Lung tissue proteomics identifies elevated transglutaminase 2 levels in stable chronic obstructive pulmonary disease

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 310, Issue 11, 2016, Pages L1155-L1165

  Ohlmeier, Steffen ^a   Nieminen, Pentti ^a   Gao, Jing ^b   Kanerva, Tinja ^b   Rönty, Mikko ^c   Toljamo, Tuula ^d   Bergmann, Ulrich ^a   Mazur, Witold ^b   Pulkkinen, Ville ^b  

^a UNIVERSITY OF OULU   (Finland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d LAPLAND CENTRAL HOSPITAL   (Finland)

Author keywords

Chronic obstructive pulmonary disease (COPD); Difference gel electrophoresis (DIGE); Idiopathic pulmonary fibrosis (IPF); Lung tissue; Two dimensional gel electrophoresis (2 DE); 1 antitrypsin deficiency (AATD)

Indexed keywords

ALPHA 1 ANTITRYPSIN; CATHEPSIN D; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; CYSTEINE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; TRIPEPTIDYL PEPTIDASE I; GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTEOME;

ADULT; AGED; ALPHA 1 ANTITRYPSIN DEFICIENCY; ARTICLE; CHRONIC COUGH; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; CORRELATIONAL STUDY; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FIBROSING ALVEOLITIS; GENE EXPRESSION PROFILING; HUMAN; HUMAN TISSUE; LUNG FUNCTION; LUNG PARENCHYMA; LUNG TRANSPLANTATION; MAJOR CLINICAL STUDY; MALE; MASS SPECTROMETRY; MIDDLE AGED; PLASMA; PRIORITY JOURNAL; PROTEOMICS; SMOKING; SPUTUM; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; WESTERN BLOTTING; ADVERSE EFFECTS; BLOOD; CASE CONTROL STUDY; ENZYMOLOGY; LUNG; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY;

AGED; CASE-CONTROL STUDIES; FEMALE; GTP-BINDING PROTEINS; HUMANS; LUNG; MALE; MIDDLE AGED; PROTEOME; PROTEOMICS; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; SMOKING; TRANSGLUTAMINASES;

EID: 84979221358     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00021.2016     Document Type: Article

References (40)

