Down-regulation of 8-oxoguanine DNA glycosylase 1 expression in the airway epithelium ameliorates allergic lung inflammation

DNA Repair

Volumn 12, Issue 1, 2013, Pages 18-26

  Bacsi, Attila ^a,b   Aguilera Aguirre, Leopoldo ^a   Szczesny, Bartosz ^a   Radak, Zsolt ^a,c   Hazra, Tapas K ^a   Sur, Sanjiv ^a   Ba, Xueqing ^a,d   Boldogh, Istvan ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c UNIVERSITY OF PHYSICAL EDUCATION   (Hungary)

^d NORTHEAST NORMAL UNIVERSITY   (China)

Author keywords

8 oxoG; 8 Oxoguanine; 8 Oxoguanine DNA glycosylase 1; AECs; AHR; Allergic inflammation; AP sites; APE1; BALF; BER; CA; DNA repair; DSB; FapyG; GSH, GSSG; H2DCF DA; MEF; Neil1D Neil2D; Neil1P Neil2P; NOX; Ogg1; Ogg1D; Ogg1P; Oxidative DNA damage; Oxidative stress; ROS; RWPE; SSBs

Indexed keywords

8 OXOGUANINE DNA GLYCOSYLASE 1; CYTOKINE; DNA GLYCOSYLTRANSFERASE; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ALLERGIC AIRWAY INFLAMMATION; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; CELL INFILTRATION; DNA STRAND BREAKAGE; DOWN REGULATION; EOSINOPHILIA; FEMALE; GENE OVEREXPRESSION; INFLAMMATORY CELL; METAPLASIA; MOUSE; MUCUS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAGWEED POLLEN; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT ALLERGY; SENSITIZATION;

AMBROSIA; ANIMALS; CELL LINE; DNA; DNA BREAKS, SINGLE-STRANDED; DNA GLYCOSYLASES; DNA REPAIR; DOWN-REGULATION; GUANINE; LUNG; MICE; MICE, INBRED C57BL; PNEUMONIA; POLLEN; RESPIRATORY HYPERSENSITIVITY; RESPIRATORY MUCOSA; RNA, SMALL INTERFERING;

AMBROSIA; AMBROSIA ARTEMISIIFOLIA; MUS;

EID: 84871716320     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2012.10.002     Document Type: Article

References (65)

