Cell activation and HIV-1 replication in unstimulated CD4+ T lymphocytes ingesting exosomes from cells expressing defective HIV-1

Retrovirology

Volumn 11, Issue 1, 2014, Pages

  Arenaccio, Claudia ^a,b   Chiozzini, Chiara ^a   Columba Cabezas, Sandra ^a   Manfredi, Francesco ^a   Federico, Maurizio ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b ROMA TRE UNIVERSITY   (Italy)

Author keywords

ADAM17; Defective HIV 1; Exosomes; Nef

Indexed keywords

3,3' (1,4 PHENYLENE)BIS[N [4 (4,5 DIHYDRO 1H IMIDAZOL 2 YL)PHENYL]ACRYLAMIDE]; GAG PROTEIN; INTERLEUKIN 2; NEF PROTEIN; SPHINGOMYELIN PHOSPHODIESTERASE INHIBITOR; SPIROEPOXIDE; TAPI 2; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA ANTIBODY; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME INHIBITOR; TUMOR NECROSIS FACTOR ALPHA RECEPTOR; TUMOR NECROSIS FACTOR ALPHA RECEPTOR 1; TUMOR NECROSIS FACTOR ALPHA RECEPTOR 2; UNCLASSIFIED DRUG; ZIDOVUDINE; CAP24 PROTEIN; VIRUS PROTEIN; ADAM PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2; TUMOR NECROSIS FACTOR-ALPHA CONVERTASE;

ARTICLE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; COCULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; DEFECTIVE VIRUS; DISEASE PREDISPOSITION; EMBRYO; EXOSOME; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; LYMPHOCYTE FUNCTION; NONHUMAN; NORMAL HUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; T CELL CULTURE; VIRUS EXPRESSION; VIRUS GENOME; VIRUS INHIBITION; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS STRAIN; CELL COUNT; CELL INTERACTION; INFECTION SENSITIVITY; INTRACELLULAR SIGNALING; PROTEIN INTERACTION; PROTEIN SECRETION; T LYMPHOCYTE ACTIVATION; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL CULTURE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; PHYSIOLOGY; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ADAM PROTEINS; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; EXOSOMES; HIV-1; HUMANS; INTERLEUKIN-2; LYMPHOCYTE ACTIVATION; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE II; TUMOR NECROSIS FACTOR-ALPHA; VIRUS REPLICATION;

EID: 84904615306     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-11-46     Document Type: Article

References (52)

