Endocytic internalization in yeast and animal cells: Similar and different

Journal of Cell Science

Volumn 111, Issue 8, 1998, Pages 1031-1037

  Geli, M Isabel ^a   Riezman, Howard ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Animal cell; Endocytosis; Uptake; Yeast

Indexed keywords

CLATHRIN;

ANIMAL CELL; CELL MEMBRANE; ENDOCYTOSIS; INTERNALIZATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; YEAST;

ENDOCYTOSIS; EUKARYOTIC CELLS; YEASTS;

EID: 0031980575     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (102)

1. AiKen, C., Konner, J., Landau, N. R., Lenburg, M. E. and Trono, D. (1994). Nef induces CD4 endocytosis: requirement for a critical dileucine motif in the membrane proximal CD4 cytoplasmatic domain, Cell 76 , 853-864.
2. Anderson, R. G. W., Brown, M. S. and Goldstein, J. L. (1977a). Role of coated endocytic vesicles in the uptake of receptor bound L.D.L. lipoprotein in human fibroblast. Cell 10, 351-364
3. Anderson, R. G. W., Goldstein, J. I., and Brown, M. S. (1977b). A mutation that impairs the ability of lipoprotein receptors to localise in coated pits on the cell surface of human tibroblast. Nature 270, 695-699.
4. Ahle, S. and Cngewickell, E. (1989). Identification of the clathrin binding subunit in the HA2 adaptor protein complex J. Biol. Chem. 264, 20089-20093.
5. Ayscough, K. R. and Drubin, D. G. (1996). Actin general principles from studies in yeast. Annu. Rev. Cell. Dev. Biol. 12, 129-160.
6. Bénédetti, 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 organisation in yeast. Mol. Biol. Cell 5, 1023-1037
7. Benmerah, A., Gagnon, J., Begue, B., Megarbane, B., Dautry-Varsat, A. and Cerf-Bensussan, N. (1995). The tyrosine kinase substrate eps15 is constitutively associated with the plasma membrane adaptor AP-2. J. Cell Biol. 131, 1831-1838.
8. Benmerah, A., Begue, B., Dautry-Varsat, A. and Cerf-Bensussan, N. (1996). The ear of α-adaptin interacts with the COOH-terminal domain of the eps15 protein. J. Biol. Chem. 271, 12111-12116.
9. Carter, L. L., Redelmeier, T. E., Woollenweber, L. A. and Schmid S. L. (1993). Multiple GTP-binding proteins participate in clathrin-coated vesicle-mediated endocytosis. J. Cell Biol. 120, 37-45.
10. Chen, M. S., Obar, R. A., Schroeder, C. C., Austin, I. W., Poodry, C. A., Wadsworth, S. C. and Vallee, R. B. (1991). Multiple forms of dynamin are encoded by Shibire, a Drosophila gene involved in endocytosis. Nature 351, 583-586.
11. Cheney, R. E. and Mooseker, M. S. (1992). Unconventional myosins. Curr. Opin. Cell Biol. 4, 27-35.
12. Chin, D. J., Straubinger, R. M., Acton, S., Nathke, I. and Brodsky, F. M. (1989). 100-kDa polypeptides in peripheral clathrin-coated vesicles are required for receptor-mediated endocytosis. Proc. Nat. Acad. Sci. USA 86, 9289-9839.
13. Chvatchko, Y., Howald, I. and Riezman, H. (1986) Two yeast mutants defective in endocytosis are defective in pheromone response. Cell 46, 355-364.
14. Coué, M., Brenner, S., Spector, I. and Korn E. (1987). Inhibitron of actin polymenzation by latrunculin A. FEBS Lett. 213, 316-318.
15. Crowther, R. A., Finch, J. T. and Pearse, B. M. F. (1976). On the structure of coated vesicles. J. Mol. Biol. 103, 785-798.
16. Dai, J. and Sheetz, M. P. (1995). Regulation of exocytosis, endocytosis and membrane shape by membrane tension Cold Spring Harb. Symp. Quant. Biol. 60, 567-571.
17. Damke, H., Baba, T., Warnock, D. E. and Schmid, S. L. (1994). Induction of human dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127, 915-934.
18. David, C., Solimena, M. and de Camilli, P. (1994). Autoimmunity in stiff-Man syndrome with breast cancer is targeted to the C-terminal region of human amphiphysin, a protein similar to the yeast proteins. Rvs167 and Rvs161 FEBS Lett. 351, 73-79.
