March8 inhibits HIV-1 infection by reducing virion incorporation of envelope glycoproteins

Nature Medicine

Volumn 21, Issue 12, 2015, Pages 1502-1507

  Tada, Takuya ^a   Zhang, Yanzhao ^a,b   Koyama, Takayoshi ^a   Tobiume, Minoru ^a   Tsunetsugu Yokota, Yasuko ^a   Yamaoka, Shoji ^b   Fujita, Hideaki ^c   Tokunaga, Kenzo ^a  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c NAGASAKI INTERNATIONAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; MEMBRANE ASSOCIATED RING CH 8; PROTEIN INHIBITOR; UNCLASSIFIED DRUG; G PROTEIN, VESICULAR STOMATITIS VIRUS; MARCH8 PROTEIN, HUMAN; MEMBRANE PROTEIN; MESSENGER RNA; PROTEIN BINDING; UBIQUITIN PROTEIN LIGASE; VIRUS ENVELOPE PROTEIN;

CELL PROLIFERATION; CELL SURFACE; CONTROLLED STUDY; DEGRADATION; DENDRITIC CELL; FEMALE; FLOW CYTOMETRY; HELA CELL LINE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOFLUORESCENCE MICROSCOPY; INTERNAL RIBOSOME ENTRY SITE; LETTER; LONG TERMINAL REPEAT; MACROPHAGE; MURINE LEUKEMIA VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIMIAN IMMUNODEFICIENCY VIRUS; TARGET CELL; VESICULOVIRUS; VIRION; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS INFECTIVITY; VIRUS PARTICLE; CELL MEMBRANE; CHEMISTRY; DOWN REGULATION; GENE SILENCING; GENETIC TRANSDUCTION; GENETICS; HEK293 CELL LINE; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LENTIVIRINAE; METABOLISM; PATHOGENICITY; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

CELL MEMBRANE; DOWN-REGULATION; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GENE SILENCING; HEK293 CELLS; HIV INFECTIONS; HIV-1; HUMANS; LENTIVIRUS; MACROPHAGES; MEMBRANE GLYCOPROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA, MESSENGER; TRANSDUCTION, GENETIC; UBIQUITIN-PROTEIN LIGASES; VIRAL ENVELOPE PROTEINS; VIRION;

EID: 84949624636     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3956     Document Type: Letter

References (55)

