The biogenesis of the MHC class II compartment in human I-cell disease B lymphoblasts

Journal of Cell Biology

Volumn 132, Issue 5, 1996, Pages 769-785

  Glickman, Jonathan N ^a   Morton, Phillip A ^b   Slot, Jan W ^c   Kornfeld, Stuart ^a   Geuze, Hans J ^c  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MONSANTO COMPANY   (United States)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN D; CELL MARKER; LYSOSOME ENZYME; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MANNOSE 6 PHOSPHATE; SOMATOMEDIN B RECEPTOR;

ANTIGEN PRESENTING CELL; ARTICLE; CELL LABELING; ENZYME ACTIVITY; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; LYSOSOME; MAJOR HISTOCOMPATIBILITY COMPLEX; MUCOLIPIDOSIS TYPE 2; PRIORITY JOURNAL; PROTEIN DEGRADATION;

ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; B-LYMPHOCYTES; BIOLOGICAL TRANSPORT; CATHEPSIN D; CELL COMPARTMENTATION; CELL LINE; CLATHRIN; COATED VESICLES; ENDOCYTOSIS; GLYCOPROTEINS; GOLGI APPARATUS; HEMATOPOIETIC STEM CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; INTRACELLULAR MEMBRANES; LYSOSOMES; MUCOLIPIDOSES; PEPSINOGENS;

EID: 0029978280     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.132.5.769     Document Type: Article

References (95)

1. Ahle, S., A. Mann, U. Eichelsberger, and E. Ungewickell. 1988 Structural relationships between clathrin assembly proteins from the Golgi and the plasma membrane. EMBO (Eur Mol. Biol. Organ.) J. 4:919-929.
2. Allan, V.J., and T.E. Kreis. 1986. A microtubule-binding protein associated with membranes of the Golgi apparatus. J. Cell Biol 103:2229-2239.
3. Amigorena, S., J.R. Drake, P. Webster, and I. Mellman. 1994 Transient accumulation of new class II MHC molecules in a novel endocytic compartment in B lymphoctes. Nature (Lond). 369.113-120
4. Anderson, M.S., and J. Miller. 1992. Invariant chain can function as a chaperon protein for class II major histocompatibility complex molecules. Proc. Natl. Acad. Sci USA. 89:2282-2286.
5. Balch, W.E., W G. Dunphy, W A. Braell, and J.E. Rothman. 1984. Reconstitution of the transport of protein between successive compartments of the Golgi measured by the coupled incorporation of N-acetylglucosamine. Cell. 39:405-416.
6. Bakke, O , and B. Dobberstein 1990. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments Cell 63:707-716.
7. Baranski, T.J., P.L. Faust, and S. Kornfeld 1990. Generation of a lysosomal targeting signal in the secretory protein pepsinogen. Cell 63:281-291.
8. Barnes, K.A , and R N. Mitchell. 1995. Detection of functional class II-associated antigen: role of a low density endosomal compartment in antigen processing. J. Exp. Med 181:1715-1727.
9. Benaroch, P., M. Yilla, G. Raposo, K Ito, K Miwa, H.J. Geuze, and H.L. Pleogh 1995. How MHC class II molecules reach the endocytic pathway. EMBO (Eur. Mol. Biol. Organ.) J. 14:37-49.
10. Bischoff, J., and R. Kornfeld 1984. The effect of 1-deoxymannojirimycin on rat liver α-mannosidases Biochem. Biophys Res. Commun. 125:324-331.
11. Bleekemolen, J.E., M. Stein, K. von Figura, J.W. Slot, and H.J. Geuze. 1988. The two mannose 6-phosphate receptors have almost identical subcellular distributions in U937 monocytes. Eur. J. Cell Biol. 47:366-372.
12. Brown, W.J. 1990. Cation-independent mannose 6-phosphate receptors are concentrated in trans Golgi elements in normal and I-cell disease fibroblasts. Eur. J. Cell Biol. 51:201-218.
