, Volume 52, Issue 12, pp 1033–1041 | Cite as

Actin-, myosin- and ubiquitin-dependent endocytosis

  • H. Riezman
  • A. Munn
  • M. I. Geli
  • L. Hicke
Milti-Author Reviews


Endocytosis is a general term that is used to describe the internalization of external and plasma membrane molecules into the cell interior. In fact, several different mechanisms exist for the internalization step of this process. In this review we emphasize the work on the actin-dependent pathways, in particular in the yeastSaccharomyces cerevisiae, because several components of the molecular machinery are identified. In this yeast, the analysis of endocytosis in various mutants reveals a requirement for actin, calmodulin, a type I myosin, as well as a number of other proteins that affect actin dynamics. Some of these proteins have homology to proteins in animal cells that are believed to be involved in endocytosis. In addition, the demonstration that ubiquitination of some cell surface molecules is required for their efficient internalization is described. We compare the actin, myosin and ubiquitin requirements for endocytosis with recent results found studying these processes usingDictyostelium discoideum and animal cells.

Key words

Ubiquitin yeast Saccharomyces cerevisiae Dictyostelium discoideum cytoskeleton mutants endocytosis actin myosin calmodulin 


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  1. 1.
    Greenberg S., el Khoury J., di Virgilio F., Kaplan E. M. and Silverstein S. C. (1991) Ca(2+)-independent F-actin assembly and disassembly during Fc receptor-mediated phagocytosis in mouse macrophages. J. Cell Biol.113: 757–767CrossRefPubMedGoogle Scholar
  2. 2.
    Greenberg S., Chang P. and Silverstein S. C. (1993) Tyrosine phosphorylation is required for Fc receptor-mediated phagocytosis in mouse macrophages. J. Exp. Med.177: 529–534CrossRefPubMedGoogle Scholar
  3. 3.
    Nobes C. and Hall A. (1994) Regulation and function of the Rho subfamily of small GTPases. Curr. Opin. Genet. Dev.4: 77–81CrossRefPubMedGoogle Scholar
  4. 4.
    Pearse B. M. and Robinson M. S. (1990) Clathrin, adaptors and sorting. Annu. Rev. Cell Biol.6: 151–171CrossRefPubMedGoogle Scholar
  5. 5.
    Hinshaw J. E. and Schmid S. L. (1995) Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding (see comments). Nature374: 190–192CrossRefPubMedGoogle Scholar
  6. 6.
    Takel K., McPherson P. S., Schmid S. L. and De Camilli P.. (1995) Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature374: 186–190PubMedGoogle Scholar
  7. 7.
    Damke H., Baba T., Warnock D. E. and Schmid S. L. (1994) Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol.127: 915–934CrossRefPubMedGoogle Scholar
  8. 8.
    Gottlieb T. A., Ivanov I. E., Adesnik M. and Sabatini D. D. (1993) Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J. Cell Biol.120: 695–710CrossRefPubMedGoogle Scholar
  9. 9.
    Sandvig K., Garred O., Holm P. K. and van Deurs B. (1993) Endocytosis and intracellular transport of protein toxins. Biochem. Soc. Trans.21: 707–711PubMedGoogle Scholar
  10. 10.
    Anderson R. G., Kamen B. A., Rothberg K. G. and Lacey S. W. (1992) Potocytosis: sequestration and transport of small molecules by caveolae. Science255: 410–411PubMedGoogle Scholar
  11. 11.
    Mayor S., Rothberg K. G. and Maxfield F. R. (1994) Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science264: 1948–1951PubMedGoogle Scholar
  12. 12.
    Parton R. G., Joggerst B. and Simons K. (1994) Regulated internalization of caveolae. J. Cell Biol.127: 1199–1215CrossRefPubMedGoogle Scholar
  13. 13.
