Role of hemeoxygenase-1 in the neurodegenerative disorders;Papel de la hemooxigenasa-1 en las enfermedades neurodegenerativas

Revista de Neurologia

Volumn 43, Issue 9, 2006, Pages 556-562

  Orozco Ibarra, M ^a   Chirino, Y I ^a   Pedraza Chaverrí, José ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Alzheimer disease; Hemeoxygenase 1; Huntington disease; Iron deposition; Neurodegeneration; Parkinson disease

Indexed keywords

BILIVERDIN; CARBON MONOXIDE; HEME OXYGENASE 1; HEME OXYGENASE 2; IRON;

ALZHEIMER DISEASE; AUTOPSY; CELL CULTURE; CELL DEATH; CELL PROTECTION; DEGENERATIVE DISEASE; HUMAN; HUNTINGTON CHOREA; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; REVIEW; BIOSYNTHESIS; ENZYMOLOGY; PHYSIOLOGY;

HEME OXYGENASE-1; HUMANS; NEURODEGENERATIVE DISEASES;

EID: 34250841425     PISSN: 02100010     EISSN: None     Source Type: Journal    
DOI: 10.33588/rn.4309.2005487     Document Type: Review

References (79)

1. Zarkovic K. 4-hydroxynonenal and neurodegenerative diseases. Mol Aspects Med 2003; 24: 293-303.
2. Calabrese V, Lodi R, Tonon C, D'Agata V, Sapienza M, Scapagnini G, et al. Oxidative stress, mitochondrial dysfunction and cellular stress response in Friedrich's ataxia. J Neurol Sci 2005; 233: 145-62.
3. Miwa H, Kubo T, Morita S, Nakanishi I, Kondo T. Oxidative stress and microglial activation in substantia nigra following striatal MPP+. Neuroreport 2004; 15: 1039-44.
4. Schipper HM, Liberman A, Stopa EG. Neural heme oxygenase-1 expression in idiopathic Parkinson's disease. Exp Neurol 1998; 150: 60-8.
5. Browne S, Ferrante R, Beal M. Oxidative stress in Huntington's disease. Brain Pathol 1999; 9: 147-63.
6. Ryter SW, Tyrrell RM. The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties. Free Radic Biol Med 2000; 28: 289-309.
7. Schipper HM. Heme oxygenase-1: transducer of pathological brain iron sequestration under oxidative stress. Ann N Y Acad Sci 2004; 1012: 84-93.
8. Wagener FA, Volk HD, Willis D, Abraham NG, Soares MP, Adema GJ, et al. Different faces of the heme-heme oxygenase system in inflammation. Pharmacol Rev 2003; 55: 551-71.
9. Dennery PA. Regulation and role of heme oxygenase in oxidative injury. Curr Top Cell Regul 2000; 36: 181-99.
10. Scapagnini G, D'Agata V, Calabrese V, Pascale A, Colombrita C, Alkon D, et al. Gene expression profiles of heme oxygenase isoforms in the rat brain. Brain Res 2002; 954: 51-9.
11. Ryter SW, Otterbein LE. Carbon monoxide in biology and medicine. Bioessays 2004; 26: 270-80.
12. Halliwell B, Gutteridge JM. Free radicals in biology and medicine. Oxford: Oxford University Press; 1999.
13. Grosser N, Oberle S, Berndt G, Erdmann K, Hemmerle A, Schroder H. Antioxidant action of L-alanine: heme oxygenase-1 and ferritin as possible mediators. Biochem Biophys Res Commun 2004; 314: 351-5.
14. Shibahara S, Muller R, Taguchi H, Yoshida T. Cloning and expression of cDNA for rat heme oxygenase. Proc Natl Acad Sci U S A 1985; 82: 7865-9.
15. Maines MD, Trakshel GM, Kutty RK. Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible. J Biol Chem 1986; 261: 411-9.
16. Bergeron M, Ferriero DM, Sharp FR. Developmental expression of heme oxygenase-1 (HSP32) in rat brain: an immunocytochemical study. Brain Res Dev Brain Res 1998; 105: 181-94.
17. Colombrita C, Calabrese V, Stella AM, Mattei F, Alkon DL, Scapagnini G. Regional rat brain distribution of heme oxygenase-1 and manganese superoxide dismutase mRNA: relevance of redox homeostasis in the aging processes. Exp Biol Med 2003; 228: 517-24.
