Ability to develop broadly neutralizing HIV-1 antibodies is not restricted by the germline Ig gene repertoire

Journal of Immunology

Volumn 194, Issue 9, 2015, Pages 4371-4378

  Scheepers, Cathrine ^a,b   Shrestha, Ram K ^c   Lambson, Bronwen E ^a,b   Jackson, Katherine J L ^d,e   Wright, Imogen A ^c   Naicker, Dshanta ^a   Goosen, Mark ^a   Berrie, Leigh ^a   Ismail, Arshad ^a   Garrett, Nigel ^f,g   Karim, Quarraisha Abdool ^f,h   Karim, Salim S Abdool ^f,h   Moore, Penny L ^a,b,f   Travers, Simon A ^c   Morris, Lynn ^a,b,f  

^a NATIONAL INSTITUTE FOR COMMUNICABLE DISEASES   (South Africa)

^b UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^c UNIVERSITY OF THE WESTERN CAPE   (South Africa)

^d UNIVERSITY OF NEW SOUTH WALES   (Australia)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF KWAZULU NATAL   (South Africa)

^g UNIVERSITY OF KWAZULU NATAL   (South Africa)

^h Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; NEUTRALIZING ANTIBODY; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN VARIABLE REGION;

ADULT; ALLELE; ANTIBODY PRODUCTION; ARTICLE; CLINICAL ARTICLE; FEMALE; GENE REARRANGEMENT; GERM LINE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOGLOBULIN HEAVY CHAIN GENE; IMMUNOGLOBULIN VARIABLE REGION; PRIORITY JOURNAL; SOUTH AFRICAN; BLACK PERSON; GENETICS; GERM CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOGLOBULIN GENE; IMMUNOLOGY; METABOLISM; PHYLOGENY; YOUNG ADULT;

ADULT; AFRICAN CONTINENTAL ANCESTRY GROUP; ALLELES; ANTIBODIES, NEUTRALIZING; FEMALE; GENES, IMMUNOGLOBULIN; GERM CELLS; HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN VARIABLE REGION; PHYLOGENY; YOUNG ADULT;

EID: 84928485677     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500118     Document Type: Article

References (38)

