Membrane embedded HIV-1 envelope on the surface of a virus-like particle elicits broader immune responses than soluble envelopes

Virology

Volumn 358, Issue 2, 2007, Pages 334-346

  McBurney, Sean P ^a   Young, Kelly R ^a   Ross, Ted M ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Env; HIV; Mucosal vaccination; Vaccine; VLP

Indexed keywords

ANTIGEN; ANTISERUM; GAG PROTEIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; MONOMER; PROTEINASE; REV PROTEIN; RNA DIRECTED DNA POLYMERASE; TRANSACTIVATOR PROTEIN; VIRUS ANTIBODY; VIRUS DNA; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN; VPU PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ARTICLE; BAGG ALBINO MOUSE; CELLULAR IMMUNITY; CONTROLLED STUDY; DNA PACKAGING; FEMALE; GENE DELETION; GENE MUTATION; GENETIC CODE; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE RESPONSE; IN VITRO STUDY; LONG TERMINAL REPEAT; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN DOMAIN; SUPERNATANT; VACCINATION; VIRUS ENVELOPE; VIRUS EXPRESSION; VIRUS GENOME; VIRUS LIKE AGENT; VIRUS PARTICLE; VIRUS PURIFICATION; VIRUS TITRATION;

ADMINISTRATION, INTRANASAL; AIDS VACCINES; ANIMALS; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; FEMALE; GENE PRODUCTS, ENV; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; IMMUNIZATION; IMMUNIZATION SCHEDULE; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; MICE; MICE, INBRED BALB C; NEUTRALIZATION TESTS; PLASMIDS; VACCINES, SYNTHETIC; VIRAL ENVELOPE PROTEINS; VIRION;

HUMAN IMMUNODEFICIENCY VIRUS 1; MUS; PRIMATES;

EID: 33846420615     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2006.08.032     Document Type: Article

References (101)

1. Adams O., and Scheid A. Stepwise deletion of the HIV type 1 glycoprotein 41 N terminus leads to an increasing export of microvesicles containing uncleaved Env glycoprotein. AIDS Res. Hum. Retroviruses 17 14 (2001) 1345-1356
2. Amara R.R., Villinger F., Altman J.D., Lydy S.L., O'Neil S.P., Staprans S.I., 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 5514 (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. Ball J.M., Henry N.L., Montelaro R.C., and Newman M.J. A versatile synthetic peptide-based ELISA for identifying antibody epitopes. J. Immunol. Methods 171 1 (1994) 37-44
5. Barnett S.W., Lu S., Srivastava I., Cherpelis S., Gettie A., Blanchard J., Wang S., Mboudjeka I., Leung L., Lian Y., Fong A., Buckner C., Ly A., Hilt S., Ulmer J., Wild C.T., Mascola J.R., and Stamatatos L. The ability of an oligomeric human immunodeficiency virus type 1 (HIV-1) envelope antigen to elicit neutralizing antibodies against primary HIV-1 isolates is improved following partial deletion of the second hypervariable region. J. Virol. 75 12 (2001) 5526-5540
6. Beddows S., Schulke N., Kirschner M., Barnes K., Franti M., Michael E., Ketas T., Sanders R.W., Maddon P.J., Olson W.C., and Moore J.P. Evaluating the immunogenicity of a disulfide-stabilized, cleaved, trimeric form of the envelope glycoprotein complex of human immunodeficiency virus type 1. J. Virol. 79 14 (2005) 8812-8827
7. Bou-Habib D.C., Roderiquez G., Oravecz T., Berman P.W., Lusso P., and Norcross M.A. Cryptic nature of envelope V3 region epitopes protects primary monocytotropic human immunodeficiency virus type 1 from antibody neutralization. J. Virol. 68 9 (1994) 6006-6013
8. Bower J.F., Yang X., Sodroski J., and Ross T.M. Elicitation of neutralizing antibodies with DNA vaccines expressing soluble stabilized human immunodeficiency virus type 1 envelope glycoprotein trimers conjugated to C3d. J. Virol. 78 9 (2004) 4710-4719
9. Bower J.F., Sanders K.L., and Ross T.M. C3d enhances immune responses using low doses of DNA expressing the HIV-1 envelope from codon-optimized gene sequences. Curr. HIV Res. 3 2 (2005) 191-198
