Advertisement

Inflammation Research

, Volume 67, Issue 7, pp 579–588 | Cite as

A review on heme oxygenase-1 induction: is it a necessary evil

  • Ajaz Ahmad Waza
  • Zeenat Hamid
  • Sajad Ali
  • Shabir Ahmad Bhat
  • Musadiq Ahmad Bhat
Review
  • 161 Downloads

Abstract

Heme oxygenase-1 (HO-1) is considered to be the main protein in diseases arising as a result of oxidative and inflammatory insults. Tremendous research has been carried out on HO-1 since years, pertaining its cytoprotective effect against oxidative injury and other cellular stresses. HO-1, by regulating intracellular levels of pro-oxidant heme, or by other benefits of its by-products such as carbon monoxide (CO) and biliverdin (BV) had become an important candidate protein to be up-regulated to combat diverse stressful events. Although the beneficial effects of HO-1 induction have been reported in a number of cells and tissues, a growing body of evidence indicates that this increased HO-1 expression may lead to the progression of several diseases such as neurodegeneration, carcinogenesis. But it is not clear, what accounts for the increased expression of HO-1 in cells and tissues. The observed friendly role of HO-1 in a wide range of stress conditions since times is now doubtful. Therefore, more studies are needed to elucidate the exact role of HO-1 in various stressful events. Being more concise, elucidating the effect of HO-1 up-regulation on critical genes involved in particular diseases such as cancer will help to a larger extent to comprehend the exact role of HO-1. This review will assist in understanding the dual role (protective and detrimental) of HO-1 and the signaling pathway involved and will help in unraveling the doubtful role of HO-1 induction.

Keywords

Bilirubin Carbon monoxide Cytoprotection Heme Heme oxygenase Oxidative dysregulation 

Notes

Acknowledgements

Council of Scientific and Industrial Research (CSIR) GOI, New Delhi is acknowledged for providing fellowship to Ajaz Ahmad Waza (CSIR-RA fellow) (9/251 (0077)/2k17).

Compliance with ethical standards

Conflict of interest

The authors declare that no competing interests exist.

