1932

Abstract

We describe the domestication of the species, explore its value to agriculture and bioscience, and compare its immunoglobulin (Ig) genes to those of other vertebrates. For encyclopedic information, we cite earlier reviews and chapters. We provide current gene maps for the heavy and light chain loci and describe their polygeny and polymorphy. B-cell and antibody repertoire development is a major focus, and we present findings that challenge several mouse-centric paradigms. We focus special attention on the role of ileal Peyer's patches, the largest secondary lymphoid tissues in newborn piglets and a feature of all artiodactyls. We believe swine fetal development and early class switch evolved to provide natural secretory IgA antibodies able to prevent translocation of bacteria from the gut while the bacterial PAMPs drive development of adaptive immunity. We discuss the value of using the isolator piglet model to address these issues.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-022516-022818
2017-02-08
2024-06-12
Loading full text...

Full text loading...

/deliver/fulltext/animal/5/1/annurev-animal-022516-022818.html?itemId=/content/journals/10.1146/annurev-animal-022516-022818&mimeType=html&fmt=ahah

Literature Cited

  1. Groves C. 1.  1981. Ancestor for the pigs: taxonomy and phylogeny of the genus Sus. Tech. Bull. 3, Dep. Prehist., Res. School Pac. Stud. Aust. Natl. Univ., Canberra, Aust. [Google Scholar]
  2. Ruvinsky A, Rothschild MF. 2.  1998. Systematics and evolution of the pig. The Genetics of the Pig MF Rothschild, A Ruvinsky 2–16 Willingford, UK: CAB Int. [Google Scholar]
  3. Larson G, Cucchi T, Dobney K. 3.  2011. Genetic aspects of pig domestication. The Genetics of the Pig MF Rothschild, A Ruvinsky 14–37 Willingford, UK: CAB Int., 2nd ed.. [Google Scholar]
  4. Lloyd-Jones O. 4.  1915. What is a breed?. J. Hered. 6:19–24 [Google Scholar]
  5. Buchanan DS, Stalder K. 5.  2011. Breeds of pigs. The Genetics of the Pig MF Rothschild, A Ruvinsky 445–72 Willingford, UK: CAB Int, 2nd ed.. [Google Scholar]
  6. Sachs DH, Sykes M, Robson M, Cooper MJ. 6.  2001. Xenotransplantation. Adv. Immunol. 79:129–223 [Google Scholar]
  7. Lunney JK, Eguchi-Ogawa T, Uenishi H, Wertz N, Butler JE. 7.  2011. Immunogenetics. Genetics of the Pig MF Rothschild, A Ruvinsky 101–33 Willingford, UK: CAB Int., 2nd ed.. [Google Scholar]
  8. 8. Natl. Chick. Counc 2016. Per Capita Consumption of Poultry and Livestock, 1965 to Estimated 2016, in Pounds. Washington, DC: Natl. Chick. Counc http://www.nationalchickencouncil.org/about-the-industry/statistics/per-capita-consumption-of-poultry-and-livestock-1965-to-estimated-2012-in-pounds/ [Google Scholar]
  9. Butler JE, Zhao Y, Sinkora M, Wertz N, Kacskovics I. 9.  2009. Immunoglobulins, antibody repertoire and B cell development. Dev. Comp. Immunol. 33:321–33 [Google Scholar]
  10. Butler JE, Rainard P, Lippolis J, Salmon H, Kacskovics I. 10.  2015. The mammary gland in mucosal and regional immunity. Mucosal Immunology J Mestecky, W Strober, MW Russell, H Cheoutre, BN Lambrecht, BL Kelsall 2269–306 Cambridge, UK: Academic., 4th ed.. [Google Scholar]
  11. Butler JE, Wertz N. 11.  2012. The porcine antibody repertoire: variations on the textbook theme. Front. Immunol. 3:1–14 [Google Scholar]
  12. Butler JE, Lager KM, Golde W, Faaberg KS, Sinkora M. 12.  et al. 2014. Porcine reproductive and respiratory syndrome (PRRS): an immune dysregulatory pandemic. Immunol. Res. 59:81–108 [Google Scholar]
  13. Lemke CD, Haynes JS, Spaete R, Adolphson D, Vorwald A. 13.  et al. 2004. Lymphoid hyperplasia resulting in immune dysregulation is caused by PRRSV infection in pigs. J. Immunol. 172:1916–25 [Google Scholar]
