Adaptive immune response in JAM-C-deficient mice: Normal initiation but reduced IgG memory

Journal of Immunology

Volumn 182, Issue 8, 2009, Pages 4728-4736

  Zimmerli, Claudia ^a   Lee, Boris P L ^a   Palmer, Gaby ^a,b   Gabay, Cem ^a,b   Adams, Ralf ^c   Aurrand Lions, Michel ^a,d   Imhof, Beat A ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY HOSPITAL   (Switzerland)

^c MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^d INSTITUT PAOLI CALMETTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CD11B ANTIGEN; GLYCOPROTEIN P 15095; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G2A; LYMPHOCYTE ANTIGEN; LYMPHOCYTE ANTIGEN JAM C; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; IMMUNOGLOBULIN; JAM3 PROTEIN, MOUSE; LIGAND;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY TITER; ARTHRITIS; ARTICLE; CELL INTERACTION; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; DENDRITIC CELL; IMMUNIZATION; IMMUNOMODULATION; LYMPH NODE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL MOTION; CYTOLOGY; GENETICS; IMMUNITY; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; METABOLISM;

ANIMALS; CELL ADHESION MOLECULES; CELL MOVEMENT; CELL SURVIVAL; CELLS, CULTURED; DENDRITIC CELLS; IMMUNE SYSTEM PROCESSES; IMMUNOGLOBULIN G; IMMUNOGLOBULINS; IMMUNOLOGIC MEMORY; LIGANDS; MICE; MICE, INBRED C57BL;

EID: 65249144059     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0803892     Document Type: Article

References (65)

1. Imhof, B. A., C. Zimmerli, G. Gliki, D. Ducrest-Gay, P. Juillard, P. Hammel, R. Adams, and M. Aurrand-Lions. 2007. Pulmonary dysfunction and impaired granulocyte homeostasis result in poor survival of Jam-C-deficient mice. J. Pathol. 212: 198-208.
2. Bradfield, P. F., S. Nourshargh, M. Aurrand-Lions, and B. A. Imhof. 2007. JAM family and related proteins in leukocyte migration (Vestweber series). Arterioscler. Thromb. Vasc. Biol. 27: 2104-2112.
3. Scheiermann, C., P. Meda, M. Aurrand-Lions, R. Madani, Y. Yiangou, P. Coffey, T. E. Salt, D. Ducrest-Gay, D. Caille, O. Howell, et al. 2007. Expression and function of junctional adhesion molecule-C in myelinated peripheral nerves. Science 318: 1472-1475. (Pubitemid 350208962)
4. Ebnet, K., M. Aurrand-Lions, A. Kuhn, F. Kiefer, S. Butz, K. Zander, M. K. Meyer zu Brickwedde, A. Suzuki, B. A. Imhof, and D. Vestweber. 2003. The junctional adhesion molecule (JAM) family members JAM-2 and JAM-3 associate with the cell polarity protein PAR-3: a possible role for JAMs in endothelial cell polarity. J. Cell. Sci. 116: 3879-3891.
5. Lamagna, C., K. M. Hodivala-Dilke, B. A. Imhof, and M. Aurrand-Lions. 2005. Antibody against junctional adhesion molecule-C inhibits angiogenesis and tumor growth. Cancer Res. 65: 5703-5710. (Pubitemid 40911173)
6. Praetor, A., J. M. McBride, H. Chiu, L. Rangell, L. Cabote, W. P. Lee, J. Cupp, D. M. Danilenko, and S. Fong. 2008. Genetic deletion of JAM-C reveals a role in myeloid progenitor generation. Blood In press.
7. Orlova, V. V., M. Economopoulou, F. Lupu, S. Santoso, and T. Chavakis. 2006. Junctional adhesion molecule-C regulates vascular endothelial permeability by modulating VE-cadherin-mediated cell-cell contacts. J. Exp. Med. 203: 2703-2714.
8. Cunningham, S. A., M. P. Arrate, J. M. Rodriguez, R. J. Bjercke, P. Vanderslice, A. P. Morris, and T. A. Brock. 2000. A novel protein with homology to the junctional adhesion molecule. Characterization of leukocyte interactions. J. Biol. Chem. 275: 34750-34756.
