Pathogenic strains of viruses that infect humans are encapsulated in membranes derived from the host cell in which they infect. After replication, these viruses are released by a budding process that requires cell/viral membrane scission. As such, this represents a natural target for innate immunity mechanisms to interdict enveloped virus spread and recent advances in this field will be the subject of this paper. 1. Budding of Retroviruses Retroviruses, such as human immunodeficiency virus type 1 (HIV-1) and avian sarcoma/leukosis virus (ASLV), bud from cells using a similar mechanism (see Figure 1). Monoubiquitination of viral Gag polyproteins, catalyzed by an E1, E2, and E3 ubiquitin ligase complex, is important in the process where the ubiquitin most likely serves as a ligand for assembly of various protein budding complexes [1–5]. A recent study, however, has presented evidence that either ubiquitination of Gag or ubiquitination of transacting proteins can be used to assemble downstream virus-budding complexes [6]. Ubiquitin is a 76-amino-acid cell regulatory protein that is conjugated to proteins at lysine residues. Free ubiquitin in the cytosol is activated in an ATP-dependent reaction by an E1 enzyme, which then transfers the ubiquitin to a cysteine residue of an E2 ubiquitin-conjugating enzyme. The E2 protein interacts with a specific E3 ubiquitin ligase, which selects the target protein for the covalent transfer of the ubiquitin. Figure 1: Parallel pathways used by ASLV and HIV-1 Gag to bud from cells. Retroviruses recruit components of the ESCRT machinery to assemble budding complexes. Step 1: HIV-1 and ASLV Gag L-domains bind to Tsg101 and Nedd4, respectively. They also bind the Alix adaptor protein. Whether these initial interactions take place in the cytosol or at the plasma membrane remains to be defined. Step 2: Nedd4 mediates ubiquitination of ASV Gag. HIV-1 Gag is ubiquitinated by an unidentified E3 ligase. Step 3: Gag oligomerization in the cytosol increases membrane avidity and in conjunction with the M domain signal at the N-terminus of Gag targets the polyproteins to sites of assembly/budding on the plasma membrane. ASLV Gag assembles on rhodamine labeled phosphatidylethanolamine (N-Rh-PE)-positive, endosome-derived membranes. HIV-1 Gag assembles on N-Rh-PE-negative membranes. Step 4: The ASLV Gag/Nedd4/Alix complex recruits ESCRT-II proteins while the HIV-1 Gag/Tsg101/Alix complex recruits the remainder of the ESCRT-I proteins. Each early budding complex then recruits the same ESCRT-III machinery which promotes the membrane
References
[1]
D. G. Demirov and E. O. Freed, “Retrovirus budding,” Virus Research, vol. 106, no. 2, pp. 87–102, 2004.
[2]
J. Martin-Serrano, T. Zang, and P. D. Bieniasz, “HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress,” Nature Medicine, vol. 7, no. 12, pp. 1313–1319, 2001.
[3]
J. Martin-Serrano, “The role of ubiquitin in retroviral egress,” Traffic, vol. 8, no. 10, pp. 1297–1303, 2007.
[4]
A. Patnaik, V. Chau, and J. W. Wills, “Ubiquitin is part of the retrovirus budding machinery,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 24, pp. 13069–13074, 2000.
[5]
M. L. Vana, Y. Tang, A. Chen, G. Medina, C. Carter, and J. Leis, “Role of Nedd4 and ubiquitination of rous sarcoma virus Gag in budding of virus-like particles from cells,” Journal of Virology, vol. 78, no. 24, pp. 13943–13953, 2004.
[6]
M. Zhadina and P. D. Bieniasz, “Functional interchangeability of late domains, late domain cofactors and ubiquitin in viral budding,” Plos Pathogens, vol. 6, no. 10, Article ID e1001153, 2010.
[7]
G. Medina, Y. Zhang, Y. Tang et al., “The functionally exchangeable L domains in RSV and HIV-1 Gag direct particle release through pathways linked by Tsg101,” Traffic, vol. 6, no. 10, pp. 880–894, 2005.