  14. Sun X-Z, Wertz N, Lager KL, Tobin G, Butler JE. 14.  2012. Antibody repertoire development in fetal and neonatal piglets. XXIII: Fetal piglets infected with a vaccine strain of PRRS virus display the same immune dysregulation seen in isolator piglets. Vaccine 30:3646–52 [Google Scholar]
  15. Sun X-Z, Wertz N, Lager KM, Butler JE. 15.  2013. Antibody repertoire development in fetal and neonatal piglets. XV. Porcine circovirus type 2 infection results in serum IgG antibodies to ORF2, elevated IgA levels but little evidence of immune suppression. Vaccine 31:141–48 [Google Scholar]
  16. Butler JE, Weber P, Wertz N, Lager KM. 16.  2008. Porcine reproductive and respiratory syndrome virus (PRRSV) subverts development of adaptive immunity by proliferation of germline-encoded B cells with hydrophobic HCDR3s. J. Immunol. 180:2347–56 [Google Scholar]
  17. Urbaniak K, Markowska-Daniel L. 17.  2014. In vivo reassortment of influenza viruses. Acta Biochim. Pol. 61:427–31 [Google Scholar]
  18. Tumbleson ME. 18.  1986. Swine in Biomedical Research 1–3 New York: Plenum [Google Scholar]
  19. Rodgers CS, Stoltz DA, Meyerholz DK, Ostedgaards LS, Rohhlima T. 19.  et al. 2008. Disruption of the CFTR gene produces a model of cystic fibrosis in newborn pigs. Science 321:1837–41 [Google Scholar]
  20. Sieren JC, Meyerholz DK, Wang X-J, Davis BT, Newell JD Jr.. 20.  et al. 2014. Development and translational imaging of a TP53 porcine tumorigenesis model. J. Clin. Investig. 124:4052–66 [Google Scholar]
  21. Mendicino M, Ramsoondar J, Phelps C, Vaught T, Ball S. 21.  et al. 2008. Targeted disruption of the porcine immunoglobulin heavy chain locus produces a null phenotype. Transgenic Res. 20:625–41 [Google Scholar]
  22. Ramsoondar J, Mendicino M, Phelps C, Vaught T, Ball S. 22.  et al. 2011. Targeted disruption of the porcine immunoglobulin kappa light chain locus. Transgenic Res. 20:643–53 [Google Scholar]
  23. Ito T, Sendai Y, Samazaki S, Seki-Soma M, Hirose K. 23.  et al. 2014. Generation of recombination activating gene-1-deficient neonatal piglets: a model of T and B cell deficient severe combined immune deficiency. PLOS ONE 9:12e113833 [Google Scholar]
  24. Nguyen TV, Yuan L, Azevedo MS, Jeong KI, Gonzalez AM, Saif LJ. 24.  2007. Transfer of maternal cytokines to suckling piglets: in vivo and in vitro models with implication for immunomodulation of neonatal immunity. Vet. Immunol. Immunopathol. 117:236–48 [Google Scholar]
  25. Klobasa F, Habe F, Butler JE. 25.  1990. Maternal-neonatal immunoregulation: Suppression of de novo immunoglobulin synthesis of IgG and IgA, but not IgM, in neonatal piglets by bovine colostrum, is lost upon storage. Am. J. Vet. Res. 51:1407–12 [Google Scholar]
  26. Butler JE, Sinkora M. 26.  2007. The isolator piglet: a model for studying the development of adaptive immunity. Immunol. Res. 39:33–51 [Google Scholar]
  27. Butler JE. 27.  2015. Collection, handling and analysis of specimens for studies of mucosal immunity in animals of veterinary importance. Mucosal Immunology J Mestecky, W Strober, MW Russell, H Cheoutre, BN Lambrecht, BL Kelsall 2369–91 Appendix III. Cambridge, UK: Academic, 4th ed.. [Google Scholar]
  28. Butler JE, Klobasa F, Werhahn E, Cambier JC. 28.  1986. Swine as a model for the study of maternal-neonatal immunoregulation. The Swine in Biomedical Research ME Tumbleson 1883–99 New York: Plenum [Google Scholar]
  29. Padlan EA. 29.  1994. Anatomy of the antibody molecule. Mol. Immunol. 31:169–217 [Google Scholar]
  30. Butler JE, Weber P, Sinkora M, Sun J, Ford SJ, Christenson R. 30.  2000. Antibody repertoire development in fetal and neonatal piglets. II. Characterization of heavy chain complementarity-determining region 3 diversity in the developing fetus. J. Immunol. 165:6999–7011 [Google Scholar]
