Sequential and Simultaneous Immunization of Rabbits with HIV-1 Envelope Glycoprotein SOSIP.664 Trimers from Clades A, B and C

PLoS Pathogens

Volumn 12, Issue 9, 2016, Pages

  Klasse, P J ^a   LaBranche, Celia C ^b   Ketas, Thomas J ^a   Ozorowski, Gabriel ^c   Cupo, Albert ^a   Pugach, Pavel ^a   Ringe, Rajesh P ^a   Golabek, Michael ^a   van Gils, Marit J ^c,d   Guttman, Miklos ^e   Lee, Kelly K ^e   Wilson, Ian A ^c   Butera, Salvatore T ^c   Ward, Andrew B ^c   Montefiori, David C ^b   Sanders, Rogier W ^a,d   Moore, John P ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

^e UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUTRALIZING ANTIBODY; VIRUS ENVELOPE PROTEIN; GLYCOPROTEIN; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; RECOMBINANT PROTEIN;

AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS TYPE 1 SUBTYPE A; HUMAN IMMUNODEFICIENCY VIRUS TYPE 1 SUBTYPE B; HUMAN IMMUNODEFICIENCY VIRUS TYPE 1 SUBTYPE C; IC50; IMMUNIZATION; NONHUMAN; RABBIT; SIZE EXCLUSION CHROMATOGRAPHY; ANIMAL; GENETICS; HIV INFECTIONS; HUMAN; IMMUNOLOGY; LEPORIDAE; PROTEIN MULTIMERIZATION; VIROLOGY;

AIDS VACCINES; ANIMALS; ANTIBODIES, NEUTRALIZING; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; FEMALE; GLYCOPROTEINS; HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HUMANS; IMMUNIZATION; PROTEIN MULTIMERIZATION; RABBITS; RECOMBINANT PROTEINS;

EID: 84989899203     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005864     Document Type: Article

References (57)

