Trade-offs in antibody repertoires to complex antigens

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 370, Issue 1676, 2015, Pages

  Childs, Lauren M ^a   Baskerville, Edward B ^b   Cobey, Sarah ^b  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Affinity maturation; Antibody repertoire evolution; Germinal centre reaction; NK model

Indexed keywords

ANTIGEN; CLONE; GENETIC VARIATION; GERM CELL; IMMUNE RESPONSE; MATURATION; PATHOGEN;

EPITOPE; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL; ANTIBODY AFFINITY; ANTIBODY SPECIFICITY; ANTIGEN MEDIATED CLONAL SELECTION; ANTIGENIC VARIATION; B LYMPHOCYTE; BIOLOGICAL MODEL; COMPUTER SIMULATION; CYTOLOGY; GENE REARRANGEMENT; GENETICS; GERMINAL CENTER; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; MOLECULAR EVOLUTION;

ANIMALS; ANTIBODY AFFINITY; ANTIBODY DIVERSITY; ANTIGENIC VARIATION; B-LYMPHOCYTES; CLONAL SELECTION, ANTIGEN-MEDIATED; COMPUTER SIMULATION; EVOLUTION, MOLECULAR; GENE REARRANGEMENT, B-LYMPHOCYTE; GERMINAL CENTER; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNODOMINANT EPITOPES; IMMUNOLOGIC MEMORY; MODELS, GENETIC; MODELS, IMMUNOLOGICAL; RECEPTORS, ANTIGEN, B-CELL;

EID: 84937717442     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2014.0245     Document Type: Article

References (67)