1. Dharajiya N., Boldogh I., Cardenas V., Sur S. Role of pollen NAD(P)H oxidase in allergic inflammation. Curr. Opin. Allergy Clin. Immunol. 2008, 8:57-62.
2. Vrtala S., Grote M., Duchene M., van Ree R., Kraft D., Scheiner O., Valenta R. Properties of tree and grass pollen allergens: reinvestigation of the linkage between solubility and allergenicity. Int. Arch. Allergy Immunol. 1993, 102:160-169.
3. D'Amato G., Liccardi G., D'Amato M., Cazzola M. Outdoor air pollution, climatic changes and allergic bronchial asthma. Eur. Respir. J. 2002, 20:763-776.
4. Annesi-Maesano I., Rouve S., Desqueyroux H., Jankovski R., Klossek J.M., Thibaudon M., Demoly P., Didier A. Grass pollen counts, air pollution levels and allergic rhinitis severity. Int. Arch. Allergy Immunol. 2012, 158:397-404.
5. Boldogh I., Bacsi A., Choudhury B.K., Dharajiya N., Alam R., Hazra T.K., Mitra S., Goldblum R.M., Sur S. ROS generated by pollen NADPH oxidase provide a signal that augments antigen-induced allergic airway inflammation. J. Clin. Invest. 2005, 115:2169-2179.
6. Bacsi A., Choudhury B.K., Dharajiya N., Sur S., Boldogh I. Subpollen particles: carriers of allergenic proteins and oxidases. J. Allergy Clin. Immunol. 2006, 118:844-850.
7. Yadav U.C., Naura A.S., Aguilera-Aguirre L., Ramana K.V., Boldogh I., Sur S., Boulares H.A., Srivastava S.K. Aldose reductase inhibition suppresses the expression of Th2 cytokines and airway inflammation in ovalbumin-induced asthma in mice. J. Immunol. 2009, 183:4723-4732.
8. Yadav U.C., Aguilera-Aguirre L., Ramana K.V., Boldogh I., Srivastava S.K. Aldose reductase inhibition prevents metaplasia of airway epithelial cells. PLoS ONE 2010, 5:e14440.
9. Bacsi A., Dharajiya N., Choudhury B.K., Sur S., Boldogh I. Effect of pollen-mediated oxidative stress on immediate hypersensitivity reactions and late-phase inflammation in allergic conjunctivitis. J. Allergy Clin. Immunol. 2005, 116:836-843.
10. Csillag A., Boldogh I., Pazmandi K., Magyarics Z., Gogolak P., Sur S., Rajnavolgyi E., Bacsi A. Pollen-induced oxidative stress influences both innate and adaptive immune responses via altering dendritic cell functions. J. Immunol. 2010, 184:2377-2385.
11. Dharajiya N., Choudhury B.K., Bacsi A., Boldogh I., Alam R., Sur S. Inhibiting pollen reduced nicotinamide adenine dinucleotide phosphate oxidase-induced signal by intrapulmonary administration of antioxidants blocks allergic airway inflammation. J. Allergy Clin. Immunol. 2007, 119:646-653.
12. Dharajiya N., Vaidya S., Sinha M., Luxon B., Boldogh I., Sur S. Allergen challenge induces Ifng dependent GTPases in the lungs as part of a Th1 transcriptome response in a murine model of allergic asthma. PLoS ONE 2009, 4:e8172.
13. Aguilera-Aguirre L., Bacsi A., Saavedra-Molina A., Kurosky A., Sur S., Boldogh I. Mitochondrial dysfunction increases allergic airway inflammation. J. Immunol. 2009, 183:5379-5387.
14. Dizdaroglu M. Oxidative damage to DNA in mammalian chromatin. Mutat. Res. 1992, 275:331-342.
15. Steenken S., Jovanovic S.V. How easily oxidizable is DNA?. One-electron reduction potentials of adenosine and guanosine radicals in aqueous solution. J. Am. Chem. Soc. 1997, 119:617-618.
16. Chan S.W., Dedon P.C. The biological and metabolic fates of endogenous DNA damage products. J. Nucleic Acids 2010, 2010:929047.
17. Dedon P.C., DeMott M.S., Elmquist C.E., Prestwich E.G., McFaline J.L., Pang B. Challenges in developing DNA and RNA biomarkers of inflammation. Biomark Med 2007, 1:293-312.
18. Radak Z., Boldogh I. 8-Oxo-7, 8-dihydroguanine: links to gene expression, aging, and defense against oxidative stress. Free Radic. Biol. Med. 2010, 49:587-596.
19. Mitra S., Hazra T.K., Roy R., Ikeda S., Biswas T., Lock J., Boldogh I., Izumi T. Complexities of DNA base excision repair in mammalian cells. Mol. Cells 1997, 7:305-312.
20. Hegde H.P.M.L., Rao K.S., Mitra S. Oxidative genome damage and its repair in neurodegenerative diseases: function of transition metals as a double-edged sword. J. Alzheimers Dis. 2011, 24:183-198.
21. Nishimura S. Involvement of mammalian OGG1(MMH) in excision of the 8-hydroxyguanine residue in DNA. Free Radic. Biol. Med. 2002, 32:813-821.
