Vitamin A and Retinoic Acid in the Regulation of B-Cell Development and Antibody Production

Vitamins and Hormones

Volumn 86, Issue , 2011, Pages 103-126

  Ross, A Catharine ^a,b   Chen, Qiuyan ^a   Ma, Yifan ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

B cell activation; B cell differentiation; B cell proliferation; Class switch recombination; Germinal center formation; Immunization; Retinoic acid; Transcription factors; Vitamin A status

Indexed keywords

RETINOIC ACID; RETINOL;

ANIMAL; ANTIBODY PRODUCTION; B LYMPHOCYTE; BOOK; CELL DIFFERENTIATION; CYTOLOGY; GERMINAL CENTER; HUMAN; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTIBODY FORMATION; B-LYMPHOCYTES; CELL DIFFERENTIATION; GERMINAL CENTER; HUMANS; SIGNAL TRANSDUCTION; TRETINOIN; VITAMIN A;

EID: 79952685385     PISSN: 00836729     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386960-9.00005-8     Document Type: Book

References (98)

1. Allen C.D., Cyster J.G. Follicular dendritic cell networks of primary follicles and germinal centers: Phenotype and function. Semin. Immunol. 2008, 20:14-25.
2. Allman D., Jain A., Dent A., Maile R.R., Selvaggi T., Kehry M.R., Staudt L.M. BCL-6 expression during B-cell activation. Blood 1996, 87:5257-5268.
3. Altucci L., Gronemeyer H. Nuclear receptors in cell life and death. Trends Endocrinol. Metab. 2001, 12:460-468.
4. Angelin-Duclos C., Cattoretti G., Lin K.I., Calame K. Commitment of B lymphocytes to a plasma cell fate is associated with Blimp-1 expression in vivo. J. Immunol. 2000, 165:5462-5471.
5. Balmer J.E., Blomhoff R. Gene expression regulation by retinoic acid. J. Lipid Res. 2002, 43:1773-1808.
6. Barrington R.A., Schneider T.J., Pitcher L.A., Mempel T.R., Ma M., Barteneva N.S., Carroll M.C. Uncoupling CD21 and CD19 of the B-cell coreceptor. Proc. Natl. Acad. Sci. USA 2009, 106:14490-14495.
7. Bastien J., Rochette-Egly C. Nuclear retinoid receptors and the transcription of retinoid-target genes. Gene 2004, 328:1-16.
8. Benson M.J., Pino-Lagos K., Rosemblatt M., Noelle R.J. 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. 2007, 204:1765-1774.
9. Blomhoff H.K., Smeland E.B., Erikstein B., Rasmussen A.M., Skrede B., Skjonsberg C., Blomhoff R. Vitamin A is a key regulator for cell growth, cytokine production, and differentiation in normal B cells. J. Biol. Chem. 1992, 267:23988-23992.
10. Bosma M., Sidell N. Retinoic acid inhibits Ca2+ currents and cell proliferation in a B-lymphocyte cell line. J. Cell. Physiol. 1988, 135:317-323.
11. Brigl M., Brenner M.B. How invariant natural killer T cells respond to infection by recognizing microbial or endogenous lipid antigens. Semin. Immunol. 2010, 22:79-86.
12. Calame K.L., Lin K.I., Tunyaplin C. Regulatory mechanisms that determine the development and function of plasma cells. Annu. Rev. Immunol. 2003, 21:205-230.
13. Cancro M.P. Signalling crosstalk in B cells: Managing worth and need. Nat. Rev. Immunol. 2009, 9:657-661.
14. Cattoretti G., Chang C.C., Cechova K., Zhang J., Ye B.H., Falini B., Louie D.C., Offit K., Chaganti R.S., Dalla-Favera R. BCL-6 protein is expressed in germinal-center B cells. Blood 1995, 86:45-53.
