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

Journal of Immunology

Volumn 169, Issue 12, 2002, Pages 6822-6830

  Butler, John E ^a   Weber, Patrick ^a   Sinkora, Marek ^a,b   Baker, Diane ^c   Schoenherr, Amanda ^a   Mayer, Balazs ^d   Francis, David ^c  

^a UNIVERSITY OF IOWA   (United States)

^b INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^c SOUTH DAKOTA STATE UNIVERSITY   (United States)

^d UNIVERSITY OF VETERINARY MEDICINE   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; FLUORESCEIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; KEYHOLE LIMPET HEMOCYANIN; T DEPENDENT ANTIGEN; TRINITROPHENYL; TYPE 2 T INDEPENDENT ANTIGEN; UNCLASSIFIED DRUG; BACTERIUM ANTIBODY; DRUG DERIVATIVE; FLUORESCEIN ISOTHIOCYANATE; FLUORESCEIN ISOTHIOCYANATE KEYHOLE LIMPET HEMOCYANIN; FLUORESCEIN ISOTHIOCYANATE-KEYHOLE LIMPET HEMOCYANIN; HEMOCYANIN; IMMUNOGLOBULIN; KEYHOLE-LIMPET HEMOCYANIN; THYMUS INDEPENDENT ANTIGEN; TRINITROPHENYL KEYHOLE LIMPET HEMOCYANIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ARTICLE; B LYMPHOCYTE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; FETUS; GERMFREE ANIMAL; IMMUNIZATION; NEWBORN; NONHUMAN; PERITONEUM; PRIORITY JOURNAL; ANIMAL; BIOSYNTHESIS; BLOOD; COMPARATIVE STUDY; CYTOLOGY; ESCHERICHIA COLI O157; GROWTH, DEVELOPMENT AND AGING; ILEUM; IMMUNOLOGY; INTESTINE MUCOSA; MICROBIOLOGY; PATHOGENICITY; PEYER PATCH; SPECIES DIFFERENCE; SWINE;

ANIMALS; ANIMALS, NEWBORN; ANTIBODIES, BACTERIAL; ANTIGENS, T-INDEPENDENT; B-LYMPHOCYTES; CELL DIFFERENTIATION; ESCHERICHIA COLI; ESCHERICHIA COLI O157; FETUS; FLUORESCEIN-5-ISOTHIOCYANATE; HEMOCYANIN; ILEUM; IMMUNIZATION, SECONDARY; IMMUNOGLOBULIN G; IMMUNOGLOBULINS; INTESTINAL MUCOSA; PEYER'S PATCHES; SPECIES SPECIFICITY; SWINE;

EID: 0037114154     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.169.12.6822     Document Type: Article

References (75)

