Viral Miniproteins

Literature Cited

1. Acharya R, Carnevale V, Fiorin G, Levine BG, Polishchuk AL. 1.  et al. 2010. Structure and mechanism of proton transport through the transmembrane tetrameric M2 protein bundle of the influenza A virus. Proc. Natl. Acad. Sci. USA 107:15075–80 [Google Scholar]
2. Adduci AJ, Schlegel R. 2.  1999. The transmembrane domain of the E5 oncoprotein contains functionally discrete helical faces. J. Biol. Chem. 274:10249–58 [Google Scholar]
3. Alix E, Blanc-Potard AB. 3.  2008. Peptide-assisted degradation of the Salmonella MgtC virulence factor. EMBO J. 27:546–57 [Google Scholar]
4. Alix E, Blanc-Potard AB. 4.  2009. Hydrophobic peptides: novel regulators within bacterial membrane. Mol. Microbiol. 72:5–11 [Google Scholar]
5. Arias JF, Iwabu Y, Tokunaga K. 5.  2011. Structural basis for the antiviral activity of BST-2/tetherin and its viral antagonism. Front. Microbiol. 2:250 [Google Scholar]
6. Arias JF, Iwabu Y, Tokunaga K. 6.  2012. Sites of action of HIV-1 Vpu in BST-2/tetherin downregulation. Curr. HIV Res. 10:283–91 [Google Scholar]
7. Balannik V, Carnevale V, Fiorin G, Levine BG, Lamb RA. 7.  et al. 2010. Functional studies and modeling of pore-lining residue mutants of the influenza A virus M2 ion channel. Biochemistry 49:696–708 [Google Scholar]
8. Balannik V, Wang J, Ohigashi Y, Jing X, Magavern E. 8.  et al. 2009. Design and pharmacological characterization of inhibitors of amantadine-resistant mutants of the M2 ion channel of influenza A virus. Biochemistry 48:11872–82 [Google Scholar]
9. Bao X, Kolli D, Liu T, Shan Y, Garofalo RP, Casola A. 9.  2008. Human metapneumovirus small hydrophobic protein inhibits NF-κB transcriptional activity. J. Virol. 82:8224–29 [Google Scholar]
10. Betakova T, Wolffe EJ, Moss B. 10.  2000. The vaccinia virus A14.5L gene encodes a hydrophobic 53-amino-acid virion membrane protein that enhances virulence in mice and is conserved among vertebrate poxviruses. J. Virol. 74:4085–92 [Google Scholar]
11. Binette J, Dube M, Mercier J, Halawani D, Latterich M, Cohen EA. 11.  2007. Requirements for the selective degradation of CD4 receptor molecules by the human immunodeficiency virus type 1 Vpu protein in the endoplasmic reticulum. Retrovirology 4:75 [Google Scholar]
12. Bolduan S, Votteler J, Lodermeyer V, Greiner T, Koppensteiner H. 12.  et al. 2011. Ion channel activity of HIV-1 Vpu is dispensable for counteraction of CD317. Virology 416:75–85 [Google Scholar]
13. Bruce EA, Medcalf L, Crump CM, Noton SL, Stuart AD. 13.  et al. 2009. Budding of filamentous and non-filamentous influenza A virus occurs via a VPS4 and VPS28-independent pathway. Virology 390:268–78 [Google Scholar]
14. Butticaz C, Michielin O, Wyniger J, Telenti A, Rothenberger S. 14.  2007. Silencing of both β-TrCP1 and HOS (β-TrCP2) is required to suppress human immunodeficiency virus type 1 Vpu-mediated CD4 down-modulation. J. Virol. 81:1502–5 [Google Scholar]
15. Cady SD, Schmidt-Rohr K, Wang J, Soto CS, Degrado WF, Hong M. 15.  2010. Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers. Nature 463:689–92Amantadine binds inside the influenza A virus M2 channel, inhibiting proton transport and blocking infection. [Google Scholar]
16. Cammett TJ, Jun SJ, Cohen EB, Barrera FN, Engelman DM, DiMaio D. 16.  2010. Construction and genetic selection of small transmembrane proteins that activate the human erythropoietin receptor. Proc. Natl. Acad. Sci. USA 107:3447–52The transmembrane domain of a traptamer targets it to a novel target, the erythropoietin receptor. [Google Scholar]
17. Chacón KM, Petti LM, Scheideman EH, Pirazzoli V, Politi K, DiMaio D. 17.  2014. De novo selection of oncogenes. Proc. Natl. Acad. Sci. USA 111:E6–14 [Google Scholar]
18. Chen BJ, Lamb RA. 18.  2008. Mechanisms for enveloped virus budding: Can some viruses do without an ESCRT?. Virology 372:221–32 [Google Scholar]
