FOXO3 deficiency leads to increased susceptibility to cigarette smoke-induced inflammation, airspace enlargement, and chronic obstructive pulmonary disease

Journal of Immunology

Volumn 187, Issue 2, 2011, Pages 987-998

  Hwang, Jae Woong ^a   Rajendrasozhan, Saravanan ^a   Yao, Hongwei ^a   Chung, Sangwoon ^a   Sundar, Isaac K ^a   Huyck, Heidie L ^a   Pryhuber, Gloria S ^a   Kinnula, Vuokko L ^b   Rahman, Irfan ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

CIGARETTE SMOKE; DNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR FKHRL1;

AIRWAY ENLARGEMENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CHRONIC OBSTRUCTIVE LUNG DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE PREDISPOSITION; DOWN REGULATION; FOXO3 GENE; GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG EMPHYSEMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RESPIRATORY TRACT DISEASE; RESPIRATORY TRACT INFLAMMATION;

ANIMALS; DOWN-REGULATION; FORKHEAD TRANSCRIPTION FACTORS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INFLAMMATION; LUNG; MICE; MICE, 129 STRAIN; MICE, KNOCKOUT; MICE, TRANSGENIC; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; PULMONARY EMPHYSEMA; SMOKING;

EID: 79960527353     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001861     Document Type: Article

References (66)

