A tyrosine-based signal plays a critical role in the targeting and function of adenovirus RIDα protein

Journal of Virology

Volumn 81, Issue 19, 2007, Pages 10437-10450

  Cianciola, Nicholas L ^a   Crooks, Denise ^a,b   Shah, Ankur H ^a   Carlin, Cathleen ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CELL PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; HYBRID PROTEIN; PROTEIN RIDALPHA; TYROSINE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ADENOVIRUS; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; EARLY REGION 3 GENE; GENE FUNCTION; GENETIC ANALYSIS; GENETIC CODE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNITY; LIFE CYCLE; LYSOSOME; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; TRANSGENE; VIRUS GENE;

ADAPTOR PROTEIN COMPLEX 1; ADAPTOR PROTEIN COMPLEX 2; ADENOVIRIDAE; AMINO ACID SEQUENCE; CELL MEMBRANE; CYTOPLASM; DOWN-REGULATION; ENDOSOMES; GLUTATHIONE TRANSFERASE; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; POINT MUTATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TRANS-GOLGI NETWORK; TYROSINE; VIRAL PROTEINS;

ADENOVIRIDAE; HUMAN ADENOVIRUS; MAMMALIA;

EID: 34648816169     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00399-07     Document Type: Article

References (47)

1. Avila, M. M., G. Carballal, H. Rovaletti, B. Ebekian, M. Cusminsky, and M. Weissenbacher. 1989. Viral etiology in acute lower respiratory infections in children from a closed community. Am. Rev. Respir. Dis. 140:634-637.
2. Bonifacino, J., and L. Traub. 2003. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72:395-447.
3. Brandt, C. D., H. W. Kim, A. J. Vargosko, B. C. Jeffries, J. O. Arrobio, B. Rindge, R. H. Parrott, and R. M. Chanock. 1969. Infections in 18,000 infants and children in a controlled study of respiratory tract disease. I. Adenovirus pathogenicity in relation to serologic type and illness syndrome. Am. J. Epidemiol. 90:484-500.
4. Bretscher, A. 1989. Rapid phosphorylation and reorganization of ezrin and spectrin accompany morphological changes in A431 cells induced by EGF. J. Cell Biol. 108:921-930.
5. Carlin, C. R., and B. B. Knowles. 1986. Biosynthesis and glycosylation of the epidermal growth factor receptor in human tumor-derived cell lines A431 and Hep 3B. Mol. Cell. Biol. 6:257-264.
6. Carlin, C. R., D. Simon, J. Mattison, and B. B. Knowles. 1988. Expression and biosynthetic variation of the epidermal growth factor receptor in human hepatoma-derived cell lines. Mol. Cell. Biol. 8:25-34.
7. Carlin, C. R., A. E. Tollefson, H. A. Brady, B. L. Hoffman, and W. Wold. 1989. Epidermal growth factor receptor is down-regulated by a 10,400 MW protein encoded by the E3 region of adenovirus. Cell 57:135-144.
8. Chavrier, P., R. G. Parton, H. P. Hauri, K. Simons, and M. Zerial. 1990. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62:317-329.
9. Chin, Y. R., and M. S. Horwitz. 2005. Mechanism for removal of tumor necrosis factor receptor 1 from the cell surface by the adenovirus RIDα/β complex. J. Virol. 79:13606-13617.
10. Crooks, D., S. J. Kil, J. M. McCaffery, and C. Carlin. 2000. E3-13.7 integral membrane proteins encoded by human adenoviruses alter epidermal growth factor receptor trafficking by interacting directly with receptors in early endosomes. Mol. Biol. Cell 11:3559-3572.
11. Fessier, S., F. Delgado-Lopez, and M. Horwitz. 2004. Mechanisms of E3 modulation of immune and inflammatory responses. Curr. Top. Microbiol. Immunol. 273:113-135.
