Environmental cues, dendritic cells and the programming of tissue-selective lymphocyte trafficking

Nature Immunology

Volumn 9, Issue 9, 2008, Pages 981-987

  Sigmundsdottir, Hekla ^a,b   Butcher, Eugene C ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA PALO ALTO HEALTH CARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLECALCIFEROL; CYTOKINE; DERMATOLOGICAL AGENT; IMMUNOGLOBULIN A; RETINOIC ACID RECEPTOR AGONIST; RETINOL; VITAMIN D RECEPTOR AGONIST;

ANTIGEN ANTIBODY REACTION; ANTIGENICITY; AUTOIMMUNE DISEASE; B LYMPHOCYTE; CELL INTERACTION; CELL PROLIFERATION; CELLULAR IMMUNITY; CYTOKINE RELEASE; CYTOLOGY; DENDRITIC CELL; DIETARY INTAKE; DRUG EFFICACY; EFFECTOR CELL; ENVIRONMENTAL FACTOR; HELPER CELL; HUMAN; IMMUNOREACTIVITY; IMMUNOREGULATION; IMMUNOSTIMULATION; INFLAMMATION; INTESTINE CELL; LYMPHATIC DRAINAGE; LYMPHOCYTE FUNCTION; LYMPHOCYTE HOMING; LYMPHOCYTE MIGRATION; MEMORY T LYMPHOCYTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PSORIASIS; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE; REVIEW; SIGNAL TRANSDUCTION; SKIN CELL; SKIN INFLAMMATION; SUN EXPOSURE; T LYMPHOCYTE; ULTRAVIOLET B RADIATION; UPREGULATION; VITAMIN D METABOLISM;

ANIMALS; CELL ADHESION MOLECULES; CELL MOVEMENT; DENDRITIC CELLS; HUMANS; IMMUNOLOGIC MEMORY; LYMPH NODES; RECEPTORS, LYMPHOCYTE HOMING; T-LYMPHOCYTE SUBSETS;

EID: 50049106591     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.f.208     Document Type: Review

References (70)