19. Chichón FJ, Rodríguez MJ, Risco C, Fraile-Ramos A, Fernández JJ. 19.  et al. 2009. Membrane remodelling during vaccinia virus morphogenesis. Biol. Cell 101:401–14 [Google Scholar]
20. Corteggio A, Altamura G, Roperto F, Borzacchiello G. 20.  2013. Bovine papillomavirus E5 and E7 oncoproteins in naturally occurring tumors: Are two better than one?. Infect. Agents Cancer 8:1 [Google Scholar]
21. DiMaio D, Petti LM. 21.  2013. The E5 proteins. Virology 445:99–114 [Google Scholar]
22. Drummond-Barbosa DA, Vaillancourt RR, Kazlauskas A, DiMaio D. 22.  1995. Ligand-independent activation of the platelet-derived growth factor β receptor: requirements for bovine papillomavirus E5-induced mitogenic signaling. Mol. Cell. Biol. 15:2570–81 [Google Scholar]
23. Dube M, Bego MG, Paquay C, Cohen EA. 23.  2010. Modulation of HIV-1-host interaction: role of the Vpu accessory protein. Retrovirology 7:114 [Google Scholar]
24. Dube M, Paquay C, Roy BB, Bego MG, Mercier J, Cohen EA. 24.  2011. HIV-1 Vpu antagonizes BST-2 by interfering mainly with the trafficking of newly synthesized BST-2 to the cell surface. Traffic 12:1714–29 [Google Scholar]
25. Duff KC, Ashley RH. 25.  1992. The transmembrane domain of influenza A M2 protein forms amantadine-sensitive proton channels in planar lipid bilayers. Virology 190:485–89 [Google Scholar]
26. Edwards AP, Xie Y, Bowers L, DiMaio D. 26.  2013. Compensatory mutants of the bovine papillomavirus E5 protein and the platelet-derived growth factor β receptor reveal a complex direct transmembrane interaction. J. Virol. 87:10936–45 [Google Scholar]
27. Edwards D, Fenizia C, Gold H, Fernanda de Castro-Amarante M, Buchmann C. 27.  et al. 2011. Orf-I and Orf-II-encoded proteins in HTLV-1 infection and persistence. Viruses 3:861–85 [Google Scholar]
28. Fehrmann F, Klumpp DJ, Laimins LA. 28.  2003. Human papillomavirus type 31 E5 protein supports cell cycle progression and activates late viral functions upon epithelial differentiation. J. Virol. 77:2819–31 [Google Scholar]
29. Fontaine F, Fuchs RT, Storz G. 29.  2011. Membrane localization of small proteins in Escherichia coli. J. Biol. Chem. 86:32464–74 [Google Scholar]
30. Freeman-Cook L, Dixon AM, Frank JB, Xia Y, Ely L. 30.  et al. 2004. Selection and characterization of small random transmembrane proteins that bind and activate the platelet-derived growth factor β receptor. J. Mol. Biol. 338:907–20 [Google Scholar]
31. Freeman-Cook LL, Edwards APB, Dixon AM, Yates KE, Ely L. 31.  et al. 2005. Specific locations of hydrophilic amino acids in constructed transmembrane ligands of the platelet-derived growth factor β receptor. J. Mol. Biol. 345:907–21 [Google Scholar]
32. Fuentes S, Tran KC, Luthra P, Teng MN, He B. 32.  2007. Function of the respiratory syncytial virus small hydrophobic protein. J. Virol. 81:8361–66 [Google Scholar]
33. Fujita K, Omura S, Silver J. 33.  1997. Rapid degradation of CD4 in cells expressing human immunodeficiency virus type 1 Env and Vpu is blocked by proteasome inhibitors. J. Gen. Virol. 78:Pt. 3619–25 [Google Scholar]
34. Gan SW, Tan E, Lin X, Yu D, Wang J. 34.  et al. 2012. The small hydrophobic protein of the human respiratory syncytial virus forms pentameric ion channels. J. Biol. Chem. 287:24671–89 [Google Scholar]
35. Genther SM, Sterling S, Duensing S, Munger K, Sattler C, Lambert PF. 35.  2003. Quantitative role of the human papillomavirus type 16 E5 gene during the productive stage of the viral life cycle. J. Virol. 77:2832–42 [Google Scholar]
36. Genther-Williams SM, Disbrow GL, Schlegel R, Lee D, Threadgill DW, Lambert PF. 36.  2005. Requirement of epidermal growth factor receptor for hyperplasia induced by E5, a high-risk human papillomavirus oncogene. Cancer Res. 65:6534–42 [Google Scholar]
37. Goebel SJ, Johnson GP, Perkus ME, Davis SW, Winslow JP, Paoletti E. 37.  1990. The complete DNA sequence of vaccinia virus. Virology 179:247–66, 517–63 [Google Scholar]
