Evolution of B cell immunity

Annual Review of Animal Biosciences

Volumn 1, Issue , 2013, Pages 65-97

  Parra, David ^a   Takizawa, Fumio ^a   Sunyer, J Oriol ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

adaptive immunity; antibody diversification; immunoglobulin; innate immunity; phagocytosis; variable lymphocyte receptor (VLR)

Indexed keywords

ANIMAL; B LYMPHOCYTE; CELLULAR IMMUNITY; EVOLUTION; GENETICS; IMMUNOLOGY; INVERTEBRATE; PHYSIOLOGY; VERTEBRATE;

ANIMALS; B-LYMPHOCYTES; BIOLOGICAL EVOLUTION; IMMUNITY, CELLULAR; INVERTEBRATES; VERTEBRATES;

EID: 84897521761     PISSN: 21658102     EISSN: 21658110     Source Type: Journal    
DOI: 10.1146/annurev-animal-031412-103651     Document Type: Review

References (173)

1. Chen G, Zhuchenko O, Kuspa A. 2007. Immune-like phagocyte activity in the social amoeba. Science 317:678-81
2. Bhaya D, Davison M, Barrangou R. 2011. CRISPR-Cas systems in bacteria and archaea: Versatile small RNAs for adaptive defense and regulation. Annu. Rev. Genet. 45:273-97
3. Medzhitov R. 2007. Recognition of microorganisms and activation of the immune response. Nature 449:819-26
4. Pancer Z, Cooper MD. 2006. The evolution of adaptive immunity. Annu. Rev. Immunol. 24:497-518
5. Matsunaga T, Rahman A. 1998. What brought the adaptive immune system to vertebrates?-The jaw hypothesis and the seahorse. Immunol. Rev. 166:177-86
6. Hsu E. 1998. Mutation, selection, and memory in B lymphocytes of exothermic vertebrates. Immunol. Rev. 162:25-36
7. Kawamoto H, Katsura Y. 2009. A new paradigm for hematopoietic cell lineages: Revision of the classical concept of the myeloid-lymphoid dichotomy. Trends Immunol. 30:193-200
8. Li J, Barreda DR, Zhang YA, Boshra H, Gelman AE, et al. 2006. B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat. Immunol. 7:1116-24
9. Lund FE, Randall TD. 2010. Effector and regulatory B cells: Modulators of CD4\+ T cell immunity. Nat. Rev. Immunol. 10:236-47
10. CooperMD,Peterson RD, GoodRA. 1965. Delineation of the thymic and bursal lymphoid systems in the chicken. Nature 205:143-46
11. Rowley AF, Powell A. 2007. Invertebrate immune systems-Specific, quasi-specific, or nonspecific? J. Immunol. 179:7209-14
12. Little TJ, Hultmark D, Read AF. 2005. Invertebrate immunity and the limits of mechanistic immunology. Nat. Immunol. 6:651-54
13. Alt FW, Rathbun G, Oltz E, Taccioli G, Shinkai Y. 1992. Function and control of recombinationactivating gene activity. Ann. N.Y. Acad. Sci. 651:277-94
14. Boehm T, Bleul CC. 2007. The evolutionary history of lymphoid organs. Nat. Immunol. 8:131-35
15. Pancer Z, Mayer WE, Klein J, Cooper MD. 2004. Prototypic T cell receptor and CD4-like coreceptor are expressed by lymphocytes in the agnathan sea lamprey. Proc. Natl. Acad. Sci. USA 101:13273-78
16. Fugmann SD, Messier C, Novack LA, Cameron RA, Rast JP. 2006. An ancient evolutionary origin of the Rag1/2 gene locus. Proc. Natl. Acad. Sci. USA 103:3728-33
17. Boehm T, McCurley N, Sutoh Y, Schorpp M, Kasahara M, Cooper MD. 2012. VLR-based adaptive immunity. Annu. Rev. Immunol. 30:203-20
18. Hirano M, Das S, Guo P, Cooper MD. 2011. The evolution of adaptive immunity in vertebrates. Adv. Immunol. 109:125-57
19. Dooley H, Flajnik MF. 2006. Antibody repertoire development in cartilaginous fish. Dev. Comp. Immunol. 30:43-56
20. Rumfelt LL, Avila D, Diaz M, Bartl S, McKinney EC, Flajnik MF. 2001. A shark antibody heavy chain encoded by a nonsomatically rearranged VDJ is preferentially expressed in early development and is convergent with mammalian IgG. Proc. Natl. Acad. Sci. USA 98:1775-80
