Genomic analysis reveals pre-and postchallenge differences in a rhesus macaque AIDS vaccine trial: Insights into mechanisms of vaccine efficacy

Journal of Virology

Volumn 85, Issue 2, 2011, Pages 1099-1116

  Palermo, Robert E ^a   Patterson, L Jean ^b   Aicher, Lauri D ^a   Korth, Marcus J ^a   Robert Guroff, Marjorie ^b   Katze, Michael G ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT; GLYCOPROTEIN GP 140; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; INTERLEUKIN 27; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; RECOMBINANT VACCINE;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENOMICS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMORAL IMMUNITY; IMMUNE RESPONSE; MALE; NONHUMAN; PRIORITY JOURNAL; RHESUS MONKEY; VIREMIA;

ADENOVIRIDAE; AIDS VACCINES; ANIMALS; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENETIC VECTORS; HIV; IMMUNIZATION, SECONDARY; INJECTIONS, INTRAMUSCULAR; MACACA MULATTA; MALE; MICROARRAY ANALYSIS; RECOMBINATION, GENETIC; SAIDS VACCINES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VACCINATION; VIRAL LOAD; VIREMIA;

ANIMALIA; HUMAN ADENOVIRUS TYPE 5; HUMAN IMMUNODEFICIENCY VIRUS; LENTIVIRUS; MACACA MULATTA; SIMIAN IMMUNODEFICIENCY VIRUS; SIMIAN-HUMAN IMMUNODEFICIENCY VIRUS;

EID: 78650655851     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01522-10     Document Type: Article

References (111)

1. Aasa-Chapman, M. M., S. Holuigue, K. Aubin, M. Wong, N. A. Jones, D. Cornforth, P. Pellegrino, P. Newton, I. Williams, P. Borrow, and A. McKnight. 2005. Detection of antibody-dependent complement-mediated inactivation of both autologous and heterologous virus in primary human immunodeficiency virus type 1 infection. J. Virol. 79:2823-2830.
2. Abbas, A. K., and A. H. Lichtman. 2005. Cellular and molecular immunology, 5th ed., p. 189-215. Elsevier Saunders, Philadelphia, PA.
3. Adams, J. C. 2004. Roles of fascin in cell adhesion and motility. Curr. Opin. Cell Biol. 16:590-596.
4. Addo, M. M., X. G. Yu, A. Rathod, D. Cohen, R. L. Eldridge, D. Strick, M. N. Johnston, C. Corcoran, A. G. Wurcel, C. A. Fitzpatrick, M. E. Feeney, W. R. Rodriguez, N. Basgoz, R. Draenert, D. R. Stone, C. Brander, P. J. Goulder, E. S. Rosenberg, M. Altfeld, and B. D. Walker. 2003. Comprehensive epitope analysis of human immunodeficiency virus type 1 (HIV-1)-specific T-cell responses directed against the entire expressed HIV-1 genome demonstrate broadly directed responses, but no correlation to viral load. J. Virol. 77:2081-2092.
5. Aittomaki, S., J. Yang, E. W. Scott, M. C. Simon, and O. Silvennoinen. 2004. Molecular basis of Stat1 and PU. 1 cooperation in cytokine-induced Fcγ receptor I promoter activation. Int. Immunol. 16:265-274.
6. Al-Alwan, M. M., G. Rowden, T. D. Lee, and K. A. West. 2001. Fascin is involved in the antigen presentation activity of mature dendritic cells. J. Immunol. 166:338-345.
7. Ang, X. L., and J. Wade Harper. 2005. SCF-mediated protein degradation and cell cycle control. Oncogene 24:2860-2870.
8. Arguni, E., M. Arima, N. Tsuruoka, A. Sakamoto, M. Hatano, and T. Tokuhisa. 2006. JunD/AP-1 and STAT3 are the major enhancer molecules for high Bcl6 expression in germinal center B cells. Int. Immunol. 18:1079-1089.
9. Azam, S., E. Drobetsky, and D. Ramotar. 2007. Overexpression of the cis/trans isomerase PTPA triggers caspase 3-dependent apoptosis. Apoptosis 12:1243-1255.
10. Baas, T., C. R. Baskin, D. L. Diamond, A. Garcia-Sastre, H. Bielefeldt-Ohmann, T. M. Tumpey, M. J. Thomas, V. S. Carter, T. H. Teal, N. Van Hoeven, S. Proll, J. M. Jacobs, Z. R. Caldwell, M. A. Gritsenko, R. R. Hukkanen, D. G. Camp II, R. D. Smith, and M. G. Katze. 2006. Integrated molecular signature of disease: analysis of influenza virus-infected macaques through functional genomics and proteomics. J. Virol. 80:10813-10828.