10. Burton D.R., Desrosiers R.C., Doms R.W., Koff W.C., Kwong P.D., Moore J.P., Nabel G.J., Sodroski J., Wilson I.A., and Wyatt R.T. HIV vaccine design and the neutralizing antibody problem. Nat. Immunol. 5 3 (2004) 233-236
11. Calarese D.A., Scanlan C.N., Zwick M.B., Deechongkit S., Mimura Y., Kunert R., Zhu P., Wormald M.R., Stanfield R.L., Roux K.H., Kelly J.W., Rudd P.M., Dwek R.A., Katinger H., Burton D.R., and Wilson I.A. Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science 300 5628 (2003) 2065-2071
12. Center R.J., Schuck P., Leapman R.D., Arthur L.O., Earl P.L., Moss B., and Lebowitz J. Oligomeric structure of virion-associated and soluble forms of the simian immunodeficiency virus envelope protein in the prefusion activated conformation. Proc. Natl. Acad. Sci. U.S.A. 98 26 (2001) 14877-14882
13. Chakrabarti B.K., Ling X., Yang Z.Y., Montefiori D.C., Panet A., Kong W.P., Welcher B., Louder M.K., Mascola J.R., and Nabel G.J. Expanded breadth of virus neutralization after immunization with a multiclade envelope HIV vaccine candidate. Vaccine 23 26 (2005) 3434-3445
14. Chan D.C., Fass D., Berger J.M., and Kim P.S. Core structure of gp41 from the HIV envelope glycoprotein. Cell 89 2 (1997) 263-273
15. Chertova E., Bess Jr. J.W., Crise B.J., Sowder I.R., Schaden T.M., Hilburn J.M., Hoxie J.A., Benveniste R.E., Lifson J.D., Henderson L.E., and Arthur L.O. Envelope glycoprotein incorporation, not shedding of surface envelope glycoprotein (gp120/SU), Is the primary determinant of SU content of purified human immunodeficiency virus type 1 and simian immunodeficiency virus. J. Virol. 76 11 (2002) 5315-5325
16. Cleveland S.M., Buratti E., Jones T.D., North P., Baralle F., McLain L., McInerney T., Durrani Z., and Dimmock N.J. Immunogenic and antigenic dominance of a nonneutralizing epitope over a highly conserved neutralizing epitope in the gp41 envelope glycoprotein of human immunodeficiency virus type 1: its deletion leads to a strong neutralizing response. Virology 266 1 (2000) 66-78
17. Cleveland S.M., McLain L., Cheung L., Jones T.D., Hollier M., and Dimmock N.J. A region of the C-terminal tail of the gp41 envelope glycoprotein of human immunodeficiency virus type 1 contains a neutralizing epitope: evidence for its exposure on the surface of the virion. J. Gen. Virol. 84 Pt. 3 (2003) 591-602
18. Cole K.S., Paliotti M.J., Murphey-Corb M., and Montelaro R.C. Maturation of envelope-specific antibody responses to linear determinants in monkeys inoculated with attenuated SIV. J. Med. Primatol. 29 3-4 (2000) 220-230
19. Conley A.J., Kessler II J.A., Boots L.J., McKenna P.M., Schleif W.A., Emini E.A., Mark III G.E., Katinger H., Cobb E.K., Lunceford S.M., Rouse S.R., and Murthy K.K. The consequence of passive administration of an antihuman immunodeficiency virus type 1 neutralizing monoclonal antibody before challenge of chimpanzees with a primary virus isolate. J. Virol. 70 10 (1996) 6751-6758
20. Dettenhofer M., and Yu X.F. Highly purified human immunodeficiency virus type 1 reveals a virtual absence of Vif in virions. J. Virol. 73 2 (1999) 1460-1467
21. Doan L.X., Li M., Chen C., and Yao Q. Virus-like particles as HIV-1 vaccines. Rev. Med. Virol. (2004)
22. Egan M.A. Current prospects for the development of a therapeutic vaccine for the treatment of HIV type 1 infection. AIDS Res. Hum. Retrovir. 20 8 (2004) 794-806
23. Ellenberger D., Li B., Smith J., Yi H., Folks T., Robinson H., and Butera S. Optimization of a multi-gene HIV-1 recombinant subtype CRF02_AG DNA vaccine for expression of multiple immunogenic forms. Virology 319 1 (2004) 118-130