1. Cebra, J. J., H.-Q. Jiang, J. Sterzl, and H. Tlaskalova-Hogenova. 1998. The role of mucosal microbiota in the development and maintenance of the mucosal immune system. In Mucosal Immunology, Chapt. 17, P. O. Ogra, J. Mestecky, M. E. Iamm, W. Strober, J. R. McGhee, and J. Bienenstock, eds. Academic Press, New York, pp. 267-280
2. Gustafsson, B. E., and C. B. Laurell. 1959. Gammaglobulin production in germfree rats after bacterial contamination. J. Exp. Med. 110:675.
3. Thorbecke, G. J. 1959. Some histological and functional aspects of lymphoid tissue in germfree animals. I. Morphological studies. Ann. NY Acad. Sci. 78:237.
4. Ohwaki, M., N. Yasutake, H. Yasui, and R. Ogura. 1976. Comparative study on humoral immune responses in germfree and conventional mice. Immunology 32:43.
5. Olson, G. B., and B. S. Wostman. 1996. Cellular and humoral immune response of germfree mice stimulated with 7S H6S or Salmonella typhimurium. J. Immunol. 97:275.
6. Butler, J. E., J. Sun, P. Navarro, P. Weber, and D. Francis. 2000. Antibody repertoire development in fetal and newborn piglets. III. Colonization of the gastrointestinal tract selectively diversifies and expands the pre-immune repertoire in mucosal lymphoid tissue. Immunology 100:119.
7. Tlaskalova, H., V. Kamarytova, and L. Mandel. 1970. The immune response of germ-free piglets after peroral monocontamination with living Escherichia coli strain 086. I. The fate of antigen, dynamics and site of antibody formation, nature of antibodies and formation of heterohaemogglutinins. Folio Biol. 16:177.
8. Drasar, B. S., and P. A. Barrow. 1985. Aspects of Microbiology, Vol. 10: Intestinal microbiology. Van Nostrand Reinhold, Wokingham, U.K.
9. Ducluzeau, R. 1967. Equilibre antres deux souches bacterinnes Escherichia coli et Staphylococcus pyogenes selon les conditions der leur en seman canmen dans le tube digestifdes souris axenique. CR Acad Sci D (Paris) 265:1657.
10. Kenworthy, R., and W. E. Crabb. 1963. Intestinal flora of young pigs, with reference to early weaning. Escherichia coli and scowers. J. Comp. Pathol. 73:215.
11. McAllister, J. S., J. J. Kurtz, and E. C. Short, Jr. 1979. Changes in the intestinal flora of young pigs with post-weaning diarrhea or edema disease. J. Anim. Sci. 49:868.
12. Smith, H. W., and J. E. T. Jones. 1963. The effect of the addition of copper sulfate to the diet on the bacterial flora of the alimentary tract of the pig. J. Appl. Bacteriol. 26:262.
13. Mestecky, J., and J. R. McGhee. 1987. Immunoglobulin A (IgA): molecular and cellular interactions involved in IgA biosynthesis and immune response. Adv. Immunol. 40:153.
14. Yoshimura, A., E. Lien, R. R. Ingalls, E. Tuomanen, R. Dziarski, and D. Golenboek. 1999. Cutting edge: recognition of Gram-positive cell wall components by the innate immune system occurs via Toll-like receptor 2. J. Immunol. 163:1.
15. Ellouz, F., A. Adam, R. Ciorbaru, and E. Lederer. 1974. Minimal structural requirements for adjuvant activity of bacterial peptidoglycan derivatives. Biochem. Biophys. Res. Commun. 59:1317.
16. Nagao, S., T. Miki, and A. Tanaka. 1981. Macrophage activation by muramyl dipeptide (MDP) without lymphocyte participation. Microbiol. Immunol. 25:41.
17. Takada, H., and S. Kotani. 1985. Immunopharmacological activities of synthetic muramyl-peptides. In Immunology of the Bacterial Cell Envelope. D. E. S. Stewart-Tull and M. Davis, eds. John Wiley & Sons, Chichester, U.K., pp. 119-152.
18. Cario, E., I. M. Roseberg, S. L. Brandwein, P. L. Beck, H. C. Reinecker, and D. K. Podolsky. 2000. Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing Toll-like receptors. J. Immunol. 164:966.
