IFITM Proteins Restrict HIV-1 Infection by Antagonizing the Envelope Glycoprotein

Cell Reports

Volumn 13, Issue 1, 2015, Pages 145-156

  Yu, Jingyou ^a   Li, Minghua ^a   Wilkins, Jordan ^a   Ding, Shilei ^c,d   Swartz, Talia H ^b   Esposito, Anthony M ^b   Zheng, Yi Min ^a   Freed, Eric O ^e   Liang, Chen ^c,d   Chen, Benjamin K ^b   Liu, Shan Lu ^a  

^a University of Missouri   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c MCGILL UNIVERSITY   (Canada)

^d MCGILL UNIVERSITY   (Canada)

^e NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON INDUCED TRANSMEMBRANE 2 PROTEIN; INTERFERON INDUCED TRANSMEMBRANE 3 PROTEIN; MEMBRANE PROTEIN; MUTANT PROTEIN; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VIRUS GLYCOPROTEIN; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 160; GLYCOPROTEIN GP 41; IFITM2 PROTEIN, HUMAN; IFITM3 PROTEIN, HUMAN; RNA BINDING PROTEIN;

ARTICLE; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INFECTION PREVENTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; T LYMPHOCYTE; VIRION; VIRUS CELL INTERACTION; VIRUS INHIBITION; VIRUS ISOLATION; CELL COMMUNICATION; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HELA CELL LINE; HOST PATHOGEN INTERACTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; IMMUNOLOGY; JURKAT CELL LINE; METABOLISM; MONONUCLEAR CELL; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION; SIMIAN IMMUNODEFICIENCY VIRUS; VIROLOGY; VIRUS ENTRY;

CELL COMMUNICATION; GENE EXPRESSION REGULATION; HEK293 CELLS; HELA CELLS; HIV ENVELOPE PROTEIN GP120; HIV ENVELOPE PROTEIN GP160; HIV ENVELOPE PROTEIN GP41; HIV-1; HIV-2; HOST-PATHOGEN INTERACTIONS; HUMANS; JURKAT CELLS; LEUKOCYTES, MONONUCLEAR; MEMBRANE PROTEINS; PRIMARY CELL CULTURE; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; SIMIAN IMMUNODEFICIENCY VIRUS; VIRION; VIRUS INTERNALIZATION;

EID: 84943348177     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.08.055     Document Type: Article

References (49)