1. Luster, A.D., Alon, R. & von Andrian, U.H. Immune cell migration in inflammation: Present and future therapeutic targets. Nat. Immunol. 6, 1182-1190 (2005).
2. Johansson-Lindbom, B. & Agace, W.W. Generation of gut-homing T-cells and their localization to the small intestinal mucosa. Immunol. Rev. 215, 226-242 (2007).
3. Schon, M.P., Zollner, T.M. & Boehncke, W.H. The molecular basis of lymphocyte recruitment to the skin: Clues for pathogenesis and selective therapies of inflammatory disorders. J. Invest Dermatol. 121 951-962 (2003).
4. Butcher, E.C. The multistep model of leukocyte trafficking: A personal perspective from 15 years later. in Leukocyte Trafficking: Molecular Mechanisms, Therapeutic Targets, and Methods (eds. Hamann, A. & Engelhardt, B.) 3-13 (Wiley-VCH, Weinheim, Germany, 2005).
5. Butcher, E.C. & Picker, L.J. Lymphocyte homing and homeostasis. Science 272, 60-66 (1996).
6. Stolen, C.M. et al. Absence of the endothelial oxidase AOC3 leads to abnormal leukocyte traffic in vivo. Immunity 22, 105-115 (2005).
7. Honjo, M. et al. Lectin-like oxidized LDL receptor-1 is a cell-adhesion molecule involved in endotoxin-induced inflammation. Proc. Natl. Acad. Sci. USA 100, 1274-1279 (2003).
8. Jalkanen, S. et al. Lymphocyte migration into the skin: The role of lymphocyte homing receptor (CD44) and endothelial cell antigen (HECA-452). J. Invest. Dermatol. 94, 786-792 (1990).
9. Salmi, M., Tohka, S., Berg, E.L., Butcher, E.C. & Jalkanen, S. Vascular adhesion protein 1 (VAP-1) mediates lymphocyte subtype-specific, selectin-independent recognition of vascular endothelium in human lymph nodes. J. Exp. Med. 186, 589-600 (1997).
10. Mora, J.R. Homing imprinting and immunomodulation in the gut: Role of dendritic cells and retinoids. Inflamm. Bowel Dis. 14, 275-289 (2008).
11. Salmi, M. & Jalkanen, S. Lymphocyte homing to the gut: Attraction, adhesion, and commitment. Immunol. Rev. 206, 100-113 (2005).
12. Kupper, T.S. & Fuhlbrigge, R.C. Immune surveillance in the skin: mechanisms and clinical consequences. Nat. Rev. Immunol. 4, 211-222 (2004).
13. Arvilommi, A.M., Salmi, M., Kalimo, K. & Jalkanen, S. Lymphocyte binding to vascular endothelium in inflamed skin revisited: A central role for vascular adhesion protein-1 (VAP-1). Eur. J. Immunol. 26, 825-833 (1996).
14. Schaerli, P. et al. A Skin-selective homing mechanism for human immune surveillance T cells. J. Exp. Med. 199, 1265-1275 (2004).
15. Gunther, C. et al. CCL18 is expressed in atopic dermatitis and mediatet skin homing of human memory T cells. J. Immunol. 174 1723-1728 (2005).
16. Wardlaw, A.J., Guillen, C. & Morgan, A. Mechanisms of T cell migration to the lung. Clin. Exp. Allergy 35, 4-7 (2005).
17. Engelhardt, B. & Ransohoff, R.M. The ins and outs of T-lymphocyte trafficking to the CNS: Anatomical sites and molecular mechanisms. Trends Immunol. 26, 485-495 (2005).
18. Kunkel, E.J. & Butcher, E.C. Plasma-cell homing. Nat. Rev. Immunol. 3, 822-829 (2003).
19. Hieshima, K. et al. CC chemokine ligands 25 and 28 play essential roles in intestinal extravasation of IgA antibody-secreting cells. J. Immunol. 173, 3668-3675 (2004).
20. Wilson, E. & Butcher, E.C. CCL28 controls immunoglobulin (Ig)A plasma cell accumulation in the lactating mammary gland and IgA antibody transfer to the neonate. J. Exp. Med. 200, 805-809 (2004).
21. Butcher, E.C. The regulation of lymphocyte traffic. Curr. Top. Microbiol. Immunol. 128, 85-122 (1986).
22. Young, A.J., Hay, J.B. & Mackay, C.R. Lymphocyte recirculation and life span in vivo. Curr. Top. Microbiol. Immunol. 184, 161-173 (1993).
23. Campbell, D.J. & Butcher, E.C. Rapid acquisition of tissue-specific homing phenotypes by CD4+ T cells activated in cutaneous or mucosal lymphoid tissues. J. Exp. Med. 195, 135-141 (2002).
