Tax-interacting protein 1 coordinates the spatiotemporal activation of Rho GTPases and regulates the infiltrative growth of human glioblastoma

Oncogene

Volumn 33, Issue 12, 2014, Pages 1558-1569

  Wang, H ^a   Han, M ^a,b,c   Whetsell, W ^a   Wang, J ^a,d   Rich, J ^e   Hallahan, D ^f   Han, Z ^a,d  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KUNMING INSTITUTE OF ZOOLOGY   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^d VANDERBILT INGRAM CANCER CENTER   (United States)

^e LERNER RESEARCH INSTITUTE   (United States)

^f WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ARHGEF7; Cell migration; Glioblastoma; Rho GTPases; Rhotekin; Tax interacting protein 1

Indexed keywords

ARHGEF 7 PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN CDC42; RAC1 PROTEIN; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHOTEKIN PROTEIN; TAX INTERACTING PROTEIN 1; TAX PROTEIN; TUMOR MARKER; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CANCER PROGNOSIS; CANCER STAGING; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVATION; GENE SILENCING; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; TUMOR INVASION; TUMOR MODEL;

MURINAE;

ANIMALS; BETA CATENIN; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; GLIOBLASTOMA; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MOLECULAR TARGETED THERAPY; NEOPLASM INVASIVENESS; NEOPLASM STAGING; PROGNOSIS; PROTEIN TRANSPORT; RHO GTP-BINDING PROTEINS; RHO GUANINE NUCLEOTIDE EXCHANGE FACTORS; SPATIO-TEMPORAL ANALYSIS;

EID: 84897088816     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.97     Document Type: Article

References (46)