15. Chappell C.P., Jacob J. Germinal-center-derived B-cell memory. Adv. Exp. Med. Biol. 2007, 590:139-148.
16. Chen Q., Ross A.C. Vitamin A and immune function: Retinoic acid modulates population dynamics in antigen receptor and CD38-stimulated splenic B cells. Proc. Natl. Acad. Sci. USA 2005, 102:14142-14149.
17. Chen Q., Ross A.C. Retinoic acid promotes mouse splenic B cell surface IgG expression and maturation stimulated by CD40 and IL-4. Cell. Immunol. 2007, 249:37-45.
18. Chen Q., Ma Y., Ross A.C. Opposing cytokine-specific effects of all trans-retinoic acid on the activation and expression of signal transducer and activator of transcription (STAT)-1 in THP-1 cells. Immunology 2002, 107:199-208.
19. Chen X., Esplin B.L., Garrett K.P., Welner R.S., Webb C.F., Kincade P.W. Retinoids accelerate B lineage lymphoid differentiation. J. Immunol. 2008, 180:138-145.
20. Chen X., Welner R.S., Kincade P.W. A possible contribution of retinoids to regulation of fetal B lymphopoiesis. Eur. J. Immunol. 2009, 39:2515-2524.
21. Cozine C.L., Wolniak K.L., Waldschmidt T.J. The primary germinal center response in mice. Curr. Opin. Immunol. 2005, 17:298-302.
22. Crotty S., Johnston R.J., Schoenberger S.P. Effectors and memories: Bcl-6 and Blimp-1 in T and B lymphocyte differentiation. Nat. Immunol. 2010, 11:114-120.
23. Cyster J.G., Ansel K.M., Reif K., Ekland E.H., Hyman P.L., Tang H.L., Luther S.A., Ngo V.N. Follicular stromal cells and lymphocyte homing to follicles. Immunol. Rev. 2000, 176:181-193.
24. de Yebenes V.G., Ramiro A.R. Activation-induced deaminase: Light and dark sides. Trends Mol. Med. 2006, 12:432-439.
25. DeCicco K.L., Ross A.C. All-trans-retinoic acid and polyriboinosinoic:polyribocytidylic acid cooperate to elevate anti-tetanus immunoglobulin G and immunoglobulin M responses in vitamin A-deficient Lewis rats and Balb/c mice. Proc. Nutr. Soc. 2000, 59:519-529.
26. DeCicco K.L., Zolfaghari R., Li N., Ross A.C. Retinoic acid and polyriboinosinic acid act synergistically to enhance the antibody response to tetanus toxoid during vitamin A deficiency: Possible involvement of interleukin-2 receptor-beta, signal transducer and activator of transcription-1, and interferon regulatory factor-1. J. Infect. Dis. 2000, 182(Suppl 1):S29-S36.
27. DeCicco K.L., Youngdahl J.D., Ross A.C. All-trans-retinoic acid and polyriboinosinic:polyribocytidylic acid in combination potentiate specific antibody production and cell-mediated immunity. Immunology 2001, 104:341-348.
28. Dhordain P., Albagli O., Lin R.J., Ansieau S., Quief S., Leutz A., Kerckaert J.P., Evans R.M., Leprince D. Corepressor SMRT binds the BTB/POZ repressing domain of the LAZ3/BCL6 oncoprotein. Proc. Natl. Acad. Sci. USA 1997, 94:10762-10767.
29. DiLillo D.J., Matsushita T., Tedder T.F. B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann. N Y Acad. Sci. 2010, 1183:38-57.
30. Ertesvag A., Aasheim H.C., Naderi S., Blomhoff H.K. Vitamin A potentiates CpG-mediated memory B-cell proliferation and differentiation: Involvement of early activation of p38MAPK. Blood 2007, 109:3865-3872.
31. Fahlman C., Jacobsen S.E., Smeland E.B., Lomo J., Naess C.E., Funderud S., Blomhoff H.K. All-trans- and 9-cis-retinoic acid inhibit growth of normal human and murine B cell precursors. J. Immunol. 1995, 155:58-65.
