Sensing of HIV-1 entry triggers a type I interferon response in human primary macrophages

Journal of Virology

Volumn 91, Issue 15, 2017, Pages

  Decalf, Jérémie ^a   Desdouits, Marion ^a   Rodrigues, Vasco ^a   Gobert, François Xavier ^a   Gentili, Matteo ^a   Marques Ladeira, Santy ^a   Chamontin, Célia ^b   Mougel, Marylène ^b   de Alencar, Bruna Cunha ^a,c   Benaroch, Philippe ^a  

^a PSL RESEARCH UNIVERSITY   (France)

^b UNIV MONTPELLIER   (France)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Human immunodeficiency virus; Innate immunity; Interferons; Macrophages; Virus entry

Indexed keywords

INTERFERON; TBK1 PROTEIN; UNCLASSIFIED DRUG; VIRAL PROTEIN; VIRUS ENVELOPE PROTEIN; VIRUS RNA; PROTEIN SERINE THREONINE KINASE; TBK1 PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INTRACELLULAR SIGNALING; MACROPHAGE; MONOCYTE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; VIRUS CELL INTERACTION; VIRUS DETECTION; VIRUS ENTRY; VIRUS GENOME; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TRANSMISSION; CELL CULTURE; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; PHYSIOLOGY; TIME FACTOR; VIROLOGY;

CELLS, CULTURED; HIV-1; HUMANS; IMMUNITY, INNATE; INTERFERON TYPE I; MACROPHAGES; PROTEIN-SERINE-THREONINE KINASES; TIME FACTORS; VIRUS INTERNALIZATION;

EID: 85023187640     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00147-17     Document Type: Article

References (56)

