Simulation of B cell affinity maturation explains enhanced antibody cross-reactivity induced by the polyvalent malaria vaccine AMA1

Journal of Immunology

Volumn 193, Issue 5, 2014, Pages 2073-2086

  Chaudhury, Sidhartha ^a   Reifman, Jaques ^a   Wallqvist, Anders ^a  

^a U S ARMY MEDICAL RESEARCH AND MATERIEL COMMAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMA1 VACCINE; APICAL MEMBRANE ANTIGEN 1; MALARIA VACCINE; UNCLASSIFIED DRUG; APICAL MEMBRANE ANTIGEN I, PLASMODIUM; MEMBRANE PROTEIN; NEUTRALIZING ANTIBODY; PARASITE ANTIGEN; PROTOZOAL PROTEIN; PROTOZOON ANTIBODY;

ANTIBODY AFFINITY; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; CELL MATURATION; CONTROLLED STUDY; DRUG CROSS REACTIVITY; DRUG DETERMINATION; DRUG SPECIFICITY; HUMORAL IMMUNITY; LYMPHOCYTE SUBPOPULATION; PLASMODIUM FALCIPARUM; POPULATION DYNAMICS; STOCHASTIC MODEL; THEORETICAL MODEL; VACCINATION; BIOLOGICAL MODEL; CROSS REACTION; HUMAN; IMMUNOLOGY; MICROBIOLOGY;

ANTIBODIES, NEUTRALIZING; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; B-LYMPHOCYTES; CROSS REACTIONS; HUMANS; MALARIA VACCINES; MEMBRANE PROTEINS; MODELS, IMMUNOLOGICAL; PROTOZOAN PROTEINS;

EID: 84907033460     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401054     Document Type: Article

References (72)