References

  1. 1.
    Maines MD, Gibbs PE. 30 some years of heme oxygenase: from a “molecular wrecking ball” to a “mesmerizing” trigger of cellular events. Biochem Biophys Res Commun. 2005;338:568–77.CrossRefPubMedGoogle Scholar
  2. 2.
    Nitti M, Piras S, Marinari UM, Moretta L, Pronzato MA, Furfaro AL. HO-1 induction in cancer progression: a matter of cell adaptation. Antioxidants. 2017;6:29.CrossRefPubMedCentralGoogle Scholar
  3. 3.
    Hayashi S, Omata Y, Sakamoto H, Higashimoto Y, Hara T, Sagara Y, Noguchi M. Characterization of rat heme oxygenase-3 gene. Implication of processed pseudogenes derived from heme oxygenase-2 gene. Gene. 2004;336:241–50.CrossRefPubMedGoogle Scholar
  4. 4.
    Lin Q, Weis S, Yang G, Weng YH, Helston R, et al. Heme oxygenase-1 protein localizes to the nucleus and activates transcription factors important in oxidative stress. J Biol Chem. 2007;282:20621–33.CrossRefPubMedGoogle Scholar
  5. 5.
    Slebos DJ, Ryter SW, van der Toorn M, Liu F, Guo F, et al. Mitochondrial localization and function of heme oxygenase-1 in cigarette smoke-induced cell death. Am J Respir Cell Mol Biol. 2007;36:409–17.CrossRefPubMedGoogle Scholar
  6. 6.
    Kapturczak MH, Wasserfall C, Brusko T, Campbell-Thompson M, Ellis TM, et al. Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse. Am J Pathol. 2004;165:1045–53.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Bindu S, Pal C, Dey S, Goyal M, Alam A, et al. Translocation of heme oxygenase-1 to mitochondria is a novel cytoprotective mechanism against non-steroidal anti-inflammatory drug-induced mitochondrial oxidative stress, apoptosis, and gastric mucosal injury. J Biol Chem. 2011;286:39387–402.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Sacca P, Meiss R, Casas G, Mazza O, Calvo JC, et al. Nuclear translocation of haeme oxygenase-1 is associated to prostate cancer. Br J Cancer. 2007;97:1683–9.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Hsu FF, Yeh CT, Sun YJ, Chiang MT, Lan WM, et al. Signal peptide peptidase-mediated nuclear localization of heme oxygenase-1 promotes cancer cell proliferation and invasion independent of its enzymatic activity. Oncogene. 2015;34:2360–70.CrossRefPubMedGoogle Scholar
  10. 10.
    Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev. 2006;86:583–650.CrossRefPubMedGoogle Scholar
  11. 11.
    Son Y, Lee JH, Chung HT, Pae HO. Therapeutic roles of heme oxygenase-1 in metabolic diseases: curcumin and resveratrol analogues as possible inducers of heme oxygenase-1. Oxid Med Cell Longev. 2013;2013:639541.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Li Volti G, Sacerdoti D, Di Giacomo C, Barcellona ML, Scacco A, et al. Natural heme oxygenase-1 inducers in hepatobiliary function. World J Gastroenterol. 2008;14:6122–32.CrossRefPubMedGoogle Scholar
  13. 13.
    Doberer D, Haschemi A, Andreas M, Zapf TC, Clive B, et al. Haem arginate infusion stimulates haem oxygenase-1 expression in healthy subjects. Br J Pharmacol. 2010;161:1751–62.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Guijarro-Munoz I, Compte M, Alvarez-Cienfuegos A, Alvarez-Vallina L, Sanz L. Lipopolysaccharide activates toll-like receptor 4 (TLR4)-mediated NF-kappaB signaling pathway and proinflammatory response in human pericytes. J Biol Chem. 2014;289:2457–68.CrossRefPubMedGoogle Scholar
  15. 15.
    Arango Duque G, Descoteaux A. Macrophage cytokines: involvement in immunity and infectious diseases. Front Immunol. 2014;5:491.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Konrad FM, Knausberg U, Hone R, Ngamsri KC, Reutershan J. Tissue heme oxygenase-1 exerts anti-inflammatory effects on LPS-induced pulmonary inflammation. Mucosal Immunol. 2016;9:98–111.CrossRefPubMedGoogle Scholar
  17. 17.
