Optimality of mutation and selection in germinal centers

PLoS Computational Biology

Volumn 6, Issue 6, 2010, Pages 1-9

  Zhang, Jingshan ^a   Shakhnovich, Eugene I ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL PROLIFERATION; COARSE-GRAINED MODELING;

AFFINITY MATURATION; B CELLS; CELL POPULATIONS; COARSE-GRAINED MODELING; COMPREHENSIVE ANALYSIS; DYNAMICS THEORY; GERMINAL CENTERS; HYPER MUTATION; MUTATION RATES; OPTIMALITY;

ANTIBODIES;

ANTIGEN ANTIBODY COMPLEX; ARTICLE; B LYMPHOCYTE; BOTTLENECK POPULATION; CONTROLLED STUDY; EVOLUTION; GERMINAL CENTER; LYMPHOCYTE MIGRATION; MUTATION RATE; POPULATION DYNAMICS; POPULATION SIZE; PRE B LYMPHOCYTE; SOMATIC HYPERMUTATION; ALGORITHM; ANIMAL; ANTIBODY AFFINITY; BIOLOGICAL MODEL; CELL MOTION; CYTOLOGY; GENETIC SELECTION; HUMAN; IMMUNOLOGY; MUTATION; PHYSIOLOGY; PROTEIN DATABASE; PROTEIN DOMAIN; SPLEEN; STATISTICAL MODEL;

ALGORITHMS; ANIMALS; ANTIBODY AFFINITY; B-LYMPHOCYTES; CELL MOVEMENT; DATABASES, PROTEIN; GERMINAL CENTER; HUMANS; MODELS, IMMUNOLOGICAL; MODELS, STATISTICAL; MUTATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; SELECTION, GENETIC; SPLEEN;

EID: 77955483636     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000800     Document Type: Article

References (54)

