PECAM-1-regulated signalling thresholds control tolerance in anergic transgenic B-cells

Molecular Immunology

Volumn 45, Issue 6, 2008, Pages 1767-1781

  Wong, Mae Xhum ^a   Hayball, John D ^b   Jackson, Denise E ^a  

^a AUSTIN RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

Author keywords

Cell surface molecules; Tolerance suppression anergy; Transgenic knockout mice

Indexed keywords

ANTIBODY; CALCIUM ION; CD31 ANTIGEN; IMMUNOGLOBULIN; IMMUNOGLOBULIN M; INTERLEUKIN 4; LIPOPOLYSACCHARIDE; LYMPHOCYTE ANTIGEN RECEPTOR; PROTEIN TYROSINE PHOSPHATASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIBODY PRODUCTION; ARTICLE; B LYMPHOCYTE; BONE MARROW; BREEDING; CLONAL ANERGY; CONTROLLED STUDY; CROSS LINKING; FEMALE; IMMUNOLOGICAL TOLERANCE; IMMUNOREACTIVITY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR AFFINITY; SERUM; SIGNAL TRANSDUCTION; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIGENS, CD31; AUTOANTIBODIES; B-LYMPHOCYTES; BONE MARROW; CALCIUM; CELL PROLIFERATION; CROSS-LINKING REAGENTS; IMMUNE TOLERANCE; IMMUNOGLOBULIN M; INTERLEUKIN-4; LIPOPOLYSACCHARIDES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MURAMIDASE; SIGNAL TRANSDUCTION;

MUS; MUS MUSCULUS;

EID: 38949192899     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2007.09.024     Document Type: Article

References (44)

