Induction of hemeoxygenase-1 expression after inhibition of hemeoxygenase activity promotes inflammation and worsens ischemic brain damage in mice

Neuroscience

Volumn 243, Issue , 2013, Pages 22-32

  Perez de Puig I ^a,b   Martin A ^a,b,c   Gorina, R ^a,b,d   de la Rosa, X ^a,b   Martinez, E ^a,b   Planas, A M ^a,b  

^a INST D INVESTIGACIONS B   (Spain)

^b INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^c CIC BIOMAGUNE   (Spain)

^d UNIVERSITY OF BERN   (Switzerland)

Author keywords

Bach 1; Brain damage; Hemeoxygenase (HO); HO 1; Stroke

Indexed keywords

HEME OXYGENASE; HEME OXYGENASE 1; INTERLEUKIN 1BETA; PROTOPORPHYRIN ZINC; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ZINC PROTOPORPHYRIN IX;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD VESSEL; BRAIN INFARCTION SIZE; CARBOXY TERMINUS HELICASE 1 GENE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME INDUCTION; ENZYME INHIBITION; GENE; GENE REPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYPOXIC ISCHEMIC ENCEPHALOPATHY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEUTROPHIL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; BLOTTING, WESTERN; BRAIN ISCHEMIA; ENZYME INHIBITORS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; HEME OXYGENASE-1; INFLAMMATION; MALE; MEMBRANE PROTEINS; MICE; PROTOPORPHYRINS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84876992081     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.03.046     Document Type: Article

References (62)