19. david, C., McPherson, P. S., Mundigl, O. and de Camilli, P. (1996). A role of amphiphysin in synaptic vesicle endocytosis suggested by its binding to dynamin in nerve terminals. Proc. Nat. Acad. Sci. USA 93, 331-335.
20. Davis, N. G., Horecka, J. L. and Sprague, G. F. (1993) Cis- and trans-functions required for endocytosis of the yeast pheromone receptors. J Cell Biol. 122, 53-65
21. Deckert, M., Ticchioni, M. and Bernard, A. (1996). Endocytosis of GPI-anchored proteins in human lymphocytes: role of glycolipid-based domains, actin cytoskeleton, and protein kinases. J. Cell Biol. 133, 791-799.
22. Dulic, V., Egerton, M., Elguindi, I., Raths, S., Singer, B. and Riezman, H. (1991). Yeast endocytosis assays. Meth. Enzymol. 194, 697-710.
23. Fazioli, F., Minichiello, L., Matoskova, B., Wong, W. T. and Di Fiore, P. P. (1993). Eps15, a novel tyrosine kinase substrate, exhibits transforming activity. Mol. Cell Biol. 13, 5814-5828.
24. Fra, A. M., Williamson, E., Simsons, K. and Parton, R. G. (1995) De nova formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc. Nat. Acad. Sci. USA 92, 8655-8659.
25. Gammie, A. E., Kurihara, L. J., Vallee, R. B. and Rose, M. D. (1995) DNMI, a dynamin related gene, participates in endosomal trafficking in yeast. J. Cell Biol. 130, 533-566.
26. Geli, M. I. and Riezman, H. (1996). Role of type I myosins in receptor-mediated endocytosis in yeast. Science 272, 533-535.
27. Geli, M. I., Wesp, A. and Riezman, H. (1998). Distinct functions of calmoduim are required for the uptake step of receptor-mediated endocytosis in yeast, the type 1 myosin Myso5p is one of the calmodulin targets. EMBO J. 17, 635-647.
28. Givan, S. A. and Sprague, G. F. (1997) The ankyrin repeat-containing protein Akr??1p is required for the endocytosis of yeast pheromone receptors. Moll. Biol. Cell 8, 117-027.
29. Grigliatti, T. A., Hall, L., Kosenbluth, R. and Suzuki, D. T. (1973). Temperature sensitise mutants in Drosophila melanogaster. XIV. Selection of immobile adults. Mol. Gen. Genet. 120, 107-114.
30. Gottlieb, T. A., Ivannv, I. E., Adesnik, M. and Sahatini, D. D. (1993). Actin microtilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J. Cell Biol. 120, 695-710.
31. Hein, C. and André, B. (1997). A C-terminal di-leucine motif and nearby sequences are required for NH4(+)-induced inactivation and degradation of the general amino acid permease. Gap1p. of Sacharomyces cerevisiae. Mol. Microbiol. 24, 607-616.
32. Hicke, L. and Riezman, H. (1996) Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84, 277-287.
33. Hicke, L., Zanolari, B., Pypaert, M., Rohrer, J. and Riezman, H. (1997). Transport throught the yeast endocytic pathway occurs through morphologically distinct compartment and requires an active secretory pathway and Sec18p/N-ethylmaleimide-sensitive fusion protein. Mol. Biol. Cell 8, 13-31.
34. Hill, K. L., Catlett, N. L. and Weisman, L. S. (1996). Actin and myosin function in directed vacuole movement during cell division in Saccharomyces cerevisiae. J. Cell Biol. 135, 1535-1549.
35. Hinshaw, J. E. and Schmid, S. L. (1995). Dynamin self-assembles into rings suggesting a mechanism for vesicle coated budding, Nature 374, 190-192.
36. Huang, K. M., Gullberg, L., Nelson, K. K., Stefan C. J., Blumer, K. and Lemmon, S. K. (1997). Novel functions of clathrin light chains: clalhrin heavy chain trimerization is defective in light chain deficient yeast. J. Cell Sci. 110, 899-910.
37. Jones, B. A. and Fangman, W. L. (1992). Mitochondrial DNA maintenance in yeast requires a protein containing a region related to the GTP-binding domain of dynamin. Genes Dev. 6, 380-389.
