Inhibition of transglutaminase 2, a novel target for pulmonary fibrosis, by two small electrophilic molecules

American Journal of Respiratory Cell and Molecular Biology

Volumn 50, Issue 4, 2014, Pages 737-747

  Olsen, Keith C ^a   Epa, Amali P ^a   Kulkarni, Ajit A ^a   Kottmann, R Matthew ^a   McCarthy, Claire E ^a   Johnson, Gail V ^a   Thatcher, Thomas H ^a   Phipps, Richard P ^a   Sime, Patricia J ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

2 cyano 3,12 dioxooleana 1,9 dien 28 oic acid; Fibroblast; Pulmonary fibrosis; Transglutaminase 2

Indexed keywords

15 DEOXY DELTA 12,14 PROSTAGLANDIN J 2; ANTIOXIDANT; BARDOXOLONE; COLLAGEN GEL; ELECTROPHILE; FIBRONECTIN; INTEGRIN; MITOGEN ACTIVATED PROTEIN KINASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; REACTIVE OXYGEN METABOLITE; SCLEROPROTEIN; TERPENOID; UNCLASSIFIED DRUG;

ANTIFIBROTIC ACTIVITY; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; CROSS LINKING; DONOR; DRUG ACTIVITY; DRUG TARGETING; ELECTROPHILICITY; ENZYME INHIBITION; GENETIC TRANSFECTION; HUMAN; IN VITRO STUDY; LUNG FIBROSIS; PROMOTER REGION; PROTEIN EXPRESSION; WESTERN BLOTTING;

CASE-CONTROL STUDIES; CELL MOVEMENT; CELL SHAPE; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLASTS; HUMANS; IDIOPATHIC PULMONARY FIBROSIS; LUNG; MAP KINASE KINASE KINASES; MAP KINASE SIGNALING SYSTEM; MOLECULAR TARGETED THERAPY; OLEANOLIC ACID; PHOSPHORYLATION; PROSTAGLANDIN D2; PROTEIN KINASE INHIBITORS; TRANSGLUTAMINASES;

EID: 84898741590     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2013-0092OC     Document Type: Article

References (54)