[8]
A. Ono and E. O. Freed, “Plasma membrane rafts play a critical role in HIV-1 assembly and release,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 24, pp. 13925–13930, 2001.
[9]
A. Kikonyogo, F. Bouamr, M. L. Vana et al., “Proteins related to the Nedd4 family of ubiquitin protein ligases interact with the L domain of Rous sarcoma virus and are required for gag budding from cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 20, pp. 11199–11204, 2001.
[10]
L. VerPlank, B. Agresta, T. Grassa, A. Kikonyogo, J. Leis, and C. Carter, “Tsg101, the prototype of a class of dominant-negative ubiquitin regulators, binds human immunodeficiency virus type 1 Pr55Gag: the L domain is a determining of binding,” Proceedings National Academy Science USA, vol. 98, pp. 7724–7729, 2001.
[11]
K. A. Dilley, D. Gregory, M. C. Johnson, and V. M. Vogt, “An LYPSL late domain in the Gag protein contributes to the efficient release and replication of Rous sarcoma virus,” Journal of Virology, vol. 84, no. 13, pp. 6276–6287, 2010.
[12]
B. Strack, A. Calistri, S. Craig, E. Popova, and H. G. G？ttlinger, “AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding,” Cell, vol. 114, no. 6, pp. 689–699, 2003.
[13]
H. G. Gottlinger, T. Dorfman, J. G. Sodroski, and W. A. Haseltine, “Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 8, pp. 3195–3199, 1991.
[14]
J. W. Wills, C. E. Cameron, C. B. Wilson, Y. Xiang, R. P. Bennett, and J. Leis, “An assembly domain of the Rous sarcoma virus Gag protein required late in budding,” Journal of Virology, vol. 68, no. 10, pp. 6605–6618, 1994.
[15]
Y. Xiang, C. E. Cameron, J. W. Wills, and J. Leis, “Fine mapping and characterization of the Rous sarcoma virus Pr76gaglate assembly domain,” Journal of Virology, vol. 70, no. 8, pp. 5695–5700, 1996.
[16]
B. A. Puffer, L. J. Parent, J. W. Wills, and R. C. Montelaro, “Equine infectious anemia virus utilizes a YXXL motif within the late assembly domain of the Gag p9 protein,” Journal of Virology, vol. 71, no. 9, pp. 6541–6546, 1997.
[17]
G. Medina, A. Pincetic, L. S. Ehrlich et al., “Tsg101 can replace Nedd4 function in ASV Gag release but not membrane targeting,” Virology, vol. 377, no. 1, pp. 30–38, 2008.
[18]
D. E. Ott, L. V. Coren, R. C. Sowder, J. Adams, and U. Schubert, “Retroviruses have differing requirements for proteasome function in the budding process,” Journal of Virology, vol. 77, no. 6, pp. 3384–3393, 2003.
[19]
H.-Y. Chung, E. Moirta, U. Schwedler, et al., “Nedd4L overexpression rescues the release and infectivity of human immunodeficiency virus type 1 constructs lacking PTAP and YPXL late domains,” Journal Virology, vol. 82, no. 10, pp. 4884–4897, 2008.
[20]
Y. Usami, S. Popov, E. Popova, and H. G. G？ttlinger, “Efficient and specific rescue of human immunodeficiency virus type 1 budding defects by a Nedd4-like ubiquitin ligase,” Journal of Virology, vol. 82, no. 10, pp. 4898–4907, 2008.
[21]
E. Weiss, E. Popova, H. Yamanaka, H. Kim, J. Huibregtse, and H. Gottlinger, “Rescue of HIV-1 release by targeting widely divergent Nedd4-type ubiquitin ligases and isolated catalytic hect domains to Gag,” Plos Pathogens, vol. 6, Article ID e1001107, 13 pages, 2010.
[22]
F. Bouamr, J. A. Melillo, M. Q. Wang et al., “PPPYEPTAP motif is the late domain of human T-Cell leukemia virus Type 1 Gag and mediates its functional interaction with cellular proteins Nedd4 and Tsg101,” Journal of Virology, vol. 77, no. 22, pp. 11882–11895, 2003.