1. Agosto L.M., Zhong P., Munro J., Mothes W. Highly active antiretroviral therapies are effective against HIV-1 cell-to-cell transmission. PLoS Pathog. 2014, 10:e1003982.
2. Amini-Bavil-Olyaee S., Choi Y.J., Lee J.H., Shi M., Huang I.C., Farzan M., Jung J.U. The antiviral effector IFITM3 disrupts intracellular cholesterol homeostasis to block viral entry. Cell Host Microbe 2013, 13:452-464.
3. Brass A.L., Huang I.C., Benita Y., John S.P., Krishnan M.N., Feeley E.M., Ryan B.J., Weyer J.L., van der Weyden L., Fikrig E., et al. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 2009, 139:1243-1254.
4. Chesarino N.M., McMichael T.M., Hach J.C., Yount J.S. Phosphorylation of the antiviral protein interferon-inducible transmembrane protein 3 (IFITM3) dually regulates its endocytosis and ubiquitination. J. Biol. Chem. 2014, 289:11986-11992.
5. Chutiwitoonchai N., Hiyoshi M., Hiyoshi-Yoshidomi Y., Hashimoto M., Tokunaga K., Suzu S. Characteristics of IFITM, the newly identified IFN-inducible anti-HIV-1 family proteins. Microbes Infect. 2013, 15:280-290.
6. Compton A.A., Bruel T., Porrot F., Mallet A., Sachse M., Euvrard M., Liang C., Casartelli N., Schwartz O. IFITM proteins incorporated into HIV-1 virions impair viral fusion and spread. Cell Host Microbe 2014, 16:736-747.
7. Côté M., Zheng Y.M., Li K., Xiang S.-H., Albritton L.M., Liu S.-L. Critical role of leucine-valine change in distinct low pH requirements for membrane fusion between two related retrovirus envelopes. J. Biol. Chem. 2012, 287:7640-7651.
8. Dale B.M., Alvarez R.A., Chen B.K. Mechanisms of enhanced HIV spread through T-cell virological synapses. Immunol. Rev. 2013, 251:113-124.
9. Desai T.M., Marin M., Chin C.R., Savidis G., Brass A.L., Melikyan G.B. IFITM3 restricts influenza A virus entry by blocking the formation of fusion pores following virus-endosome hemifusion. PLoS Pathog. 2014, 10:e1004048.
10. Diamond M.S., Farzan M. The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat. Rev. Immunol. 2013, 13:46-57.
11. Ding S., Pan Q., Liu S.L., Liang C. HIV-1 mutates to evade IFITM1 restriction. Virology 2014, 454-455:11-24.
12. Freed E.O., Martin M.A. HIV-1 infection of non-dividing cells. Nature 1994, 369:107-108.
13. Freed E.O., Martin M.A. Domains of the human immunodeficiency virus type 1 matrix and gp41 cytoplasmic tail required for envelope incorporation into virions. J. Virol. 1996, 70:341-351.
14. Goujon C., Moncorgé O., Bauby H., Doyle T., Ward C.C., Schaller T., Hué S., Barclay W.S., Schulz R., Malim M.H. Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection. Nature 2013, 502:559-562.
15. Hrecka K., Hao C., Gierszewska M., Swanson S.K., Kesik-Brodacka M., Srivastava S., Florens L., Washburn M.P., Skowronski J. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 2011, 474:658-661.
16. Huang I.C., Bailey C.C., Weyer J.L., Radoshitzky S.R., Becker M.M., Chiang J.J., Brass A.L., Ahmed A.A., Chi X., Dong L., et al. Distinct patterns of IFITM-mediated restriction of filoviruses, SARS coronavirus, and influenza A virus. PLoS Pathog. 2011, 7:e1001258.
17. Jia R., Pan Q., Ding S., Rong L., Liu S.L., Geng Y., Qiao W., Liang C. The N-terminal region of IFITM3 modulates its antiviral activity by regulating IFITM3 cellular localization. J. Virol. 2012, 86:13697-13707.
18. Jia R., Xu F., Qian J., Yao Y., Miao C., Zheng Y.M., Liu S.L., Guo F., Geng Y., Qiao W., Liang C. Identification of an endocytic signal essential for the antiviral action of IFITM3. Cell. Microbiol. 2014, 16:1080-1093.
19. Jiang D., Weidner J.M., Qing M., Pan X.B., Guo H., Xu C., Zhang X., Birk A., Chang J., Shi P.Y., et al. Identification of five interferon-induced cellular proteins that inhibit west nile virus and dengue virus infections. J. Virol. 2010, 84:8332-8341.
20. Kane M., Yadav S.S., Bitzegeio J., Kutluay S.B., Zang T., Wilson S.J., Schoggins J.W., Rice C.M., Yamashita M., Hatziioannou T., Bieniasz P.D. MX2 is an interferon-induced inhibitor of HIV-1 infection. Nature 2013, 502:563-566.
21. LaBranche C.C., Sauter M.M., Haggarty B.S., Vance P.J., Romano J., Hart T.K., Bugelski P.J., Marsh M., Hoxie J.A. A single amino acid change in the cytoplasmic domain of the simian immunodeficiency virus transmembrane molecule increases envelope glycoprotein expression on infected cells. J. Virol. 1995, 69:5217-5227.
22. Laguette N., Sobhian B., Casartelli N., Ringeard M., Chable-Bessia C., Ségéral E., Yatim A., Emiliani S., Schwartz O., Benkirane M. SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 2011, 474:654-657.
23. Li K., Markosyan R.M., Zheng Y.-M., Golfetto O., Bungart B., Li M., Ding S., He Y., Liang C., Lee J.C., et al. IFITM proteins restrict viral membrane hemifusion. PLoS Pathog. 2013, 9:e1003124.
