An indispensable role for the chemokine receptor CCR10 in IgA antibody-secreting cell accumulation

Journal of Immunology

Volumn 181, Issue 9, 2008, Pages 6309-6315

  Morteau, Olivier ^a,d   Gerard, Craig ^a   Lu, Bao ^a   Ghiran, Sorina ^a   Rits, Miriam ^a   Fujiwara, Yuko ^a   Law, Yuetching ^b   Distelhorst, Kathryn ^b   Nielsen, Elizabeth M ^b   Hill, Erica D ^b   Kwan, Raymond ^c   Lazarus, Nicole H ^c   Butcher, Eugene C ^c   Wilson, Eric ^b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b BRIGHAM YOUNG UNIVERSITY   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Medigene UK Limited   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR10; IMMUNOGLOBULIN A; CCR10 PROTEIN, MOUSE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; CELL SECRETION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; GASTROINTESTINAL TRACT; IN VIVO STUDY; LACTATION; LYMPHOCYTE HOMING; MAMMARY GLAND; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; ANTIBODY PRODUCING CELL; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; CELL LINE; CYTOLOGY; GENETICS; IMMUNOLOGY; LARGE INTESTINE; LYMPHOCYTE COUNT; METABOLISM; MOUSE MUTANT; NEUTROPHIL CHEMOTAXIS; PHYSIOLOGY; SECRETION; SMALL INTESTINE; UDDER;

ANIMALS; ANTIBODY-PRODUCING CELLS; CELL LINE; CHEMOTAXIS, LEUKOCYTE; IMMUNOGLOBULIN A; INTESTINE, LARGE; INTESTINE, SMALL; LACTATION; LYMPHOCYTE COUNT; MAMMARY GLANDS, ANIMAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, CCR10;

EID: 58749117434     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.9.6309     Document Type: Article

References (45)