[23]
E. Gottwein, J. Bodem, B. Müller, A. Schmechel, H. Zentgraf, and H. G. Kr？usslich, “The Mason-Pfizer monkey virus PPPY and PSAP motifs both contribute to virus release,” Journal of Virology, vol. 77, no. 17, pp. 9474–9485, 2003.
[24]
J. G. Carlton and J. Martin-Serrano, “Parallels between cytokinesis and retroviral budding: a role for the budding: a role for the ESCRT,” Science, vol. 316, no. 5833, pp. 1908–1912, 2007.
[25]
U. K. von Schwedler, M. Stuchell, B. Muller, et al., “The protein network of HIV budding,” Cell, vol. 114, pp. 701–713, 2003.
[26]
M. Babst, “A protein's final ESCRT,” Traffic, vol. 6, no. 1, pp. 2–9, 2005.
[27]
J. E. Garrus, U. K. von Schwedler, O. W. Pornillos et al., “Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding,” Cell, vol. 107, no. 1, pp. 55–65, 2001.
[28]
A. Pincetic, G. Medina, C. Carter, and J. Leis, “Avian sarcoma virus and human immunodeficiency virus, type 1 use different subsets of ESCRT proteins to facilitate the budding process,” Journal of Biological Chemistry, vol. 283, no. 44, pp. 29822–29830, 2008.
[29]
A. Pincetic and J. Leis, “The mechanism of budding of retroviruses from cell membranes,” Advances in Virology, vol. 2009, Article ID 623969, 9 pages, 2009.
[30]
S. Lata, G. Schoehn, J. Solomons, R. Pires, H. G. G？ttlinger, and W. Weissenhorn, “Structure and function of ESCRT-III,” Biochemical Society Transactions, vol. 37, no. 1, pp. 156–160, 2009.
[31]
E. Morita, V. Sandrin, J. McCullough, A. Katsuyama, I. Baci Hamilton, and W. I. Sundquist, “ESCRT-III protein requirements for HIV-1 budding,” Cell Host and Microbe, vol. 9, no. 3, pp. 235–242, 2011.
[32]
A. Scott, H. Y. Chung, M. Gonciarz-Swiatek et al., “Structural and mechanistic studies of VPS4 proteins,” The EMBO Journal, vol. 24, no. 20, pp. 3658–3669, 2005.
[33]
H. T. H. Tsang, J. W. Connell, S. E. Brown, A. Thompson, E. Reid, and C. M. Sanderson, “A systematic analysis of human CHMP protein interactions: additional MIT domain-containing proteins bind to multiple components of the human ESCRT III complex,” Genomics, vol. 88, no. 3, pp. 333–346, 2006.
[34]
C. Kieffer, J. J. Skalicky, E. Morita et al., “Two distinct modes of ESCRT-III recognition are required for VPS4 functions in lysosomal protein targeting and HIV-1 budding,” Developmental Cell, vol. 15, no. 1, pp. 62–73, 2008.
[35]
M. D. Stuchell-Brereton, J. J. Skalicky, C. Kieffer, M. A. Karren, S. Ghaffarian, and W. I. Sundquist, “ESCRT-III recognition by VPS4 ATPases,” Nature, vol. 449, no. 7163, pp. 740–744, 2007.
[36]
D. M. Ward, M. B. Vaughn, S. L. Shiflett et al., “The role of LIP5 and CHMP5 in multivesicular body formation and HIV-1 budding in mammalian cells,” Journal of Biological Chemistry, vol. 280, no. 11, pp. 10548–10555, 2005.
[37]
S. Shim, S. A. Merrill, and P. I. Hanson, “Novel interactions of ESCRT-III with LIP5 and VPS4 and their implications for ESCRT-III disassembly,” Molecular Biology of the Cell, vol. 19, no. 6, pp. 2661–2672, 2008.
[38]
I. F. Azmi, B. A. Davies, J. Xiao, M. Babst, Z. Xu, and D. J. Katzmann, “ESCRT-III family members stimulate Vps4 ATPase activity directly or via Vta1,” Developmental Cell, vol. 14, no. 1, pp. 50–61, 2008.