21. Ohta Y, Flajnik M. 2006. IgD, like IgM, is a primordial immunoglobulin class perpetuated in most jawed vertebrates. Proc. Natl. Acad. Sci. USA 103:10723-28
22. Rumfelt LL, McKinney EC, Taylor E, Flajnik MF. 2002. The development of primary and secondary lymphoid tissues in the nurse shark Ginglymostoma cirratum: B-cell zones precede dendritic cell immigration and T-cell zone formation during ontogeny of the spleen. Scand. J. Immunol. 56:130-48
23. Miracle AL, Anderson MK, Litman RT, Walsh CJ, Luer CA, et al. 2001. Complex expression patterns of lymphocyte-specific genes during the development of cartilaginous fish implicate unique lymphoid tissues in generating an immune repertoire. Int. Immunol. 13:567-80
24. Dooley H, FlajnikMF.2005. Shark immunity bites back: Affinity maturation andmemory response in the nurse shark, Ginglymostoma cirratum. Eur. J. Immunol. 35:936-45
25. Flajnik MF. 2002. Comparative analyses of immunoglobulin genes: Surprises and portents. Nat. Rev. Immunol. 2:688-98
26. Hansen JD, Landis ED, Phillips RB. 2005. Discovery of a unique Ig heavy-chain isotype (IgT) in rainbow trout: Implications for a distinctive B cell developmental pathway in teleost fish. Proc. Natl. Acad. Sci. USA 102:6919-24
27. Danilova N, Bussmann J, Jekosch K, Steiner LA. 2005. The immunoglobulin heavy-chain locus in zebrafish: Identification and expression of a previously unknown isotype, immunoglobulin Z. Nat. Immunol. 6:295-302
28. Flajnik MF, Kasahara M. 2010. Origin and evolution of the adaptive immune system: Genetic events and selective pressures. Nat. Rev. Genet. 11:47-59
29. Salinas I, Zhang YA, Sunyer JO. 2011. Mucosal immunoglobulins and B cells of teleost fish. Dev. Comp. Immunol. 35:1346-65
30. Zhang YA, Salinas I, Li J, Parra D, Bjork S, et al. 2010. IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat. Immunol. 11:827-35
31. Edholm ES, Bengten E, Wilson M. 2011. Insights into the function of IgD. Dev. Comp. Immunol. 35:1309-16
32. Ramirez-Gomez F, Greene W, Rego K, Hansen JD, Costa G, et al. 2012. Discovery and characterization of secretory IgD in rainbow trout: Secretory IgD is produced through a novel splicing mechanism. J. Immunol. 188:1341-49
33. Edholm ES, Bengten E, Stafford JL, Sahoo M, Taylor EB, et al. 2010. Identification of two IgD\+ B cell populations in channel catfish, Ictalurus punctatus. J. Immunol. 185:4082-94
34. Hamuro K, Suetake H, Saha NR, Kikuchi K, Suzuki Y. 2007. A teleost polymeric Ig receptor exhibiting two Ig-like domains transports tetrameric IgM into the skin. J. Immunol. 178:5682-89
35. Schorpp M, BialeckiM, Diekhoff D, Walderich B, Odenthal J, et al. 2006. Conserved functions of Ikaros in vertebrate lymphocyte development: Genetic evidence for distinct larval and adult phases of T cell development and two lineages of B cells in zebrafish. J. Immunol. 177:2463-76
36. Hansen JD, Zapata AG. 1998. Lymphocyte development in fish and amphibians. Immunol. Rev. 166:199-220
37. Zapata A, Diez B, Cejalvo T, Gutiérrez-de Frías C, Cortés A. 2006. Ontogeny of the immune system of fish. Fish Shellfish Immunol. 20:126-36
38. Trede NS, Langenau DM, Traver D, Look AT, Zon LI. 2004. The use of zebrafish to understand immunity. Immunity 20:367-79
39. Danilova N, Steiner LA. 2002. B cells develop in the zebrafish pancreas. Proc. Natl. Acad. Sci. USA 99:13711-16
40. Olsen MM, Kania PW, Heinecke RD, Skjoedt K, Rasmussen KJ, Buchmann K. 2011. Cellular and humoral factors involved in the response of rainbow trout gills to Ichthyophthirius multifiliis infections: Molecular and immunohistochemical studies. Fish Shellfish Immunol. 30:859-69