1. Price JV, Vance RE. 2014. The macrophage paradox. Immunity 41: 685-693. https://doi.org/10.1016/j.immuni.2014.10.015
2. Orenstein JM, Fox C, Wahl SM. 1997. Macrophages as a source of HIV during opportunistic infections. Science 276:1857-1861. https://doi.org/ 10.1126/science.276.5320.1857
3. Sattentau QJ, Stevenson M. 2016. Macrophages and HIV-1: an unhealthy constellation. Cell Host Microbe 19:304-310. https://doi.org/10.1016/j.chom.2016.02.013
4. Gartner S, Markovits P, Markovitz D, Kaplan M, Gallo R, Popovic M. 1986. The role of mononuclear phagocytes in HTLV-III/LAV infection. Science 233:215-219. https://doi.org/10.1126/science.3014648
5. Gaudin R, Berre S, Cunha de Alencar B, Decalf J, Schindler M, Gobert F-X, Jouve M, Benaroch P. 2013. Dynamics of HIV-containing compartments in macrophages reveal sequestration of virions and transient surface connections. PLoS One 8:e69450. https://doi.org/10.1371/journal.pone.0069450
6. Benaroch P, Billard E, Gaudin R, Schindler M, Jouve M. 2010. HIV-1 assembly in macrophages. Retrovirology 7:29. https://doi.org/10.1186/ 1742-4690-7-29
7. Lorenzo-Redondo R, Fryer HR, Bedford T, Kim E-Y, Archer J, Kosakovsky Pond SL, Chung Y-S, Penugonda S, Chipman JG, Fletcher CV, Schacker TW, Malim MH, Rambaut A, Haase AT, McLean AR, Wolinsky SM. 2016. Persistent HIV-1 replication maintains the tissue reservoir during therapy. Nature 530:51-56. https://doi.org/10.1038/nature16933
8. Honeycutt JB, Wahl A, Baker C, Spagnuolo RA, Foster J, Zakharova O, Wietgrefe S, Caro-Vegas C, Madden V, Sharpe G, Haase AT, Eron JJ, Garcia JV. 2016. Macrophages sustain HIV replication in vivo independently of T cells. J Clin Investig 126:1353-1366. https://doi.org/10.1172/JCI84456
9. Honeycutt JB, Thayer WO, Baker CE, Ribeiro RM, Lada SM, Cao Y, Cleary RA, Hudgens MG, Richman DD, Garcia JV. 2017. HIV persistence in tissue macrophages of humanized myeloid-only mice during antiretroviral therapy. Nat Med 308:387
10. Iwasaki A. 2012. Innate immune recognition of HIV-1. Immunity 37: 389-398. https://doi.org/10.1016/j.immuni.2012.08.011
11. Lahaye X, Manel N. 2015. Viral and cellular mechanisms of the innate immune sensing of HIV. Curr Opin Virol 11C:55-62. https://doi.org/10.1016/j.coviro.2015.01.013
12. Lahaye X, Satoh T, Gentili M, Cerboni S, Conrad C, Hurbain I, Marjou El A, Lacabaratz C, Lelièvre J-D, Manel N. 2013. The capsids of HIV-1 and HIV-2 determine immune detection of the viral cDNA by the innate sensor cGAS in dendritic cells. Immunity 39:1132-1142. https://doi.org/ 10.1016/j.immuni.2013.11.002
13. Rasaiyaah J, Tan CP, Fletcher AJ, Price AJ, Blondeau C, Hilditch L, Jacques DA, Selwood DL, James LC, Noursadeghi M, Towers GJ. 2013. HIV-1 evades innate immune recognition through specific cofactor recruitment. Nature 503:402-405. https://doi.org/10.1038/nature12769
14. Laguette N, Sobhian B, Casartelli N, Ringeard M, Chable-Bessia C, Ségéral E, Yatim A, Emiliani S, Schwartz O, Benkirane M. 2011. SAMHD1 is the dendritic-and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 474:654-657. https://doi.org/10.1038/nature10117
15. Hrecka K, Hao C, Gierszewska M, Swanson SK, Kesik-Brodacka M, Srivastava S, Florens L, Washburn MP, Skowronski J. 2011. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 474:658-661. https://doi.org/10.1038/nature10195
16. Lahouassa H, Daddacha W, Hofmann H, Ayinde D, Logue EC, Dragin L, Bloch N, Maudet C, Bertrand M, Gramberg T, Pancino G, Priet S, Canard B, Laguette N, Benkirane M, Transy C, Landau NR, Kim B, Margottin-Goguet F. 2012. SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates. Nat Immunol 13:223-228. https://doi.org/10.1038/ni.2236
17. Gao D, Wu J, Wu Y-T, Du F, Aroh C, Yan N, Sun L, Chen ZJ. 2013. Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 341:903-906. https://doi.org/10.1126/science.1240933
18. Yan N, Regalado-Magdos AD, Stiggelbout B, Lee-Kirsch MA, Lieberman J. 2010. The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat Immunol 11: 1005-1013. https://doi.org/10.1038/ni.1941
19. Nasr N, Maddocks S, Turville SG, Harman AN, Woolger N, Helbig KJ, Wilkinson J, Bye CR, Wright TK, Rambukwelle D, Donaghy H, Beard MR, Cunningham AL. 2012. HIV-1 infection of human macrophages directly induces viperin which inhibits viral production. Blood 120:778-788. https://doi.org/10.1182/blood-2012-01-407395
20. Woelk CH, Ottones F, Plotkin CR, Du P, Royer CD, Rought SE, Lozach J, Sasik R, Kornbluth RS, Richman DD, Corbeil J. 2004. Interferon gene expression following HIV type 1 infection of monocyte-derived macrophages. AIDS Res Hum Retrovir 20:1210-1222. https://doi.org/10.1089/ aid.2004.20.1210
