Antigen endocytosis and presentation mediated by human membrane IgG1 in the absence of the IgA/Igβ dimer

EMBO Journal

Volumn 16, Issue 13, 1997, Pages 3842-3850

  Knight, Andrew M ^a   Lucocq, John M ^a   Prescott, Alan R ^a   Ponnambalam, Sreenivasan ^a   Watts, Colin ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Antigen presentation; Class II MCH; Endocytosis; IG ; Ig ; mIgG

Indexed keywords

B LYMPHOCYTE ANTIGEN; DIMER; IMMUNOGLOBULIN G1; LYMPHOCYTE ANTIGEN RECEPTOR; MEMBRANE PROTEIN;

ANIMAL CELL; ANTIGEN PRESENTATION; ARTICLE; B LYMPHOCYTE; CHIMERA; CONTRAST; CONTROLLED STUDY; ENDOCYTOSIS; NONHUMAN; PRIORITY JOURNAL; SURFACE PROPERTY;

AMINO ACID SEQUENCE; ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, CD; ANTIGENS, CD4; ANTIGENS, CD79; CELL LINE, TRANSFORMED; CELL MEMBRANE; CHO CELLS; CRICETINAE; CYTOPLASM; DIMERIZATION; ENDOCYTOSIS; HELA CELLS; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN GAMMA-CHAINS; IMMUNOGLOBULIN HEAVY CHAINS; MOLECULAR SEQUENCE DATA; RECEPTORS, ANTIGEN, B-CELL; TUMOR CELLS, CULTURED;

EID: 0030997471     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.13.3842     Document Type: Article

References (55)

