P52 overexpression increases epithelial apoptosis, enhances lung injury, and reduces survival after lipopolysaccharide treatment

Journal of Immunology

Volumn 196, Issue 4, 2016, Pages 1891-1899

  Saxon, Jamie A ^a   Cheng, Dong Sheng ^b   Han, Wei ^b   Polosukhin, Vasiliy V ^b   McLoed, Allyson G ^a   Richmond, Bradley W ^a,b   Gleaves, Linda A ^b   Tanjore, Harikrishna ^b   Sherrill, Taylor P ^b   Barham, Whitney ^a   Yull, Fiona E ^a   Blackwell, Timothy S ^a,b,c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN P100; LIPOPOLYSACCHARIDE;

ADULT RESPIRATORY DISTRESS SYNDROME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL STRESS; CELL SURVIVAL; CLARA CELL; CONTROLLED STUDY; EPITHELIUM CELL; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LUNG INJURY; MORTALITY; MOUSE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RESPIRATORY EPITHELIUM; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; RESPIRATORY MUCOSA; TRANSGENIC MOUSE; UPREGULATION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMMUNOHISTOCHEMISTRY; LIPOPOLYSACCHARIDES; MICE; MICE, TRANSGENIC; NF-KAPPA B P52 SUBUNIT; PNEUMONIA; REAL-TIME POLYMERASE CHAIN REACTION; RESPIRATORY DISTRESS SYNDROME, ADULT; RESPIRATORY MUCOSA; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84958576266     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501555     Document Type: Article

References (32)

