Retinoic acid, acting as a highly specific IgA isotype switch factor, cooperates with TGF-β1 to enhance the overall IgA response

Journal of Leukocyte Biology

Volumn 94, Issue 2, 2013, Pages 325-335

  Seo, Goo Young ^a   Jang, Young Saeng ^a   Kim, Hyun A ^a   Lee, Mi Ra ^a   Park, Mi Hee ^a   Park, Seok Rae ^b   Lee, Jeong Min ^a   Choe, Jongseon ^a   Kim, Pyeung Hyeun ^a  

^a Kangwon National University   (South Korea)

^b Konyang University   (South Korea)

Author keywords

Class switch; Gut homing molecule; Mucosal immunity

Indexed keywords

CHEMOKINE RECEPTOR CCR9; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G2B; RETINOIC ACID; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; CELL CLONE; CONTROLLED STUDY; DRUG EFFECT; IMMUNOGLOBULIN PRODUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CLASS SWITCH; GUT-HOMING MOLECULE; MUCOSAL IMMUNITY;

ANIMALS; CELLS, CULTURED; CLONAL SELECTION, ANTIGEN-MEDIATED; ENDOTOXINS; GENES, IMMUNOGLOBULIN; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOGLOBULIN G; INTEGRINS; LYMPH NODES; MESENTERY; MICE; MICE, INBRED BALB C; PEYER'S PATCHES; RECEPTORS, CCR; RECEPTORS, LYMPHOCYTE HOMING; RECEPTORS, RETINOIC ACID; TRANSFORMING GROWTH FACTOR BETA1; TRETINOIN;

EID: 84880998384     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0313128     Document Type: Article

References (53)