32. Fields A.L., Soprano D.R., Soprano K.J. Retinoids in biological control and cancer. J. Cell. Biochem. 2007, 102:886-898.
33. Fukuda T., Yoshida T., Okada S., Hatano M., Miki T., Ishibashi K., Okabe S., Koseki H., Hirosawa S., Taniguchi M., Miyasaka N., Tokuhisa T. Disruption of the Bcl6 gene results in an impaired germinal center formation. J. Exp. Med. 1997, 186:439-448.
34. Hoag K.A., Nashold F.E., Goverman J., Hayes C.E. Retinoic acid enhances the T helper 2 cell development that is essential for robust antibody responses through its action on antigen-presenting cells. J. Nutr. 2002, 132:3736-3739.
35. Horcher M., Souabni A., Busslinger M. Pax5/BSAP maintains the identity of B cells in late B lymphopoiesis. Immunity 2001, 14:779-790.
36. Hoshino K., Takeuchi O., Kawai T., Sanjo H., Ogawa T., Takeda Y., Takeda K., Akira S. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: Evidence for TLR4 as the Lps gene product. J. Immunol. 1999, 162:3749-3752.
37. Hu C.C., Dougan S.K., McGehee A.M., Love J.C., Ploegh H.L. XBP-1 regulates signal transduction, transcription factors and bone marrow colonization in B cells. EMBO J. 2009, 28:1624-1636.
38. Ishiura N., Nakashima H., Watanabe R., Kuwano Y., Adachi T., Takahashi Y., Tsubata T., Okochi H., Tamaki K., Tedder T.F., Fujimoto M. Differential phosphorylation of functional tyrosines in CD19 modulates B-lymphocyte activation. Eur. J. Immunol. 2010, 40:1192-1204.
39. Iwakoshi N.N., Lee A.H., Glimcher L.H. The X-box binding protein-1 transcription factor is required for plasma cell differentiation and the unfolded protein response. Immunol. Rev. 2003, 194:29-38.
40. Iwata M., Hirakiyama A., Eshima Y., Kagechika H., Kato C., Song S.Y. Retinoic acid imprints gut-homing specificity on T cells. Immunity 2004, 21:527-538.
41. Jacob J., Kassir R., Kelsoe G. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. I. The architecture and dynamics of responding cell populations. J. Exp. Med. 1991, 173:1165-1175.
42. Kallies A., Nutt S.L. Terminal differentiation of lymphocytes depends on Blimp-1. Curr. Opin. Immunol. 2007, 19:156-162.
43. Klein U., Dalla-Favera R. Germinal centres: Role in B-cell physiology and malignancy. Nat. Rev. Immunol. 2008, 8:22-33.
44. Krieg A.M., Yi A.K., Matson S., Waldschmidt T.J., Bishop G.A., Teasdale R., Koretzky G.A., Klinman D.M. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 1995, 374:546-549.
45. Kuwata T., Wang I.-M., Tamura T., Ponnamperuma R.M., Levine R., Holmes K.L., Morse H.C., DeLuca L.M., Ozato K. Vitamin A deficiency in mice causes a systemic expansion of myeloid cells. Blood 2000, 95:3349-3356.
46. Lahvis G.P., Cerny J. Induction of germinal center B cell markers in vitro by activated CD4+ T lymphocytes: The role of CD40 ligand, soluble factors, and B cell antigen receptor cross-linking. J. Immunol. 1997, 159:1783-1793.
47. Lang G.A., Devera T.S., Lang M.L. Requirement for CD1d expression by B cells to stimulate NKT cell-enhanced antibody production. Blood 2008, 111:2158-2162.
48. Lin K.I., Angelin-Duclos C., Kuo T.C., Calame K. Blimp-1-dependent repression of Pax-5 is required for differentiation of B cells to immunoglobulin M-secreting plasma cells. Mol. Cell. Biol. 2002, 22:4771-4780.
