8-Oxoguanine-DNA glycosylase 1 deficiency modifies allergic airway inflammation by regulating STAT6 and IL-4 in cells and in mice

Free Radical Biology and Medicine

Volumn 52, Issue 2, 2012, Pages 392-401

  Li, Guoping ^a,b   Yuan, Kefei ^a   Yan, Chunguang ^a,c   Fox III, John ^a   Gaid, Madeleine ^a   Breitwieser, Wayne ^d   Bansal, Arvind K ^d   Zeng, Huawei ^e   Gao, Hongwei ^c   Wu, Min ^a  

^a UNIVERSITY OF NORTH DAKOTA   (United States)

^b SOUTHWEST MEDICAL UNIVERSITY   (China)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d Altru Hospital   (United States)

^e GRAND FORKS HUMAN NUTRITION RESEARCH CENTER   (United States)

Author keywords

Airway inflammation; Free radicals; HDM extracts; Knockout mice; Oxidative stress; Th2 cytokines

Indexed keywords

8 OXOGUANINE DNA GLYCOSYLASE 1; GAMMA INTERFERON; HOUSE DUST ALLERGEN; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 6; OVALBUMIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; STAT6 PROTEIN; UNCLASSIFIED DRUG;

ALLERGIC DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CULTURE; CELL INFILTRATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME DEFICIENCY; EPITHELIUM CELL; LUNG PARENCHYMA; MOUSE; NONHUMAN; OBSTRUCTIVE AIRWAY DISEASE; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ANIMALS; ASTHMA; CELL LINE; CYTOKINES; DNA GLYCOSYLASES; DNA REPAIR; EPITHELIAL CELLS; INFLAMMATION; INTERLEUKIN-4; LUNG; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B; OVALBUMIN; OXIDATIVE STRESS; PHOSPHORYLATION; PYROGLYPHIDAE; RANDOM ALLOCATION; REACTIVE OXYGEN SPECIES; STAT6 TRANSCRIPTION FACTOR; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

MUS; PYROGLYPHIDAE;

EID: 84855432271     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.10.490     Document Type: Article

References (66)

