Shedding of interleukin-6 receptor and tumor necrosis factor α. Contribution of the stalk sequence to the cleavage pattern of transmembrane proteins

European Journal of Biochemistry

Volumn 267, Issue 9, 2000, Pages 2624-2631

  Althoff, Katja ^a   Reddy, Pranitha ^b   Voltz, Nicole ^a   Rose John, Stefan ^a,c   Müllberg, Jürgen ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b AMGEN INC   (United States)

^c UNIVERSITY OF KIEL   (Germany)

Author keywords

Cleavage site; IL 6R; Shedding; TACE; TNF

Indexed keywords

COMPLEMENTARY DNA; INTERLEUKIN 6 RECEPTOR; MEMBRANE PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CELL CLONE; CHIMERA; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBROBLAST; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION;

ADAM PROTEINS; ANIMALS; COS CELLS; FIBROBLASTS; HYDROLYSIS; MEMBRANE PROTEINS; METALLOENDOPEPTIDASES; MICE; RECEPTORS, INTERLEUKIN-6; RECOMBINANT FUSION PROTEINS; SUBSTRATE SPECIFICITY; TETRADECANOYLPHORBOL ACETATE; TUMOR NECROSIS FACTOR-ALPHA;

ANIMALIA;

EID: 0034026325     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.2000.01278.x     Document Type: Article

References (46)

