The NRF2 activation and antioxidative response are not impaired overall during hyperoxia-induced lung epithelial cell death

Oxidative Medicine and Cellular Longevity

Volumn , Issue , 2013, Pages

  Potteti, Haranatha R ^a   Reddy, Narsa M ^a   Hei, Tom K ^b   Kalvakolanu, Dhananjaya V ^c   Reddy, Sekhar P ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b Department of Medicine   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE LUNG INJURY; ANTIOXIDATIVE RESPONSE; CHROMATIN IMMUNOPRECIPITATION ASSAY; EXPRESSION LEVELS; LUNG EPITHELIAL CELLS; NUCLEAR ACCUMULATION; RESPIRATORY DISTRESS SYNDROME; TARGET GENE EXPRESSION;

BIOLOGICAL ORGANS; CHEMICAL COMPOUNDS; ENDOTHELIAL CELLS; GENE EXPRESSION; OXIDANTS;

CELL DEATH;

TRANSCRIPTION FACTOR NRF2; ANTIOXIDANT; HEME OXYGENASE 1; HMOX1 PROTEIN, HUMAN; NQO1 PROTEIN, HUMAN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE);

ARTICLE; CELL DEATH; CELL NUCLEUS; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPEROXIA; LUNG ALVEOLUS EPITHELIUM; CELL SURVIVAL; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; LUNG; METABOLISM; PATHOLOGY; PROMOTER REGION; PROTEIN BINDING;

ANTIOXIDANTS; CELL DEATH; CELL NUCLEUS; CELL SURVIVAL; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HEME OXYGENASE-1; HUMANS; HYPEROXIA; LUNG; NAD(P)H DEHYDROGENASE (QUINONE); NF-E2-RELATED FACTOR 2; PROMOTER REGIONS, GENETIC; PROTEIN BINDING;

EID: 84878336762     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2013/798401     Document Type: Article

References (47)

