A new crucial protein interaction element that targets the adenovirus E4-ORF1 oncoprotein to membrane vesicles

Journal of Virology

Volumn 81, Issue 9, 2007, Pages 4787-4797

  Chung, Sang Hyuk ^a   Frese, Kristopher K ^a,b   Weiss, Robert S ^a,c   Venkataram Prasad, B V ^a   Javier, Ronald T ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b CRUK Cambridge Research Institute   (United Kingdom)

^c Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; ONCOPROTEIN; PDZ PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOPROTEIN; PROTEIN DLG1; PROTEIN MAGI 1; PROTEIN MUPP1; PROTEIN PATJ; PROTEIN ZO 2; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ADENOVIRUS; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL TRANSFORMATION; CONTROLLED STUDY; CYTOPLASM; E1A ONCOGENE; E1B ONCOGENE; E4 ORF1 ONCOGENE; ENZYME ACTIVATION; GENE MUTATION; HUMAN; HUMAN ADENOVIRUS; HUMAN ADENOVIRUS 9; HUMAN CELL; ISOMERIZATION; MEMBRANE VESICLE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADENOVIRUS E4 PROTEINS; ADENOVIRUSES, HUMAN; AMINO ACID SEQUENCE; ANIMALS; CELL LINE; COMPUTATIONAL BIOLOGY; CYTOPLASMIC VESICLES; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT;

ADENOVIRIDAE; ANIMALIA; HUMAN ADENOVIRUS TYPE 9;

EID: 34247576593     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02855-06     Document Type: Article

References (67)