1. 1. Müllberg, J., Schooltink, H., Stoyan, T., Gunther, M., Graeve, L., Buse, G., Mackiewicz, A., Heinrich, P.C. & Rose-John, S. (1993) The soluble interleukin-6 receptor is generated by shedding. Eur. J. Immunol. 23, 473-480.
2. 2. Crowe, P.D., Walter, B.N., Mohler, K.M., Otten Evans, C., Black, R.A. & Ware, C.F. (1995) A metalloprotease inhibitor blocks shedding of the 80-kD TNF receptor and TNF processing in T lymphocytes. J Exp. Med. 181, 1205-1210.
3. 3. Watanabe, N., Nakada, K. & Kobayashi, Y. (1998) Processing and release of tumor necrosis factor alpha. Eur J. Biochem. 253, 576-582.
4. 4. Migaki, G.I., Kahn, J. & Kishimoto, T.K. (1995) Mutational analysis of the membrane-proximal cleavage site of L-selectin: relaxed sequence specificity surrounding the cleavage site. J. Exp. Med. 182, 549-557.
5. 5. Ehlers, M.R., Schwager, S.L., Scholle, R.R., Manji, G.A., Brandt, W.F. & Riordan, J.F. (1996) Proteolytic release of membrane-bound angiotensin-converting enzyme: role of the juxtamembrane stalk sequence. Biochemistry 35, 9549-9559.
6. 6. Lammich, S., Kojro, E., Postina, R., Gilbert, S., Pfeiffer, R., Jasionowski, M., Haass, C. & Fahrenholz, F. (1999) Constitutive and regulated alpha-secretase cleavage of Alzheimer's amyloid precursor protein by a disintegrin metalloprotease. Proc. Natl Acad. Sci. USA 96, 3922-3927.
7. 7. Merlos-Suarez, A. & Arribas, J. (1999) Mechanisms controlling the shedding of transmembrane molecules. Biochem. Soc. Trans. 27, 243-246.
8. 8. Müllberg, J., Rauch, C.T., Wolfson, M.F., Castner, B., Fitzner, J.N., Otten Evans, C., Mohler, K.M., Cosman, D. & Black, R.A. (1997) Further evidence for a common mechanism for shedding of cell surface proteins. FEBS Lett. 401, 235-238.
9. 9. McGeehan, G.M., Becherer, J.D., Bast, R.C. Jr, Boyer, C.M., Champion, B., Connolly, K.M., Conway, J.G., Furdon, P., Karp, S., Kidao, S., McElroy, A.B., Nichols, J., Pryzwanszky, M., Schoenen, F., Sedut, L., Truesdale, A., Verghese, M., Warner, J. & Ways, J.P. (1994) Regulation of tumour necrosis factor-alpha processing by a metalloproteinase inhibitor. Nature 370, 558-561.
10. 10. Gearing, A.J., Beckett, P., Christodoulou, M., Churchill, M., Clements, J., Davidson, A.H., Drummond, A.H., Galloway, W.A., Gilbert, R., Gordon, J.L., Leber, T.M., Mangan, M., Miller, K., Nayee, P., Owen, K., Patel, S., Thomas, W., Wells, G., Wood, L.M. & Woolley, K. (1994) Processing of tumour necrosis factor-alpha precursor by metalloproteinases. Nature 370, 555-557.
11. 11. Mohler, K.M., Sleath, P.R., Fitzner, J.N., Cerretti, D.P., Alderson, M., Kerwar, S.S., Torrance, D.S., Otten Evans, C., Greenstreet, T., Weerawarna, K., Kronheim, S.R., Petersen, M., Gerhart, M., Kozlosky, C.J., March, C.J. & Black, R.A. (1994) Protection against a lethal dose of endotoxin by an inhibitor of tumour necrosis factor processing. Nature 370, 218-220.
12. 12. Arribas, J. & Massague, J. (1995) Transforming growth factor-alpha and beta-amyloid precursor protein share a secretory mechanism. J. Cell Biol. 124, 433-441.
13. 13. Arribas, J., Coodly, L., Vollmer, P., Kishimoto, T.K., Rose-John, S. & Massague, J. (1996) Diverse cell surface protein ectodomains are shed by a system sensitive to metalloprotease inhibitors. J. Biol. Chem. 271, 11376-11382.
14. 14. Aggarwal, B.B., Kohr, W.J., Hass, P.E., Moffat, B., Spencer, S.A., Henzel, W.J., Bringman, T.S., Nedwin, G.E., Goeddel, D.V. & Harkins, R.N. (1985) Human tumor necrosis factor. Production, purification, and characterization. J. Biol. Chem. 260, 2345-2354.
15. 15. Tang, P., Hung, M.C. & Klostergaard, J. (1996) Length of the linking domain of human pro-tumor necrosis factor determines the cleavage processing. Biochemistry 35, 8226-8233.
