Activated microglia are less vulnerable to hemin toxicity due to nitric oxide-dependent inhibition of JNK and p38 MAPK activation

Journal of Immunology

Volumn 187, Issue 3, 2011, Pages 1314-1321

  Cai, Ying ^a,b   Cho, Geum Sil ^a   Ju, Chung ^a   Wang, Si Ling ^b   Ryu, Jong Hoon ^c   Shin, Chan Young ^d,e   Kim, Hee Sun ^f   Nam, Kung Woo ^a   Anthony Jalin, Angela M A ^a   Sun, Woong ^a   Choi, In Young ^a   Kim, Won Ki ^a  

^a Korea University College of Medicine   (South Korea)

^b SHENYANG PHARMACEUTICAL UNIVERSITY   (China)

^c Kyung Hee University   (South Korea)

^d Konkuk University School of Medicine   (South Korea)

^e Konkuk University   (South Korea)

^f Ewha Womans University School of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

3,3 BIS(2 AMINOETHYL) 1 HYDROXY 2 OXOTRIAZENE; HEME OXYGENASE 1; HEMIN; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; N6 (1 IMINOETHYL)LYSINE; NITRIC OXIDE; PROTOPORPHYRIN TIN; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; CELL ACTIVATION; CELL SURVIVAL; CONTROLLED STUDY; CORPUS CALLOSUM; EMBRYO; ENZYME ACTIVATION; MALE; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; ASTROCYTES; CELLS, CULTURED; HEMIN; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIPOPOLYSACCHARIDES; MALE; MAP KINASE SIGNALING SYSTEM; MICROGLIA; MICROINJECTIONS; NEURONS; NITRIC OXIDE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 80051610850     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002925     Document Type: Article

References (44)