18. Morse D, Choi AM. Heme oxygenase-1. The 'emerging molecule' has arrived. Am J Respir Cell Mol Biol 2002; 27: 8-16.
19. Applegate LA, Luscher P, Tyrrell RM. Induction of heme oxygenase: a general response to oxidant stress in cultured mammalian cells. Cancer Res 1991; 51: 974-8.
20. Immenschuh S, Ramadori G. Gene regulation of heme oxygenase-1 as a therapeutic target. Biochem Pharmacol 2000; 60: 1121-8.
21. Lavrovsky Y, Schwartzman ML, Levere RD, Kappas A, Abraham NG. 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 1994; 91: 5987-91.
22. Calabrese V, Ravagna A, Colombrita C, Scapagnini G, Guagliano E, Calvani M, et al. Acetylcarnitine induces heme oxygenase in rat astrocytes and protects against oxidative stress: involvement of the transcription factor Nrf2. J Neurosci Res 2005; 79: 509-21.
23. 7. Free Radic Biol Med 2003; 34: 1390-8.
24. Rezzani R, Rodella L, Buffoli B, Goodman AA, Abraham NG, Lianos EA, et al. Change in renal heme oxygenase expression in cyclosporine A-induced injury. J Histochem Cytochem 2005; 53: 105-12.
25. Wang XH, Wang K, Zhang F, Li XC, Li J, De W, et al. Heme oxygenase-1 alleviates ischemia/reperfusion injury in aged liver. World J Gastroenterol 2005; 11: 690-4.
26. Liu LG, Yan H, Zhang W, Yao P, Zhang XP, Sun XF, et al. Induction of heme oxygenase-1 in human hepatocytes to protect them from ethanol-induced cytotoxicity. Biomed Environ Sci 2004; 17: 315-26.
27. Le WD, Xie WJ, Appel SH. Protective role of heme oxygenase-1 in oxidative stress-induced neuronal injury. J Neurosci Res 1999; 56: 652-8.
28. Chen K, Gunter K, Maines MD. Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death. J Neurochem 2000; 75: 304-13.
29. Dwyer BE, Nishimura RN, Lu SY, Alcaraz A. Transient induction of heme oxygenase after cortical stab wound injury. Brain Res Mol Brain Res 1996; 38: 251-9.
30. Matsuoka Y, Okazaki M, Kitamura Y. Induction of inducible heme oxygenase (HO-1) in the central nervous system: is HO-1 helpful or harmful? Neurotox Res 1999; 1: 113-7.
31. Fukuda K, Richmon JD, Sato M, Sharp FR, Panter SS, Noble LJ. Induction of heme oxygenase-1 (HO-1) in glia after traumatic brain injury. Brain Res 1996; 736: 68-75.
32. Kitamura Y, Matsuoka Y, Nomura Y, Taniguchi T. Induction of inducible nitric oxide synthase and heme oxygenase-1 in rat glial cells. Life Sci 1998; 62: 1717-21.
33. Smith MA, Kutty RK, Richey PL, Yan SD, Stern D, Chader GJ, et al. Heme oxygenase-1 is associated with the neurofibrillary pathology of Alzheimer's disease. Am J Pathol 1994; 145: 42-7.
34. Castellani R, Smith MA, Richey PL, Kalaria R, Gambetti P, Perry G. Evidence for oxidative stress in Pick disease and corticobasal degeneration. Brain Res 1995; 696: 268-71.
35. Premkumar DR, Smith MA, Richey PL, Petersen RB, Castellani R, Kutty RK, et al. Induction of heme oxygenase-1 mRNA and protein in neocortex and cerebral vessels in Alzheimer's disease. J Neurochem 1995; 65: 1399-402.
36. Ávila de Grado J. Las proteínas implicadas en la enfermedad de Alzheimer. In García AG, Gandía L, eds. Fronteras en la enfermedad de Alzheimer. Madrid: Farmaindustria; 2002. p. 69-70.
37. Selkoe DJ. The molecular pathology of Alzheimer's disease. Neuron 1991; 6: 487-98.
38. Honda K, Casadesus G, Petersen RB, Perry G, Smith MA. Oxidative stress and redox-active iron in Alzheimer's disease. Ann N Y Acad Sci 2004; 1012: 179-82.
39. LeVine SM. Iron deposits in multiple sclerosis and Alzheimer's disease brains. Brain Res 1997; 760: 298-303.
