Skip to main content
SpringerLink
Log in

Role of Nrf2-mediated heme oxygenase-1 upregulation in adaptive survival response to nitrosative stress

  • Published:
Archives of Pharmacal Research Aims and scope Submit manuscript

Abstract

Nitrosative stress caused by reactive nitrogen species such as nitric oxide and peroxynitrite overproduced during inflammation leads to cell death and has been implicated in the pathogenesis of many human ailments. However, relatively mild nitrosative stress may fortify cellular defense capacities, rendering cells tolerant or adaptive to ongoing and subsequent cytotoxic challenges, a phenomenon known as ‘preconditioning’ or ‘hormesis’. One of the key components of cellular stress response is heme oxygenase-1 (HO-1), the rate limiting enzyme in the process of degrading potentially toxic free heme into biliverdin, free iron and carbon monoxide. HO-1 is upregulated by a wide array of stimuli and has antioxidant, anti-inflammatory and other cytoprotective functions. This review is intended to provide readers with a welldocumented account of the research done in the area of cellular adaptive survival response against nitrosative stress with special focus on the role of HO-1 upregulation, especially through activation of the transcription factor, Nrf2.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abraham, N. G., Kushida, T., McClung, J., Weiss, M., Quan, S., Lafaro, R., Darzynkiewicz, Z., and Wolin, M., Heme oxygenase-1 attenuates glucose-mediated cell growth arrest and apoptosis in human microvessel endothelial cells. Circ. Res.. 93, 507–514 (2003).

    Article  PubMed  CAS  Google Scholar 

  • Bauer, P. M., Buga, G. M., Fukuto, J. M., Pegg, A. E., and Ignarro, L. J., Nitric oxide inhibits ornithine decarboxylase via S-nitrosylation of cysteine 360 in the active site of the enzyme. J. Biol. Chem., 276, 34458–34464 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Beckman, J. S., Oxidative damage and tyrosine nitration from peroxynitrite. Chem. Res. Toxicol., 9, 836–844 (1996).

    Article  PubMed  CAS  Google Scholar 

  • Bishop, A., Marquis, J. C., Cashman, N. R., and Demple, B., Adaptive resistance to nitric oxide in motor neurons. Free Radic. Biol. Med., 26, 978–986 (1999).

    Article  PubMed  CAS  Google Scholar 

  • Bishop, A., Yet, S. F., Lee, M. E., Perrella, M. A., and Demple, B., A key role for heme oxygenase-1 in nitric oxide resistance in murine motor neurons and glia. Biochem. Biophys. Res. Commun., 325, 3–9 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Bloom, D., Dhakshinamoorthy, S., and Jaiswal, A. K., Site-directed mutagenesis of cysteine to serine in the DNA binding region of Nrf2 decreases its capacity to upregulate antioxidant response element-mediated expression and antioxidant induction of NAD(P)H:quinone oxidoreductase1 gene. Oncogene, 21, 2191–2200 (2002).

    Article  PubMed  CAS  Google Scholar 

  • Bloom, D. A. and Jaiswal, A. K., Phosphorylation of Nrf2 at Ser40 by protein kinase C in response to antioxidants leads to the release of Nrf2 from INrf2, but is not required for Nrf2 stabilization/accumulation in the nucleus and transcriptional activation of antioxidant response element-mediated NAD(P)H:quinone oxidoreductase-1 gene expression. J. Biol. Chem., 278, 44675–44682 (2003).

    Article  PubMed  CAS  Google Scholar 

  • Botta, D., Franklin, C. C., White, C. C., Krejsa, C. M., Dabrowski, M. J., Pierce, R. H., Fausto, N., and Kavanagh, T. J., Glutamate-cysteine ligase attenuates TNF-induced mitochondrial injury and apoptosis. Free Radic. Biol. Med., 37, 632–642 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Bouton, C., Raveau, M., and Drapier, J. C., Modulation of iron regulatory protein functions. Further insights into the role of nitrogen- and oxygen-derived reactive species. J. Biol. Chem., 271, 2300–2306 (1996).