13. Calafat, J , M. Nijenhuis, H. Janssen, A. Tulp, S. Dussetjee, R Wubbolts, and J. Neefjes 1994 Major histocompatibility complex class II molecules induce the formation of endocytic MHC-like structures J Cell Biol. 126:967-977
14. Castellino, R. and R.N. Germain. 1995. Extensive trafficking of MHC class II mvariant chain complexes in the endocytic pathway and appearance of peptide-loaded class II in multiple compartments. Immunity 2:73-88
15. Chen, H.J , J. Remmler, J.C. Delaney, D.J. Messner, and P Lobel. 1993. Mutational analysis of the cation-independent mannose 6-phosphate/insulin-like growth factor II receptor. J. Biol. Chem. 268:22338-22346.
16. Claesson-Welsh, L., and P.A. Peterson. 1985. Implication of the invariant chain γ-chain on the intracellular transport of class II histocompatibility antigens. J. Immunol. 135:3551-3558.
17. Cresswell, P 1994. Assembly, transport, and function of MHC class II molecules. Annu. Rev. Immunol 12:259-293.
18. de Curtis, I , and K. Simons 1989. Isolation of exocytic carrier vesicles from BHK cells. Cell. 58,719-727.
19. Denzin, L.K , and P. Cresswell. 1995. HLA-DM induces CLIP dissociation from MHC class II αβ dimers and facilitates peptide loading. Cell. 82.155-165.
20. DiCioccio, R., and A.L. Miller 1991. Biosynthesis, processing, and secretion of α-L-fucosidase in lymphoid cells from patients with I-cell disease and pseudo-Hurler polydystrophy. Glycobiology 1:595-604.
21. Duden, R., G Griffiths, R. Frank, P. Argos, and T.E. Kreis 1991. β-COP, a 100 kd protein associated with non-clathrin-coated vesicles and the Golgi complex, shows homology to β-adaptin. Cell 64:649-665.
22. Elliott, E.A., J.R. Drake, S. Amigorena, J. Elsemore, P. Webstei, I. Mellman, and R A. Flavell 1994. The invariant chain is required for intracellular transport and function of major histocompatibility complex class II molecules. J. Exp. Med. 179.681-694.
23. Geuze, H.J. 1994. A novel lysosomal compartment engaged in antigen presentation. Eur. J Cell Biol. 64:3-6.
24. Geuze, H.J., J.W. Slot, G.J. Strous, A. Hasilik, and K. von Figura. 1985. Possible pathways for lysosomal enzyme delivery. J. Cell Biol. 101:2253-2262.
25. Geuze, H.J., W. Stoorvogel, G J Strous, J.W Slot, J.E Bleekemolen, and I. Mellman 1988. Sorting of mannose 6-phosphate receptors and lysosomal membrane proteins in endocytic vesicles. J Cell Biol. 107:2491-2501.
26. Geuze, H.J., J.W. Slot, and A.L. Schwartz. 1992. The trans-Golgi exits of MPR. In Hepatic Endocytosis of Lipids and Proteins. E Windler and H. Greten, editors. Zuckschwerdt Verlag, NY. 37-43.
27. Gieselmann, V., R. Pohlmann, A. Hasilik, and K. von Figura. 1983. Biosynthesis and transport of cathepsin D in cultured human fibroblasts. J. Cell Biol. 97:1-5.
28. Glickman, J.N., and S. Kornfeld. 1993. Mannose 6-phosphate-independent targeting of lysosomal enzymes in I-Cell Disease B lymphoblasts J. Cell Biol 123:99-108.
29. Goldberg, D.E., and S. Kornfeld. 1983. Evidence for extensive subcellular organization of asparagine-linked oligosaccharide processing and lysosomal enzyme phosphorylation. J. Biol. Chem. 258:3159-3165.
30. Griffiths, G.M , and S. Isaaz. 1993 Granzymes A and B are targeted to the lytic granules of lymphocytes by the mannose 6-phosphate receptor. J. Cell Biol. 120:885-896
31. Griffiths, G , B. Hoflack, K. Simons, I. Mellman, and S. Kornfeld. 1988. The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell. 52: 329-341.