1. Allman D., Lindsley R.D., DeMuth W., Rudd K., Shinton S.A., and Hardy R.R. Resolution of three nonproliferative immature splenic B cell subsets reveals multiple selection points during peripheral B cell maturation. J. Immunol. 167 (2001) 6834-6840
2. Ashman L.K., and Aylett G.W. Expression of CD31 epitopes on human lymphocytes: CD31 monoclonal antibodies differentiate between naïve (CD45RA+) and memory (CD45RA-) CD4-positive T cells. Tissue Antigens 38 5 (1991) 208-212
3. Baba T.W., Giroir B.P., and Humphries E.H. Cell lines derived from avian lymphocytes exhibit two distinct phenotypes. Virology 144 (1985) 139-151
4. Baldwin H.S., Shen H.M., Yan H.C., DeLisser H., Chung A., Mickanin C., Trask T., Kitschbaum N.E., Newman P.J., Albelda S.M., and Buck C.A. Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31): alternatively spliced, functionally distinct isoforms expressed during mammalian cardiovascular development. Development 120 9 (1994) 2539-2953
5. Cooke M.P., Heath A.W., Shokat K.M., Zeng Y., Finkelman F.D., Linsley P.S., Howard M., and Goodnow C.C. Immunoglobulin signal transduction guides the specificity of B cell-T cell interactions and is blocked in tolerant self-reactive B cells. J. Exp. Med. 179 (1994) 425-438
6. Cornall R.J., Cheng A.M., Pawson T., and Goodnow C.C. Role of Syk in B-cell development and antigen-receptor signaling. Proc. Natl. Acad. Sci. U.S.A. 97 4 (2000) 1713-1718
7. Cornall R.J., Cyster J.G., Hibbs M.L., Dunn A.R., Otipoby K.L., Clark E.A., and Goodnow C.C. Polygenic autoimmune traits: Lyn, CD22 and SHP-1 are limiting elements of a biochemical pathway regulating BCR signaling and selection. Immunity 8 (1998) 497-508
8. Cyster J.G., and Goodnow C.C. Protein tyrosine phosphatase 1C negatively regulates antigen receptor signaling in B lymphocytes and determines thresholds for negative selection. Immunity 2 (1995) 13-24
9. Cyster J.G., Healy J.I., Kishihara K., Mak T., Thomas M.L., and Goodnow C.C. Regulation of B-lymphocyte negative and positive selection by tyrosine phosphatase, CD45. Nature 381 6580 (1996) 325-328
10. DeLisser H.M., Helmke B.P., Cao G., Egan P.M., Taichman D., Fehrenbach M., Zaman A., Cui Z., Mohan G.S., Baldwin H.S., Davies P.F., and Savani R.C. Loss of PECAM-1 function impairs alveolarization. J. Biol. Chem. 281 13 (2006) 8724-8731
11. Duncan G.S., Andrew D.P., Takimoto H., Kaufman S.A., Yoshida H., Spellberg J., Luis de la Pompa J., Elia A., Wakeham A., Karan-Tamir B., Muller W.A., Senaldi G., Zukowski M.M., and Mak T.W. Genetic evidence for functional redundancy of Platelet/Endothelial Cell Adhesion Molecule-1 (PECAM-1): CD31-deficient mice reveal PECAM-1-dependent and PECAM-1-independent functions. J. Immunol. 162 5 (1999) 3022-3030
12. Falati S., Patil S., Gross P.L., Stapleton M., Merrill-Skoloff G., Pixton K.L., Weiler H., Cooley B., Newman D.K., Newman P.J., Furie B.C., Furie B., and Gibbins J.M. Platelet PECAM-1 inhibits thrombus formation in vivo. Blood 107 2 (2006) 535-541
13. Gao C., Sun W., Christofidou-Solomidou M., Sawada M., Newman D.K., Bergom C., Albelda S.M., Matsuyama S., and Newman P.J. PECAM-1 functions as a specific and potent inhibitor of mitochondrial-dependent apoptosis. Blood 102 1 (2003) 169-179
14. Gauld S.B., Benschop R.J., Merrell K.T., and Cambier J.C. Maintenance of B cell anergy requires constant antigen receptor occupancy and signaling. Nat. Immunol. 6 11 (2005) 1072-1074
15. Goodnow C.C., Crosbie J., Adelstein S., Lavoie T.B., Smith-Gill S.J., Brink R.A., Pritchard-Briscoe H., Wotherspoon J.S., Loblay R.H., Raphael K., Trent R.J., and Basten A. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 334 (1998) 676-682
16. Goodnow C.C., Crosbie J., Jorgensen H., Brink R.A., and Basten A. Induction of self-tolerance in mature peripheral B lymphocytes. Nature 342 (1989) 385-391
17. Goodnow C.C. Balancing immunity and tolerance: deleting and tuning lymphocyte repertoires. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 2264-2271
18. Graesser D., Solowiej A., Bruckner M., Osterweil E., Juedes A., Davis S., Ruddle N.H., Engelhardt B., and Madri J.A. Altered vascular permeability and early onset of experimental autoimmune encephalomyelitis in PECAM-1-deficient mice. J. Clin. Invest. 109 3 (2002) 383-392
19. Hartley S.B., Crosbie J., Brink R., Kantor A.A., Basten A., and Goodnow C.C. Elimination from peripheral lymphoid tissues of self-reactive B lymphocytes recognizing membrane-bound antigens. Nature 353 (1991) 765-769
20. Hartley S.B., Cooke M.P., Fulcher D.A., Harris A.W., Cory S., Basten A., and Goodnow C.C. Elimination from peripheral lymphoid tissues of self-reactive B lymphocytes recognizing membrane-bound antigens. Nature 353 (1993) 765-769
21. Henshall T.L., Jones K.L., Wilkinson R., and Jackson D.E. Src homology 2 domain-containing protein-tyrosine phosphatases, SHP-1 and SHP-2, are required for platelet endothelial cell adhesion molecule-1/CD31-mediated inhibitory signaling. J. Immunol. 166 5 (2001) 3098-3106