    Article  PubMed  CAS  Google Scholar 

  • Buckley, B. J., Li, S., and Whorton, A. R., Keap1 modification and nuclear accumulation in response to S-nitrosocysteine. Free Radic. Biol. Med., 44, 692–698 (2008).

    Article  PubMed  CAS  Google Scholar 

  • Buckley, B. J., Marshall, Z. M., and Whorton, A. R., Nitric oxide stimulates Nrf2 nuclear translocation in vascular endothelium. Biochem. Biophys. Res. Commun., 307, 973–979 (2003).

    Article  PubMed  CAS  Google Scholar 

  • Buckley, B. J. and Whorton, A. R., Adaptive responses to peroxynitrite: increased glutathione levels and cystine uptake in vascular cells. Am. J. Physiol. Cell Physiol., 279, C1168–1176 (2000).

    PubMed  CAS  Google Scholar 

  • Choi, B. M., Pae, H. O., Jang, S. I., Kim, Y. M., and Chung, H. T., Nitric oxide as a pro-apoptotic as well as anti-apoptotic modulator. J. Biochem. Mol. Biol., 35, 116–126 (2002).

    PubMed  CAS  Google Scholar 

  • Chung, H. T., Choi, B. M., Kwon, Y. G., and Kim, Y. M., Interactive relations between nitric oxide (NO) and carbon monoxide (CO): heme oxygenase-1/CO pathway is a key modulator in NO-mediated antiapoptosis and anti-inflammation. Methods Enzymol., 441, 329–338 (2008).

    Article  PubMed  CAS  Google Scholar 

  • Cobbs, C. S., Whisenhunt, T. R., Wesemann, D. R., Harkins, L. E., Van Meir, E. G., and Samanta, M., Inactivation of wild-type p53 protein function by reactive oxygen and nitrogen species in malignant glioma cells. Cancer Res., 63, 8670–8673 (2003).

    PubMed  CAS  Google Scholar 

  • Colasanti, M. and Suzuki, H., The dual personality of NO. Trends Pharmacol. Sci., 21, 249–252 (2000).

    Article  PubMed  CAS  Google Scholar 

  • Cui, S., Reichner, J. S., Mateo, R. B., and Albina, J. E., Activated murine macrophages induce apoptosis in tumor cells through nitric oxide-dependent or -independent mechanisms. Cancer Res., 54, 2462–2467 (1994).

    PubMed  CAS  Google Scholar 

  • De Backer, O., Elinck, E., Blanckaert, B., Leybaert, L., Motterlini, R., and Lefebvre, R. A. Water-soluble CO-releasing molecules reduce the development of postoperative ileus via modulation of MAPK/HO-1 signalling and reduction of oxidative stress. Gut, 58, 347–356 (2009).

    Article  PubMed  CAS  Google Scholar 

  • Dhakshinamoorthy, S. and Porter, A. G., Nitric oxide-induced transcriptional up-regulation of protective genes by Nrf2 via the antioxidant response element counteracts apoptosis of neuroblastoma cells. J. Biol. Chem., 279, 20096–20107 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Dinkova-Kostova, A. T., Holtzclaw, W. D., Cole, R. N., Itoh, K., Wakabayashi, N., Katoh, Y., Yamamoto, M., and Talalay, P., Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc. Natl. Acad. Sci. USA, 99, 11908–11913 (2002).

    Article  PubMed  CAS  Google Scholar 

  • Downard, P. J., Wilson, M. A., Spain, D. A., Matheson, P. J., Siow, Y., and Garrison, R. N., Heme oxygenase-dependent carbon monoxide production is a hepatic adaptive response to sepsis. J. Surg. Res., 71, 7–12 (1997).

    Article  PubMed  CAS  Google Scholar 

  • Drapier, J. C. and Hibbs, J. B. Jr., Murine cytotoxic activated macrophages inhibit aconitase in tumor cells. Inhibition involves the iron-sulfur prosthetic group and is reversible. J. Clin. Invest., 78, 790–797 (1986).

    Article  PubMed  CAS  Google Scholar 

  • Drapier, J. C., Wietzerbin, J., and Hibbs, J. B. Jr., Interferon-gamma and tumor necrosis factor induce the L-arginine-dependent cytotoxic effector mechanism in murine macrophages. Eur. J. Immunol., 18, 1587–1592 (1988).

