter polymorphism and susceptibility to coronary artery disease in diabetic patients Diabetes Care 31 2008 1615 1620
96. G.F. Vile, and R.M. Tyrrell Oxidative stress resulting from ultraviolet A irradiation of human skin fibroblasts leads to a heme oxygenase-dependent increase in ferritin J. Biol. Chem. 268 1993 14678 14681
97. H. Ren, and et al. Induction of haem oxygenase-1 causes cortical non-haem iron increase in experimental pneumococcal meningitis: evidence that concomitant ferritin up-regulation prevents iron-induced oxidative damage J. Neurochem. 100 2007 532 544
98. K. Erdmann, and et al. L-methionine reduces oxidant stress in endothelial cells: role of heme oxygenase-1, ferritin, and nitric oxide AAPS J. 7 2005 E195 E200
99. R. Gozzelino, and M.P. Soares Coupling heme and iron metabolism via ferritin H chain Antioxid. Redox. Signal. 20 2014 1754 1769
100. G. Balla, and et al. Ferritin: a cytoprotective antioxidant strategm of endothelium J. Biol. Chem. 267 1992 18148 18153
101. F. Maccarinelli, and et al. Mice lacking mitochondrial ferritin are more sensitive to doxorubicin-mediated cardiotoxicity J. Mol. Med. 92 2014 859 869
102. K. Yunoki, and et al. Association between hemoglobin scavenger receptor and heme oxygenase-1-related anti-inflammatory mediators in human coronary stable and unstable plaques Hum. Pathol. 44 2013 2256 2265
103. N. Puri, and et al. Heme induced oxidative stress attenuates sirtuin1 and enhances adipogenesis in mesenchymal stem cells and mouse pre-adipocytes J. Cell Biochem. 113 2012 1926 1935
104. J.L. Chertkov, and et al. Hemin stimulation of hemopoiesis in murine long-term bone marrow culture Exp. Hematol. 19 1991 905 909
105. J.D. Lutton, and et al. Synergistic effect of heme and IL-1 on hematopoietic stromal regeneration after radiation Am. J. Hematol. 44 1993 172 178
106. I. Barbagallo, and et al. Overexpression of heme oxygenase-1 increases human osteoblast stem cell differentiation J. Bone Miner. Metab. 28 2010 276 288
107. L. Vanella, and et al. HO-1 expression increases mesenchymal stem cell-derived osteoblasts but decreases adipocyte lineage Bone 46 2010 236 243
108. A.P. Burgess, and et al. Heme oxygenase (HO-1) rescue of adipocyte dysfunction in HO-2 deficient mice via recruitment of epoxyeicosatrienoic acids (EETs) and adiponectin Cell Physiol. Biochem. 29 2012 99 110
109. D.H. Kim, and et al. Epoxyeicosatrienoic acid agonist regulates human mesenchymal stem cell-derived adipocytes through activation of HO-1-pAKT signaling and a decrease in PPARgamma Stem Cells Dev. 19 2010 1863 1873
110. L. Vanella, and et al. Crosstalk between EET and HO-1 downregulates Bach1 and adipogenic marker expression in mesenchymal stem cell derived adipocytes Prostaglandins Other Lipid Mediat. 96 2011 54 62
111. R.A. Galbraith, and A. Kappas Regulation of food intake and body weight in rats by the synthetic heme analogue cobalt protoporphyrin Am. J. Physiol. 261 1991 R1388 R1394
112. G. Kronke, and et al. Expression of heme oxygenase-1 in human vascular cells is regulated by peroxisome proliferator-activated receptors Arterioscler. Thromb. Vasc. Biol. 27 2007 1276 1282
113. A. Burgess, and et al. Adipocyte heme oxygenase-1 induction attenuates metabolic syndrome in both male and female obese mice Hypertension 56 2010 1124 1130
114. S.J. Peterson, and et al. L-4F treatment reduces adiposity, increases adiponectin levels, and improves insulin sensitivity in obese mice J. Lipid Res. 49 2008 1658 1669