16. 16. Perez, C., Albert, I., DeFay, K., Zachariades, N., Gooding, L. & Kriegler, M. (1990) A nonsecretable cell surface mutant of tumor necrosis factor (TNF) kills by cell-to-cell contact. Cell 63, 251-258.
17. 17. Müllberg, J., Schooltink, H., Stoyan, T., Heinrich, P.C. & Rose-John, S. (1992) Protein kinase C activity is rate limiting for shedding of the interleukin-6 receptor. Biochem. Biophys. Res. Commun. 189, 794-800.
18. 18. Müllberg, J., Dittrich, E., Graeve, L., Gerhartz, C., Yasukawa, K., Taga, T., Kishimoto, T., Heinrich, P.C. & Rose-John, S. (1993) Differential shedding of the two subunits of the interleukin-6 receptor. FEBS Lett. 332, 174-178.
19. 19. Müllberg, J., Oberthur, W., Lottspeich, F., Mehl, E., Dittrich, E., Graeve, L., Heinrich, P.C. & Rose-John, S. (1994) The soluble human IL-6 receptor. Mutational characterization of the proteolytic cleavage site. J. Immunol. 152, 4958-4968.
20. 20. Müllberg, J., Durie, F.H., Otten Evans, C., Alderson, M.R., Rose-John, S., Cosman, D., Black, R.A. & Mohler, K.M. (1995) A metalloprotease inhibitor blocks shedding of the IL-6 receptor and the p60 TNF receptor. J. Immunol. 155, 5198-5205.
21. 21. Black, R.A., Rauch, C.T., Kozlosky, C.J., Peschon, J.J., Slack, J.L., Wolfson, M.F., Castner, B.J., Stocking, K.L., Reddy, P., Srinivasan, S., Nelson, N., Boiani, N., Schooley, K.A., Gerhart, M., Davis, R., Fitzner, J.N., Johnson, R.S., Paxton, R.J., March, C.J. & Cerretti, D.P. (1997) A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 385, 729-733.
22. 22. Moss, M.L., Jin, S.L., Milla, M.E., Bickett, D.M., Burkhart, W., Carter, H.L., Chen, W.J., Clay, W.C., Didsbury, J.R., Hassler, D., Hoffman, C.R., Kost, T.A., Lambert, M.H., Leesnitzer, M.A., McCauley, P., McGeehan, G., Mitchell, J., Moyer, M., Pahel, G., Rocque, W., Overton, L.K., Schoenen, F., Seaton, T., Su, J.L., Warner, J., Willard, D. & Becherer, J.D. (1997) Cloning of a disintegrin metalloproteinase that processes precursor tumour-necrosis factor-alpha. Nature 385, 733-736.
23. 23. Blobel, C.P. (1997) Metalloprotease-disintegrins: links to cell adhesion and cleavage of TNF alpha and Notch. Cell 90, 589-592.
24. 24. Wolfsberg, T.G., Straight, P.D., Gerena, R.L., Huovila, A.P., Primakoff, P., Myles, D.G. & White, J.M. (1995) ADAM, a widely distributed and developmentally regulated gene family encoding membrane proteins with a disintegrin and metalloprotease domain. Dev. Biol. 169, 278-283.
25. 25. Peschon, J.J., Slack, J.L., Reddy, P., Stocking, K.L., Sunnarborg, S.W., Lee, D.C., Russell, W.E., Castner, B.J., Johnson, R.S., Fitzner, J.N., Boyce, R.W., Nelson, N., Kozlosky, C.J., Wolfson, M.F., Rauch, C.T., Cerretti, D.P., Paxton, R.J., March, C.J. & Black, R.A. (1998) An essential role for ectodomain shedding in mammalian development. Science 282, 1281-1284.
26. 26. Howard, L., Lu, X., Mitchell, S., Griffiths, S. & Glynn, P. (1996) Molecular cloning of MADM: a catalytically active mammalian disintegrin-metalloprotease expressed in various cell types. Biochem. J. 317, 45-50.
27. 27. Rosendahl, M.S., Ko, S.C., Long, D.L., Brewer, M.T., Rosenzweig, B., Hedl, E., Anderson, L., Pyle, S.M., Moreland, J., Meyers, M.A., Kohno, T., Lyons, D. & Lichenstein, H.S. (1997) Identification and characterization of a pro-tumor necrosis factor-alpha-processing enzyme from the ADAM family of zinc metalloproteases. J. Biol. Chem. 272, 24588-24593.
28. 28. Chantry, A., Gregson, N.A. & Glynn, P. (1989) A novel metalloproteinase associated with brain myelin membranes. Isolation and characterization. J. Biol Chem. 264, 21603-21607.
29. 29. Overell, R.W., Weisser, K.E. & Cosman, D. (1988) Stably transmitted triple-promoter retroviral vectors and their use in transformation of primary mammalian cells. Mol Cell Biol. 8, 1803-1808.