1. Almansa R, Socias L, Sanchez-Garcia M, Martin-Loeches I, del Olmo M, Andaluz-Ojeda D, Bobillo F, Rico L, Herrero A, Roig V, San-Jose CA, Rosich S, Barbado J, Disdier C, de Lejarazu RO, Gallegos MC, Fernandez V, Bermejo-Martin JF. Critical COPD respiratory illness is linked to increased transcriptomic activity of neutrophil proteases genes. BMC Res Notes 5: 401, 2012.
2. Casado B, Iadarola P, Pannell LK, Luisetti M, Corsico A, Ansaldo E, Ferrarotti I, Boschetto P, Baraniuk JN. Protein expression in sputum of smokers and chronic obstructive pulmonary disease patients: a pilot study by CapLC-ESI-Q-TOF. J Proteome Res 6: 4615-4623, 2007.
3. Chilosi M, Poletti V, Rossi A. The pathogenesis of COPD and IPF: distinct horns of the same devil? Respir Res 13: 3, 2012.
4. Choi CM, Jang SJ, Park SY, Choi YB, Jeong JH, Kim DS, Kim HK, Park KS, Nam BH, Kim HR, Kim SY, Hong KM. Transglutaminase 2 as an independent prognostic marker for survival of patients with nonadenocarcinoma subtype of non-small cell lung cancer. Mol Cancer 10: 119, 2011.
5. Gao J, Ohlmeier S, Nieminen P, Toljamo T, Tiitinen S, Kanerva T, Bingle L, Araujo B, Rönty M, Hoyhtya M, Bingle CD, Mazur W, Pulkkinen V. Elevated sputum BPIFB1 levels in smokers with chronic obstructive pulmonary disease: a longitudinal study. Am J Physiol Lung Cell Mol Physiol 309: L17-L26, 2015.
6. Glare EM, Divjak M, Bailey MJ, Walters EH. β-Actin and GAPDH housekeeping gene expression in asthmatic airways is variable and not suitable for normalising mRNA levels. Thorax 57: 765-770, 2002.
7. Gray RD, MacGregor G, Noble D, Imrie M, Dewar M, Boyd AC, Innes JA, Porteous DJ, Greening AP. Sputum proteomics in inflammatory and suppurative respiratory diseases. Am J Respir Crit Care Med 178: 444-452, 2008.
8. Hallstrand TS, Wurfel MM, Lai Y, Ni Z, Gelb MH, Altemeier WA, Beyer RP, Aitken ML, Henderson WR. Transglutaminase 2, a novel regulator of eicosanoid production in asthma revealed by genome-wide expression profiling of distinct asthma phenotypes. PLoS One 5: e8583, 2010.
9. Ishii T, Wallace AM, Zhang X, Gosselink J, Abboud RT, English JC, Pare PD, Sandford AJ. Stability of housekeeping genes in alveolar macrophages from COPD patients. Eur Respir J 27: 300-306, 2006.
10. Iwamoto H, Gao J, Pulkkinen V, Toljamo T, Nieminen P, Mazur W. Soluble receptor for advanced glycation end-products and progression of airway disease. BMC Pulm Med 14: 68, 2014.
11. Keillor JW, Apperley KY, Akbar A. Inhibitors of tissue transglutaminase. Trends Pharmacol Sci 36: 32-40, 2015.
12. Kelsen SG, Duan X, Ji R, Perez O, Liu C, Merali S. Cigarette smoke induces an unfolded protein response in the human lung: a proteomic approach. Am J Respir Cell Mol Biol 38: 541-550, 2008.
13. Kinnula VL, Ishikawa N, Bergmann U, Ohlmeier S. Proteomic approaches for studying human parenchymal lung diseases. Expert Rev Proteomics 6: 619-629, 2009.
14. Lai TS, Greenberg CS. TGM2 and implications for human disease: role of alternative splicing. Front Biosci (Landmark Ed) 18: 504-519, 2013.
15. Lee EJ, In KH, Kim JH, Lee SY, Shin C, Shim JJ, Kang KH, Yoo SH, Kim CH, Kim HK, Lee SH, Uhm CS. Proteomic analysis in lung tissue of smokers and COPD patients. Chest 135: 344-352, 2009.
16. Linja-Aho A, Mazur W, Toljamo T, Nieminen P, Ohlmeier S, Rönty M, Kinnula VL. Distribution and levels of α-1-antitrypsin in the lung and plasma in smokers and chronic obstructive pulmonary disease. Apmis 121: 11-21, 2013.
17. Maiuri L, Luciani A, Giardino I, Raia V, Villella VR, D’Apolito M, Pettoello-Mantovani M, Guido S, Ciacci C, Cimmino M, Cexus ON, Londei M, Quaratino S. Tissue transglutaminase activation modulates inflammation in cystic fibrosis via PPARgamma down-regulation. J Immunol 180: 7697-7705, 2008.
18. Mazur W, Toljamo T, Ohlmeier S, Vuopala K, Nieminen P, Kobayashi H, Kinnula VL. Elevation of surfactant protein A in plasma and sputum in cigarette smokers. Eur Respir J 38: 277-284, 2011.
19. Merkel D, Rist W, Seither P, Weith A, Lenter MC. Proteomic study of human bronchoalveolar lavage fluids from smokers with chronic obstructive pulmonary disease by combining surface-enhanced laser desorption/ ionization-mass spectrometry profiling with mass spectrometric protein identification. Proteomics 5: 2972-2980, 2005.
20. Needham M, Stockley RA. α 1-Antitrypsin deficiency. 3: Clinical manifestations and natural history. Thorax 59: 441-445, 2004.