[39]
M. Perez, R. C. Craven, and J. C. de la Torre, “The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 22, pp. 12978–12983, 2003.
[40]
S. Urata, T. Noda, Y. Kawaoka, H. Yokosawa, and J. Yasuda, “Cellular factors required for Lassa virus budding,” Journal of Virology, vol. 80, no. 8, pp. 4191–4195, 2006.
[41]
S. Urata, T. Noda, Y. Kawaoka, S. Morikawa, H. Yokosawa, and J. Yasuda, “Interaction of Tsg101 with Marburg virus VP40 depends on the PPPY motif, but not the PT/SAP motif as in the case of Ebola virus, and Tsg101 plays a critical role in the budding of Marburg virus-like particles induced by VP40, NP, and GP,” Journal of Virology, vol. 81, no. 9, pp. 4895–4899, 2007.
[42]
C. Lambert, T. D？ring, and R. Prange, “Hepatitis B virus maturation is sensitive to functional inhibition of ESCRT-III, Vps4, and γ2-adaptin,” Journal of Virology, vol. 81, no. 17, pp. 9050–9060, 2007.
[43]
C. M. Crump, C. Yates, and T. Minson, “Herpes simplex virus type 1 cytoplasmic envelopment requires functional Vps4,” Journal of Virology, vol. 81, no. 14, pp. 7380–7387, 2007.
[44]
A. P. Schmitt, G. P. Leser, E. Morita, W. I. Sundquist, and R. A. Lamb, “Evidence for a new viral late-domain core sequence, FPIV, necessary for budding of a paramyxovirus,” Journal of Virology, vol. 79, no. 5, pp. 2988–2997, 2005.
[45]
M. Li, P. T. Schmitt, Z. Li, T. S. McCrory, B. He, and A. P. Schmitt, “Mumps virus matrix, fusion, and nucleocapsid proteins cooperate for efficient production of virus-like particles,” Journal of Virology, vol. 83, no. 14, pp. 7261–7272, 2009.
[46]
T. Irie and R. N. Harty, “L-domain flanking sequences are important for host interactions and efficient budding of vesicular stomatitis virus recombinants,” Journal of Virology, vol. 79, no. 20, pp. 12617–12622, 2005.
[47]
C. Wirblich, G. S. Tan, A. Papaneri et al., “PPEY motif within the Rabies Virus (RV) matrix protein is essential for efficient virion release and RV pathogenicity,” Journal of Virology, vol. 82, no. 19, pp. 9730–9738, 2008.
[48]
R. N. Harty, M. E. Brown, G. Wang, J. Huibregtse, and F. P. Hayes, “A PPxY motif within the VP40 protein of Ebola virus interacts physically and functionally with a ubiquitin ligase: implications for filovirus budding,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 25, pp. 13871–13876, 2000.
[49]
A. Okumura, P. M. Pitha, and R. N. Harty, “ISG15 inhibits Ebola VP40 VLP budding in an L-domain-dependent manner by blocking Nedd4 ligase activity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 10, pp. 3974–3979, 2008.
[50]
L. S. Silvestri, G. Ruthel, G. Kallstrom et al., “Involvement of vacuolar protein sorting pathway in Ebola virus release independent of TSG101 interaction,” Journal of Infectious Diseases, vol. 196, supplement 2, pp. S264–S270, 2007.
[51]
J. Timmins, G. Schoehn, S. Ricard-Blum et al., “Ebola virus matrix protein VP40 interaction with human cellular factors Tsg101 and Nedd4,” Journal of Molecular Biology, vol. 326, no. 2, pp. 493–502, 2003.
[52]
Y. Ariumi, M. Kuroki, M. Maki et al., “The ESCRT system is required for hepatitis C virus production,” Plos ONE, vol. 6, no. 1, pp. 1–10, 2011.
[53]
L. Corless, C. M. Crump, S. D. C. Griffin, and M. Harris, “Vps4 and the ESCRT-III complex are required for the release of infectious hepatitis C virus particles,” Journal of General Virology, vol. 91, no. 2, pp. 362–372, 2010.
