Secreted protein acidic and rich in cysteine (SPARC) is upregulated by transforming growth factor (TGF)-β and is required for TGF-β-induced hydrogen peroxide production in fibroblasts

Fibrogenesis and Tissue Repair

Volumn 6, Issue 1, 2013, Pages

  Shibata, Saiko ^a   Ishiyama, Junichi ^a  

^a KYORIN PHARMACEUTICAL CO LTD   (Japan)

Author keywords

Fibroblast; Hydrogen peroxide; Pulmonary fibrosis; SPARC; TGF

Indexed keywords

ACETYLCYSTEINE; HYDROGEN PEROXIDE; INTEGRIN LINKED KINASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 14; OSTEONECTIN; PHOSPHATIDYLINOSITOL 3 KINASE; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENUATION; CELL ACTIVATION; CELL DAMAGE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; FETUS; FIBROSING ALVEOLITIS; GENE EXPRESSION REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; LUNG ALVEOLUS EPITHELIUM; LUNG FIBROBLAST; MALE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; OSTEONECTIN GENE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; REGULATOR GENE; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84875654096     PISSN: None     EISSN: 17551536     Source Type: Journal    
DOI: 10.1186/1755-1536-6-6     Document Type: Article

References (47)

1. Meltzer EB, Noble PW. Idiopathic pulmonary fibrosis. Orphanet J Rare Dis 2008, 3:8. 10.1186/1750-1172-3-8, 2330030, 18366757.
2. Barbas-Filho JV, Ferreira MA, Sesso A, Kairalla RA, Carvalho CR, Capelozzi VL. Evidence of type II pneumocyte apoptosis in the pathogenesis of idiopathic pulmonary fibrosis (IFP)/usual interstitial pneumonia (UIP). J Clin Pathol 2001, 54:132-138. 10.1136/jcp.54.2.132, 1731356, 11215282.
3. Harari S, Caminati A. IPF: new insight on pathogenesis and treatment. Allergy 2010, 65:537-553. 10.1111/j.1398-9995.2009.02305.x, 20121758.
4. Thannickal VJ, Horowitz JC. Evolving concepts of apoptosis in idiopathic pulmonary fibrosis. Proc Am Thorac Soc 2006, 3:350-356. 10.1513/pats.200601-001TK, 2231523,2231523, 16738200.
5. Hardie WD, Hagood JS, Dave V, Perl AK, Whitsett JA, Korfhagen TR, Glasser S. Signaling pathways in the epithelial origins of pulmonary fibrosis. Cell Cycle 2010, 9:2769-2776. 10.4161/cc.9.14.12268, 3040960, 20676040.
6. Cantin AM, North SL, Fells GA, Hubbard RC, Crystal RG. Oxidant-mediated epithelial cell injury in idiopathic pulmonary fibrosis. J Clin Invest 1987, 79:1665-1673. 10.1172/JCI113005, 424497, 3034979.
7. Kliment CR, Oury TD. Oxidative stress, extracellular matrix targets, and idiopathic pulmonary fibrosis. Free Radic Biol Med 2010, 49:707-717. 10.1016/j.freeradbiomed.2010.04.036, 20452419.
8. Beeh KM, Beier J, Haas IC, Kornmann O, Micke P, Buhl R. Glutathione deficiency of the lower respiratory tract in patients with idiopathic pulmonary fibrosis. Eur Respir J 2002, 19:1119-1123. 10.1183/09031936.02.00262402, 12108866.
9. Meyer A, Buhl R, Magnussen H. The effect of oral N-acetylcysteine on lung glutathione levels in idiopathic pulmonary fibrosis. Eur Respir J 1994, 7:431-436. 10.1183/09031936.94.07030431, 8013597.