1. Taraseviciene-Stewart, L., and N. F. Voelkel. 2008. Molecular pathogenesis of emphysema. J. Clin. Invest. 118: 394-402.
2. Bracke, K. R., A. I. D'hulst, T. Maes, K. B. Moerloose, I. K. Demedts, S. Lebecque, G. F. Joos, and G. G. Brusselle. 2006. Cigarette smoke-induced pulmonary inflammation and emphysema are attenuated in CCR6-deficient mice. J. Immunol. 177: 4350-4359.
3. Maeno, T., A. M. Houghton, P. A. Quintero, S. Grumelli, C. A. Owen, and S. D. Shapiro. 2007. CD8+ T cells are required for inflammation and destruction in cigarette smoke-induced emphysema in mice. J. Immunol. 178: 8090-8096.
4. Barnes, P. J. 2000. Chronic obstructive pulmonary disease. N. Engl. J. Med. 343: 269-280.
5. MacNee, W., and R. M. Tuder. 2009. New paradigms in the pathogenesis of chronic obstructive pulmonary disease I. Proc. Am. Thorac. Soc. 6: 527-531.
6. Karrasch, S., O. Holz, and R. A. Jörres. 2008. Aging and induced senescence as factors in the pathogenesis of lung emphysema. Respir. Med. 102: 1215-1230.
7. Hogg, J. C., F. Chu, S. Utokaparch, R. Woods, W. M. Elliott, L. Buzatu, R. M. Cherniack, R. M. Rogers, F. C. Sciurba, H. O. Coxson, and P. D. Paré. 2004. The nature of small-airway obstruction in chronic obstructive pulmonary disease. N. Engl. J. Med. 350: 2645-2653.
8. Huang, H., and D. J. Tindall. 2007. Dynamic FoxO transcription factors. J. Cell Sci. 120: 2479-2487.
9. Arden, K. C. 2008. FOXO animal models reveal a variety of diverse roles for FOXO transcription factors. Oncogene 27: 2345-2350. (Pubitemid 351501785)
10. Salih, D. A., and A. Brunet. 2008. FoxO transcription factors in the maintenance of cellular homeostasis during aging. Curr. Opin. Cell Biol. 20: 126-136.
11. Kops, G. J., T. B. Dansen, P. E. Polderman, I. Saarloos, K. W. Wirtz, P. J. Coffer, T. T. Huang, J. L. Bos, R. H. Medema, and B. M. Burgering. 2002. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419: 316-321.
12. van der Horst, A., and B. M. Burgering. 2007. Stressing the role of FoxO proteins in lifespan and disease. Nat. Rev. Mol. Cell Biol. 8: 440-450.
13. Birkenkamp, K. U., and P. J. Coffer. 2003. FOXO transcription factors as regulators of immune homeostasis: molecules to die for? J. Immunol. 171: 1623-1629.
14. Becker, T., G. Loch, M. Beyer, I. Zinke, A. C. Aschenbrenner, P. Carrera, T. Inhester, J. L. Schultze, and M. Hoch. 2010. FOXO-dependent regulation of innate immune homeostasis. Nature 463: 369-373.
15. Potente, M., C. Urbich, K. Sasaki, W. K. Hofmann, C. Heeschen, A. Aicher, R. Kollipara, R. A. DePinho, A. M. Zeiher, and S. Dimmeler. 2005. Involvement of Foxo transcription factors in angiogenesis and postnatal neovascularization. J. Clin. Invest. 115: 2382-2392.
16. Ronnebaum, S. M., and C. Patterson. 2010. The FoxO family in cardiac function and dysfunction. Annu. Rev. Physiol. 72: 81-94.
17. Cui, M., Y. Huang, Y. Zhao, and J. Zheng. 2008. Transcription factor FOXO3a mediates apoptosis in HIV-1-infected macrophages. J. Immunol. 180: 898-906.
18. Dejean, A. S., D. R. Beisner, I. L. Ch'en, Y. M. Kerdiles, A. Babour, K. C. Arden, D. H. Castrillon, R. A. DePinho, and S. M. Hedrick. 2009. Transcription factor Foxo3 controls the magnitude of T cell immune responses by modulating the function of dendritic cells. Nat. Immunol. 10: 504-513.
19. Jonsson, H., P. Allen, and S. L. Peng. 2005. Inflammatory arthritis requires Foxo3a to prevent Fas ligand-induced neutrophil apoptosis. Nat. Med. 11: 666-671.
20. Vernooy, J. H., K. R. Bracke, N. E. Drummen, N. S. Pauwels, L. Zabeau, R. J. van Suylen, J. Tavernier, G. F. Joos, E. F. Wouters, and G. G. Brusselle. 2010. Leptin modulates innate and adaptive immune cell recruitment after cigarette smoke exposure in mice. J. Immunol. 184: 7169-7177.
