Presenilin/γ-secretase and α-secretase-like peptidases cleave human MHC Class I proteins

Biochemical Journal

Volumn 401, Issue 1, 2007, Pages 121-127

  Carey, Bryce W ^a   Kim, Doo Y ^a   Kovacs, Dora M ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

and secretases; A disintegrin and metalloproteinase (ADAM); Human leucocyte antigen; Matrix metalloproteinase (MMP); MHC class I; Presenilin

Indexed keywords

BIODEGRADATION; BRAIN; CELL CULTURE; DISEASES; ENZYME KINETICS;

A DISINTEGRIN AND METALLOPROTEINASE (ADAM); HUMAN LEUCOCYTE ANTIGENS; MATRIX METALLOPROTEINASE (MMP); PRESENILIN;

PROTEINS;

ALPHA SECRETASE; GAMMA SECRETASE; GAMMA SECRETASE INHIBITOR; HLA A2 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL LINE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL LINE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; T LYMPHOCYTE;

AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CHO CELLS; CRICETINAE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA-A2 ANTIGEN; HUMANS; IMMUNOHISTOCHEMISTRY; MAJOR HISTOCOMPATIBILITY COMPLEX; PRESENILINS; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY; TRANSFECTION;

CRICETINAE;

EID: 33846322244     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20060847     Document Type: Article

References (40)

