25-Hydroxycholesterol promotes fibroblast-mediated tissue remodeling through NF-κB dependent pathway

Experimental Cell Research

Volumn 319, Issue 8, 2013, Pages 1176-1186

  Ichikawa, Tomohiro ^a   Sugiura, Hisatoshi ^b   Koarai, Akira ^a   Kikuchi, Takashi ^a   Hiramatsu, Masataka ^a   Kawabata, Hiroki ^a   Akamatsu, Keiichiro ^a   Hirano, Tsunahiko ^a   Nakanishi, Masanori ^a   Matsunaga, Kazuto ^a   Minakata, Yoshiaki ^a   Ichinose, Masakazu ^b  

^a WAKAYAMA MEDICAL UNIVERSITY   (Japan)

^b TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

25 hydroxycholesterol; Fibroblast; Tissue remodeling

Indexed keywords

25 HYDROXYCHOLESTEROL; ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 1; GELATINASE A; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NEUTRALIZING ANTIBODY; PROTEIN C JUN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR RELA; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; CELL DIFFERENTIATION; CELL NUCLEUS; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX; FETUS; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG FIBROBLAST; LUNG PARENCHYMA; MYOFIBROBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 84876070841     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.02.014     Document Type: Article

References (51)

1. Busse W., Elias J., Sheppard D., Banks-Schlegel S. Airway remodeling and repair. Am. J. Respir. Crit. Care Med. 1999, 160:1035-1042.
2. Barnes P.J. Chronic obstructive pulmonary disease. N. Engl. J. Med. 2000, 343:269-280.
3. Hardie W.D., Glasser S.W., Hagood J.S. Emerging concepts in the pathogenesis of lung fibrosis. Am. J. Pathol. 2009, 175:3-16.
4. Kranenburg A.R., Willems-Widyastuti A., Moori W.J., Sterk P.J., Alagappan V.K., de Boer W.I., Sharma H.S. Enhanced bronchial expression of extracellular matrix proteins in chronic obstructive pulmonary disease. Am. J. Clin. Pathol. 2006, 126:725-735.
5. Burgel P.R. The role of small airways in obstructive airway diseases. Eur. Respir. Rev. 2011, 20:23-33.
6. Roomi M.W., Monterrey J.C., Kalinovsky T., Rath M., Niedzwiecki A. Distinct patterns of matrix metalloproteinase-2 and -9 expression in normal human cell lines. Oncol. Rep. 2009, 21:821-826.
7. Ning W., Dong Y., Sun J., Li C., Matthay M.A., Feghali-Bostwick C.A., Choi A.M. Cigarette smoke stimulates matrix metalloproteinase-2 activity via EGR-1 in human lung fibroblasts. Am. J. Respir. Cell Mol. Biol. 2007, 36:480-490.
8. Kitamura H., Cambier S., Somanath S., Barker T., Minagawa S., Markovics J., Goodsell A., Publicover J., Reichardt L., Jablons D., Wolters P., Hill A., Marks J.D., Lou J., Pittet J.F., Gauldie J., Baron J.L., Nishimura S.L. Mouse and human lung fibroblasts regulate dendritic cell trafficking, airway inflammation, and fibrosis through integrin alphavbeta8-mediated activation of TGF-beta. J. Clin. Invest. 2011, 121:2863-2875.
9. Lund E.G., Kerr T.A., Sakai J., Li W.P., Russell D.W. cDNA cloning of mouse and human cholesterol 25-hydroxylases, polytopic membrane proteins that synthesize a potent oxysterol regulator of lipid metabolism. J. Biol. Chem. 1998, 273:34316-34327.
10. Ikonen E., Jansen M. Cellular sterol trafficking and metabolism: spotlight on structure. Curr. Opin. Cell Biol. 2008, 20:371-377.
11. Schroepfer G.J. Oxysterols: modulators of cholesterol metabolism and other processes. Physiol. Rev. 2000, 80:361-554.