12. Giard, D. J., S. A. Aaronson, G. J. Todaro, P. Arnstein, J. H. Kersey, H. Dosik, and W. P. Parks. 1973. In vitro cultivation of human tumors. J. Natl. Cancer Inst. 51:1417-1423.
13. Ginsberg, H. 1999. The life and times of adenoviruses. Adv. Virus Res. 54:1-13.
14. Ginsberg, H. 1996. The ups and downs of adenovirus vectors. Bull. N.Y. Acad. Med. 73:53-58.
15. Ginsberg, H. S., and G. A. Prince. 1994. The molecular basis of adenovirus pathogenesis. Infect. Agents Dis. 3:1-8.
16. Graham, F. L., J. Smiley, W. C. Russell, and R. Nairn. 1977. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J. Gen. Virol. 36:59-74.
17. Greaves, J., and L. H. Chamberlain. 2007. Palmitoylation-dependent protein sorting. J. Cell Biol. 176:249-254.
18. Green, S. A., K. P. Zimmer, G. Griffiths, and I. Mellman. 1987. Kinetics of intracellular transport and sorting of lysosomal membrane and plasma membrane proteins. J. Cell Biol. 105:1227-1240.
19. Gu, F., and J. Gruenberg. 1999. Biogenesis of transport intermediates in the endocytic pathway. FEBS Lett. 452:61-66.
20. Hayflick, L. 1965. The limited in vitro lifetime of human diploid cell strains. Exp. Cell Res. 37:614-636.
21. Hilgendorf, A., J. Lindberg, Z. Ruzsics, S. Honing, A. Elsing, M. Lofqvist, H. Engelmann, and H.-G. Burgert. 2003. Two distinct transport motifs in the adenovirus E3 proteins act in concert to down-modulate apoptosis receptors and the epidermal growth factor receptor. J. Biol. Chem. 278:51872-51884.
22. Hirota, K., M. Murata, T. Itoh, J. Yodoi, and K. Fukuda. 2001. Redox-sensitive transactivation of epidermal growth factor receptor by tumor necrosis factor confers the NF-kappa B activation. J. Biol. Chem. 276:25953-25958.
23. Hobert, M. E., S. Kil, and C. R. Carlin. 1997. The cytoplasmic juxtamembrane domain of the epidermal growth factor receptor contains a novel autonomous basolateral sorting signal. J. Biol. Chem. 272:32901-32909.
24. Hoffman, B. L., K. Takishima, M. R. Rosner, and C. Carlin. 1993. Adenovirus and protein kinase C have distinct molecular requirements for regulating epidermal growth factor receptor trafficking. J. Cell. Physiol. 157:535-543.
25. Hoffman, B. L., A. Ullrich, W. Wold, and C. Carlin. 1990. Retrovirus-mediated transfer of an adenovirus gene encoding an integral membrane protein is sufficient to down regulate the receptor for epidermal growth factor. Mol. Cell. Biol. 10:5521-5524.
26. Hoffman, P., and C. Carlin. 1994. Adenovirus E3 protein causes constitutively internalized EGF receptors to accumulate in a prelysosomal compartment, resulting in enhanced degradation. Mol. Cell. Biol. 14:3695-3706.
27. Hoffman, P., M. B. Yaffe, B. L. Hoffman, S. Yei, W. S. M. Wold, and C. Carlin. 1992. Characterization of the adenovirus E3 protein that down-regulates the epidermal growth factor receptor. J. Biol. Chem. 267:13480-13487.
28. Hoffman, P. H., P. Rajakumar, B. Hoffman, R. Heuertz, W. S. M. Wold, and C. R. Carlin. 1992. Evidence for intracellular down-regulation of the epidermal growth factor receptor during adenovirus infection by an EGF-independent mechanism. J. Virol. 66:197-203.
29. Horwitz, M. S. 2004. Function of adenovirus E3 proteins and their interactions with immunoregulatory cell proteins. J. Gene Med. 6(Suppl. 1):S172-S183.
30. Husain, M., and B. Moss. 2003. Intracellular trafficking of a palmitoylated membrane-associated protein component of enveloped vaccinia virus. J. Virol. 77:9008-9019.
