Role of Rho-family proteins in cell adhesion and cancer

Current Opinion in Cell Biology

Volumn 15, Issue 5, 2003, Pages 583-589

  Malliri, Angeliki ^a   Collard, John G ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; RHO FACTOR; WNT PROTEIN;

CANCER GROWTH; CARCINOGENESIS; CELL ADHESION; CELL CYCLE; CELL MIGRATION; CELL TRANSFORMATION; DISEASE COURSE; DOWNSTREAM PROCESSING; IN VITRO STUDY; LYMPHATIC SYSTEM TUMOR; MUTANT; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN MODIFICATION; REVIEW; SIGNAL TRANSDUCTION; SKIN CANCER; SURVIVAL RATE; TRANSCRIPTION INITIATION; TUMOR CELL;

EID: 0141756144     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(03)00098-X     Document Type: Review

References (49)

1. Boettner B., van Aelst L. The role of Rho GTPases in disease development. Gene. 286:2002;155-174 This extensive review gives an overview on what is known on the role of Rho proteins in disease development including cancer.
2. Schmidt A., Hall A. Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev. 16:2002;1587-1609 This is an overview of the large number of activators (GEFs) of Rho-like GTPases, their specificity and mode of activation.
3. Manser E., Loo T.H., Koh C.G., Zhao Z.S., Chen X.Q., Tan L., Tan I., Leung T., Lim L. PAK kinases are directly coupled to the PIX family of nucleotide exchange factors. Mol Cell. 1:1998;183-192.
4. Buchsbaum R.J., Connolly B.A., Feig L.A. Interaction of Rac exchange factors Tiam1 and Ras-GRF1 with a scaffold for the p38 mitogen-activated protein kinase cascade. Mol Cell Biol. 22:2002;4073-4085 This study shows that Tiam1 is able to bind a scaffold protein for the p38 mitogen-activated protein kinase, which promotes its activation.
5. •] - show that a guanine nucleotide exchange factor can contribute to Rac signalling specificity by its ability to form a complex with a scaffold that binds components of one of the many known Rac effector pathways.
6. Sahai E., Marshall C.J. Rho-GTPases and cancer. Nat Rev Cancer. 2:2002;133-142 This is an extensive overview of data that implicate Rho-like proteins in various types of cancer.
7. Whitehead I.P., Campbell S., Rossman K.L., Der C.J. Dbl family proteins. Biochim Biophys Acta. 1332:1997;F1-23.
8. Stam J.C., Collard J.G. The DH protein family, exchange factors for Rho-like GTPases. Prog Mol Subcell Biol. 22:1999;51-83.
9. Perona R., Esteve P., Jimenez B., Ballestero R.P., Cajal S.R. Tumorigenic activity of rho genes from Aplysia californica. Oncogene. 8:1993;1285-1292.
10. van Leeuwen F.N., van der Kammen R.A., Habets G.G.M., Collard J.G. Oncogenic activity of Tiam1 and Rac1 in NIH3T3 cells. Oncogene. 11:1995;2215-2221.
11. Khosravi-Far R., Solski P.A., Clark G.J., Kinch M.S., Der C.J. Activation of Rac and Rho, and mitogen activated protein kinases, are required for Ras transformation. Mol Cell Biol. 15:1995;6443-6453.
12. Qiu R.G., Chen J., Kirn D., McCormick F., Symons M. An essential role for Rac in Ras transformation. Nature. 374:1995;457-459.
13. Westwick J.K., Lee R.J., Lambert Q.T., Symons M., Pestell R.G., Der C.J., Whitehead I.P. Transforming potential of Dbl family proteins correlates with transcription from the cyclin D1 promoter but not with activation of Jun NH2-terminal kinase, p38/Mpk2, serum response factor, or c-Jun. J Biol Chem. 273:1998;16739-16747.
14. Bar-Sagi D., Hall A. Ras and Rho GTPases: a family reunion. Cell. 103:2000;227-238.
15. Schmitz A.A., Govek E.E., Bottner B., van Aelst L. Rho GTPases: signaling, migration, and invasion. Exp Cell Res. 261:2000;1-12.
16. Etienne-Manneville S., Hall A. Rho GTPases in cell biology. Nature. 420:2002;629-635 Recent overview on the roles of Rho GTPases in a large variety of biological processes.
17. Braga V. Epithelial cell shape: cadherins and small GTPases. Exp Cell Res. 261:2000;83-90.
