Viral channel proteins in intracellular protein-protein communication: Vpu of HIV-1, E5 of HPV16 and p7 of HCV

Biochimica et Biophysica Acta - Biomembranes

Volumn 1838, Issue 4, 2014, Pages 1113-1121

  Fischer, Wolfgang B ^a   Li, Li Hua ^a   Mahato, Dhani Ram ^a   Wang, Yi Ting ^a   Chen, Chin Pei ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

E5 of HPV16; p7 of HCV; Viral channel proteins; Viral host protein protein interaction; Vpu of HIV 1

Indexed keywords

16 KDA PROTEIN; CD4 ANTIGEN; CD74 ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 4; HLA ANTIGEN CLASS 1; MEMBRANE PROTEIN; MICROORGANISM PROTEIN; PROTEIN BST 2; PROTEIN E5; PROTEIN NTB A; PROTEIN P7; TETRATRICOPEPTIDE REPEAT PROTEIN; TWIK RELATED ACID SENSITIVE POTASSIUM CHANNEL; UNCLASSIFIED DRUG; VIRUS PROTEIN; VPU PROTEIN;

ENDOPLASMIC RETICULUM; GAP JUNCTION; HEPATITIS C VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN PAPILLOMAVIRUS TYPE 16; KOILOCYTOSIS; MEMBRANE DAMAGE; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REVIEW;

HEPATITIS C VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN PAPILLOMAVIRUS TYPE 16;

E5 OF HPV16; P7 OF HCV; VIRAL CHANNEL PROTEINS; VIRAL-HOST PROTEIN-PROTEIN INTERACTION; VPU OF HIV-1;

ANTIGENS, CD; ANTIGENS, CD4; GPI-LINKED PROTEINS; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; MODELS, MOLECULAR; NERVE TISSUE PROTEINS; ONCOGENE PROTEINS, VIRAL; POTASSIUM CHANNELS, TANDEM PORE DOMAIN; RECEPTORS, CELL SURFACE; VIRAL PROTEINS; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EID: 84895553393     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.08.017     Document Type: Review

References (122)

1. W.B. Fischer, and M.S.P. Sansom Viral ion channels: structure and function Biochim. Biophys. Acta 1561 2002 27 45
2. W.B. Fischer, Y.-T. Wang, C. Schindler, and C.-P. Chen Mechanism of function of viral channel proteins and implications for drug development Int. Rev. Cell Mol. Biol. 294 2012 259 321
3. M.E. Gonzales, and L. Carrasco Viroporins FEBS Lett. 552 2003 28 34
4. J.L. Nieva, V. Madan, and L. Carrasco Viroporins: structure and biological functions Nat. Rev. Microbiol. 10 2012 563 574
5. L. Carrasco Modification of membrane permeability by animal viruses Adv. Virus Res. 45 1995 61 112
6. K. Wang, S. Xie, and B. Sun Viral proteins function as ion channels Biochim. Biophys. Acta 1808 2010 510 515
7. U. Schubert, A.V. Ferrer-Montiel, M. Oblatt-Montal, P. Henklein, K. Strebel, and M. Montal 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 1996 12 18
8. M.J. Coady, N.G. Daniel, E. Tiganos, B. Allain, J. Friborg, J.-Y. Lapointe, and E.A. Cohen Effects of Vpu expression on Xenopus oocyte membrane conductance Virology 244 1998 39 49
9. R.L. Willey, F. Maldarelli, M.A. Martin, and K. Strebel Human immunodeficiency virus type 1 Vpu protein induces rapid degradation of CD4 J. Virol. 66 1992 7193 7200
10. U. Schubert, and K. Strebel Differential activities of the human immunodeficiency virus type 1-encoded Vpu protein are regulated by phosphorylation and occur in different cellular compartments J. Virol. 68 1994 2260 2272
11. L.F. Wetherill, K.K. Holmes, M. Verow, M. Müller, G. Howell, M. Harris, C. Fishwick, N. Stonehouse, R. Foster, G.E. Blair, S. Griffin, and A. Macdonald High-risk human papillomavirus E5 oncoprotein displays channel-forming activity sensitive to small-molecule inhibitors J. Virol. 86 2012 5341 5351
12. K. Strebel, T. Klimkait, and M.A. Martin Novel gene of HIV-1, vpu, and its 16-kilodalton product Science 241 1988 1221 1223