  31. Sinkora M, Butler JE. 31.  2016. Progress in the use of swine in developmental immunology of B and T lymphocytes. Dev. Comp. Immunol. 58:1–17 [Google Scholar]
  32. Pettinello R, Dooley H. 32.  2014. The immunoglobulins of cold-blooded vertebrates. Biomolecules 4:1045–69 [Google Scholar]
  33. Sun Y, Zhao Y. 33.  2014. Immunoglobulin genes in tetrapods. Comparative Immunoglobulin Gene Genetics A Kaushik, Y Pasman 19–34 Toronto, Can./Boca Raton, FL: Apple Acad./CRC [Google Scholar]
  34. Butler JE. 34.  1997. Immunoglobulin gene organization and the mechanism of repertoire development. Scand. J. Immunol. 45:455–62 [Google Scholar]
  35. Butler JE. 35.  2006. Preface: why I agreed to do this. Dev. Comp. Immunol. 30:1–17 [Google Scholar]
  36. Pancer Z, Sha NR, Kasamatsu J, Suzuki T, Amemiya CT. 36.  et al. 2005. Variable lymphocyte receptors in hagfish. PNAS 102:9224–29 [Google Scholar]
  37. Dooley H, Flajnik MF. 37.  2006. Antibody repertoire development in cartilaginous fish. Dev. Comp Immunol. 30:43–56 [Google Scholar]
  38. Greenberg AS, Avila D, Hughes M, Hughes A, McKinney EC, Flajnik MF. 38.  1995. A new antigen receptor gene family that undergoes rearrangement and extensive somatic diversification in sharks. Nature 374:168–73 [Google Scholar]
  39. Zhang YA, Salinas L, Li J, Parra D, Bjork S. 39.  et al. 2010. IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat. Immunol. 11:827–35 [Google Scholar]
  40. Zhao Y, Pan-Hammarström Q, Yu S, Wertz N, Zhang X. 40.  et al. 2006. Identification of IgF, a hinge-region containing Ig class and IgD in Xenopus tropicalis. PNAS 103:12087–92 [Google Scholar]
  41. Ros F, Puels J, Reichenberger N, Van Schooten W, Buelow R, Platzer J. 41.  2004. Sequence analysis of 0.5 Mb of the rabbit germline immunoglobulin heavy chain locus. Gene 330:49–59 [Google Scholar]
  42. Guo Y, Bao Y, Meng Q, Hu X, Meng Q. 42.  et al. 2012. Immunoglobulin genomics in the guinea pig (Cavia porcellus). PLOS ONE 7:e39298 [Google Scholar]
  43. De Genst E, Saerens D, Muyldermanns S, Conrath K. 43.  2006. Antibody repertoire development in camelids. Dev. Comp. Immunol. 30:187–98 [Google Scholar]
  44. Zhao Y, Cui H, Whittington CM, Wei Z, Zhang X. 44.  et al. 2009. Ornithorhynchus anatinus (platypus) links the evolution of immunoglobulin genes in eutherian mammals and non-mammalian tetrapods. J. Immunol. 183:3285–93 [Google Scholar]
  45. Hood L, Gray WR, Saunders BG, Dreyer WJ. 45.  1967. Light chain evolution. Cold Spring Harb. Symp. Quant. Biol. 32:133–46 [Google Scholar]
  46. Ratcliffe MJH. 46.  2006. Antibodies, immunoglobulin genes and the bursa of Fabricius in chicken B cell development. Dev. Comp. Immunol. 30:101–18 [Google Scholar]
  47. Reynaud CA, Anquez V, Dahan A, Weill JC. 47.  1987. A hyperconversion mechanism generates the chicken preimmune light chain repertoire. Cell 48:379–88 [Google Scholar]
  48. Sun J, Butler JE. 48.  1996. Molecular characteristics of VDJ transcripts from a newborn piglet. Immunology 88:331–39 [Google Scholar]
  49. Butler JE, Sun J, Navarro P. 49.  1996. The swine immunoglobulin heavy chain locus has a single JH and no identifiable IgD. Int. Immunol. 8:1897–904 [Google Scholar]
  50. Eguchi-Ogawa T, Sun X-Z, Wertz N, Uenishi H, Puimi F. 50.  et al. 2010. Antibody repertoire development in fetal and neonatal piglets. XI. The relationship of VDJ usage and the genomic organization of the variable heavy chain locus. J. Immunol. 184:3734–42 [Google Scholar]