19. Hoshino, K., K. Takeda, T. Kawai, H. Sanjo, T. Ogawa, Y. Takeda, K. Takeda, and S. Akira. 1999. Toll-like receptor 4 (TLR-4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 and the LPS gene product. J. Immunol. 162:3749.
20. Wechsler-Reya, R. J., and J. G. Moore. 1996. Lipopolysaccharide prevents apoptosis and induces responsiveness to antigen receptor cross-linking in immature B-cells. Immunology 89:356.
21. McFadden, S. F., and E. S. Vitetta. 1984. sIgD-negative B cells from neonatal mice do not respond to the thymus-independent TNP-Ba in limiting dilution cultures. J. Immunol. 132:1717.
22. Nossal, G. J. V., and B. L. Pike. 1984. A reappraisal of "T-independent" antigens. II. Studies on single, hapten-specific B-cells from neonatal CBA/H or CBA/N mice fail to support classification into TI-1 and TI-2 categories. J. Immunol. 132:1696.
23. Nordin, A. A., and M. H. Schrier, 1982. T-cell control of the antibody response to the T-independent antigen DAGG-Ficoll. J. Immunol. 129:557.
24. Krieg, A. M., and H. Wagner. 2000. Causing a commotion in the blood: immunotherapy progresses from bacteria to bacterial DNA. Immunol. Today 21:521.
25. Butler, J. E. 1974. Immunoglobulins of the mammary secretions. In: Lactation: A Comprehensive Treatise. Vol. III. Chapt. 5. B. L. Larson and V. Smith, eds. Academic Press, New York, pp. 217-255.
26. Butler, J. E. 1998. Immunoglobulins and immune cells in animal milks. In Mucosal Immunology, Chapt. 98, P. L. Ogra, J. Mestecky, M. E. Lamm, W. Strober, J. R. McGhee, and J. Bienenstock, eds. Academic Press, New York, pp. 1531-1554.
27. Butler, J. E., J. Sun, P. Weber, S. P. Ford, Z. Rehakova, J. Sinkora, and K. Lager. 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.
28. Sinkora, M., J. Sinkorova, and J. E. Butler. 2002. B cell development and VDJ rearrangement in the fetal pig. Vet. Immunol. Immunopathol. 87:341.
29. Butler, J. E., J. Sun, P. Weber, S. P. Ford, Z. Rehakova, J. Sinkora, D. Francis, and K. Lager. 2002. Switch recombination in fetal porcine thymus is uncoupled from somatic mutation. Vet. Immunol. Immunopath. 87:307.
30. Miniatis, O. P., and D. Jol. 1978. Gnotobiotic pigs derivision and rearing. Can. J. Compl. Med. 42:428.
31. Francis, D. H., J. E. Collins, and J. R. Duimstra. 1986. Infection of gnotobiotic pigs with Escherichia coli 0157:H7 strain associated with an outbreak of hemorrhagic colitis. Infect. Immun. 51:953.
32. Inman, J. K. 1975. Thymus-independent antigens: the preparation of covalent, hapten-Ficoll conjugates. J. Immunol. 114:704.
33. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with the Folin phenol reaction. J. Biol. Chem. 177:13.
34. Butler, J. E., L. Ni, W. R. Brown, B. Rosenberg, J. Chang, and E. W. Voss, Jr. 1993. The immunochemistry of sandwich ELISA. VI. Greater than ninety percent of monoclonal and seventy-five percent of polyclonal anti-fluoresyl capture antibodies (CAbs) are denatured by passive adsorption. Mol. Immunol. 30:1165.
35. Butler, J. E. 1994. Enzyme-linked immunosorbent assay. In Immunochemistry, Chapt. 29. C. J. Van Oss and M. H. V. Regenmortel, eds. Marcel Dekker, New York, pp. 759-803.
36. Butler, J. E., and R. G. Hamilton. 1991. Quantitation of specific antibodies: methods of expression, standards, solid-phase considerations and specific applications. In Immunochemistry of Solid-Phase Immunoassay, Chapt. 9. J. E. Butler, ed. CRC Press, Boca Raton, pp. 173-198.
37. Peterman, J. 1991. Immunochemical considerations in the analyses of data from non-competitive solid-phase immunoassay. In Immunochemistry of Solid-Phase Immunoassay. J. E. Butler, ed. CRC Press, Boca Raton, pp. 47-66.
