Sestrin-2, a repressor of PDGFRβ signalling, promotes cigarette-smoke-induced pulmonary emphysema in mice and is upregulated in individuals with COPD

DMM Disease Models and Mechanisms

Volumn 6, Issue 6, 2013, Pages 1378-1387

  Heidler, Juliana ^a   Fysikopoulos, Athanasios ^b   Wempe, Frank ^a   Seimetz, Michael ^b   Bangsow, Thorsten ^a   Tomasovic, Ana ^a   Veit, Florian ^b   Scheibe, Susan ^b   Pichl, Alexandra ^b   Weisel, Friederike ^b   Lloyd, K C Kent ^c   Jaksch, Peter ^d   Klepetko, Walter ^d   Weissmann, Norbert ^b   Von Melchner, Harald ^a  

^a GOETHE UNIVERSITY MEDICAL SCHOOL   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CIGARETTE SMOKE; ELASTASE; MEMBRANE PROTEIN; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; SESTRIN 2 PROTEIN; SUPEROXIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; EMBRYO; ENVIRONMENTAL EXPOSURE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; LUNG ALVEOLUS CELL; LUNG COMPLIANCE; LUNG EMPHYSEMA; LUNG HEMODYNAMICS; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; REPRESSOR GENE; SIGNAL TRANSDUCTION;

ANIMALS; HUMANS; LUNG; MICE; MICE, KNOCKOUT; NUCLEAR PROTEINS; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; PULMONARY EMPHYSEMA; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SMOKE; SUPEROXIDES; UP-REGULATION;

EID: 84888879285     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.013482     Document Type: Article

References (36)