1. I. Ohno Bronchial asthma and psychological stress Rinsho Byori 58 2010 292 299
2. D.H. Broide Molecular and cellular mechanisms of allergic disease J. Allergy Clin. Immunol. 108 2001 S65 S71
3. D.K. Agrawal, and Z. Shao Pathogenesis of allergic airway inflammation Curr. Allergy Asthma Rep. 10 2010 39 48
4. A. Nadeem, S.K. Chhabra, A. Masood, and H.G. Raj Increased oxidative stress and altered levels of antioxidants in asthma J. Allergy Clin. Immunol. 111 2003 72 78 (Pubitemid 36143294)
5. A.J. Dozor The role of oxidative stress in the pathogenesis and treatment of asthma Ann. N. Y. Acad. Sci. 1203 2010 133 137
6. S.E. Gomez-Mejiba, Z. Zhai, H. Akram, Q.N. Pye, K. Hensley, B.T. Kurien, R.H. Scofield, and D.C. Ramirez Inhalation of environmental stressors & chronic inflammation: autoimmunity and neurodegeneration Mutat. Res. 674 2009 62 72
7. Z. Wu, D.R. Turner, and D.B. Oliveira IL-4 gene expression up-regulated by mercury in rat mast cells: a role of oxidant stress in IL-4 transcription Int. Immunol. 13 2001 297 304 (Pubitemid 32179077)
8. I. Boldogh, A. Bacsi, B.K. Choudhury, N. Dharajiya, R. Alam, T.K. Hazra, S. Mitra, R.M. Goldblum, and S. Sur ROS generated by pollen NADPH oxidase provide a signal that augments antigen induced allergic airway inflammation J. Clin. Invest. 115 2005 2169 2179 (Pubitemid 41134158)
9. Y.S. Cho, and H.B. Moon The role of oxidative stress in the pathogenesis of asthma Allergy Asthma Immunol. Res. 2 2010 183 187
10. P. Kirkham, and I. Rahman Oxidative stress in asthma and COPD: antioxidants as a therapeutic strategy Pharmacol. Ther. 111 2006 476 494 (Pubitemid 43832007)
11. D. Zeyrek, A. Cakmak, A. Atas, A. Kocyigit, and O. Erel DNA damage in children with asthma bronchiale and its association with oxidative and antioxidative measurements Pediatr. Allergy Immunol. 20 2009 370 376
12. B. Batar, M. Guven, I. Onaran, B. Tutluoglu, and G. Kanigur-Sultuybek DNA repair gene XRCC1 polymorphisms and the risk of asthma in a Turkish population Allergy Asthma Proc. 31 2010 349 354
13. M. Wu, H. Huang, W. Zhang, S. Kannan, A. Weaver, M. Mckibben, D. Herington, H. Zeng, and H. Gao Host DNA repair proteins in response to P. aeruginosa in lung epithelial cells and in mice Infect. Immun. 79 2011 75 87
14. H.M. Nash, S.D. Bruner, O.D. Scharer, T. Kawate, T.A. Addona, E. Spooner, W.S. Lane, and G.L. Verdine Cloning of a yeast 8-oxoguanine DNA glycosylase reveals the existence of a base excision repair protein superfamily Curr. Biol. 6 1996 968 980 (Pubitemid 26350717)
15. T. Izumi, L.R. Wiederhold, G. Roy, R. Roy, A. Jaiswal, K.K. Bhakat, and S. Mitra Mammalian DNA base excision repair proteins: their interactions and role in repair of oxidative DNA damage Toxicology 193 2003 43 65 (Pubitemid 37340143)
16. C.K. Youn, P.I. Song, M.H. Kim, J.S. Kim, J.W. Hyun, S.J. Choi, S.P. Yoon, M.H. Chung, I.Y. Chang, and H.J. You Human 8-oxoguanine DNA glycosylase suppresses the oxidative stress-induced apoptosis through a p53-mediated signaling pathway in human fibroblasts Mol. Cancer Res. 5 2007 1083 1098 (Pubitemid 350070763)
17. A.L. Lu, X. Li, Y. Gu, P.M. Wright, and D.Y. Chang Repair of oxidative DNA damage: mechanisms and functions Cell Biochem. Biophys. 35 2001 141 170 (Pubitemid 33622685)
18. L. Virág, and C. Szabó The therapeutic potential of poly(ADP-ribose) polymerase inhibitors Pharmacol. Rev. 54 2002 375 429
19. F. Cardozo-Pelaez, D.P. Cox, and C. Bolin Lack of the DNA repair enzyme OGG1 sensitizes dopamine neurons to manganese toxicity during development Gene Expr. 12 2005 315 323 (Pubitemid 41729062)
