1α,25-dihydroxyvitamin D3 increases IgA serum antibody responses and IgA antibody-secreting cell numbers in the Peyer's patches of pigs after intramuscular immunization

Clinical and Experimental Immunology

Volumn 135, Issue 3, 2004, Pages 380-390

  Van Der Stede, Y ^a,c   Verfaillie, T ^a   Cox, E ^a   Verdonck, F ^a   Goddeeris, B M ^a,b  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c Lab Animal Health Care Antwerpen   (Belgium)

Author keywords

1 ,25(OH)2D3; Cytokine mRNA expression; IgA; Pigs

Indexed keywords

CALCITRIOL; CYTOKINE; GAMMA INTERFERON; HUMAN SERUM ALBUMIN; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN M ANTIBODY; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; STEROID HORMONE; TRANSFORMING GROWTH FACTOR BETA; DIHYDROXY VITAMIN D3; DIHYDROXY-VITAMIN D3; DRUG DERIVATIVE; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; IMMUNOLOGICAL ADJUVANT; SERUM ALBUMIN; VITAMIN D;

ACTIVE IMMUNIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE ACTIVATION; BONE MARROW; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFECT; GENE EXPRESSION; INTESTINE LYMPHATIC TISSUE; LAMINA PROPRIA; LYMPH NODE; NONHUMAN; NUCLEOTIDE SEQUENCE; PEYER PATCH; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; SWINE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; VITAMIN SUPPLEMENTATION; ANIMAL; BIOSYNTHESIS; BLOOD; GENETICS; IMMUNIZATION; IMMUNOLOGY; IMMUNOPHENOTYPING; INTRAMUSCULAR DRUG ADMINISTRATION; METHODOLOGY; MUCOSAL IMMUNITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; CYTOKINES; GENE EXPRESSION; IMMUNITY, MUCOSAL; IMMUNIZATION; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; IMMUNOPHENOTYPING; INJECTIONS, INTRAMUSCULAR; LYMPH NODES; PEYER'S PATCHES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SERUM ALBUMIN; SWINE; VITAMIN D;

EID: 1542329521     PISSN: 00099104     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2003.02377.x     Document Type: Article

References (72)