24. Iwata, M. et al. Retinoic acid imprints gut-homing specificity on T cells. Immunity 21, 527-538 (2004).
25. Sigmundsdottir, H. et al. DCs metabolize sunlight-induced vitamin D3 to 'program' T cell attraction to the epidermal chemokine CCL27. Nat. Immunol. 8, 285-293 (2007).
26. Napoli, J.L. Retinoic acid biosynthesis and metabolism. FASEB J. 10, 993-1001 (1996).
27. Moore, T. Vitamin A and carotene. VI. The conversion of carotene to vitamin A in vivo. Biochem. J. 24, 692-702 (1930).
28. Svensson, M. et al. Retinoic acid receptor signaling levels and antigen dose regulate gut homing receptor expression on CD8+ T cells. Mucosal Immunol. 1, 38-48 (2008).
29. Johansson-Lindbom, B. et al. Functional specialization of gut CD103+ dendritic cells in the regulation of tissue-selective T cell homing. J. Exp. Med. 202, 1063-1073 (2005).
30. Szatmari, I. et al. PPARγy controls CD1d expression by turning on retinoic acid synthesis in developing human dendritic cells. J. Exp. Med. 203, 2351-2362 (2006).
31. Saurer, L., McCullough, K.C. & Summerfield, A. In vitro induction of mucosa-type dendritic cells by all-trans retinoic acid. J. Immunol. 179, 3504-3514 (2007).
32. Stenstad, H. et al. Gut-associated lymphoid tissue-primed CD4+ T cells display CCR9-dependent and -independent homing to the small intestine. Blood 107, 3447-3454 (2006).
33. Meurens, F. et al. Commensal bacteria and expression of two major intestinal chemokines, TECK/CCL25 and MEC/CCL28, and their receptors. PLOS ONE 2, e677(2007).
34. Enioutina, E.Y., Bareyan, D. & Daynes, R.A. TLR ligands that stimulate the metabolism of vitamin D3 in activated murine dendritic cells can function as effective mucosal adjuvants to subcutaneously administered vaccines. Vaccine 26, 601-613 (2008).
35. Webb, A.R. & Holick, M.F. The role of sunlight in the cutaneous production of vitamin D3. Annu. Rev. Nutr. 8, 375-399 (1988).
36. Holick, M.F. et al. Photosynthesis of previtamin D3 in human skin and the physiologic consequences. Science 210, 203-205 (1980).
37. Prosser, D.E. & Jones, G. Enzymes involved in the activation and inactivation of vitamin D. Trends Biochem. Sci. 29, 664-673 (2004).
38. Lehmann, B., Rudolph, T., Pietzsch, J. & Meurer, M. Conversion of vitamin D3 to 1,25-dihydroxyvitamin D3 in human skin equivalents. Exp. Dermatol. 9, 97-103 (2000).
39. Liu, P.T. et al. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311, 1770-1773 (2006).
40. Reiss, Y., Proudfoot, A.E., Power, C.A., Campbell, J.J. & Butcher, E.C. CC chemokine receptor (CCR)4 and the CCR10 ligand cutaneous T cell-attracting chemokine (CTACK) in lymphocyte trafficking to inflamed skin. J. Exp. Med. 194, 1541-1647 (2001).
41. Campbell, J.J. et al. The chemokine receptor CCR4 in vascular recognition by cutaneous but not intestinal memory T cells. Nature 400, 776-780 (1999).
42. Homey, B. et al. Cutting edge: The orphan chemokine receptor G protein-coupled receptor-2 (GPR-2, CCR10) binds the skin-associated chemokine CCL27 (CTACK/ALP/ILC). J. Immunol. 164, 3465-3470 (2000).
43. Lazarus, N.H. et al. A common mucosal chemokine (mucosae-associated epithelial chemokine/CCL28) selectively attracts IgA plasmablasts. J. Immunol. 170, 3799-3805 (2003).
44. Shirakawa, A.-K. et al. 1,25-Dihydroxyvitamin D3 induces CCR10 expression in terminally differentiating human B cells. J. Immunol. 180, 2786-2795 (2008).
45. Eksteen, B. et al. Epithelial inflammation is associated with CCL28 production and the recruitment of regulatory T cells expressing CCR10. J. Immunol. 177, 593-603 (2006).
46. Mangelsdorf, D.J. & Evans, R.M. The RXR heterodimers and orphan receptors. Cell 83, 841-850 (1995).
47. Mora, J.R. et al. Reciprocal and dynamic control of CD8 T cell homing by dendritic cells from skin- and gut-associated lymphoid tissues. J. Exp. Med. 201, 303-316 (2005).