1. Bae, S. H., Sung, S. H., Oh, S. Y., Lim, J. M., Lee, S. K., Park, Y. N., Lee, H. E., Kang, D. and Rhee, S. G. (2013). Sestrins activate Nrf2 by promoting p62-dependent autophagic degradation of Keap1 and prevent oxidative liver damage. Cell Metab. 17, 73-84.
2. Boström, H., Willetts, K., Pekny, M., Levéen, P., Lindahl, P., Hedstrand, H., Pekna, M., Hellström, M., Gebre-Medhin, S., Schalling, M. et al. (1996). PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 85, 863-873.
3. Budanov, A. V. and Karin, M. (2008). p53 target genes sestrin1 and sestrin2 connect genotoxic stress and mTOR signaling. Cell 134, 451-460.
4. Budanov, A. V., Shoshani, T., Faerman, A., Zelin, E., Kamer, I., Kalinski, H., Gorodin, S., Fishman, A., Chajut, A., Einat, P. et al. (2002). Identification of a novel stressresponsive gene Hi95 involved in regulation of cell viability. Oncogene 21, 6017-6031.
5. Budanov, A. V., Sablina, A. A., Feinstein, E., Koonin, E. V. and Chumakov, P. M. (2004). Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD. Science 304, 596-600.
6. Chedid, M., Rubin, J. S., Csaky, K. G. and Aaronson, S. A. (1994). Regulation of keratinocyte growth factor gene expression by interleukin 1. J. Biol. Chem. 269, 10753-10757.
7. Choi, M. H., Lee, I. K., Kim, G. W., Kim, B. U., Han, Y. H., Yu, D. Y., Park, H. S., Kim, K. Y., Lee, J. S., Choi, C. et al. (2005). Regulation of PDGF signalling and vascular remodelling by peroxiredoxin II. Nature 435, 347-353.
8. Dabovic, B., Chen, Y., Choi, J., Vassallo, M., Dietz, H. C., Ramirez, F., von Melchner, H., Davis, E. C. and Rifkin, D. B. (2009). Dual functions for LTBP in lung development: LTBP-4 independently modulates elastogenesis and TGF-beta activity. J. Cell. Physiol. 219, 14-22.
9. Dumitrascu, R., Weissmann, N., Ghofrani, H. A., Dony, E., Beuerlein, K., Schmidt, H., Stasch, J. P., Gnoth, M. J., Seeger, W., Grimminger, F. et al. (2006). Activation of soluble guanylate cyclase reverses experimental pulmonary hypertension and vascular remodeling. Circulation 113, 286-295.
10. Finkel, T. (2011). Signal transduction by reactive oxygen species. J. Cell Biol. 194, 7-15.
11. Fischer, H., Taylor, N., Allerstorfer, S., Grusch, M., Sonvilla, G., Holzmann, K., Setinek, U., Elbling, L., Cantonati, H., Grasl-Kraupp, B. et al. (2008). Fibroblast growth factor receptor-mediated signals contribute to the malignant phenotype of non-small cell lung cancer cells: therapeutic implications and synergism with epidermal growth factor receptor inhibition. Mol. Cancer Ther. 7, 3408-3419.
12. Hägerstrand, D., Hesselager, G., Achterberg, S., Wickenberg Bolin, U., Kowanetz, M., Kastemar, M., Heldin, C. H., Isaksson, A., Nistér, M. and Ostman, A. (2006). Characterization of an imatinib-sensitive subset of high-grade human glioma cultures. Oncogene 25, 4913-4922.
13. Heidler, J., Al-Furoukh, N., Kukat, C., Salwig, I., Ingelmann, M. E., Seibel, P., Krüger, M., Holtz, J., Wittig, I., Braun, T. et al. (2011). Nitric oxide-associated protein 1 (NOA1) is necessary for oxygen-dependent regulation of mitochondrial respiratory complexes. J. Biol. Chem. 286, 32086-32093.
14. Hersh, C. P., Demeo, D. L., Lazarus, R., Celedón, J. C., Raby, B. A., Benditt, J. O., Criner, G., Make, B., Martinez, F. J., Scanlon, P. D. et al. (2006). Genetic association analysis of functional impairment in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 173, 977-984.
15. Kolla, V., Gonzales, L. W., Gonzales, J., Wang, P., Angampalli, S., Feinstein, S. I. and Ballard, P. L. (2007). Thyroid transcription factor in differentiating type II cells: regulation, isoforms, and target genes. Am. J. Respir. Cell Mol. Biol. 36, 213-225.
16. Levéen, P., Pekny, M., Gebre-Medhin, S., Swolin, B., Larsson, E. and Betsholtz, C. (1994). Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities. Genes Dev. 8, 1875-1887.
17. Manning, B. D. (2004). Balancing Akt with S6K: implications for both metabolic diseases and tumorigenesis. J. Cell Biol. 167, 399-403.