1. Bates, P. A., L. A. Kelley, R. M. MacCallum, and M. J. Sternberg. 2001. Enhancement of protein modeling by human intervention in applying the automatic programs 3D-JIGSAW and 3D-PSSM. Proteins 45:39-46.
2. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
3. Camonis, J. H., and M. A. White. 2005. Ral GTPases: corrupting the exocyst in cancer cells. Trends Cell Biol. 15:327-332.
4. Cantley, L. C. 2002. The phosphoinositide 3-kinase pathway. Science 296: 1655-1657.
5. Ceresa, B. P., A. W. Kao, S. R. Santeler, and J. E. Pessin. 1998. Inhibition of clathrin-mediated endocytosis selectively attenuates specific insulin receptor signal transduction pathways. Mol. Cell. Biol. 18:3862-3870.
6. Chetkovich, D. M., R. C. Bunn, S. H. Kuo, Y. Kawasaki, M. Kohwi, and D. S. Bredt. 2002. Postsynaptic targeting of alternative postsynaptic density-95 isoforms by distinct mechanisms. J. Neurosci. 22:6415-6425.
7. Chlenski, A., K. V. Ketels, M. S. Tsao, M. S. Talamonti, M. R. Anderson, R. Oyasu, and D. G. Scarpelli. 1999. Tight junction protein ZO-2 is differentially expressed in normal pancreatic ducts compared to human pancreatic adenocarcinoma. Int. J. Cancer 82:137-144.
8. Coyne, C. B., T. Voelker, S. L. Pichla, and J. M. Bergelson. 2004. The coxsackievirus and adenovirus receptor interacts with the multi-PDZ domain protein-1 (MUPP-1) within the tight junction. J. Biol. Chem. 279:48079-48084.
9. DiMaio, D., and D. Mattoon. 2001. Mechanisms of cell transformation by papillomavirus E5 proteins. Oncogene 20:7866-7873.
10. Fallon, L., C. M. Belanger, A. T. Corera, M. Kontogiannea, E. Regan-Klapisz, F. Moreau, J. Voortman, M. Haber, G. Rouleau, T. Thorarinsdottir, A. Brice, P. M. van Bergen En Henegouwen, and E. A. Fon. 2006. A regulated interaction with the UIM protein Eps15 implicates parkin in EGF receptor trafficking and P1(3)K-Akt signalling. Nat. Cell Biol. 8:834-842.
11. Fisher, P. B., L. E. Babiss, I. B. Weinstein, and H. S. Ginsberg. 1982. Analysis of type 5 adenovirus transformation with a cloned rat embryo cell line (CREF). Proc. Natl. Acad. Sci. USA 79:3527-3531.
12. Frese, K. K., I. J. Latorre, S. H. Chung, G. Caruana, A. Bernstein, S. N. Jones, L. A. Donehower, M. J. Justice, C. C. Garner, and R. T. Javier. 2006. Oncogenic function for the Dlg1 mammalian homolog of the Drosophila discs-large tumor suppressor. EMBO J. 25:1406-1417.
13. Frese, K. K., S. S. Lee, D. L. Thomas, I. J. Latorre, R. S. Weiss, B. A. Glaunsinger, and R. T. Javier. 2003. Selective PDZ protein-dependent stimulation of phosphatidylinositol 3-kinase by the adenovirus E4-ORF1 oncoprotein. Oncogene 22:710-721.
14. Glaunsinger, B. A., S. S. Lee, M. Thomas, L. Banks, and R. Javier. 2000. Interactions of the PDZ-protein MAGI-1 with adenovirus E4-ORF1 and high-risk papillomavirus E6 oncoproteins. Oncogene 19:5270-5280.
15. Glaunsinger, B. A., R. S. Weiss, S. S. Lee, and R. Javier. 2001. Link of the unique oncogenic properties of adenovirus type 9 E4-ORF1 to a select interaction with the candidate tumor suppressor protein ZO-2. EMBO J. 20:5578-5586.
16. Hamazaki, Y., M. Itoh, H. Sasaki, M. Furuse, and S. Tsukita. 2002. Multi-PDZ domain protein 1 (MUPP1) is concentrated at tight junctions through its possible interaction with claudin-1 and junctional adhesion molecule. J. Biol. Chem. 277:455-461.
17. Helt, A. M., and D. A. Galloway. 2003. Mechanisms by which DNA tumor virus oncoproteins target the Rb family of pocket proteins. Carcinogenesis 24:159-169.
18. Hirata, A., M. Higuchi, A. Niinuma, M. Ohashi, M. Fukushi, M. Oie, T. Akiyama, Y. Tanaka, F. Gejyo, and M. Fujii. 2004. PDZ domain-binding motif of human T-cell leukemia virus type 1 Tax oncoprotein augments the transforming activity in a rat fibroblast cell line. Virology 318:327-336.
19. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
20. Huang, M., and G. C. Prendergast. 2006. RhoB in cancer suppression. Histol. Histopathol. 21:213-218.
21. Ide, N., Y. Hata, H. Nishioka, K. Hirao, I. Yao, M. Deguchi, A. Mizoguchi, H. Nishimori, T. Tokino, Y. Nakamura, and Y. Takai. 1999. Localization of membrane-associated guanylate kinase (MAG1)-1/BA1-associated protein (BAP) 1 at tight junctions of epithelial cells. Oncogene 18:7810-7815.
22. Javier, R., K. Raska, Jr., G. J. Macdonald, and T. Shenk. 1991. Human adenovirus type 9-induced rat mammary tumors. J. Virol. 65:3192-3202.