41. Warr GW. 1997. The adaptive immune system of fish. Dev. Biol. Stand. 90:15-21
42. Ye J, Kaattari I, Kaattari S. 2011. Plasmablasts and plasma cells: Reconsidering teleost immune system organization. Dev. Comp. Immunol. 35:1273-81
43. Kaattari SL, Zhang HL, Khor IW, Kaattari IM, Shapiro DA. 2002. Affinity maturation in trout: Clonal dominance of high affinity antibodies late in the immune response. Dev. Comp. Immunol. 26:191-200
44. Zhang Y-A, Salinas I, Sunyer JO. 2011. Recent findings on the structure and function of teleost IgT. Fish Shellfish Immunol. 31:627-34
45. Verland HS, Pettersen EF, Rønneseth A, Wergeland HI. 2010. Phagocytosis by B-cells and neutrophils in Atlantic salmon (Salmo salar L.) and Atlantic cod (Gadus morhua L.). Fish Shellfish Immunol. 28:193-204
46. Du Pasquier L, Robert J, Courtet M, Mussmann R. 2000. B-cell development in the amphibian Xenopus. Immunol. Rev. 175:201-13
47. Du Pasquier L, Schwager J, Flajnik MF. 1989. The immune system of Xenopus. Annu. Rev. Immunol. 7:251-75
48. Robert J, Ohta Y. 2009. Comparative and developmental study of the immune system in Xenopus. Dev. Dyn. 238: 1249-70
49. Zhao Y, Pan-Hammarstrom Q, Yu S, Wertz N, Zhang X, et al. 2006. Identification of IgF, a hingeregion-containing Ig class, and IgD in Xenopus tropicalis. Proc. Natl. Acad. Sci. USA 103:12087-92
50. Schaerlinger B, Bascove M, Frippiat JP. 2008. A new isotype of immunoglobulin heavy chain in the urodele amphibian Pleurodeles waltl predominantly expressed in larvae. Mol. Immunol. 45:776-86
51. Schaerlinger B, Frippiat JP. 2008. IgX antibodies in the urodele amphibian Ambystoma mexicanum. Dev. Comp. Immunol. 32:908-15
52. Marr S, Morales H, Bottaro A, Cooper M, Flajnik M, Robert J. 2007. Localization and differential expression of activation-induced cytidine deaminase in the amphibian Xenopus upon antigen stimulation and during early development. J. Immunol. 179:6783-89
53. Golub R, André S, Hassanin A, Affaticati P, Larijani M, Fellah JS. 2004. Early expression of two TdT isoforms in the hematopoietic system of the Mexican axolotl. Implications for the evolutionary origin of the N-nucleotide addition. Immunogenetics 56:204-13
54. Fellah JS, Vaulot D, Tournefier A, Charlemagne J. 1989. Ontogeny of immunoglobulin expression in the Mexican axolotl. Development 107:253-63
55. Mussmann R, Du Pasquier L, Hsu E. 1996. Is Xenopus IgX an analog of IgA? Eur. J. Immunol. 26:2823-30
56. Maniero GD, Morales H, Gantress J, Robert J. 2006. Generation of a long-lasting, protective, and neutralizing antibody response to the ranavirus FV3 by the frog Xenopus. Dev. Comp. Immunol. 30:649-57
57. Ramsey JP, Reinert LK, Harper LK, Woodhams DC, Rollins-Smith LA. 2010. Immune defenses against Batrachochytrium dendrobatidis, a fungus linked to global amphibian declines, in the South African clawed frog, Xenopus laevis. Infect. Immun. 78:3981-92
58. Chen G, Robert J. 2011. Antiviral immunity in amphibians. Viruses 3:2065-86
59. Du CC, Mashoof SM, Criscitiello MF. 2012. Oral immunization of the African clawed frog (Xenopus laevis) upregulates the mucosal immunoglobulin IgX. Vet. Immunol. Immunopathol. 145:493-98
60. Kvell K, Cooper EL, Engelmann P, Bovari J, Nemeth P. 2007. Blurring borders: Innate immunity with adaptive features. Clin. Dev. Immunol. 2007:83671
61. Zimmerman LM, Paitz RT, Vogel LA, Bowden RM. 2010. Variation in the seasonal patterns of innate and adaptive immunity in the red-eared slider (Trachemys scripta). J. Exp. Biol. 213:1477-83
62. Zimmerman LM, Vogel LA, Bowden RM. 2010. Understanding the vertebrate immune system: Insights from the reptilian perspective. J. Exp. Biol. 213:661-71