13. E.A. Cohen, E.F. Terwilliger, J.G. Sodroski, and W.A. Haseltine Identification of a protein encoded by the vpu gene of HIV-1 Nature 334 1988 532 534
14. G.D. Ewart, T. Sutherland, P.W. Gage, and G.B. Cox The Vpu protein of human immunodeficiency virus type 1 forms cation-selective ion channels J. Virol. 70 1996 7108 7115
15. T. Mehnert, Y.H. Lam, P.J. Judge, A. Routh, D. Fischer, A. Watts, and W.B. Fischer Towards a mechanism of function of the viral ion channel Vpu from HIV-1 J. Biomol. Struct. Dyn. 24 2007 589 596
16. T. Mehnert, A. Routh, P.J. Judge, Y.H. Lam, D. Fischer, A. Watts, and W.B. Fischer Biophysical characterisation of Vpu from HIV-1 suggests a channel-pore dualism Proteins 70 2008 1488 1497
17. M.E. Gonzales, and L. Carrasco The human immunodeficiency virus type 1 Vpu protein enhances membrane permeability Biochemistry 37 1998 13710 13719
18. S. Bolduan, J. Votteler, V. Lodermeyer, T. Greiner, H. Koppensteiner, M. Schindler, G. Thiel, and U. Schubert Ion channel activity of HIV-1 Vpu is dispensable for counteraction of CD317 Virology 416 2011 75 85
19. A.L. Grice, I.D. Kerr, and M.S.P. Sansom Ion channels formed by HIV-1 Vpu: a modelling and simulation study FEBS Lett. 405 1997 299 304
20. G. Patargias, H. Martay, and W.B. Fischer Reconstructing potentials of mean force from short steered molecular dynamics simulations of Vpu from HIV-1 J. Biomol. Struct. Dyn. 26 2009 1 12
21. F.S. Cordes, A.D. Tustian, M.S. Sansom, A. Watts, and W.B. Fischer Bundles consisting of extended transmembrane segments of Vpu from HIV-1: computer simulations and conductance measurements Biochemistry 41 2002 7359 7365
22. C.F. Lopez, M. Montal, J.K. Blasie, M.L. Klein, and P.B. Moore Molecular dynamics investigation of membrane-bound bundles of the channel-forming transmembrane domain of viral protein U from the human immunodeficiency virus HIV-1 Biophys. J. 83 2002 1259 1267
23. L.-H. Li, H.-J. Hsu, and W.B. Fischer Assembling viral channel forming proteins: Vpu from HIV-1 Biopolymers 99 2013 517 529
24. S. Bour, U. Schubert, and K. Strebel The human immunodeficiency virus type 1 Vpu protein specifically binds to the cytoplasmic domain of CD4: implications for the mechanism of degradation J. Virol. 69 1995 1510 1520
25. F.P. Blanchet, J.P. Mitchell, and V. Piguet TrCP dependency of HIV-1 Vpu-induced downregulation of CD4 and BST-2/tetherin Curr. HIV Res. 10 2012 307 314
26. F. Margottin, S.P. Bour, H. Durand, L. Selig, S. Benichou, V. Richard, D.D. Thomas, K. Strebel, and R. Benarous 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 1998 565 574
27. U. Schubert, S. Bour, A.V. Ferrer-Montiel, M. Montal, F. Maldarelli, and K. Strebel The two biological activities of human immunodeficiency virus type 1 Vpu protein involve two separable structural domains J. Virol. 70 1996 809 819
28. M.-Y. Chen, F. Maldarelli, M.A. Martin, and K. Strebel Human immunodeficiency virus type 1 Vpu protein induces degradation of CD4 in vitro: the cytoplasmic domain contributes to Vpu sensitivity J. Virol. 67 1993 3877 3884
29. J. Shin, R.L. Dunbrack, S. Lee, and J.L. Strominger Phosphorylation- dependent down-modulation of CD4 requires a specific structure within the cytoplasmic domain of CD4 J. Biol. Chem. 266 1991 10658 10665
30. M. Wittlich, P. Thiagarajan, B.W. Koenig, R. Hartmann, and D. Willbold NMR structure of the transmembrane and cytoplasmic domains of human CD4 in micelles Biochim. Biophys. Acta 1798 2010 122 127