1. Bjoraker JA, Ryu JH, Edwin MK, Myers JL, Tazelaar HD, Schroeder DR, Offord KP. Prognostic significance of histopathologic subsets in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 1998;157:199-203. (Pubitemid 28071283)
2. White ES, Lazar MH, Thannickal VJ. Pathogenetic mechanisms in usual interstitial pneumonia/idiopathic pulmonary fibrosis. J Pathol 2003; 201:343-354. (Pubitemid 37408254)
3. Phan SH. The myofibroblast in pulmonary fi brosis. Chest 2002;122: 286S-289S.
4. Raghu G, Collard HR, Egan JJ, Martinez FJ, Behr J, Brown KK, Colby TV, Cordier JF, Flaherty KR, Lasky JA, et al. An official ATS/ERS/JRS/ALAT statement: idiopathic pulmonary fibrosis: evidence-based guidelines for diagnosis and management. Am J Respir Crit CareMed 2011;183:788-824.
5. Chen JS, Mehta K. Tissue transglutaminase: an enzyme with a split personality. Int J Biochem Cell Biol 1999;31:817-836. (Pubitemid 29354079)
6. Akimov SS, Belkin AM. Cell-surface transglutaminase promotes fibronectin assembly via interaction with the gelatin-binding domain of fibronectin: a role in TGFbeta-dependent matrix deposition. J Cell Sci 2001;114:2989-3000. (Pubitemid 32821537)
7. Akimov SS, Belkin AM. Cell surface tissue transglutaminase is involved in adhesion and migration of monocytic cells on fibronectin. Blood 2001;98:1567-1576.
8. Akimov SS, Krylov D, Fleischman LF, Belkin AM. Tissue transglutaminase is an integrin-binding adhesion coreceptor for fibronectin. J Cell Biol 2000;148:825-838.
9. Chen R, Gao B, Huang C, Olsen B, Rotundo RF, Blumenstock F, Saba TM. Transglutaminase-mediated fibronectin multimerization in lung endothelial matrix in response to TNF-alpha. Am J Physiol Lung Cell Mol Physiol 2000;279:L161-L174. (Pubitemid 30619536)
10. Johnson TS, Griffin M, Thomas GL, Skill J, Cox A, Yang B, Nicholas B, Birckbichler PJ, Muchaneta-Kubara C, Meguid El Nahas A. The role of transglutaminase in the rat subtotal nephrectomy model of renal fibrosis. J Clin Invest 1997;99:2950-2960. (Pubitemid 27278672)
11. Johnson TS, Fisher M, Haylor JL, Hau Z, Skill NJ, Jones R, Saint R, Coutts I, Vickers ME, El Nahas AM, et al. Transglutaminase inhibition reduces fibrosis and preserves function in experimental chronic kidney disease. J Am Soc Nephrol 2007;18:3078-3088. (Pubitemid 350223968)
12. Grenard P, Bresson-Hadni S, El Alaoui S, Chevallier M, Vuitton DA, Ricard-Blum S. Transglutaminase-mediated cross-linking is involved in the stabilization of extracellular matrix in human liver fibrosis. J Hepatol 2001;35:367-375. (Pubitemid 32844191)
13. Qiu JF, Zhang ZQ, Chen W, Wu ZY. Cystamine ameliorates liver fibrosis induced by carbon tetrachloride via inhibition of tissue transglutaminase. World J Gastroenterol 2007;13:4328-4332. (Pubitemid 47377137)
14. Zhang Z, Vezza R, Plappert T, McNamara P, Lawson JA, Austin S, Pratico D, Sutton MS, FitzGerald GA. Cox-2-dependent cardiac failure in Gh/tTG transgenic mice. Circ Res 2003;92:1153-1161. (Pubitemid 36665862)
15. Olsen KC, Sapinoro RE, Kottman RM, Kulkarni AA, Iismaa SE, Johnson GV, Thatcher TH, Phipps RP, Sime PJ. Transglutaminase 2 and its role in pulmonary fibrosis. Am J Respir Crit Care Med 2011;184:699-707.
16. Oh K, Park HB, Byoun OJ, Shin DM, Jeong EM, Kim YW, Kim YS, Melino G, Kim IG, Lee DS. Epithelial transglutaminase 2 is needed for T cell interleukin-17 production and subsequent pulmonary inflammation and fibrosis in bleomycin-treated mice. J Exp Med 2011;208:1707-1719.
17. Siegel M, Khosla C. Transglutaminase 2 inhibitors and their therapeutic role in disease states. Pharmacol Ther 2007;115:232-245. (Pubitemid 47042912)
18. Burgess HA, Daugherty LE, Thatcher TH, Lakatos HF, Ray DM, Redonnet M, Phipps RP, Sime PJ. PPARgamma agonists inhibit TGF-beta induced pulmonary myofibroblast differentiation and collagen production: implications for therapy of lung fibrosis. Am J Physiol Lung Cell Mol Physiol 2005;288:L1146-L1153. (Pubitemid 40695441)
