GCF2/LRRFIP1 promotes colorectal cancer metastasis and liver invasion through integrin-dependent RhoA activation

Cancer Letters

Volumn 325, Issue 1, 2012, Pages 99-107

  Ariake, Kyohei ^a   Ohtsuka, Hideo ^a   Motoi, Fuyuhiko ^a   Douchi, Daisuke ^a   Oikawa, Masaya ^a   Rikiyama, Toshiki ^a   Fukase, Koji ^a   Katayose, Yu ^a   Egawa, Shinichi ^a   Unno, Michiaki ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

Colorectal cancer; GCF2; Integrin; LRRFIP1; RhoA

Indexed keywords

BINDING PROTEIN; FIBRONECTIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; INTEGRIN; LEUCINE RICH REPEAT IN FLIGHTLESS 1 INTERACTING PROTEIN 1; LEUKEMIA ASSOCIATED RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CELL ADHESION; CELL INVASION; CELL MIGRATION; COLORECTAL CANCER; CONTROLLED STUDY; HUMAN; HUMAN CELL; LIVER METASTASIS; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; CELL ADHESION; CELL MOVEMENT; COLORECTAL NEOPLASMS; FIBRONECTINS; FOCAL ADHESION KINASE 1; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HT29 CELLS; HUMANS; INTEGRINS; LIVER NEOPLASMS; MICE; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; RHOA GTP-BINDING PROTEIN; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION;

MUS;

EID: 84865284125     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.06.012     Document Type: Article

References (49)

