Browse > Article
http://dx.doi.org/10.4046/trd.2010.69.5.337

The Role of Transglutaminase-2 in Fibroproliferation after Lipopolysaccharide-induced Acute Lung Injury  

Kim, Je-Hyeong (Division of Pulmonary, Sleep and Critical Care Medicine, Department of Internal Medicine, Korea University Ansan Hospital)
Publication Information
Tuberculosis and Respiratory Diseases / v.69, no.5, 2010 , pp. 337-347 More about this Journal
Abstract
Background: Transglutaminase-2 (TG-2) has been reported to play an important role in the process of fibrosis. However, TG-2 studies on fibroproliferation of acute lung injury (ALI) are absent. The purpose of this study was to investigate the role of TG-2 in the fibroproliferation of lipopolysaccharide (LPS)-induced ALI. Methods: The male C57BL/6 mice of 5 weeks age were divided into 3 groups; control group (n=30) in which $50{\mu}L$ of saline was given intratracheally (IT), LPS group (n=30) in which LPS 0.5 mg/kg/$50{\mu}L$ of saline was given IT, and LPS+Cyst group treated with intraperitoneal 200 mg/kg of cystamine, competitive inhibitor of TG-2, after induction of ALI by LPS. TG-2 activity and nuclear factor $(NF)-{\kappa}B$ were measured in lung tissue homogenate. Tumor necrosis factor (TNF)-${\alpha}$, interleukin (IL)-$1{\beta}$, IL-6, myeloperoxidase (MPO), and transforming growth factor (TGF)-${\beta}1$ were measured using bronchoalveolar lavage fluids. Histopathologic ALI score and Mallory's phosphotunistic acid hematoxylin (PTAH) for collagen and fibronectin deposition were performed. Results: The TG-2 activities in the LPS group were significantly higher than the control and LPS+Cyst groups (p<0.05). The TNF-${\alpha}$ and IL-$1{\beta}$ concentrations and $NF-{\kappa}B$ activity were lower in the LPS+Cyst group than the LPS group (p<0.05). The LPS+Cyst group showed lower MPO, ALI score, TGF-${\beta}1$ concentration, and Mallory's PTAH stain than the LPS group, but the differences were not significant (p>0.05). Conclusion: Inhibition of TG-2 activity in the LPS-induced ALI prevented early inflammatory parameters, but had limited effects on late ALI and fibroproliferative parameters.
Keywords
Acute Lung Injury; Lipopolysaccharides; Inflammation; Fibrosis;
Citations & Related Records

Times Cited By SCOPUS : 0
연도 인용수 순위
  • Reference
1 Shweke N, Boulos N, Jouanneau C, Vandermeersch S, Melino G, Dussaule JC, et al. Tissue transglutaminase contributes to interstitial renal fibrosis by favoring accumulation of fibrillar collagen through TGF-beta activation and cell infiltration. Am J Pathol 2008;173:631-42.   DOI   ScienceOn
2 Suh GY, Ham HS, Lee SH, Choi JC, Koh WJ, Kim SY, et al. A Peptide with anti-transglutaminase activity decreases lipopolysaccharide-induced lung inflammation in mice. Exp Lung Res 2006;32:43-53.   DOI   ScienceOn
3 Lee ZW, Kwon SM, Kim SW, Yi SJ, Kim YM, Ha KS. Activation of in situ tissue transglutaminase by intracellular reactive oxygen species. Biochem Biophys Res Commun 2003;305:633-40.   DOI   ScienceOn
4 Kuncio GS, Tsyganskaya M, Zhu J, Liu SL, Nagy L, Thomazy V, et al. TNF-alpha modulates expression of the tissue transglutaminase gene in liver cells. Am J Physiol 1998;274:G240-5.