1. Hraber, P., M. S. Seaman, R. T. Bailer, J. R. Mascola, D. C. Montefiori, and B. T. Korber. 2014. Prevalence of broadly neutralizing antibody responses during chronic HIV-1 infection. AIDS 28: 163-169.
2. Stamatatos, L., L. Morris, D. R. Burton, and J. R. Mascola. 2009. Neutralizing antibodies generated during natural HIV-1 infection: good news for an HIV-1 vaccine? Nat. Med. 15: 866-870.
3. Kwong, P. D., and J. R. Mascola. 2012. Human antibodies that neutralize HIV-1: identification, structures, and B cell ontogenies. Immunity 37: 412-425.
4. Scharf, L., J. F. Scheid, J. H. Lee, A. P. West, Jr., C. Chen, H. Gao, P. N. Gnanapragasam, R. Mares, M. S. Seaman, A. B. Ward, et al. 2014. Antibody 8ANC195 reveals a site of broad vulnerability on the HIV-1 envelope spike. Cell Reports 7: 785-795.
5. Breden, F., C. Lepik, N. S. Longo, M. Montero, P. E. Lipsky, and J. K. Scott. 2011. Comparison of antibody repertoires produced by HIV-1 infection, other chronic and acute infections, and systemic autoimmune disease. PLoS ONE 6: e16857.
6. Gorny, M. K., X. H. Wang, C. Williams, B. Volsky, K. Revesz, B. Witover, S. Burda, M. Urbanski, P. Nyambi, C. Krachmarov, et al. 2009. Preferential use of the VH5-51 gene segment by the human immune response to code for antibodies against the V3 domain of HIV-1. Mol. Immunol. 46: 917-926.
7. Gorny, M. K., J. Sampson, H. Li, X. Jiang, M. Totrov, X. H. Wang, C. Williams, T. O'Neal, B. Volsky, L. Li, et al. 2011. Human anti-V3 HIV-1 monoclonal antibodies encoded by the VH5-51/VL lambda genes define a conserved antigenic structure. PLoS ONE 6: e27780.
8. Gorny, M. K., R. Pan, C. Williams, X. H. Wang, B. Volsky, T. O'Neal, B. Spurrier, J. M. Sampson, L. Li, M. S. Seaman, et al. 2012. Functional and immunochemical cross-reactivity of V2-specific monoclonal antibodies from HIV-1-infected individuals. Virology 427: 198-207.
9. Jardine, J., J.-P. Julien, S. Menis, T. Ota, O. Kalyuzhniy, A. McGuire, D. Sok, P.-S. Huang, S. MacPherson, M. Jones, et al. 2013. Rational HIV immunogen design to target specific germline B cell receptors. Science 340: 711-716.
10. Scheid, J. F., H. Mouquet, B. Ueberheide, R. Diskin, F. Klein, T. Y. Oliveira, J. Pietzsch, D. Fenyo, A. Abadir, K. Velinzon, et al. 2011. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333: 1633-1637.
11. West, A. P., Jr., R. Diskin, M. C. Nussenzweig, and P. J. Bjorkman. 2012. Structural basis for germ-line gene usage of a potent class of antibodies targeting the CD4-binding site of HIV-1 gp120. Proc. Natl. Acad. Sci. USA 109: E2083-E2090.
12. Corti, D., A. L. Suguitan, Jr., D. Pinna, C. Silacci, B. M. Fernandez-Rodriguez, F. Vanzetta, C. Santos, C. J. Luke, F. J. Torres-Velez, N. J. Temperton, et al. 2010. Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. J. Clin. Invest. 120: 1663-1673.
13. Lingwood, D., P. M. McTamney, H. M. Yassine, J. R. Whittle, X. Guo, J. C. Boyington, C. J. Wei, and G. J. Nabel. 2012. Structural and genetic basis for development of broadly neutralizing influenza antibodies. Nature 489: 566-570.
14. Lefranc, M. P., and G. Lefranc. 2001. The Immunoglobulin FactsBook. Academic Press: London.
15. Watson, C. T., and F. Breden. 2012. The immunoglobulin heavy chain locus: genetic variation, missing data, and implications for human disease. Genes Immun. 13: 363-373.
16. Watson, C. T., K. M. Steinberg, J. Huddleston, R. L. Warren, M. Malig, J. Schein, A. J. Willsey, J. B. Joy, J. K. Scott, T. A. Graves, et al. 2013. Complete haplotype sequence of the human immunoglobulin heavy-chain variable, diversity, and joining genes and characterization of allelic and copy-number variation. Am. J. Hum. Genet. 92: 530-546.
17. van Loggerenberg, F., K. Mlisana, C. Williamson, S. C. Auld, L. Morris, C. M. Gray, Q. Abdool Karim, A. Grobler, N. Barnabas, I. Iriogbe, S. S. Abdool Karim; CAPRISA 002 Acute Infection Study Team. 2008. Establishing a cohort at high risk of HIV infection in South Africa: challenges and experiences of the CAPRISA 002 acute infection study. PLoS ONE 3: e1954.
18. Abdool Karim, Q., S. S. Abdool Karim, J. A. Frohlich, A. C. Grobler, C. Baxter, L. E. Mansoor, A. B. Kharsany, S. Sibeko, K. P. Mlisana, Z. Omar, et al; CAPRISA 004 Trial Group. 2010. Effectiveness and safety of tenofovir gel, an antiretroviral microbicide, for the prevention of HIV infection in women. Science 329: 1168-1174.
