Cleaning up after ICH: The role of Nrf2 in modulating microglia function and hematoma clearance

Journal of Neurochemistry

Volumn 133, Issue 1, 2015, Pages 144-152

  Zhao, Xiurong ^a   Sun, Guanghua ^a   Ting, Shun Ming ^a   Song, Shen ^a   Zhang, Jie ^a   Edwards, Nancy J ^a   Aronowski, Jaroslaw ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

hematoma; intracerebral hemorrhage; microglia; Nrf2; phagocytosis; sulforaphane

Indexed keywords

CD36 ANTIGEN; DNA; NEUTRALIZING ANTIBODY; PEROXIDE; SCAVENGER RECEPTOR; SULFORAPHANE; TERT BUTYLHYDROQUINONE; TRANSCRIPTION FACTOR NRF2; 2-TERT-BUTYLHYDROQUINONE; HYDROGEN PEROXIDE; HYDROQUINONE DERIVATIVE; ISOTHIOCYANIC ACID DERIVATIVE; SULFORAFAN; TRANSCRIPTION FACTOR NF E2 P45 SUBUNIT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIOXIDANT ACTIVITY; ARTICLE; BLOOD COMPONENT; BRAIN DAMAGE; BRAIN HEMATOMA; BRAIN HEMORRHAGE; CONTROLLED STUDY; ERYTHROCYTE; KNOCKOUT MOUSE; MACROPHAGE; MALE; MICROGLIA; MICROGLIAL CELL CULTURE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; RAT; UPREGULATION; ANIMAL; BIOSYNTHESIS; BRAIN; CELL COUNT; CELL CULTURE; DRUG EFFECTS; GENETICS; METABOLISM; PATHOLOGY;

ANIMALIA; MUS; RATTUS;

ANIMALS; ANTIGENS, CD36; BRAIN; CELL COUNT; CELLS, CULTURED; CEREBRAL HEMORRHAGE; HYDROGEN PEROXIDE; HYDROQUINONES; ISOTHIOCYANATES; MICE; MICE, KNOCKOUT; MICROGLIA; NF-E2 TRANSCRIPTION FACTOR, P45 SUBUNIT; PHAGOCYTOSIS;

EID: 84924540176     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12974     Document Type: Article

References (50)

