Pim1 kinase protects airway epithelial cells from cigarette smoke-induced damage and airway inflammation

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 307, Issue 3, 2014, Pages

  de Vries, M ^a   Heijink, I H ^a   Gras, R ^a   den Boef, L E ^a   Reinders Luinge, M ^a   Pouwels, S D ^a   Hylkema, M N ^a   van der Toorn, M ^a   Brouwer, U ^a   van Oosterhout, A J M ^a   Nawijn, M C ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Cell survival; Chronic obstructive pulmonary disease; Damage associated molecular patterns; Innate immune response; Mice

Indexed keywords

CIGARETTE SMOKE; DOUBLE STRANDED DNA; HEAT SHOCK PROTEIN 70; PROTEIN KINASE PIM 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL SURVIVAL; CELL VIABILITY; CHRONIC OBSTRUCTIVE LUNG DISEASE; CIGARETTE SMOKE INDUCED DAMAGE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; INNATE IMMUNITY; LUNG ALVEOLUS EPITHELIUM; LUNG LAVAGE; LUNG PARENCHYMA; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY TRACT INFLAMMATION; RISK FACTOR; SMOKING; SURVIVAL; WILD TYPE;

CELL SURVIVAL; CHRONIC OBSTRUCTIVE PULMONARY DISEASE; DAMAGE-ASSOCIATED MOLECULAR PATTERNS; INNATE IMMUNE RESPONSE; MICE;

ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CELL DEATH; CELLS, CULTURED; CHEMOKINES; EPITHELIAL CELLS; FEMALE; HSP70 HEAT-SHOCK PROTEINS; INFLAMMATION; LUNG; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED BALB C; NEUTROPHILS; PROTO-ONCOGENE PROTEINS C-PIM-1; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; SMOKING;

EID: 84905259531     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00156.2013     Document Type: Article

References (37)

