Rap1 stabilizes β-catenin and enhances β-catenin-dependent transcription and invasion in squamous cell carcinoma of the head and neck

Clinical Cancer Research

Volumn 16, Issue 1, 2010, Pages 65-76

  Goto, Mitsuo ^a   Mitra, Raj S ^a   Liu, Min ^a   Lee, Julia ^b   Henson, Bradley S ^a   Carey, Thomas ^b   Bradford, Carol ^b   Prince, Mark ^b   Wang, Cun Yu ^a   Fearon, Eric R ^b   D'Silva, Nisha J ^a,b  

^a UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; LITHIUM CHLORIDE; MATRILYSIN; RAP1 PROTEIN; SMALL INTERFERING RNA; T CELL FACTOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TCF4; UNCLASSIFIED DRUG;

ARTICLE; CANCER INVASION; CANCER RADIOTHERAPY; CONTROLLED STUDY; CYTOSOL; DISEASE SEVERITY; GENE EXPRESSION; GENE OVEREXPRESSION; GENE TRANSLOCATION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GROWTH INHIBITION; HEAD AND NECK CARCINOMA; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HEAD AND NECK SURGERY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; PRIORITY JOURNAL; PROGNOSIS; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RECEPTOR DOWN REGULATION; SQUAMOUS CELL CARCINOMA; TRANSCRIPTION REGULATION; TUMOR LOCALIZATION;

BETA CATENIN; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAD AND NECK NEOPLASMS; HUMANS; SIGNAL TRANSDUCTION; TELOMERE-BINDING PROTEINS; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION; WNT PROTEINS;

EID: 74949088546     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-09-1122     Document Type: Article

References (51)

