RalA suppresses early stages of Ras-induced squamous cell carcinoma progression

Oncogene

Volumn 29, Issue 1, 2010, Pages 45-55

  Sowalsky, A G ^a   Alt Holland, A ^b   Shamis, Y ^a   Garlick, J A ^b   Feig, L A ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TUFTS UNIVERSITY SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

E cadherin; Ral; Ras; Squamous cell carcinoma; Tumor progression

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; RALA PROTEIN; RAS PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CANCER MODEL; CELL TRANSFORMATION; CONTROLLED STUDY; DOWN REGULATION; EARLY CANCER; GENE EXPRESSION REGULATION; GENE SILENCING; HEAD AND NECK CARCINOMA; HUMAN; HUMAN CELL; KERATINOCYTE; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; ONCOGENE RAS; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SKIN CARCINOGENESIS; SQUAMOUS CELL CARCINOMA; TUMOR GROWTH;

ANIMALS; BLOTTING, WESTERN; CADHERINS; CARCINOMA, SQUAMOUS CELL; CELL CULTURE TECHNIQUES; CELL LINE; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; DISEASE PROGRESSION; HUMANS; IMMUNOHISTOCHEMISTRY; KERATINOCYTES; MALE; MICE; MICE, NUDE; NEOPLASM STAGING; RAL GTP-BINDING PROTEINS; RAS PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SKIN NEOPLASMS; SKIN TRANSPLANTATION; SKIN, ARTIFICIAL; TISSUE ENGINEERING; VESICULAR TRANSPORT PROTEINS;

EID: 73849139962     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2009.307     Document Type: Article

References (47)