1. Caamanõ, J. H., C. A. Rizzo, S. K. Durham, D. S. Barton, C. Raventós-Suárez, C. M. Snapper, and R. Bravo. 1998. Nuclear factor (NF)-k B2 (p100/p52) is required for normal splenic microarchitecture and B cell-mediated immune responses. J. Exp. Med. 187: 185-196.
2. Franzoso, G., L. Carlson, L. Poljak, E. W. Shores, S. Epstein, A. Leonardi, A. Grinberg, T. Tran, T. Scharton-Kersten, M. Anver, et al. 1998. Mice deficient in nuclear factor (NF)-kB/p52 present with defects in humoral responses, germinal center reactions, and splenic microarchitecture. J. Exp. Med. 187: 147-159.
3. Weih, F., D. Carrasco, S. K. Durham, D. S. Barton, C. A. Rizzo, R.-P. Ryseck, S. A. Lira, and R. Bravo. 1995. Multiorgan inflammation and hematopoietic abnormalities in mice with a targeted disruption of RelB, a member of the NF-k B/Rel family. Cell 80: 331-340.
4. Dejardin, E., N. M. Droin, M. Delhase, E. Haas, Y. Cao, C. Makris, Z.-W. Li, M. Karin, C. F. Ware, and D. R. Green. 2002. The lymphotoxin-b receptor induces different patterns of gene expression via two NF-kappaB pathways. Immunity 17: 525-535.
5. Weih, D. S., Z. B. Yilmaz, and F. Weih. 2001. Essential role of RelB in germinal center and marginal zone formation and proper expression of homing chemokines. J. Immunol. 167: 1909-1919.
6. Cheng, D.-S., W. Han, S. M. Chen, T. P. Sherrill, M. Chont, G.-Y. Park, J. R. Sheller, V. V. Polosukhin, J. W. Christman, F. E. Yull, and T. S. Blackwell. 2007. Airway epithelium controls lung inflammation and injury through the NFkB pathway. J. Immunol. 178: 6504-6513.
7. Tully, J. E., J. D. Nolin, A. S. Guala, S. M. Hoffman, E. C. Roberson, K. G. Lahue, J. van der Velden, V. Anathy, T. S. Blackwell, and Y. M. Janssen-Heininger. 2012. Cooperation between classical and alternative NF-kB pathways regulates proinflammatory responses in epithelial cells. Am. J. Respir. Cell Mol. Biol. 47: 497-508.
8. Zhu, Z., B. Ma, R. J. Homer, T. Zheng, and J. A. Elias. 2001. Use of the tetracycline-controlled transcriptional silencer (tTS) to eliminate transgene leak in inducible overexpression transgenic mice. J. Biol. Chem. 276: 25222-25229.
9. Tichelaar, J. W., W. Lu, and J. A. Whitsett. 2000. Conditional expression of fibroblast growth factor-7 in the developing and mature lung. J. Biol. Chem. 275: 11858-11864.
10. Zaynagetdinov, R., G. T. Stathopoulos, T. P. Sherrill, D.-S. Cheng, A. G. McLoed, J. A. Ausborn, V. V. Polosukhin, L. Connelly, W. Zhou, B. Fingleton, et al. 2012. Epithelial nuclear factor-kB signaling promotes lung carcinogenesis via recruitment of regulatory T lymphocytes. Oncogene 31: 3164-3176.
11. Stathopoulos, G. T., T. P. Sherrill, D.-S. Cheng, R. M. Scoggins, W. Han, V. V. Polosukhin, L. Connelly, F. E. Yull, B. Fingleton, and T. S. Blackwell. 2007. Epithelial NF-kappaB activation promotes urethane-induced lung carcinogenesis. Proc. Natl. Acad. Sci. USA 104: 18514-18519.
12. Lawson, W. E., V. V. Polosukhin, G. T. Stathopoulos, O. Zoia, W. Han, K. B. Lane, B. Li, E. F. Donnelly, G. E. Holburn, K. G. Lewis, et al. 2005. Increased and prolonged pulmonary fibrosis in surfactant protein C-deficient mice following intratracheal bleomycin. Am. J. Pathol. 167: 1267-1277.
13. Petty, J. M., V. Sueblinvong, C. C. Lenox, C. C. Jones, G. P. Cosgrove, C. D. Cool, P. R. Rai, K. K. Brown, D. J. Weiss, M. E. Poynter, and B. T. Suratt. 2007. Pulmonary stromal-derived factor-1 expression and effect on neutrophil recruitment during acute lung injury. J. Immunol. 178: 8148-8157.
14. Hojgaard, A., R. Close, D. M. Dunn, R. B. Weiss, J. J. Weis, and J. H. Weis. 2006. Altered localization of CXCL13 expressing cells in mice deficient in Pactolus following an inflammatory stimulus. Immunology 119: 212-223.
15. Proietto, A. I., S. van Dommelen, P. Zhou, A. Rizzitelli, A. D'Amico, R. J. Steptoe, S. H. Naik, M. H. Lahoud, Y. Liu, P. Zheng, et al. 2008. Dendritic cells in the thymus contribute to T-regulatory cell induction. Proc. Natl. Acad. Sci. USA 105: 19869-19874.
