IFN-λ inhibits drug-resistant HIV infection of macrophages

Frontiers in Immunology

Volumn 8, Issue MAR, 2017, Pages

  Wang, Xu ^a   Wang, He ^a   Liu, Man Qing ^b   Li, Jie Liang ^a   Zhou, Run Hong ^a   Zhou, Yu ^a   Wang, Yi Zhong ^a   Zhou, Wang ^b   Ho, Wen Zhe ^a,c  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Wuhan Centers for Disease Prevention and Control   (China)

^c WUHAN UNIVERSITY   (China)

Author keywords

Antiretrovirals; Drug resistant HIV; IFN ; Mx2; Tetherin

Indexed keywords

CELL PROTEIN; EFAVIRENZ; ENFUVIRTIDE; GAG PROTEIN; GAMMA INTERFERON; INDINAVIR; MYXOVIRUS RESISTANCE PROTEIN; TETHERIN; UNCLASSIFIED DRUG;

ANTIVIRAL ACTIVITY; ARTICLE; CELL DENSITY; CONTROLLED STUDY; DRUG RESISTANT HUMAN IMMUNODEFICIENCY VIRUS INFECTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MACROPHAGE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

EID: 85017204325     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.00210     Document Type: Article

References (68)

1. Cole SR, Li R, Anastos K, Detels R, Young M, Chmiel JS, et al. Accounting for leadtime in cohort studies: evaluating when to initiate HIV therapies. Stat Med (2004) 23:3351-63. doi:10.1002/sim.1579
2. Qian K, Morris-Natschke SL, Lee KH. HIV entry inhibitors and their potential in HIV therapy. Med Res Rev (2009) 29:369-93. doi:10.1002/med.20138
3. Cheung PK, Wynhoven B, Harrigan PR. 2004: which HIV-1 drug resistance mutations are common in clinical practice? AIDS Rev (2004) 6:107-16.
4. Wainberg MA, Turner D. Resistance issues with new nucleoside/nucleotide backbone options. J Acquir Immune Defic Syndr (2004) 37(Suppl 1):S36-43. doi:10.1097/01.qai.0000137005.63376.6e
5. Gavegnano C, Detorio MA, Bassit L, Hurwitz SJ, North TW, Schinazi RF. Cellular pharmacology and potency of HIV-1 nucleoside analogs in primary human macrophages. Antimicrob Agents Chemother (2013) 57:1262-9. doi:10.1128/AAC.02012-12
6. Jin X, McGrath MS, Xu H. Inhibition of HIV expression and integration in macrophages by methylglyoxal-bis-guanylhydrazone. J Virol (2015) 89:11176-89. doi:10.1128/JVI.01692-15
7. Kuhl BD, Cheng V, Wainberg MA, Liang C. Tetherin and its viral antagonists. J Neuroimmune Pharmacol (2011) 6:188-201. doi:10.1007/s11481-010-9256-1
8. Nasr N, Maddocks S, Turville SG, Harman AN, Woolger N, Helbig KJ, et al. HIV-1 infection of human macrophages directly induces viperin which inhibits viral production. Blood (2012) 120:778-88. doi:10.1182/blood-2012-01-407395
9. Dumoutier L, Tounsi A, Michiels T, Sommereyns C, Kotenko SV, Renauld JC. Role of the interleukin (IL)-28 receptor tyrosine residues for antiviral and antiproliferative activity of IL-29/interferon-lambda 1: similarities with type I interferon signaling. J Biol Chem (2004) 279:32269-74. doi:10.1074/jbc.M404789200
10. Meager A, Visvalingam K, Dilger P, Bryan D, Wadhwa M. Biological activity of interleukins-28 and-29: comparison with type I interferons. Cytokine (2005) 31:109-18. doi:10.1016/j.cyto.2005.04.003
11. Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK, et al. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol (2003) 4:69-77. doi:10.1038/ni875
12. Suppiah V, Moldovan M, Ahlenstiel G, Berg T, Weltman M, Abate ML, et al. IL28B is associated with response to chronic hepatitis C interferon-alpha and ribavirin therapy. Nat Genet (2009) 41:1100-4. doi:10.1038/ng.447
13. Ank N, Iversen MB, Bartholdy C, Staeheli P, Hartmann R, Jensen UB, et al. An important role for type III interferon (IFN-lambda/IL-28) in TLR-induced antiviral activity. J Immunol (2008) 180:2474-85. doi:10.4049/jimmunol.180.4.2474
14. Pagliaccetti NE, Robek MD. Interferon-lambda in HCV infection and therapy. Viruses (2010) 2:1589-602. doi:10.3390/v2081589