32. Guy, K., V. Van Heyningen, B.B Cohen, D L Deane, and C.M. Steel. 1982. Differential expression and serologically distinct subpopulations of human Ia antigens detected with monoclonal antibodies to the Ia alpha and beta chains. Eur. J. Immunol. 12:942-948.
33. Harding, C.V., and H.J. Geuze. 1992. Class II MHC molecules are present in macrophage lysosomes and phagolysosomes that function in the phagocytic processing of Listeria monocytogenes for presentation to T cells. J. Cell Biol. 119:531-542.
34. Harding, C V , and H.J. Geuze, 1993a. Immunogenic peptides bind to class II MHC molecules in an early lysosomal compartment. J Immunol. 151:3988-3998.
35. Harding, C.V., and H.J. Geuze. 1993b. Antigen processing and intracellular traffic of antigens and MHC molecules. Curr. Opin. Cell Biol 5:596-605.
36. Harding, C V., D.S. Collins, J.W. Slot, H.J. Geuze, and E.R Unanue. 1991. Liposome-encapsuiated antigens are processed in lysosomes, recycled and presented to T cells. Cell. 64:393-401.
37. Hasilik, A., A. Waheed, and K. von Figura. 1981. Enzymatic phosphorylation of lysosomal enzymes in the presence of UDP N-acetylglucosamine: absence of the activity in I-Cell fibroblasts. Biochem Biophys. Res. Commun. 98:761-767.
38. Johnson, K.F., and S. Kornfeld. 1992. The cytoplasmic tail of the mannose 6-phosphate/insulin-like growth factor II receptor has two signals for lysosomal enzyme sorting in the Golgi. J. Cell Biol 119:249-257
39. Kleijmeer, M.J., M.A. Ossevoort, C.J.H. Van Veen, J.J. van Hellemond, J.J. Necfjes, W.M., Kast, C.J.M. Melief, and H.J Geuze. 1995. MHC class II compartments and the kinetics of antigen presentation in activated spleen dendritic cells. J. Immunol. 154(II):5715-5724.
40. Klumperman, J., A. Hille, T. Veenendaal, V. Oorschot, W Stoorvogel, K. von Figura, and H.J. Geuze 1993. Differences in the endosomal distributions of the two mannose 6-phosphate receptors. J. Cell Biol. 121.997-1010
41. Kornfeld, S., and I. Mellman. 1989. The biogenesis of lysosomes. Annu. Rev. Cell Biol. 5:483-525.
42. Laemmli, U K. 1970. Cleavage of structural protein during the assembly of the head of bacteriophage T4. Nature (Lond.), 227:680-685.
43. Lamb, C.A., J.W. Yewdell, J.R. Benninck, and P. Cresswell. 1991. Invariant chain targets HLA class II molecules to acidic endosomes containing internalized influenza virus. Proc. Natl. Acad. Sci. USA. 88:5998-6002.
44. Layet, C., and R.N. Germain. 1991. Invariant chain promotes egress of poorly expressed, haplotype-mismatched class II major histocompatibility complex Aa-Ab dimer from the endoplasmic reticulum/cis-Golgi compartment. Proc. Natl. Acad Sci. USA 88:2346-2350.
45. Letourneur, F , and R.D. Klausner. 1992. A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal enzyme targeting and endocytosis of CD3 chains Cell. 69:1143-1157.
46. Liou, W., and J.W. Slot 1994. Improved fine structure in immunolabeled cryo-sections after modifying the sectioning and pick-up conditions. Proc Int Conf. Electron Microsc pp. 13
47. Little, L.E., M. Alcouloumre, A Drotar, S. Herman, R Robertson, R Y. Yeh, and A.L. Miller. 1987. Properties of N-acetylglucosamine 1-phosphotransferase from human lymphoblasts. Biochem. J. 248:151-159
48. Lotteau, V., L. Teyton, A. Peleraux, T. Nilsson, L. Karlson, S L. Schmid, V. Quaranta, and P.A. Peterson 1990. Intracellular transport of class II MHC molecules directed by invariant chain Nature (Lond.). 348:600-605
49. Ludwig, T , G. Griffiths, and B. Hoflack. 1991. Distribution of newly synthesized lysosomal enzymes in the endocytic pathway of normal rat kidney cells. J Cell Biol 115.1561-1572.