24. Ellenberger D., Wyatt L., Li B., Buge S., Lanier N., Rodriguez I.V., Sariol C.A., Martinez M., Monsour M., Vogt J., Smith J., Otten R., Montefiori D., Kraiselburd E., Moss B., Robinson H., McNicholl J., and Butera S. Comparative immunogenicity in rhesus monkeys of multi-protein HIV-1 (CRF02_AG) DNA/MVA vaccines expressing mature and immature VLPs. Virology 340 1 (2005) 21-32
25. Farzan M., Choe H., Desjardins E., Sun Y., Kuhn J., Cao J., Archambault D., Kolchinsky P., Koch M., Wyatt R., and Sodroski J. Stabilization of human immunodeficiency virus type 1 envelope glycoprotein trimers by disulfide bonds introduced into the gp41 glycoprotein ectodomain. J. Virol. 72 9 (1998) 7620-7625
26. Foresman L., Jia F., Li Z., Wang C., Stephens E.B., Sahni M., Narayan O., and Joag S.V. Neutralizing antibodies administered before, but not after, virulent SHIV prevent infection in macaques. AIDS Res. Hum. Retrovir. 14 12 (1998) 1035-1043
27. Forthal D.N., Landucci G., Haubrich R., Keenan B., Kuppermann B.D., Tilles J.G., and Kaplan J. Antibody dependent cellular cytotoxicity independently predicts survival in severely immunocompromised human immunodeficiency virus-infected patients. J. Infect. Dis. 180 4 (1999) 1338-1341
28. Forthal D.N., Landucci G., and Daar E.S. Antibody from patients with acute human immunodeficiency virus (HIV) infection inhibits primary strains of HIV type 1 in the presence of natural-killer effector cells. J. Virol. 75 15 (2001) 6953-6961
29. Fung M.S., Sun C.R., Gordon W.L., Liou R.S., Chang T.W., Sun W.N., Daar E.S., and Ho D.D. Identification and characterization of a neutralization site within the second variable region of human immunodeficiency virus type 1 gp120. J. Virol. 66 2 (1992) 848-856
30. Gallichan W.S., Woolstencroft R.N., Guarasci T., McCluskie M.J., Davis H.L., and Rosenthal K.L. Intranasal immunization with CpG oligodeoxynucleotides as an adjuvant dramatically increases IgA and protection against herpes simplex virus-2 in the genital tract. J. Immunol. 166 5 (2001) 3451-3457
31. Gardner M., Rosenthal A., Jennings M., Yee J., Antipa L., and Robinson Jr. E. Passive immunization of rhesus macaques against SIV infection and disease. AIDS Res. Hum. Retrovir. 11 7 (1995) 843-854
32. 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 viraemia in rhesus macaques challenged with SIVmac251. J. Immunol. 174 4 (2005) 2185-2189
33. Gorny M.K., Xu J.Y., Gianakakos V., Karwowska S., Williams C., Sheppard H.W., Hanson C.V., and Zolla-Pazner S. Production of site-selected neutralizing human monoclonal antibodies against the third variable domain of the human immunodeficiency virus type 1 envelope glycoprotein. Proc. Natl. Acad. Sci. U.S.A. 88 8 (1991) 3238-3242
34. Gorny M.K., Xu J.Y., Karwowska S., Buchbinder A., and Zolla-Pazner S. Repertoire of neutralizing human monoclonal antibodies specific for the V3 domain of HIV-1 gp120. J. Immunol. 150 2 (1993) 635-643
35. Gorny M.K., Moore J.P., Conley A.J., Karwowska S., Sodroski J., Williams C., Burda S., Boots L.J., and Zolla-Pazner S. Human anti-V2 monoclonal antibody that neutralizes primary but not laboratory isolates of human immunodeficiency virus type 1. J. Virol. 68 12 (1994) 8312-8320
36. Gorny M.K., VanCott T.C., Hioe C., Israel Z.R., Michael N.L., Conley A.J., Williams C., Kessler II J.A., Chigurupati P., Burda S., and Zolla-Pazner S. Human monoclonal antibodies to the V3 loop of HIV-1 with intra- and interclade cross-reactivity. J. Immunol. 159 10 (1997) 5114-5122
37. Green T.D., Montefiori D.C., and Ross T.M. Enhancement of antibodies to the human immunodeficiency virus type 1 envelope by using the molecular adjuvant C3d. J. Virol. 77 3 (2003) 2046-2055