10. Bocchino M, Agnese S, Fagone E, Svegliati S, Grieco D, Vancheri C, Gabrielli A, Sanduzzi A, Avvedimento EV. Reactive oxygen species are required for maintenance and differentiation of primary lung fibroblasts in idiopathic pulmonary fibrosis. PLoS One 2010, 5:e14003. 10.1371/journal.pone.0014003, 2982828, 21103368.
11. Thannickal VJ, Fanburg BL. Activation of an H2O2-generating NADH oxidase in human lung fibroblasts by transforming growth factor beta 1. J Biol Chem 1995, 270:30334-30338. 10.1074/jbc.270.51.30334, 8530457.
12. Thannickal VJ, Aldweib KD, Fanburg BL. Tyrosine phosphorylation regulates H2O2 production in lung fibroblasts stimulated by transforming growth factor beta1. J Biol Chem 1998, 273:23611-23615. 10.1074/jbc.273.36.23611, 9722602.
13. Willis BC, Borok Z. TGF-beta-induced EMT: mechanisms and implications for fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol 2007, 293:L525-534. 10.1152/ajplung.00163.2007, 17631612.
14. Gharaee-Kermani M, Hu B, Phan SH, Gyetko MR. Recent advances in molecular targets and treatment of idiopathic pulmonary fibrosis: focus on TGFbeta signaling and the myofibroblast. Curr Med Chem 2009, 16:1400-1417. 10.2174/092986709787846497, 19355895.
15. Hohenester E, Sasaki T, Giudici C, Farndale RW, Bachinger HP. Structural basis of sequence-specific collagen recognition by SPARC. Proc Natl Acad Sci U S A 2008, 105:18273-18277. 10.1073/pnas.0808452105, 2587565, 19011090.
16. Bradshaw AD, Sage EH. SPARC, a matricellular protein that functions in cellular differentiation and tissue response to injury. J Clin Invest 2001, 107:1049-1054. 10.1172/JCI12939, 209289, 11342565.
17. Weaver MS, Workman G, Sage EH. The copper binding domain of SPARC mediates cell survival in vitro via interaction with integrin beta1 and activation of integrin-linked kinase. J Biol Chem 2008, 283:22826-22837. 10.1074/jbc.M706563200, 2504874, 18503049.
18. Francki A, McClure TD, Brekken RA, Motamed K, Murri C, Wang T, Sage EH. SPARC regulates TGF-beta1-dependent signaling in primary glomerular mesangial cells. J Cell Biochem 2004, 91:915-925. 10.1002/jcb.20008, 15034927.
19. Strandjord TP, Madtes DK, Weiss DJ, Sage EH. Collagen accumulation is decreased in SPARC-null mice with bleomycin-induced pulmonary fibrosis. Am J Physiol 1999, 277:L628-635.
20. Zhou X, Tan FK, Guo X, Wallis D, Milewicz DM, Xue S, Arnett FC. Small interfering RNA inhibition of SPARC attenuates the profibrotic effect of transforming growth factor beta1 in cultured normal human fibroblasts. Arthritis Rheum 2005, 52:257-261. 10.1002/art.20785, 15641096.
21. Wrana JL, Overall CM, Sodek J. Regulation of the expression of a secreted acidic protein rich in cysteine (SPARC) in human fibroblasts by transforming growth factor beta. Comparison of transcriptional and post-transcriptional control with fibronectin and type I collagen. Eur J Biochem 1991, 197:519-528. 10.1111/j.1432-1033.1991.tb15940.x, 1709099.
22. Socha MJ, Manhiani M, Said N, Imig JD, Motamed K. Secreted protein acidic and rich in cysteine deficiency ameliorates renal inflammation and fibrosis in angiotensin hypertension. Am J Pathol 2007, 171:1104-1112. 10.2353/ajpath.2007.061273, 1988862, 17717147.