1. Bouillon R, Garmyn M, Verstuyft A, Segaert S, Casteels K, Mathieu C. Paracrine role for calcitriol in the immune system and skin creates new therapeutical possibilities for vitamin D analogs. Eur J Endocrinol 1995; 133:7-16.
2. 3. Transplant Proc 2001; 33:58-9.
3. Lemire JM, Adams JS, Sakai R, Jordan SC. 1-alpha,25-dihydroxyvitamin D3 suppresses proliferation and immunoglobulin production by normal human peripheral blood monomorphonuclear cells. J Clin Invest 1984; 74:657-61.
4. Veldman CM, Cantorna MT, DeLuca HF. Expression of 1α,25- dihydroxyvitamin D(3) receptor in the immune system. Arch Biochem Biophys 2000; 374:334-8.
5. Morgan JW, Reddy GS, Uskokovic MR et al. Functional block for 1 alpha,25-dihydroxyvitamin D3-mediated gene regulation in human B lymphocytes. J Biol Chem 1994; 269:13437-43.
6. Morgan JW, Morgan DM, Lasky SR, Ford D, Kouttab N, Maizel AL. Requirements for the induction of vitamin D-mediated gene regulation in normal human B lymphocytes. J Immunol 1996; 157:2900-8.
7. Morgan JW, Sliney DJ, Morgan DM, Maizel AL. Differential regulation of gene transcription in subpopulations of human B lymphocytes by vitamin D3. Endocrinology 1999; 140:381-91.
8. Abe E, Miyaura C, Sakagami H et al. Differentiation of mouse myeloid leukemia cells induced by 1 alpha,25-dihydroxyvitamin D3. Proc Natl Acad Sci USA 1981; 78:4990-4.
9. Penna G, Adorini L. 1-alpha,25-dihydroxyvitamin D3 inhibits differentiation, maturation, activation, and survival of dendritic cells leading to impaired alloreactive T cell activation. J Immunol 2000; 164:2405-11.
10. Griffin MD, Lutz W, Phan VA, Bachman LA, McKean DJ, Kumar R. Dendritic cell modulation by 1alpha,25 dihydroxyvitamin D3 and its analogs: a vitamin D receptor-dependent pathway that promotes a persistent state of immaturity in vitro and in vivo. Proc Natl Acad Sci USA 2001; 98:6800-5.
11. Rigby WF, Stacy T, Fanger MW. Inhibition of T lymphocyte mitogenesis by 1α,25-dihydroxyvitamin D3 (calcitriol). J Clin Invest 1984; 74:1451-5.
12. Bhalla AK, Amento EP, Serog B, Glimcher LH. 1α,25-Dihydroxyvitamin D3 inhibits antigen-induced T cell activation. J Immunol 1984; 133:1748-54.
13. D'Ambrosio D, Cippitelli M, Coccilo GM et al. Inhibition of IL-12 production by 1α,25-dihydroxyvitamin D3. J Clin Invest 1998; 101:252-62.
14. Cippitelli M, Santoni A. Vitamin D3: a transcriptional modulator of the interferon-γ gene. Eur J Immunol 1998; 28:3017-30.
15. Alroy I, Towers T, Freedman L. Transcriptional repression of the interleukin-2 gene by vitamin D3. Direct inhibition of NFATp/AP-1 complex formation by a nuclear hormone receptor. Mol Cell Biol 1995; 15:5789-99.
16. Takeuchi A, Reddy GS, Kobayashi T, Okano T, Park J, Sharma S. Nuclear factor of activated T-cells (NFAT) as a molecular target for 1γ,25-dihydroxyvitamin D3-mediated effects. J Immunol 1998; 160:209-18.
17. Towers TL, Freedman LP. Granulocyte-macrophage colony stimulating factor gene transcription is directly repressed by the vitamin D3 receptor. J Biol Chem 1998; 273:8483-91.
18. Daynes RA, Araneo BA. The development of effective vaccine adjuvants employing natural regulators of T-cell lymphokine production in vivo. In: Ades, EW, Rest, RF, Morse, SA, eds. Annals of the New York Academy of Sciences: microbial pathogenesis and immune response. New York: New York Academy of Science, 1994:144-61.
19. Daynes A, Elena Y, Enioutina SB et al. The induction of common mucosal immunity by hormonally immunomodulated peripheral immunisation. Infect Immun 1996; 64:1100-9.
20. Cantorna TM, Woodward WD, Hayes CE, DeLuca HF. 1γ,25- dihydroxyvitamin D3 is a positive regulator for the two anti-encephalitogenic cytokines TGF-β1 and IL-4. J Immunol 1998; 160:5314-9.
21. Fukaura H, Kent SC, Pietrusewicz MJ, Khy SJ, Weiner HL, Hafler DA. Induction of circulating myelin basic protein and proteolipid protein-specific transforming growth factor-beta 1-secreting Th3 T cells by oral administration of myelin in multiple sclerosis patients. J Clin Invest 1996; 98:70-7.
22. 3 stimulates transforming growth factor-beta 1 synthesis by mouse renal proximal tubular cells. Kidney Blood Press Res 1999; 22:99-105.
23. Letterio JJ, Roberts AB. Regulation of immune responses by TGF-β. Annu Rev Immunol 1998; 16:137-61.
24. McGhee JR, Mestecky J, Dertzbaugh MT, Eldridge JH, Hirasawa M, Kiyono H. The mucosal immune system: from fundamental concepts to vaccine development. Vaccine 1992; 10:75-88.
