Peroxiredoxin I is a ROS/p38 MAPK-dependent inducible antioxidant that regulates NF-κB-mediated iNOS induction and microglial activation

Journal of Neuroimmunology

Volumn 259, Issue 1-2, 2013, Pages 26-36

  Kim, Sun Uk ^a,h   Park, Young Ho ^a,h   Min, Ju Sik ^b   Sun, Hu Nan ^c   Han, Ying Hao ^c   Hua, Jin Mei ^c   Lee, Tae Hoon ^d   Lee, Sang Rae ^a   Chang, Kyu Tae ^a   Kang, Sang Won ^e   Kim, Jin Man ^f   Yu, Dae Yeul ^a   Lee, Sang Ho ^g   Lee, Dong Seok ^b  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b Kyungpook National University   (South Korea)

^c HEILONGJIANG BAYI AGRICULTURAL UNIVERSITY   (China)

^d Chonnam National University   (South Korea)

^e Ewha Womans University   (South Korea)

^f Chungnam National University   (South Korea)

^g Korea University   (South Korea)

^h University of Science and Technology (UST)   (South Korea)

Author keywords

Antioxidants; Inflammation; Lipopolysaccharides; Microglia activation; Peroxiredoxin; Reactive oxygen species

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PEROXIREDOXIN 1; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BRAIN CORTEX; BRAIN REGION; CELL ACTIVATION; CELL STIMULATION; CONTROLLED STUDY; DEGENERATIVE DISEASE; ENZYME ACTIVITY; HIPPOCAMPUS; IMMUNOREACTIVITY; IMMUNOREGULATION; MALE; MICROGLIA; MOUSE; NERVE CELL CULTURE; NERVOUS SYSTEM INFLAMMATION; NEUROIMMUNOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; UPREGULATION;

ANIMALS; ANTIOXIDANTS; CELL LINE, TRANSFORMED; CELL NUCLEUS; HIPPOCAMPUS; LIPOPOLYSACCHARIDES; MICE; MICE, KNOCKOUT; MICROGLIA; NEUROIMMUNOMODULATION; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; ORGAN CULTURE TECHNIQUES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PEROXIREDOXINS; PRIMARY CELL CULTURE; REACTIVE OXYGEN SPECIES; TRANSCRIPTIONAL ACTIVATION;

EID: 84877596486     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2013.03.006     Document Type: Article

References (55)