1. Amigorena, S., Drake, J.R., Webster, P. and Mellman, I. (1994) Transient accumulation of new class II MHC molecules in a novel endocytic compartment in B lymphocytes. Nature, 369, 113-120.
2. Bensmana, M. and Lefranc, M.-P. (1990) Gene segments encoding membrane domains of the human immunoglobulin gamma 3 and alpha chains. Immunogenetics, 32, 321-330.
3. Bonnerot, C., Lankar, D., Hanau, D., Spehner, D. Davoust, J. Salamero, J. and Friedman, W.H. (1995) Role of B cell receptor Ig alpha and Ig beta subunits in MHC class II-restricted antigen presentation. Immunity, 3, 335-347.
4. Cambier, J.C., Pleiman, C.M. and Clark, M.R. (1994) Signal transduction by the B cell antigen receptor and its coreceptors. Annu. Rev. Immunol., 12, 457-486.
5. Davidson, H.W. and Watts, C. (1989) Epitope-directed processing of specific antigen by B lymphocytes. J. Cell Biol., 109, 85-92.
6. Demotz, S., Lanzavecchia, A., Eisel, U., Niemann, H., Widmann, C. and Corradin, G. (1989) Delineation of several DR-restricted tetanus toxin T cell epitopes. J. Immunol., 142, 394-402.
7. Gong, S. and Nussenzweig, M.C. (1996) Regulation of an early developmental checkpoint in the B cell pathway by Igβ. Science, 272, 411-414.
8. Grupp, S.A., Campbell, K., Mitchell, R.N., Cambier, J.C. and Abbas, A.K. (1993) Signaling-defective mutants of the B lymphocyte antigen receptor fail to associate with Ig-alpha and Ig-beta/gamma. J. Biol. Chem., 268, 25776-25779.
9. Hieter, P.A., Max, E.E., Seidman, J.G., Maizel, J.V. and Leder, P. (1980) Cloned human and mouse kappa immunoglobulin constant and J regions conserve homology in functional segments. Cell, 22, 197-207.
10. Hombach, J., Leclercq, L., Radbruch, A., Rajewsky, K. and Reth, M. (1988) A novel 34-kd protein co-isolated with the IgM molecule in surface IgM-expressing cells. EMBO J., 7, 3451-3456.
11. Hombach, J., Tsubata, T., Leclercq, L., Stappert, H. and Reth, M. (1990) Molecular components of the B-cell antigen receptor complex of the IgM class. Nature, 343, 760-762.
12. Kinoshita, K., Shimizu, A. and Honjo, T. (1991) The membrane exons of the pseudo-γ-chain gene of the human immunoglobulin are apparently functional and highly homologous to those of the γ1 gene. Immunol. Lett., 27, 151-156.
13. Kitamura, D., Roes, J., Kühn, R. and Rajewsky, K. (1991) A B cell-deficient mouse by targetted disruption of the membrane exon of the immunoglobulin μ chain gene. Nature, 350, 423-126.
14. Lampson, L.A. and Levy, R. (1980) Two populations of Ia-like molecules on a human B cell line. J. Immunol., 125, 293-299.
15. Lanzavecchia, A. (1985) Antigen-specific interaction between T and B cells. Nature, 314, 537-539.
16. Larrick, J.W., Danielsson, L., Brenner, C.A., Abrahamson, M., Fry, K.E. and Borrebaeck, C.A.K. (1989) Rapid cloning of rearranged immunoglobulin genes from human hybridoma cells using mixed primers and the polymerase chain reaction. Biochem. Biophys. Res. Commun., 160, 1250-1256.
17. Love, J.M., Knight, A.M., McAteer, M.A. and Todd, J.A. (1990) Towards construction of a high resolution map of the mouse genome using PCR-analysed microsatellites. Nucleic Acids Res., 18, 4123-4130.
18. Lucocq, J.M., Berger, E. and Hug, C. (1995) The pathway of Golgi cluster formation in okadaic acid-treated cells. J. Struct. Biol., 115, 318-330.
19. Matsuuchi, L., Gold, M.R., Travis, A., Grosschedl, R., DeFranco, A.L. and Kelly, R.B. (1992) The membrane IgM-associated proteins MB-1 and Ig-β are sufficient to promote surface expression of a partially functional B-cell antigen receptor in a nonlymphoid cell. Proc. Natl Acad. Sci. USA, 89, 3404-3408.
20. Mellman, I. and Plutner, H. (1984) Internalization and degradation of macrophage Fc receptors bound to polyvalent immune complexes. J. Cell Biol., 98, 1170-1177.
21. Michnoff, C.H., Parikh, V.S., Lelsz, D.L. and Tucker, P.W. (1994) Membrane immunoglobulin (Ig) M alters Igα and Igβ association and signal transduction. J. Biol. Chem., 269, 24237-24244.
22. Mikaelian, I. and Sergent, A. (1992) A general and fast method to generate multiple site directed mutations. Nucleic Acids Res., 20, 376.
23. Mitchell, R.N., Barnes, K.A., Grupp, S.A., Sanchez, M., Misulovin, Z., Nussenzweig, M.C. and Abbas, A.K. (1995) Intracellular targeting of antigens internalized by membrane immunoglobulin in B lymphocytes. J. Exp. Med., 181, 1705-1714.
24. Naim, H.Y. and Roth, M.G. (1994) Characteristics of the internalization signal in the Y543 influenza virus hemagglutinin suggest a model for recognition of internalization signals containing tyrosine. J. Biol. Chem., 269, 3928-3933.
25. Nakamura, T., Kubagawa, H. and Cooper, M.D. (1992) Heterogeneity of immunoglobulin-associated molecules on human B cells identified by monoclonal antibodies. Proc. Natl Acad. Sci. USA, 89, 8522-8526.
26. Niebling, W.L. and Pierce, S.K. (1993) Antigen entry into early endosomes is insufficient for MHC class II processing. J. Immunol. 150, 2687-2697.
27. Nijman, H.W. et al. (1995) Antigen capture and major histocompatibility class II compartments of freshly isolated and cultured human blood dendritic cells. J. Exp. Med., 182, 163-174.
28. Papavasilou, F., Misulovin, Z. and Nussenzweig, M.C. (1995a) The role of Igβ in precursor B cell transition and allelic exclusion. Science, 268, 408-411.
29. Papavasilou, F., Jankovic, M., Suh, H. and Nussenzweig, M.C. (1995b) The cytoplasmic domains of immunoglobulin (Ig) alpha and Ig beta can independently induce the precursor B cell transition and allelic exclusion. J. Exp. Med., 182, 1389-1394.
