Deficiency of the LIM-only protein FHL2 reduces intestinal tumorigenesis in Apc Mutant Mice

PLoS ONE

Volumn 5, Issue 4, 2010, Pages

  Labalette, Charlotte ^a,b   Nouët, Yann ^a,b   Levillayer, Florence ^a,b   Colnot, Sabine ^b,c   Chen, Ju ^d   Claude, Valere ^e   Huerre, Michel ^a   Perret, Christine ^b,c   Buendia, Marie Annick ^a,b   Wei, Yu ^a,b  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c INSTITUT COCHIN   (France)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e SERVICE D ENDOCRINOLOGIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; BETA CATENIN; FOUR AND A HALF LIM ONLY PROTEIN; PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN; FHL2 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; MUSCLE PROTEIN; TRANSCRIPTION FACTOR;

ADENOMA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CANCER RISK; CARCINOGENESIS; CELL MIGRATION; COLORECTAL CARCINOMA; CONTROLLED STUDY; DYSPLASIA; FEMALE; GENE DELETION; GENE MUTATION; INTESTINE EPITHELIUM CELL; INTESTINE TUMOR; INTESTINECARCINOGENESIS; MALE; MOUSE; MOUSE MUTANT; NONHUMAN; PROTEIN DEFICIENCY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RISK REDUCTION; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; UPREGULATION; ACTIVE TRANSPORT; ANIMAL; CELL PROLIFERATION; DRUG EFFECT; GENETICS; HUMAN; METABOLISM; MUTATION; TRANSCRIPTION INITIATION; TRANSGENIC MOUSE;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL PROLIFERATION; GENES, APC; HOMEODOMAIN PROTEINS; HUMANS; INTESTINAL NEOPLASMS; MICE; MICE, TRANSGENIC; MUSCLE PROTEINS; MUTATION; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION; WNT PROTEINS;

EID: 77956420064     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010371     Document Type: Article

References (49)

