The platelet-derived growth factor ß receptor as a target of the bovine papillomavirus E5 protein

zur Hausen, 1991, Viruses in human cancers, Science, 254, 1167, 10.1126/science.1659743 Drummond-Barbosa, 1997, Virocrine transformation, Biochem. Biophys. Acta, 1332, M1 DiMaio, 1998, Virocrine transformation: the intersection between viral transforming proteins and cellular signal transduction pathways, Annu. Rev. Microbiol., 52, 397, 10.1146/annurev.micro.52.1.397 Schlegel, 1986, The E5 transforming gene of bovine papillomavirus encodes a small hydrophobic protein, Science, 233, 464, 10.1126/science.3014660 Surti, 1998, Structural models of the bovine papillomavirus E5 protein, Proteins: structure, function, and genetics, 33, 601, 10.1002/(SICI)1097-0134(19981201)33:4<601::AID-PROT12>3.0.CO;2-I DiMaio, 1986, Translation of open reading frame E5 of bovine papillomavirus is required for its trasnforming activity, Proc. Natl. Acad. Sci. USA, 83, 1797, 10.1073/pnas.83.6.1797 Schiller, 1986, E5 open reading frame of bovine papillomavirus type 1 encodes a transforming gene, J. Virol., 57, 1, 10.1128/jvi.57.1.1-6.1986 Burkhardt, 1987, Genetic and biochemical definition of the bovine papillomavirus E5 transforming protein, EMBO J., 6, 2381, 10.1002/j.1460-2075.1987.tb02515.x Bergman, 1988, The E5 gene of bovine papillomavirus type 1 is sufficient for complete oncogenic transformation of mouse fibroblasts, Oncogene, 2, 453 Burkhardt, 1989, The E5 oncoprotein of bovine papillomavirus is oriented asymmetrically in Golgi and plasma membranes, Virology, 170, 334, 10.1016/0042-6822(89)90391-7 Burnett, 1992, Localization of bovine papillomavirus type 1 E5 protein to transformed basal keratinocytes and permissive differentiated cells in fibropapilloma tissue, Proc. Natl. Acad. Sci. USA, 89, 5665, 10.1073/pnas.89.12.5665 Horwitz, 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 Horwitz, 1989, Transforming activity of a sixteen-amino-acid segment of the bovine papillomavirus E5 protein linked to random sequences of hydrophobic amino acids, J. Virol., 63, 4515, 10.1128/jvi.63.11.4515-4519.1989 Kulke, 1992, The central hydrophobic domain of the bovine papillomavirus E5 transforming protein can be functionally replaced by many random hydrophobic sequences containing a glutamine, J. Virol., 66, 505, 10.1128/jvi.66.1.505-511.1992 Meyer, 1994, Cellular transformation by a transmembrane peptide: structural requirements for the bovine papillomavirus E5 oncoprotein, Proc. Natl. Acad. Sci. USA, 91, 4634, 10.1073/pnas.91.11.4634 Martin, 1989, The bovine papillomavirus E5 transforming protein can stimulate the transforming activity of EGF and CSF-1 receptors, Cell, 59, 21, 10.1016/0092-8674(89)90866-0 Settleman, 1989, Genetic evidence that acute morphologic transformation, stimulation of cellular DNA synthesis, and focus formation are mediated by a single activity of the bovine papillomavirus E5 protein, Mol. Cell Biol., 9, 5563 Petti, 1991, Activation of the platelet-derived growth factor receptor by the bovine papillomavirus E5 protein, EMBO J., 10, 845, 10.1002/j.1460-2075.1991.tb08017.x Nilson, 1993, Platelet-derived growth factor receptor can mediate tumorigenic transformation by the bovine papillomavirus E5 protein, Mol. Cell Biol., 13, 4137 Petti, 1994, Specific interaction between the bovine papillomavirus E5 protein and the platelet-derived growth factor receptor in stably transformed and acutely transfected cells, J. Virol., 68, 3582, 10.1128/jvi.68.6.3582-3592.1994 Petti, 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. USA, 89, 6736, 10.1073/pnas.89.15.6736 Goldstein, 1994, The bovine papillomavirus type 1 E5 transforming protein specifically binds and activates the ß-type receptor for