    Article  PubMed  CAS  Google Scholar 

  • Durante, W., Kroll, M. H., Christodoulides, N., Peyton, K. J., and Schafer, A. I., Nitric oxide induces heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth muscle cells. Circ. Res., 80, 557–564 (1997).

    PubMed  CAS  Google Scholar 

  • Esch, T., Stefano, G. B., Fricchione, G. L., and Benson, H., Stress-related diseases — a potential role for nitric oxide. Med. Sci. Monit., 8, RA103–118 (2002).

    PubMed  CAS  Google Scholar 

  • Fang, F. C., Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J. Clin. Invest., 99, 2818–2825 (1997).

    Article  PubMed  CAS  Google Scholar 

  • Fehsel, K., Kroncke, K. D., Meyer, K. L., Huber, H., Wahn, V., and Kolb-Bachofen, V., Nitric oxide induces apoptosis in mouse thymocytes. J. Immunol., 155, 2858–2865 (1995).

    PubMed  CAS  Google Scholar 

  • Ferris, C. D., Jaffrey, S. R., Sawa, A., Takahashi, M., Brady, S. D., Barrow, R. K., Tysoe, S. A., Wolosker, H., Baranano, D. E., Dore, S., Poss, K. D., and Snyder, S. H., Haem oxygenase-1 prevents cell death by regulating cellular iron. Nat. Cell Biol., 1, 152–157 (1999).

    Article  PubMed  CAS  Google Scholar 

  • Foresti, R., Clark, J. E., Green, C. J., and Motterlini, R., Thiol compounds interact with nitric oxide in regulating heme oxygenase-1 induction in endothelial cells. Involvement of superoxide and peroxynitrite anions. J. Biol. Chem., 272, 18411–18417 (1997).

    Article  PubMed  CAS  Google Scholar 

  • Fujii, H., Takahashi, T., Nakahira, K., Uehara, K., Shimizu, H., Matsumi, M., Morita, K., Hirakawa, M., Akagi, R., and Sassa, S., Protective role of heme oxygenase-1 in the intestinal tissue injury in an experimental model of sepsis. Crit. Care Med., 31, 893–902 (2003).

    Article  PubMed  CAS  Google Scholar 

  • Furchgott, R. F. and Jothianandan, D., Endothelium-dependent and -independent vasodilation involving cyclic GMP: relaxation induced by nitric oxide, carbon monoxide and light. Blood Vessels, 28, 52–61 (1991).

    PubMed  CAS  Google Scholar 

  • Gegg, M. E., Beltran, B., Salas-Pino, S., Bolanos, J. P., Clark, J. B., Moncada, S., and Heales, S. J., Differential effect of nitric oxide on glutathione metabolism and mitochondrial function in astrocytes and neurones: implications for neuroprotection/neurodegeneration? J. Neurochem., 86, 228–237 (2003).

    Article  PubMed  CAS  Google Scholar 

  • Gong, P., Cederbaum, A. I., and Nieto, N., Heme oxygenase-1 protects HepG2 cells against cytochrome P450 2E1-dependent toxicity. Free Radic. Biol. Med., 36, 307–318 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Griffith, O. W., and Mulcahy, R. T., The enzymes of glutathione synthesis: gamma-glutamylcysteine synthetase. Adv. Enzymol. Relat. Areas Mol. Biol., 73, 209–267, xii (1999).

    Article  PubMed  CAS  Google Scholar 

  • Grilli, A., De Lutiis, M. A., Patruno, A., Speranza, L., Gizzi, F., Taccardi, A. A., Di Napoli, P., De Caterina, R., Conti, P., and Felaco, M., Inducible nitric oxide synthase and heme oxygenase-1 in rat heart: direct effect of chronic exposure to hypoxia. Ann. Clin. Lab. Sci., 33, 208–215 (2003).

    PubMed  CAS  Google Scholar 

  • Guzik, T. J., Korbut, R., and Adamek-Guzik, T., Nitric oxide and superoxide in inflammation and immune regulation. J. Physiol. Pharmacol., 54, 469–487 (2003).