50. Marks, M.S., J.S. Blum, and P. Cresswell. 1990. Invariant chain trimers are sequestered in the rough endoplasmic reticulum in the absence of association with HLA class II antigens. J. Cell Biol. 111:839-855.
51. Marks, M.S., P.A Roche, E. VanDonselaar, L Woodruff, P Peters, and J.S. Bonifacino 1995. A lysosomal targeting signal in the cytoplasmic tail of the β chain directs HLA-DM to MHC class II compartments. J. Cell Biol. 131: 351-369.
52. Mellman, I., P. Pierre, and S. Amigorena. 1995. Lonely MHC molecules seeking immunogenic peptides for meaningful relationship. Curr Opin. Cell Biol. 7: 564-572.
53. Metzelaar, M.J., P.L J. Wijngaard, P J. Peters, J.J Sixma, H.K. Nieuwenhuis, and H.C. Clevers. 1991. CD63 antigen: a novel lysosomal membrane glycoprotein, cloned by a screening method for intracellular antigens in eukaryotic cells. J. Biol. Chem. 266:3239-3245.
54. Mitchell, R.N., K.A. Barnes, S.A. Grupp, M. Sanchez, Z. Misulovin, M.C Nussenzweig, and A.K. Abbas. 1995. Intracellular targeting of antigens internalized by membrane immunoglobulin in B lymphocytes. J. Exp. Med. 181: 1709-1714.
55. Morton, P.A., M.L. Zacheis, K.S Giacoletto, J.A. Manning, and B.D. Schwartz. 1995. Delivery of nascent MHC class II-invariant chain complexes to lysosomal compartments and proteolysis of invariant chain by cysteine proteases precedes peptide binding in B-lymphoblastoid cells. J. Immunol. 154:137-150.
56. Näthke, I., J. Heuser, A. Lupas, J. Stock, C.W. Turck, and F.M. Brodsky. 1992. Folding and trimerization of clathrin subunits at the triskelion hub. Cell. 68: 899-910
57. Neefjes, J J., and H.L. Ploegh. 1992. Inhibition of endosomal proteolytic activity by leupeptin blocks surface expression of MHC class II molecules and their conversion to SDS resistant αβ heterodimers in endosomes. EMBO (Eur. Mol. Biol. Organ) J. 11:411-416.
58. Neefjes, J J., V. Stollorz, P J. Peters, H J. Geuze, and H L. Ploegh. 1990. The biosynthetic pathway of MHC class II but not MHC class I molecules intersects the endocytic route. Cell 61:171-183.
59. Neefjes, J.J., T N.M. Schumacher, and H.L. Plocgh. 1991. Assembly and intracellular transport of major histocompatibility complex molecules. Curr Opin Cell Biol. 3:601-609.
60. Nijman, H.W., M.J. Kleijmeer, M.A. Ossevoort, V.M.J. Dorschot, M.P.M Vierboom, M. van der Keur, P. Kenemans, W.M. Kast, H.J. Geuze, and C.J.M. Melief, 1995. Antigen capture and major histocompatibility class II compartments of freshly isolated and cultured human blood dendritic cells. J Exp. Med. 182:163-174.
61. Odorizzi, C.G., I.S. Trowbridge, L. Xue, C R. Hopkins, C.D. Davis, and J.F. Collawn 1994. Sorting signals in the MHC class II invariant chain cytoplasmic tail and transmembrane region determine trafficking to an endocytic processing compartment J. Cell Biol. 126:317-330.