38. Grundner C., Li Y., Louder M., Mascola J., Yang X., Sodroski J., and Wyatt R. Analysis of the neutralizing antibody response elicited in rabbits by repeated inoculation with trimeric HIV-1 envelope glycoproteins. Virology 331 1 (2005) 33-46
39. Haigwood N.L. Predictive value of primate models for AIDS. AIDS Rev. 6 4 (2004) 187-198
40. Haigwood N.L., Watson A., Sutton W.F., McClure J., Lewis A., Ranchalis J., Travis B., Voss G., Letvin N.L., Hu S.L., Hirsch V.M., and Johnson P.R. Passive immune globulin therapy in the SIV/macaque model: early intervention can alter disease profile. Immunol. Lett. 51 1-2 (1996) 107-114
41. Hamer D.H. Can HIV be cured? Mechanisms of HIV persistence and strategies to combat it. Curr. HIV Res. 2 2 (2004) 99-111
42. Hammonds J., Chen X., Ding L., Fouts T., De Vico A., zur Megede J., Barnett S., and Spearman P. Gp120 stability on HIV-1 virions and Gag-Env pseudovirions is enhanced by an uncleaved Gag core. Virology 314 2 (2003) 636-649
43. Hammonds J., Chen X., Fouts T., Devico A., Montefiori D., and Spearman P. Induction of neutralizing antibodies against human immunodeficiency virus type 1 primary isolates by Gag-Env pseudovirion immunization. J. Virol. 79 23 (2005) 14804-14814
44. Hill C.P., Worthylake D., Bancroft D.P., Christensen A.M., and Sundquist W.I. Crystal structures of the trimeric human immunodeficiency virus type 1 matrix protein: implications for membrane association and assembly. Proc. Natl. Acad. Sci. U.S.A. 93 7 (1996) 3099-3104
45. Hollier M.J., and Dimmock N.J. The C-terminal tail of the gp41 transmembrane envelope glycoprotein of HIV-1 clades A, B, C, and D may exist in two conformations: an analysis of sequence, structure, and function. Virology 337 2 (2005) 284-296
46. Horner A.A., Ronaghy A., Cheng P.M., Nguyen M.D., Cho H.J., Broide D., and Raz E. Immunostimulatory DNA is a potent mucosal adjuvant. Cell. Immunol. 190 1 (1998) 77-82
47. Huang Y., Kong W.P., and Nabel G.J. Human immunodeficiency virus type 1-specific immunity after genetic immunization is enhanced by modification of Gag and Pol expression. J. Virol. 75 10 (2001) 4947-4951
48. Kang S.M., and Compans R.W. Enhancement of mucosal immunization with virus-like particles of simian immunodeficiency virus. J. Virol. 77 6 (2003) 3615-3623
49. Kennedy R.C., Henkel R.D., Pauletti D., Allan J.S., Lee T.H., Essex M., and Dreesman G.R. Antiserum to a synthetic peptide recognizes the HTLV-III envelope glycoprotein. Science 231 4745 (1986) 1556-1559
50. Kwong P.D., Wyatt R., Robinson J., Sweet R.W., Sodroski J., and Hendrickson W.A. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393 6686 (1998) 648-659
51. Letvin N.L., Huang Y., Chakrabarti B.K., Xu L., Seaman M.S., Beaudry K., Korioth-Schmitz B., Yu F., Rohne D., Martin K.L., Miura A., Kong W.P., Yang Z.Y., Gelman R.S., Golubeva O.G., Montefiori D.C., Mascola J.R., and Nabel G.J. Heterologous envelope immunogens contribute to AIDS vaccine protection in rhesus monkeys. J. Virol. 78 14 (2004) 7490-7497
52. Li A., Baba T.W., Sodroski J., Zolla-Pazner S., Gorny M.K., Robinson J., Posner M.R., Katinger H., Barbas III C.F., Burton D.R., Chou T.C., and Ruprecht R.M. Synergistic neutralization of a chimeric SIV/HIV type 1 virus with combinations of human anti-HIV type 1 envelope monoclonal antibodies or hyperimmune globulins. AIDS Res. Hum. Retrovir. 13 8 (1997) 647-656
53. 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
54. Mascola J.R., Lewis M.G., Stiegler G., Harris D., VanCott T.C., Hayes D., Louder M.K., Brown C.R., Sapan C.V., Frankel S.S., Lu Y., Robb M.L., Katinger H., and Birx D.L. Protection of Macaques against pathogenic simian/human immunodeficiency virus 89.6 PD by passive transfer of neutralizing antibodies. J. Virol. 73 5 (1999) 4009-4018