1. 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.
2. Correia, B. E., Y. E. Ban, M. A. Holmes, H. Xu, K. Ellingson, Z. Kraft, C. Carrico, E. Boni, D. N. Sather, C. Zenobia, et al. 2010. Computational design of epitope-scaffolds allows induction of antibodies specific for a poorly immunogenic HIV vaccine epitope. Structure 18: 1116-1126.
3. McLellan, J. S., B. E. Correia, M. Chen, Y. Yang, B. S. Graham, W. R. Schief, and P. D. Kwong. 2011. Design and characterization of epitope-scaffold immunogens that present the motavizumab epitope from respiratory syncytial virus. J. Mol. Biol. 409: 853-866.
4. Klinman, N. R. 1976. The acquisition of b-cell competence and diversity. Am. J. Pathol. 85: 693-704.
5. Küppers, R., M. Zhao, M. L. Hansmann, and K. Rajewsky. 1993. Tracing B cell development in human germinal centres by molecular analysis of single cells picked from histological sections. EMBO J. 12: 4955-4967.
6. Bell, G. I. 1970. Mathematical model of clonal selection and antibody production. J. Theor. Biol. 29: 191-232.
7. Bell, G. I. 1970. Mathematical model of clonal selection and antibody production. Nature 228: 739-744.
8. Bell, G. I. 1971. Mathematical model of clonal selection and antibody production. II. J. Theor. Biol. 33: 339-378.
9. Oprea, M., and A. S. Perelson. 1997. Somatic mutation leads to efficient affinity maturation when centrocytes recycle back to centroblasts. J. Immunol. 158: 5155-5162.
10. Kepler, T. B., and A. S. Perelson. 1993. Somatic hypermutation in B cells: an optimal control treatment. J. Theor. Biol. 164: 37-64.
11. Kepler, T. B., and A. S. Perelson. 1993. Cyclic re-entry of germinal center B cells and the efficiency of affinity maturation. Immunol. Today 14: 412-415.
12. Seiden, P. E., and F. Celada. 1992. A model for simulating cognate recognition and response in the immune system. J. Theor. Biol. 158: 329-357.
13. Celada, F., and P. E. Seiden. 1996. Affinity maturation and hypermutation in a simulation of the humoral immune response. Eur. J. Immunol. 26: 1350-1358.
14. Meyer-Hermann, M. 2002. A mathematical model for the germinal center morphology and affinity maturation. J. Theor. Biol. 216: 273-300.
15. Meyer-Hermann, M., A. Deutsch, and M. Or-Guil. 2001. Recycling probability and dynamical properties of germinal center reactions. J. Theor. Biol. 210: 265-285.
16. Farmer, J. D., N. H. Packard, and A. S. Perelson. 1986. The immune system, adaptation, and machine learning. Physica D 22: 187-204.
17. Perelson, A. S., and G. F. Oster. 1979. Theoretical studies of clonal selection: minimal antibody repertoire size and reliability of self-non-self discrimination. J. Theor. Biol. 81: 645-670.
18. Smith, D. J., S. Forrest, R. R. Hightower, and A. S. Perelson. 1997. Deriving shape space parameters from immunological data. J. Theor. Biol. 189: 141-150.
19. Smith, D. J., S. Forrest, D. H. Ackley, and A. S. Perelson. 1999. Variable efficacy of repeated annual influenza vaccination. Proc. Natl. Acad. Sci. USA 96: 14001-14006.
20. Henrickson, S. E., T. R. Mempel, I. B. Mazo, B. Liu, M. N. Artyomov, H. Zheng, A. Peixoto, M. P. Flynn, B. Senman, T. Junt, et al. 2008. T cell sensing of antigen dose governs interactive behavior with dendritic cells and sets a threshold for T cell activation. Nat. Immunol. 9: 282-291.
21. Zheng, H., B. Jin, S. E. Henrickson, A. S. Perelson, U. H. von Andrian, and A. K. Chakraborty. 2008. How antigen quantity and quality determine T-cell decisions in lymphoid tissue. Mol. Cell. Biol. 28: 4040-4051.
22. Kosmrlj, A., A. K. Jha, E. S. Huseby, M. Kardar, and A. K. Chakraborty. 2008. How the thymus designs antigen-specific and self-tolerant T cell receptor sequences. Proc. Natl. Acad. Sci. USA 105: 16671-16676.