18. Fukata M., Kaibuchi K. Rho-family GTPases in cadherin-mediated cell-cell adhesion. Nat Rev Mol Cell Biol. 2:2001;887-897.
19. Bracke M.E., Van Roy F.M., Mareel M.M. The e-cadherin/catenin complex in invasion and metastasis. Curr Top Microbiol Immunol. 213:1996;123-161.
20. Birchmeier W., Behrens J. Cadherin expression in carcinomas: role in the formation of cell junctions and the prevention of invasiveness. Biochim Biophys Acta. 1198:1994;11-26.
21. Keely P.J., Westwick J.K., Whitehead I.P., Der C.J., Parise L.V. Cdc42 and Rac1 induce integrin-mediated cell motility and invasiveness through PI(3)K. Nature. 390:1997;632-636.
22. Sander E.E., van Delft S., ten Klooster J.P., Reid T., Van der Kammen R.A., Michiels F., Collard J.G. Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase. J Cell Biol. 143:1998;1385-1398.
23. Sander E.E., ten Klooster J.P., van Delft S., Van der Kammen R.A., Collard J.G. Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J Cell Biol. 147:1999;1009-1022.
24. Zondag G.C., Evers E.E., ten Klooster J.P., Janssen L., van Der K., Collard J.G. Oncogenic Ras downregulates Rac activity, which leads to increased Rho activity and epithelial-mesenchymal transition. J Cell Biol. 149:2000;775-782.
25. Hordijk P.L., ten Klooster J.P., Van der Kammen R.A., Michiels F., Oomen L.C., Collard J.G. Inhibition of invasion of epithelial cells by Tiam1-Rac signaling. Science. 278:1997;1464-1466.
26. Nimnual A.S., Taylor L.J., Bar-Sagi D. Redox-dependent downregulation of Rho by Rac. Nat Cell Biol. 5:2003;236-241 This study provides a mechanistic explanation of how Rac downregulates Rho activity. Rac-mediated production of reactive oxygen species (ROS) inhibits a protein tyrosine phosphatase leading to increased phosphorylation and activation of p190RhoGAP and thereby downregulation of Rho activity.
27. Renshaw M.W., Price L.S., Schwartz M.A. Focal adhesion kinase mediates the integrin signaling requirement for growth factor activation of MAP kinase. J Cell Biol. 147:1999;611-618.
28. Danen E.H., Sonneveld P., Sonnenberg A., Yamada K.M. Dual stimulation of Ras/mitogen-activated protein kinase and RhoA by cell adhesion to fibronectin supports growth-factor-stimulated cell cycle progression. J Cell Biol. 151:2000;1413-1422.
29. Mettouchi A., Klein S., Guo W., Lopez-Lago M., Lemichez E., Westwick J.K., Giancotti F.G. Integrin-specific activation of Rac controls progression through the G(1) phase of the cell cycle. Mol Cell. 8:2001;115-127.
30. Liu A.X., Rane N., Liu J.P., Prendergast G.C. RhoB is dispensable for mouse development, but it modifies susceptibility to tumor formation as well as cell adhesion and growth factor signaling in transformed cells. Mol Cell Biol. 21:2001;6906-6912 This study demonstrates that RhoB-deficient mice produce increased numbers of Ras-induced skin tumours most likely by a RhoB-dependent effect on apoptosis.
31. Malliri A., Van der Kammen R.A., Clark K., Van Der Valk M., Michiels F., Collard J.G. Mice deficient in the Rac activator Tiam1 are resistant to Ras-induced skin tumours. Nature. 417:2002;867-871 This study shows that Tiam1-deficient mice are resistant to Ras-induced skin tumours and demonstrates for the first time a role of a Rac guanine nucleotide exchange factor in various aspects of tumourigenesis in vivo. Tiam1/Rac signalling affects apoptosis, growth and progression of tumours.
32. Robles A.I., Rodriguez-Puebla M.L., Glick A.B., Trempus C., Hansen L., Sicinski P., Tennant R.W., Weinberg R.A., Yuspa S.H., Conti C.J. Reduced skin tumor development in cyclin D1-deficient mice highlights the oncogenic Ras pathway in vivo. Genes Dev. 12:1998;2469-2474.
33. Yu Q., Geng Y., Sicinski P. Specific protection against breast cancers by cyclin D1 ablation. Nature. 411:2001;1017-1021.
34. Joneson T., Bar-Sagi D. Suppression of Ras-induced apoptosis by the Rac GTPase. Mol Cell Biol. 19:1999;5892-5901.