38. Kohtz, D. S., Hanson, V. and Puszkin, S. (1990). Novel proteins mediate an interaction between clathrin coated vesicles and polymerizing actin filaments. Eur. J. Biochem. 192, 291-298.
39. Kosaka, T. and Ikeda, K. (1983). Possible temperature-dependent blockage of synaptic vesicle recycling induced by a single gene mutation in Drosophila. J. Neurobiol. 14, 207-225.
40. Kübler, E. and Riezman, H. (1993) Actin and fimbrin are required for the internalization step of endocytosis in yeast. EMBO J. 12, 2855-2862.
41. Kübler, E., Schimmöller, F. and Riezman, H. (1994). Calcium-independent calmodulin requirement for endocytosis in yeast. EMBO J. 13, 5539-5546.
42. Kyle, M. E., Nakae, D., Sakaida, I., Miccadei, S. and Farber, J. L. (1988). Endocytosis of superoxide dismutase is required in order for the enzyme to protect hepathocytes from the cytotoxicity of hydrogen peroxide. J. Biol. Chem. 263, 3784-3789.
43. Lamaze, C. and Schmid, S. L. (1995). The emergence of clathrin-independent pinocytic pathways. Curr. Open. Cell Biol. 7, 573-580.
44. Lamaze, C., Fujimoto, L. M., Yin, H. L. and Schmid, S. L. (1997) The actin cytoskeleton is required for receptor-mediated endocytosis in mammalian cells. J. Biol. Chem. 272, 20332-20335.
45. Luna, E. J. (1991). Molecular links between the cytoskeleton and membranes. Curr. Opin. Cell Biol. 3, 120-126.
46. Luo, W. J. and Chang, A. (1997). Novel genes involved in endosomal traffic in yeast revealed by suppression of a targeting-defective plasma membrane ATPase mutant. J. Cell Biol. 138, 731-746.
47. McMahon, H. T., Wigge, P. and Smith, C. (1997) Clathrin interacts specifically with amphiphysin and is displaced by dynamin. FEBS Lett. 413, 319-322.
48. Marks, M. S., Ohno, H., Kirchhausen, T. and Bonifacino, J. S. (1997). Protein sorting by tyrosinebased signals: adapting to the Ys and wherefores. Trends Cell Biol. 7, 124-128.
49. Moreau, V., Galan, J. M., Devilliers, G., Haguenauer-Tsapis, R. and Winsor, B. (1997). The yeast actin-related protein Arp2p is required for the internalization step of endocytosis. Mol. Biol. Cell. 8, 1361-1375.
50. Mundigl, O., Ochoa, G. C., David, C., Kabanov, A. V. and de Camilli, P. (1997). Amphiphysin, a dynamin binding protein is implicated in the function of the actin based cytoskeleton. ASCB abstract number 486.
51. Munn, A. L. and Riezman, H. (1994). Endocytosis is required for the growth of vacuolar H(+)-ATPase-defective yeast: identification of six new END genes. J. Cell Biol. 127, 373-386.
52. Munn, A. L., Stevenson, B. J., Geli, M. I. and Riezman, H. (1995). end5, end6 and end7 mutations that cause actin delocalization and block the internalization step of endocytosis in Saccharomyces cerevesiae. Mol. Biol. Cell 6, 1721-1742.
53. Oh, P. and Schnitzer, J. E. (1996). Dynumin-mediated fission of caveolae from plasma membranes. ASCB. Abstract number 483.
54. Ohno, H., Steward, J., Fournier, M. C., Bosshart, H., Rhee, I., Miyatake, S., Saito, T., Gallusser, A., Kirchhausen, T. and Bonifacino, J. S. (1995) Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269, 1872-1875.
55. Ohya, V. and Bolstein, D. (1994). Diverse essential functions revealed by complementing yeast calmodulin mutants. Science 263, 963-966.
56. Paiade, G. E. (1953). The fine structure of Wood capillaries. J. Appl. Phys. 24, 1424.
57. Parton, R. G., Joggerst, B. and Simons, K. (1994). Regulated internalization of caveolae. J. Cell Biol. 127, 1199-1215.
58. Parton, R. G. (1996). Caveolae and caveolin. Curr. Opin. Cell Biol. 8, 542-548.
59. Pearse, B. M. F. (1975). Coated vesicles from pig brain: purification and biochemical characterization. J. Mol. Biol. 97, 93-98.
60. Pearse, B. M. F. and Robinson, M. S. (1990). Clathrin, adaptors and sorting. Annu. Rev. Cell Biol. 6, 151-171.