19. Ferguson HE, Kulkarni A, Lehmann GM, Garcia-Bates TM, Thatcher TH, Huxlin KR, Phipps RP, Sime PJ. Electrophilic peroxisome proliferator-activated receptor-gamma ligands have potent antifibrotic effects in human lung fibroblasts. Am J Respir Cell Mol Biol 2009;41:722-730.
20. Kulkarni AA, Thatcher TH, Olsen KC, Maggirwar SB, Phipps RP, Sime PJ. Ppar-gamma ligands repress TGFbeta-induced myofibroblast differentiation by targeting the PI3K/AKT pathway: implications for therapy of fibrosis. PLoS ONE 2011;6:e15909.
21. Genovese T, Cuzzocrea S, Di Paola R, Mazzon E, Mastruzzo C, Catalano P, Sortino M, Crimi N, Caputi AP, Thiemermann C, et al. Effect of rosiglitazone and 15-deoxy-delta12,14-prostaglandin J2 on bleomycin-induced lung injury. Eur Respir J 2005;25:225-234. (Pubitemid 40246521)
22. 2: the anti-inflammatory prostaglandin? Clin Immunol 2005;114:100-109.
23. Suh N, Wang Y, Honda T, Gribble GW, Dmitrovsky E, Hickey WF, Maue RA, Place AE, Porter DM, Spinella MJ, et al. A novel synthetic oleanane triterpenoid, 2-cyano-3,12-dioxoolean-1,9-dien-28-oic acid, with potent differentiating, antiproliferative, and anti-inflammatory activity. Cancer Res 1999;59:336-341. (Pubitemid 29048864)
24. Forman BM, Tontonoz P, Chen J, Brun RP, Spiegelman BM, Evans RM. 15-deoxy-delta 12, 14-prostaglandin J2 is a ligand for the adipocyte determination factor PPAR gamma. Cell 1995;83:803-812. (Pubitemid 3006324)
25. Kliewer SA, Lenhard JM, Willson TM, Patel I, Morris DC, Lehmann JM. A prostaglandin J2 metabolite binds peroxisome proliferator-activated receptor gamma and promotes adipocyte differentiation. Cell 1995;83:813-819. (Pubitemid 3006325)
26. Kulkarni AA, Thatcher TH, Hsiao HM, Olsen KC, Kottmann RM, Morrissette J, Wright TW, Phipps RP, Sime PJ. The triterpenoid CDDO-Me inhibits bleomycin-induced lung inflammation and fibrosis. PLoS ONE 2013;8:e63798.
27. Hsiao HM, Sapinoro RE, Thatcher TH, Croasdell A, Levy EP, Fulton RA, Olsen KC, Pollock SJ, Serhan CN, Phipps RP, et al. A novel anti-in flammatory and pro-resolving role for resolvin D1 in acute cigarette smoke-induced lung inflammation. PLoS ONE 2013;8:e58258.
28. Stephens P, Grenard P, Aeschlimann P, Langley M, Blain E, Errington R, Kipling D, Thomas D, Aeschlimann D. Crosslinking and G-protein functions of transglutaminase 2 contribute differentially to fibroblast wound healing responses. J Cell Sci 2004;117:3389-3403. (Pubitemid 39139922)
29. Ferguson HE, Thatcher TH, Olsen KC, Garcia-Bates TM, Baglole CJ, Kottmann RM, Strong ER, Phipps RP, Sime PJ. Peroxisome proliferator-activated receptor-gamma ligands induce heme oxygenase-1 in lung fibroblasts by a PPARgamma-independent, glutathione-dependent mechanism. Am J Physiol Lung Cell Mol Physiol 2009;297:L912-L919.
30. Cowley S, Paterson H, Kemp P, Marshall CJ. Activation of map kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells. Cell 1994;77:841-852. (Pubitemid 24187682)
31. Hocking DC, Sottile J, Langenbach KJ. Stimulation of integrin-mediated cell contractility by fibronectin polymerization. J Biol Chem 2000;275:10673-10682. (Pubitemid 30202135)
32. Sporn MB, Liby KT, Yore MM, Fu L, Lopchuk JM, Gribble GW. New synthetic triterpenoids: potent agents for prevention and treatment of tissue injury caused by inflammatory and oxidative stress. J Nat Prod 2011;74:537-545.
33. Akimov SS, Belkin AM. Opposing roles of Ras/Raf oncogenes and the MEK1/ERK signaling module in regulation of expression and adhesive function of surface transglutaminase. J Biol Chem 2003;278:35609-35619. (Pubitemid 37102334)
34. Antonyak MA, McNeill CJ, Wakshlag JJ, Boehm JE, Cerione RA. Activation of the Ras-ERK pathway inhibits retinoic acid-induced stimulation of tissue transglutaminase expression in NIH 3T3 cells. J Biol Chem 2003;278:15859-15866. (Pubitemid 36799701)
35. Ohori M, Kinoshita T, Yoshimura S, Warizaya M, Nakajima H, Miyake H. Role of a cysteine residue in the active site of ERK and the MAPKK family. Biochem Biophys Res Commun 2007;353: 633-637. (Pubitemid 46048715)
36. MR K, Gauldie J. Idiopathic pulmonary fibrosis: the matrix is the message. Am J Respir Crit Care Med 2011;184:627-629.
