The Short Isoform of the CEACAM1 Receptor in Intestinal T Cells Regulates Mucosal Immunity and Homeostasis via Tfh Cell Induction

Immunity

Volumn 37, Issue 5, 2012, Pages 930-946

  Chen, Lanfen ^a   Chen, Zhangguo ^a   Baker, Kristi ^a   Halvorsen, Elizabeth M ^b   Pires da Cunha, Andre ^b   Flak, Magdalena B ^a   Gerber, Georg ^a   Huang, Yu Hwa ^a   Hosomi, Shuhei ^a   Arthur, Janelle C ^c   Dery, Ken J ^d   Nagaishi, Takashi ^e   Beauchemin, Nicole ^f   Holmes, Kathryn V ^g   Ho, Joshua W K ^a   Shively, John E ^d   Jobin, Christian ^c   Onderdonk, Andrew B ^a   Bry, Lynn ^a   Weiner, Howard L ^b   Higgins, Darren E ^b   Blumberg, Richard S ^a   more..

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^e TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^f MCGILL UNIVERSITY   (Canada)

^g UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 1; IMMUNOGLOBULIN A; ISOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HELPER CELL; HOMEOSTASIS; INTESTINE; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE;

AMINO ACID MOTIFS; ANIMALS; CARCINOEMBRYONIC ANTIGEN; CYTOPLASM; HOMEOSTASIS; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; INTESTINES; LISTERIA MONOCYTOGENES; LISTERIOSIS; LYMPHOCYTE ACTIVATION; METAGENOME; MICE; MICE, INBRED C57BL; NFATC TRANSCRIPTION FACTORS; PROTEIN ISOFORMS; RECEPTORS, IMMUNOLOGIC; T-LYMPHOCYTES; TYROSINE;

EID: 84869187290     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2012.07.016     Document Type: Article

References (66)