1. Qureshi, A. I., S. Tuhrim, J. P. Broderick, H. H. Batjer, H. Hondo, and D. F. Hanley. 2001. Spontaneous intracerebral hemorrhage. N. Engl. J. Med. 344: 1450-1460. (Pubitemid 32402103)
2. Zhao, X., J. Grotta, N. Gonzales, and J. Aronowski. 2009. Hematoma resolution as a therapeutic target: the role of microglia/macrophages. Stroke 40: S92-S94.
3. Elijovich, L., P. V. Patel, and J. C. Hemphill III. 2008. Intracerebral hemorrhage. Semin. Neurol. 28: 657-667.
4. Robinson, S. R., T. N. Dang, R. Dringen, and G. M. Bishop. 2009. Hemin toxicity: a preventable source of brain damage following hemorrhagic stroke. Redox Rep. 14: 228-235.
5. Zhao, X., G. Sun, J. Zhang, R. Strong, W. Song, N. Gonzales, J. C. Grotta, and J. Aronowski. 2007. Hematoma resolution as a target for intracerebral hemorrhage treatment: role for peroxisome proliferator-activated receptor gamma in microglia/macrophages. Ann. Neurol. 61: 352-362. (Pubitemid 46676735)
6. Aronowski, J., and C. E. Hall. 2005. New horizons for primary intracerebral hemorrhage treatment: experience from preclinical studies. Neurol. Res. 27: 268-279. (Pubitemid 40523798)
7. Wang, J., and S. Doré. 2007. Inflammation after intracerebral hemorrhage. J. Cereb. Blood Flow Metab. 27: 894-908doi:10.1038/sj.jcbfm.9600403 (Pubitemid 46659028)
8. Qureshi, A. I., A. D. Mendelow, and D. F. Hanley. 2009. Intracerebral haemorrhage. Lancet 373: 1632-1644.
9. Lim, J. H., J. C. Lee, Y. H. Lee, I. Y. Choi, Y. K. Oh, H. S. Kim, J. S. Park, and W. K. Kim. 2006. Simvastatin prevents oxygen and glucose deprivation/ reoxygenation-induced death of cortical neurons by reducing the production and toxicity of 4-hydroxy-2E-nonenal. J. Neurochem. 97: 140-150.
10. Juckett, M., Y. Zheng, H. Yuan, T. Pastor, W. Antholine, M. Weber, and G. Vercellotti. 1998. Heme and the endothelium: effects of nitric oxide on catalytic iron and heme degradation by heme oxygenase. J. Biol. Chem. 273: 23388-23397. (Pubitemid 28417528)
11. Foresti, R., and R. Motterlini. 1999. The heme oxygenase pathway and its interaction with nitric oxide in the control of cellular homeostasis. Free Radic. Res. 31: 459-475.
12. Ashino, T., R. Yamanaka, M. Yamamoto, H. Shimokawa, K. Sekikawa, Y. Iwakura, S. Shioda, S. Numazawa, and T. Yoshida. 2008. Negative feedback regulation of lipopolysaccharide-induced inducible nitric oxide synthase gene expression by heme oxygenase-1 induction in macrophages. Mol. Immunol. 45: 2106-2115. (Pubitemid 351226260)
13. Wang, J., and S. Doré. 2007. Heme oxygenase-1 exacerbates early brain injury after intracerebral haemorrhage. Brain 130: 1643-1652. (Pubitemid 47355932)
14. Orihara, Y., K. Ikematsu, R. Tsuda, and I. Nakasono. 2001. Induction of nitric oxide synthase by traumatic brain injury. Forensic Sci. Int. 123: 142-149. (Pubitemid 33122033)
15. Junttila, M. R., S. P. Li, and J. Westermarck. 2008. Phosphatase-mediated crosstalk between MAPK signaling pathways in the regulation of cell survival. FASEB J. 22: 954-965. (Pubitemid 351519953)
16. Zwerina, J., S. Tzima, S. Hayer, K. Redlich, O. Hoffmann, B. Hanslik-Schnabel, J. S. Smolen, G. Kollias, and G. Schett. 2005. Heme oxygenase 1 (HO-1) regulates osteoclastogenesis and bone resorption. FASEB J. 19: 2011-2013. (Pubitemid 41759748)
17. Burguillos, M. A., T. Deierborg, E. Kavanagh, A. Persson, N. Hajji, A. Garcia- Quintanilla, J. Cano, P. Brundin, E. Englund, J. L. Venero, and B. Joseph. 2011. Caspase signalling controls microglia activation and neurotoxicity. Nature 472: 319-324. .
18. Saijo, K., B. Winner, C. T. Carson, J. G. Collier, L. Boyer, M. G. Rosenfeld, F. H. Gage, and C. K. Glass. 2009. A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell 137: 47-59.
19. van Rossum, D., and U. K. Hanisch. 2004. Microglia. Metab. Brain Dis. 19: 393-411.
20. Lee, J. C., G. S. Cho, H. J. Kim, J. H. Lim, Y. K. Oh, W. Nam, J. H. Chung, and W. K. Kim. 2005. Accelerated cerebral ischemic injury by activated macrophages/microglia after lipopolysaccharide microinjection into rat corpus callosum. Glia 50: 168-181. (Pubitemid 40695270)
21. Letarte, P. B., K. Lieberman, K. Nagatani, R. A. Haworth, G. B. Odell, and T. A. Duff. 1993. Hemin: levels in experimental subarachnoid hematoma and effects on dissociated vascular smooth-muscle cells. J. Neurosurg. 79: 252-255. (Pubitemid 23215844)
22. Hosoda, K., N. Tamaki, M. Masumura, S. Matsumoto, and F. Maeda. 1987. Magnetic resonance images of chronic subdural hematomas. J. Neurosurg. 67: 677-683. (Pubitemid 17161396)