63. Gambón-Deza F, Sánchez-Espinel C, Mirete-Bachiller S, Magadán-Mompó S. 2012. Snakes antibodies. Dev. Comp. Immunol. 38:1-9
64. WuQ, WeiZ,Yang Z,Wang T, Ren L, et al. 2010. Phylogeny, genomic organization and expression of l and k immunoglobulin light chain genes in a reptile, Anolis carolinensis. Dev. Comp. Immunol. 34:579-89
65. Turchin A, Hsu E. 1996. The generation of antibody diversity in the turtle. J. Immunol. 156:3797-805
66. Portis JL, Coe JE. 1975. IgM the secretory immunoglobulin of reptiles and amphibians. Nature 258:547-48
67. Kawaguchi S, Hiruki T, Harada T, Morikawa S. 1980. Frequencies of cell-surface or cytoplasmic IgMbearing cells in the spleen, thymus and peripheral blood of the snake, Elaphe quadrivirgata. Dev. Comp. Immunol. 4:559-63
68. Wei Z, Wu Q, Ren L, Hu X, Guo Y, et al. 2009. Expression of IgM, IgD, and IgY in a reptile, Anolis carolinensis. J. Immunol. 183:3858-64
69. Warr GW, Magor KE, Higgins DA. 1995. IgY: Clues to the origins of modern antibodies. Immunol. Today 16:392-98
70. Gambón-Deza F, Sánchez Espinel C. 2008. IgD in the reptile leopard gecko. Mol. Immunol. 45:3470-76
71. Gambón-Deza F, Sánchez Espinel C, Valdueza Beneitez J. 2007. A novel IgA-like immunoglobulin in the reptile Eublepharis macularius. Dev. Comp. Immunol. 31:596-605
72. Natarajan K, Muthukkaruppan VR. 1985. Distribution and ontogeny of B cells in the garden lizard, Calotes versicolor. Dev. Comp. Immunol. 9:301-10
73. Dbrowski Z, Sano Martins IS, Tabarowski Z, Witkowska-Pelc E, Spadacci Morena DD, et al. 2007. Haematopoiesis in snakes (Ophidia) in early postnatal development. Cell Tissue Res. 328:291-99
74. Sano-Martins IS, Dabrowski Z, Tabarowski Z, Witkowska-Pelc E, SpadacciMorena DD, Spodaryk K. 2002. Haematopoiesis and a new mechanism for the release of mature blood cells from the bone marrow into the circulation in snakes (Ophidia). Cell Tissue Res. 310:67-75
75. Zapata A, Leceta J, Barrutia MG. 1981. Ultrastructure of splenic white pulp of the turtle, Mauremys caspica. Cell Tissue Res. 220:845-55
76. Cooper EL, Klumpau AE, Zapata AG. 1985. Reptilian immunity. In Biology of the Reptilia, ed. C Gans, pp. 599-678. New York: Academic Press.
77. Xu Z, Wang GL, Nie P. 2009. IgM, IgD and IgY and their expression pattern in the Chinese soft-shelled turtle Pelodiscus sinensis. Mol. Immunol. 46:2124-32
78. Hussein MF, Badir N, el-Ridi R, el-Deeb S. 1979. Effect of splenectomy on the humoral immune response in the lizard, Scincus scincus. Experientia 35:869-70
79. El-Ridi R, Badir N, El-Rouby S. 1981. Effect of seasonal variations on the immune system of the snake, Psammophis schokari. J. Exp. Zool. 216:357-65
80. Zimmerman LM, Vogel LA, Edwards KA, Bowden RM. 2010. Phagocytic B cells in a reptile. Biol. Lett. 6:270-73
81. Glick B, Chang TS, Jaap RG. 1956. The bursa of Fabricius and antibody production. Poult. Sci. 35:224-25
82. Ribatti D, Crivellato E, Vacca A. 2006. The contribution of Bruce Glick to the definition of the role played by the bursa of Fabricius in the development of the B cell lineage. Clin. Exp. Immunol. 145:1-4
83. Cooper MD. 2010. A life of adventure in immunobiology. Annu. Rev. Immunol. 28:1-19
84. Das S, Mohamedy U, Hirano M, Nei M, Nikolaidis N. 2010. Analysis of the immunoglobulin light chain genes in zebra finch: Evolutionary implications. Mol. Biol. Evol. 27:113-20
85. Watanabe H, Kobayashi K, Isayama Y. 1975. Peculiar secretory IgA system identified in chickens. II. Identification and distribution of free secretory component and immunoglobulins of IgA, IgM, and IgG in chicken external secretions. J. Immunol. 115:998-1001