1. Aho TL, Sandholm J, Peltola KJ, Mankonen HP, Lilly M, Koskinen PJ. Pim-1 kinase promotes inactivation of the proapoptotic Bad protein by phosphorylating it on the Ser112 gatekeeper site. FEBS Lett 571: 43-49, 2004.
2. Andersen CL, Jensen JL, Orntoft TF. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64: 5245-5250, 2004.
3. Barnes PJ. Immunology of asthma and chronic obstructive pulmonary disease. Nat Rev Immunol 8: 183-192, 2008.
4. Brusselle GG, Joos GF, Bracke KR. New insights into the immunology of chronic obstructive pulmonary disease. Lancet 378: 1015-1026, 2011.
5. Cosio MG, Saetta M, Agusti A. Immunologic aspects of chronic obstructive pulmonary disease. N Engl J Med 360: 2445-2454, 2009.
6. Danial NN. BAD: undertaker by night, candyman by day. Oncogene 27, Suppl 1: S53-S70, 2008.
7. Doz E, Noulin N, Boichot E, Guenon I, Fick L, Le Bert M, Lagente V, Ryffel B, Schnyder B, Quesniaux VF, Couillin I. Cigarette smokeinduced pulmonary inflammation is TLR4/MyD88 and IL-1R1/MyD88 signaling dependent. J Immunol 180: 1169-1178, 2008.
8. Foell D, Wittkowski H, Vogl T, Roth J. S100 proteins expressed in phagocytes: a novel group of damage-associated molecular pattern molecules. J Leukoc Biol 81: 28-37, 2007.
9. Gopal R, Monin L, Torres D, Slight S, Mehra S, McKenna KC, Fallert Junecko BA, Reinhart TA, Kolls J, Baez-Saldana R, Cruz-Lagunas A, Rodriguez-Reyna TS, Kumar NP, Tessier P, Roth J, Selman M, Becerril-Villanueva E, Baquera-Heredia J, Cumming B, Kasprowicz VO, Steyn AJ, Babu S, Kaushal D, Zuniga J, Vogl T, Rangel-Moreno J, Khader SA. S100A8/A9 proteins mediate neutrophilic inflammation and lung pathology during tuberculosis. Am J Respir Crit Care Med 188: 1137-1146, 2013.
10. Green DR, Ferguson T, Zitvogel L, Kroemer G. Immunogenic and tolerogenic cell death. Nat Rev Immunol 9: 353-363, 2009.
11. Groskreutz DJ, Monick MM, Babor EC, Nyunoya T, Varga SM, Look DC, Hunninghake GW. Cigarette smoke alters respiratory syncytial virus-induced apoptosis and replication. Am J Respir Cell Mol Biol 41: 189-198, 2009.
12. Hacker S, Lambers C, Hoetzenecker K, Pollreisz A, Aigner C, Lichtenauer M, Mangold A, Niederpold T, Zimmermann M, Taghavi S, Klepetko W, Ankersmit HJ. Elevated HSP27, HSP70 and HSP90 alpha in chronic obstructive pulmonary disease: markers for immune activation and tissue destruction. Clin Lab 55: 31-40, 2009.
13. Harada C, Kawaguchi T, Ogata-Suetsugu S, Yamada M, Hamada N, Maeyama T, Souzaki R, Tajiri T, Taguchi T, Kuwano K, Nakanishi Y. EGFR tyrosine kinase inhibition worsens acute lung injury in mice with repairing airway epithelium. Am J Respir Crit Care Med 183: 743-751, 2011.
14. Krysko DV, Agostinis P, Krysko O, Garg AD, Bachert C, Lambrecht BN, Vandenabeele P. Emerging role of damage-associated molecular patterns derived from mitochondria in inflammation. Trends Immunol 32: 157-164, 2011.
15. Li CJ, Ning W, Matthay MA, Feghali-Bostwick CA, Choi AM. MAPK pathway mediates EGR-1-HSP70-dependent cigarette smoke-induced chemokine production. Am J Physiol Lung Cell Mol Physiol 292: L1297-L1303, 2007.
16. Macdonald A, Campbell DG, Toth R, McLauchlan H, Hastie CJ, Arthur JS. Pim kinases phosphorylate multiple sites on Bad and promote 14-3-3 binding and dissociation from Bcl-XL. BMC Cell Biol 7: 1, 2006.
17. Maes T, Bracke KR, Vermaelen KY, Demedts IK, Joos GF, Pauwels RA, Brusselle GG. Murine TLR4 is implicated in cigarette smokeinduced pulmonary inflammation. Int Arch Allergy Immunol 141: 354-368, 2006.
18. Morris A, Kinnear G, Wan WY, Wyss D, Bahra P, Stevenson CS. Comparison of cigarette smoke-induced acute inflammation in multiple strains of mice and the effect of a matrix metalloproteinase inhibitor on these responses. J Pharmacol Exp Ther 327: 851-862, 2008.
19. Mortaz E, Henricks PA, Kraneveld AD, Givi ME, Garssen J, Folkerts G. Cigarette smoke induces the release of CXCL-8 from human bronchial epithelial cells via TLRs and induction of the inflammasome. Biochim Biophys Acta 1812: 1104-1110, 2011.