12. Adams C.M., Reitz J., De Brabander J.K., Feramisco J.D., Li L., Brown M.S., Goldstein J.L. Cholesterol and 25-hydroxycholesterol inhibit activation of SREBPs by different mechanisms, both involving SCAP and Insigs. J. Biol. Chem. 2004, 279:52772-52780.
13. Rosklint T., Ohlsson B.G., Wiklund O., Noren K., Hulten L.M. Oxysterols induce interleukin-1beta production in human macrophages. Eur. J. Clin. Invest. 2002, 32:35-42.
14. Erridge C., Webb D.J., Spickett C.M. 25-Hydroxycholesterol, 7beta-hydroxycholesterol and 7-ketocholesterol upregulate interleukin-8 expression independently of Toll-like receptor 1, 2, 4 or 6 signalling in human macrophages. Free Radic. Res. 2007, 41:260-266.
15. Dugas B., Charbonnier S., Baarine M., Ragot K., Delmas D., Menetrier F., Lherminier J., Malvitte L., Khalfaoui T., Bron A., Creuzot-Garcher C., Latruffe N., Lizard G. Effects of oxysterols on cell viability, inflammatory cytokines, VEGF, and reactive oxygen species production on human retinal cells: cytoprotective effects and prevention of VEGF secretion by resveratrol. Eur. J. Nutr. 2010, 49:435-446.
16. Bauman D.R., Bitmansour A.D., McDonald J.G., Thompson B.M., Liang G., Russell D.W. 25-Hydroxycholesterol secreted by macrophages in response to Toll-like receptor activation suppresses immunoglobulin A production. Proc. Natl. Acad. Sci. USA 2009, 106:16764-16769.
17. Gold E.S., Ramsey S.A., Sartain M.J., Selinummi J., Podolsky I., Rodriguez D.J., Moritz R.L., Aderem A. ATF3 protects against atherosclerosis by suppressing 25-hydroxycholesterol-induced lipid body formation. J. Exp. Med. 2012, 209:807-817.
18. Wang F., Xia W., Liu F., Li J., Wang G., Gu J. Interferon regulator factor 1/retinoic inducible gene I (IRF1/RIG-I) axis mediates 25-hydroxycholesterol-induced interleukin-8 production in atherosclerosis. Cardiovasc. Res. 2012, 93:190-199.
19. Sugiura H., Koarai A., Ichikawa T., Minakata Y., Matsunaga K., Hirano T., Akamatsu K., Yanagisawa S., Furusawa M., Uno Y., Yamasaki M., Satomi Y., Ichinose M. Increased 25-hydroxycholesterol concentrations in the lungs of patients with chronic obstructive pulmonary disease. Respirology 2012, 17:533-540.
20. H. Sugiura, H. Kawabata, T. Ichikawa, A. Koarai, S. Yanagisawa, T. Kikuchi, Y. Minakata, K. Matsunaga, M. Nakanishi, T. Hirano, K. Akamatsu, K. Furukawa, M. Ichinose, Inhibitory effects of theophylline on the peroxynitrite-augmented release of matrix metalloproteinases by lung fibroblasts, Am. J. Physiol. Lung Cell Mol. Physiol. (2012).
21. Lee K.Y., Ito K., Hayashi R., Jazrawi E.P., Barnes P.J., Adcock I.M. NF-kappaB and activator protein 1 response elements and the role of histone modifications in IL-1beta-induced TGF-beta1 gene transcription. J. Immunol. 2006, 176:603-615.
22. Hinz B., Phan S.H., Thannickal V.J., Galli A., Bochaton-Piallat M.L., Gabbiani G. The myofibroblast: one function, multiple origins. Am. J. Pathol. 2007, 170:1807-1816.
23. Leask A., Abraham D.J. TGF-beta signaling and the fibrotic response. FASEB J. 2004, 18:816-827.
24. Hinz B., Celetta G., Tomasek J.J., Gabbiani G., Chaponnier C. Alpha-smooth muscle actin expression upregulates fibroblast contractile activity. Mol. Biol. Cell 2001, 12:2730-2741.