11. Baechler, E. C., F. M. Batliwalla, G. Karypis, P. M. Gaffney, K. Moser, W. A. Ortmann, K. J. Espe, S. Balasubramanian, K. M. Hughes, J. P. Chan, A. Begovich, S. Y. Chang, P. K. Gregersen, and T. W. Behrens. 2004. Expression levels for many genes in human peripheral blood cells are highly sensitive to ex vivo incubation. Genes Immun. 5:347-353.
12. Balajee, A. S., and C. R. Geard. 2001. Chromatin-bound PCNA complex formation triggered by DNA damage occurs independent of the ATM gene product in human cells. Nucleic Acids Res. 29:1341-1351.
13. Barnett, S. W., B. Burke, Y. Sun, E. Kan, H. Legg, Y. Lian, K. Bost, F. Zhou, A. Goodsell, J. Zur Megede, J. Polo, J. Donnelly, J. Ulmer, G. R. Otten, C. J. Miller, M. Vajdy, and I. K. Srivastava. 2010. Antibody-mediated protection against mucosal simian-human immunodeficiency virus challenge of macaques immunized with alphavirus replicon particles and boosted with trimeric envelope glycoprotein in MF59 adjuvant. J. Virol. 84:5975-5985.
14. Barouch, D. H., J. Kunstman, M. J. Kuroda, J. E. Schmitz, S. Santra, F. W. Peyerl, G. R. Krivulka, K. Beaudry, M. A. Lifton, D. A. Gorgone, D. C. Montefiori, M. G. Lewis, S. M. Wolinsky, and N. L. Letvin. 2002. Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes. Nature 415:335-339.
15. Baskin, C. R., H. Bielefeldt-Ohmann, A. Garcia-Sastre, T. M. Tumpey, N. Van Hoeven, V. S. Carter, M. J. Thomas, S. Proll, A. Solorzano, R. Billharz, J. L. Fornek, S. Thomas, C. H. Chen, E. A. Clark, K. Murali-Krishna, and M. G. Katze. 2007. Functional genomic and serological analysis of the protective immune response resulting from vaccination of macaques with an NS1-truncated influenza virus. J. Virol. 81:11817-11827.
16. Baskin, C. R., H. Bielefeldt-Ohmann, T. M. Tumpey, P. J. Sabourin, J. P. Long, A. Garcia-Sastre, A. E. Tolnay, R. Albrecht, J. A. Pyles, P. H. Olson, L. D. Aicher, E. R. Rosenzweig, K. Murali-Krishna, E. A. Clark, M. S. Kotur, J. L. Fornek, S. Proll, R. E. Palermo, C. L. Sabourin, and M. G. Katze. 2009. Early and sustained innate immune response defines pathology and death in nonhuman primates infected by highly pathogenic influenza virus. Proc. Natl. Acad. Sci. U. S. A. 106:3455-3460.
17. Betts, M. R., D. R. Ambrozak, D. C. Douek, S. Bonhoeffer, J. M. Brenchley, J. P. Casazza, R. A. Koup, and L. J. Picker. 2001. Analysis of total human immunodeficiency virus (HIV)-specific CD4(+) and CD8(+) T-cell responses: relationship to viral load in untreated HIV infection. J. Virol. 75:11983-11991.
18. Bosinger, S. E., Q. Li, S. N. Gordon, N. R. Klatt, L. Duan, L. Xu, N. Francella, A. Sidahmed, A. J. Smith, E. M. Cramer, M. Zeng, D. Masopust, J. V. Carlis, L. Ran, T. H. Vanderford, M. Paiardini, R. B. Isett, D. A. Baldwin, J. G. Else, S. I. Staprans, G. Silvestri, A. T. Haase, and D. J. Kelvin. 2009. Global genomic analysis reveals rapid control of a robust innate response in SIV-infected sooty mangabeys. J. Clin. Invest. 119:3556-3572.
19. Bossen, C., and P. Schneider. 2006. BAFF, APRIL and their receptors: structure, function and signaling. Semin. Immunol. 18:263-275.
20. Bosshart, H., and M. Heinzelmann. 2002. Arginine-rich cationic polypeptides amplify lipopolysaccharide-induced monocyte activation. Infect. Immun. 70:6904-6910.
21. Brown, S. A., S. L. Surman, R. Sealy, B. G. Jones, K. S. Slobod, K. Branum, T. D. Lockey, N. Howlett, P. Freiden, P. Flynn, and J. L. Hurwitz. 2010. Heterologous prime-boost HIV-1 vaccination regimens in pre-clinical and clinical trials. Viruses 2:435-467.
22. Buchbinder, S. P., D. V. Mehrotra, A. Duerr, D. W. Fitzgerald, R. Mogg, D. Li, P. B. Gilbert, J. R. Lama, M. Marmor, C. Del Rio, M. J. McElrath, D. R. Casimiro, K. M. Gottesdiener, J. A. Chodakewitz, L. Corey, and M. N. Robertson. 2008. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 372:1881-1893.