38. Goldstein DJ, Andresson T, Sparkowski JJ, Schlegel R. 38.  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. 11:4851–59 [Google Scholar]
39. Goldstein DJ, Finbow ME, Andresson T, McLean P, Smith K. 39.  et al. 1991. Bovine papillomavirus E5 oncoprotein binds to the 16K component of vacuolar H⁺-ATPases. Nature 352:347–49 [Google Scholar]
40. Goldstein DJ, Li W, Wang L-M, Heidaran MA, Aaronson SA. 40.  et al. 1994. The bovine papillomavirus type 1 E5 transforming protein specifically binds and activates the β-type receptor for platelet-derived growth factor but not other tyrosine kinase-containing receptors to induce cellular transformation. J. Virol. 68:4432–41 [Google Scholar]
41. Habermann A, Krijnse-Locker J, Oberwinkler H, Eckhardt M, Homann S. 41.  et al. 2010. CD317/tetherin is enriched in the HIV-1 envelope and downregulated from the plasma membrane upon virus infection. J. Virol. 84:4646–58 [Google Scholar]
42. Hay AJ, Wolstenholme AJ, Skehel JJ, Smith MH. 42.  1985. The molecular basis of the specific anti-influenza action of amantadine. EMBO J. 4:3021–24 [Google Scholar]
43. He B, Leser GP, Paterson RG, Lamb RA. 43.  1998. The paramyxovirus SV5 small hydrophobic (SH) protein is not essential for virus growth in tissue culture cells. Virology 250:30–40 [Google Scholar]
44. He B, Lin GY, Durbin JE, Durbin RK, Lamb RA. 44.  2001. The SH integral membrane protein of the paramyxovirus simian virus 5 is required to block apoptosis in MDBK cells. J. Virol. 75:4068–79 [Google Scholar]
45. Helenius A. 45.  1992. Unpacking the incoming influenza virus. Cell 69:577–78 [Google Scholar]
46. Hemm MR, Paul BJ, Schneider TD, Storz G, Rudd KE. 46.  2008. Small membrane proteins found by comparative genomics and ribosome binding site models. Mol. Microbiol. 70:1487–501 [Google Scholar]
47. Hobbs EC, Fontaine F, Yin X, Storz G. 47.  2011. An expanding universe of small proteins. Curr. Opin. Microbiol. 14:167–73 [Google Scholar]
48. Holsinger LJ, Lamb RA. 48.  1991. Influenza virus M2 integral membrane protein is a homotetramer stabilized by formation of disulfide bonds. Virology 183:32–43 [Google Scholar]
49. Horwitz BH, Burkhardt AL, Schlegel R, DiMaio D. 49.  1988. 44-amino-acid E5 transforming protein of bovine papillomavirus requires a hydrophobic core and specific carboxyl-terminal amino acids. Mol. Cell. Biol. 8:4071–78 [Google Scholar]
50. Hu F, Luo W, Cady SD, Hong M. 50.  2011. Conformational plasticity of the influenza A M2 transmembrane helix in lipid bilayers under varying pH, drug binding, and membrane thickness. Biochim. Biophys. Acta 1808:415–23 [Google Scholar]
51. Hu F, Luo W, Hong M. 51.  2010. Mechanisms of proton conduction and gating in influenza M2 proton channels from solid-state NMR. Science 330:505–8 [Google Scholar]
52. Iwabu Y, Fujita H, Kinomoto M, Kaneko K, Ishizaka Y. 52.  et al. 2009. HIV-1 accessory protein Vpu internalizes cell-surface BST-2/tetherin through transmembrane interactions leading to lysosomes. J. Biol. Chem. 284:35060–72 [Google Scholar]
53. Jing X, Ma C, Ohigashi Y, Oliveira FA, Jardetzky TS. 53.  et al. 2008. Functional studies indicate amantadine binds to the pore of the influenza A virus M2 proton-selective ion channel. Proc. Natl. Acad. Sci. USA 105:10967–72 [Google Scholar]
54. King G, Oates J, Patel D, van den Berg HA, Dixon AM. 54.  2011. Towards a structural understanding of the smallest known oncoprotein: investigation of the bovine papillomavirus E5 protein using solution-state NMR. Biochim. Biophys. Acta 1808:1493–501 [Google Scholar]
55. Klein O, Kegler-Ebo D, Su J, Smith S, DiMaio D. 55.  1999. The bovine papillomavirus E5 protein requires a juxtamembrane negative charge for activation of the platelet-derived growth factor β receptor and transformation of C127 cells. J. Virol. 73:3264–72 [Google Scholar]
56. Klein O, Polack GW, Surti T, Kegler-Ebo D, Smith SO, DiMaio D. 56.  1998. Role of glutamine 17 of the bovine papillomavirus E5 protein in platelet-derived growth factor β receptor activation and cell transformation. J. Virol. 72:8921–32 [Google Scholar]