22. Izumi T., Wiederhold L.R., Roy G., Roy R., Jaiswal A., Bhakat K.K., Mitra S., Hazra T.K. Mammalian DNA base excision repair proteins: their interactions and role in repair of oxidative DNA damage. Toxicology 2003, 193:43-65.
23. McCullough A.K., Dodson M.L., Lloyd R.S. Initiation of base excision repair: glycosylase mechanisms and structures. Annu. Rev. Biochem. 1999, 68:255-285.
24. Dodson M.L., Michaels M.L., Lloyd R.S. Unified catalytic mechanism for DNA glycosylases. J. Biol. Chem. 1994, 269:32709-32712.
25. Hazra T.K., Izumi T., Boldogh I., Imhoff B., Kow Y.W., Jaruga P., Dizdaroglu M., Mitra S. Identification and characterization of a human DNA glycosylase for repair of modified bases in oxidatively damaged DNA. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:3523-3528.
26. Hazra T.K., Kow Y.W., Hatahet Z., Imhoff B., Boldogh I., Mokkapati S.K., Mitra S., Izumi T. Identification and characterization of a novel human DNA glycosylase for repair of cytosine-derived lesions. J. Biol. Chem. 2002, 277:30417-30420.
27. Holgate S.T. The sentinel role of the airway epithelium in asthma pathogenesis. Immunol. Rev. 2011, 242:205-219.
28. Swamy M., Jamora C., Havran W., Hayday A. Epithelial decision makers: in search of the 'epimmunome'. Nat. Immunol. 2010, 11:656-665.
29. Locksley R.M. Asthma and allergic inflammation. Cell 2010, 140:777-783.
30. Klungland A., Rosewell I., Hollenbach S., Larsen E., Daly G., Epe B., Seeberg E., Lindahl T., Barnes D.E. Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:13300-13305.
31. Bacsi A., Chodaczek G., Hazra T.K., Konkel D., Boldogh I. Increased ROS generation in subsets of OGG1 knockout fibroblast cells. Mech. Ageing Dev. 2007, 128:637-649.
32. Davidson D.J., Gray M.A., Kilanowski F.M., Tarran R., Randell S.H., Sheppard D.N., Argent B.E., Dorin J.R. Murine epithelial cells: isolation and culture. J. Cyst. Fibros. 2004, 3(Suppl. 2):59-62.
33. Knaapen A.M., Seiler F., Schilderman P.A., Nehls P., Bruch J., Schins R.P., Borm P.J. Neutrophils cause oxidative DNA damage in alveolar epithelial cells. Free Radic. Biol. Med. 1999, 27:234-240.
34. Das A., Hazra T.K., Boldogh I., Mitra S., Bhakat K.K. Induction of the human oxidized base-specific DNA glycosylase NEIL1 by reactive oxygen species. J. Biol. Chem. 2005, 280:35272-35280.
35. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
36. Olive P.L., Wlodek D., Banath J.P. DNA double-strand breaks measured in individual cells subjected to gel electrophoresis. Cancer Res. 1991, 51:4671-4676.
37. Bacsi A., Kannan S., Lee M.S., Hazra T.K., Boldogh I. Modulation of DNA-dependent protein kinase activity in chlorambucil-treated cells. Free Radic. Biol. Med. 2005, 39:1650-1659.
38. Maiti A.K., Boldogh I., Spratt H., Mitra S., Hazra T.K. Mutator phenotype of mammalian cells due to deficiency of NEIL1 DNA glycosylase, an oxidized base-specific repair enzyme. DNA Repair (Amst.) 2008, 7:1213-1220.
39. Bhakat K.K., Mokkapati S.K., Boldogh I., Hazra T.K., Mitra S. Acetylation of human 8-oxoguanine-DNA glycosylase by p300 and its role in 8-oxoguanine repair in vivo. Mol. Cell. Biol. 2006, 26:1654-1665.
40. Taube C., Dakhama A., Rha Y.H., Takeda K., Joetham A., Park J.W., Balhorn A., Takai T., Poch K.R., Nick J.A., Gelfand E.W. Transient neutrophil infiltration after allergen challenge is dependent on specific antibodies and Fc gamma III receptors. J. Immunol. 2003, 170:4301-4309.
41. Knaapen A.M., Gungor N., Schins R.P., Borm P.J., Van Schooten F.J. Neutrophils and respiratory tract DNA damage and mutagenesis: a review. Mutagenesis 2006, 21:225-236.
42. Izumi T., Schein C.H., Oezguen N., Feng Y., Braun W. Effects of backbone contacts 3' to the abasic site on the cleavage and the product binding by human apurinic/apyrimidinic endonuclease (APE1). Biochemistry 2004, 43:684-689.
43. Mitra S., Izumi T., Boldogh I., Bhakat K.K., Hill J.W., Hazra T.K. Choreography of oxidative damage repair in mammalian genomes. Free Radic. Biol. Med. 2002, 33:15-28.
44. Alam R., Gorska M.M. Mitogen-activated protein kinase signalling and ERK1/2 bistability in asthma. Clin. Exp. Allergy 2011, 41:149-159.
45. Cadet J., Douki T., Ravanat J.L. One-electron oxidation of DNA and inflammation processes. Nat. Chem. Biol. 2006, 2:348-349.
46. Reynaert N.L. Glutathione biochemistry in asthma. Biochim. Biophys. Acta 2011, 1810:1045-1051.