1. Cao Y, Qin L, Zhang L, Safrit J, Ho DD. Virologic and immunologic characterization of long-term survivors of human immunodeficiency virus type 1 infection. N Engl J Med 1995, 332:201-208.
2. Daar ES, Chernyavskiy T, Zhao JQ, Krogstad P, Chen IS, Zack JA. Sequential determination of viral load and phenotype in human immunodeficiency virus type 1 infection. AIDS Res Hum Retroviruses 1995, 11:3-9.
3. Sanchez G, Xu X, Chermann JC, Hirsch I. Accumulation of defective viral genomes in peripheral blood mononuclear cells of human immunodeficiency virus type 1-infected individuals. J Virol 1997, 71:2233-2240.
4. Fourati S, Lambert-Niclot S, Soulie C, Malet I, Valantin MA, Descours B, Ait-Arkoub Z, Mory B, Carcelain G, Katlama C, Calvez V, Marcelin AG. HIV-1 genome is often defective in PBMCs and rectal tissues after long-term HAART as a result of APOBEC3 editing and correlates with the size of reservoirs. J Antimicrob Chemother 2012, 67:2323-2326.
5. Ho Y-C, Shan L, Hosmane NN, Wang J, Laskey SB, Rosenbloom DIS, Lai J, Blankson JN, Siliciano JD, Siliciano RF. Replication-competent noninduced proviruses in the latent reservoir increase barrier to HIV-1 cure. Cell 2013, 155:540-551.
6. Saurya S, Lichtenstein Z, Karpas A. Characterization of pol, vif, vpr, and vpu genes of HIV type 1 in AIDS patients with high viral load and stable CD4+ T cell counts on combination therapy. AIDS Res Hum Retroviruses 2002, 18:1151-1155.
7. Saurya S, Lichtenstein Z, Karpas A. Characterization of nef gene of HIV type 1 in highly active antiretroviral therapy treated AIDS patients with discordance between viral load and CD4+ T cell counts. AIDS Res Hum Retroviruses 2002, 18:983-987.
8. Saurya S, Lichtenstein Z, Karpas A. Characterization of gag gene of plasma HIV type 1 in combination therapy-treated AIDS patients with high viral load and stable CD4+ T cell counts. AIDS Res Hum Retroviruses 2003, 19:73-76.
9. Saurya S, Lichtenstein Z, Karpas A. Defective rev response element (RRE) and rev gene in HAART treated AIDS patients with discordance between viral load and CD4+ T-cell counts. J Clin Virol 2005, 33:324-327.
10. Saurya S, Lichtenstein Z, Karpas A. Deletions in env gene of HIV-1 in AIDS patients treated with highly active antiretroviral therapy (HAART). J Med Virol 2003, 71:167-172.
11. Federico M, Titti F, Butto S, Orecchia A, Carlini F, Taddeo B, Macchi B, Maggiano N, Verani P, Rossi GB. Biologic and molecular characterization of producer and nonproducer clones from HUT-78 cells infected with a patient HIV isolate. AIDS Res Hum Retroviruses 1989, 5:385-396.
12. D'Aloja P, Olivetta E, Bona R, Nappi F, Pedacchia D, Pugliese K, Ferrari G, Verani P, Federico M. Gag, vif and nef genes contribute to the homologous viral interference induced by a nonproducer human immunodeficiency virus type 1 (HIV-1) variant: identification of novel HIV-1-inhibiting viral protein mutants. J Virol 1998, 72:4308-4319.
13. D'Aloja P, Santarcangelo AC, Arold S, Baur A, Federico M. Genetic and functional analysis of the human immunodeficiency virus (HIV) type 1-inhibiting F12-HIVnef allele. J Gen Virol 2001, 82:2735-2745.
14. Fackler OT, d'Aloja P, Baur AS, Federico M, Peterlin BM. Nef from human immunodeficiency virus type 1(F12) inhibits viral production and infectivity. J Virol 2001, 75:6601-6608.
15. Vallanti G, Lupo R, Federico M, Mavilio F, Bovolenta C. T lymphocytes transduced with a lentiviral vector expressing F12-vif are protected from HIV-1 infection in an APOBEC3G-independent manner. Mol Ther 2005, 12:697-706.
16. Gyorgy B, Szabo TG, Pasztoi M, Pal Z, Misjak P, Aradi B, Laszlo V, Pallinger E, Pap E, Kittel A, Nagy G, Falus A, Buzas EI. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci 2011, 68:2667-2688.
17. Booth AM, Fang Y, Fallon JK, Yang JM, Hildreth JEK, Gould SJ. Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane. J Cell Biol 2006, 172:923-935.
18. Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics 2010, 73:1907-1920.
19. Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT, Carter BS, Krichevsky AM, Breakefield XO. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008, 10:1470-1476.
20. Fang Y, Wu N, Gan X, Yan WH, Morrell JC, Gould SJ. Higher-order oligomerization targets plasma membrane proteins and HIV gag to exosomes. PLoS Biol 2007, 5:1267-1283.
21. Lenassi M, Cagney G, Liao MF, Vaupotic T, Bartholomeeusen K, Cheng YF, Krogan NJ, Plemenitas A, Peterlin BM. HIV Nef is secreted in exosomes and triggers apoptosis in bystander CD4(+) T cells. Traffic 2010, 11:110-122.
22. Muratori C, Cavallin LE, Kratzel K, Tinari A, De Milito A, Fais S, D'Aloja P, Federico M, Vullo V, Fomina A, Mesri EA, Superti F, Baur AS. Massive secretion by T cells is caused by HIV Nef in infected cells and by Nef transfer to bystander cells. Cell Host Microbe 2009, 6:218-230.
23. Chairoungdua A, Smith DL, Pochard P, Hull M, Caplan MJ. Exosome release of beta-catenin: a novel mechanism that antagonizes Wnt signaling. J Cell Biol 2010, 190:1079-1091.
24. Kogure T, Lin W-L, Yan IK, Braconi C, Patel T. Intercellular nanovesicle-mediated microRNA transfer: a mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology 2011, 54:1237-1248.
25. Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem 2010, 285:17442-17452.
