LIM-Only Protein FHL2 Is a Negative Regulator of Transforming Growth Factor β1 Expression

REFERENCES

• Massague J. 2012. TGFbeta signalling in context. Nat Rev Mol Cell Biol 13:616–630. https://doi.org/10.1038/nrm3434.
   PubMed Web of Science ®Google Scholar
• Geiser AG, Kim SJ, Roberts AB, Sporn MB. 1991. Characterization of the mouse transforming growth factor-beta 1 promoter and activation by the Ha-ras oncogene. Mol Cell Biol 11:84–92. https://doi.org/10.1128/MCB.11.1.84.
   PubMed Web of Science ®Google Scholar
• Kim SJ, Glick A, Sporn MB, Roberts AB. 1989. Characterization of the promoter region of the human transforming growth factor-beta 1 gene. J Biol Chem 264:402–408.
   PubMed Web of Science ®Google Scholar
• Van Obberghen-Schilling E, Roche NS, Flanders KC, Sporn MB, Roberts AB. 1988. Transforming growth factor beta 1 positively regulates its own expression in normal and transformed cells. J Biol Chem 263:7741–7746.
   PubMed Web of Science ®Google Scholar
• Samson T, Smyth N, Janetzky S, Wendler O, Muller JM, Schule R, von der Mark H, von der Mark K, Wixler V. 2004. The LIM-only proteins FHL2 and FHL3 interact with alpha- and beta-subunits of the muscle alpha7beta1 integrin receptor. J Biol Chem 279:28641–28652. https://doi.org/10.1074/jbc.M312894200.
   PubMedGoogle Scholar
• Park J, Will C, Martin B, Gullotti L, Friedrichs N, Buettner R, Schneider H, Ludwig S, Wixler V. 2008. Deficiency in the LIM-only protein FHL2 impairs assembly of extracellular matrix proteins. FASEB J 22:2508–2520. https://doi.org/10.1096/fj.07-095521.
   PubMedGoogle Scholar
• Wixler V, Geerts D, Laplantine E, Westhoff D, Smyth N, Aumailley M, Sonnenberg A, Paulsson M. 2000. The LIM-only protein DRAL/FHL2 binds to the cytoplasmic domain of several alpha and beta integrin chains and is recruited to adhesion complexes. J Biol Chem 275:33669–33678. https://doi.org/10.1074/jbc.M002519200.
   PubMed Web of Science ®Google Scholar
• Bai S, Kitaura H, Zhao H, Chen J, Muller JM, Schule R, Darnay B, Novack DV, Ross FP, Teitelbaum SL. 2005. FHL2 inhibits the activated osteoclast in a TRAF6-dependent manner. J Clin Invest 115:2742–2751. https://doi.org/10.1172/JCI24921.
   PubMedGoogle Scholar
• Muller JM, Isele U, Metzger E, Rempel A, Moser M, Pscherer A, Breyer T, Holubarsch C, Buettner R, Schule R. 2000. FHL2, a novel tissue-specific coactivator of the androgen receptor. EMBO J 19:359–369. https://doi.org/10.1093/emboj/19.3.359.
   PubMed Web of Science ®Google Scholar
• Martin B, Schneider R, Janetzky S, Waibler Z, Pandur P, Kuhl M, Behrens J, von der Mark K, Starzinski-Powitz A, Wixler V. 2002. The LIM-only protein FHL2 interacts with beta-catenin and promotes differentiation of mouse myoblasts. J Cell Biol 159:113–122. https://doi.org/10.1083/jcb.200202075.
   PubMedGoogle Scholar
• Morlon A, Sassone-Corsi P. 2003. The LIM-only protein FHL2 is a serum-inducible transcriptional coactivator of AP-1. Proc Natl Acad Sci U S A 100:3977–3982. https://doi.org/10.1073/pnas.0735923100.
   PubMedGoogle Scholar
• Wei Y, Renard CA, Labalette C, Wu Y, Levy L, Neuveut C, Prieur X, Flajolet M, Prigent S, Buendia MA. 2003. Identification of the LIM protein FHL2 as a coactivator of beta-catenin. J Biol Chem 278:5188–5194. https://doi.org/10.1074/jbc.M207216200.
   PubMedGoogle Scholar
• Dahan J, Nouet Y, Jouvion G, Levillayer F, Adib-Conquy M, Cassard-Doulcier AM, Tebbi A, Blanc F, Remy L, Chen J, Cairo S, Werts C, Si-Tahar M, Tordjmann T, Buendia MA, Wei Y. 2013. LIM-only protein FHL2 activates NF-kappaB signaling in the control of liver regeneration and hepatocarcinogenesis. Mol Cell Biol 33:3299–3308. https://doi.org/10.1128/MCB.00105-13.
