Unregulated brain iron deposition in transgenic mice over-expressing HMOX1 in the astrocytic compartment

Journal of Neurochemistry

Volumn 123, Issue 2, 2012, Pages 325-336

  Song, Wei ^a   Zukor, Hillel ^a   Lin, Shih Hsiung ^a   Liberman, Adrienne ^a   Tavitian, Ayda ^a   Mui, Jeannie ^b,c   Vali, Hojatollah ^b   Fillebeen, Carine ^a   Pantopoulos, Kostas ^a   Wu, Ting Di ^d,e   Guerquin Kern, Jean Luc ^d   Schipper, Hyman M ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d Centre Universitaire   (France)

^e INSTITUT CURIE   (France)

Author keywords

aging; astrocyte; heme oxygenase 1; iron; macroautophagy; transgenic mice

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; HEME OXYGENASE 1; IRON BINDING PROTEIN; IRON OXIDE; IRON REGULATORY FACTOR; MANGANESE SUPEROXIDE DISMUTASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN MITOCHONDRION; CELL COMPARTMENTALIZATION; CELL DAMAGE; CELL INCLUSION; CONTROLLED STUDY; EMBRYO; FEMALE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE OVEREXPRESSION; HMOX1 GENE; IN VIVO STUDY; INTRACELLULAR SIGNALING; IRON BALANCE; IRON STORAGE; MACROAUTOPHAGY; MALE; MASS SPECTROMETRY; MOLECULAR PROBE; MOUSE; NEURODEGENERATION WITH BRAIN IRON ACCUMULATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; TRANSGENIC MOUSE; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; ASTROCYTES; BRAIN; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEME OXYGENASE-1; HUMANS; IRON; IRON OVERLOAD; MICE; MICE, TRANSGENIC; UP-REGULATION;

ANIMALIA; MAMMALIA; MUS; MUS MUSCULUS;

EID: 84867070957     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07914.x     Document Type: Article

References (74)