1. Beschorner R., Adjodah D., Schwab J.M., Mittelbronn M., Pedal I., Mattern R., Schluesener H.J., Meyermann R. Long-term expression of heme oxygenase (HO-1, HSP-32) following focal cerebral infarctions and traumatic brain injury in humans. Acta Neuropathol 2000, 100:377-384.
2. Bidmon H.J., Emde B., Oermann E., Kubitz R., Witte O.W., Zilles K. Heme oxygenase-1 (HSP-32) and heme oxygenase-2 induction in neurons and glial cells of cerebral regions and its relation to iron accumulation after focal cortical photothrombosis. Exp Neurol 2001, 168:1-22.
3. Bouet V., Boulouard M., Toutain J., Divoux D., Bernaudin M., Schumann-Bard P., Freret T. The adhesive removal test: a sensitive methods to assess sensorimotor deficicts in mice. Nat Prot 2009, 4:1560-1564.
4. Cervera A., Justicia C., Reverter J.C., Planas A.M., Chamorro A. Steady plasma concentration of unfractionated heparin reduces infarct volume and prevents inflammatory damage after transient focal cerebral ischemia in the rat. J Neurosci Res 2004, 77:565-572.
5. Chen J., Tu Y., Connolly E.C., Ronnett G.V. Heme oxygenase-2 protects against glutathione depletion-induced neuronal apoptosis mediated by bilirubin and cyclic GMP. Curr Neurovasc Res 2005, 2:121-131.
6. Collino M., Aragno M., Mastrocola R., Benetti E., Gallicchio M., Dianzani C., Danni O., Thiemermann C., Fantozzi R. Oxidative stress and inflammatory response evoked by transient cerebral ischemia/reperfusion: effects of the PPAR-alpha agonist WY14643. Free Radic Biol Med 2006, 41:579-589.
7. Cruse I., Maines M.D. Evidence suggesting that the two forms of heme oxygenase are products of different genes. J Biol Chem 1988, 263:3348-3353.
8. Downard P.J., Wilson M.A., Spain D.A., Matheson P.J., Siow Y., Garrison R.N. Heme oxygenase-dependent carbon monoxide production is a hepatic adaptive response to sepsis. J Surg Res 1997, 71:7-12.
9. Famakin B., Mou Y., Spatz M., Lawal M., Hallenbeck J. Downstream Toll-like receptor signaling mediates adaptor-specific cytokine expression following focal cerebral ischemia. J Neuroinflamm 2012, 9:174.
10. Fauconneau B., Petegnief V., Sanfeliu C., Piriou A., Planas A.M. Induction of heat shock proteins by sodium arsenite in cultured astrocytes and reduction of hydrogen peroxide-induced cell death. J Neurochem 2002, 83:1338-1348.
11. Foresti R., Sarathchandra P., Clark J.E., Green C.J., Motterlini R. Peroxynitrite induces haem oxygenase-1 in vascular endothelial cells: a link to apoptosis. Biochem J 1999, 339:729-736.
12. Freitas A., Alves-Filho J.C., Secco D.D., Neto A.F., Ferreira S.H., Barja Fidalgo C., Cunha F.Q. Heme oxygenase/carbon monoxide-biliverdin pathway down regulates neutrophil rolling, adhesion and migration in acute inflammation. Br J Pharmacol 2006, 149:345-354.
13. Fu R., Zhao Z.Q., Zhao H.Y., Zhao J.S., Zhu X.L. Expression of heme oxygenase-1 protein and messenger RNA in permanent cerebral ischemia in rats. Neurol Res 2006, 28:38-45.
14. Geddes J.W., Pettigrew L.C., Holtz M.L., Craddock S.D., Maines M.D. Permanent focal and transient global cerebral ischemia increase glial and neuronal expression of heme oxygenase-1, but not heme oxygenase-2, protein in rat brain. Neurosci Lett 1996, 210:205-208.
15. Guix F.X., Ill-Raga G., Bravo R., Nakaya T., de Fabritiis G., Coma M., Miscione G.P., Villà-Freixa J., Suzuki T., Fernàndez-Busquets X., Valverde M.A., de Strooper B., Muñoz F.J. Amyloid-dependent triosephosphate isomerase nitrotyrosination induces glycation and tau fibrillation. Brain 2009, 132:1335-1345.
16. Hastka J., Lasserre J.J., Schwarzbeck A., Strauch M., Hehlmann R. Zinc protoporphyrin in anemia of chronic disorders. Blood 1993, 81:1200-1204.
17. Igarashi K., Sun J. The heme-Bach1 pathway in the regulation of oxidative stress response and erythroid differentiation. Antioxid Redox Signal 2006, 8:107-118.
18. Imaizumi Y., Mizushima H., Dohi K., Ohtaki H., Funahashi H., Shioda S. Hippocampal heme oxigenase-1 in a murine cardiac arrest model. Acta Neurochir 2003, 86:101-103.
19. Kadoya C., Domino E.F., Yang G.Y., Stern J.D., Betz A.L. Preischemic but not postischemic zinc protoporphyrin treatment reduces infarct size and edema accumulation after temporary focal cerebral ischemia in rats. Stroke 1995, 26:1035-1038.
20. Keyse S.M., Tyrrell R.M. Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci U S A 1989, 86:99-103.
