GM-CSF DNA: An adjuvant for higher avidity IgG, rectal IgA, and increased protection against the acute phase of a SHIV-89.6P challenge by a DNA/MVA immunodeficiency virus vaccine

Virology

Volumn 369, Issue 1, 2007, Pages 153-167

  Lai, Lilin ^a   Vödrös, Dalma ^a   Kozlowski, Pamela A ^b   Montefiori, David C ^c   Wilson, Robert L ^b   Akerstrom, Vicki L ^b   Chennareddi, Lakshmi ^a   Yu, Tianwei ^a,d   Kannanganat, Sunil ^a   Ofielu, Lazarus ^a   Villinger, Francois ^e   Wyatt, Linda S ^f   Moss, Bernard ^f   Amara, Rama Rao ^a   Robinson, Harriet L ^a  

^a EMORY UNIVERSITY   (United States)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d EMORY UNIVERSITY   (United States)

^e EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Ab avidity; GM CSF adjuvant; Immunodeficiency virus; Rectal IgA; Vaccine

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR VACCINE; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G;

ANTIBODY RESPONSE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; T LYMPHOCYTE; VIREMIA;

ADJUVANTS, IMMUNOLOGIC; AIDS VACCINES; ANIMALS; ANTIBODIES, VIRAL; ANTIBODY AFFINITY; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; IMMUNIZATION, SECONDARY; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INJECTIONS, INTRADERMAL; INJECTIONS, INTRAMUSCULAR; MACACA MULATTA; RECTUM; SAIDS VACCINES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; VACCINES, DNA; VACCINIA VIRUS; VIRAL LOAD; VIRAL VACCINES; VIREMIA;

ANIMALIA; SIMIAN-HUMAN IMMUNODEFICIENCY VIRUS;

EID: 35649027418     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2007.07.017     Document Type: Article

References (52)

