Copper-dependent degradation of the Saccharomyces cerevisiae plasma membrane copper transporter Ctr1p in the apparent absence of endocytosis

EMBO Journal

Volumn 15, Issue 14, 1996, Pages 3515-3523

  Ooi, Chean Eng ^a   Rabinovich, Efrat ^a,b   Dancis, Andrew ^a   Bonifacino, Juan S ^a   Klausner, Richard D ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

Copper homeostasis; Copper transporter; Endocytosis; Plasma membrane protein turnover; Protein degradation

Indexed keywords

CARRIER PROTEIN; COPPER; FUNGAL PROTEIN; MEMBRANE PROTEIN;

ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; FUNGUS MUTANT; INTERNALIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN METABOLISM; SACCHAROMYCES CEREVISIAE;

FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 0029994433     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00720.x     Document Type: Article

References (54)

1. Ammerer, G., Hunter, C.P., Rothman, J.H., Saari, G.C., Valls, L.A. and Stevens, T.H. (1986) PEP4 gene of Saccharomyces cerevisiae encodes proteinase A, a vacuolar enzyme required for processing of vacuolar precursors. Mol. Cell. Biol., 6, 2490-2499.
2. Barnathan, E.S., Kuo, A., Rosenfeld, A., Kariko, K., Leski, M., Robbiati, F., Nolli, M.L., Henkin, J. and Cines, D.B. (1990) Interaction of single-chain urokinase-type plasminogen activator with human endothelial cells. J. Biol. Chem., 265, 2865-2872.
3. Basu, A., Raghunath, M., Bishayee, S. and Das, M. (1989) Inhibition of tyrosine kinase activity of the epidermal growth factor (EGF) receptor by a truncated receptor form that binds to EGF: role for interreceptor interaction in kinase regulation. Mol. Cell. Biol., 9, 671-677.
4. Bazil, V. and Strominger, J.L. (1993) CD43, the major sialoglycoprotein of human leukocytes, is proteolytically cleaved from the surface of stimulated lymphocytes and granulocytes. Proc. Natl Acad. Sci. USA, 90, 3792-3796.
5. Benedetti, H., Raths, S., Crausaz, F. and Riezman, H. (1994) The END3 gene encodes a protein that is required for the internalization step of endocytosis and for actin cytoskeleton organization in yeast. Mol. Biol. Cell, 5, 1023-1037.
6. Cao, J., Sato, H., Takino, T. and Seiki, M. (1995) The C-terminal region of membrane type metalloproteinase is a functional transmembrane domain required for pro-gelatinase A activation. J. Biol. Chem., 270, 801-805.
7. Cha, J.-S. and Cooksey, D.A. (1991) Copper resistance in Psuedomonas syringae mediated by periplasmic and outer membrane proteins. Proc. Natl. Acad. Sci. USA, 88, 8915-8919.
8. Dancis, A., Yuan, D.S., Haile, D., Askwith, C., Eide, D., Moehle, C., Kaplan, J. and Klausner, R.D. (1994a) Molecular characterization of a copper transport protein in S.cerevisiae: an unexpected role for copper in iron transport. Cell, 76, 393-402.
9. Dancis, A., Haile, D., Yuan, D.S. and Klausner, R.D. (1994b) The Saccharomyces cerevisiae copper transport protein (Ctr1p). Biochemical characterization, regulation by copper, and physiologic role in copper uptake. J. Biol. Chem., 269, 25660-25667.
10. Davis, C.G., Lehrman, M.A., Russell, D.W., Anderson, R.G.W., Brown, M.S. and Goldstein, J.L. (1986) The J.D. mutation in familial hypercholesterolemia: amino acid substitution in the cytoplasmic domain impedes internalization of LDL receptors. Cell, 45, 15-24.
11. Davis, N.G., Horecka, J.L. and Sprague, G.F., Jr (1993) Cis- and trans-acting functions required for endocytosis of yeast pheromone receptors. J. Cell Biol., 122, 53-65.
12. Downing, J.R., Roussel, M.F. and Sherr, C.J. (1989) Ligand and protein kinase C downmodulate the colony-stimulating factor 1 receptor by independent mechanisms. Mol. Cell. Biol., 9, 2890-2896.