31. E. Tiganos, X.-J. Yao, J. Friborg, N. Daniel, and E.A. Cohen Putative a-helical structures in the human immunodeficiency virus type 1 Vpu protein and CD4 are involved in binding and degradation of the CD4 molecule J. Virol. 71 1997 4452 4460
32. 1H NMR-spectroscopy Int. J. Pept. Protein Res. 45 1995 35 43
33. T. Federau, U. Schubert, J. Floßdorf, P. Henklein, D. Schomburg, and V. Wray Solution structure of the cytoplasmic domain of the human immunodeficiency virus type 1 encoded virus protein U (Vpu) Int. J. Pept. Protein Res. 47 1996 297 310
34. D. Willbold, S. Hoffmann, and P. Rösch Secondary structure and tertiary fold of the human immunodeficiency virus protein U (Vpu) cytoplasmatic domain in solution Eur. J. Biochem. 245 1997 581 588
35. 56 Int. J. Biol. Macromol. 30 2002 23 40
36. F.M. Marassi, C. Ma, H. Gratkowski, S.K. Straus, K. Strebel, M. Oblatt-Montal, M. Montal, and S.J. Opella Correlation of the structural and functional domains in the membrane protein Vpu from HIV-1 Proc. Natl. Acad. Sci. U. S. A. 96 1999 14336 14341
37. P. Henklein, R. Kinder, U. Schubert, and B. Bechinger Membrane interactions and alignment of structures within the HIV-1 Vpu cytoplasmic domain: effect of phosphorylation of serines 52 and 56 FEBS Lett. 482 2000 220 224
38. K. Hsu, J. Seharaseyon, P. Dong, S. Bour, and E. Marbán Mutual functional destruction of HIV-1 Vpu and host TASK-1 channel Mol. Cell 14 2004 259 267
39. K. Hsu, J. Han, K. Shinlapawittayatorn, I. Deschenes, and E. Marbán Membrane potential depolarization as a triggering mechanism for Vpu-mediated HIV-1 release Biophys. J. 99 2010 1718 1725
40. L. Herrero, N. Monroy, and M.E. Gonzáles HIV-1 Vpu protein mediates the transport of potassium in Saccharomyces cerevisiae Biochemistry 52 2013 171 177
41. N. van Damme, D. Goff, C. Katsura, R.L. Jorgensen, R. Mitchell, M.C. Johnson, E.B. Stephens, and J. Guatelli 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 2008 1 8
42. S.J.D. Neil, T. Zang, and P.D. Bieniasz Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu Nature 451 2008 425 431
43. D.T. Evans, R. Serra-Moreno, R.K. Singh, and J. Guatelli BST-2/tetherin: a new component of the innate immune response to enveloped viruses Trends Microbiol. 18 2010 388 396
44. M. Dubé, B.B. Roy, P. Guiot-Guillain, J. Binette, J. Mercier, A. Chiasson, and É.A. Cohen Antagonism of tetherin restriction of HIV-1 release by Vpu involves binding and sequestration of the restriction factor in a perinuclear compartment PLoS Pathog. 6 2010 e1000856
45. M.W. McNatt, T. Zang, and P.D. Bieniasz Vpu binds directly to tetherin and displaces it from nascent virions PLoS Pathog. 9 2013 e1003299
46. S. Kupzig, V. Korolchuk, R. Rollason, A. Sugden, A. Wilde, and G. Banting Bst-2/HM1.24 is a raft-associated apical membrane protein with an unusual topology Traffic 4 2003 694 709
47. K. Miyakawa, T. Sawasaki, S. Matsunaga, A. Tokarev, G. Quinn, H. Kimura, M. Nomaguchi, A. Adachi, N. Yamamoto, J. Guatelli, and A. Ryo Interferon-induced SCYL2 limits release of HIV-1 by triggering PP2A-mediated dephosphorylation of the viral protein Vpu Sci. Signal. 5 2012 ra73
48. M. Skasko, A. Tokarev, C.-C. Chen, W.B. Fischer, S.K. Pillai, and J. Guatelli BST-2 is rapidly down-regulated from the cell surface by the HIV-1 protein Vpu: evidence for a post-ER mechanism of Vpu-action Virology 411 2011 65 77
49. J. Zhou, Z. Zhang, Z. Mi, X. Wang, Q. Zhang, X. Li, C. Liang, and S. Cen Characterization of the interface of the bone marrow stromal cell antigen 2-Vpu protein complex via computational chemistry Biochemistry 51 2012 1288 1296