57. Klimkait T, Strebel K, Hoggan MD, Martin MA, Orenstein JM. 57.  1990. The human immunodeficiency virus type 1-specific protein vpu is required for efficient virus maturation and release. J. Virol. 64:621–29 [Google Scholar]
58. Kochendoerfer GG, Salom D, Lear JD, Wilk-Orescan R, Kent SB, DeGrado WF. 58.  1999. Total chemical synthesis of the integral membrane protein influenza A virus M2: role of its C-terminal domain in tetramer assembly. Biochemistry 38:11905–13 [Google Scholar]
59. Lai CC, Henningson C, DiMaio D. 59.  1998. Bovine papillomavirus E5 protein induces oligomerization and trans-phosphorylation of the platelet-derived growth factor β receptor. Proc. Natl. Acad. Sci. USA 95:15241–46 [Google Scholar]
60. Leechanachai P, Banks L, Moreau F, Matlashewski G. 60.  1992. The E5 gene from human papillomavirus type 16 is an oncogene which enhances growth factor-mediated signal transduction to the nucleus. Oncogene 7:19–25 [Google Scholar]
61. Lehnert U, Xia Y, Royce TE, Goh CS, Liu Y. 61.  et al. 2004. Computational analysis of membrane proteins: genomic occurrence, structure prediction and helix interactions. Q. Rev. Biophys. 37:121–46 [Google Scholar]
62. Leptak C, Ramon Y, Cajal S, Kulke R, Horwitz BH. 62.  et al. 1991. Tumorigenic transformation of murine keratinocytes by the E5 genes of bovine papillomavirus type 1 and human papillomavirus type 16. J. Virol. 65:7078–83 [Google Scholar]
63. Li C, Qin H, Gao FP, Cross TA. 63.  2007. Solid-state NMR characterization of conformational plasticity within the transmembrane domain of the influenza A M2 proton channel. Biochim. Biophys. Acta 1768:3162–70 [Google Scholar]
64. Li Z, Xu J, Patel J, Fuentes S, Lin Y. 64.  et al. 2011. Function of the small hydrophobic protein of J paramyxovirus. J. Virol. 85:32–42 [Google Scholar]
65. Lin Y, Bright AC, Rothermel TA, He B. 65.  2003. Induction of apoptosis by paramyxovirus simian virus 5 lacking a small hydrophobic gene. J. Virol. 77:3371–83 [Google Scholar]
66. Ma C, Polishchuk AL, Ohigashi Y, Stouffer AL, Schon A. 66.  et al. 2009. Identification of the functional core of the influenza A virus A/M2 proton-selective ion channel. Proc. Natl. Acad. Sci. USA 106:12283–88 [Google Scholar]
67. Mackenzie KR. 67.  2006. Folding and stability of α-helical integral membrane proteins. Chem. Rev. 106:1931–77 [Google Scholar]
68. Magadán JG, Bonifacino JS. 68.  2012. Transmembrane domain determinants of CD4 downregulation by HIV-1 Vpu. J. Virol. 86:757–72 [Google Scholar]
69. Magadán JG, Pérez-Victoria FJ, Sougrat R, Ye Y, Strebel K, Bonifacino JS. 69.  2010. Multilayered mechanism of CD4 downregulation by HIV-1 Vpu involving distinct ER retention and ERAD targeting steps. PLoS Pathog. 6:e1000869 [Google Scholar]
70. Margottin F, Bour SP, Durand H, Selig L, Benichou S. 70.  et al. 1998. A novel human WD protein, h-βTrCp, that interacts with HIV-1 Vpu connects CD4 to the ER degradation pathway through an F-box motif. Mol. Cell 1:565–74HIV Vpu targets CD4 for degradation by targeting it to the SCF ubiquitin ligase complex. [Google Scholar]
71. Maruri-Avidal L, Domi A, Weisberg AS, Moss B. 71.  2011. Participation of vaccinia virus L2 protein in the formation of crescent membranes and immature virions. J. Virol. 85:2504–11 [Google Scholar]
72. Maruri-Avidal L, Weisberg AS, Moss B. 72.  2013. Direct formation of vaccinia virus membranes from the endoplasmic reticulum in the absence of the newly characterized L2-interacting protein A30.5. J. Virol. 87:12313–26 [Google Scholar]
73. Mattoon D, Gupta K, Doyon J, Loll PJ, DiMaio D. 73.  2001. Identification of the transmembrane dimer interface of the bovine papillomavirus E5 protein. Oncogene 20:3824–34 [Google Scholar]
74. McCown MF, Pekosz A. 74.  2006. Distinct domains of the influenza A virus M2 protein cytoplasmic tail mediate binding to the M1 protein and facilitate infectious virus production. J. Virol. 80:8178–89 [Google Scholar]
