Cell-to-Cell Transmission of HIV-1 Is Required to Trigger Pyroptotic Death of Lymphoid-Tissue-Derived CD4 T Cells

Cell Reports

Volumn 12, Issue 10, 2015, Pages 1555-1563

  Galloway, Nicole L K ^a   Doitsh, Gilad ^a   Monroe, Kathryn M ^a   Yang, Zhiyuan ^a   Muñoz Arias, Isa ^a   Levy, David N ^b   Greene, Warner C ^a,c  

^a GLADSTONE INSTITUTE OF VIROLOGY AND IMMUNOLOGY   (United States)

^b NEW YORK UNIVERSITY COLLEGE OF DENTISTRY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA CONVERTING ENZYME; LACTATE DEHYDROGENASE; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; VIRUS DNA; CELL ADHESION MOLECULE;

ANTIGEN RECOGNITION; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ADHESION; CELL SURVIVAL; CELL TO CELL TRANSMISSION; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; DISEASE COURSE; ENZYME ACTIVATION; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INNATE IMMUNITY; INOCULATION; LYMPHOID TISSUE; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYROPTOTIC DEATH; SPINOCULATION; VIRAL PHENOMENA AND FUNCTIONS; VIRION; VIROLOGICAL SYNAPSE; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS TRANSMISSION; CELL CULTURE; COCULTURE; HUMAN; METABOLISM; PATHOLOGY; PHYSIOLOGY; TRANSMISSION; VIROLOGY;

APOPTOSIS; CASPASE 1; CD4-POSITIVE T-LYMPHOCYTES; CELL ADHESION MOLECULES; CELLS, CULTURED; COCULTURE TECHNIQUES; HIV INFECTIONS; HIV-1; HUMANS; LYMPHOID TISSUE;

EID: 84941182496     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.08.011     Document Type: Article

References (53)