50. M. Skasko, Y. Wang, Y. Tian, A. Tokarev, J. Munguia, A. Ruiz, E.B. Stephens, S.J. Opella, and J. Guatelli HIV-1 Vpu protein antagonizes the innate restriction factor BST-2 via lipid-embedded helix-helix interactions J. Biol. Chem. 287 2012 58 67
51. M. Lv, J. Wang, T. Zuo, Y. Zhu, W. Kong, and X. Yu Polarity changes in the transmembrane domain core of HIV-1 Vpu inhibits anti-tetherin activity PLoS One 6 2011 e20890
52. B. Sowrirajan, and E. Barker The natural killer cell cytotoxic function is modulated by HIV-1 accessory proteins Viruses 3 2011 1091 1111
53. A.H. Shah, B. Sowrirajan, Z.B. Davis, J.P. Ward, E.M. Campbell, V. Planelles, and E. Barker Degranulation of natural killer cells following interaction with HIV-1-infected cells is hindered by downmodulation of NTB-A by Vpu Cell Host Microbe 8 2010 397 409
54. T. Kerkau, I. Bacik, J.R. Bennink, J.W. Yewdell, T. Hunig, A. Schimpl, and U. Schubert The human immunodeficiency virus type 1 (HIV-1) vpu protein interferes with an early step in the biosynthesis of major histocompatibility complex (MHC) class I molecules J. Exp. Med. 185 1997 1295 1305
55. A. Hussain, C. Wesley, M. Khalid, A. Chaudhry, and S. Jameel Human immunodeficiency virus type 1 Vpu protein interacts with CD74 and modulates major histocompatibility complex class II presentation J. Virol. 82 2008 893 902
56. J.W. Yewdell, and A.B. Hill Viral interference with antigen presentation Nat. Immunol. 3 2002 1019 1024
57. M.A. Callahan, M.A. Handley, Y.-H. Lee, K.J. Talbot, J.W. Harper, and A.T. Panganiban Functional interaction of human immunodeficiency virus type 1 Vpu and Gag with a novel membrane of the tetratricopeptide repeat protein family J. Virol. 72 1998 5189 5197
58. P. Evans, W. Dampier, L. Ungar, and A. Tozeren Prediction of HIV-1 virus-host protein interactions using virus and host sequence motifs BMC Med. Genomics 2 2009 27
59. L. Gissmann, M. Boshart, M. Dürst, H. Ikenberg, D. Wagner, and H. zur Hausen Presence of human papillomavirus (HPV) DNA in genital tumors J. Invest. Dermatol. 83 1984 265 288
60. H. zur Hausen Papillomaviruses in human cancers Mol. Carcinog. 1 1988 147 150
61. H. zur Hausen Papillomaviruses in anogenital cancer as a model to understand the role of viruses in human cancers Cancer Res. 49 1989 4677 4681
62. A. Schneider-Gadicke, and E. Schwarz Different human cervical carcinoma cell lines show similar transcription patterns of human papillomavirus type 18 early genes EMBO J. 5 1986 2285 2292
63. D. Smotkin, and F.O. Wettstein Transcription of human papillomavirus type 16 early genes in a cervical cancer and a cancer-derived cell line and identification of the E7 protein Proc. Natl. Acad. Sci. U. S. A. 83 1986 4680 4684
64. P. Leechanachai, L. Banks, F. Moreau, and G.M. Matlashewski The E5 gene from human papillomavirus type 16 is an oncogene which enhances growth factor-mediated signal transduction to the nucleus Oncogene 7 1992 19 25
65. C. Leptak, S. Ramon, Y. Cajal, R. Kulke, B.H. Horowitz, D.J. Riese II, G.P. Dotto, and D. DiMaio Tumorigenic transformation of murine keratinocytes by the E5 genes of bovine papillomavirus type 1 and human papillomavirus type 16 J. Virol. 65 1991 7078 7083
66. E. Schwarz, U.K. Freese, L. Gissmann, W. Mayer, B. Roggenbuck, A. Stremlau, and H. zur Hausen Structure and transcription of human papillomavirus sequences in cervical carcinoma cells Nature 314 1985 111 114
67. H. zur Hausen, and E.M. de Villiers Human papillomaviruses Annu. Rev. Microbiol. 48 1994 427 447