1. Braet F., Nagatsuma K., Saito M., Soon L., Wisse E., Matsuura T. The hepatic sinusoidal endothelial lining and colorectal liver metastases. World J. Gastroenterol. 2007, 13:821-825.
2. Hahn E., Wick G., Pencev D., Timpl R. Distribution of basement membrane proteins in normal and fibrotic human liver: collagen type IV, laminin, and fibronectin. Gut 1980, 21:63-71.
3. Haier J., Nasralla M., Nicolson G.L. Different adhesion properties of highly and poorly metastatic HT-29 colon carcinoma cells with extracellular matrix components: role of integrin expression and cytoskeletal components. Br. J. Cancer 1999, 80:1867-1874.
4. Akiyama S.K., Olden K., Yamada K.M. Fibronectin and integrins in invasion and metastasis. Cancer Metast. Rev. 1995, 14:173-189.
5. Klemke M., Weschenfelder T., Konstandin M.H., Samstag Y. High affinity interaction of integrin alpha4beta1 (VLA-4) and vascular cell adhesion molecule 1 (VCAM-1) enhances migration of human melanoma cells across activated endothelial cell layers. J. Cell. Physiol. 2007, 212:368-374.
6. Brakebusch C., Bouvard D., Stanchi F., Sakai T., Fassler R. Integrins in invasive growth. J. Clin. Invest. 2002, 109:999-1006.
7. Hood J.D., Cheresh D.A. Role of integrins in cell invasion and migration. Nat. Rev. Cancer 2002, 2:91-100.
8. Felding-Habermann B., O'Toole T.E., Smith J.W., Fransvea E., Ruggeri Z.M., Ginsberg M.H., Hughes P.E., Pampori N., Shattil S.J., Saven A., Mueller B.M. Integrin activation controls metastasis in human breast cancer. Proc. Natl. Acad. Sci. USA 2001, 98:1853-1858.
9. Heyder C., Gloria-Maercker E., Hatzmann W., Niggemann B., Zanker K.S., Dittmar T. Role of the beta1-integrin subunit in the adhesion, extravasation and migration of T24 human bladder carcinoma cells. Clin. Exp. Metast. 2005, 22:99-106.
10. Dubash A.D., Wennerberg K., Garcia-Mata R., Menold M.M., Arthur W.T., Burridge K. A novel role for Lsc/p115 RhoGEF and LARG in regulating RhoA activity downstream of adhesion to fibronectin. J. Cell Sci. 2007, 120:3989-3998.
11. Ridley A.J., Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 1992, 70:389-399.
12. Narumiya S. The small GTPase Rho: cellular functions and signal transduction. J. Biochem. 1996, 120:215-228.
13. Lamarche N., Hall A. GAPs for rho-related GTPases. Trends Genet. 1994, 10:436-440.
14. Boguski M.S., McCormick F. Proteins regulating ras and its relatives. Nature 1993, 366:643-654.
15. Zhai J., Lin H., Nie Z., Wu J., Canete-Soler R., Schlaepfer W.W., Schlaepfer D.D. Direct interaction of focal adhesion kinase with p190RhoGEF. J. Biol. Chem. 2003, 278:24865-24873.
16. Reed A.L., Yamazaki H., Kaufman J.D., Rubinstein Y., Murphy B., Johnson A.C. Molecular cloning and characterization of a transcription regulator with homology to GC-binding factor. J. Biol. Chem. 1998, 273:21594-21602.
17. Sjoblom T., Jones S., Wood L.D., Parsons D.W., Lin J., Barber T.D., Mandelker D., Leary R.J., Ptak J., Silliman N., Szabo S., Buckhaults P., Farrell C., Meeh P., Markowitz S.D., Willis J., Dawson D., Willson J.K., Gazdar A.F., Hartigan J., Wu L., Liu C., Parmigiani G., Park B.H., Bachman K.E., Papadopoulos N., Vogelstein B., Kinzler K.W., Velculescu V.E. The consensus coding sequences of human breast and colorectal cancers. Science 2006, 314:268-274.
18. Shibutani M., Lazarovici P., Johnson A.C., Katagiri Y., Guroff G. Transcriptional down-regulation of epidermal growth factor receptors by nerve growth factor treatment of PC12 cells. J. Biol. Chem. 1998, 273:6878-6884.
19. Rikiyama T., Curtis J., Oikawa M., Zimonjic D.B., Popescu N., Murphy B.A., Wilson M.A., Johnson A.C. GCF2: expression and molecular analysis of repression. Biochim. Biophys. Acta 2003, 1629:15-25.
20. Suriano A.R., Sanford A.N., Kim N., Oh M., Kennedy S., Henderson M.J., Dietzmann K., Sullivan K.E. GCF2/LRRFIP1 represses tumor necrosis factor alpha expression. Mol. Cell Biol. 2005, 25:9073-9081.
21. Dai P., Jeong S.Y., Yu Y., Leng T., Wu W., Xie L., Chen X. Modulation of TLR signaling by multiple MyD88-interacting partners including leucine-rich repeat Fli-I-interacting proteins. J. Immunol. 2009, 182:3450-3460.
22. Fong K.S., de Couet H.G. Novel proteins interacting with the leucine-rich repeat domain of human flightless-I identified by the yeast two-hybrid system. Genomics 1999, 58:146-157.
23. Ohtsuka H., Oikawa M., Kyohei A., Rikiyama T., Motoi F., Katayose Y., Unno M., Johnson A.C. GCF2 interacts with dishevelled and regulates Wnt signaling pathways in human carcinoma cell lines. Int. J. Cancer 2011, 129:1599-1610.