21. Essers, M. A., L. M. de Vries-Smits, N. Barker, P. E. Polderman, B. M. Burgering, and H. C. Korswagen. 2005. Functional interaction between beta-catenin and FOXO in oxidative stress signaling. Science 308: 1181-1184.
22. Olmos, Y., I. Valle, S. Borniquel, A. Tierrez, E. Soria, S. Lamas, and M. Monsalve. 2009. Mutual dependence of Foxo3a and PGC-1alpha in the induction of oxidative stress genes. J. Biol. Chem. 284: 14476-14484.
23. Czymai, T., D. Viemann, C. Sticht, G. Molema, M. Goebeler, and M. Schmidt. 2010. FOXO3 modulates endothelial gene expression and function by classical and alternative mechanisms. J. Biol. Chem. 285: 10163-10178.
24. van der Vos, K. E., and P. J. Coffer. 2008. FOXO-binding partners: it takes two to tango. Oncogene 27: 2289-2299.
25. Hu, M. C., D. F. Lee, W. Xia, L. S. Golfman, F. Ou-Yang, J. Y. Yang, Y. Zou, S. Bao, N. Hanada, H. Saso, et al. 2004. IkappaB kinase promotes tumorigenesis through inhibition of forkhead FOXO3a. Cell 117: 225-237. (Pubitemid 38496242)
26. Brunet, A., J. Park, H. Tran, L. S. Hu, B. A. Hemmings, and M. E. Greenberg. 2001. Protein kinase SGK mediates survival signals by phosphorylating the forkhead transcription factor FKHRL1 (FOXO3a). Mol. Cell. Biol. 21: 952-965.
27. van der Horst, A., L. G. Tertoolen, L. M. de Vries-Smits, R. A. Frye, R. H. Medema, and B. M. Burgering. 2004. FOXO4 is acetylated upon peroxide stress and deacetylated by the longevity protein hSir2(SIRT1). J. Biol. Chem. 279: 28873-28879.
28. Motta, M. C., N. Divecha, M. Lemieux, C. Kamel, D. Chen, W. Gu, Y. Bultsma, M. McBurney, and L. Guarente. 2004. Mammalian SIRT1 represses forkhead transcription factors. Cell 116: 551-563. (Pubitemid 38264432)
29. Nasrin, N., S. Ogg, C. M. Cahill, W. Biggs, S. Nui, J. Dore, D. Calvo, Y. Shi, G. Ruvkun, and M. C. Alexander-Bridges. 2000. DAF-16 recruits the CREBbinding protein coactivator complex to the insulin-like growth factor binding protein 1 promoter in HepG2 cells. Proc. Natl. Acad. Sci. USA 97: 10412-10417.
30. Brunet, A., L. B. Sweeney, J. F. Sturgill, K. F. Chua, P. L. Greer, Y. Lin, H. Tran, S. E. Ross, R. Mostoslavsky, H. Y. Cohen, et al. 2004. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303: 2011-2015. (Pubitemid 38393275)
31. Kume, S., T. Uzu, K. Horiike, M. Chin-Kanasaki, K. Isshiki, S. Araki, T. Sugimoto, M. Haneda, A. Kashiwagi, and D. Koya. 2010. Calorie restriction enhances cell adaptation to hypoxia through Sirt1-dependent mitochondrial autophagy in mouse aged kidney. J. Clin. Invest. 120: 1043-1055.
32. Yang, S. R., J. Wright, M. Bauter, K. Seweryniak, A. Kode, and I. Rahman. 2007. Sirtuin regulates cigarette smoke-induced proinflammatory mediator release via RelA/p65 NF-kappaB in macrophages in vitro and in rat lungs in vivo: implications for chronic inflammation and aging. Am. J. Physiol. Lung Cell. Mol. Physiol. 292: L567-L576.
33. Rajendrasozhan, S., S. R. Yang, V. L. Kinnula, and I. Rahman. 2008. SIRT1, an antiinflammatory and antiaging protein, is decreased in lungs of patients with chronic obstructive pulmonary disease.Am. J. Respir. Crit. CareMed. 177: 861-870.
34. Nakamaru, Y., C. Vuppusetty, H. Wada, J. C. Milne, M. Ito, C. Rossios, M. Elliot, J. Hogg, S. Kharitonov, H. Goto, et al. 2009. A protein deacetylase SIRT1 is a negative regulator of metalloproteinase-9. FASEB J. 23: 2810-2819.
35. Caito, S., J. W. Hwang, S. Chung, H. Yao, I. K. Sundar, and I. Rahman. 2010. PARP-1 inhibition does not restore oxidant-mediated reduction in SIRT1 activity. Biochem. Biophys. Res. Commun. 392: 264-270.