    Rothberg, K. G., Ying, Y. S., Kamen B. A. and Anderson R. G. (1990) Cholesterol controls the clustering of the glycophospholipid-anchored membrane receptor for 5-methyltetrahydrofolate. J. Cell Biol.111: 2931–2938CrossRefPubMedGoogle Scholar
  14. 14.
    Smart E. J., Foster D. C., Ying Y. S., Kamen B. A. and Anderson R. G. (1994) Protein kinase C activators inhibit receptor-mediated potocytosis by preventing internalization of caveolae. J. Cell Biol.124: 307–313CrossRefPubMedGoogle Scholar
  15. 15.
    O'Halloran T. J. and Anderson R. G. (1992) Clathrin heavy chain is required for pinocytosis, the presence of large vacuoles, and development inDictyostelium. J. Cell Biol.118: 1371–1377CrossRefPubMedGoogle Scholar
  16. 16.
    Riezman H. (1985) Endocytosis in yeast: several of the yeast secretory mutants are defective in endocytosis. Cell40: 1001–1009CrossRefPubMedGoogle Scholar
  17. 17.
    Jenness D. D., Burkholder A. C. and Hartwell L. H. (1983) Binding of alpha-factor pheromone to yeast a cells: chemical and genetic evidence for an alpha-factor receptor. Cell35: 521–529PubMedGoogle Scholar
  18. 18.
    Chvatchko Y., Howald I. and Riezman H. (1986) Two yeast mutants defective in endocytosis are defective in pheromone response. Cell46: 355–364CrossRefPubMedGoogle Scholar
  19. 19.
    Jenness D. D. and Spatrick P. (1986) Downregulation of the alpha-factor pheromone receptor inS. cerevisiae. Cell46: 345–353CrossRefPubMedGoogle Scholar
  20. 20.
    Singer-Krüger B., Frank R., Crausaz F. and Riezman H. (1993) Partial purification and characterization of early and late endosomes from yeast: identification of four novel proteins. J. Biol. Chem.268: 14376–14386PubMedGoogle Scholar
  21. 20a.
    Hicke L., Zanolari B., Pypaert M., Rohrer J. and Riezman H. (1996) Transport through the yeast endocytic pathway occurs through morphologically distinct compartments and requires an active secretory pathway and Sec 18/NSF, Mol. Biol. Cell7: in pressGoogle Scholar
  22. 21.
    Singer B. and Riezman H. (1990) Detection of an intermediate compartment involved in transport of alpha-factor from the plasma membrane to the vacuole in yeast. J. Cell Biol.110: 1911–1922CrossRefPubMedGoogle Scholar
  23. 22.
    Schandel K. A. and Jenness D. D. (1994) Direct evidence for ligand-induced internalization of the yeast alpha-factor pheromone receptor. Mol. Cell Biol.14: 7245–7255PubMedGoogle Scholar
  24. 23.
    Davis N. G., Horecka J. L. and Sprague G. F. Jr. (1993) Cis- and trans-acting functions required for endocytosis of the yeast pheromone receptors. J. Cell Biol.122: 53–65CrossRefPubMedGoogle Scholar
  25. 24.
    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: 1707–1716CrossRefPubMedGoogle Scholar
  26. 25.
    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: 9833–9841PubMedGoogle Scholar
  27. 26.
    Lai K., Bolognese C. P., Swift S. and McGraw P. (1995) Regulation of inositol transport inSaccharomyces cerevisiae involves inositol-induced changes in permease stability and endocytic degradation in the vacuole. J. Biol. Chem.270: 2525–2534CrossRefPubMedGoogle Scholar
  28. 27.
    Riballo E. and Lagunas R. (1994) Involvement of endocytosis in catabolite inactivation of the transport systems inSaccharomyces cerevisiae. Folia Microbiol.39: 542Google Scholar
  29. 28.
    Kölling R. and Hollenberg C. P. (1994) The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO J13: 3261–3271PubMedGoogle Scholar
  30. 29.
    Berkower C., Loayza D. and Michaelis S. (1994) Metabolic instability and constitutive endocytosis of STE6, the a-factor transporter ofSaccharomyces cerevisiae. Mol. Biol. Cell5: 1185–1198PubMedGoogle Scholar
  31. 30.
