Dual functionality of myeloperoxidase in rotenone-exposed brain-resident immune cells

American Journal of Pathology

Volumn 179, Issue 2, 2011, Pages 964-979

  Chang, Chi Young ^a,b   Song, Mi Jeon ^a,b   Jeon, Sae Bom ^a,c   Yoon, Hee Jung ^a   Lee, Dae Kee ^b   Kim, In Hoo ^a   Suk, Kyungho ^d   Choi, Dong Kug ^e   Park, Eun Jung ^a  

^a National Cancer Center   (South Korea)

^b Ewha Womans University   (South Korea)

^c Ajou University School of Medicine   (South Korea)

^d Kyungpook National University School of Medicine   (South Korea)

^e Konkuk University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

MYELOPEROXIDASE; REACTIVE OXYGEN METABOLITE; ROTENONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN PROTECTION; CELL ACTIVATION; CELL DEATH; CELL FUNCTION; CELL VIABILITY; CONTROLLED STUDY; EFFECTOR CELL; ENZYME ACTIVITY; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; MICROGLIA; MOUSE; NERVE INJURY; NEUROPROTECTION; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; UPREGULATION;

ANIMALS; BRAIN; CELL SURVIVAL; FEMALE; HUMANS; IMMUNE SYSTEM; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, BIOLOGICAL; NEURONS; PEROXIDASE; PHAGOCYTOSIS; RATS; RATS, SPRAGUE-DAWLEY; ROTENONE; UNCOUPLING AGENTS;

EID: 80052514464     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.04.033     Document Type: Article

References (63)