    Lee JH, Jung NH, Lee BH, Kim SH, Jun JH. Suppression of heme oxygenase-1 by prostaglandin E2-protein kinase A-A-kinase anchoring protein signaling is central for augmented cyclooxygenase-2 expression in lipopolysaccharide-stimulated RAW 264.7 macrophages. Allergy Asthma Immunol Res. 2013;5:329–36.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Rushworth SA, MacEwan DJ, O’Connell MA. Lipopolysaccharide-induced expression of NAD(P)H:quinone oxidoreductase 1 and heme oxygenase-1 protects against excessive inflammatory responses in human monocytes. J Immunol. 2008;181:6730–7.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Camhi SL, Alam J, Wiegand GW, Chin BY, Choi AM. Transcriptional activation of the HO-1 gene by lipopolysaccharide is mediated by 5′ distal enhancers: role of reactive oxygen intermediates and AP-1. Am J Respir Cell Mol Biol. 1998;18:226–34.CrossRefPubMedGoogle Scholar
  20. 20.
    Upadhyay S, Dixit M. Role of polyphenols and other phytochemicals on molecular signaling. Oxid Med Cell Longev. 2015;2015:504253.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Mollazadeh H, Cicero AFG, Blesso CN, Pirro M, Majeed M, Sahebkar A. Immune modulation by curcumin: the role of interleukin-10. Crit Rev Food Sci Nutr. 2017:1–13.  https://doi.org/10.1080/10408398.2017.1358139
  22. 22.
    Pae HO, Jeong GS, Jeong SO, Kim HS, Kim SA, et al. Roles of heme oxygenase-1 in curcumin-induced growth inhibition in rat smooth muscle cells. Exp Mol Med. 2007;39:267–77.CrossRefPubMedGoogle Scholar
  23. 23.
    Kim SY, Park E, Park JA, Choi BS, Kim S, et al. The plant phenolic diterpene carnosol suppresses sodium nitroprusside-induced toxicity in c6 glial cells. J Agric Food Chem. 2010;58:1543–50.CrossRefPubMedGoogle Scholar
  24. 24.
    Kundu J, Chae IG, Chun KS. Fraxetin induces heme oxygenase-1 expression by activation of Akt/Nrf2 or AMP-activated protein kinase alpha/Nrf2 pathway in HaCaT cells. J Cancer Prev. 2016;21:135–43.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Farombi EO, Surh YJ. Heme oxygenase-1 as a potential therapeutic target for hepatoprotection. J Biochem Mol Biol. 2006;39:479–91.PubMedGoogle Scholar
  26. 26.
    Alam J, Cook JL. How many transcription factors does it take to turn on the heme oxygenase-1 gene? Am J Respir Cell Mol Biol. 2007;36:166–74.CrossRefPubMedGoogle Scholar
  27. 27.
    Immenschuh S, Ramadori G. Gene regulation of heme oxygenase-1 as a therapeutic target. Biochem Pharmacol. 2000;60:1121–8.CrossRefPubMedGoogle Scholar
  28. 28.
    Chen HG, Xie KL, Han HZ, Wang WN, Liu DQ, Wang GL, Yu YH. Heme oxygenase-1 mediates the anti-inflammatory effect of molecular hydrogen in LPS-stimulated RAW 264.7 macrophages. Int J Surg. 2013;11:1060–6.CrossRefPubMedGoogle Scholar
  29. 29.
    Otterbein LE, Bach FH, Alam J, Soares M, Tao H, Lu, et al. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med. 2000;6:422–8.CrossRefPubMedGoogle Scholar
  30. 30.
    Morse D, Pischke SE, Zhou Z, Davis RJ, Flavell RA, et al. Suppression of inflammatory cytokine production by carbon monoxide involves the JNK pathway and AP-1. J Biol Chem. 2003;278:36993–8.CrossRefPubMedGoogle Scholar
  31. 31.
    Lee TS, Chau LY. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med. 2002;8:240–6.CrossRefPubMedGoogle Scholar
  32. 32.
    Hayashi S, Takamiya R, Yamaguchi T, Matsumoto K, Tojo SJ, et al. Induction of heme oxygenase-1 suppresses venular leukocyte adhesion elicited by oxidative stress: role of bilirubin generated by the enzyme. Circ Res. 1999;85:663–71.CrossRefPubMedGoogle Scholar
  33. 33.
    Ndisang JF, Jadhav A. Heme oxygenase system enhances insulin sensitivity and glucose metabolism in streptozotocin-induced diabetes. Am J Physiol Endocrinol Metab. 2009;296:E829–41.CrossRefPubMedGoogle Scholar
  34. 34.