21. Koistinaho J., Miettinen S., Keinänen R., Vartiainen N., Roivainen R., Laitinen J.T. Long-term induction of haem oxygenase-1 (HSP-32) in astrocytes and microglia following transient focal brain ischaemia in the rat. Eur J Neurosci 1996, 8:2265-2272.
22. Kullberg M.C., Ward J.M., Gorelick P.L., Caspar P., Hieny S., Cheever A., Jankovic D., Sher A. Helicobacter hepaticus triggers colitis in specific-pathogen-free interleukin-10 (IL-10)-deficient mice through an IL-12- and gamma interferon-dependent mechanism. Infect Immun 1998, 66:5157-5166.
23. Lee T.S., Chau L.Y. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med 2002, 8:240-246.
24. Li M., Zhang X., Cui L., Yang R., Wang L., Liu L., Du W. The neuroprotection of oxymatrine in cerebral ischemia/reperfusion is related to nuclear factor erythroid 2-related factor 2 (nrf2)-mediated antioxidant response: role of nrf2 and hemeoxygenase-1 expression. Biol Pharm Bull 2011, 34:595-601.
25. Liesz A., Hagmann S., Zschoche C., Adamek J., Zhou W., Sun L., Hug A., Zorn M., Dalpke A., Nawroth P., Veltkamp R. The spectrum of systemic immune alterations after murine focal ischemia: immunodepression versus immunomodulation. Stroke 2009, 40:2849-2858.
26. Lin T.N., Cheung W.M., Wu J.S., Chen J.J., Lin H., Chen J.J., Liou J.Y., Shyue S.K., Wu K.K. 15d-prostaglandin J2 protects brain from ischemia-reperfusion injury. Arterioscler Thromb Vasc Biol 2006, 26:481-487.
27. Lin Q., Weis S., Yang G., Weng Y.H., Helston R., Rish K., Smith A., Bordner J., Polte T., Gaunitz F., Dennery P.A. Heme oxygenase-1 protein localizes to the nucleus and activates transcription factors important in oxidative stress. J Biol Chem 2007, 282:20621-20633.
28. Linnenbaum M., Busker M., Kraehling J.R., Behrends S. Heme oxygenase isoforms differ in their subcellular trafficking during hypoxia and are differentially modulated by cytochrome P450 reductase. PLoS One 2012, 7:e35483.
29. Masini E., Vannacci A., Marzocca C., Pierpaoli S., Giannini L., Fantappié O., Mazzanti R., Mannaioni P.F. Heme oxygenase-1 and the ischemia-reperfusion injury in the rat heart. Exp Biol Med (Maywood) 2003, (22):546-549.
30. Matsuoka Y., Kitamura Y., Okazaki M., Sakata M., Tsukahara T., Taniguchi T. Induction of heme oxygenase-1 and major histocompatibility complex antigens in transient forebrain ischemia. J Cereb Blood Flow Metab 1998, 18:824-832.
31. Matsuoka Y., Okazaki M., Zhao H., Asai S., Ishikawa K., Kitamura Y. Phosphorylation of c-Jun and its localization with heme oxygenase-1 and cyclooxygenase-2 in CA1 pyramidal neurons after transient forebrain ischemia. J Cereb Blood Flow Metab 1999, 19:1247-1255.
32. Metzgeroth G., Schultheis B., Dorn-Beineke A., Hehlmann R., Hastka J. Zinc protoporphyrin, a useful parameter to address hyperferritinemia. Ann Hematol 2007, 86:363-368.
33. Moreira T.J., Cebere A., Cebers G., Ostenson C.G., Efendic S., Liljequist S. Reduced HO-1 protein expression is associated with more severe neurodegeneration after transient ischemia induced by cortical compression in diabetic Goto-Kakizaki rats. J Cereb Blood Flow Metab 2007, 27:1710-1723.
34. Namiranian K., Koehler R.C., Sapirstein A., Doré S. Stroke outcomes in mice lacking the genes for neuronal heme oxygenase-2 and nitric oxide synthase. Curr Neurovasc Res 2005, 2:23-27.
35. Nimura T., Weinstein P.R., Massa S.M., Panter S., Sharp F.R. Heme oxygenase-1 (HO-1) protein induction in rat brain following focal ischemia. Brain Res Mol Brain Res 1996, 37:201-208.
36. Otterbein L.E., Bach F.H., Alam J., Soares M., Tao Lu H., Wysk M., Davis R.J., Flavell R.A., Choi A.M. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 2000, 6:422-428.
37. Panahian N., Yoshiura M., Maines M.D. Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J Neurochem 1999, 72:1187-1203.
38. Paschen W., Uto A., Djuricic B., Schmitt J. Hemeoxygenase expression after reversible ischemia of rat brain. Neurosci Lett 1994, 180:5-8.
39. Pereira M.P., Hurtado O., Cárdenas A., Alonso-Escolano D., Boscá L., Vivancos J., Nombela F., Leza J.C., Lorenzo P., Lizasoain I., Moro M.A. The nonthiazolidinedione PPARgamma agonist L-796,449 is neuroprotective in experimental stroke. J Neuropathol Exp Neurol 2005, 64:797-805.
40. Raju V.S., Maines M.D. Coordinated expression and mechanism of induction of HSP32 (heme oxygenase-1) mRNA by hyperthermia in rat organs. Biochim Biophys Acta 1994, 1217:273-280.