platelet-derived growth factor but not other tyrosine kinase-containing receptors to induce cellular transformation, J. Virol., 68, 4432, 10.1128/jvi.68.7.4432-4441.1994 Drummond-Barbosa, 1995, Ligand-independent activation of the platelet-derived growth factor szlig receptor: requirements for bovine papillomavirus E5-induced mitogenic signaling, Mol. Cell Biol., 15, 2570, 10.1128/MCB.15.5.2570 Cohen, 1993, Transformation-specific interaction of the bovine papillomavirus E5 oncoprotein with the platelet-derived growth factor receptor transmembrane domain and the epidermal growth factor receptor cytoplasmic domain, J. Virol., 67, 5303, 10.1128/jvi.67.9.5303-5311.1993 Kulke, 1991, Biological activities of the E5 protein of the deer papillomavirus in mouse C127 cells: morphologic transformation, induction of cellular DNA synthesis and activation of the PDGF receptor, J. Virol., 65, 4943, 10.1128/jvi.65.9.4943-4949.1991 Lai, 1998, Bovine papillomavirus E5 protein induces oligomerization and trans-phosphorylation of the platelet-derived growth factor ß receptor, Proc. Natl. Acad. Sci. USA, 95, 15241, 10.1073/pnas.95.26.15241 Lai CC, Henningson C, DiMaio D. Bovine papillomavirus E5 protein induces the formation of signal transduction complexes containing dimeric activated PDGF ß receptor and associated signaling proteins. J Biol Chem 2000;275:9832–40 Nilson, 1995, Mutational analysis of the interaction between the bovine papillomavirus E5 transforming protein and the endogenous ß receptor for platelet-derived growth factor in mouse C127 cells, J. Virol., 69, 5869, 10.1128/jvi.69.9.5869-5874.1995 Kovalenko, 1994, Selective platelet-derived growth factor receptor kinase blockers reverse sis-transformation., Cancer Res., 54, 6106 Klein, 1998, Role of glutamine 17 of the bovine papillomavirus E5 protein in platelet-derived growth factor ß receptor activation and cell transformation, J. Virol., 72, 8921, 10.1128/JVI.72.11.8921-8932.1998 Riese, 1995, An intact PDGF signalling pathway is required for efficient growth transformation of mouse C127 cells by the bovine papillomavirus E5 protein, Oncogene, 10, 1431 Klein, 1999, The bovine papillomavirus E5 protein requires a juxtamembrane negative charge for activation of the platelet-derived growth factor ß receptor and transformation of C127 cells, J. Virol., 73, 3264, 10.1128/JVI.73.4.3264-3272.1999 Doolittle, 1983, Simian sarcoma virus onc gene v-sis is derived from the gene (or genes) encoding a platelet-derived growth factor, Science, 221, 275, 10.1126/science.6304883 Waterfield, 1983, Platelet-derived growth factor is structurally related to the putative transforming protein p28sis of simian sarcoma virus, Nature, 304, 35, 10.1038/304035a0 Sparkowski, 1996, E5 oncoprotein transmembrane mutants dissociate fibroblast transforming activity from 16-kilodalton protein binding and platelet-derived growth factor receptor binding and phosphorylation, J. Virol., 70, 2420, 10.1128/jvi.70.4.2420-2430.1996 Adduci, 1999, The transmembrane domain of the E5 oncoprotein contains functionally discrete helical faces, J. Biol. Chem., 274, 10249, 10.1074/jbc.274.15.10249 Suprynowicz, 2000, E5 oncoprotein mutants activate phosphoinositide 3-kinase independently of platelet-derived growth factor receptor activation, J. Biol. Chem., 275, 5111, 10.1074/jbc.275.7.5111 Goldstein, 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, 10.1002/j.1460-2075.1992.tb05591.x Staebler, 1995, Mutational analysis of the ß-type platelet-derived growth factor receptor defines the site of interaction with the bovine papillomavirus type 1 E5 transforming protein, J. Virol., 69, 6507, 10.1128/jvi.69.10.6507-6517.1995 Petti, 1997, Identification of amino acids in the transmembrane and juxtamembrane