Deletion of the hemopexin or heme oxygenase-2 gene aggravates brain injury following stroma-free hemoglobin-induced intracerebral hemorrhage

Journal of Neuroinflammation

Volumn 13, Issue 1, 2016, Pages

  Ma, Bo ^a   Day, Jason Patrick ^a   Phillips, Harrison ^a   Slootsky, Bryan ^a   Tolosano, Emanuela ^b   Doré, Sylvain ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Fluoro Jade; Hemorrhagic stroke; Iron; Microglia; Perls; Phagocytosis

Indexed keywords

BINDING PROTEIN; HEME OXYGENASE 2; HEMOGLOBIN; HEMOPEXIN; IONIZED CALCIUM BINDING ADAPTER PROTEIN 1; UNCLASSIFIED DRUG; ACYL COENZYME A DEHYDROGENASE; ARABIDOPSIS PROTEIN; FLUORESCEIN DERIVATIVE; FLUORO JADE; HEME OXYGENASE; HEME OXYGENASE-2; HEMOGLOBIN, STROMA FREE; IBR3 PROTEIN, ARABIDOPSIS; NERVE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR ASSESSMENT; BRAIN HEMORRHAGE; BRAIN INJURY; CELL ACTIVATION; CELL CULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORPUS STRIATUM; FLUORO JADE B STAINING; FUNCTIONAL ASSESSMENT; GENE DELETION; HO2 GENE; HPX GENE; IMMUNOHISTOCHEMISTRY; IRON OVERLOAD; KNOCKOUT MOUSE; MALE; MICROGLIA; MOUSE; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PATHOGENESIS; PATHOLOGICAL ANATOMY; PERL STAINING; PHAGOCYTOSIS; STAINING; ANIMAL; BRAIN INJURIES; C57BL MOUSE; CHEMICALLY INDUCED; COMPLICATION; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; GENETICS; METABOLISM; MORTALITY; MOTOR ACTIVITY; NEUROLOGIC EXAMINATION; TIME FACTOR; TRANSGENIC MOUSE;

ACYL-COA DEHYDROGENASE; ANIMALS; ARABIDOPSIS PROTEINS; BRAIN INJURIES; CELLS, CULTURED; CEREBRAL HEMORRHAGE; DISEASE MODELS, ANIMAL; FLUORESCEINS; HEME OXYGENASE (DECYCLIZING); HEMOGLOBINS; HEMOPEXIN; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; MOTOR ACTIVITY; NERVE TISSUE PROTEINS; NEUROLOGIC EXAMINATION; PHAGOCYTOSIS; TIME FACTORS;

EID: 84957960233     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-016-0490-1     Document Type: Article

References (71)