    Egner R., Mahe Y., Pandjaitan R., and Kuchler K. (1995) Endocytosis and vacuolar degradation of the plasma membrane-localized Pdr5 ATP-binding cassette multidrug transporter inSaccharomyces cerevisiae. Mol. Cell Biol.15: 5879–5887PubMedGoogle Scholar
  32. 31.
    Piper R. C., Cooper A. A., Yang H., and Stevens T. H. (1995) VPS27 controls vacuolar and endocytic traffic through a prevacuolar compartment inSaccharomyces cerevisiae. J. Cell Biol.131: 603–617CrossRefPubMedGoogle Scholar
  33. 32.
    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: 779–792CrossRefPubMedGoogle Scholar
  34. 33.
    Raths S., Rohrer J., Crausaz F. and Riezman H. (1993) end3 and end4: two mutants defective in receptor-mediated and fluid- phase endocytosis inSaccharomyces cerevisiae. J. Cell Biol.120: 55–65CrossRefPubMedGoogle Scholar
  35. 34.
    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 inSaccharomyces cerevisiae. Mol. Biol. Cell6: 1721–1742PubMedGoogle Scholar
  36. 35.
    Sivadon P., Bauer F., Aigle M. and Crouzet M. (1995) Actin cytoskeleton and budding pattern are altered in the yeast rvs161 mutant: the Rvs161 protein shares common domains with the brain protein amphiphysin. Mol. Gen. Genet.246: 485–495CrossRefPubMedGoogle Scholar
  37. 36.
    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. Natl. Acad. Sci. USA93: 331–335CrossRefPubMedGoogle Scholar
  38. 37.
    Bauer F., Urdaci M., Aigle M. and Crouzet M. (1993) Alteration of a yeast SH3 protein leads to conditional viability with defects in cytoskeletal and budding patterns. Mol. Cell Biol.13: 5070–5084PubMedGoogle Scholar
  39. 38.
    Donnelly S. F., Pocklington M. J., Pallotta D. and Orr E. (1993) A proline-rich protein, verprolin, involved in cytoskeletal organization and cellular growth in the yeastSaccharomyces cerevisiae. Mol. Microbiol.10: 585–596PubMedGoogle Scholar
  40. 39.
    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. Cell5: 1023–1037PubMedGoogle Scholar
  41. 40.
    Holtzman D. A., Yang S. and Drubin D. G. (1993) Syntheticlethal interactions identify two novel genes, SLA1 and SLA2, that control membrane cytoskeleton assembly inSaccharomyces cerevisiae. J. Cell Biol.122: 635–644CrossRefPubMedGoogle Scholar
  42. 41.
    Wong W. T., Schumacher C., Salcini A. E., Romano A., Castagnino P., Pelicci P. G. and Di Fiore P. (1995) A protein-binding domain, EH, identified in the receptor tyrosine kinase substrate Eps15 and conserved in evolution. Proc. Natl. Acad. Sci. U.S.A.92: 9530–9534PubMedGoogle Scholar
  43. 42.
    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: 1831–1838CrossRefPubMedGoogle Scholar
  44. 43.
    Silveira L. A., 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: 1437–1449CrossRefPubMedGoogle Scholar
  45. 44.
    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: 1453–1461CrossRefPubMedGoogle Scholar
  46. 45.
    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: 373–386CrossRefPubMedGoogle Scholar
  47. 46.
    Nelson H. and Nelson N. (1990) Disruption of genes encoding subunits of yeast vacuolar H(+)-ATPase causes conditional lethality. Proc. Natl. Acad. Sci. USA87: 3503–3507PubMedGoogle Scholar
  48. 47.
    Herman P. K. and Emr S. D. (1990) Characterization of VPS34, a gene required for vacuolar protein sorting and vacuole segregation inSaccharomyces cerevisiae. Mol. Cell Biol.10: 6742–6754PubMedGoogle Scholar
  49. 48.
    Rothman J. H., Howald I. and Stevens T. H. (1989) Characterization of genes required for protein sorting and vacuolar function in the yeastSaccharomyces cerevisiae. EMBO J.8: 2057–2065PubMedGoogle Scholar
  50. 49.