38. Butler, J. E., J. E. Spradling, J. H. Peterman, K. S. Joshi, and S. J. Challacombe. 1990. Humoral immunity in root caries in an elderly population. I. Establishment of a reliable approach for measuring specific antibodies in serum and saliva, their specific activities, rate of salivary secretion and relationship to other, salivary proteins. Oral Microbiol. Immunol. 58:107.
39. Czerkinsky, C., A. S. Rees, L. A. Bergmeier, and S. J. Challacombe. 1983. The detection and specificity of class specific antibodies to whole bacterial cells using a solid phase immunoassay. Clin. Exp. Immunol. 53:192.
40. Whalen, B. J., and I. Goldschneider. 1993. Identification and characterization of B-cell precursors in rat lymphoid tissues. I. Adoptive transfer assay for precursors of TI-1, TI-2 and TD antigen-reactive B-cells. Cell. Immunol. 151:168.
41. Mosier, D. E., J. J. Mond, and E. A. Goldings. 1977. The ontogeny of thymic independent antibody responses in vitro in normal mice and mice with an x-linked B-cell defect. J. Immunol. 119:1874.
42. Mond, J. J., I. Scher, D. E. Mosier, M. Baese, and W. E. Paul. 1978. T-independent responses in B-cell defective CBA/N mice to Brucella abortus and to trinitrophenyl (TNP) conjugates of Brucella abortis. Eur. J. Immunol. 8:459.
43. Snapper, C. M., F. R. Rosas, M. A. Moorman, and J. J. Mond. 1997. Restoration of T cell-independent type 2 induction of Ig secretion by neonatal B cells in vitro. J. Immunol. 158:2731.
44. Kepron, M. R., Y.-W. Chen, J. W Uhr, and E. S. Vitetta. 1989. IL-4 induces the specific rearrangement of γl genes on the expressed and unexpressed chromosomes of lipopolysaccharide-activated normal murine B-cells. J. Immunol. 143:334.
45. Li, M., J. W. Chung, and N. Maizels. 1997. Developmental specificity of immunoglobulin heavy chain switch region recombination activities. Mol. Immunol. 34:201.
46. Stavnezer, J., G. Radcliffe, Y. Lin, J. Nietupski, L. Berggren, R. Sitia, and E. Severinson. 1988. Immunoglobulin heavy chain switching may be directed by poor induction of transcripts from constant region genes. Proc. Natl. Acad. Sci. USA 85:7704.
47. Sparwasser, T., T. Miethke, G. Lipford, A. Evdmann, H. Hacker, K. Heeg, and H. Wagner. 1997. Macrophages sense pathogens via DNA motifs: induction of tumor necrosis factor-α-mediated shock. Eur. J. Immunol. 27:1671.
48. Makeshita, F., C. A. Leifer, I. Gursel, K. J. Ishii, S. Takeshita, M. Gursel, and D. M. Klinman. 2001. Cutting edge: role of Toll-like receptor 9 in CpG DNA induced activation of human cells. J. Immunol. 167:3555.
49. Janeway, C. A., Jr., P. Travers, M. Walport, and J. D. Capra. 1999. Immunobiology. Garland, New York.
50. Mitsuyama, M., R. Ohara, K. Amako, K. Nomoto, T. Yokokkura, and K. Nomoto. 1986. Ontogeny of macrophage function to release superoxide anion in conventional and germfree mice. Infect. Immun. 52:236.
51. Talafantova, M., and L. Mandel. 1985. Protective activity of Streptococcus faecalis against pathogenic action of Escherichia coli 055 in gnotobiotic piglets. Folia Microbiol. 30:329.
52. Chelvarajan, R. L., N. L. Gilbert, and S. Bondada. 1998. Neonatal murine B lymphocytes respond to polysaccharide antigens in the presence of IL-1 and IL-6. J. Immunol. 161:3315.
53. Letvin, N. L., B. Benacerraf, and R. N. Germain. 1981. B-lymphocyte responses to trinitrophenyl-conjugated Ficoll: requirement for T-lymphocytes and Ig-bearing adherent cells. Proc. Natl. Acad. Sci USA 78:5113.
54. Mond, J. J., P. K. A. Mongini, D. Sieckmann, and W. E. Paul. 1980. Role of T-lymphocytes in the response to TNP-AECM-Ficoll. J. Immunol. 215:1066.
55. Mond, J. J., J. Farrar, W. E. Paul, J. Fuller-Farvar, M. E. Schaefer, and M. J. Howard. 1983. T-cell independence and factor reconstitution of in vitro antibody respones to TNP-B. abortus and TNP-Ficoll: restoration of depleted responses with chromatographed fractions of a T-cell derived factor. J. Immunol. 131:633.