62. Okada, S., M. Handa, T. Hashimoto, J. Nishimoto, K. Inui, M. Furuyama, J Furuyama, H. Yabuachi, M. Tate, S. Gasa, and A. Makita. 1988. Biochemical studies on lymphoblastoid cells with inherited N-acetylglucosamine 1-phosphotransferase deficiency (I-Cell Disease). Biochem. Int. 17.375-383.
63. Parham, P., C.J. Barnstable, and W F Bodmer. 1979. Use of monoclonal antibody (W6/32) in structural studies of HLA-A,B,C antigens. J. Immunol 123. 342-349.
64. Pearse, B M.F 1982. Coated vesicles from human placenta carry ferritin, transferrin, and immunoglobulin G. Proc Natl. Acad Sci. USA. 79:451-455.
65. Peters, P.J., J.J. Neefjes, V. Oorschot, H L. Ploegh, and H.J. Geuze 1991a. Segregation of MHC class II molecules from MHC class I molecules in the Golgi complex for transport to lysosomal compartments. Nature (Lond.). 349.669-676.
66. Peters, P.J., J. Borst, V Oorschot, M Fukuda, O. Krahenbuhl, J. Tschopp, J.W. Slot, and H.J. Geuze. 1991b. Cytolytic T lymphocyte granules are secretory lysosomes, containing both perform and granzymes. J Exp. Med 173:1099-1109
67. Peters, P.J., G. Raposo, J.J. Neefjes, V. Oorschot, R.L. Leyendekker, H.J. Geuze, and H.L. Ploegh 1995 Major histocompatibility complex class II compartments in human B lymphoblastoid cells are distinct from early endosomes. J Exp. Med 182:325-334.
68. Pieters, J., H Horstmann, O. Bakke, G. Griffiths, and J. Lipp. 1991. Intracellular transport and localization of major histocompatibility complex class II molecules and associated invariant chain. J. Cell Biol 115:1213-1223.
69. Pieters, J.H., O. Bakke, and B. Dobberstein. 1993. The MHC class II-associated invariant chain contains two endosomal targeting signals within its cytoplasmic tail. J. Cell Sci 106:831-846.
70. Pohl, T. 1990. Concentration of proteins and removal of solutes. Methods Enzymol. 182:68-83.
71. Qiu, Y., X. Wu, A. Wandinger-Ness, D.P. Dalke, and S.K Pierce 1994 Separation of subcellular compartments containing distinct functional forms of MHC class II 1994. J. Cell Biol 125.595-605.
72. Raposo, G., H.W. Nijman, W. Stoorvogel, R. Leyendekker, C.V. Harding, C J.N. Meliet, and H.J. Geuze. 1995 B-lymphocytes secrete antigen presenting vesicles. J Exp Med. In press.
73. Reitman, M.L , A.P. Varki, and S. Kornfeld. 1981. Fifaroblasts from patients with I-cell disease and pseudo-Hurler polydystrophy are deficient in UDP-N-acetylglucosamine: glycoprotein N-acetylglucosamine-1-phosphotransferase. J. Clin. Invest. 67:1574-1579.
74. Riberdy, J M., R R. Avva, H.J. Geuze, and P. Cresswell 1994. Transport and intracellular distribution of MHC class II molecules and associated invariant chain in normal and antigen-processing mutant cell lines. J. Cell Biol 125(6): 1225-1237.
75. Robinson, M S. 1987. 100-kD coated vesicle proteins: molecular heterogeneity and intracellular distribution studied with monoclonal antibodies. J. Cell Biol. 104:887-895.
76. Robinson, M S., and T.E. Kreis. 1992. Recruitment of coat proteins onto Golgi membranes in intact and permeabilized cells: effects of brefeldin A and G protein activators. Cell 69:129-138.
77. Roche, P.A., and P. Cresswell. 1991 Proteolysis of the class II-associated invariant chain generates a peptide binding site in intracellular HLA-DR molecules. Proc. Natl. Acad. Sci. USA. 88:3150-3154.
78. Roche, P A., C.L. Teletski, E. Stang, O. Bakke, and E.O. Long 1993. Cell surface HLA-DR-invariant chain complexes are targeted to endosomes by rapid internalization. Proc. Natl Acad Sci. USA 90:8581-8583.