55. Mascola J.R., Stiegler G., VanCott T.C., Katinger H., Carpenter C.B., Hanson C.E., Beary H., Hayes D., Frankel S.S., Birx D.L., and Lewis M.G. Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies. Nat. Med. 6 2 (2000) 207-210
56. McCluskie M.J., and Davis H.L. CpG DNA is a potent enhancer of systemic and mucosal immune responses against hepatitis B surface antigen with intranasal administration to mice. J. Immunol. 161 9 (1998) 4463-4466
57. McCune J.M., Rabin L.B., Feinberg M.B., Lieberman M., Kosek J.C., Reyes G.R., and Weissman I.L. Endoproteolytic cleavage of gp160 is required for the activation of human immunodeficiency virus. Cell 53 1 (1988) 55-67
58. Miller M.A., Murphey-Corb M., and Montelaro R.C. Identification of broadly reactive continuous antigenic determinants of simian immunodeficiency virus glycoproteins. AIDS Res. Hum. Retrovir. 8 6 (1992) 1153-1164
59. Modrow S., Hahn B.H., Shaw G.M., Gallo R.C., Wong-Staal F., and Wolf H. Computer-assisted analysis of envelope protein sequences of seven human immunodeficiency virus isolates: prediction of antigenic epitopes in conserved and variable regions. J. Virol. 61 2 (1987) 570-578
60. Moldoveanu Z., Vzorov A.N., Huang W.Q., Mestecky J., and Compans R.W. Induction of immune responses to SIV antigens by mucosally administered vaccines. AIDS Res. Hum. Retrovir. 15 16 (1999) 1469-1476
61. Montefiori, D.C., in press. 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., Coico, R. (Eds.). Current Protocols in Immunology. John Wiley and Sons.
62. Mouland A.J., Mercier J., Luo M., Bernier L., DesGroseillers L., and Cohen E.A. The double-stranded RNA-binding protein Staufen is incorporated in human immunodeficiency virus type 1: evidence for a role in genomic RNA encapsidation. J. Virol. 74 12 (2000) 5441-5451
63. Murthy K.K., Cobb E.K., Rouse S.R., McClure H.M., Payne J.S., Salas M.T., and Michalek G.R. Active and passive immunization against HIV type 1 infection in chimpanzees. AIDS Res. Hum. Retrovir. 14 Suppl. 3 (1998) S271-S276
64. Pancera M., Lebowitz J., Schon A., Zhu P., Freire E., Kwong P.D., Roux K.H., Sodroski J., and Wyatt R. Soluble mimetics of human immunodeficiency virus type 1 viral spikes produced by replacement of the native trimerization domain with a heterologous trimerization motif: characterization and ligand binding analysis. J. Virol. 79 15 (2005) 9954-9969
65. Pancera M., and Wyatt R. Selective recognition of oligomeric HIV-1 primary isolate envelope glycoproteins by potently neutralizing ligands requires efficient precursor cleavage. Virology 332 1 (2005) 145-156
66. Peng B., Wang L.R., Gomez-Roman V.R., Davis-Warren A., Montefiori D.C., Kalyanaraman V.S., Venzon D., Zhao J., Kan E., Rowell T.J., Murthy K.K., Srivastava I., Barnett S.W., and Robert-Guroff M. Replicating rather than nonreplicating adenovirus-human immunodeficiency virus recombinant vaccines are better at eliciting potent cellular immunity and priming high-titer antibodies. J. Virol. 79 16 (2005) 10200-10209
67. Putney S.D., Matthews T.J., Robey W.G., Lynn D.L., Robert-Guroff M., Mueller W.T., Langlois A.J., Ghrayeb J., Petteway Jr. S.R., Weinhold K.J., et al. HTLV-III/LAV-neutralizing antibodies to an E. coli-produced fragment of the virus envelope. Science 234 4782 (1986) 1392-1395
68. Rao M., Matyas G.R., Vancott T.C., Birx D.L., and Alving C.R. Immunostimulatory CpG motifs induce CTL responses to HIV type I oligomeric gp140 envelope protein. Immunol. Cell. Biol. 82 5 (2004) 523-530