61. Piasek, A. and Thyberg, J. (1980). Effects of colchicine on endocytosis of horseradish peroxidase by rat peritoneal macrophages, J. Cell Sci. 45, 59-71.
62. 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. Localisation of a binding site. J. Biol. Chem. 270, 2395-2402.
63. Pollard, T. D., Doberstein, S. K. and Zot, H. G. (1991) Myosin-I. Annu. Rev. Physiol. 53, 653-681.
64. Pratten, M. K. and Lloyd, J. B. (1979). Effect of temperature, metabolic inhibitors and some other factors in fluid-phase adsorptive pinocytosis by rat peritoneal macrophages. Biochem. J. 180, 567-571.
65. Prescianotto-Baschong, C. and Riezman, H. (1998). Morphology of the yeast endocytic pathway. Mol. Biol. Cell. 9, 173-189.
66. Raths, S., Rohrer J., Crausaz, F. and Riezman, H. (1993). end3 and end4: two mutants defective in receptor-mediated and fluid-phase endocytosis in Succharomyces cerevesiae. J. Cell Biol. 120, 55-65.
67. Riezman, H., Munn, A., Geli, M. I. and Hicke, L. (1996) Actin-myosin-and ubiquitin-depedent endocytosis. Experientia 52, 1033-1041.
68. Robinson, M. S. (1997). Coats and vesicle budding. Trends Cell Biol. 7, 99-102.
69. Rohrer, J., Benedetti, H., Zanolari, B. and Riezman, H. (1993) Identification of a novel sequence mediating regulated endocytosis of the G-protein couple alpha-pheromone receptor in yeast. Mol. Biol. Cell. 4, 511-521.
70. Roth, T. F. and Porter, K. R. (1964). Yolk protein uptake in the oocyte of the mosquito Aedes aegypti. J. Cell Biol. 20, 313-330.
71. Rothberg, K. G., Heuse, J. E., Donzell, W. C., Wing, Y. S., Glenney, J. R. and Anderson, R. G. W. (1992). Caveolin, a protein component of caveolae membrane coats. Cell 68, 673-682.
72. Salcini, A. E., Confalonieri, S., Doria, M., Santolini, E., Tassi, E., Minenkova, O., Cesareni, G., Pelicci, P. G. and Di Fiore, P. P. (1997). Binding specificity and in vivo targets of the EH domain, a novel protein-protein interaction module, Genes. Dev. 11, 2239-2249.
73. Salisbury, J. L., Condeelis, J. S. and Satir, P. (1980). Role of coated vesicles. microfilaments and calmodulin in receptor-mediated endocytosis by cultured B lymphoblastoid cells. J. Cell Biol. 87, 132-141.
74. Sandvig, K. and van Deurs, B. (1990) Selective modulation of the endocytic uptake of ricin and fluid phase markers without alteration in transferrin endocytosis. J. Biol. Chem. 265, 6382-6388.
75. Schmid, S. L. and Carter, L. L. (1990) ATP is required for receptor-mediated endocytosis in intact cells. J. Cell Biol. 111, 2307-2318
76. Schmid, S. L. and Smythe, E. (1991) Stage-specific assay for coated pit formation and coated vesicle budding in vitro. J. Cell Biol. 114, 869-880.
77. Schmid, S. L. (1992) The mechanism of receptor-mediated endocytosis: more questions than answers BioEssays 14, 589-596.
78. Schnitzer, J. E., Oh, P., Pinney, E. and Allard, J. (1994). Filipin sensitive caveolae-mediated transport in endothelium: reduced transcytosis. scavenger endocytosis and capillary permeability of select macromolecules. J. Cell Biol. 127, 1217-1232.
79. Schnitzer, J. E., Oh, P. and McIntosh, D. P. (1996) Role of GTP hydrolysis in fission of caveolae directly from plasma membranes. Science 274, 239-242.
80. Singer-Krüger, B., Frank, R., Crausaz, F. and Riezman, H. (1993) Partial purification and yeast characterization of early and late endosomes in yeast. J. Biol. Chem. 268, 14376-14386.
81. Shupliakuv, O., Low, P., Grabs, D., Gad, H., Chen, H., David, D. Takei, K., de Camilli, P. and Brodin, L. (1997). Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276, 259-263.
82. Smythe, E., Pypaert, M., Lucocq, J. and Warren, G. (1989). Formation of coated vesicles from coated pits in broken A431 cells. J. Cell Biol. 108, 843-853.