1. Wixler V, Geerts D, Laplantine E, Westhoff D, Smyth N, et al. (2000) The LIMonly 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.
2. Samson T, Smyth N, Janetzky S, Wendler O, Muller JM, et al. (2004) The LIMonly proteins FHL2 and FHL3 interact with alpha- and beta-subunits of the muscle alpha7beta1 integrin receptor. J Biol Chem 279: 28641-28652.
3. Gabriel B, Mildenberger S, Weisser CW, Metzger E, Gitsch G, et al. (2004) Focal adhesion kinase interacts with the transcriptional coactivator FHL2 and both are overexpressed in epithelial ovarian cancer. Anticancer Res 24: 921-927.
4. Park J, Will C, Martin B, Gullotti L, Friedrichs N, et al. (2008) Deficiency in the LIM-only protein FHL2 impairs assembly of extracellular matrix proteins. Faseb J 22: 2508-2020.
5. Labalette C, Nouet Y, Sobczak-Thepot J, Armengol C, Levillayer F, et al. (2008) The LIM-only protein FHL2 regulates cyclin D1 expression and cell proliferation. J Biol Chem 283: 15201-15208.
6. Muller JM, Metzger E, Greschik H, Bosserhoff AK, Mercep L, et al. (2002) The transcriptional coactivator FHL2 transmits Rho signals from the cell membrane into the nucleus. Embo J 21: 736-748.
7. Du X, Hublitz P, Gunther T, Wilhelm D, Englert C, et al. (2002) The LIM-only coactivator FHL2 modulates WT1 transcriptional activity during gonadal differentiation. Biochim Biophys Acta 1577: 93-101.
8. Morlon A, Sassone-Corsi P (2003) The LIM-only protein FHL2 is a seruminducible transcriptional coactivator of AP-1. Proc Natl Acad Sci U S A 100: 3977-3982.
9. Fimia GM, De Cesare D, Sassone-Corsi P (2000) A family of LIM-only transcriptional coactivators: tissue-specific expression and selective activation of CREB and CREM. Mol Cell Biol 20: 8613-8622.
10. McLoughlin P, Ehler E, Carlile G, Licht JD, Schafer BW (2002) The LIM-only protein DRAL/FHL2 interacts with and is a corepressor for the promyelocytic leukemia zinc finger protein. J Biol Chem 277: 37045-37053.
11. Chen D, Xu W, Bales E, Colmenares C, Conacci-Sorrell M, et al. (2003) SKI activates Wnt/beta-catenin signaling in human melanoma. Cancer Res 63: 6626-6634.
12. Martin B, Schneider R, Janetzky S, Waibler Z, Pandur P, et al. (2002) The LIMonly protein FHL2 interacts with beta-catenin and promotes differentiation of mouse myoblasts. J Cell Biol 159: 113-122.
13. Wei Y, Renard CA, Labalette C, Wu Y, Levy L, et al. (2003) Identification of the LIM protein FHL2 as a coactivator of beta-catenin. J Biol Chem 278: 5188-5194.
14. Yang Y, Hou H, Haller EM, Nicosia SV, Bai W (2005) Suppression of FOXO1 activity by FHL2 through SIRT1-mediated deacetylation. Embo J 24: 1021-1032.
15. Gunther T, Poli C, Muller JM, Catala-Lehnen P, Schinke T, et al. (2005) Fhl2 deficiency results in osteopenia due to decreased activity of osteoblasts. Embo J 24: 3049-3056.
16. Philippar U, Schratt G, Dieterich C, Muller JM, Galgoczy P, et al. (2004) The SRF target gene Fhl2 antagonizes RhoA/MAL-dependent activation of SRF. Mol Cell 16: 867-880.
17. Paul C, Lacroix M, Iankova I, Julien E, Schafer BW, et al. (2006) The LIM-only protein FHL2 is a negative regulator of E4F1. Oncogene 25: 5475-5484.
18. 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.
19. Kong Y, Shelton JM, Rothermel B, Li X, Richardson JA, et al. (2001) Cardiacspecific LIM protein FHL2 modifies the hypertrophic response to betaadrenergic stimulation. Circulation 103: 2731-2738.
20. Wixler V, Hirner S, Muller JM, Gullotti L, Will C, et al. (2007) Deficiency in the LIM-only protein Fhl2 impairs skin wound healing. J Cell Biol 177: 163-172.
21. Kirfel J, Pantelis D, Kabba M, Kahl P, Roper A, et al. (2008) Impaired intestinal wound healing in Fhl2-deficient mice is due to disturbed collagen metabolism. Exp Cell Res 314: 3684-3691.
22. Chu PH, Yeh LK, Lin HC, Jung SM, Ma DH, et al. (2008) Deletion of the FHL2 gene attenuating neovascularization after corneal injury. Invest Ophthalmol Vis Sci 49: 5314-5318.
23. Labalette C, Nouet Y, Levillayer F, Armengol C, Renard CA, et al. (2008) The LIM-Only Protein FHL2 Mediates Ras-Induced Transformation through Cyclin D1 and p53 Pathways. PLoS ONE 3: e3761.
24. Wang J, Yang Y, Xia HH, Gu Q, Lin MC, et al. (2007) Suppression of FHL2 expression induces cell differentiation and inhibits gastric and colon carcinogenesis. Gastroenterology 132: 1066-1076.
25. Martin BT, Kleiber K, Wixler V, Raab M, Zimmer B, et al. (2007) FHL2 regulates cell cycle-dependent and doxorubicin-induced p21Cip1/Waf1 expression in breast cancer cells. Cell Cycle 6: 1779-1788.