49. Lomo J., Smeland E.B., Ulven S., Natarajan V., Blomhoff R., Gandhi U., Dawson M.I., Blomhoff H.K. RAR-, not RXR, ligands inhibit cell activation and prevent apoptosis in B-lymphocytes. J. Cell. Physiol. 1998, 175:68-77.
50. Ma Y., Ross A.C. The anti-tetanus immune response of neonatal mice is augmented by retinoic acid combined with polyriboinosinic:polyribocytidylic acid. Proc. Natl. Acad. Sci. USA 2005, 102:13556-13561.
51. Ma Y., Ross A.C. Toll-like receptor 3 ligand and retinoic acid enhance germinal center formation and increase the tetanus toxoid vaccine response. Clin. Vaccine Immunol. 2009, 16:1476-1484.
52. Ma Y., Chen Q., Ross A.C. Retinoic acid and polyriboinosinic:polyribocytidylic acid stimulate robust anti-tetanus antibody production while differentially regulating type 1/type 2 cytokines and lymphocyte populations. J. Immunol. 2005, 174:7961-7969.
53. MacLennan I.C., Liu Y.J., Johnson G.D. Maturation and dispersal of B-cell clones during T cell-dependent antibody responses. Immunol. Rev. 1992, 126:143-161.
54. McHeyzer-Williams L.J., Malherbe L.P., McHeyzer-Williams M.G. Helper T cell-regulated B cell immunity. Curr. Top. Microbiol. Immunol. 2006, 311:59-83.
55. Mora J.R., Iwata M., Eksteen B., Song S.Y., Junt T., Senman B., Otipoby K.L., Yokota A., Takeuchi H., Ricciardi-Castagnoli P., Rajewsky K., Adams D.H., et al. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 2006, 314:1157-1160.
56. Morgan M.A., Magnusdottir E., Kuo T.C., Tunyaplin C., Harper J., Arnold S.J., Calame K., Robertson E.J., Bikoff E.K. Blimp-1/Prdm1 alternative promoter usage during mouse development and plasma cell differentiation. Mol. Cell. Biol. 2009, 29:5813-5827.
57. Mucida D., Park Y., Kim G., Turovskaya O., Scott I., Kronenberg M., Cheroutre H. Reciprocal Th-17 and regulatory T cell differentiation mediated by retinoic acid. Science 2007, 17:256-260.
58. Muindi J.R.F., Young C.W., Warrell R.P. Clinical pharmacology of all-trans retinoic acid. Leukemia 1994, 8:1807-1812.
59. Naderi S., Blomhoff H.K. Retinoic acid prevents phosphorylation of pRB in normal human B lymphocytes: Regulation of cyclin E, cyclin A, and p21(Cip1). Blood 1999, 94:1348-1358.
60. Napoli J.L. Enzymology and biogenesis of retinoic acid. Vitamin A and Retinoids: An Update of Biological Aspects and Clinical Applications 2000, 17-27. Birkhèuser Verlag, Basel. M.A. Livrea (Ed.).
61. Northrup D.L., Allman D. Transcriptional regulation of early B cell development. Immunol. Res. 2008, 42:106-117.
62. Park C.S., Choi Y.S. How do follicular dendritic cells interact intimately with B cells in the germinal centre?. Immunology 2005, 114:2-10.
63. Park H.Y., Park J.Y., Kim J.W., Lee M.J., Jang M.J., Lee S.Y., Baek D.W., Park Y.M., Lee S.W., Yoon S., Bae Y.S., Kwak J.Y. Differential expression of dendritic cell markers by all-trans retinoic acid on human acute promyelocytic leukemic cell line. Int. Immunopharmacol. 2004, 4:1587-1601.
64. Reichert R.A., Gallatin W.M., Weissman I.L., Butcher E.C. Germinal center B cells lack homing receptors necessary for normal lymphocyte recirculation. J. Exp. Med. 1983, 157:813-827.