23. Lee, H. Y., D. J. Topham, S. Y. Park, J. Hollenbaugh, J. Treanor, T. R. Mosmann, X. Jin, B. M. Ward, H. Miao, J. Holden-Wiltse, et al. 2009. Simulation and prediction of the adaptive immune response to influenza A virus infection. J. Virol. 83: 7151-7165.
24. Cheng, Y., D. Ghersi, C. Calcagno, L. K. Selin, R. Puzone, and F. Celada. 2009. A discrete computer model of the immune system reveals competitive interactions between the humoral and cellular branch and between cross-reacting memory and naive responses. Vaccine 27: 833-845.
25. Hancioglu, B., D. Swigon, and G. Clermont. 2007. A dynamical model of human immune response to influenza A virus infection. J. Theor. Biol. 246: 70-86.
26. Woo, H. J., and J. Reifman. 2012. A quantitative quasispecies theory-based model of virus escape mutation under immune selection. Proc. Natl. Acad. Sci. USA 109: 12980-12985.
27. van Deutekom, H. W., G. Wijnker, and R. J. de Boer. 2013. The rate of immune escape vanishes when multiple immune responses control an HIV infection. J. Immunol. 191: 3277-3286.
28. Nagaraja, S., A. Wallqvist, J. Reifman, and A. Y. Mitrophanov. 2014. Computational approach to characterize causative factors and molecular indicators of chronic wound inflammation. J. Immunol. 192: 1824-1834.
29. Gillespie, D. T. 1977. Exact stochastic simulation of coupled chemical reactions. J. Phys. Chem. 81: 2340-2361.
30. Huang, J. W., and J. M. Yang. 2011. Changed epitopes drive the antigenic drift for influenza A (H3N2) viruses. BMC Bioinformatics 12(Suppl. 1): S31.
31. Smith, D. J., A. S. Lapedes, J. C. de Jong, T. M. Bestebroer, G. F. Rimmelzwaan, A. D. Osterhaus, and R. A. Fouchier. 2004. Mapping the antigenic and genetic evolution of influenza virus. Science 305: 371-376.
32. Crawford, H., P. C. Matthews, M. Schaefer, J. M. Carlson, A. Leslie, W. Kilembe, S. Allen, T. Ndung'u, D. Heckerman, E. Hunter, and P. J. Goulder. 2011. The hypervariable HIV-1 capsid protein residues comprise HLA-driven CD8+ T-cell escape mutations and covarying HLA-independent polymorphisms. J. Virol. 85: 1384-1390.
33. Fischer, W., V. V. Ganusov, E. E. Giorgi, P. T. Hraber, B. F. Keele, T. Leitner, C. S. Han, C. D. Gleasner, L. Green, C. C. Lo, et al. 2010. Transmission of single HIV-1 genomes and dynamics of early immune escape revealed by ultra-deep sequencing. PLoS ONE 5: e12303.
34. van Gils, M. J., E. M. Bunnik, J. A. Burger, Y. Jacob, B. Schweighardt, T. Wrin, and H. Schuitemaker. 2010. Rapid escape from preserved cross-reactive neutralizing humoral immunity without loss of viral fitness in HIV-1-infected progressors and long-term nonprogressors. J. Virol. 84: 3576-3585.
35. Dowd, K. A., D. M. Netski, X. H. Wang, A. L. Cox, and S. C. Ray. 2009. Selection pressure from neutralizing antibodies drives sequence evolution during acute infection with hepatitis C virus. Gastroenterology 136: 2377-2386.
36. Cento, V., C. Mirabelli, S. Dimonte, R. Salpini, Y. Han, P. Trimoulet, A. Bertoli, V. Micheli, G. Gubertini, G. Cappiello, et al. 2013. Overlapping structure of hepatitis B virus (HBV) genome and immune selection pressure are critical forces modulating HBV evolution. J. Gen. Virol. 94: 143-149.
37. Remarque, E. J., B. W. Faber, C. H. Kocken, and A. W. Thomas. 2008. Apical membrane antigen 1: a malaria vaccine candidate in review. Trends Parasitol. 24: 74-84.
38. Coley, A. M., K. Parisi, R. Masciantonio, J. Hoeck, J. L. Casey, V. J. Murphy, K. S. Harris, A. H. Batchelor, R. F. Anders, and M. Foley. 2006. The most polymorphic residue on Plasmodium falciparum apical membrane antigen 1 determines binding of an invasion-inhibitory antibody. Infect. Immun. 74: 2628-2636.
39. Kohler, B., R. Puzone, P. E. Seiden, and F. Celada. 2000. A systematic approach to vaccine complexity using an automaton model of the cellular and humoral immune system. I. Viral characteristics and polarized responses. Vaccine 19: 862-876.