    PubMed  CAS  Google Scholar 

  • Hara, E., Takahashi, K., Takeda, K., Nakayama, M., Yoshizawa, M., Fujita, H., Shirato, K., and Shibahara, S., Induction of heme oxygenase-1 as a response in sensing the signals evoked by distinct nitric oxide donors. Biochem. Pharmacol., 58, 227–236 (1999).

    Article  PubMed  CAS  Google Scholar 

  • Heneka, M. T., Loschmann, P. A., Gleichmann, M., Weller, M., Schulz, J. B., Wullner, U., and Klockgether, T., Induction of nitric oxide synthase and nitric oxide-mediated apoptosis in neuronal PC12 cells after stimulation with tumor necrosis factor-alpha/lipopolysaccharide. J. Neurochem., 71, 88–94 (1998).

    Article  PubMed  CAS  Google Scholar 

  • Hess, D. T., Matsumoto, A., Kim, S. O., Marshall, H. E., and Stamler, J. S., Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell. Biol., 6, 150–166 (2005).

    Article  PubMed  CAS  Google Scholar 

  • Husain, M., Bourret, T. J., McCollister, B. D., Jones-Carson, J., Laughlin, J., and Vazquez-Torres, A., Nitric oxide evokes an adaptive response to oxidative stress by arresting respiration. J. Biol. Chem., 283, 7682–7689 (2008).

    Article  PubMed  CAS  Google Scholar 

  • Ischiropoulos, H., Biological selectivity and functional aspects of protein tyrosine nitration. Biochem. Biophys. Res. Commun., 305, 776–783 (2003).

    Article  PubMed  CAS  Google Scholar 

  • Itoh, K., Wakabayashi, N., Katoh, Y., Ishii, T., Igarashi, K., Engel, J. D., and Yamamoto, M., Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev., 13, 76–86 (1999).

    Article  PubMed  CAS  Google Scholar 

  • Jackson, R. M., Parish, G., and Helton, E. S., Peroxynitrite modulates MnSOD gene expression in lung epithelial cells. Free Radic. Biol. Med., 25, 463–472 (1998).

    Article  PubMed  CAS  Google Scholar 

  • Jain, A. K., Mahajan, S., and Jaiswal, A. K., Phosphorylation and dephosphorylation of tyrosine 141 regulate stability and degradation of INrf2: a novel mechanism in Nrf2 activation. J. Biol. Chem., 283, 17712–17720 (2008).

    Article  PubMed  CAS  Google Scholar 

  • Jang, J. H., Aruoma, O. I., Jen, L. S., Chung, H. Y., and Surh, Y.-J., Ergothioneine rescues PC12 cells from beta-amyloid-induced apoptotic death. Free Radic. Biol. Med., 36, 288–299 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Kang, K. W., Choi, S. H., and Kim, S. G., Peroxynitrite activates NF-E2-related factor 2/antioxidant response element through the pathway of phosphatidylinositol 3-kinase: the role of nitric oxide synthase in rat glutathione S-transferase A2 induction. Nitric Oxide, 7, 244–253 (2002).

    Article  PubMed  CAS  Google Scholar 

  • Kim, H. P., Ryter, S. W., and Choi, A. M., CO as a cellular signaling molecule. Annu. Rev. Pharmacol. Toxicol., 46, 411–449 (2006).

    Article  PubMed  CAS  Google Scholar 

  • Kim, J. W., Li, M. H., Jang, J. H., Na, H. K., Song, N. Y., Lee, C., Johnson, J. A., and Surh, Y. -J., 15-Deoxy-Delta(12,14)-prostaglandin J2 rescues PC12 cells from H2O2-induced apoptosis through Nrf2-mediated upregulation of heme oxygenase-1: potential roles of Akt and ERK1/2. Biochem. Pharmacol., 76, 1577–1589 (2008).

    Article  PubMed  CAS  Google Scholar 

  • Kolb, J. P., Mechanisms involved in the pro- and anti-apoptotic role of NO in human leukemia. Leukemia, 14, 1685–1694 (2000).