15. Sheppard P, Kindsvogel W, Xu W, Henderson K, Schlutsmeyer S, Whitmore TE, et al. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat Immunol (2002) 4:63-8. doi:10.1038/ni873
16. Robek MD, Boyd BS, Chisari FV. Lambda interferon inhibits hepatitis B and C virus replication. J Virol (2005) 79:3851-4. doi:10.1128/JVI.79.6.3851-3854.2005
17. Hou W, Wang X, Ye L, Zhou L, Yang ZQ, Riedel E, et al. Lambda interferon inhibits human immunodeficiency virus type 1 infection of macrophages. J Virol (2009) 83:3834-42. doi:10.1128/JVI.01773-08
18. Liu MQ, Zhou DJ, Wang X, Zhou W, Ye L, Li JL, et al. IFN-lambda3 inhibits HIV infection of macrophages through the JAK-STAT pathway. PLoS One (2012) 7:e35902. doi:10.1371/journal.pone.0035902
19. Ank N, West H, Bartholdy C, Eriksson K, Thomsen AR, Paludan SR. lambda interferon (IFN-lambda), a type III IFN, is induced by viruses and IFNs and displays potent antiviral activity against select virus infections in vivo. J Virol (2006) 80:4501-9. doi:10.1128/JVI.80.9.4501-4509.2006
20. Ank N, West H, Paludan SR. IFN-lambda: novel antiviral cytokines. J Interferon Cytokine Res (2006) 26:373-9. doi:10.1089/jir.2006.26.373
21. Sommereyns C, Paul S, Staeheli P, Michiels T. IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog (2008) 4:e1000017. doi:10.1371/journal.ppat.1000017
22. Witte K, Gruetz G, Volk HD, Looman AC, Asadullah K, Sterry W, et al. Despite IFN-lambda receptor expression, blood immune cells, but not keratinocytes or melanocytes, have an impaired response to type III interferons: implications for therapeutic applications of these cytokines. Genes Immun (2009) 10:702-14. doi:10.1038/gene.2009.72
23. Zhou L, Wang X, Wang YJ, Zhou Y, Hu S, Ye L, et al. Activation of toll-like receptor-3 induces interferon-lambda expression in human neuronal cells. Neuroscience (2009) 159:629-37. doi:10.1016/j.neuroscience.2008.12.036
24. Li J, Hu S, Zhou L, Ye L, Wang X, Ho J, et al. Interferon lambda inhibits herpes simplex virus type I infection of human astrocytes and neurons. Glia (2011) 59:58-67. doi:10.1002/glia.21076
25. Ge D, Fellay J, Thompson AJ, Simon JS, Shianna KV, Urban TJ, et al. Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature (2009) 461:399-401. doi:10.1038/nature08309
26. Tanaka Y, Nishida N, Sugiyama M, Kurosaki M, Matsuura K, Sakamoto N, et al. Genome-wide association of IL28B with response to pegylated interferon-alpha and ribavirin therapy for chronic hepatitis C. Nat Genet (2009) 41:1105-9. doi:10.1038/ng.449
27. Thomas DL, Thio CL, Martin MP, Qi Y, Ge D, O'Huigin C, et al. Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature (2009) 461:798-801. doi:10.1038/nature08463
28. Vierling JM, Lataillade M, Gane EJ, Lüth S, Serfaty L, Taliani G, et al. Sustained virologic response (SVR12) in HCV genotype 1 patients receiving peginterferon lambda in combination with ribavirin and either daclatasvir or asunaprevir: interim results from the D-LITE study. Hepatol Int (2013) 7(suppl 1):S438-9. doi:10.1007/s12072-013-9429-0
29. Andersen H, Meyer J, Freeman J, Doyle SE, Klucher K, Miller DM, et al. Peginterferon lambda-1a, a new therapeutic for hepatitis C infection, from bench to clinic. J Clin Transl Hepatol (2013) 1:116-24. doi:10.14218/JCTH.2013.00014
30. Fredlund P, Hillson J, Gray T, Shemanski L, Dimitrova D, Srinivasan S. Peginterferon lambda-1a is associated with a low incidence of autoimmune thyroid disease in chronic hepatitis C. J Interferon Cytokine Res (2015) 35:841-3. doi:10.1089/jir.2014.0233
31. Flisiak R, Kawazoe S, Znoyko O, Assy N, Gadano A, Kao JH, et al. Peginterferon lambda-1a/ribavirin with daclatasvir or peginterferon alfa-2a/ribavirin with telaprevir for chronic hepatitis C genotype 1b. J Interferon Cytokine Res (2016) 36(11):635-43. doi:10.1089/jir.2015.0173