  51. Butler JE, Weber P, Sinkora M, Baker D, Schoenherr A. 51.  et al. 2002. Antibody repertoire development in fetal and neonatal piglets. VIII. Colonization is required for newborn piglets to make serum antibodies to T-dependent and type 2 T-independent antigens. J. Immunol. 169:6822–30 [Google Scholar]
  52. Butler JE, Francis D, Freeling J, Weber P, Sun J, Krieg AM. 52.  2005. Antibody repertoire development in fetal and neonatal piglets. IX. Three PAMPs act synergistically to allow germfree piglets to respond to TI-2 and TD antigens. J. Immunol. 175:6772–85 [Google Scholar]
  53. Zhao Y, Pan-Hammarstrom Q, Kacskovics L, Hammarstrom L. 53.  2003. The porcine Igδ gene: unique chimeric splicing of the first constant region domain in its heavy chain transcripts. J. Immunol. 171:1312–18 [Google Scholar]
  54. Dmitriev OY, Lutsenko S, Muyldermans S. 54.  2016. Nanobodies as probes for protein dynamics in vitro and in cells. J. Biol. Chem. 291:3767–75 [Google Scholar]
  55. Sun J, Kacskovics I, Brown WR, Butler JE. 55.  1994. Expressed swine VH genes belong to a small VH gene family homologous to human VH III. J. Immunol. 153:5618–27 [Google Scholar]
  56. Butler JE, Weber P, Wertz N. 56.  2006. Antibody repertoire development in fetal and neonatal piglets. XIII. Hybrid VH genes and the pre-immune repertoire revisited. J. Immunol. 177:5459–70 [Google Scholar]
  57. Schwartz JC, Lefranc M-P, Murtaugh MP. 57.  2012. Evolution of the porcine (Sus scrofa domestica) immunoglobulin kappa locus through germline gene conversion. Immunogenetics 64:303–11 [Google Scholar]
  58. Butler JE, Wertz N, Sun J, Wang H, Chardon P. 58.  et al. 2004. Antibody repertoire in fetal and neonatal pigs. VII. Characterization of the pre-immune κ light chain repertoire. J. Immunol. 173:6794–805 [Google Scholar]
  59. Kirschbaum T, Jaenichen R, Zachau HG. 59.  1996. The mouse immunoglobulin κ locus contains about 140 variable gene segments. Eur. J. Immunol. 26:1613–20 [Google Scholar]
  60. Ekman A, Niku M, Liljavirta J, Iivanainen A. 60.  2009. Bos taurus genome sequence reveals the assortment of immunoglobulin and surrogate light chain genes in domestic cattle. BMC Immunol 10:22 [Google Scholar]
  61. Schwartz JC, Lefranc M-P, Murtaugh MP. 61.  2012. Organization, complexity and allelic diversity of the porcine (Sus scrofa domestica) immunoglobulin lambda locus. Immunogenetics 64:399–407 [Google Scholar]
  62. Sanchez P, Nadel B, Cazenave P-A. 62.  1991. Vλ-Jλ rearrangements are restricted within a V-J-C recombination unit in the mouse. Eur. J. Immunol. 21:907–11 [Google Scholar]
  63. Wertz N, Vazquez J, Wells KD, Sun J, Butler JE. 63.  2013. Antibody repertoire development in fetal and neonatal piglets. XII. Three IGLV genes comprise 70% of the pre-immune repertoire and there is little junction diversity. Mol. Immunol. 55:319–28 [Google Scholar]
  64. Butler JE, Sun XZ, Wertz N. 64.  2011. Immunoglobulin polygeny: an evolutionary perspective. Gene Duplication F Friedberg 113–40 Rijeka, Croatia: InTech [Google Scholar]
  65. Butler JE, Sun X, Wertz N, Lager KM, Chaloner K. 65.  et al. 2011. Antibody repertoire development in fetal and neonatal piglets. XXI. Usage of most VH genes remains constant during fetal and postnatal development. Mol. Immunol. 49:483–94 [Google Scholar]
  66. Kehoe MJ, Capra JD. 66.  1974. Nature and significance of immunoglobulin subclasses. N.Y. State J. Med. 74:489–91 [Google Scholar]
  67. Butler JE. 67.  1974. Immunoglobulins of the mammary secretions. Lactation: A Comprehensive Treatise III BL Larson, V Smith 217–55 Cambridge, UK: Academic [Google Scholar]
  68. Butler JE. 68.  1983. Bovine immunoglobulins: an augmented review. Vet. Immunol. Immunopathol. 4:43–152 [Google Scholar]