23. Chan, E. Y., W. J. Qian, D. L. Diamond, T. Liu, M. A. Gritsenko, M. E. Monroe, D. G. Camp II, R. D. Smith, and M. G. Katze. 2007. Quantitative analysis of human immunodeficiency virus type 1-infected CD4+ cell proteome: dysregulated cell cycle progression and nuclear transport coincide with robust virus production. J. Virol. 81:7571-7583.
24. Chan, E. Y., J. N. Sutton, J. M. Jacobs, A. Bondarenko, R. D. Smith, and M. G. Katze. 2009. Dynamic host energetics and cytoskeletal proteomes in human immunodeficiency virus type 1-infected human primary CD4 cells: analysis by multiplexed label-free mass spectrometry. J. Virol. 83:9283-9295.
25. Churchill, G. A. 2002. Fundamentals of experimental design for cDNA microarrays. Nat. Genet. 32(Suppl.):490-495.
26. Cilloniz, C., M. J. Pantin-Jackwood, C. Ni, A. G. Goodman, X. Peng, S. C. Proll, V. S. Carter, E. R. Rosenzweig, K. J. Szretter, J. M. Katz, M. J. Korth, D. E. Swayne, T. M. Tumpey, and M. G. Katze. 2010. Lethal dissemination of H5N1 influenza virus is associated with dysregulation of inflammation and lipoxin signaling in a mouse model of infection. J. Virol. 84:7613-7624.
27. Cilloniz, C., K. Shinya, X. Peng, M. J. Korth, S. C. Proll, L. D. Aicher, V. S. Carter, J. H. Chang, D. Kobasa, F. Feldmann, J. E. Strong, H. Feldmann, Y. Kawaoka, and M. G. Katze. 2009. Lethal influenza virus infection in macaques is associated with early dysregulation of inflammatory related genes. PLoS Pathog. 5:e1000604.
28. Deeks, S. G., C. M. Kitchen, L. Liu, H. Guo, R. Gascon, A. B. Narvaez, P. Hunt, J. N. Martin, J. O. Kahn, J. Levy, M. S. McGrath, and F. M. Hecht. 2004. Immune activation set point during early HIV infection predicts subsequent CD4+ T-cell changes independent of viral load. Blood 104: 942-947.
29. de Lang, A., T. Baas, T. Teal, L. M. Leijten, B. Rain, A. D. Osterhaus, B. L. Haagmans, and M. G. Katze. 2007. Functional genomics highlights differential induction of antiviral pathways in the lungs of SARS-CoV-infected macaques. PLoS Pathog. 3:e112.
30. Demberg, T., R. H. Florese, M. J. Heath, K. Larsen, I. Kalisz, V. S. Kalyanaraman, E. M. Lee, R. Pal, D. Venzon, R. Grant, L. J. Patterson, B. Korioth-Schmitz, A. Buzby, D. Dombagoda, D. C. Montefiori, N. L. Letvin, A. Cafaro, B. Ensoli, and M. Robert-Guroff. 2007. A replication-competent adenovirus-human immunodeficiency virus (Ad-HIV) tat and Ad-HIV env priming/Tat and envelope protein boosting regimen elicits enhanced protective efficacy against simian/human immunodeficiency virus SHIV89.6P challenge in rhesus macaques. J. Virol. 81:3414-3427.
31. Dennis, G., Jr., B. T. Sherman, D. A. Hosack, J. Yang, W. Gao, H. C. Lane, and R. A. Lempicki. 2003. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 4:P3.
32. Duerr, A., J. N. Wasserheit, and L. Corey. 2006. HIV vaccines: new frontiers in vaccine development. Clin. Infect. Dis. 43:500-511.
33. Duncan, R., L. Bazar, G. Michelotti, T. Tomonaga, H. Krutzsch, M. Avigan, and D. Levens. 1994. A sequence-specific, single-strand binding protein activates the far upstream element of c-myc and defines a new DNAbinding motif. Genes Dev. 8:465-480.
34. Emslie, D., K. D'Costa, J. Hasbold, D. Metcalf, K. Takatsu, P. O. Hodgkin, and L. M. Corcoran. 2008. Oct2 enhances antibody-secreting cell differentiation through regulation of IL-5 receptor alpha chain expression on activated B cells. J. Exp. Med. 205:409-421.
35. Fakruddin, J. M., R. A. Lempicki, R. J. Gorelick, J. Yang, J. W. Adelsberger, A. J. Garcia-Pineres, L. A. Pinto, H. C. Lane, and T. Imamichi. 2007. Noninfectious papilloma virus-like particles inhibit HIV-1 replication: implications for immune control of HIV-1 infection by IL-27. Blood 109:1841-1849.
36. Fan, H., and P. S. Hegde. 2005. The transcriptome in blood: challenges and solutions for robust expression profiling. Curr. Mol. Med. 5:3-10.