1. Bricault CA, Kovacs JM, Nkolola JP, Yusim K, Giorgi EE, Shields JL, et al. A multivalent clade C HIV-1 Env trimer cocktail elicits a higher magnitude of neutralizing antibodies than any individual component. J Virol. 2015;89(5):2507–19. doi: 10.1128/JVI.03331-1425540368; PubMed Central PMCID: PMCPMC4325749.
2. Chakrabarti BK, Feng Y, Sharma SK, McKee K, Karlsson Hedestam GB, Labranche CC, et al. Robust neutralizing antibodies elicited by HIV-1 JRFL envelope glycoprotein trimers in nonhuman primates. J Virol. 2013;87(24):13239–51. doi: 10.1128/JVI.01247-1324067980; PubMed Central PMCID: PMCPMC3838230.
3. Forsell MN, Schief WR, Wyatt RT, Immunogenicity of HIV-1 envelope glycoprotein oligomers. Curr Opin HIV AIDS. 2009;4(5):380–7. doi: 10.1097/COH.0b013e32832edc1920048701.
4. Nkolola JP, Bricault CA, Cheung A, Shields J, Perry J, Kovacs JM, et al. Characterization and immunogenicity of a novel mosaic M HIV-1 gp140 trimer. J Virol. 2014;88(17):9538–52. doi: 10.1128/JVI.01739-1424965452; PubMed Central PMCID: PMCPMC4136343.
5. Sanders RW, van Gils MJ, Derking R, Sok D, Ketas TJ, Burger JA, et al. HIV-1 VACCINES. HIV-1 neutralizing antibodies induced by native-like envelope trimers. Science. 2015;349(6244):aac4223. doi: 10.1126/science.aac422326089353; PubMed Central PMCID: PMCPMC4498988.
6. Burton DR, Desrosiers RC, Doms RW, Koff WC, Kwong PD, Moore JP, et al. HIV vaccine design and the neutralizing antibody problem. Nat Immunol. 2004;5(3):233–6. Epub 2004/02/27. doi: 10.1038/ni0304-233 ni0304-233 [pii]. 14985706.
7. Julien JP, Cupo A, Sok D, Stanfield RL, Lyumkis D, Deller MC, et al. Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science. 2013;342(6165):1477–83. Epub 2013/11/02. science.1245625 [pii] doi: 10.1126/science.124562524179159; PubMed Central PMCID: PMC3886632.
8. Klein F, Mouquet H, Dosenovic P, Scheid JF, Scharf L, Nussenzweig MC, Antibodies in HIV-1 vaccine development and therapy. Science. 2013;341(6151):1199–204. Epub 2013/09/14. 341/6151/1199 [pii] doi: 10.1126/science.124114424031012; PubMed Central PMCID: PMC3970325.
9. Lyumkis D, Julien JP, de Val N, Cupo A, Potter CS, Klasse PJ, et al. Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science. 2013;342(6165):1484–90. Epub 2013/11/02. science.1245627 [pii] doi: 10.1126/science.124562724179160; PubMed Central PMCID: PMC3954647.
10. Sanders RW, Derking R, Cupo A, Julien JP, Yasmeen A, de Val N, et al. A next-generation cleaved, soluble HIV-1 Env Trimer, BG505 SOSIP.664 gp140, expresses multiple epitopes for broadly neutralizing but not non-neutralizing antibodies. PLoS Pathog. 2013;9(9):e1003618. Epub 2013/09/27. doi: 10.1371/journal.ppat.1003618 PPATHOGENS-D-13-01512 [pii]. 24068931; PubMed Central PMCID: PMC3777863.
11. Yasmeen A, Ringe R, Derking R, Cupo A, Julien JP, Burton DR, et al. Differential binding of neutralizing and non-neutralizing antibodies to native-like soluble HIV-1 Env trimers, uncleaved Env proteins, and monomeric subunits. Retrovirology. 2014;11(1):41. Epub 2014/06/03. 1742-4690-11-41 [pii] doi: 10.1186/1742-4690-11-4124884783; PubMed Central PMCID: PMC4067080.
12. Pancera M, Zhou T, Druz A, Georgiev IS, Soto C, Gorman J, et al. Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature. 2014;514(7523):455–61. doi: 10.1038/nature1380825296255; PubMed Central PMCID: PMCPMC4348022.
13. Sanders RW, Vesanen M, Schuelke N, Master A, Schiffner L, Kalyanaraman R, et al. Stabilization of the soluble, cleaved, trimeric form of the envelope glycoprotein complex of human immunodeficiency virus type 1. J Virol. 2002;76(17):8875–89. 12163607; PubMed Central PMCID: PMCPMC136973.
14. Julien JP, Lee JH, Ozorowski G, Hua Y, Torrents de la Pena A, de Taeye SW, et al. Design and structure of two HIV-1 clade C SOSIP.664 trimers that increase the arsenal of native-like Env immunogens. Proc Natl Acad Sci U S A. 2015;112(38):11947–52. doi: 10.1073/pnas.150779311226372963; PubMed Central PMCID: PMCPMC4586835.