47. Hill J.W., Hazra T.K., Izumi T., Mitra S. Stimulation of human 8-oxoguanine-DNA glycosylase by AP-endonuclease: potential coordination of the initial steps in base excision repair. Nucleic Acids Res. 2001, 29:430-438.
48. Gungor N., Haegens A., Knaapen A.M., Godschalk R.W., Chiu R.K., Wouters E.F., van Schooten F.J. Lung inflammation is associated with reduced pulmonary nucleotide excision repair in vivo. Mutagenesis 2010, 25:77-82.
49. Izumi T., Hazra T.K., Boldogh I., Tomkinson A.E., Park M.S., Ikeda S., Mitra S. Requirement for human AP endonuclease 1 for repair of 3'-blocking damage at DNA single-strand breaks induced by reactive oxygen species. Carcinogenesis 2000, 21:1329-1334.
50. Sidorenko V.S., Nevinsky G.A., Zharkov D.O. Mechanism of interaction between human 8-oxoguanine-DNA glycosylase and AP endonuclease. DNA Repair (Amst.) 2007, 6:317-328.
51. Freund A., Patil C.K., Campisi J. p38MAPK is a novel DNA damage response-independent regulator of the senescence-associated secretory phenotype. EMBO J. 2011, 30:1536-1548.
52. Jamaluddin M., Wang S., Boldogh I., Tian B., Brasier A.R. TNF-alpha-induced NF-kappaB/RelA Ser(276) phosphorylation and enhanceosome formation is mediated by an ROS-dependent PKAc pathway. Cell Signal. 2007, 19:1419-1433.
53. Yang Y., Xia F., Hermance N., Mabb A., Simonson S., Morrissey S., Gandhi P., Munson M., Miyamoto S., Kelliher M.A. A cytosolic ATM/NEMO/RIP1 complex recruits TAK1 to mediate the NF-kappaB and p38 mitogen-activated protein kinase (MAPK)/MAPK-activated protein 2 responses to DNA damage. Mol. Cell. Biol. 2011, 31:2774-2786.
54. Biton S., Ashkenazi A. NEMO and RIP1 control cell fate in response to extensive DNA damage via TNF-alpha feedforward signaling. Cell 2011, 145:92-103.
55. Hadian K., Krappmann D. Signals from the nucleus: activation of NF-kappaB by cytosolic ATM in the DNA damage response. Sci. Signal. 2011, 4:pe2.
56. Oumouna M., Datta R., Oumouna-Benachour K., Suzuki Y., Hans C., Matthews K., Fallon K., Boulares H. Poly(ADP-ribose) polymerase-1 inhibition prevents eosinophil recruitment by modulating Th2 cytokines in a murine model of allergic airway inflammation: a potential specific effect on IL-5. J. Immunol. 2006, 177:6489-6496.
57. Caldecott K.W. Single-strand break repair and genetic disease. Nat. Rev. Genet. 2008, 9:619-631.
58. Westbrook A.M., Schiestl R.H. Atm-deficient mice exhibit increased sensitivity to dextran sulfate sodium-induced colitis characterized by elevated DNA damage and persistent immune activation. Cancer Res. 2010, 70:1875-1884.
59. Marichal T., Ohata K., Bedoret D., Mesnil C., Sabatel C., Kobiyama K., Lekeux P., Coban C., Akira S., Ishii K.J., Bureau F., Desmet C.J. DNA released from dying host cells mediates aluminum adjuvant activity. Nat. Med. 2011, 17:996-1002.
60. Fortoul T.I., Valverde M., Lopez Mdel C., Bizarro P., Lopez I., Sanchez I., Colin-Barenque L., Avila-Costa M.R., Rojas E., Ostrosky-Shejet P. Single-cell gel electrophoresis assay of nasal epithelium and leukocytes from asthmatic and nonasthmatic subjects in Mexico City. Arch. Environ. Health 2003, 58:348-352.
61. Vartanian V., Lowell B., Minko I.G., Wood T.G., Ceci J.D., George S., Ballinger S.W., Corless C.L., McCullough A.K., Lloyd R.S. The metabolic syndrome resulting from a knockout of the NEIL1 DNA glycosylase. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:1864-1869.
62. Banerjee D., Mandal S.M., Das A., Hegde M.L., Das S., Bhakat K.K., Boldogh I., Sarkar P.S., Mitra S., Hazra T.K. Preferential repair of oxidized base damage in the transcribed genes of mammalian cells. J. Biol. Chem. 2011, 286:6006-6016.
63. Osborn O., Olefsky J.M. The cellular and signaling networks linking the immune system and metabolism in disease. Nat. Med. 2012, 18:363-374.
64. Mabley J.G., Pacher P., Deb A., Wallace R., Elder R.H., Szabo C. Potential role for 8-oxoguanine DNA glycosylase in regulating inflammation. FASEB J. 2005, 19:290-292.
65. Li G., Yuan K., Yan C., Fox J., Gaid M., Breitwieser W., Bansal A.K., Zeng H., Gao H., Wu M. 8-Oxoguanine-DNA glycosylase 1 deficiency modifies allergic airway inflammation by regulating STAT6 and IL-4 in cells and in mice. Free Radic. Biol. Med. 2012, 52:392-401.