68. M.H. Stoler, C.R. Rhodes, A. Whitbeck, S.M. Wolinsky, L.T. Chow, and T.R. Broker Human papillomavirus type 16 and 18 gene expression in cervical neoplasias Hum. Pathol. 23 1992 117 127
69. E. Krawczyk, F.A. Suprynowicz, X. Liu, Y. Dai, D.P. Hartmann, J. Hanover, and R. Schlegel Koilocytosis. A cooperative interaction between the human papillomavirus E5 and E6 oncoproteins Am. J. Pathol. 173 2008 682 688
70. M. Conrad, V.J. Bubb, and R. Schlegel 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 1993 6170 6178
71. T.-C. Tsai, and S.-L. Chen The biochemical and biological functions of human papillomavirus type 16 E5 protein Arch. Virol. 148 2003 1445 1453
72. B. Kell, R.J. Jewers, J. Cason, F. Pakarian, J.N. Kaye, and J.M. Best Detection of E5 oncoprotein in human papillomavirus type 16-positive cervical scrapes using antibodies raised to synthetic peptides J. Gen. Virol. 75 1994 2451 2456
73. C.E. Gieswein, F.J. Sharom, and A.G. Wildeman Oligomerization of the E5 protein of human papillomavirus type 16 occurs through multiple hydrophobic regions Virology 313 2003 415 426
74. E. Krawczyk, F.A. Suprynowicz, S.R. Sudarshan, and H.B. Schlegel Membrane orientation of the human papillomavirus type 16 E5 oncoprotein J. Virol. 84 2010 1696 1703
75. C.G. Ullman, P.I. Haris, B. Kell, J. Cason, R.J. Jewers, J.M. Best, V.C. Emery, and S.J. Perkins Hypothetical structure of the membrane-associated E5 oncoprotein of human papillomavirus type 16 Biochem. Soc. Trans. 22 1994 439S
76. A. Alonso, and J. Reed Modelling of the human papillomavirus type 16 E5 protein Biochim. Biophys. Acta 1601 2002 9 18
77. WafI/SdiI/CipI gene expression in fibroblasts and keratinocytes J. Virol. 70 1996 7535 7539
78. S.-L. Chen, S.-T. Lin, T.-C. Tsai, W.-C. Hsiao, and Y.-P. Tsao ErbB4 (JM-b/CYT-1)-induced expression and phosphorylation of c-Jun is abrogated by human papillomavirus type 16 E5 protein Oncogene 26 2007 42 53
79. A. Venuti, F. Paolini, L. Nasir, A. Corteggio, S. Roperto, M.S. Campo, and G. Borzacchiello Papillomavirus E5: the smallest oncoprotein with many functions Mol. Cancer 10 2011
80. D.J. Goldstein, R. Kulke, D. Dimaio, and R. Schlegel A glutamine residue in the membrane-associating domain of the bovine papillomavirus type E5 oncoprotein mediates its binding to a transmembrane component of the vacuolar H(+)-ATPase J. Virol. 66 1992 405 413
81. +-ATPase is not sufficient for biological activity, using mammalian and yeast expression systems Virology 272 2000 315 325
82. +-ATPase can be dissociated from the E5-mediated epidermal growth factor receptor overactivation Oncogene 19 2000 3727 3732
83. G.H. Ashrafi, M.R. Haghshenas, B. Marchetti, P.M. O'Brian, and M.S. Campo E5 protein of human papillomavirus type 16 selectively downregulates surface HLA class I Int. J. Cancer 113 2005 276 283
84. E.H. Araibi, B. Marchetti, G.H. Ashrafi, and M.S. Campo Down regulation of major histocompatibility complex class I in bovine papillomas J. Gen. Virol. 85 2004 2809 2814
85. G.H. Ashrafi, M. Haghshenas, B. Marchetti, and M.S. Campo E5 protein of human papillomavirus 16 downreguates HLA class I and interacts with the heavy chain via its first hydrophobic domain Int. J. Cancer 119 2006 2105 2112
86. M. Gruener, I.G. Bravo, F. Momburg, A. Alonso, and P. Tomakidi The E5 protein of the human papillomavirus type 16 down-regulates HLA-1 surface expression in calnexin-expressing but not in calnexin-deficient cells Virol. J. 4 2007 116 (111-115)
87. M. Conrad, D.J. Goldstein, T. Andersson, and R. Schlegel The E5 protein of HPV-6, but not HPV-16, associates efficiently with cellular growth factor receptors Virology 200 1994 796 800