[54]
T. Pawliczek and C. M. Crump, “Herpes simplex virus type 1 production requires a functional ESCRT-III complex but is independent of TSG101 and ALIX expression,” Journal of Virology, vol. 83, no. 21, pp. 11254–11264, 2009.
[55]
G. M. Taylor, P. I. Hanson, and M. Kielian, “Ubiquitin depletion and dominant-negative VPS4 inhibit rhabdovirus budding without affecting alphavirus budding,” Journal of Virology, vol. 81, no. 24, pp. 13631–13639, 2007.
[56]
A. P. Schmitt, G. P. Leser, D. L. Waning, and R. A. Lamb, “Requirements for budding of paramyxovirus simian virus 5 virus-like particles,” Journal of Virology, vol. 76, no. 8, pp. 3952–3964, 2002.
[57]
A. Salditt, S. Koethe, C. Pohl, et al., “Measles virus M protein-driven particle production does not involve the endosomal sorting complex required for transport (ESCRT) system,” Journal General Virology, vol. 91, pp. 1464–1472, 2010.
[58]
T. J. Utley, N. A. Ducharme, V. Varthakavi et al., “Respiratory syncytial virus uses a Vps4-independent budding mechanism controlled by Rab11-FIP2,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 29, pp. 10209–10214, 2008.
[59]
A. Fraile-Ramos, A. Pelchen-Matthews, C. Risco et al., “The ESCRT machinery is not required for human cytomegalovirus envelopment,” Cellular Microbiology, vol. 9, no. 12, pp. 2955–2967, 2007.
[60]
R. Tandon, D. P. AuCoin, and E. S. Mocarski, “Human cytomegalovirus exploits ESCRT machinery in the process of virion maturation,” Journal of Virology, vol. 83, no. 20, pp. 10797–10807, 2009.
[61]
T. Irie, J. M. Licata, J. P. McGettigan, M. J. Schnell, and R. N. Harty, “Budding of PPxY-containing rhabdoviruses is not dependent on host proteins TSG101 and VPS4A,” Journal of Virology, vol. 78, no. 10, p. 5532, 2004.
[62]
B. J. Chen and R. A. Lamb, “Mechanisms for enveloped virus budding: can some viruses do without an ESCRT?” Virology, vol. 372, no. 2, pp. 221–232, 2007.
[63]
J. C. C. Lai, W. W. L. Chan, F. Kien, J. M. Nicholls, J. S. M. Peiris, and J. M. Garcia, “Formation of virus-like particles from human cell lines exclusively expressing influenza neuraminidase,” Journal of General Virology, vol. 91, no. 9, pp. 2322–2330, 2010.
[64]
J. S. Rossman, X. Jing, G. P. Leser, and R. A. Lamb, “Influenza virus M2 protein mediates ESCRT-independent membrane scission,” Cell, vol. 142, no. 6, pp. 902–913, 2010.
[65]
J. S. Rossman, X. Jing, G. P. Leser, V. Balannik, L. H. Pinto, and R. A. Lamb, “Influenza virus M2 ion channel protein is necessary for filamentous virion formation,” Journal of Virology, vol. 84, no. 10, pp. 5078–5088, 2010.
[66]
M. A. Yondola, F. Fernandes, A. Belicha-Villanueva et al., “Budding capability of the influenza virus neuraminidase can be modulated by tetherin,” Journal of Virology, vol. 85, no. 6, pp. 2480–2491, 2011.
[67]
S. Goodbourn, L. Didcock, and R. E. Randall, “Interferons: cell signalling, immune modulation, antiviral responses and virus countermeasures,” Journal of General Virology, vol. 81, no. 10, pp. 2341–2364, 2000.
[68]
L. G. Guidotti and F. V. Chisari, “Noncytolytic control of viral infections by the innate and adaptive immune response,” Annual Review of Immunology, vol. 19, pp. 65–91, 2001.
[69]
S. Neil and P. Bieniasz, “Human immunodeficiency virus, restriction factors, and interferon,” Journal of Interferon and Cytokine Research, vol. 29, no. 9, pp. 569–580, 2009.