30. Patel, K.J. and Neuberger, M.S. (1993) Antigen presentation by the B cell antigen receptor is driven by the α/β sheath and occurs independently of its cytoplasmic tyrosines. Cell, 74, 939-946.
31. Pelchen-Mathews, A., Armes, J.E., Griffiths, G. and Marsh, M. (1991) Differential endocytosis of CD4 in lymphocytic and non lymphocytic cells. J. Exp. Med., 173, 575-587.
32. Peters, P.J., Neefjes, J.J., Oorschot, V., Ploegh, H.L. and Geuze, H.J. (1991) Segregation of MHC class II molecules from MHC class I molecules in the Golgi complex for transport to lysosomal compartments. Nature, 349, 669-676.
33. Pieters, J., Horstmann, H., Bakke, O., Griffiths, G. and Lipp, J. (1991) Intracellular transport and localization of major histocompatibility complex class II molecules and associated invariant chain. J. Cell Biol., 115, 1213-1223.
34. Ponnambalam, S., Rabouille, C., Luzio, J.P., Nilsson, T. and Warren, G. (1994) The TGN38 glycoprotein contains two non-overlapping signals that mediate localization to the trans-Golgi Network. J. Cell Biol., 125, 253-268.
35. Reth, M. (1992) Antigen receptors on B lymphocytes. Annu. Rev. Immunol., 10, 97-121.
36. Rock, K.L., Benacerraf, B. and Abbas, A.K. (1984) Antigen presentation by hapten-specific B lymphocytes. I. Role of surface immunoglobulin receptors. J. Exp. Med., 160, 1102-1113.
37. Sanchez, M., Misulovin, Z., Burkhardt, A.L., Mahajan, S., Costa, T., Franke, R., Bolen, J.B. and Nussenzweig, M. (1993) Signal transduction by immunoglobulin is mediated through Iga and Igβ. J. Exp. Med., 178, 1049-1055.
38. Sanderson, F., Kleijmeer, M.J., Kelly, A., Verwoerd, D., Tulp, A., Neefjes, J.J., Geuze, H.I. and Trowsdale, J. (1994) Accumulation of HLA-DM, a regulator of antigen presentation, in MHC class II compartments. Science, 266, 1566-1569.
39. Sauter, M.M. et al. (1996) An internalization signal in the Simian Immunodeficiency Virus transmembrane protein cytoplasmic domain modulates expression of envelope glycoproteins on the cell surface. J. Cell Biol., 132, 795-811.
40. Shaw, A.C., Mitchell, R.N., Weaver, Y.K., Campos-Torres, J., Abbas, A.K. and Leder, P. (1990) Mutations of immunoglobulin transmembrane and cytoplasmic domains: effects on intracellular signalling and antigen presentation. Cell. 63, 381-392.
41. Sun, L.K., Liou, R.S., Sun, N.C., Gossett, L.A., Sun, C. Davis, F.M., MacGlashan, D.W., Jr and Chang, T.W. (1991) Transfectomas expressing both secreted and membrane-bound forms of chimeric IgE with anti-viral specificity. J. Immunol., 146, 199-205.
42. Swier, K. and Miller, J. (1995) Efficient internalization of MHC class II-invariant chain complexes is not sufficient for invariant chain proteolysis and class II antigen presentation. J. Immunol., 155, 630-643.
43. Torres, R.M., Flaswinkel, H., Reth, M. and Rajewsky, K. (1996) Aberrant B cell development and immune response in mice with a compromised BCR complex. Science, 272, 1804-1808.
44. Trowbridge, I.S., Collawn, J.F. and Hopkins, C.R. (1993) Signal-dependent membrane protein trafficking in the endocytic pathway. Annu. Rev. Cell Biol. 9, 129-161.
45. Tulp, A., Verwoerd, B., Dobberstein, B., Ploegh, H.L. and Pieters, J. (1994) Isolation and characterization of the intracellular MHC class II compartment. Nature, 369, 120-126.
46. van Noesel,C.J.M., Brouns, G.S., van Schijndel, G.M.W., Bende, R.J., Mason, D.Y., Borst, J. and van Lier, R.A.W. (1992) Comparison of human B cell antigen receptor complexes: membrane-expressed forms of immunoglobulin (Ig)M, IgD, and IgG are associated with structurally related heterodimers. J. Exp. Med., 175, 1511-1519.
47. Venkitaraman, A.R., Williams, G.T., Dariavach, P. and Neuberger, M.S. (1991) The B-cell antigen receptor of the five immunoglobulin classes Nature, 352, 777-781.
48. Verschuren, M.C., Comans-Bitter, W.M., Kapteijn, C.A., Mason, D.Y., Brouns, G.S., Borst, J., Drexler, H.G. and van Dongen, J.J.M. (1993) Transcription and protein expression of mb-1 and B29 genes in human hematopoietic malignancies and cell lines. J. Leukemia, 7, 1939-1947.
49. Watts, C. (1997) Capture and processing of exogenous antigens for presentation on MHC molecules. Annu. Rev. Immunol., 15, 821-850.
50. Watts, C. and Davidson, H.W. (1988) Endocytosis and recycling of specific antigen by human B cell lines. EMBO J., 7, 1937-1945
51. Weiser, R. Riesterer, C. and Reth, M. (1994) The internalization of the IgG2a antigen receptor does not require the association with Igα and Igβ but the activation of protein tyrosine kinases does Eur. J. Immunol., 24, 665-671.
52. West, M.A., Lucocq, J.M. and Watts, C. (1994) Antigen processing and class II MHC peptide-loading compartments in human B-lymphoblastoid cells. Nature, 369, 147-151.
53. Williams, G.T., Venkitaraman, A.R., Gilmore, D.J. and Neuberger, M.S. (1990) The sequence of the μ transmembrane segment determines the tissue specificity of the transport of immunoglobulin M to the cell surface. J. Exp. Med., 171, 947-952.
54. Williams, G.T., Peaker, C.J., Patel, K.J. and Neuberger, M.S. (1994) The alpha/beta sheath and its cytoplasmic tyrosines are required for signaling by the B-cell antigen receptor but not for capping or for serine/threonine-kinase recruitment. Proc. Natl Acad. Sci. USA, 91, 474-478.
55. Yon, J. and Fried, M. (1989) Precise gene fusion by PCR. Nucleic Acids Res., 17, 4895.