Cytokine and gene transcription profiles of immune responses elicited by HIV lipopeptide vaccine in HIV-negative volunteers

AIDS

Volumn 27, Issue 9, 2013, Pages 1421-1431

  Richert, Laura ^a,b   Hue, Sophie ^c,d,e   Hocini, Hakim ^c,e   Raimbault, Mathieu ^a,b   Lacabaratz, Christine ^c,d,e   Surenaud, Mathieu ^c,e   Wiedemann, Aurélie ^c,d,e   Tisserand, Pascaline ^c,e   Durier, Christine ^b   Salmon, Dominique ^f   Lelièvre, Jean Daniel ^c,d,e   Chêne, Geneviève ^a,b,g   Thiébaut, Rodolphe ^a,b   Lévy, Yves ^c,d,e  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b INSERM   (France)

^c HENRI MONDOR HOSPITAL   (France)

^d FACULTÉ DE MÉDECINE   (France)

^e Mondor Immunology Center   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

^g BORDEAUX UNIVERSITY HOSPITAL   (France)

Author keywords

Cellular factors cytokines; Cellular immunity; Clinical trial; HIV; Lipopeptides; Transcriptome; Vaccine

Indexed keywords

CXCL9 CHEMOKINE; GAG PROTEIN; GAMMA INTERFERON; HUMAN IMMUNODEFICIENCY VIRUS LIPOPEPTIDE 5 VACCINE; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; INTERLEUKIN 13; INTERLEUKIN 5; INTERLEUKIN 6; METALLOTHIONEIN; PEPTIDE VACCINE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; IMMUNOGENICITY; LYMPHOCYTE PROLIFERATION; MALE; MICROARRAY ANALYSIS; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHASE 2 CLINICAL TRIAL; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL;

EID: 84879092040     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0b013e32835f5b60     Document Type: Article

References (46)

1. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, Paris R, et al. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 2009; 361:2209-2220.
2. McElrath MJ, Haynes BF. Induction of immunity to human immunodeficiency virus type-1 by vaccination. Immunity 2010; 33:542-554.
3. Virgin HW, Walker BD. Immunology and the elusive AIDS vaccine. Nature 2010; 464:224-231.
4. Potter SJ, Lacabaratz C, Lambotte O, Perez-Patrigeon S, Vingert B, Sinet M, et al. Preserved central memory and activated effector memory CD4R T-cell subsets in human immunodeficiency virus controllers: an ANRS EP36 study. J Virol 2007; 81:13904-13915.
5. Saez-Cirion A, Lacabaratz C, Lambotte O, Versmisse P, Urrutia A, Boufassa F, et al. HIV controllers exhibit potent CD8 T cell capacity to suppress HIV infection ex vivo and peculiar cytotoxic T lymphocyte activation phenotype. Proc Natl Acad Sci U S A 2007; 104:6776-6781.
6. Barouch DH, Liu J, Li H, Maxfield LF, Abbink P, Lynch DM, et al. Vaccine protection against acquisition of neutralization-resistant SIV challenges in rhesus monkeys. Nature 2012; 482:89-93.
7. Pulendran B, Li S, Nakaya HI. Systems vaccinology. Immunity 2010; 33:516-529.
8. Andrieu M, Desoutter JF, Loing E, Gaston J, Hanau D, Guillet JG, et al. Two human immunodeficiency virus vaccinal lipopeptides follow different cross-presentation pathways in human dendritic cells. J Virol 2003; 77:1564-1570.
9. Andrieu M, Loing E, Desoutter JF, Connan F, Choppin J, Gras-Masse H, et al. Endocytosis of an HIV-derived lipopeptide into human dendritic cells followed by class I-restricted CD8(R) T lymphocyte activation. Eur J Immunol 2000; 30:3256-3265.
10. Zhu X, Ramos TV, Gras-Masse H, Kaplan BE, Ben-Mohamed L. Lipopeptide epitopes extended by an Nepsilon-palmitoyllysine moiety increase uptake and maturation of dendritic cells through a Toll-like receptor-2 pathway and trigger a Th1-dependent protective immunity. Eur J Immunol 2004; 34:3102-3114.
11. Gahery-Segard H, Pialoux G, Charmeteau B, Sermet S, Poncelet H, Raux M, et al. Multiepitopic B- and T-cell responses induced in humans by a human immunodeficiency virus type 1 lipopeptide vaccine. J Virol 2000; 74:1694-1703.
12. Durier C, Launay O, Meiffredy V, Saidi Y, Salmon D, Levy Y, et al. Clinical safety of HIV lipopeptides used as vaccines in healthy volunteers and HIV-infected adults. AIDS 2006; 20:1039-1049.
13. Salmon-Ceron D, Durier C, Desaint C, Cuzin L, Surenaud M, Hamouda NB, et al. Immunogenicity and safety of an HIV-1 lipopeptide vaccine in healthy adults: a phase 2 placebo-controlled ANRS trial. AIDS 2010; 24:2211-2223.
14. Gahery-Segard H, Pialoux G, Figueiredo S, Igea C, Surenaud M, Gaston J, et al. Long-term specific immune responses induced in humans by a human immunodeficiency virus type 1 lipopeptide vaccine: characterization of CD8R-T-cell epitopes recognized. J Virol 2003; 77:11220-11231.
15. Launay O, Durier C, Desaint C, Silbermann B, Jackson A, Pialoux G, et al. Cellular immune responses induced with dose-sparing intradermal administration of HIV vaccine to HIV-uninfected volunteers in the ANRS VAC16 trial. PLoS One 2007; 2:e725.
16. Pialoux G, Gahery-Segard H, Sermet S, Poncelet H, Fournier S, Gerard L, et al. Lipopeptides induce cell-mediated anti-HIV immune responses in seronegative volunteers. AIDS 2001; 15:1239-1249.
17. Goonetilleke N, Moore S, Dally L, Winstone N, Cebere I, Mahmoud A, et al. Induction of multifunctional human immunodeficiency virus type 1 (HIV-1)-specific T cells capable of proliferation in healthy subjects by using a prime-boost regimen of DNA- and modified vaccinia virus Ankara-vectored vaccines expressing HIV-1 Gag coupled to CD8R T-cell epitopes. J Virol 2006; 80:4717-4728.
18. Tassignon J, Burny W, Dahmani S, Zhou L, Stordeur P, Byl B, et al. Monitoring of cellular responses after vaccination against tetanus toxoid: comparison of the measurement of IFN-gamma production by ELISA, ELISPOT, flow cytometry and real-time PCR. J Immunol Methods 2005; 305:188-198.
19. Dunning MJ, Barbosa-Morais NL, Lynch AG, Tavaré S, Ritchie ME. Statistical issues in the analysis of Illumina data. BMC Bioinformatics 2008; 9:85.
20. Benjamini Y, Hochberg Y. On the adaptive control of the false discovery rate in multiple testing with independent statistics. J Ed Behav Stat 2000; 25:60-83.
21. Marschner IC, Betensky RA, DeGruttola V, Hammer SM, Kuritzkes DR. Clinical trials using HIV-1 RNA-based primary endpoints: statistical analysis and potential biases. J Acquir Immune Defic Syndr Hum Retrovirol 1999; 20:220-227.