32. Tian RR, Guo HX, Wei JF, Yang CK, He SH, Wang JH. IFN-lambda inhibits HIV-1 integration and post-transcriptional events in vitro, but there is only limited in vivo repression of viral production. Antiviral Res (2012) 95:57-65. doi:10.1016/j.antiviral.2012.04.011
33. Liang H, Wang X, Chen H, Song L, Ye L, Wang SH, et al. Methamphetamine enhances HIV infection of macrophages. Am J Pathol (2008) 172:1617-24. doi:10.2353/ajpath.2008.070971
34. Wang X, Ye L, Hou W, Zhou Y, Wang YJ, Metzger DS, et al. Cellular microRNA expression correlates with susceptibility of monocytes/macrophages to HIV-1 infection. Blood (2009) 113:671-4. doi:10.1182/blood-2008-09-175000
35. Berger EA, Doms RW, Fenyo EM, Korber BT, Littman DR, Moore JP, et al. A new classification for HIV-1. Nature (1998) 391:240. doi:10.1038/35091
36. Larder BA, Darby G, Richman DD. HIV with reduced sensitivity to zidovudine (AZT) isolated during prolonged therapy. Science (1989) 243:1731-4. doi:10.1126/science.2467383
37. Willey RL, Smith DH, Lasky LA, Theodore TS, Earl PL, Moss B, et al. In vitro mutagenesis identifies a region within the envelope gene of the human immunodeficiency virus that is critical for infectivity. J Virol (1988) 62:139-47.
38. Ho WZ, Lioy J, Song L, Cutilli JR, Polin RA, Douglas SD. Infection of cord blood monocyte-derived macrophages with human immunodeficiency virus type 1. J Virol (1992) 66:573-9.
39. Li Y, Wang X, Tian S, Guo CJ, Douglas SD, Ho WZ. Methadone enhances human immunodeficiency virus infection of human immune cells. J Infect Dis (2002) 185:118-22. doi:10.1086/338011
40. Wang X, Douglas SD, Metzger DS, Guo CJ, Li Y, O'Brien CP, et al. Alcohol potentiates HIV-1 infection of human blood mononuclear phagocytes. Alcohol Clin Exp Res (2002) 26:1880-6. doi:10.1097/01.ALC.0000042148.50808.04
41. Zhou Y, Wang X, Liu M, Hu Q, Song L, Ye L, et al. A critical function of toll-like receptor-3 in the induction of anti-human immunodeficiency virus activities in macrophages. Immunology (2010) 131:40-9. doi:10.1111/j.1365-2567.2010.03270.x
42. Ye L, Wang X, Wang S, Wang Y, Song L, Hou W, et al. CD56+ T cells inhibit hepatitis C virus replication in human hepatocytes. Hepatology (2009) 49:753-62. doi:10.1002/hep.22715
43. Wang X, Ye L, Zhou Y, Liu MQ, Zhou DJ, Ho WZ. Inhibition of anti-HIV microRNA expression: a mechanism for opioid-mediated enhancement of HIV infection of monocytes. Am J Pathol (2011) 178:41-7. doi:10.1016/j.ajpath.2010.11.042
44. Zhang H, Yang B, Pomerantz RJ, Zhang C, Arunachalam SC, Gao L. The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature (2003) 424:94-8. doi:10.1038/nature01707
45. Kawai S, Azuma Y, Fujii E, Furugaki K, Ozaki S, Matsumoto T, et al. Interferon-alpha enhances CD317 expression and the antitumor activity of anti-CD317 monoclonal antibody in renal cell carcinoma xenograft models. Cancer Sci (2008) 99:2461-6. doi:10.1111/j.1349-7006.2008.00968.x
46. Neil SJ, Zang T, Bieniasz PD. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature (2008) 451:425-30. doi:10.1038/nature06553
47. Goujon C, Moncorge O, Bauby H, Doyle T, Ward CC, Schaller T, et al. Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection. Nature (2013) 502:559-62. doi:10.1038/nature12542
48. Kane M, Yadav SS, Bitzegeio J, Kutluay SB, Zang T, Wilson SJ, et al. MX2 is an interferon-induced inhibitor of HIV-1 infection. Nature (2013) 502:563-6. doi:10.1038/nature12653
49. Liu Z, Pan Q, Ding S, Qian J, Xu F, Zhou J, et al. The interferon-inducible MxB protein inhibits HIV-1 infection. Cell Host Microbe (2013) 14:398-410. doi:10.1016/j.chom.2013.08.015
50. Wang Y, Li J, Wang X, Zhou Y, Zhang T, Ho W. Comparison of antiviral activity of lambda-interferons against HIV replication in macrophages. J Interferon Cytokine Res (2015) 35:213-21. doi:10.1089/jir.2014.0064