1. Bos JL, de Rooij J, Reedquist KA. Rap1 signalling: adhering to new models. Nat Rev Mol Cell Biol 2001;2:369-77.
2. Stork PJ, Dillon TJ. Multiple roles of Rap1 in hematopoietic cells: complementary versus antagonistic functions. Blood 2005;106:2952-61.
3. Mochizuki N, Ohba Y, Kiyokawa E, et al. Activation of the ERK/MAPK pathway by an isoform of rap1GAP associated with G α(i). Nature 1999;400:891-4.
4. Rubinfeld B, Munemitsu S, Clark R, et al. Molecular cloning of a GTPase activating protein specific for the Krev-1 protein p21rap1. Cell 1991;65:1033-42.
5. Su L, Hattori M, Moriyama M, et al. AF-6 controls integrin-mediated cell adhesion by regulating Rap1 activation through the specific recruitment of Rap1GTP and SPA-1. J Biol Chem 2003;278:15232-8.
6. Takai Y, Sasaki T, Matozaki T. Small GTP-binding proteins. Physiol Rev 2001;81:153-208.
7. Kooistra MR, Dube N, Bos JL. Rap1: a key regulator in cell-cell junction formation. J Cell Sci 2007;120:17-22.
8. Zhang Z, Mitra RS, Henson BS, et al. Rap1GAP inhibits tumor growth in oropharyngeal squamous cell carcinoma. Am J Pathol 2006;168:585-96.
9. Mitra RS, Goto M, Lee JS, et al. Rap1GAP promotes invasion via induction of matrix metalloproteinase 9 secretion, which is associated with poor survival in low N-stage squamous cell carcinoma. Cancer Res 2008;68:3959-69.
10. Mitra RS, Zhang Z, Henson BS, Kurnit DM, Carey TE, D'Silva NJ. Rap1A and rap1B ras-family proteins are prominently expressed in the nucleus of squamous carcinomas: nuclear translocation of GTP-bound active form. Oncogene 2003;22:6243-56.
11. Leethanakul C, Patel V, Gillespie J, et al. Distinct pattern of expression of differentiation and growth-related genes in squamous cell carcinomas of the head and neck revealed by the use of laser capture microdissection and cDNA arrays. Oncogene 2000;19:3220-4.
12. Rhee CS, Sen M, Lu D, et al. Wnt and frizzled receptors as potential targets for immunotherapy in head and neck squamous cell carcinomas. Oncogene 2002;21:6598-605.
13. Yang F, Zeng Q, Yu G, Li S, Wang CY. Wnt/β-catenin signaling inhibits death receptor-mediated apoptosis and promotes invasive growth of HNSCC. Cell Signal 2006;18:679-87.
14. Behrens J, von Kries JP, Kuhl M, et al. Functional interaction of β-catenin with the transcription factor LEF-1. Nature 1996;382:638-42.
15. Molenaar M, van de Wetering M, Oosterwegel M, et al. XTcf-3 transcription factor mediates β-catenin-induced axis formation in Xenopus embryos. Cell 1996;86:391-9.
16. Nelson WJ, Nusse R. Convergence of Wnt, β-catenin, and cadherin pathways. Science 2004;303:1483-7.
17. Hart MJ, de los Santos R, Albert IN, Rubinfeld B, Polakis P. Downregulation of β-catenin by human Axin and its association with the APC tumor suppressor, β-catenin and GSK3β. Curr Biol 1998;8:573-81.
18. Sakanaka C, Weiss JB, Williams LT. Bridging of β-catenin and glycogen synthase kinase-3β by axin and inhibition of β-catenin- mediated transcription. Proc Natl Acad Sci U S A 1998;95:3020-3.
19. Fagotto F, Gluck U, Gumbiner BM. Nuclear localization signal-independent and importin/karyopherin-independent nuclear import of β-catenin. Curr Biol 1998;8:181-90.
20. Hajra KM, Fearon ER. Cadherin and catenin alterations in human cancer. Genes Chromosomes Cancer 2002;34:255-68.
21. Fujita Y, Hogan C, Braga VM. Regulation of cell-cell adhesion by Rap1. Methods Enzymol 2006;407:359-72.
22. Hogan C, Serpente N, Cogram P, et al. Rap1 regulates the formation of E-cadherin-based cell-cell contacts. Mol Cell Biol 2004;24:6690-700.
23. Price LS, Hajdo-Milasinovic A, Zhao J, Zwartkruis FJ, Collard JG, Bos JL. Rap1 regulates E-cadherin-mediated cell-cell adhesion. J Biol Chem 2004;279:35127-32.
24. Asuri S, Yan J, Paranavitana NC, Quilliam LA. E-cadherin disengagement activates the Rap1 GTPase. J Cell Biochem 2008;105:1027-37.
25. Winer IS, Bommer GT, Gonik N, Fearon ER. Lysine residues Lys-19 and Lys-49 of β-catenin regulate its levels and function in T cell factor transcriptional activation and neoplastic transformation. J Biol Chem 2006;281:26181-7.
26. Feng Y, Bommer GT, Zhai Y, et al. Drosophila split ends homologue SHARP functions as a positive regulator of Wnt/β-catenin/T-cell factor signaling in neoplastic transformation. Cancer Res 2007;67:482-91.