1. Agosto L.M., Uchil P.D., Mothes W. HIV cell-to-cell transmission: effects on pathogenesis and antiretroviral therapy. Trends Microbiol. 2015, 23:289-295.
2. Bounou S., Leclerc J.E., Tremblay M.J. Presence of host ICAM-1 in laboratory and clinical strains of human immunodeficiency virus type 1 increases virus infectivity and CD4(+)-T-cell depletion in human lymphoid tissue, a major site of replication in vivo. J. Virol. 2002, 76:1004-1014.
3. Cooper A., García M., Petrovas C., Yamamoto T., Koup R.A., Nabel G.J. HIV-1 causes CD4 cell death through DNA-dependent protein kinase during viral integration. Nature 2013, 498:376-379.
4. Cummins N.W., Badley A.D. Mechanisms of HIV-associated lymphocyte apoptosis: 2010. Cell Death Dis. 2010, 1:e99.
5. Decker T., Lohmann-Matthes M.L. A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. J. Immunol. Methods 1988, 115:61-69.
6. Deeks S.G. HIV infection, inflammation, immunosenescence, and aging. Annu. Rev. Med. 2011, 62:141-155.
7. Dinarello C.A. Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 2009, 27:519-550.
8. Doitsh G., Cavrois M., Lassen K.G., Zepeda O., Yang Z., Santiago M.L., Hebbeler A.M., Greene W.C. Abortive HIV infection mediates CD4 T cell depletion and inflammation in human lymphoid tissue. Cell 2010, 143:789-801.
9. Doitsh G., Galloway N.L., Geng X., Yang Z., Monroe K.M., Zepeda O., Hunt P.W., Hatano H., Sowinski S., Muñoz-Arias I., Greene W.C. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 2014, 505:509-514.
10. Dustin M.L., Rothlein R., Bhan A.K., Dinarello C.A., Springer T.A. Induction by IL 1 and interferon-γ: tissue distribution, biochemistry, and function of a natural adherence molecule (ICAM-1). J. Immunol. 1986. 137: 245-254. J. Immunol. 2011, 186:5024-5033.
11. Eckstein D.A., Penn M.L., Korin Y.D., Scripture-Adams D.D., Zack J.A., Kreisberg J.F., Roederer M., Sherman M.P., Chin P.S., Goldsmith M.A. HIV-1 actively replicates in naive CD4(+) T cells residing within human lymphoid tissues. Immunity 2001, 15:671-682.
12. Février M., Dorgham K., Rebollo A. CD4+ T cell depletion in human immunodeficiency virus (HIV) infection: role of apoptosis. Viruses 2011, 3:586-612.
13. Fink S.L., Cookson B.T. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect. Immun. 2005, 73:1907-1916.
14. Finkel T.H., Tudor-Williams G., Banda N.K., Cotton M.F., Curiel T., Monks C., Baba T.W., Ruprecht R.M., Kupfer A. Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV- and SIV-infected lymph nodes. Nat. Med. 1995, 1:129-134.
15. Fortin J.F., Cantin R., Lamontagne G., Tremblay M. Host-derived ICAM-1 glycoproteins incorporated on human immunodeficiency virus type 1 are biologically active and enhance viral infectivity. J. Virol. 1997, 71:3588-3596.
16. Gao D., Wu J., Wu Y.T., Du F., Aroh C., Yan N., Sun L., Chen Z.J. Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 2013, 341:903-906.
17. Garg H., Joshi A., Freed E.O., Blumenthal R. Site-specific mutations in HIV-1 gp41 reveal a correlation between HIV-1-mediated bystander apoptosis and fusion/hemifusion. J. Biol. Chem. 2007, 282:16899-16906.
18. Garg H., Mohl J., Joshi A. HIV-1 induced bystander apoptosis. Viruses 2012, 4:3020-3043.
19. Gelderblom H.C., Vatakis D.N., Burke S.A., Lawrie S.D., Bristol G.C., Levy D.N. Viral complementation allows HIV-1 replication without integration. Retrovirology 2008, 5:60.
20. Geng X., Doitsh G., Yang Z., Galloway N.L., Greene W.C. Efficient delivery of lentiviral vectors into resting human CD4 T cells. Gene Ther. 2014, 21:444-449.
21. Girard J.P., Moussion C., Förster R. HEVs, lymphatics and homeostatic immune cell trafficking in lymph nodes. Nat. Rev. Immunol. 2012, 12:762-773.
22. Glushakova S., Baibakov B., Margolis L.B., Zimmerberg J. Infection of human tonsil histocultures: a model for HIV pathogenesis. Nat. Med. 1995, 1:1320-1322.
23. Gougeon M.L., Lecoeur H., Dulioust A., Enouf M.G., Crouvoiser M., Goujard C., Debord T., Montagnier L. Programmed cell death in peripheral lymphocytes from HIV-infected persons: increased susceptibility to apoptosis of CD4 and CD8 T cells correlates with lymphocyte activation and with disease progression. J. Immunol. 1996, 156:3509-3520.
24. Hayashi T., Nishitsuji H., Takamori A., Hasegawa A., Masuda T., Kannagi M. DNA-dependent activator of IFN-regulatory factors enhances the transcription of HIV-1 through NF-kappaB. Microbes Infect. 2010, 12:937-947.
25. Holm G.H., Gabuzda D. Distinct mechanisms of CD4+ and CD8+ T-cell activation and bystander apoptosis induced by human immunodeficiency virus type 1 virions. J. Virol. 2005, 79:6299-6311.
26. Hubbard A.K., Rothlein R. Intercellular adhesion molecule-1 (ICAM-1) expression and cell signaling cascades. Free Radic. Biol. Med. 2000, 28:1379-1386.