20. N.J. Hodges, and J.K. Chipman Down-regulation of the DNA-repair endonuclease 8-oxo-guanine DNA glycosylase 1 (hOGG1) by sodium dichromate in cultured human A549 lung carcinoma cells Carcinogenesis 23 2002 55 60 (Pubitemid 34213551)
21. M. Osterod, S. Hollenbach, J.G. Hengstler, D.E. Barnes, T. Lindahl, and B. Epe Age-related and tissue-specific accumulation of oxidative DNA base damage in 7,8-dihydro-8-oxoguanine-DNA glycosylase (Ogg1) deficient mice Carcinogenesis 22 2001 1459 1463 (Pubitemid 32898703)
22. Y. He, Y. Xu, M. Wu, M. Kobune, M.R. Kelley, and W.J. Martin II E. coli FPG and human Ogg1 reduce DNA damage and cytotoxicity by BCNU in human lung cells Am. J. Physiol. Lung Cell. Mol. Physiol. 182 2002 L50 L55
23. M. Wu, Y. He, Y. Xu, M. Kobune, M.R. Kelley, and W.J. Martin II Protection of human lung cells against hyperoxia using the DNA base excision repair genes hOgg1 and Fpg Am. J. Respir. Crit. Care Med. 166 2002 192 199 (Pubitemid 34765456)
24. A.W. Dobson, V. Grishko, S.P. LeDoux, M.R. Kelley, G.L. Wilson, and M.N. Gillespie Enhanced mtDNA repair capacity protects pulmonary artery endothelial cells from oxidant-mediated death Am. J. Physiol. Lung Cell. Mol. Physiol. 283 2002 L205 L210
25. Y. Xu, W.K. Hansen, T.A. Rosenquist, D.A. Williams, M. Limp-Foster, and M.R. Kelley Protection of mammalian cells against chemotherapeutic agents thiotepa, 1,3-N, N′-bis(2-chloroethyl)-N-nitrosourea, and mafosfamide using the DNA base excision repair genes Fpg and a-hOgg1: implications for protective gene therapy applications J. Pharmacol. Exp. Ther. 296 2001 825 831 (Pubitemid 32187354)
26. M. Wu, A. Audet, J. Cusic, D. Seeger, R. Cochran, and O. Ghribi Broad DNA repair responses in neural injury are associated with activation of the IL-6 pathway in cholesterol-fed rabbits J. Neurochem. 111 2009 1011 1021
27. P.H. Danielsen, S. Loft, N.R. Jacobsen, K.A. Jensen, H. Autrup, J.L. Ravanat, H. Wallin, and P. Møller Oxidative stress, inflammation, and DNA damage in rats after intratracheal instillation or oral exposure to ambient air and wood smoke particulate matter Toxicol. Sci. 118 2010 574 585
28. J.G. Mabley, P. Pacher, A. Deb, R. Wallace, R.H. Elder, and C. Szabo Potential role for 8-oxoguanine DNA glycosylase in regulating inflammation FASEB J. 19 2005 290 292 (Pubitemid 40189285)
29. E. Touati, V. Michel, J.M. Thiberge, P. Avé, M. Huerre, F. Bourgade, A. Klungland, and A. Labigne Deficiency in OGG-1 protects against inflammation and mutagenic effects associated with H. pylori infection in mouse Helicobacter 11 2006 494 505 (Pubitemid 44352621)
30. A. Klungland, I. Rosewell, S. Hollenbach, E. Larsen, G. Daly, B. Epe, E. Seeberg, T. Lindahl, and D.E. Barnes Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage Proc. Natl. Acad. Sci. U. S. A. 96 1999 13300 13305
31. M. Wu, S. Hussain, H.Y. He, R. Pasula, P.A. Smith, and W.J. Martin II Genetically engineered macrophages expressing IFN-γ restore alveolar immune function in scid mice Proc. Natl. Acad. Sci. U. S. A. 98 2001 14589 14594 (Pubitemid 33121436)
32. M. Wu, R. Pasula, P.A. Smith, and W.J. Martin II Mapping alveolar binding sites in vivo using phage display peptide libraries Gene Ther. 10 2003 1429 1436 (Pubitemid 36987136)
33. B.W.J. Loo, W. Meyer-Ilse, and S.S. Rothman Automatic image acquisition, calibration and montage assembly for biological X-ray microscopy J. Microsc. 197 2000 185 201 (Pubitemid 30096718)