9. Lamagna, C., P. Meda, G. Mandicourt, J. Brown, R. J. Gilbert, E. Y. Jones, F. Kiefer, P. Ruga, B. A. Imhof, and M. Aurrand-Lions. 2005. Dual interaction of JAM-C with JAM-B and α(M)β2 integrin: function in junctional complexes and leukocyte adhesion. Mol. Biol. Cell 16: 4992-5003. (Pubitemid 41416476)
10. Santoso, S., V. V. Orlova, K. Song, U. J. Sachs, C. L. Andrei-Selmer, and T. Chavakis. 2005. The homophilic binding of junctional adhesion molecule-C mediates tumor cell-endothelial cell interactions. J. Biol. Chem. 280: 36326-36333. (Pubitemid 41633906)
11. Santoso, S., U. J. Sachs, H. Kroll, M. Linder, A. Ruf, K. T. Preissner, and T. Chavakis. 2002. The junctional adhesion molecule 3 (JAM-3) on human platelets is a counterreceptor for the leukocyte integrin Mac-1. J. Exp. Med. 196: 679-691. (Pubitemid 35024445)
12. Langer, H. F., K. Daub, G. Braun, T. Schonberger, A. E. May, M. Schaller, G. M. Stein, K. Stellos, A. Bueltmann, D. Siegel-Axel, et al. 2007. Platelets recruit human dendritic cells via Mac-1/JAM-C interaction and modulate dendritic cell function in vitro. Arterioscler. Thromb. Vasc. Biol. 27: 1463-1470.
13. Chavakis, T., T. Keiper, R. Matz-Westphal, K. Hersemeyer, U. J. Sachs, P. P. Nawroth, K. T. Preissner, and S. Santoso. 2004. The junctional adhesion molecule-C promotes neutrophil transendothelial migration in vitro and in vivo. J. Biol. Chem. 279: 55602-55608. (Pubitemid 40066564)
14. Palmer, G., N. Busso, M. Aurrand-Lions, D. Talabot-Ayer, V. Chobaz-Peclat, C. Zimmerli, P. Hammel, B. A. Imhof, and C. Gabay. 2007. Expression and function of junctional adhesion molecule-C in human and experimental arthritis. Arthritis Res. Ther. 9: R65. (Pubitemid 47249055)
15. Vonlaufen, A., M. Aurrand-Lions, C. M. Pastor, C. Lamagna, A. Hadengue, B. A. Imhof, and J. L. Frossard. 2006. The role of junctional adhesion molecule C (JAM-C) in acute pancreatitis. J. Pathol. 209: 540-548. (Pubitemid 44194569)
16. Aurrand-Lions, M., C. Lamagna, J. P. Dangerfield, S. Wang, P. Herrera, S. Nourshargh, and B. A. Imhof. 2005. Junctional adhesion molecule-C regulates the early influx of leukocytes into tissues during inflammation. J. Immunol. 174: 6406-6415. (Pubitemid 40663834)
17. Bradfield, P. F., C. Scheiermann, S. Nourshargh, C. Ody, F. W. Luscinskas, G. E. Rainger, G. B. Nash, M. Miljkovic-Licina, M. Aurrand-Lions, and B. A. Imhof. 2007. JAM-C regulates unidirectional monocyte transendothelial migration in inflammation. Blood.
18. Aurrand-Lions, M., L. Duncan, C. Ballestrem, and B. A. Imhof. 2001. JAM-2, a novel immunoglobulin superfamily molecule, expressed by endothelial and lymphatic cells. J. Biol. Chem. 276: 2733-2741. (Pubitemid 37376652)
19. Pfeiffer, F., V. Kumar, S. Butz, D. Vestweber, B. A. Imhof, J. V. Stein, and B. Engelhardt. 2008. Distinct molecular composition of blood and lymphatic vascular endothelial cell junctions establishes specific functional barriers within the peripheral lymph node. Eur. J. Immunol. 38: 2142-2155.