27. Jakobsen M.R., Bak R.O., Andersen A., Berg R.K., Jensen S.B., Tengchuan J., Laustsen A., Hansen K., Ostergaard L., Fitzgerald K.A., et al. IFI16 senses DNA forms of the lentiviral replication cycle and controls HIV-1 replication. Proc. Natl. Acad. Sci. USA 2013, 110:E4571-E4580.
28. Jekle A., Keppler O.T., De Clercq E., Schols D., Weinstein M., Goldsmith M.A. In vivo evolution of human immunodeficiency virus type 1 toward increased pathogenicity through CXCR4-mediated killing of uninfected CD4 T cells. J. Virol. 2003, 77:5846-5854.
29. Jolly C. Cell-to-cell transmission of retroviruses: Innate immunity and interferon-induced restriction factors. Virology 2011, 411:251-259.
30. Jolly C., Sattentau Q.J. Retroviral spread by induction of virological synapses. Traffic 2004, 5:643-650.
31. Jolly C., Kashefi K., Hollinshead M., Sattentau Q.J. HIV-1 cell to cell transfer across an Env-induced, actin-dependent synapse. J. Exp. Med. 2004, 199:283-293.
32. Jolly C., Mitar I., Sattentau Q.J. Adhesion molecule interactions facilitate human immunodeficiency virus type 1-induced virological synapse formation between T cells. J. Virol. 2007, 81:13916-13921.
33. Komoriya A., Packard B.Z., Brown M.J., Wu M.L., Henkart P.A. Assessment of caspase activities in intact apoptotic thymocytes using cell-permeable fluorogenic caspase substrates. J. Exp. Med. 2000, 191:1819-1828.
34. Laguette N., Brégnard C., Hue P., Basbous J., Yatim A., Larroque M., Kirchhoff F., Constantinou A., Sobhian B., Benkirane M. Premature activation of the SLX4 complex by Vpr promotes G2/M arrest and escape from innate immune sensing. Cell 2014, 156:134-145.
35. Lahaye X., Satoh T., Gentili M., Cerboni S., Conrad C., Hurbain I., El Marjou A., Lacabaratz C., Lelièvre J.D., Manel N. The capsids of HIV-1 and HIV-2 determine immune detection of the viral cDNA by the innate sensor cGAS in dendritic cells. Immunity 2013, 39:1132-1142.
36. Lehmann M., Nikolic D.S., Piguet V. How HIV-1 takes advantage of the cytoskeleton during replication and cell-to-cell transmission. Viruses 2011, 3:1757-1776.
37. Levy D.N., Aldrovandi G.M., Kutsch O., Shaw G.M. Dynamics of HIV-1 recombination in its natural target cells. Proc. Natl. Acad. Sci. USA 2004, 101:4204-4209.
38. Manel N., Hogstad B., Wang Y., Levy D.E., Unutmaz D., Littman D.R. A cryptic sensor for HIV-1 activates antiviral innate immunity in dendritic cells. Nature 2010, 467:214-217.
39. Martin N., Sattentau Q. Cell-to-cell HIV-1 spread and its implications for immune evasion. Curr. Opin. HIV AIDS 2009, 4:143-149.
40. Monroe K.M., Yang Z., Johnson J.R., Geng X., Doitsh G., Krogan N.J., Greene W.C. IFI16 DNA sensor is required for death of lymphoid CD4 T cells abortively infected with HIV. Science 2014, 343:428-432.
41. Moore J.P., Kitchen S.G., Pugach P., Zack J.A. The CCR5 and CXCR4 coreceptors--central to understanding the transmission and pathogenesis of human immunodeficiency virus type 1 infection. AIDS Res. Hum. Retroviruses 2004, 20:111-126.
42. O'Doherty U., Swiggard W.J., Malim M.H. Human immunodeficiency virus type 1 spinoculation enhances infection through virus binding. J. Virol. 2000, 74:10074-10080.
43. Pace M.J., Graf E.H., Agosto L.M., Mexas A.M., Male F., Brady T., Bushman F.D., O'Doherty U. Directly infected resting CD4+T cells can produce HIV Gag without spreading infection in a model of HIV latency. PLoS Pathog. 2012, 8:e1002818.
44. Packard B.Z., Komoriya A. A method in enzymology for measuring hydrolytic activities in live cell environments. Methods Enzymol. 2008, 450:1-19.
45. Phillips D.M. The role of cell-to-cell transmission in HIV infection. AIDS 1994, 8:719-731.
46. Saphire A.C., Bobardt M.D., Gallay P.A. Cyclophilin a plays distinct roles in human immunodeficiency virus type 1 entry and postentry events, as revealed by spinoculation. J. Virol. 2002, 76:4671-4677.
47. Sato H., Orenstein J., Dimitrov D., Martin M. Cell-to-cell spread of HIV-1 occurs within minutes and may not involve the participation of virus particles. Virology 1992, 186:712-724.
48. Sattentau Q.J. Cell-to-Cell Spread of Retroviruses. Viruses 2010, 2:1306-1321.
49. Sourisseau M., Sol-Foulon N., Porrot F., Blanchet F., Schwartz O. Inefficient human immunodeficiency virus replication in mobile lymphocytes. J. Virol. 2007, 81:1000-1012.
50. Stetson D.B., Ko J.S., Heidmann T., Medzhitov R. Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 2008, 134:587-598.
51. Sun L., Wu J., Du F., Chen X., Chen Z.J. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 2013, 339:786-791.
52. Thomas C. Roadblocks in HIV research: five questions. Nat. Med. 2009, 15:855-859.
53. Yan N., Regalado-Magdos A.D., Stiggelbout B., Lee-Kirsch M.A., Lieberman J. The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat. Immunol. 2010, 11:1005-1013.