1. Abbas K., Breton J., Picot C.R., Quesniaux V., Bouton C., Drapier J.C. Signaling events leading to peroxiredoxin 5 up-regulation in immunostimulated macrophages. Free Radic. Biol. Med. 2009, 47:794-802.
2. Acharya A., Das I., Chandhok D., Saha T. Redox regulation in cancer: a double-edged sword with therapeutic potential. Oxidative Med. Cell. Longev. 2010, 3:23-34.
3. Basso M., Giraudo S., Corpillo D., Bergamasco B., Lopiano L., Fasano M. Proteome analysis of human substantia nigra in Parkinson's disease. Proteomics 2004, 4:3943-3952.
4. Bonda D.J., Wang X., Perry G., Nunomura A., Tabaton M., Zhu X., Smith M.A. Oxidative stress in Alzheimer disease: a possibility for prevention. Neuropharmacology 2010, 59:290-294.
5. Calabrese V., Guagliano E., Sapienza M., Panebianco M., Calafato S., Puleo E., Pennisi G., Mancuso C., Butterfield D.A., Stella A.G. Redox regulation of cellular stress response in aging and neurodegenerative disorders: role of vitagenes. Neurochem. Res. 2007, 32:757-773.
6. Chen J.C., Ho F.M., Pei-Dawn Lee C., Chen C.P., Jeng K.C., Hsu H.B., Lee S.T., Wen Tung W., Lin W.W. Inhibition of iNOS gene expression by quercetin is mediated by the inhibition of IkappaB kinase, nuclear factor-kappa B and STAT1, and depends on heme oxygenase-1 induction in mouse BV-2 microglia. Eur. J. Pharmacol. 2005, 521:9-20.
7. Chiche J.D., Schlutsmeyer S.M., Bloch D.B., de la Monte S.M., Roberts J.D., Filippov G., Janssens S.P., Rosenzweig A., Bloch K.D. Adenovirus-mediated gene transfer of cGMP-dependent protein kinase increases the sensitivity of cultured vascular smooth muscle cells to the antiproliferative and pro-apoptotic effects of nitric oxide/cGMP. J. Biol. Chem. 1998, 273:34263-34271.
8. Chowdhury N.J., Misbahuddin M., Rahman M.S. Corn extracts lower tissue arsenic level in rat. Bangladesh Med. Res. Counc. Bull. 2009, 35:21-25.
9. Coyle J.T., Puttfarcken P. Oxidative stress, glutamate, and neurodegenerative disorders. Science 1993, 262:689-695.
10. Diet A., Abbas K., Bouton C., Guillon B., Tomasello F., Fourquet S., Toledano M.B., Drapier J.C. Regulation of peroxiredoxins by nitric oxide in immunostimulated macrophages. J. Biol. Chem. 2007, 282:36199-36205.
11. Domingues A.F., Arduino D.M., Esteves A.R., Swerdlow R.H., Oliveira C.R., Cardoso S.M. Mitochondria and ubiquitin-proteasomal system interplay: relevance to Parkinson's disease. Free Radic. Biol. Med. 2008, 45:820-825.
12. Dumont M., Beal M.F. Neuroprotective strategies involving ROS in Alzheimer disease. Free Radic. Biol. Med. 2011, 51:1014-1026.
13. Gloire G., Legrand-Poels S., Piette J. NF-kappaB activation by reactive oxygen species: fifteen years later. Biochem. Pharmacol. 2006, 72:1493-1505.
14. Himadri P., Kumari S.S., Chitharanjan M., Dhananjay S. Role of oxidative stress and inflammation in hypoxia-induced cerebral edema: a molecular approach. High Alt Med. Biol. 2010, 11:231-244.
15. Huang X., Moir R.D., Tanzi R.E., Bush A.I., Rogers J.T. Redox-active metals, oxidative stress, and Alzheimer's disease pathology. Ann. N. Y. Acad. Sci. 2004, 1012:153-163.
16. Hurd T.R., DeGennaro M., Lehmann R. Redox regulation of cell migration and adhesion. Trends Cell Biol. 2012, 22:107-115.
17. 2+ channel activation in vitro. J. Neurosci. 1999, 19:802-812.
18. Ishii K., Muelhauser F., Liebl U., Picard M., Kuhl S., Penke B., Bayer T., Wiessler M., Hennerici M., Beyreuther K., Hartmann T., Fassbender K. Subacute NO generation induced by Alzheimer's beta-amyloid in the living brain: reversal by inhibition of the inducible NO synthase. FASEB J. 2000, 14:1485-1489.
19. Ishii T., Warabi E., Yanagawa T. Novel roles of peroxiredoxins in inflammation, cancer and innate immunity. J. Clin. Biochem. Nutr. 2012, 50:91-105.