1. Schroeter, E. H., Kisslinger, J. A. and Kopan, R. (1998) Notch-1 signalling requites ligand-induced proteolytic release of intracellular domain. Nature 393, 382-386
2. De Strooper, B. (2003) Aph-1, Pen-2, and Nicastrin with Presenilin generate an active gamma-secretase complex. Neuron 38, 9-12
3. Ni, C. Y., Yuan, H. and Carpenter, G. (2003) Role of the ErbB-4 carboxyl terminus in gamma-secretase cleavage. J. Biol. Chem. 278, 4561-4565
4. Marambaud, P., Shioi, J., Serban, G., Georgakopoulos, A., Sarner, S., Nagy, V., Baki, L., Wen, P., Efthimiopoulos, S., Shao, Z. et al. (2002) A presenilin-1/gamma-secretase cleavage releases the E-cadherin intracellular domain and regulates disassembly of adherens junctions. EMBO J. 21, 1948-1956
5. Lammich, S., Okochi, M., Takeda, M., Kaether, C., Capell, A., Zimmer, A. K., Edbauer, D., Walter, J., Steiner, H. and Haass, C. (2002) Presenilin-dependent intramembrane proteolysis of CD44 leads to the liberation of its intracellular domain and the secretion of an A β-like peptide. J. Biol. Chem. 277, 44754-44759
6. Murakami, D., Okamoto, I., Nagano, O., Kawano, Y., Tomita, T., Iwatsubo, T., De Strooper, B., Yumoto, E. and Saya, H. (2003) Presenilin-dependent gamma-secretase activity mediates the intramembranous cleavage of CD44. Oncogene 22, 1511-1516
7. Vidal, G. A., Naresh, A., Marrero, L. and Jones, F. E. (2005) Presenilin-dependent gamma-secretase processing regulates multiple ERBB4/HER4 activities. J. Biol. Chem. 280, 19777-19783
8. Kim, D. Y., Ingano, L. A. and Kovacs, D. M. (2002) Nectin-1alpha, an immunoglobulin-like receptor involved in the formation of synapses, is a substrate for presenilin/gamma-secretase-like cleavage. J. Biol. Chem. 277, 49976-49981
9. Kim, D. Y., Ingano, L. A., Carey, B. W., Pettingell, W. H. and Kovacs, D. M. (2005) Presenilin/gamma-secretase-mediated cleavage of the voltage-gated sodium channel beta2-subunit regulates cell adhesion and migration. J. Biol. Chem. 280, 23251-23261
10. Rosenstein, Y., Ratnofsky, S., Burakoff, S. J. and Hermann, S. H. (1989) Direct evidence for binding of CD8 to HLA class I antigens. J. Exp. Med. 169, 149-160
11. Huppa, J. B. and Davis, M. M. (2003) T-cell-antigen recognition and the immunological synapse. Nat. Rev. Immunol. 3, 973-983
12. Andersson, C. X., Fernandez-Rodriguez, J., Laos, S., Baeckstrom, D., Haass, C. and Hansson, G. C. (2005) Shedding and gamma-secretase-mediated intramembrane proteolysis of the mucin-type molecule CD43. Biochem. J. 387, 377-384
13. Andersson, C. X., Fernandez-Rodriguez, J., Laos, S., Sikut, R., Sikut, A., Baeckstrom, D. and Hansson, G. C. (2004) CD43 has a functional NLS, interacts with beta-catenin, and affects gene expression. Biochem. Biophys. Res. Commun. 316, 12-17
14. Corriveau, R. A., Huh, G. S. and Shatz, C. J. (1998) Regulation of class I MHC gene expression in the developing and mature CNS by neural activity. Neuron 21, 505-520
15. Huh, G. S., Boulanger, L. M., Du, H., Riquelme, P. A., Brotz, T. M. and Shatz, C. J. (2000) Functional requirement for class I MHC in CNS development and plasticity. Science 290, 2155-2159
16. Linda, H., Hammarberg, H., Cullheim, S., Levinovitz, A., Khademi, M. and Olsson, T. (1998) Expression of MHC class I and beta2-microglobulin in rat spinal motoneurons: regulatory influences by IFN-gamma and axotomy. Exp. Neurol. 150, 282-295
17. Oliveira, A. L., Thams, S., Lidman, O., Piehl, F., Hokfelt, T., Karre, K., Linda, H. and Cullheim, S. (2004) A role for MHC class I molecules in synaptic plasticity and regeneration of neurons after axotomy. Proc. Natl. Acad. Sci. U.S.A. 101, 17843-17848
18. Story, C. M., Furman, M. H. and Ploegh, H. L. (1999) The cytosolic tail of class I MHC heavy chain is required for its dislocation by the human cytomegalovirus US2 and US11 gene products. Proc. Natl. Acad. Sci. U.S.A. 96, 8516-8521
19. Stam, N. J., Spits, H. and Ploegh, H. L. (1986) Monoclonal antibodies raised against denatured HLA-B locus heavy chains permit biochemical characterization of certain HLA-C locus products. J. Immunol. 137, 2299-2306
20. Parham, P., Barnstable, C. J. and Bodmer, W. F. (1979) Use of a monoclonal antibody (W6/32) in structural studies of HLA-A,B,C, antigens. J. Immunol. 123, 342-349
21. Santos, S. G., Powis, S. J. and Arosa, F. A. (2004) Misfolding of major histocompatibility complex class I molecules in activated T cells allows cis-interactions with receptors and signaling molecules and is associated with tyrosine phosphorylation. J. Biol. Chem. 279, 53062-53070