75. McNatt MW, Zang T, Hatziioannou T, Bartlett M, Fofana IB. 75.  et al. 2009. Species-specific activity of HIV-1 Vpu and positive selection of tetherin transmembrane domain variants. PLoS Pathog. 5:e1000300 [Google Scholar]
76. Mercer J, Traktman P. 76.  2003. Investigation of structural and functional motifs within the vaccinia virus A14 phosphoprotein, an essential component of the virion membrane. J. Virol. 77:8857–71 [Google Scholar]
77. Meyer AN, Xu Y-F, Webster MK, Smith AS, Donoghue DJ. 77.  1994. Cellular transformation by a transmembrane peptide: structural requirements for the bovine papillomavirus E5 oncoprotein. Proc. Natl. Acad. Sci. USA 91:4634–38 [Google Scholar]
78. Nappi VM, Petti LM. 78.  2002. Multiple transmembrane amino acid requirements suggest a highly specific interaction between the bovine papillomavirus E5 oncoprotein and the platelet-derived growth factor β receptor. J. Virol. 76:7976–86 [Google Scholar]
79. Nappi VM, Schaefer JA, Petti LM. 79.  2002. Molecular examination of the transmembrane requirements of the platelet-derived growth factor β receptor for a productive interaction with the bovine papillomavirus E5 oncoprotein. J. Biol. Chem. 277:47149–59 [Google Scholar]
80. Neil SJ, Zang T, Bieniasz PD. 80.  2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425–30HIV Vpu antagonizes the ability of tetherin to inhibit HIV release. [Google Scholar]
81. Nichols RJ, Stanitsa E, Unger B, Traktman P. 81.  2008. The vaccinia virus gene I2L encodes a membrane protein with an essential role in virion entry. J. Virol. 82:10247–61 [Google Scholar]
82. Nieva JL, Madan V, Carrasco L. 82.  2012. Viroporins: structure and biological functions. Nat. Rev. Microbiol. 10:563–74An overview of viroporins, an important class of viral miniproteins. [Google Scholar]
83. Nilson LA, DiMaio D. 83.  1993. Platelet-derived growth factor receptor can mediate tumorigenic transformation by the bovine papillomavirus E5 protein. Mol. Cell. Biol. 13:4137–45 [Google Scholar]
84. Opatowsky Y, Lax I, Tomé F, Bleichert F, Unger VM, Schlessinger J. 84.  2014. Structure, domain organization, and different conformational states of stem cell factor-induced intact KIT dimers. Proc. Natl. Acad. Sci. USA 111:1772–77 [Google Scholar]
85. Park SH, Mrse AA, Nevzorov AA, Mesleh MF, Oblatt-Montal M. 85.  et al. 2003. Three-dimensional structure of the channel-forming trans-membrane domain of virus protein “u” (Vpu) from HIV-1. J. Mol. Biol. 333:409–24 [Google Scholar]
86. Perez-Caballero D, Zang T, Ebrahimi A, McNatt MW, Gregory DA. 86.  et al. 2009. Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 139:499–511 [Google Scholar]
87. Petti L, DiMaio D. 87.  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 89:6736–40 [Google Scholar]
88. Petti L, DiMaio D. 88.  1994. Specific interaction between the bovine papillomavirus E5 transforming protein and the β receptor for platelet-derived growth factor in stably transformed and acutely transfected cells. J. Virol. 68:3582–92 [Google Scholar]
89. Petti L, Nilson LA, DiMaio D. 89.  1991. Activation of the platelet-derived growth factor receptor by the bovine papillomavirus E5 transforming protein. EMBO J. 10:845–55The 44-amino-acid bovine papillomavirus E5 oncoprotein activates the PDGF β receptor. [Google Scholar]
90. Petti LM, Reddy V, Smith SO, DiMaio D. 90.  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. 71:7318–27 [Google Scholar]
91. Petti LM, Talbert-Slagle K, Hochstrasser ML, DiMaio D. 91.  2013. A single amino acid substitution converts a transmembrane protein activator of the platelet-derived growth factor β receptor into an inhibitor. J. Biol. Chem. 288:27273–86 [Google Scholar]
92. Pim D, Collins M, Banks L. 92.  1992. Human papillomavirus type 16 E5 gene stimulates the transforming activity of the epidermal growth factor receptor. Oncogene 7:27–32 [Google Scholar]