1. Ahmad A. S., Zhuang H., and, Dore S., (2006) Heme oxygenase-1 protects brain from acute excitotoxicity. Neuroscience 141, 1703-1708.
2. Alaoui-Jamali M. A., Bismar T. A., Gupta A., et al,. (2009) A novel experimental heme oxygenase-1-targeted therapy for hormone-refractory prostate cancer. Cancer Res. 69, 8017-8080.
3. Baranano D. E., and, Snyder S. H., (2001) Neural roles for heme oxygenase: contrasts to nitric oxide synthase. Proc. Natl Acad. Sci. USA 98, 10996-11002.
4. Beschorner R., Adjodah D., Schwab J. M., Mittelbronn M., Pedal I., Mattern R., Schluesener H. J., and, Meyermann R., (2000) Long-term expression of heme oxygenase-1 (HO-1, HSP-32) following focal cerebral infarctions and traumatic brain injury in humans. Acta Neuropathol. 100, 377-384.
5. Bonda D. J., Wang X. L., Perry G., Nunomura A., Tabaton M., Zhu X. W., and, Smith M. A., (2010) Oxidative stress in Alzheimer disease: A possibility for prevention. Neuropharmacology 59, 290-294.
6. Brusilow S. W., Koehler R. C., Traystman R. J., and, Cooper A. J., (2010) Astrocyte glutamine synthetase: importance in hyperammonemic syndromes and potential target for therapy. Neurotherapeutics 7, 452-470.
7. Bubber P., Haroutunian V., Fisch G., Blass J. P., and, Gibson G. E., (2005) Mitochondrial abnormalities in Alzheimer brain: mechanistic implications. Ann. Neurol. 57, 695-703.
8. Butterfield D. A., Poon H. F., St Clair D., Keller J. N., Pierce W. M., Klein J. B., and, Markesbery W. R., (2006a) Redox proteomics identification of oxidatively modified hippocampal proteins in mild cognitive impairment: insights into the development of Alzheimer's disease. Neurobiol. Dis. 22, 223-232.
9. Butterfield D. A., Reed T., Perluigi M., De Marco C., Coccia R., Cini C., and, Sultana R., (2006b) Elevated protein-bound levels of the lipid peroxidation product, 4-hydroxy-2-nonenal, in brain from persons with mild cognitive impairment. Neurosci. Lett. 397, 170-173.
10. Dennery P. A., (2000) Regulation and role of heme oxygenase in oxidative injury. Curr. Top. Cell. Regul. 36, 181-199.
11. Dore S., Takahashi M., Ferris C. D., Zakhary R., Hester L. D., Guastella D., and, Snyder S. H., (1999) Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc Natl Acad Sci U S A 96, 2445-2450.
12. Drummond G. S., and, Kappas A., (2004) Chemoprevention of severe neonatal hyperbilirubinemia. Semin. Perinatol. 28, 365-368.
13. Dumont M., Lin M. T., and, Beal M. F., (2010) Mitochondria and antioxidant targeted therapeutic strategies for Alzheimer's disease. J. Alzheimers Dis. 20, S633-S643.
14. Ewing J. F., and, Maines M. D., (1995) Immunohistochemical localization of biliverdin reductase in rat brain: age related expression of protein and transcript. Brain Res. 672, 29-41.
15. Fernandez-Gonzalez A., Perez-Otano I., and, Morgan J. I., (2000) MPTP selectively induces haem oxygenase-1 expression in striatal astrocytes. Eur. J. Neurosci. 12, 1573-1583.
16. Frankel D., and, Schipper H. M., (1999) Cysteamine pretreatment of the astroglial substratum (mitochondrial iron sequestration) enhances PC12 cell vulnerability to oxidative injury. Exp. Neurol. 160, 376-385.
17. Frankel D., Mehindate K., and, Schipper H. M., (2000) Role of heme oxygenase-1 in the regulation of manganese superoxide dismutase gene expression in oxidatively-challenged astroglia. J. Cell. Physiol. 185, 80-86.
18. Gains M. J., Roth K. A., and, LeBlanc A. C., (2006) Prion protein protects against ethanol-induced Bax-mediated cell death in vivo. NeuroReport 17, 903-906.
19. Guerquin-Kern J. L., Wu T. D., Quintana C., and, Croisy A., (2005) Progress in analytical imaging of the cell by dynamic secondary ion mass spectrometry (SIMS microscopy). Biochim. Biophys. Acta 1724, 228-238.
20. Ham D., and, Schipper H. M., (2000) Heme oxygenase-1 induction and mitochondrial iron sequestration in astroglia exposed to amyloid peptides. Cell. Mol. Biol. (Noisy-le-grand), 46, 587-596.
21. Hirai K., Aliev G., Nunomura A., et al,. (2001) Mitochondrial abnormalities in Alzheimer's disease. J. Neurosci. 21, 3017-3023.
22. Hulsebosch C. E., (2008) Gliopathy ensures persistent inflammation and chronic pain after spinal cord injury. Exp. Neurol. 214, 6-9.
23. Jefferies W. A., Food M. R., Gabathuler R., Rothenberger S., Yamada T., Yasuhara O., and, McGeer P. L., (1996) Reactive microglia specifically associated with amyloid plaques in Alzheimer's disease brain tissue express melanotransferrin. Brain Res. 712, 122-126.
24. Kappas A., Drummond G. S., and, Galbraith R. A., (1993) Prolonged clinical use of a heme oxygenase inhibitor: hematological evidence for an inducible but reversible iron-deficiency state. Pediatrics 91, 537-539.