31. Glued, ORP1L, and the receptor βIII spectrin. J. Cell Biol. 176:459-471.
32. 680 mediate selective sorting of ligand-receptor complexes in early endocytic compartments. J. Cell. Physiol. 185:47-60.
33. Kil, S. J., M. E. Hobert, and C. Carlin. 1999. A leucine-based determinant in the EGF receptor juxtamembrane domain is required for the efficient transport of ligand-receptor complexes to lysosomes. J. Biol. Chem. 274:3141-3150.
34. Klausner, R. D., J. Van Renswoude, G. Ashwell, C. Kempf, A. N. Schecter, A. Dean, and K. R. Bridges. 1983. Receptor-mediated endocytosis of transferrin in K562 cells. J. Biol. Chem. 258:4715-4724.
35. Kuivinen, E., B. L. Hoffman, P. A. Hoffman, and C. R. Carlin. 1993. Structurally related class I and class II receptor protein tyrosine kinases are down-regulated by the same E3 protein coded by human group C adenoviruses. J. Cell Biol. 120:1271-1279.
36. Low, S. H., B. L. Tang, S. H. Wong, and W. Hong. 1992. Selective inhibition of protein targeting to the apical domain of MDCK cells by brefeldin A. J. Cell Biol. 118:51-62.
37. Marks, M. S., H. Ohno, T. Kirchhausen, and J. S. Bonifacino. 1997. Protein sorting by tyrosine-based signals: adapting to the Ys and wherefores. Trends Cell Biol. 7:124-128.
38. Monick, M. M., K. Cameron, J. Staber, L. S. Powers, T. O. Yarovinsky, J. G. Koland, and G. W. Hunninghake. 2005. Activation of the epidermal growth factor receptor by respiratory syncytial virus results in increased inflammation and delayed apoptosis. J. Biol. Chem. 280:2147-2158.
39. Ohno, H., R. C. Aguilar, D. Yeh, D. Taura, T. Saito, and J. S. Bonifacino. 1998. The medium subunits of adaptor complexes recognize distinct but overlapping sets of tyrosine-based sorting signals. J. Biol. Chem. 273:25915-25921.
40. Puck, T. T., S. J. Cieciura, and A. Robinson. 1958. Genetics of somatic mammalian cells. III. Long-term cultivation of euploid cells from human and animal subjects. J. Exp. Med. 108:945-956.
41. Robinson, M. 1993. Assembly and targeting of adaptin chimeras in transfected cells. J. Cell Biol. 123:67-77.
42. Robinson, M. S., and J. S. Bonifacino. 2001. Adaptor-related proteins. Curr. Opin. Cell Biol. 13:444-453.
43. Stewart, A., A. Tollefson, P. Krajcsi, S. Yei, and W. Wold. 1995. The adenovirus E3 10.4K and 14.5K proteins, which function to prevent cytolysis by tumor necrosis factor and to down-regulate the epidermal growth factor receptor, are localized in the plasma membrane. J. Virol. 69:172-181.
44. Tsacoumangos, A., S. J. Kil, L. Ma, F. D. Sonnichsen, and C. Carlin. 2005. A novel dileucine lysosomal-sorting-signal mediates intracellular EGF-receptor retention independently of protein ubiquitylation. J. Cell Sci. 118:3959-3971.
45. Vinogradova, O., C. R. Carlin, F. D. Sonnichsen, and C. R. Sanders. 1998. A membrane setting for the sorting motifs present in the adenovirus E3-13.7 protein which down-regulates the epidermal growth factor receptor. J. Biol. Chem. 273:17343-17350.
46. Waterfield, M. D., E. L. V. Mayes, P. Stroobant, P. L. P. Bennet, S. Young, P. N. Goodfellow, G. S. Banting, and B. Ozanne. 1982. A monoclonal antibody to the human epidermal growth factor receptor. J. Cell. Biochem. 20:149-161.
47. Weiel, J. E., and T. A. Hamilton. 1984. Quiescent lymphocytes express intracellular transferrin receptors. Biochem. Biophys. Res. Commun. 119:598-603.