1. Donnan GA, Hankey GJ, Davis SM. Intracerebral haemorrhage: a need for more data and new research directions. Lancet Neurol. 2010;9:133-4.
2. Umbreit J. Methemoglobin--it's not just blue: a concise review. Am J Hematol. 2007;82:134-44.
3. Jeney V, Balla J, Yachie A, Varga Z, Vercellotti GM, Eaton JW, et al. Pro-oxidant and cytotoxic effects of circulating heme. Blood. 2002;100:879-87.
4. Bunn HF, Jandl JH. Exchange of heme among hemoglobins and between hemoglobin and albumin. J Biol Chem. 1968;243:465-75.
5. Pohlman TH, Harlan JM. Adaptive responses of the endothelium to stress. J Surg Res. 2000;89:85-119.
6. Balla J, Jacob HS, Balla G, Nath K, Eaton JW, Vercellotti GM. Endothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage. Proc Natl Acad Sci U S A. 1993;90:9285-9.
7. Wagener FA, Eggert A, Boerman OC, Oyen WJ, Verhofstad A, Abraham NG, et al. Heme is a potent inducer of inflammation in mice and is counteracted by heme oxygenase. Blood. 2001;98:1802-11.
8. Paoli M, Marles-Wright J, Smith A. Structure-function relationships in heme-proteins. DNA Cell Biol. 2002;21:271-80.
9. Wagner KR, Sharp FR, Ardizzone TD, Lu A, Clark JF. Heme and iron metabolism: role in cerebral hemorrhage. J Cereb Blood Flow Metab. 2003;23:629-52.
10. Grinshtein N, Bamm VV, Tsemakhovich VA, Shaklai N. Mechanism of low-density lipoprotein oxidation by hemoglobin-derived iron. Biochemistry. 2003;42:6977-85.
11. Belcher JD, Beckman JD, Balla G, Balla J, Vercellotti G. Heme degradation and vascular injury. Antioxid Redox Signal. 2010;12:233-48.
12. Aronowski J, Zhao X. Molecular pathophysiology of cerebral hemorrhage: secondary brain injury. Stroke. 2011;42:1781-6.
13. Tolosano E, Altruda F. Hemopexin: structure, function, and regulation. DNA Cell Biol. 2002;21:297-306.
14. Deuel JW, Vallelian F, Schaer CA, Puglia M, Buehler PW, Schaer DJ. Different target specificities of haptoglobin and hemopexin define a sequential protection system against vascular hemoglobin toxicity. Free Radic Biol Med. 2015;89:931.
15. Buehler PW, Abraham B, Vallelian F, Linnemayr C, Pereira CP, Cipollo JF, et al. Haptoglobin preserves the CD163 hemoglobin scavenger pathway by shielding hemoglobin from peroxidative modification. Blood. 2009;113:2578-86.
16. Gutteridge JM, Smith A. Antioxidant protection by haemopexin of haem-stimulated lipid peroxidation. Biochem J. 1988;256:861-5.
17. Hvidberg V, Maniecki MB, Jacobsen C, Hojrup P, Moller HJ, Moestrup SK. Identification of the receptor scavenging hemopexin-heme complexes. Blood. 2005;106:2572-9.
18. Williams KR, Saunders AM, Roses AD, Armati PJ. Uptake and internalization of exogenous apolipoprotein E3 by cultured human central nervous system neurons. Neurobiol Dis. 1998;5:271-9.
19. Borda JT, Alvarez X, Mohan M, Hasegawa A, Bernardino A, Jean S, et al. CD163, a marker of perivascular macrophages, is up-regulated by microglia in simian immunodeficiency virus encephalitis after haptoglobin-hemoglobin complex stimulation and is suggestive of breakdown of the blood-brain barrier. Am J Pathol. 2008;172:725-37.
20. Zhao X, Song S, Sun G, Strong R, Zhang J, Grotta JC, et al. Neuroprotective role of haptoglobin after intracerebral hemorrhage. J Neurosci. 2009;29:15819-27.
21. Li RC, Saleem S, Zhen G, Cao W, Zhuang H, Lee J, et al. Heme-hemopexin complex attenuates neuronal cell death and stroke damage. J Cereb Blood Flow Metab. 2009;29:953-64.
22. Sutherland BA, Rahman RM, Clarkson AN, Shaw OM, Nair SM, Appleton I. Cerebral heme oxygenase 1 and 2 spatial distribution is modulated following injury from hypoxia-ischemia and middle cerebral artery occlusion in rats. Neurosci Res. 2009;65:326-34.
23. Morris CM, Candy JM, Edwardson JA, Bloxham CA, Smith A. Evidence for the localization of haemopexin immunoreactivity in neurones in the human brain. Neurosci Lett. 1993;149:141-4.
24. Dwyer BE, Nishimura RN, Lu SY. Differential expression of heme oxygenase-1 in cultured cortical neurons and astrocytes determined by the aid of a new heme oxygenase antibody. Response to oxidative stress. Brain Res Mol Brain Res. 1995;30:37-47.