26. Kosaka N, Iguchi H, Yoshioka Y, Hagiwara K, Takeshita F, Ochiya T. Competitive interactions of cancer cells and normal cells via secretory microRNAs. J Biol Chem 2012, 287:1397-1405.
27. Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, Schwille P, Bruegger B, Simons M. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008, 319:1244-1247.
28. Yuyama K, Sun H, Mitsutake S, Igarashi Y. Sphingolipid-modulated exosome secretion promotes clearance of amyloid-beta by microglia. J Biol Chem 2012, 287:10977-10989.
29. Rieu S, Geminard C, Rabesandratana H, Sainte-Marie J, Vidal M. Exosomes released during reticulocyte maturation bind to fibronectin via integrin alpha 4 beta 1. Eur J Biochem 2000, 267:583-590.
30. Cantin R, Diou J, Belanger D, Tremblay AM, Gilbert C. Discrimination between exosomes and HIV-1: Purification of both vesicles from cell-free supernatants. J Immunol Methods 2008, 338:21-30.
31. Lattanzi L, Federico M. A strategy of antigen incorporation into exosomes: Comparing cross-presentation levels of antigens delivered by engineered exosomes and by lentiviral virus-like particles. Vaccine 2012, 30:7229-7237.
32. Columba Cabezas S, Federico M. Sequences within RNA coding for HIV-1 Gag p17 are efficiently targeted to exosomes. Cell Microbiol 2013, 15:412-429.
33. Vatakis DN, Bristol G, Wilkinson TA, Chow SA, Zack JA. Immediate activation fails to rescue efficient human immunodeficiency virus replication in quiescent CD4(+) T cells. J Virol 2007, 81:3574-3582.
34. Wu Y, Beddall MH, Marsh JW. Rev-dependent indicator T cell line. Curr HIV Res 2007, 5:394-402.
35. Lee JH, Wittki S, Brau T, Dreyer FS, Kratzel K, Dindorf J, Johnston ICD, Gross S, Kremmer E, Zeidler R, Schlotzer-Schrehardt U, Lichtenheld M, Saksela K, Harrer T, Schuler G, Federico M, Baur AS. HIV Nef, paxillin, and Pak1/2 regulate activation and secretion of TACE/ADAM10 proteases. Mol Cell 2013, 49:668-679.
36. Gooz M. ADAM-17: the enzyme that does it all. Crit Rev Biochem Mol Biol 2010, 45:146-169.
37. Moss ML, Rasmussen FH. Fluorescent substrates for the proteinases ADAM17, ADAM10, ADAM8, and ADAM12 useful for high-throughput inhibitor screening. Anal Biochem 2007, 366:144-148.
38. Wolf D, Witte V, Clark P, Blume K, Lichtenheld MG, Baur AS. HIV Nef enhances Tat-mediated viral transcription through a hnRNP-K-nucleated signaling complex. Cell Host Microbe 2008, 4:398-408.
39. Olivetta E, Pugliese K, Bona R, D'Aloja P, Ferrantelli F, Santarcangelo AC, Mattia G, Verani P, Federico M. Cis expression of the F12 human immunodeficiency virus (HIV) nef allele transforms the highly productive NL4-3 HIV type 1 to a replication-defective strain: Involvement of both Env gp41 and CD4 intracytoplasmic tails. J Virol 2000, 74:483-492.
40. Janini M, Rogers M, Birx DR, McCutchan FE. Human immunodeficiency virus type 1 DNA sequences genetically damaged by hypermutation are often abundant in patient peripheral blood mononuclear cells and may be generated during near-simultaneous infection and activation of CD4(+) T cells. J Virol 2001, 75:7973-7986.
41. Fourati S, Lambert-Niclot S, Soulie C, Wirden M, Malet I, Valantin MA, Tubiana R, Simon A, Katlama C, Carcelain G, Calvez V, Marcelin AG. Differential impact of APOBEC3-driven mutagenesis on HIV evolution in diverse anatomical compartments. AIDS 2014, 28:487-491.
42. Carlini F, Nicolini A, d'Aloja P, Federico M, Verani P. The non-producer phenotype of the human immunodeficiency virus type 1 provirus F12/HIV-1 is the result of multiple genetic variations. J Gen Virol 1996, 77:2009-2013.
43. Zack JA, Arrigo SJ, Weitsman SR, Go AS, Haislip A, Chen ISY. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 1990, 61:213-222.
44. Zack JA, Haislip AM, Krogstad P, Chen ISY. Incompletely reverse-transcribed human immunodeficiency virus type 1 genomes in quiescent cells can function as intermediates in the retroviral life cycle. J Virol 1992, 66:1717-1725.
45. Ghose R, Liou LY, Herrmann CH, Rice AP. Induction of TAK (cyclin T1/P-TEFb) in purified resting CD4(+) T lymphocytes by combination of cytokines. J Virol 2001, 75:11336-11343.
46. McNamara LA, Ganesh JA, Collins KL. Latent HIV-1 infection occurs in multiple subsets of hematopoietic progenitor cells and is reversed by NF-kappa B activation. J Virol 2012, 86:9337-9350.
47. Herbein G, Khan KA. Is HIV infection a TNF receptor signaling-driven disease?. Trends Immunol 2008, 29:61-67.
48. Chowers MY, Spina CA, Kwoh TJ, Fitch NJS, Richman DD, Guatelli JC. Optimal infectivity in-vitro of human immunodeficiency virus type 1 requires an intact nef gene. J Virol 1994, 68:2906-2914.
49. Federico M, Percario Z, Olivetta E, Fiorucci G, Muratori C, Micheli A, Romeo G, Affabris E. HIV-1 Nef activates STAT1 in human monocytes/macrophages through the release of soluble factors. Blood 2001, 98:2752-2761.
50. Park IW, He JJ. HIV-1 is budded from CD4+T lymphocytes independently of exosomes. Virol J 2010, 7:234.
51. Dettenhofer M, Yu XF. Highly purified human immunodeficiency virus type 1 reveals a virtual absence of vif in virions. J Virol 1999, 73:1460-1467.
52. Muratori C, Sistigu A, Ruggiero E, Falchi M, Bacigalupo I, Palladino C, Toschi E, Federico M. Macrophages transmit human immunodeficiency virus type 1 products to CD4-negative cells: Involvement of matrix metalloproteinase 9. J Virol 2007, 81:9078-9087.