35. van Leeuwen F.N., Kain H.E., Kammen R.A., Michiels F., Kranenburg O.W., Collard J.G. The guanine nucleotide exchange factor Tiam1 affects neuronal morphology; opposing roles for the small GTPases Rac and Rho. J Cell Biol. 139:1997;797-807.
36. Kozma R., Sarner S., Ahmed S., Lim L. Rho family GTPases and neuronal growth cone remodelling: relationship between increased complexity induced by Cdc42Hs, Rac1, and acetylcholine and collapse induced by RhoA and lysophosphatidic acid. Mol Cell Biol. 17:1997;1201-1211.
37. Fleming I.N., Gray A., Downes C.P. Regulation of the Rac1-specific exchange factor Tiam1 involves both phosphoinositide 3-kinase-dependent and -independent components. Biochem J. 351:2000;173-182.
38. Lambert J.M., Lambert Q.T., Reuther G.W., Malliri A., Siderovski D.P., Sondek J., Collard J.G., Der C.J. Tiam1 mediates Ras activation of Rac by a PI(3)K-independent mechanism. Nat Cell Biol. 4:2002;621-625 This study shows that the Rac activator Tiam1 is able to bind to activated Ras, providing a direct link between Ras- and Rac signalling.
39. Frame S., Balmain A. Integration of positive and negative growth signals during Ras pathway activation in vivo. Curr Opin Genet Dev. 10:2000;106-113.
40. Cleverley S.C., Costello P.S., Henning S.W., Cantrell D.A. Loss of Rho function in the thymus is accompanied by the development of thymic lymphoma. Oncogene. 19:2000;13-20.
41. Jonkers J., Korswagen H.C., Acton D., Breuer M., Berns A. Activation of a novel proto-oncogene, Frat1, contributes to progression of mouse T-cell lymphomas. EMBO J. 16:1997;441-450.
42. Preudhomme C., Roumier C., Hildebrand M.P., Dallery-Prudhomme E., Lantoine D., Lai J.L., Daudignon A., Adenis C., Bauters F., Fenaux P.et al. Nonrandom 4p13 rearrangements of the RhoH/TTF gene, encoding a GTP-binding protein, in non-Hodgkin's lymphoma and multiple myeloma. Oncogene. 19:2000;2023-2032.
43. Pasqualucci L., Neumeister P., Goossens T., Nanjangud G., Chaganti R.S., Kuppers R., Dalla-Favera R. Hypermutation of multiple proto-oncogenes in B-cell diffuse large-cell lymphomas. Nature. 412:2001;341-346.
44. van Noort M., Clevers H. TCF transcription factors, mediators of Wnt signaling in development and cancer. Dev Biol. 244:2002;1-8.
45. Tao W., Pennica D., Xu L., Kalejta R.F., Levine A.J. Wrch-1, a novel member of the Rho gene family that is regulated by Wnt-1. Genes Dev. 15:2001;1796-1807.
46. Kawasaki Y., Senda T., Ishidate T., Koyama R., Morishita T., Iwayama Y., Higuchi O., Akiyama T. Asef, a link between the tumor suppressor APC and G-protein signaling. Science. 289:2000;1194-1197.
47. Kawasaki Y., Sato R., Akiyama T. Mutated APC and Asef are involved in the migration of colorectal tumour cells. Nat Cell Biol. 5:2003;211-215 This paper shows that the binding of truncated adenomatous polyposis coli (APC) to Asef decreases E-cadherin-mediated cell-cell adhesion and promotes the migration of epithelial MDCK cells and colorectal cancer cells. These results suggest that the APC-Asef complex might contribute to aberrant migratory behaviour of colorectal tumour cells.
48. Etienne-Manneville S., Hall A. Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature. 421:2003;753-756 Cdc42-dependent phosphorylation of glycogen synthase kinase-3β occurs specifically at the leading edge of migrating cells, and induces the interaction of adenomatous polyposis coli protein with the plus ends of microtubules, which is required for cell polarisation and directed cell migration.
49. Habas R., Dawid I.B., He X. Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation. Genes Dev. 17:2003;295-309 This paper shows that Wnt/Fz signalling activates Rac and Rho through the cytoplasmic Dishevelled protein. Wnt/Fz activation of Rac and Rho is proposed to be required for cell polarity and movements during vertebrate gastrulation.