Polarized transport of MHC class II molecules in Madin-Darby canine kidney cells is directed by a leucine-based signal in the cytoplasmic tail of the β-chain

Journal of Immunology

Volumn 163, Issue 5, 1999, Pages 2540-2548

  Simonsen, Anne ^a,c   Pedersen, Ketil Whither ^a   Nordeng, Tommy W ^a   Von Der Lippe, Alexander ^a   Stang, Espen ^a,c   Long, Eric O ^b   Bakke, Oddmund ^a,d  

^a UNIVERSITY OF OSLO   (Norway)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

^d National Hospital ^*  (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

HLA DR ANTIGEN; HYBRID PROTEIN; LEUCINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PHENYLALANINE;

ANIMAL CELL; ANTIGEN PRESENTATION; ARTICLE; CELL CLONE; CELL MEMBRANE; CELL SELECTION; ENDOSOME; GENETIC TRANSFECTION; INFLUENZA VIRUS; INTERNALIZATION; KIDNEY CELL; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

AMINO ACID SEQUENCE; ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; BIOLOGICAL TRANSPORT; CELL COMPARTMENTATION; CELL LINE; CELL MEMBRANE; CELL POLARITY; CYTOPLASM; DOGS; ENDOSOMES; HISTOCOMPATIBILITY ANTIGENS CLASS II; HLA-D ANTIGENS; HLA-DR1 ANTIGEN; HUMANS; KIDNEY; LEUCINE; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 0033197976     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. Kelley, V. R., and G. G. Singer. 1993. The antigen presentation function of renal tubular epithelial cells. Exp. Nephrol. 1:102.
2. Mayrhofer, G. 1995. Absorption and presentation of antigens by epithelial cells of the small intestine: hypotheses and predictions relating to the pathogenesis of coeliac disease. Immunol. Cell Biol. 73:433.
3. Bakke, O., and B. Dobberstein. 1990. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 63:707.
4. Lotteau, V., L. Teyton, A. Peleraux, T. Nilsson, L. Karlsson, S. L. Schmid, V. Quaranta, and P. A. Peterson. 1990. Intracellular transport of class II MHC molecules directed by invariant chain. Nature 348:600.
5. Simonsen, A., F. Momburg, J. Drexler, G. J. Hämmerling, and O. Bakke. 1993. Intracellular distribution of the MHC class II molecules and the associated invariant chain (Ii) in different cell lines. Int. Immunol. 5:903.
6. Bremnes, B., T. Madsen, M. Gedde-Dahl, and O. Bakke. 1994. An LI and ML motif in the cytoplasmic tail of the MHC-associated invariant chain mediate rapid internalization. J. Cell Sci. 107:2021.
7. Busch, R., and E. D. Mellins. 1996. Developing and shedding inhibitions: how MHC class II molecules reach maturity. Curr. Opin. Immunol. 8:51.
8. Nordeng, T. W., J.-P. Gorvel, and O. Bakke. 1998. Intracellular transport of molecules engaged in the presentation of exogenous antigen. Curr. Top. Microb. Immunol. 232:179.
9. Harding, C. V., and E. R. Unanue. 1989. Antigen processing and intracellular Ia: possible roles of endocytosis and protein synthesis in Ia function. J. Immunol. 142:12.
10. Pinet, V., M. S. Malnati, and E. O. Long. 1994. Two processing pathways for the MHC class II-restricted presentation of exogenous influenza virus antigen. J. Immunol. 152:4852.
11. Pinet, V., M. Vergelli, R. Martin, O. Bakke, and E. O. Long. 1995. Antigen presentation mediated by recycling of surface HLA-DR molecules. Nature 375: 603.
12. Pinet, V. M., and E. O. Long. 1998. Peptide loading onto recycling HLA-DR molecules occurs in early endosomes. Eur. J. Immunol. 28:799.