  69. Mossman TR, Coffman RL. 69.  1989. TH1 and TH2 cells: Different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 7:143–73 [Google Scholar]
  70. Spieker-Polet H, Yam PC, Knight KL. 70.  1993. Differential expression of 13 IgA-heavy chain genes in rabbit lymphoid tissues. J. Immunol. 150:5457–65 [Google Scholar]
  71. Wagner B. 71.  2006. Immunoglobulins and immunoglobulin genes of the horse. Dev. Comp. Immunol. 30:155–64 [Google Scholar]
  72. Butler JE, Wertz N, Deschacht N, Kacskovics I. 72.  2009. Porcine IgG: structure, genetics and evolution. Immunogenetics 61:209–30 [Google Scholar]
  73. Lefranc M-P, Lefranc G, Rabbitts TH. 73.  1982. Inherited deletion of immunoglobulin heavy chain constant region genes in normal individuals. Nature 300:760–62 [Google Scholar]
  74. Migone N, Oliviero S, de Lange G, Delacroix DL, Boschis D. 74.  et al. 1984. Multiple gene deletions within the human immunoglobulin heavy chain cluster. PNAS 81:5811–15 [Google Scholar]
  75. Schwartz JC, Murtaugh MP. 75.  2014. Characterization of a polymorphic IGLV gene in pigs (Sus scrofa). Immunogenetics 66:509–11 [Google Scholar]
  76. Brown WR, Kacskovics I, Amendt B, Shinde R, Blackmore N. 76.  et al. 1995. The hinge deletion variant of porcine IgA results from a mutation at the splice acceptor site in the first Cα intron. J. Immunol. 154:3836–42 [Google Scholar]
  77. Navarro P, Christenson R, Ekhardt G, Lunney JK, Rothschild M. 77.  et al. 2000. Genetic differences in the frequency of the hinge variants of porcine IgA is breed dependent. Vet. Immunol. Immunopathol. 73:287–95 [Google Scholar]
  78. Eguchi-Ogawa T, Toki D, Wertz N, Butler JE, Uenishi H. 78.  2012. Complete structure of the genomic sequence encoding the constant regions of the porcine immunoglobulin heavy chain. Mol. Immunol. 52:97–107 [Google Scholar]
  79. Butler JE, Wertz N, Sun X-Z, Lunney JK, Muyldermanns S. 79.  2012. Resolution of an immunodiagnostic dilemma: heavy chain chimeric antibodies for species in which plasmacytomas are unknown. Mol. Immunol. 53:140–48 [Google Scholar]
  80. Kloep A, Wertz N, Mendicino M, Butler JE. 80.  2012. Linkage haplotype for IgG and IgA subclass genes. Immunogenetics 64:469–73 [Google Scholar]
  81. Knight KL. 81.  1992. Restrictive VH gene usage and generation of antibody diversity in rabbits. Annu. Rev. Immunol. 10:593–616 [Google Scholar]
  82. Cook GP, Tomlinson LM. 82.  1995. The human immunoglobulin VH repertoire. Immunol. Today 16:237–42 [Google Scholar]
  83. Guo X, Schwartz JC, Murtaugh MP. 83.  2016. Genome variation in the porcine immunoglobulin variable region. Immunogenetics 68:285–93 [Google Scholar]
  84. Butler JE, Wertz N. 84.  2006. Antibody repertoire development in fetal and neonatal piglets. XVII. IgG subclass transcription revisited with emphasis on new IgG3. J. Immunol. 177:5480–89 [Google Scholar]
  85. Navarro P, Christenson R, Weber P, Rothschild M, Ekhard G. 85.  et al. 2000. Porcine IgA allotypes are not equally transcribed or expressed in heterozygous swine. Mol. Immunol. 37:653–64 [Google Scholar]
  86. Klobasa F, Habe F, Werhahn E, Butler JE. 86.  1985. Changes in the concentration of serum IgG, IgA, and IgM of sows throughout the reproductive cycle. Vet. Immunol. Immunopathol. 10:341–53 [Google Scholar]
  87. Werhahn E, Klobasa F, Butler JE. 87.  1981. Investigation of some factors which influence the absorption of IgG by the neonatal piglet. Vet. Immunol. Immunopathol. 2:35–51 [Google Scholar]
  88. Klobasa F, Werhahn E, Butler JE. 88.  1987. The composition of sow milk during lactation. J. Anim. Sci. 64:1458–66 [Google Scholar]