34. Y. Suzaki, K. Hamada, T. Nomi, T. Ito, M. Sho, Y. Kai, Y. Nakajima, and H. Kimura A small-molecule compound targeting CCR5 and CXCR3 prevents airway hyperresponsiveness and inflammation Eur. Respir. J. 31 2008 783 789
35. T. Ashcroft, J.M. Simpson, and V. Timbrell Simple method of estimating severity of pulmonary fibrosis on a numerical scale J. Clin. Pathol. 41 1988 467 470 (Pubitemid 18098428)
36. S. Kannan, H. Huang, D. Seeger, A. Audet, Y. Chen, C. Huang, H. Gao, S. Li, and M. Wu Alveolar epithelial type II cells activate alveolar macrophages and mitigate P. aeruginosa infection PLoS One 4 2009 e4891
37. M. Wu, T. Sherwin, W.L. Brown, and P.G. Stockley Delivery of antisense oligonucleotides to leukaemia cells by RNA bacteriophage capsids Nanomedicine 1 2005 67 76 (Pubitemid 43963614)
38. S. Kannan, A. Audet, H. Huang, L.J. Chen, and M. Wu Cholesterol-rich membrane rafts and Lyn are involved in phagocytosis during Pseudomonas aeruginosa infection J. Immunol. 180 2008 2396 2408
39. M. Wu, P.G. Stockley, and W.J. Martin II An improved Western blotting effectively reduces the background Electrophoresis 23 2002 2373 2376
40. 6-methylguanine- DNA methyltransferease Am. J. Physiol. Lung Cell. Mol. Physiol. 280 2001 L755 L761
41. G.P. Li, Z.G. Liu, J. Qiu, P.X. Ran, and N.S. Zhong DNA vaccine encoding Der p 2 allergen generates immunologic protection in recombinant Der p 2 allergen-induced allergic airway inflammation mice model Chin. Med. J. (English) 118 2005 534 540 (Pubitemid 40515012)
42. N.C. de Souza-Pinto, L. Eide, B.A. Hogue, T. Thybo, T. Stevnsner, E. Seeberg, A. Klungland, and V.A. Bohr Repair of 8-oxodeoxyguanosine lesions in mitochondrial DNA depends on the oxoguanine DNA glycosylase (OGG1) gene and 8-oxoguanine accumulates in the mitochondrial DNA of OGG1-defective mice Cancer Res. 61 2001 5378 5381 (Pubitemid 32694914)
43. R.R. Bartz, H.B. Suliman, P. Fu, K. Welty-Wolf, M.S. Carraway, N.C. MacGarvey, C.M. Withers, T.E. Sweeney, and C.A. Piantadosi Staphylococcus aureus sepsis and mitochondrial accrual of the 8-oxoguanine DNA glycosylase DNA repair enzyme in mice Am. J. Respir. Crit. Care Med. 183 2011 226 233
44. K. Hashiguchi, J.A. Stuart, N.C. de Souza-Pinto, and V.A. Bohr The C-terminal alphaO helix of human Ogg1 is essential for 8-oxoguanine DNA glycosylase activity: the mitochondrial beta-Ogg1 lacks this domain and does not have glycosylase activity Nucleic Acids Res. 32 2004 5596 5608 (Pubitemid 39545676)
45. A. Bacsi, G. Chodaczek, T.K. Hazra, D. Konkel, and I. Boldogh Increased ROS generation in subsets of OGG-1 knockout fibroblast cells Mech. Ageing Dev. 128 2007 637 649 (Pubitemid 350299047)
46. J.I. MacDonald, and F. Possmayer Stimulation of phosphatidylcholine biosynthesis in mouse MLE-12 type-II cells by conditioned medium from cortisol-treated rat fetal lung fibroblasts Biochem. J. 312 1995 425 431 (Pubitemid 26002206)
47. X. Fang, Y. Song, J. Hirsch, L.J. Galietta, N. Pedemonte, R.L. Zemans, G. Dolganov, A.S. Verkman, and M.A. Matthay Contribution of CFTR to apical-basolateral fluid transport in cultured human alveolar epithelial type II cells Am. J. Physiol. Lung Cell. Mol. Physiol. 290 2006 L242 L249
48. M. Fukunaga, Y. Gon, S. Nunomura, T. Inoue, M. Yoshioka, S. Hashimoto, and C. Ra Protease-mediated house dust mite allergen-induced reactive oxygen species production by neutrophils Int. Arch. Allergy Immunol. 155 2011 104 109
49. S. Simone, Y. Gorin, C. Velagapudi, H.E. Abboud, and S.L. Habib Mechanism of oxidative DNA damage in diabetes: tuberin inactivation and downregulation of DNA repair enzyme 8-oxo-7,8-dihydro-2′-deoxyguanosine-DNA glycosylase Diabetes 57 2008 2626 2636