40. Stanisic, D. I., J. S. Richards, F. J. McCallum, P. Michon, C. L. King, S. Schoepflin, P. R. Gilson, V. J. Murphy, R. F. Anders, I. Mueller, and J. G. Beeson. 2009. Immunoglobulin G subclass-specific responses against Plasmodium falciparum merozoite antigens are associated with control of parasitemia and protection from symptomatic illness. Infect. Immun. 77: 1165-1174.
41. Thera, M. A., O. K. Doumbo, D. Coulibaly, M. B. Laurens, A. Ouattara, A. K. Kone, A. B. Guindo, K. Traore, I. Traore, B. Kouriba, et al. 2011. A field trial to assess a blood-stage malaria vaccine. N. Engl. J. Med. 365: 1004-1013.
42. Duan, J., J. Mu, M. A. Thera, D. Joy, S. L. Kosakovsky Pond, D. Diemert, C. Long, H. Zhou, K. Miura, A. Ouattara, et al. 2008. Population structure of the genes encoding the polymorphic Plasmodium falciparum apical membrane antigen 1: implications for vaccine design. Proc. Natl. Acad. Sci. USA 105: 7857-7862.
43. Takala, S. L., D. Coulibaly, M. A. Thera, A. H. Batchelor, M. P. Cummings, A. A. Escalante, A. Ouattara, K. Traore, A. Niangaly, A. A. Djimde, et al. 2009. Extreme polymorphism in a vaccine antigen and risk of clinical malaria: implications for vaccine development. Sci. Transl. Med. 1: 2ra5.
44. Dutta, S., S. Y. Lee, A. H. Batchelor, and D. E. Lanar. 2007. Structural basis of antigenic escape of a malaria vaccine candidate. Proc. Natl. Acad. Sci. USA 104: 12488-12493.
45. Coley, A. M., A. Gupta, V. J. Murphy, T. Bai, H. Kim, M. Foley, R. F. Anders, and A. H. Batchelor. 2007. Structure of the malaria antigen AMA1 in complex with a growth-inhibitory antibody. PLoS Pathog. 3: 1308-1319.
46. Drew, D. R., A. N. Hodder, D. W. Wilson, M. Foley, I. Mueller, P. M. Siba, A. E. Dent, A. F. Cowman, and J. G. Beeson. 2012. Defining the antigenic diversity of Plasmodium falciparum apical membrane antigen 1 and the requirements for a multi-allele vaccine against malaria. PLoS ONE 7: e51023.
47. Dutta, S., L. S. Dlugosz, D. R. Drew, X. Ge, D. Ababacar, Y. I. Rovira, J. K. Moch, M. Shi, C. A. Long, M. Foley, et al. 2013. Overcoming antigenic diversity by enhancing the immunogenicity of conserved epitopes on the malaria vaccine candidate apical membrane antigen-1. [Published erratum appears in 2014 PLos Pathog. 10(1).] PLoS Pathog. 9: e1003840.
48. Kusi, K. A., B. W. Faber, A. W. Thomas, and E. J. Remarque. 2009. Humoral immune response to mixed PfAMA1 alleles; multivalent PfAMA1 vaccines induce broad specificity. PLoS ONE 4: e8110.
49. Miura, K., R. Herrera, A. Diouf, H. Zhou, J. Mu, Z. Hu, N. J. MacDonald, K. Reiter, V. Nguyen, R. L. Shimp, Jr., et al. 2013. Overcoming allelic specificity by immunization with five allelic forms of Plasmodium falciparum apical membrane antigen 1. Infect. Immun. 81: 1491-1501.
50. Kennedy, M. C., J. Wang, Y. Zhang, A. P. Miles, F. Chitsaz, A. Saul, C. A. Long, L. H. Miller, and A. W. Stowers. 2002. In vitro studies with recombinant Plasmodium falciparum apical membrane antigen 1 (AMA1): production and activity of an AMA1 vaccine and generation of a multiallelic response. Infect. Immun. 70: 6948-6960.
51. Kusi, K. A., B. W. Faber, V. Riasat, A. W. Thomas, C. H. Kocken, and E. J. Remarque. 2010. Generation of humoral immune responses to multi-allele PfAMA1 vaccines; effect of adjuvant and number of component alleles on the breadth of response. PLoS ONE 5: e15391.
52. Berek, C., and C. Milstein. 1988. The dynamic nature of the antibody repertoire. Immunol. Rev. 105: 5-26.
53. Lodish, H., D. Baltimore, A. Berk, S. L. Zipursky, P. Matsudaira, and J. Darnell. 1999. Molecular Cell Biology. Scientific American Books, New York.
54. Tangye, S. G., D. T. Avery, E. K. Deenick, and P. D. Hodgkin. 2003. Intrinsic differences in the proliferation of naive and memory human B cells as a mechanism for enhanced secondary immune responses. J. Immunol. 170: 686-694.