1. Stavnezer, J. (2000) Molecular processes that regulate class switching. Curr. Top. Microbiol. Immunol. 245, 127-168.
2. Muramatsu, M., Kinoshita, K, Fagarasan, S., Yamada, S., Shinkai, Y, Honjo, T. (2000) Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102, 553-563.
3. Xu, Z., Zan, H., Pone, E. J., Mai, T., Casali, P. (2012) Immunoglobulin class-switch DNA recombination: induction, targeting and beyond. Nat. Rev. Immunol. 12, 517-531.
4. Cerutti, A., Cols, M., Puga, I. (2013) Marginal zone B cells: virtues of innate-like antibody-producing lymphocytes. Nat. Rev. Immunol 13, 118-132.
5. McIntyre, T. M., Klinman, D. R., Rothman, P., Lugo, M., Dasch, J. R, Mond, J. J., Snapper, C. M. (1993) Transforming growth factor β 1 selectivity stimulates immunoglobulin G2b secretion by lipopolysaccharide-activated murine B cells. J. Exp. Med. 177, 1031-1037.
6. Lebman, D. A., Lee, F. D., Coffman, R L. (1990) Mechanism for transforming growth factor β and IL-2 enhancement of IgA expression in lipopolysaccharide-stimulated B cell cultures. J. Immunol. 144, 952-959.
7. Zan, H., Cerutti, A., Dramitinos, P., Schaffer, A., Casali, P. (1998) CD40 engagement triggers switching to IgA1 and IgA2 in human B cells through induction of endogenous TGF-β: evidence for TGF-β but not IL-10-dependent direct Sμ→Sα and sequential Sμ→S γ, S→γ →Sα DNA recombination. J. Immunol. 161, 5217-5225.
8. Kim, P. H., Kagnoff, M. F. (1990) Transforming growth factor β 1 increases IgA isotype switching at the clonal level. J. Immunol. 145, 3773-3778.
9. van Ginkel, F. W., Wahl, S. M., Kearney, J. F., Kweon, M. N., Fujihashi, K, Burrows, P. D., Kiyono, H., McGhee, J. R (1999) Partial IgA-defi-ciency with increased Th2-type cytokines in TGF-β 1 knockout mice. J. Immunol. 163, 1951-1957.
10. Cazac, B. B., Roes, J. (2000) TGF-β receptor controls B cell responsiveness and induction of IgA in vivo. Immunity 13, 443-451.
11. Seo, G. Y, Youn, J., Kim, P. H. (2009) IL-21 ensures TGF-β 1-induced IgA isotype expression in mouse Peyer's patches. J. Leukoc. Biol. 85, 744-750.
12. Tsuji, M., Komatsu, N., Kawamoto, S., Suzuki, K, Kanagawa, O., Honjo, T., Hori, S., Fagarasan, S. (2009) Preferential generation of follicular B helper T cells from Foxp3+ T cells in gut Peyer's patches. Science 323, 1488-1492.
13. Iwata, M., Hirakiyama, A., Eshima, Y, Kagechika, H., Kato, C, Song, S. Y (2004) Retinoic acid imprints gut-homing specificity on T cells. Immunity 21, 527-538.
14. Mora, J. R, Iwata, M., Eksteen, B., Song, S. Y, Junt, T., Senman, B., Oti-poby, K. L., Yokota, A., Takeuchi, H., Ricciardi-Castagnoli, P., Rajewsky, K, Adams, D. H., von Andrian, U. H. (2006) Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 314, 1157-1160.
15. Coombes, J. L., Siddiqui, K. R, Arancibia-Carcamo, C. V., Hall, J., Sun, C. M., Belkaid, Y, Powrie, F. (2007) A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-β and retinoic acid-dependent mechanism. J. Exp. Med. 204, 1757-1764.
16. Sun, C. M., Hall, J. A., Blank, R B., Bouladoux, N., Oukka, M., Mora, J. R, Belkaid, Y (2007) Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204, 1775-1785.
17. Benson, M. J., Pino-Lagos, K, Rosemblatt, M., Noelle, R J. (2007) All-trans retinoic acid mediates enhanced T reg cell growth, differentiation, and gut homing in the face of high levels of co-stimulation. J. Exp. Med. 204, 1765-1774.
18. Mucida, D., Park, Y., Kim, G., Turovskaya, O., Scott, I., Kronenberg, M., Cheroutre, H. (2007) Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 317, 256-260.
19. Tokuyama, H., Tokuyama, Y. (1993) Retinoids enhance IgA production by lipopolysaccharide-stimulated murine spleen cells. Cell. Immunol. 150, 353-363.
20. Tokuyama, H., Tokuyama, Y (1995) Endogenous cytokine expression profiles in retinoic acid-induced IgA production by LPS-stimulated murine splenocytes. Cell. Immunol. 166, 247-253.
21. Park, M-H., Park, S-R, Lee, M-R, Kim, Y-H., Kim, P-H. (2011) Retinoic acid induces expression of Ig germ line a transcript, an IgA isotype switching indicative, through retinoic acid receptor. Genes Genom. 33, 83-88.
22. Kim, P. H., Kagnoff, M. F. (1990) Transforming growth factor-β 1 is a costimulator for IgA production. J. Immunol. 144, 3411-3416.
23. Frangakis, M. V., Koopman, W. J., Kiyono, H., Michalek, S. M., McGhee, J. R (1982) An enzymatic method for preparation of dissociated murine Peyer's patch cells enriched for macrophages. J. Immunol. Methods 48, 33-44.
24. Yasui, H., Mike, A, Ohwaki, M. (1989) Immunogenicity of bifidobacterium breve and change in antibody production in Peyer's patches after oral administration. J. Dairy Sci. 72, 30-35.
25. Park, S. R, Lee, J. H., Kim, P. H. (2001) Smad3 and Smad4 mediate transforming growth factor-β1-induced IgA expression in murine B lymphocytes. Eur. J. Immunol. 31, 1706-1715.
26. Fazekas de St Groth, B. (1982) The evaluation of limiting dilution assays. J. Immunol. Methods 49, R11-R23.
27. Tokuyama, H., Tokuyama, Y (1999) The regulatory effects of all-trans-retinoic acid on isotype switching: retinoic acid induces IgA switch rearrangement in cooperation with IL-5 and inhibits IgG1 switching. Cell. Immunol. 192, 41-47.
28. Coffman, R L., Lebman, D. A, Shrader, B. (1989) Transforming growth factor β specifically enhances IgA production by lipopolysaccharide-stim-ulated murine B lymphocytes. J. Exp. Med. 170, 1039-1044.
29. Sonoda, E., Matsumoto, R, Hitoshi, Y, Ishii, T., Sugimoto, M., Araki, S., Tominaga, A, Yamaguchi, N., Takatsu, K. (1989) Transforming growth factor β induces IgA production and acts additively with interleukin 5 for IgA production. J. Exp. Med. 170, 1415-1420.