1. R.L. Miller, M. James-Kracke, G.Y. Sun, and A.Y. Sun Oxidative and inflammatory pathways in Parkinson's disease Neurochem Res 34 2009 55 65
2. D.A. Drechsel, and M. Patel Role of reactive oxygen species in the neurotoxicity of environmental agents implicated in Parkinson's disease Free Radic Biol Med 44 2008 1873 1886
3. R. Betarbet, T.B. Sherer, G. MacKenzie, M. Garcia-Osuna, A.V. Panov, and J.T. Greenamyre Chronic systemic pesticide exposure reproduces features of Parkinson's disease Nat Neurosci 3 2000 1301 1306
4. D.J. Talpade, J.G. Greene, D.S. Higgins Jr, and J.T. Greenamyre In vivo labeling of mitochondrial complex I (NADH: ubiquinone oxidoreductase) in rat brain using [(3)H]dihydrorotenone J Neurochem 75 2000 2611 2621
5. S.M. Fleming, C. Zhu, P.O. Fernagut, A. Mehta, C.D. DiCarlo, R.L. Seaman, and M.F. Chesselet Behavioral and immunohistochemical effects of chronic intravenous and subcutaneous infusions of varying doses of rotenone Exp Neurol 187 2004 418 429 (Pubitemid 38610288)
6. R. Betarbet, R.H. Porter, and J.T. Greenamyre GluR1 glutamate receptor subunit is regulated differentially in the primate basal ganglia following nigrostriatal dopamine denervation J Neurochem 74 2000 1166 1174 (Pubitemid 30104314)
7. H.M. Gao, B. Liu, and J.S. Hong Critical role for microglial NADPH oxidase in rotenone-induced degeneration of dopaminergic neurons J Neurosci 23 2003 6181 6187 (Pubitemid 36875618)
8. M. Alam, and W.J. Schmidt Rotenone destroys dopaminergic neurons and induces parkinsonian symptoms in rats Behav Brain Res 136 2002 317 324 (Pubitemid 35246417)
9. D.J. Moore, A.B. West, V.L. Dawson, and T.M. Dawson Molecular pathophysiology of Parkinson's disease Annu Rev Neurosci 28 2005 57 87 (Pubitemid 41098899)
10. R. Zhang, M.L. Brennan, Z. Shen, J.C. MacPherson, D. Schmitt, C.E. Molenda, and S.L. Hazen Myeloperoxidase functions as a major enzymatic catalyst for initiation of lipid peroxidation at sites of inflammation J Biol Chem 277 2002 46116 46122 (Pubitemid 35417600)
11. R.A. Matthijsen, D. Huugen, N.T. Hoebers, B. de Vries, C.J. Peutz-Kootstra, Y. Aratani, M.R. Daha, J.W. Tervaert, W.A. Buurman, and P. Heeringa Myeloperoxidase is critically involved in the induction of organ damage after renal ischemia reperfusion Am J Pathol 171 2007 1743 1752
12. Y. Sawayama, Y. Miyazaki, K. Ando, K. Horio, C. Tsutsumi, D. Imanishi, H. Tsushima, Y. Imaizumi, T. Hata, T. Fukushima, S. Yoshida, Y. Onimaru, M. Iwanaga, J. Taguchi, K. Kuriyama, and M. Tomonaga Expression of myeloperoxidase enhances the chemosensitivity of leukemia cells through the generation of reactive oxygen species and the nitration of protein Leukemia 22 2008 956 964 (Pubitemid 351689877)
13. D. Lau, H. Mollnau, J.P. Eiserich, B.A. Freeman, A. Daiber, U.M. Gehling, J. Brummer, V. Rudolph, T. Munzel, T. Heitzer, T. Meinertz, and S. Baldus Myeloperoxidase mediates neutrophil activation by association with CD11b/CD18 integrins Proc Natl Acad Sci U S A 102 2005 431 436 (Pubitemid 40116784)
14. J.P. Eiserich, S. Baldus, M.L. Brennan, W. Ma, C. Zhang, A. Tousson, L. Castro, A.J. Lusis, W.M. Nauseef, C.R. White, and B.A. Freeman Myeloperoxidase, a leukocyte-derived vascular NO oxidase Science 296 2002 2391 2394 (Pubitemid 34734213)
15. D. El Kebir, L. Jozsef, W. Pan, and J.G. Filep Myeloperoxidase delays neutrophil apoptosis through CD11b/CD18 integrins and prolongs inflammation Circ Res 103 2008 352 359
16. T.O. Hirche, J.P. Gaut, J.W. Heinecke, and A. Belaaouaj Myeloperoxidase plays critical roles in killing Klebsiella pneumoniae and inactivating neutrophil elastase: effects on host defense J Immunol 174 2005 1557 1565
17. A. Daugherty, J.L. Dunn, D.L. Rateri, and J.W. Heinecke Myeloperoxidase, a catalyst for lipoprotein oxidation, is expressed in human atherosclerotic lesions J Clin Invest 94 1994 437 444 (Pubitemid 24218123)
18. D.K. Choi, S. Pennathur, C. Perier, K. Tieu, P. Teismann, D.C. Wu, V. Jackson-Lewis, M. Vila, J.P. Vonsattel, J.W. Heinecke, and S. Przedborski Ablation of the inflammatory enzyme myeloperoxidase mitigates features of Parkinson's disease in mice J Neurosci 25 2005 6594 6600 (Pubitemid 40995291)
19. R.M. Nagra, B. Becher, W.W. Tourtellotte, J.P. Antel, D. Gold, T. Paladino, R.A. Smith, J.R. Nelson, and W.F. Reynolds Immunohistochemical and genetic evidence of myeloperoxidase involvement in multiple sclerosis J Neuroimmunol 78 1997 97 107 (Pubitemid 27394430)