20. Ishii T., Yamada M., Sato H., Matsue M., Taketani S., Nakayama K., Sugita Y., Bannai S. Cloning and characterization of a 23-kDa stress-induced mouse peritoneal macrophage protein. J. Biol. Chem. 1993, 268:18633-18636.
21. Jeong W.S., Kim I.W., Hu R., Kong A.N. Modulatory properties of various natural chemopreventive agents on the activation of NF-kappaB signaling pathway. Pharm. Res. 2004, 21:661-670.
22. Jin M.H., Lee Y.H., Kim J.M., Sun H.N., Moon E.Y., Shong M.H., Kim S.U., Lee S.H., Lee T.H., Yu D.Y., Lee D.S. Characterization of neural cell types expressing peroxiredoxins in mouse brain. Neurosci. Lett. 2005, 381:252-257.
23. Jurgens H.A., Johnson R.W. Dysregulated neuronal-microglial cross-talk during aging, stress and inflammation. Exp. Neurol. 2012, 233:40-48.
24. Kim E.J., Kwon K.J., Park J.Y., Lee S.H., Moon C.H., Baik E.J. Neuroprotective effects of prostaglandin E2 or cAMP against microglial and neuronal free radical mediated toxicity associated with inflammation. J. Neurosci. Res. 2002, 70:97-107.
25. Kim S.H., Fountoulakis M., Cairns N., Lubec G. Protein levels of human peroxiredoxin subtypes in brains of patients with Alzheimer's disease and Down syndrome. J. Neural Transm. 2001, (Supplementum):223-235.
26. Kim S.U., Hwang C.N., Sun H.N., Jin M.H., Han Y.H., Lee H., Kim J.M., Kim S.K., Yu D.Y., Lee D.S., Lee S.H. Peroxiredoxin I is an indicator of microglia activation and protects against hydrogen peroxide-mediated microglial death. Biol. Pharm. Bull. 2008, 31:820-825.
27. Kim S.U., Jin M.H., Kim Y.S., Lee S.H., Cho Y.S., Cho K.J., Lee K.S., Kim Y.I., Kim G.W., Kim J.M., Lee T.H., Lee Y.H., Shong M., Kim H.C., Chang K.T., Yu D.Y., Lee D.S. Peroxiredoxin II preserves cognitive function against age-linked hippocampal oxidative damage. Neurobiol. Aging 2011, 32:1054-1068.
28. Kim Y.J., Ahn J.Y., Liang P., Ip C., Zhang Y., Park Y.M. Human prx1 gene is a target of Nrf2 and is up-regulated by hypoxia/reoxygenation: implication to tumor biology. Cancer Res. 2007, 67:546-554.
29. Krapfenbauer K., Engidawork E., Cairns N., Fountoulakis M., Lubec G. Aberrant expression of peroxiredoxin subtypes in neurodegenerative disorders. Brain Res. 2003, 967:152-160.
30. Krapfenbauer K., Yoo B.C., Fountoulakis M., Mitrova E., Lubec G. Expression patterns of antioxidant proteins in brains of patients with sporadic Creutzfeldt-Jakob disease. Electrophoresis 2002, 23:2541-2547.
31. Lee Y.J., Goo J.S., Kim J.E., Nam S.H., Hwang I.S., Choi S.I., Lee H.R., Lee E.P., Choi H.W., Kim H.S., Lee J.H., Jung Y.J., Kim H.J., Hwang D.Y. Peroxiredoxin I regulates the component expression of gamma-secretase complex causing the Alzheimer's disease. Lab. Anim. Res. 2011, 27:293-299.
32. Li Q., Verma I.M. NF-kappaB regulation in the immune system. Nat. Rev. Immunol. 2002, 2:725-734.
33. Lund S., Christensen K.V., Hedtjarn M., Mortensen A.L., Hagberg H., Falsig J., Hasseldam H., Schrattenholz A., Porzgen P., Leist M. The dynamics of the LPS triggered inflammatory response of murine microglia under different culture and in vivo conditions. J. Neuroimmunol. 2006, 180:71-87.
34. Melo A., Monteiro L., Lima R.M., Oliveira D.M., Cerqueira M.D., El-Bacha R.S. Oxidative stress in neurodegenerative diseases: mechanisms and therapeutic perspectives. Oxidative Med. Cell. Longev. 2011, 2011:467180.
35. Nakano H., Nakajima A., Sakon-Komazawa S., Piao J.H., Xue X., Okumura K. Reactive oxygen species mediate crosstalk between NF-kappaB and JNK. Cell Death Differ. 2006, 13:730-737.
36. Olson J.K., Miller S.D. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J. Immunol. 2004, 173:3916-3924.
37. Pawate S., Shen Q., Fan F., Bhat N.R. Redox regulation of glial inflammatory response to lipopolysaccharide and interferongamma. J. Neurosci. Res. 2004, 77:540-551.
