Respiratory tract epithelial cells express retinaldehyde dehydrogenase ALDH1A and enhance IgA production by stimulated B cells in the presence of vitamin A

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Rudraraju, Rajeev ^a   Jones, Bart G ^a   Surman, Sherri L ^a   Sealy, Robert E ^a   Thomas, Paul G ^a,b   Hurwitz, Julia L ^a,b  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN A; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN ALDH1A; RETINAL DEHYDROGENASE; RETINOL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE ACTIVATION; CELL ISOLATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; IMMUNOFLUORESCENCE; IMMUNOGLOBULIN PRODUCTION; MACROPHAGE; MOUSE; NONHUMAN; NOSE; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; RESPIRATORY EPITHELIUM; RESPIRATORY SYSTEM; SPLEEN CELL; STAINING; UPREGULATION;

ALDEHYDE DEHYDROGENASE; ANIMALS; ANTIBODY FORMATION; ANTIGENS, CD11C; B-LYMPHOCYTES; CELL LINE; COCULTURE TECHNIQUES; CYTOKINES; DENDRITIC CELLS; GENE EXPRESSION; IMMUNOGLOBULIN A; MICE; RESPIRATORY MUCOSA; RNA, MESSENGER; SPLEEN; VITAMIN A;

EID: 84897948147     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086554     Document Type: Article

References (64)

1. Iwata M, Hirakiyama A, Eshima Y, Kagechika H, Kato C, et al. (2004) Retinoic acid imprints gut-homing specificity on T cells. Immunity 21: 527-538. (Pubitemid 39370508)
2. Mark M, Ghyselinck NB, Chambon P (2006) Function of retinoid nuclear receptors: lessons from genetic and pharmacological dissections of the retinoic acid signaling pathway during mouse embryogenesis. Annu Rev Pharmacol Toxicol 46: 451-480. (Pubitemid 43271197)
3. Cassani B, Villablanca EJ, De CJ, Wang S, Mora JR (2012) Vitamin A and immune regulation: role of retinoic acid in gut-associated dendritic cell education, immune protection and tolerance. Mol Aspects Med 33: 63-76.
4. Sommer A, Tarwotjo I, Hussaini G, Susanto D (1983) Increased mortality in children with mild vitamin A deficiency. Lancet 2: 585-588. (Pubitemid 13051044)
5. Sommer A, Katz J, Tarwotjo I (1984) Increased risk of respiratory disease and diarrhea in children with preexisting mild vitamin A deficiency. Am J Clin Nutr 40: 1090-1095. (Pubitemid 15210589)
6. Stephens D, Jackson PL, Gutierrez Y (1996) Subclinical vitamin A deficiency: a potentially unrecognized problem in the United States. Pediatr Nurs 22: 377-89, 456.
7. Njuguna M, Msukwa G, Shilio B, Tumwesigye C, Courtright P, et al. (2009) Causes of severe visual impairment and blindness in children in schools for the blind in eastern Africa: changes in the last 14 years. Ophthalmic Epidemiol 16: 151-155.
8. Mora JR, Iwata M, Von Andrian UH (2008) Vitamin effects on the immune system: vitamins A and D take centre stage. Nat Rev Immunol 8: 685-698.
9. Shenai JP, Chytil F, Jhaveri A, Stahlman MT (1981) Plasma vitamin A and retinol-binding protein in premature and term neonates. J Pediatr 99: 302-305. (Pubitemid 11046516)
10. Schleicher RL, Sternberg MR, Pfeiffer CM (2013) Race-ethnicity is a strong correlate of circulating fat-soluble nutrient concentrations in a representative sample of the U.S. Population. J Nutr 143: 966S-976S.
11. Napoli JL (2012) Physiological insights into all-trans-retinoic acid biosynthesis. Biochim Biophys Acta 1821: 152-167.
12. Mora JR, Von Andrian UH (2009) Role of retinoic acid in the imprinting of gut-homing IgA-secreting cells. Semin Immunol 21: 28-35.