55. Liu, Y. J., J. Zhang, P. J. Lane, E. Y. Chan, and I. C. MacLennan. 1991. Sites of specific B cell activation in primary and secondary responses to T cell-dependent and T cell-independent antigens. Eur. J. Immunol. 21: 2951-2962.
56. Smith, K. G., T. D. Hewitson, G. J. Nossal, and D. M. Tarlinton. 1996. The phenotype and fate of the antibody-forming cells of the splenic foci. Eur. J. Immunol. 26: 444-448.
57. Driver, D. J., L. J. McHeyzer-Williams, M. Cool, D. B. Stetson, and M. G. McHeyzer-Williams. 2001. Development and maintenance of a B2202 memory B cell compartment. J. Immunol. 167: 1393-1405.
58. Liu, X. Q., D. N. Hart, G. G. MacPherson, M. F. Good, and M. N. Wykes. 2008. Soluble CD38 significantly prolongs the lifespan of memory B-cell responses. Immunology 125: 14-20.
59. Dogan, I., B. Bertocci, V. Vilmont, F. Delbos, J. Mégret, S. Storck, C. A. Reynaud, and J. C. Weill. 2009. Multiple layers of B cell memory with different effector functions. Nat. Immunol. 10: 1292-1299.
60. Vieira, P., and K. Rajewsky. 1988. The half-lives of serum immunoglobulins in adult mice. Eur. J. Immunol. 18: 313-316.
61. Morell, A., W. D. Terry, and T. A. Waldmann. 1970. Metabolic properties of IgG subclasses in man. J. Clin. Invest. 49: 673-680.
62. Konterman, R. 2012. Therapeutic Proteins: Strategies to Modulate Their Plasma Half-lives. Wiley-Blackwell, Weinham, Germany.
63. Zhang, J., I. C. MacLennan, Y. J. Liu, and P. J. Lane. 1988. Is rapid proliferation in B centroblasts linked to somatic mutation in memory B cell clones? Immunol. Lett. 18: 297-299.
64. Liao, Y. C., M. S. Lee, C. Y. Ko, and C. A. Hsiung. 2008. Bioinformatics models for predicting antigenic variants of influenza A/H3N2 virus. Bioinformatics 24: 505-512.
65. Pan, K., K. C. Subieta, and M. W. Deem. 2011. A novel sequence-based antigenic distance measure for H1N1, with application to vaccine effectiveness and the selection of vaccine strains. Protein Eng. Des. Sel. 24: 291-299.
66. DeKosky, B. J., G. C. Ippolito, R. P. Deschner, J. J. Lavinder, Y. Wine, B. M. Rawlings, N. Varadarajan, C. Giesecke, T. Dörner, S. F. Andrews, et al. 2013. High-throughput sequencing of the paired human immunoglobulin heavy and light chain repertoire. Nat. Biotechnol. 31: 166-169.
67. 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.
68. Remarque, E. J., B. W. Faber, C. H. Kocken, and A. W. Thomas. 2008. A diversity-covering approach to immunization with Plasmodium falciparum apical membrane antigen 1 induces broader allelic recognition and growth inhibition responses in rabbits. Infect. Immun. 76: 2660-2670.
69. Guenaga, J., P. Dosenovic, G. Ofek, D. Baker, W. R. Schief, P. D. Kwong, G. B. Karlsson Hedestam, and R. T. Wyatt. 2011. Heterologous epitope-scaffold prime:boosting immuno-focuses B cell responses to the HIV-1 gp41 2F5 neutralization determinant. PLoS ONE 6: e16074.
70. Beltramello, M., K. L. Williams, C. P. Simmons, A. Macagno, L. Simonelli, N. T. Quyen, S. Sukupolvi-Petty, E. Navarro-Sanchez, P. R. Young, A. M. de Silva, et al. 2010. The human immune response to Dengue virus is dominated by highly cross-reactive antibodies endowed with neutralizing and enhancing activity. Cell Host Microbe 8: 271-283.
71. Dejnirattisai, W., A. Jumnainsong, N. Onsirisakul, P. Fitton, S. Vasanawathana, W. Limpitikul, C. Puttikhunt, C. Edwards, T. Duangchinda, S. Supasa, et al. 2010. Cross-reacting antibodies enhance dengue virus infection in humans. Science 328: 745-748.
72. Smith, S. A., Y. Zhou, N. P. Olivarez, A. H. Broadwater, A. M. de Silva, and J. E. Crowe, Jr. 2012. Persistence of circulating memory B cell clones with potential for dengue virus disease enhancement for decades following infection. J. Virol. 86: 2665-2675.