Rtp801, a suppressor of mTOR signaling, is an essential mediator of cigarette smoke-induced pulmonary injury and emphysema

Nature Medicine

Volumn 16, Issue 7, 2010, Pages 767-773

  Yoshida, Toshinori ^a   Mett, Igor ^b   Bhunia, Anil K ^a   Bowman, Joel ^c   Perez, Mario ^c   Zhang, Li ^c   Gandjeva, Aneta ^c   Zhen, Lijie ^a   Chukwueke, Ugonma ^a   Mao, Tianzhi ^a   Richter, Amy ^a   Brown, Emile ^a   Ashush, Hagit ^b   Notkin, Natalie ^b   Gelfand, Anna ^b   Thimmulappa, Rajesh K ^d   Rangasamy, Tirumalai ^d   Sussan, Thomas ^d   Cosgrove, Gregory ^e   Mouded, Majd ^f   Shapiro, Steven D ^f   Petrache, Irina ^a,g   Biswal, Shyam ^d   Feinstein, Elena ^b   Tuder, Rubin M ^a,c   more..

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b QBI Enterprises Ltd   (Israel)

^c UNIVERSITY OF COLORADO   (United States)

^d The Johns Hopkins University   (United States)

^e DEPARTMENT OF MEDICINE   (United States)

^f UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^g INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN; CIGARETTE SMOKE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; PROTEIN; PROTEIN RTP 801; RAPAMYCIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL DEATH; CIGARETTE SMOKING; CONTROLLED STUDY; ENVIRONMENTAL STRESS; GENE AMPLIFICATION; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG ALVEOLUS CELL; LUNG EMPHYSEMA; LUNG INJURY; LUNG PARENCHYMA; MALE; MEDIATOR; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PNEUMONIA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; ENZYME ACTIVATION; HOMEOSTASIS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LUNG; MICE; MICE, KNOCKOUT; NF-KAPPA B; PROTEIN-SERINE-THREONINE KINASES; PULMONARY ALVEOLI; PULMONARY EMPHYSEMA; SMOKING; TRANSCRIPTION FACTORS;

MAMMALIA; MUS;

EID: 77954470662     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.2157     Document Type: Article

References (56)

