Fundamental characteristics of the immunoglobulin V H repertoire of chickens in comparison with those of humans, mice, and camelids

Journal of Immunology

Volumn 188, Issue 1, 2012, Pages 322-333

  Wu, Leeying ^a   Oficjalska, Katarzyna ^a   Lambert, Matthew ^a   Fennell, Brian J ^a   Darmanin Sheehan, Alfredo ^a   Shúilleabháin, Deirdre Ní ^a   Autin, Bénédicte ^a   Cummins, Emma ^a   Tchistiakova, Lioudmila ^a   Bloom, Laird ^a   Paulsen, Janet ^a   Gill, Davinder ^a   Cunningham, Orla ^a   Finlay, William J J ^a  

^a PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AMINO ACID; CYSTEINE; DISULFIDE; GLYCINE; IMMUNOGLOBULIN; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOGLOBULIN VH; PROTEIN; PROTEIN CDR3; SERINE; SOLVENT; THREONINE; TYROSINE; UNCLASSIFIED DRUG;

ADULT ANIMAL; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ARTIODACTYLA; B LYMPHOCYTE; BINDING AFFINITY; BINDING SITE; CHICKEN; CONTROLLED STUDY; DISULFIDE BOND; GENE MUTATION; GERM LINE; HUMORAL IMMUNITY; MOUSE; NONHUMAN; PHAGE DISPLAY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE; SPECIES DIFFERENCE;

AMINO ACID SUBSTITUTION; ANIMALS; ANTIBODY AFFINITY; CAMELS; CHICKENS; COMPLEMENTARITY DETERMINING REGIONS; DISULFIDES; HUMANS; IMMUNOGLOBULIN HEAVY CHAINS; MICE; MUTATION; PROTEIN STABILITY; SPECIES SPECIFICITY;

EID: 84855361545     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102466     Document Type: Article

References (71)