25. Enioutina EY, Visic D, McGee A, Daynes RA. The induction of systemic and mucosal immune responses following the subcuteneous immunisation of mature adult mice: characterisation of the antibodies in mucosal secretions of animals immunized with antigen formulations containing a vitamin D3 adjuvant. Vaccine 1999; 17:3050-64.
26. Enioutina EY, Visic D, Daynes RA. The induction of systemic and mucosal immune responses to antigen-adjuvant compositions administered into the skin: alterations in the migratory properties of dendritic cells appears to be important for stimulating mucosal immunity. Vaccine 2000; 18:2753-67.
27. Van der Stede Y, Cox E, Van den Broeck W, Goddeeris BM. Enhanced induction of the IgA response in pigs by calcitriol after intramuscular immunisation. Vaccine 2001; 19:1870-8.
28. Van den Broeck W, Cox E, Goddeeris BM. Induction of immune responses in pigs following oral administration of purified F4 fimbriae. Vaccine, 1999; 17:2020-9.
29. Van der Heijden PJ, Stok W, Bianchi ATJ. Contribution of immunoglobulins secreting cells in the murine small intestine to the total 'bacground' immunoglobulin production. Immunology 1987; 62:551-5.
30. Pescovitz MD, Lunney JK, Sachs DH. Preparation and characterization of monoclonal antibodies reactive with porcine PBL. J Immunol 1984; 133:368.
31. Zuckermann FA, Gaskins HR. distribution of porcine CD4/CD8 double positive T lymphocytes in mucosa-associated lymphoid tissues. Immunology 1996; 87:493-9.
32. Van Zaane D, Hulst MM. Monoclonal antibodies against porcine immunoglobulin isotypes. Vet Immunol Immunopathol 1987; 16:23-36.
33. Hammerberg C, Shurig GG. Characterization of monoclonal antibodies directed against swine leukocytes. Vet Immunol Immunopathol 1986; 11:107.
34. Bailey M, Stevens K, Bland PW, Stokes CR. A monoclonal antibody recognizing an epitope associated with pig interleukin-2 receptors. J Immunol Meth 1992; 153:85-91.
35. Verfaillie T, Cox E, To LT et al. Comparative analysis of porcine cytokine production by mRNA and protein detection. Vet Immunol Immunopathol 2001; 81:97-112.
36. Dozois CM, Oswald E, Gautier N, Serthelon J-P, Fairbrother JM, Oswald IP. Reverse transcription-polymerase chain reaction method to analyze the porcine cytokin gene expression. Vet Immunol Immunpathol 1997; 58:287-300.
37. Goodall JC, Emery DC, Bailey M, English LS, Hall L. cDNA cloning of porcine interleukin 2 by polymerase chain reaction. Biochem Biophys Acta 1991; 1089:257-8.
38. Bailey M, Perry AC, Bland PW, Stokes CR, Hall L. Nucleotide and deduced amino acid sequence of porcine interleukin 4 cDNA derived from lamina propria lymphocytes. Biochim Biophys Acta 1993; 1171:328-30.
39. Richards CD, Saklatvala J. Molecular cloning and sequence of porcine interleukin 6 cDNA and expression of mRNA in synovial fibroblasts in vitro. Cytokine 1991; 3:269-76.
40. Blancho G, Gianello P, Germana S, Baetscher M, Sachs DH, LeGuern C. Molecular identification of porcine interleukin 10: regulation of expression in a kidney allograft model. Proc Natl Acad Sci USA 1995; 92:2800-4.
41. Dijkmans R, Vandenbroeck K, Beuken E, Billiau A. Sequence of the porcine interferon-gamma (IFN-γ) gene. Nucl Acids Res 1990; 18:4259.
42. Derynck R, Goeddel DV, Ullrich A et al. Synthesis of messenger RNAs for transforming growth factors alpha and beta and the epidermal growth factor receptor by human tumors. Cancer Res 1987; 47:707-12.
43. Vanderpooten A, Goddeeris BM, De Roose P, Hedrickx L, Biront P, Desmettre P. Evaluation of parenteral vaccination methods with glycoproteins against Aujeszky's disease in pigs. Vet Microbiol 1997; 55:81-9.
44. 3 enhances milk antibody titers to Escherichia coli 35 vaccine. J Dairy Sci 1999; 82:1904-9.
45. Lemire JM, Archer DC, Beck L, Spiegelberg HL. Immunosuppressive actions of 1,25-dihydroxyvitamin D3: preferential inhibition of Th1 function. J Nutr 1995; 125 (Suppl.):1704S-8.
46. Mosmann TR, Sad S. The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol Today 1996; 17:138-46.
47. Crawley A, Raymond C, Wilkie BN. Differential control of immunoglobulin isotype production by porcine B-cells cultured with cytokines. Vet Immunol Immunopathol 2002; 91:141-54.
48. Pierce NF, Gowans JL. Cellular kinetics of the intestinal immune response to cholera toxoid in rats. J Exp Med 1975; 142:1550-63.