  89. Bohl EH, Saif LJ. 89.  1975. Passive immunity in transmissible gastroenteritis of swine: immunoglobulin characteristics of antibodies in milk after inoculating virus by different routes. Infect. Immun. 11:23–32 [Google Scholar]
  90. Tlaskalova-Hogenova H, Mandel L, Trebichavsky I, Kovaru F, Barot R, Sterzl J. 90.  1994. Development of immune responses in early pig ontogeny. Vet. Immunol. Immunopathol. 43:135–42 [Google Scholar]
  91. McAleer J, Weber P, Sun J, Butler JE. 91.  2005. Antibody repertoire development in fetal and neonatal piglets. XI. The thymic B cell repertoire develops independently from that in blood and mesenteric lymph nodes. Immunology 114:171–83 [Google Scholar]
  92. Sinkora M, Sinkorova J, Butler JE. 92.  2002. B cell development and VDJ rearrangement in the fetal pig. Vet. Immunol. Immunopathol. 87:341–46 [Google Scholar]
  93. Sinkora J, Rehakova Z, Sinkora M, Cukrowska C, Tlaskalova-Hogenova H. 93.  2002. Early development of immune system in pigs. Vet. Immunol. Immunopathol. 87:301–6 [Google Scholar]
  94. Sinkora M, Butler JE, Holtmeier W, Sinkorova J. 94.  2005. Lymphocyte development in fetal piglets: facts and surprises. Vet. Immunol. Immunopathol. 108:177–84 [Google Scholar]
  95. Sinkora M, Butler JE. 95.  2009. The ontogeny of the porcine immune system. Dev. Comp. Immunol. 33:273–83 [Google Scholar]
  96. Butler JE, Santiago-Mateo K, Sun X-Z, Wertz N, Sinkora M, Francis DH. 96.  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 [Google Scholar]
  97. Sinkora M, Stepanova K, Butler JE, Francis D, Santiago-Mateo K. 97.  et al. 2011. Ileal Peyer's patches (IPP) 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 [Google Scholar]
  98. Butler JE, Sinkora M. 98.  2013. The enigma of the lower gut-associated lymphoid tissue (GALT). J. Leukoc. Biol. 94:259–70 [Google Scholar]
  99. Sinkora M, Sinkorova J. 99.  2014. B cell lymphogenesis in swine is located in the bone marrow. J. Immunol. 193:5023–32 [Google Scholar]
  100. Sinkora M, Sinkorova J, Stepanova K. 100.  2017. Ig light chain precedes heavy chain rearrangement during development of B cells in swine. J. Immunol. 198:2 In press [Google Scholar]
  101. Sinkora M, Sun J, Sinkorova J, Christenson RK, Ford SP, Butler JE. 101.  2003. Antibody repertoire development in fetal and neonatal piglets. VI. B-cell lymphogenesis occurs at multiple sites with differences in the frequency of in-frame rearrangements. J. Immunol. 170:1781–88 [Google Scholar]
  102. Sun X-Z, Wertz N, Lager K, Sinkora M, Stepanova K. 102.  et al. 2012. Antibody repertoire development in fetal and neonatal piglets. XXII. λ rearrangement precedes κ rearrangement during B-cell lymphogenesis in swine. Immunology. 137:149–59 [Google Scholar]
  103. Mussmann R, Courtet M, Du Pasquier L. 103.  1998. Development of the early B cell population in Xenopus. Eur. J. Immunol. 28:2947–59 [Google Scholar]
  104. Iacoangeli A, Lui A, Naik U, Ohta Y, Flajnik M, Hsu E. 104.  2015. Biased immunoglobulin light chain gene usage in the shark. J. Immunol. 195:3992–4000 [Google Scholar]
  105. Butler JE, Sun J, Weber P, Ford SP, Rehakova Z. 105  et al. 2001. Antibody repertoire development in fetal and neonatal piglets. IV. Switch recombination, primarily in fetal thymus, occurs independent of environmental antigen and is only weakly associated with repertoire diversification. J. Immunol. 167:3239–49 [Google Scholar]
  106. Butler JE, Santiago-Mateo K, Wertz N, Sun X-Z, Sinkora M, Francis DL. 106.  2016. Antibody repertoire development in fetal and neonatal piglets. XXIV. Hypothesis: The ileal Peyers patches (IPP) are the major source of primary, undiversitifed IgA antibodies in newborn piglets. Dev. Comp. Immunol. 65:340–61 [Google Scholar]