1. Yoshida, T. & Tuder, R.M. Pathobiology of cigarette smoke-induced chronic obstructive pulmonary disease. Physiol. Rev. 87, 1047-1082 (2007).
2. Tuder, R.M., Yoshida, T., Arap, W., Pasqualini, R. & Petrache, I. Cellular and molecular mechanisms of alveolar destruction in emphysema: an evolutionary perspective. Proc. Am. Thorac. Soc. 3, 503-510 (2006).
3. Tuder, R.M. et al. Oxidative stress and apoptosis interact and cause emphysema due to vascular endothelial growth factor receptor blockade. Am. J. Respir. Cell Mol. Biol. 29, 88-97 (2003).
4. Ryter, S.W., Chen, Z.H., Kim, H.P. & Choi, A.M. Autophagy in chronic obstructive pulmonary disease: homeostatic or pathogenic mechanism? Autophagy 5, 235-237 (2009).
5. Houghton, A.M. et al. Elastin fragments drive disease progression in a murine model of emphysema. J. Clin. Invest. 116, 753-759 (2006).
6. Petrache, I. et al. Ceramide upregulation causes pulmonary cell apoptosis and emphysema-like disease in mice. Nat. Med. 11, 491-498 (2005).
7. Weathington, N.M. et al. A novel peptide CXCR ligand derived from extracellular matrix degradation during airway infammation. Nat. Med. 12, 317-323 (2006).
8. Shoshani, T. et al. Identifcation of a novel hypoxia-inducible factor 1-responsive gene, RTP801, involved in apoptosis. Mol. Cell. Biol. 22, 2283-2293 (2002).
9. Ellisen, L.W. et al. REDD1, a developmentally regulated transcriptional target of p63 and p53, links p63 to regulation of reactive oxygen species. Mol. Cell 10, 995-1005 (2002).
10. Brafman, A. et al. Inhibition of oxygen-induced retinopathy in RTP801-defcient mice. Invest. Ophthalmol. Vis. Sci. 45, 3796-3805 (2004).
11. Brugarolas, J. et al. Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev. 18, 2893-2904 (2004).
12. Reiling, J.H. & Hafen, E. The hypoxia-induced paralogs Scylla and Charybdis inhibit growth by down-regulating S6K activity upstream of TSC in Drosophila. Genes Dev. 18, 2879-2892 (2004).
13. Sofer, A., Lei, K., Johannessen, C.M. & Ellisen, L.W. Regulation of mTOR and cell growth in response to energy stress by REDD1. Mol. Cell. Biol. 25, 5834-5845 (2005).
14. Corradetti, M.N., Inoki, K. & Guan, K.L. The stress-inducted proteins RTP801 and RTP801L are negative regulators of the mammalian target of rapamycin pathway. J. Biol. Chem. 280, 9769-9772 (2005).
15. Arsham, A.M., Howell, J.J. & Simon, M.C. A novel hypoxia-inducible factor-independent hypoxic response regulating mammalian target of rapamycin and its targets. J. Biol. Chem. 278, 29655-29660 (2003).
16. Hudson, C.C. et al. Regulation of hypoxia-inducible factor 1α expression and function by the mammalian target of rapamycin. Mol. Cell. Biol. 22, 7004-7014 (2002).
17. Katiyar, S. et al. REDD1, an inhibitor of mTOR signalling, is regulated by the CUL4A-DDB1 ubiquitin ligase. EMBO Rep. 10, 866-872 (2009).
18. Rahman, I. et al. 4-Hydroxy-2-nonenal, a specifc lipid peroxidation product, is elevated in lungs of patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 166, 490-495 (2002).
19. Rangasamy, T. et al. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J. Clin. Invest. 114, 1248-1259 (2004).
20. Sussan, T.E. et al. Targeting Nrf2 with the triterpenoid CDDO-imidazolide attenuates cigarette smoke-induced emphysema and cardiac dysfunction in mice. Proc. Natl. Acad. Sci. USA 106, 250-255 (2009).
21. Lin, L., Stringfeld, T.M., Shi, X. & Chen, Y. Arsenite induces a cell stress-response gene, RTP801, through reactive oxygen species and transcription factors Elk-1 and CCAAT/enhancer-binding protein. Biochem. J. 392, 93-102 (2005).
22. Marwick, J.A. et al. Cigarette smoke alters chromatin remodeling and induces proinfammatory genes in rat lungs. Am. J. Respir. Cell Mol. Biol. 31, 633-642 (2004).
23. Vlahos, R. et al. Differential protease, innate immunity and NF-κB induction profles during lung infammation induced by subchronic cigarette smoke exposure in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 290, L931-L945 (2006).
24. Iimuro, Y. et al. NFκB prevents apoptosis and liver dysfunction during liver regeneration. J. Clin. Invest. 101, 802-811 (1998).
25. Campbell, K.J. & Perkins, N.D. Post-translational modifcation of RelA(p65) NF-κB. Biochem. Soc. Trans. 32, 1087-1089 (2004).
26. Zampetaki, A., Mitsialis, S.A., Pfeilschifter, J. & Kourembanas, S. Hypoxia induces macrophage infammatory protein-2 (MIP-2) gene expression in murine macrophages via NF-κB: the prominent role of p42/p44 and PI3 kinase pathways. FASEB J. 18, 1090-1092 (2004).
27. Wikenheiser, K.A. et al. Production of immortalized distal respiratory epithelial cell lines from surfactant protein C/simian virus 40 large tumor antigen transgenic mice. Proc. Natl. Acad. Sci. USA 90, 11029-11033 (1993).