27. 2+-mediated activation of Rap1 in human platelets. EMBO J 1997;16:252-9.
28. Wolf GT, Urba S, Hazuka M. Induction chemotherapy for organ preservation in advanced squamous cell carcinoma of the oral cavity and oropharynx. Recent Results Cancer Res 1994;134:133-43.
29. Uraguchi M, Morikawa M, Shirakawa M, Sanada K, Imai K. Activation of WNT family expression and signaling in squamous cell carcinomas of the oral cavity. J Dent Res 2004;83:327-32.
30. Tsuchiya R, Yamamoto G, Nagoshi Y, Aida T, Irie T, Tachikawa T. Expression of adenomatous polyposis coli (APC) in tumorigenesis of human oral squamous cell carcinoma. Oral Oncol 2004;40:932-40.
31. Lanning CC, Daddona JL, Ruiz-Velasco R, Shafer SH, Williams CL. The Rac1 C-terminal polybasic region regulates the nuclear localization and protein degradation of Rac1. J Biol Chem 2004;279:44197-210.
32. Lanning CC, Ruiz-Velasco R, Williams CL. Novel mechanism of the co-regulation of nuclear transport of SmgGDS and Rac1. J Biol Chem 2003;278:12495-506.
33. Esufali S, Bapat B. Cross-talk between Rac1 GTPase and dysregulated Wnt signaling pathway leads to cellular redistribution of β-catenin and TCF/LEF-mediated transcriptional activation. Oncogene 2004;23:8260-71.
34. -/- colon carcinoma. Science 1997;275:1784-7.
35. Crawford HC, Fingleton BM, Rudolph-Owen LA, et al. The metalloproteinase matrilysin is a target of β-catenin transactivation in intestinal tumors. Oncogene 1999;18:2883-91.
36. Werner JA, Dunne AA, Ramaswamy A, et al. Sentinel node detection in N0 cancer of the pharynx and larynx. Br J Cancer 2002;87:711-5.
37. De Angelis T, Noe A, Chatterjee M, Mulholland J. Stromelysin-1 activation correlates with invasiveness in squamous cell carcinoma. J Invest Dermatol 2002;118:759-66.
38. Impola U, Jeskanen L, Ravanti L, et al. Expression of matrix metalloproteinase (MMP)-7 and MMP-13 and loss of MMP-19 and p16 are associated with malignant progression in chronic wounds. Br J Dermatol 2005;152:720-6.
39. Impola U, Uitto VJ, Hietanen J, et al. Differential expression of matrilysin-1 (MMP-7), 92 kD gelatinase (MMP-9), and metalloelastase (MMP-12) in oral verrucous and squamous cell cancer. J Pathol 2004;202:14-22.
40. Margulis A, Zhang W, Alt-Holland A, Crawford HC, Fusenig NE, Garlick JA. E-cadherin suppression accelerates squamous cell carcinoma progression in three-dimensional, human tissue constructs. Cancer Res 2005;65:1783-91.
41. Pelosi G, Scarpa A, Veronesi G, et al. A subset of high-grade pulmonary neuroendocrine carcinomas shows up-regulation of matrix metalloproteinase-7 associated with nuclear β-catenin immunoreactivity, independent of EGFR and HER-2 gene amplification or expression. Virchows Arch 2005;447:969-77.
42. Chen YJ, Lin SC, Kao T, et al. Genome-wide profiling of oral squamous cell carcinoma. J Pathol 2004;204:326-32.
43. Ginos MA, Page GP, Michalowicz BS, et al. Identification of a gene expression signature associated with recurrent disease in squamous cell carcinoma of the head and neck. Cancer Res 2004;64:55-63.
44. Takeda K, Kinoshita I, Shimizu Y, et al. Clinicopathological significance of expression of p-c-Jun, TCF4 and β-catenin in colorectal tumors. BMC Cancer 2008;8:328.
45. Weber A, Hengge UR, Stricker I, et al. Protein microarrays for the detection of biomarkers in head and neck squamous cell carcinomas. Hum Pathol 2007;38:228-38.
46. Kitayama H, Sugimoto Y, Matsuzaki T, Ikawa Y, Noda M. A ras-related gene with transformation suppressor activity. Cell 1989;56:77-84.
47. Yoshida Y, Kawata M, Miura Y, et al. Microinjection of smg/rap1/Krev-1 p21 into Swiss 3T3 cells induces DNA synthesis and morphological changes. Mol Cell Biol 1992;12:3407-14.
48. Knox AL, Brown NH. Rap1 GTPase regulation of adherens junction positioning and cell adhesion. Science 2002;295:1285-8.
49. Yajnik V, Paulding C, Sordella R, et al. DOCK4, a GTPase activator, is disrupted during tumorigenesis. Cell 2003;112:673-84.
50. Balzac F, Avolio M, Degani S, et al. E-cadherin endocytosis regulates the activity of Rap1: a traffic light GTPase at the crossroads between cadherin and integrin function. J Cell Sci 2005;118:4765-83.
51. Chelsky D, Ralph R, Jonak G. Sequence requirements for synthetic peptide-mediated translocation to the nucleus. Mol Cell Biol 1989;9:2487-92.