1. Ho Y. S., Vincent R., Dey M. S., Slot J. W., Crapo J. D., Transgenic models for the study of lung antioxidant defense: enhanced manganese-containing superoxide dismutase activity gives partial protection to b6c3 hybrid mice exposed to hyperoxia. American Journal of Respiratory Cell and Molecular Biology 1998 18 4 538 547 2-s2.0-0032036316 (Pubitemid 128353628)
2. Lee P. J., Choi A. M. K., Pathways of cell signaling in hyperoxia. Free Radical Biology and Medicine 2003 35 4 341 350 2-s2.0-0142011659 10.1016/S0891-5849(03)00279-X (Pubitemid 37289165)
3. Saugstad O. D., Bronchopulmonary dysplasia-oxidative stress and antioxidants. Seminars in Neonatology 2003 8 1 39 49 2-s2.0-0037300018 10.1016/S1084-2756(02)00194-X (Pubitemid 36356492)
4. Fridovich I., Oxygen toxicity: a radical explanation. Journal of Experimental Biology 1998 201 8 1203 1209 2-s2.0-0032053161 (Pubitemid 28278324)
5. Halliwell B., Gutteridge J. M. C., Cross C. E., Free radicals, antioxidants, and human disease: where are we now? Journal of Laboratory and Clinical Medicine 1992 119 6 598 620 2-s2.0-0026636441
6. MacNee W., Rahman I., Is oxidative stress central to the pathogenesis of chronic obstructive pulmonary disease? Trends in Molecular Medicine 2000 7 2 55 62 2-s2.0-0034474704 10.1016/S1471-4914(01)01912-8 (Pubitemid 32194683)
7. Crapo J. D., Morphologic changes in pulmonary oxygen toxicity. Annual Review of Physiology 1986 48 721 731 2-s2.0-0022559220 (Pubitemid 16047645)
8. Cho H. Y., Jedlicka A. E., Reddy S. P. M., Kensler T. W., Yamamoto M., Zhang L. Y., Kleeberger S. R., Role of NRF2 in protection against hyperoxic lung injury in mice. American Journal of Respiratory Cell and Molecular Biology 2002 26 2 175 182 2-s2.0-0036007313 (Pubitemid 34107870)
9. Cho H. Y., Jedlicka A. E., Reddy S. P. M., Zhang L. Y., Kensler T. W., Kleeberger S. R., Linkage analysis of susceptibility to hyperoxia Nrf2 is a candidate gene. American Journal of Respiratory Cell and Molecular Biology 2002 26 1 42 51 2-s2.0-0036006792 (Pubitemid 34029819)
10. Reddy N. M., Suryanarayana V., Kalvakolanu D. V., Yamamoto M., Kensler T. W., Hassoun P. M., Kleeberger S. R., Reddy S. P., Innate immunity against bacterial infection following hyperoxia exposure is impaired in NRF2-deficient mice. Journal of Immunology 2009 183 7 4601 4608 2-s2.0-70449723401 10.4049/jimmunol.0901754
11. Cho H. Y., van Houten B., Wang X., Miller-DeGraff L., Fostel J., Gladwell W., Perrow L., Panduri V., Kobzik L., Yamamoto M., Bell D. A., Kleeberger S. R., Targeted deletion of nrf2 impairs lung development and oxidant injury in neonatal mice. Antioxidants and Redox Signaling 2012 17 8 1066 1082
12. McGrath-Morrow S., Lauer T., Yee M., Neptune E., Podowski M., Thimmulappa R. K., O'Reilly M., Biswal S., Nrf2 increases survival and attenuates alveolar growth inhibition in neonatal mice exposed to hyperoxia. American Journal of Physiology 2009 296 4 L565 L573 2-s2.0-65549171199 10.1152/ajplung.90487.2008
13. Reddy N. M., Kleeberger S. R., Cho H. Y., Yamamoto M., Kensler T. W., Biswal S., Reddy S. P., Deficiency in Nrf2 GSH signaling impairs type II cell growth and enhances sensitivity to oxidants. American Journal of Respiratory Cell and Molecular Biology 2007 37 1 3 8 2-s2.0-34347222551 10.1165/rcmb.2007- 0004RC (Pubitemid 46999531)
14. Papaiahgari S., Kleeberger S. R., Cho H. Y., Kalvakolanu D. V., Reddy S. P., NADPH oxidase and ERK signaling regulates hyperoxia-induced Nrf2-ARE transcriptional response in pulmonary epithelial cells. Journal of Biological Chemistry 2004 279 40 42302 42312 2-s2.0-4744360664 10.1074/jbc.M408275200 (Pubitemid 39313679)
15. Morito N., Yoh K., Itoh K., Hirayama A., Koyama A., Yamamoto M., Takahashi S., Nrf2 regulates the sensitivity of death receptor signals by affecting intracellular glutathione levels. Oncogene 2003 22 58 9275 9281 2-s2.0-1642540092 10.1038/sj.onc.1207024 (Pubitemid 38122039)
16. Cullinan S. B., Zhang D., Hannink M., Arvisais E., Kaufman R. J., Diehl J. A., Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Molecular and Cellular Biology 2003 23 20 7198 7209 2-s2.0-0141752795 10.1128/MCB.23.20.7198-7209.2003 (Pubitemid 37211002)