30. 30. Stoyan, T., Michaelis, U., Schooltink, H., Van Dam, M., Rudolph, R., Heinrich, P.C. & Rose-John, S. (1993) Recombinant soluble human interleukin-6 receptor. Expression in Escherichia coli, renaturation and purification. Eur. J. Biochem. 216, 239-245.
31. 31. McMahan, C.J., Slack, J.L., Mosley, B., Cosman, D., Lupton, S.D., Brunton, L.L., Grubin, C.E., Wignall, J.M., Jenkins, N.A., Brannan, C.I., Copeland, N.G., Huebner, K., Croce, C.M., Cannizzarro, L.A., Benjamin, D., Dower, S.K., Spriggs, M.K. & Sims, J.E. (1991) A novel IL-1 receptor, cloned from B cells by mammalian expression, is expressed in many cell types. EMBO J. 10, 2821-2832.
32. 32. Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA.
33. 33. Cerretti, D.P. (1999) Characterization of the tumour necrosis factor alpha-converting enzyme, TACE/ADAM17. Biochem. Soc. Trans. 27, 219-223.
34. 34. Massague, J. & Pandiella, A. (1993) Membrane-anchored growth factors. Annu. Rev. Biochem. 62, 515-541.
35. 35. Robache-Gallea, S., Morand, V., Bruneau, J.M., Schoot, B., Tagat, E., Realo, E., Chouaib, S. & Roman-Roman, S. (1995) In vitro processing of human tumor necrosis factor-alpha. J. Biol. Chem. 270, 23688-23692.
36. 36. Arribas, J., Lopez-Casillas, F. & Massague, J. (1997) Role of the juxtamembrane domains of the transforming growth factor-alpha precursor and the beta-amyloid precursor protein in regulated ectodomain shedding. J. Biol. Chem. 272, 17160-17165.
37. 37. Black, R.A. & White, J.M. (1998) ADAMs: focus on the protease domain. Curr. Opin. Cell Biol. 10, 654-659.
38. 38. Maskos, K., Fernandez Catalan, C., Huber, R., Bourenkov, G.P., Bartunik, H., Ellestad, G.A., Reddy, P., Wolfson, M.F., Rauch, C.T., Castner, B.J., Davis, R., Clarke, H.R., Petersen, M., Fitzner, J.N., Cerretti, D.P., March, C.J., Paxton, R.J., Black, R.A. & Bode, W. (1998) Crystal structure of the catalytic domain of human tumor necrosis factor-alpha-converting enzyme. Proc. Natl Acad. Sci. USA 95, 3408-3412.
39. 39. Sadhukhan, R., Sen, G.C., Ramchandran, R. & Sen, I. (1998) The distal ectodomain of angiotensin-converting enzyme regulates its cleavage-secretion from the cell surface. Proc. Natl Acad. Sci. USA 95, 138-143.
40. 40. Sadhukhan, R., Santhamma, K.R., Reddy, P., Peschon, J.J., Black, R.A. & Sen, I. (1999) Unaltered cleavage and secretion of angiotensin-converting enzyme in tumor necrosis factor-alpha-converting enzyme-deficient mice. J. Biol. Chem. 274, 10511-10516.
41. 41. Yamasaki, K., Taga, T., Hirata, Y., Yawata, H., Kawanishi, Y., Seed, B., Taniguchi, T., Hirano, T. & Kishimoto, T. (1988) Cloning and expression of the human interleukin-6 (BSF-2/IFN beta 2) receptor. Science 241, 825-828.
42. 42. Tang, P., Hung, M.C. & Klostergaard, J. (1996) Human pro-tumor necrosis factor is a homotrimer. Biochemistry 35, 8216-8225.
43. 43. Walev, I., Vollmer, P., Palmer, M., Bhakdi, S. & Rose-John, S. (1996) Pore-forming toxins trigger shedding of receptors for interleukin 6 and lipopolysaccharide. Proc. Natl Acad. Sci. USA 93, 7882-7887.
44. 44. Vollmer, P., Walev, I., Rose-John, S. & Bhakdi, S. (1996) Novel pathogenic mechanism of microbial metalloproteinases: liberation of membrane-anchored molecules in biologically active form exemplified by studies with the human interleukin-6 receptor. Infect. Immun. 64, 3646-3651.
45. 45. Schwager, S.L., Chubb, A.J., Scholle, R.R., Brandt, W.F., Mentele, R., Riordan, J.F., Sturrock, E.D. & Ehlers, M.R. (1999) Modulation of juxtamembrane cleavage ('shedding') of angiotensin-converting enzyme by stalk glycosylation: evidence for an alternative shedding protease. Biochemistry 38, 10388-10397.
46. 46. Jones, S.A., Novick, D., Horiuchi, S., Yamamoto, N., Szalai, A.J. & Fuller, G.M. (1999) C-reactive protein: a physiological activator of interleukin 6 receptor shedding. J. Exp. Med. 189, 599-604.