25. Batra V., Musani A.I., Hastie A.T., Khurana S., Carpenter K.A., Zangrilli J.G., Peters S.P. Bronchoalveolar lavage fluid concentrations of transforming growth factor (TGF)-beta1, TGF-beta2, interleukin (IL)-4 and IL-13 after segmental allergen challenge and their effects on alpha-smooth muscle actin and collagen III synthesis by primary human lung fibroblasts. Clin. Exp. Allergy 2004, 34:437-444.
26. Garrett Q., Khaw P.T., Blalock T.D., Schultz G.S., Grotendorst G.R., Daniels J.T. Involvement of CTGF in TGF-beta1-stimulation of myofibroblast differentiation and collagen matrix contraction in the presence of mechanical stress. Invest. Ophthalmol. Vis. Sci. 2004, 45:1109-1116.
27. Ichikawa T., Sugiura H., Koarai A., Yanagisawa S., Kanda M., Hayata A., Furukawa K., Akamatsu K., Hirano T., Nakanishi M., Matsunaga K., Minakata Y., Ichinose M. Peroxynitrite augments fibroblast-mediated tissue remodeling via myofibroblast differentiation. Am. J. Physiol. Lung Cell Mol. Physiol. 2008, 295:L800-808.
28. Sugiura H., Ichikawa T., Koarai A., Yanagisawa S., Minakata Y., Matsunaga K., Hirano T., Akamatsu K., Ichinose M. Activation of Toll-like receptor 3 augments myofibroblast differentiation. Am. J. Respir. Cell Mol. Biol. 2009, 40:654-662.
29. Vignola A.M., Chanez P., Chiappara G., Merendino A., Pace E., Rizzo A., la Rocca A.M., Bellia V., Bonsignore G., Bousquet J. Transforming growth factor-beta expression in mucosal biopsies in asthma and chronic bronchitis. Am. J. Respir. Crit. Care Med. 1997, 156:591-599.
30. Takizawa H., Tanaka M., Takami K., Ohtoshi T., Ito K., Satoh M., Okada Y., Yamasawa F., Nakahara K., Umeda A. Increased expression of transforming growth factor-beta1 in small airway epithelium from tobacco smokers and patients with chronic obstructive pulmonary disease (COPD). Am. J. Respir. Crit. Care Med. 2001, 163:1476-1483.
31. Khalil N., Parekh T.V., O'Connor R., Antman N., Kepron W., Yehaulaeshet T., Xu Y.D., Gold L.I. Regulation of the effects of TGF-beta 1 by activation of latent TGF-beta 1 and differential expression of TGF-beta receptors (T beta R-I and T beta R-II) in idiopathic pulmonary fibrosis. Thorax 2001, 56:907-915.
32. Oikonomidi S., Kostikas K., Tsilioni I., Tanou K., Gourgoulianis K.I., Kiropoulos T.S. Matrix metalloproteinases in respiratory diseases: from pathogenesis to potential clinical implications. Curr. Med. Chem. 2009, 16:1214-1228.
33. Vignola A.M., Riccobono L., Mirabella A., Profita M., Chanez P., Bellia V., Mautino G., D'Accardi P., Bousquet J., Bonsignore G. Sputum metalloproteinase-9/tissue inhibitor of metalloproteinase-1 ratio correlates with airflow obstruction in asthma and chronic bronchitis. Am. J. Respir. Crit. Care Med. 1998, 158:1945-1950.
34. Baraldo S., Bazzan E., Zanin M.E., Turato G., Garbisa S., Maestrelli P., Papi A., Miniati M., Fabbri L.M., Zuin R., Saetta M. Matrix metalloproteinase-2 protein in lung periphery is related to COPD progression. Chest 2007, 132:1733-1740.
35. Pardo A., Selman M. Matrix metalloproteases in aberrant fibrotic tissue remodeling. Proc. Am. Thorac. Soc. 2006, 3:383-388.
36. Overall C.M., Wrana J.L., Sodek J. Transcriptional and post-transcriptional regulation of 72-kDa gelatinase/type IV collagenase by transforming growth factor-beta 1 in human fibroblasts. Comparisons with collagenase and tissue inhibitor of matrix metalloproteinase gene expression. J. Biol. Chem. 1991, 266:14064-14071.