48. Dudda, J.C. et al. Dendritic cells govern induction and reprogramming of polarized tissue-selective homing receptor patterns of T cells: Important roles for soluble factors and tissue microenvironments. Eur. J. Immunol. 35, 1056-1065 (2005).
49. Boonstra, A. et al. 1α,25-Dihydroxyvitamin D3 has a direct effect on naive CD4+ T cells to enhance the development of Th2 cells. J. Immunol. 167, 4974-4980 (2001).
50. Iwata, M., Eshima, Y. & Kagechika, H. 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 (2003).
51. Adorini, L. Tolerogenic dendritic cells induced by vitamin D receptor ligands enhance regulatory T cells inhibiting autoimmune diabetes. Ann. NY Acad. Sci. 987, 258-261 (2003).
52. Coombes, J.L. et al. 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 (2007).
53. Kang, S.G. et al. Metabolites induce gut-homing FoxP3+ regulatory T cells. J. Immunol. 179, 3724-3733 (2007).
54. 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. 204, 1765-1774 (2007).
55. Sun, C.-M. et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204, 1775-1785 (2007).
56. Mucida, D. et al. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 317, 256-260 (2007).
57. Gregori, S. et al. Regulatory T cells induced by 1α,25-dihydroxyvitamin D3 and mycophenolate mofetil treatment mediate transplantation tolerance. J. Immunol. 167, 1945-1953 (2001).
58. Prystowsky, J.H., Muzio, P.J., Sevran, S. & Clemens, T.L. Effect of UVB phototherapy and oral calcitriol (1,25-dihydroxyvitamin D3) on vitamin D photosynthesis in patients with psoriasis. J. Am. Acad. Dermatol. 35, 690-695 (1996).
59. Zhu, Y., Mahon, B.D., Froicu, M. & Cantorna, M.T. Calcium and 1α,25-dihydroxyvitamin D3 target the TNF-α pathway to suppress experimental inflammatory bowel disease. Eur. J. Immunol. 35 217-224 (2005).
60. Penna, G., Amuchastegui, S., Laverny, G. & Adorini, L. Vitamin D receptor agonists in the treatment of autoimmune diseases: Selective targeting of myeloid but not plasmacytoid dendritic cells. J. Bone Miner. Res. 22, V69-V73 (2007).
61. Kunkel, E.J. et al. CCR10 expression is a common feature of circulating and mucosal epithelial tissue IgA Ab-secreting cells. J. Clin. Invest. 111, 1001-1010 (2003).
62. Jaimes, M.C. et al. Maturation and trafficking markers on rotavirus-specific B cells during acute infection and convalescence in children. J. Virol. 78, 10967-10976 (2004).
63. Mora, J.R. et al. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 314, 1157-1160 (2006).
64. Kim, C.H. et al. Rules of chemokine receptor association with T cell polarization in vivo. J. Clin. Invest. 108, 1331-1339 (2001).
65. Wagers, A.J., Waters, C.M., Stoolman, L.M. & Kansas, G.S. Interleukin 12 and interleukin 4 control T cell adhesion to endothelial selectins through opposite effects on α1,3-fucosyltransferase VII gene expression. J. Exp. Med. 188, 2225-2231 (1998).
66. Picker, L.J. et al. Control of lymphocyte recirculation in man. II. Differential regulation of the cutaneous lymphocyte-associated antigen, a tissue-selective homing receptor for skin-homing T cells. J. Immunol. 150, 1122-1136 (1993).
67. Kim, C.H., Nagata, K. & Butcher, E.C. Dendritic cells support sequential reprogramming of chemoattractant receptor profiles during naive to effector T cell differentiation. J. Immunol. 171, 152-158 (2003).
68. Campbell, D.J., Kim, C.H. & Butcher, E.C. Separable effector T cell populations specialized for B cell help or tissue inflammation. Nat. Immunol. 2, 876-881 (2001).
69. Huehn, J. & Hamann, A. Homing to suppress: Address codes for Treg migration. Trends Immunol. 26, 632-636 (2005).
70. Sather, B.D. et al. Altering the distribution of Foxp3+ regulatory T cells results in tissue-specific inflammatory disease. J. Exp. Med. 204, 1335-1347 (2007).