20. P.S. Green, A.J. Mendez, J.S. Jacob, J.R. Crowley, W. Growdon, B.T. Hyman, and J.W. Heinecke Neuronal expression of myeloperoxidase is increased in Alzheimer's disease J Neurochem 90 2004 724 733 (Pubitemid 38989404)
21. E. Gray, T.L. Thomas, S. Betmouni, N. Scolding, and S. Love Elevated activity and microglial expression of myeloperoxidase in demyelinated cerebral cortex in multiple sclerosis Brain Pathol 18 2008 86 95
22. W.F. Reynolds, J. Rhees, D. Maciejewski, T. Paladino, H. Sieburg, R.A. Maki, and E. Masliah Myeloperoxidase polymorphism is associated with gender specific risk for Alzheimer's disease Exp Neurol 155 1999 31 41 (Pubitemid 29072602)
23. R.A. Maki, V.A. Tyurin, R.C. Lyon, R.L. Hamilton, S.T. DeKosky, V.E. Kagan, and W.F. Reynolds Aberrant expression of myeloperoxidase in astrocytes promotes phospholipid oxidation and memory deficits in a mouse model of Alzheimer disease J Biol Chem 284 2009 3158 3169
24. Y. Du, C.P. Chen, C.Y. Tseng, Y. Eisenberg, and B.L. Firestein Astroglia-mediated effects of uric acid to protect spinal cord neurons from glutamate toxicity Glia 55 2007 463 472 (Pubitemid 46383176)
25. I. Jou, J.H. Lee, S.Y. Park, H.J. Yoon, E.H. Joe, and E.J. Park Gangliosides trigger inflammatory responses via TLR4 in brain glia Am J Pathol 168 2006 1619 1630
26. B.S. Han, H.S. Hong, W.S. Choi, G.J. Markelonis, T.H. Oh, and Y.J. Oh Caspase-dependent and -independent cell death pathways in primary cultures of mesencephalic dopaminergic neurons after neurotoxin treatment J Neurosci 23 2003 5069 5078 (Pubitemid 36793234)
27. S.B. Jeon, H.J. Yoon, S.H. Park, I.H. Kim, and E.J. Park Sulfatide, a major lipid component of myelin sheath, activates inflammatory responses as an endogenous stimulator in brain-resident immune cells J Immunol 181 2008 8077 8087
28. S.B. Jeon, H.J. Yoon, C.Y. Chang, H.S. Koh, S.H. Jeon, and E.J. Park Galectin-3 exerts cytokine-like regulatory actions through the JAK-STAT pathway J Immunol 185 2010 7037 7046
29. H.M. Gao, J.S. Hong, W. Zhang, and B. Liu Distinct role for microglia in rotenone-induced degeneration of dopaminergic neurons J Neurosci 22 2002 782 790 (Pubitemid 34141759)
30. H.M. Gao, J.S. Hong, W. Zhang, and B. Liu Synergistic dopaminergic neurotoxicity of the pesticide rotenone and inflammogen lipopolysaccharide: relevance to the etiology of Parkinson's disease J Neurosci 23 2003 1228 1236 (Pubitemid 36258901)
31. C.A. Colton Heterogeneity of microglial activation in the innate immune response in the brain J Neuroimmune Pharmacol 4 2009 399 418
32. K.A. Kigerl, J.C. Gensel, D.P. Ankeny, J.K. Alexander, D.J. Donnelly, and P.G. Popovich Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord J Neurosci 29 2009 13435 13444
33. S.K. Biswas, and A. Mantovani Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm Nat Immunol 11 2010 889 896
34. E. Caron, and A. Hall Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases Science 282 1998 1717 1721 (Pubitemid 28549289)
35. H. Neumann, M.R. Kotter, and R.J. Franklin Debris clearance by microglia: an essential link between degeneration and regeneration Brain 132 2009 288 295
36. K. Setsukinai, Y. Urano, K. Kakinuma, H.J. Majima, and T. Nagano Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species J Biol Chem 278 2003 3170 3175 (Pubitemid 36801227)
37. R. Dringen, P.G. Pawlowski, and J. Hirrlinger Peroxide detoxification by brain cells J Neurosci Res 79 2005 157 165 (Pubitemid 40116430)
38. S.J. Klebanoff Myeloperoxidase: friend and foe J Leukoc Biol 77 2005 598 625 (Pubitemid 40628741)
39. R. Zhang, M.L. Brennan, X. Fu, R.J. Aviles, G.L. Pearce, M.S. Penn, E.J. Topol, D.L. Sprecher, and S.L. Hazen Association between myeloperoxidase levels and risk of coronary artery disease JAMA 286 2001 2136 2142 (Pubitemid 34041599)
40. X. Fu, J.L. Kao, C. Bergt, S.Y. Kassim, N.P. Huq, A. d'Avignon, W.C. Parks, R.P. Mecham, and J.W. Heinecke Oxidative cross-linking of tryptophan to glycine restrains matrix metalloproteinase activity: specific structural motifs control protein oxidation J Biol Chem 279 2004 6209 6212 (Pubitemid 38248751)
41. G. Zabucchi, R. Menegazzi, M.R. Soranzo, and P. Patriarca Uptake of human eosinophil peroxidase by human neutrophils Am J Pathol 124 1986 510 518 (Pubitemid 16029455)
42. L. Tian, H. Rauvala, and C.G. Gahmberg Neuronal regulation of immune responses in the central nervous system Trends Immunol 30 2009 91 99
43. K. Biber, H. Neumann, K. Inoue, and H.W. Boddeke Neuronal "On" and "Off" signals control microglia Trends Neurosci 30 2007 596 602