69. Reading S.A., Heap C.J., and Dimmock N.J. A novel monoclonal antibody specific to the C-terminal tail of the gp41 envelope transmembrane protein of human immunodeficiency virus type 1 that preferentially neutralizes virus after it has attached to the target cell and inhibits the production of infectious progeny. Virology 315 2 (2003) 362-372
70. Sanders R.W., Vesanen M., Schuelke N., Master A., Schiffner L., Kalyanaraman R., Paluch M., Berkhout B., Maddon P.J., Olson W.C., Lu M., and Moore J.P. Stabilization of the soluble, cleaved, trimeric form of the envelope glycoprotein complex of human immunodeficiency virus type 1. J. Virol. 76 17 (2002) 8875-8889
71. Sauter S.L., Rahman A., and Muralidhar G. Non-replicating viral vector-based AIDS vaccines: interplay between viral vectors and the immune system. Curr. HIV Res. 3 2 (2005) 157-181
72. Schulke N., Vesanen M.S., Sanders R.W., Zhu P., Lu M., Anselma D.J., Villa A.R., Parren P.W., Binley J.M., Roux K.H., Maddon P.J., Moore J.P., and Olson W.C. Oligomeric and conformational properties of a proteolytically mature, disulfide-stabilized human immunodeficiency virus type 1 gp140 envelope glycoprotein. J. Virol. 76 15 (2002) 7760-7776
73. Shibata R., Igarashi T., Haigwood N., Buckler-White A., Ogert R., Ross W., Willey R., Cho M.W., and Martin M.A. Neutralizing antibody directed against the HIV-1 envelope glycoprotein can completely block HIV-1/SIV chimeric virus infections of macaque monkeys. Nat. Med. 5 2 (1999) 204-210
74. Si Z., Phan N., Kiprilov E., and Sodroski J. Effects of HIV type 1 envelope glycoprotein proteolytic processing on antigenicity. AIDS Res. Hum. Retrovir. 19 3 (2003) 217-226
75. Slobod K.S., Coleclough C., Bonsignori M., Brown S.A., Zhan X., Surman S., Zirkel A., Jones B.G., Sealy R.E., Stambas J., Brown B., Lockey T.D., Freiden P.J., Doherty P.C., Blanchard J.L., Martin L.N., and Hurwitz J.L. HIV vaccine rationale, design and testing. Curr. HIV Res. 3 2 (2005) 107-112
76. Sminia T., and Draal G. Nasal-associated lymphoid tissue. In: Ogra P.L., Lamm M.E., Bienenstock J., Mestecky J., Stober W., and McGhee J.R. (Eds). Mucosal Immunology vol. 2 (1999), Academic Press, London 357-364
77. Smith J., Amara R., McClure H., Patel M., S S., Yi H., Chennareddi L., Herndon J., Butera S., Heneine W., Ellenberger D., B P., Earl P., Wyatt L., Moss B., and Robinson H. Multiprotein HIV-1 clade B DNA/MVA vaccine: construction, safety, and immunogenicity. AIDS Res. Hum. Retrovir. 20 (2003) 654-665
78. 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. Retrovir. 20 12 (2004) 1335-1347
79. Spearman P. HIV vaccine development: lessons from the past and promise for the future. Curr. HIV Res. 1 1 (2003) 101-120
80. Spenlehauer C., Saragosti S., Fleury H.J., Kirn A., Aubertin A.M., and Moog C. Study of the V3 loop as a target epitope for antibodies involved in the neutralization of primary isolates versus T-cell-line-adapted strains of human immunodeficiency virus type 1. J. Virol. 72 12 (1998) 9855-9864
81. Srivastava I.K., Stamatatos L., Legg H., Kan E., Fong A., Coates S.R., Leung L., Wininger M., Donnelly J.J., Ulmer J.B., and Barnett S.W. Purification and characterization of oligomeric envelope glycoprotein from a primary R5 subtype B human immunodeficiency virus. J. Virol. 76 6 (2002) 2835-2847
82. Stamatatos L., and Cheng-Mayer C. Structural modulations of the envelope gp120 glycoprotein of human immunodeficiency virus type 1 upon oligomerization and differential V3 loop epitope exposure of isolates displaying distinct tropism upon virion-soluble receptor binding. J. Virol. 69 10 (1995) 6191-6198
83. Tan K., Liu J., Wang J., Shen S., and Lu M. Atomic structure of a thermostable subdomain of HIV-1 gp41. Proc. Natl. Acad. Sci. U.S.A. 94 23 (1997) 12303-12308