1. Mosier DE. 2000 Virus and target cell evolution in human immunodeficiency virus type 1 infection. Immunol. Res. 21, 253-258. (doi:10.1385/IR:21:2- 3:253)
2. Liao HX et al. 2013 Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496, 469-476. (doi:10.1038/nature12053)
3. Ciupe SM, Ribeiro RM, Perelson AS. 2014 Antibody responses during hepatitis B viral infection. PLoS Comput. Biol. 10, e1003730. (doi:10.1371/journal. pcbi.1003730)
4. Donelson JE, Hill KL, El-Sayed N. 1998 Multiple mechanisms of immune evasion by African trypanosomes. Mol. Biochem. Parasitol. 91, 51-66. (doi:10.1016/S0166-6851(97)00209-0)
5. Oladiran A, Belosevic M. 2012 Immune evasion strategies of trypanosomes: a review. J. Parasitol. 98, 284-292. (doi:10.1645/GE-2925.1)
6. Scherf A, Lopez-Rubio JJ, Riviere L. 2008 Antigenic variation in Plasmodium falciparum. Annu. Rev. Microbiol. 62, 445-470. (doi:10.1146/annurev. micro.61.080706.093134)
7. Pasternak ND, Dzikowski R. 2009 PfEMP1: an antigen that plays a key role in the pathogenicity and immune evasion of the malaria parasite Plasmodium falciparum. Int. J. Biochem. Cell Biol. 41, 1463-1466. (doi:10.1016/j.biocel.2008.12.012)
8. Howard R. 1984 Antigenic variation of bloodstage malaria parasites. Phil. Trans. R. Soc. Lond. B 307, 141-158. (doi:10.1098/rstb.1984.0115)
9. Cobey S. 2014 Pathogen evolution and the immunological niche. Ann. NY Acad. Sci. 1320, 1-15. (doi:10.1111/nyas.12493)
10. Lipsitch M, O'Hagan JJ. 2007 Patterns of antigenic diversity and the mechanisms that maintain them. J. R. Soc. Interface 4, 787-802. (doi:10.1098/rsif. 2007.0229)
11. Parameswaran P et al. 2013 Convergent antibody signatures in human dengue. Cell Host Microbe 13, 691-700. (doi:10.1016/j.chom.2013.05.008)
12. Crompton PD et al. 2010 A prospective analysis of the Ab response to Plasmodium falciparum before and after a malaria season by protein microarray. Proc. Natl Acad. Sci. USA 107, 6958-6963. (doi:10. 1073/pnas.1001323107)
13. Turner L, Wang CW, Lavstsen T, Mwakalinga SB, Sauerwein RW, Hermsen CC, Theander TG. 2011 Antibodies against PfEMP1, RIFIN, MSP3 and GLURP are acquired during controlled Plasmodium falciparum malaria infections in naı¨ve volunteers. PLoS ONE 6, e29025. (doi:10.1371/journal.pone. 0029025)
14. Giha H, Nasr A, Iriemenam N, Berzins K, Troye- Blomberg M, Arnot D, ElGhazali G. 2012 A malaria serological map indicating the intersection between parasite antigenic diversity and host antibody repertoires. Eur. J. Clin. Microbiol. Infect. Dis. 31, 3117-3125. (doi:10.1007/s10096-012-1673-z)
15. Eisen HN, Siskind GW. 1964 Variations in affinities of antibodies during the immune response. Biochemistry 3, 996-1008. (doi:10.1021/ bi00895a027)
16. Victora GD, Nussenzweig MC. 2012 Germinal centers. Annu. Rev. Immunol. 30, 429-457. (doi:10. 1146/annurev-immunol-020711-075032)
17. Harris RS, Kong Q, Maizels N. 1999 Somatic hypermutation and the three R's: repair, replication and recombination. Mutat. Res. Rev. Mutat. Res. 436, 157-178. (doi:10.1016/S1383-5742(99) 00003-4)
18. Smith KG, Light A, Nossal G, Tarlinton DM. 1997 The extent of affinity maturation differs between the memory and antibody-forming cell compartments in the primary immune response. EMBO J. 16, 2996-3006. (doi:10.1093/emboj/16. 11.2996)
19. Fish S, Manser T. 1987 Influence of the macromolecular form of a B cell epitope on the expression of antibody variable and constant region structure. J. Exp. Med. 166, 711-724. (doi:10.1084/ jem.166.3.711)
20. Smith KG, Hewitson TD, Nossal G, Tarlinton DM. 1996 The phenotype and fate of the antibodyforming cells of the splenic foci. Eur. J. Immunol. 26, 444-448. (doi:10.1002/eji.1830260226)
21. Moser K, Tokoyoda K, Radbruch A, MacLennan I, Manz RA. 2006 Stromal niches, plasma cell differentiation and survival. Curr. Opin. Immunol. 18, 265-270. (doi:10.1016/j.coi.2006. 03.004)
22. Oracki SA, Walker JA, Hibbs ML, Corcoran LM, Tarlinton DM. 2010 Plasma cell development and survival. Immunol. Rev. 237, 140-159. (doi:10. 1111/j.1600-065X.2010.00940.x)
