Invariant chain-induced B cell differentiation requires intramembrane proteolytic release of the cytosolic domain

Immunity

Volumn 17, Issue 5, 2002, Pages 549-560

  Matza, Didi ^a   Kerem, Anat ^a   Medvedovsky, Helena ^a   Lantner, Frida ^a   Shachar, Idit ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MEMBRANE PROTEIN;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; CELL DIVISION; CELL MATURATION; CONTROLLED STUDY; CYTOSOLIC FRACTION; HUMAN; HUMAN CELL; LYMPHOCYTE MEMBRANE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

EID: 0036849769     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-7613(02)00455-7     Document Type: Article

References (41)

1. Agami R., Bernards R. Distinct initiation and maintenance mechanisms cooperate to induce G1 cell cycle arrest in response to DNA damage. Cell. 109:2000;55-66.
2. Anderson K.S., Cresswell P. A role for calnexin (IP90) in the assembly of class II MHC molecules. EMBO J. 13:1994;675-682.
3. Bakke O., Dobberstein B. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell. 63:1990;707-716.
4. Brown M.S., Goldstein J.L. The SREBP pathway. regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor Cell. 89:1997;331-340.
5. Cooper K.F., Mallory M.J., Smith J.B., Strich R. Stress and developmental regulation of the yeast C-type cyclin Ume3p (Srb11p/Ssn8p). EMBO J. 16:1997;4665-4675.
6. Cresswell P. Assembly, transport, and function of MHC class II molecules. Annu. Rev. Immunol. 12:1994;259-293.
7. Duncan E.A., Brown M.S., Goldstein J.L., Sakai J. Cleavage site for sterol-regulated protease localized to a leu-Ser bond in the lumenal loop of sterol regulatory element-binding protein-2. J. Biol. Chem. 272:1997;12778-12785.
8. Erickson A.H., Blobel G. Early events in the biosynthesis of the lysosomal enzyme cathepsin D. J. Biol. Chem. 254:1979;11771-11774.
9. Flaishon L., Hershkovitz R., Lantner F., Lider O., Alon R., Levo Y., Flavell R.A., Shachar I. Autocrine secretion of interferon γ negatively regulates homing of immature B cells. J. Exp. Med. 192:2000;1381-1387.
10. Frauwirth K., Shastri N. Mutation of the invariant chain transmembrane region inhibits II degradation, prolongs association with MHC class II, and selectively disrupts antigen presentation. Cell. Immunol. 209:2001;97-108.
11. Hammond C., Denzin L.K., Pan M., Griffith J.M., Geuze H.J., Cresswell P. The tetraspan protein CD82 is a resident of MHC class II compartments where it associates with HLA-DR, -DM, and -DO molecules. J. Immunol. 161:1998;3282-3291.
12. Harding C.V., Unanue E.R. Cellular mechanisms of antigen processing and the function of class I and II major histocompatibility complex molecules. Cell Regul. 1:1990;499-509.
13. Haze K., Yoshida H., Yanagi H., Yura T., Mori K. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell. 10:1999;3787-3799.
14. Hoppe T., Rape M., Jentsch S. Membrane-bound transcription factors. regulated release by RIP or RUP Curr. Opin. Cell Biol. 13:2001;344-348.
15. Kenty G., Bikoff E.K. BALB/C invariant chain mutant mice display relatively efficient maturation of CD4+ T cell in the periphery and secondary proliferative responses elicited upon peptide challenge. J. Immunol. 163:1999;232-242.
16. Kenty G., Martin W.D., Van Kaer L., Bikoff E.K. MHC class II expression in double mutant mice lacking invariant chain and DM functions. J. Immunol. 160:1998;606-614.
17. Lamb C.A., Yewdell J.W., Bennink J.R., Cresswell P. Invariant chain targets HLA class II molecules to acidic endosomes containing internalized influenza virus. Proc. Natl. Acad. Sci. USA. 88:1991;5998-6002.
18. Lipp J., Dobberstein B. The membrane-spanning segment of invariant chain (I gamma) contains a potentially cleavable signal sequence. Cell. 46:1986;1103-1112.
19. Loder F., Mutschler B., Ray R.J., Paige C.J., Sideras P., Torres R., Lamers M.C., Carsetti R. B cell development in the spleen takes place in discrete steps and is determined by the quality of B cell receptor-derived signals. J. Exp. Med. 190:1999;75-90.