[70]
D. Wolf and S. P. Goff, “Host restriction factors blocking retroviral replication,” Annual Review of Genetics, vol. 42, pp. 143–163, 2008.
[71]
J. P. Donahue, M. L. Vetter, N. A. Mukhtar, and R. T. D'Aquila, “The HIV-1 Vif PPLP motif is necessary for human APOBEC3G binding and degradation,” Virology, vol. 377, no. 1, pp. 49–53, 2008.
[72]
S. Sebastian and J. Luban, “TRIM5α selectively binds a restriction-sensitive retroviral capsid,” Retrovirology, vol. 2, article 40, 2005.
[73]
M. Stremlau, M. Perron, M. Lee et al., “Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5α restriction factor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 14, pp. 5514–5519, 2006.
[74]
T. Sakuma, T. Noda, S. Urata, Y. Kawaoka, and J. Yasuda, “Inhibition of Lassa and Marburg virus production by tetherin,” Journal Virology, vol. 83, no. 5, pp. 2382–2385, 2009.
[75]
S. J. D. Neil, T. Zang, and P. D. Bieniasz, “Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu,” Nature, vol. 451, no. 7177, pp. 425–430, 2008.
[76]
N. Van Damme, D. Goff, C. Katsura, et al., “The interferon-induced protein BST-2 restricts HIV-1 release and is down regulated from the cell surface by the viral Vpu protein,” Cell Host & Microbe, vol. 3, no. 4, pp. 245–252, 2008.
[77]
B. D. Kuhl, R. D. Sloan, D. A. Donahue, T. Bar-Magen, C. Liang, and M. A. Wainberg, “Tetherin restricts direct cell-to-cell infection of HIV-1,” Retrovirology, vol. 7, article 115, 2010.
[78]
C. T. Dao and D. E. Zhang, “ISG15: a ubiquitin-like enigma,” Frontiers in Bioscience, vol. 10, no. 2, pp. 2701–2722, 2005.
[79]
O. Haller, G. Kochs, and F. Weber, “The interferon response circuit: induction and suppression by pathogenic viruses,” Virology, vol. 344, no. 1, pp. 119–130, 2006.
[80]
D. P. Bednarik, J. D. Mosca, N. B. K. Raj, and P. M. Pitha, “Inhibition of human immunodeficiency virus (HIV) replication by HIV-trans-activated α2-interferon,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 13, pp. 4958–4962, 1989.
[81]
R. N. Harty, P. M. Pitha, and A. Okumura, “Antiviral activity of innate immune protein ISG15,” Journal of Innate Immunity, vol. 1, no. 5, pp. 397–404, 2009.
[82]
Y. J. Jeon, H. M. Yoo, and C. H. Chung, “ISG15 and immune diseases,” Biochimica et Biophysica Acta, vol. 1802, no. 5, pp. 485–496, 2010.
[83]
Z. Kuang, E. J. Seo, and J. Leis, “Mechanism of inhibition of retrovirus release from cells by interferon-induced gene ISG15,” Journal of Virology, vol. 85, no. 14, pp. 7153–7161, 2011.
[84]
A. Pincetic, Z. Kuang, E. J. Seo, and J. Leis, “The interferon-induced gene ISG15 blocks retrovirus release from cells late in the budding process,” Journal of Virology, vol. 84, no. 9, pp. 4725–4736, 2010.
[85]
G. Poli, J. M. Orenstein, A. Kinter, T. M. Folks, and A. S. Fauci, “Interferon-α but not AZT suppresses HIV expression in chronically infected cell lines,” Science, vol. 244, no. 4904, pp. 575–577, 1989.
[86]
Y. Shirazi and P. M. Pitha, “Alpha interferon inhibits early stages of the human immunodeficiency virus type 1 replication cycle,” Journal of Virology, vol. 66, no. 3, pp. 1321–1328, 1992.
[87]
B. Skaug and Z. J. Chen, “Emerging role of ISG15 in antiviral immunity,” Cell, vol. 143, no. 2, pp. 187–190, 2010.
[88]
W. Zou, V. Papov, O. Malakhova et al., “ISG15 modification of ubiquitin E2 Ubc13 disrupts its ability to form thioester bond with ubiquitin,” Biochemical and Biophysical Research Communications, vol. 336, no. 1, pp. 61–68, 2005.