13. Zhong, G. M., P. Romagnoli, and R. N. Germain. 1997. Related leucine-based cytoplasmic targeting signals in invariant chain and major histocompatibility complex class II molecules control endocytic presentation of distinct determinants in a single protein. J. Exp. Med. 185:429.
14. Van Eijkeren, M. A., P. J. Peters, and H. J. Geuze. 1991. Polarized expression of major histocompatibility complex class I molecules in human endometrial and endocervical epithelial cells. Eur. J. Immunol. 21:3049.
15. Boudier, J. A., J. Fantini, C. Gerard, and B. Verrier. 1993. Polarized distribution of γ interferon-stimulated MHC antigens and transferrin receptors in a clonal cell line isolated from Fisher rat thyroid (FRT cells). Cell Tissue Res. 272:23.
16. Rabenandrasana, C., S. Baghdiguian, J. Marvaldi, and J. Fantini. 1990. CD4 molecules are restricted to the basolateral membrane domain of in vitro differentiated human colon cancer cells (HT29-D4). FEBS Lett. 265:75.
17. Selby, W. S., G. Janossy, G. Goldstein, and D. P. Jewell. 1981. T lymphocyte subsets in human intestinal mucosa: the distribution and relationship to MHC-derived antigens. Clin. Exp. Immunol. 44:453.
18. Hart, D. N., S. V. Fuggle, K. A. Williams, J. W. Fabre, A. Ting, and P. J. Morris. 1981. Localization of HLA-ABC and DR antigens in human kidney. Transplantation 31:428.
19. Skoskiewicz, M. J., R. B. Colvin, E. E. Schneeberger, and P. S. Russell. 1985. Widespread and selective induction of major histocompatibility complex-determined antigens in vivo by γ interferon. J. Exp. Med. 162:1645.
20. Bland, P. W., and L. G. Warren. 1986. Antigen presentation by epithelial cells of the rat small intestine. I. Kinetics, antigen specificity and blocking by anti-Ia antisera. Immunology 58:1.
21. Sarles, J., J. P. Gorvel, D. Olive, S. Maroux, C. Mawas, and F. Giraud. 1987. Subcellular localization of class 1 (A,B,C) and class II (DR and DQ) MHC antigens in jejunal epithelium of children with coeliac disease. J. Pediatr. Gastroenterol. Nutr. 6:51.
22. Parton, R. G., K. Prydz, M. Bomsel, K. Simons, and G. Griffiths. 1989. Meeting of the apical and basolateral endocytic pathways of the Madin-Darby canine kidney cell in late endosomes. J. Cell Biol. 109:3259.
23. Musch, A., H. X. Xu, D. Shields, and E. Rodriguez-Boulan. 1996. Transport of vesicular stomatitis virus G protein to the cell surface is signal mediated in polarized and nonpolarized cells. J. Cell Biol. 133:543.
24. Yoshimori, T., P. Keller, M. G. Roth, and K. Simons. 1996. Different biosynthetic transport routes to the plasma membrane in BHK and CHO cells. J. Cell Biol. 133:247.
25. Wandinger-Ness, A., M. K. Bennett, C. Antony, and K. Simons. 1990. Distinct transport vesicles mediate the delivery of plasma membrane proteins to the apical and basolateral domains of MDCK cells. J. Cell Biol. 111:987.
26. Mellman, I., E. Yamamoto, J. A. Whitney, M. Kim, W. Hunziker, and K. Matter. 1993. Molecular sorting in polarized and non-polarized cells: common problems, common solutions. J. Cell Sci. 106 (Suppl. 17):1.
27. Mellman, I. 1996. Endocytosis and molecular sorting. Annu. Rev. Cell Biol. 12: 575.
28. Mostov, K. E., and M. H. Cardone. 1995. Regulation of protein traffic in polarized epithelial cells. BioEssays 17:129.
29. Aroeti, B., and K. E. Mostov. 1994. Polarized sorting of the polymeric immunoglobulin receptor in the exocytotic and endocytotic pathways is controlled by the same amino acids. EMBO J. 13:2297.