50. G. Mazzarella, A. Bianco, E. Catena, R. De Palma, and G.F. Abbate Th1/Th2 lymphocyte polarization in asthma Allergy 55 2000 6 9 (Pubitemid 30430371)
51. J.F. Alcorn, C.R. Crowe, and J.K. Kolls TH17 cells in asthma and COPD Annu. Rev. Physiol. 72 2010 495 516
52. + T cells Iran. J. Allergy Asthma Immunol. 9 2010 59 67
53. M. Jaiswal, N.F. LaRusso, R.A. Shapiro, T.R. Billiar, and G.J. Gores Nitric oxide-mediated inhibition of DNA repair potentiates oxidative DNA damage in cholangiocytes Gastroenterology 120 2001 190 199 (Pubitemid 32061883)
54. A.B. Pernis, and P.B. Rothman JAK-STAT signaling in asthma J. Clin. Invest. 109 2002 1279 1283 (Pubitemid 34546890)
55. R. Datta, A.S. Naura, M. Zerfaoui, Y. Errami, M. Oumouna, H. Kim, J. Ju, V.P. Ronchi, A.L. Haas, and A.H. Boulares PARP-1 deficiency blocks IL-5 expression through calpain-dependent degradation of STAT-6 in a murine asthma model Allergy 66 2011 853 861
56. A. Hoshino, T. Tsuji, J. Matsuzaki, T. Jinushi, S. Ashino, T. Teramura, K. Chamoto, Y. Tanaka, Y. Asakura, and T. Sakurai STAT6-mediated signaling in Th2-dependent allergic asthma: critical role for the development of eosinophilia, airway hyper-responsiveness and mucus hypersecretion, distinct from its role in Th2 differentiation Int. Immunol. 16 2004 1497 1505 (Pubitemid 39341563)
57. Y.M. Janssen-Heininger, M.E. Poynter, S.W. Aesif, C. Pantano, J.L. Ather, N.L. Reynaert, K. Ckless, V. Anathy, J. van der Velden, and C.G. Irvin Nuclear factor kappaB, airway epithelium, and asthma: avenues for redox control Proc. Am. Thorac. Soc. 6 2009 249 255
58. J.D. Crapo Oxidative stress as an initiator of cytokine release and cell damage Eur. Respir. J. 44 2003 4s 6s (Pubitemid 37222052)
59. L. Zhang, M. Wang, X. Kang, P. Boontheung, N. Li, A.E. Nel, and J.A. Loo Oxidative stress and asthma: proteome analysis of chitinase-like proteins and FIZZ1 in lung tissue and bronchoalveolar lavage fluid J. Proteome Res. 8 2009 1631 1638
60. J.H. Leem, J.H. Kim, K.H. Lee, Y. Hong, K.H. Lee, D. Kang, and H.J. Kwon Asthma attack associated with oxidative stress by exposure to ETS and PAH J. Asthma 42 2005 463 467 (Pubitemid 41475848)
61. N. Dharajiya, B.K. Choudhury, A. Bacsi, I. Boldogh, R. Alam, and S. Sur Inhibiting pollen reduced nicotinamide adenine dinucleotide phosphate oxidase-induced signal by intrapulmonary administration of antioxidants blocks allergic airway inflammation J. Allergy Clin. Immunol. 119 2007 646 653 (Pubitemid 46335816)
62. A.R. Collins, V. Harrington, J. Drew, and R. Melvin Nutritional modulation of DNA repair in a human intervention study Carcinogenesis 24 2003 511 515 (Pubitemid 36432648)
63. H.F. Kauffman, M. Tamm, J.A. Timmerman, and P. Borger House dust mite major allergens Der p 1 and Der p 5 activate human airway-derived epithelial cells by protease-dependent and protease-independent mechanisms Clin. Mol. Allergy 4 2006 5
64. S.H. Shin, and M.K. Ye Th2 responses elicited by nasal epithelial cells exposed to house dust mite extract Clin. Exp. Otorhinolaryngol. 2 2009 175 180
65. C. Osterlund, H. Grönlund, G. Gafvelin, and A. Bucht Non-proteolytic aeroallergens from mites, cat and dog exert adjuvant-like activation of bronchial epithelial cells Int. Arch. Allergy Immunol. 155 2010 111 118
66. M.A. Stacey, G. Sun, G. Vassalli, M. Marini, A. Bellini, and S. Mattoli The allergen Der p1 induces NF-κB activation through interference with IκBα function in asthmatic bronchial epithelial cells Biochem. Biophys. Res. Commun. 236 1997 522 526 (Pubitemid 27373332)