  107. Allen WD, Porter P. 107.  1973. The relative distribution of IgM and IgA cells in intestinal mucosa and lymphoid tissues of the young unweaned pig and their significance in ontogenesis of secretory immunity. Immunology 24:493–501 [Google Scholar]
  108. Pabst R, Geist M, Rothkoetter HJ, Fritz FJ. 108.  1988. Postnatal development and lymphocyte production of jejunal and ileal Peyer's patches in normal and gnotobiotic pigs. Immunology 64:539–44 [Google Scholar]
  109. Butler JE, Klobasa F, Werhahn E. 109.  1981. The differential localization of IgA, IgM, and IgG in the gut of suckled neonatal piglets. Vet. Immunol. Immunopathol. 2:53–65 [Google Scholar]
  110. Pollard M, Sharon S. 110.  1970. Response of the Peyers patches in germfree mice in antigen stimulation. Infect. Immun. 2:96–100 [Google Scholar]
  111. Macpherson A, Harris N. 111.  2004. Interactions between commensal intestinal bacteria and the immune system. Nat. Rev. Immunol. 4:478–85 [Google Scholar]
  112. Neutra MR, Frey A, Kraehenbuhl J-P. 112.  1996. Epithelial M cells: gateway for mucosal infection and immunization. Cell 86:345–48 [Google Scholar]
  113. Binns RM, Licence SY. 113.  1985. Patterns of migration of labelled blood lymphocyte subpopulations: evidence for two types of Peyer's patch in the young pig. Adv. Exp. Med. Biol. 186:661–68 [Google Scholar]
  114. Carlens O. 114.  1928. Studien ueber das lymphatische Gewebe des Darm Kanals bei einigen der Mengenverhaeltnisse und alter involution diese Gewebe in Duenndarm des Rindes. Z. Anat. Entwickl.-Gesh. 86:393–493 [Google Scholar]
  115. Barman NN, Bianchi ATJ, Zwart RJ, Pabst R, Rothkötter HJ. 115.  1997. Jejunal and ileal Peyer's patches in pigs differ in their postnatal development. Anat. Embryol. 195:41–50 [Google Scholar]
  116. Reynolds JD, Morris B. 116.  1983. The evolution and involution of Peyer's patches in fetal and postnatal sheep. Eur. J. Immunol. 13:627–35 [Google Scholar]
  117. Griebel PJ, Hein WR. 117.  1996. Expanding the role of Peyer's patches in B cell ontogeny. Immunol. Today 17:30–39 [Google Scholar]
  118. Reynolds JD, Kennedy L, Peppard J, Pabst R. 118.  1991. Ileal Peyer's patch emigrants are predominately B cells and travel to all lymphoid tissues in sheep. Eur. J. Immunol. 21:283–89 [Google Scholar]
  119. Wesermann DR, Portuguese AJ, Meyer AM, Gallager MP, Cluff-Jones K. 119.  et al. 2013. Microbial colonization influences early B-lineage development in the gut lamina propria. Nature 501:112–15 [Google Scholar]
  120. Reynaud CA, Garcia C, Hein WR, Weill JC. 120.  1995. Hypermutation generating the sheep immunoglobulin repertoire is an antigen-independent process. Cell 80:115–25 [Google Scholar]
  121. Butler JE, Sinkora M. 121.  2013. The enigma of the lower gut-associated lymphoid tissue (GALT). J. Lymph. Biol. 94:1–12 [Google Scholar]
  122. Tlaskalova-Hogenova H, Kverka M, Verdu EF, Wells JM. 122.  2015. Gnotobiology and the study of complex interactions between the intestinal microbiota, probiotics and the host. Mucosal Immunology J Mestecky, W Strober, MW Russell, H Cheroutre, BN Lambrecht, BL Kelsall 109–33 Cambridge, UK: Academic, 4th ed.. [Google Scholar]
  123. Heremans JF. 123.  1974. Immunoglobulin A. The Antigens M Sela 365–522 Cambridge, UK: Academic [Google Scholar]
  124. Johnansson MEV, Ambort D, Pelaseyed T, Schütte A, Gustafsson JK. 124.  et al. 2011. Composition and functional role of the mucus layers in the intestine. Cell. Mol. Life Sci. 68:3635–41 [Google Scholar]
  125. Lanning DK, Rhee K-J, Knight KL. 125.  2005. Intestinal bacteria and development of the B-lymphocyte repertoire. Trends Immunol 26:420–26 [Google Scholar]