1. Abou-Rjaily G.A., Lee S.J., May D., Al-Share Q.Y., Deangelis A.M., Ruch R.J., Neumaier M., Kalthoff H., Lin S.H., Najjar S.M. CEACAM1 modulates epidermal growth factor receptor-mediated cell proliferation. J. Clin. Invest. 2004, 114:944-952.
2. Azuz-Lieberman N., Markel G., Mizrahi S., Gazit R., Hanna J., Achdout H., Gruda R., Katz G., Arnon T.I., Battat S., et al. The involvement of NK cells in ankylosing spondylitis. Int. Immunol. 2005, 17:837-845.
3. Barreau F., Meinzer U., Chareyre F., Berrebi D., Niwa-Kawakita M., Dussaillant M., Foligne B., Ollendorff V., Heyman M., Bonacorsi S., et al. CARD15/NOD2 is required for Peyer's patches homeostasis in mice. PLoS ONE 2007, 2:e523.
4. Baumgart M., Dogan B., Rishniw M., Weitzman G., Bosworth B., Yantiss R., Orsi R.H., Wiedmann M., McDonough P., Kim S.G., et al. Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn's disease involving the ileum. ISME J. 2007, 1:403-418.
5. Bjørneklett A., Fausa O., Midtvedt T. Bacterial overgrowth in jejunal and ileal disease. Scand. J. Gastroenterol. 1983, 18:289-298.
6. Boirivant M., Amendola A., Butera A., Sanchez M., Xu L., Marinaro M., Kitani A., Di Giacinto C., Strober W., Fuss I.J. A transient breach in the epithelial barrier leads to regulatory T-cell generation and resistance to experimental colitis. Gastroenterology 2008, 135:1612-1623.
7. Borsutzky S., Cazac B.B., Roes J., Guzmán C.A. TGF-beta receptor signaling is critical for mucosal IgA responses. J. Immunol. 2004, 173:3305-3309.
8. Boullier S., Tanguy M., Kadaoui K.A., Caubet C., Sansonetti P., Corthésy B., Phalipon A. Secretory IgA-mediated neutralization of Shigella flexneri prevents intestinal tissue destruction by down-regulating inflammatory circuits. J. Immunol. 2009, 183:5879-5885.
9. Boulton I.C., Gray-Owen S.D. Neisserial binding to CEACAM1 arrests the activation and proliferation of CD4+ T lymphocytes. Nat. Immunol. 2002, 3:229-236.
10. Cazac B.B., Roes J. TGF-beta receptor controls B cell responsiveness and induction of IgA in vivo. Immunity 2000, 13:443-451.
11. Cerutti A. The regulation of IgA class switching. Nat. Rev. Immunol. 2008, 8:421-434.
12. Chen C.J., Shively J.E. The cell-cell adhesion molecule carcinoembryonic antigen-related cellular adhesion molecule 1 inhibits IL-2 production and proliferation in human T cells by association with Src homology protein-1 and down-regulates IL-2 receptor. J. Immunol. 2004, 172:3544-3552.
13. Chen T., Zimmermann W., Parker J., Chen I., Maeda A., Bolland S. Biliary glycoprotein (BGPa, CD66a, CEACAM1) mediates inhibitory signals. J. Leukoc. Biol. 2001, 70:335-340.
14. Chen D., Iijima H., Nagaishi T., Nakajima A., Russell S., Raychowdhury R., Morales V., Rudd C.E., Utku N., Blumberg R.S. Carcinoembryonic antigen-related cellular adhesion molecule 1 isoforms alternatively inhibit and costimulate human T cell function. J. Immunol. 2004, 172:3535-3543.
15. Chen Z., Chen L., Qiao S.W., Nagaishi T., Blumberg R.S. Carcinoembryonic antigen-related cell adhesion molecule 1 inhibits proximal TCR signaling by targeting ZAP-70. J. Immunol. 2008, 180:6085-6093.
16. Cong Y., Wang L., Konrad A., Schoeb T., Elson C.O. Curcumin induces the tolerogenic dendritic cell that promotes differentiation of intestine-protective regulatory T cells. Eur. J. Immunol. 2009, 39:3134-3146.
17. Coutelier J.P., Godfraind C., Dveksler G.S., Wysocka M., Cardellichio C.B., Noël H., Holmes K.V. B lymphocyte and macrophage expression of carcinoembryonic antigen-related adhesion molecules that serve as receptors for murine coronavirus. Eur. J. Immunol. 1994, 24:1383-1390.
18. Dery K.J., Gaur S., Gencheva M., Yen Y., Shively J.E., Gaur R.K. Mechanistic control of carcinoembryonic antigen-related cell adhesion molecule-1 (CEACAM1) splice isoforms by the heterogeneous nuclear ribonuclear proteins hnRNP L, hnRNP A1, and hnRNP M. J. Biol. Chem. 2011, 286:16039-16051.
19. Donda A., Mori L., Shamshiev A., Carena I., Mottet C., Heim M.H., Beglinger C., Grunert F., Rochlitz C., Terracciano L., et al. Locally inducible CD66a (CEACAM1) as an amplifier of the human intestinal T cell response. Eur. J. Immunol. 2000, 30:2593-2603.
20. Dveksler G.S., Pensiero M.N., Dieffenbach C.W., Cardellichio C.B., Basile A.A., Elia P.E., Holmes K.V. Mouse hepatitis virus strain A59 and blocking antireceptor monoclonal antibody bind to the N-terminal domain of cellular receptor. Proc. Natl. Acad. Sci. USA 1993, 90:1716-1720.