    Schu P. V., Takegawa K., Fry M. J., Stack J. H., Waterfield, M. D. and Emr S. D. (1993) Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science260: 88–91PubMedGoogle Scholar
  51. 50.
    Singer-Krüger B., Stenmark H., Dusterhoft A., Philippsen P., Yoo J. S. et al. (1994) Role of three rab5-like GTPases, Ypt51p, Ypt52p, and Ypt53p, in the endocytic and vacuolar protein sorting pathways of yeast. J. Cell Biol.125: 283–298CrossRefPubMedGoogle Scholar
  52. 51.
    Singer-Krüger B., Stenmark H. and Zerial M. (1995) Yeast Ypt51p and mammalian Rab5: counterparts with similar function in the early endocytic pathway. J. Cell Sci.108: 3509–3521PubMedGoogle Scholar
  53. 52.
    Wichmann H., Hengst L. and Gallwitz D. (1992) Endocytosis in yeast: evidence for the involvement of a small GTP-binding protein (Ypt7p). Cell71: 1131–1142PubMedGoogle Scholar
  54. 53.
    Schimmöller F. and Riezman H. (1993) Involvement of Ypt7p, a small GTPase, in traffic from late endosome to the vacuole in yeast. J. Cell Sci.016: 823–830Google Scholar
  55. 54.
    Gammie A. E., Kurihara L. J., Vallee R. B., and Rose M. D. (1995) DNM1, a dynamin-related gene, participates in endosomal trafficking in yeast. J. Cell Biol.130: 553–566CrossRefPubMedGoogle Scholar
  56. 55.
    Kübler E. and Riezman H. (1993) Actin and fimbrin are required for the internalization step of endocytosis in yeast. EMBO J.12: 2855–2862PubMedGoogle Scholar
  57. 56.
    Hasson T. and Mooseker M. S. (1995) Molecular motors, membrane movements and physiology: emerging roles for myosins. Curr. Opin. Cell Biol.7: 587–594CrossRefPubMedGoogle Scholar
  58. 57.
    Kübler E., Schimmöller F. and Riezman H. (1994) Calcium-independent calmodulin requirement for endocytosis in yeast. EMBO J.13: 5539–5546PubMedGoogle Scholar
  59. 58.
    Goodson H. V. and Spudich J. A. (1995) Identification and molecular characterization of a yeast myosin I Cell Motil. Cytoskeleton30: 73–84CrossRefPubMedGoogle Scholar
  60. 59.
    Geli M. I. and Riezman H. (1996) Role of type I myosins in receptor-mediated endocytosis in yeast. Science272: 533–535PubMedGoogle Scholar
  61. 60.
    Novak K. D., Peterson M. D., Reedy M. C. and Titus M. A. (1995)Dictyostelium myosin I double mutants exhibit conditional defects in pinocytosis. J. Cell Biol.131: 1205–1221CrossRefPubMedGoogle Scholar
  62. 61.
    Jung G., Wu X. and Hammer J. A. (1996)Dictyostelium mutants lacking multiple classic myosin I isoforms reveal combinations of shared and distinct functions. J. Cell Biol.133: 305–323CrossRefPubMedGoogle Scholar
  63. 62.
    Titus M. A., Wessels D., Spudich J. A. and Soll D. (1993) The unconventional myosin encoded by the myoA gene plays a role inDictyostelium motility. Mol. Biol. Cell4: 233–246PubMedGoogle Scholar
  64. 63.
    Wessels D., Murray J., Jung G., Hammer J. A. and Soll D. R. (1991) Myosin IB null mutants ofDictyostelium exhibit abnormalities in motility. Cell Motil. Cytoskeleton20: 301–315CrossRefPubMedGoogle Scholar
  65. 64.
    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: 73–79CrossRefPubMedGoogle Scholar
  66. 65.
    O Halloran T. J. and Anderson R. G. (1992) Clathrin heavy chain is required for pinocytosis, the presence of large vacuoles, and development inDictyostelium. J. Cell Biol.118: 1371–1377CrossRefPubMedGoogle Scholar
  67. 66.
    Sandvig K. and van Deurs B. (1991) Endocytosis without clathrin (a minireview). Cell Biol. Int. Rep.15: 3–8CrossRefPubMedGoogle Scholar
  68. 67.
    Lamaze C. and Schmid S. L. (1995) The emergence of clathrin-independent pinocytic pathways. Curr. Opin. Cell Biol.7: 573–580CrossRefPubMedGoogle Scholar
  69. 68.
    Watts C. and Marsh M. (1992) Endocytosis: what goes in and how? J. Cell Sci.103: 1–8PubMedGoogle Scholar