86. Ratcliffe MJ. 2006. Antibodies, immunoglobulin genes and the bursa of Fabricius in chicken B cell development. Dev. Comp. Immunol. 30:101-18
87. Magor KE. 2011. Immunoglobulin genetics and antibody responses to influenza in ducks. Dev. Comp. Immunol. 35:1008-16
88. Arakawa H, Buerstedde J-M. 2009. Activation-induced cytidine deaminase-mediated hypermutation in the DT40 cell line. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364:639-44
89. Brand A, Galton J, Gilmour DG. 1983. Committed precursors of B and T lymphocytes in chick embryo bursa of Fabricius, thymus, and bone marrow. Eur. J. Immunol. 13:449-55
90. Kincade PW, Cooper MD. 1973. Immunoglobulin A: Site and sequence of expression in developing chicks. Science 179:398-400
91. Lawrence EC, Arnaud-Battandier F, Koski IR, Dooley NJ, Muchmore AV, Blaese RM. 1979. Tissue distribution of immunoglobulin-secreting cells in normal and IgA-deficient chickens. J. Immunol. 123:1767-71
92. Cihak J, Hoffmann-Fezer G, Ziegler-Heibrock HW, Stein H, Kaspers B, et al. 1991. T cells expressing the Vb1 T-cell receptor are required for IgA production in the chicken. Proc. Natl. Acad. Sci. USA 88:10951-55
93. Kincade PW, Cooper MD. 1971. Development and distribution of immunoglobulin-containing cells in the chicken. An immunofluorescent analysis using purified antibodies to m, g and light chains. J. Immunol. 106:371-82
94. Muir WI, Bryden WL, Husband AJ. 2000. Immunity, vaccination and the avian intestinal tract. Dev. Comp. Immunol. 24:325-42
95. Casteleyn C,DoomM, Lambrechts E, Van den Broeck W, Simoens P, Cornillie P. 2010. Locations of gutassociated lymphoid tissue in the 3-month-old chicken: A review. Avian Pathol. 39:143-50
96. Imamura K, Yasuda M, Riwar B, Inui S, Ekino S. 2009. Characteristic cellular composition of germinal centers. Comp. Immunol. Microbiol. Infect. Dis. 32:419-28
97. Arakawa H, Furusawa S, Ekino S, Yamagishi H. 1996. Immunoglobulin gene hyperconversion ongoing in chicken splenic germinal centers. EMBO J. 15:2540-46
98. Mehr R, Edelman H, Sehgal D, Mage R. 2004. Analysis of mutational lineage trees from sites of primary and secondary Ig gene diversification in rabbits and chickens. J. Immunol. 172:4790-96
99. Hofmann J, Greter M, Du Pasquier L, Becher B. 2010. B-cells need a proper house, whereas T-cells are happy in a cave: The dependence of lymphocytes on secondary lymphoid tissues during evolution. Trends Immunol. 31:144-53
100. Lundqvist ML,Middleton DL, Radford C, Warr GW, Magor KE. 2006. Immunoglobulins of the nongalliform birds: Antibody expression and repertoire in the duck. Dev. Comp. Immunol. 30:93-100
101. Smialek M, Tykalowski B, Stenzel T, Koncicki A. 2011. Local immunity of the respiratory mucosal system in chickens and turkeys. Pol. J. Vet. Sci. 14:291-97
102. Haghighi HR, Gong J, Gyles CL, Hayes MA, Zhou H, et al. 2006. Probiotics stimulate production of natural antibodies in chickens. Clin. Vaccine Immunol. 13:975-80
103. Ulmer-FrancoAM,Cherian G, Quezada N, FasenkoGM,McMullenLM.2012. Hatching egg and newly hatched chick yolk sac total IgY content at 3 broiler breeder flock ages. Poult. Sci. 91:758-64
104. Kovacs-Nolan J, Mine Y. 2012. Egg yolk antibodies for passive immunity. Annu. Rev. Food Sci. Technol. 3:163-82
105. Gerber HA, Morris B, Trevella W. 1986. The role of gut-associated lymphoid tissues in the generation of immunoglobulin-bearing lymphocytes in sheep. Aust. J. Exp. Biol. Med. Sci. 64(Pt. 3):201-13