28. DeYoung, M.P., Horak, P., Sofer, A., Sgroi, D. & Ellisen, L.W. Hypoxia regulates TSC1/2-mTOR signaling and tumor suppression through REDD1-mediated 14-3-3 shuttling. Genes Dev. 22, 239-251 (2008).
29. Flotte, T.R. & Carter, B.J. Adeno-associated virus vectors for gene therapy. Gene Ther. 2, 357-362 (1995).
30. Hautamaki, R.D., Kobayashi, D.K., Senior, R.M. & Shapiro, S.D. Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice. Science 277, 2002-2004 (1997).
31. Inoki, K., Ouyang, H., Li, Y. & Guan, K.L. Signaling by target of rapamycin proteins in cell growth control. Microbiol. Mol. Biol. Rev. 69, 79-100 (2005).
32. Shi, M.M., Chong, I., Godleski, J.J. & Paulauskis, J.D. Regulation of macrophage infammatory protein-2 gene expression by oxidative stress in rat alveolar macrophages. Immunology 97, 309-315 (1999).
33. Guerassimov, A. et al. The development of emphysema in cigarette smoke-exposed mice is strain dependent. Am. J. Respir. Crit. Care Med. 170, 974-980 (2004).
34. Churg, A. et al. Macrophage metalloelastase mediates acute cigarette smoke-induced infammation via tumor necrosis factor-alpha release. Am. J. Respir. Crit. Care Med. 167, 1083-1089 (2003).
35. Elias, J.A., Kang, M.J., Crouthers, K., Homer, R. & Lee, C.G. State of the art. Mechanistic heterogeneity in chronic obstructive pulmonary disease: insights from transgenic mice. Proc. Am. Thorac. Soc. 3, 494-498 (2006).
36. Giordano, R.J. et al. Targeted induction of lung endothelial cell apoptosis causes emphysema-like changes in the mouse. J. Biol. Chem. 283, 29447-29460 (2008).
37. Tuder, R.M., Petrache, I., Elias, J.A., Voelkel, N.F. & Henson, P.M. Apoptosis and emphysema: the missing link. Am. J. Respir. Cell Mol. Biol. 28, 551-554 (2003).
38. Gery, S. et al. RTP801 is a novel retinoic acid-responsive gene associated with myeloid differentiation. Exp. Hematol. 35, 572-578 (2007).
39. Vandivier, R.W., Henson, P.M. & Douglas, I.S. Burying the dead: the impact of failed apoptotic cell removal (efferocytosis) on chronic infammatory lung disease. Chest 129, 1673-1682 (2006).
40. Lee, S.H. et al. Antielastin autoimmunity in tobacco smoking-induced emphysema. Nat. Med. 13, 567-569 (2007).
41. Cosio, M.G., Saetta, M. & Agusti, A. Immunologic aspects of chronic obstructive pulmonary disease. N. Engl. J. Med. 360, 2445-2454 (2009).
42. Rahman, I. & Adcock, I.M. Oxidative stress and redox regulation of lung infammation in COPD. Eur. Respir. J. 28, 219-242 (2006).
43. Kang, M.J. et al. Cigarette smoke selectively enhances viral PAMP and viruses-induced pulmonary innate immunity and remodeling responses. J. Clin. Invest. 118, 2771-2784 (2008).
44. Kim, H.P. et al. Autophagic proteins regulate cigarette smoke-induced apoptosis: protective role of heme oxygenase-1. Autophagy 4, 887-895 (2008).
45. Gibbs, P.E. & Maines, M.D. Biliverdin inhibits activation of NF-κB: reversal of inhibition by human biliverdin reductase. Int. J. Cancer 121, 2567-2574 (2007).
46. Weichhart, T. et al. The TSC-mTOR signaling pathway regulates the innate infammatory response. Immunity 29, 565-577 (2008).
47. Shah, O.J., Wang, Z. & Hunter, T. Inappropriate activation of the TSC/Rheb/mTOR/S6K cassette induces IRS1/2 depletion, insulin resistance, and cell survival defciencies. Curr. Biol. 14, 1650-1656 (2004).
48. Bhaskar, P.T. et al. mTORC1 hyperactivity inhibits serum deprivation-induced apoptosis via increased hexokinase II and GLUT1 expression, sustained Mcl-1 expression, and glycogen synthase kinase 3beta inhibition. Mol. Cell. Biol. 29, 5136-5147 (2009).
49. Zhang, Q., Adiseshaiah, P., Kalvakolanu, D.V. & Reddy, S.P. A phosphatidylinositol 3-kinase-regulated Akt-independent signaling promotes cigarette smoke-induced FRA-1 expression. J. Biol. Chem. 281, 10174-10181 (2006).
50. Lee, D.F. et al. IKKβ Suppression of TSC1 links infammation and tumor angiogenesis via the mTOR pathway. Cell 130, 440-455 (2007).
51. Morelon, E., Stern, M. & Kreis, H. Interstitial pneumonitis associated with sirolimus therapy in renal-transplant recipients. N. Engl. J. Med. 343, 225-226 (2000).
52. Fujitani, Y. & Triflieff, A. In vivo and in vitro effects of SAR 943, a rapamycin analogue, on airway infammation and remodeling. Am. J. Respir. Crit. Care Med. 167, 193-198 (2003).
53. Petrache, I. et al. α-1 antitrypsin inhibits caspase-3 activity, preventing lung endothelial cell apoptosis. Am. J. Pathol. 169, 1155-1166 (2006).
54. Neuhaus, P., Klupp, J. & Langrehr, J.M. mTOR inhibitors: an overview. Liver Transpl. 7, 473-484 (2001).
55. Faivre, S., Kroemer, G. & Raymond, E. Current development of mTOR inhibitors as anticancer agents. Nat. Rev. Drug Discov. 5, 671-688 (2006).
56. McGrath-Morrow, S.A. et al. Vascular endothelial growth factor receptor 2 blockade disrupts postnatal lung development. Am. J. Respir. Cell Mol. Biol. 32, 420-427 (2005).