13. Ellis, V., Scully, M.F. and Kakkar, V.V. (1989) Plasminogen activation initiated by single-chain urokinase-type plasminogen activator. Potentiation by U937 monocytes. J. Biol. Chem., 264, 2185-2188.
14. Flickinger, T.W., Maihle, N.J. and Kung, H.J. (1992) An alternatively processed mRNA from the avian c-erbB gene encodes a soluble, truncated form of the receptor that can block ligand-dependent transformation. Mol. Cell. Biol., 12, 883-893.
15. Gruenberg, J. and Howell, K.E. (1989) Membrane traffic in endocytosis: insights from cell-free assays. Annu. Rev. Cell Biol., 5, 453-481.
16. Halliwell, B. and Gutteridge, J.M. (1988) Free Radicals in Biology and Medicine. Clarendon Press, Oxford.
17. Ito, H., Fukuda, Y., Murata, K. and Kimura, A. (1983) Transformation of intact yeast cells treated with alkali cations. J. Bacteriol., 153, 163-168.
18. Jenness, D.D. and Spatrick, P. (1986) Down regulation of the a factor pheromone receptor in S.cerevisiae. Cell, 46, 345-353.
19. Jones, E.W. (1991) Three proteolytic systems in the yeast Saccharomyces cerevisiae. J. Biol. Chem., 266, 7963-7966.
20. Kahn, J., Ingraham, R.H, Shirley, F., Migaki, G.I. and Kishimoto, T.K. (1994) Membrane proximal cleavage of L-selectin: identification of the cleavage site and a 6-kD transmembrane peptide fragment of L-selectin. J. Cell Biol., 125, 461-470.
21. Kaushal, G.P., Walker, P.D. and Shah, S.V. (1994) An old enzyme with a new function: purification and characterization of a distinct matrix-degrading metalloproteinase in rat kidney cortex and its identification as meprin. J. Cell Biol., 126, 1319-1327.
22. Klausner, R.D., Harford, J. and van Renswoude, J. (1984) Rapid internalization of the transferrin receptor in K562 cells is triggered by ligand binding or treatment with a phorbol ester. Proc. Natl Acad. Sci. USA, 81, 3005-3009.
23. Kriegler, M., Perez, C., DeFay, K., Albert, I. and Lu, S.D. (1988) A novel form of TNF/cachectin is a cell surface cytotoxic transmembrane protein: ramifications for the complex physiology of TNF. Cell, 53, 45-53.
24. Kubler, E. and Riezman, H. (1993) Actin and fimbrin are required for the internalization step of endocytosis in yeast. EMBO J., 12, 2855-2862.
25. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
26. Lai, K., Bolognese, C.P., Swift, S. and McGraw, P. (1995) Regulation of inositol transport in Saccharomyces cerevisiae involves inositol-induced changes in permease stability and endocytic degradation in the vacuole. J. Biol. Chem., 270, 2525-2534.
27. Li, H.H. and Merchant, S. (1995) Degradation of plastocyanin in copper-deficient Chlamydomonas reinhardtii. Evidence for a protease-susceptible conformation of the apoprotein and regulated proteolysis. J. Biol. Chem., 270, 23504-23510.
28. Linder, M.C. (1991) Introduction and overview of copper as an element essential in life. In Linder, M.C. (ed.), Biochemistry of Copper. Plenum Press, New York, pp. 1-13.
29. +-ATPase of Saccharomyces cerevisiae. J. Biol. Chem., 270, 6815-6823.
30. O'Bryan, J.P., Fridell, Y.-W., Koski, R., Varnum, B. and Liu, E.T. (1995) The transforming receptor tyrosine kinase, Axl, is post-translationally regulated by proteolytic cleavage. J. Biol. Chem., 270, 551-557.
31. Odermatt, A., Suter, H., Krapf, R. and Solioz, M. (1993) Primary structure of two P-type ATPases involved in copper homeostasis in Enterococcus hirae. J. Biol. Chem., 268, 12775-12779.
32. Oshumi, Y., Kitamoto, K. and Anraku, Y. (1988) Changes induced in the permeability barrier of the yeast plasma membrane by cupric ion. J. Bacteriol., 170, 2676-2682.
33. Pandiella, A., Bosenberg, M.W., Huang, E.J., Besmer, P. and Massague, J. (1992) Cleavage of membrane-anchored growth factors involves distinct protease activities regulated through common mechanisms. J. Biol. Chem., 267, 24028-24033.