88. S.W. Straight, P.M. Hinkle, R.J. Jewers, and D.J. McCance 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 1993 4521 4532
89. E. Krawczyk, F.A. Suprynowicz, J.D. Hebert, C.M. Kamonjoh, and R. Schlegel The human papillomavirus type 16 E5 oncoprotein translocates calpactin I to the perinuclear region J. Virol. 85 2011 10968 10975
90. Y. Wakana, S. Takai, K.-i. Nakajima, K. Tani, A. Yamamoto, P. Watson, D.J. Stephens, H.-P. Hauri, and M. Tagaya Bap31 is an itinerant protein that moves between the peripheral endoplasmic reticulum (ER) and a juxtanuclear compartment related to ER-associated degradation Mol. Biol. Cell 19 2008 1825 1836
91. J.A. Regan, and L.A. Laimins Bap31 is a novel target of the human papillomavirus E5 protein J. Virol. 82 2008 10042 10051
92. E. Krawczyk, J.A. Hanover, R. Schlegel, and F.A. Suprynowicz Karyopherin β3: a new cellular target for HOV-16 E5 oncoprotein Biochem. Biophys. Res. Commun. 371 2008 684 688
93. S.R. Sudarshan, R. Schlegel, and X. Liu The HPV-16 E5 protein represses expression of stress pathway genes XBP-1 and COX-2 in genital keratinocytes Biochem. Biophys. Res. Commun. 399 2010 617 622
94. P. Tomakidi, H. Cheng, A. Kohl, G. Komposch, and A. Alonso Connexin 43 expression is downregulated in raft cultures of human keratinocytes expressing the human papillomavirus type 16 E5 protein Cell Tissue Res. 301 2000 323 327
95. F.A. Suprynowicz, G.L. Disbrow, E. Krawczyk, V. Simic, K. Lantzky, and R. Schlegel HPV-16 E5 oncoprotein upregulates lipid raft components caveolin-1 and ganglioside GM1 at the plasma membrane of cervical cells Oncogene 27 2008 1071 1078
96. G. Cui, C. Fang, and K. Han Prediction of protein-protein interactions between viruses and human by an SVM model BMC Bioinformatics 13 2012 S5
97. C. Lin, B.D. Lindenbach, B.M. Pragai, D.W. McCourt, and C.M. Rice Processing in the hepatitis C virus E2-NS2 region: identification of p7 and two distinct E2-specific products with different C termini J. Virol. 68 1994 5063 5073
98. K. Elbers, N. Tautz, P. Becher, D. Stoll, T. Rumenapf, and H.J. Thiel Processing in the pestivirus E2-NS2 region: identification of proteins p7 and E2p7 J. Virol. 70 1996 4131 4135
99. E. Steinmann, and T. Pietschmann Hepatitis C virus p7 - a viroporin crucial for virus assembly and emerging target for antiviral therapy Viruses 2 2010 2078 2095
100. S.D.C. Griffin Plugging the holes in hepatitis C virus antiviral therapy Proc. Natl. Acad. Sci. U. S. A. 106 2009 12567 12568
101. C.T. Jones, C.L. Murray, D.K. Eastman, J. Tassello, and C.M. Rice Hepatitis C virus p7 and NS2 proteins are essential for production of infectious virus J. Virol. 81 2007 8374 8383
102. E. Steinmann, F. Penin, S. Kallis, A.H. Patel, R. Bartenschlager, and T. Pietschmann Hepatitis C virus p7 protein is crucial for assembly and release of infectious virions PLoS Pathog. 3 2007 962 971
103. S. Carrère-Kremer, C. Montpellier-Pala, L. Cocquerel, C. Wychowski, F. Penin, and J. Dubuisson Subcellular localization and topology of the p7 polypeptide of hepatitis C virus J. Virol. 76 2002 3720 3730
104. A. Premkumar, L. Wilson, G.D. Ewart, and P.W. Gage Cation-selective ion channels formed by p7 of hepatitis C virus are blocked by hexamethylene amiloride FEBS Lett. 557 2004 99 103
105. R. Montserret, N. Saint, C. Vanbelle, A.G. Salvay, J.P. Simorre, C. Ebel, N. Sapay, J.-G. Renisio, A. Böckmann, E. Steinmann, T. Pietschmann, J. Dubuisson, C. Chipot, and F. Penin NMR structure and ion channel activity of the p7 protein from hepatitis C virus J. Biol. Chem. 285 2010 31446 31461