115. A. Nicolai, and et al. Heme oxygenase-1 induction remodels adipose tissue and improves insulin sensitivity in obesity-induced diabetic rats Hypertension 53 2009 508 515
116. L. Vanella, and et al. Increased heme-oxygenase 1 expression decreases adipocyte differentiation and lipid accumulation in mesenchymal stem cells via upregulation of the canonical Wnt signaling cascade Stem Cell Res. Ther. 4 2013 28
117. A.A. Elmarakby, and et al. Induction of hemeoxygenase-1 reduces renal oxidative stress and inflammation in diabetic spontaneously hypertensive rats Int. J. Hypertens. 2012 2012 957235
118. A.A. Elmarakby, and et al. Induction of hemeoxygenase-1 reduces glomerular injury and apoptosis in diabetic spontaneously hypertensive rats Am. J. Physiol. Renal Physiol. 302 2012 F791 F800
119. T. Iwai, and et al. Cobalt protoporphyrin attenuates rat obstructive nephropathy: role of cellular infiltration Urology 72 2008 432 438
120. X. Liu, and et al. Sirt1 mediates the effect of the heme oxygenase inducer, cobalt protoporphyrin, on ameliorating liver metabolic damage caused by a high-fat diet J. Hepatol. 63 2015 713 721
121. K. Sodhi, and et al. Fructose mediated non-alcoholic fatty liver is attenuated by HO-1-SIRT1 module in murine hepatocytes and mice fed a high fructose diet PLoS. ONE 10 2015 e0128648
122. K. Sodhi, and et al. EET agonist prevents adiposity and vascular dysfunction in rats fed a high fat diet via a decrease in Bach 1 and an increase in HO-1 levels Prost. Other Lipid Mediat. 98 2012 133 142
123. K. Vivot, and et al. Pro-inflammatory and pro-oxidant status of pancreatic islet in vitro is controlled by TLR-4 and HO-1 pathways PLoS. ONE 9 2014 e107656
124. A.T. Turer, and P.E. Scherer Adiponectin: mechanistic insights and clinical implications Diabetologia 55 2012 2319 2326
125. K. Sharma, and et al. Adiponectin regulates albuminuria and podocyte function in mice J. Clin. Invest. 118 2008 1645 1656
126. F.M. Konrad, and et al. Heme oxygenase-1 attenuates acute pulmonary inflammation by decreasing the release of segmented neutrophils from the bone marrow Am. J. Physiol. Lung Cell. Mol. Physiol. 307 2014 L707 L717
127. S. Turkseven, and et al. Antioxidant mechanism of heme oxygenase-1 involves an increase in superoxide dismutase and catalase in experimental diabetes Am. J. Physiol. Heart Circ. Physiol. 289 2005 H701 H707
128. B. Bakhautdin, and et al. Protective role of HO-1 and carbon monoxide in ethanol-induced hepatocyte cell death and liver injury in mice J. Hepatol. 61 2014 1029 1037
129. Z. Ungvari, and et al. Resveratrol confers endothelial protection via activation of the antioxidant transcription factor Nrf2 Am. J. Physiol. Heart Circ. Physiol. 299 2010 H18 H24
130. I. Barbagallo, and et al. Potential therapeutic effects of natural heme oxygenase-1 inducers in cardiovascular diseases Antioxid. Redox. Signal. 18 2013 507 521
131. U.M. Jamal, and et al. A functional link between heme oxygenase-1 and tristetraprolin in the anti-inflammatory effects of nicotine Free Radic. Biol. Med. 65 2013 1331 1339
132. S.K. Kim, and et al. Resveratrol induces hepatic mitochondrial biogenesis through the sequential activation of nitric oxide and carbon monoxide production Antioxid. Redox. Signal. 20 2014 2589 2605
133. T.M. Chen, and et al. Effects of heme oxygenase-1 upregulation on blood pressure and cardiac function in an animal model of hypertensive myocardial infarction Int. J. Mol. Sci. 14 2013 2684 2706