30. Simonsen, A., E. Stang, B. Bremnes, M. Roe, K. Prydz, and O. Bakke. 1997. Sorting of MHC class II molecules and the associated invariant chain (Ii) in polarized MDCK cells. J. Cell Sci. 110:597.
31. Lampson, L. A., and R. Levy. 1980. Two populations of Ia-like molecules on a human B cell line. J. Immunol. 125:293.
32. Wraight, C. J., P. van Endert, P. Moller, J. Lipp, N. R. Ling, I. C. MacLennan, N. Koch, and G. Moldenhauer. 1990. Human major histocompatibility complex class II invariant chain is expressed on the cell surface. J. Biol. Chem. 265:5787.
33. van Genderen, I. L., G. van Meer, J. W. Slot, H. J. Geuze, and W. F. Voorhout. 1991. Subcellular localization of Forssman glycolipid in epithelial MDCK cells by immuno-electron microscopy after freeze-substitution. J. Cell Biol. 115:1009.
34. Karp, D. R., and E. O. Long. 1992. Identification of HLA-DR1 β chain residues critical for binding staphylococcal enterotoxins A and E. J. Exp. Med. 175:415.
35. Kunkel, T. A., J. D. Roberts, and R. A. Zakour. 1987. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154:367.
36. Long, E. O., S. Rosen-Bronson, D. R. Karp, M. Malnati, R. P. Sekaly, and D. Jaraquemada. 1991. Efficient cDNA expression vectors for stable and transient expression of HLA-DR in transfected fibroblast and lymphoid cells. Hum. Immunol. 31:229.
37. Wigler, M., A. Pellicer, S. Silverstein, R. Axel, G. Urlaub, and L. Chasin. 1979. DNA-mediated transfer of the adenine phosphoribosyltransferase locus into mammalian cells. Proc. Natl. Acad. Sci. USA 76:1373.
38. Balcarova-Stander, J., S. E. Pfeiffer, S. D. Fuller, and K. Simons. 1984. Development of cell surface polarity in the epithelial Madin-Darby canine kidney (MDCK) cell line. EMBO J. 3:2687.
39. Urban, J., K. Parczyk, A. Leutz, M. Kayne, and C. Kondor-Koch. 1987. Constitutive apical secretion of an 80-kD sulfated glycoprotein complex in the polarized epithelial Madin-Darby canine kidney cell line. J. Cell Biol. 105:2735.
40. Berod, A., B. K. Hartman, and J. F. Pujol. 1981. Importance of fixation in immunohistochemistry: use of formaldehyde solutions at variable pH for the localization of tyrosine hydroxylase. J. Histochem. Cytochem. 29:844.
41. Roth, J. 1983. The colloidal gold marker system for light and electron microscopic cytochemistry. In Techniques in Immunocytochemistry 2. G. R. Bullock and P. Petrusz, eds. Academic Press, London, p. 217.
42. Griffiths, G., K. Simons, G. Warren, and K. T. Tokuyasu. 1983. Immunoelectron microscopy using thin, frozen sections: application to studies of the intracellular transport of Semliki Forest virus spike glycoproteins. Methods Enzymol. 96:466.
43. 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.
44. Gorvel, J.-P., J.-M. Escola, E. Stang, and O. Bakke. 1995. Invariant chain induces a delayed transport from early to late endosomes. J. Biol. Chem. 270:2741.
45. Copier, J., M. J. Kleijmeer, S. Ponnambalam, V. Oorschot, P. Potter, J. Trowsdale, and A. Kelly. 1996. Targeting signal and subcellular compartments involved in the intracellular trafficking of HLA-DMB. J. Immunol. 157:1017.
46. Marks, M. S., P. A. Roche, E. Van Donselaar, L. Woodruff, P. J. 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.
47. Lindstedt, R., M. Liljedahl, A. Peleraux, P. A. Peterson, and L. Karlsson. 1995. The MHC class II molecule H2-M is targeted to an endosomal compartment by a lyrosine-based targeting motif. Immunity 3:561.