  126. Weinstein PD, Anderson AO, Mage RG. 126.  1994. Rabbit IgH sequences in appendix germinal centers: VH diversification by gene conversion-like and hypermutation mechanisms. Immunity 1:647–59 [Google Scholar]
  127. Sehgal D, Mage RG, Schiaffella E. 127.  1998. VH mutant rabbits lacking the VH1a2 gene develop a2+ B cells in the appendix by gene conversion-like alteration of a rearranged VH4 gene. J. Immunol. 160:1246–55 [Google Scholar]
  128. Cukrowska B, Kozakova H, Rehakova Z, Sinkora J, Tlaskalova-Hogenova H. 128.  2001. Specific antibody and immunoglobulin response after intestinal colonization of germ-free piglets with non-pathogenic Escherichia coli086. Immunobiology 204:425–33 [Google Scholar]
  129. Kandasamy S, Chattha KS, Vlasova AN, Rajashekora G, Saif LJ. 129.  2014. Lactobacilli and Bifidobacteria enhance mucosal B cell responses and differentially modulate system antibody responses to an oral human rotavirus vaccine in a neonatal gnotobiotic pig disease model. Gut Microbes 5:639–51 [Google Scholar]
  130. Wen K, Tin C, Wang H, Yang X, Li G. 130.  et al. 2014. Probiotic Lactobacillus rhaminous GG enhanced Th1 cellular immunity but did not affect antibody responses in a human gut microbiota transplant neonatal gnotobiotic pig model. PLOS ONE 9:4e94504 [Google Scholar]
  131. Wells JM, Rossi O, Meijerink M, van Baarlen P. 131.  2011. Epithelial crosstalk at the microbiota-mucosal interface. PNAS 108:4607–14 [Google Scholar]
  132. Kawai T, Akira S. 132.  2006. Innate immune recognition of viral infection. Nat. Immunol. 7:131–37 [Google Scholar]
  133. Butler JE, Lemke CD, Weber P, Sinkora M, Lager LM. 133.  2012. Antibody repertoire development in fetal and neonatal piglets. XIX. Undiversified B cells with hydrophobic HCDR3s preferentially proliferate in the porcine reproductive and respiratory syndrome. J. Immunol. 178:6320–31 [Google Scholar]
  134. Ippolito GC, Schelonka RL, Zemlin M, Zhaung Y, Gartland GL. 134.  et al. 2006. Forced enrichment for hydrophobic amino acids in immunoglobulin CDR3-H3 impairs splenic B cell development but not antibody production. J. Exp. Med. 203:1567–78 [Google Scholar]
  135. Cukrowska B, Sinkora J, Rehakova Z, Sinkora M, Splichal I. 135.  et al. 1996. Isotype and antibody specificity of spontaneously formed immunoglobulins in pig fetuses and germ-free piglets: production by CD5 B cells. Immunology 88:611–17 [Google Scholar]
  136. Macpherson A, Gatto D, Sainsbury E, Harriman G, Hengartner H, Zinkernagel R. 136.  2000. A primitive T cell-independent mechanism of intestinal mucosal IgA response to commensal bacteria. Science 288:2222–26 [Google Scholar]
  137. Van der Waaij LA, Limburg PC, Mesander G, van der Waaij D. 137.  1996. In vivo coating of anaerobic bacteria in human feces. Gut 38:348–54 [Google Scholar]
  138. Mathias A, Corthesy B. 138.  2011. Recognition of gram-positive intestinal bacteria by hybridoma- and colostrum-derived secretory immunoglobulin A is mediated by carbohydrates. J. Biol. Chem. 286:17239–47 [Google Scholar]
  139. Dallas SD, Rolfe RD. 139.  1998. Binding of Clostridium difficile toxin A to human milk secretory component. J. Med. Microbiol. 47:879–88 [Google Scholar]
  140. Perrier C, Sprenger N, Corthesy B. 140.  2006. Glycans on secretory component participate in innate protection against mucosal pathogens. J. Biol. Chem. 281:14280–87 [Google Scholar]
  141. Sait LC, Galic M, Price JD, Simpfendorfer DA, Uren TK. 141.  et al. 2007. Secretory antibodies reduce systemic responses against the gastrointestinal commensal gut flora. Int. Immunol. 19:257–65 [Google Scholar]
/content/journals/10.1146/annurev-animal-022516-022818
Loading
/content/journals/10.1146/annurev-animal-022516-022818
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error