Novel functions of clathrin light chains: Clathrin heavy chain trimerization is defective in light chain-deficient yeast

Journal of Cell Science

Volumn 110, Issue 7, 1997, Pages 899-910

  Huang, Kristen M ^a   Gullberg, Lisa ^a   Nelson, Karen K ^a   Stefan, Christopher J ^b   Blumer, Kendall ^b   Lemmon, Sandra K ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Clathrin; Endocytosis; Golgi retention; Saccharomyces cerevisiae; Triskelion

Indexed keywords

CLATHRIN;

ARTICLE; ENDOCYTOSIS; GENE DELETION; GOLGI COMPLEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; YEAST;

CLATHRIN; ENDOCYTOSIS; YEASTS;

SACCHAROMYCES CEREVISIAE; TRISKELION;

EID: 0030975677     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. Ahle, S. and Ungewickell, E. (1989). Identification of a clathrin binding subunit in the HA2 adaptor protein complex. J. Biol. Chem. 264, 20089-20093.
2. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
3. Bar-Zvi, D. and Branton, D. (1986). Clathrin-coated vesicles contain two protein kinase activities: Phosphorylation of clathrin B-light chain by casein kinase II. J. Biol. Chem. 261, 9614-9621.
4. Blumer, K. J., Reneke, J. E. and Thorner, J. (1988). The STE2 gene product is the ligand-binding component of the α-factor receptor of Saccharomyces cerevisiae. J. Biol. Chem. 263, 10836-10842.
5. Brodsky, F. M., Hill, B. L., Acton, S. L., Nathke, I., Wong, D. H., Ponnambalam, S. and Parham, P. (1991). Clathrin light chains - Arrays of protein motifs that regulate coated-vesicle dynamics. Trends Biochem. Sci. 16, 208-213.
6. Christianson, T. W., Sikorski, R. S., Dante, M., Shero, J. H. and Hieter, P. (1992). Multifunctional yeast high-copy-number shuttle vectors. Gene 110, 119-122.
7. De Luca-Flaherty, C., McKay, D. B., Parham, P. and Hill, B. L. (1990). Uncoating protein (hsc70) binds a conformationally labile domain of clathrin light chain LCa to stimulate ATP hydrolysis. Cell 62, 875-887.
8. Dulic, V., Egerton, M., Elguindi, I., Raths, S., Singer, B. and Riezman, H. (1991). Yeast endocytosis assays. Meth. Enzymol. 194, 697-710.
9. Fuller, R. S., Sterne, R. E. and Thorner, J. (1988). Enzymes required for yeast prohormone processing. Annu. Rev. Physiol. 50, 345-362.
10. Gallusser, A. and Kirchhausen, T. (1993). The beta 1-subunit and beta 2-subunit of the AP complexes are the clathrin coat assembly components. EMBO J. 12, 5237-5244.
11. Guthrie, C. and Fink, G. R. (1991). Guide to yeast genetics and molecular biology. Meth. Enzymol. 194, 1-933.
12. Horazdovsky, B. F. and Emr, S. D. (1993). The VPS16 gene product associates with a sedimentable protein complex and is essential for vacuolar protein sorting in yeast. J. Biol. Chem. 268, 4953-4962.
13. Jackson, A. P., Seow, H.-F., Holmes, N., Drickamer, K. and Parham, P. (1987). Clathrin light chains contain brain-specific insertion sequences and a region of homology with intermediate filaments. Nature 326, 154-159.
14. Keen, J. H., Willingham, M. C. and Pastan, I. H. (1979). Clathrin-coated vesicles: Isolation, dissociation and factor-dependent reassociation of clathrin baskets. Cell 16, 303-312.
15. Keen, J. H., Beck, K. A., Kirchhausen, T. and Jarrett, T. (1991). Clathrin domains involved in recognition by assembly protein AP-2. J. Biol. Chem. 266, 7950-7956.
16. Kirchhausen, T., Harrison, S. C., Parham, P. and Brodsky, F. M. (1983). Location and distribution of the light chains in clathrin trimers. Proc. Nat. Acad. Sci. USA 80, 2481-2485.
17. Kirchhausen, T., Harrison, S. C., Chow, E. P., Mattaliano, R. J., Ramachandran, K. L., Smart, J. and Brosius, J. (1987a) Clathrin heavy chain: molecular cloning and complete primary structure. Proc. Natl. Acad. Sci. USA 84, 2612-2616.
18. Kirchhausen, T., Scarmato, P., Harrison, S. C., Monroe, J. J., Chow, E. P., Mattaliano, R. J., Ramachandran, K. L., Smart, J. E., Ahn, A. H. and Brosius, J. (1987b). Clathrin light chains LCA and LCB are similar. polymorphic and share repeated heptad motifs. Science 236, 320-324.