domains of the platelet-derived growth factor receptor required for productive interaction with the bovine papillomavirus E5 protein, J. Virol., 71, 7318, 10.1128/jvi.71.10.7318-7327.1997 Heldin, 1998, Signal transduction via platelet-derived growth factor receptors, Biochim. Biophys. Acta, 1378, F79 Andresson, 1995, Vacuolar H+-ATPase mutants transform cells and define a binding site for the papillomavirus E5 oncoprotein, J. Biol. Chem., 270, 6830, 10.1074/jbc.270.12.6830 Goldstein, 1992, A glutamine residue in the membrane-associating domain of the BPV-1 E5 oncoprotein mediates its binding to a transmembrane component of the vacuolar H+-ATPase, J. Virol., 66, 405, 10.1128/jvi.66.1.405-413.1992 Schapiro, 2000, Golgi alkalinization by the papillomavirus E5 oncoprotein, J. Cell Biol., 148, 305, 10.1083/jcb.148.2.305 Cohen, 1993, The conserved C-terminal domain of the bovine papillomavirus E5 oncoprotein can associate with an α-adaptin-like molecule: a possible link between growth factor receptors and viral transformation, Mol. Cell Biol., 13, 6462 Conrad, 1993, The human papillomavirus type 6 and 16 E5 proteins are membrane-associated proteins which associate with the 16-kilodalton pore-forming protein, J. Virol., 67, 6170, 10.1128/jvi.67.10.6170-6178.1993 Leptak C, Ramon y Cajal S, Kulke R, Riese DR, Horwitz BH, Dotto GP, DiMaio D. Tumorigenic transformation of mouse keratinocytes by the E5 genes of human papillomavirus type 16 and bovine papillomavirus type 1 J. Virol. 65 1991 7078 7083. Correction: J. Virol. 66: 1833 Ullrich, 1990, Signal transduction by receptors with tyrosine kinase activity, Cell, 61, 203, 10.1016/0092-8674(90)90801-K Keating, 1988, Autocrine stimulation of intracellular PDGF receptors in v-sis-transformed cells, Science, 239, 914, 10.1126/science.2829358 Sparkowski, 1995, E5 oncoprotein retained in the endoplasmic reticulum/cis Golgi still induces PDGF receptor autophosphorylation but does not transform cells, EMBO J., 14, 3055, 10.1002/j.1460-2075.1995.tb07308.x Bernard, 1999, Phosphospecific antibodies reveal temporal regulation of platelet-derived growth factor ß receptor signaling, Exp. Cell. Res., 253, 704, 10.1006/excr.1999.4715 Burke, 1997, Dimerization of the p185neu transmembrane domain is necessary but not sufficient for transformation, Oncogene, 14, 687, 10.1038/sj.onc.1200873 Burke, 1998, Activation of neu (ErbB-2) mediated by disulfide bond-induced dimerization reveals a receptor tyrosine kinase dimer interface, Mol. Cell Biol., 18, 5371, 10.1128/MCB.18.9.5371 Remy, 1999, Erythropoietin receptor activation by a ligand-induced conformation change, Science, 283, 990, 10.1126/science.283.5404.990 Ghai, 1996, The E5 gene product of rhesus papillomavirus is an activator of endogenous Ras and phosphatidylinositol-3′-kinase in NIH 3T3 cells, Proc. Natl. Acad. Sci. USA, 93, 12879, 10.1073/pnas.93.23.12879 Carroll, 1996, The TEL/platelet-derived growth factor ß receptor (PDGF ß R) fusion in chronic myelomonocytic leukemia is a transforming protein that self-associates and activates PDGF ß R kinase-dependent signaling pathways, Proc. Natl. Acad. Sci. USA, 93, 14845, 10.1073/pnas.93.25.14845 Irusta, 1998, A single amino acid substitution in a WW-like domain of diverse members of the PDGF receptor subfamily of tyrosine kinases causes constitutive receptor activation, EMBO J., 17, 6912, 10.1093/emboj/17.23.6912 Petti, 1998, Oncogenic activation of the PDGF ß receptor by the transmembrane domain of p185neu∗, Oncogene, 16, 843, 10.1038/sj.onc.1201590 Ross, 1998, Fusion of Huntington interacting protein 1 to platelet-derived growth factor ß receptor (PDGFßR) in chronic myelomonocytic leukemia with t(5;7) (q33; q11.2), Blood, 91, 4419, 10.1182/blood.V91.12.4419