106. Butler JE, Santiago-Mateo K, Sun XZ, Wertz N, Sinkora M, Francis DH. 2011. Antibody repertoire development in fetal and neonatal piglets. XX. B cell lymphogenesis is absent in the ileal Peyer's patches, their repertoire development is antigen dependent, and they are not required for B cell maintenance. J. Immunol. 187:5141-49
107. SinkoraM,Stepanova K, Butler JE, Francis D, Santiago-Mateo K, et al. 2011. Ileal Peyer's patches are not necessary for systemic B cell development and maintenance and do not contribute significantly to the overall B cell pool in swine. J. Immunol. 187:5150-61
108. Han JH, Akira S, Calame K, Beutler B, Selsing E, Imanishi-Kari T. 2007. Class switch recombination and somatic hypermutation in early mouse B cells are mediated by B cell and Toll-like receptors. Immunity 27:64-75
109. Gurish MF, Bryce PJ, Tao H, Kisselgof AB, Thornton EM, et al. 2004. IgE enhances parasite clearance and regulates mast cell responses in mice infected with Trichinella spiralis. J. Immunol. 172:1139-45
110. Watanabe N, Bruschi F, Korenaga M. 2005. IgE: A question of protective immunity in Trichinella spiralis infection. Trends Parasitol. 21:175-78
111. Cerutti A, Chen K, Chorny A. 2011. Immunoglobulin responses at the mucosal interface. Annu. Rev. Immunol. 29:273-93
112. Snoeck V, Peters IR, Cox E. 2006. The IgA system: A comparison of structure and function in different species. Vet. Res. 37:455-67
113. Bakema JE, van Egmond M. 2011. The human immunoglobulin A Fc receptor FcaRI: A multifaceted regulator of mucosal immunity. Mucosal Immunol. 4:612-24
114. Pasquier B, Launay P, Kanamaru Y, Moura IC, Pfirsch S, et al. 2005. Identification of FcaRI as an inhibitory receptor that controls inflammation: Dual role of FcRg ITAM. Immunity 22:31-42
115. Chen K, Cerutti A. 2010. New insights into the enigma of immunoglobulin D. Immunol. Rev. 237:160-79
116. Chen K, Cerutti A. 2011. The function and regulation of immunoglobulin D. Curr. Opin. Immunol. 23:345-52
117. Gray D, Gray M. 2010. What are regulatory B cells? Eur. J. Immunol. 40:2677-79
118. YoshimotoM,Montecino-Rodriguez E, Ferkowicz MJ, Porayette P, Shelley WC, et al. 2011. Embryonic day 9 yolk sac and intra-embryonic hemogenic endothelium independently generate a B-1 and marginal zone progenitor lacking B-2 potential. Proc. Natl. Acad. Sci. USA 108:1468-73
119. Ghosn EEB, Sadate-Ngatchou P, Yang Y, Herzenberg LA. 2011. Distinct progenitors for B-1 and B-2 cells are present in adult mouse spleen. Proc. Natl. Acad. Sci. USA 108:2879-84
120. Esplin BL, Welner RS, Zhang Q, Borghesi LA, Kincade PW. 2009. A differentiation pathway for B1 cells in adult bone marrow. Proc. Natl. Acad. Sci. USA 106:5773-78
121. Barber CL, Montecino-Rodriguez E, Dorshkind K. 2011. Reduced production of B-1-specified common lymphoid progenitors results in diminished potential of adult marrow to generate B-1 cells. Proc. Natl. Acad. Sci. USA 108:13700-4
122. Weill JC, Weller S, Reynaud CA. 2009. Human marginal zone B cells. Annu. Rev. Immunol. 27:267-85
123. Griffin DO, Holodick NE, Rothstein TL. 2011. Human B1 cells in umbilical cord and adult peripheral blood express the novel phenotype CD20\+CD27\+CD43\ +CD70-. J. Exp. Med. 208:67-80
124. Baumgarth N. 2011. The double life of a B-1 cell: Self-reactivity selects for protective effector functions. Nat. Rev. Immunol. 11:34-46
125. Pillai S, Cariappa A, Moran ST. 2005. Marginal zone B cells. Annu. Rev. Immunol. 23:161-96
126. Mauri C, Ehrenstein MR. 2008. The 'short' history of regulatory B cells. Trends Immunol. 29:34-40
127. Bemark M, Boysen P, Lycke NY. 2012. Induction of gut IgA production through T cell-dependent and T cell-independent pathways. Ann. N.Y. Acad. Sci. 1247:97-116