1. Burns, J. W., M. Siadat-Pajouh, A. A. Krishnaney, and H. B. Greenberg. 1996. Protective effect of rotavirus VP6-specific IgA monoclonal antibodies that lack neutralizing activity. Science 272: 104-107.
2. Williams, R. C., and R. J. Gibbons. 1972. Inhibition of bacterial adherence by secretory immunoglobulin A: a mechanism of antigen disposal. Science 177: 697-699.
3. Russell, M. W., M. Kilian, and M. E. Lamm. 1999. Biological activities of IgA. In Mucosal Immunology, 2nd Ed. P. L. Ogra, J. Mestecky, M. E. Lamm, W. Strober, J. Bienenstock, and J. R. McGhee, eds. Academic Press, San Diego, pp. 225-240.
4. Hanson, L. A., and E. Telemo. 1999. Immunobiology and epidemiology of breastfeeding in relation to prevention of infections from a global perspective. In Mucosal Immunology, 2nd Ed. P. L. Ogra, J. Mestecky, M. E. Lamm, W. Strober, J. Bienenstock, and J. R. McGhee, eds. Academic Press, San Diego, pp. 1501-1510.
5. Roux, M. E., M. McWilliams, J. M. Phillips-Quagliata, P. Weisz-Carrington, and M. E. Lamm. 1977. Origin of IgA-secreting plasma cells in the mammary gland. J. Exp. Med. 146: 1311-1322.
6. Tanneau, G. M., L. Hibrand-Saint Oyant, C. C. Chevaleyre, and H. P. Salmon. 1999. Differential recruitment of T- and IgA B-lymphocytes in the developing mammary gland in relation to homing receptors and vascular addressins. J. Histochem. Cytochem. 47: 1581-1592.
7. Wilson, E., and E. C. Butcher. 2004. 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. (Pubitemid 39299466)
8. Goldblum, R. M., S. Ahlstedt, B. Carlsson, L. A. Hanson, U. Jodal, G. Lidin-Janson, and A. Sohl-Akerlund. 1975. Antibody-forming cells in human colostrum after oral immunization. Nature 257: 797-798.
9. Reiss, Y., A. E. Proudfoot, C. A. Power, J. J. Campbell, and E. C. Butcher. 2001. 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: 1541-1547. (Pubitemid 33081528)
10. Chen, L., S. X. Lin, R. Agha-Majzoub, L. Overbergh, C. Mathieu, and L. S. Chan. 2006. CCL27 is a critical factor for the development of atopic dermatitis in the keratin-14 IL-4 transgenic mouse model. Int. Immunol. 18: 1233-1242. (Pubitemid 44349298)
11. + plasmablast recruitment to the intestinal lamina propria after rotavirus infection. J. Immunol. 176: 5749-5759.
12. Homey, B., H. Alenius, A. Muller, H. Soto, E. P. Bowman, W. Yuan, L. McEvoy, A. I. Lauerma, T. Assmann, E. Bunemann, et al. 2002. CCL27-CCR10 interactions regulate T cell-mediated skin inflammation. Nat. Med. 8: 157-165. (Pubitemid 34155127)
13. Hieshima, K., Y. Kawasaki, H. Hanamoto, T. Nakayama, D. Nagakubo, A. Kanamaru, and O. Yoshie. 2004. CC chemokine ligands 25 and 28 play essential roles in intestinal extravasation of IgA antibody-secreting cells. J. Immunol. 173: 3668-3675. (Pubitemid 39280727)
14. Pan, J., E. J. Kunkel, U. Gosslar, N. Lazarus, P. Langdon, K. Broadwell, M. A. Vierra, M. C. Genovese, E. C. Butcher, and D. Soler. 2000. A novel chemokine ligand for CCR10 and CCR3 expressed by epithelial cells in mucosal tissues. J. Immunol. 165: 2943-2949. (Pubitemid 30728140)
15. Hanamoto, H., T. Nakayama, H. Miyazato, S. Takegawa, K. Hieshima, Y. Tatsumi, A. Kanamaru, and O. Yoshie. 2004. Expression of CCL28 by Reed-Sternberg cells defines a major subtype of classical Hodgkin's disease with frequent infiltration of eosinophils and/or plasma cells. Am. J. Pathol. 164: 997-1006. (Pubitemid 38235481)
16. McDermott, M. R., and J. Bienenstock. 1979. Evidence for a common mucosal immunologic system. I. Migration of B immunoblasts into intestinal, respiratory, and genital tissues. J. Immunol. 122: 1892-1898.
17. Lazarus, N. H., E. J. Kunkel, B. Johnston, E. Wilson, K. R. Youngman, and E. C. Butcher. 2003. A common mucosal chemokine (mucosae-associated epithelial chemokine/CCL28) selectively attracts IgA plasmablasts. J. Immunol. 170: 3799-3805.
18. Jarmin, D. I., M. Rits, D. Bota, N. P. Gerard, G. J. Graham, I. Clark-Lewis, and C. Gerard. 2000. Cutting edge: identification of the orphan receptor G-protein-coupled receptor 2 as CCR10, a specific receptor for the chemokine ESkine. J. Immunol. 164: 3460-3464. (Pubitemid 30169793)
19. Bhat, M. A., J. C. Rios, Y. Lu, G. P. Garcia-Fresco, W. Ching, M. St. Martin, J. Li, S. Einheber, M. Chesler, J. Rosenbluth, et al. 2001. Axon-Glia interactions and the domain organization of myelinated axons requires neurexin IV/Caspr/Paranodin. Neuron 30: 369-383.
20. Wang, W., H. Soto, E. R. Oldham, M. E. Buchanan, B. Homey, D. Catron, N. Jenkins, N. G. Copeland, D. J. Gilbert, N. Nguyen, et al. 2000. Identification of a novel chemokine (CCL28), which binds CCR10 (GPR2). J. Biol. Chem. 275: 22313-22323. (Pubitemid 30621816)
21. Bowman, E. P., N. A. Kuklin, K. R. Youngman, N. H. Lazarus, E. J. Kunkel, J. Pan, H. B. Greenberg, and E. C. Butcher. 2002. The intestinal chemokine thymus-expressed chemokine (CCL25) attracts IgA antibody-secreting cells. J. Exp. Med. 195: 269-275.