40. Wang J, Xiong S, Xie C, Markesbery WR, Lovell MA. Increased oxidative damage in nuclear and mitochondrial DNA in Alzheimer's disease. J Neurochem 2005; 93: 953-62.
41. Takata K, Kitamura Y, Kakimura J, Shibagaki K, Taniguchi T, Gebicke-Haerter PJ, et al. Possible protective mechanisms of heme oxygenase-1 in the brain. Ann N Y Acad Sci 2002; 977: 501-6.
42. Yan SD, Chen X, Schmidt AM, Brett J, Godman G, Zou YS, et al. Glycated tau protein in Alzheimer disease: a mechanism for induction of oxidant stress. Proc Natl Acad Sci U S A 1994; 91: 7787-91.
43. Schipper HM, Cisse S, Stopa EG. Expression of heme oxygenase-1 in the senescent and Alzheimer-diseased brain. Ann Neurol 1995; 37: 758-68.
44. Pappolla MA, Chyan YJ, Omar RA, Hsiao K, Perry G, Smith MA, et al. Evidence of oxidative stress and in vivo neurotoxicity of beta-amyloid in a transgenic mouse model of Alzheimer's disease: a chronic oxidative paradigm for testing antioxidant therapies in vivo. Am J Pathol 1998; 152: 871-7.
45. Smith MA, Hirai K, Hsiao K, Pappolla MA, Harris PL, Siedlak SL, et al. Amyloid-beta deposition in Alzheimer transgenic mice is associated with oxidative stress. J Neurochem 1998; 70: 2212-5.
46. Ham D, Schipper HM. Heme oxygenase-1 induction and mitochondrial iron sequestration in astroglia exposed to amyloid peptides. Cell Mol Biol 2000; 46: 587-96.
47. Song W, Su H, Song S, Paudel HK, Schipper HM. Over-expression of heme oxygenase-1 promotes oxidative mitochondrial damage in rat astroglia. J Cell Physiol 2006; 206: 655-63.
48. Takahashi M, Dore S, Ferris CD, Tomita T, Sawa A, Wolosker H, et al. Amyloid precursor proteins inhibit heme oxygenase activity and augment neurotoxicity in Alzheimer's disease. Neuron 2000; 28: 461-73.
49. Schipper HM, Chertkow H, Mehindate K, Frankel D, Melmed C, Bergman H. Evaluation of heme oxygenase-1 as a systemic biological marker of sporadic AD. Neurology 2000; 54: 1297-304.
50. Ishizuka K, Kimura T, Yoshitake J, Akaike T, Shono M, Takamatsu J, et al. Possible assessment for antioxidant capacity in Alzheimer's disease by measuring lymphocyte heme oxygenase-1 expression with realtime RT-PCR. Ann N Y Acad Sci 2002; 977: 173-8.
51. Klockgether T. Parkinson's disease: clinical aspects. Cell Tissue Res 2004; 318: 115-20.
52. Graham JM, Paley MN, Grunewald RA, Hoggard N, Griffiths PD. Brain iron deposition in Parkinson's disease imaged using the PRIME magnetic resonance sequence. Brain 2000; 123: 2423-31.
53. Shimura-Miura H, Hattori N, Kang D, Miyako K, Nakabeppu Y, Mizuno Y. Increased 8-oxo-dGTPase in the mitochondria of substantia nigral neurons in Parkinson's disease. Ann Neurol 1999; 46: 920-4.
54. Koutsilieri E, Scheller C, Grunblatt E, Nara K, Li J, Riederer P. Free radicals in Parkinson's disease. J Neurol 2002; 249 (Suppl 2): S1-5.
55. Castellani R, Smith MA, Richey PL, Perry G. Glycoxidation and oxidative stress in Parkinson disease and diffuse Lewy body disease. Brain Res 1996; 737: 195-200.
56. Yoo MS, Chun HS, Son JJ, DeGiorgio LA, Kim DJ, Peng C, et al. Oxidative stress regulated genes in nigral dopaminergic neuronal cells: correlation with the known pathology in Parkinson's disease. Brain Res Mol Brain Res 2003; 110: 76-84.
57. Chun HS, Gibson GE, DeGiorgio LA, Zhang H, Kidd VJ, Son JH. Dopaminergic cell death induced by MPP(+), oxidant and specific neurotoxicants shares the common molecular mechanism. J Neurochem 2001; 76: 1010-21.
58. Schipper HM. Glial HO-1 expression, iron deposition and oxidative stress in neurodegenerative diseases. Neurotox Res 1999; 1: 57-70.