21. Edlund M., Blikstad I., Obrink B. Calmodulin binds to specific sequences in the cytoplasmic domain of C-CAM and down-regulates C-CAM self-association. J. Biol. Chem. 1996, 271:1393-1399.
22. Fagarasan S. Evolution, development, mechanism and function of IgA in the gut. Curr. Opin. Immunol. 2008, 20:170-177.
23. Fagarasan S., Kinoshita K., Muramatsu M., Ikuta K., Honjo T. In situ class switching and differentiation to IgA-producing cells in the gut lamina propria. Nature 2001, 413:639-643.
24. Fantini M.C., Dominitzki S., Rizzo A., Neurath M.F., Becker C. In vitro generation of CD4+ CD25+ regulatory cells from murine naive T cells. Nat. Protoc. 2007, 2:1789-1794.
25. Fazilleau N., Mark L., McHeyzer-Williams L.J., McHeyzer-Williams M.G. Follicular helper T cells: lineage and location. Immunity 2009, 30:324-335.
26. Gencheva M., Chen C.J., Nguyen T., Shively J.E. Regulation of CEACAM1 transcription in human breast epithelial cells. BMC Mol. Biol. 2010, 11:79.
27. Gibbons D.L., Spencer J. Mouse and human intestinal immunity: same ballpark, different players; different rules, same score. Mucosal Immunol. 2011, 4:148-157.
28. Good-Jacobson K.L., Szumilas C.G., Chen L., Sharpe A.H., Tomayko M.M., Shlomchik M.J. PD-1 regulates germinal center B cell survival and the formation and affinity of long-lived plasma cells. Nat. Immunol. 2010, 11:535-542.
29. Gray-Owen S.D., Blumberg R.S. CEACAM1: contact-dependent control of immunity. Nat. Rev. Immunol. 2006, 6:433-446.
30. Greenwald R.J., Freeman G.J., Sharpe A.H. The B7 family revisited. Annu. Rev. Immunol. 2005, 23:515-548.
31. Hapfelmeier S., Lawson M.A., Slack E., Kirundi J.K., Stoel M., Heikenwalder M., Cahenzli J., Velykoredko Y., Balmer M.L., Endt K., et al. Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses. Science 2010, 328:1705-1709.
32. Hashizume T., Togawa A., Nochi T., Igarashi O., Kweon M.N., Kiyono H., Yamamoto M. Peyer's patches are required for intestinal immunoglobulin A responses to Salmonella spp. Infect. Immun. 2008, 76:927-934.
33. Hermann-Kleiter N., Baier G. NFAT pulls the strings during CD4+ T helper cell effector functions. Blood 2010, 115:2989-2997.
34. Huber M., Izzi L., Grondin P., Houde C., Kunath T., Veillette A., Beauchemin N. The carboxyl-terminal region of biliary glycoprotein controls its tyrosine phosphorylation and association with protein-tyrosine phosphatases SHP-1 and SHP-2 in epithelial cells. J. Biol. Chem. 1999, 274:335-344.
35. Hurst S.D., Cooper C.J., Sitterding S.M., Choi J., Jump R.L., Levine A.D., Barrett T.A. The differentiated state of intestinal lamina propria CD4+ T cells results in altered cytokine production, activation threshold, and costimulatory requirements. J. Immunol. 1999, 163:5937-5945.
36. Iijima H., Neurath M.F., Nagaishi T., Glickman J.N., Nieuwenhuis E.E., Nakajima A., Chen D., Fuss I.J., Utku N., Lewicki D.N., et al. Specific regulation of T helper cell 1-mediated murine colitis by CEACAM1. J. Exp. Med. 2004, 199:471-482.
37. Kammerer R., Hahn S., Singer B.B., Luo J.S., von Kleist S. Biliary glycoprotein (CD66a), a cell adhesion molecule of the immunoglobulin superfamily, on human lymphocytes: structure, expression and involvement in T cell activation. Eur. J. Immunol. 1998, 28:3664-3674.
38. Kaser A., Lee A.H., Franke A., Glickman J.N., Zeissig S., Tilg H., Nieuwenhuis E.E., Higgins D.E., Schreiber S., Glimcher L.H., Blumberg R.S. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 2008, 134:743-756.
39. Kirshner J., Schumann D., Shively J.E. CEACAM1, a cell-cell adhesion molecule, directly associates with annexin II in a three-dimensional model of mammary morphogenesis. J. Biol. Chem. 2003, 278:50338-50345.
40. Kuespert K., Pils S., Hauck C.R. CEACAMs: their role in physiology and pathophysiology. Curr. Opin. Cell Biol. 2006, 18:565-571.
41. + T lymphocyte activation. J. Immunol 2008, 180:6827-6835.
42. Leung N., Turbide C., Olson M., Marcus V., Jothy S., Beauchemin N. Deletion of the carcinoembryonic antigen-related cell adhesion molecule 1 (Ceacam1) gene contributes to colon tumor progression in a murine model of carcinogenesis. Oncogene 2006, 25:5527-5536.
43. Linterman M.A., Pierson W., Lee S.K., Kallies A., Kawamoto S., Rayner T.F., Srivastava M., Divekar D.P., Beaton L., Hogan J.J., et al. Foxp3+ follicular regulatory T cells control the germinal center response. Nat. Med. 2011, 17:975-982.
44. Lobo E.O., Zhang Z., Shively J.E. Pivotal advance: CEACAM1 is a negative coreceptor for the B cell receptor and promotes CD19-mediated adhesion of B cells in a PI3K-dependent manner. J. Leukoc. Biol. 2009, 86:205-218.