20. Gunn, M. D., S. Kyuwa, C. Tam, T. Kakiuchi, A. Matsuzawa, L. T. Williams, and H. Nakano. 1999. Mice lacking expression of secondary lymphoid organ chemokine have defects in lymphocyte homing and dendritic cell localization. J. Exp. Med. 189: 451-460.
21. Ohl, L., M. Mohaupt, N. Czeloth, G. Hintzen, Z. Kiafard, J. Zwirner, T. Blankenstein, G. Henning, and R. Forster. 2004. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 21: 279-288. (Pubitemid 39094056)
22. Johnson, L. A., and D. G. Jackson. 2008. Cell traffic and the lymphatic endothelium. Ann. NY Acad. Sci. 1131: 119-133.
23. Bennouna, S., S. K. Bliss, T. J. Curiel, and E. Y. Denkers. 2003. Cross-talk in the innate immune system: neutrophils instruct recruitment and activation of dendritic cells during microbial infection. J. Immunol. 171: 6052-6058. (Pubitemid 37467225)
24. Ludwig, I. S., T. B. Geijtenbeek, and Y. van Kooyk. 2006. Two way communication between neutrophils and dendritic cells. Curr. Opin. Pharmacol. 6: 408-413.
25. Munz, C., R. M. Steinman, and S. Fujii. 2005. Dendritic cell maturation by innate lymphocytes: coordinated stimulation of innate and adaptive immunity. J. Exp. Med. 202: 203-207. (Pubitemid 41043815)
26. Lammermann, T., B. L. Bader, S. J. Monkley, T. Worbs, R. Wedlich-Soldner, K. Hirsch, M. Keller, R. Forster, D. R. Critchley, R. Fassler, and M. Sixt. 2008. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 453: 51-55. (Pubitemid 351630331)
27. Watanabe, H., M. Unger, B. Tuvel, B. Wang, and D. N. Sauder. 2002. Contact hypersensitivity: the mechanism of immune responses and T cell balance. J. Interferon Cytokine Res. 22: 407-412. (Pubitemid 34579542)
28. Granucci, F., I. Zanoni, and P. Ricciardi-Castagnoli. 2008. Central role of dendritic cells in the regulation and deregulation of immune responses. Cell. Mol. Life Sci. 65: 1683-1697.
29. Stein, J. V., and C. Nombela-Arrieta. 2005. Chemokine control of lymphocyte trafficking: a general overview. Immunology 116: 1-12.
30. Wallet, M. A., P. Sen, and R. Tisch. 2005. Immunoregulation of dendritic cells. Clin. Med. Res. 3: 166-175.
31. Behrens, E. M., U. Sriram, D. K. Shivers, M. Gallucci, Z. Ma, T. H. Finkel, and S. Gallucci. 2007. Complement receptor 3 ligation of dendritic cells suppresses their stimulatory capacity. J. Immunol. 178: 6268-6279.
32. Skoberne, M., S. Somersan, W. Almodovar, T. Truong, K. Petrova, P. M. Henson, and N. Bhardwaj. 2006. The apoptotic-cell receptor CR3, but not αvβ5, is a regulator of human dendritic-cell immunostimulatory function. Blood 108: 947-955. (Pubitemid 44154630)
33. Varga, G., S. Balkow, M. K. Wild, A. Stadtbaeumer, M. Krummen, T. Rothoeft, T. Higuchi, S. Beissert, K. Wethmar, K. Scharffetter-Kochanek, et al. 2007. Active MAC-1 (CD11b/CD18) on DCs inhibits full T-cell activation. Blood 109: 661-669. (Pubitemid 46105967)
34. Garside, P., E. Ingulli, R. R. Merica, J. G. Johnson, R. J. Noelle, and M. K. Jenkins. 1998. Visualization of specific B and T lymphocyte interactions in the lymph node. Science 281: 96-99. (Pubitemid 28354051)
35. MacLennan, I. C., A. Gulbranson-Judge, K. M. Toellner, M. Casamayor-Palleja, E. Chan, D. M. Sze, S. A. Luther, and H. A. Orbea. 1997. The changing preference of T and B cells for partners as T-dependent antibody responses develop. Immunol. Rev. 156: 53-66.