19. Gray, E. S., M. C. Madiga, T. Hermanus, P. L. Moore, C. K. Wibmer, N. L. Tumba, L. Werner, K. Mlisana, S. Sibeko, C. Williamson, et al; CAP-RISA002 Study Team. 2011. The neutralization breadth of HIV-1 develops incrementally over four years and is associated with CD4+ T cell decline and high viral load during acute infection. J. Virol. 85: 4828-4840.
20. Wang, Y., K. J. Jackson, B. Gäeta, W. Pomat, P. Siba, W. A. Sewell, and A. M. Collins. 2011. Genomic screening by 454 pyrosequencing identifies a new human IGHV gene and sixteen other new IGHVallelic variants. Immunogenetics 63: 259-265.
21. Shrestha, R. K., B. Lubinsky, V. B. Bansode, M. B. Moinz, G. P. McCormack, and S. A. Travers. 2014. QTrim: a novel tool for the quality trimming of sequence reads generated using the Roche/454 sequencing platform. BMC Bioinformatics 15: 33.
22. Zhang, J., K. Kobert, T. Flouri, and A. Stamatakis. 2014. PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30: 614-620.
23. Wright, I. A., and S. A. Travers. 2014. RAMICS: trainable, high-speed and biologically relevant alignment of high-throughput sequencing reads to coding DNA. Nucleic Acids Res. 42: e106.
24. Boyd, S. D., E. L. Marshall, J. D. Merker, J. M. Maniar, L. N. Zhang, B. Sahaf, C. D. Jones, B. B. Simen, B. Hanczaruk, K. D. Nguyen, et al. 2009. Measurement and clinical monitoring of human lymphocyte clonality by massively parallel VDJ pyrosequencing. Sci. Transl. Med. 1: 12ra23.
25. Jackson, K. J., Y. Liu, K. M. Roskin, J. Glanville, R. A. Hoh, K. Seo, E. L. Marshall, T. C. Gurley, M. A. Moody, B. F. Haynes, et al. 2014. Human responses to influenza vaccination show seroconversion signatures and convergent antibody rearrangements. Cell Host Microbe 16: 105-114.
26. Parameswaran, P., Y. Liu, K. M. Roskin, K. K. Jackson, V. P. Dixit, J.-Y. Lee, K. L. Artiles, S. Zompi, M. J. Vargas, B. B. Simen, et al. 2013. Convergent antibody signatures in human dengue. Cell Host Microbe 13: 691-700.
27. Wang, C., Y. Liu, L. T. Xu, K. J. Jackson, K. M. Roskin, T. D. Pham, J. Laserson, E. L. Marshall, K. Seo, J.-Y. Lee, et al. 2014. Effects of aging, cytomegalovirus infection, and EBV infection on human B cell repertoires. J. Immunol. 192: 603-611.
28. Wang, Y., K. J. Jackson, J. Davies, Z. Chen, B. A. Gaeta, J. Rimmer, W. A. Sewell, and A. M. Collins. 2014. IgE-associated IGHV genes from venom and peanut allergic individuals lack mutational evidence of antigen selection. PLoS ONE 9: e89730.
29. The International Immunogenetics Information System Database. Available at: http://www.imgt.org/. Accessed: June 2014.
30. Immunoglobulin Polymorphism Database. Available at: http://cgi.cse.unsw.edu.au/~ihmmune/IgPdb/. Accessed: June 2014.
31. National Center for Biotechnology Information dbSNP - Short Genetic Variation Database. Available at: http://www.ncbi.nlm.nih.gov/SNP/. Accessed: June 2014.
32. National Center for Biotechnology Information GenBank. Available at: http://www.ncbi.nlm.nih.gov/genbank/. Accessed: June 2014.
33. National Center for Biotechnology Information. Immunoglobulin BLAST Tool. Available at: http://www.ncbi.nlm.nih.gov/igblast/. Accessed: June 2014.
34. Simek, M. D., W. Rida, F. H. Priddy, P. Pung, E. Carrow, D. S. Laufer, J. K. Lehrman, M. Boaz, T. Tarragona-Fiol, G. Miiro, et al. 2009. Human immunodeficiency virus type 1 elite neutralizers: individuals with broad and potent neutralizing activity identified by using a high-throughput neutralization assay together with an analytical selection algorithm. J. Virol. 83: 7337-7348.
35. Walker, L. M., M. Huber, K. J. Doores, E. Falkowska, R. Pejchal, J.-P. Julien, S.-K. Wang, A. Ramos, P.-Y. Chan-Hui, M. Moyle, et al; Protocol G Principal Investigators. 2011. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477: 466-470.
36. Liao, H.-X., R. Lynch, T. Zhou, F. Gao, S. M. Alam, S. D. Boyd, A. Z. Fire, K. M. Roskin, C. A. Schramm, Z. Zhang, et al NISC Comparative Sequencing Program. 2013. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496: 469-476.
37. Doria-Rose, N. A., C. A. Schramm, J. Gorman, P. L. Moore, J. N. Bhiman, B. J. DeKosky, M. J. Ernandes, I. S. Georgiev, H. J. Kim, M. Pancera, et al NISC Comparative Sequencing Program. 2014. Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature 509: 55-62.
38. McGuire, A. T., J. A. Glenn, A. Lippy, and L. Stamatatos. 2014. Diverse recombinant HIV-1 Envs fail to activate B cells expressing the germline B cell receptors of the broadly neutralizing anti-HIV-1 antibodies PG9 and 447-52D. J. Virol. 88: 2645-2657.