1. Bartee, E., Mansouri, M., Hovey Nerenberg, B.T., Gouveia, K. & Fruh, K. Downregulation of major histocompatibility complex class I by human ubiquitin ligases related to viral immune evasion proteins. J. Virol. 78, 1109-1120 (2004).
2. Goto, E. et al. c-MIR, a human E3 ubiquitin ligase, is a functional homolog of herpesvirus proteins MIR1 and MIR2 and has similar activity. J. Biol. Chem. 278, 14657-14668 (2003).
3. van de Kooij, B. et al. Ubiquitination by the membrane-Associated RING-CH-8 (March-8) ligase controls steady-state cell surface expression of tumor necrosis factor-related apoptosis inducing ligand (TRAIL) receptor 1. J. Biol. Chem. 288, 6617-6628 (2013).
4. Fujita, H., Iwabu, Y., Tokunaga, K. & Tanaka, Y. Membrane-Associated RING-CH (March) 8 mediates the ubiquitination and lysosomal degradation of the transferrin receptor. J. Cell Sci. 126, 2798-2809 (2013).
5. Chen, R., Li, M., Zhang, Y., Zhou, Q. & Shu, H.B. The E3 ubiquitin ligase March8 negatively regulates IL-1?-induced NF-?B activation by targeting the IL1RAP coreceptor for ubiquitination and degradation. Proc. Natl. Acad. Sci. USA 109, 14128-14133 (2012).
6. Ohmura-Hoshino, M. et al. Inhibition of MHC class II expression and immune responses by c-MIR. J. Immunol. 177, 341-354 (2006).
7. Tze, L.E. et al. CD83 increases MHC II and CD86 on dendritic cells by opposing IL-10-driven March1-mediated ubiquitination and degradation. J. Exp. Med. 208, 149-165 (2011).
8. Ishido, S., Wang, C., Lee, B.S., Cohen, G.B. & Jung, J.U. Downregulation of major histocompatibility complex class I molecules by Kaposi's sarcoma-Associated herpesvirus K3 and K5 proteins. J. Virol. 74, 5300-5309 (2000).
9. Coscoy, L. & Ganem, D. Kaposi's sarcoma-Associated herpesvirus encodes two proteins that block cell surface display of MHC class I chains by enhancing their endocytosis. Proc. Natl. Acad. Sci. USA 97, 8051-8056 (2000).
10. Stevenson, P.G., Efstathiou, S., Doherty, P.C. & Lehner, P.J. Inhibition of MHC class I-restricted antigen presentation by gamma 2-herpesviruses. Proc. Natl. Acad. Sci. USA 97, 8455-8460 (2000).
11. Lapaque, N., Jahnke, M., Trowsdale, J. & Kelly, A.P. The HLA-DR? chain is modified by polyubiquitination. J. Biol. Chem. 284, 7007-7016 (2009).
12. Bartee, E. et al. Membrane-Associated RING-CH proteins associate with Bap31 and target CD81 and CD44 to lysosomes. PLoS ONE 5, e15132 (2010).
13. Eyster, C.A. et al. March ubiquitin ligases alter the itinerary of clathrin-independent cargo from recycling to degradation. Mol. Biol. Cell 22, 3218-3230 (2011).
14. Harris, R.S. et al. DNA deamination mediates innate immunity to retroviral infection. Cell 113, 803-809 (2003).
15. Sheehy, A.M., Gaddis, N.C., Choi, J.D. & Malim, M.H. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418, 646-650 (2002).
16. Stremlau, M. et al. The cytoplasmic body component TRIM5? restricts HIV-1 infection in Old World monkeys. Nature 427, 848-853 (2004).
17. Van Damme, N. et al. 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, 245-252 (2008).
18. Neil, S.J., Zang, T. & Bieniasz, P.D. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451, 425-430 (2008).
19. Laguette, N. et al. SAMHD1 is the dendritic-And myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 474, 654-657 (2011).
20. Hrecka, K. et al. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 474, 658-661 (2011).
21. Liu, Z. et al. The interferon-inducible MxB protein inhibits HIV-1 infection. Cell Host Microbe 14, 398-410 (2013).
22. Kane, M. et al. MX2 is an interferon-induced inhibitor of HIV-1 infection. Nature 502, 563-566 (2013).
23. Goujon, C. et al. Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection. Nature 502, 559-562 (2013).
24. Yang, H.C., Shen, L., Siliciano, R.F. & Pomerantz, J.L. Isolation of a cellular factor that can reactivate latent HIV-1 without T cell activation. Proc. Natl. Acad. Sci. USA 106, 6321-6326 (2009).
25. Jahnke, M., Trowsdale, J. & Kelly, A.P. Structural requirements for recognition of major histocompatibility complex class II by membrane-Associated RING-CH (March) protein E3 ligases. J. Biol. Chem. 287, 28779-28789 (2012).
26. Mashiba, M., Collins, D.R., Terry, V.H. & Collins, K.L. Vpr overcomes macrophage-specific restriction of HIV-1 Env expression and virion production. Cell Host Microbe 16, 722-735 (2014).
27. Haller, C. et al. HIV-1 Nef and Vpu are functionally redundant broad-spectrum modulators of cell surface receptors, including tetraspanins. J. Virol. 88, 14241-14257 (2014).
28. Tokarev, A. & Guatelli, J. Misdirection of membrane trafficking by HIV-1 Vpu and Nef: Keys to viral virulence and persistence. Cell. Logist. 1, 90-102 (2011).
