Compromised peroxisomes in idiopathic pulmonary fibrosis, a vicious cycle inducing a higher fibrotic response via TGF-β signaling

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 16, 2015, Pages E2048-E2057

  Oruqaj, Gani ^a   Karnati, Srikanth ^a   Vijayan, Vijith ^a   Kotarkonda, Lakshmi Kanth ^a   Boateng, Eistine ^a   Zhang, Wenming ^b   Ruppert, Clemens ^c,d   Günther, Andreas ^c,d   Shi, Wei ^b   Baumgart Vogt, Eveline ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b CHILDREN S HOSPITAL LOS ANGELES   (United States)

^c Fachbereich Medizin der Universitat Marburg   (Germany)

^d JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

Author keywords

Fibrosis; Inflammation; Lung; Peroxisome; TGF 1

Indexed keywords

CIPROFIBRATE; COLLAGEN; CYTOKINE; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR AGONIST; PIRINIXIC ACID; RECOMBINANT INTERLEUKIN 6; RECOMBINANT TRANSFORMING GROWTH FACTOR BETA1; RECOMBINANT TUMOR NECROSIS FACTOR ALPHA; SMAD PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR AP 1; AUTACOID; COLLAGEN TYPE 1; INTERLEUKIN 6; MEMBRANE PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEX13 PROTEIN, HUMAN; REACTIVE OXYGEN METABOLITE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOGENESIS; CELL DIFFERENTIATION; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FIBROSING ALVEOLITIS; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; LIPID METABOLISM; LUNG FIBROBLAST; LUNG FIBROSIS; MALE; MOLECULAR PATHOLOGY; MOUSE; MYOFIBROBLAST; NONHUMAN; OXIDATION REDUCTION REACTION; PATHOGENESIS; PEROXISOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; WESTERN BLOTTING; AGONISTS; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; DISEASE MODEL; FIBROBLAST; GENE SILENCING; LUNG; METABOLISM; MIDDLE AGED; PATHOLOGY; SIGNAL TRANSDUCTION;

MUS;

ANIMALS; COLLAGEN TYPE I; DISEASE MODELS, ANIMAL; DOWN-REGULATION; FEMALE; FIBROBLASTS; GENE KNOCKDOWN TECHNIQUES; HUMANS; IDIOPATHIC PULMONARY FIBROSIS; INFLAMMATION MEDIATORS; INTERLEUKIN-6; LIPID METABOLISM; LUNG; MALE; MEMBRANE PROTEINS; MICE, INBRED C57BL; MIDDLE AGED; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; PEROXISOMES; PPAR ALPHA; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SMAD PROTEINS; TRANSCRIPTION FACTOR AP-1; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84928243126     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1415111112     Document Type: Article

References (40)