38. Park Y.H., Kim S.U., Lee B.K., Kim H.S., Song I.S., Shin H.J., Han Y.H., Chang K.T., Kim J.M., Lee D.S., Kim Y.H., Choi C.M., Kim B.Y., Yu D.Y. Prx I suppresses K-ras-driven lung tumorigenesis by opposing redox-sensitive ERK/cyclin D1 pathway. Antioxid. Redox Signal. 2013, (in press). 10.1089/ars.2011.4421.
39. Peng T., Lu X., Feng Q. Pivotal role of gp91phox-containing NADH oxidase in lipopolysaccharide-induced tumor necrosis factor-alpha expression and myocardial depression. Circulation 2005, 111:1637-1644.
40. Peristeris P., Clark B.D., Gatti S., Faggioni R., Mantovani A., Mengozzi M., Orencole S.F., Sironi M., Ghezzi P. N-acetylcysteine and glutathione as inhibitors of tumor necrosis factor production. Cell. Immunol. 1992, 140:390-399.
41. Rohl C., Armbrust E., Herbst E., Jess A., Gulden M., Maser E., Rimbach G., Bosch-Saadatmandi C. Mechanisms involved in the modulation of astroglial resistance to oxidative stress induced by activated microglia: antioxidative systems, peroxide elimination, radical generation, lipid peroxidation. Neurotox. Res. 2010, 17:317-331.
42. Sun H.N., Kim S.U., Huang S.M., Kim J.M., Park Y.H., Kim S.H., Yang H.Y., Chung K.J., Lee T.H., Choi H.S., Min J.S., Park M.K., Kim S.K., Lee S.R., Chang K.T., Lee S.H., Yu D.Y., Lee D.S. Microglial peroxiredoxin V acts as an inducible anti-inflammatory antioxidant through cooperation with redox signaling cascades. J. Neurochem. 2010, 114:39-50.
43. Sun J., Ramnath R.D., Zhi L., Tamizhselvi R., Bhatia M. Substance P enhances NF-kappaB transactivation and chemokine response in murine macrophages via ERK1/2 and p38 MAPK signaling pathways. Am. J. Physiol. Cell Physiol. 2008, 294:C1586-C1596.
44. Tae Lim Y., Song D.S., Won T.J., Lee Y.J., Yoo J.S., Hyung K.E., Yoon J.W., Park S.Y., Hwang K.W. Peroxiredoxin-1, a possible target in modulating inflammatory cytokine production in macrophage like cell line RAW264.7. Microbiol. Immunol. 2012, 56:411-419.
45. Takahashi M. Oxidative stress and redox regulation on in vitro development of mammalian embryos. J. Reprod. Dev. 2012, 58:1-9.
46. Torres M. Mitogen-activated protein kinase pathways in redox signaling. Front. Biosci. 2003, 8:d369-d391.
47. Torres M., Forman H.J. Redox signaling and the MAP kinase pathways. Biofactors 2003, 17:287-296.
48. Watters J.J., Sommer J.A., Pfeiffer Z.A., Prabhu U., Guerra A.N., Bertics P.J. A differential role for the mitogen-activated protein kinases in lipopolysaccharide signaling: the MEK/ERK pathway is not essential for nitric oxide and interleukin 1beta production. J. Biol. Chem. 2002, 277:9077-9087.
49. Weber C., Sejersgard Jakobsen T., Mortensen S.A., Paulsen G., Holmer G. Antioxidative effect of dietary coenzyme Q10 in human blood plasma. Int. J. Vitam. Nutr. Res. 1994, 64:311-315.
50. Wiser J., Alexis N.E., Jiang Q., Wu W., Robinette C., Roubey R., Peden D.B. In vivo gamma-tocopherol supplementation decreases systemic oxidative stress and cytokine responses of human monocytes in normal and asthmatic subjects. Free Radic. Biol. Med. 2008, 45:40-49.
51. Xu C., Shen G., Chen C., Gelinas C., Kong A.N. Suppression of NF-kappaB and NF-kappaB-regulated gene expression by sulforaphane and PEITC through IkappaBalpha, IKK pathway in human prostate cancer PC-3 cells. Oncogene 2005, 24:4486-4495.
52. Zhang Y., Du Y., Le W., Wang K., Kieffer N., Zhang J. Redox control of the survival of healthy and diseased cells. Antioxid. Redox. Signal. 2011, 15:2867-2908.
53. Zhang Y.L., Dong C. MAP kinases in immune responses. Cell. Mol. Immunol. 2005, 2:20-27.
54. Zhu H., Santo A., Li Y. The antioxidant enzyme peroxiredoxin and its protective role in neurological disorders. Exp. Biol. Med. 2012, 237:143-149.
55. Zhu J., Grace M., Casale J., Chang A.T., Musco M.L., Bordens R., Greenberg R., Schaefer E., Indelicato S.R. Characterization of replication-competent adenovirus isolates from large-scale production of a recombinant adenoviral vector. Hum. Gene. Ther. 1999, 10:113-121.