15. Pugach P, Ozorowski G, Cupo A, Ringe R, Yasmeen A, de Val N, et al. A native-like SOSIP.664 trimer based on an HIV-1 subtype B env gene. J Virol. 2015;89(6):3380–95. doi: 10.1128/JVI.03473-1425589637; PubMed Central PMCID: PMCPMC4337520.
16. de Taeye SW, Ozorowski G, Torrents de la Pena A, Guttman M, Julien JP, van den Kerkhof TL, et al. Immunogenicity of stabilized HIV-1 envelope trimers with reduced exposure of non-neutralizing epitopes. Cell. 2015;163(7):1702–15. doi: 10.1016/j.cell.2015.11.05626687358.
17. Kwong PD, Mascola JR, Human antibodies that neutralize HIV-1: identification, structures, and B cell ontogenies. Immunity. 2012;37(3):412–25. doi: 10.1016/j.immuni.2012.08.01222999947; PubMed Central PMCID: PMCPMC4706166.
18. Moore PL, Williamson C, Morris L, Virological features associated with the development of broadly neutralizing antibodies to HIV-1. Trends Microbiol. 2015;23(4):204–11. doi: 10.1016/j.tim.2014.12.00725572881; PubMed Central PMCID: PMCPMC4380704.
19. Ward AB, Wilson IA, Insights into the trimeric HIV-1 envelope glycoprotein structure. Trends Biochem Sci. 2015;40(2):101–7. doi: 10.1016/j.tibs.2014.12.00625600289; PubMed Central PMCID: PMCPMC4310573.
20. West AP, Jr.Scharf L, Scheid JF, Klein F, Bjorkman PJ, Nussenzweig MC, Structural insights on the role of antibodies in HIV-1 vaccine and therapy. Cell. 2014;156(4):633–48. doi: 10.1016/j.cell.2014.01.05224529371; PubMed Central PMCID: PMCPMC4041625.
21. Dosenovic P, von Boehmer L, Escolano A, Jardine J, Freund NT, Gitlin AD, et al. Immunization for HIV-1 broadly neutralizing antibodies in human Ig knockin mce. Cell. 2015;161(7):1505–15. doi: 10.1016/j.cell.2015.06.00326091035; PubMed Central PMCID: PMCPMC4604566.
22. Hoot S, McGuire AT, Cohen KW, Strong RK, Hangartner L, Klein F, et al. Recombinant HIV envelope proteins fail to engage germline versions of anti-CD4bs bNAbs. PLoS Pathog. 2013;9(1):e1003106. doi: 10.1371/journal.ppat.100310623300456; PubMed Central PMCID: PMCPMC3536657.
23. McGuire AT, Hoot S, Dreyer AM, Lippy A, Stuart A, Cohen KW, et al. Engineering HIV envelope protein to activate germline B cell receptors of broadly neutralizing anti-CD4 binding site antibodies. J Exp Med. 2013;210(4):655–63. doi: 10.1084/jem.2012282423530120; PubMed Central PMCID: PMCPMC3620356.
24. Medina-Ramirez M, Sanders RW, Klasse PJ, Targeting B-cell germlines and focusing affinity maturation: the next hurdles in HIV-1-vaccine development?Expert Rev Vaccines. 2014;13(4):449–52. doi: 10.1586/14760584.2014.89446924606603; PubMed Central PMCID: PMCPMC4141483.
25. Sliepen K, Medina-Ramirez M, Yasmeen A, Moore JP, Klasse PJ, Sanders RW, Binding of inferred germline precursors of broadly neutralizing HIV-1 antibodies to native-like envelope trimers. Virology. 2015;486:116–20. doi: 10.1016/j.virol.2015.08.00226433050.
26. de Taeye SW, Moore JP, Sanders RW, HIV-1 Envelope Trimer Design and Immunization Strategies To Induce Broadly Neutralizing Antibodies. Trends Immunol. 2016;37(3):221–32. doi: 10.1016/j.it.2016.01.00726869204.
27. Xiao X, Chen W, Feng Y, Zhu Z, Prabakaran P, Wang Y, et al. Germline-like predecessors of broadly neutralizing antibodies lack measurable binding to HIV-1 envelope glycoproteins: implications for evasion of immune responses and design of vaccine immunogens. Biochem Biophys Res Commun. 2009;390(3):404–9. doi: 10.1016/j.bbrc.2009.09.02919748484; PubMed Central PMCID: PMCPMC2787893.
28. Gao F, Bonsignori M, Liao HX, Kumar A, Xia SM, Lu X, et al. Cooperation of B cell lineages in induction of HIV-1-broadly neutralizing antibodies. Cell. 2014;158(3):481–91. doi: 10.1016/j.cell.2014.06.02225065977; PubMed Central PMCID: PMCPMC4150607.
29. Liao HX, Lynch R, Zhou T, Gao F, Alam SM, Boyd SD, et al. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature. 2013;496(7446):469–76. doi: 10.1038/nature1205323552890; PubMed Central PMCID: PMCPMC3637846.
30. Wibmer CK, Bhiman JN, Gray ES, Tumba N, Abdool Karim SS, Williamson C, et al. Viral escape from HIV-1 neutralizing antibodies drives increased plasma neutralization breadth through sequential recognition of multiple epitopes and immunotypes. PLoS Pathog. 2013;9(10):e1003738. doi: 10.1371/journal.ppat.100373824204277; PubMed Central PMCID: PMCPMC3814426.