36. Tarlinton, D., A. Radbruch, F. Hiepe, and T. Dorner. 2008. Plasma cell differentiation and survival. Curr. Opin. Immunol. 20: 162-169.
37. Allen, C. D., T. Okada, and J. G. Cyster. 2007. Germinal-center organization and cellular dynamics. Immunity. 27: 190-202.
38. Moser, K., G. Muehlinghaus, R. Manz, H. Mei, C. Voigt, T. Yoshida, T. Dorner, F. Hiepe, and A. Radbruch. 2006. Long-lived plasma cells in immunity and immunopathology. Immunol. Lett. 103: 83-85. (Pubitemid 43162920)
39. Manz, R. A., A. E. Hauser, F. Hiepe, and A. Radbruch. 2005. Maintenance of serum antibody levels. Annu. Rev. Immunol. 23: 367-386.
40. Gliki, G., K. Ebnet, M. Aurrand-Lions, B. A. Imhof, and R. H. Adams. 2004. Spermatid differentiation requires the assembly of a cell polarity complex down-stream of junctional adhesion molecule-C. Nature 431: 320-324. (Pubitemid 39265668)
41. Ruedl, C., P. Koebel, M. Bachmann, M. Hess, and K. Karjalainen. 2000. Anatomical origin of dendritic cells determines their life span in peripheral lymph nodes. J. Immunol. 165: 4910-4916.
42. Lutz, M. B., N. Kukutsch, A. L. Ogilvie, S. Rossner, F. Koch, N. Romani, and G. Schuler. 1999. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223: 77-92.
43. Stockinger, B., T. Zal, A. Zal, and D. Gray. 1996. B cells solicit their own help from T cells. J. Exp. Med. 183: 891-899. (Pubitemid 26113961)
44. Martin-Fontecha, A., S. Sebastiani, U. E. Hopken, M. Uguccioni, M. Lipp, A. Lanzavecchia, and F. Sallusto. 2003. Regulation of dendritic cell migration to the draining lymph node: impact on T lymphocyte traffic and priming. J. Exp. Med. 198: 615-621. (Pubitemid 37040395)
45. Nossal, G. J., and M. Karvelas. 1990. Soluble antigen abrogates the appearance of anti-protein IgG1-forming cell precursors during primary immunization. Proc. Natl. Acad. Sci. USA 87: 1615-1619. (Pubitemid 20080359)
46. Busso, N., A. So, V. Chobaz-Peclat, C. Morard, E. Martinez-Soria, D. Talabot-Ayer, and C. Gabay. 2002. Leptin signaling deficiency impairs humoral and cellular immune responses and attenuates experimental arthritis. J. Immunol. 168: 875-882. (Pubitemid 34049591)
47. + cells in mouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells. J. Exp. Med. 194: 1171-1178.
48. Coxon, A., P. Rieu, F. J. Barkalow, S. Askari, A. H. Sharpe, U. H. von Andrian, M. A. Arnaout, and T. N. Mayadas. 1996. A novel role for the β 2 integrin CD11b/CD18 in neutrophil apoptosis: a homeostatic mechanism in inflammation. Immunity 5: 653-666. (Pubitemid 27062073)
49. Randolph, G. J., V. Angeli, and M. A. Swartz. 2005. Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat. Rev. Immunol. 5: 617-628.
50. Grabbe, S., M. Steinert, K. Mahnke, A. Schwartz, T. A. Luger, and T. Schwarz. 1996. Dissection of antigenic and irritative effects of epicutaneously applied haptens in mice: evidence that not the antigenic component but nonspecific proinflammatory effects of haptens determine the concentration-dependent elicitation of allergic contact dermatitis. J. Clin. Invest. 98: 1158-1164. (Pubitemid 26299929)
51. Klein, U., and R. Dalla-Favera. 2008. Germinal centers: role in B-cell physiology and malignancy. Nat. Rev. Immunol. 8: 22-33.