37. Favre, D., S. Lederer, B. Kanwar, Z. M. Ma, S. Proll, Z. Kasakow, J. Mold, L. Swainson, J. D. Barbour, C. R. Baskin, R. Palermo, I. Pandrea, C. J. Miller, M. G. Katze, and J. M. McCune. 2009. Critical loss of the balance between Th17 and T regulatory cell populations in pathogenic SIV infection. PLoS Pathog. 5:e1000295.
38. Fellay, J., K. V. Shianna, D. Ge, S. Colombo, B. Ledergerber, M. Weale, K. Zhang, C. Gumbs, A. Castagna, A. Cossarizza, A. Cozzi-Lepri, A. De Luca, P. Easterbrook, P. Francioli, S. Mallal, J. Martinez-Picado, J. M. Miro, N. Obel, J. P. Smith, J. Wyniger, P. Descombes, S. E. Antonarakis, N. L. Letvin, A. J. McMichael, B. F. Haynes, A. Telenti, and D. B. Goldstein. 2007. A whole-genome association study of major determinants for host control of HIV-1. Science 317:944-947.
39. Florese, R. H., T. Demberg, P. Xiao, L. Kuller, K. Larsen, L. E. Summers, D. Venzon, A. Cafaro, B. Ensoli, and M. Robert-Guroff. 2009. Contribution of nonneutralizing vaccine-elicited antibody activities to improved protective efficacy in rhesus macaques immunized with Tat/Env compared with multigenic vaccines. J. Immunol. 182:3718-3727.
40. Franke, T. F., C. P. Hornik, L. Segev, G. A. Shostak, and C. Sugimoto. 2003. PI3K/Akt and apoptosis: size matters. Oncogene 22:8983-8998.
41. Garrison, S. P., J. R. Jeffers, C. Yang, J. A. Nilsson, M. A. Hall, J. E. Rehg, W. Yue, J. Yu, L. Zhang, M. Onciu, J. T. Sample, J. L. Cleveland, and G. P. Zambetti. 2008. Selection against PUMA gene expression in Myc-driven B-cell lymphomagenesis. Mol. Cell. Biol. 28:5391-5402.
42. Gaucher, D., R. Therrien, N. Kettaf, B. R. Angermann, G. Boucher, A. Filali-Mouhim, J. M. Moser, R. S. Mehta, D. R. Drake III, E. Castro, R. Akondy, A. Rinfret, B. Yassine-Diab, E. A. Said, Y. Chouikh, M. J. Cameron, R. Clum, D. Kelvin, R. Somogyi, L. D. Greller, R. S. Balderas, P. Wilkinson, G. Pantaleo, J. Tartaglia, E. K. Haddad, and R. P. Sekaly. 2008. Yellow fever vaccine induces integrated multilineage and polyfunctional immune responses. J. Exp. Med. 205:3119-3131.
43. George, M. D., D. Verhoeven, Z. McBride, and S. Dandekar. 2006. Gene expression profiling of gut mucosa and mesenteric lymph nodes in simian immunodeficiency virus-infected macaques with divergent disease course. J. Med. Primatol. 35:261-269.
44. Gomez-Roman, V. R., L. J. Patterson, D. Venzon, D. Liewehr, K. Aldrich, R. Florese, and M. Robert-Guroff. 2005. Vaccine-elicited antibodies mediate antibody-dependent cellular cytotoxicity correlated with significantly reduced acute viremia in rhesus macaques challenged with SIVmac251. J. Immunol. 174:2185-2189.
45. Goulder, P. J., and D. I. Watkins. 2008. Impact of MHC class I diversity on immune control of immunodeficiency virus replication. Nat. Rev. Immunol. 8:619-630.
46. Grandori, C., S. M. Cowley, L. P. James, and R. N. Eisenman. 2000. The Myc/Max/Mad network and the transcriptional control of cell behavior. Annu. Rev. Cell Dev. Biol. 16:653-699.
47. Greasley, P. J., C. Bonnard, and B. Amati. 2000. Myc induces the nucleolin and BN51 genes: possible implications in ribosome biogenesis. Nucleic Acids Res. 28:446-453.
48. Hidajat, R., P. Xiao, Q. Zhou, D. Venzon, L. E. Summers, V. S. Kalyanaraman, D. C. Montefiori, and M. Robert-Guroff. 2009. Correlation of vaccineelicited systemic and mucosal nonneutralizing antibody activities with reduced acute viremia following intrarectal simian immunodeficiency virus SIVmac251 challenge of rhesus macaques. J. Virol. 83:791-801.
49. Hipfner, D. R., and S. M. Cohen. 2004. Connecting proliferation and apoptosis in development and disease. Nat. Rev. Mol. Cell Biol. 5:805-815.
50. Huang da, W., B. T. Sherman, and R. A. Lempicki. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4:44-57.
51. Huber, M., M. Fischer, B. Misselwitz, A. Manrique, H. Kuster, B. Niederost, R. Weber, V. von Wyl, H. F. Gunthard, and A. Trkola. 2006. Com-plement lysis activity in autologous plasma is associated with lower viral loads during the acute phase of HIV-1 infection. PLoS Med. 3:e441.