  70. 69.
    Jackman M. R., Shurety W., Ellis J. A. and Luzio J. P. (1994) Inhibition of apical but not basolateral endocytosis of ricin and folate in Caco-2 cells by cytochalasin D. J. Cell Sci.107: 2547–2556PubMedGoogle Scholar
  71. 70.
    Riezman H. (1993) Three clathrin-dependent budding steps and cell polarity. Trends Cell Biol.3: 330–332CrossRefPubMedGoogle Scholar
  72. 71.
    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: 291–298CrossRefPubMedGoogle Scholar
  73. 72.
    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: 132–141CrossRefPubMedGoogle Scholar
  74. 73.
    Cohen C. J., Bacon R., Clarke M., Joiner K. and Mellman I. (1994)Dictyostelium discoideum mutants with conditional defects in phagocytosis. J. Cell Biol.126: 955–966CrossRefPubMedGoogle Scholar
  75. 74.
    Bacon R. A., Cohen C. J., Lewin D. A. and Mellman I. (1994)Dictyostelium discoideum mutants with temperature-sensitive defects in endocytosis. J. Cell Biol.127: 387–399CrossRefPubMedGoogle Scholar
  76. 75.
    Maniak M., Rauchenberger R., Albrecht R., Murphy J. and Gerisch G. (1995) Coronin involved in phagocytosis: dynamics of particle-induced relocalization visualized by a green fluorescent protein Tag. Cell83: 915–924CrossRefPubMedGoogle Scholar
  77. 76.
    Swanson J. A. and Watts C. (1995) Macropinocytosis. Trends Cell Biol.5: 424–428.CrossRefPubMedGoogle Scholar
  78. 77.
    Wu L., Valkema R., Van Haastert P. J. and Devreotes, P. N. (1995) The G protein beta subunit is essential for multiple responses to chemoattractants inDictyostelium. J. Cell Biol.129: 1667–1675.PubMedGoogle Scholar
  79. 78.
    Allen L. H. and Aderem A. (1995) A role for MARCKS, the alpha isozyme of protein kinase C and myosin I in zymosan phagocytosis by macrophages. J. Exp. Med.182: 829–840CrossRefPubMedGoogle Scholar
  80. 79.
    Baines I. C., Corigliano Murphy A. and Korn E. D. (1995) Quantification and localization of phosphorylated myosin I isoforms inAcanthamoeba castellanii. J. Cell Biol.130: 591–603CrossRefPubMedGoogle Scholar
  81. 80.
    Furukawa R. and Fechheimer M. (1994) Differential localization of alpha-actinin and the 30 kD actin-bundling protein in the cleavage furrow, phagocytic cup, and contractile vacuole ofDictyostelium discoideum. Cell Motil. Cytoskeleton29: 46–56PubMedGoogle Scholar
  82. 81.
    Fukui Y., Lynch T. J., Brzeska H. and Korn E. D. (1989) Myosin I is located at the leading edges of locomotingDictyostelium amoebae. Nature341: 328–331CrossRefPubMedGoogle Scholar
  83. 82.
    Condeelis J. (1993) Life at the leading edge: the formation of cell protrussions. Annu. Rev. Cell Biol.9: 411–444CrossRefPubMedGoogle Scholar
  84. 83.
    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: 129–161CrossRefPubMedGoogle Scholar
  85. 84.
    Ciechanover A. (1994) The ubiquitin-proteasome proteolytic pathway. Cell79: 13–21CrossRefPubMedGoogle Scholar
  86. 85.
    Yee N. S., Hsiau C. W., Serve H., Vosseller K. and Besmer P. (1994) Mechanism of down-regulation of c-kit receptor: roles of receptor tyrosine kinase, phosphatidylinositol 3′-kinase and protein kinase C. J. Biol. Chem.269: 31991–31998PubMedGoogle Scholar
  87. 86.
    Miyazawa K., Toyama K., Gotoh A., Hendrie P. C., Mantel C. and Broxmeyer H.E. (1994) Ligand-dependent polyubiquitination of c-kit gene product: a possible mechanism of receptor down modulation in M07e cells. Blood83: 137–145PubMedGoogle Scholar
  88. 87.
    Paolini R. and Kinet, J. P. (1993) Cell surface control of the multiubiquitination and deubiquitination of high-affinity immunoglobulin E receptors. EMBO J.12: 779–786PubMedGoogle Scholar
  89. 88.