51. Vilcek J. Novel interferons. Nat Immunol (2003) 4:8-9. doi:10.1038/ni0103-8
52. Li M, Liu X, Zhou Y, Su SB. Interferon-lambdas: the modulators of antivirus, antitumor, and immune responses. J Leukoc Biol (2009) 86:23-32. doi:10.1189/jlb.1208761
53. Josephson K, Logsdon NJ, Walter MR. Crystal structure of the IL-10/IL-10R1 complex reveals a shared receptor binding site. Immunity (2001) 15:35-46. doi:10.1016/S1074-7613(01)00169-8
54. Steen HC, Gamero AM. Interferon-lambda as a potential therapeutic agent in cancer treatment. J Interferon Cytokine Res (2010) 30:597-602. doi:10.1089/jir.2010.0058
55. Lasfar A, Abushahba W, Balan M, Cohen-Solal KA. Interferon lambda: a new sword in cancer immunotherapy. Clin Dev Immunol (2011) 2011:349575. doi:10.1155/2011/349575
56. Jordan WJ, Eskdale J, Srinivas S, Pekarek V, Kelner D, Rodia M, et al. Human interferon lambda-1 (IFN-lambda1/IL-29) modulates the Th1/Th2 response. Genes Immun (2007) 8:254-61. doi:10.1038/sj.gene.6364348
57. Guenterberg KD, Grignol VP, Raig ET, Zimmerer JM, Chan AN, Blaskovits FM, et al. Interleukin-29 binds to melanoma cells inducing Jak-STAT signal transduction and apoptosis. Mol Cancer Ther (2010) 9:510-20. doi:10.1158/1535-7163.MCT-09-0461
58. Jordan WJ, Eskdale J, Boniotto M, Rodia M, Kellner D, Gallagher G. Modulation of the human cytokine response by interferon lambda-1 (IFN-lambda1/IL-29). Genes Immun (2007) 8:13-20. doi:10.1038/sj.gene.6364348
59. Marcello T, Grakoui A, Barba-Spaeth G, Machlin ES, Kotenko SV, Macdonald MR, et al. Interferons alpha and lambda inhibit hepatitis C virus replication with distinct signal transduction and gene regulation kinetics. Gastroenterology (2006) 131:1887-98. doi:10.1053/j.gastro.2006.09.052
60. Brand S, Beigel F, Olszak T, Zitzmann K, Eichhorst ST, Otte JM, et al. IL-28A and IL-29 mediate antiproliferative and antiviral signals in intestinal epithelial cells and murine CMV infection increases colonic IL-28A expression. Am J Physiol Gastrointest Liver Physiol (2005) 289:G960-8. doi:10.1152/ajpgi.00126.2005
61. Almeida GM, De Oliveira DB, Magalhaes CL, Bonjardim CA, Ferreira PC, Kroon EG. Antiviral activity of type I interferons and interleukins 29 and 28a (type III interferons) against Apeu virus. Antiviral Res (2008) 80:302-8. doi:10.1016/j.antiviral.2008.06.016
62. Ma D, Jiang D, Qing M, Weidner JM, Qu X, Guo H, et al. Antiviral effect of interferon lambda against West Nile virus. Antiviral Res (2009) 83:53-60. doi:10.1016/j.antiviral.2009.03.006
63. Palma-Ocampo HK, Flores-Alonso JC, Vallejo-Ruiz V, Reyes-Leyva J, Flores-Mendoza L, Herrera-Camacho I, et al. Interferon lambda inhibits dengue virus replication in epithelial cells. Virol J (2015) 12:150. doi:10.1186/s12985-015-0383-4
64. Ank N, Paludan SR. Type III IFNs: new layers of complexity in innate antiviral immunity. Biofactors (2009) 35:82-7. doi:10.1002/biof.19
65. Muzammil, Jayanthi D, Faizuddin M, Noor Ahamadi HM. Association of interferon lambda-1 with herpes simplex viruses-1 and-2, Epstein-Barr virus, and human cytomegalovirus in chronic periodontitis. J Investig Clin Dent (2015). doi:10.1111/jicd.12200
66. Mordstein M, Kochs G, Dumoutier L, Renauld JC, Paludan SR, Klucher K, et al. Interferon-lambda contributes to innate immunity of mice against influenza A virus but not against hepatotropic viruses. PLoS Pathog (2008) 4:e1000151. doi:10.1371/journal.ppat.1000151
67. Mordstein M, Neugebauer E, Ditt V, Jessen B, Rieger T, Falcone V, et al. Lambda interferon renders epithelial cells of the respiratory and gastrointestinal tracts resistant to viral infections. J Virol (2010) 84:5670-7. doi:10.1128/JVI.00272-10
68. Hermant P, Michiels T. Interferon-lambda in the context of viral infections: production, response and therapeutic implications. J Innate Immun (2014) 6:563-74. doi:10.1159/000360084