[89]
Y. G. Chang, X. Z. Yan, Y. Y. Xie et al., “Different roles for two ubiquitin-like domains of ISG15 in protein modification,” Journal of Biological Chemistry, vol. 283, no. 19, pp. 13370–13377, 2008.
[90]
J. Narasimhan, M. Wang, Z. Fu, J. M. Klein, A. L. Haas, and J. J. P. Kim, “Crystal structure of the interferon-induced ubiquitin-like protein ISG15,” Journal of Biological Chemistry, vol. 280, no. 29, pp. 27356–27365, 2005.
[91]
K. R. Loeb and A. L. Haas, “The interferon-inducible 15-kDa ubiquitin homolog conjugates to intracellular proteins,” Journal of Biological Chemistry, vol. 267, no. 11, pp. 7806–7813, 1992.
[92]
C. Zhao, C. Denison, J. M. Huibregtse, S. Gygi, and R. M. Krug, “Human ISG15 conjugation targets both IFN-induced and constitutively expressed proteins functioning in diverse cellular pathways,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 29, pp. 10200–10205, 2005.
[93]
C. Zhao, T.-Y. Hsiang, R. L. Kuo, and R. M. Krug, “ISG15 conjugation system targets the viral NS1 protein in influenza A virus-infected cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 5, pp. 2253–2258, 2010.
[94]
N. V. Giannakopoulos, E. Arutyunova, C. Lai, D. J. Lenschow, A. L. Haas, and H. W. Virgin, “ISG15 Arg151 and the ISG15-conjugating enzyme UbE1L are important for innate immune control of sindbis virus,” Journal of Virology, vol. 83, no. 4, pp. 1602–1610, 2009.
[95]
W. Yuan and R. M. Krug, “Influenza B virus NS1 protein inhibits conjugation of the interferon (IFN)-induced ubiquitin-like ISG15 protein,” The EMBO Journal, vol. 20, no. 3, pp. 362–371, 2001.
[96]
K. L. Kim, N. V. Giannakopoulos, H. W. Virgin, and D. E. Zhang, “Interferon-inducible ubiquitin E2, Ubc8, is a conjugating enzyme for protein ISGylation,” Molecular and Cellular Biology, vol. 24, no. 21, pp. 9592–9600, 2004.
[97]
M. Zhadina and P. D. Bieniasz, “Functional interchangeability of late domains, late domain cofactors and ubiquitin in viral budding,” Plos Pathog, vol. 6, no. 10, Article ID e1001153, 2010.
[98]
A. Dastur, S. Beaudenon, M. Kelley, R. M. Krug, and J. M. Huibregtse, “Herc5, an interferon-induced HECT E3 enzyme, is required for conjugation of ISG15 in human cells,” Journal of Biological Chemistry, vol. 281, no. 7, pp. 4334–4338, 2006.
[99]
J. J. Y. Wong, Y. F. Pung, N. S. K. Sze, and K. C. Chin, “HERC5 is an IFN-induced HECT-type E3 protein ligase that mediates type I IFN-induced ISGylation of protein targets,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 28, pp. 10735–10740, 2006.
[100]
N. V. Giannakopoulos, J. K. Luo, V. Papov et al., “Proteomic identification of proteins conjugated to ISG15 in mouse and human cells,” Biochemical and Biophysical Research Communications, vol. 336, no. 2, pp. 496–506, 2005.
[101]
L. Chen, S. Li, and I. McGilvray, “The ISG15/USP18 ubiquitin-like pathway (ISGylation system) in Hepatitis C Virus infection and resistance to interferon therapy,” International Journal of Biochemistry and Cell Biology, vol. 43, no. 10, pp. 1427–1431, 2011.
[102]
I. F. Pitha-Rowe and P. M. Pitha, “Viral defense, carcinogenesis and ISG15: novel roles for an old ISG,” Cytokine and Growth Factor Reviews, vol. 18, no. 5-6, pp. 409–417, 2007.