134. V. Clerigues, and et al. Haem oxygenase-1 counteracts the effects of interleukin-1beta on inflammatory and senescence markers in cartilage-subchondral bone explants from osteoarthritic patients Clin. Sci. 122 2012 239 250
135. H. Yin, and et al. Heme oxygenase-1 upregulation improves lipopolysaccharide-induced acute lung injury involving suppression of macrophage migration inhibitory factor Mol. Immunol. 47 2010 2443 2449
136. H.O. Pae, and et al. Heme oxygenase-1 attenuates contact hypersensitivity induced by 2,4-dinitrofluorobenzene in mice Immunopharmacol. Immunotoxicol. 30 2008 207 216
137. E.M. George, and et al. The heme oxygenases: important regulators of pregnancy and preeclampsia Am. J. Physiol. Regul. Integr. Comp. Physiol. 307 2014 R769 R777
138. S.F. Yet, and et al. Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice J. Clin. Invest. 103 1999 R23 R29
139. C. Cai, and et al. The heme oxygenase 1 inducer (CoPP) protects human cardiac stem cells against apoptosis through activation of the extracellular signal-regulated kinase (ERK)/NRF2 signaling pathway and cytokine release J. Biol. Chem. 287 2012 33720 33732
140. B. Dawn, and R. Bolli HO-1 induction by HIF-1: a new mechanism for delayed cardioprotection? Am. J. Physiol. Heart Circ. Physiol. 289 2005 H522 H524
141. A.B. Stein, and et al. Carbon monoxide induces a late preconditioning-mimetic cardioprotective and antiapoptotic milieu in the myocardium J. Mol. Cell. Cardiol. 52 2012 228 236
142. C. Cheng, and et al. Heme oxygenase 1 determines atherosclerotic lesion progression into a vulnerable plaque Circulation 119 2009 3017 3027
143. P. Li, and et al. Epoxyeicosatrienoic acids enhance embryonic haematopoiesis and adult marrow engraftment Nature 523 2015 468 471
144. Y. Lavrovsky, and et al. Identification of binding sites for transcription factors NF-kappa B and AP-2 in the promoter region of the human heme oxygenase 1 gene Proc. Natl. Acad. Sci. U.S.A. 91 1994 5987 5991
145. Y. Lavrovsky, and et al. Downregulation of the human heme oxygenase gene by glucocorticoids and identification of 56b regulatory elements Biochem. Biophys. Res. Commun. 218 1996 759 765
146. N.G. Abraham, and et al. Modulation of erythropoiesis by novel human bone marrow cytochrome P450-dependent metabolites of arachidonic acid Blood 78 1991 1461 1466
147. L. Kang, and et al. Induction and functional significance of the heme oxygenase system in pathological shear stress in vivo Am. J. Physiol. Heart Circ. Physiol. 308 2015 H1402 H1413
148. K.A. Nath Heme oxygenase-1: a provenance for cytoprotective pathways in the kidney and other tissues Kidney Int. 70 2006 432 443
149. A. Agarwal, and H.S. Nick Renal response to tissue injury: lessons from heme oxygenase-1 GeneAblation and expression J. Am. Soc. Nephrol. 11 2000 965 973
150. J. Deshane, and et al. Heme oxygenase-1 expression in disease states Acta Biochim. Pol. 52 2005 273 284
151. J-I. Kaide, and et al. Carbon monoxide of vascular origin attenuates the sensitivity of renal arterial vessels to vasoconstrictors J. Clin. Invest. 107 2001 1163 1171
152. H.E. Sabaawy, and et al. Human heme oxygenase-1 gene transfer lowers blood pressure and promotes growth in spontaneously hypertensive rats Hypertension 38 2001 210 215
153. N. Li, and et al. Role of renal medullary heme oxygenase in the regulation of pressure natriuresis and arterial blood pressure Hypertension 49 2007 148 154