52. Cera, M. R., A. Del Prete, A. Vecchi, M. Corada, I. Martin-Padura, T. Motoike, P. Tonetti, G. Bazzoni, W. Vermi, F. Gentili, et al. 2004. Increased DC trafficking to lymph nodes and contact hypersensitivity in junctional adhesion molecule-A-deficient mice. J. Clin. Invest. 114: 729-738.
53. Cunningham, S. A., J. M. Rodriguez, M. P. Arrate, T. M. Tran, and T. A. Brock. 2002. JAM2 interacts with α4β1: facilitation by JAM3. J. Biol. Chem. 277: 27589-27592.
54. Ludwig, R. J., T. M. Zollner, S. Santoso, K. Hardt, J. Gille, H. Baatz, P. S. Johann, J. Pfeffer, H. H. Radeke, M. P. Schon, et al. 2005. Junctional adhesion molecules (JAM)-B and -C contribute to leukocyte extravasation to the skin and mediate cutaneous inflammation. J. Invest. Dermatol. 125: 969-976.
55. Rosen, H., and S. Gordon. 1987. Monoclonal antibody to the murine type 3 complement receptor inhibits adhesion of myelomonocytic cells in vitro and inflammatory cell recruitment in vivo. J. Exp. Med. 166: 1685-1701. (Pubitemid 18000348)
56. Rahman, Z. S., S. P. Rao, S. L. Kalled, and T. Manser. 2003. Normal induction but attenuated progression of germinal center responses in BAFF and BAFF-R signaling-deficient mice. J. Exp. Med. 198: 1157-1169.
57. Gatto, D., T. Pfister, A. Jegerlehner, S. W. Martin, M. Kopf, and M. F. Bachmann. 2005. Complement receptors regulate differentiation of bone marrow plasma cell precursors expressing transcription factors Blimp-1 and XBP-1. J. Exp. Med. 201: 993-1005. (Pubitemid 40524468)
58. Roozendaal, R., and M. C. Carroll. 2007. Complement receptors CD21 and CD35 in humoral immunity. Immunol. Rev. 219: 157-166. (Pubitemid 47390008)
59. Ahearn, J. M., M. B. Fischer, D. Croix, S. Goerg, M. Ma, J. Xia, X. Zhou, R. G. Howard, T. L. Rothstein, and M. C. Carroll. 1996. Disruption of the Cr2 locus results in a reduction in B-1a cells and in an impaired B cell response to T-dependent antigen. Immunity. 4: 251-262.
60. Huber, C., C. Thielen, H. Seeger, P. Schwarz, F. Montrasio, M. R. Wilson, E. Heinen, Y. X. Fu, G. Miele, and A. Aguzzi. 2005. Lymphotoxin-β receptor-dependent genes in lymph node and follicular dendritic cell transcriptomes. J. Immunol. 174: 5526-5536. (Pubitemid 40593193)
61. Kunkel, E. J., and E. C. Butcher. 2003. Plasma-cell homing. Nat. Rev. Immunol. 3: 822-829.
62. Bullard, D. C., E. J. Kunkel, H. Kubo, M. J. Hicks, I. Lorenzo, N. A. Doyle, C. M. Doerschuk, K. Ley, and A. L. Beaudet. 1996. Infectious susceptibility and severe deficiency of leukocyte rolling and recruitment in E-selectin and P-selectin double mutant mice. J. Exp. Med. 183: 2329-2336.
63. Pabst, O., T. Peters, N. Czeloth, G. Bernhardt, K. Scharffetter-Kochanek, and R. Forster. 2005. Cutting edge: egress of newly generated plasma cells from peripheral lymph nodes depends on β 2 integrin. J. Immunol. 174: 7492-7495. (Pubitemid 40806251)
64. Underhill, G. H., H. A. Minges Wols, J. L. Fornek, P. L. Witte, and G. S. Kansas. 2002. IgG plasma cells display a unique spectrum of leukocyte adhesion and homing molecules. Blood 99: 2905-2912.
65. Moser, K., K. Tokoyoda, A. Radbruch, I. MacLennan, and R. A. Manz. 2006. Stromal niches, plasma cell differentiation and survival. Curr. Opin. Immunol. 18: 265-270.