93. Pinto LH, Dieckmann GR, Gandhi CS, Papworth CG, Braman J. 93.  et al. 1997. A functionally defined model for the M2 proton channel of influenza A virus suggests a mechanism for its ion selectivity. Proc. Natl. Acad. Sci. USA 94:11301–6 [Google Scholar]
94. Pinto LH, Holsinger LJ, Lamb RA. 94.  1992. Influenza virus M2 protein has ion channel activity. Cell 69:517–28 [Google Scholar]
95. Pinto LH, Lamb RA. 95.  2006. The M2 proton channels of influenza A and B viruses. J. Biol. Chem. 281:8997–9000 [Google Scholar]
96. Pinto LH, Lamb RA. 96.  2007. Controlling influenza virus replication by inhibiting its proton channel. Mol. Biosyst. 3:18–23 [Google Scholar]
97. Popot J-L, Engelman DM. 97.  2000. Helical membrane protein folding, stability, and evolution. Annu. Rev. Biochem. 69:881–922 [Google Scholar]
98. Ptacek JB, Edwards APB, Freeman-Cook LL, DiMaio D. 98.  2007. Packing contacts can mediate highly specific interactions between artificial transmembrane proteins and the PDGFβ receptor. Proc. Natl. Acad. Sci. USA 104:11945–50 [Google Scholar]
99. Raghava S, Giorda KM, Romano FB, Heuck AP, Hebert DN. 99.  2011. The SV40 late protein VP4 is a viroporin that forms pores to disrupt membranes for viral release. PLoS Pathog. 7:e1002116 [Google Scholar]
100. Roberts KL, Leser GP, Ma C, Lamb RA. 100.  2013. The amphipathic helix of influenza A virus M2 protein is required for filamentous bud formation and scission of filamentous and spherical particles. J. Virol. 87:9973–82 [Google Scholar]
101. Rodríguez JR, Risco C, Carrascosa JL, Esteban M, Rodríguez D. 101.  1998. Vaccinia virus 15-kilodalton (A14L) protein is essential for assembly and attachment of viral crescents to virosomes. J. Virol. 72:1287–96 [Google Scholar]
102. Rossman JS, Jing X, Leser GP, Lamb RA. 102.  2010. Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 142:902–13The influenza A virus M2 protein inserts into cell membranes to facilitate virus release. [Google Scholar]
103. Satheshkumar PS, Chavre J, Moss B. 103.  2013. Role of the vaccinia virus O3 protein in cell entry can be fulfilled by its Sequence flexible transmembrane domain. Virology 444:148–57 [Google Scholar]
104. Satheshkumar PS, Moss B. 104.  2009. Characterization of a newly identified 35-amino-acid component of the vaccinia virus entry/fusion complex conserved in all chordopoxviruses. J. Virol. 83:12822–32The 35-amino-acid O3L virion protein is required for poxvirus entry. [Google Scholar]
105. Satheshkumar PS, Moss B. 105.  2012. Sequence-divergent chordopoxvirus homologs of the O3 protein maintain functional interactions with components of the vaccinia virus entry-fusion complex. J. Virol. 86:1696–705 [Google Scholar]
106. Scheideman EH, Marlatt SA, Xie Y, Hu Y, Sutton RE, DiMaio D. 106.  2012. Transmembrane protein aptamers that inhibit CCR5 expression and HIV coreceptor function. J. Virol. 86:10281–92 [Google Scholar]
107. Schlegel R, Wade-Glass M, Rabson MS, Yang YC. 107.  1986. The E5 transforming gene of bovine papillomavirus encodes a small, hydrophobic polypeptide. Science 233:464–67 [Google Scholar]
108. Schneider D. 108.  2004. Rendezvous in a membrane: close packing, hydrogen bonding, and the formation of transmembrane helix oligomers. FEBS Lett. 577:5–8 [Google Scholar]
109. Schneider D, Finger C, Prodohl A, Volkmer T. 109.  2007. From interactions of single transmembrane helices to folding of α-helical membrane proteins: analyzing transmembrane helix-helix interactions in bacteria. Curr. Protein Pept. Sci. 8:45–61 [Google Scholar]
110. Schnell JR, Chou JJ. 110.  2008. Structure and mechanism of the M2 proton channel of influenza A virus. Nature 451:591–95 [Google Scholar]
111. Schubert U, Anton LC, Bacik I, Cox JH, Bour S. 111.  et al. 1998. CD4 glycoprotein degradation induced by human immunodeficiency virus type 1 Vpu protein requires the function of proteasomes and the ubiquitin-conjugating pathway. J. Virol. 72:2280–88 [Google Scholar]