1. Beuming T, Skrabanek L, Niv MY, Mukherjee P, Weinstein H. PDZBase: a proteinprotein interaction database for PDZ-domains. Bioinformatics (Oxford, England) 2005; 21: 827-828.
2. Subbaiah VK, Kranjec C, Thomas M, Banks L. PDZ domains: the building blocks regulating tumorigenesis. Biochem J 2011; 439: 195-205.
3. Molina JR, Agarwal NK, Morales FC, Hayashi Y, Aldape KD, Cote G et al. PTEN, NHERF1 and PHLPP form a tumor suppressor network that is disabled in glioblastoma. Oncogene 2012; 31: 1264-1274.
4. Besser J, Leito JT, van der Meer DL, Bagowski CP. Tip-1 induces filopodia growth and is important for gastrulation movements during zebrafish development. Dev Growth Differ 2007; 49: 205-214.
5. Olalla L, Gutierrez A, Jimenez AJ, Lopez-Tellez JF, Khan ZU, Perez J et al. Expression of the scaffolding PDZ protein glutaminase-interacting protein in mammalian brain. J Neurosci Res 2008; 86: 281-292.
6. Han M, Wang H, Zhang HT, Han Z. The PDZ protein TIP-1 facilitates cell migration and pulmonary metastasis of human invasive breast cancer cells in athymic mice. Biochem Biophys Res Commun 2012; 422: 139-145.
7. Alewine C, Olsen O, Wade JB, Welling PA. TIP-1 has pdz scaffold antagonist activity. Mol Biol Cell 2006; 17: 4200-4211.
8. Hampson L, Li C, Oliver AW, Kitchener HC, Hampson IN. The PDZ protein Tip-1 is a gain of function target of the HPV16 E6 oncoprotein. Int J Oncol 2004; 25: 1249-1256.
9. Kanamori M, Sandy P, Marzinotto S, Benetti R, Kai C, Hayashizaki Y et al. The PDZ protein tax-interacting protein-1 inhibits beta-catenin transcriptional activity and growth of colorectal cancer cells. J Biol Chem 2003; 278: 38758-38764.
10. Reynaud C, Fabre S, Jalinot P. The PDZ protein TIP-1 interacts with the Rho effector rhotekin and is involved in Rho signaling to the serum response element. J Biol Chem 2000; 275: 33962-33968.
11. Zencir S, Ovee M, Dobson MJ, Banerjee M, Topcu Z, Mohanty S. Identification of brain-specific angiogenesis inhibitor 2 as an interaction partner of glutaminase interacting protein. Biochem Biophys Res Commun 2011; 411: 792-797.
12. Oliver AW, He X, Borthwick K, Donne AJ, Hampson L, Hampson IN. The HPV16 E6 binding protein Tip-1 interacts with ARHGEF16, which activates Cdc42. Br J Cancer 2011; 104: 324-331.
13. Jaffe AB, Hall A. Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 2005; 21: 247-269.
14. Salhia B, Tran NL, Chan A, Wolf A, Nakada M, Rutka F et al. The guanine nucleotide exchange factors trio, Ect2, and Vav3 mediate the invasive behavior of glioblastoma. Am J Pathol 2008; 173: 1828-1838.
15. Hwang SL, Hong YR, Sy WD, Lieu AS, Lin CL, Lee KS et al. Rac1 gene mutations in human brain tumours. Eur J Surg Oncol 2004; 30: 68-72.
16. Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Gene Dev 2007; 21: 2683-2710.
17. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 2009; 10: 459-466.
18. Olalla L, Aledo JC, Bannenberg G, Marquez J. The C-terminus of human glutaminase L mediates association with PDZ domain-containing proteins. FEBS Lett 2001; 488: 116-122.
19. Rousset R, Fabre S, Desbois C, Bantignies F, Jalinot P. The C-terminus of the HTLV-1 Tax oncoprotein mediates interaction with the PDZ domain of cellular proteins. Oncogene 1998; 16: 643-654.
20. Durney MA, Birrane G, Anklin C, Soni A, Ladias JA. Solution structure of the human Tax-interacting protein-1. J Biomol NMR 2009; 45: 329-334.
21. Zhang J, Yan X, Shi C, Yang X, Guo Y, Tian C et al. Structural basis of [beta]-catenin recognition by Tax-interacting protein-1. J Mol Biol 2008; 384: 255-263.
22. Osmani N, Vitale N, Borg JP, Etienne-Manneville S. Scrib controls Cdc42 localization and activity to promote cell polarization during astrocyte migration. Curr Biol 2006; 16: 2395-2405.
23. Audebert S, Navarro C, Nourry C, Chasserot-Golaz S, Lecine P, Bellaiche Y et al. Mammalian Scribble forms a tight complex with the beta PIX exchange factor. Curr Biol 2004; 14: 987-995.
24. Iden S, Collard JG. Crosstalk between small GTPases and polarity proteins in cell polarization. Nat Rev Mol Cell Biol 2008; 9: 846-859.
25. Rincon E, Saez de Guinoa J, Gharbi SI, Sorzano CO, Carrasco YR, Merida I. Translocation dynamics of sorting nexin 27 in activated T cells. J Cell Sci 2011; 124(Pt 5): 776-788.
26. Machacek M, Hodgson L, Welch C, Elliott H, Pertz O, Nalbant P et al. Coordination of Rho GTPase activities during cell protrusion. Nature 2009; 461: 99-103.
27. Pertz O, Hodgson L, Klemke RL, Hahn KM. Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 2006; 440: 1069-1072.
28. Wang H, Yan H, Fu A, Han M, Hallahan D, Han Z. TIP-1 translocation onto the cell plasma membrane is a molecular biomarker of tumor response to ionizing radiation. PloS one 2010; 5: e12051.
29. Freije WA, Castro-Vargas FE, Fang Z, Horvath S, Cloughesy T, Liau LM et al. Gene expression profiling of gliomas strongly predicts survival. Cancer Res 2004; 64: 6503-6510.
30. Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, Wu TD et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 2006; 9: 157-173.
31. Han M, Wang H, Zhang HT, Han Z. Expression of TIP-1 confers radioresistance of malignant glioma cells. PloS one 2012; 7: e45402.
32. Hampson L, He XT, Oliver AW, Hadfield JA, Kemp T, Butler J et al. Analogues of Y27632 increase gap junction communication and suppress the formation of transformed NIH3T3 colonies. Br J Cancer 2009; 101: 829-839.
33. Garcia-Mata R, Burridge K. Catching a GEF by its tail. Trend Cell Biol 2007; 17: 36-43.
34. ten Klooster JP, Jaffer ZM, Chernoff J, Hordijk PL. Targeting and activation of Rac1 are mediated by the exchange factor {beta}-Pix. J Cell Biol 2006; 172: 759-769.
35. Hall A. Rho GTPases and the actin cytoskeleton. Science 1998; 279: 509-514.
36. Amano M, Chihara K, Kimura K, Fukata Y, Nakamura N, Matsuura Y et al. Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science 1997; 275: 1308-1311.
37. Dickinson DJ, Nelson WJ, Weis WI. A polarized epithelium organized by beta-and alpha-catenin predates cadherin and metazoan origins. Science 2011; 331: 1336-1339.
38. Ji H, Wang J, Nika H, Hawke D, Keezer S, Ge Q et al. EGF-induced ERK activation promotes CK2-mediated disassociation of alpha-catenin from beta-catenin and transactivation of beta-catenin. Mol Cell 2009; 36: 547-559.
39. Burger PC, Dubois PJ, Schold Jr SC, Smith Jr KR, Odom GL, Crafts DC et al. Computerized tomographic and pathologic studies of the untreated, quiescent, and recurrent glioblastoma multiforme. J Neurosurg 1983; 58: 159-169.
40. Han M, Wang H, Zhang HT, Han Z. Expression of Tax-interacting protein 1 (TIP-1) facilitates angiogenesis and tumor formation of human glioblastoma cells in nude mice. Cancer Lett 2013; 328: 55-64.
41. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444: 756-760.
42. Mayhew MW, Webb DJ, Kovalenko M, Whitmore L, Fox JW, Horwitz AF. Identification of protein networks associated with the PAK1-betaPIX-GIT1- paxillin signaling complex by mass spectrometry. J Proteome Res 2006; 5: 2417-2423.
43. Etienne-Manneville S. In vitro assay of primary astrocyte migration as a tool to study Rho GTPase function in cell polarization. Meth Enzymol 2006; 406: 565-578.
44. Geng L, Shinohara ET, Kim D, Tan J, Osusky K, Shyr Y et al. STI571 (Gleevec) improves tumor growth delay and survival in irradiated mouse models of glioblastoma. Int J Radiat Oncol Biol Phys 2006; 64: 263-271.
45. Akella NS, Ding Q, Menegazzo I, Wang W, Gillespie GY, Grammer JR et al. A novel technique to quantify glioma tumor invasion using serial microscopy sections. J Neurosci Methods 2006; 153: 183-189.
46. Cavenee WK, Furnari FB, Nagane M, Huang H-JS, Newcomb EW, Bigner DD et al. Diffuse astrocytomas. Pathology and Genetics of Tumors of the Nervous System Kleihues P, Cavenee WK (eds) IARC Press: Lyon, 2000, pp 10-21.