Compensatory mutants of the bovine papillomavirus E5 protein and the platelet-derived growth factor β receptor reveal a complex direct transmembrane interaction

Journal of Virology

Volumn 87, Issue 20, 2013, Pages 10935-10945

  Edwards, Anne P B ^a   Xie, Yanhua ^a   Bowers, Lara ^a   DiMaio, Daniel ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

E5 PROTEIN; ISOLEUCINE; LEUCINE; MEMBRANE PROTEIN; MUTANT PROTEIN; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; UNCLASSIFIED DRUG; VIRUS PROTEIN; ONCOGENE PROTEIN E5, BOVINE PAPILLOMAVIRUS TYPE 1; ONCOPROTEIN; PLATELET DERIVED GROWTH FACTOR RECEPTOR;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BAF3 CELL; BOVINE PAPILLOMAVIRUS; CELL LINE; COMPLEX FORMATION; CONTROLLED STUDY; GENE DELETION; GENE MUTATION; HUMAN; HUMAN CELL; NONHUMAN; PAPILLOMA VIRUS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; AMINO ACID SEQUENCE; ANIMAL; CATTLE; GENETICS; METABOLISM; MISSENSE MUTATION; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; CATTLE; CELL LINE; DNA MUTATIONAL ANALYSIS; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION, MISSENSE; ONCOGENE PROTEINS, VIRAL; PROTEIN INTERACTION MAPPING; RECEPTORS, PLATELET-DERIVED GROWTH FACTOR; SEQUENCE DELETION;

EID: 84886919852     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01475-13     Document Type: Article

References (39)