13. Samarut E, Rochette-Egly C (2012) Nuclear retinoic acid receptors: conductors of the retinoic acid symphony during development. Mol Cell Endocrinol 348: 348-360.
14. Tokuyama H, Tokuyama Y (1993) Retinoids enhance IgA production by lipopolysaccharide-stimulated murine spleen cells. Cell Immunol 150: 353-363. (Pubitemid 23290339)
15. Mora JR, Iwata M, Eksteen B, Song SY, Junt T, et al. (2006) Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 314: 1157-1160. (Pubitemid 44789048)
16. Mora JR, Bono MR, Manjunath N, Weninger W, Cavanagh LL, et al. (2003) Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature 424: 88-93. (Pubitemid 36834847)
17. Bahl R, Bhandari N, Kant S, Molbak K, Ostergaard E, et al. (2002) Effect of vitamin A administered at Expanded Program on Immunization contacts on antibody response to oral polio vaccine. Eur J Clin Nutr 56: 321-325. (Pubitemid 34413825)
18. Rudraraju R, Surman SL, Jones BG, Sealy R, Woodland DL, et al. (2012) Reduced frequencies and heightened CD103 expression among virus-induced CD8 (+) T cells in the respiratory tract airways of vitamin A-deficient mice. Clin Vaccine Immunol 19: 757-765.
19. Surman SL, Rudraraju R, Sealy R, Jones B, Hurwitz JL (2012) Vitamin A deficiency disrupts vaccine-induced antibody-forming cells and the balance of IgA/IgG isotypes in the upper and lower respiratory tract. Viral Immunol 25: 341-344.
20. Wilson CM, Gatewood JW, McCormack JM, Walker WS (1991) Immortalization of growth factor-dependent mouse splenic macrophages derived from cloned progenitors. J Immunol Methods 137: 17-25.
21. Kappler JW, Skidmore B, White J, Marrack P (1981) Antigen-inducible, H-2-restricted, interleukin-2-producing T cell hybridomas. Lack of independent antigen and H-2 recognition. J Exp Med 153: 1198-1214. (Pubitemid 11107588)
22. McCormack JM, Askew D, Walker WS (1993) Alloantigen presentation by individual clones of mouse splenic macrophages. Selective expression of IL-1 alpha in response to CD8+ T cell-derived IFN-gamma defines the alloantigen-presenting phenotype. J Immunol 151: 5218-5227. (Pubitemid 23332331)
23. Tokuyama Y, Tokuyama H (1996) Retinoids as Ig isotype-switch modulators. The role of retinoids in directing isotype switching to IgA and IgG1 (IgE) in association with IL-4 and IL-5. Cell Immunol 170: 230-234. (Pubitemid 26227848)
24. Xu LL, Warren MK, Rose WL, Gong W, Wang JM (1996) Human recombinant monocyte chemotactic protein and other C-C chemokines bind and induce directional migration of dendritic cells in vitro. J Leukoc Biol 60: 365-371. (Pubitemid 26325618)
25. Yokota A, Takeuchi H, Maeda N, Ohoka Y, Kato C, et al. (2009) GM-CSF and IL-4 synergistically trigger dendritic cells to acquire retinoic acid-producing capacity. Int Immunol 21: 361-377.
26. Ortega-Cava CF, Ishihara S, Rumi MA, Kawashima K, Ishimura N, et al. (2003) Strategic compartmentalization of Toll-like receptor 4 in the mouse gut. J Immunol 170: 3977-3985. (Pubitemid 36428158)
27. Jersmann HP (2005) Time to abandon dogma: CD14 is expressed by non-myeloid lineage cells. Immunol Cell Biol 83: 462-467.
28. Pugin J, Schurer-Maly CC, Leturcq D, Moriarty A, Ulevitch RJ, et al. (1993) Lipopolysaccharide activation of human endothelial and epithelial cells is mediated by lipopolysaccharide-binding protein and soluble CD14. Proc Natl Acad Sci U S A 90: 2744-2748. (Pubitemid 23113493)
29. Rudraraju R, Surman S, Jones B, Sealy R, Woodland DL, et al. (2011) Phenotypes and functions of persistent Sendai virus-induced antibody forming cells and CD8+ T cells in diffuse nasal-associated lymphoid tissue typify lymphocyte responses of the gut. Virology 410: 429-436.