25. Krum J. M., (1994) Experimental gliopathy in the adult rat CNS: effect on the blood-spinal cord barrier. Glia 11, 354-366.
26. Laplante F., Srivastava L. K., and, Quirion R., (2004) Alterations in dopaminergic modulation of prefrontal cortical acetylcholine release in post-pubertal rats with neonatal ventral hippocampal lesions. J. Neurochem. 89, 314-323.
27. Leveugle B., Spik G., Perl D. P., Bouras C., Fillit H. M., and, Hof P. R., (1994) The iron-binding protein lactotransferrin is present in pathologic lesions in a variety of neurodegenerative disorders: a comparative immunohistochemical analysis. Brain Res. 650, 20-31.
28. Lin Y., Vreman H. J., Wong R. J., Tjoa T., Yamauchi T., and, Noble-Haeusslein L. J., (2007) Heme oxygenase-1 stabilizes the blood-spinal cord barrier and limits oxidative stress and white matter damage in the acutely injured murine spinal cord. J. Cereb. Blood Flow Metab. 27, 1010-1021.
29. Llesuy S. F., and, Tomaro M. L., (1994) Heme oxygenase and oxidative stress. Evidence of involvement of bilirubin as physiological protector against oxidative damage. Biochim. Biophys. Acta 1223, 9-14.
30. Matsuoka Y., Kitamura Y., Okazaki M., Kakimura J., Tooyama I., Kimura H., and, Taniguchi T., (1998) Kainic acid induction of heme oxygenase in vivo and in vitro. Neuroscience 85, 1223-1233.
31. Mattson M. P., (2002) Contributions of mitochondrial alterations, resulting from bad genes and a hostile environment, to the pathogenesis of Alzheimer's disease. Int. Rev. Neurobiol. 53, 387-409.
32. McLaren J., Brawer J. R., and, Schipper H. M., (1992) Iron content correlates with peroxidase activity in cysteamine-induced astroglial organelles. J. Histochem. Cytochem. 40, 1887-1897.
33. Meguro R., Asano Y., Odagiri S., Li C., and, Shoumura K., (2008) Cellular and subcellular localizations of nonheme ferric and ferrous iron in the rat brain: a light and electron microscopic study by the perfusion-Perls and -Turnbull methods. Arch. Histol. Cytol. 71, 205-222.
34. Moreira P. I., Santos M. S., and, Oliveira C. R., (2007a) Alzheimer's disease: a lesson from mitochondrial dysfunction. Antioxid. Redox Signal. 9, 1621-1630.
35. Moreira P. I., Siedlak S. L., Wang X., et al,. (2007b) Autophagocytosis of mitochondria is prominent in Alzheimer disease. J. Neuropathol. Exp. Neurol. 66, 525-532.
36. Moreira P. I., Siedlak S. L., Wang X., et al,. (2007c) Increased autophagic degradation of mitochondria in Alzheimer disease. Autophagy 3, 614-615.
37. Nakagami T., Toyomura K., Kinoshita T., and, Morisawa S., (1993) A beneficial role of bile pigments as an endogenous tissue protector: anti-complement effects of biliverdin and conjugated bilirubin. Biochim. Biophys. Acta 1158, 189-193.
38. Nixon R. A., Wegiel J., Kumar A., Yu W. H., Peterhoff C., Cataldo A., and, Cuervo A. M., (2005) Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J. Neuropathol. Exp. Neurol. 64, 113-122.
39. Nunomura A., Perry G., Pappolla M. A., Friedland R. P., Hirai K., Chiba S., and, Smith M. A., (2000) Neuronal oxidative stress precedes amyloid-beta deposition in Down syndrome. J. Neuropathol. Exp. Neurol. 59, 1011-1017.
40. Nunomura A., Perry G., Aliev G., et al,. (2001) Oxidative damage is the earliest event in Alzheimer disease. J. Neuropathol. Exp. Neurol. 60, 759-767.
41. Osada T., Uehara H., Kim H., and, Ikai A., (2003) mRNA analysis of single living cells. J. Nanobiotechnol. 1, 2.
42. Panahian N., Yoshiura M., and, Maines M. D., (1999) Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J. Neurochem. 72, 1187-1203.
43. Parker Jr W. D., and, Parks J. K., (1995) Cytochrome c oxidase in Alzheimer's disease brain: purification and characterization. Neurology, 45, 482-486.
44. Pratico D., Uryu K., Leight S., Trojanoswki J. Q., and, Lee V. M., (2001) Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis. J. Neurosci., 21, 4183-4187.
45. Preisig-Muller R., Mederos y Schnitzler M., Derst C., and, Daut J., (1999) Separation of cardiomyocytes and coronary endothelial cells for cell-specific RT-PCR. Am. J. Physiol., 277, H413-H416.
46. Premkumar D. R., Smith, M. A, Richey P. L., Petersen R. B., Castellani R., Kutty R. K., Wiggert B., Perry G., and, Kalaria R. N., (1995) Induction of heme oxygenase-1 mRNA and protein in neocortex and cerebral vessels in Alzheimer's disease. J. Neurochem., 65, 1399-1402.
47. Quintana C., Bellefqih S., Laval J. Y., Guerquin-Kern J. L., Wu T. D., Avila J., Ferrer I., Arranz R., and, Patino C., (2006) Study of the localization of iron, ferritin, and hemosiderin in Alzheimer's disease hippocampus by analytical microscopy at the subcellular level. J. Struct. Biol. 153, 42-54.
48. Ryter S. W., and, Tyrrell R. M., (2000) The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties. Free Radic. Biol. Med. 28, 289-309.