31. Malherbe DC, Doria-Rose NA, Misher L, Beckett T, Puryear WB, Schuman JT, et al. Sequential immunization with a subtype B HIV-1 envelope quasispecies partially mimics the in vivo development of neutralizing antibodies. J Virol. 2011;85(11):5262–74. doi: 10.1128/JVI.02419-1021430056; PubMed Central PMCID: PMCPMC3094990.
32. Malherbe DC, Pissani F, Sather DN, Guo B, Pandey S, Sutton WF, et al. Envelope variants circulating as initial neutralization breadth developed in two HIV-infected subjects stimulate multiclade neutralizing antibodies in rabbits. J Virol. 2014;88(22):12949–67. doi: 10.1128/JVI.01812-1425210191; PubMed Central PMCID: PMCPMC4249069.
33. Chalkley RJ, Baker PR, Huang L, Hansen KC, Allen NP, Rexach M, et al. Comprehensive analysis of a multidimensional liquid chromatography mass spectrometry dataset acquired on a quadrupole selecting, quadrupole collision cell, time-of-flight mass spectrometer: II. New developments in Protein Prospector allow for reliable and comprehensive automatic analysis of large datasets. Mol Cell Proteomics. 2005;4(8):1194–204. doi: 10.1074/mcp.D500002-MCP20015937296.
34. Ringe RP, Yasmeen A, Ozorowski G, Go EP, Pritchard LK, Guttman M, et al. Influences on the Design and Purification of Soluble, Recombinant Native-Like HIV-1 Envelope Glycoprotein Trimers. J Virol. 2015;89(23):12189–210. doi: 10.1128/JVI.01768-1526311893.
35. Chung NP, Matthews K, Kim HJ, Ketas TJ, Golabek M, de Los Reyes K, et al. Stable 293 T and CHO cell lines expressing cleaved, stable HIV-1 envelope glycoprotein trimers for structural and vaccine studies. Retrovirology. 2014;11:33. doi: 10.1186/1742-4690-11-3324767177; PubMed Central PMCID: PMCPMC4032163.
36. Chung KY, Coyle EM, Jani D, King LR, Bhardwaj R, Fries L, et al. ISCOMATRIX adjuvant promotes epitope spreading and antibody affinity maturation of influenza A H7N9 virus like particle vaccine that correlate with virus neutralization in humans. Vaccine. 2015;33(32):3953–62. doi: 10.1016/j.vaccine.2015.06.04726093202.
37. Seaman MS, Janes H, Hawkins N, Grandpre LE, Devoy C, Giri A, et al. Tiered categorization of a diverse panel of HIV-1 Env pseudoviruses for assessment of neutralizing antibodies. J Virol. 2010;84(3):1439–52. doi: 10.1128/JVI.02108-0919939925; PubMed Central PMCID: PMCPMC2812321.
38. Seaman MS, Leblanc DF, Grandpre LE, Bartman MT, Montefiori DC, Letvin NL, et al. Standardized assessment of NAb responses elicited in rhesus monkeys immunized with single- or multi-clade HIV-1 envelope immunogens. Virology. 2007;367(1):175–86. doi: 10.1016/j.virol.2007.05.02417599382; PubMed Central PMCID: PMCPMC2075526.
39. Wei X, Decker JM, Liu H, Zhang Z, Arani RB, Kilby JM, et al. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob Agents Chemother. 2002;46(6):1896–905. 12019106; PubMed Central PMCID: PMCPMC127242.
40. Marozsan AJ, Kuhmann SE, Morgan T, Herrera C, Rivera-Troche E, Xu S, et al. Generation and properties of a human immunodeficiency virus type 1 isolate resistant to the small molecule CCR5 inhibitor, SCH-417690 (SCH-D). Virology. 2005;338(1):182–99. doi: 10.1016/j.virol.2005.04.03515935415.
41. Li M, Salazar-Gonzalez JF, Derdeyn CA, Morris L, Williamson C, Robinson JE, et al. Genetic and neutralization properties of subtype C human immunodeficiency virus type 1 molecular env clones from acute and early heterosexually acquired infections in Southern Africa. J Virol. 2006;80(23):11776–90. doi: 10.1128/JVI.01730-0616971434; PubMed Central PMCID: PMCPMC1642599.
42. deCamp A, Hraber P, Bailer RT, Seaman MS, Ochsenbauer C, Kappes J, et al. Global panel of HIV-1 Env reference strains for standardized assessments of vaccine-elicited neutralizing antibodies. J Virol. 2014;88(5):2489–507. doi: 10.1128/JVI.02853-1324352443; PubMed Central PMCID: PMCPMC3958090.
43. Long EM, Rainwater SM, Lavreys L, Mandaliya K, Overbaugh J, HIV type 1 variants transmitted to women in Kenya require the CCR5 coreceptor for entry, regardless of the genetic complexity of the infecting virus. AIDS Res Hum Retroviruses. 2002;18(8):567–76. doi: 10.1089/08892220275374791412036486.