23. Regan, R. F., Y. Wang, X. Ma, A. Chong, and Y. Guo. 2001. Activation of extracellular signal-regulated kinases potentiates hemin toxicity in astrocyte cultures. J. Neurochem. 79: 545-555. (Pubitemid 33029928)
24. Regan, R. F., Y. Guo, and N. Kumar. 2000. Heme oxygenase-1 induction protects murine cortical astrocytes from hemoglobin toxicity. Neurosci. Lett. 282: 1-4. (Pubitemid 30129154)
25. Wang, X., T. Mori, T. Sumii, and E. H. Lo. 2002. Hemoglobin-induced cytotoxicity in rat cerebral cortical neurons: caspase activation and oxidative stress. Stroke 33: 1882-1888. (Pubitemid 34761080)
26. Benvenisti-Zarom, L., J. Chen-Roetling, and R. F. Regan. 2006. Inhibition of the ERK/MAP kinase pathway attenuates heme oxygenase-1 expression and hememediated neuronal injury. Neurosci. Lett. 398: 230-234. (Pubitemid 44274990)
27. Wu, J., S. Yang, G. Xi, S. Song, G. Fu, R. F. Keep, and Y. Hua. 2008. Microglial activation and brain injury after intracerebral hemorrhage. Acta Neurochir. Suppl. 105: 59-65.
28. Gao, Z., J. Wang, R. Thiex, A. D. Rogove, F. L. Heppner, and S. E. Tsirka. 2008. Microglial activation and intracerebral hemorrhage. Acta Neurochir. Suppl. 105: 51-53.
29. Salvemini, D., V. Mollace, A. Pistelli, E. Anggård, and J. Vane. 1992. Cultured astrocytoma cells generate a nitric oxide-like factor from endogenous L-arginine and glyceryl trinitrate: effect of E. coli lipopolysaccharide. Br. J. Pharmacol. 106: 931-936.
30. Buskila, Y., S. Farkash, M. Hershfinkel, and Y. Amitai. 2005. Rapid and reactive nitric oxide production by astrocytes in mouse neocortical slices. Glia 52: 169- 176.
31. Akama, K. T., and L. J. Van Eldik. 2000. Beta-amyloid stimulation of inducible nitric-oxide synthase in astrocytes is interleukin-1beta- and tumor necrosis factor-alpha (TNFalpha)-dependent, and involves a TNFalpha receptor-associated factor- and NFkappaB-inducing kinase-dependent signaling mechanism. J. Biol. Chem. 275: 7918-7924. (Pubitemid 30159700)
32. Saura, J. 2007. Microglial cells in astroglial cultures: a cautionary note. J. Neuroinflammation 4: 26.
33. Motterlini, R., R. Foresti, M. Intaglietta, and R. M. Winslow. 1996. NO-mediated activation of heme oxygenase: endogenous cytoprotection against oxidative stress to endothelium. Am. J. Physiol. 270: H107-H114.
34. Wagner, K. R., Y. Hua, G. M. de Courten-Myers, J. P. Broderick, R. N. Nishimura, S. Y. Lu, and B. E. Dwyer. 2000. Tin-mesoporphyrin, a potent heme oxygenase inhibitor, for treatment of intracerebral hemorrhage: in vivo and in vitro studies. Cell. Mol. Biol. (Noisy-le-grand) 46: 597-608.
35. Koeppen, A. H., A. C. Dickson, and J. Smith. 2004. Heme oxygenase in experimental intracerebral hemorrhage: the benefit of tin-mesoporphyrin. J. Neuropathol. Exp. Neurol. 63: 587-597. (Pubitemid 38736422)
36. Gong, Y., H. Tian, G. Xi, R. F. Keep, J. T. Hoff, and Y. Hua. 2006. Systemic zinc protoporphyrin administration reduces intracerebral hemorrhage-induced brain injury. Acta Neurochir. Suppl. 96: 232-236.
37. Torres, M., and H. J. Forman. 2003. Redox signaling and the MAP kinase pathways. Biofactors 17: 287-296. (Pubitemid 37267162)
38. Park, G. H., S. J. Jeon, H. M. Ko, J. R. Ryu, J. M. Lee, H. Y. Kim, S. H. Han, Y. S. Kang, S. H. Park, C. Y. Shin, and K. H. Ko. 2010. Activation of microglial cells via protease-activated receptor 2 mediates neuronal cell death in cultured rat primary neuron. Nitric Oxide 22: 18-29.
39. Lee, S., and K. Suk. 2007. Heme oxygenase-1 mediates cytoprotective effects of immunostimulation in microglia. Biochem. Pharmacol. 74: 723-729. (Pubitemid 47087765)
40. Sugaya, K., M. Chouinard, and M. McKinney. 1997. Immunostimulation protects microglial cells from nitric oxide-mediated apoptosis. Neuroreport 8: 2241-2245. (Pubitemid 27319680)
41. Boehme, S. A., F. M. Lio, D. Maciejewski-Lenoir, K. B. Bacon, and P. J. Conlon. 2000. The chemokine fractalkine inhibits Fas-mediated cell death of brain microglia. J. Immunol. 165: 397-403. (Pubitemid 30429532)
42. Soriano, S. G., L. S. Amaravadi, Y. F. Wang, H. Zhou, G. X. Yu, J. R. Tonra, V. Fairchild-Huntress, Q. Fang, J. H. Dunmore, D. Huszar, and Y. Pan. 2002. Mice deficient in fractalkine are less susceptible to cerebral ischemia-reperfusion injury. J. Neuroimmunol. 125: 59-65. (Pubitemid 34327454)
43. Block, M. L., L. Zecca, and J. S. Hong. 2007. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 8: 57-69. (Pubitemid 46011999)
44. Wang, J. 2010. Preclinical and clinical research on inflammation after intracerebral hemorrhage. Prog. Neurobiol. 92: 463-477.