52. Huynh, K. D., W. Fischle, E. Verdin, and V. J. Bardwell. 2000. BCoR, a novel corepressor involved in BCL-6 repression. Genes Dev. 14:1810-1823.
53. Inui, S., K. Kuwahara, J. Mizutani, K. Maeda, T. Kawai, H. Nakayasu, and N. Sakaguchi. 1995. Molecular cloning of a cDNA clone encoding a phosphoprotein component related to the Ig receptor-mediated signal transduction. J. Immunol. 154:2714-2723.
54. Jacquelin, B., V. Mayau, B. Targat, A. S. Liovat, D. Kunkel, G. Petitjean, M. A. Dillies, P. Roques, C. Butor, G. Silvestri, L. D. Giavedoni, P. Lebon, F. Barre-Sinoussi, A. Benecke, and M. C. Muller-Trutwin. 2009. Nonpathogenic SIV infection of African green monkeys induces a strong but rapidly controlled type I IFN response. J. Clin. Invest. 119:3544-3555.
55. Jourdan, M., A. Caraux, J. De Vos, G. Fiol, M. Larroque, C. Cognot, C. Bret, C. Duperray, D. Hose, and B. Klein. 2009. An in vitro model of differentiation of memory B cells into plasmablasts and plasma cells including detailed phenotypic and molecular characterization. Blood 114:5173-5181.
56. Juliano, R. L. 2002. Signal transduction by cell adhesion receptors and the cytoskeleton: functions of integrins, cadherins, selectins, and immunoglobulin-superfamily members. Annu. Rev. Pharmacol. Toxicol. 42:283-323.
57. Katze, M. G., J. L. Fornek, R. E. Palermo, K. A. Walters, and M. J. Korth. 2008. Innate immune modulation by RNA viruses: emerging insights from functional genomics. Nat. Rev. Immunol. 8:644-654.
58. Kipps, T. J. 2006. Chapter 14. The cluster of differentiation (CD) antigens. In M. A. Lichtman, E. Beutler, T. J. Kipps, U. Seligsohn, K. Kaushansky, and J. T. Prchal (ed.), Williams hematology, 7th ed. McGraw-Hill, New York, NY.
59. Klatt, N. R., E. Shudo, A. M. Ortiz, J. C. Engram, M. Paiardini, B. Lawson, M. D. Miller, J. Else, I. Pandrea, J. D. Estes, C. Apetrei, J. E. Schmitz, R. M. Ribeiro, A. S. Perelson, and G. Silvestri. 2010. CD8+ lymphocytes control viral replication in SIVmac239-infected rhesus macaques without decreasing the lifespan of productively infected cells. PLoS Pathog. 6:e1000747.
60. Kobasa, D., S. M. Jones, K. Shinya, J. C. Kash, J. Copps, H. Ebihara, Y. Hatta, J. H. Kim, P. Halfmann, M. Hatta, F. Feldmann, J. B. Alimonti, L. Fernando, Y. Li, M. G. Katze, H. Feldmann, and Y. Kawaoka. 2007. Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 445:319-323.
61. Lederer, S., D. Favre, K. A. Walters, S. Proll, B. Kanwar, Z. Kasakow, C. R. Baskin, R. Palermo, J. M. McCune, and M. G. Katze. 2009. Transcriptional profiling in pathogenic and non-pathogenic SIV infections reveals significant distinctions in kinetics and tissue compartmentalization. PLoS Pathog. 5:e1000296.
62. Lee, T. D., M. L. Gonzalez, P. Kumar, P. Grammas, and H. A. Pereira. 2003. CAP37, a neutrophil-derived inflammatory mediator, augments leukocyte adhesion to endothelial monolayers. Microvasc. Res. 66:38-48.
63. Letvin, N. L. 2007. Correlates of immune protection and the development of a human immunodeficiency virus vaccine. Immunity 27:366-369.
64. Li, X., A. Zimmerman, N. G. Copeland, D. J. Gilbert, N. A. Jenkins, and H. L. Yin. 1996. The mouse thymosin beta 4 gene: structure, promoter identification, and chromosome localization. Genomics 32:388-394.
65. Li, Y., E. Y. Chan, and M. G. Katze. 2007. Functional genomics analyses of differential macaque peripheral blood mononuclear cell infections by human immunodeficiency virus-1 and simian immunodeficiency virus. Virology 366:137-149.
66. Lubeck, M. D., R. Natuk, M. Myagkikh, N. Kalyan, K. Aldrich, F. Sinangil, S. Alipanah, S. C. Murthy, P. K. Chanda, S. M. Nigida, Jr., P. D. Markham, S. Zolla-Pazner, K. Steimer, M. Wade, M. S. Reitz, Jr., L. O. Arthur, S. Mizutani, A. Davis, P. P. Hung, R. C. Gallo, J. Eichberg, and M. Robert-Guroff. 1997. Long-term protection of chimpanzees against high-dose HIV-1 challenge induced by immunization. Nat. Med. 3:651-658.