18. Mellström, K., Heldin, C. H. and Westermark, B. (1988). Induction of circular membrane ruffling on human fibroblasts by platelet-derived growth factor. Exp. Cell Res. 177, 347-359.
19. Mittal, M., Roth, M., König, P., Hofmann, S., Dony, E., Goyal, P., Selbitz, A. C., Schermuly, R. T., Ghofrani, H. A., Kwapiszewska, G. et al. (2007). Hypoxiadependent regulation of nonphagocytic NADPH oxidase subunit NOX4 in the pulmonary vasculature. Circ. Res. 101, 258-267.
20. Ohnishi, K., Sakai, F., Kudoh, S. and Ohno, R. (2006). Twenty-seven cases of druginduced interstitial lung disease associated with imatinib mesylate. Leukemia 20, 1162-1164.
21. Rahman, I. (2012). Pharmacological antioxidant strategies as therapeutic interventions for COPD. Biochim. Biophys. Acta 1822, 714-728.
22. Rahman, I. and MacNee, W. (2012). Antioxidant pharmacological therapies for COPD. Curr. Opin. Pharmacol. 12, 256-265.
23. Repapi, E., Sayers, I., Wain, L. V., Burton, P. R., Johnson, T., Obeidat, M., Zhao, J. H., Ramasamy, A., Zhai, G., Vitart, V. et al.; Wellcome Trust Case Control Consortium; NSHD Respiratory Study Team (2010). Genome-wide association study identifies five loci associated with lung function. Nat. Genet. 42, 36-44.
24. Seimetz, M., Parajuli, N., Pichl, A., Veit, F., Kwapiszewska, G., Weisel, F. C., Milger, K., Egemnazarov, B., Turowska, A., Fuchs, B. et al. (2011). Inducible NOS inhibition reverses tobacco-smoke-induced emphysema and pulmonary hypertension in mice. Cell 147, 293-305.
25. Shapiro, S. D. (2000). Animal models for chronic obstructive pulmonary disease: age of klotho and marlboro mice. Am. J. Respir. Cell Mol. Biol. 22, 4-7.
26. Shin, B. Y., Jin, S. H., Cho, I. J. and Ki, S. H. (2012). Nrf2-ARE pathway regulates induction of Sestrin-2 expression. Free Radic. Biol. Med. 53, 834-841.
27. Sterner-Kock, A., Thorey, I. S., Koli, K., Wempe, F., Otte, J., Bangsow, T., Kuhlmeier, K., Kirchner, T., Jin, S., Keski-Oja, J. et al. (2002). Disruption of the gene encoding the latent transforming growth factor-beta binding protein 4 (LTBP-4) causes abnormal lung development, cardiomyopathy, and colorectal cancer. Genes Dev. 16, 2264-2273.
28. Thamsen, M., Kumsta, C., Li, F. and Jakob, U. (2011). Is overoxidation of peroxiredoxin physiologically significant? Antioxid. Redox Signal. 14, 725-730.
29. Tuder, R. M. and Petrache, I. (2012). Pathogenesis of chronic obstructive pulmonary disease. J. Clin. Invest. 122, 2749-2755.
30. Ware, L. B. and Matthay, M. A. (2002). Keratinocyte and hepatocyte growth factors in the lung: roles in lung development, inflammation, and repair. Am. J. Physiol. 282, L924-L940.
31. Weichhart, T., Costantino, G., Poglitsch, M., Rosner, M., Zeyda, M., Stuhlmeier, K. M., Kolbe, T., Stulnig, T. M., Hörl, W. H., Hengstschläger, M. et al. (2008). The TSCmTOR signaling pathway regulates the innate inflammatory response. Immunity 29, 565-577.
32. Wempe, F., De-Zolt, S., Koli, K., Bangsow, T., Parajuli, N., Dumitrascu, R., Sterner-Kock, A., Weissmann, N., Keski-Oja, J. and von Melchner, H. (2010). Inactivation of sestrin 2 induces TGF-beta signaling and partially rescues pulmonary emphysema in a mouse model of COPD. Dis. Model. Mech. 3, 246-253.
33. Woo, H. A., Bae, S. H., Park, S. and Rhee, S. G. (2009). Sestrin 2 is not a reductase for cysteine sulfinic acid of peroxiredoxins. Antioxid. Redox Signal. 11, 739-745.
34. Yildirim, A. O., Muyal, V., John, G., Müller, B., Seifart, C., Kasper, M. and Fehrenbach, H. (2010). Palifermin induces alveolar maintenance programs in emphysematous mice. Am. J. Respir. Crit. Care Med. 181, 705-717.
35. Yoshida, T. and Tuder, R. M. (2007). Pathobiology of cigarette smoke-induced chronic obstructive pulmonary disease. Physiol. Rev. 87, 1047-1082.
36. Yoshida, T., Mett, I., Bhunia, A. K., Bowman, J., Perez, M., Zhang, L., Gandjeva, A., Zhen, L., Chukwueke, U., Mao, T. et al. (2010). Rtp801, a suppressor of mTOR signaling, is an essential mediator of cigarette smoke-induced pulmonary injury and emphysema. Nat. Med. 16, 767-773.