1. Fuh, G. 2007. Synthetic antibodies as therapeutics. Expert Opin. Biol. Ther. 7: 73-87. (Pubitemid 46110333)
2. Hoogenboom, H. R. 2005. Selecting and screening recombinant antibody libraries. Nat. Biotechnol. 23: 1105-1116. (Pubitemid 41486392)
3. Nishibori, N., H. Horiuchi, S. Furusawa, and H. Matsuda. 2006. Humanization of chicken monoclonal antibody using phage-display system. Mol. Immunol. 43: 634-642. (Pubitemid 41785391)
4. Tsurushita, N., M. Park, K. Pakabunto, K. Ong, A. Avdalovic, H. Fu, A. Jia, M. Vásquez, and S. Kumar. 2004. Humanization of a chicken anti-IL-12 monoclonal antibody. J. Immunol. Methods 295: 9-19. (Pubitemid 41057764)
5. Akamatsu, Y., K. Pakabunto, Z. Xu, Y. Zhang, and N. Tsurushita. 2007. Whole IgG surface display on mammalian cells: application to isolation of neutralizing chicken monoclonal anti-IL-12 antibodies. J. Immunol. Methods 327: 40-52. (Pubitemid 47444311)
6. Ratcliffe, M. J. 2006. Antibodies, immunoglobulin genes and the bursa of Fabricius in chicken B cell development. Dev. Comp. Immunol. 30: 101-118. (Pubitemid 41405789)
7. Reynaud, C. A., V. Anquez, A. Dahan, and J. C. Weill. 1985. A single rearrangement event generates most of the chicken immunoglobulin light chain diversity. Cell 40: 283-291. (Pubitemid 15138456)
8. Reynaud, C. A., A. Dahan, V. Anquez, and J. C. Weill. 1989. Somatic hyperconversion diversifies the single Vh gene of the chicken with a high incidence in the D region. Cell 59: 171-183. (Pubitemid 19248567)
9. Ivanov, I. I., R. L. Schelonka, Y. Zhuang, G. L. Gartland, M. Zemlin, and H. W. Schroeder, Jr. 2005. Development of the expressed Ig CDR-H3 repertoire is marked by focusing of constraints in length, amino acid use, and charge that are first established in early B cell progenitors. J. Immunol. 174: 7773-7780. (Pubitemid 40806284)
10. Link, J. M., M. A. Hellinger, and H. W. Schroeder, Jr. 2002. The Rhesus monkey immunoglobulin IGHD and IGHJ germline repertoire. Immunogenetics 54: 240-250. (Pubitemid 34824134)
11. Link, J. M., J. E. Larson, and H.W. Schroeder. 2005. Despite extensive similarity in germline DH and JH sequence, the adult Rhesus macaque CDR-H3 repertoire differs from human. Mol. Immunol. 42: 943-955. (Pubitemid 40489020)
12. Schroeder, H. W., Jr., J. L. Hillson, and R. M. Perlmutter. 1987. Early restriction of the human antibody repertoire. Science 238: 791-793.
13. Schroeder, H. W., Jr., G. C. Ippolito, and S. Shiokawa. 1998. Regulation of the antibody repertoire through control of HCDR3 diversity. Vaccine 16: 1383-1390. (Pubitemid 28364672)
14. Zemlin, M., M. Klinger, J. Link, C. Zemlin,K. Bauer, J. A.Engler, H. W. Schroeder, Jr., and P. M. Kirkham. 2003. Expressed murine and human CDR-H3 intervals of equal length exhibit distinct repertoires that differ in their amino acid composition and predicted range of structures. J. Mol. Biol. 334: 733-749. (Pubitemid 37433888)
15. Sidhu, S. S., and F. A. Fellouse. 2006. Synthetic therapeutic antibodies. Nat. Chem. Biol. 2: 682-688. (Pubitemid 44764210)
16. Sidhu, S. S., B. Li, Y. Chen, F. A. Fellouse, C. Eigenbrot, and G. Fuh. 2004. Phage-displayed antibody libraries of synthetic heavy chain complementarity determining regions. J. Mol. Biol. 338: 299-310. (Pubitemid 38447087)
17. Parvari, R., A. Avivi, F. Lentner, E. Ziv, S. Tel-Or, Y. Burstein, and I. Schechter. 1988. Chicken immunoglobulin gamma-heavy chains: limited VH gene repertoire, combinatorial diversification by D gene segments and evolution of the heavy chain locus. EMBO J. 7: 739-744.
18. Schroeder, H. W., Jr. 2006. Similarity and divergence in the development and expression of the mouse and human antibody repertoires. Dev. Comp. Immunol. 30: 119-135.
19. Schroeder, H. W., Jr., J. L. Hillson, and R. M. Perlmutter. 1990. Structure and evolution of mammalian VH families. Int. Immunol. 2: 41-50.