    Article  PubMed  CAS  Google Scholar 

  • Kurozumi, R., Takahashi, M., and Kojima, S., Involvement of mitochondrial peroxynitrite in nitric oxide-induced glutathione synthesis. Biol. Pharm. Bull., 28, 779–785 (2005).

    Article  PubMed  CAS  Google Scholar 

  • Lee, B. S., Heo, J., Kim, Y. M., Shim, S. M., Pae, H. O., and Chung, H. T., Carbon monoxide mediates heme oxygenase 1 induction via Nrf2 activation in hepatoma cells. Biochem. Biophys. Res. Commun., 343, 965–972 (2006).

    Article  PubMed  CAS  Google Scholar 

  • Lee, J. M. and Johnson, J. A., An important role of Nrf2-ARE pathway in the cellular defense mechanism. J. Biochem. Mol. Biol., 37, 139–143 (2004).

    PubMed  CAS  Google Scholar 

  • Leon, L., Jeannin, J. F., and Bettaieb, A., Post-translational modifications induced by nitric oxide (NO): implication in cancer cells apoptosis. Nitric Oxide, 19, 77–83 (2008).

    Article  PubMed  CAS  Google Scholar 

  • Li, H., Marshall, Z. M., and Whorton, A. R., Stimulation of cystine uptake by nitric oxide: regulation of endothelial cell glutathione levels. Am. J. Physiol., 276, C803–811 (1999).

    PubMed  CAS  Google Scholar 

  • Li, M. H., Cha, Y. N., and Surh, Y.-J., Carbon monoxide protects PC12 cells from peroxynitrite-induced apoptotic death by preventing the depolarization of mitochondrial transmembrane potential. Biochem. Biophys. Res. Commun., 342, 984–990 (2006a).

    Article  PubMed  CAS  Google Scholar 

  • Li, M. H., Cha, Y. N., and Surh, Y.-J., Peroxynitrite induces HO-1 expression via PI3K/Akt-dependent activation of NF-E2-related factor 2 in PC12 cells. Free Radic. Biol. Med., 41, 1079–1091 (2006b).

    Article  PubMed  CAS  Google Scholar 

  • Li, M. H., Jang, J. H., Na, H. K., Cha, Y. N., and Surh, Y. J., Carbon monoxide produced by heme oxygenase-1 in response to nitrosative stress induces expression of glutamate-cysteine ligase in PC12 cells via activation of phosphatidylinositol 3-kinase and Nrf2 signaling. J. Biol. Chem., 282, 28577–28586 (2007).

    Article  PubMed  CAS  Google Scholar 

  • Lim, S. Y., Jang, J. H., Na, H. K., Lu, S. C., Rahman, I., and Surh, Y.-J., 15-Deoxy-Delta12,14-prostaglandin J(2) protects against nitrosative PC12 cell death through up-regulation of intracellular glutathione synthesis. J. Biol. Chem., 279, 46263–46270 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Liu, X. M., Peyton, K. J., Ensenat, D., Wang, H., Hannink, M., Alam, J., and Durante, W., 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 (2007).

    Article  PubMed  CAS  Google Scholar 

  • Maines, M. D., Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J., 2, 2557–2568 (1988).

    PubMed  CAS  Google Scholar 

  • Maines, M. D., The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol., 37, 517–554 (1997).

    Article  PubMed  CAS  Google Scholar 

  • Mallis, R. J., Buss, J. E., and Thomas, J. A., Oxidative modification of H-ras: S-thiolation and S-nitrosylation of reactive cysteines. Biochem. J., 355, 145–153 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Mann, G. E., Rowlands, D. J., Li, F. Y., de Winter, P., and Siow, R. C., Activation of endothelial nitric oxide synthase by dietary isoflavones: role of NO in Nrf2-mediated antioxidant gene expression. Cardiovasc. Res., 75, 261–274 (2007).

    Article  PubMed  CAS  Google Scholar 

  • Manna, S. K., Kuo, M. T., and Aggarwal, B. B., Overexpression of gamma-glutamylcysteine synthetase suppresses tumor necrosis factor-induced apoptosis and activation of nuclear transcription factor-kappa B and activator protein-1. Oncogene, 18, 4371–4382 (1999).