22. Carreno, B. M. and Hansen, T. H. (1994) Exogenous peptide ligand influences the expression and half-life of free HLA class I heavy chains ubiquitously detected at the cell surface. Eur. J. Immunol. 24, 1285-1292
23. Demaria, S., Schwab, R. and Bushkin, Y. (1992) The origin and fate of beta 2m-free MHC class I molecules induced on activated T cells. Cell. Immunol. 142, 103-113
24. Rein, R. S., Seemann, G. H., Neefjes, J. J., Hochstenbach, F. M., Stam, N. J. and Ploegh, H. L. (1987) Association with beta 2-microglobulin controls the expression of transfected human class I genes. J. Immunol. 138, 1178-1183
25. Chersi, A., Rosano, L. and Tanigaki, N. (2000) Polystyrene beads coated with antibodies directed to HLA class I intracytoplasmic domain: the use in quantitative measurement of peptide-HLA class I binding by flow cytometry. Hum. Immunol. 61, 1298-1306
26. Lammich, S., Okochi, M., Takeda, M., Kaether, C., Capell, A., Zimmer, A. K., Edbauer, D., Walter, J., Steiner, H. and Haass, C. (2002) Presenilin-dependent intramembrane proteolysis of CD44 leads to the liberation of its intracellular domain and the secretion of an Aβ-like peptide. J. Biol. Chem. 277, 44754-44759
27. Boulanger, L. M., Huh, G. S. and Shatz, C. J. (2001) Neuronal plasticity and cellular immunity: shared molecular mechanisms. Curr. Opin. Neurobiol. 11, 568-578
28. Boulanger, L. M. and Shatz, C. J. (2004) Immune signalling in neural development, synaptic plasticity and disease. Nat. Rev. Neurosci. 5, 521-531
29. Domeniconi, M., Zampieri, N., Spencer, T., Hilaire, M., Mellado, W., Chao, M. V. and Filbin, M. T. (2005) MAG induces regulated intramembrane proteolysis of the p75 neurotrophin receptor to inhibit neurite outgrowth. Neuron 46, 849-855
30. Gur, H., el-Zaatari, F., Geppert, T. D., Wacholtz, M. C., Taurog, J. D. and Lipsky, P. E. (1990) Analysis of T cell signaling by class I MHC molecules: the cytoplasmic domain is not required for signal transduction. J. Exp. Med. 172, 1267-1270
31. Gur, H., Geppert, T. D., Wacholtz, M. C. and Lipsky, P. E. (1999) The cytoplasmic and the transmembrane domains are not sufficient for class I MHC signal transduction. Cell. Immunol. 191, 105-116
32. Gur, H., Geppert, T. D. and Lipsky, P. E. (1997) Structural analysis of class I MHC molecules: the cytoplasmic domain is not required for cytoskeletal association, aggregation and internalization. Mol. Immunol. 34, 125-132
33. Skov, S., Odum, N. and Claesson, M. H. (1995) MHC class I signaling in T cells leads to tyrosine kinase activity and PLC-γ1 phosphorylation. J. Immunol. 154, 1167-1176
34. Skov, S., Nielsen, M., Bregenholt, S., Odum, N. and Claesson, M. H. (1998) Activation of Stat-3 is involved in the induction of apoptosis after ligation of major histocompatibility complex class I molecules on human Jurkat T cells. Blood 91, 3566-3573
35. Skov, S., Bregenholt, S. and Claesson, M. H. (1997) MHC class I ligation of human T cells activates the ZAP70 and p56lck tyrosine kinases, leads to an alternative phenotype of the TCR/CD3 zeta-chain, and induces apoptosis. J. Immunol. 158, 3189-3196
36. Lamberth, K. and Claesson, M. H. (2001) Ligation of major histocompatibility complex class I antigens (MHC-I) prevents apoptosis induced by Fas or SAPK/JNK activation in T-lymphoma cells. Tissue Antigens 58, 171-180
37. Demaria, S., Schwab, R., Gottesman, S. R. and Bushkin, Y. (1994) Soluble beta 2-microglobulin-free class I heavy chains are released from the surface of activated and leukemia cells by a metalloprotease. J. Biol. Chem. 269, 6689-6694
38. Demaria, S., DeVito-Haynes, L. D., Salter, R. D., Burlingham, W. J. and Bushkin, Y. (1999) Peptide-conformed beta2m-free class I heavy chains are intermediates in generation of soluble HLA by the membrane-bound metalloproteinase. Hum. Immunol. 60, 1216-1226
39. Lorenzo, M. E., Jung, J. U. and Ploegh, H. L. (2002) Kaposi's sarcoma-associated herpesvirus K3 utilizes the ubiquitin-proteasome system in routing class major histocompatibility complexes to late endocytic compartments. J. Virol. 76, 5522-5531
40. Schulz, J. G., Annaert, W., Vandekerckhove, J., Zimmermann, P., De Strooper, B. and David, G. (2003) Syndecan 3 intramembrane proteolysis is presenilin/γ-secretase-dependent and modulates cytosolic signaling. J. Biol. Chem. 278, 48651-48657