44. Landau NR, Page KA, Littman DR, Pseudotyping with human T-cell leukemia virus type I broadens the human immunodeficiency virus host range. J Virol. 1991;65(1):162–9. 1845882; PubMed Central PMCID: PMCPMC240501.
45. Hoffenberg S, Powell R, Carpov A, Wagner D, Wilson A, Kosakovsky Pond S, et al. Identification of an HIV-1 clade A envelope that exhibits broad antigenicity and neutralization sensitivity and elicits antibodies targeting three distinct epitopes. J Virol. 2013;87(10):5372–83. doi: 10.1128/JVI.02827-1223468492; PubMed Central PMCID: PMCPMC3648150.
46. Wu X, Parast AB, Richardson BA, Nduati R, John-Stewart G, Mbori-Ngacha D, et al. Neutralization escape variants of human immunodeficiency virus type 1 are transmitted from mother to infant. J Virol. 2006;80(2):835–44. doi: 10.1128/JVI.80.2.835-844.200616378985; PubMed Central PMCID: PMCPMC1346878.
47. Tang H, Robinson JE, Gnanakaran S, Li M, Rosenberg ES, Perez LG, et al. Epitopes immediately below the base of the V3 loop of gp120 as targets for the initial autologous neutralizing antibody response in two HIV-1 subtype B-infected individuals. J Virol. 2011;85(18):9286–99. doi: 10.1128/JVI.02286-1021734041; PubMed Central PMCID: PMCPMC3165744.
48. Lee JH, de Val N, Lyumkis D, Ward AB, Model building and refinement of a natively glycosylated HIV-1 Env protein by high-resolution cryoelectron microscopy. Structure. 2015;23(10):1943–51. doi: 10.1016/j.str.2015.07.02026388028; PubMed Central PMCID: PMCPMC4618500.
49. Lee JH, Ozorowski G, Ward AB, Cryo-EM structure of a native, fully glycosylated, cleaved HIV-1 envelope trimer. Science. 2016;351(6277):1043–8. doi: 10.1126/science.aad245026941313.
50. Crooks ET, Tong T, Chakrabarti B, Narayan K, Georgiev IS, Menis S, et al. Vaccine-elicited Tier 2 HIV-1 neutralizing antibodies bind to quaternary epitopes involving glycan-deficient patches proximal to the CD4 binding site. PLoS Pathog. 2015;11(5):e1004932. doi: 10.1371/journal.ppat.100493226023780; PubMed Central PMCID: PMCPMC4449185.
51. Cheng C, Pancera M, Bossert A, Schmidt SD, Chen RE, Chen X, et al. Immunogenicity of a Prefusion HIV-1 Envelope Trimer in Complex with a Quaternary-Structure-Specific Antibody. J Virol. 2015;90(6):2740–55. doi: 10.1128/JVI.02380-1526719262.
52. Nkolola JP, Peng H, Settembre EC, Freeman M, Grandpre LE, Devoy C, et al. Breadth of neutralizing antibodies elicited by stable, homogeneous clade A and clade C HIV-1 gp140 envelope trimers in guinea pigs. J Virol. 2010;84(7):3270–9. doi: 10.1128/JVI.02252-0920053749; PubMed Central PMCID: PMCPMC2838122.
53. Haynes BF, Shaw GM, Korber B, Kelsoe G, Sodroski J, Hahn BH, et al. HIV-Host interactions: implications for vaccine design. Cell Host Microbe. 2016;19(3):292–303. doi: 10.1016/j.chom.2016.02.00226922989; PubMed Central PMCID: PMCPMC4823811.
54. Hu JK, Crampton JC, Cupo A, Ketas T, van Gils MJ, Sliepen K, et al. Murine antibody responses to cleaved soluble HIV-1 envelope trimers are highly restricted in specificity. J Virol. 2015;89(20):10383–98. doi: 10.1128/JVI.01653-1526246566; PubMed Central PMCID: PMCPMC4580201.
55. Garces F, Lee JH, de Val N, de la Pena AT, Kong L, Puchades C, et al. Affinity maturation of a potent family of HIV antibodies is primarily focused on accommodating or avoiding glycans. Immunity. 2015;43(6):1053–63. doi: 10.1016/j.immuni.2015.11.00726682982; PubMed Central PMCID: PMCPMC4692269.
56. Kong L, Ju B, Chen Y, He L, Ren L, Liu J, et al. Key gp120 Glycans Pose Roadblocks to the Rapid Development of VRC01-Class Antibodies in an HIV-1-Infected Chinese Donor. Immunity. 2016;44(4):939–50. doi: 10.1016/j.immuni.2016.03.00627067056; PubMed Central PMCID: PMCPMC4862659.
57. Lynch RM, Wong P, Tran L, O'Dell S, Nason MC, Li Y, et al. HIV-1 fitness cost associated with escape from the VRC01 class of CD4 binding site neutralizing antibodies. J Virol. 2015;89(8):4201–13. doi: 10.1128/JVI.03608-1425631091; PubMed Central PMCID: PMCPMC4442379.