    Article  PubMed  CAS  Google Scholar 

  • Mannick, J. B., Hausladen, A., Liu, L., Hess, D. T., Zeng, M., Miao, Q. X., Kane, L. S., Gow, A. J., and Stamler, J. S., Fas-induced caspase denitrosylation. Science, 284, 651–654 (1999).

    Article  PubMed  CAS  Google Scholar 

  • Mariotto, S., Menegazzi, M., and Suzuki, H., Biochemical aspects of nitric oxide. Curr. Pharm. Des., 10, 1627–1645 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Messmer, U. K., Reimer, D. M., Reed, J. C., and Brune, B., Nitric oxide induced poly(ADP-ribose) polymerase cleavage in RAW 264.7 macrophage apoptosis is blocked by Bcl-2. FEBS Lett., 384, 162–166 (1996).

    Article  PubMed  CAS  Google Scholar 

  • Moellering, D., McAndrew, J., Patel, R. P., Cornwell, T., Lincoln, T., Cao, X., Messina, J. L., Forman, H. J., Jo, H., and Darley-Usmar, V. M., Nitric oxide-dependent induction of glutathione synthesis through increased expression of gamma-glutamylcysteine synthetase. Arch. Biochem. Biophys., 358, 74–82 (1998).

    Article  PubMed  CAS  Google Scholar 

  • Moncada, S., Palmer, R. M., and Higgs, E. A., Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev., 43, 109–142 (1991).

    PubMed  CAS  Google Scholar 

  • Moriya, R., Uehara, T., and Nomura, Y., Mechanism of nitric oxide-induced apoptosis in human neuroblastoma SH-SY5Y cells. FEBS Lett., 484, 253–260 (2000).

    Article  PubMed  CAS  Google Scholar 

  • Motohashi, H. and Yamamoto, M., Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol. Med., 10, 549–557 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Motterlini, R., Hidalgo, A., Sammut, I., Shah, K. A., Mohammed, S., Srai, K., and Green, C. J., A precursor of the nitric oxide donor SIN-1 modulates the stress protein heme oxygenase-1 in rat liver. Biochem. Biophys. Res. Commun., 225, 167–172 (1996).

    Article  PubMed  CAS  Google Scholar 

  • Mulcahy, R. T., Bailey, H. H., and Gipp, J. J., Transfection of complementary DNAs for the heavy and light subunits of human gamma-glutamylcysteine synthetase results in an elevation of intracellular glutathione and resistance to melphalan. Cancer Res., 55, 4771–4775 (1995).

    PubMed  CAS  Google Scholar 

  • Murphy, M. P., Nitric oxide and cell death. Biochim. Biophys. Acta, 1411, 401–414 (1999).

    Article  PubMed  CAS  Google Scholar 

  • Naughton, P., Hoque, M., Green, C. J., Foresti, R., and Motterlini, R., Interaction of heme with nitroxyl or nitric oxide amplifies heme oxygenase-1 induction: involvement of the transcription factor Nrf2. Cell. Mol. Biol. (Noisy-le-grand), 48, 885–894 (2002).

    CAS  Google Scholar 

  • Nazarewicz, R. R., Zenebe, W. J., Parihar, A., Larson, S. K., Alidema, E., Choi, J., and Ghafourifar, P., Tamoxifen induces oxidative stress and mitochondrial apoptosis via stimulating mitochondrial nitric oxide synthase. Cancer Res., 67, 1282–1290 (2007).

    Article  PubMed  CAS  Google Scholar 

  • Nguyen, T., Sherratt, P. J., and Pickett, C. B., Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu. Rev. Pharmacol. Toxicol., 43, 233–260 (2003).

    Article  PubMed  CAS  Google Scholar 

  • Nizamutdinova, I. T., Lee, J. H., Seo, H. G., Chang, K. C., and Kim, H. J., NS398 protects cells from sodium nitroprusside-mediated cytotoxicity through enhancing HO-1 induction independent of COX-2 inhibition. Arch. Pharm. Res., 32, 99–107 (2009).