21. Coberley CR, Kohler JJ, Brown JN, Oshier JT, Baker HV, Popp MP, Sleasman JW, Goodenow MM. 2004. Impact on genetic networks in human macrophages by a CCR5 strain of human immunodeficiency virus type 1. J Virol 78:11477-11486. https://doi.org/10.1128/JVI.78.21.11477-11486.2004
22. Diget EA, Zuwala K, Berg RK, Laursen RR, Søby S, stergaard L, Melchjorsen J, Mogensen TH. 2013. Characterization of HIV-1 infection and innate sensing in different types of primary human monocyte-derived macrophages. Mediators Inflamm 2013:1-11
23. Jakobsen MR, Bak RO, Andersen A, Berg RK, Jensen SB, Tengchuan J, Jin T, Laustsen A, Hansen K, Ostergaard L, Fitzgerald KA, Xiao TS, Mikkelsen JG, Mogensen TH, Paludan SR. 2013. IFI16 senses DNA forms of the lentiviral replication cycle and controls HIV-1 replication. Proc Natl Acad Sci U S A 110:E4571-E4580. https://doi.org/10.1073/pnas.1311669110
24. Schoggins JW, Rice CM. 2011. Interferon-stimulated genes and their antiviral effector functions. Curr Opin Virol 1:519-525. https://doi.org/ 10.1016/j.coviro.2011.10.008
25. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, Rice CM. 2011. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472:481-485. https://doi.org/10.1038/nature09907
26. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102:15545-15550. https://doi.org/10.1073/pnas.0506580102
27. Mootha VK, Lindgren CM, Eriksson K-F, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstråle M, Laurila E, Houstis N, Daly MJ, Patterson N, Mesirov JP, Golub TR, Tamayo P, Spiegelman B, Lander ES, Hirschhorn JN, Altshuler D, Groop LC. 2003. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34:267-273. https://doi.org/10.1038/ng1180
28. Rossio JL, Esser MT, Suryanarayana K, Schneider DK, Bess JW, Vasquez GM, Wiltrout TA, Chertova E, Grimes MK, Sattentau Q, Arthur LO, Henderson LE, Lifson JD. 1998. Inactivation of human immunodeficiency virus type 1 infectivity with preservation of conformational and functional integrity of virion surface proteins. J Virol 72:7992-8001
29. Hooker CW, Lott WB, Harrich D. 2001. Inhibitors of human immunodeficiency virus type 1 reverse transcriptase target distinct phases of early reverse transcription. J Virol 75:3095-3104. https://doi.org/10.1128/JVI.75.7.3095-3104.2001
30. Lepelley A, Louis S, Sourisseau M, Law HKW, Pothlichet J, Schilte C, Chaperot L, Plumas J, Randall RE, Si-Tahar M, Mammano F, Albert ML, Schwartz O. 2011. Innate sensing of HIV-infected cells. PLoS Pathog 7:e1001284. https://doi.org/10.1371/journal.ppat.1001284
31. Pichlmair A, Diebold SS, Gschmeissner S, Takeuchi Y, Ikeda Y, Collins MK, Reis e Sousa C. 2007. Tubulovesicular structures within vesicular stomatitis virus G protein-pseudotyped lentiviral vector preparations carry DNA and stimulate antiviral responses via Toll-like receptor 9. J Virol 81:539-547. https://doi.org/10.1128/JVI.01818-06
32. Lau L, Gray EE, Brunette RL, Stetson DB. 2015. DNA tumor virus oncogenes antagonize the cGAS-STING DNA-sensing pathway. Science 350: 568-571. https://doi.org/10.1126/science.aab3291
33. Gentili M, Kowal J, Tkach M, Satoh T, Lahaye X, Conrad C, Boyron M, Lombard B, Durand S, Kroemer G, Loew D, Dalod M, Théry C, Manel N. 2015. Transmission of innate immune signaling by packaging of cGAMP in viral particles. Science 349:1232-1236. https://doi.org/10.1126/science.aab3628
34. Reimer T, Brcic M, Schweizer M, Jungi TW. 2008. Poly(I:C) and LPS induce distinct IRF3 and NF-κB signaling during type-I IFN and TNF responses in human macrophages. J Leukoc Biol 83:1249-1257. https://doi.org/10.1189/jlb.0607412
35. Gough DJ, Messina NL, Clarke CJP, Johnstone RW, Levy DE. 2012. Constitutive type I interferon modulates homeostatic balance through tonic signaling. Immunity 36:166-174. https://doi.org/10.1016/j.immuni.2012.01.011
36. Clark K, Plater L, Peggie M, Cohen P. 2009. Use of the pharmacological inhibitor BX795 to study the regulation and physiological roles of TBK1 and IkappaB kinase epsilon: a distinct upstream kinase mediates Ser-172 phosphorylation and activation. J Biol Chem 284:14136-14146. https:// doi.org/10.1074/jbc.M109.000414
37. Manel N, Hogstad B, Wang Y, Levy DE, Unutmaz D, Littman DR. 2010. A cryptic sensor for HIV-1 activates antiviral innate immunity in dendritic cells. Nature 467:214-217. https://doi.org/10.1038/nature09337