112. Schubert U, Ferrer-Montiel AV, Oblatt-Montal M, Henklein P, Strebel K, Montal M. 112.  1996. Identification of an ion channel activity of the Vpu transmembrane domain and its involvement in the regulation of virus release from HIV-1-infected cells. FEBS Lett. 398:12–18 [Google Scholar]
113. Shim AH, Liu H, Focia PJ, Chen X, Lin PC, He X. 113.  2010. Structures of a platelet-derived growth factor/propeptide complex and a platelet-derived growth factor/receptor complex. Proc. Natl. Acad. Sci. USA 107:11307–12 [Google Scholar]
114. Skasko M, Wang Y, Tian Y, Tokarev A, Munguia J. 114.  et al. 2012. HIV-1 Vpu protein antagonizes innate restriction factor BST-2 via lipid-embedded helix-helix interactions. J. Biol. Chem. 287:58–67 [Google Scholar]
115. Sood CL, Ward JM, Moss B. 115.  2008. Vaccinia virus encodes I5, a small hydrophobic virion membrane protein that enhances replication and virulence in mice. J. Virol. 82:10071–78 [Google Scholar]
116. Staebler A, Pierce JH, Brazinski S, Heidaran MA, Li W. 116.  et al. 1995. Mutational analysis of the β-type platelet-derived growth factor receptor defines the site of interaction with the bovine papillomavirus type 1 E5 transforming protein. J. Virol. 69:6507–17 [Google Scholar]
117. Stern-Ginossar N, Weisburd B, Michalski A, Le VT, Hein MY. 117.  et al. 2012. Decoding human cytomegalovirus. Science 338:1088–93 [Google Scholar]
118. Stouffer AL, Ma C, Cristian L, Ohigashi Y, Lamb RA. 118.  et al. 2008. The interplay of functional tuning, drug resistance, and thermodynamic stability in the evolution of the M2 proton channel from the influenza A virus. Structure 16:1067–76 [Google Scholar]
119. Straight SW, Herman B, McCance DJ. 119.  1995. The E5 oncoprotein of human papillomavirus type 16 inhibits the acidification of endosomes in human keratinocytes. J. Virol. 69:3185–92 [Google Scholar]
120. Straight SW, Hinkle PM, Jewers RJ, McCance DJ. 120.  1993. The E5 oncoprotein of human papillomavirus type 16 transforms fibroblasts and effects the downregulation of the epidermal growth factor receptor in keratinocytes. J. Virol. 67:4521–32 [Google Scholar]
121. Strebel K, Klimkait T, Martin MA. 121.  1988. A novel gene of HIV-1, vpu, and its 16-kilodalton product. Science 241:1221–23 [Google Scholar]
122. Sugrue RJ, Hay AJ. 122.  1991. Structural characteristics of the M2 protein of influenza A viruses: evidence that it forms a tetrameric channel. Virology 180:617–24 [Google Scholar]
123. Surti T, Klein O, Aschheim K, DiMaio D, Smith SO. 123.  1998. Structural models of the bovine papillomavirus E5 protein. Proteins 33:601–12 [Google Scholar]
124. Suzuki H, Saito R, Masuda H, Oshitani H, Sato M, Sato I. 124.  2003. Emergence of amantadine-resistant influenza A viruses: epidemiological study. J. Infect. Chemother. 9:195–200 [Google Scholar]
125. Suzuki T, Orba Y, Okada Y, Sunden Y, Kimura T. 125.  et al. 2010. The human polyoma JC virus agnoprotein acts as a viroporin. PLoS Pathog. 6:e1000801 [Google Scholar]
126. Takeuchi K, Tanabayashi K, Hishiyama M, Yamada A. 126.  1996. The mumps virus SH protein is a membrane protein and not essential for virus growth. Virology 225:156–62 [Google Scholar]
127. Talbert-Slagle K, Marlatt S, Barrera FN, Khurana E, Oates J. 127.  et al. 2009. Artificial transmembrane oncoproteins smaller than the bovine papillomavirus E5 protein redefine the sequence requirements for activation of the platelet-derived growth factor β receptor. J. Virol. 83:9773–85 [Google Scholar]
128. Terwilliger EF, Cohen EA, Lu YC, Sodroski JG, Haseltine WA. 128.  1989. Functional role of human immunodeficiency virus type 1 vpu. Proc. Natl. Acad. Sci. USA 86:5163–67 [Google Scholar]
129. Traktman P, Liu K, DeMasi J, Rollins R, Jesty S, Unger B. 129.  2000. Elucidating the essential role of the A14 phosphoprotein in vaccinia virus morphogenesis: construction and characterization of a tetracycline-inducible recombinant. J. Virol. 74:3682–95 [Google Scholar]