30. Tripathi S, Tecle T, Verma A, Crouch E, White M, et al. (2013) The human cathelicidin LL-37 inhibits influenza A viruses through a mechanism distinct from that of surfactant protein D or defensins. J Gen Virol 94: 40-49.
31. Doss M, White MR, Tecle T, Gantz D, Crouch EC, et al. (2009) Interactions of alpha-, beta-, and theta-defensins with influenza A virus and surfactant protein D. J Immunol 182: 7878-7887.
32. Proud D, Leigh R (2011) Epithelial cells and airway diseases. Immunol Rev 242: 186-204.
33. Wang Y, Devkota S, Musch MW, Jabri B, Nagler C, et al. (2010) Regional mucosa-associated microbiota determine physiological expression of TLR2 and TLR4 in murine colon. PLOS ONE 5: e13607.
34. Kanneganti TD. (2010) Central roles of NLRs and inflammasomes in viral infection. Nat Rev Immunol 10: 688-698.
35. Zaki MH, Boyd KL, Vogel P, Kastan MB, Lamkanfi M, et al. (2010) The NLRP3 inflammasome protects against loss of epithelial integrity and mortality during experimental colitis. Immunity 32: 379-391.
36. Willart MA, Deswarte K, Pouliot P, Braun H, Beyaert R, et al. (2012) Interleukin-1alpha controls allergic sensitization to inhaled house dust mite via the epithelial release of GM-CSF and IL-33. J Exp Med 209: 1505-1517.
37. Kumar H, Kawai T, Akira S (2011) Pathogen recognition by the innate immune system. Int Rev Immunol 30: 16-34.
38. Franchi L, Munoz-Planillo R, Nunez G (2012) Sensing and reacting to microbes through the inflammasomes. Nat Immunol 13: 325-332.
39. Hancock RE, Nijnik A, Philpott DJ (2012) Modulating immunity as a therapy for bacterial infections. Nat Rev Microbiol 10: 243-254.
40. Abreu MT (2010) Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol 10: 131-144.
41. Brandl K, Sun L, Neppl C, Siggs OM, Le Gall SM, et al. (2010) MyD88 signaling in nonhematopoietic cells protects mice against induced colitis by regulating specific EGF receptor ligands. Proc Natl Acad Sci U S A 107: 19967-19972.
42. Shaykhiev R, Behr J, Bals R (2008) Microbial patterns signaling via Toll-like receptors 2 and 5 contribute to epithelial repair, growth and survival. PLOS ONE 3: e1393.
43. Costa-Pereira AP, Tininini S, Strobl B, Alonzi T, Schlaak JF, et al. (2002) Mutational switch of an IL-6 response to an interferon-gamma-like response. Proc Natl Acad Sci U S A 99: 8043-8047. (Pubitemid 34651002)
44. Van Amersfoort ES, Van Berkel TJ, Kuiper J (2003) Receptors, mediators, and mechanisms involved in bacterial sepsis and septic shock. Clin Microbiol Rev 16: 379-414. (Pubitemid 36871313)
45. Patke CL, Shearer WT (2000) gp120- and TNF-alpha-induced modulation of human B cell function: proliferation, cyclic AMP generation, Ig production, and B-cell receptor expression. J Allergy Clin Immunol 105: 975-982. (Pubitemid 30324407)
46. Rumbo M, Anderle P, Didierlaurent A, Sierro F, Debard N, et al. (2004) How the gut links innate and adaptive immunity. Ann N Y Acad Sci 1029: 16-21. (Pubitemid 40298511)
47. Churchill L, Friedman B, Schleimer RP, Proud D (1992) Production of granulocyte-macrophage colony-stimulating factor by cultured human tracheal epithelial cells. Immunology 75: 189-195.
48. Cromwell O, Hamid Q, Corrigan CJ, Barkans J, Meng Q, et al. (1992) Expression and generation of interleukin-8, IL-6 and granulocyte-macrophage colony-stimulating factor by bronchial epithelial cells and enhancement by IL-1 beta and tumour necrosis factor-alpha. Immunology 77: 330-337.