22. Kunkel, E. J., J. J. Campbell, G. Haraldsen, J. Pan, J. Boisvert, A. I. Roberts, E. C. Ebert, M. A. Vierra, S. B. Goodman, M. C. Genovese, et al. 2000. Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: epithelial expression of tissue-specific chemokines as an organizing principle in regional immunity. J. Exp. Med. 192: 761-768.
23. Pabst, O., L. Ohl, M. Wendland, M. A. Wurbel, E. Kremmer, B. Malissen, and R. Forster. 2004. Chemokine receptor CCR9 contributes to the localization of plasma cells to the small intestine. J. Exp. Med. 199: 411-416. (Pubitemid 38252052)
24. Butcher, E. C., and L. J. Picker. 1996. Lymphocyte homing and homeostasis. Science 272: 60-66.
25. Shamri, R., V. Grabovsky, J. M. Gauguet, S. Feigelson, E. Manevich, W. Kolanus, M. K. Robinson, D. E. Staunton, U. H. von Andrian, and R. Alon. 2005. Lymphocyte arrest requires instantaneous induction of an extended LFA-1 conformation mediated by endothelium-bound chemokines. Nat. Immunol. 6: 497-506. (Pubitemid 41716763)
26. 4 integrin clustering by immobilized chemokines stimulates leukocyte tethering and rolling on endothelial vascular cell adhesion molecule 1 under flow conditions. J. Exp. Med. 192: 495-506.
27. Wilson, E., J. F. Hedges, E. C. Butcher, M. Briskin, and M. A. Jutila. 2002. Bovine γδ T cell subsets express distinct patterns of chemokine responsiveness and adhesion molecules: a mechanism for tissue-specific γδ T cell subset accumulation. J. Immunol. 169: 4970-4975. (Pubitemid 35217163)
28. Yopp, A. C., J. C. Ochando, M. Mao, L. Ledgerwood, Y. Ding, and J. S. Bromberg. 2005. Sphingosine 1-phosphate receptors regulate chemokine-driven transendothelial migration of lymph node but not splenic T cells. J. Immunol. 175: 2913-2924.
29. Johnston, B., A. R. Burns, M. Suematsu, T. B. Issekutz, R. C. Woodman, and P. Kubes. 1999. Chronic inflammation up-regulates chemokine receptors and induces neutrophil migration to monocyte chemoattractant protein-1. J. Clin. Invest. 103: 1269-1276. (Pubitemid 29218297)
30. Huber, A. R., S. L. Kunkel, R. F. Todd III, and S. J. Weiss. 1991. Regulation of transendothelial neutrophil migration by endogenous interleukin-8. Science 254: 99-102.
31. Okada, T., and J. G. Cyster. 2007. CC chemokine receptor 7 contributes to Gi-dependent T cell motility in the lymph node. J. Immunol. 178: 2973-2978. (Pubitemid 46333176)
32. Asperti-Boursin, F., E. Real, G. Bismuth, A. Trautmann, and E. Donnadieu. 2007. CCR7 ligands control basal T cell motility within lymph node slices in a phosphoinositide 3-kinase-independent manner. J. Exp. Med. 204: 1167-1179. (Pubitemid 46798159)
33. Ma, Q., D. Jones, and T. A. Springer. 1999. The chemokine receptor CXCR4 is required for the retention of B lineage and granulocytic precursors within the bone marrow microenvironment. Immunity 10: 463-471.
34. 7-mediated adhesion of lymphocytes to mucosal addressin cell adhesion molecule-1 (MAdCAM-1) under flow. J. Immunol. 161: 952-956.
35. Cyster, J. G. 1999. Chemokines and cell migration in secondary lymphoid organs. Science 286: 2098-2102. (Pubitemid 129516279)
36. Eksteen, B., A. Miles, S. M. Curbishley, C. Tselepis, A. J. Grant, L. S. Walker, and D. H. Adams. 2006. Epithelial inflammation is associated with CCL28 production and the recruitment of regulatory T cells expressing CCR10. J. Immunol. 177: 593-603. (Pubitemid 43939173)
37. Inokuma, D., R. Abe, Y. Fujita, M. Sasaki, A. Shibaki, H. Nakamura, J. R. McMillan, T. Shimizu, and H. Shimizu. 2006. CTACK/CCL27 accelerates skin regeneration via accumulation of bone marrow-derived keratinocytes. Stem Cells 24: 2810-2816. (Pubitemid 46053018)
38. Soler, D., T. L. Humphreys, S. M. Spinola, and J. J. Campbell. 2003. CCR4 versus CCR10 in human cutaneous TH lymphocyte trafficking. Blood 101: 1677-1682. (Pubitemid 36237558)
39. + T cell dependent. Infect. Immun. 59: 3630-3638.
40. Macpherson, A. J., D. Gatto, E. Sainsbury, G. R. Harriman, H. Hengartner, and R. M. Zinkernagel. 2000. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 288: 2222-2226.
41. Yamamoto, M., P. Rennert, J. R. McGhee, M. N. Kweon, S. Yamamoto, T. Dohi, S. Otake, H. Bluethmann, K. Fujihashi, and H. Kiyono. 2000. Alternate mucosal immune system: organized Peyer's patches are not required for IgA responses in the gastrointestinal tract. J. Immunol. 164: 5184-5191. (Pubitemid 30305194)
42. Bergqvist, P., E. Gardby, A. Stensson, M. Bemark, and N. Y. Lycke. 2006. Gut IgA class switch recombination in the absence of CD40 does not occur in the lamina propria and is independent of germinal centers. J. Immunol. 177: 7772-7783. (Pubitemid 44846293)
43. Bienenstock, J., M. McDermott, D. Befus, and M. O'Neill. 1978. A common mucosal immunologic system involving the bronchus, breast and bowel. Adv. Exp. Med. Biol. 107: 53-59.
44. Kunkel, E. J., and E. C. Butcher. 2003. Plasma-cell homing. Nat. Rev. Immunol. 3: 822-829.
45. Brandtzaeg, P., E. S. Baekkevold, I. N. Farstad, F. L. Jahnsen, F. E. Johansen, E. M. Nilsen, and T. Yamanaka. 1999. Regional specialization in the mucosal immune system: what happens in the microcompartments? Immunol. Today 20: 141-151. (Pubitemid 29130344)