17. Piao C. Q., Liu L., Zhao Y. L., Balajee A. S., Suzuki M., Hei T. K., Immortalization of human small airway epithelial cells by ectopic expression of telomerase. Carcinogenesis 2005 26 4 725 731 2-s2.0-17844377872 10.1093/carcin/bgi016 (Pubitemid 41214334)
18. Moehlenkamp J. D., Johnson J. A., Activation of antioxidant/electrophile- responsive elements in IMR-32 human neuroblastoma cells. Archives of Biochemistry and Biophysics 1999 363 1 98 106 2-s2.0-0033102622 10.1006/abbi.1998.1046 (Pubitemid 29394335)
19. Singh A., Misra V., Thimmulappa R. K., Lee H., Ames S., Hoque M. O., Herman J. G., Baylin S. B., Sidransky D., Gabrielson E., Brock M. V., Biswal S., Dysfunctional KEAP1-NRF2 interaction in non-small-cell lung cancer. PLoS Medicine 2006 3 10 1865 1876 2-s2.0-33750885385 10.1371/journal.pmed.0030420 (Pubitemid 44721825)
20. Padmanabhan B., Tong K. I., Ohta T., Nakamura Y., Scharlock M., Ohtsuji M., Kang M. I., Kobayashi A., Yokoyama S., Yamamoto M., Structural basis for defects of Keap1 activity provoked by its point mutations in lung cancer. Molecular Cell 2006 21 5 689 700 2-s2.0-33344456501 10.1016/j.molcel.2006.01.013 (Pubitemid 43290735)
21. Suzuki T., Maher J., Yamamoto M., Select heterozygous Keap1 mutations have a dominant-negative effect on wild-type Keap1 in vivo. Cancer Research 2011 71 5 1700 1709 2-s2.0-79952221884 10.1158/0008-5472.CAN-10-2939
22. Kensler T. W., Wakabayashi N., Biswal S., Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annual Review of Pharmacology and Toxicology 2007 47 89 116 2-s2.0-33847050801 10.1146/annurev.pharmtox.46.120604.141046
23. Barazzone C., Horowitz S., Donati Y. R., Rodriguez I., Piguet P. F., Oxygen toxicity in mouse lung: pathways to cell death. American Journal of Respiratory Cell and Molecular Biology 1998 19 4 573 581 2-s2.0-0032185795 (Pubitemid 128354238)
24. Kobayashi M., Yamamoto M., Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxidants and Redox Signaling 2005 7 3-4 385 394 2-s2.0-14044254798 10.1089/ars.2005.7.385 (Pubitemid 40279806)
25. Cho H. Y., Reddy S. P., Kleeberger S. R., Nrf2 defends the lung from oxidative stress. Antioxidants & Redox Signaling 2006 8 1-2 76 87. Review (Pubitemid 43324533)
26. Huang H. C., Nguyen T., Pickett C. B., Regulation of the antioxidant response element by protein kinase C-mediated phosphorylation of NF-E2-related factor 2. Proceedings of the National Academy of Sciences of the United States of America 2000 97 23 12475 12480 2-s2.0-0033731182 10.1073/pnas.220418997
27. Huang H. C., Nguyen T., Pickett C. B., Phosphorylation of Nrf2 at Ser-40 by protein kinase C regulates antioxidant response element-mediated transcription. Journal of Biological Chemistry 2002 277 45 42769 42774 2-s2.0-0037044791 10.1074/jbc.M206911200 (Pubitemid 35285650)
28. Papaiahgari S., Zhang Q., Kleeberger S. R., Cho H. Y., Reddy S. P., Hyperoxia stimulates an Nrf2-ARE transcriptional response via ROS-EGFR-P13K-Akt/ERK MAP kinase signaling in pulmonary epithelial cells. Antioxidants and Redox Signaling 2006 8 1-2 43 52 2-s2.0-33644649422 10.1089/ars.2006.8.43 (Pubitemid 43324529)
29. Lim J. H., Kim K. M., Kim S. W., Hwang O., Choi H. J., Bromocriptine activates NQO1 via Nrf2-PI3K/Akt signaling: novel cytoprotective mechanism against oxidative damage. Pharmacological Research 2008 57 5 325 331 2-s2.0-44549085003 10.1016/j.phrs.2008.03.004
30. Theodore M., Kawai Y., Yang J., Kleshchenko Y., Reddy S. P., Villalta F., Arinze I. J., Multiple nuclear localization signals function in the nuclear import of the transcription factor Nrf2. Journal of Biological Chemistry 2008 283 14 8984 8994 2-s2.0-44049093741 10.1074/jbc.M709040200
31. Kaspar J. W., Jaiswal A. K., Antioxidant-induced phosphorylation of tyrosine 486 leads to rapid nuclear export of Bach1 that allows Nrf2 to bind to the antioxidant response element and activate defensive gene expression. Journal of Biological Chemistry 2010 285 1 153 162 2-s2.0-73649134320 10.1074/jbc.M109.040022