19. Kirchhausen, T. (1990). Identification of a putative yeast homolog of the mammalian β chains of the clathrin associated protein complexes. Mol. Cell. Biol. 10, 6089-6090.
20. Kirchhausen, T. (1993). Coated pits and coated vesicles - sorting it all out. Curr. Opin. Struct. Biol. 3, 182-188.
21. Kirchhausen, T. and Toyoda, T. (1993). Immunoelectron microscopic evidence for the extended conformation of light chains in clathrin trimers. J. Biol. Chem. 268, 10268-10273.
22. Kunkel, T. A., Roberts, J. D. and Zakour, R. A. (1987). Rapid and efficient site-specific mutagenesis without phenotypic selection. Meth. Enzymol. 154, 367-382.
23. Kurjan, J. (1992). Pheromone response in yeast. Annu. Rev. Biochem. 61, 1097-1129.
24. Lemmon, S. K. and Jones, E. W. (1987). Clathrin requirement for normal growth of yeast. Science 238, 504-509.
25. Lemmon, S. K., Lemmon, V. P. and Jones, E. W. (1988). Characterization of yeast clathrin and anti-clathrin heavy chain monoclonal antibodies. J. Cell. Biochem. 36, 329-340.
26. Lemmon, S. K., Freund, C. L., Conley, K. and Jones, E. W. (1990). Genetic instability of clathrin deficient strains of Saccharomyces cerevisiae. Genetics 124, 27-38.
27. Lemmon, S. K., Pellicena-palle, A., Conley, K. and Freund, C. L. (1991). Sequence of the clathrin heavy chain from Saccharomyces cerevisiae and requirement of the COOH terminus for clathrin function. J. Cell Biol. 112, 65-80.
28. Lindner, R. and Ungewickell, E. (1991). Light-chain-independent binding of adaptors, AP180 and auxilin to clathrin. Biochemistry 30, 9097-9101.
29. Lisanti, M. P., Shapiro, L. S., Moskowitz, N., Hua, E. L., Puszkin, S. and Schook, W. (1982). Isolation and preliminary characterization of clathrin-associated proteins. Eur. J. Biochem. 125, 463-470.
30. Liu, S. H., Wong, M. L., Craik, C. S. and Brodsky, F. M. (1995). Regulation of clathrin assembly and trimerization defined using recombinant triskelion hubs. Cell 83, 257-267.
31. Mooibroek, M. J., Michiel, D. F. and Wang, J. H. (1987). Clathrin light chains are calcium binding proteins. J. Biol. Chem. 262, 25-28.
32. Mortimer, R. K. and Johnston, J. R. (1986). Genealogy of principal strains of the yeast genetic stock center. Genetics 113, 35-43.
33. Munn, A. L., Silveira, L., Elgort, M. and Payne, G. S. (1991). Viability of clathrin heavy-chain-deficient Saccharomyces cerevisiae is compromised by mutations at numerous loci - implications for the suppression hypothesis. Mol. Cell. Biol. 11, 3868-3878.
34. Murphy, J. E. and Keen, J. H. (1992). Recognition sites for clathrin-associated protein AP-2 and protein AP-3 on clathrin triskelia. J. Biol. Chem. 267, 10850-10855.
35. Nakano, A., Brada, D. and Schekman, R. (1988). A membrane glycoprotein. Sec 12p, required for protein transport from the endoplasmic reticulum to the Golgi apparatus in yeast. J. Cell Biol. 107, 851-863.
36. Nathke, I., Hill, B. L., Parham, P. and Brodsky, F. M. (1990). The calcium-binding site of clathrin light chains. J. Biol. Chem. 265, 18621-18627.
37. Nathke, I. S., Heuser, J., Lupas, A., Stock, J., Turck, C. W. and Brodsky, F. M. (1992). Folding and trimerization of clathrin subunits at the triskelion hub. Cell 68, 899-910.
38. Nelson, K. K. and Lemmon, S. K. (1993). Suppressors of clathrin deficiency: Overexpression of ubiquitin rescues lethal strains of clathrin-deficient Saccharomyces cerevisiae. Mol. Cell. Biol. 13, 521-532.
39. Nelson, K. K., Holmer, M. and Lemmon, S. (1996). SCD5, a suppressor of clathrin deficiency, encodes a novel protein with a late secretory function in yeast. Mol. Biol. Cell. 7, 245-260.
40. Payne, G. S. and Schekman, R. (1985). A test of clathrin function in protein secretion and cell growth. Science 230, 1009-1014.
41. Payne, G. S., Baker, D., Van Tuinen, E. and Schekman, R. (1988). Protein transport to the vacuole and receptor-mediated endocytosis by clathrin heavy chain-deficient yeast. J. Cell Biol. 106, 1453-1461.
42. Payne, G. S. and Schekman, R. (1989). Clathrin: a role in the intracellular retention of a Golgi membrane protein. Science 245, 1358-1365.