84. Tang S., Murakami T., Cheng N., Steven A.C., Freed E.O., and Levin J.G. Human immunodeficiency virus type 1 N-terminal capsid mutants containing cores with abnormally high levels of capsid protein and virtually no reverse transcriptase. J. Virol. 77 23 (2003) 12592-12602
85. Tilney N.L. Patterns of lymphatic drainage in the adult laboratory rat. J. Anat. 109 Pt. 3 (1971) 369-383
86. Tochikubo K., Isaka M., Yasuda Y., Kozuka S., Matano K., Miura Y., and Taniguchi T. Recombinant cholera toxin B subunit acts as an adjuvant for the mucosal and systemic responses of mice to mucosally co-administered bovine serum albumin. Vaccine 16 2-3 (1998) 150-155
87. Trkola A., Purtscher M., Muster T., Ballaun C., Buchacher A., Sullivan N., Srinivasan K., Sodroski J., Moore J.P., and Katinger H. Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J. Virol. 70 2 (1996) 1100-1108
88. VanCott T.C., Mascola J.R., Kaminski R.W., Kalyanaraman V., Hallberg P.L., Burnett P.R., Ulrich J.T., Rechtman D.J., and Birx D.L. Antibodies with specificity to native gp120 and neutralization activity against primary human immunodeficiency virus type 1 isolates elicited by immunization with oligomeric gp160. J. Virol. 71 6 (1997) 4319-4330
89. Wang C.T., Lai H.Y., and Li J.J. Analysis of minimal human immunodeficiency virus type 1 gag coding sequences capable of virus-like particle assembly and release. J. Virol. 72 10 (1998) 7950-7959
90. Wu H.Y., Nguyen H.H., and Russell M.W. Nasal lymphoid tissue (NALT) as a mucosal immune inductive site. Scand. J. Immunol. 46 5 (1997) 506-513
91. Wyatt R., Kwong P.D., Desjardins E., Sweet R.W., Robinson J., Hendrickson W.A., and Sodroski J.G. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393 6686 (1998) 705-711
92. Wyatt L.S., Earl P.L., Liu J.Y., Smith J.M., Montefiori D.C., Robinson H.L., and Moss B. Multiprotein HIV type 1 clade B DNA and MVA vaccines: construction, expression, and immunogenicity in rodents of the MVA component. AIDS Res. Hum. Retrovir. 20 6 (2004) 645-653
93. Wyatt R., and Sodroski J. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280 5371 (1998) 1884-1888
94. Yang X., Farzan M., Wyatt R., and Sodroski J. Characterization of stable, soluble trimers containing complete ectodomains of human immunodeficiency virus type 1 envelope glycoproteins. J. Virol. 74 12 (2000) 5716-5725
95. Yang X., Wyatt R., and Sodroski J. Improved elicitation of neutralizing antibodies against primary human immunodeficiency viruses by soluble stabilized envelope glycoprotein trimers. J. Virol. 75 3 (2001) 1165-1171
96. Yang X., Lee J., Mahony E.M., Kwong P.D., Wyatt R., and Sodroski J. Highly stable trimers formed by human immunodeficiency virus type 1 envelope glycoproteins fused with the trimeric motif of T4 bacteriophage fibritin. J. Virol. 76 9 (2002) 4634-4642
97. York J., Follis K.E., Trahey M., Nyambi P.N., Zolla-Pazner S., and Nunberg J.H. Antibody binding and neutralization of primary and T-cell line-adapted isolates of human immunodeficiency virus type 1. J. Virol. 75 6 (2001) 2741-2752
98. Young K.R., and Ross T.M. Particle-based vaccines for HIV-1 infection. Curr. Drug Targets Infect. Disord. 3 2 (2003) 151-169
99. Young K., and Ross T.M. Elicitation of immunity to HIV-1 gag is determined by Gag structure. AIDS Res. Hum. Retrovir. (2005)
100. Young K.R., Smith J.M., and Ross T.M. Characterization of a DNA vaccine expressing a human immunodeficiency virus-like particle. Virology 327 2 (2004) 262-272
101. Zhang C.W., Chishti Y., Hussey R.E., and Reinherz E.L. Expression, purification, and characterization of recombinant HIV gp140. The gp41 ectodomain of HIV or simian immunodeficiency virus is sufficient to maintain the retroviral envelope glycoprotein as a trimer. J. Biol. Chem. 276 43 (2001) 39577-39585