45. Macpherson A.J., Slack E. The functional interactions of commensal bacteria with intestinal secretory IgA. Curr. Opin. Gastroenterol. 2007, 23:673-678.
46. Macpherson A.J., Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 2004, 303:1662-1665.
47. Macpherson A.J., Hunziker L., McCoy K., Lamarre A. IgA responses in the intestinal mucosa against pathogenic and non-pathogenic microorganisms. Microbes Infect. 2001, 3:1021-1035.
48. Manohar M., Baumann D.O., Bos N.A., Cebra J.J. Gut colonization of mice with actA-negative mutant of Listeria monocytogenes can stimulate a humoral mucosal immune response. Infect. Immun. 2001, 69:3542-3549.
49. Massacand J.C., Kaiser P., Ernst B., Tardivel A., Bürki K., Schneider P., Harris N.L. Intestinal bacteria condition dendritic cells to promote IgA production. PLoS ONE 2008, 3:e2588.
50. Morales V.M., Christ A., Watt S.M., Kim H.S., Johnson K.W., Utku N., Texieira A.M., Mizoguchi A., Mizoguchi E., Russell G.J., et al. Regulation of human intestinal intraepithelial lymphocyte cytolytic function by biliary glycoprotein (CD66a). J. Immunol. 1999, 163:1363-1370.
51. Nagaishi T., Pao L., Lin S.H., Iijima H., Kaser A., Qiao S.W., Chen Z., Glickman J., Najjar S.M., Nakajima A., et al. SHP1 phosphatase-dependent T cell inhibition by CEACAM1 adhesion molecule isoforms. Immunity 2006, 25:769-781.
52. Nakajima A., Iijima H., Neurath M.F., Nagaishi T., Nieuwenhuis E.E., Raychowdhury R., Glickman J., Blau D.M., Russell S., Holmes K.V., Blumberg R.S. Activation-induced expression of carcinoembryonic antigen-cell adhesion molecule 1 regulates mouse T lymphocyte function. J. Immunol. 2002, 168:1028-1035.
53. Niemir Z.I., Stein H., Noronha I.L., Krüger C., Andrassy K., Ritz E., Waldherr R. PDGF and TGF-beta contribute to the natural course of human IgA glomerulonephritis. Kidney Int. 1995, 48:1530-1541.
54. Ochi H., Abraham M., Ishikawa H., Frenkel D., Yang K., Basso A.S., Wu H., Chen M.L., Gandhi R., Miller A., et al. Oral CD3-specific antibody suppresses autoimmune encephalomyelitis by inducing CD4+ CD25- LAP+ T cells. Nat. Med. 2006, 12:627-635.
55. Oestreich K.J., Yoon H., Ahmed R., Boss J.M. NFATc1 regulates PD-1 expression upon T cell activation. J. Immunol. 2008, 181:4832-4839.
56. Oida T., Zhang X., Goto M., Hachimura S., Totsuka M., Kaminogawa S., Weiner H.L. CD4+CD25- T cells that express latency-associated peptide on the surface suppress CD4+CD45RBhigh-induced colitis by a TGF-beta-dependent mechanism. J. Immunol. 2003, 170:2516-2522.
57. Pan H., Shively J.E. Carcinoembryonic antigen-related cell adhesion molecule-1 regulates granulopoiesis by inhibition of granulocyte colony-stimulating factor receptor. Immunity 2010, 33:620-631.
58. Schumann D., Chen C.J., Kaplan B., Shively J.E. Carcinoembryonic antigen cell adhesion molecule 1 directly associates with cytoskeleton proteins actin and tropomyosin. J. Biol. Chem. 2001, 276:47421-47433.
59. Seder R.A., Ahmed R. Similarities and differences in CD4+ and CD8+ effector and memory T cell generation. Nat. Immunol. 2003, 4:835-842.
60. Shannon C.E. The mathematical theory of communication. 1963. MD Comput. 1997, 14:306-317.
61. Singer B.B., Scheffrahn I., Heymann R., Sigmundsson K., Kammerer R., Obrink B. Carcinoembryonic antigen-related cell adhesion molecule 1 expression and signaling in human, mouse, and rat leukocytes: evidence for replacement of the short cytoplasmic domain isoform by glycosylphosphatidylinositol-linked proteins in human leukocytes. J. Immunol. 2002, 168:5139-5146.
62. Suzuki K., Meek B., Doi Y., Muramatsu M., Chiba T., Honjo T., Fagarasan S. Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proc. Natl. Acad. Sci. USA 2004, 101:1981-1986.
63. Taylor J.M., Ziman M.E., Fong J., Solnick J.V., Vajdy M. Possible correlates of long-term protection against Helicobacter pylori following systemic or combinations of mucosal and systemic immunizations. Infect. Immun. 2007, 75:3462-3469.
64. van der Waaij L.A., Limburg P.C., Mesander G., van der Waaij D. In vivo IgA coating of anaerobic bacteria in human faeces. Gut 1996, 38:348-354.
65. Wijburg O.L., Uren T.K., Simpfendorfer K., Johansen F.E., Brandtzaeg P., Strugnell R.A. Innate secretory antibodies protect against natural Salmonella typhimurium infection. J. Exp. Med. 2006, 203:21-26.
66. Wollert T., Pasche B., Rochon M., Deppenmeier S., van den Heuvel J., Gruber A.D., Heinz D.W., Lengeling A., Schubert W.D. Extending the host range of Listeria monocytogenes by rational protein design. Cell 2007, 129:891-902.