LIM-only protein FHL2 activates NF-KB signaling in the control of liver regeneration and hepatocarcinogenesis

Molecular and Cellular Biology

Volumn 33, Issue 16, 2013, Pages 3299-3308

  Dahan, Jennifer ^a   Nouët, Yann ^a   Jouvion, Grégory ^a   Levillayer, Florence ^a   Adib Conquy, Minou ^a   Cassard Doulcier, Anne Marie ^b,c   Tebbi, Ali ^a   Blan, Fany ^a   Remy, Lauriane ^a   Chen, Ju ^d   Cairo, Stefano ^e   Werts, Catherine ^a   Si Tahar, Mustapha ^a   Tordjmann, Thierry ^c   Buendia, Marie Annick ^a   Weia, Yu ^a  

^a INSTITUT PASTEUR   (France)

^b Universite Paris Sud   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e XenTech   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DIETHYLNITROSAMINE; FOUR AND A HALF LIM ONLY PROTEIN 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; PROTEIN; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER SUSCEPTIBILITY; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; IN VITRO STUDY; IN VIVO STUDY; KNOCKOUT MOUSE; LIVER CARCINOGENESIS; LIVER CELL; LIVER INJURY; LIVER REGENERATION; MOUSE; NONHUMAN; PARTIAL HEPATECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ANIMALS; CELL LINE; CYTOKINES; DIETHYLNITROSAMINE; GENE DELETION; HUMANS; LIM-HOMEODOMAIN PROTEINS; LIPOPOLYSACCHARIDES; LIVER; LIVER NEOPLASMS; LIVER REGENERATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE PROTEINS; NF-KAPPA B; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED FACTOR 6; TRANSCRIPTION FACTORS;

EID: 84881307280     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00105-13     Document Type: Article

References (44)