23. Waghray M, Cui Z, Horowitz JC, Subramanian IM, Martinez FJ, Toews GB, Thannickal VJ. Hydrogen peroxide is a diffusible paracrine signal for the induction of epithelial cell death by activated myofibroblasts. FASEB J 2005, 19:854-856.
24. Chen F, Haigh S, Barman S, Fulton DJ. From form to function: the role of Nox4 in the cardiovascular system. Front Physiol 2012, 3:412. 3485577, 23125837.
25. Geiser T, Ishigaki M, van Leer C, Matthay MA, Broaddus VC. H(2)O(2) inhibits alveolar epithelial wound repair in vitro by induction of apoptosis. Am J Physiol Lung Cell Mol Physiol 2004, 287:L448-453. 10.1152/ajplung.00177.2003, 15121637.
26. Wallach-Dayan SB, Izbicki G, Cohen PY, Gerstl-Golan R, Fine A, Breuer R. Bleomycin initiates apoptosis of lung epithelial cells by ROS but not by Fas/FasL pathway. Am J Physiol Lung Cell Mol Physiol 2006, 290:L790-L796. 10.1152/ajplung.00300.2004, 16306138.
27. Carnesecchi S, Deffert C, Donati Y, Basset O, Hinz B, Preynat-Seauve O, Guichard C, Arbiser JL, Banfi B, Pache JC, Barazzone-Argiroffo C, Krause KH. A key role for NOX4 in epithelial cell death during development of lung fibrosis. Antioxid Redox Signal 2011, 15:607-619. 10.1089/ars.2010.3829, 3163392, 21391892.
28. Hecker L, Vittal R, Jones T, Jagirdar R, Luckhardt TR, Horowitz JC, Pennathur S, Martinez FJ, Thannickal VJ. NADPH oxidase-4 mediates myofibroblast activation and fibrogenic responses to lung injury. Nat Med 2009, 15:1077-1081. 10.1038/nm.2005, 2743335, 19701206.
29. Hagiwara SI, Ishii Y, Kitamura S. Aerosolized administration of N-acetylcysteine attenuates lung fibrosis induced by bleomycin in mice. Am J Respir Crit Care Med 2000, 162:225-231.
30. Homma S, Azuma A, Taniguchi H, Ogura T, Mochiduki Y, Sugiyama Y, Nakata K, Yoshimura K, Takeuchi M, Kudoh S. Efficacy of inhaled N-acetylcysteine monotherapy in patients with early stage idiopathic pulmonary fibrosis. Respirology 2012, 17:467-477. 10.1111/j.1440-1843.2012.02132.x, 22257422.
31. Arnold SA, Brekken RA. SPARC: a matricellular regulator of tumorigenesis. J Cell Commun Signal 2009, 3:255-273. 10.1007/s12079-009-0072-4, 2778590,2778590, 19809893.
32. Shi Q, Bao S, Song L, Wu Q, Bigner DD, Hjelmeland AB, Rich JN. Targeting SPARC expression decreases glioma cellular survival and invasion associated with reduced activities of FAK and ILK kinases. Oncogene 2007, 26:4084-4094. 10.1038/sj.onc.1210181, 17213807.
33. Vecchione C, Carnevale D, Di Pardo A, Gentile MT, Damato A, Cocozza G, Antenucci G, Mascio G, Bettarini U, Landolfi A, Iorio L, Maffei A, Lembo G. Pressure-induced vascular oxidative stress is mediated through activation of integrin-linked kinase 1/betaPIX/Rac-1 pathway. Hypertension 2009, 54:1028-1034. 10.1161/HYPERTENSIONAHA.109.136572, 19770407.
34. Bettink SI, Werner C, Chen CH, Muller P, Schirmer SH, Walenta KL, Bohm M, Laufs U, Friedrich EB. Integrin-linked kinase is a central mediator in angiotensin II type 1- and chemokine receptor CXCR4 signaling in myocardial hypertrophy. Biochem Biophys Res Commun 2010, 397:208-213. 10.1016/j.bbrc.2010.05.086, 20493167.