    Cenciarelli C., Hou D., Hsu K. C., Rellahan B. L., Wiest D. L., Smith H. T. et al. (1992) Activation-induced ubiquitination of the T cell antigen receptor. Science257: 795–797PubMedGoogle Scholar
  90. 89.
    Galcheva Gargova Z., Theroux S. J. and Davis R. J. (1995) The epidermal growth factor receptor is covalently linked to ubiquitin. Oncogene11: 2649–2655PubMedGoogle Scholar
  91. 90.
    Mori S., Heldin C. H. and Claesson Welsh L. (1992) Ligand-induced polyubiquitination of the platelet-derived growth factor beta-receptor. J. Biol. Chem.267: 6429–6434PubMedGoogle Scholar
  92. 91.
    Strous G., van Kerkhof P., Govers R., Ciechanover A. and Schwartz A.L. (1996) The ubiquitin conjugation system is required for ligand-induced endocytosis and degradation of the growth hormone receptor. EMBO J.15: 3806–3812PubMedGoogle Scholar
  93. 92.
    Bardwell L., Cook J. G., Inouye C. J. and Thorner J. (1994) Signal propagation and regulation in the mating pheromone response pathway of the yeastSaccharomyces cerevisiae. Dev. Biol.166: 363–379CrossRefPubMedGoogle Scholar
  94. 93.
    Reneke J. E., Blumer K. J., Courchesne W. E. and Thorner J. (1988) The carboxy-terminal segments of the yeast alpha-factor receptor is a regulatory domain. Cell55: 221–234CrossRefPubMedGoogle Scholar
  95. 94.
    Hicke L. and Riezman H. (1996) Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell84: 277–287CrossRefPubMedGoogle Scholar
  96. 95.
    Rohrer J., Benedetti H., Zanolari B. and Riezman H. (1993) Identification of a novel sequence mediating regulated endocytosis of the G protein-coupled alpha-pheromone receptor in yeast. Mol. Biol. Cell4: 511–521PubMedGoogle Scholar
  97. 96.
    Chen Z., Hagler J., Palombella V. J., Melandri F., Scherer D., Ballard D. et al. (1995) Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway. Genes Dev.9: 1586–1597PubMedGoogle Scholar
  98. 97.
    Deshaies R. J., Chau V. and Kirschner M. (1995) Ubiquitination of the G1 cyclin Cln2p by a Cdc34p-dependent pathway. EMBO J.14: 303–312PubMedGoogle Scholar
  99. 98.
    Yaglom J., Linskens M. H., Sadis S., Rubin D. M., Futcher B. and Finley D. (1995) p34Cdc28-mediated control of Cln3 cyclin degradation. Mol. Cell Biol.15: 731–741PubMedGoogle Scholar
  100. 99.
    Egner R. and Kuchler K. (1996) The yeast multidrug transporter Pdr5 of the plasma membrane is ubiquitinated prior to endocytosis and degradation in the vacuole. FEBS Lett.378: 177–181CrossRefPubMedGoogle Scholar
  101. 100.
    Hein C., Springael J. Y., Volland C., Haguenauer-Tsapis R. and Andre B. (1995) NP11, an essential yeast gene involved in induced degradation of Gap1 and Fur4 permeases, encodes the Rsp5 ubiquitin-protein ligase. Mol. Microbiol.18: 77–87CrossRefPubMedGoogle Scholar
  102. 101.
    Galan J. M., Moreau V., Andre B., Volland C. and Haguenauer-Tsapis R. (1996) Ubiquitination mediated by the Npi1p/Rsp5p ubiquitin-protein ligase is required for endocytosis of the yeast uracil permease. J. Biol. Chem.271: 10946–10952CrossRefPubMedGoogle Scholar
  103. 102.
    Chang, C. P., Lazar C. S., Walsh B. J., Komuro M., Collawn J. F., Kuhn L. A. et al. (1993) Ligand-induced internalization of the epidermal growth factor receptor is mediated by multiple endocytic codes analogous to the tyrosine motif found in constitutively internalized receptors. J. Biol. Chem.268: 19312–19320PubMedGoogle Scholar

Copyright information

© Birkhäuser Verlag 1996

Authors and Affiliations

  • H. Riezman
    • 1
  • A. Munn
    • 1
  • M. I. Geli
    • 1
  • L. Hicke
    • 1
  1. 1.Biozentrum of the University of BaselBasel(Switzerland)

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