16. Blackwell, T. S., L. H. Lancaster, T. R. Blackwell, A. Venkatakrishnan, and J. W. Christman. 1999. Differential NF-kB activation after intratracheal endotoxin. Am. J. Physiol. 277: L823-L830.
17. Solan, N. J., H. Miyoshi, E. M. Carmona, G. D. Bren, and C. V. Paya. 2002. RelB cellular regulation and transcriptional activity are regulated by p100. J. Biol. Chem. 277: 1405-1418.
18. Coope, H. J., P. G. Atkinson, B. Huhse, M. Belich, J. Janzen, M. J. Holman, G. G. B. Klaus, L. H. Johnston, and S. C. Ley. 2002. CD40 regulates the processing of NF-kB2 p100 to p52. EMBO J. 21: 5375-5385.
19. McMillan, D. H., C. J. Baglole, T. H. Thatcher, S. Maggirwar, P. J. Sime, and R. P. Phipps. 2011. Lung-targeted overexpression of the NF-kB member RelB inhibits cigarette smoke-induced inflammation. Am. J. Pathol. 179: 125-133.
20. Iannetti, A., A. C. Ledoux, S. J. Tudhope, H. Sellier, B. Zhao, S. Mowla, A. Moore, H. Hummerich, B. E. Gewurz, S. J. Cockell, et al. 2014. Regulation of p53 and Rb links the alternative NF-kB pathway to EZH2 expression and cell senescence. PLoS Genet. 10: e1004642.
21. Nadiminty, N., J. Y. Chun, W. Lou, X. Lin, and A. C. Gao. 2008. NF-kB2/p52 enhances androgen-independent growth of human LNCaP cells via protection from apoptotic cell death and cell cycle arrest induced by androgen-deprivation. Prostate 68: 1725-1733.
22. Connelly, L., C. Robinson-Benion, M. Chont, L. Saint-Jean, H. Li, V. V. Polosukhin, T. S. Blackwell, and F. E. Yull. 2007. A transgenic model reveals important roles for the NF-kB alternative pathway (p100/p52) in mammary development and links to tumorigenesis. J. Biol. Chem. 282: 10028-10035.
23. Ishikawa, H., D. Carrasco, E. Claudio, R.-P. Ryseck, and R. Bravo. 1997. Gastric hyperplasia and increased proliferative responses of lymphocytes in mice lacking the COOH-terminal ankyrin domain of NF-kB2. J. Exp. Med. 186: 999-1014.
24. Neff, S. B., B. R. Z'graggen, T. A. Neff, M. Jamnicki-Abegg, D. Suter, R. C. Schimmer, C. Booy, H. Joch, T. Pasch, P. A. Ward, and B. Beck-Schimmer. 2006. Inflammatory response of tracheobronchial epithelial cells to endotoxin. Am. J. Physiol. Lung Cell. Mol. Physiol. 290: L86-L96.
25. Vernooy, J. H., M. A. Dentener, R. J. van Suylen, W. A. Buurman, and E. F. Wouters. 2001. Intratracheal instillation of lipopolysaccharide in mice induces apoptosis in bronchial epithelial cells: no role for tumor necrosis factor-A and infiltrating neutrophils. Am. J. Respir. Cell Mol. Biol. 24: 569-576.
26. Kawasaki, M., K. Kuwano, N. Hagimoto, T. Matsuba, R. Kunitake, T. Tanaka, T. Maeyama, and N. Hara. 2000. Protection from lethal apoptosis in lipopolysaccharide-induced acute lung injury in mice by a caspase inhibitor. Am. J. Pathol. 157: 597-603.
27. Bardales, R. H., S.-S. Xie, R. F. Schaefer, and S.-M. Hsu. 1996. Apoptosis is a major pathway responsible for the resolution of type II pneumocytes in acute lung injury. Am. J. Pathol. 149: 845-852.
28. Guinee, D., Jr., M. Fleming, T. Hayashi, M. Woodward, J. Zhang, J. Walls, M. Koss, V. Ferrans, and W. Travis. 1996. Association of p53 and WAF1 expression with apoptosis in diffuse alveolar damage. Am. J. Pathol. 149: 531-538.
29. Lee, K. S., Y. H. Choi, Y. S. Kim, S. H. Baik, Y. J. Oh, S. S. Sheen, J. H. Park, S. C. Hwang, and K. J. Park. 2008. Evaluation of bronchoalveolar lavage fluid from ARDS patients with regard to apoptosis. Respir. Med. 102: 464-469.
30. Albertine, K. H., M. F. Soulier, Z. Wang, A. Ishizaka, S. Hashimoto, G. A. Zimmerman, M. A. Matthay, and L. B. Ware. 2002. Fas and fas ligand are up-regulated in pulmonary edema fluid and lung tissue of patients with acute lung injury and the acute respiratory distress syndrome. Am. J. Pathol. 161: 1783-1796.
31. Galani, V., E. Tatsaki, M. Bai, P. Kitsoulis, M. Lekka, G. Nakos, and P. Kanavaros. 2010. The role of apoptosis in the pathophysiology of Acute Respiratory Distress Syndrome (ARDS): an up-to-date cell-specific review. Pathol. Res. Pract. 206: 145-150.
32. Matthay, M. A., and J. P. Wiener-Kronish. 1990. Intact epithelial barrier function is critical for the resolution of alveolar edema in humans. Am. Rev. Respir. Dis. 142: 1250-1257.