35. McDonald PC, Fielding AB, Dedhar S. Integrin-linked kinase-essential roles in physiology and cancer biology. J Cell Sci 2008, 121:3121-3132. 10.1242/jcs.017996, 18799788.
36. Hordijk PL. Regulation of NADPH oxidases: the role of Rac proteins. Circ Res 2006, 98:453-462. 10.1161/01.RES.0000204727.46710.5e, 16514078.
37. Thannickal VJ. Mechanisms of pulmonary fibrosis: role of activated myofibroblasts and NADPH oxidase. Fibrogenesis Tissue Repair 5 Suppl 2012, 1:23.
38. Lyle AN, Deshpande NN, Taniyama Y, Seidel-Rogol B, Pounkova L, Du P, Papaharalambus C, Lassegue B, Griendling KK. Poldip2, a novel regulator of Nox4 and cytoskeletal integrity in vascular smooth muscle cells. Circ Res 2009, 105:249-259. 10.1161/CIRCRESAHA.109.193722, 2744198, 19574552.
39. Goyal P, Weissmann N, Rose F, Grimminger F, Schafers HJ, Seeger W, Hanze J. Identification of novel Nox4 splice variants with impact on ROS levels in A549 cells. Biochem Biophys Res Commun 2005, 329:32-39. 10.1016/j.bbrc.2005.01.089, 15721269.
40. Pandey D, Chen F, Patel A, Wang CY, Dimitropoulou C, Patel VS, Rudic RD, Stepp DW, Fulton DJ. SUMO1 negatively regulates reactive oxygen species production from NADPH oxidases. Arterioscler Thromb Vasc Biol 2011, 31:1634-1642. 10.1161/ATVBAHA.111.226621, 3464053, 21527745.
41. Fujita T, Shiba H, Van Dyke TE, Kurihara H. Differential effects of growth factors and cytokines on the synthesis of SPARC, DNA, fibronectin and alkaline phosphatase activity in human periodontal ligament cells. Cell Biol Int 2004, 28:281-286. 10.1016/j.cellbi.2003.12.007, 15109984.
42. Mu Y, Gudey SK, Landstrom M. Non-Smad signaling pathways. Cell Tissue Res 2012, 347:11-20. 10.1007/s00441-011-1201-y, 21701805.
43. Kang HR, Lee CG, Homer RJ, Elias JA. Semaphorin 7A plays a critical role in TGF-beta1-induced pulmonary fibrosis. J Exp Med 2007, 204:1083-1093. 10.1084/jem.20061273, 2118575, 17485510.
44. Vittal R, Horowitz JC, Moore BB, Zhang H, Martinez FJ, Toews GB, Standiford TJ, Thannickal VJ. Modulation of prosurvival signaling in fibroblasts by a protein kinase inhibitor protects against fibrotic tissue injury. Am J Pathol 2005, 166:367-375. 10.1016/S0002-9440(10)62260-2, 1602319, 15681821.
45. Matsuoka H, Arai T, Mori M, Goya S, Kida H, Morishita H, Fujiwara H, Tachibana I, Osaki T, Hayashi S. A p38 MAPK inhibitor, FR-167653, ameliorates murine bleomycin-induced pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2002, 283:L103-112.
46. Li W, Fan J, Chen M, Guan S, Sawcer D, Bokoch GM, Woodley DT. Mechanism of human dermal fibroblast migration driven by type I collagen and platelet-derived growth factor-BB. Mol Biol Cell 2004, 15:294-309. 307548, 14595114.
47. Gao Z, Sasaoka T, Fujimori T, Oya T, Ishii Y, Sabit H, Kawaguchi M, Kurotaki Y, Naito M, Wada T, Ishizawa S, Kobayashi M, Nabeshima Y, Sasahara M. Deletion of the PDGFR-beta gene affects key fibroblast functions important for wound healing. J Biol Chem 2005, 280:9375-9389.