128. Murphy KP, Travers P, Walport M, Janeway C. 2012. Janeway's Immunobiology. New York: Garland Science.
129. Lang VR, Mielenz D, Neubert K, Böhm C, Schett G, et al. 2010. The early marginal zone B cell-initiated T-independent type 2 response resists the proteasome inhibitor bortezomib. J. Immunol. 185:5637-47
130. Martin F, Oliver AM, Kearney JF. 2001. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14:617-29
131. Parra D, Rieger AM, Li J, Zhang YA, Randall LM, et al. 2012. Pivotal advance: Peritoneal cavity B-1 B cells have phagocytic and microbicidal capacities and present phagocytosed antigen to CD4\+ T cells. J. Leukoc. Biol. 91:525-36
132. Gao J, Ma X, Gu W, Fu M, An J, et al. 2012. Novel functions of murine B1 cells: Active phagocytic and microbicidal abilities. Eur. J. Immunol. 42:982-92
133. Nakashima M, Kinoshita M, Nakashima H, Habu Y, Miyazaki H, et al. 2012. Pivotal advance: Characterization of mouse liver phagocytic B cells in innate immunity. J. Leukoc. Biol. 91:537-46
134. Kawamoto H. 2006. A close developmental relationship between the lymphoid and myeloid lineages. Trends Immunol. 27:169-75
135. Duan B, Morel L. 2006. Role of B-1a cells in autoimmunity. Autoimmun. Rev. 5:403-8
136. Ekser B, Ezzelarab M, Hara H, van der Windt DJ, Wijkstrom M, et al. 2012. Clinical xenotransplantation: The next medical revolution? Lancet 379:672-83
137. Dvorankova B, Broz L, Pafcuga I, Kapounkova Z, Konigova R. 2004. The role of skin bank in the treatment of severely burnt patients. Acta Chir. Plast. 46:51-55
138. Chen RH, Adams DH. 2001. Transgenic porcine valves show no signs of delayed cardiac xenograft rejection. Ann. Thorac. Surg. 71:S389-92
139. Bracy JL, Cretin N, Cooper DK, Iacomini J. 1999. Xenoreactive natural antibodies. Cell. Mol. Life Sci. 56:1001-7
140. Ohdan H, Sykes M. 2003. B cell tolerance to xenoantigens. Xenotransplantation 10:98-106
141. Dufour V, Malinge S, Nau F. 1996. The sheep Ig variable region repertoire consists of a single VH family. J. Immunol. 156:2163-70
142. Sinclair MC, Gilchrist J, Aitken R. 1997. Bovine IgG repertoire is dominated by a single diversified VH gene family. J. Immunol. 159:3883-89
143. Becker RS, Knight KL. 1990. Somatic diversification of immunoglobulin heavy chain VDJ genes: Evidence for somatic gene conversion in rabbits. Cell 63:987-97
144. Jenne CN, Kennedy LJ, Reynolds JD. 2006. Antibody repertoire development in the sheep. Dev. Comp. Immunol. 30:165-74
145. Press CM, McCullagh P, Landsverk T. 2001. Effect of early fetal splenectomy on prenatal B-cell development in sheep. Immunology 102:131-36
146. Knight KL, Winstead CR. 1997. Generation of antibody diversity in rabbits. Curr. Opin. Immunol. 9:228-32
147. Severson KM, Mallozzi M, Driks A, Knight KL. 2010. B cell development in GALT: Role of bacterial superantigen-like molecules. J. Immunol. 184:6782-89
148. Jasper PJ, Zhai SK, Kalis SL, Kingzette M, Knight KL. 2003. B lymphocyte development in rabbit: Progenitor B cells and waning of B lymphopoiesis. J. Immunol. 171:6372-80
149. Sehgal D, Schiaffella E, Anderson AO, Mage RG. 1998. Analyses of single B cells by polymerase chain reaction reveal rearranged VH with germline sequences in spleens of immunized adult rabbits: Implications for B cell repertoire maintenance and renewal. J. Immunol. 161:5347-56
150. Lee F, Chen J-L, Lin C-M,Wang F-I. 2011. Presence of bluetongue virus in the marginal zone of the spleen in acute infected sheep. Vet. Microbiol. 152:96-100
151. Booth JS, Griebel PJ, Babiuk LA, Mutwiri GK. 2009. A novel regulatory B-cell population in sheep Peyer's patches spontaneously secretes IL-10 and downregulates TLR9-induced IFNa responses. Mucosal Immunol. 2:265-75