41. Ren J., Fan C., Chen N., Huang J., Yang Q. Resveratrol pretreatment attenuates cerebral ischemic injury by upregulating expression of transcription factor Nrf2 and HO-1 in rats. Neurochem Res 2011, 36:2352-2362.
42. Ricchetti G.A., Williams L.M., Foxwell B.M. Heme oxygenase 1 expression induced by IL-10 requires STAT-3 and phosphoinositol-3 kinase and is inhibited by lipopolysaccharide. J Leukoc Biol 2004, 76:719-726.
43. Roh Y.M., Kim K., Kim H. Zinc protoporphyrin IX concentrations between normal adults and the lead-exposed workers measured by HPLC, spectrofluorometer, and hematofluorometer. Ind Health 2000, 38:372-379.
44. Ryter S.W., Alam J., Choi A.M. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 2006, 86:583-650.
45. Saleem S., Zhuang H., Biswal S., Christen Y., Doré S. Ginkgo biloba extract neuroprotective action is dependent on heme oxygenase 1 in ischemic reperfusion brain injury. Stroke 2008, 39:3389-3396.
46. Seldon M.P., Silva G., Pejanovic N., Larsen R., Gregoire I.P., Filipe J., Anrather J., Soares M.P. Heme oxygenase-1 inhibits the expression of adhesion molecules associated with endothelial cell activation via inhibition of NF-kappaB RelA phosphorylation at serine 276. J Immunol 2007, 179:7840-7851.
47. Shibahara S., Muller R.M., Taguchi H. Transcriptional control of rat heme oxygenase by heat shock. J Biol Chem 1987, 262:12889-12892.
48. Soares M.P., Seldon M.P., Gregoire I.P., Vassilevskaia T., Berberat P.O., Yu J., Tsui T.Y., Bach F.H. Heme oxygenase-1 modulates the expression of adhesion molecules associated with endothelial cell activation. J Immunol 2004, 172:3553-3563.
49. Srisook K., Kim C., Cha Y.N. Molecular mechanisms involved in enhancing HO-1 expression: de-repression by heme and activation by Nrf2, the "one-two" punch. Antioxid Redox Signal 2005, 7:1674-1687.
50. Takeda A., Onodera H., Sugimoto A., Itoyama Y., Kogure K., Shibahara S. Increased expression of heme oxygenase mRNA in rat brain following transient forebrain ischemia. Brain Res 1994, 666:120-124.
51. Takizawa S., Hirabayashi H., Matsushima K., Tokuoka K., Shinohara Y. Induction of heme oxygenase protein protects neurons in cortex and striatum, but not in hippocampus, against transient forebrain ischemia. J Cereb Blood Flow Metab 1998, 18:559-569.
52. Tenhunen R., Marver H., Schmid R. Microsomal heme oxygenase, characterization of the enzyme. J Biol Chem 1969, 244:6388-6394.
53. Terry C.M., Clikeman J.A., Hoidal J.R., Callahan K.S. TNFalpha and IL-1alpha induce heme oxygenase-1 via protein kinase C, Ca2+, and phospholipase A2 in endothelial cells. Am J Physiol Heart Circ Physiol 1999, 276:H1493-H1501.
54. Tushar J.V., Work J., Issekutz A.C., Granger D.N. Heme oxygenase modulates selectin expression in different regional vascular beds. Am J Physiol Heart Circ Physiol 2000, 278:H1613-H1617.
55. Verma A., Hirsch D.J., Glatt C.E., Ronnett G.V., Snyder S.H. Carbon monoxide: a putative neuronal messenger. Science 1993, 259:381-384.
56. Wagener F.A., DaSilva J.L., Farley T., De Witte T., Kappas A., Abraham N.G. Differential effects of heme oxygenase isoforms on heme mediation of endothelial intracellular adhesion molecule 1 expression. J Pharmacol Exp Ther 1999, 291:416-423.
57. Wei C.L., Lee K.H., Khoo H.E., Hon W.M. Expression of haem oxygenase in cirrhotic rat liver. J Pathol 2003, 199:324-334.
58. Yang G., Nguyen X., Ou J., Rekulapelli P., Stevenson D.K., Dennery P.A. Unique effects of zinc protoporphyrin on HO-1 induction and apoptosis. Blood 2001, 97:1306-1313.
59. Yang C., Zhang X., Fan H., Liu Y. Curcumin upregulates transcription factor Nrf2, HO-1 expression and protects rat brains against focal ischemia. Brain Res 2009, 1282:133-141.
60. Zhao Y.J., Yang G.Y., Domino E.F. Zinc protoporphyrin, zinc ion, and protoporphyrin reduce focal cerebral ischemia. Stroke 1996, 27:2299-2303.
61. Zhao J., Kobori N., Aronowski J., Dash P.K. Sulforaphane reduces infarct volume following focal cerebral ischemia in rodents. Neurosci Lett 2006, 393:108-112.
62. Zhou C., Zhou J., Sheng F., Zhu H., Deng X., Xia B., Lin J. The heme oxygenase-1 inhibitor ZnPPIX induces non-canonical, Beclin 1-independent, autophagy through p38 MAPK pathway. Acta Biochim Biophys Sin (Shanghai) 2012, 40:815-822.