25. Fukuda K, Panter SS, Sharp FR, Noble LJ. Induction of heme oxygenase-1 (HO-1) after traumatic brain injury in the rat. Neurosci Lett. 1995;199:127-30.
26. Matz PG, Weinstein PR, Sharp FR. Heme oxygenase-1 and heat shock protein 70 induction in glia and neurons throughout rat brain after experimental intracerebral hemorrhage. Neurosurgery. 1997;40:152-60.
27. Zakhary R, Gaine SP, Dinerman JL, Ruat M, Flavahan NA, Snyder SH. Heme oxygenase 2: endothelial and neuronal localization and role in endothelium-dependent relaxation. Proc Natl Acad Sci U S A. 1996;93:795-8.
28. Zhao H, Wong RJ, Nguyen X, Kalish F, Mizobuchi M, Vreman HJ, et al. Expression and regulation of heme oxygenase isozymes in the developing mouse cortex. Pediatr Res. 2006;60:518-23.
29. Doré S. Decreased activity of the antioxidant heme oxygenase enzyme: implications in ischemia and in Alzheimer's disease. Free Radic Biol Med. 2002;32:1276-82.
30. Kim YS, Doré S. Catalytically inactive heme oxygenase-2 mutant is cytoprotective. Free Radic Biol Med. 2005;39:558-64.
31. Scapagnini G, D'Agata V, Calabrese V, Pascale A, Colombrita C, Alkon D, Cavallaro S: Gene expression profiles of heme oxygenase isoforms in the rat brain. Brain research. 2002;954:51-59.
32. Chang EF, Wong RJ, Vreman HJ, Igarashi T, Galo E, Sharp FR, et al. Heme oxygenase-2 protects against lipid peroxidation-mediated cell loss and impaired motor recovery after traumatic brain injury. J Neurosci. 2003;23:3689-96.
33. McCoubrey Jr WK, Huang TJ, Maines MD. Heme oxygenase-2 is a hemoprotein and binds heme through heme regulatory motifs that are not involved in heme catalysis. J Biol Chem. 1997;272:12568-74.
34. Yi L, Jenkins PM, Leichert LI, Jakob U, Martens JR, Ragsdale SW. Heme regulatory motifs in heme oxygenase-2 form a thiol/disulfide redox switch that responds to the cellular redox state. J Biol Chem. 2009;284:20556-61.
35. Dore S, Takahashi M, Ferris CD, Zakhary R, Hester LD, Guastella D, et al. Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc Natl Acad Sci U S A. 1999;96:2445-50.
36. Dore S, Sampei K, Goto S, Alkayed NJ, Guastella D, Blackshaw S, et al. Heme oxygenase-2 is neuroprotective in cerebral ischemia. Mol Med. 1999;5:656-63.
37. Maines MD. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol. 1997;37:517-54.
38. Zhao X, Sun G, Zhang J, Strong R, Song W, Gonzales N, et al. Hematoma resolution as a target for intracerebral hemorrhage treatment: role for peroxisome proliferator-activated receptor gamma in microglia/macrophages. Ann Neurol. 2007;61:352-62.
39. Streit WJ. Microglia as neuroprotective, immunocompetent cells of the CNS. Glia. 2002;40:133-9.
40. Neumann J, Gunzer M, Gutzeit HO, Ullrich O, Reymann KG, Dinkel K. Microglia provide neuroprotection after ischemia. FASEB J. 2006;20:714-6.
41. Lalancette-Hebert M, Gowing G, Simard A, Weng YC, Kriz J. Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci. 2007;27:2596-605.
42. Meyer-Luehmann M, Spires-Jones TL, Prada C, Garcia-Alloza M, de Calignon A, Rozkalne A, et al. Rapid appearance and local toxicity of amyloid-beta plaques in a mouse model of Alzheimer's disease. Nature. 2008;451:720-4.
43. Nimmerjahn A, Kirchhoff F, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science. 2005;308:1314-8.
44. Tolosano E, Hirsch E, Patrucco E, Camaschella C, Navone R, Silengo L, et al. Defective recovery and severe renal damage after acute hemolysis in hemopexin-deficient mice. Blood. 1999;94:3906-14.
45. Poss KD, Thomas MJ, Ebralidze AK, O'Dell TJ, Tonegawa S. Hippocampal long-term potentiation is normal in heme oxygenase-2 mutant mice. Neuron. 1995;15:867-73.
46. Qu Y, Chen J, Benvenisti-Zarom L, Ma X, Regan RF. Effect of targeted deletion of the heme oxygenase-2 gene on hemoglobin toxicity in the striatum. J Cereb Blood Flow Metab. 2005;25:1466-75.
47. Singh N, Ma B, Leonardo CC, Ahmad AS, Narumiya S, Doré S. Role of PGE(2) EP1 receptor in intracerebral hemorrhage-induced brain injury. Neurotox Res. 2013;24:549-59.