24. Li M., Ablan S.D., Miao C., Zheng Y.M., Fuller M.S., Rennert P.D., Maury W., Johnson M.C., Freed E.O., Liu S.L. TIM-family proteins inhibit HIV-1 release. Proc. Natl. Acad. Sci. USA 2014, 111:E3699-E3707.
25. Li K., Jia R., Li M., Zheng Y.M., Miao C., Yao Y., Ji H.L., Geng Y., Qiao W., Albritton L.M., et al. A sorting signal suppresses IFITM1 restriction of viral entry. J. Biol. Chem. 2015, 290:4248-4259.
26. Lin T.Y., Chin C.R., Everitt A.R., Clare S., Perreira J.M., Savidis G., Aker A.M., John S.P., Sarlah D., Carreira E.M., et al. Amphotericin B increases influenza A virus infection by preventing IFITM3-mediated restriction. Cell Rep. 2013, 5:895-908.
27. Liu S.-L., Lerman M.I., Miller A.D. Putative phosphatidylinositol 3-kinase (PI3K) binding motifs in ovine betaretrovirus Env proteins are not essential for rodent fibroblast transformation and PI3K/Akt activation. J. Virol. 2003, 77:7924-7935.
28. Liu Z., Pan Q., Ding S., Qian J., Xu F., Zhou J., Cen S., Guo F., Liang C. The interferon-inducible MxB protein inhibits HIV-1 infection. Cell Host Microbe 2013, 14:398-410.
29. Lu J., Pan Q., Rong L., He W., Liu S.L., Liang C. The IFITM proteins inhibit HIV-1 infection. J. Virol. 2011, 85:2126-2137.
30. Mazurov D., Ilinskaya A., Heidecker G., Lloyd P., Derse D. Quantitative comparison of HTLV-1 and HIV-1 cell-to-cell infection with new replication dependent vectors. PLoS Pathog. 2010, 6:e1000788.
31. Murakami T., Freed E.O. The long cytoplasmic tail of gp41 is required in a cell type-dependent manner for HIV-1 envelope glycoprotein incorporation into virions. Proc. Natl. Acad. Sci. USA 2000, 97:343-348.
32. Neil S.J., Zang T., Bieniasz P.D. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 2008, 451:425-430.
33. Perreira J.M., Chin C.R., Feeley E.M., Brass A.L. IFITMs restrict the replication of multiple pathogenic viruses. J. Mol. Biol. 2013, 425:4937-4955.
34. Puryear W.B., Akiyama H., Geer S.D., Ramirez N.P., Yu X., Reinhard B.M., Gummuluru S. Interferon-inducible mechanism of dendritic cell-mediated HIV-1 dissemination is dependent on Siglec-1/CD169. PLoS Pathog. 2013, 9:e1003291.
35. Roy N.H., Lambelé M., Chan J., Symeonides M., Thali M. Ezrin is a component of the HIV-1 virological presynapse and contributes to the inhibition of cell-cell fusion. J. Virol. 2014, 88:7645-7658.
36. Sadler A.J., Williams B.R. Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 2008, 8:559-568.
37. Schoggins J.W., Wilson S.J., Panis M., Murphy M.Y., Jones C.T., Bieniasz P., Rice C.M. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 2011, 472:481-485.
38. 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 2002, 418:646-650.
39. Smith S., Weston S., Kellam P., Marsh M. IFITM proteins-cellular inhibitors of viral entry. Curr. Opin. Virol. 2014, 4:71-77.
40. Stremlau M., Owens C.M., Perron M.J., Kiessling M., Autissier P., Sodroski J. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 2004, 427:848-853.
41. Swartz T.H., Esposito A.M., Durham N.D., Hartmann B.M., Chen B.K. P2X-selective purinergic antagonists are strong inhibitors of HIV-1 fusion during both cell-to-cell and cell-free infection. J. Virol. 2014, 88:11504-11515.
42. Tartour K., Appourchaux R., Gaillard J., Nguyen X.N., Durand S., Turpin J., Beaumont E., Roch E., Berger G., Mahieux R., et al. IFITM proteins are incorporated onto HIV-1 virion particles and negatively imprint their infectivity. Retrovirology 2014, 11:103.
43. Van Damme N., Goff D., Katsura C., Jorgenson R.L., Mitchell R., Johnson M.C., Stephens E.B., Guatelli J. 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 2008, 3:245-252.
44. Weidner J.M., Jiang D., Pan X.B., Chang J., Block T.M., Guo J.T. Interferon-induced cell membrane proteins, IFITM3 and tetherin, inhibit vesicular stomatitis virus infection via distinct mechanisms. J. Virol. 2010, 84:12646-12657.
45. Wen X., Ding L., Wang J.J., Qi M., Hammonds J., Chu H., Chen X., Hunter E., Spearman P. ROCK1 and LIM kinase modulate retrovirus particle release and cell-cell transmission events. J. Virol. 2014, 88:6906-6921.
46. Yount J.S., Karssemeijer R.A., Hang H.C. S-palmitoylation and ubiquitination differentially regulate interferon-induced transmembrane protein 3 (IFITM3)-mediated resistance to influenza virus. J. Biol. Chem. 2012, 287:19631-19641.
47. Zhao X., Guo F., Liu F., Cuconati A., Chang J., Block T.M., Guo J.T. Interferon induction of IFITM proteins promotes infection by human coronavirus OC43. Proc. Natl. Acad. Sci. USA 2014, 111:6756-6761.
48. Zhong P., Agosto L.M., Munro J.B., Mothes W. Cell-to-cell transmission of viruses. Curr. Opin. Virol. 2013, 3:44-50.
49. Zhu X., He Z., Yuan J., Wen W., Huang X., Hu Y., Lin C., Pan J., Li R., Deng H., et al. IFITM3-containing exosome as a novel mediator for anti-viral response in dengue virus infection. Cell. Microbiol. 2015, 17:105-118.