38. Matthews T, Salgo M, Greenberg M, Chung J, DeMasi R, Bolognesi D. 2004. Case history. Enfuvirtide: the first therapy to inhibit the entry of HIV-1 into host CD4 lymphocytes. Nat Rev Drug Discov 3:215-225
39. Harman AN, Nasr N, Feetham A, Galoyan A, Alshehri AA, Rambukwelle D, Botting RA, Hiener BM, Diefenbach E, Diefenbach RJ, Kim M, Mansell A, Cunningham AL. 2015. HIV blocks interferon induction in human dendritic cells and macrophages by dysregulation of TBK1. J Virol 89: 6575-6584. https://doi.org/10.1128/JVI.00889-15
40. Pertel T, Hausmann S, Morger D, Züger S, Guerra J, Lascano J, Reinhard C, Santoni FA, Uchil PD, Chatel L, Bisiaux A, Albert ML, Strambio-De-Castillia C, Mothes W, Pizzato M, Grütter MG, Luban J. 2011. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 472: 361-365. https://doi.org/10.1038/nature09976
41. Boelens MC, Wu TJ, Nabet BY, Xu B, Qiu Y, Yoon T, Azzam DJ, Twyman-Saint Victor C, Wiemann BZ, Ishwaran H, Brugge Ter PJ, Jonkers J, Slingerland J, Minn AJ. 2014. Exosome transfer from stromal to breast cancer cells regulates therapy resistance pathways. Cell 159:499-513. https://doi.org/10.1016/j.cell.2014.09.051
42. Jouvenet N, Lainé S, Pessel-Vivares L, Mougel M. 2011. Cell biology of retroviral RNA packaging. RNA Biol 8:572-580. https://doi.org/10.4161/ rna.8.4.16030
43. Holm CK, Jensen SB, Jakobsen MR, Cheshenko N, Horan KA, Moeller HB, Gonzalez-Dosal R, Rasmussen SB, Christensen MH, Yarovinsky TO, Rixon FJ, Herold BC, Fitzgerald KA, Paludan SR. 2012. Virus-cell fusion as a trigger of innate immunity dependent on the adaptor STING. Nat Immunol 13:737-743. https://doi.org/10.1038/ni.2350
44. Noyce RS, Taylor K, Ciechonska M, Collins SE, Duncan R, Mossman KL. 2011. Membrane perturbation elicits an IRF3-dependent, interferonindependent antiviral response. J Virol 85:10926-10931. https://doi.org/ 10.1128/JVI.00862-11
45. Holm CK, Rahbek SH, Gad HH, Bak RO, Jakobsen MR, Jiang Z, Hansen AL, Jensen SK, Sun C, Thomsen MK, Laustsen A, Nielsen CG, Severinsen K, Xiong Y, Burdette DL, Hornung V, Lebbink RJ, Duch M, Fitzgerald KA, Bahrami S, Mikkelsen JG, Hartmann R, Paludan SR. 2016. Influenza A virus targets a cGAS-independent STING pathway that controls enveloped RNA viruses. Nat Commun 7:10680. https://doi.org/10.1038/ncomms10680
46. Thomas JA, Ott DE, Gorelick RJ. 2007. Efficiency of human immunodeficiency virus type 1 postentry infection processes: evidence against disproportionate numbers of defective virions. J Virol 81:4367-4370. https://doi.org/10.1128/JVI.02357-06
47. Miyauchi K, Kim Y, Latinovic O, Morozov V, Melikyan GB. 2009. HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 137:433-444. https://doi.org/10.1016/j.cell.2009.02.046
48. Maréchal V, Prevost MC, Petit C, Perret E, Heard JM, Schwartz O. 2001. Human immunodeficiency virus type 1 entry into macrophages mediated by macropinocytosis. J Virol 75:11166-11177. https://doi.org/10.1128/JVI.75.22.11166-11177.2001
49. Li Q, Li W, Yin W, Guo J, Zhang Z-P, Zeng D, Zhang X, Wu Y, Zhang X-E, Cui Z. 2017. Single-particle tracking of human immunodeficiency virus type 1 productive entry into human primary macrophages. ACS Nano 11:3890-3903. https://doi.org/10.1021/acsnano.7b00275
50. Freed EO, Englund G, Martin MA. 1995. Role of the basic domain of human immunodeficiency virus type 1 matrix in macrophage infection. J Virol 69:3949-3954
51. Simon-Loriere E, Galetto R, Hamoudi M, Archer J, Lefeuvre P, Martin DP, Robertson DL, Negroni M. 2009. Molecular mechanisms of recombination restriction in the envelope gene of the human immunodeficiency virus. PLoS Pathog 5:e1000418. https://doi.org/10.1371/journal.ppat.1000418
52. Kauffmann A, Gentleman R, Huber W. 2009. arrayQualityMetrics-a bioconductor package for quality assessment of microarray data. Bioinformatics 25:415-416. https://doi.org/10.1093/bioinformatics/btn647
53. Gautier L, Cope L, Bolstad BM, Irizarry RA. 2004. affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20:307-315. https://doi.org/10.1093/bioinformatics/btg405
54. Ritchie ME, Phipson B, Di Wu Hu Y, Law CW, Shi W, Smyth GK. 2015. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 43:e47. https://doi.org/10.1093/ nar/gkv007
55. Culhane AC, Thioulouse J, Perrière G, Higgins DG. 2005. MADE4: an R package for multivariate analysis of gene expression data. Bioinformatics 21:2789-2790. https://doi.org/10.1093/bioinformatics/bti394
56. Subramanian A, Kuehn H, Gould J, Tamayo P, Mesirov JP. 2007. GSEA-P: a desktop application for gene set enrichment analysis. Bioinformatics 23:3251-3253. https://doi.org/10.1093/bioinformatics/btm369