56. Umesaki, Y., H. Setoyama, S. Matsumoto, and Y. Okada. 1993. Expansion of α/β T-cell receptor-bearing intestinal intraepithelial lymphocytes after microbial colonization in germfree mice and its independence from thymus. Immunology 79:32.
57. Bandiera, A., T. Monta-Sanatos, S. Itohata, S. Degermann, C. Heusser, S. Tonegawa, and M. Coutinho. 1990. Localization of γ/δ T-cells is independent of normal microbial colonization. J. Exp. Med. 172:239.
58. Zhang, J., Y. J. Lui, I. C. MacLennan, D. Gray, and P. J. Lane. 1988. B cell memory to thymus-independent antigens type I and type 2; the role of lipopolysaccharide in B memory induction. Eur. J. Immunol. 18:1417.
59. Shu, Q., and H. S. Gill. 2001. A dietary probiotic (Bifidobacterium lactis HNO19) reduces the severity of Escherichia coli O157:H7 infection in mice. Med. Microbiol. Immunol. 189:147.
60. Matzinger, P. 2001. Assay I: the danger model in its historical context. Scand. J. Immunol. 54:4.
61. MacPherson, A. J., D. Gatto, E. Sainsburg, G. R. Harriman, H. Hengartner, and R. M. Zingernagel. 2000. A primitive T-cell independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 288:2222.
62. Ochsenbein, A. F., and R. Zinkernagel. 2000. Natural antibodies and complement link innate and acquired immunity. Immunol. Today 1:624.
63. Butler, J. E., J. Sun, P. Weber, and R. Christenson. 2000. Antibody repertoire development in fetal and neonatal piglets. II. Characterization of CDR3 diversity in the developing fetus. J. Immunol. 165:6999.
64. Heidt, P. J., and J. M. Vossen. 1992. Experimental and clinical gnotobiotics: influence of the microflora on graft-versus-host disease after allogenic bone marrow transplantation. J. Med. 23:161.
65. Taurog, J. E., J. A. Richardson, J. T. Croft, W. A. Simmons, M. Zhou, J. L. Fernandez-Sueiro, E. Balish, and R. E. Hammer. 1994. The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats. J. Exp. Med. 180:2359.
66. Pendergast, J. K., L. E. McGuigan, A. F. Geczy, Y. D. L. Kwong, and J. P. Edmonds. 1984. Persistence of HLA-B27 cross-reactive bacteria in the bowel flora of patients with ankylosing spondylitus. Infect. Immun. 46:686.
67. Pabst, R., M. Geist, H. J. Rothkötter, and F. J. Fritz. 1988. Postnatal development and lymphocyte production of jejunal and ileal Peyer's patches in normal and gnotobiotic pig. Immunology 64:539.
68. Uhr, G. 1993. Vergleichende Untersuchungen am Darmtrakt des Wild-und Hauschweines unter besonderer Berücksichtigung des Darmschleimhaut-immunosystem. Habilitationsschrift Tieärztlichen Hochschule, Hannover.
69. Reynaud, C. A. C. R. McKay, R. G. Müller, and J. C. Weil. 1991. Somatic generation of diversity in a mammalian primary lymphoid organ: the sheep ileal Peyer's patches. Cell 64:995.
70. Butler, J. E. 1997. Immunoglobulin gene organization and the mechanism of repertoire development. Scand. J. Immunol. 45:455.
71. Navarro, P., R. Christenson, P. Weber, M. Rothschild, G. Ekhard, J. Lemky, and J. Butler. 2000. Porcine IgA allotypes are not equally transcribed or expressed in heterozygous swine. Mol. Immunol. 37:653.
72. Reynolds, J. D., and B. Morris. 1984. The effect of antigen on the development of Peyer's patches in sheep. Eur. J. Immunol. 14:1.
73. Miyakawa, M., Y. Sumi, K. Sakurai, M. Ukai, N. Hirabayashi and G. Ito. 1969. Serum γ-globulin and lymphoid tissue in the germfree rats. Acta Haematol. Jpn 32:501.
74. Knight, K. L., and M. A. Crane. 1994. Generating the antibody repertoire in rabbit. Adv. Immunol. 56:179.
75. H diversification by gene conversion-like and hypermutation mechanisms. Immunity 1:647.