37. Martin-Chouly C.A., Astier A., Jacob C., Pruniaux M.P., Bertrand C., Lagente V. Modulation of matrix metalloproteinase production from human lung fibroblasts by type 4 phosphodiesterase inhibitors. Life Sci. 2004, 75:823-840.
38. Atkinson J.J., Senior R.M. Matrix metalloproteinase-9 in lung remodeling. Am. J. Respir. Cell Mol. Biol. 2003, 28:12-24.
39. Moreau M., Brocheriou I., Petit L., Ninio E., Chapman M.J., Rouis M. Interleukin-8 mediates downregulation of tissue inhibitor of metalloproteinase-1 expression in cholesterol-loaded human macrophages: relevance to stability of atherosclerotic plaque. Circulation 1999, 99:420-426.
40. Vandenbroucke R.E., Dejonckheere E., Libert C. A therapeutic role for matrix metalloproteinase inhibitors in lung diseases?. Eur. Respir. J. 2011, 38:1200-1214.
41. Kelly E.A., Busse W.W., Jarjour N.N. Increased matrix metalloproteinase-9 in the airway after allergen challenge. Am. J. Respir. Crit. Care Med. 2000, 162:1157-1161.
42. Russell R.E., Culpitt S.V., DeMatos C., Donnelly L., Smith M., Wiggins J., Barnes P.J. Release and activity of matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 by alveolar macrophages from patients with chronic obstructive pulmonary disease. Am. J. Respir. Cell Mol. Biol. 2002, 26:602-609.
43. Xu L., Bai Q., Rodriguez-Agudo D., Hylemon P.B., Heuman D.M., Pandak W.M., Ren S. Regulation of hepatocyte lipid metabolism and inflammatory response by 25-hydroxycholesterol and 25-hydroxycholesterol-3-sulfate. Lipids 2010, 45:821-832.
44. Palozza P., Simone R., Catalano A., Monego G., Barini A., Mele M.C., Parrone N., Trombino S., Picci N., Ranelletti F.O. Lycopene prevention of oxysterol-induced proinflammatory cytokine cascade in human macrophages: inhibition of NF-kappaB nuclear binding and increase in PPARgamma expression. J. Nutr. Biochem. 2011, 22:259-268.
45. Hanley K., Ng D.C., He S.S., Lau P., Min K., Elias P.M., Bikle D.D., Mangelsdorf D.J., Williams M.L., Feingold K.R. Oxysterols induce differentiation in human keratinocytes and increase Ap-1-dependent involucrin transcription. J. Invest. Dermatol. 2000, 114:545-553.
46. Bonniaud P., Kolb M., Galt T., Robertson J., Robbins C., Stampfli M., Lavery C., Margetts P.J., Roberts A.B., Gauldie J. Smad3 null mice develop airspace enlargement and are resistant to TGF-beta-mediated pulmonary fibrosis. J. Immunol. 2004, 173:2099-2108.
47. Kenyon N.J., Ward R.W., McGrew G., Last J.A. TGF-beta1 causes airway fibrosis and increased collagen I and III mRNA in mice. Thorax 2003, 58:772-777.
48. Lukyanenko Y.O., Chen J.J., Hutson J.C. Production of 25-hydroxycholesterol by testicular macrophages and its effects on Leydig cells. Biol. Reprod. 2001, 64:790-796.
49. Diczfalusy U., Olofsson K.E., Carlsson A.M., Gong M., Golenbock D.T., Rooyackers O., Flaring U., Bjorkbacka H. Marked upregulation of cholesterol 25-hydroxylase expression by lipopolysaccharide. J. Lipid Res. 2009, 50:2258-2264.
50. Johnson K.A., Morrow C.J., Knight G.D., Scallen T.J. In vivo formation of 25-hydroxycholesterol from endogenous cholesterol after a single meal, dietary cholesterol challenge. J. Lipid Res. 1994, 35:2241-2253.
51. Rahman I., Adcock I.M. Oxidative stress and redox regulation of lung inflammation in COPD. Eur. Respir. J. 2006, 28:219-242.