1. Lehnert U, Xia Y, Royce TE, Goh CS, Liu Y, Senes A, Yu H, Zhang ZL, Engelman DM, Gerstein M. 2004. Computational analysis of membrane proteins: genomic occurrence, structure prediction and helix interactions. Q. Rev. Biophys. 37:121-146.
2. MacKenzie KR. 2006. Folding and stability of α-helical integral membrane proteins. Chem. Rev. 106:1931-1977.
3. Schneider D, Finger C, Prodohl A, Volkmer T. 2007. From interactions of single transmembrane helices to folding of alpha-helical membrane proteins: analyzing transmembrane helix-helix interactions in bacteria. Curr. Protein Pept. Sci. 8:45-61.
4. Lemmon MA, Flanagan JM, Treutlein HR, Zhang J, Engelman DM. 1992. Sequence specificity in the dimerization of transmembrane α-helices. Biochemistry 31:12719-12725.
5. Call ME, Pyrdol J, Wiedmann M, Wucherpfennig KW. 2002. The organizing principle in the formation of the T cell receptor-CD3 complex. Cell 111:967-979.
6. Cosson P, Lankford SP, Bonifacino JS, Klausner RD. 1991. Membrane protein association by potential intramembrane charge pairs. Nature 351: 414-416.
7. Manolios N, Bonifacino JS, Klausner RD. 1990. Transmembrane helical interactions and the assembly of the T cell receptor complex. Science 249: 274-277.
8. Cammett TJ, Jun SJ, Cohen EB, Barrera FN, Engelman DM, DiMaio D. 2010. Construction and genetic selection of small transmembrane proteins that activate the human erythropoietin receptor. Proc. Natl. Acad. Sci. U. S. A. 107:3447-3452.
9. Freeman-Cook L, Dixon AM, Frank JB, Xia Y, Ely L, Gerstein M, Engelman DM, DiMaio D. 2004. Selection and characterization of small random transmembrane proteins that bind and activate the plateletderived growth factor β receptor. J. Mol. Biol. 338:907-920.
10. Freeman-Cook LL, Edwards APB, Dixon AM, Yates KE, Ely L, Engelman DM, DiMaio D. 2005. Specific locations of hydrophilic amino acids in constructed transmembrane ligands of the platelet-derived growth factor β receptor. J. Mol. Biol. 345:907-921.
11. Ptacek JB, Edwards APB, Freeman-Cook LL, DiMaio D. 2007. Packing contacts can mediate highly specific interactions between artificial transmembrane proteins and the PDGF β receptor. Proc. Natl. Acad. Sci. U. S. A. 104:11945-11950.
12. Scheideman EH, Marlatt SA, Xie Y, Hu Y, Sutton RE, DiMaio D. 2012. Transmembrane protein aptamers that inhibit CCR5 expression and HIV coreceptor function. J. Virol. 86:10281-10292.
13. Schlegel R, Wade-Glass M, Rabson MS, Yang Y-C. 1986. The E5 transforming gene of bovine papillomavirus encodes a small hydrophobic protein. Science 233:464-467.
14. Talbert-Slagle K, DiMaio D. 2009. The bovine papillomavirus E5 protein and the PDGF β receptor: it takes two to tango. Virology 384:345-351.
15. Goldstein DJ, Andresson T, Sparkowski JJ, Schlegel R. 1992. The BPV-1 E5 protein, the 16 kDa membrane pore-forming protein and the PDGF receptor exist in a complex that is dependent on hydrophobic transmembrane interactions. EMBO J. 11:4851-4859.
16. Petti L, DiMaio D. 1992. Stable association between the bovine papillomavirus E5 transforming protein and activated platelet-derived growth factor receptor in transformed mouse cells. Proc. Natl. Acad. Sci. U. S. A. 89:6736-6740.
17. Drummond-Barbosa DA, Vaillancourt RR, Kazlauskas A, DiMaio D. 1995. Ligand-independent activation of the platelet-derived growth factor beta receptor: requirements for bovine papillomavirus E5-induced mitogenic signaling. Mol. Cell. Biol. 15:2570-2581.
18. Goldstein DJ, Kulke R, DiMaio D, Schlegel R. 1992. A glutamine residue in the membrane-associating domain of the bovine papillomavirus type 1 E5 oncoprotein mediates its binding to a transmembrane component of the vacuolar H(+)-ATPase. J. Virol. 66:405-413.
19. Lai CC, Henningson C, DiMaio D. 1998. Bovine papillomavirus E5 protein induces oligomerization and trans-phosphorylation of the platelet- derived growth factor β receptor. Proc. Natl. Acad. Sci. U. S. A. 95: 15241-15246.
20. Nilson LA, DiMaio D. 1993. Platelet-derived growth factor receptor can mediate tumorigenic transformation by the bovine papillomavirus E5 protein. Mol. Cell. Biol. 13:4137-4145.
21. Petti L, Nilson LA, DiMaio D. 1991. Activation of the platelet-derived growth factor receptor by the bovine papillomavirus E5 transforming protein. EMBO J. 10:845-855.
22. Goldstein DJ, Li W, Wang L-M, Heidaran MA, Aaronson SA, Shinn R, Schlegel R, Pierce JH. 1994. The bovine papillomavirus type 1 E5 transforming protein specifically binds and activates the beta-type receptor for platelet-derived growth factor but not other tyrosine kinase-containing receptors to induce cellular transformation. J. Virol. 68:4432-4441.
23. Nappi VM, Petti LM. 2002. Multiple transmembrane amino acid requirements suggest a highly specific interaction between the bovine papillomavirus E5 oncoprotein and the platelet-derived growth factor beta receptor. J. Virol. 76:7976-7986.
24. Nappi VM, Schaefer JA, Petti LM. 2002. Molecular examination of the transmembrane requirements of the platelet-derived growth factor beta receptor for a productive interaction with the bovine papillomavirus E5 oncoprotein. J. Biol. Chem. 277:47149-47159.
25. Petti L, DiMaio D. 1994. Specific interaction between the bovine papillomavirus E5 transforming protein and the beta receptor for plateletderived growth factor in stably transformed and acutely transfected cells. J. Virol. 68:3582-3592.
26. Staebler A, Pierce JH, Brazinski S, Heidaran MA, Li W, Schlegel R, Goldstein DJ. 1995. Mutational analysis of the beta-type platelet-derived growth factor receptor defines the site of interaction with the bovine papillomavirus type 1 E5 transforming protein. J. Virol. 69:6507-6517.
27. Horwitz BH, Burkhardt AL, Schlegel R, DiMaio D. 1988. 44-amino-acid E5 transforming protein of bovine papillomavirus requires a hydrophobic core and specific carboxyl-terminal amino acids. Mol. Cell. Biol. 8:4071-4078.
28. Meyer AN, Xu Y-F, Webster MK, Smith AS, Donoghue DJ. 1994. Cellular transformation by a transmembrane peptide: structural requirements for the bovine papillomavirus E5 oncoprotein. Proc. Natl. Acad. Sci. U. S. A. 91:4634-4638.
29. Nilson LA, Gottlieb RL, Polack GW, DiMaio D. 1995. Mutational analysis of the interaction between the bovine papillomavirus E5 transforming protein and the endogenous beta receptor for platelet-derived growth factor in mouse C127 cells. J. Virol. 69:5869-5874.
30. Petti LM, Reddy V, Smith SO, DiMaio D. 1997. Identification of amino acids in the transmembrane and juxtamembrane domains of the plateletderived growth factor receptor required for productive interaction with the bovine papillomavirus E5 protein. J. Virol. 71:7318-7327.
31. Burkhardt A, Willingham M, Gay C, Jeang K-T, Schlegel R. 1989. The E5 oncoprotein of bovine papillomavirus is oriented asymmetrically in Golgi and plasma membranes. Virology 170:334-339.
32. Klein O, Kegler-Ebo D, Su J, Smith S, DiMaio D. 1999. The bovine papillomavirus E5 protein requires a juxtamembrane negative charge for activation of the platelet-derived growth factor beta receptor and transformation of C127 cells. J. Virol. 73:3264-3272.
33. Klein O, Polack GW, Surti T, Kegler-Ebo D, Smith SO, DiMaio D. 1998. Role of glutamine 17 of the bovine papillomavirus E5 protein in plateletderived growth factor beta receptor activation and cell transformation. J. Virol. 72:8921-8932.
34. King G, Oates J, Patel D, van den Berg HA, Dixon AM. 2011. Towards a structural understanding of the smallest known oncoprotein: investigation of the bovine papillomavirus E5 protein using solution-state NMR. Biochim. Biophys. Acta 1808:1493-1501.
35. Surti T, Klein O, Aschheim K, DiMaio D, Smith SO. 1998. Structural models of the bovine papillomavirus E5 protein. Proteins 33:601-612.
36. Naviaux RK, Costanzi E, Haas M, Verma IM. 1996. The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J. Virol. 70:5701-5705.
37. Talbert-Slagle K, Marlatt S, Barrera FN, Khurana E, Oates J, Gerstein M, Engelman DM, Dixon AM, DiMaio D. 2009. Artificial transmembrane oncoproteins smaller than the bovine papillomavirus E5 protein redefine the sequence requirements for activation of the platelet-derived growth factor beta receptor. J. Virol. 83:9773-9785.
38. MacKenzie KR, Fleming KG. 2008. Association energetics of membrane spanning alpha-helices. Curr. Opin. Struct. Biol. 18:412-419.
39. MacKenzie KR, Engelman DM. 1998. Structure-based prediction of the stability of transmembrane helix-helix interactions: the sequence dependence of glycophorin A dimerization. Proc. Natl. Acad. Sci. U. S. A. 95: 3583-3590.