43. Pearse, B. M. F. (1975). Coated vesicles from pig brain: purification and biochemical characterization. J. Mol. Biol. 97, 93-98.
44. Pearse, B. M. F. and Crowther, R. A. (1987). Structure and assembly of coated vesicles. Annu. Rev. Biophys. Chem. 16, 49-68.
45. Phan, H. L., Finlay, J. A., Chu, D. S., Tan, P., Kirchhausen, T. and Payne, G. S. (1994). The Saccharomyces cerevisiae APS1 gene encodes a homologue of the small subunit of the mammalian clathrin AP-1 complex: Evidence for functional interaction with clathrin at the Golgi complex. EMBO J. 13, 1706-1717.
46. Pley, U. M., Hill, B. L., Alibert, C., Brodsky, F. M. and Parham, P. (1995). The interaction of calmodulin with clathrin-coated vesicles, triskelions and light chains - localization of a binding site. J. Biol. Chem. 270, 2395-2402.
47. Rad, M. R., Phan, H. L., Kirchrath, L., Tan, P. K., Kirchhausen, T., Hollenberg, C. P. and Payne, G. S. (1995). Saccharomyces cerevisiae Apl2p, a homologue of the mammalian clathrin AP β subunit, plays a role in clathrin-dependent Golgi functions. J. Cell Sci. 108, 1605-1615.
48. Riezman, H. (1993). Yeast endocytosis. Trends Cell Biol. 3, 273-277.
49. Robinson, M. S. (1994). The role of clathrin, adaptors and dynamin in endocytosis. Curr. Opin. Cell Biol. 6, 538-544.
50. Rothman, J. E. and Schmid, S. L. (1986). Enzymatic recycling of clathrin from coated vesicles. Cell 46, 5-9.
51. Scarmato, P. and Kirchhausen, T. (1990). Analysis of clathrin light chain-heavy chain interactions using truncated mutants of rat liver light chain LCB3. J. Biol. Chem. 265, 3661-3668.
52. Schmid, S. L. and Damke, H. (1995). Coated vesicles: a diversity of form and function. FASEB J. 9, 1445-1453.
53. Seeger, M. and Payne, G. S. (1992). Selective and immediate effects of clathrin heavy chain mutations on Golgi membrane protein retention in Saccharomyces cerevisiae. J. Cell Biol. 118, 531-540.
54. Shih, W., Gallusser, A. and Kirchhausen, T. (1995). A clathrin-binding site in the hinge of the beta 2 chain of mammalian AP-2 complexes. J. Biol. Chem. 270, 31083-31090.
55. Sikorski, R. S. and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
56. Silveira, L., Wong, D. H., Masiarz, F. R. and Schekman, R. (1990). Yeast clathrin has a distinctive light chain that is important for cell growth. J. Cell Biol. 111, 1437-1449.
57. Sprague, G. F. and Thorner, J. W. (1992). Pheromone response and signal transduction during the mating process of Saccharomyces cerevisiae. In The Molecular and Cellular Biology of the Yeast Saccharomyces (ed. E. W. Jones, J. R. Pringle and J. R. Broach), pp. 657-744. Cold Spring Harbor Laboratory Press, Cold Spring Harbor. NY.
58. Stepp, J. D., Pellicena-Palle, A., Hamilton, S., Kirchhausen, T. and Lemmon, S. K. (1995). A late Golgi sorting function for Saccharomyces cerevisiae Apm1p, but not for Apm2p, a second yeast clathrin AP medium chain-related protein. Mol. Biol. Cell. 6, 41-58.
59. 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.
60. Ungewickell, E. and Branton, D. (1981). Assembly units of clathrin coats. 289, 420-422.
61. Ungewickell, E. (1983). Biochemical and immunological studies on clathrin light chains and their binding sites on clathrin triskelions. EMBO J. 2, 1401-1408.
62. Ungewickell, E. and Ungewickell, H. (1991). Bovine brain clathrin light chains impede heavy chain assembly in vitro. J. Biol. Chem. 266, 12710-12714.
63. Ungewickell, E., Ungewickell, H., Holstein, S. E. H., Lindner, R., Prasad, K., Barouch, W., Martin, B., Greene, L. E. and Eisenberg, E. (1995). Role of auxilin in uncoating clathrin-coated vesicles. Nature 378, 632-635.
64. Walworth, N. C., Goud, B., Ruohola, H. and Novick, P. J. (1989). Fractionation of yeast organelles. Meth. Cell Biol. 31, 335-354.
65. Wilde, A. and Brodsky, F. M. (1996). In vivo phosphorylation of adaptors regulates their interaction with clathrin. J. Cell Biol. 135, 635-645.
66. Winkler, F. K. and Stanley, K. K. (1983). Clathrin heavy chain, light chain interaction. EMBO J. 2, 1393-1400.