154. F. Rodriguez, and et al. Effects of exogenous heme on renal function. Role of heme oxygenase and cyclooxygenase Hypertension 42 2003 680 684
155. F. Rodriguez, and et al. Nitric oxide synthesis inhibition promotes renal production of carbon monoxide Hypertension 43 2004 347 351
156. R.A. Johnson, and et al. Heme oxygenase substrates acutely lower blood pressure in hypertensive rats Am. J. Physiol. 271 1996 H1132 H1138
157. Z. Li, and et al. Upregulation of heme oxygenase-1 potentiates EDH-type relaxations in the mesenteric artery of the spontaneously hypertensive rat Am. J. Physiol. Heart Circ. Physiol. 305 2013 H1471 H1483
158. J. Kaide, and et al. Vascular CO counterbalances the sensitizing influence of 20-HETE on agonist-induced vasoconstriction Hypertension 44 2004 210 216
159. D.E. Stec, and et al. Expression of heme oxygenase-1 in thick ascending loop of henle attenuates angiotensin II-dependent hypertension J. Am. Soc. Nephrol. 23 2012 834 841
160. D.C. Zeldin Epoxygenase pathways of arachidonic acid metabolism J. Biol. Chem. 276 2001 36059 36062
161. J.H. Capdevila, and et al. Cytochrome P450 and arachidonic acid bioactivation. Molecular and functional properties of the arachidonate monooxygenase J. Lipid Res. 41 2000 163 181
162. K. Node, and et al. Anti-inflammatory properties of cytochrome P450 epoxygenase-derived eicosanoids Science 285 1999 1276 1279
163. M. Spiecker, and J.K. Liao Vascular protective effects of cytochrome p450 epoxygenase-derived eicosanoids Arch. Biochem. Biophys. 433 2005 413 420
164. A. Burgess, and et al. Epoxyeicosatrienoic acids and heme oxygenase-1 interaction attenuates diabetes and metabolic syndrome complications Prostaglandins Other Lipid Mediat. 97 2012 1 16
165. N.G. Abraham, and et al. CYP2J2 targeting to endothelial cells attenuates adiposity and vascular dysfunction in mice fed a high-fat diet by reprogramming adipocyte phenotype Hypertension 64 2014 1352 1361
166. A. Fedorenko, and et al. Mechanism of fatty-acid-dependent UCP1 uncoupling in brown fat mitochondria Cell 151 2012 400 413
167. C. Kusmic, and et al. Improved myocardial perfusion in chronic diabetic mice by the up-regulation of pLKB1 and AMPK signaling J. Cell. Biochem. 109 2010 1033 1044
168. L.E. Otterbein, and et al. Exogenous administration of heme oxygenase-1 by gene transfer provides protection against hyperoxia-induced lung injury J. Clin. Invest. 103 1999 1047 1054
169. J.N. Fain, and et al. Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans Endocrinology 145 2004 2273 2282
170. S. Tiwari, and J.F. Ndisang The heme oxygenase system and type-1 diabetes Curr. Pharm. Des. 20 2014 1328 1337
171. M. Mishra, and J.F. Ndisang A critical and comprehensive insight on heme oxygenase and related products including carbon monoxide, bilirubin, biliverdin and ferritin in type-1 and type-2 diabetes Curr. Pharm. Des. 20 2014 1370 1391
172. J. Cao, and et al. High-fat diet exacerbates renal dysfunction in SHR: reversal by induction of HO-1-adiponectin axis Obesity 20 2012 945 953
173. E. Csongradi, and et al. Chronic HO-1 induction with cobalt protoporphyrin (CoPP) treatment increases oxygen consumption, activity, heat production and lowers body weight in obese melanocortin-4 receptor-deficient mice Int. J. Obes. (Lond.) 36 2012 244 253
174. S.J. Peterson, and et al. The L-4F mimetic peptide prevents insulin resistance through increased levels of HO-1, pAMPK, and pAKT in obese mice J. Lipid Res. 50 2009 1293 1304