48. Hershberg, R. M., D. H. Cho, A. Youakim, M. B. Bradley, J. S. Lee, P. E. Framson, and G. T. Nepom. 1998. Highly polarized HLA class II antigen processing and presentation by human intestinal epithelial cells. J. Clin. Invest. 102:792.
49. Nabavi, N., Z. Ghogawala, A. Myer, I. J. Griffith, W. F. Wade, Z. Z. Chen, D. J. McKean, and L. H. Glimcher. 1989. Antigen presentation abrogated in cells expressing truncated Ia molecules. J. Immunol. 142:1444.
50. St-Pierre, Y., N. Nabavi, Z. Ghogawala, L. H. Glimcher, and T. H. Watts. 1989. A functional role for signal transduction via the cytoplasmic domains of MHC class II proteins. J. Immunol. 143:808.
51. Smiley, S. T., T. M. Laufer, D. Lo, L. H. Glimcher, and M. J. Grusby. 1995. Transgenic mice expressing MHC class II molecules with truncated αβ cytoplasmic domains reveal signaling-independent defects in antigen presentation. Int. Immunol. 7:665.
52. Smiley, S. T., A. Y. Rudensky, L. H. Glimcher, and M. J. Grusby. 1996. Truncation of the class II β-chain cytoplasmic domain influences the level of class II invariant chain-derived peptide complexes. Proc. Natl. Acad. Sci. USA 93:241.
53. Simonsen, A., B. Bremnes, T. W. Nordeng, and O. Bakke. 1998. The leucine-based motif (DDQxxLI) is recognized both for internalization and basolateral sorting of invariant chain in MDCK cells. Eur. J. Cell Biol. 76:25.
54. 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.
55. Bénaroch, P., M. Yilla, G. Raposo, K. Ito, K. Miwa, H. J. Geuze, and H. L. Ploegh. 1995. How MHC class II molecules reach the endocytic pathway. EMBO J. 14:37.
56. Sant, A. J., and J. Miller. 1994. MHC class II antigen processing: biology of invariant chain. Curr. Opin. Immunol. 6:57.
57. Nordeng, T. W., and O. Bakke. 1994. The biological role of invariant chain (Ii) in MHC class II antigen presentation. Immunol. Lett. 43:47.
58. Chervonsky, A. V., L. Gordon, and A. J. Sant. 1994. A segment of the MHC class II β chain plays a critical role in targeting class II molecules to the endocytic pathway. Int. Immunol. 6:973.
59. Tan, L. J., S. Ceman, A. Chervonsky, J. Rodriguez-Paris, T. L. Steck, and A. J. Sant. 1997. Late events in the intracellular sorting of major histocompatibility complex class II molecules are regulated by the 80-82 segment of the class II β chain. Eur. J. Immunol. 27:1479.
60. Apodaca, G., L. A. Katz, and K. E. Mostov. 1994. Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes. J. Cell Biol. 125:67.
61. Peters, P. J., G. Raposo, J. J. Neefjes, V. Oorschot, R. L. Leijendekker, 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.
62. 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 lymphocytes. Nature 369:113.
63. Kleijmeer, M. J., S. Morkowski, J. M. Griffith, A. Y. Rudensky, and H. J. Geuze. 1997. Major histocompatibility complex class II compartments in human and mouse B lymphoblasts represent conventional endocytic compartments. J. Cell Biol. 139:639.
64. 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 266:1566.
65. Pierre, P., L. K. Denzin, C. Hammond, J. R. Drake, S. Amigorena, P. Cresswell, and I. Mellman. 1996. HLA-DM is localized to conventional and unconventional MHC class II-containing endocytic compartments. Immunity 4:229.
66. Stang, E., C. B. Guerra, M. Amaya, Y. Paterson, O. Bakke, and E. D. Mellins. 1998. DR/CLIP (class II-associated invariant chain peptides) and DR/peptide complexes colocalize in prelysosomes in human B lymphoblastoid cells. J. Immunol. 160:4696.