1. Cui Y, et al. (2011) Oxidative stress contributes to the induction and persistence of TGF-β1 induced pulmonary fibrosis. Int J Biochem Cell Biol 43(8):1122-1133.
2. Katzenstein AL, Myers JL (1998) Idiopathic pulmonary fibrosis: Clinical relevance of pathologic classification. Am J Respir Crit Care Med 157(4 Pt 1):1301-1315.
3. Kuhn C, McDonald JA (1991) The roles of the myofibroblast in idiopathic pulmonary fibrosis. Ultrastructural and immunohistochemical features of sites of active extracellular matrix synthesis. Am J Pathol 138(5):1257-1265.
4. Pardo A, Selman M (2002) Molecular mechanisms of pulmonary fibrosis. Front Biosci 7: d1743-1761.
5. Warburton D, Shi W, Xu B (2013) TGF-β-Smad3 signaling in emphysema and pulmonary fibrosis: An epigenetic aberration of normal development? Am J Physiol Lung Cell Mol Physiol 304(2):L83-L85.
6. Zhao J, et al. (2002) Smad3 deficiency attenuates bleomycin-induced pulmonary fibrosis in mice. Am J Physiol Lung Cell Mol Physiol 282(3):L585-L593.
7. Sullivan DE, Ferris M, Nguyen H, Abboud E, Brody AR (2009) TNF-alpha induces TGF-beta1 expression in lung fibroblasts at the transcriptional level via AP-1 activation. J Cell Mol Med 13(8B):1866-1876.
8. Karnati S, Baumgart-Vogt E (2008) Peroxisomes in mouse and human lung: Their involvement in pulmonary lipid metabolism. Histochem Cell Biol 130(4):719-740.
9. Karnati S, Baumgart-Vogt E (2009) Peroxisomes in airway epithelia and future prospects of these organelles for pulmonary cell biology. Histochem Cell Biol 131(4):447-454.
10. Ahlemeyer B, Gottwald M, Baumgart-Vogt E (2012) Deletion of a single allele of the Pex11β gene is sufficient to cause oxidative stress, delayed differentiation and neuronal death in mouse brain. Dis Model Mech 5(1):125-140.
11. Steinberg SJ, et al. (2006) Peroxisome biogenesis disorders. Biochim Biophys Acta 1763(12):1733-1748.
12. Rahman I, Swarska E, Henry M, Stolk J, MacNee W (2000) Is there any relationship between plasma antioxidant capacity and lung function in smokers and in patients with chronic obstructive pulmonary disease? Thorax 55(3):189-193.
13. Li X, et al. (2002) PEX11 beta deficiency is lethal and impairs neuronal migration but does not abrogate peroxisome function. Mol Cell Biol 22(12):4358-4365.
14. Boor P, et al. (2011) The peroxisome proliferator-activated receptor-α agonist, BAY PP1, attenuates renal fibrosis in rats. Kidney Int 80(11):1182-1197.
15. Rahman I, MacNee W (2000) Regulation of redox glutathione levels and gene transcription in lung inflammation: Therapeutic approaches. Free Radic Biol Med 28(9):1405-1420.
16. Grant P, et al. (2013) The biogenesis protein PEX14 is an optimal marker for the identification and localization of peroxisomes in different cell types, tissues, and species in morphological studies. Histochem Cell Biol 140(4):423-442.
17. Baarine M, et al. (2012) Evidence of oxidative stress in very long chain fatty acid - treated oligodendrocytes and potentialization of ROS production using RNA interference-directed knockdown of ABCD1 and ACOX1 peroxisomal proteins. Neuroscience 213:1-18.
18. Beier K, Völkl A, Fahimi HD (1997) TNF-alpha downregulates the peroxisome proliferator activated receptor-alpha and the mRNAs encoding peroxisomal proteins in rat liver. FEBS Lett 412(2):385-387.
19. Gäbele E, et al. (2009) TNFalpha is required for cholestasis-induced liver fibrosis in the mouse. Biochem Biophys Res Commun 378(3):348-353.
20. Verjee LS, et al. (2013) Unraveling the signaling pathways promoting fibrosis in Dupuytren's disease reveals TNF as a therapeutic target. Proc Natl Acad Sci USA 110(10):E928-E937.
21. Junn E, et al. (2000) Requirement of hydrogen peroxide generation in TGF-beta 1 signal transduction in human lung fibroblast cells: Involvement of hydrogen peroxide and Ca2+ in TGF-beta 1-induced IL-6 expression. J Immunol 165(4):2190-2197.
22. Verrecchia F, et al. (2001) Smad3/AP-1 interactions control transcriptional responses to TGF-beta in a promoter-specific manner. Oncogene 20(26):3332-3340.
23. Rajasekaran S, Vaz M, Reddy SP (2012) Fra-1/AP-1 transcription factor negatively regulates pulmonary fibrosis in vivo. PLoS ONE 7(7):e41611.
24. Roy S, et al. (2010) Fra-2 mediates oxygen-sensitive induction of transforming growth factor beta in cardiac fibroblasts. Cardiovasc Res 87(4):647-655.
25. Liu W, et al. (2013) Antiflammin-1 attenuates bleomycin-induced pulmonary fibrosis in mice. Respir Res 14:101.
26. Pantelidis P, Fanning GC, Wells AU, Welsh KI, Du Bois RM (2001) Analysis of tumor necrosis factor-alpha, lymphotoxin-alpha, tumor necrosis factor receptor II, and interleukin-6 polymorphisms in patients with idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 163(6):1432-1436.
27. Qiu Z, Fujimura M, Kurashima K, Nakao S, Mukaida N (2004) Enhanced airway inflammation and decreased subepithelial fibrosis in interleukin 6-deficient mice following chronic exposure to aerosolized antigen. Clin Exp Allergy 34(8):1321-1328.
28. Saito F, et al. (2008) Role of interleukin-6 in bleomycin-induced lung inflammatory changes in mice. Am J Respir Cell Mol Biol 38(5):566-571.
29. Fourtounis J, et al. (2012) Gene expression profiling following NRF2 and KEAP1 siRNA knockdown in human lung fibroblasts identifies CCL11/Eotaxin-1 as a novel NRF2 regulated gene. Respir Res 13:92.
30. Ogata T, et al. (2002) Stimulation of peroxisome-proliferator-activated receptor alpha (PPAR alpha) attenuates cardiac fibrosis and endothelin-1 production in pressure-overloaded rat hearts. Clin Sci (Lond) 103(Suppl 48):284S-288S.
31. Genovese T, et al. (2005) Role of endogenous and exogenous ligands for the peroxisome proliferator-activated receptor alpha in the development of bleomycin-induced lung injury. Shock 24(6):547-555.
32. Kintscher U, et al. (2002) PPARalpha inhibits TGF-beta-induced beta5 integrin transcription in vascular smooth muscle cells by interacting with Smad4. Circ Res 91(11):e35-e44.
33. Shimizu M, Takeshita A, Tsukamoto T, Gonzalez FJ, Osumi T (2004) Tissue-selective, bidirectional regulation of PEX11 alpha and perilipin genes through a common peroxisome proliferator response element. Mol Cell Biol 24(3):1313-1323.
34. Colasante C, Chen J, Ahlemeyer B, Baumgart-Vogt E (2015) Peroxisomes in cardiomyocytes and the peroxisome / peroxisome proliferator-activated receptor-loop. Thromb Haemost 113(3):452-463.
35. Chytil A, Magnuson MA, Wright CV, Moses HL (2002) Conditional inactivation of the TGF-beta type II receptor using Cre:Lox. Genesis 32(2):73-75.
36. Sauer B (1993) Manipulation of transgenes by site-specific recombination: Use of Cre recombinase. Methods Enzymol 225:890-900.
37. Bivas-Benita M, Zwier R, Junginger HE, Borchard G (2005) Non-invasive pulmonary aerosol delivery in mice by the endotracheal route. Eur J Pharm Biopharm 61(3):214-218.
38. Nenicu A, et al. (2007) Peroxisomes in human and mouse testis: Differential expression of peroxisomal proteins in germ cells and distinct somatic cell types of the testis. Biol Reprod 77(6):1060-1072.
39. Vijayan V, Baumgart-Vogt E, Naidu S, Qian G, Immenschuh S (2011) Bruton's tyrosine kinase is required for TLR-dependent heme oxygenase-1 gene activation via Nrf2 in macrophages. J Immunol 187(2):817-827.
40. Ahlemeyer B, Neubert I, Kovacs WJ, Baumgart-Vogt E (2007) Differential expression of peroxisomal matrix and membrane proteins during postnatal development of mouse brain. J Comp Neurol 505(1):1-17.