175. J.F. Ndisang, and et al. The heme oxygenase system suppresses perirenal visceral adiposity, abates renal inflammation and ameliorates diabetic nephropathy in Zucker diabetic fatty rats PLoS ONE 9 2014 e87936
176. T.N. Salley, and et al. The heme oxygenase system rescues hepatic deterioration in the condition of obesity co-morbid with type-2 diabetes PLoS ONE 8 2013 e79270
177. D.H. Kim, and et al. Heme oxygenase-mediated increases in adiponectin decrease fat content and inflammatory cytokines, tumor necrosis factor-alpha and interleukin-6 in Zucker rats and reduce adipogenesis in human mesenchymal stem cells J. Pharmacol. Exp. Ther. 325 2008 833 840
178. J. Cao, and et al. Lentiviral-human heme oxygenase targeting endothelium improved vascular function in angiotensin II animal model of hypertension Hum. Gene Ther. 22 2011 271 282
179. J.Y. Huang, and et al. Adipose overexpression of heme oxygenase-1 does not protect against high fat diet-induced insulin resistance in mice PLoS ONE 8 2013 e55369
180. N.G. Abraham, and G. Drummond CD163-Mediated hemoglobin-heme uptake activates macrophage HO-1, providing an antiinflammatory function Circ. Res. 99 2006 911 914
181. P. Philippidis, and et al. Hemoglobin scavenger receptor CD163 mediates interleukin-10 release and heme oxygenase-1 synthesis: antiinflammatory monocyte-macrophage responses in vitro, in resolving skin blisters in vivo, and after cardiopulmonary bypass surgery Circ. Res. 94 2004 119 126
182. S. Shakeri-Manesch, and et al. Diminished upregulation of visceral adipose heme oxygenase-1 correlates with waist-to-hip ratio and insulin resistance Int. J. Obes. 33 2009 1257 1264
183. V.G. Nielsen, and et al. Bariatric patients have plasmatic hypercoagulability and systemic upregulation of heme oxygenase activity Blood Coagul. Fibrinolysis 26 2015 200 204
184. P.A. Rodgers, and et al. Sources of carbon monoxide (CO) in biological systems and applications of CO detection technologies Semin. Perinatol. 18 1994 2 10
185. M.A. Di Noia, and et al. Heme oxygenase-1 enhances renal mitochondrial transport carriers and cytochrome c oxidase activity in experimental diabetes J. Biol. Chem. 281 2006 15687 15693
186. X. Shen, and et al. Cardiac mitochondrial damage and biogenesis in a chronic model of type 1 diabetes Am. J. Physiol. Endocrinol. Metab. 287 2004 E896 E905
187. L.M. Sparks, and et al. A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle Diabetes 54 2005 1926 1933
188. D. Detaille, and et al. Metformin prevents high-glucose-induced endothelial cell death through a mitochondrial permeability transition-dependent process Diabetes 54 2005 2179 2187
189. D.P. Converso, and et al. HO-1 is located in liver mitochondria and modulates mitochondrial heme content and metabolism FASEB J. 20 2006 1236 1238
190. J. Kim, and et al. In vivo regulation of the heme oxygenase-1 gene in humanized transgenic mice Kidney Int. 82 2012 278 291
191. S. Varma, and et al. Hyperglycemia Alters PI3k and Akt Signaling and Leads to Endothelial Cell Proliferative Dysfunction Am. J. Physiol. Heart Circ. Physiol. 289 2005 H1744 H1751
192. J. Bojunga, and et al. Antioxidative treatment prevents activation of death-receptor- and mitochondrion-dependent apoptosis in the hearts of diabetic rats Diabetologia 47 2004 2072 2080
193. W. Chen, and et al. Insulin-like growth factor (IGF)-I/IGF-binding protein-3 complex: therapeutic efficacy and mechanism of protection against type 1 diabetes Endocrinology 145 2004 627 638