44. E.J. Park, K.A. Ji, S.B. Jeon, W.H. Choi, I.O. Han, H.J. You, J.H. Kim, I. Jou, and E.H. Joe Rac1 contributes to maximal activation of STAT1 and STAT3 in IFN-gamma-stimulated rat astrocytes J Immunol 173 2004 5697 5703 (Pubitemid 39392158)
45. A. Nimmerjahn, F. Kirchhoff, and F. Helmchen Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo Science 308 2005 1314 1318 (Pubitemid 40746128)
46. V.H. Perry, J.A. Nicoll, and C. Holmes Microglia in neurodegenerative disease Nat Rev Neurol 6 2010 193 201
47. N.G. Innamorato, I. Lastres-Becker, and A. Cuadrado Role of microglial redox balance in modulation of neuroinflammation Curr Opin Neurol 22 2009 308 314
48. J. Arnhold, and J. Flemmig Human myeloperoxidase in innate and acquired immunity Arch Biochem Biophys 500 2010 92 106
49. F.C. Barone, L.M. Hillegass, W.J. Price, R.F. White, E.V. Lee, G.Z. Feuerstein, H.M. Sarau, R.K. Clark, and D.E. Griswold Polymorphonuclear leukocyte infiltration into cerebral focal ischemic tissue: myeloperoxidase activity assay and histologic verification J Neurosci Res 29 1991 336 345
50. Y. Matsuo, H. Onodera, Y. Shiga, M. Nakamura, M. Ninomiya, T. Kihara, and K. Kogure Correlation between myeloperoxidase-quantified neutrophil accumulation and ischemic brain injury in the rat: effects of neutrophil depletion Stroke 25 1994 1469 1475 (Pubitemid 24198597)
51. S. Baldus, C. Heeschen, T. Meinertz, A.M. Zeiher, J.P. Eiserich, T. Munzel, M.L. Simoons, and C.W. Hamm Myeloperoxidase serum levels predict risk in patients with acute coronary syndromes Circulation 108 2003 1440 1445 (Pubitemid 37176448)
52. J.A. Vita, M.L. Brennan, N. Gokce, S.A. Mann, M. Goormastic, M.H. Shishehbor, M.S. Penn, J.F. Keaney Jr, and S.L. Hazen Serum myeloperoxidase levels independently predict endothelial dysfunction in humans Circulation 110 2004 1134 1139 (Pubitemid 39319014)
53. M. Brennan, A. Gaur, A. Pahuja, A.J. Lusis, and W.F. Reynolds Mice lacking myeloperoxidase are more susceptible to experimental autoimmune encephalomyelitis J Neuroimmunol 112 2001 97 105
54. M.L. Brennan, M.M. Anderson, D.M. Shih, X.D. Qu, X. Wang, A.C. Mehta, L.L. Lim, W. Shi, S.L. Hazen, J.S. Jacob, J.R. Crowley, J.W. Heinecke, and A.J. Lusis Increased atherosclerosis in myeloperoxidase-deficient mice J Clin Invest 107 2001 419 430 (Pubitemid 32167988)
55. C. Milla, S. Yang, D.N. Cornfield, M.L. Brennan, S.L. Hazen, A. Panoskaltsis-Mortari, B.R. Blazar, and I.Y. Haddad Myeloperoxidase deficiency enhances inflammation after allogeneic marrow transplantation Am J Physiol Lung Cell Mol Physiol 287 2004 L706 L714
56. D. Kutter, P. Devaquet, G. Vanderstocken, J.M. Paulus, V. Marchal, and A. Gothot Consequences of total and subtotal myeloperoxidase deficiency: risk or benefit Acta Haematol 104 2000 10 15
57. J.P. Eiserich, M. Hristova, C.E. Cross, A.D. Jones, B.A. Freeman, B. Halliwell, and A. van der Vliet Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils Nature 391 1998 393 397 (Pubitemid 28093514)
58. S. Baldus, T. Heitzer, J.P. Eiserich, D. Lau, H. Mollnau, M. Ortak, S. Petri, B. Goldmann, H.J. Duchstein, J. Berger, U. Helmchen, B.A. Freeman, T. Meinertz, and T. Munzel Myeloperoxidase enhances nitric oxide catabolism during myocardial ischemia and reperfusion Free Radic Biol Med 37 2004 902 911 (Pubitemid 39078559)
59. V. Brovkovych, X.P. Gao, E. Ong, S. Brovkovych, M.L. Brennan, X. Su, S.L. Hazen, A.B. Malik, and R.A. Skidgel Augmented inducible nitric oxide synthase expression and increased NO production reduce sepsis-induced lung injury and mortality in myeloperoxidase-null mice Am J Physiol Lung Cell Mol Physiol 295 2008 L96 L103
60. R.A. Clark, P.J. Stone, A. El Hag, J.D. Calore, and C. Franzblau Myeloperoxidase-catalyzed inactivation of alpha 1-protease inhibitor by human neutrophils J Biol Chem 256 1981 3348 3353 (Pubitemid 11076993)
61. F. Ginhoux, M. Greter, M. Leboeuf, S. Nandi, P. See, S. Gokhan, M.F. Mehler, S.J. Conway, L.G. Ng, E.R. Stanley, I.M. Samokhvalov, and M. Merad Fate mapping analysis reveals that adult microglia derive from primitive macrophages Science 330 2010 841 845
62. N.P. Hailer, F.L. Heppner, D. Haas, and R. Nitsch Fluorescent dye prelabelled microglial cells migrate into organotypic hippocampal slice cultures and ramify Eur J Neurosci 9 1997 863 866 (Pubitemid 27190097)
63. G. Schmitz, K. Leuthauser-Jaschinski, and E. Orso Are circulating monocytes as microglia orthologues appropriate biomarker targets for neuronal diseases Cent Nerv Syst Agents Med Chem 9 2009 307 330