23. Amanna IJ, Carlson NE, Slifka MK. 2007 Duration of humoral immunity to common viral and vaccine antigens. N Engl. J. Med. 357, 1903-1915. (doi:10. 1056/NEJMoa066092)
24. Purtha WE, Tedder TF, Johnson S, Bhattacharya D, Diamond MS. 2011 Memory B cells, but not long-lived plasma cells, possess antigen specificities for viral escape mutants. J. Exp. Med. 208, 2599-2606. (doi:10.1084/jem.20110740)
25. Schwickert TA, Lindquist RL, Shakhar G, Livshits G, Skokos D, Kosco-Vilbois MH, Dustin ML, Nussenzweig MC. 2007 In vivo imaging of germinal centres reveals a dynamic open structure. Nature 446, 83-87. (doi:10.1038/nature05573)
26. Zhang Y et al. 2013 Germinal center B cells govern their own fate via antibody feedback. J. Exp. Med. 210, 457-464. (doi:10.1084/jem.20120150)
27. Bell GI. 1970 Mathematical model of clonal selection and antibody production. J. Theor. Biol. 29, 191-232. (doi:10.1016/0022-5193 (70)90019-6)
28. Bell GI. 1971 Mathematical model of clonal selection and antibody production. II. J. Theor. Biol. 33, 339-378. (doi:10.1016/0022-5193(71)90071-3)
29. Kepler TB, Perelson AS. 1993 Cyclic re-entry of germinal center B cells and the efficiency of affinity maturation. Immunol. Today 14, 412-415. (doi:10. 1016/0167-5699(93)90145-B)
30. Kepler TB, Perelson AS. 1993 Somatic hypermutation in B cells: an optimal control treatment. J. Theor. Biol. 164, 37-64. (doi:10. 1006/jtbi.1993.1139)
31. Oprea M, Perelson AS. 1997 Somatic mutation leads to efficient affinity maturation when centrocytes recycle back to centroblasts. J. Immunol. 158, 5155-5162.
32. Kes¸mir C, De Boer RJ. 1999 A mathematical model on germinal center kinetics and termination. J. Immunol. 163, 2463-2469.
33. Meyer-Hermann M, Deutsch A, Or-Guil M. 2001 Recycling probability and dynamical properties of germinal center reactions. J. Theor. Biol. 210, 265-285. (doi:10.1006/jtbi.2001.2297)
34. Iber D, Maini PK. 2002 A mathematical model for germinal centre kinetics and affinity maturation. J. Theor. Biol. 219, 153-175. (doi:10.1006/jtbi. 2002.3079)
35. Meyer-Hermann M. 2002 A mathematical model for the germinal center morphology and affinity maturation. J. Theor. Biol. 216, 273-300. (doi:10. 1006/jtbi.2002.2550)
36. Figge MT. 2005 Stochastic discrete event simulation of germinal center reactions. Phys. Rev. E 71, 051907. (doi:10.1103/PhysRevE. 71.051907)
37. Meyer-Hermann ME, Maini PK, Iber D. 2006 An analysis of B cell selection mechanisms in germinal centers. Math. Med. Biol. 23, 255-277. (doi:10. 1093/imammb/dql012)
38. Zhang J, Shakhnovich EI. 2010 Optimality of mutation and selection in germinal centers. PLoS Comput. Biol. 6, e1000800. (doi:10.1371/journal. pcbi.1000800)
39. Chaudhury S, Reifman J, Wallqvist A. 2014 Simulation of B cell affinity maturation explains enhanced antibody cross-reactivity induced by the polyvalent malaria vaccine AMA1. J. Immunol. 193, 2073-2086. (doi:10.4049/jimmunol.1401054)
40. Wang S et al. 2015 Manipulating the selection forces during affinity maturation to generate crossreactive HIV antibodies. Cell 160, 785-797. (doi:10. 1016/j.cell.2015.01.027)
41. Perelson AS, Oster GF. 1979 Theoretical studies of clonal selection: minimal antibody repertoire size and reliability of self-non-self discrimination. J. Theor. Biol. 81, 645-670. (doi:10.1016/0022- 5193(79)90275-3)
42. Sherrington D, Kirkpatrick S. 1975 Solvable model of a spin-glass. Phys. Rev. Lett. 35, 1792-1796. (doi:10.1103/PhysRevLett.35.1792)
43. Edwards SF, Anderson PW. 1975 Theory of spin glasses. J. Phys. F Metal Phys. 5, 965-974. (doi:10. 1088/0305-4608/5/5/017)
44. Derrida B. 1981 Random-energy model: an exactly solvable model of disordered systems. Phys. Rev. B 24, 2613-2626. (doi:10.1103/PhysRevB.24.2613)
45. Binder K, Young AP. 1986 Spin glasses: experimental facts, theoretical concepts, and open questions. Rev. Modern Phys. 58, 801-976. (doi:10. 1103/RevModPhys.58.801)
46. Kauffman SA, Weinberger ED. 1989 The NK model of rugged fitness landscapes and its application to maturation of the immune response. J. Theor. Biol. 141, 211-245. (doi:10.1016/S0022-5193(89) 80019-0)