1. Johannessen M, Moller S, Hansen T, Moens U, Van Ghelue M. 2006. The multifunctional roles of the four-and-a-half-LIM only protein FHL2. Cell. Mol. Life Sci. 63:268-284.
2. Muller JM, Isele U, Metzger E, Rempel A, Moser M, Pscherer A, Breyer T, Holubarsch C, Buettner R, Schule R. 2000. FHL2, a novel tissuespecific coactivator of the androgen receptor. EMBO J. 19:359-369.
3. Kobayashi S, Shibata H, Yokota K, Suda N, Murai A, Kurihara I, Saito I, Saruta T. 2004. FHL2, UBC9, and PIAS1 are novel estrogen receptor alpha-interacting proteins. Endocr. Res. 30:617-621.
4. 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.
5. Chen D, Xu W, Bales E, Colmenares C, Conacci-Sorrell M, Ishii S, Stavnezer E, Campisi J, Fisher DE, Ben-Ze'ev A, Medrano EE. 2003. SKI activates Wnt/beta-catenin signaling in human melanoma. Cancer Res. 63:6626-6634.
6. 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.
7. 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.
8. 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.
9. 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.
10. 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.
11. Brun J, Fromigue O, Dieudonne FX, Marty C, Chen J, Dahan J, Wei Y, Marie PJ. 2012. The LIM-only protein FHL2 controls mesenchymal cell osteogenic differentiation and bone formation through Wnt5a and Wnt10b. Bone 53:6-12.
12. Mille F, Thibert C, Fombonne J, Rama N, Guix C, Hayashi H, Corset V, Reed JC, Mehlen P. 2009. The patched dependence receptor triggers apoptosis through a DRAL-caspase-9 complex. Nat. Cell Biol. 11:739- 746.
13. 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.
14. Hayden MS, Ghosh S. 2012. NF-kappaB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev. 26:203-234.
15. Smale ST. 2011. Hierarchies of NF-kappaB target-gene regulation. Nat. Immunol. 12:689-694.
16. Wong CH, Mak GW, Li MS, Tsui SK. 2012. The LIM-only protein FHL2 regulates interleukin-6 expression through p38 MAPK mediated NFkappaB pathway in muscle cells. Cytokine 59:286-293.
17. Stilo R, Leonardi A, Formisano L, Di Jeso B, Vito P, Liguoro D. 2002. TUCAN/CARDINAL and DRAL participate in a common pathway for modulation of NF-kappaB activation. FEBS Lett. 521:165-169.
18. Sun B, Karin M. 2008. NF-kappaB signaling, liver disease and hepatoprotective agents. Oncogene 27:6228-6244.
19. Beg AA, Sha WC, Bronson RT, Ghosh S, Baltimore D. 1995. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappa B. Nature 376:167-170.
20. Liu F, Xia Y, Parker AS, Verma IM. 2012. IKK biology. Immunol. Rev. 246:239-253.
21. Maeda S, Kamata H, Luo JL, Leffert H, Karin M. 2005. IKKbeta couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis. Cell 121:977-990.
22. Luedde T, Beraza N, Kotsikoris V, van Loo G, Nenci A, De Vos R, Roskams T, Trautwein C, Pasparakis M. 2007. Deletion of NEMO/ IKKgamma in liver parenchymal cells causes steatohepatitis and hepatocellular carcinoma. Cancer Cell 11:119-132.
23. Pikarsky E, Porat RM, Stein I, Abramovitch R, Amit S, Kasem S, Gutkovich-Pyest E, Urieli-Shoval S, Galun E, Ben-Neriah Y. 2004. NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature 431:461-466.
24. 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.
25. Chu PH, Bardwell WM, Gu Y, Ross J, Jr, Chen J. 2000. FHL2 (SLIM3) is not essential for cardiac development and function. Mol. Cell. Biol. 20:7460-7462.
26. Nicou A, Serriere V, Prigent S, Boucherie S, Combettes L, Guillon G, Alonso G, Tordjmann T. 2003. Hypothalamic vasopressin release and hepatocyte Ca2 signaling during liver regeneration: an interplay stimulating liver growth and bile flow. FASEB J. 17:1901-1903.
27. 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.
28. Cougot D, Allemand E, Riviere L, Benhenda S, Duroure K, Levillayer F, Muchardt C, Buendia MA, Neuveut C. 2012. Inhibition of PP1 phosphatase activity by HBx: a mechanism for the activation of hepatitis B virus transcription. Sci. Signal. 5:ra1.
29. Guillot L, Balloy V, McCormack FX, Golenbock DT, Chignard M, Si-Tahar M. 2002. Cutting edge: the immunostimulatory activity of the lung surfactant protein-A involves Toll-like receptor 4. J. Immunol. 168: 5989-5992.
30. 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 proinflammatory phenotype at an early stage of steatohepatitis. J. Hepatol. 57:141-149.
31. Taub R. 2004. Liver regeneration: from myth to mechanism. Nat. Rev. Mol. Cell Biol. 5:836-847.
32. Fausto N, Laird AD, Webber EM. 1995. Liver regeneration. 2. Role of growth factors and cytokines in hepatic regeneration. FASEB J. 9:1527- 1536.
33. Teramoto K, Bowers JL, Khettry U, Palombo JD, Clouse ME. 1993. A rat fatty liver transplant model. Transplantation 55:737-741.
34. Weltman MD, Farrell GC, Liddle C. 1996. Increased hepatocyte CYP2E1 expression in a rat nutritional model of hepatic steatosis with inflammation. Gastroenterology 111:1645-1653.
35. Cornell RP, Liljequist BL, Bartizal KF. 1990. Depressed liver regeneration after partial hepatectomy of germ-free, athymic and lipopolysaccharide- resistant mice. Hepatology 11:916-922.
36. He G, Karin M. 2011. NF-kappaB and STAT3-key players in liver inflammation and cancer. Cell Res. 21:159-168.
37. Naugler WE, Sakurai T, Kim S, Maeda S, Kim K, Elsharkawy AM, Karin M. 2007. Gender disparity in liver cancer due to sex differences in MyD88- dependent IL-6 production. Science 317:121-124.
38. He G, Yu GY, Temkin V, Ogata H, Kuntzen C, Sakurai T, Sieghart W, Peck-Radosavljevic M, Leffert HL, Karin M. 2010. Hepatocyte IKKbeta/ NF-kappaB inhibits tumor promotion and progression by preventing oxidative stress-driven STAT3 activation. Cancer Cell 17:286-297.
39. Deng L, Wang C, Spencer E, Yang L, Braun A, You J, Slaughter C, Pickart C, Chen ZJ. 2000. Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103:351-361.
40. Chen ZJ. 2005. Ubiquitin signalling in the NF-kappaB pathway. Nat. Cell Biol. 7:758-765.
41. Hubbi ME, Gilkes DM, Baek JH, Semenza GL. 2012. Four-and-a-half LIM domain proteins inhibit transactivation by hypoxia-inducible factor 1. J. Biol. Chem. 287:6139-6149.
42. Bai S, Zha J, Zhao H, Ross FP, Teitelbaum SL. 2008. Tumor necrosis factor receptor-associated factor 6 is an intranuclear transcriptional coactivator in osteoclasts. J. Biol. Chem. 283:30861-30867.
43. Qian Z, Mao L, Fernald AA, Yu H, Luo R, Jiang Y, Anastasi J, Valk PJ, Delwel R, Le Beau MM. 2009. Enhanced expression of FHL2 leads to abnormal myelopoiesis in vivo. Leukemia 23:1650-1657.
44. Labalette C, Nouet Y, Levillayer F, Colnot S, Chen J, Claude V, Huerre M, Perret C, Buendia MA, Wei Y. 2010. Deficiency of the LIM-only protein FHL2 reduces intestinal tumorigenesis in Apc mutant mice. PLoS One 5:e10371. doi:10.1371/journal.pone.0010371.