23. Javier, R. T. 1994. Adenovirus type 9 E4 open reading frame 1 encodes a transforming protein required for the production of mammary tumors in rats. J. Virol. 68:3917-3924.
24. Jesaitis, L. A., and D. A. Goodenough. 1994. Molecular characterization and tissue distribution of ZO-2, a tight junction protein homologous to ZO-1 and the Drosophila discs-large tumor suppressor protein. J. Cell Biol. 124:949-961.
25. Katso, R., K. Okkenhaug, K. Ahmadi, S. White, J. Timms, and M. D. Waterfield. 2001. Cellular function of phosphoinositide 3-kinases: implications for development, homeostasis, and cancer. Annu. Rev. Cell Dev. Biol. 17:615-675.
26. Latorre, I. J., M. H. Roh, K. K. Frese, R. S. Weiss, B. Margolis, and R. T. Javier. 2005. Viral oncoprotein-induced mislocalization of select PDZ proteins disrupts tight junctions and causes polarity defects in epithelial cells. J. Cell Sci. 118:4283-4293.
27. Lee, O. K., K. K. Frese, J. S. James, D. Chadda, Z. H. Chen, R. T. Javier, and K. O. Cho. 2003. Discs-Large and Strabismus are functionally linked to plasma membrane formation. Nat. Cell Biol. 5:987-993.
28. Lee, S. S., B. Glaunsinger, F. Mantovani, L. Banks, and R. T. Javier. 2000. Multi-PDZ domain protein MUPP1 is a cellular target for both adenovirus E4-ORF1 and high-risk papillomavirus type 18 E6 oncoproteins. J. Virol. 74:9680-9693.
29. Lee, S. S., R. S. Weiss, and R. T. Javier. 1997. Binding of human virus oncoproteins to hDlg/SAP97, a mammalian homolog of the Drosophila discs large tumor suppressor protein. Proc. Natl. Acad. Sci. USA 94:6670-6675.
30. Lemmers, C., E. Medina, M. H. Delgrossi, D. Michel, J. P. Arsanto, and A. Le Bivic. 2002. hINAD1/PATJ, a homolog of discs lost, interacts with crumbs and localizes to tight junctions in human epithelial cells. J. Biol. Chem. 277:25408-25415.
31. Li, L., and S. N. Cohen. 1996. Tsg101: a novel tumor susceptibility gene isolated by controlled homozygous functional knockout of allelic loci in mammalian cells. Cell 85:319-329.
32. Lu, H., and D. Bilder. 2005. Endocytic control of epithelial polarity and proliferation in Drosophila. Nat. Cell Biol. 7:1232-1239.
33. Massimi, P., N. Gammoh, M. Thomas, and L. Banks. 2004. HPV E6 specifically targets different cellular pools of its PDZ domain-containing tumour suppressor substrates for proteasome-mediated degradation. Oncogene 23: 8033-8039.
34. Matter, K., and M. S. Balda. 2003. Signalling to and from tight junctions. Nat. Rev. MoI. Cell. Biol. 4:225-236.
35. McAllister, R. M., M. B. Gardner, A. E. Greene, C. Bradt, W. W. Nichols, and B. H. Landing. 1971. Cultivation in vitro of cells derived from a human osteosarcoma. Cancer 27:397-402.
36. Mills, G. B., Y. Lu, X. Fang, H. Wang, A. Eder, M. Mao, R. Swaby, K. W. Cheng, D. Stokoe, K. Siminovitch, R. Jaffe, and J. Gray. 2001. The role of genetic abnormalities of PTEN and the phosphatidylinositol 3-kinase pathway in breast and ovarian tumorigenesis, prognosis, and therapy. Semin. Oncol. 28:125-141.
37. Mol, C. D., J. M. Harris, E. M. McIntosh, and J. A. Tainer. 1996. Human dUTP pyrophosphatase: uracil recognition by a beta hairpin and active sites formed by three separate subunits. Structure 4:1077-1092.
38. Morgenstern, J. P., and H. Land. 1990. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18:3587-3596.
39. Nguyen, M. L., M. M. Nguyen, D. Lee, A. E. Griep, and P. F. Lambert. 2003. The PDZ ligand domain of the human papillomavirus type 16 E6 protein is required for E6's induction of epithelial hyperplasia in vivo. J. Virol. 77: 6957-6964.
40. Nyman, P. O. 2001. Introduction. dUTPases. Curr. Protein Pept. Sci. 2:277-285.
41. Patrie, K. M., A. J. Drescher, M. Goyal, R. C. Wiggins, and B. Margolis. 2001. The membrane-associated guanylate kinase protein MAGI-1 binds megalin and is present in glomerular podocytes. J. Am. Soc. Nephrol. 12: 667-677.
42. Pear, W. S., G. P. Nolan, M. L. Scott, and D. Baltimore. 1993. Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. USA 90:8392-8396.
43. Puthenveedu, M. A., and M. von Zastrow. 2006. Cargo regulates clathrin-coated pit dynamics. Cell 127:113-124.
44. Rao, D. S., S. V. Bradley, P. D. Kumar, T. S. Hyun, D. Saint-Dic, K. Oravecz-Wilson, C. G. Kleer, and T. S. Ross. 2003. Altered receptor trafficking in Huntingtin Interacting Protein 1-transformed cells. Cancer Cell 3:471-482.
45. Richardson, D. S., A. Z. Lai, and L. M. Mulligan. 2006. RET ligand-induced internalization and its consequences for downstream signaling. Oncogene 25:3206-3211.