49. Fuhrman JA, Cebra JJ. Special features of the priming process for a secretory IgA response. B cell priming with cholera toxin. J Exp Med 1981; 153:534-44.
50. Yuan L, Geyer A, Saif L. Short-term immunoglobulin A B-cell memory resides in intestinal lymphoid tissues but not in bone marrow of gnotbiotic pigs inoculated with Wa human rotavirus. Immunology 2001; 103:188-98.
51. Coffin SE, Offit PA. Induction of mucosal B-cell memory by intramuscular inoculation of mice with rotavirus. J Virol 1998; 72:3479-83.
52. Coffin SE, Moser CA, Cohen MS, Clark HF, Offit AP. Immunologic correlates of protection against rotavirus challenge after intramuscular immunisation of mice. J Virol 1997; 71:7851-6.
53. Van der Stede Y, Cox E, Verdonck F, Vancaeneghem S, Goddeeris BM. Reduced faecal excretion of F4+-E. coli by intramuscular immunisation of suckling piglets by addition of 1α,25-dihydroxyvitamin D3 of CpG-oligodeoxynucleotides. Vaccine 2003; 21:1023-32.
54. Pabst R, Geist M, Röthkötter HJ, Fritz FJ. Postnatal development and lymphocyte production of jejunal and ileal Peyer's patches in normal and gnotobiotic pigs. Immunology 1988; 64:539-44.
55. Bianchi ATJ, Scholten JW, Moonen-Leusen HWM, Boersma WJ. Development of the natural response of immunoglobulin secreting cells in the pig as function of organ, age and housing. Dev Comp Immunol 1999; 23:511-20.
56. Barman NN, Bianchi ATJ, Zwart RJ, Pabst R, Röthkötter HJ. Jejunal and ileal Peyer's patches in pigs differ in their postnatal development. Anat Embryol 1996; 195:41-50.
57. Fujita T, Matsui T, Nakao Y, Watanabe S. T lymphocyte subsets in osteoporosis. Effect of 1-alpha hydroxyvitamin D3. Miner Electrolyte Metab 1984; 10:375-8.
58. Matsui T, Nakao Y, Koizumi T, Nakagawa T, Fujita T. 1, 25-Dihydroxyvitamin D3 regulates proliferation of activated T-lymphocyte subsets. Life Sci 1985; 37:95-101.
59. Zofkova I, Kancheva RL. The effect of 1α,25 (OH)2 vitamin D3 on CD4+/CD8+ subsets of T lymphocytes in postmenopausal women. Life Sci 1997; 61:147-52.
60. 3-treated monocytes. Arthritis Rheum 1992; 35:110-9.
61. Xu H, Soruri A, Gieseler RK, Peters JH. 1,25-Dihydroxyvitamin D3 exerts opposing effects to IL-4 on MHC class-II antigen expression, accessory activity, and phagocytosis of human monocytes. Scand J Immunol 1993; 38:535-40.
62. 3 and cytokines on the expression of MHC antigens, complement receptors and other antigens on human blood monocytes and U 937 cells: role in cell differentiation, activation and phagocytosis. Immunology 1997; 90:286.
63. Lunney JK, Walker K, Goldman T et al. Overview of the first international workshop to define swine leukocyte cluster of differentiation (CD) antigens. Vet Immunol Immunopathol 1994; 43:193-206.
64. Denham S, Shimizu M, Bianchi ATJ, Zwart RJ, Carr MM, Parkhouse RME. Monoclonal antibodies recognising differentiation antigens on B-cells. Vet Immunol Immunopathol 1994; 43:259-67.
65. Morgan JW, Kouttab N, Ford D, Maizel AL. Vitamin D-mediated gene regulation in phenotypically defined human B cell subpopulations. Endoricnology 2000; 141:3225-34.
66. Mathieu C, Adorini L. The coming of age of 1,25-dihydroxyvitamin D3 analogs as immunomodulatory agents. Trends Mol Med 2002; 8:174-9.
67. Boonstra A, Barrat FJ, Crain C, Heath VL, Savelkoul HF, O'Garra A. 1alpha,25-Dihydroxyvitamin D3 has a direct effect on naive CD4(+) T cells to enhance the development of Th2 cells. J Immunol 2001; 167:4974-80.
68. Staeva-Vieira TP, Freedman LP. 1,25-dihydroxyvitamin D3 inhibits IFN-gamma and IL-4 levels during in vitro polarization of primary murine CD4+ T cells. J Immunol 2002; 168:1181-9.
69. Lebman DA, Lee FD, Doffman RL. Mechanism for transforming growth factor β and IL-2 enhancement of IgA expression in lipopolysaccharide-stimulated B cell cultures. J Immunol 1990; 144:942-59.
70. Wanidworanun C, Strober W. Predominant role of tumor necrosis factor-alpha in human monocytes IL-10 synthesis. J Immunol 1993; 151:6853-61.
71. Randow F, Syrbe U, Meisel C et al. Mechanism of endotoxin desensitisation: involvement of interleukin 10 and transforming growth factor beta. J Exp Med 1995; 181:1887-92.
72. Brown WC, Woods VM, Chitko-McKown CG, Hash SM, Rice-Ficht AC. Interleukin-10 is expressed by bovine type 1, type 2 helper, and unrestricted parasite-specific T-cell clones and inhibits proliferation of all three subsets in an accessory-dependent manner. J Virol 1994; 62:4697-708.