32. Karapetian R. N., Evstafieva A. G., Abaeva I. S., Chichkova N. V., Filonov G. S., Rubtsov Y. P., Sukhacheva E. A., Melnikov S. V., Schneider U., Wanker E. E., Vartapetian A. B., Nuclear oncoprotein prothymosin α is a partner of Keap1: implications for expression of oxidative stress-protecting genes. Molecular and Cellular Biology 2005 25 3 1089 1099 2-s2.0-19944430116 10.1128/MCB.25.3.1089-1099.2005 (Pubitemid 40165815)
33. Gerald D., Berra E., Frapart Y. M., Chan D. A., Giaccia A. J., Mansuy D., Pouysségur J., Yaniv M., Mechta-Grigoriou F., JunD reduces tumor angiogenesis by protecting cells from oxidative stress. Cell 2004 118 6 781 794 2-s2.0-4544346656 10.1016/j.cell.2004.08.025 (Pubitemid 39221736)
34. MacLaren A., Black E. J., Clark W., Gillespie D. A. F., C-Jun-deficient cells undergo premature senescence as a result of spontaneous DNA damage accumulation. Molecular and Cellular Biology 2004 24 20 9006 9018 2-s2.0-4744345878 10.1128/MCB.24.20.9006-9018.2004 (Pubitemid 39313905)
35. Meixner A., Karreth F., Kenner L., Penninger J. M., Wagner E. F., Jun and JunD-dependent functions in cell proliferation and stress response. Cell Death and Differentiation 2010 17 9 1409 1419 2-s2.0-77955712545 10.1038/cdd.2010.22
36. Weitzman J. B., Fiette L., Matsuo K., Yaniv M., JunD protects cells from p53-dependent senescence and apoptosis. Molecular Cell 2000 6 5 1109 1119 2-s2.0-0033634878
37. Igarashi K., Kataoka K., Itoh K., Hayashi N., Nishizawa M., Yamamoto M., Regulation of transcription by dimerization of erythroid factor NF-E2 p45 with small Maf proteins. Nature 1994 367 6463 568 572 2-s2.0-0028118492 10.1038/367568a0 (Pubitemid 24055517)
38. Venugopal R., Jaiswal A. K., Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes. Oncogene 1998 17 24 3145 3156 2-s2.0-0032542213 (Pubitemid 29020810)
39. Dang C. V., O'Donnell K. A., Zeller K. I., Nguyen T., Osthus R. C., Li F., The c-Myc target gene network. Seminars in Cancer Biology 2006 16 4 253 264 2-s2.0-33748171960 10.1016/j.semcancer.2006.07.014 (Pubitemid 44311039)
40. Dhakshinamoorthy S., Jain A. K., Bloom D. A., Jaiswal A. K., Bach1 competes with Nrf2 leading to negative regulation of the antioxidant response element (ARE)-mediated NAD(P)H:quinone oxidoreductase 1 gene expression and induction in response to antioxidants. Journal of Biological Chemistry 2005 280 17 16891 16900 2-s2.0-20444480956 10.1074/jbc.M500166200 (Pubitemid 41389148)
41. Vaz M., Machireddy N., Irving A., Potteti H. R., Chevalier K., Kalvakolanu D., Reddy S. P., Oxidant-induced cell death and Nrf2-dependent antioxidative response are controlled by Fra-1/AP-1. Molecular and Cellular Biology 2012 32 9 1694 1709
42. Greenbaum D., Colangelo C., Williams K., Gerstein M., Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biology 2003 4 9, article 117 2-s2.0-0141920354 10.1186/gb-2003-4-9-117 (Pubitemid 37236319)
43. Ning J. L., Mo L. W., Lai X. N., Low-and high-dose hydrogen peroxide regulation of transcription factor NF-E2-related factor 2. Chinese Medical Journal 2010 123 8 1063 1069 2-s2.0-77951211681 10.3760/cma.j.issn.0366-6999. 2010.08.016
44. Villeneuve N. F., Sun Z., Chen W., Zhang D. D., Nrf2 and p21 regulate the fine balance between life and death by controlling ROS levels. Cell Cycle 2009 8 20 3255 3256 2-s2.0-70350228784
45. Reddy N. M., Kleeberger S. R., Yamamoto M., Kensler T. W., Scollick C., Biswal S., Reddy S. P., Genetic dissection of the Nrf2-dependent redox signaling-regulated transcriptional programs of cell proliferation and cytoprotection. Physiological Genomics 2007 32 1 74 81 2-s2.0-37449000924 10.1152/physiolgenomics.00126.2007
46. Malhotra D., Portales-Casamar E., Singh A., Srivastava S., Arenillas D., Happel C., Shyr C., Wakabayashi N., Kensler T. W., Wasserman W. W., Biswal S., Global mapping of binding sites for Nrf2 identifies novel targets in cell survival response through chip-seq profiling and network analysis. Nucleic Acids Research 2010 38 17 5718 5734 2-s2.0-77957237159 10.1093/nar/gkq212 gkq212
47. Taguchi K., Fujikawa N., Komatsu M., Ishii T., Unno M., Akaike T., Motohashi H., Yamamoto M., Keap1 degradation by autophagy for the maintenance of redox homeostasis. Proceedings of the National Academy of Sciences of the United States of America 2010 109 34 13561 13566