20. Parvari, R., E. Ziv, F. Lantner, D. Heller, and I. Schechter. 1990. Somatic diversification of chicken immunoglobulin light chains by point mutations. Proc. Natl. Acad. Sci. USA 87: 3072-3076.
21. Reynaud, C. A., V. Anquez, and J. C. Weill. 1991. The chicken D locus and its contribution to the immunoglobulin heavy chain repertoire. Eur. J. Immunol. 21: 2661-2670.
22. Reynaud, C. A., V. Anquez, H. Grimal, and J. C. Weill. 1987. A hyperconversion mechanism generates the chicken light chain preimmune repertoire. Cell 48: 379-388.
23. Weill, J. C., and C. A. Reynaud. 1992. Early B-cell development in chickens, sheep and rabbits. Curr. Opin. Immunol. 4: 177-180.
24. Parvari, R., E. Ziv, F. Lantner, S. Tel-Or, Y. Burstein, and I. Schechter. 1987. A few germline genes encode the variable regions of chicken immunoglobulin light and g-heavy chains. Prog. Clin. Biol. Res. 238: 15-26.
25. Parvari, R., E. Ziv, F. Lentner, S. Tel-Or, Y. Burstein, and I. Schechter. 1987. Analyses of chicken immunoglobulin light chain cDNA clones indicate a few germline V lambda genes and allotypes of the C lambda locus. EMBO J. 6: 97-102.
26. Reynaud, C. A., A. Dahan, and J. C. Weill. 1983. Complete sequence of a chicken lambda light chain immunoglobulin derived from the nucleotide sequence of its mRNA. Proc. Natl. Acad. Sci. USA 80: 4099-4103.
27. Finlay, W. J., N. C. deVore, E. N. Dobrovolskaia, A. Gam, C. S. Goodyear, and J. E. Slater. 2005. Exploiting the avian immunoglobulin system to simplify the generation of recombinant antibodies to allergenic proteins. Clin. Exp. Allergy 35: 1040-1048. (Pubitemid 41603138)
28. Finlay, W. J., I. Shaw, J. P. Reilly, and M. Kane. 2006. Generation of high-affinity chicken single-chain Fv antibody fragments for measurement of the Pseudonitzschia pungens toxin domoic acid. Appl. Environ. Microbiol. 72: 3343-3349. (Pubitemid 43727985)
29. Yamanaka, H. I., T. Inoue, and O. Ikeda-Tanaka. 1996. Chicken monoclonal antibody isolated by a phage display system. J. Immunol. 157: 1156-1162.
30. Finlay, W. J., L. Bloom, and O. Cunningham. 2011. Phage display: a powerful technology for the generation of high specificity affinity reagents from alternative immune sources. Methods Mol. Biol. 681: 87-101.
31. Andris-Widhopf, J., C. Rader, P. Steinberger, R. Fuller, and C. F. Barbas, III. 2000. Methods for the generation of chicken monoclonal antibody fragments by phage display. J. Immunol. Methods 242: 159-181.
32. Finlay, W. J., O. Cunningham, M. A. Lambert, A. Darmanin-Sheehan, X. Liu, B. J. Fennell, C. M. Mahon, E. Cummins, J. M. Wade, C. M. O'Sullivan, et al. 2009. Affinity maturation of a humanized rat antibody for anti-RAGE therapy: comprehensive mutagenesis reveals a high level of mutational plasticity both inside and outside the complementarity-determining regions. J. Mol. Biol. 388: 541-558.
33. Finlay, W. J., L. Bloom, and O. Cunningham. 2011. Optimized generation of high-affinity, high-specificity single-chain Fv antibodies from multiantigen immunized chickens. Methods Mol. Biol. 681: 383-401.
34. Cummins, E., D. P. Luxenberg, F. McAleese, A. Widom, B. J. Fennell, A. Darmanin-Sheehan, M. J. Whitters, L. Bloom, D. Gill, and O. Cunningham. 2008. A simple high-throughput purification method for hit identification in protein screening. J. Immunol. Methods 339: 38-46.
35. Kirsch, M., M. Zaman, D. Meier, S. Dübel, and M. Hust. 2005. Parameters affecting the display of antibodies on phage. J. Immunol. Methods 301: 173-185. (Pubitemid 40961984)
36. Röthlisberger, D., A. Honegger, and A. Plückthun. 2005. Domain interactions in the Fab fragment: a comparative evaluation of the single-chain Fv and Fab format engineered with variable domains of different stability. J. Mol. Biol. 347: 773-789. (Pubitemid 40357919)