29. Tokunaga, K. et al. Molecular basis for cell tropism of CXCR4-dependent human immunodeficiency virus type 1 isolates. J. Virol. 75, 6776-6785 (2001).
30. Pham, H.M., Argañaraz, E.R., Groschel, B., Trono, D. & Lama, J. Lentiviral vectors interfering with virus-induced CD4 down-modulation potently block human immunodeficiency virus type 1 replication in primary lymphocytes. J. Virol. 78, 13072-13081 (2004).
31. Wiznerowicz, M. & Trono, D. Conditional suppression of cellular genes: lentivirus vector-mediated drug-inducible Rna interference. J. Virol. 77, 8957-8961 (2003).
32. Iwabu, Y. et al. HIV-1 accessory protein Vpu internalizes cell-surface BST-2/tetherin through transmembrane interactions leading to lysosomes. J. Biol. Chem. 284, 35060-35072 (2009).
33. Tobiume, M., Lineberger, J.E., Lundquist, C.A., Miller, M.D. & Aiken, C. Nef does not affect the efficiency of human immunodeficiency virus type 1 fusion with target cells. J. Virol. 77, 10645-10650 (2003).
34. Kinomoto, M. et al. Amino acid 36 in the human immunodeficiency virus type 1 gp41 ectodomain controls fusogenic activity: implications for the molecular mechanism of viral escape from a fusion inhibitor. J. Virol. 79, 5996-6004 (2005).
35. Kinomoto, M. et al. All APOBEC3 family proteins differentially inhibit LINE-1 retrotransposition. Nucleic Acids Res. 35, 2955-2964 (2007).
36. Daito, T. et al. A novel borna disease virus vector system that stably expresses foreign proteins from an intercistronic noncoding region. J. Virol. 85, 12170-12178 (2011).
37. Adachi, A. et al. Productive, persistent infection of human colorectal cell lines with human immunodeficiency virus. J. Virol. 61, 209-213 (1987).
38. Koyanagi, Y. et al. Dual infection of the central nervous system by AIDS viruses with distinct cellular tropisms. Science 236, 819-822 (1987).
39. Kitagawa, Y. et al. Inhibitory function of adapter-related protein complex 2 ? 1 subunit in the process of nuclear translocation of human immunodeficiency virus type 1 genome. Virology 373, 171-180 (2008).
40. Mochizuki, N. et al. An infectious DNA clone of HIV type 1 subtype C. AIDS Res. Hum. Retroviruses 15, 1321-1324 (1999).
41. Shibata, R. et al. Mutational analysis of the human immunodeficiency virus type 2 (HIV-2) genome in relation to HIV-1 and simian immunodeficiency virus SIV (AGM). J. Virol. 64, 742-747 (1990).
42. Naidu, Y.M. et al. Characterization of infectious molecular clones of simian immunodeficiency virus (SIVmac) and human immunodeficiency virus type 2: persistent infection of rhesus monkeys with molecularly cloned SIVmac. J. Virol. 62, 4691-4696 (1988).
43. Niwa, H., Yamamura, K. & Miyazaki, J. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108, 193-199 (1991).
44. Fouchier, R.A., Meyer, B.E., Simon, J.H., Fischer, U. & Malim, M.H. HIV-1 infection of non-dividing cells: evidence that the amino-terminal basic region of the viral matrix protein is important for Gag processing but not for post-entry nuclear import. EMBO J. 16, 4531-4539 (1997).
45. Iwabu, Y. et al. Differential anti-APOBEC3G activity of HIV-1 Vif proteins derived from different subtypes. J. Biol. Chem. 285, 35350-35358 (2010).
46. Ross, T.M., Oran, A.E. & Cullen, B.R. Inhibition of HIV-1 progeny virion release by cell-surface CD4 is relieved by expression of the viral Nef protein. Curr. Biol. 9, 613-621 (1999).
47. Dong, B. et al. An infectious retrovirus susceptible to an IFN antiviral pathway from human prostate tumors. Proc. Natl. Acad. Sci. USA 104, 1655-1660 (2007).
48. Shalem, O. et al. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 343, 84-87 (2014).
49. Nomaguchi, M., Doi, N. & Adachi, A. Virological characterization of HIV-2 vpx gene mutants in various cell systems. Microbes Infect. 16, 695-701 (2014).
50. Nakai-Murakami, C. et al. HIV-1 Vpr induces ATM-dependent cellular signal with enhanced homologous recombination. Oncogene 26, 477-486 (2007).
51. Otake, K. et al. The carboxyl-terminal region of HIV-1 Nef protein is a cell surface domain that can interact with CD4+ T cells. J. Immunol. 153, 5826-5837 (1994).
52. Maldarelli, F., Chen, M.Y., Willey, R.L. & Strebel, K. Human immunodeficiency virus type 1 Vpu protein is an oligomeric type I integral membrane protein. J. Virol. 67, 5056-5061 (1993).
53. Koyama, T., Sun, B., Tokunaga, K., Tatsumi, M. & Ishizaka, Y. DNA damage enhances integration of HIV-1 into macrophages by overcoming integrase inhibition. Retrovirology 10, 21 (2013).
54. Tsunetsugu-Yokota, Y. et al. Monocyte-derived cultured dendritic cells are susceptible to human immunodeficiency virus infection and transmit virus to resting T cells in the process of nominal antigen presentation. J. Virol. 69, 4544-4547 (1995).
55. Perez-Caballero, D. et al. Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 139, 499-511 (2009).