37. Milam JE, Keshamouni VG, Phan SH, Hu B, Gangireddy SR, Hogaboam CM, Standiford TJ, Thannickal VJ, Reddy RC. PPAR-gamma agonists inhibit profibrotic phenotypes in human lung fibroblasts and bleomycin-induced pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2008;294:L891-L901.
38. Tontonoz P, Spiegelman BM. Fat and beyond: the diverse biology of PPARgamma. Annu Rev Biochem 2008;77:289-312.
39. Liby K, Hock T, Yore MM, Suh N, Place AE, Risingsong R, Williams CR, Royce DB, Honda T, Honda Y, et al. The synthetic triterpenoids, CDDO and CDDO-imidazolide, are potent inducers of heme oxygenase-1 and NRF2/ARE signaling. Cancer Res 2005;65:4789-4798. (Pubitemid 40740817)
40. Pitha-Rowe I, Liby K, Royce D, Sporn M. Synthetic triterpenoids attenuate cytotoxic retinal injury: cross-talk between NRF2 and PI3K/AKT signaling through inhibition of the lipid phosphatase PTEN. Invest Ophthalmol Vis Sci 2009;50:5339-5347.
41. Baglole CJ, Sime PJ, Phipps RP. Cigarette smoke-induced expression of heme oxygenase-1 in human lung fibroblasts is regulated by intracellular glutathione. Am J Physiol Lung Cell Mol Physiol 2008; 295:L624-L636.
42. Homma S, Azuma A, Taniguchi H, Ogura T, Mochiduki Y, Sugiyama Y, Nakata K, Yoshimura K, Takeuchi M, Kudoh S, et al. Efficacy of inhaled n-acetylcysteine monotherapy in patients with early stage idiopathic pulmonary fibrosis. Respirology 2012;17:467-477.
43. Balklava Z, Verderio E, Collighan R, Gross S, Adams J, Griffin M. Analysis of tissue transglutaminase function in the migration of Swiss 3T3 fibroblasts: the active-state conformation of the enzyme does not affect cell motility but is important for its secretion. J Biol Chem 2002;277:16567-16575. (Pubitemid 34967673)
44. Yoshida K, Kuwano K, Hagimoto N, Watanabe K, Matsuba T, Fujita M, Inoshima I, Hara N. Map kinase activation and apoptosis in lung tissues from patients with idiopathic pulmonary fibrosis. J Pathol 2002;198:388-396. (Pubitemid 35277390)
45. Hu Y, Peng J, Feng D, Chu L, Li X, Jin Z, Lin Z, Zeng Q. Role of extracellular signal-regulated kinase, p38 kinase, and activator protein-1 in transforming growth factor-beta1-induced alpha smooth muscle actin expression in human fetal lung fibroblasts in vitro. Lung 2006;184:33-42.
46. Caraci F, Gili E, Calafiore M, Failla M, La Rosa C, Crimi N, Sortino MA, Nicoletti F, Copani A, Vancheri C. TGF-beta1 targets the GSK-3beta/beta-catenin pathway via ERK activation in the transition of human lung fibroblasts into myofibroblasts. Pharmacol Res 2008;57:274-282.
47. Galuppo M, Esposito E, Mazzon E, Di Paola R, Paterniti I, Impellizzeri D, Cuzzocrea S. MEK inhibition suppresses the development of lung fibrosis in the bleomycin model. Naunyn Schmiedebergs Arch Pharmacol 2011;384:21- 37.
48. KonoplevaM, Contractor R, Kurinna SM, Chen W, AndreeffM, Ruvolo PP. The novel triterpenoid CDDO-Me suppresses MAPK pathways and promotes p38 activation in acute myeloid leukemia cells. Leukemia 2005;19:1350-1354. (Pubitemid 41136327)
49. Li H, Pauza CD. Effects of 15-deoxy-delta12,14-prostaglandin J2 (15d-PGJ2) and rosiglitazone on human gammadelta2 t cells. PLoS ONE 2009;4:e7726.
50. Uchida K, Shibata T. 15-deoxy-delta(12,14)-prostaglandin J2: an electrophilic trigger of cellular responses. Chem Res Toxicol 2008; 21:138-144. (Pubitemid 351219715)
51. Yore MM, Kettenbach AN, Sporn MB, Gerber SA, Liby KT. Proteomic analysis shows synthetic oleanane triterpenoid binds to mTOR. PLoS ONE 2011;6:e22862.
52. Klock C, Diraimondo TR, Khosla C. Role of transglutaminase 2 in celiac disease pathogenesis. Semin Immunopathol 2012;34:513-522.
53. Pergola PE, Krauth M, Huff JW, Ferguson DA, Ruiz S, Meyer CJ, Warnock DG. Effect of bardoxolone methyl on kidney function in patients with T2D and stage 3b-4 CKD. Am J Nephrol 2011;33:469-476.
54. Pergola PE, Raskin P, Toto RD, Meyer CJ, Huff JW, Grossman EB, Krauth M, Ruiz S, Audhya P, Christ-Schmidt H, et al.; BEAM Study Investigators. Bardoxolone methyl and kidney function in CKD with type 2 diabetes. N Engl J Med 2011;365:327-336.