34. Prat, M., Crepaldi, T., Gandino, L., Giordano, S., Longati, P. and Comoglio, P. (1991) C-terminal truncated forms of Met, the hepatocyte growth factor receptor. Mol. Cell. Biol., 11, 5954-5962.
35. Pearse, B.M.F. and Robinson, M.S. (1990) Clathrin, adaptors and sorting. Annu. Rev. Cell Biol., 6, 151-171.
36. Raths, S., Rohrer, J., Crausaz, F. and Riezman, H. (1993) end3 and end4: two mutants defective in receptor-mediated and fluid-phase endocytosis in Saccharomyces cerevisiae. J. Cell Biol., 120, 55-65.
37. Riezman, H. (1993) Yeast endocytosis. Trends Cell Biol., 3, 273-277.
38. Roberts, C.J., Raymond, C.K., Yamashiro, C.T. and Stevens, T.H. (1991) Methods for studying the yeast vacuole. Methods Enzymol., 194, 644-661.
39. Rohrer, J., Benedetti, H., Zanolari, B. and Riezman, H. (1993) Identification of a novel sequence mediating regulated endocytosis of the G protein-coupled α-pheromone receptor in yeast. Mol. Biol. Cell, 4, 511-521.
40. Schandel, K.A. and Jenness, D.D. (1994) Direct evidence for ligand-induced internalization of the yeast α-factor pheromone receptor. Mol. Cell. Biol., 14, 7245-7255.
41. Serrano, R. (1991) In Broach, J.R., Pringle, J. and Jones, E.W. (eds), Molecular Biology of the Yeast Saccharomyces. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 523-586.
42. Singer, B. and Riezman, H. (1990) Detection of an intermediate compartment involved in transport of α-factor from the plasma membrane to the vacuole in yeast. J. Cell Biol., 110, 1911-1922.
43. Singer-Kruger, B., Frank, R., Crausaz, F. and Riezman, H. (1993) Partial purification and characterization of early and late endosomes from yeast. J. Biol. Chem., 268, 14376-14386.
44. Smythe, E. and Warren, G. (1991) The mechanism of receptor-mediated endocytosis. Eur. J. Biochem., 202, 689-699.
45. Tan, P.K., Davis, N.G., Sprague, G.F. and Payne, G.S. (1993) Clathrin facilitates the internalization of seven transmembrane segment receptors for mating pheromones in yeast. J. Cell Biol., 123, 1707-1716.
46. Trowbridge, I.S. (1991) Endocytosis and signals for internalization. Curr. Opin. Cell Biol., 3, 634-641.
47. Trowbridge, I.S., Collawn, J.F. and Hopkins, C.R. (1993) Signal-dependent membrane protein trafficking in the endocytic pathway. Annu. Rev. Cell Biol., 9, 129-161.
48. Vida, T.A. and Emr, S.D. (1995) A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol., 128, 779-792.
49. Volland, C., Urban-Grimal, D., Geraud, G. and Haguenauer-Tsapis, R. (1994) Endocytosis and degradation of the yeast uracil permease under adverse conditions. J. Biol. Chem., 269, 9833-9841.
50. Voorhees, P., Deignan, E., van Donselaar, E., Humphrey, J., Marks, M.S., Peters, P.J. and Bonifacino, J.S. (1995) An acidic sequence within the cytoplasmic domain of furin functions as a determinant of trans-Golgi network localization and internalization from the cell surface. EMBO J., 14, 4961-4975.
51. Wilson, I.A., Niman, H.L., Houghten, R.A., Cherenson, A.R., Conolly, M.L. and Lerner, R.A. (1984) The strucutre of an antigenic determinant in a protein. Cell, 37, 767-778.
52. Wolfsberg, T.G., Primakoff, P., Myles, D.G. and White, J.M. (1995) ADAM, a novel family of membrane proteins containing a disintegrin and a metalloprotease domain: multipotential functions in cell-cell and cell-matrix interactions. J. Cell Biol., 131, 275-278.
53. Woolford, C.A., Daniels, L.B., Park, F.J., Jones, E.W., Van Arsdell, J.N. and Innis, M.A. (1986) The PEP4 gene encodes an aspartyl protease implicated in the posttranslational regulation of Saccharomyces cerivisiae vacuolar hydrolases. Mol. Cell. Biol., 6, 2500-2510.
54. Yuan, D.S., Stearman, R., Dancis, A., Dunn, T., Beeler, T. and Klausner, R.D. (1995) The Menkes/Wilson disease gene homologue in yeast provides copper to a ceruloplasmin-like oxidase required for iron uptake. Proc. Natl Acad. Sci. USA, 92, 2632-2636.