26. Li M, Wang J, Ng SS, Chan CY, Chen AC, et al. (2008) The four-and-a-half- LIM protein 2 (FHL2) is overexpressed in gliomas and associated with oncogenic activities. Glia 56: 1328-1338.
27. Kahl P, Gullotti L, Heukamp LC, Wolf S, Friedrichs N, et al. (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.
28. Gabriel B, Fischer DC, Orlowska-Volk M, zur Hausen A, Schule R, et al. (2006) Expression of the transcriptional coregulator FHL2 in human breast cancer: a clinicopathologic study. J Soc Gynecol Investig 13: 69-75.
29. Yan J, Zhu J, Zhong H, Lu Q, Huang C, et al. (2003) BRCA1 interacts with FHL2 and enhances FHL2 transactivation function. FEBS Lett 553: 183-189.
30. Campo-Fernandez B, Morandell D, Santer FR, Zwerschke W, Jansen-Durr P (2007) Identification of the FHL2 transcriptional coactivator as a new functional target of the E7 oncoprotein of human papillomavirus type 16. J Virol 81: 1027-1032.
31. Clevers H (2006) Wnt/beta-catenin signaling in development and disease. Cell 127: 469-480.
32. Colnot S, Niwa-Kawakita M, Hamard G, Godard C, Le Plenier S, et al. (2004) Colorectal cancers in a new mouse model of familial adenomatous polyposis: influence of genetic and environmental modifiers. Lab Invest 84: 1619-1630.
33. 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.
34. Bai S, Kitaura H, Zhao H, Chen J, Muller JM, et al. (2005) FHL2 inhibits the activated osteoclast in a TRAF6-dependent manner. J Clin Invest 115: 2742-2751.
35. Wilding J, Straub J, Bee J, Churchman M, Bodmer W, et al. (2002) Cyclin D1 is not an essential target of beta-catenin signaling during intestinal tumorigenesis, but it may act as a modifier of disease severity in multiple intestinal neoplasia (Min) mice. Cancer Res 62: 4562-4565.
36. Hulit J, Wang C, Li Z, Albanese C, Rao M, et al. (2004) Cyclin D1 genetic heterozygosity regulates colonic epithelial cell differentiation and tumor number in ApcMin mice. Mol Cell Biol 24: 7598-7611.
37. Sansom OJ, Reed KR, van de Wetering M, Muncan V, Winton DJ, et al. (2005) Cyclin D1 is not an immediate target of beta-catenin following Apc loss in the intestine. J Biol Chem 280: 28463-28467.
38. Sansom OJ, Meniel VS, Muncan V, Phesse TJ, Wilkins JA, et al. (2007) Myc deletion rescues Apc deficiency in the small intestine. Nature 446: 676-679.
39. Liu W, Dong X, Mai M, Seelan RS, Taniguchi K, et al. (2000) Mutations in AXIN2 cause colorectal cancer with defective mismatch repair by activating beta-catenin/TCF signalling. Nat Genet 26: 146-147.
40. Wilson CL, Heppner KJ, Labosky PA, Hogan BL, Matrisian LM (1997) Intestinal tumorigenesis is suppressed in mice lacking the metalloproteinase matrilysin. Proc Natl Acad Sci U S A 94: 1402-1407.
41. Nateri AS, Spencer-Dene B, Behrens A (2005) Interaction of phosphorylated c- Jun with TCF4 regulates intestinal cancer development. Nature 437: 281-285.
42. Wang D, Wang H, Shi Q, Katkuri S, Walhi W, et al. (2004) Prostaglandin E(2) promotes colorectal adenoma growth via transactivation of the nuclear peroxisome proliferator-activated receptor delta. Cancer Cell 6: 285-295.
43. Mahmoud NN, Boolbol SK, Bilinski RT, Martucci C, Chadburn A, et al. (1997) Apc gene mutation is associated with a dominant-negative effect upon intestinal cell migration. Cancer Res 57: 5045-5050.
44. Mahmoud NN, Dannenberg AJ, Mestre J, Bilinski RT, Churchill MR, et al. (1998) Aspirin prevents tumors in a murine model of familial adenomatous polyposis. Surgery 124: 225-231.
45. Mahmoud NN, Bilinski RT, Churchill MR, Edelmann W, Kucherlapati R, et al. (1999) Genotype-phenotype correlation in murine Apc mutation: differences in enterocyte migration and response to sulindac. Cancer Res 59: 353-359.
46. Fenton JI, Wolff MS, Orth MW, Hord NG (2002) Membrane-type matrix metalloproteinases mediate curcumin-induced cell migration in non-tumorigenic colon epithelial cells differing in Apc genotype. Carcinogenesis 23: 1065-1070.
47. Sansom OJ, Mansergh FC, Evans MJ, Wilkins JA, Clarke AR (2007) Deficiency of SPARC suppresses intestinal tumorigenesis in APCMin/+ mice. Gut 56: 1410-1414.
48. Heemers HV, Regan KM, Dehm SM, Tindall DJ (2007) Androgen induction of the androgen receptor coactivator four and a half LIM domain protein-2: evidence for a role for serum response factor in prostate cancer. Cancer Res 67: 10592-10599.
49. Muller JM, Isele U, Metzger E, Rempel A, Moser M, et al. (2000) FHL2, a novel tissue-specific coactivator of the androgen receptor. Embo J 19: 359-369