5 Shin DM, Jeon JH, Kim CW, Cho SY, Kwon JC, Lee HJ, et al. Cell type-specific activation of intracellular transglutaminase 2 by oxidative stress or ultraviolet irradiation: implications of transglutaminase 2 in age-related cataractogenesis. J Biol Chem 2004;279:15032-9.   DOI   ScienceOn
6 Scott KF, Meyskens FL Jr, Russell DH. Retinoids increase transglutaminase activity and inhibit ornithine decarboxylase activity in Chinese hamster ovary cells and in melanoma cells stimulated to differentiate. Proc Natl Acad Sci U S A 1982;79:4093-7.   DOI   ScienceOn
7 Esposito C, Paparo F, Caputo I, Porta R, Salvati VM, Mazzarella G, et al. Expression and enzymatic activity of small intestinal tissue transglutaminase in celiac disease. Am J Gastroenterol 2003;98:1813-20.   DOI   ScienceOn
8 Lee J, Kim YS, Choi DH, Bang MS, Han TR, Joh TH, et al. Transglutaminase 2 induces nuclear factor-kappaB activation via a novel pathway in BV-2 microglia. J Biol Chem 2004;279:53725-35.   DOI   ScienceOn
9 Griffin M, Smith LL, Wynne J. Changes in transglutaminase activity in an experimental model of pulmonary fibrosis induced by paraquat. Br J Exp Pathol 1979;60:653-61.
10 Tomashefski JF Jr. Pulmonary pathology of acute respiratory distress syndrome. Clin Chest Med 2000;21:435-66.   DOI   ScienceOn
11 Dhainaut JF, Charpentier J, Chiche JD. Transforming growth factor-beta: a mediator of cell regulation in acute respiratory distress syndrome. Crit Care Med 2003;31 Suppl 4:S258-64.   DOI
12 Chesnutt AN, Matthay MA, Tibayan FA, Clark JG. Early detection of type III procollagen peptide in acute lung injury. Pathogenetic and prognostic significance. Am J Respir Crit Care Med 1997;156:840-5.   DOI   ScienceOn
13 Steinberg KP, Hudson LD. Acute lung injury and acute respiratory distress syndrome: the clinical syndrome. Clin Chest Med 2000;21:401-17.   DOI   ScienceOn
14 Martin C, Papazian L, Payan MJ, Saux P, Gouin F. Pulmonary fibrosis correlates with outcome in adult respiratory distress syndrome: a study in mechanically ventilated patients. Chest 1995;107:196-200.   DOI   ScienceOn
15 Grenard P, Bates MK, Aeschlimann D. Evolution of transglutaminase genes: identification of a transglutaminase gene cluster on human chromosome 15q15. Structure of the gene encoding transglutaminase X and a novel gene family member, transglutaminase Z. J Biol Chem 2001;276:33066-78.   DOI   ScienceOn
16 Park KC, Chung KC, Kim YS, Lee J, Joh TH, Kim SY. Transglutaminase 2 induces nitric oxide synthesis in BV-2 microglia. Biochem Biophys Res Commun 2004; 323:1055-62.   DOI   ScienceOn
17 Kim JH, Suk MH, Yoon DW, Kim HY, Jung KH, Kang EH, et al. Inflammatory and transcriptional roles of poly (ADP-ribose) polymerase in ventilator-induced lung injury. Crit Care 2008;12:R108.   DOI
18 Annes JP, Munger JS, Rifkin DB. Making sense of latent TGFbeta activation. J Cell Sci 2003;116:217-24.   DOI   ScienceOn
19 Shin DM, Jeon JH, Kim CW, Cho SY, Lee HJ, Jang GY, et al. TGFbeta mediates activation of transglutaminase 2 in response to oxidative stress that leads to protein aggregation. FASEB J 2008;22:2498-507.   DOI   ScienceOn
20 Verderio EA, Johnson T, Griffin M. Tissue transglutaminase in normal and abnormal wound healing: review article. Amino Acids 2004;26:387-404.
21 Rojas M, Woods CR, Mora AL, Xu J, Brigham KL. Endotoxin-induced lung injury in mice: structural, functional, and biochemical responses. Am J Physiol Lung Cell Mol Physiol 2005;288:L333-41.