47. Sun J, Earl DJ, Deem MW. 2005 Glassy dynamics in the adaptive immune response prevents autoimmune disease. Phys. Rev. Lett. 95, 148104. (doi:10.1103/PhysRevLett.95.148104)
48. Sun J, Earl DJ, Deem MW. 2006 Localization and glassy dynamics in the immune system. Modern Phys. Lett. B 20, 63-95. (doi:10.1142/S021798 4906010494)
49. Deem MW, Lee HY. 2003 Sequence space localization in the immune system response to vaccination and disease. Phys. Rev. Lett. 91, 068101. (doi:10.1103/PhysRevLett.91.068101)
50. Szendro IG, Schenk MF, Franke J, Krug J, de Visser JAG. 2013 Quantitative analyses of empirical fitness landscapes. J. Stat. Mech. Theory Exp. 2013, P01005. (doi:10.1088/1742-5468/2013/01/P01005)
51. Figge MT, Garin A, Gunzer M, Kosco-Vilbois M, Toellner KM, Meyer-Hermann M. 2008 Deriving a germinal center lymphocyte migration model from two-photon data. J. Exp. Med. 205, 3019-3029. (doi:10.1084/jem.20081160)
52. Solomon A, Weiss DT. 1995 Structural and functional properties of human lambda-light-chain variable-region subgroups. Clin. Diagn. Lab. Immunol. 2, 387.
53. Etchebest C, Benros C, Bornot A, Camproux AC, De Brevern A. 2007 A reduced amino acid alphabet for understanding and designing protein adaptation to mutation. Eur. Biophys. J. 36, 1059-1069. (doi:10. 1007/s00249-007-0188-5)
54. Bacardit J, Stout M, Hirst J, Valencia A, Smith R, Krasnogor N. 2009 Automated alphabet reduction for protein datasets. BMC Bioinform. 10, 6. (doi:10. 1186/1471-2105-10-6)
55. Melo F, Marti-Renom MA. 2006 Accuracy of sequence alignment and fold assessment using reduced amino acid alphabets. PROTEINS Struct. Funct. Bioinform. 63, 986-995. (doi:10.1002/prot. 20881)
56. Wang J, Wang W. 1999 A computational approach to simplifying the protein folding alphabet. Nat. Struct. Mol. Biol. 6, 1033-1038. (doi:10.1038/ 14918)
57. Mun˜oz E, Deem MW. 2008 Amino acid alphabet size in protein evolution experiments: better to search a small library thoroughly or a large library sparsely? Protein Eng. Design Sel. 21, 311-317. (doi:10.1093/ protein/gzn007)
58. Kroese FG, Wubbena AS, Seijen HG, Nieuwenhuis P. 1987 Germinal centers develop oligoclonally. Eur. J. Immunol. 17, 1069-1072. (doi:10.1002/eji. 1830170726)
59. Berek C, Griffiths G, Milstein C. 1985 Molecular events during maturation of the immune response to oxazolone. Nature 316, 412-418. (doi:10.1038/ 316412a0)
60. Wittenbrink N, Klein A, Weiser AA, Schuchhardt J, Or-Guil M. 2011 Is there a typical germinal center? A large-scale immunohistological study on the cellular composition of germinal centers during the Hapten-carrier-driven primary immune response in mice. J. Immunol. 187, 6185-6196. (doi:10.4049/ jimmunol.1101440)
61. Victora GD, Mesin L. 2014 Clonal and cellular dynamics in germinal centers. Curr. Opin. Immunol. 28, 90-96. (doi:10.1016/j.coi.2014.02.010)
62. Wittenbrink N, Weber TS, Klein A, Weiser AA, Zuschratter W, Sibila M, Schuchhardt J, Or-Guil M. 2010 Broad volume distributions indicate nonsynchronized growth and suggest sudden collapses of germinal center B cell populations. J. Immunol. 184, 1339-1347. (doi:10.4049/ jimmunol.0901040)
63. Murphy K. 2011 Janeway's immunobiology. London, UK: Garland Science.
64. Shlomchik MJ, Weisel F. 2012 Germinal center selection and the development of memory B and plasma cells. Immunol. Rev. 247, 52-63. (doi:10. 1111/j.1600-065X.2012.01124.x)
65. Nahum JR, Godfrey-Smith P, Harding BN, Marcus JH, Carlson-Stevermer J, Kerr B. 2015 A tortoise-hare pattern seen in adapting structured and unstructured populations suggests a rugged fitness landscape in bacteria. Proc. Natl Acad. Sci. USA 112, 7530-7535. (doi:10.1073/pnas.1410631112)
66. Kwong PD, Mascola JR, Nabel GJ. 2013 Broadly neutralizing antibodies and the search for an HIV-1 vaccine: the end of the beginning. Nat. Rev. Immunol. 13, 693-701. (doi:10.1038/nri3516)
67. Wang C et al. 2015 B-cell repertoire responses to varicella-zoster vaccination in human identical twins. Proc. Natl Acad. Sci. USA 112, 500-505. (doi:10.1073/pnas.1415875112)