106. T. Whitfield, A.J. Miles, J.C. Scheinost, J. Offer, P. Wentworth Jr., R.A. Dwek, B.A. Wallace, P.C. Biggin, and N. Zitzmann The influence of different lipid environment on the structure and function of the hepatitis C virus p7 ion channel protein Mol. Membr. Biol. 28 2011 254 264
107. C.F. Chew, R. Vijayan, J. Chang, N. Zitzmann, and P.C. Biggin Determination of pore-lining residues in the hepatitis C virus p7 protein Biophys. J. 96 2009 L10 L12
108. D. Pavlovic, D.C.A. Neville, O. Argaud, B. Blumberg, R.A. Dwek, W.B. Fischer, and N. Zitzmann The hepatitis C virus p7 protein forms an ion channel that is inhibited by long-alkyl-chain iminosugar derivatives Proc. Natl. Acad. Sci. U. S. A. 100 2003 6104 6108
109. S.D.C. Griffin, L.P. Beales, D.S. Clarke, O. Worsfold, S.D. Evans, J. Jäger, M.P.G. Harris, and D.J. Rowlands The p7 protein of hepatitis C virus forms an ion channel that is blocked by the antiviral drug, amantadine FEBS Lett. 535 2003 34 38
110. D. Clarke, S. Griffin, L. Beales, C.S. Gelais, S. Burgess, M. Harris, and D. Rowlands Evidence for the formation of a heptameric ion channel complex by the hepatitis C virus p7 protein in vitro J. Biol. Chem. 281 2006 37057 37068
111. P. Luik, C. Chew, J. Aittoniemi, J. Chang, P. Wentworth Jr., R. Dwek, P.C. Biggin, C. Vénien-Bryan, and N. Zitzmann The 3-dimensional structure of the hepatitis C virus p7 ion channel by electron microscopy Proc. Natl. Acad. Sci. U. S. A. 106 2009 12712 12716
112. G.A. Cook, and S.J. Opella NMR studies of the p7 protein from hepatitis C virus Eur. Biophys. J. 39 2010 1097 1104
113. G.A. Cook, and S.J. Opella Secondary structure, dynamics, and architecture of the p7 membrane protein from hepatitis C virus by NMR spectroscopy Biochim. Biophys. Acta 1808 2011 1448 1453
114. G. Patargias, N. Zitzmann, R. Dwek, and W.B. Fischer Protein-protein interactions: modeling the hepatitis C virus ion channel p7 J. Med. Chem. 49 2006 648 655
115. D.E. Chandler, F. Penin, K. Schulten, and C. Chipot The p7 protein of hepatitis C virus forms structurally plastic, minimalist ion channels PLoS Comput. Biol. 8 2012 e1002702
116. Q. Li, A.L. Brass, A. Ng, Z. Hu, R.J. Xavier, T.J. Liang, and S.J. Elledge A genome-wide genetic screen for host factors required for hepatitis C virus propagation Proc. Natl. Acad. Sci. U. S. A. 106 2009 16410 16415
117. J.C. Lin, W.-H. Ho, A. Gurney, and A. Rosenthal The netrin-G1 ligand NGL-1 promotes the outgrowth of thalamocortical axons Nat. Neurosci. 6 2003 1270 1276
118. Y. Wang, C. Hudak, and H.S. Sul Role of preadipocyte factor 1 in adipocyte differentiation Clin. Lipidol. 5 2010 109 115
119. S.J. Bray Notch signalling: a simple pathway becomes complex Nat. Rev. Mol. Cell Biol. 7 2006 678 689
120. G. Randal, M. Panis, J.D. Cooper, T.L. Tellinghuisen, K.E. Sukhodolets, S. Pfeffer, M. Landthaler, P. Landgraf, S. Kan, B.D. Lindenbach, M. Chien, D.B. Weir, J.J. Russo, J. Ju, M.J. Brownstein, R. Sheridan, C. Sander, M. Zavolan, T. Tuschl, and C.M. Rice Cellular cofactors affecting hepatitis C virus infection and replication Proc. Natl. Acad. Sci. U. S. A. 104 2007 12884 12889
121. J.G. Magadán, and J.S. Bonifacino Transmembrane domain determinants of CD4 downregulation by HIV-1 Vpu J. Virol. 86 2012 757 772
122. M. Lazarczyk, P. Cassonnet, C. Pons, Y. Jacob, and M. Favre The EVER proteins as a natural barrier against papillomavirus: a new insight into the pathogenesis of human papilloma infections Microbiol. Mol. Biol. Rev. 73 2008 348 370