    Galeotti C, Hegde P, Das M, Stephen-Victor E, Canale F, et al. Heme oxygenase-1 is dispensable for the anti-inflammatory activity of intravenous immunoglobulin. Sci Rep. 2016;6:19592.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Liu Z, Zhou T, Ziegler AC, Dimitrion P, Zuo L. Oxidative stress in neurodegenerative diseases: from molecular mechanisms to clinical applications. Oxid Med Cell Longev. 2017;2017:2525967.PubMedPubMedCentralGoogle Scholar
  36. 36.
    Chen J. Heme oxygenase in neuroprotection: from mechanisms to therapeutic implications. Rev Neurosci. 2014;25:269–80.CrossRefPubMedGoogle Scholar
  37. 37.
    Chen K, Gunter K, Maines MD. Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death. J Neurochem. 2000;75:304–13.CrossRefPubMedGoogle Scholar
  38. 38.
    Takeda A, Perry G, Abraham NG, Dwyer BE, Kutty RK, et al. Overexpression of heme oxygenase in neuronal cells, the possible interaction with Tau. J Biol Chem. 2000;275:5395–9.CrossRefPubMedGoogle Scholar
  39. 39.
    Hung SY, Liou HC, Kang KH, Wu RM, Wen CC, et al. Overexpression of heme oxygenase-1 protects dopaminergic neurons against 1-methyl-4-phenylpyridinium-induced neurotoxicity. Mol Pharmacol. 2008;74:1564–75.CrossRefPubMedGoogle Scholar
  40. 40.
    Sun GY, Chen Z, Jasmer KJ, Chuang DY, Gu Z, Hannink M, Simonyi A. Quercetin attenuates inflammatory responses in BV-2 microglial cells: role of MAPKs on the Nrf2 pathway and induction of heme oxygenase-1. PloS One. 2015;10:e0141509.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Vairano M, Dello Russo C, Pozzoli G, Tringali G, Preziosi P, Navarra P. A functional link between heme oxygenase and cyclo-oxygenase activities in cortical rat astrocytes. Biochem Pharmacol. 2001;61:437–41.CrossRefPubMedGoogle Scholar
  42. 42.
    Chen-Roetling J, Regan RF. Effect of heme oxygenase-1 on the vulnerability of astrocytes and neurons to hemoglobin. Biochem Biophys Res Commun. 2006;350:233–7.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Song W, Patel A, Han D, Paudel HK, Schipper HM. Heme oxygenase-1 promotes proteosomal degradation of tau and alpha-synuclein in human neuroblastoma cells. Alzheimer Assoc. 2008; 4(Supplement):T410.Google Scholar
  44. 44.
    Bolisetty S, Traylor A, Zarjou A, Johnson MS, Benavides GA, et al. Mitochondria-targeted heme oxygenase-1 decreases oxidative stress in renal epithelial cells. Am J Physiol Renal Physiol. 2013;305:F255–64.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Roger VL, Go AS, Lloyd-Jones DM, Adams RJ, Berry JD, et al. American Heart Association Statistics, S. Stroke Statistics. Heart disease and stroke statistics–2011 update: a report from the. American Heart Association. Circulation. 2011;123:e18–e209.CrossRefPubMedGoogle Scholar
  46. 46.
    Ewing JF, Raju VS, Maines MD. Induction of heart heme oxygenase-1 (HSP32) by hyperthermia: possible role in stress-mediated elevation of cyclic 3′:5′-guanosine monophosphate. J Pharmacol Exp Ther. 1994;271:408–14.PubMedGoogle Scholar
  47. 47.
    Yet SF, Perrella MA, Layne MD, Hsieh CM, Maemura K, et al. Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice. J Clin Invest. 1999;103:R23–29.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Yet SF, Tian R, Layne MD, Wang ZY, Maemura K, et al. Cardiac-specific expression of heme oxygenase-1 protects against ischemia and reperfusion injury in transgenic mice. Circ Res. 2001;89:168–73.CrossRefPubMedGoogle Scholar
  49. 49.
    Wang G, Hamid T, Keith RJ, Zhou G, Partridge CR, et al. Cardioprotective and antiapoptotic effects of heme oxygenase-1 in the failing heart. Circulation. 2010;121:1912–25.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Tang YL, Qian K, Zhang YC, Shen L, Phillips MI. A vigilant, hypoxia-regulated heme oxygenase-1 gene vector in the heart limits cardiac injury after ischemia-reperfusion in vivo. J Cardiovasc Pharmacol Ther. 2005;10:251–63.CrossRefPubMedGoogle Scholar
  51. 51.