30. Seo, G. Y, Park, S. R., Kim, P. H. (2009) Analyses of TGF-β1-inducible Ig germ-line 72b promoter activity: involvement of Smads and NF-kB. Eur. J. Immunol. 39, 1157-1166.
31. Blomhoff, H. K, Smeland, E. B., Erikstein, B., Rasmussen, A. M., Skrede, B., Skjonsberg, C, Blomhoff, R (1992) Vitamin A is a key regulator for cell growth, cytokine production, and differentiation in normal B cells. J. Biol. Chem. 267, 23988-23992.
32. Bosma, M., Sidell, N. (1988) Retinoic acid inhibits Ca2+ currents and cell proliferation in a B-lymphocyte cell line. J. Cell. Physiol. 135, 317-323.
33. Shockett, P., Stavnezer, J. (1991) Effect of cytokines on switching to IgA and a germline transcripts in the B lymphoma I.29 jx. Transforming growth factor-β activates transcription of the unrearranged C a gene. J. Immunol. 147, 4374-4383.
34. Lebman, D. A, Nomura, D. Y, Coffman, R L., Lee, F. D. (1990) Molecular characterization of germ-line immunoglobulin A transcripts produced during transforming growth factor type β-induced isotype switching. Proc. Natl. Acad. Sci. USA 87, 3962-3966.
35. Li, S. C, Rothman, P. B., Zhang, J., Chan, C, Hirsh, D., Alt, F. W. (1994) Expression of I ^-C 7 hybrid germline transcripts subsequent to immunoglobulin heavy chain class switching. Int. Immunol. 6, 491-497.
36. Kinoshita, K, Harigai, M., Fagarasan, S., Muramatsu, M., Honjo, T. (2001) A hallmark of active class switch recombination: transcripts directed by I promoters on looped-out circular DNAs. Proc. Natl. Acad. Sci. USA 98, 12620-12623.
37. Hammerschmidt, S. I., Friedrichsen, M., Boelter, J., Lyszkiewicz, M., Kremmer, E., Pabst, O., Forster, R (2011) Retinoic acid induces homing of protective T and B cells to the gut after subcutaneous immunization in mice. J. Clin. Invest. 121, 3051-3061.
38. Watanabe, K, Sugai, M., Nambu, Y, Osato, M., Hayashi, T., Kawaguchi, M., Komori, T., Ito, Y, Shimizu, A. (2010) Requirement for Runx proteins in IgA class switching acting downstream of TGF-β 1 and retinoic acid signaling. J. Immunol. 184, 2785-2792.
39. Nolting, J., Daniel, C, Reuter, S., Stuelten, C, Li, P., Sucov, H., Kim, B. G., Letterio, J. J., Kretschmer, K, Kim, H. J., von Boehmer, H. (2009) Retinoic acid can enhance conversion of naive into regulatory T cells independently of secreted cytokines.J. Exp. Med. 206, 2131-2139.
40. Chang, S. Y, Cha, H. R, Igarashi, O., Rennert, P. D., Kissenpfennig, A, Malissen, B., Nanno, M., Kiyono, H., Kweon, M. N. (2008) Cutting edge: Langerin+ dendritic cells in the mesenteric lymph node set the stage for skin and gut immune system cross-talk. J. Immunol. 180, 4361-4365.
41. Massacand, J. C, Kaiser, P., Ernst, B., Tardivel, A., Burki, K, Schneider, P., Harris, N. L. (2008) Intestinal bacteria condition dendritic cells to promote IgA production. PLoS One 3, e2588.
42. Uematsu, S., Fujimoto, K, Jang, M. H., Yang, B. G., Jung, Y J., Nishiyama, M., Sato, S., Tsujimura, T., Yamamoto, M., Yokota, Y, Kiyono, H., Miyasaka, M., Ishii, K. J., Akira, S. (2008) Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat. Immunol. 9, 769-776.
43. Eksteen, B., Mora, J. R., Haughton, E. L., Henderson, N. C, Lee-Turner, L., Villablanca, E. J., Curbishley, S. M., Aspinall, A. I., von An-drian, U. H., Adams, D. H. (2009) Gut homing receptors on CD8 T cells are retinoic acid dependent and not maintained by liver dendritic or stellate cells. Gastroenterology 137, 320-329.
44. Kang, S. G., Park, J., Cho, J. Y, Ulrich, B., Kim, C. H. (2011) Complementary roles of retinoic acid and TGF-β1 in coordinated expression of mucosal integrins by T cells. Mucosal Immunol. 4, 66-82.
45. Bastien, J., Rochette-Egly, C. (2004) Nuclear retinoid receptors and the transcription of retinoid-target genes. Gene 328, 1-16.
46. Rastinejad, F., Wagner, T., Zhao, Q., Khorasanizadeh, S. (2000) Structure of the RXR-RAR DNA-binding complex on the retinoic acid response element DR1. EMBOJ. 19, 1045-1054.
47. Ohoka, Y, Yokota, A., Takeuchi, H., Maeda, N., Iwata, M. (2011) Retinoic acid-induced CCR9 expression requires transient TCR stimulation and cooperativity between NFATc2 and the retinoic acid receptor/reti-noid X receptor complex. J. Immunol. 186, 733-744.
48. Xiao, S., Jin, H., Korn, T., Liu, S. M., Oukka, M., Lim, B., Kuchroo, V. K. (2008) Retinoic acid increases Foxp3+ regulatory T cells and inhibits development of Th17 cells by enhancing TGF-β-driven Smad3 signaling and inhibiting IL-6 and IL-23 receptor expression. J. Immunol. 181, 2277-2284.
49. Pendaries, V., Verrecchia, F., Michel, S., Mauviel, A. (2003) Retinoic acid receptors interfere with the TGF-β/Smad signaling pathway in a ligand-specific manner. Oncogene 22, 8212-8220.
50. Schambach, F., Schupp, M., Lazar, M. A, Reiner, S. L. (2007) Activation of retinoic acid receptor-a favours regulatory T cell induction at the expense of IL-17-secreting T helper cell differentiation. Eur. J. Immunol. 37, 2396-2399.
51. Xanthou, M. (1998) Immune protection of human milk. Biol. Neonate 74, 121-133.
52. Haskell, M. J., Brown, K. H. (1999) Maternal vitamin A nutriture and the vitamin A content of human milk. J. Mammary Gland Biol. Neoplasia 4, 243-257.
53. Chun, S-K, Nam, M-S., Juhn-Su Goh, Wan-Sup Kim, Young-Hwan Han, Kim, P-H. (2004) Kinetics and biological function of transforming growth factor-β isoforms in bovine and human colostrum. J. Microbiol. BioTech. 14, 1267-1274.