49. Sayre L. M., Smith M. A., and, Perry G., (2001) Chemistry and biochemistry of oxidative stress in neurodegenerative disease. Curr. Med. Chem. 8, 721-738.
50. Schipper H. M., (1998) Experimental induction of corpora amylacea in adult rat brain. Microsc. Res. Tech. 43, 43-48.
51. Schipper H. M., (1999) Glial HO-1 expression, iron deposition and oxidative stress in neurodegenerative diseases. Neurotox. Res. 1, 57-70.
52. Schipper H. M., (2000) Heme oxygenase-1: role in brain aging and neurodegeneration. Exp. Gerontol. 35, 821-830.
53. Schipper H. M., (2004a) Brain iron deposition and the free radical-mitochondrial theory of ageing. Ageing Res. Rev. 3, 265-301.
54. Schipper H. M., (2004b) Heme oxygenase-1: transducer of pathological brain iron sequestration under oxidative stress. Ann. N. Y. Acad. Sci. 1012, 84-93.
55. Schipper H. M., (2004c) Heme oxygenase expression in human central nervous system disorders. Free Radic. Biol. Med. 37, 1995-2011.
56. Schipper H. M., and, Ponka P., (2009) Inherited disorders of brain iron homeostasis, in Iron Deficiency and Overload: From Basic Biology to Clinical Medicine, (, Yehudah S., and, Mostofsky D. I., eds), pp. 251-276. Human Press Inc., Totowa, NJ.
57. Schipper H. M., Cisse S., and, Stopa E. G., (1995) Expression of heme oxygenase-1 in the senescent and Alzheimer-diseased brain. Ann. Neurol. 37, 758-768.
58. Schipper H. M., Liberman A., and, Stopa E. G., (1998) Neural heme oxygenase-1 expression in idiopathic Parkinson's disease. Exp. Neurol. 150, 60-68.
59. Schipper H. M., Bernier L., Mehindate K., and, Frankel D., (1999) Mitochondrial iron sequestration in dopamine-challenged astroglia: role of heme oxygenase-1 and the permeability transition pore. J. Neurochem. 72, 1802-1811.
60. Schipper H. M., Bennett D. A., Liberman A., Bienias J. L., Schneider J. A., Kelly J., and, Arvanitakis Z., (2006) Glial heme oxygenase-1 expression in Alzheimer disease and mild cognitive impairment. Neurobiol. Aging 27, 252-261.
61. Schipper H. M., Gupta A., and, Szarek W. A., (2009a) Suppression of glial HO-1 activity as a potential neurotherapeutic intervention in AD. Curr. Alzheimer Res. 6, 424-430.
62. Schipper H. M., Song W., Zukor H., Hascalovici J. R., and, Zeligman D., (2009b) Heme oxygenase-1 and neurodegeneration: expanding frontiers of engagement. J. Neurochem. 110, 469-485.
63. Song W., Su H., Song S., Paudel H. K., and, Schipper H. M., (2006) Over-expression of heme oxygenase-1 promotes oxidative mitochondrial damage in rat astroglia. J. Cell. Physiol. 206, 655-663.
64. Song L., Song W., and, Schipper H. M., (2007) Astroglia overexpressing heme oxygenase-1 predispose co-cultured PC12 cells to oxidative injury. J. Neurosci. Res. 85, 2186-2195.
65. Song W., Patel A., Qureshi H. Y., Han D., Schipper H. M., and, Paudel H. K., (2009) The Parkinson disease-associated A30P mutation stabilizes alpha-synuclein against proteasomal degradation triggered by heme oxygenase-1 over-expression in human neuroblastoma cells. J. Neurochem. 110, 719-733.
66. Song W., Zukor H., Lin S. H,. et al. (2012) Schizophrenia-like features in transgenic mice overexpressing human HO-1 in the astrocytic compartment. J. Neurosci. 32, 10841-10853.
67. Stocker R., Yamamoto Y., McDonagh A. F., Glazer A. N., and, Ames B. N., (1987) Bilirubin is an antioxidant of possible physiological importance. Science 235, 1043-1046.
68. Terman A., Gustafsson B., and, Brunk U. T., (2006) The lysosomal-mitochondrial axis theory of postmitotic aging and cell death. Chem. Biol. Interact. 163, 29-37.
69. Vaya J., Song W., Khatib S., Geng G., and, Schipper H. M., (2007) Effects of heme oxygenase-1 expression on sterol homeostasis in rat astroglia. Free Radic. Biol. Med. 42, 864-871.
70. Wang J., and, Dore S., (2007) Heme oxygenase-1 exacerbates early brain injury after intracerebral haemorrhage. Brain 130, 1643-1652.
71. Wang X., Su B., Lee H. G., Li X., Perry G., Smith M. A., and, Zhu X., (2009) Impaired balance of mitochondrial fission and fusion in Alzheimer's disease. J. Neurosci. 29, 9090-9103.
72. Yuan Y., Guo J. Z., and, Zhou Q. X., (2008) The homeostasis of iron and suppression of HO-1 involved in the protective effects of nimodipine on neurodegeneration induced by aluminum overloading in mice. Eur. J. Pharmacol. 586, 100-105.
73. Zhang J., and, Piantadosi C. A., (1992) Mitochondrial oxidative stress after carbon monoxide hypoxia in the rat brain. J. Clin. Invest. 90, 1193-1199.
74. Zukor H., Song W., Liberman A., Mui J., Vali H., Fillebeen C., Pantopoulos K., Wu T. D., Guerquin-Kern J. L., and, Schipper H. M., (2009) HO-1-mediated macroautophagy: a mechanism for unregulated iron deposition in aging and degenerating neural tissues. J. Neurochem. 109, 776-791.