    Article  PubMed  CAS  Google Scholar 

  • Otterbein, L., Sylvester, S. L., and Choi, A. M., Hemoglobin provides protection against lethal endotoxemia in rats: the role of heme oxygenase-1. Am. J. Respir. Cell Mol. Biol., 13, 595–601 (1995).

    PubMed  CAS  Google Scholar 

  • Otterbein, L. E. and Choi, A. M., Heme oxygenase: colors of defense against cellular stress. Am. J. Physiol. Lung. Cell. Mol. Physiol., 279, L1029–1037 (2000).

    PubMed  CAS  Google Scholar 

  • Pacher, P., Beckman, J. S., and Liaudet, L., Nitric oxide and peroxynitrite in health and disease. Physiol. Rev., 87, 315–424 (2007).

    Article  PubMed  CAS  Google Scholar 

  • Packer, M. A. and Murphy, M. P., Peroxynitrite formed by simultaneous nitric oxide and superoxide generation causes cyclosporin-A-sensitive mitochondrial calcium efflux and depolarisation. Eur. J. Biochem., 234, 231–239 (1995).

    Article  PubMed  CAS  Google Scholar 

  • Park, H. S., Huh, S. H., Kim, M. S., Lee, S. H., and Choi, E. J., Nitric oxide negatively regulates c-Jun N-terminal kinase/stress-activated protein kinase by means of S-nitrosylation. Proc. Natl. Acad. Sci. U S A, 97, 14382–14387 (2000).

    Article  PubMed  CAS  Google Scholar 

  • Park, Y. S., Fujiwara, N., Koh, Y. H., Miyamoto, Y., Suzuki, K., Honke, K., and Taniguchi, N., Induction of thioredoxin reductase gene expression by peroxynitrite in human umbilical vein endothelial cells. Biol. Chem., 383, 683–691 (2002).

    Article  PubMed  CAS  Google Scholar 

  • Piantadosi, C. A., Carbon monoxide, reactive oxygen signaling, and oxidative stress. Free Radic. Biol. Med., 45, 562–569 (2008).

    Article  PubMed  CAS  Google Scholar 

  • Rahman, I., Regulation of nuclear factor-kappa B, activator protein-1, and glutathione levels by tumor necrosis factor-alpha and dexamethasone in alveolar epithelial cells. Biochem. Pharmacol., 60, 1041–1049 (2000).

    Article  PubMed  CAS  Google Scholar 

  • Reiter, C. D., Teng, R. J., and Beckman, J. S., Superoxide reacts with nitric oxide to nitrate tyrosine at physiological pH via peroxynitrite. J. Biol. Chem., 275, 32460–32466 (2000).

    Article  PubMed  CAS  Google Scholar 

  • Reynaert, N. L., Ckless, K., Korn, S. H., Vos, N., Guala, A. S., Wouters, E. F., van der Vliet, A., and Janssen-Heininger, Y. M., Nitric oxide represses inhibitory kappaB kinase through S-nitrosylation. Proc. Natl. Acad. Sci. U S A, 101, 8945–8950 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Ridnour, L. A., Sim, J. E., Choi, J., Dickinson, D. A., Forman, H. J., Ahmad, I. M., Coleman, M. C., Hunt, C. R., Goswami, P. C., and Spitz, D. R., Nitric oxide-induced resistance to hydrogen peroxide stress is a glutamate cysteine ligase activity-dependent process. Free Radic. Biol. Med., 38, 1361–1371 (2005).

    Article  PubMed  CAS  Google Scholar 

  • Stamler, J. S., Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell, 78, 931–936 (1994).

    Article  PubMed  CAS  Google Scholar 

  • Stocker, R., Yamamoto, Y., McDonagh, A. F., Glazer, A. N., and Ames, B. N., Bilirubin is an antioxidant of possible physiological importance. Science, 235, 1043–1046 (1987).

    Article  PubMed  CAS  Google Scholar 

  • Stuehr, D. J., Mammalian nitric oxide synthases. Biochim. Biophys. Acta., 1411, 217–230 (1999).

    Article  PubMed  CAS  Google Scholar 

  • Surh, Y. J., Kundu, J. K., and Na, H. K., Nrf2 as a master redox switch in turning on the cellular signaling involved in the induction of cytoprotective genes by some chemopreventive phytochemicals. Planta Med., 74, 1526–1539 (2008).