1. MacLennan IC (1994) Germinal centers. Annu Rev Immunol 12: 117-139.
2. Rajewsky K (1996) Clonal selection and learning in the antibody system. Nature 381: 751-758.
3. Allen CD, Okada T, Cyster JG (2007) Germinal-center organization and cellular dynamics. Immunity 27: 190-202.
4. Schwickert TA, Lindquist RL, Shakhar G, Livshits G, Skokos D, et al. (2007) In vivo imaging of germinal centres reveals a dynamic open structure. Nature 446: 83-87.
5. Neuberger MS (2002) Novartis Medal Lecture. Antibodies: a paradigm for the evolution of molecular recognition. Biochem Soc Trans 30: 341-350.
6. Kepler TB, Perelson AS (1993) Somatic hypermutation in B cells: an optimal control treatment. J Theor Biol 164: 37-64.
7. Oprea M, Perelson AS (1997) Somatic mutation leads to efficient affinity maturation when centrocytes recycle back to centroblasts. J Immunol 158: 5155-5162.
8. Kleinstein SH, Singh JP (2001) Toward quantitative simulation of germinal center dynamics: biological and modeling insights from experimental validation. J Theor Biol 211: 253-275.
9. Berek C, Milstein C (1987) Mutation drift and repertoire shift in the maturation of the immune response. Immunol Rev 96: 23-41.
10. Kepler TB, Perelson AS (1995) Modeling and optimization of populations subject to time-dependent mutation. Proc Natl Acad Sci U S A 92: 8219-8223.
11. Torigoe H, Nakayama T, Imazato M, Shimada I, Arata Y, et al. (1995) The affinity maturation of anti-4-hydroxy-3-nitrophenylacetyl mouse monoclonal antibody. A calorimetric study of the antigen-antibody interaction. J Biol Chem 270: 22218-22222.
12. Sharon J (1990) Structural correlates of high antibody affinity: three engineered amino acid substitutions can increase the affinity of an anti-p-azophenylarsonate antibody 200-fold. Proc Natl Acad Sci U S A 87: 4814-4817.
13. Ulrich HD, Mundorff E, Santarsiero BD, Driggers EM, Stevens RC, et al. (1997) The interplay between binding energy and catalysis in the evolution of a catalytic antibody. Nature 389: 271-275.
14. Yang PL, Schultz PG (1999) Mutational analysis of the affinity maturation of antibody 48G7. J Mol Biol 294: 1191-1201.
15. Deem MW, Lee HY (2003) Sequence space localization in the immune system response to vaccination and disease. Phys Rev Lett 91: 068101.
16. Kroese FG, Wubbena AS, Seijen HG, Nieuwenhuis P (1987) Germinal centers develop oligoclonally. Eur J Immunol 17: 1069-1072.
17. Coffey F, Alabyev B, Manser T (2009) Initial clonal expansion of germinal center B cells takes place at the perimeter of follicles. Immunity 30: 599-609.
18. McHeyzer-Williams MG, McLean MJ, Lalor PA, Nossal GJ (1993) Antigendriven B cell differentiation in vivo. J Exp Med 178: 295-307.
19. Han S, Zheng B, Dal Porto J, Kelsoe G (1995) In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. IV. Affinity-dependent, antigen-driven B cell apoptosis in germinal centers as a mechanism for maintaining self-tolerance. J Exp Med 182: 1635-1644.
20. Jacob J, Przylepa J, Miller C, Kelsoe G (1993) In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. III. The kinetics of V region mutation and selection in germinal center B cells. J Exp Med 178: 1293-1307.
21. Pascual V, Liu YJ, Magalski A, de Bouteiller O, Banchereau J, et al. (1994) Analysis of somatic mutation in five B cell subsets of human tonsil. J Exp Med 180: 329-339.
22. Allen CD, Okada T, Tang HL, Cyster JG (2007) Imaging of germinal center selection events during affinity maturation. Science 315: 528-531.
23. Hanna MG, Jr. (1964) An Autoradiographic Study of the Germinal Center in Spleen White Pulp During Early Intervals of the Immune Response. Lab Invest 13: 95-104.
24. Zhang J, MacLennan IC, Liu YJ, Lane PJ (1988) Is rapid proliferation in B centroblasts linked to somatic mutation in memory B cell clones? Immunol Lett 18: 297-299.
25. Shannon M, Mehr R (1999) Reconciling repertoire shift with affinity maturation: the role of deleterious mutations. J Immunol 162: 3950-3956.
26. Shlomchik MJ, Watts P, Weigert MG, Litwin S (1998) Clone: a Monte-Carlo computer simulation of B cell clonal expansion, somatic mutation, and antigendriven selection. Curr Top Microbiol Immunol 229: 173-197.
27. Kumar MD, Gromiha MM (2006) PINT: Protein-protein Interactions Thermodynamic Database. Nucleic Acids Res 34: D195-198.
28. Kocks C, Rajewsky K (1988) Stepwise intraclonal maturation of antibody affinity through somatic hypermutation. Proc Natl Acad Sci U S A 85: 8206-8210.
29. Batista FD, Neuberger MS (1998) Affinity dependence of the B cell response to antigen: a threshold, a ceiling, and the importance of off-rate. Immunity 8: 751-759.
30. Tsimring LS, Levine H, Kessler DA (1996) RNA virus evolution via a fitnessspace model. Phys Rev Lett 76: 4440-4443.
31. Kuppers R, Zhao M, Hansmann ML, Rajewsky K (1993) Tracing B cell development in human germinal centres by molecular analysis of single cells picked from histological sections. Embo J 12: 4955-4967.
32. Desai MM, Fisher DS (2007) Beneficial mutation selection balance and the effect of linkage on positive selection. Genetics 176: 1759-1798.
33. Rouzine IM, Brunet E, Wilke CO (2008) The traveling-wave approach to asexual evolution: Muller's ratchet and speed of adaptation. Theor Popul Biol 73: 24-46.
34. Brunet E, Rouzine IM, Wilke CO (2008) The stochastic edge in adaptive evolution. Genetics 179: 603-620.
35. Rouzine IM, Wakeley J, Coffin JM (2003) The solitary wave of asexual evolution. Proc Natl Acad Sci U S A 100: 587-592.
36. Liu YJ, Zhang J, Lane PJ, Chan EY, MacLennan IC (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.
37. Jacob J, Kassir R, Kelsoe G (1991) In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. I. The architecture and dynamics of responding cell populations. J Exp Med 173: 1165-1175.
38. Smith KG, Light A, Nossal GJ, 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.
39. Or-Guil M, Wittenbrink N, Weiser AA, Schuchhardt J (2007) Recirculation of germinal center B cells: a multilevel selection strategy for antibody maturation. Immunol Rev 216: 130-141.
40. Shahaf G, Barak M, Zuckerman NS, Swerdlin N, Gorfine M, et al. (2008) Antigen-driven selection in germinal centers as reflected by the shape characteristics of immunoglobulin gene lineage trees: a large-scale simulation study. J Theor Biol 255: 210-222.
41. Jacob J, Kelsoe G (1992) In situ studies of the primary immune response to (4- hydroxy-3-nitrophenyl)acetyl. II. A common clonal origin for periarteriolar lymphoid sheath-associated foci and germinal centers. J Exp Med 176: 679-687.
42. Iber D, Maini PK (2002) A mathematical model for germinal centre kinetics and affinity maturation. J Theor Biol 219: 153-175.
43. Kesmir C, De Boer RJ (1999) A mathematical model on germinal center kinetics and termination. J Immunol 163: 2463-2469.
44. Meyer-Hermann M, Deutsch A, Or-Guil M (2001) Recycling probability and dynamical properties of germinal center reactions. J Theor Biol 210: 265-285.
45. Wedemayer GJ, Patten PA, Wang LH, Schultz PG, Stevens RC (1997) Structural insights into the evolution of an antibody combining site. Science 276: 1665-1669.
46. Berek C, Berger A, Apel M (1991) Maturation of the immune response in germinal centers. Cell 67: 1121-1129.
47. Sharon J, Gefter ML, Wysocki LJ, Margolies MN (1989) Recurrent somatic mutations in mouse antibodies to p-azophenylarsonate increase affinity for hapten. J Immunol 142: 596-601.
48. Siekevitz M, Kocks C, Rajewsky K, Dildrop R (1987) Analysis of somatic mutation and class switching in naive and memory B cells generating adoptive primary and secondary responses. Cell 48: 757-770.
49. O'Connor BP, Vogel LA, Zhang W, Loo W, Shnider D, et al. (2006) Imprinting the fate of antigen-reactive B cells through the affinity of the B cell receptor. J Immunol 177: 7723-7732.
50. Paus D, Phan TG, Chan TD, Gardam S, Basten A, et al. (2006) Antigen recognition strength regulates the choice between extrafollicular plasma cell and germinal center B cell differentiation. J Exp Med 203: 1081-1091.
51. Ziegner M, Steinhauser G, Berek C (1994) Development of antibody diversity in single germinal centers: selective expansion of high-affinity variants. Eur J Immunol 24: 2393-2400.
52. Radmacher MD, Kelsoe G, Kepler TB (1998) Predicted and inferred waiting times for key mutations in the germinal centre reaction: evidence for stochasticity in selection. Immunol Cell Biol 76: 373-381.
53. Meyer-Hermann ME, Maini PK, Iber D (2006) An analysis of B cell selection mechanisms in germinal centers. Math Med Biol 23: 255-277.
54. Celada F, Seiden PE (1996) Affinity maturation and hypermutation in a simulation of the humoral immune response. Eur J Immunol 26: 1350-1358.