194. S. Srinivasan, and et al. Diabetic peripheral neuropathy: evidence for apoptosis and associated mitochondrial dysfunction Diabetes 49 2000 1932 1938
195. T.J. Huang, and et al. Insulin enhances mitochondrial inner membrane potential and increases ATP levels through phosphoinositide 3-kinase in adult sensory neurons Mol. Cell. Neurosci. 28 2005 42 54
196. A.L. Nascimento, and et al. Ultraviolet A (320-380 nm) radiation causes an alteration in the binding of a specific protein/protein complex to a short region of the promoter of the human heme oxygenase 1 gene Nucleic Acids Res. 21 1993 1103 1109
197. J. Dulak, and et al. Heme oxygenase-1 and carbon monoxide in vascular pathobiology: focus on angiogenesis Circulation 117 2008 231 241
198. A. Rabinovitch, and et al. Cytotoxic effects of cytokines on rat islets: evidence for involvement of free radicals and lipid peroxidation Diabetologia 35 1992 409 413
199. B.M. Choi, and et al. Critical role of heme oxygenase-1 in Foxp3-mediated immune suppression Biochem. Biophys. Res. Commun. 327 2005 1066 1071
200. H.O. Pae, and et al. Carbon monoxide produced by heme oxygenase-1 suppresses T cell proliferation via inhibition of IL-2 production J. Immunol. 172 2004 4744 4751
201. S. Chen, and et al. Interleukin 10 attenuates neointimal proliferation and inflammation in aortic allografts by a heme oxygenase-dependent pathway Proc. Natl. Acad. Sci. U.S.A. 102 2005 7251 7256
202. C. Chauveau, and et al. Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression Blood 106 2005 1694 1702
203. A.K. Choudhary, and et al. Administration of heme arginate ameliorates murine type 2 diabetes independently of heme oxygenase activity PLoS. ONE 8 2013 e78209
204. A. Pileggi, and et al. Heme oxygenase-1 induction in islet cells results in protection from apoptosis and improved in vivo function after transplantation Diabetes 50 2001 1983 1991
205. E.M. Harrison, and et al. Insulin induces heme oxygenase-1 through the phosphatidylinositol 3-kinase/Akt pathway and the Nrf2 transcription factor in renal cells FEBS J. 273 2006 2345 2356
206. Y. Qi, and et al. Adiponectin acts in the brain to decrease body weight Nat. Med. 10 2004 524 529
207. N. Halberg, and et al. Systemic fate of the adipocyte-derived factor adiponectin Diabetes 58 2009 1961 1970
208. J.Y. Kim, and et al. Obesity-associated improvements in metabolic profile through expansion of adipose tissue J. Clin. Invest. 117 2007 2621 2637
209. A.R. Nawrocki, and et al. Mice lacking adiponectin show decreased hepatic insulin sensitivity and reduced responsiveness to peroxisome proliferator-activated receptor gamma agonists J. Biol. Chem. 281 2006 2654 2660
210. N. Yamada, and et al. Microsatellite polymorphism in the heme oxygenase-1 gene promoter is associated with susceptibility to emphysema Am. J. Hum. Genet. 66 2000 187 195
211. M. Exner, and et al. Heme oxygenase-1 gene promoter microsatellite polymorphism is associated with restenosis after percutaneous transluminal angioplasty J. Endovasc. Ther. 8 2001 433 440
212. T. Inoguchi, and et al. Relationship between Gilbert syndrome and prevalence of vascular complications in patients with diabetes JAMA 298 2007 1398 1400
213. Y.H. Chen, and et al. Microsatellite polymorphism in promoter of heme oxygenase-1 gene is associated with susceptibility to coronary artery disease in type 2 diabetic patients Hum. Genet. 111 2002 1 8