67. Malkevitch, N. V., L. J. Patterson, M. K. Aldrich, Y. Wu, D. Venzon, R. H. Florese, V. S. Kalyanaraman, R. Pal, E. M. Lee, J. Zhao, A. Cristillo, and M. Robert-Guroff. 2006. Durable protection of rhesus macaques immunized with a replicating adenovirus-SIV multigene prime/protein boost vaccine regimen against a second SIVmac251 rectal challenge: role of SIV-specific CD8+ T cell responses. Virology 353:83-98.
68. McElrath, M. J., S. C. De Rosa, Z. Moodie, S. Dubey, L. Kierstead, H. Janes, O. D. Defawe, D. K. Carter, J. Hural, R. Akondy, S. P. Buchbinder, M. N. Robertson, D. V. Mehrotra, S. G. Self, L. Corey, J. W. Shiver, and D. R. Casimiro. 2008. HIV-1 vaccine-induced immunity in the test-ofconcept Step Study: a case-cohort analysis. Lancet 372:1894-1905.
69. Milutinovic, S., Q. Zhuang, and M. Szyf. 2002. Proliferating cell nuclear antigen associates with histone deacetylase activity, integrating DNA replication and chromatin modification. J. Biol. Chem. 277:20974-20978.
70. Mistry, A. R., and C. A. O'Callaghan. 2007. Regulation of ligands for the activating receptor NKG2D. Immunology 121:439-447.
71. Morrow, G., L. Vachot, P. Vagenas, and M. Robbiani. 2008. Current concepts of HIV transmission. Curr. Infect. Dis. Rep. 10:133-139.
72. Murphy, D. J., M. R. Junttila, L. Pouyet, A. Karnezis, K. Shchors, D. A. Bui, L. Brown-Swigart, L. Johnson, and G. I. Evan. 2008. Distinct thresholds govern Myc's biological output in vivo. Cancer Cell 14:447-457.
73. Neil, S. J., T. Zang, and P. D. Bieniasz. 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425-430.
74. Nomura, M., S. Shimizu, T. Sugiyama, M. Narita, T. Ito, H. Matsuda, and Y. Tsujimoto. 2003. 14-3-3 interacts directly with and negatively regulates pro-apoptotic Bax. J. Biol. Chem. 278:2058-2065.
75. Ohtsuka, T., H. Ryu, Y. A. Minamishima, S. Macip, J. Sagara, K. I. Nakayama, S. A. Aaronson, and S. W. Lee. 2004. ASC is a Bax adaptor and regulates the p53-Bax mitochondrial apoptosis pathway. Nat. Cell Biol. 6:121-128.
76. Patterson, L. J., J. Beal, T. Demberg, R. H. Florese, N. Malkevich, D. Venzon, K. Aldrich, E. Richardson, V. S. Kalyanaraman, I. Kalisz, E. M. Lee, D. C. Montefiori, F. A. Robey, and M. Robert-Guroff. 2008. Replicating adenovirus HIV/SIV recombinant priming alone or in combination with a gp140 protein boost results in significant control of viremia following a SHIV89.6P challenge in Mamu-A*01 negative rhesus macaques. Virology 374:322-337.
77. Patterson, L. J., N. Malkevitch, D. Venzon, J. Pinczewski, V. R. Gomez-Roman, L. Wang, V. S. Kalyanaraman, P. D. Markham, F. A. Robey, and M. Robert-Guroff. 2004. Protection against mucosal simian immunodeficiency virus SIV(mac251) challenge by using replicating adenovirus-SIV multigene vaccine priming and subunit boosting. J. Virol. 78:2212-2221.
78. Peng, X., E. Y. Chan, Y. Li, D. L. Diamond, M. J. Korth, and M. G. Katze. 2009. Virus-host interactions: from systems biology to translational research. Curr. Opin. Microbiol. 12:432-438.
79. Pereyra, F., S. Palmer, T. Miura, B. L. Block, A. Wiegand, A. C. Rothchild, B. Baker, R. Rosenberg, E. Cutrell, M. S. Seaman, J. M. Coffin, and B. D. Walker. 2009. Persistent low-level viremia in HIV-1 elite controllers and relationship to immunologic parameters. J. Infect. Dis. 200:984-990.
80. Pflanz, S., J. C. Timans, J. Cheung, R. Rosales, H. Kanzler, J. Gilbert, L. Hibbert, T. Churakova, M. Travis, E. Vaisberg, W. M. Blumenschein, J. D. Mattson, J. L. Wagner, W. To, S. Zurawski, T. K. McClanahan, D. M. Gorman, J. F. Bazan, R. de Waal Malefyt, D. Rennick, and R. A. Kastelein. 2002. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4(+) T cells. Immunity 16:779-790.