   PubMedGoogle Scholar
• Nouet Y, Dahan J, Labalette C, Levillayer F, Julien B, Jouvion G, Cairo S, Vives FL, Ribeiro A, Huerre M, Colnot S, Perret C, Nhieu JT, Tordjmann T, Buendia MA, Wei Y. 2012. The four and a half LIM-only protein 2 regulates liver homeostasis and contributes to carcinogenesis. J Hepatol 57:1029–1036. https://doi.org/10.1016/j.jhep.2012.06.035.
   PubMedGoogle Scholar
• Ding L, Wang Z, Yan J, Yang X, Liu A, Qiu W, Zhu J, Han J, Zhang H, Lin J, Cheng L, Qin X, Niu C, Yuan B, Wang X, Zhu C, Zhou Y, Li J, Song H, Huang C, Ye Q. 2009. Human four-and-a-half LIM family members suppress tumor cell growth through a TGF-beta-like signaling pathway. J Clin Invest 119:349–361. https://doi.org/10.1172/JCI35930.
   PubMedGoogle Scholar
• Xia T, Levy L, Levillayer F, Jia B, Li G, Neuveut C, Buendia MA, Lan K, Wei Y. 2013. The four and a half LIM-only protein 2 (FHL2) activates transforming growth factor beta (TGF-beta) signaling by regulating ubiquitination of the E3 ligase Arkadia. J Biol Chem 288:1785–1794. https://doi.org/10.1074/jbc.M112.439760.
   PubMedGoogle Scholar
• Levy L, Hill CS. 2005. Smad4 dependency defines two classes of transforming growth factor {beta} (TGF-{beta}) target genes and distinguishes TGF-{beta}-induced epithelial-mesenchymal transition from its antiproliferative and migratory responses. Mol Cell Biol 25:8108–8125. https://doi.org/10.1128/MCB.25.18.8108-8125.2005.
   PubMed Web of Science ®Google Scholar
• Zhang W, Jiang B, Guo Z, Sardet C, Zou B, Lam CS, Li J, He M, Lan HY, Pang R, Hung IF, Tan VP, Wang J, Wong BC. 2010. Four-and-a-half LIM protein 2 promotes invasive potential and epithelial-mesenchymal transition in colon cancer. Carcinogenesis 31:1220–1229. https://doi.org/10.1093/carcin/bgq094.
   PubMed Web of Science ®Google Scholar
• Gullotti L, Czerwitzki J, Kirfel J, Propping P, Rahner N, Steinke V, Kahl P, Engel C, Schule R, Buettner R, Friedrichs N. 2011. FHL2 expression in peritumoural fibroblasts correlates with lymphatic metastasis in sporadic but not in HNPCC-associated colon cancer. Lab Invest 91:1695–1705. https://doi.org/10.1038/labinvest.2011.109.
   PubMedGoogle Scholar
• Westphal P, Mauch C, Florin A, Czerwitzki J, Olligschlager N, Wodtke C, Schule R, Buttner R, Friedrichs N. 2015. Enhanced FHL2 and TGF-beta1 expression is associated with invasive growth and poor survival in malignant melanomas. Am J Clin Pathol 143:248–256. https://doi.org/10.1309/AJCPXEC6CIT2TXAF.
   PubMedGoogle Scholar
• Seki E, Brenner DA. 2015. Recent advancement of molecular mechanisms of liver fibrosis. J Hepatobiliary Pancreat Sci 22:512–518. https://doi.org/10.1002/jhbp.245.
   PubMed Web of Science ®Google Scholar
• Levy L, Howell M, Das D, Harkin S, Episkopou V, Hill CS. 2007. Arkadia activates Smad3/Smad4-dependent transcription by triggering signal-induced SnoN degradation. Mol Cell Biol 27:6068–6083. https://doi.org/10.1128/MCB.00664-07.
   PubMed Web of Science ®Google Scholar
• Messeguer X, Escudero R, Farre D, Nunez O, Martinez J, Alba MM. 2002. PROMO: detection of known transcription regulatory elements using species-tailored searches. Bioinformatics 18:333–334. https://doi.org/10.1093/bioinformatics/18.2.333.
   PubMed Web of Science ®Google Scholar
• Birchenall-Roberts MC, Ruscetti FW, Kasper J, Lee HD, Friedman R, Geiser A, Sporn MB, Roberts AB, Kim SJ. 1990. Transcriptional regulation of the transforming growth factor beta 1 promoter by v-src gene products is mediated through the AP-1 complex. Mol Cell Biol 10:4978–4983. https://doi.org/10.1128/MCB.10.9.4978.
   PubMedGoogle Scholar
• Seki E, De Minicis S, Osterreicher CH, Kluwe J, Osawa Y, Brenner DA, Schwabe RF. 2007. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat Med 13:1324–1332. https://doi.org/10.1038/nm1663.