65. Rose M.L., Birbeck M.S., Wallis V.J., Forrester J.A., Davies A.J. Peanut lectin binding properties of germinal centres of mouse lymphoid tissue. Nature 1980, 284:364-366.
66. Ross A.C. Retinoids and the immune system. The Retinoids: Biology, Chemistry, and Medicine 1994, 521-543. Raven Press, New York. 2nd ed.
67. Ross A.C. Diet in vitamin A research. Retinoids, Methods and Protocols 2010, 295-313. Humana Press, Springer, New York. H. Sun, G.H. Travis (Eds.).
68. Ross A.C., Zolfaghari R., Weisz J. Vitamin A: Recent advances in the biotransformation, transport, and metabolism of retinoids. Curr. Opin. Gastroenterol. 2001, 17:184-192.
69. Ross A.C., Chen Q., Ma Y. Augmentation of antibody responses by retinoic acid and costimulatory molecules. Semin. Immunol. 2009, 21:42-50.
70. Saito M., Gao J., Basso K., Kitagawa Y., Smith P.M., Bhagat G., Pernis A., Pasqualucci L., Dalla-Favera R. A signaling pathway mediating downregulation of BCL6 in germinal center B cells is blocked by BCL6 gene alterations in B cell lymphoma. Cancer Cell 2007, 12:280-292.
71. Sanderson R.D., Lalor P., Bernfield M. B lymphocytes express and lose syndecan at specific stages of differentiation. Cell Regul. 1989, 1:27-35.
72. Scheffel F., Heine G., Henz B.M., Worm M. Retinoic acid inhibits CD40 plus IL-4 mediated IgE production through alterations of sCD23, sCD54 and IL-6 production. Inflamm. Res. 2005, 54:113-118.
73. Sciammas R., Shaffer A.L., Schatz J.H., Zhao H., Staudt L.M., Singh H. Graded expression of interferon regulatory factor-4 coordinates isotype switching with plasma cell differentiation. Immunity 2006, 25:225-236.
74. Shaffer A.L., Yu X., He Y., Boldrick J., Chan E.P., Staudt L.M. BCL-6 represses genes that function in lymphocyte differentiation, inflammation, and cell cycle control. Immunity 2000, 13:199-212.
75. Shaffer A.L., Lin K.I., Kuo T.C., Yu X., Hurt E.M., Rosenwald A., Giltnane J.M., Yang L., Zhao H., Calame K., Staudt L.M. Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program. Immunity 2002, 17:51-62.
76. Shapiro-Shelef M., Calame K. Regulation of plasma-cell development. Nat. Rev. Immunol. 2005, 5:230-242.
77. Siebenlist U., Brown K., Claudio E. Control of lymphocyte development by nuclear factor-kappaB. Nat. Rev. Immunol. 2005, 5:435-445.
78. Smeland E.B., Rusten L., Jacobsen S.E.W., Skrede B., Blomhoff R., Wang M.Y., Funderud S., Kvalheim G., Blomhoff H.K. All-trans retinoic acid inhibits granulocyte colony-stimulating factor-induced proliferation of CD34 human hematopoietic progenitor cells. Blood 1994, 9:2940-2945.
79. Stadanlick J.E., Kaileh M., Karnell F.G., Scholz J.L., Miller J.P., Quinn W.J., Brezski R.J., Treml L.S., Jordan K.A., Monroe J.G., Sen R., Cancro M.P. Tonic B cell antigen receptor signals supply an NF-kappaB substrate for prosurvival BLyS signaling. Nat. Immunol. 2008, 9:1379-1387.
80. Stavnezer J., Guikema J.E., Schrader C.E. Mechanism and regulation of class switch recombination. Annu. Rev. Immunol. 2008, 26:261-292.
81. Steiniger B., Barth P. Microanatomy and function of the spleen. Adv. Anat. Embryol. Cell Biol. 2000, 151(III-IX):1-101.