    Schillaci G, Pirro M, Ronti T, Gemelli F, Pucci G, et al. Prognostic impact of prolonged ventricular repolarization in hypertension. Arch Int Med. 2006;166:909–13.CrossRefGoogle Scholar
  52. 52.
    Mordukhovich I, Kloog I, Coull B, Koutrakis P, Vokonas P, Schwartz J. Association between particulate air pollution and QT interval duration in an elderly cohort. Epidemiology. 2016;27:284–90.PubMedPubMedCentralGoogle Scholar
  53. 53.
    Grochot-Przeczek A, Kotlinowski J, Kozakowska M, Starowicz K, Jagodzinska J, et al. Heme oxygenase-1 is required for angiogenic function of bone marrow-derived progenitor cells: role in therapeutic revascularization. Antioxid Redox Signal. 2014;20:1677–92.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Pirro M, Schillaci G, Romagno PF, Mannarino MR, Bagaglia F, et al. Influence of short-term rosuvastatin therapy on endothelial progenitor cells and endothelial function. J Cardiovasc Pharmacol Ther. 2009;14:14–21.CrossRefPubMedGoogle Scholar
  55. 55.
    Lin HH, Chen YH, Yet SF, Chau LY. After vascular injury, heme oxygenase-1/carbon monoxide enhances re-endothelialization via promoting mobilization of circulating endothelial progenitor cells. J Thromb Haemost JTH. 2009;7:1401–8.CrossRefPubMedGoogle Scholar
  56. 56.
    Bianconi V, Sahebkar A, Kovanen P, Bagaglia F, Ricciuti B, et al. Endothelial and cardiac progenitor cells for cardiovascular repair: a controversial paradigm in cell therapy. Pharmacol Ther. 2018;181:156–68.CrossRefPubMedGoogle Scholar
  57. 57.
    Sikorski EM, Hock T, Hill-Kapturczak N, Agarwal A. The story so far: molecular regulation of the heme oxygenase-1 gene in renal injury. Am J Physiol Renal Physiol. 2004;286:F425–441.CrossRefPubMedGoogle Scholar
  58. 58.
    Lever JM, Boddu R, George JF, Agarwal A. Heme oxygenase-1 in kidney health and disease. Antioxid Redox Signal. 2016;25:165–83.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Feitoza CQ, Goncalves GM, Bertocchi AP, Wang PW, Damiao MJ, et al. A role for HO-1 in renal function impairment in animals subjected to ischemic and reperfusion injury and treated with immunosuppressive drugs. Transp Proc. 2007;39:424–6.CrossRefGoogle Scholar
  60. 60.
    Aizawa T, Ishizaka N, Taguchi J, Nagai R, Mori I, et al. Heme oxygenase-1 is upregulated in the kidney of angiotensin II-induced hypertensive rats: possible role in renoprotection. Hypertension. 2000;35:800–6.CrossRefPubMedGoogle Scholar
  61. 61.
    Aycan-Ustyol E, Kabasakal M, Bekpinar S, Alp-Yildirim FI, Tepe O, et al. Vascular function and arginine and dimethylarginines in gentamicin-induced renal failure: a possible effect of heme oxygenase 1 inducer hemin. Can J Physiol Pharmacol. 2017;95:1406–13.CrossRefPubMedGoogle Scholar
  62. 62.
    Origassa CS, Camara NO. Cytoprotective role of heme oxygenase-1 and heme degradation derived end products in liver injury. World J Hepatol. 2013;5:541–9.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    McNally SJ, Harrison EM, Ross JA, Garden OJ, Wigmore SJ. Curcumin induces heme oxygenase-1 in hepatocytes and is protective in simulated cold preservation and warm reperfusion injury. Transplantation. 2006;81:623–6.CrossRefPubMedGoogle Scholar
  64. 64.
    Waza. AA, Hamid Z. Majoon-e-Dabeed-ul-Ward protects lung cells against ethanol-induced cell death and activates Nrf2/HO-1 signaling pathway. Int J Res BioSci. 2018;7:1–7.Google Scholar
  65. 65.
    McCarter SD, Badhwar A, Scott JR, Akyea TG, Bihari A, et al. Remote liver injury is attenuated by adenovirus-mediated gene transfer of heme oxygenase-1 during the systemic inflammatory response syndrome. Microcirculation. 2004;11:587–95.CrossRefPubMedGoogle Scholar
  66. 66.
    Sass G, Soares MC, Yamashita K, Seyfried S, Zimmermann WH, et al. Heme oxygenase-1 and its reaction product, carbon monoxide, prevent inflammation-related apoptotic liver damage in mice. Hepatology. 2003;38:909–18.CrossRefPubMedGoogle Scholar