[103]
A. Okumura, G. Lu, I. Pitha-Rowe, and P. M. Pitha, “Innate antiviral response targets HIV-1 release by the induction of ubiquitin-like protein ISG15,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 5, pp. 1440–1445, 2006.
[104]
P. M. Pitha, B. Fernie, F. Maldarelli, T. Hattman, and N. A. Wivel, “Effect of interferon on mouse leukemia virus (MuLV). V. abnormal proteins on virions of Rauscher MuLV produced in the presence of interferon,” Journal General Virology, vol. 46, no. 1, pp. 97–110, 1980.
[105]
D. J. Lenschow, C. Lai, N. Frias-Staheli et al., “IFN-stimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 4, pp. 1371–1376, 2007.
[106]
S. W. Werneke, C. Schilte, A. Rohatgi, et al., “ISG15 is critical in the control of Chikungunya virus infection independent of UbE1L mediated conjugation,” Plos Pathogens, vol. 7, no. 10, Article ID e1002322, 2011.
[107]
D. J. Lenschow, N. V. Giannakopoulos, L. J. Gunn et al., “Identification of interferon-stimulated gene 15 as an antiviral molecule during Sindbis virus infection in vivo,” Journal of Virology, vol. 79, no. 22, pp. 13974–13983, 2005.
[108]
O. A. Malakhova and D. E. Zhang, “ISG15 inhibits Nedd4 ubiquitin E3 activity and enhances the innate antiviral response,” Journal of Biological Chemistry, vol. 283, no. 14, pp. 8783–8787, 2008.
[109]
B. Mangeat, G. Gers-Huber, M. Lehmann, M. Zufferey, J. Luban, and V. Piguet, “HIV-1 Vpu neutralizes the antiviral factor tetherin/BST-2 by binding it and directing its beta-TrCP2-dependent degradation,” PLoS Pathogens, vol. 5, no. 9, Article ID e1000574, 2009.
[110]
C. Pardieu, R. Vigan, S. J. Wilson et al., “The RING-CH ligase K5 antagonizes restriction of KSHV and HIV-1 particle release by mediating ubiquitin-dependent endosomal degradation of tetherin,” Plos pathogens, vol. 6, no. 4, Article ID e1000843, 16 pages, 2010.
[111]
G. A. Versteeg, B. G. Hale, S. van Boheemen, T. Wolff, D. J. Lenschow, and A. García-Sastre, “Species-specific antagonism of host ISGylation by the influenza B virus NS1 protein,” Journal of Virology, vol. 84, no. 10, pp. 5423–5430, 2010.
[112]
W. Yuan, J. M. Aramini, G. T. Montelione, and R. M. Krug, “Structural basis for ubiquitin-like ISG 15 protein binding to the NS1 protein of influenza B virus: a protein-protein interaction function that is not shared by the corresponding N-terminal domain of the NS1 protein of influenza A virus,” Virology, vol. 304, no. 2, pp. 291–301, 2002.
[113]
L. Li, D. Wang, Y. Jiang, et al., “Crystal structure of human ISG15 protein in complex with Influenza B Virus NS1B,” Journal Biological Chemistry, vol. 286, no. 35, pp. 30258–30262, 2011.
[114]
M. D. Arguello and J. Hiscott, “Ub surprised: viral ovarian tumor domain proteases remove ubiquitin and ISG15 conjugates,” Cell Host and Microbe, vol. 2, no. 6, pp. 367–369, 2007.
[115]
Z. Sun, Y. Li, R. Ransburgh, E. J. Snijder, and Y. Fang, “Nonstructural protein 2 of porcine reproductive and respiratory syndrome virus inhibits the antiviral function of interferon-stimulated gene 15,” Journal Virology, vol. 86, no. 7, pp. 3839–3850, 2012.
[116]
S. Guerra, A. Cáceres, K. P. Knobeloch, I. Horak, and M. Esteban, “Vaccinia virus E3 protein prevents the antiviral action of ISG15,” Plos Pathogens, vol. 4, no. 7, Article ID e1000096, 2008.