49. Roy RM, Wuthrich M, Klein BS (2012) Chitin elicits CCL2 from airway epithelial cells and induces CCR2-dependent innate allergic inflammation in the lung. J Immunol 189: 2545-2552.
50. Suzuki Y, Suda T, Furuhashi K, Shibata K, Hashimoto D, et al. (2012) Mouse CD11bhigh lung dendritic cells have more potent capability to induce IgA than CD103+ lung dendritic cells in vitro. Am J Respir Cell Mol Biol 46: 773-780.
51. Iwata M, Eshima Y, Kagechika H (2003) Retinoic acids exert direct effects on T cells to suppress Th1 development and enhance Th2 development via retinoic acid receptors. Int Immunol 15: 1017-1025. (Pubitemid 36987299)
52. Cantorna MT, Nashold FE, Chun TY, Hayes CE (1996) Vitamin A down-regulation of IFN-gamma synthesis in cloned mouse Th1 lymphocytes depends on the CD28 costimulatory pathway. J Immunol 156: 2674-2679. (Pubitemid 126660610)
53. Panee J (2012) Monocyte Chemoattractant Protein 1 (MCP-1) in obesity and diabetes. Cytokine 60: 1-12.
54. Struyf S, Van CE, Paemen L, Put W, Lenaerts JP, et al. (1998) Synergistic induction of MCP-1 and -2 by IL-1beta and interferons in fibroblasts and epithelial cells. J Leukoc Biol 63: 364-372. (Pubitemid 28106851)
55. Loudon PT, Yager EJ, Lynch DT, Narendran A, Stagnar C, et al. (2010) GM-CSF increases mucosal and systemic immunogenicity of an H1N1 influenza DNA vaccine administered into the epidermis of non-human primates. PLOS One 5: e11021.
56. Eo SK, Lee S, Chun S, Rouse BT (2001) Modulation of immunity against herpes simplex virus infection via mucosal genetic transfer of plasmid DNA encoding chemokines. J Virol 75: 569-578. (Pubitemid 32037259)
57. Ramsay AJ, Husband AJ, Ramshaw IA, Bao S, Matthaei KI, et al. (1994) The role of interleukin-6 in mucosal IgA antibody responses in vivo. Science 264: 561-563. (Pubitemid 24185859)
58. Beagley KW, Eldridge JH, Lee F, Kiyono H, Everson MP, et al. (1989) Interleukins and IgA synthesis. Human and murine interleukin 6 induce high rate IgA secretion in IgA-committed B cells. J Exp Med 169: 2133-2148. (Pubitemid 19162972)
59. Buck J, Ritter G, Dannecker L, Katta V, Cohen SL, et al. (1990) Retinol is essential for growth of activated human B cells. J Exp Med 171: 1613-1624. (Pubitemid 20167554)
60. Amaral CT, Pontes NN, Maciel BL, Bezerra HS, Triesta AN, et al. (2013) Vitamin A deficiency alters airway resistance in children with acute upper respiratory infection. Pediatr Pulmonol 48: 481-489.
61. Lam HS, Chow CM, Poon WT, Lai CK, Chan KC, et al. (2006) Risk of vitamin A toxicity from candy-like chewable vitamin supplements for children. Pediatrics 118: 820-824. (Pubitemid 46085448)
62. Schuster GU, Kenyon NJ, Stephensen CB (2008) Vitamin A deficiency decreases and high dietary vitamin A increases disease severity in the mouse model of asthma. J Immunol 180: 1834-1842.
63. de Francisco A, Chakraborty J, Chowdhury HR, Yunus M, Baqui AH, et al. (1993) Acute toxicity of vitamin A given with vaccines in infancy. Lancet 342: 526-527. (Pubitemid 23259188)
64. Hathcock JN, Hattan DG, Jenkins MY, McDonald JT, Sundaresan PR, et al. (1990) Evaluation of vitamin A toxicity. Am J Clin Nutr 52: 183-202.