Nrf2 modulates host defense during streptococcus pneumoniae pneumonia in mice

Journal of Immunology

Volumn 197, Issue 7, 2016, Pages 2864-2879

  Gomez, John C ^a,b   Dang, Hong ^b   Martin, Jessica R ^a,b   Doerschuk, Claire M ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR; INTERLEUKIN 12P70; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR; NFE2L2 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL TRANSMISSION; CARBOXY TERMINAL SEQUENCE; CELL MIGRATION; COMPLEMENT ACTIVATION; CONTROLLED STUDY; DISEASE SEVERITY; DOWN REGULATION; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; HOST RESISTANCE; MORTALITY RATE; MOUSE; NEUTROPHIL; NONHUMAN; OXIDATIVE STRESS; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REDOX STRESS; STREPTOCOCCUS PNEUMONIA; STREPTOCOCCUS PNEUMONIAE; SURVIVAL RATE; UPREGULATION; ANIMAL; C57BL MOUSE; DEFICIENCY; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY;

ANIMALS; APOPTOSIS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; NF-E2-RELATED FACTOR 2; PNEUMONIA, PNEUMOCOCCAL; STREPTOCOCCUS PNEUMONIAE;

EID: 84989956131     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1600043     Document Type: Article

References (29)

1. Nguyen, T., P. J. Sherratt, H. C. Huang, C. S. Yang, and C. B. Pickett. 2003. Increased protein stability as a mechanism that enhances Nrf2-mediated transcriptional activation of the antioxidant response element. Degradation of Nrf2 by the 26 S proteasome. J. Biol. Chem. 278: 4536-4541.
2. Ma, Q. 2013. Role of nrf2 in oxidative stress and toxicity. Annu. Rev. Pharmacol. Toxicol. 53: 401-426.
3. Cho, H. Y., and S. R. Kleeberger. 2015. Association of Nrf2 with airway pathogenesis: lessons learned from genetic mouse models. Arch. Toxicol. 89: 1931- 1957.
4. Thimmulappa, R. K., H. Lee, T. Rangasamy, S. P. Reddy, M. Yamamoto, T. W. Kensler, and S. Biswal. 2006. Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J. Clin. Invest. 116: 984-995.
5. Kong, X., R. Thimmulappa, P. Kombairaju, and S. Biswal. 2010. NADPH oxidase-dependent reactive oxygen species mediate amplified TLR4 signaling and sepsis-induced mortality in Nrf2-deficient mice. J. Immunol. 185: 569-577.
6. Athale, J., A. Ulrich, N. C. MacGarvey, R. R. Bartz, K. E. Welty-Wolf, H. B. Suliman, and C. A. Piantadosi. 2012. Nrf2 promotes alveolar mitochondrial biogenesis and resolution of lung injury in Staphylococcus aureus pneumonia in mice. Free Radic. Biol. Med. 53: 1584-1594.
7. Chang, A. L., A. Ulrich, H. B. Suliman, and C. A. Piantadosi. 2015. Redox regulation of mitophagy in the lung during murine Staphylococcus aureus sepsis. Free Radic. Biol. Med. 78: 179-189.
8. Harvey, C. J., R. K. Thimmulappa, S. Sethi, X. Kong, L. Yarmus, R. H. Brown, D. Feller-Kopman, R. Wise, and S. Biswal. 2011. Targeting Nrf2 signaling improves bacterial clearance by alveolar macrophages in patients with COPD and in a mouse model. Sci. Transl. Med. 3: 78ra32.
9. Reddy, N. M., V. Suryanarayana, D. V. Kalvakolanu, M. Yamamoto, T. W. Kensler, P. M. Hassoun, S. R. Kleeberger, and S. P. Reddy. 2009. Innate immunity against bacterial infection following hyperoxia exposure is impaired in NRF2-deficient mice. J. Immunol. 183: 4601-4608.
10. Yamada, M., J. C. Gomez, P. E. Chugh, C. A. Lowell, M. C. Dinauer, D. P. Dittmer, and C. M. Doerschuk. 2011. Interferon-g production by neutrophils during bacterial pneumonia in mice. Am. J. Respir. Crit. Care Med. 183: 1391-1401.
11. Itoh, K., T. Chiba, S. Takahashi, T. Ishii, K. Igarashi, Y. Katoh, T. Oyake, N. Hayashi, K. Satoh, I. Hatayama, et al. 1997. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 236: 313-322.