130. Unger B, Mercer J, Boyle KA, Traktman P. 130.  2013. Biogenesis of the vaccinia virus membrane: genetic and ultrastructural analysis of the contributions of the A14 and A17 proteins. J. Virol. 87:1083–97 [Google Scholar]
131. Unger B, Nichols RJ, Stanitsa ES, Traktman P. 131.  2008. Functional characterization of the vaccinia virus I5 protein. Virol. J. 5:148 [Google Scholar]
132. Unger B, Traktman P. 132.  2004. Vaccinia virus morphogenesis: A13 phosphoprotein is required for assembly of mature virions. J. Virol. 78:8885–901 [Google Scholar]
133. van Damme N, Goff D, Katsura C, Jorgenson RL, Mitchell R. 133.  et al. 2008. The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 3:245–52 [Google Scholar]
134. Venkataraman P, Lamb RA, Pinto LH. 134.  2005. Chemical rescue of histidine selectivity filter mutants of the M2 ion channel of influenza A virus. J. Biol. Chem. 280:21463–72 [Google Scholar]
135. Votteler J, Sundquist WI. 135.  2013. Virus budding and the ESCRT pathway. Cell Host Microbe 14:232–41 [Google Scholar]
136. Wang C, Lamb RA, Pinto LH. 136.  1995. Activation of the M2 ion channel of influenza virus: a role for the transmembrane domain histidine residue. Biophys. J. 69:1363–71 [Google Scholar]
137. Wang J, Ma C, Balannik V, Pinto LH, Lamb RA, Degrado WF. 137.  2011. Exploring the requirements for the hydrophobic scaffold and polar amine in inhibitors of M2 from influenza A virus. ACS Med. Chem. Lett. 2:307–12 [Google Scholar]
138. Wang J, Ma C, Fiorin G, Carnevale V, Wang T. 138.  et al. 2011. Molecular dynamics simulation directed rational design of inhibitors targeting drug-resistant mutants of influenza A virus M2. J. Am. Chem. Soc. 133:12834–41 [Google Scholar]
139. Wang J, Pielak RM, McClintock MA, Chou JJ. 139.  2009. Solution structure and functional analysis of the influenza B proton channel. Nat. Struct. Mol. Biol. 16:1267–71 [Google Scholar]
140. Wang J, Qiu JX, Soto C, DeGrado WF. 140.  2011. Structural and dynamic mechanisms for the function and inhibition of the M2 proton channel from influenza A virus. Curr. Opin. Struct. Biol. 21:68–80 [Google Scholar]
141. Watanabe S, Watanabe T, Kawaoka Y. 141.  2009. Influenza A virus lacking M2 protein as a live attenuated vaccine. J. Virol. 83:5947–50 [Google Scholar]
142. Watanabe T, Watanabe S, Ito H, Kida H, Kawaoka Y. 142.  2001. Influenza A virus can undergo multiple cycles of replication without M2 ion channel activity. J. Virol. 75:5656–62 [Google Scholar]
143. Watanabe T, Watanabe S, Kim JH, Hatta M, Kawaoka Y. 143.  2008. Novel approach to the development of effective H5N1 influenza A virus vaccines: use of M2 cytoplasmic tail mutants. J. Virol. 82:2486–92 [Google Scholar]
144. Wetherill LF, Holmes KK, Verow M, Muller M, Howell G. 144.  et al. 2012. High-risk human papillomavirus E5 oncoprotein displays channel-forming activity sensitive to small-molecule inhibitors. J. Virol. 86:5341–51 [Google Scholar]
145. Wilson RL, Fuentes SM, Wang P, Taddeo EC, Klatt A. 145.  et al. 2006. Function of small hydrophobic proteins of paramyxovirus. J. Virol. 80:1700–9The simian virus 5 SH protein can be replaced by the divergent mumps virus SH protein. [Google Scholar]
146. Windisch D, Hoffmann S, Afonin S, Vollmer S, Benamira S. 146.  et al. 2010. Structural role of the conserved cysteines in the dimerization of the viral transmembrane oncoprotein E5. Biophys. J. 99:1764–72 [Google Scholar]
147. Yang X, Tschaplinski TJ, Hurst GB, Jawdy S, Abraham PE. 147.  et al. 2011. Discovery and annotation of small proteins using genomics, proteomics, and computational approaches. Genome Res 21:634–41 [Google Scholar]
148. Yuzawa S, Opatowsky Y, Zhang Z, Mandiyan V, Lax I, Schlessinger J. 148.  2007. Structural basis for activation of the receptor tyrosine kinase KIT by stem cell factor. Cell 130:323–34 [Google Scholar]