20. Long E.O. Intracellular traffic and antigen processing. Immunol. Today. 10:1989;232-234.
21. Lotteau V., Teyton L., Peleraux A., Nilsson T., Karlsson L., Schmid S.L., Quaranta V., Peterson P.A. Intracellular transport of class II MHC molecules directed by invariant chain. Nature. 348:1990;600-605.
22. Marks M.S., Blum J.S., Cresswell P. Invariant chain trimers are sequestered in the rough endoplasmic reticulum in the absence of association with HLA class II antigens. J. Cell Biol. 111:1990;839-855.
23. Matza D., Wolstein O., Dikstein R., Shachar I. Invariant chain induces B cell maturation by activating TAFII105-NF-kB-dependent transcription program. J. Biol. Chem. 276:2001;27203-27206.
24. Matza D., Lantner D., Bogoch Y., Flaishon L., Hershkoviz R., Shachar I. Invariant chain induces B cell maturation in a process which is independent of its chaperonic activity. Proc. Natl. Acad. Sci. USA. 99:2002;3018-3023.
25. Neefjes J.J., Stollorz V., Peters P.J., Geuze H.J., Ploegh H.L. The biosynthetic pathway of MHC class II but not class I molecules intersects the endocytic route. Cell. 61:1990;171-183.
26. Niwa M., Sidrauski C., Kaufman R.J., Walter P. A role for presenilin-1 in nuclear accumulation of Ire1 fragments and induction of the mammalian unfolded protein response. Cell. 99:1999;691-702.
27. Odorizzi C.G., Trowbridge I.S., Xue L., Hopkins C.R., Davis C.D., Collawn J.F. Sorting signals in the MHC class II invariant chain cytoplasmic tail and transmembrane region determine trafficking to an endocytic processing compartment. J. Cell Biol. 126:1994;317-330.
28. Pieters J., Bakke O., Dobberstein B. The MHC class II-associated invariant chain contains two endosomal targeting signals within its cytoplasmic tail. J. Cell Sci. 106:1993;831-846.
29. Pond L., Kuhn L.A., Teyton L., Schutze M.P., Tainer J.A., Jackson M.R., Peterson P.A. A role for acidic residues in di-leucine motif-based targeting to the endocytic pathway. J. Biol. Chem. 270:1995;19989-19997.
30. Roche P.A., Cresswell P. Proteolysis of the class II-associated invariant chain generates a peptide binding site in intracellular HLA-DR molecules. Proc. Natl. Acad. Sci. USA. 88:1991;3150-3154.
31. Roche P.A., Marks M.S., Cresswell P. Formation of a nine-subunit complex by HLA class II glycoproteins and the invariant chain. Nature. 354:1991;392-396.
32. Romagnoli P., Layet C., Yewdell J., Bakke O., Germain R.N. Relationship between invariant chain expression and major histocompatibility complex class II transport into early and late endocytic compartments. J. Exp. Med. 177:1993;583-596.
33. Schagger H., von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:1987;368-379.
34. Shachar I., Flavell R.A. Requirement for invariant chain in B cell maturation and function. Science. 274:1996;106-108.
35. Shachar I., Elliot E.A., Chasnoff B., Grewal I.S., Flavell R.A. Reconstitution of invariant chain function in transgenic mice in vivo by individual p31 and p41 isoform. Immunity. 3:1995;373-383.
36. Stang E., Bakke O. MHC class II-associated invariant chain-induced enlarged endosomal structures. a morphological study Exp. Cell Res. 235:1997;79-92.
37. Stumptner-Cuvelette P., Benaroch P. Multiple roles of the invariant chain in MHC class II function. Biochim. Biophys. Acta. 1542:2002;1-13.
38. Unanue E.R. Antigen-presenting function of the macrophage. Annu. Rev. Immunol. 2:1984;395-428.
39. Wang X., Sato R., Brown M.S., Hua X., Goldstein J.L. SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis. Cell. 77:1994;53-62.
40. Weinmaster G. Notch signal transduction. a real rip and more Curr. Opin. Genet. Dev. 10:2000;363-369.
41. Zur A., Brandeis M. Securin degradation is mediated by fzy and fzr, and is required for complete chromatid separation but not for cytokinesis. EMBO J. 20:2001;792-801.