22. Thiebaut R, Jacqmin-Gadda H. Mixed models for longitudinal left-censored repeated measures. Comput Methods Programs Biomed 2004; 74:255-260.
23. Benjamini Y, Yekutieli D. The control of the false discovery rate in multiple testing under dependency. Ann Stat 2001; 29:1165-1188.
24. Bolstad BM, Irizarry RA, Astrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003; 19:185-193.
25. Shi W, Oshlack A, Smyth GK. Optimizing the noise versus bias trade-off for Illumina whole genome expression Bead Chips. Nucleic Acids Res 2010; 38:e204.
26. Smyth GK. Limma: linear models for microarray data. In: Gentleman R, Carey V, Huber W, Irizarry R, Dudoit S, editors. Bioinformatics and computational biology solutions using R and Bioconductor New York: Springer; 2005. pp. 397-420.
27. Xie Y, Wang X, Story M. Statistical methods of background correction for Illumina Bead Array data. Bioinformatics 2009; 25:751-757.
28. Li C, Rabinovic A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 2007; 8:118-127.
29. Archer KJ, Reese SE. Detection call algorithms for high-throughput gene expression microarray data. Briefings in Bioinformatics 2010; 11:244-252.
30. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004; 3:Article3.
31. Benjamini Y, Krieger AM, Yekutieli D. Adaptive linear step-up procedures that control the false discovery rate. Biometrika 2006; 93:491-507.
32. Winstone N, Guimaraes-Walker A, Roberts J, Brown D, Loach V, Goonetilleke N, et al. Increased detection of proliferating, polyfunctional, HIV-1-specific T cells in DNA-modified vaccinia virus Ankara-vaccinated human volunteers by cultured IFN-gamma ELISPOT assay. Eur J Immunol 2009; 39:975-985.
33. Keating SM, Bejon P, Berthoud T, Vuola JM, Todryk S, Webster DP, et al. Durable human memory T cells quantifiable by cultured enzyme-linked immunospot assays are induced by heterologous prime boost immunization and correlate with protection against malaria. J Immunol 2005; 175:5675-5680.
34. Reece WH, Pinder M, Gothard PK, Milligan P, Bojang K, Doherty T, et al. A CD4(R) T-cell immune response to a conserved epitope in the circumsporozoite protein correlates with protection from natural Plasmodium falciparum infection and disease. Nat Med 2004; 10:406-410.
35. Hansen SG, Ford JC, Lewis MS, Ventura AB, Hughes CM, Coyne-Johnson L, et al. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 2011; 473:523-527.
36. Miles AT, Hawksworth GM, Beattie JH, Rodilla V. Induction, regulation, degradation, and biological significance of mammalian metallothioneins. Crit Rev Biochem Mol Biol 2000; 35:35-70.
37. Nagel WW, Vallee BL. Cell cycle regulation of metallothionein in human colonic cancer cells. Proc Natl Acad Sci U S A 1995; 92:579-583.
38. Studer R, Vogt CP, Cavigelli M, Hunziker PE, Kagi JH. Metallothionein accretion in human hepatic cells is linked to cellular proliferation. Biochem J 1997; 328 (Pt 1):63-67.
39. Lee WW, Cui D, Czesnikiewicz-Guzik M, Vencio RZ, Shmulevich I, Aderem A, et al. Age-dependent signature of metallothionein expression in primary CD4 T cell responses is due to sustained zinc signaling. Rejuvenation Res 2008; 11:1001-1011.
40. Schwarz MA, Lazo JS, Yalowich JC, Reynolds I, Kagan VE, Tyurin V, et al. Cytoplasmic metallothionein overexpression protects NIH 3T3 cells from tert-butyl hydroperoxide toxicity. J Biol Chem 1994; 269:15238-15243.
41. Lazo JS, Schwarz MA, Pitt BR. Metallothionein and cell death. In: Collery PH, Poirier LA, Littlefield NA, Etienne JC, editors. Metalions in biology and medicine Paris: John Libbey Eurotext; 1994. pp. 15b-16b.
42. Hoeffel G, Ripoche AC, Matheoud D, Nascimbeni M, Escriou N, Lebon P, et al. Antigen crosspresentation by human plas-macytoid dendritic cells. Immunity 2007; 27:481-492.
43. Querec TD, Akondy RS, Lee EK, Cao W, Nakaya HI, Teuwen D, et al. Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat Immunol 2009; 10:116-125.
44. Flatz L, Roychoudhuri R, Honda M, Filali-Mouhim A, Goulet JP, Kettaf N, et al. Single-cell gene-expression profiling reveals qualitatively distinct CD8 T cells elicited by different gene-based vaccines. Proc Natl Acad Sci U S A 2011; 108:5724-5729.
45. Palermo RE, Patterson LJ, Aicher LD, Korth MJ, Robert-Guroff M, Katze MG. Genomic analysis reveals pre and postchallenge differences in a rhesus macaque AIDS vaccine trial: insights into mechanisms of vaccine efficacy. J Virol 2011; 85:1099-1116.
46. Eller MA, Slike BM, Cox JH, Lesho E, Wang Z, Currier JR, et al. A double-blind randomized phase I clinical trial targeting ALVAC-HIV vaccine to human dendritic cells. PLoS One 2011; 6:e24254.