214. H. Kaneda, and et al. Heme oxygenase-1 gene promoter polymorphism is associated with coronary artery disease in Japanese patients with coronary risk factors Arterioscler. Thromb. Vasc. Biol. 22 2002 1680 1685
215. G. Endler, and et al. A microsatellite polymorphism in the heme oxygenase-1 gene promoter is associated with increased bilirubin and HDL levels but not with coronary artery disease Thromb. Haemost. 91 2004 155 161
216. K. Tiroch, and et al. Heme oxygenase-1 gene promoter polymorphism and restenosis following coronary stenting Eur. Heart J. 28 2007 968 973
217. A.E. Courtney, and et al. Association of functional heme oxygenase-1 gene promoter polymorphism with renal transplantation outcomes Am. J. Transplant. 7 2007 908 913
218. K. Ono, and et al. A promoter variant of the heme oxygenase-1 gene may reduce the incidence of ischemic heart disease in Japanese Atherosclerosis 173 2004 315 319
219. J.S. Wijpkema, and et al. Restenosis after percutaneous coronary intervention is associated with the angiotensin-II type-1 receptor 1166A/C polymorphism but not with polymorphisms of angiotensin-converting enzyme, angiotensin-II receptor, angiotensinogen or heme oxygenase-1 Pharmacogenet. Genomics 16 2006 331 337
220. R. Pechlaner, and et al. Heme oxygenase-1 gene promoter microsatellite polymorphism is associated with progressive atherosclerosis and incident cardiovascular disease Arterioscler. Thromb. Vasc. Biol. 35 2015 229 236
221. P.E. Gibbs, and et al. Human biliverdin reductase-based peptides activate and inhibit glucose uptake through direct interaction with the kinase domain of insulin receptor FASEB J. 28 2014 2478 2491
222. L. Yang, and et al. Heme oxygenase-1 gene expression modulates angiotensin II-induced increase in blood pressure Hypertension 43 2004 1221 1226
223. L.G. Melo, and et al. Gene therapy strategy for long-term myocardial protection using adeno-associated virus-mediated delivery of heme oxygenase gene Circulation 105 2002 602 607
224. Y.L. Tang, and et al. A vigilant, hypoxia-regulated heme oxygenase-1 gene vector in the heart limits cardiac injury after ischemia-reperfusion in vivo J. Cardiovasc. Pharmacol. Ther. 10 2005 251 263
225. C.A. Adin, and et al. Protective effects of exogenous bilirubin on ischemia-reperfusion injury in the isolated, perfused rat kidney Am. J. Physiol. Renal Physiol. 288 2005 F778 F784
226. B.J. Wu, and et al. Niacin inhibits vascular inflammation via the induction of heme oxygenase-1 Circulation 125 2012 150 158
227. M.F. Mrad, and et al. Statins modulate transcriptional activity of heme-oxygenase-1 promoter in NIH 3T3 Cells J. Cell. Biochem. 113 2012 3466 3475
228. N.G. Abraham Molecular regulation - biological role of heme in hematopoiesis Blood Rev. 5 1991 19 28
229. + regulatory T cells J. Immunol. 174 2005 5181 5186
230. + regulatory T cells is dependent on expression of heme oxygenase-1 in antigen-presenting cells Am. J. Pathol. 173 2008 154 160
231. T. Minamino, and et al. Targeted expression of heme oxygenase-1 prevents the pulmonary inflammatory and vascular responses to hypoxia Proc. Natl. Acad. Sci. U.S.A. 98 2001 8798 8803
232. M.P. Soares, and et al. Heme oxygenase-1 modulates the expression of adhesion molecules associated with endothelial cell activation J. Immunol. 172 2004 3553 3563
233. D. Sacerdoti, and et al. Rat mesenteric arterial dilator response to 11,12-epoxyeicosatrienoic acid is mediated by activating heme oxygenase Am. J. Physiol. Heart Circ. Physiol. 291 2006 H1999 H2002