36. Lin, L., J. D. Hron, and S. L. Peng. 2004. Regulation of NF-kappaB, Th activation, and autoinflammation by the forkhead transcription factor Foxo3a. Immunity 21: 203-213.
37. Rytilä, P., T. Rehn, H. Ilumets, A. Rouhos, A. Sovijärvi, M. Myllärniemi, and V. L. Kinnula. 2006. Increased oxidative stress in asymptomatic current chronic smokers and GOLD stage 0 COPD. Respir. Res. 7: 69.
38. Castrillon, D. H., L. Miao, R. Kollipara, J. W. Horner, and R. A. DePinho. 2003. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 301: 215-218.
39. Pryhuber, G. S., H. L. Huyck, S. Bhagwat, M. A. O'Reilly, J. N. Finkelstein, F. Gigliotti, and T. W. Wright. 2008. Parenchymal cell TNF receptors contribute to inflammatory cell recruitment and respiratory failure in Pneumocystis carinii-induced pneumonia. J. Immunol. 181: 1409-1419.
40. Rajendrasozhan, S., S. Chung, I. K. Sundar, H. Yao, and I. Rahman. 2010. Targeted disruption of NF-kappaB1 (p50) augments cigarette smoke-induced lung inflammation and emphysema in mice: a critical role of p50 in chromatin remodeling. Am. J. Physiol. Lung Cell. Mol. Physiol. 298: L197-L209.
41. Yao, H., I. Edirisinghe, S. Rajendrasozhan, S. R. Yang, S. Caito, D. Adenuga, and I. Rahman. 2008. Cigarette smoke-mediated inflammatory and oxidative responses are strain-dependent in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 294: L1174-L1186.
42. Yao, H., I. Edirisinghe, S. R. Yang, S. Rajendrasozhan, A. Kode, S. Caito, D. Adenuga, and I. Rahman. 2008. Genetic ablation of NADPH oxidase enhances susceptibility to cigarette smoke-induced lung inflammation and emphysema in mice. Am. J. Pathol. 172: 1222-1237.
43. Rangasamy, T., C. Y. Cho, R. K. Thimmulappa, L. Zhen, S. S. Srisuma, T. W. Kensler, M. Yamamoto, I. Petrache, R. M. Tuder, and S. Biswal. 2004. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J. Clin. Invest. 114: 1248-1259.
44. Ishii, Y., K. Itoh, Y. Morishima, T. Kimura, T. Kiwamoto, T. Iizuka, A. E. Hegab, T. Hosoya, A. Nomura, T. Sakamoto, et al. 2005. Transcription factor Nrf2 plays a pivotal role in protection against elastase-induced pulmonary inflammation and emphysema. J. Immunol. 175: 6968-6975. (Pubitemid 41598943)
45. Guerassimov, A., Y. Hoshino, Y. Takubo, A. Turcotte, M. Yamamoto, H. Ghezzo, A. Triantafillopoulos, K. Whittaker, J. R. Hoidal, and M. G. Cosio. 2004. The development of emphysema in cigarette smoke-exposed mice is strain dependent. Am. J. Respir. Crit. Care Med. 170: 974-980.
46. Foronjy, R. F., B. A. Mercer, M. W. Maxfield, C. A. Powell, J. D'Armiento, and Y. Okada. 2005. Structural emphysema does not correlate with lung compliance: lessons from the mouse smoking model. Exp. Lung Res. 31: 547-562.
47. Massett, M. P., and B. C. Berk. 2005. Strain-dependent differences in responses to exercise training in inbred and hybrid mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288: R1006-R1013.
48. Rahman, I., A. A. van Schadewijk, A. J. Crowther, P. S. Hiemstra, J. Stolk, W. MacNee, and W. I. De Boer. 2002. 4-Hydroxy-2-nonenal, a specific lipid peroxidation product, is elevated in lungs of patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 166: 490-495.
49. Yang, S. R., A. S. Chida, M. R. Bauter, N. Shafiq, K. Seweryniak, S. B. Maggirwar, I. Kilty, and I. Rahman. 2006. Cigarette smoke induces proinflammatory cytokine release by activation of NF-kappaB and post-translational modifications of histone deacetylase in macrophages. Am. J. Physiol. Lung Cell. Mol. Physiol. 291: L46-L57.
50. Yang, S. R., S. Valvo, H. Yao, A. Kode, S. Rajendrasozhan, I. Edirisinghe, S. Caito, D. Adenuga, R. Henry, G. Fromm, et al. 2008. IKK alpha causes chromatin modification on pro-inflammatory genes by cigarette smoke in mouse lung. Am. J. Respir. Cell Mol. Biol. 38: 689-698.