1. Allen T.M., Sidney J., del Guercio M.F., Glickman R.L., Lensmeyer G.L., Wiebe D.A., DeMars R., Pauza C.D., Johnson R.P., Sette A., and Watkins D.I. Characterization of the peptide binding motif of a rhesus MHC class I molecule (Mamu-A*01) that binds an immunodominant CTL epitope from simian immunodeficiency virus. J. Immunol. 160 12 (1998) 6062-6071
2. Amara R.R., Villinger F., Altman J.D., Lydy S.L., O'Neil S.P., Staprans S., Montefiori D.C., Xu Y., Herndon J.G., Wyatt L.S., Candido M.A., Kozyr N.L., Earl P.L., Smith J.M., Ma H.-L., Grimm B.D., Hulsey M.L., Miller J., McClure H.M., McNicholl J.M., Moss B., and Robinson H.L. Control of a mucosal challenge and prevention of AIDS by a multiprotein DNA/MVA vaccine. Science 292 (2001) 69-74
3. Amara R.R., Smith J.M., Staprans S.I., Montefiori D.C., Villinger F., Altman J.D., O'Neil S.P., Kozyr N.L., Xu Y., Wyatt L.S., Earl P.L., Herndon J.G., McNicholl J.M., McClure H.M., Moss B., and Robinson H.L. Critical role for Env as well as Gag-Pol in control of a simian-human immunodeficiency virus 89.6P challenge by a DNA prime/recombinant modified vaccinia virus Ankara vaccine. J. Virol. 76 12 (2002) 6138-6146
4. Banchereau J., and Steinman R.M. Dendritic cells and the control of immunity. Nature 392 6673 (1998) 245-252
5. Barouch D.H., Santra S., Tenner-Racz K., Racz P., Kuroda M.J., Schmitz J.E., Jackson S.S., Lifton M.A., Freed D.C., Perry H.C., Davies M.E., Shiver J.W., and Letvin N.L. Potent CD4+ T cell responses elicited by a bicistronic HIV-1 DNA vaccine expressing gp120 and GM-CSF. J. Immunol. 168 2 (2002) 562-568
6. Bertley F.M., Kozlowski P.A., Wang S.W., Chappelle J., Patel J., Sonuyi O., Mazzara G., Montefiori D., Carville A., Mansfield K.G., and Aldovini A. Control of simian/human immunodeficiency virus viremia and disease progression after IL-2-augmented DNA-modified vaccinia virus Ankara nasal vaccination in nonhuman primates. J. Immunol. 172 6 (2004) 3745-3757
7. Borrello I., and Pardoll D. GM-CSF-based cellular vaccines: a review of the clinical experience. Cytokine Growth Factor Rev. 13 2 (2002) 185-193
8. Burdin N., Galibert L., Garrone P., Durand I., Banchereau J., and Rousset F. Inability to produce IL-6 is a functional feature of human germinal center B lymphocytes. J. Immunol. 156 11 (1996) 4107-4113
9. Cole K.S., Rowles J.L., Jagerski B.A., Murphey-Corb M., Unangst T., Clements J.E., Robinson J., Wyand M.S., Desrosiers R.C., and Montelaro R.C. Evolution of envelope-specific antibody responses in monkeys experimentally infected or immunized with simian immunodeficiency virus and its association with the development of protective immunity. J. Virol. 71 7 (1997) 5069-5079
10. Connick E., Marr D.G., Zhang X.Q., Clark S.J., Saag M.S., Schooley R.T., and Curiel T.J. HIV-specific cellular and humoral immune responses in primary HIV infection. AIDS Res. Hum. Retroviruses 12 12 (1996) 1129-1140
11. Dranoff G., Jaffee E., Lazenby A., Golumbek P., Levitsky H., Brose K., Jackson V., Hamada H., Pardoll D., and Mulligan R.C. Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc. Natl. Acad. Sci. U. S. A. 90 8 (1993) 3539-3543
12. Edwards T.G., Wyss S., Reeves J.D., Zolla-Pazner S., Hoxie J.A., Doms R.W., and Baribaud F. Truncation of the cytoplasmic domain induces exposure of conserved regions in the ectodomain of human immunodeficiency virus type 1 envelope protein. J. Virol. 76 6 (2002) 2683-2691
13. Evans R., Shultz L.D., Dranoff G., Fuller J.A., and Kamdar S.J. CSF-1 regulation of Il6 gene expression by murine macrophages: a pivotal role for GM-CSF. J. Leukoc. Biol. 64 6 (1998) 810-816
14. Forthal D.N., Gilbert P.B., Landucci G., and Phan T. Recombinant gp120 vaccine-induced antibodies inhibit clinical strains of HIV-1 in the presence of Fc receptor-bearing effector cells and correlate inversely with HIV infection rate. J. Immunol. 178 10 (2007) 6596-6603
15. Geissler M., Gesien A., Tokushige K., and Wands J.R. Enhancement of cellular and humoral immune responses to hepatitis C virus core protein using DNA-based vaccines augmented with cytokine-expressing plasmids. J. Immunol. 158 3 (1997) 1231-1237
16. Gomez-Roman V.R., Patterson L.J., Venzon D., Liewehr D., Aldrich K., Florese R., and Robert-Guroff M. Vaccine-elicited antibodies mediate antibody-dependent cellular cytotoxicity correlated with significantly reduced acute viremia in rhesus macaques challenged with SIVmac251. J. Immunol. 174 4 (2005) 2185-2189