81. Plevy, S. E., J. H. Gemberling, S. Hsu, A. J. Dorner, and S. T. Smale. 1997. Multiple control elements mediate activation of the murine and human interleukin 12 p40 promoters: evidence of functional synergy between C/EBP and Rel proteins. Mol. Cell. Biol. 17:4572-4588.
82. Ploix, C., D. Lo, and M. J. Carson. 2001. A ligand for the chemokine receptor CCR7 can influence the homeostatic proliferation of CD4 T cells and progression of autoimmunity. J. Immunol. 167:6724-6730.
83. Querec, T. D., R. S. Akondy, E. K. Lee, W. Cao, H. I. Nakaya, D. Teuwen, A. Pirani, K. Gernert, J. Deng, B. Marzolf, K. Kennedy, H. Wu, S. Bennouna, H. Oluoch, J. Miller, R. Z. Vencio, M. Mulligan, A. Aderem, R. Ahmed, and B. Pulendran. 2009. Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat. Immunol. 10:116-125.
84. Reid, S., and E. C. Snow. 1996. The regulated expression of cell cyclerelated proteins as B-lymphocytes enter and progress through the G1 cell cycle stage following delivery of complete versus partial activation stimuli. Mol. Immunol. 33:1139-1151.
85. Rerks-Ngarm, S., P. Pitisuttithum, S. Nitayaphan, J. Kaewkungwal, J. Chiu, R. Paris, N. Premsri, C. Namwat, M. de Souza, E. Adams, M. Benenson, S. Gurunathan, J. Tartaglia, J. G. McNeil, D. P. Francis, D. Stablein, D. L. Birx, S. Chunsuttiwat, C. Khamboonruang, P. Thongcharoen, M. L. Robb, N. L. Michael, P. Kunasol, and J. H. Kim. 2009. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361:2209-2220.
86. Robert-Guroff, M., H. Kaur, L. J. Patterson, M. Leno, A. J. Conley, P. M. McKenna, P. D. Markham, E. Richardson, K. Aldrich, K. Arora, L. Murty, L. Carter, S. Zolla-Pazner, and F. Sinangil. 1998. Vaccine protection against a heterologous, non-syncytium-inducing, primary human immunodeficiency virus. J. Virol. 72:10275-10280.
87. San-Marina, S., Y. Han, F. Suarez Saiz, M. R. Trus, and M. D. Minden. 2008. Lyl1 interacts with CREB1 and alters expression of CREB1 target genes. Biochim. Biophys. Acta 1783:503-517.
88. Schmitz, J. E., M. J. Kuroda, S. Santra, V. G. Sasseville, M. A. Simon, M. A. Lifton, P. Racz, K. Tenner-Racz, M. Dalesandro, B. J. Scallon, J. Ghrayeb, M. A. Forman, D. C. Montefiori, E. P. Rieber, N. L. Letvin, and K. A. Reimann. 1999. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283:857-860.
89. Schroder, K., P. J. Hertzog, T. Ravasi, and D. A. Hume. 2004. Interferongamma: an overview of signals, mechanisms and functions. J. Leukoc. Biol. 75:163-189.
90. Schwartz, O., V. Marechal, S. Le Gall, F. Lemonnier, and J. M. Heard. 1996. Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat. Med. 2:338-342.
91. Shen-Orr, S. S., R. Tibshirani, P. Khatri, D. L. Bodian, F. Staedtler, N. M. Perry, T. Hastie, M. M. Sarwal, M. M. Davis, and A. J. Butte. 2010. Cell type-specific gene expression differences in complex tissues. Nat. Methods 7:287-289.
92. Smider, V., and G. Chu. 1997. The end-joining reaction in V(D)J recombination. Semin. Immunol. 9:189-197.
93. Stoughton, R., and H. Dai. February 2002. Statistical combining of cell expression profiles. U.S. patent 6,351,712.
94. Stumptner-Cuvelette, P., S. Morchoisne, M. Dugast, S. Le Gall, G. Raposo, O. Schwartz, and P. Benaroch. 2001. HIV-1 Nef impairs MHC class II antigen presentation and surface expression. Proc. Natl. Acad. Sci. U. S. A. 98:12144-12149.
95. Su, A. I., T. Wiltshire, S. Batalov, H. Lapp, K. A. Ching, D. Block, J. Zhang, R. Soden, M. Hayakawa, G. Kreiman, M. P. Cooke, J. R. Walker, and J. B. Hogenesch. 2004. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. U. S. A. 101:6062-6067.
96. Swanson, J. A., and A. D. Hoppe. 2004. The coordination of signaling during Fc receptor-mediated phagocytosis. J. Leukoc. Biol. 76:1093-1103.
97. Takino, T., M. Nakada, H. Miyamori, Y. Watanabe, T. Sato, D. Gantulga, K. Yoshioka, K. M. Yamada, and H. Sato. 2005. JSAP1/JIP3 cooperates with focal adhesion kinase to regulate c-Jun N-terminal kinase and cell migration. J. Biol. Chem. 280:37772-37781.