51. Kode, A., S. R. Yang, and I. Rahman. 2006. Differential effects of cigarette smoke on oxidative stress and proinflammatory cytokine release in primary human airway epithelial cells and in a variety of transformed alveolar epithelial cells. Respir. Res. 7: 132.
52. Cho, H. Y., A. E. Jedlicka, S. P. Reddy, T. W. Kensler, M. Yamamoto, L. Y. Zhang, and S. R. Kleeberger. 2002. Role of NRF2 in protection against hyperoxic lung injury in mice. Am. J. Respir. Cell Mol. Biol. 26: 175-182.
53. Couillin, I., V. Vasseur, S. Charron, P. Gasse, M. Tavernier, J. Guillet, V. Lagente, L. Fick,M. Jacobs, F. R. Coelho, et al. 2009. IL-1R1/MyD88 signaling is critical for elastase-induced lung inflammation and emphysema. J. Immunol. 183: 8195-8202.
54. -/- mice demonstrate reduced numbers of pre-B and recirculating B cells but normal splenic B cell sub-population distribution. Int. Immunol. 21: 831-842.
55. Snoeks, L., C. R. Weber, K. Wasland, J. R. Turner, C. Vainder, W. Qi, and S. D. Savkovic. 2009. Tumor suppressor FOXO3 participates in the regulation of intestinal inflammation. Lab. Invest. 89: 1053-1062.
56. Tothova, Z., R. Kollipara, B. J. Huntly, B. H. Lee, D. H. Castrillon, D. E. Cullen, E. P. McDowell, S. Lazo-Kallanian, I. R. Williams, C. Sears, et al. 2007. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128: 325-339. (Pubitemid 46137992)
57. Miyamoto, K., K. Y. Araki, K. Naka, F. Arai, K. Takubo, S. Yamazaki, S. Matsuoka, T. Miyamoto, K. Ito, M. Ohmura, et al. 2007. Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell 1: 101-112. (Pubitemid 46865800)
58. Valenca, S. S., P. Castro, W. A. Pimenta, M. Lanzetti, S. V. Silva, C. Barja-Fidalgo, V. L. Koatz, and L. C. Porto. 2006. Light cigarette smoke-induced emphysema and NFkappaB activation in mouse lung. Int. J. Exp. Pathol. 87: 373-381.
59. Zhou, W., Q. Cao, Y. Peng, Q. J. Zhang, D. H. Castrillon, R. A. DePinho, and Z. P. Liu. 2009. FoxO4 inhibits NF-kappaB and protects mice against colonic injury and inflammation. Gastroenterology 137: 1403-1414.
60. Clavel, S., S. Siffroi-Fernandez, A. S. Coldefy, K. Boulukos, D. F. Pisani, and B. Dérijard. 2010. Regulation of the intracellular localization of Foxo3a by stress-activated protein kinase signaling pathways in skeletal muscle cells. Mol. Cell. Biol. 30: 470-480.
61. Biswas, S. K., and I. Rahman. 2009. Environmental toxicity, redox signaling and lung inflammation: the role of glutathione. Mol. Aspects Med. 30: 60-76.
62. Chintapalli, J., S. Yang, D. Opawumi, S. R. Goyal, N. Shamsuddin, A. Malhotra, K. Reiss, and L. G. Meggs. 2007. Inhibition of wild-type p66ShcA in mesangial cells prevents glycooxidant-dependent FOXO3a regulation and promotes the survival phenotype. Am. J. Physiol. Renal Physiol. 292: F523-F530.
63. Sengupta, A., J. D. Molkentin, J. H. Paik, R. A. DePinho, and K. E. Yutzey. 2011. FoxO transcription factors promote cardiomyocyte survival upon induction of oxidative stress. J. Biol. Chem. 286: 7468-7478.
64. Dansen, T. B., L. M. Smits, M. H. van Triest, P. L. de Keizer, D. van Leenen, M. G. Koerkamp, A. Szypowska, A. Meppelink, A. B. Brenkman, J. Yodoi, et al. 2009. Redox-sensitive cysteines bridge p300/CBP-mediated acetylation and FoxO4 activity. Nat. Chem. Biol. 5: 664-672.
65. Hedrick, S. M. 2009. The cunning little vixen: Foxo and the cycle of life and death. Nat. Immunol. 10: 1057-1063.
66. van der Heide, L. P., and M. P. Smidt. 2005. Regulation of FoxO activity by CBP/p300-mediated acetylation. Trends Biochem. Sci. 30: 81-86.