59. Butterworth NJ, Williams L, Bullock JY, Love DR, Faull RL, Dragunow M. Trinucleotide (CAG) repeat length is positively correlated with the degree of DNA fragmentation in Huntington's disease striatum. Neuroscience 1998; 87: 49-53.
60. Téllez-Nagel I, Johnson AB, Terry RD. Studies on brain biopsies of patients with Huntington's chorea. J Neuropathol Exp Neurol 1974; 33: 308-32.
61. Gros-Louis F, Gaspar C, Rouleau GA. Genetics of familial and sporadic amyotrophic lateral sclerosis. Biochim Biophys Acta 2006 [E-pub ahead of print].
62. Rosen DR. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993; 364: 362.
63. Ihara Y, Nobukuni K, Takata H, Hayabara T. Oxidative stress and metal content in blood and cerebrospinal fluid of amyotrophic lateral sclerosis patients with and without a Cu, Zn-superoxide dismutase mutation. Neurol Res 2005; 27: 105-8.
64. Aguirre N, Beal MF, Matson WR, Bogdanov MB. Increased oxidative damage to DNA in an animal model of amyotrophic lateral sclerosis. Free Radic Res 2005; 39: 383-8.
65. Ferrante RJ, Shinobu LA, Schulz JB, Matthews RT, Thomas CE, Kowall NW, et al. Increased 3-nitrotyrosine and oxidative damage in mice with a human copper/zinc superoxide dismutase mutation. Ann Neurol 1997; 42: 326-34.
66. Dwyer BE, Lu SY, Nishimura RN. Heme oxygenase in the experimental ALS mouse. Exp Neurol 1998; 150: 206-12.
67. Bishop A, Yet SF, Lee ME, Perrella MA, Demple B. A key role for heme oxygenase-1 in nitric oxide resistance in murine motor neurons and glia. Biochem Biophys Res Commun 2004; 325: 3-9.
68. Adamec J, Rusnak F, Owen WG, Naylor S, Benson LM, Gacy AM, et al. Iron-dependent self-assembly of recombinant yeast frataxin: implications for Friedreich ataxia. Am J Hum Genet 2000; 67: 549-62.
69. Schoenfeld RA, Napoli E, Wong A, Zhan S, Reutenauer L, Morin D, et al. Frataxin deficiency alters heme pathway transcripts and decreases mitochondrial heme metabolites in mammalian cells. Hum Mol Genet 2005; 14: 3787-99.
70. O'Neill HA, Gakh O, Park S, Cui J, Mooney SM, Sampson M, et al. Assembly of human frataxin is a mechanism for detoxifying redoxactive iron. Biochemistry 2005; 44: 537-45.
71. Bulteau AL, O'Neill HA, Kennedy MC, Ikeda-Saito M, Isaya G, Szweda LI. Frataxin acts as an iron chaperone protein to modulate mitochondrial aconitase activity. Science 2004; 305: 242-5.
72. Edmond M, Lepage G, Vanasse M, Pandolfo M. Increased levels of plasma malondialdehyde in Friedreich ataxia. Neurology 2000; 55: 1752-3.
73. Thierbach R, Schulz TJ, Isken F, Voigt A, Mietzner B, Drewes G, et al. Targeted disruption of hepatic frataxin expression causes impaired mitochondrial function, decreased life span and tumor growth in mice. Hum Mol Genet 2005; 14: 3857-64.
74. Schultz JB, Dehmer T, Schols L, Mende H, Hardt C, Vorgerd M, et al. Oxidative stress in patients with Friedreich's ataxia. Neurology 2000; 55: 1719-21.
75. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science 1987; 235: 1043-6.
76. Kimpara T, Takeda A, Yamaguchi T, Arai H, Okita N, Takase S, et al. Increased bilirubins and their derivatives in cerebrospinal fluid in Alzheimer's disease. Neurobiol Aging 2000; 21: 551-4.
77. Takeda A, Perry G, Abraham NG, Dwyer BE, Kutty RK, Laitinen JT, et al. Overexpression of heme oxygenase in neuronal cells, the possible interaction with tau. J Biol Chem 2000; 275: 5395-9.
78. 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: 559-69.
79. Panahian N, Yoshiura M, Maines MD. Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J Neurochem 1999; 72: 1187-203.