   PubMed Web of Science ®Google Scholar
• Huss S, Stellmacher C, Goltz D, Khlistunova I, Adam AC, Trebicka J, Kirfel J, Buttner R, Weiskirchen R. 2013. Deficiency in four and one half LIM domain protein 2 (FHL2) aggravates liver fibrosis in mice. BMC Gastroenterol 13:8. https://doi.org/10.1186/1471-230X-13-8.
   PubMedGoogle Scholar
• Alnajar A, Nordhoff C, Schied T, Chiquet-Ehrismann R, Loser K, Vogl T, Ludwig S, Wixler V. 2013. The LIM-only protein FHL2 attenuates lung inflammation during bleomycin-induced fibrosis. PLoS One 8:e81356. https://doi.org/10.1371/journal.pone.0081356.
   PubMed Web of Science ®Google Scholar
• Li SY, Huang PH, Tarng C, Lin TP, Yang WC, Chang YH, Yang AH, Lin CC, Yang MH, Chen JW, Schmid-Schonbein GW, Chien S, Chu PH, Lin SJ. 2015. Four-and-a-half LIM domains protein 2 is a coactivator of Wnt signaling in diabetic kidney disease. J Am Soc Nephrol 26:3072–3084. https://doi.org/10.1681/ASN.2014100989.
   PubMedGoogle Scholar
• Fanton d'Andon M, Quellard N, Fernandez B, Ratet G, Lacroix-Lamande S, Vandewalle A, Boneca IG, Goujon JM, Werts C. 2014. Leptospira interrogans induces fibrosis in the mouse kidney through Inos-dependent, TLR- and NLR-independent signaling pathways. PLoS Negl Trop Dis 8:e2664. https://doi.org/10.1371/journal.pntd.0002664.
   PubMed Web of Science ®Google Scholar
• Wei Y, Fabre M, Branchereau S, Gauthier F, Perilongo G, Buendia MA. 2000. Activation of beta-catenin in epithelial and mesenchymal hepatoblastomas. Oncogene 19:498–504. https://doi.org/10.1038/sj.onc.1203356.
   PubMed Web of Science ®Google Scholar
• Labalette C, Renard CA, Neuveut C, Buendia MA, Wei Y. 2004. Interaction and functional cooperation between the LIM protein FHL2, CBP/p300, and beta-catenin. Mol Cell Biol 24:10689–10702. https://doi.org/10.1128/MCB.24.24.10689-10702.2004.
   PubMedGoogle Scholar
• Yan J, Zhu J, Zhong H, Lu Q, Huang C, Ye Q. 2003. BRCA1 interacts with FHL2 and enhances FHL2 transactivation function. FEBS Lett 553:183–189. https://doi.org/10.1016/S0014-5793(03)00978-5.
   PubMedGoogle Scholar
• Kahl P, Gullotti L, Heukamp LC, Wolf S, Friedrichs N, Vorreuther R, Solleder G, Bastian PJ, Ellinger J, Metzger E, Schule R, Buettner R. 2006. Androgen receptor coactivators lysine-specific histone demethylase 1 and four and a half LIM domain protein 2 predict risk of prostate cancer recurrence. Cancer Res 66:11341–11347. https://doi.org/10.1158/0008-5472.CAN-06-1570.
   PubMed Web of Science ®Google Scholar
• Chan KK, Tsui SK, Lee SM, Luk SC, Liew CC, Fung KP, Waye MM, Lee CY. 1998. Molecular cloning and characterization of FHL2, a novel LIM domain protein preferentially expressed in human heart. Gene 210:345–350. https://doi.org/10.1016/S0378-1119(97)00644-6.
   PubMed Web of Science ®Google Scholar
• Leroux A, Ferrere G, Godie V, Cailleux F, Renoud ML, Gaudin F, Naveau S, Prevot S, Makhzami S, Perlemuter G, Cassard-Doulcier AM. 2012. Toxic lipids stored by Kupffer cells correlates with their pro-inflammatory phenotype at an early stage of steatohepatitis. J Hepatol 57:141–149. https://doi.org/10.1016/j.jhep.2012.02.028.
   PubMed Web of Science ®Google Scholar
• Labalette C, Nouet Y, Sobczak-Thepot J, Armengol C, Levillayer F, Gendron MC, Renard CA, Regnault B, Chen J, Buendia MA, Wei Y. 2008. The LIM-only protein FHL2 regulates cyclin D1 expression and cell proliferation. J Biol Chem 283:15201–15208. https://doi.org/10.1074/jbc.M800708200.
   PubMedGoogle Scholar
• Inman GJ, Nicolas FJ, Callahan JF, Harling JD, Gaster LM, Reith AD, Laping NJ, Hill CS. 2002. SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol Pharmacol 62:65–74. https://doi.org/10.1124/mol.62.1.65.
   PubMed Web of Science ®Google Scholar