    Article  PubMed  CAS  Google Scholar 

  • Szabo, C., Ischiropoulos, H., and Radi, R., Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat. Rev. Drug Discov., 6, 662–680 (2007).

    Article  PubMed  CAS  Google Scholar 

  • Townsend, D. M., Tew, K. D., and Tapiero, H., The importance of glutathione in human disease. Biomed. Pharmacother., 57, 145–155 (2003).

    Article  PubMed  CAS  Google Scholar 

  • Vile, G. F., Basu-Modak, S., Waltner, C., and Tyrrell, R. M., Heme oxygenase 1 mediates an adaptive response to oxidative stress in human skin fibroblasts. Proc. Natl. Acad. Sci. U S A, 91, 2607–2610 (1994).

    Article  PubMed  CAS  Google Scholar 

  • Webster, R. P., Macha, S., Brockman, D., and Myatt, L., Peroxynitrite treatment in vitro disables catalytic activity of recombinant p38 MAPK. Proteomics, 6, 4838–4844 (2006).

    Article  PubMed  CAS  Google Scholar 

  • Wegiel, B., Chin, B. Y., and Otterbein, L. E., Inhale to survive, cycle or die? Carbon monoxide and cellular proliferation. Cell Cycle, 7, 1379–1384 (2008).

    PubMed  CAS  Google Scholar 

  • Willis, D., Moore, A. R., Frederick, R., and Willoughby, D. A., Heme oxygenase: a novel target for the modulation of the inflammatory response. Nat. Med., 2, 87–90 (1996).

    Article  PubMed  CAS  Google Scholar 

  • Wink, D. A., Hanbauer, I., Krishna, M. C., DeGraff, W., Gamson, J., and Mitchell, J. B., Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species. Proc. Natl. Acad. Sci. U S A, 90, 9813–9817 (1993).

    Article  PubMed  CAS  Google Scholar 

  • Wu, G., Fang, Y. Z., Yang, S., Lupton, J. R., and Turner, N. D., Glutathione metabolism and its implications for health. J. Nutr., 134, 489–492 (2004).

    PubMed  CAS  Google Scholar 

  • Zhu, H., Itoh, K., Yamamoto, M., Zweier, J. L., and Li, Y., Role of Nrf2 signaling in regulation of antioxidants and phase 2 enzymes in cardiac fibroblasts: protection against reactive oxygen and nitrogen species-induced cell injury. FEBS Lett., 579, 3029–3036 (2005).

    Article  PubMed  CAS  Google Scholar 

  • Zingarelli, B., O’Connor, M., Wong, H., Salzman, A. L., and Szabo, C., Peroxynitrite-mediated DNA strand breakage activates poly-adenosine diphosphate ribosyl synthetase and causes cellular energy depletion in macrophages stimulated with bacterial lipopolysaccharide. J. Immunol., 156, 350–358 (1996).

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. National Research Laboratory of Molecular Carcinogenesis and Chemoprevention, College of Pharmacy, Seoul National University, Seoul, 151-742, Korea

    Young-Joon Surh, Joydeb Kumar Kundu, Mei-Hua Li & Hye-Kyung Na

  2. Inha University College of Medicine, Incheon, Korea

    Young-Nam Cha

  3. On leave from Faculty of Pharmacy, University of Dhaka, Dhaka, 1000, Bangladesh

    Joydeb Kumar Kundu

  4. College of Pharmacy, Seoul National University, Seoul, 151-742, Korea

    Young-Joon Surh

Authors
  1. Young-Joon Surh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joydeb Kumar Kundu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mei-Hua Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hye-Kyung Na
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Young-Nam Cha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Young-Joon Surh.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Surh, YJ., Kundu, J.K., Li, MH. et al. Role of Nrf2-mediated heme oxygenase-1 upregulation in adaptive survival response to nitrosative stress. Arch. Pharm. Res. 32, 1163–1176 (2009). https://doi.org/10.1007/s12272-009-1807-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12272-009-1807-8

Key words

Search

Navigation