17. Hofmann-Lehmann R., Swenerton R.K., Liska V., Leutenegger C.M., Lutz H., McClure H.M., and Ruprecht R.M. Sensitive and robust one-tube real-time reverse transcriptase-polymerase chain reaction to quantify SIV RNA load: comparison of one- versus two-enzyme systems. AIDS Res. Hum. Retroviruses 16 13 (2000) 1247-1257
18. Huber M., Fischer M., Misselwitz B., Manrique A., Kuster H., Niederost B., Weber R., von Wyl V., Gunthard H.F., and Trkola A. Complement lysis activity in autologous plasma is associated with lower viral loads during the acute phase of HIV-1 infection. PLoS Med. 3 11 (2006) e441
19. Inaba K., Inaba M., Romani N., Aya H., Deguchi M., Ikehara S., Muramatsu S., and Steinman R.M. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 176 6 (1992) 1693-1702
20. Kamath A.T., Hanke T., Briscoe H., and Britton W.J. Co-immunization with DNA vaccines expressing granulocyte-macrophage colony-stimulating factor and mycobacterial secreted proteins enhances T-cell immunity, but not protective efficacy against Mycobacterium tuberculosis. Immunology 96 4 (1999) 511-516
21. Karlsson G.B., Halloran M., Li J., Park I.W., Gomila R., Reimann K.A., Axthelm M.K., Iliff S.A., Letvin N.L., and Sodroski J. Characterization of molecularly cloned simian-human immunodeficiency viruses causing rapid CD4+ lymphocyte depletion in rhesus monkeys. J. Virol. 71 6 (1997) 4218-4225
22. Kopf M., Herren S., Wiles M.V., Pepys M.B., and Kosco-Vilbois M.H. Interleukin 6 influences germinal center development and antibody production via a contribution of C3 complement component. J. Exp. Med. 188 10 (1998) 1895-1906
23. Kozlowski P.A., Lynch R.M., Patterson R.R., Cu-Uvin S., Flanigan T.P., and Neutra M.R. Modified wick method using Weck-Cel sponges for collection of human rectal secretions and analysis of mucosal HIV antibody. J. Acquir. Immune Defic. Syndr. 24 4 (2000) 297-309
24. Kumar S., Villinger F., Oakley M., Aguiar J.C., Jones T.R., Hedstrom R.C., Gowda K., Chute J., Stowers A., Kaslow D.C., Thomas E.K., Tine J., Klinman D., Hoffman S.L., and Weiss W.W. A DNA vaccine encoding the 42 kDa C-terminus of merozoite surface protein 1 of Plasmodium falciparum induces antibody, interferon-gamma and cytotoxic T cell responses in rhesus monkeys: immuno-stimulatory effects of granulocyte macrophage-colony stimulating factor. Immunol. Lett. 81 1 (2002) 13-24
25. Lee S.W., Cho J.H., and Sung Y.C. Optimal induction of hepatitis C virus envelope-specific immunity by bicistronic plasmid DNA inoculation with the granulocyte-macrophage colony-stimulating factor gene. J. Virol. 72 10 (1998) 8430-8436
26. Li M., Gao F., Mascola J.R., Stamatatos L., Polonis V.R., Koutsoukos M., Voss G., Goepfert P., Gilbert P., Greene K.M., Bilska M., Kothe D.L., Salazar-Gonzalez J.F., Wei X., Decker J.M., Hahn B.H., and Montefiori D.C. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J. Virol. 79 16 (2005) 10108-10125
27. Lifson J.D., Nowak M.A., Goldstein S., Rossio J.L., Kinter A., Vasquez G., Wiltrout T.A., Brown C., Schneider D., Wahl L., Lloyd A.L., Williams J., Elkins W.R., Fauci A.S., and Hirsch V.M. The extent of early viral replication is a critical determinant of the natural history of simian immunodeficiency virus infection. J. Virol. 71 12 (1997) 9508-9514
28. Mathers C.D., and Loncar D. Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med. 3 11 (2006) e442
29. Montefiori D.C. Role of complement and Fc receptors in the pathogenesis of HIV-1 infection. Springer Semin. Immunopathol. 18 3 (1997) 371-390
30. Montefiori D.C. Evaluating neutralizing antibodies against HIV, SIV and SHIV in a luciferase reporter gene assay. In: Coligan J.E., Kruisbeek A.M., Margulies D.H., Shevach E.M., Strober W., and Coico R. (Eds). Current Protocols in Immunology (2004), John Wiley and Sons, New York 12.11.1-12.11.15
31. Mora J.R., Iwata M., Eksteen B., Song S.Y., Junt T., Senman B., Otipoby K.L., Yokota A., Takeuchi H., Ricciardi-Castagnoli P., Rajewsky K., Adams D.H., and von Andrian U.H. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 314 5802 (2006) 1157-1160
32. Neutra M.R., and Kozlowski P.A. Mucosal vaccines: the promise and the challenge. Nat. Rev., Immunol. 6 2 (2006) 148-158
33. Parren P.W., and Burton D.R. The antiviral activity of antibodies in vitro and in vivo. Adv. Immunol. 77 (2001) 195-262
34. Parren P.W., Mondor I., Naniche D., Ditzel H.J., Klasse P.J., Burton D.R., and Sattentau Q.J. Neutralization of human immunodeficiency virus type 1 by antibody to gp120 is determined primarily by occupancy of sites on the virion irrespective of epitope specificity. J. Virol. 72 5 (1998) 3512-3519
35. Parren P.W., Moore J.P., Burton D.R., and Sattentau Q.J. The neutralizing antibody response to HIV-1: viral evasion and escape from humoral immunity. AIDS 13 Suppl A (1999) S137-S162