48. Clark W, Gunion-Rinker L, Lessov N, Hazel K. Citicoline treatment for experimental intracerebral hemorrhage in mice. Stroke. 1998;29:2136-40.
49. Schmued LC, Hopkins KJ. Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res. 2000;874:123-30.
50. Kitagawa H, Sasaki C, Sakai K, Mori A, Mitsumoto Y, Mori T, et al. Adenovirus-mediated gene transfer of glial cell line-derived neurotrophic factor prevents ischemic brain injury after transient middle cerebral artery occlusion in rats. J Cereb Blood Flow Metab. 1999;19:1336-44.
51. Knutson M, Wessling-Resnick M. Iron metabolism in the reticuloendothelial system. Crit Rev Biochem Mol Biol. 2003;38:61-88.
52. Li T, Pang S, Yu Y, Wu X, Guo J, Zhang S. Proliferation of parenchymal microglia is the main source of microgliosis after ischaemic stroke. Brain. 2013;136:3578-88.
53. Ohsawa K, Imai Y, Kanazawa H, Sasaki Y, Kohsaka S. Involvement of Iba1 in membrane ruffling and phagocytosis of macrophages/microglia. J Cell Sci. 2000;113(Pt 17):3073-84.
54. Sasaki Y, Ohsawa K, Kanazawa H, Kohsaka S, Imai Y. Iba1 is an actin-cross-linking protein in macrophages/microglia. Biochem Biophys Res Commun. 2001;286:292-7.
55. Qu Y, Chen-Roetling J, Benvenisti-Zarom L, Regan RF. Attenuation of oxidative injury after induction of experimental intracerebral hemorrhage in heme oxygenase-2 knockout mice. J Neurosurg. 2007;106:428-35.
56. Wang J, Doré S. Heme oxygenase 2 deficiency increases brain swelling and inflammation after intracerebral hemorrhage. Neuroscience. 2008;155:1133-41.
57. Morello N, Tonoli E, Logrand F, Fiorito V, Fagoonee S, Turco E, et al. Haemopexin affects iron distribution and ferritin expression in mouse brain. J Cell Mol Med. 2009;13:4192-204.
58. Morello N, Bianchi FT, Marmiroli P, Tonoli E, Rodriguez Menendez V, Silengo L, et al. A role for hemopexin in oligodendrocyte differentiation and myelin formation. PloS one. 2011;6:e20173.
59. Wu J, Hua Y, Keep RF, Nakamura T, Hoff JT, Xi G. Iron and iron-handling proteins in the brain after intracerebral hemorrhage. Stroke. 2003;34:2964-9.
60. Koeppen AH, Dickson AC, McEvoy JA. The cellular reactions to experimental intracerebral hemorrhage. J Neurol Sci. 1995;134(Suppl):102-12.
61. Raivich G, Bohatschek M, Kloss CU, Werner A, Jones LL, Kreutzberg GW. Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function. Brain Res Brain Res Rev. 1999;30:77-105.
62. van Rossum D, Hanisch UK. Microglia. Metab Brain Dis. 2004;19:393-411.
63. Kitamura Y, Yanagisawa D, Inden M, Takata K, Tsuchiya D, Kawasaki T, et al. Recovery of focal brain ischemia-induced behavioral dysfunction by intracerebroventricular injection of microglia. J Pharmacol Sci. 2005;97:289-93.
64. Imai F, Suzuki H, Oda J, Ninomiya T, Ono K, Sano H, et al. Neuroprotective effect of exogenous microglia in global brain ischemia. J Cereb Blood Flow Metab. 2007;27:488-500.
65. Yong VW, Rivest S. Taking advantage of the systemic immune system to cure brain diseases. Neuron. 2009;64:55-60.
66. Yrjanheikki J, Tikka T, Keinanen R, Goldsteins G, Chan PH, Koistinaho J. A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc Natl Acad Sci U S A. 1999;96:13496-500.
67. Tikka T, Fiebich BL, Goldsteins G, Keinanen R, Koistinaho J. Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci. 2001;21:2580-8.
68. Kriz J, Nguyen MD, Julien JP. Minocycline slows disease progression in a mouse model of amyotrophic lateral sclerosis. Neurobiol Dis. 2002;10:268-78.
69. Kriz J, Gowing G, Julien JP. Efficient three-drug cocktail for disease induced by mutant superoxide dismutase. Ann Neurol. 2003;53:429-36.
70. Imai Y, Kohsaka S. Intracellular signaling in M-CSF-induced microglia activation: role of Iba1. Glia. 2002;40:164-74.
71. Kovtunovych G, Eckhaus MA, Ghosh MC, Ollivierre-Wilson H, Rouault TA. Dysfunction of the heme recycling system in heme oxygenase 1-deficient mice: effects on macrophage viability and tissue iron distribution. Blood. 2010;116:6054-62.