37. Pommié, C., S. Levadoux, R. Sabatier, G. Lefranc, and M. P. Lefranc. 2004. IMGT standardized criteria for statistical analysis of immunoglobulin V-REGION amino acid properties. J. Mol. Recognit. 17: 17-32. (Pubitemid 38231461)
38. Lee, C. V., W. C. Liang, M. S. Dennis, C. Eigenbrot, S. S. Sidhu, and G. Fuh. 2004. High-affinity human antibodies from phage-displayed synthetic Fab libraries with a single framework scaffold. J. Mol. Biol. 340: 1073-1093. (Pubitemid 38976491)
39. Hoet, R. M., E. H. Cohen, R. B. Kent, K. Rookey, S. Schoonbroodt, S. Hogan, L. Rem, N. Frans, M. Daukandt, H. Pieters, et al. 2005. Generation of highaffinity human antibodies by combining donor-derived and synthetic complementarity- determining-region diversity. Nat. Biotechnol. 23: 344-348. (Pubitemid 41094423)
40. Padlan, E. A. 1994. Anatomy of the antibody molecule. Mol. Immunol. 31: 169-217. (Pubitemid 24071681)
41. Foote, J., and G. Winter. 1992. Antibody framework residues affecting the conformation of the hypervariable loops. J. Mol. Biol. 224: 487-499.
42. Kabat, E. A., T. Wu, H. M. Perry, K. S. Gottesman, and C. Foeller. 1991. Sequences of Proteins of Immunological Interest, 5th Ed. National Institutes of Health, Bethesda, MD.
43. MacCallum, R. M., A. C. Martin, and J. M. Thornton. 1996. Antibody-antigen interactions: contact analysis and binding site topography. J. Mol. Biol. 262: 732-745. (Pubitemid 26343518)
44. Shannon, C. E. 1948. A mathmatical theory of communication. Bell Syst. Tech. J. 27: 623-656.
45. Shirai, H., A. Kidera, and H. Nakamura. 1996. Structural classification of CDRH3 in antibodies. FEBS Lett. 399: 1-8.
46. North, B., A. Lehmann, and R. L. Dunbrack, Jr. 2011. A new clustering of antibody CDR loop conformations. J. Mol. Biol. 406: 228-256.
47. Fennell, B. J., A. Darmanin-Sheehan, S. E. Hufton, V. Calabro, L. Wu, M. R. Muller, W. Cao, D. Gill, O. Cunningham, and W. J. Finlay. 2010. Dissection of the IgNAR V domain: molecular scanning and orthologue database mining define novel IgNAR hallmarks and affinity maturation mechanisms. J. Mol. Biol. 400: 155-170.
48. Harmsen, M. M., R. C. Ruuls, I. J. Nijman, T. A. Niewold, L. G. Frenken, and B. de Geus. 2000. Llama heavy-chain V regions consist of at least four distinct subfamilies revealing novel sequence features. Mol. Immunol. 37: 579-590. (Pubitemid 32052527)
49. Stanfield, R. L., H. Dooley, M. F. Flajnik, and I. A. Wilson. 2004. Crystal structure of a shark single-domain antibody V region in complex with lysozyme. Science 305: 1770-1773. (Pubitemid 39249643)
50. Reynaud, C. A., B. Bertocci, A. Dahan, and J. C. Weill. 1994. Formation of the chicken B-cell repertoire: ontogenesis, regulation of Ig gene rearrangement, and diversification by gene conversion. Adv. Immunol. 57: 353-378.
51. McCormack, W. T., L. W. Tjoelker, and C. B. Thompson. 1991. Avian B-cell development: generation of an immunoglobulin repertoire by gene conversion. Annu. Rev. Immunol. 9: 219-241.
52. Rader, C., G. Ritter, S. Nathan, M. Elia, I. Gout, A. A. Jungbluth, L. S. Cohen, S. Welt, L. J. Old, and C. F. Barbas, III. 2000. The rabbit antibody repertoire as a novel source for the generation of therapeutic human antibodies. J. Biol. Chem. 275: 13668-13676. (Pubitemid 30257436)
53. Raaphorst, F. M., C. S. Raman, B. T. Nall, and J. M. Teale. 1997. Molecular mechanisms governing reading frame choice of immunoglobulin diversity genes. Immunol. Today 18: 37-43. (Pubitemid 27072432)
54. Fellouse, F. A., P. A. Barthelemy, R. F. Kelley, and S. S. Sidhu. 2006. Tyrosine plays a dominant functional role in the paratope of a synthetic antibody derived from a four amino acid code. J. Mol. Biol. 357: 100-114. (Pubitemid 43339317)