12. Subramanian, A., P. Tamayo, V. K. Mootha, S. Mukherjee, B. L. Ebert, M. A. Gillette, A. Paulovich, S. L. Pomeroy, T. R. Golub, E. S. Lander, and J. P. Mesirov. 2005. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102: 15545-15550.
13. Mootha, V. K., C. M. Lindgren, K. F. Eriksson, A. Subramanian, S. Sihag, J. Lehar, P. Puigserver, E. Carlsson, M. Ridderstrale, E. Laurila, et al. 2003. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34: 267-273.
14. Cho, H. Y., and S. R. Kleeberger. 2010. Nrf2 protects against airway disorders. Toxicol. Appl. Pharmacol. 244: 43-56.
15. Malhotra, D., E. Portales-Casamar, A. Singh, S. Srivastava, D. Arenillas, C. Happel, C. Shyr, N. Wakabayashi, T. W. Kensler, W. W. Wasserman, and S. Biswal. 2010. Global mapping of binding sites for Nrf2 identifies novel targets in cell survival response through ChIP-Seq profiling and network analysis. Nucleic Acids Res. 38: 5718-5734.
16. van Faassen, H., R. KuoLee, G. Harris, X. Zhao, J. W. Conlan, and W. Chen. 2007. Neutrophils play an important role in host resistance to respiratory infection with Acinetobacter baumannii in mice. Infect. Immun. 75: 5597-5608.
17. Huet, O., D. Ramsey, S. Miljavec, A. Jenney, C. Aubron, A. Aprico, N. Stefanovic, B. Balkau, G. A. Head, J. B. de Haan, and J. P. Chin-Dusting. 2013. Ensuring animal welfare while meeting scientific aims using a murine pneumonia model of septic shock. Shock 39: 488-494.
18. Sumi, D., Y. Shimizu, and S. Himeno. 2013. Involvement of Nrf2 activation in the upregulation of S100A9 by exposure to inorganic arsenite. Int. J. Mol. Med. 31: 259-264.
19. Chorley, B. N., M. R. Campbell, X. Wang, M. Karaca, D. Sambandan, F. Bangura, P. Xue, J. Pi, S. R. Kleeberger, and D. A. Bell. 2012. Identification of novel NRF2-regulated genes by ChIP-Seq: influence on retinoid X receptor alpha. Nucleic Acids Res. 40: 7416-7429.
20. Bartlett, J. G. 2011. Diagnostic tests for agents of community-Acquired pneumonia. Clin. Infect. Dis. 52(Suppl. 4): S296-S304.
21. Jain, S., W. H. Self, and R. G. Wunderink, CDC EPIC Study Team. 2015. Community-Acquired pneumonia requiring hospitalization. N. Engl. J. Med. 373: 2382.
22. Kong, X., R. Thimmulappa, F. Craciun, C. Harvey, A. Singh, P. Kombairaju, S. P. Reddy, D. Remick, and S. Biswal. 2011. Enhancing Nrf2 pathway by disruption of Keap1 in myeloid leukocytes protects against sepsis. Am. J. Respir. Crit. Care Med. 184: 928-938.
23. Hayes, J. D., and M. McMahon. 2006. The double-edged sword of Nrf2: subversion of redox homeostasis during the evolution of cancer. Mol. Cell 21: 732-734.
24. Sporn, M. B., and K. T. Liby. 2012. NRF2 and cancer: The good, the bad and the importance of context. Nat. Rev. Cancer 12: 564-571.
25. Davidson, B. A., R. R. Vethanayagam, M. J. Grimm, B. A. Mullan, K. Raghavendran, T. S. Blackwell, M. L. Freeman, V. Ayyasamy, K. K. Singh, M. B. Sporn, et al. 2013. NADPH oxidase and Nrf2 regulate gastric aspirationinduced inflammation and acute lung injury. J. Immunol. 190: 1714-1724.
26. Segal, B. H., W. Han, J. J. Bushey, M. Joo, Z. Bhatti, J. Feminella, C. G. Dennis, R. R. Vethanayagam, F. E. Yull, M. Capitano, et al. 2010. NADPH oxidase limits innate immune responses in the lungs in mice. PLoS One 5: e9631.
27. Thimmulappa, R. K., K. H. Mai, S. Srisuma, T. W. Kensler, M. Yamamoto, and S. Biswal. 2002. Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res. 62: 5196-5203.
28. Warburton, D., D. Tefft, A. Mailleux, S. Bellusci, J. P. Thiery, J. Zhao, S. Buckley, W. Shi, and B. Driscoll. 2001. Do lung remodeling, repair, and regeneration recapitulate respiratory ontogeny? Am. J. Respir. Crit. Care Med. 164: S59-S62.
29. Whitsett, J. A., H. M. Haitchi, and Y. Maeda. 2011. Intersections between pulmonary development and disease. Am. J. Respir. Crit. Care Med. 184: 401-406.