1. Abe T., Shimamura M., Jackman K., Kurinami H., Anrather J., Zhou P., and, Iadecola C., (2010) Key role of CD36 in Toll-like receptor 2 signaling in cerebral ischemia. Stroke 41, 898-904.
2. Alam J., Stewart D., Touchard C., Boinapally S., Choi A. M., and, Cook J. L., (1999) Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J. Biol. Chem. 274, 26071-26078.
3. Aronowski J., and, Hall C. E., (2005) New horizons for primary intracerebral hemorrhage treatment: experience from preclinical studies. Neurol. Res. 27, 268-279.
4. Asahi M., Asahi K., Wang X., and, Lo E. H., (2000) Reduction of tissue plasminogen activator-induced hemorrhage and brain injury by free radical spin trapping after embolic focal cerebral ischemia in rats. J. Cereb. Blood Flow Metab. 20, 452-457.
5. Banati R. B., Gehrmann J., Schubert P., and, Kreutzberg G. W., (1993) Cytotoxicity of microglia. Glia 7, 111-118.
6. Bowie A., and, O'Neill L. A., (2000) Oxidative stress and nuclear factor-kappaB activation: a reassessment of the evidence in the light of recent discoveries. Biochem. Pharmacol. 59, 13-23.
7. Brigelius-Flohe R., and, Flohe L., (2011) Basic principles and emerging concepts in the redox control of transcription factors. Antioxid. Redox Signal. 15, 2335-2381.
8. Broderick J. P., Brott T., Tomsick T., Miller R., and, Huster G., (1993a) Intracerebral hemorrhage more than twice as common as subarachnoid hemorrhage. J. Neurosurg. 78, 188-191.
9. Broderick J. P., Brott T. G., Duldner J. E., Tomsick T., and, Huster G., (1993b) Volume of intracerebral hemorrhage. A powerful and easy-to-use predictor of 30-day mortality. Stroke 24, 987-993.
10. Chan K., Lu R., Chang J. C., and, Kan Y. W., (1996) NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proc. Natl Acad. Sci. USA 93, 13943-13948.
11. Cho S., and, Kim E., (2009) CD36: a multi-modal target for acute stroke therapy. J. Neurochem. 109 (Suppl 1), 126-132.
12. Cho S., Park E. M., Febbraio M., Anrather J., Park L., Racchumi G., Silverstein R. L., and, Iadecola C., (2005) The class B scavenger receptor CD36 mediates free radical production and tissue injury in cerebral ischemia. J. Neurosci. 25, 2504-2512.
13. Cox G., Crossley J., and, Xing Z., (1995) Macrophage engulfment of apoptotic neutrophils contributes to the resolution of acute pulmonary inflammation in vivo. Am. J. Respir. Cell Mol. Biol. 12, 232-237.
14. Felberg R. A., Grotta J. C., Shirzadi A. L., Strong R., Narayana P., Hill-Felberg S. J., and, Aronowski J., (2002) Cell death in experimental intracerebral hemorrhage: the "black hole" model of hemorrhagic damage. Ann. Neurol. 51, 517-524.
15. Gong C., Hoff J. T., and, Keep R. F., (2000) Acute inflammatory reaction following experimental intracerebral hemorrhage in rat. Brain Res. 871, 57-65.
16. Gonzales N. R., Shah J., Sangha N., et al,. (2013) Design of a prospective, dose-escalation study evaluating the Safety of Pioglitazone for Hematoma Resolution in Intracerebral Hemorrhage (SHRINC). Int J Stroke, 8, 388-396.
17. Hanley D. F., (2009) Intraventricular hemorrhage. Severity factor and treatment target in spontaneous intracerebral hemorrhage. Stroke, 40, 1533-1538.
18. Hickenbottom S. L., Grotta J. C., Strong R., Denner L. A., and, Aronowski J., (1999) Nuclear factor-kappaB and cell death after experimental intracerebral hemorrhage in rats. Stroke, 30, 2472-2477; discussion 2477-2478.
19. Ishii T., Itoh K., Ruiz E., Leake D. S., Unoki H., Yamamoto M., and, Mann G. E., (2004) Role of Nrf2 in the regulation of CD36 and stress protein expression in murine macrophages: activation by oxidatively modified LDL and 4-hydroxynonenal. Circ. Res. 94, 609-616.
20. Itoh K., Wakabayashi N., Katoh Y., Ishii T., Igarashi K., Engel J. D., and, Yamamoto M., (1999) Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13, 76-86.
21. Kunz A., Abe T., Hochrainer K., Shimamura M., Anrather J., Racchumi G., Zhou P., and, Iadecola C., (2008) Nuclear factor-kappaB activation and postischemic inflammation are suppressed in CD36-null mice after middle cerebral artery occlusion. J. Neurosci. 28, 1649-1658.
22. Kwak M. K., Itoh K., Yamamoto M., Sutter T. R., and, Kensler T. W., (2001) Role of transcription factor Nrf2 in the induction of hepatic phase 2 and antioxidative enzymes in vivo by the cancer chemoprotective agent, 3H-1, 2-dimethiole-3-thione. Mol. Med. 7, 135-145.
23. Maderna P., and, Godson C., (2003) Phagocytosis of apoptotic cells and the resolution of inflammation. Biochim. Biophys. Acta 1639, 141-151.
24. Manoonkitiwongsa P. S., Jackson-Friedman C., McMillan P. J., Schultz R. L., and, Lyden P. D., (2001) Angiogenesis after stroke is correlated with increased numbers of macrophages: the clean-up hypothesis. J. Cereb. Blood Flow Metab. 21, 1223-1231.
25. Maruyama A., Tsukamoto S., Nishikawa K., et al,. (2008) Nrf2 regulates the alternative first exons of CD36 in macrophages through specific antioxidant response elements. Arch. Biochem. Biophys. 477, 139-145.