55. Fellouse, F. A., K. Esaki, S. Birtalan, D. Raptis, V. J. Cancasci, A. Koide, P. Jhurani, M. Vasser, C. Wiesmann, A. A. Kossiakoff, et al. 2007. High-throughput generation of synthetic antibodies from highly functional minimalist phage-displayed libraries. J. Mol. Biol. 373: 924-940. (Pubitemid 47498435)
56. Fellouse, F. A., B. Li, D. M. Compaan, A. A. Peden, S. G. Hymowitz, and S. S. Sidhu. 2005. Molecular recognition by a binary code. J. Mol. Biol. 348: 1153-1162. (Pubitemid 40602373)
57. Fellouse, F. A., C. Wiesmann, and S. S. Sidhu. 2004. Synthetic antibodies from a four-amino-acid code: a dominant role for tyrosine in antigen recognition. Proc. Natl. Acad. Sci. USA 101: 12467-12472. (Pubitemid 39122047)
58. Birtalan, S., R. D. Fisher, and S. S. Sidhu. 2010. The functional capacity of the natural amino acids for molecular recognition. Mol. Biosyst. 6: 1186-1194.
59. Li, H., Y. Jiang, E. L. Prak, M. Radic, and M. Weigert. 2001. Editors and editing of anti-DNA receptors. Immunity 15: 947-957. (Pubitemid 34075375)
60. Boswell, C. A., D. B. Tesar, K. Mukhyala, F. P. Theil, P. J. Fielder, and L. A. Khawli. 2010. Effects of charge on antibody tissue distribution and pharmacokinetics. Bioconjug. Chem. 21: 2153-2163.
61. Birtalan, S., Y. Zhang, F. A. Fellouse, L. Shao, G. Schaefer, and S. S. Sidhu. 2008. The intrinsic contributions of tyrosine, serine, glycine and arginine to the affinity and specificity of antibodies. J. Mol. Biol. 377: 1518-1528.
62. Dooley, H., M. F. Flajnik, and A. J. Porter. 2003. Selection and characterization of naturally occurring single-domain (IgNAR) antibody fragments from immunized sharks by phage display. Mol. Immunol. 40: 25-33. (Pubitemid 36937058)
63. Aitken, R., J. Gilchrist, and M. C. Sinclair. 1997. A single diversified VH gene family dominates the bovine immunoglobulin repertoire. Biochem. Soc. Trans. 25: 326S.
64. O'Brien, P. M., R. Aitken, B. W. O'Neil, and M. S. Campo. 1999. Generation of native bovine mAbs by phage display. Proc. Natl. Acad. Sci. USA 96: 640-645. (Pubitemid 29061261)
65. Sinclair, M. C., J. Gilchrist, and R. Aitken. 1997. Bovine IgG repertoire is dominated by a single diversified VH gene family. J. Immunol. 159: 3883-3889. (Pubitemid 127469644)
66. Li, F., and R. Aitken. 2004. Cloning of porcine scFv antibodies by phage display and expression in Escherichia coli. Vet. Immunol. Immunopathol. 97: 39-51. (Pubitemid 38041252)
67. Johansson, J., M. Aveskogh, B. Munday, and L. Hellman. 2002. Heavy chain V region diversity in the duck-billed platypus (Ornithorhynchus anatinus): long and highly variable complementarity-determining region 3 compensates for limited germline diversity. J. Immunol. 168: 5155-5162. (Pubitemid 34495981)
68. Friedman, M. L., C. Tunyaplin, S. K. Zhai, and K. L. Knight. 1994. Neonatal VH, D, and JH gene usage in rabbit B lineage cells. J. Immunol. 152: 632-641.
69. Popkov, M., R. G. Mage, C. B. Alexander, S. Thundivalappil, C. F. Barbas, III, and C. Rader. 2003. Rabbit immune repertoires as sources for therapeutic monoclonal antibodies: the impact of κ allotype-correlated variation in cysteine content on antibody libraries selected by phage display. J. Mol. Biol. 325: 325-335. (Pubitemid 36062691)
70. Sehgal, D., G. Johnson, T. T. Wu, and R. G. Mage. 1999. Generation of the primary antibody repertoire in rabbits: expression of a diverse set of Igk-V genes may compensate for limited combinatorial diversity at the heavy chain locus. Immunogenetics 50: 31-42.
71. Lee, C. V., S. G. Hymowitz, H. J. Wallweber, N. C. Gordon, K. L. Billeci, S. P. Tsai, D. M. Compaan, J. Yin, Q. Gong, R. F. Kelley, et al. 2006. Synthetic anti-BR3 antibodies that mimic BAFF binding and target both human and murine B cells. Blood 108: 3103-3111.