  67. 67.
    Wu H, Zhang G, Huang L, Pang H, Zhang N, Chen Y, Wang G. Hepatoprotective effect of polyphenol-enriched fraction from folium microcos on oxidative stress and apoptosis in acetaminophen-induced liver injury in mice. Oxid Med Cell Longev. 2017;2017:3631565.PubMedPubMedCentralGoogle Scholar
  68. 68.
    Tiwari S, Ndisang JF. The heme oxygenase system and type-1 diabetes. Curr Pharm Des. 2014;20:1328–37.CrossRefPubMedGoogle Scholar
  69. 69.
    Lee EM, Lee YE, Lee E, Ryu GR, Ko SH, et al. Protective effect of heme oxygenase-1 on high glucose-induced pancreatic beta-cell injury. Diabetes Metab J. 2011;35:469–79.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Castany S, Carcole M, Leanez S, Pol O. The induction of heme oxygenase 1 decreases painful diabetic neuropathy and enhances the antinociceptive effects of morphine in diabetic mice. PloS One. 2016;11:e0146427.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Prawan A, Kundu JK, Surh YJ. Molecular basis of heme oxygenase-1 induction: implications for chemoprevention and chemoprotection. Antioxid Redox Signal. 2005;7:1688–703.CrossRefPubMedGoogle Scholar
  72. 72.
    Abdalla MY, Ahmad IM, Switzer B, Britigan BE. Induction of heme oxygenase-1 contributes to survival of Mycobacterium abscessus in human macrophages-like THP-1 cells. Redox Biol. 2015;4:328–39.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Genter MB, Burman DM, Vijayakumar S, Ebert CL, Aronow BJ. Genomic analysis of alachlor-induced oncogenesis in rat olfactory mucosa. Physiol Genom. 2002;12:35–45.CrossRefGoogle Scholar
  74. 74.
    Gong P, Hu B, Cederbaum AI. Diallyl sulfide induces heme oxygenase-1 through MAPK pathway. Arch Biochem Biophys. 2004;432:252–60.CrossRefPubMedGoogle Scholar
  75. 75.
    Nuhn P, Kunzli BM, Hennig R, Mitkus T, Ramanauskas T, et al. Heme oxygenase-1 and its metabolites affect pancreatic tumor growth in vivo. Mol Cancer. 2009;8:37.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Dulak J, Deshane J, Jozkowicz A, Agarwal A. Heme oxygenase-1 and carbon monoxide in vascular pathobiology: focus on angiogenesis. Circulation. 2008;117:231–41.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Goswami A, Ranganathan P, Rangnekar VM. The phosphoinositide 3-kinase/Akt1/Par-4 axis: a cancer-selective therapeutic target. Cancer Res. 2006;66:2889–92.CrossRefPubMedGoogle Scholar
  78. 78.
    Banerjee P, Basu A, Wegiel B, Otterbein LE, Mizumura K, et al. Heme oxygenase-1 promotes survival of renal cancer cells through modulation of apoptosis- and autophagy-regulating molecules. J Biol Chem. 2012;287:32113–23.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Andreadi CK, Howells LM, Atherfold PA, Manson MM. Involvement of Nrf2, p38, B-Raf, and nuclear factor-kappaB, but not phosphatidylinositol 3-kinase, in induction of hemeoxygenase-1 by dietary polyphenols. Mol Pharmacol. 2006;69:1033–40.PubMedGoogle Scholar
  80. 80.
    Jozkowicz A, Huk I, Nigisch A, Weigel G, Dietrich W, Motterlini R, Dulak J. Heme oxygenase and angiogenic activity of endothelial cells: stimulation by carbon monoxide and inhibition by tin protoporphyrin-IX. Antioxid Redox Signal. 2003;5:155–62.CrossRefPubMedGoogle Scholar
  81. 81.
    Mayerhofer M, Florian S, Krauth MT, Aichberger KJ, Bilban M, et al. Identification of heme oxygenase-1 as a novel BCR/ABL-dependent survival factor in chronic myeloid leukemia. Cancer Res. 2004;64:3148–54.CrossRefPubMedGoogle Scholar
  82. 82.
    Nowis D, Legat M, Grzela T, Niderla J, Wilczek E, et al. Heme oxygenase-1 protects tumor cells against photodynamic therapy-mediated cytotoxicity. Oncogene. 2006;25:3365–74.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Hirai K, Sasahira T, Ohmori H, Fujii K, Kuniyasu H. Inhibition of heme oxygenase-1 by zinc protoporphyrin IX reduces tumor growth of LL/2 lung cancer in C57BL mice. Int J Cancer. 2007;120:500–5.CrossRefPubMedGoogle Scholar