26. Moi P., Chan K., Asunis I., Cao A., and, Kan Y. W., (1994) Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region. Proc. Natl Acad. Sci. USA 91, 9926-9930.
27. van Muiswinkel F. L., and, Kuiperij H. B., (2005) The Nrf2-ARE Signalling pathway: promising drug target to combat oxidative stress in neurodegenerative disorders. Curr. Drug Targets CNS Neurol. Disord. 4, 267-281.
28. Murray P. J., and, Wynn T. A., (2011) Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11, 723-737.
29. Olagnier D., Lavergne R. A., Meunier E., et al,. (2011) Nrf2, a PPARgamma alternative pathway to promote CD36 expression on inflammatory macrophages: implication for malaria. PLoS Pathog. 7, e1002254.
30. Park E. Y., and, Rho H. M., (2002) The transcriptional activation of the human copper/zinc superoxide dismutase gene by 2,3,7,8-tetrachlorodibenzo-p-dioxin through two different regulator sites, the antioxidant responsive element and xenobiotic responsive element. Mol. Cell. Biochem. 240, 47-55.
31. Ransohoff R. M., and, Perry V. H., (2009) Microglial physiology: unique stimuli, specialized responses. Annu. Rev. Immunol. 27, 119-145.
32. Ren Y., Silverstein R. L., Allen J., and, Savill J., (1995) CD36 gene transfer confers capacity for phagocytosis of cells undergoing apoptosis. J. Exp. Med. 181, 1857-1862.
33. Sambrano G. R., Parthasarathy S., and, Steinberg D., (1994) Recognition of oxidatively damaged erythrocytes by a macrophage receptor with specificity for oxidized low density lipoprotein. Proc. Natl Acad. Sci. USA 91, 3265-3269.
34. Splettstoesser W. D., and, Schuff-Werner P., (2002) Oxidative stress in phagocytes-"the enemy within". Microsc. Res. Tech. 57, 441-455.
35. Taylor R. A., and, Sansing L. H., (2013) Microglial responses after ischemic stroke and intracerebral hemorrhage. Clin. Dev. Immunol. 2013, 746068.
36. Thimmulappa R. K., Mai K. H., Srisuma S., Kensler T. W., Yamamoto M., and, Biswal S., (2002) Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res. 62, 5196-5203.
37. Wagner K. R., Sharp F. R., Ardizzone T. D., Lu A., and, Clark J. F., (2003) Heme and iron metabolism: role in cerebral hemorrhage. J. Cereb. Blood Flow Metab. 23, 629-652.
38. Wang X., Mori T., Sumii T., and, Lo E. H., (2002) Hemoglobin-induced cytotoxicity in rat cerebral cortical neurons: caspase activation and oxidative stress. Stroke 33, 1882-1888.
39. Wang J., Fields J., Zhao C., Langer J., Thimmulappa R. K., Kensler T. W., Yamamoto M., Biswal S., and, Dore S., (2007) Role of Nrf2 in protection against intracerebral hemorrhage injury in mice. Free Radic. Biol. Med. 43, 408-414.
40. Woo M. S., Wang X., Faustino J. V., Derugin N., Wendland M. F., Zhou P., Iadecola C., and, Vexler Z. S., (2012) Genetic deletion of CD36 enhances injury after acute neonatal stroke. Ann. Neurol. 72, 961-970.
41. Xi G., Keep R. F., and, Hoff J. T., (2006) Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol. 5, 53-63.
42. Yenari M. A., Xu L., Tang X. N., Qiao Y., and, Giffard R. G., (2006) Microglia potentiate damage to blood-brain barrier constituents: improvement by minocycline in vivo and in vitro. Stroke 37, 1087-1093.
43. Zhang M., Wang S., Mao L., et al,. (2014) Omega-3 fatty acids protect the brain against ischemic injury by activating Nrf2 and upregulating heme oxygenase 1. J. Neurosci. 34, 1903-1915.
44. Zhao X., Zhang Y., Strong R., Grotta J. C., and, Aronowski J., (2006) 15d-Prostaglandin J2 activates peroxisome proliferator-activated receptor-gamma, promotes expression of catalase, and reduces inflammation, behavioral dysfunction, and neuronal loss after intracerebral hemorrhage in rats. J. Cereb. Blood Flow Metab. 26, 811-820.
45. Zhao X., Sun G., Zhang J., Strong R., Dash P. K., Kan Y. W., Grotta J. C., and, Aronowski J., (2007a) Transcription factor Nrf2 protects the brain from damage produced by intracerebral hemorrhage. Stroke 38, 3280-3286.
46. Zhao X., Sun G., Zhang J., Strong R., Song W., Gonzales N., Grotta J. C., and, Aronowski J., (2007b) Hematoma resolution as a target for intracerebral hemorrhage treatment: role for peroxisome proliferator-activated receptor gamma in microglia/macrophages. Ann. Neurol. 61, 352-362.
47. Zhao X., Zhang Y., Strong R., Zhang J., Grotta J. C., and, Aronowski J., (2007c) Distinct patterns of intracerebral hemorrhage-induced alterations in NF-kappaB subunit, iNOS, and COX-2 expression. J. Neurochem. 101, 652-663.
48. Zhao X., Grotta J., Gonzales N., and, Aronowski J., (2009a) Hematoma resolution as a therapeutic target: the role of microglia/macrophages. Stroke 40, S92-S94.
49. Zhao X., Song S., Sun G., Strong R., Zhang J., Grotta J. C., and, Aronowski J., (2009b) Neuroprotective role of haptoglobin after intracerebral hemorrhage. J. Neurosci. 29, 15819-15827.
50. Zhao X., Strong R., Zhang J., Sun G., Tsien J. Z., Cui Z., Grotta J. C., and, Aronowski J., (2009c) Neuronal PPARgamma deficiency increases susceptibility to brain damage after cerebral ischemia. J. Neurosci. 29, 6186-6195.