24. Yoshioka K., Nakamori S., Itoh K. Overexpression of small GTP-binding protein RhoA promotes invasion of tumor cells. Cancer Res. 1999, 59:2004-2010.
25. Gavert N., Sheffer M., Raveh S., Spaderna S., Shtutman M., Brabletz T., Barany F., Paty P., Notterman D., Domany E., Ben-Ze'ev A. Expression of L1-CAM and ADAM10 in human colon cancer cells induces metastasis. Cancer Res. 2007, 67:7703-7712.
26. Martinez-Hernandez A. The hepatic extracellular matrix. I. Electron immunohistochemical studies in normal rat liver. Lab Invest. 1984, 51:57-74.
27. Jiang W.G. Cell adhesion molecules in the formation of liver metastasis. J. Hepatobiliary Pancreat. Surg. 1998, 5:375-382.
28. Kemperman H., Wijnands Y.M., Roos E. AlphaV Integrins on HT-29 colon carcinoma cells: adhesion to fibronectin is mediated solely by small amounts of alphaVbeta6, and alphaVbeta5 is codistributed with actin fibers. Exp. Cell Res. 1997, 234:156-164.
29. Meng X.N., Jin Y., Yu Y., Bai J., Liu G.Y., Zhu J., Zhao Y.Z., Wang Z., Chen F., Lee K.Y., Fu S.B. Characterisation of fibronectin-mediated FAK signalling pathways in lung cancer cell migration and invasion. Br. J. Cancer 2009, 101:327-334.
30. Liu H., Chen B., Zardi L., Ramos D.M. Soluble fibronectin promotes migration of oral squamous-cell carcinoma cells. Int. J. Cancer 1998, 78:261-267.
31. Enns A., Korb T., Schluter K., Gassmann P., Spiegel H.U., Senninger N., Mitjans F., Haier J. Alphavbeta5-integrins mediate early steps of metastasis formation. Eur. J. Cancer 2005, 41:1065-1072.
32. Yoshioka K., Matsumura F., Akedo H., Itoh K. Small GTP-binding protein Rho stimulates the actomyosin system, leading to invasion of tumor cells. J. Biol. Chem. 1998, 273:5146-5154.
33. Vazquez-Prado J., Basile J., Gutkind J.S. Modular architecture and novel protein-protein interactions regulating the RGS-containing Rho guanine nucleotide exchange factors. Meth. Enzymol. 2004, 390:259-285.
34. Fukuhara S., Chikumi H., Gutkind J.S. RGS-containing RhoGEFs: the missing link between transforming G proteins and Rho?. Oncogene 2001, 20:1661-1668.
35. Liu J., Bang A.G., Kintner C., Orth A.P., Chanda S.K., Ding S., Schultz P.G. Identification of the Wnt signaling activator leucine-rich repeat in flightless interaction protein 2 by a genome-wide functional analysis. Proc. Natl. Acad. Sci. USA 2005, 102:1927-1932.
36. Daneker G.W., Piazza A.J., Steele G.D., Mercurio A.M. Relationship between extracellular matrix interactions and degree of differentiation in human colon carcinoma cell lines. Cancer Res. 1989, 49:681-686.
37. Sahai E., Marshall C.J. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat. Cell Biol. 2003, 5:711-719.
38. Friedl P., Wolf K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat. Rev. Cancer 2003, 3:362-374.
39. Wolf K., Mazo I., Leung H., Engelke K., von Andrian U.H., Deryugina E.I., Strongin A.Y., Brocker E.B., Friedl P. Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 2003, 160:267-277.
40. Etienne-Manneville S., Hall A. Rho GTPases in cell biology. Nature 2002, 420:629-635.
41. Ren X.D., Kiosses W.B., Schwartz M.A. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 1999, 18:578-585.
42. Price L.S., Leng J., Schwartz M.A., Bokoch G.M. Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol. Biol Cell. 1998, 9:1863-1871.
43. Ridley A.J., Paterson H.F., Johnston C.L., Diekmann D., Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 1992, 70:401-410.
44. Raftopoulou M., Hall A. Cell migration: Rho GTPases lead the way. Dev. Biol. 2004, 265:23-32.
45. Kitzing T.M., Sahadevan A.S., Brandt D.T., Knieling H., Hannemann S., Fackler O.T., Grosshans J., Grosse R. Positive feedback between Dia1, LARG, and RhoA regulates cell morphology and invasion. Genes Dev. 2007, 21:1478-1483.
46. Wang S.J., Bourguignon L.Y. Role of hyaluronan-mediated CD44 signaling in head and neck squamous cell carcinoma progression and chemoresistance. Am. J. Pathol. 2011, 178:956-963.
47. Fukuhara S., Chikumi H., Gutkind J.S. Leukemia-associated Rho guanine nucleotide exchange factor (LARG) links heterotrimeric G proteins of the G(12) family to Rho. FEBS Lett. 2000, 485:183-188.
48. Kourlas P.J., Strout M.P., Becknell B., Veronese M.L., Croce C.M., Theil K.S., Krahe R., Ruutu T., Knuutila S., Bloomfield C.D., Caligiuri M.A. Identification of a gene at 11q23 encoding a guanine nucleotide exchange factor: evidence for its fusion with MLL in acute myeloid leukemia. Proc. Natl. Acad. Sci. USA 2000, 97:2145-2150.
49. Fukuhara S., Murga C., Zohar M., Igishi T., Gutkind J.S. A novel PDZ domain containing guanine nucleotide exchange factor links heterotrimeric G proteins to Rho. J. Biol. Chem. 1999, 274:5868-5879.