21. Nicholas BL, Skipp P, Barton S, Singh D, Bagmane D, Mould R, Angco G, Ward J, Guha-Niyogi B, Wilson S, Howarth P, Davies DE, Rennard S, O’Connor CD, Djukanovic R. Identification of lipocalin and apolipoprotein A1 as biomarkers of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 181: 1049-1060, 2010.
22. Ohlmeier S, Mazur W, Linja-Aho A, Louhelainen N, Rönty M, Toljamo T, Bergmann U, Kinnula VL. Sputum proteomics identifies elevated PIGR levels in smokers and mild-to-moderate COPD. J Proteome Res 11: 599-608, 2012.
23. Ohlmeier S, Mazur W, Salmenkivi K, Myllarniemi M, Bergmann U, Kinnula VL. Proteomic studies on receptor for advanced glycation end product variants in idiopathic pulmonary fibrosis and chronic obstructive pulmonary disease. Proteomics Clin Appl 4: 97-105, 2010.
24. Ohlmeler S, Vuolanto M, Toljamo T, Vuopala K, Salmenkivi K, Myllarniemi M, Kinnula VL. Proteomics of human lung tissue identifies surfactant protein A as a marker of chronic obstructive pulmonary disease. J Proteome Res 7: 5125-5132, 2008.
25. Olsen KC, Epa AP, Kulkarni AA, Kottmann RM, McCarthy CE, Johnson GV, Thatcher TH, Phipps RP, Sime PJ. Inhibition of transglutaminase 2, a novel target for pulmonary fibrosis, by two small electrophilic molecules. Am J Respir Cell Mol Biol 50: 737-747, 2014.
26. Paggiaro PL, Chanez P, Holz O, Ind PW, Djukanovic R, Maestrelli P, Sterk PJ. Sputum induction. Eur Respir J 20: 3s-8s, 2002.
27. Pastor MD, Nogal A, Molina-Pinelo S, Melendez R, Salinas A, De la Pena MG, Martin-Juan J, Corral J, Garcia-Carbonero R, Carnero A, Paz-Ares L. Identification of proteomic signatures associated with lung cancer and COPD. J Proteomics 89: 227-237, 2013.
28. Peltoniemi MJ, Rytila PH, Harju TH, Soini YM, Salmenkivi KM, Ruddock LW, Kinnula VL. Modulation of glutaredoxin in the lung and sputum of cigarette smokers and chronic obstructive pulmonary disease. Respir Res 7: 133, 2006.
29. Pernemalm M, De Petris L, Branca RM, Forshed J, Kanter L, Soria JC, Girard P, Validire P, Pawitan Y, van den Oord J, Lazar V, Pahlman S, Lewensohn R, Lehtio J. Quantitative proteomics profiling of primary lung adenocarcinoma tumors reveals functional perturbations in tumor metabolism. J Proteome Res 12: 3934-3943, 2013.
30. Plymoth A, Lofdahl CG, Ekberg-Jansson A, Dahlback M, Broberg P, Foster M, Fehniger TE, Marko-Varga G. Protein expression patterns associated with progression of chronic obstructive pulmonary disease in bronchoalveolar lavage of smokers. Clin Chem 53: 636-644, 2007.
31. Rytila P, Rehn T, Ilumets H, Rouhos A, Sovijarvi A, Myllarniemi M, Kinnula VL. Increased oxidative stress in asymptomatic current chronic smokers and GOLD stage 0 COPD. Respir Res 7: 69, 2006.
32. Silva GE, Sherrill DL, Guerra S, Barbee RA. Asthma as a risk factor for COPD in a longitudinal study. Chest 126: 59-65, 2004.
33. Sun Y, Mi W, Cai J, Ying W, Liu F, Lu H, Qiao Y, Jia W, Bi X, Lu N, Liu S, Qian X, Zhao X. Quantitative proteomic signature of liver cancer cells: tissue transglutaminase 2 could be a novel protein candidate of human hepatocellular carcinoma. J Proteome Res 7: 3847-3859, 2008.
34. Terracciano R, Pelaia G, Preiano M, Savino R. Asthma and COPD proteomics: Current approaches and future directions. Proteom Clin Appl 9: 203-220, 2015.
35. Toljamo T, Kaukonen M, Nieminen P, Kinnula VL. Early detection of COPD combined with individualized counselling for smoking cessation: a two-year prospective study. Scand J Prim Health Care 28: 41-46, 2010.
36. Toljamo T, Hamari A, Sotkasiira M, Nieminen P. Clinical characteristics of COPD syndrome: a 6-year follow-up study of adult smokers. Ann Med 47: 399-405, 2015.
37. Tu CJ, Mammen MJ, Li J, Shen XM, Jiang XS, Hu Q, Wang JM, Sethi S, Qu J. Large-scale, ion-current-based proteomics investigation of bronchoalveolar lavage fluid in chronic obstructive pulmonary disease patients. J Proteome Res 13: 627-639, 2014.
38. Vestbo J, Hurd SS, Agusti AG, Jones PW, Vogelmeier C, Anzueto A, Barnes PJ, Fabbri LM, Martinez FJ, Nishimura M, Stockley RA, Sin DD, Rodriguez-Roisin R. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. Am J Respir Crit Care Med 187: 347-365, 2013.
39. Witsch TJ, Niess G, Sakkas E, Likhoshvay T, Becker S, Herold S, Mayer K, Vadasz I, Roberts JD Jr, Seeger W, Morty RE. Transglutaminase 2: a new player in bronchopulmonary dysplasia? Eur Respir J 44: 109-121, 2014.
40. Young RP, Hopkins RJ, Christmas T, Black PN, Metcalf P, Gamble GD. COPD prevalence is increased in lung cancer, independent of age, sex and smoking history. Eur Respir J 34: 380-386, 2009.