83. Stang, E., Kartenbeck, J. and Parton, R. G. (1997) Major histocompatibility complex class I molecules mediate association of SV40 with caveolae. Mol. Biol. Cell 8, 47-57.
84. Strous, G. J., Van Kerkhof, P., Govers, R., Ciechanover, A. and Schwartz, A. L. (1996). The ubiquitin conjugating system is required for ligand-induced endocytosis and degradation of the growth hormone receptor. EMBO J. 15. 3806-3812.
85. Takei, K., McPherson, P. S., Schmid, S. I., and de Camilli, P. (1995). Tubular membrane invaginations coated by dynamin rings are induced by GTP-γS in nerve terminal Nature 374, 186-190.
86. 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.
87. Tan, P. K., Howard, J. P. and Payne, G. S. (1996). The sequence NPFXD defines a new class of endocytosis signal in Saccharomvces cerevisiae. J. Cell Biol. 135, 1789-1800.
88. Tang, H. V., Munn, A. and Cai, M. (1997). EH domain proteins Pan1p and End3p are components of a complex that plays a dual role in organiozation of the cortical actin cytoskeleton and endocytosis in Saccharomyces cerevisiae. Mol. Cell. Biol. 17, 4294-4304.
89. Tebar, F., Sorkina, T., Sorkin, A., Ericsson, M. and Kirchhausen T. (1996) Eps15 is a component of clathrin-coated pits and vesicles and it is located at the rim of coated pits. J. Biol. Chem. 271, 28727-28730.
90. Tran, D. J., Carpentier, J. L., Sawano, F., Gorden, P. and Orci, L. (1987) Ligands internalized through coated and non-coated invaginations follow a common intracellular pathway. Proc. Nat. Acad. Sci. USA 84, 7957-7961.
91. 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.
92. van der Bliek, A. M. and Meyerowitz, E. M. (1991). Dynamin-like protein encoded by the Drosophila Shibire gene associated with vesicular traffic. Nature 351, 411-414.
93. van der Bliek, A. M., Redelmeier, T. E., Damke, H., Tisdale, F. J., Meyerowitz, E. M. and Schmid S. L. (1993), Mutations in human dynamin block an intermediate stage in coated vesicle formation. J. Cell Biol. 122, 553-563.
94. Vater, C. A., Raymond, C. K., Kena, K., Howald-Stevenson, I. and Stevens, T. H. (1992). The VPS1 protein, a homolog of dynamin required for vacuolar protein sorting in Saccharomyces cerevesiae. is a GTPase with two functional separable domains. J. Cell Biol. 119, 773-786.
95. 3H uptake and inhibition by cytochalasin B. J. Cell Biol. 50, 804-817.
96. Warnock, D. E. and Schmid, S. L. (1996). Dynamin GTPase. a force-generating molecular switch. BioEssays 18, 885-893.
97. Wendland, B., McCaffrey, J. M., Xiao, Q. and Emr, S. D. (1996). A novel-fluorescence-activated cell sorter-based screen for yeast endocytosis mutants identifies a yeast homologue of mammalian eps15. J. Cell Biol. 135, 1485-1500.
98. Wertman, K. F., Drubin, D. G. and Botstein, D. (1992) Systematic mutalional analysis of the yeast ACT1 gene, Genetics 132, 337-350.
99. Wesp, A., Hicke, L., Palecek, J., Lombardi, R., Aust, T., Munn, A. L., and Riezman, H. (1997). End4/Sla2 interacts with actin-associated proteins for endocytosis in yeast. Mol. Biol. Cell. 8, 2291-2306.
100. Wong, W. T., Kraus, M. H., Carlomagno, F., Zelano, A., Druck, T., Croce, C. M., Huebner, K. and Di Fiore, P. P. (1994) The human eps15 gene. encoding a tyrosine substrate, is conserved in evolution and maps to 1p31-32 Oncogene 9, 1591-1597.
101. Wong, W. T., Schumacher, C., Salcini, A. E., Romano, A., Castagnino, P., Pelicci, P. G. and di Fiore, P. P. (1995). A protein-binding domain. EH, identified in the receptor tyrosme kinase substrate eps15 and conserved in evolution. Proc. Nat. Acad. Sci. USA 92, 9530-9534.
102. Yang, S., Ayscough, K. R. and Drubin, D. G. (1997). A role of the actin cytoskeleton of Saccharomyces cerevisiae in bipolar bud-site selection. J. Cell Biol. 136, 111-123.