20. Nawijn MC, Alendar A, Berns A. For better or for worse: the role of Pim oncogenes in tumorigenesis. Nat Rev Cancer 11: 23-34, 2011.
21. Nawijn MC, Hackett TL, Postma DS, van Oosterhout AJ, Heijink IH. E-cadherin: gatekeeper of airway mucosa and allergic sensitization. Trends Immunol 32: 248-255, 2011.
22. Pogacic V, Bullock AN, Fedorov O, Filippakopoulos P, Gasser C, Biondi A, Meyer-Monard S, Knapp S, Schwaller J. Structural analysis identifies imidazo[1, 2-b]pyridazines as PIM kinase inhibitors with in vitro antileukemic activity. Cancer Res 67: 6916-6924, 2007.
23. Poon IK, Hulett MD, Parish CR. Molecular mechanisms of late apoptotic/necrotic cell clearance. Cell Death Differ 17: 381-397, 2010.
24. Post S, Nawijn MC, Hackett TL, Baranowska M, Gras R, van Oosterhout AJ, Heijink IH. The composition of house dust mite is critical for mucosal barrier dysfunction and allergic sensitisation. Thorax 67: 488-495, 2012.
25. Pouwels SD, Heijink IH, Oosterhout van AJM, Nawijn MC. A specific DAMP profile identifies susceptibility to smoke induced airway inflammation. Eur Respir J 43: 1183-1186, 2014.
26. Rabe KF, Hurd S, Anzueto A, Barnes PJ, Buist SA, Calverley P, Fukuchi Y, Jenkins C, Rodriguez-Roisin R, van Weel C, Zielinski J, Global Initiative for Chronic Obstructive Lung Disease. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. Am J Respir Crit Care Med 176: 532-555, 2007.
27. Shirogane T, Fukada T, Muller JM, Shima DT, Hibi M, Hirano T. Synergistic roles for Pim-1 and c-Myc in STAT3-mediated cell cycle progression and antiapoptosis. Immunity 11: 709-719, 1999.
28. Slebos DJ, Ryter SW, van der Toorn M, Liu F, Guo F, Baty CJ, Karlsson JM, Watkins SC, Kim HP, Wang X, Lee JS, Postma DS, Kauffman HF, Choi AM. Mitochondrial localization and function of heme oxygenase-1 in cigarette smoke-induced cell death. Am J Respir Cell Mol Biol 36: 409-417, 2007.
29. Thatcher TH, McHugh NA, Egan RW, Chapman RW, Hey JA, Turner CK, Redonnet MR, Seweryniak KE, Sime PJ, Phipps RP. Role of CXCR2 in cigarette smoke-induced lung inflammation. Am J Physiol Lung Cell Mol Physiol 289: L322-L328, 2005.
30. Toorn M, Slebos DJ, de Bruin HG, Gras R, Rezayat D, Jorge L, Sandra K, Oosterhout AJ. Critical role of aldehydes in cigarette smoke-induced acute airway inflammation (Abstract). Respir Res 14: 45, 2013.
31. van der Toorn M, Slebos DJ, de Bruin HG, Leuvenink HG, Bakker SJ, Gans RO, Koeter GH, van Oosterhout AJ, Kauffman HF. Cigarette smoke-induced blockade of the mitochondrial respiratory chain switches lung epithelial cell apoptosis into necrosis. Am J Physiol Lung Cell Mol Physiol 292: L1211-L1218, 2007.
32. van der Vaart H, Postma DS, Timens W, Hylkema MN, Willemse BW, Boezen HM, Vonk JM, de Reus DM, Kauffman HF, ten Hacken NH. Acute effects of cigarette smoking on inflammation in healthy intermittent smokers. Respir Res 6: 22, 2005.
33. Vayssier M, Banzet N, Francois D, Bellmann K, Polla BS. Tobacco smoke induces both apoptosis and necrosis in mammalian cells: differential effects of HSP70. Am J Physiol Lung Cell Mol Physiol 275: L771-L779, 1998.
34. Vlahos R, Bozinovski S, Jones JE, Powell J, Gras J, Lilja A, Hansen MJ, Gualano RC, Irving L, Anderson GP. Differential protease, innate immunity, and NF-B induction profiles during lung inflammation induced by subchronic cigarette smoke exposure in mice. Am J Physiol Lung Cell Mol Physiol 290: L931-L945, 2006.
35. Warnecke-Eberz U, Bollschweiler E, Drebber U, Pohl A, Baldus SE, Hoelscher AH, Metzger R. Frequent down-regulation of pim-1 mRNA expression in non-small cell lung cancer is associated with lymph node metastases. Oncol Rep 20: 619-624, 2008.
36. Wickenden JA, Clarke MC, Rossi AG, Rahman I, Faux SP, Donaldson K, MacNee W. Cigarette smoke prevents apoptosis through inhibition of caspase activation and induces necrosis. Am J Respir Cell Mol Biol 29: 562-570, 2003.
37. Yao H, Edirisinghe I, Rajendrasozhan S, Yang SR, Caito S, Adenuga D, Rahman I. Cigarette smoke-mediated inflammatory and oxidative responses are strain-dependent in mice. Am J Physiol Lung Cell Mol Physiol 294: L1174-L1186, 2008.