234. N.G. Abraham, and et al. Modulation of cGMP by human HO-1 retrovirus gene transfer in pulmonary microvessel endothelial cells Am. J. Physiol. Lung Cell. Mol. Physiol. 283 2002 L1117 L1124
235. G. Sambuceti, and et al. 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 2009 399 407
236. J. Cao, and et al. Upregulation of heme oxygenase-1 combined with increased adiponectin lowers blood pressure in diabetic spontaneously hypertensive rats through a reduction in endothelial cell dysfunction, apoptosis and oxidative stress Int. J. Mol. Sci. 9 2008 2388 2406
237. A.L. Kruger, and et al. D-4F induces heme oxygenase-1 and extracellular superoxide dismutase, decreases endothelial cell sloughing, and improves vascular reactivity in rat model of diabetes Circulation 111 2005 3126 3134
238. X. Liu, and et al. Heme oxygenase-1 (HO-1) inhibits postmyocardial infarct remodeling and restores ventricular function FASEB J. 20 2006 207 216
239. S. Basuroy, and et al. HO-2 provides endogenous protection against oxidative stress and apoptosis caused by TNF-alpha in cerebral vascular endothelial cells Am. J. Physiol. Cell Physiol. 291 2006 C897 C908
240. R. Agarwal Proinflammatory effects of oxidative stress in chronic kidney disease: role of additional angiotensin II blockade Am. J. Physiol. Renal Physiol. 284 2003 F863 F869
241. F. Mazza, and et al. Heme oxygenase-1 gene expression attenuates angiotensin II-mediated DNA damage in endothelial cells Exp. Biol. Med. 228 2003 576 583
242. N.G. Abraham Heme oxygenase attenuated angiotensin II-mediated increase in cyclooxygenase activity and decreased isoprostane F2alpha in endothelial cells Thromb. Res. 110 2003 305 309
243. S. Quan, and et al. Expression of human heme oxygenase-1 in the thick ascending limb attenuates angiotensin II-mediated increase in oxidative injury Kidney Int. 65 2004 1628 1639
244. W. Durante, and et al. Nitric oxide induces heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth cells Circ. Res. 80 1997 557 564
245. G. Li Volti, and et al. Differential effect of heme oxygenase-1 in endothelial and smooth muscle cell cycle progression Biochem. Biophys. Res. Commun. 296 2002 1077 1082
246. X.M. Liu, and et al. Adenovirus-mediated heme oxygenase-1 gene expression stimulates apoptosis in vascular smooth muscle cells Circulation 105 2002 79 84
247. X.M. Liu, and et al. Carbon monoxide inhibits apoptosis in vascular smooth muscle cells Cardiovasc. Res. 55 2002 396 405
248. T. Morita, and et al. Carbon monoxide controls the proliferation of hypoxic smooth muscle cells J. Biol. Chem. 272 1997 32804 32809
249. V. Govindaraju, and et al. Interaction between endothelial heme oxygenase-2 and endothelin-1 in altered aortic reactivity after hypoxia in rats Am. J. Physiol. Heart Circ. Physiol. 288 2005 H962 H970
250. S.J. Stanford, and et al. Carbon monoxide inhibits endothelin-1 release by human pulmonary artery smooth muscle cells Eur. J. Pharmacol. 486 2004 349 352
251. F. Zhang, and et al. CO modulates pulmonary vascular response to acute hypoxia: relation to endothelin Am. J. Physiol. Heart Circ. Physiol. 286 2004 H137 H144
252. M. Zabalgoitia, and et al. Carbon monoxide donors or heme oxygenase-1 (HO-1) overexpression blocks interleukin-18-mediated NF-kappaB-PTEN-dependent human cardiac endothelial cell death Free Radic. Biol. Med. 44 2008 284 298