1. Bailleul B, Surani MA, White S, Barton SC, Brown K, Blessing M et al. (1990). Skin hyperkeratosis and papilloma formation in transgenic mice expressing a ras oncogene from a suprabasal keratin promoter. Cell 62: 697-708.
2. Bodemann BO, White MA. (2008). Ral GTPases and cancer: linchpin support of the tumorigenic platform. Nat Rev Cancer 8: 133-140.
3. Brymora A, Valova VA, Larsen MR, Roufogalis BD, Robinson PJ. (2001). The brain exocyst complex interacts with RalA in a GTP-dependent manner: identification of a novel mammalian Sec3 gene and a second Sec15 gene. J Biol Chem 276: 29792-29797.
4. Cantor S, Urano T, Feig LA. (1995). Identification and characterization of Ral-binding protein 1, a potential downstream target of Ral GTPases. Mol Cell Biol 15: 4578-4584.
5. Carlson MW, Alt-Holland A, Egles C, Garlick JA. (2008). Three-dimensional tissue models of normal and diseased skin. Curr Protoc Cell Biol Chapter 19, Unit 19.9.
6. Cascone I, Selimoglu R, Ozdemir C, Del Nery E, Yeaman C, White M et al. (2008). Distinct roles of RalA and RalB in the progression of cytokinesis are supported by distinct RalGEFs. EMBO J 27: 2375-2387.
7. Chen XW, Inoue M, Hsu SC, Saltiel AR. (2006). RalA-exocyst-dependent recycling endosome trafficking is required for the completion of cytokinesis. J Biol Chem 281: 38609-38616.
8. Chien Y, Kim S, Bumeister R, Loo YM, Kwon SW, Johnson CL et al. (2006). RalB GTPase-mediated activation of the IkappaB family kinase TBK1 couples innate immune signaling to tumor cell survival. Cell 127: 157-170.
9. Chien Y, White MA. (2003). RAL GTPases are linchpin modulators of human tumour-cell proliferation and survival. EMBO Rep 4: 800-806.
10. Dajee M, Lazarov M, Zhang JY, Cai T, Green CL, Russell AJ et al. (2003). NF-kappaB blockade and oncogenic Ras trigger invasive human epidermal neoplasia. Nature 421: 639-643.
11. Dlugosz A, Merlino G, Yuspa SH. (2002). Progress in cutaneous cancer research. J Investig Dermatol Symp Proc 7: 17-26.
12. Feig LA. (2003). Ral-GTPases: approaching their 15 min of fame. Trends Cell Biol 13: 419-425.
13. Fenwick R, Prasannan S, Campbell L, Nietlispach D, Evetts K, Camonis J et al. (2009). Solution structure and dynamics of the small GTPase RalB in its active conformation: significance for effector protein binding. Biochemistry e-pub ahead of print 23 January.
14. Frankel P, Aronheim A, Kavanagh E, Balda MS, Matter K, Bunney TD et al. (2005). RalA interacts with ZONAB in a cell density-dependent manner and regulates its transcriptional activity. EMBO J 24: 54-62.
15. Garlick JA. (2007). Engineering skin to study human disease-tissue models for cancer biology and wound repair. Adv Biochem Eng Biotechnol 103: 207-239.
16. Ginos MA, Page GP, Michalowicz BS, Patel KJ, Volker SE, Pambuccian SE et al. (2004). Identification of a gene expression signature associated with recurrent disease in squamous cell carcinoma of the head and neck. Cancer Res 64: 55-63.
17. Gonzalez-Garcia A, Pritchard CA, Paterson HF, Mavria G, Stamp G, Marshall CJ. (2005). RalGDS is required for tumor formation in a model of skin carcinogenesis. Cancer Cell 7: 219-226.
18. Greenberg S, Margulis A, Garlick JA. (2005). in vivo transplantation of engineered human skin. Methods Mol Biol 289: 425-430.
19. Hamad NM, Elconin JH, Karnoub AE, Bai W, Rich JN, Abraham RT et al. (2002). Distinct requirements for Ras oncogenesis in human versus mouse cells. Genes Dev 16: 2045-2057.
20. Hao Y, Wong R, Feig LA. (2008). RalGDS couples growth factor signaling to Akt activation. Mol Cell Biol 28: 2851-2859.
21. Hsu SC, TerBush D, Abraham M, Guo W. (2004). The exocyst complex in polarized exocytosis. Int Rev Cytol 233: 243-265.
22. Jeanes A, Gottardi CJ, Yap AS. (2008). Cadherins and cancer: how does cadherin dysfunction promote tumor progression? Oncogene 27: 6920-6929.
23. Jullien-Flores V, Dorseuil O, Romero F, Letourneur F, Saragosti S, Berger R et al. (1995). Bridging Ral GTPase to Rho pathways. RLIP76, a Ral effector with CDC42/Rac GTPase-activating protein activity. J Biol Chem 270: 22473-22477.
24. Kudo Y, Kitajjma S, Sato S, Miyauchi M, Ogawa I, Takata T. (2003). Establishment of an oral squamous cell carcinoma cell line with high invasive and p27 degradation activities from a lymph node metastasis. Oral Oncol 39: 515-520.
25. Lim KH, Baines AT, Fiordalisi JJ, Shipitsin M, Feig LA, Cox AD et al. (2005). Activation of RalA is critical for Ras-induced tumorigenesis of human cells. Cancer Cell 7: 533-545.
26. Lim KH, O'Hayer K, Adam SJ, Kendall SD, Campbell PM, Der CJ et al. (2006). Divergent roles for RalA and RalB in malignant growth of human pancreatic carcinoma cells. Curr Biol 16: 2385-2394.
27. Margulis A, Zhang W, Alt-Holland A, Crawford HC, Fusenig NE, Garlick JA. (2005a). E-cadherin suppression accelerates squamous cell carcinoma progression in three-dimensional, human tissue constructs. Cancer Res 65: 1783-1791.
28. Margulis A, Zhang W, Garlick JA. (2005b). in vitro fabrication of engineered human skin. Methods Mol Biol 289: 61-70.
29. Moskalenko S, Henry DO, Rosse C, Mirey G, Camonis JH, White MA. (2002). The exocyst is a Ral effector complex. Nat Cell Biol 4: 66-72.
30. Moskalenko S, Tong C, Rosse C, Mirey G, Formstecher E, Daviet L et al. (2003). Ral GTPases regulate exocyst assembly through dual subunit interactions. J Biol Chem 278: 51743-51748.
31. Onder TT, Gupta PB, Mani SA, Yang J, Lander ES, Weinberg RA. (2008). Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res 68: 3645-3654.
32. Oxford G, Owens CR, Titus BJ, Foreman TL, Herlevsen MC, Smith SC et al. (2005). RalA and RalB: antagonistic relatives in cancer cell migration. Cancer Res 65: 7111-7120.
33. Panner A, Nakamura JL, Parsa AT, Rodriguez-Viciana P, Berger MS, Stokoe D et al. (2006). mTOR-independent translational control of the extrinsic cell death pathway by RalA. Mol Cell Biol 26: 7345-7357.
34. Pierceall WE, Goldberg LH, Tainsky MA, Mukhopadhyay T, Ananthaswamy HN. (1991). Ras gene mutation and amplification in human nonmelanoma skin cancers. Mol Carcinog 4: 196-202.
35. Polzin A, Shipitsin M, Goi T, Feig LA, Turner TJ. (2002). Ral-GTPase influences the regulation of the readily releasable pool of synaptic vesicles. Mol Cell Biol 22: 1714-1722.
36. Pons M, Quintanilla M. (2006). Molecular biology of malignant melanoma and other cutaneous tumors. Clin Transl Oncol 8: 466-474.
37. Potempa S, Ridley AJ. (1998). Activation of both MAP kinase and phosphatidylinositide 3-kinase by Ras is required for hepatocyte growth factor/scatter factor-induced adherens junction disassembly. Mol Biol Cell 9: 2185-2200.
38. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D et al. (2004). ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 6: 1-6.
39. Rosse C, Hatzoglou A, Parrini MC, White MA, Chavrier P, Camonis J. (2006). RalB mobilizes the exocyst to drive cell migration. Mol Cell Biol 26: 727-734.
40. Sablina AA, Chen W, Arroyo JD, Corral L, Hector M, Bulmer SE et al. (2007). The tumor suppressor PP2A Abeta regulates the RalA GTPase. Cell 129: 969-982.
41. Shipitsin M, Feig LA. (2004). RalA but not RalB enhances polarized delivery of membrane proteins to the basolateral surface of epithelial cells. Mol Cell Biol 24: 5746-5756.
42. Singhal SS, Yadav S, Singhal J, Zajac E, Awasthi YC, Awasthi S. (2005). Depletion of RLIP76 sensitizes lung cancer cells to doxorubicin. Biochem Pharmacol 70: 481-488.
43. Smith SC, Oxford G, Baras AS, Owens C, Havaleshko D, Brautigan DL et al. (2007). Expression of ral GTPases, their effectors, and activators in human bladder cancer. Clin Cancer Res 13: 3803-3813.
44. Sugihara K, Asano S, Tanaka K, Iwamatsu A, Okawa K, Ohta Y. (2002). The exocyst complex binds the small GTPase RalA to mediate filopodia formation. Nat Cell Biol 4: 73-78.
45. Sugita S. (2008). Mechanisms of exocytosis. Acta Physiol (Oxf) 192:185-193.
46. Takai Y, Sasaki T, Matozaki T. (2001). Small GTP-binding proteins. Physiol Rev 81: 153-208.
47. Zhu AJ, Watt FM. (1996). Expression of a dominant negative cadherin mutant inhibits proliferation and stimulates terminal differentiation of human epidermal keratinocytes. J Cell Sci 109(Part 13): 3013-3023.