22 Jeitner TM, Delikatny EJ, Ahlqvist J, Capper H, Cooper AJ. Mechanism for the inhibition of transglutaminase 2 by cystamine. Biochem Pharmacol 2005;69:961-70.   DOI   ScienceOn
23 Johnson TS, Fisher M, Haylor JL, Hau Z, Skill NJ, Jones R, et al. Transglutaminase inhibition reduces fibrosis and preserves function in experimental chronic kidney disease. J Am Soc Nephrol 2007;18:3078-88.   DOI   ScienceOn
24 Aeschlimann D, Thomazy V. Protein crosslinking in assembly and remodelling of extracellular matrices: the role of transglutaminases. Connect Tissue Res 2000;41: 1-27.   DOI   ScienceOn
25 Johnson TS, Skill NJ, El Nahas AM, Oldroyd SD, Thomas GL, Douthwaite JA, et al. Transglutaminase transcription and antigen translocation in experimental renal scarring. J Am Soc Nephrol 1999;10:2146-57.
26 Mirza A, Liu SL, Frizell E, Zhu J, Maddukuri S, Martinez J, et al. A role for tissue transglutaminase in hepatic injury and fibrogenesis, and its regulation by NF-kappaB. Am J Physiol 1997;272:G281-8.
27 Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 2000;342:1334-49.   DOI   ScienceOn
28 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;13:4328-32.   DOI
29 Kim SY, Jeitner TM, Steinert PM. Transglutaminases in disease. Neurochem Int 2002;40:85-103.   DOI   ScienceOn
30 Rubenfeld GD, Caldwell E, Peabody E, Weaver J, Martin DP, Neff M, et al. Incidence and outcomes of acute lung injury. N Engl J Med 2005;353:1685-93.   DOI   ScienceOn
31 Desai SR, Wells AU, Rubens MB, Evans TW, Hansell DM. Acute respiratory distress syndrome: CT abnormalities at long-term follow-up. Radiology 1999;210:29-35.   DOI
32 McHugh LG, Milberg JA, Whitcomb ME, Schoene RB, Maunder RJ, Hudson LD. Recovery of function in survivors of the acute respiratory distress syndrome. Am J Respir Crit Care Med 1994;150:90-4.   DOI   ScienceOn
33 Davidson TA, Caldwell ES, Curtis JR, Hudson LD, Steinberg KP. Reduced quality of life in survivors of acute respiratory distress syndrome compared with critically ill control patients. JAMA 1999;281:354-60.   DOI   ScienceOn
34 Herridge MS, Cheung AM, Tansey CM, Matte-Martyn A, Diaz-Granados N, Al-Saidi F, et al. One-year outcomes in survivors of the acute respiratory distress syndrome. N Engl J Med 2003;348:683-93.   DOI   ScienceOn
35 Armstrong L, Thickett DR, Mansell JP, Ionescu M, Hoyle E, Billinghurst RC, et al. Changes in collagen turnover in early acute respiratory distress syndrome. Am J Respir Crit Care Med 1999;160:1910-5.   DOI   ScienceOn
36 Roberts ES, Zandonatti MA, Watry DD, Madden LJ, Henriksen SJ, Taffe MA, et al. Induction of pathogenic sets of genes in macrophages and neurons in Neuro- AIDS. Am J Pathol 2003;162:2041-57.   DOI   ScienceOn
37 Marshall RP, Bellingan G, Webb S, Puddicombe A, Goldsack N, McAnulty RJ, et al. Fibroproliferation occurs early in the acute respiratory distress syndrome and impacts on outcome. Am J Respir Crit Care Med 2000;162:1783-8.   DOI   ScienceOn
38 Griffin M, Casadio R, Bergamini CM. Transglutaminases: nature's biological glues. Biochem J 2002;368:377-96.   DOI   ScienceOn
39 Folk JE, Finlayson JS. The epsilon-(gamma-glutamyl)lysine crosslink and the catalytic role of transglutaminases. Adv Protein Chem 1977;31:1-133.   DOI
40 Lorand L, Weissmann LB, Epel DL, Bruner-Lorand J. Role of the intrinsic transglutaminase in the $Ca^{2+}$-mediated crosslinking of erythrocyte proteins. Proc Natl Acad Sci U S A 1976;73:4479-81.   DOI   ScienceOn