98. Tang, S. W., W. H. Chang, Y. C. Su, Y. C. Chen, Y. H. Lai, P. T. Wu, C. I. Hsu, W. C. Lin, M. K. Lai, and J. Y. Lin. 2009. MYC pathway is activated in clear cell renal cell carcinoma and essential for proliferation of clear cell renal cell carcinoma cells. Cancer Lett. 273:35-43.
99. Tarlinton, D., A. Radbruch, F. Hiepe, and T. Dorner. 2008. Plasma cell differentiation and survival. Curr. Opin. Immunol. 20:162-169.
100. Thomas, M. J., M. B. Agy, S. C. Proll, B. W. Paeper, Y. Li, K. L. Jensen, M. J. Korth, and M. G. Katze. 2006. Functional gene analysis of individual response to challenge of SIVmac239 in M. mulatta PBMC culture. Virology 348:242-252.
101. Tian, M. T., G. Gonzalez, B. Scheer, and A. L. DeFranco. 2005. Bcl10 can promote survival of antigen-stimulated B lymphocytes. Blood 106:2105-2112.
102. van Grevenynghe, J., F. A. Procopio, Z. He, N. Chomont, C. Riou, Y. Zhang, S. Gimmig, G. Boucher, P. Wilkinson, Y. Shi, B. Yassine-Diab, E. A. Said, L. Trautmann, M. El Far, R. S. Balderas, M. R. Boulassel, J. P. Routy, E. K. Haddad, and R. P. Sekaly. 2008. Transcription factor FOXO3a controls the persistence of memory CD4(+) T cells during HIV infection. Nat. Med. 14:266-274.
103. van Grevenynghe, J., R. Halwani, N. Chomont, P. Ancuta, Y. Peretz, A. Tanel, F. A. Procopio, Y. shi, E. A. Said, E. K. Haddad, and R. P. Sekaly. 2008. Lymph node architecture collapse and consequent modulation of FOXO3a pathway on memory T-and B-cells during HIV infection. Semin. Immunol. 20:196-203.
104. van 't Wout, A. B., G. K. Lehrman, S. A. Mikheeva, G. C. O'Keeffe, M. G. Katze, R. E. Bumgarner, G. K. Geiss, and J. I. Mullins. 2003. Cellular gene expression upon human immunodeficiency virus type 1 infection of CD4(+)-T-cell lines. J. Virol. 77:1392-1402.
105. Wallace, J. C., M. J. Korth, B. Paeper, S. C. Proll, M. J. Thomas, C. L. Magness, S. P. Iadonato, C. Nelson, and M. G. Katze. 2007. High-density rhesus macaque oligonucleotide microarray design using early-stage rhesus genome sequence information and human genome annotations. BMC Genomics 8:28.
106. Wong, J. K., M. C. Strain, R. Porrata, E. Reay, S. Sankaran-Walters, C. C. Ignacio, T. Russell, S. K. Pillai, D. J. Looney, and S. Dandekar. 2010. In vivo CD8+ T-cell suppression of SIV viremia is not mediated by CTL clearance of productively infected cells. PLoS Pathog. 6:e1000748.
107. Xiao, P., J. Zhao, L. J. Patterson, E. Brocca-Cofano, D. Venzon, P. A. Kozlowski, R. Hidajat, T. Demberg, and M. Robert-Guroff. 2010. Multiple vaccine-elicited nonneutralizing antienvelope antibody activities contribute to protective efficacy by reducing both acute and chronic viremia following simian/human immunodeficiency virus SHIV89.6P challenge in rhesus macaques. J. Virol. 84:7161-7173.
108. Yang, Y. H., and T. Speed. 2002. Design issues for cDNA microarray experiments. Nat. Rev. Genet. 3:579-588.
109. Ye, H., A. Dogan, L. Karran, T. G. Willis, L. Chen, I. Wlodarska, M. J. Dyer, P. G. Isaacson, and M. Q. Du. 2000. BCL10 expression in normal and neoplastic lymphoid tissue. Nuclear localization in MALT lymphoma. Am. J. Pathol. 157:1147-1154.
110. Zhan, F., E. Tian, K. Bumm, R. Smith, B. Barlogie, and J. Shaughnessy, Jr. 2003. Gene expression profiling of human plasma cell differentiation and classification of multiple myeloma based on similarities to distinct stages of late-stage B-cell development. Blood 101:1128-1140.
111. Zhou, Q., R. Hidajat, B. Peng, D. Venzon, M. K. Aldrich, E. Richardson, E. M. Lee, V. S. Kalyanaraman, G. Grimes, V. R. Gomez-Roman, L. E. Summers, N. Malkevich, and M. Robert-Guroff. 2007. Comparative evaluation of oral and intranasal priming with replication-competent adenovirus 5 host range mutant (Ad5hr)-simian immunodeficiency virus (SIV) recombinant vaccines on immunogenicity and protective efficacy against SIV-(mac251). Vaccine 25:8021-8035.