46. Roymans, D., and H. Slegers. 2001. Phosphatidylinositol 3-kinases in tumor progression. Eur. J. Biochem. 268:487-498.
47. Samuels, Y., Z. Wang, A. Bardelli, N. Silliman, J. Ptak, S. Szabo, H. Yan, A. Gazdar, S. M. Powell, G. J. Riggins, J. K. Willson, S. Markowitz, K. W. Kinzler, B. Vogelstein, and V. E. Velculescu. 2004. High frequency of mutations of the P1K3CA gene in human cancers. Science 304:554.
48. Seto, E. S., H. J. Bellen, and T. E. Lloyd. 2002. When cell biology meets development: endocytic regulation of signaling pathways. Genes Dev. 16: 1314-1336.
49. Sheng, M., and C. Sala. 2001. PDZ domains and the organization of supramolecular complexes. Annu. Rev. Neurosci. 24:1-29.
50. Shenk, T. 2001. Adenoviridae: the viruses and their replication, p. 2265-2300. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed., vol. 2. Lippincott-Raven Publishers, Philadelphia, PA.
51. Shin, K., S. Straight, and B. Margolis. 2005. PATJ regulates tight junction formation and polarity in mammalian epithelial cells. J. Cell Biol. 168:705-711.
52. Soneoka, Y., P. M. Cannon, E. E. Ramsdale, J. C. Griffiths, G. Romano, S. M. Kingsman, and A. J. Kingsman. 1995. A transient three-plasmid expression system for the production of high titer retroviral vectors. Nucleic Acids Res. 23:628-633.
53. Sorkin, A., and M. Von Zastrow. 2002. Signal transduction and endocytosis: close encounters of many kinds. Nat. Rev. Mol. Cell. Biol. 3:600-614.
54. Thomas, D. L., J. Schaaek, H. Vogel, and R. Javier. 2001. Several E4 region functions influence mammary tumorigenesis by human adenovirus type 9. J. Virol. 75:557-568.
55. Thomas, D. L., S. Shin, B. H. Jiang, H. Vogel, M. A. Ross, M. Kaplitt, T. E. Shenk, and R. T. Javier. 1999. Early region 1 transforming functions are dispensable for mammary tumorigenesis by human adenovirus type 9. J. Virol. 73:3071-3079.
56. Thomas, U., B. Phannavong, B. Muller, C. C. Garner, and E. D. Gundelfinger. 1997. Functional expression of rat synapse-associated proteins SAP97 and SAP102 in Drosophila dlg-1 mutants: effects on tumor suppression and synaptic bouton structure. Mech. Dev. 62:161-174.
57. Umeda, K., J. Ikenouchi, S. Katahira-Tayama, K. Furuse, H. Sasaki, M. Nakayama, T. Matsui, S. Tsukita, M. Furuse, and S. Tsukita. 2006. ZO-1 and ZO-2 independently determine where claudins arc polymerized in tight-junction strand formation. Cell 126:741-754.
58. Vaccari, T., and D. Bilder. 2005. The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Dev. Cell 9:687-698.
59. Wang, J. B., W. J. Wu, and R. A. Cerione. 2005. Cdc42 and Ras cooperate to mediate cellular transformation by intersectin-L. J. Biol. Chem. 280:22883-22891.
60. Watson, R. A., M. Thomas, L. Banks, and S. Roberts. 2003. Activity of the human papillomavirus E6 PDZ-binding motif correlates with an enhanced morphological transformation of immortalized human keratinocytes. J. Cell Sci. 116:4925-4934.
61. Weiss, R. S., M. O. Gold, H. Vogel, and R. T. Javier. 1997. Mutant adenovirus type 9 E4 ORF1 genes define three protein regions required for transformation of CREF cells. J. Virol. 71:4385-4394.
62. Weiss, R. S., and R. T. Javier. 1997. A carboxy-terminal region required by the adenovirus type 9 E4 ORF1 oncoprotein for transformation mediates direct binding to cellular polypeptides. J. Virol. 71:7873-7880.
63. Weiss, R. S., S. S. Lee, B. V. Prasad, and R. T. Javier. 1997. Human adenovirus early region 4 open reading frame 1 genes encode growth-transforming proteins that may be distantly related to dUTP pyrophosphatase enzymes. J. Virol. 71:1857-1870.
64. Weiss, R. S., M. J. McArthur, and R. T. Javier. 1996. Human adenovirus type 9 E4 open reading frame 1 encodes a cyloplasmic transforming protein capable of increasing the oncogenicity of CREF cells. J. Virol. 70:862-872.
65. White, E. 2001. Regulation of the cell cycle and apoptosis by the oncogenes of adenovirus. Oncogene 20:7836-7846.
66. Wilkinson, D., R. R. de Vries, J. A. Madrigal, C. B. Lock, J. P. Morgenstern, J. Trowsdale, and D. M. Altmann. 1988. Analysis of HLA-DR glycoproteins by DNA-mediated gene transfer. Definition of DR2 beta gene products and antigen presentation to T cell clones from leprosy patients. J. Exp. Med. 167:1442-1458.
67. Zimmermann, P. 2006. The prevalence and significance of PDZ domain-phosphoinositide interactions. Biochim. Biophys. Acta 1761:947-956.