82. Suzuki K., Maruya M., Kawamoto S., Sitnik K., Kitamura H., Agace W.W., Fagarasan S. The sensing of environmental stimuli by follicular dendritic cells promotes immunoglobulin A generation in the gut. Immunity 2010, 33:71-83.
83. Tran T.H., Nakata M., Suzuki K., Begum N.A., Shinkura R., Fagarasan S., Honjo T., Nagaoka H. B cell-specific and stimulation-responsive enhancers derepress Aicda by overcoming the effects of silencers. Nat. Immunol. 2010, 11:148-154.
84. Tunyaplin C., Shaffer A.L., Angelin-Duclos C.D., Yu X., Staudt L.M., Calame K.L. Direct repression of prdm1 by Bcl-6 inhibits plasmacytic differentiation. J. Immunol. 2004, 173:1158-1165.
85. Usui T., Wakatsuki Y., Matsunaga Y., Kaneko S., Koseki H., Kita T. Overexpression of B cell-specific activator protein (BSAP/Pax-5) in a late B cell is sufficient to suppress differentiation to an Ig high producer cell with plasma cell phenotype. J. Immunol. 1997, 158:3197-3204.
86. Van D.E., Kulier R., Gülmezoglu A.M., Villar J. Vitamin A supplementation during pregnancy. Cochrane Database Syst. Rev. 2002, 4:CD001996.
87. Vitoux D., Nasr R., de The H. Acute prmyelocytic leukemia: New issues on pathogenesis and treatment response. Int. J. Biochem. Cell Biol. 2007, 39:1063-1070.
88. Wakatsuki Y., Neurath M.F., Max E.E., Strober W. The B cell-specific transcription factor BSAP regulates B cell proliferation. J. Exp. Med. 1994, 179:1099-1108.
89. Watanabe K., Sugai M., Nambu Y., Osato M., Hayashi T., Kawaguchi M., Komori T., Ito Y., Shimizu A. Requirement for Runx proteins in IgA class switching acting downstream of TGF-beta 1 and retinoic acid signaling. J. Immunol. 2010, 184:2785-2792.
90. Wei L.N. Retinoid receptors and their coregulators. Annu. Rev. Pharmacol. Toxicol. 2003, 43:47-72.
91. Wei D., Yang Y., Wang W. The expression of retinoic acid receptors in lymph nodes of young children and the effect of all-trans-retinoic acid on the B cells from lymph nodes. J. Clin. Immunol. 2007, 27:88-94.
92. West K.P. Extent of vitamin A deficiency among preschool children and women of reproductive age. J. Nutr. 2002, 132:2857S-2866S.
93. Integration of vitamin A supplementation with immunization: Policy and programme implication 1998, 1-7. WHO/UNICEF.
94. Xu Z., Pone E.J., Al-Qahtani A., Park S.R., Zan H., Casali P. Regulation of aicda expression and AID activity: Relevance to somatic hypermutation and class switch DNA recombination. Crit. Rev. Immunol. 2007, 27:367-397.
95. Yamamoto Y., Tsuzuki S., Tsuzuki M., Handa K., Inaguma Y., Emi N. BCOR as a novel fusion partner of retinoic acid receptor alpha in a t(X;17)(p11;q12) variant of acute promyelocytic leukemia. Blood 2010, 116:4274-4283.
96. Zhang K. Accessibility control and machinery of immunoglobulin class switch recombination. J. Leukoc. Biol. 2003, 73:323-332.
97. Zhao Z.R., Ross A.C. Retinoic acid repletion restores the number of leukocytes and their subsets and stimulates natural cytotoxicity in vitamin A-deficient rats. J. Nutr. 1995, 125:2064-2073.
98. Zhou D., Mattner J., Cantu C., Schrantz N., Yin N., Gao Y., Sagiv Y., Hudspeth K., Wu Y.P., Yamashita T., Teneberg S., Wang D., et al. Lysosomal glycosphingolipid recognition by NKT cells. Science 2004, 306:1786-1789.