  84. 84.
    Momtazi AA, Shahabipour F, Khatibi S, Johnston TP, Pirro M, Sahebkar A. Curcumin as a microRNA regulator in cancer: a review. Rev Physiol Biochem Pharmacol. 2016;171:1–38.CrossRefPubMedGoogle Scholar
  85. 85.
    Ghattas MH, Chuang LT, Kappas A, Abraham NG. Protective effect of HO-1 against oxidative stress in human hepatoma cell line (HepG2) is independent of telomerase enzyme activity. Int J Biochem Cell Biol. 2002;34:1619–28.CrossRefPubMedGoogle Scholar
  86. 86.
    Murakami A, Fujimori Y, Yoshikawa Y, Yamada S, Tamura K, et al. Heme oxygenase-1 promoter polymorphism is associated with risk of malignant mesothelioma. Lung. 2012;190:333–7.CrossRefPubMedGoogle Scholar
  87. 87.
    Kikuchi A, Yamaya M, Suzuki S, Yasuda H, Kubo H, et al. Association of susceptibility to the development of lung adenocarcinoma with the heme oxygenase-1 gene promoter polymorphism. Hum Genet. 2005;116:354–60.CrossRefPubMedGoogle Scholar
  88. 88.
    Sawa T, Mounawar M, Tatemichi M, Gilibert I, Katoh T, Ohshima H. Increased risk of gastric cancer in Japanese subjects is associated with microsatellite polymorphisms in the heme oxygenase-1 and the inducible nitric oxide synthase gene promoters. Cancer Lett. 2008;269:78–84.CrossRefPubMedGoogle Scholar
  89. 89.
    Schipper HM, Cisse S, Stopa EG. Expression of heme oxygenase-1 in the senescent and Alzheimer-diseased brain. Ann Neurol. 1995;37:758–68.CrossRefPubMedGoogle Scholar
  90. 90.
    Yu X, Song N, Guo X, Jiang H, Zhang H, Xie J. Differences in vulnerability of neurons and astrocytes to heme oxygenase-1 modulation: implications for mitochondrial ferritin. Sci Rep. 2016;6:24200.CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Schipper HM, Song W, Zukor H, Hascalovici JR, Zeligman D. Heme oxygenase-1 and neurodegeneration: expanding frontiers of engagement. J Neurochem. 2009;110:469–85.CrossRefPubMedGoogle Scholar
  92. 92.
    Schipper HM, Song W. A heme oxygenase-1 transducer model of degenerative and developmental brain disorders. Int J Mol Sci. 2015;16:5400–19.CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Qato MK, Maines MD. Prevention of neonatal hyperbilirubinaemia in non-human primates by Zn-protoporphyrin. Biochem J. 1985;226:51–7.CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Wang J, Dore S. Heme oxygenase-1 exacerbates early brain injury after intracerebral haemorrhage. Brain. 2007;130:1643–52.CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Kadoya C, Domino EF, Yang GY, Stern JD, Betz AL. Preischemic but not postischemic zinc protoporphyrin treatment reduces infarct size and edema accumulation after temporary focal cerebral ischemia in rats. Stroke. 1995;26:1035–8.CrossRefPubMedGoogle Scholar
  96. 96.
    Lee DW, Gelein RM, Opanashuk LA. Heme-oxygenase-1 promotes polychlorinated biphenyl mixture aroclor 1254-induced oxidative stress and dopaminergic cell injury. Toxicol Sci. 2006;90:159–67.CrossRefPubMedGoogle Scholar
  97. 97.
    Ursu ON, Sauter M, Ettischer N, Kandolf R, Klingel K. Heme oxygenase-1 mediates oxidative stress and apoptosis in coxsackievirus B3-induced myocarditis. Cell Physiol Biochem. 2014;33:52–66.CrossRefPubMedGoogle Scholar
  98. 98.
    Kang J, Jeong MG, Oh S, Jang EJ, Kim HK, Hwang ES. A FoxO1-dependent, but NRF2-independent induction of heme oxygenase-1 during muscle atrophy. FEBS Lett. 2014;588:79–85.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Ajaz Ahmad Waza
    • 1
  • Zeenat Hamid
    • 2
  • Sajad Ali
    • 1
  • Shabir Ahmad Bhat
    • 1
  • Musadiq Ahmad Bhat
    • 3
  1. 1.Centre of Research for Development (CORD)University of KashmirSrinagarIndia
  2. 2.Department of BiotechnologyUniversity of KashmirSrinagarIndia
  3. 3.Maulana Azad Medical College and Associated HospitalsNew DelhiIndia

Personalised recommendations