22. Hippen K.L., Tze L.E., and Behrens T.W. CD5 maintains tolerance in anergic B cells. J. Exp. Med. 191 5 (2000) 883-889
23. Inaoke M., Sato S., Weintraub B.C., Goodnow C.C., and Tedder T.F. CD19-regulated signaling thresholds control peripheral tolerance and autoantibody production in B lymphocytes. J. Exp. Med. 186 (1997) 1923-1931
24. Jackson D.E., Gully L.M., Henshall T.L., Mardell C.E., and Macardle P.J. Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31) is associated with a naïve B-cell phenotype in human tonsils. Tissue Antigens 56 2 (2000) 105-116
25. Jones K.L., Hughan S.C., Dopheide S.M., Farndale R.W., Jackson S.P., and Jackson D.E. Platelet endothelial cell adhesion molecule-1 is a negative regulator of platelet-collagen interactions. Blood 98 5 (2001) 1456-1463
26. Lesley R., Xu Y., Kalled S.L., Hess D.M., Schwab S.R., Shu H.B., and Cyster J.G. Reduced competitiveness of autoantigen-engaged B cells due to increased dependence on BAFF. Immunity 20 6 (2004) 441-453
27. Nishimura H., Minato N., Nakano T., and Honjo T. Immunological studies on PD-1-deficient mice: implication of PD-1 as a negative regulator for B cell responses. Int. Immunol. 10 (1998) 1563-1572
28. Nishimura H., Nose M., Hiai H., Minato N., and Honjo T. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif carrying immunoreceptor. Immunity 11 (1999) 141-151
29. O'Keefe T.L., Williams G.T., Davies S.L., and Neuberger M.S. Hyperresponsive B cells in CD22-deficient mice. Science 274 (1996) 798-801
30. O'Keefe T.L., Williams G.T., Batista F.D., and Neuberger M.S. Deficiency of CD22, a B cell-specific inhibitory receptor, is sufficient to predispose to development of high affinity autoantibodies. J. Exp. Med. 189 (1999) 1307-1313
31. Oliver P.M., Vass T., Kappler J., and Marrack P. Loss of pro-apoptotic protein, Bim, breaks B cell anergy. J. Exp. Med. 203 3 (2006) 731-741
32. Pan C., Baumgarth N., and Parnes J.R. CD72-deficient mice reveal nonredundant roles of CD72 in B cell development and activation. Immunity 11 (1999) 495-506
33. Prager E., Staffler G., Majdic O., Saemann M., Godar S., Zlabinger G., and Stockinger H. Induction of hyporesponsiveness and impaired T lymphocyte activation by the CD31 receptor:ligand pathway in T cells. J. Immunol. 166 4 (2001) 2364-2371
34. Ravetch J.V., and Lanier L.L. Immune inhibitory receptors. Science 290 5489 (2000) 84-89
35. Sato S., Miller A.S., Inaoki M., Bock C.B., Jansen P.J., Tang M.L., and Tedder T.F. CD22 is both a positive and negative regulator of B lymphocyte antigen receptor signal transduction: altered signaling in CD22-deficient mice. Immunity 5 (1996) 551-562
36. Schenkel A.R., Chew T.W., Chlipala E., Harbord M.W.N., and Muller W.A. Different susceptibilities of PECAM-1-deficient mouse strains to spontaneous idiopathic pneumonitis. Exp. Mol. Path. 81 (2006) 23-30
37. Solowiej A., Biswas P., Graesser D., and Madri J.A. Lack of platelet endothelial cell adhesion molecule-1 attenuates foreign body inflammation because of decreased angiogenesis. Am. J. Pathol. 162 3 (2003) 953-962
38. Tado Y., Koarada S., Morito F., Ushiyama O., Haruta Y., Kanegae F., Ohta A., Ho A., Mak T.W., and Nagasawa K. Acceleration of the onset of collagen-induced arthritis by a deficiency of platelet endothelial cell adhesion molecule 1. Arthritis Rheum. 48 11 (2003) 3280-3290
39. Takai T., Ono M., Hikida M., Ohmori H., and Ravetch J.V. Augmented humoral and anaphylactic responses in FcγRIIb-deficient mice. Nature 379 (1996) 346-349
40. Thompson R.D., Noble K.E., Larbi K.Y., Dewar A., Duncan G.S., Mak T.W., and Nourshargh S. Platelet-endothelial cell adhesion molecule-1 (PECAM-1)-deficient mice demonstrate a transient and cytokine-specific role for PECAM-1 in leukocyte migration through perivascular basement membrane. Blood 97 6 (2001) 1854-1860
41. Ujike A., Takeda K., Nakamura A., Ebihara S., Akiyama K., and Takai T. Impaired dendritic cell maturation and increased T(H)2 responses in PIR-B(-/-) mice. Nat. Immunol. 3 6 (2002) 542-548
42. Wilkinson R., Lyons A.B., Roberts D., Wong X.M., Bartley P.A., and Jackson D.E. Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31) acts as a regulator of B-cell development, B-cell antigen receptor (BCR)-mediated activation, and autoimmune disease. Blood 100 1 (2002) 184-193
43. Wong M.X., Hayball J.D., Hogarth P.M., and Jackson D.E. The inhibitory co-receptor, PECAM-1 provides a protective effect in suppression of collagen-induced arthritis. J. Clin. Immunol. 25 1 (2005) 19-28
44. Wong M.X., Roberts D., Bartley P.A., and Jackson D.E. Absence of platelet endothelial cell adhesion molecule-1 (CD31) leads to increased severity of local and systemic IgE-mediated anaphylaxis and modulation of mast cell activation. J. Immunol. 168 12 (2002) 6455-6462