79. Sanderson, F., M J Kleijmeer, A. Kelly, D Verwoerd, A. Tulp, J.J. Neefjes, H.J. Geuze, and J. Trowsdale. 1994. Accumulation of HLA-DM, a regulator of antigen presentation in MHC class II compartments. Science (Wash. DC). 266.1566-1569.
80. r mannose 6-phosphate receptor to the trans-Golgi network. J Cell Biol. 122:541-551.
81. Serafini, T., G. Steinbeck, A. Brecht, F. Lottspeich, L. Orci, J.E. Rothman, and F.T Wieland. 1991 A coat subunit of Golgi-derived non-clathrin-coated vesicles with homology to the clathrin-coated vesicle coat protein β-adaptin. Nature (Lond.). 349.215-220.
82. Sherman, M.A., D A. Weber, and P.E. Jensen. 1995. DM enhances peptide binding to class II MHC by release of invariant chain-derived peptide. Immunity. 3:197-205.
83. Shipp, M A , P. Ahmed, C.C. Kannapell, J.C Ford, D. McCourt, J.F. Leykam, M. Zacheis, C. Bono, J.M. Davie, E. Mustain, et al. 1986 A new ploymorphic determinant on HLA-DQ molecules. Hum. Immunol. 16:24-37.
84. Slot, J.W., and H.J. Geuze. 1985. A new method of preparing gold probes for multiple-labeling cytochemistry. Eur. J. Cell Biol. 38:87-93.
85. Slot, J W., H.J. Geuze, S. Gigengack, G.E. Lienhard, and D.E. James. 1991. Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat. J. Cell Biol 113:123-135.
86. Strubin, M., B. Mach, and E.O. Long. 1984 The complete sequence of the mRNA for the HLA-DR associated invariant chain reveals a polypeptide with an unusual transmembrane polarity EMBO (Eur. Mol. Biol. Organ.) J. 3:869-872
87. Teyton, L., C. O'Sullivan, P.W. Dickson, V. Lotteau, A. Sette, P. Fink, and P.A. Peterson. 1990 Invariant chain distinguishes between the exogenous and endogenous presentation pathways. Nature (Lond). 348:39-44.
88. Tooze, S.A., and W.B. Huttner. 1990. Cell-free protein sorting to the regulated and constitutive secretory pathways. Cell. 60:837-847.
89. Tsuji, A., K Omura, and Y. Suzuki. 1988. I-Cell disease: evidence for a mannose 6-phosphate independent pathway for translocation of lysosomal enzymes in lymphoblastoid cells. Clin. Chim Acta. 176:115-122.
90. Tulp, A., D. Verwoerd, B Dobberstein, H L. Ploegh, and J. Pieters. 1994. Isolation and characterization of the intracellular MHC class II compartment. Nature (Lond). 369:120-126.
91. Viville, S., J. Neefjes, V. Lotteau, A Dierich, M. Lemeur, H. Ploegh, C. Benoist, and D. Mathis. 1993. Mice lacking the MHC class II-associated invariant chain. Cell 72:635.
92. West, M.A., J M. Lucocq, and C. Watts. 1994 Antigen processing and class II MHC peptide-loading compartments in human B lymphoblastoid cells. Nature (Lond) 369:147-151.
93. Woodman, P., and G. Warren. 1991. Isolation of functional, coated, endocytic vesicles. J. Cell Biol 112:1133-1141.
94. Wraight, C.J., P. van Endert, P. Miller, J. Lipp, N.R Ling, I C.M. MacLennan, N. Koch, and G. Moldenhauer. 1990 Human major histocompatibility complex class II invariant chain is expressed at the cell surface. J. Biol. Chem. 265:5787-5792.
95. Xu, X., W. Song, H. Cho, Y. Qiu, and S.K. Pierce. 1995. Intracellular transport of invariant chain - MHC class II complexes to the peptide-loading compartment. J Immunol. 155(6):2984-2992