36. Pasquini S., Xiang Z., Wang Y., He Z., Deng H., Blaszczyk-Thurin M., and Ertl H.C. Cytokines and costimulatory molecules as genetic adjuvants. Immunol. Cell Biol. 75 4 (1997) 397-401
37. Pitcher C.J., Hagen S.I., Walker J.M., Lum R., Mitchell B.L., Maino V.C., Axthelm M.K., and Picker L.J. Development and homeostasis of T cell memory in rhesus macaque. J. Immunol. 168 1 (2002) 29-43
38. Reimann K.A., Li J.T., Veazey R., Halloran M., Park I.W., Karlsson G.B., Sodroski J., and Letvin N.L. A chimeric simian/human immunodeficiency virus expressing a primary patient human immunodeficiency virus type 1 isolate env causes an AIDS-like disease after in vivo passage in rhesus monkeys. J. Virol. 70 10 (1996) 6922-6928
39. Reimann K.A., Li J.T., Voss G., Lekutis C., Tenner-Racz K., Racz P., Lin W., Montefiori D.C., Lee-Parritz D.E., Lu Y., Collman R.G., Sodroski J., and Letvin N.L. An env gene derived from a primary human immunodeficiency virus type 1 isolate confers high in vivo replicative capacity to a chimeric simian/human immunodeficiency virus in rhesus monkeys. J. Virol. 70 5 (1996) 3198-3206
40. Robinson H.L., Montefiori D.C., Villinger F., Robinson J.E., Sharma S., Wyatt L.S., Earl P.L., McClure H.M., Moss B., and Amara R.R. Studies on GM-CSF DNA as an adjuvant for neutralizing Ab elicited by a DNA/MVA immunodeficiency virus vaccine. Virology 352 2 (2006) 285-294
41. Rogers W.O., Weiss W.R., Kumar A., Aguiar J.C., Tine J.A., Gwadz R., Harre J.G., Gowda K., Rathore D., Kumar S., and Hoffman S.L. Protection of rhesus macaques against lethal Plasmodium knowlesi malaria by a heterologous DNA priming and poxvirus boosting immunization regimen. Infect. Immun. 70 8 (2002) 4329-4335
42. Sin J.I., Kim J.J., Ugen K.E., Ciccarelli R.B., Higgins T.J., and Weiner D.B. Enhancement of protective humoral (Th2) and cell-mediated (Th1) immune responses against herpes simplex virus-2 through co-delivery of granulocyte-macrophage colony-stimulating factor expression cassettes. Eur. J. Immunol. 28 11 (1998) 3530-3540
43. Smith S.M., Holland B., Russo C., Dailey P.J., Marx P.A., and Connor R.I. Retrospective analysis of viral load and SIV antibody responses in rhesus macaques infected with pathogenic SIV: predictive value for disease progression. AIDS Res. Hum. Retroviruses 15 18 (1999) 1691-1701
44. Smith J.M., Amara R.R., Campbell D., Xu Y., Patel M., Sharma S., Butera S.T., Ellenberger D.L., Yi H., Chennareddi L., Herndon J.G., Wyatt L.S., Montefiori D., Moss B., McClure H.M., and Robinson H.L. DNA/MVA vaccine for HIV type 1: effects of codon-optimization and the expression of aggregates or virus-like particles on the immunogenicity of the DNA prime. AIDS Res. Hum. Retroviruses 20 12 (2004) 1335-1347
45. UNAIDS. AIDS Epidemic Update (2006), UNAIDS and WHO
46. Varol C., Landsman L., Fogg D.K., Greenshtein L., Gildor B., Margalit R., Kalchenko V., Geissmann F., and Jung S. Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J. Exp. Med. 204 (2007) 171-178
47. Vermont C.L., van Dijken H.H., van Limpt C.J., de Groot R., van Alphen L., and van Den Dobbelsteen G.P. Antibody avidity and immunoglobulin G isotype distribution following immunization with a monovalent meningococcal B outer membrane vesicle vaccine. Infect. Immun. 70 2 (2002) 584-590
48. Wang R., Richie T.L., Baraceros M.F., Rahardjo N., Gay T., Banania J.G., Charoenvit Y., Epstein J.E., Luke T., Freilich D.A., Norman J., and Hoffman S.L. Boosting of DNA vaccine-elicited gamma interferon responses in humans by exposure to malaria parasites. Infect. Immun. 73 5 (2005) 2863-2872
49. Weiss W.R., Ishii K.J., Hedstrom R.C., Sedegah M., Ichino M., Barnhart K., Klinman D.M., and Hoffman S.L. A plasmid encoding murine granulocyte-macrophage colony-stimulating factor increases protection conferred by a malaria DNA vaccine. J. Immunol. 161 5 (1998) 2325-2332
50. Wright P.F., Kozlowski P.A., Rybczyk G.K., Goepfert P., Staats H.F., VanCott T.C., Trabattoni D., Sannella E., and Mestecky J. Detection of mucosal antibodies in HIV type 1-infected individuals. AIDS Res. Hum. Retroviruses 18 17 (2002) 1291-1300
51. Xiang Z., and Ertl H.C. Manipulation of the immune response to a plasmid-encoded viral antigen by coinoculation with plasmids expressing cytokines. Immunity 2 2 (1995) 129-135
52. Zhang Y., Lou B., Lal R.B., Gettie A., Marx P.A., and Moore J.P. Use of inhibitors to evaluate coreceptor usage by simian and simian/human immunodeficiency viruses and human immunodeficiency virus type 2 in primary cells. J. Virol. 74 15 (2000) 6893-6910