152. Hurley WL, Theil PK. 2011. Perspectives on immunoglobulins in colostrum and milk. Nutrients 3:442-74
153. Shek PN, Dubiski S. 1975. Maternal-foetal transfer of normal IgM in the rabbit. Immunology 29:365-69
154. Angulo-Valadez CE, Ascencio F, Jacquiet P, Dorchies P, Cepeda-Palacios R. 2011. Sheep and goat immune responses to nose bot infestation: A review. Med. Vet. Entomol. 25:117-25
155. Villa-Mancera A, Méndez-Mendoza M. 2012. Protection and antibody isotype responses against Fasciola hepatica with specific antibody to pIII-displayed peptide mimotopes of cathepsin L1 in sheep. Vet. J. 194:108-12
156. Nguyen TK, Wieland W, Santema W, Hoeboer J, van Eden W, et al. 2011. Immune response of cattle immunized with a conjugate of the glycolipid glucose monomycolate and protein. Vet. Immunol. Immunopathol. 142:265-70
157. Ogunrinade AF. 1983. IgG response in natural and experimental infections of cattle with Fasciola gigantica. Vet. Parasitol. 13:325-32
158. Mosier DA, Simons KR, ConferAW,Panciera RJ, Clinkenbeard KD. 1989. Serum IgG and IgMantibody response in cattle to antigens of Pasteurella haemolytica. Vet. Immunol. Immunopathol. 22:53-65
159. Henderson NG, Stear MJ. 2006. Eosinophil and IgA responses in sheep infected with Teladorsagia circumcincta. Vet. Immunol. Immunopathol. 112:62-66
160. Corbeil LB, Anderson ML, Corbeil RR, Eddow JM, BonDurant RH. 1998. Female reproductive tract immunity in bovine trichomoniasis. Am. J. Reprod. Immunol. 39:189-98
161. Shaw RJ, Gatehouse TK, McNeill MM. 1998. Serum IgE responses during primary and challenge infections of sheep with Trichostrongylus colubriformis. Int. J. Parasitol. 28:293-302
162. Gershwin LJ. 2009. Bovine immunoglobulin E. Vet. Immunol. Immunopathol. 132:2-6
163. Ploegaert TC, Tijhaar E, Lam TJ, Taverne-Thiele A, van der Poel JJ, et al. 2011. Natural antibodies in bovine milk and blood plasma: Variability among cows, repeatability within cows, and relation between milk and plasma titers. Vet. Immunol. Immunopathol. 144:88-94
164. Schwabacher H. 1949. The occurrence of natural antibodies in rabbit sera in relation to the paracolon group of organisms. J. Hyg. 47:115-18
165. Conticello SG. 2008. The AID/APOBEC family of nucleic acid mutators. Genome Biol. 9:229
166. Malecek K, Brandman J, Brodsky JE, Ohta Y, Flajnik MF, Hsu E. 2005. Somatic hypermutation and junctional diversification at Ig heavy chain loci in the nurse shark. J. Immunol. 175:8105-15
167. Zhu C, Feng W, Weedon J, Hua P, StefanovD, et al. 2011. The multiple shark IgHchain genes rearrange and hypermutate autonomously. J. Immunol. 187:2492-501
168. Barreto VM,Magor BG. 2011. Activation-induced cytidine deaminase structure and functions: A species comparative view. Dev. Comp. Immunol. 35:991-1007.
169. Cooper MD, Alder MN. 2006. The evolution of adaptive immune systems. Cell 124:815-22
170. Sunyer JO. 2012. Evolutionary and functional relationships of B cells from fish and mammals: Insights into their novel roles in phagocytosis and presentation of particulate antigen. Infect. Disord. Drug Targets 12:200-12
171. Herzenberg LA, Kantor AB. 1992. Layered evolution in the immune system. A model for the ontogeny and development of multiple lymphocyte lineages. Ann. N.Y. Acad. Sci. 651:1-9
172. Barr TA, Brown S, Ryan G, Zhao J, Gray D. 2007. TLR-mediated stimulation of APC: Distinct cytokine responses of B cells and dendritic cells. Eur. J. Immunol. 37:3040-53
173. Boehm T. 2011. Design principles of adaptive immune systems. Nat. Rev. Immunol. 11:307-17