Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1996 Dec 2;135(6):1485–1500. doi: 10.1083/jcb.135.6.1485

A novel fluorescence-activated cell sorter-based screen for yeast endocytosis mutants identifies a yeast homologue of mammalian eps15

PMCID: PMC2133956  PMID: 8978817

Abstract

A complete understanding of the molecular mechanisms of endocytosis requires the discovery and characterization of the protein machinery that mediates this aspect of membrane trafficking. A novel genetic screen was used to identify yeast mutants defective in internalization of bulk lipid. The fluorescent lipophilic styryl dye FM4-64 was used in conjunction with FACS to enrich for yeast mutants that exhibit internalization defects. Detailed characterization of two of these mutants, dim1-1 and dim2-1, revealed defects in the endocytic pathway. Like other yeast endocytosis mutants, the temperature-sensitive dim mutant were unable to endocytose FM4-64 or radiolabeled alpha-factor as efficiently as wild-type cells. In addition, double mutants with either dim1-delta or dim2-1 and the endocytosis mutants end4-1 or act1-1 displayed synthetic growth defects, indicating that the DIM gene products function in a common or parallel endocytic pathway. Complementation cloning of the DIM genes revealed identity of DIM1 to SHE4 and DIM2 to PAN1. Pan1p shares homology with the mammalian clathrin adaptor-associated protein, eps15. Both proteins contain multiple EH (eps15 homology) domains, a motif proposed to mediate protein-protein interactions. Phalloidin labeling of filamentous actin revealed profound defects in the actin cytoskeleton in both dim mutants. EM analysis revealed that the dim mutants accumulate vesicles and tubulo-vesicular structures reminiscent of mammalian early endosomes. In addition, the accumulation of novel plasma membrane invaginations where endocytosis is likely to occur were visualized in the mutants by electron microscopy using cationized ferritin as a marker for the endocytic pathway. This new screening strategy demonstrates a role for She4p and Pan1p in endocytosis, and provides a new general method for the identification of additional endocytosis mutants.

Full Text

The Full Text of this article is available as a PDF (4.7 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams A. E., Pringle J. R. Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae. J Cell Biol. 1984 Mar;98(3):934–945. doi: 10.1083/jcb.98.3.934. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson R. G., Brown M. S., Goldstein J. L. Role of the coated endocytic vesicle in the uptake of receptor-bound low density lipoprotein in human fibroblasts. Cell. 1977 Mar;10(3):351–364. doi: 10.1016/0092-8674(77)90022-8. [DOI] [PubMed] [Google Scholar]
  3. Bauer F., Urdaci M., Aigle M., Crouzet M. Alteration of a yeast SH3 protein leads to conditional viability with defects in cytoskeletal and budding patterns. Mol Cell Biol. 1993 Aug;13(8):5070–5084. doi: 10.1128/mcb.13.8.5070. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benmerah A., Bégue B., Dautry-Varsat A., Cerf-Bensussan N. The ear of alpha-adaptin interacts with the COOH-terminal domain of the Eps 15 protein. J Biol Chem. 1996 May 17;271(20):12111–12116. doi: 10.1074/jbc.271.20.12111. [DOI] [PubMed] [Google Scholar]
  5. Benmerah A., Gagnon J., Bègue B., Mégarbané B., Dautry-Varsat A., Cerf-Bensussan N. The tyrosine kinase substrate eps15 is constitutively associated with the plasma membrane adaptor AP-2. J Cell Biol. 1995 Dec;131(6 Pt 2):1831–1838. doi: 10.1083/jcb.131.6.1831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Boeck R., Tarun S., Jr, Rieger M., Deardorff J. A., Müller-Auer S., Sachs A. B. The yeast Pan2 protein is required for poly(A)-binding protein-stimulated poly(A)-nuclease activity. J Biol Chem. 1996 Jan 5;271(1):432–438. doi: 10.1074/jbc.271.1.432. [DOI] [PubMed] [Google Scholar]
  7. Bénédetti H., Raths S., Crausaz F., Riezman H. 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. 1994 Sep;5(9):1023–1037. doi: 10.1091/mbc.5.9.1023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cain C. C., Wilson R. B., Murphy R. F. Isolation by fluorescence-activated cell sorting of Chinese hamster ovary cell lines with pleiotropic, temperature-conditional defects in receptor recycling. J Biol Chem. 1991 Jun 25;266(18):11746–11752. [PubMed] [Google Scholar]
  9. Callebaut I., Renoir J. M., Lebeau M. C., Massol N., Burny A., Baulieu E. E., Mornon J. P. An immunophilin that binds M(r) 90,000 heat shock protein: main structural features of a mammalian p59 protein. Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6270–6274. doi: 10.1073/pnas.89.14.6270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chant J., Pringle J. R. Patterns of bud-site selection in the yeast Saccharomyces cerevisiae. J Cell Biol. 1995 May;129(3):751–765. doi: 10.1083/jcb.129.3.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Damke H., Baba T., van der Bliek A. M., Schmid S. L. Clathrin-independent pinocytosis is induced in cells overexpressing a temperature-sensitive mutant of dynamin. J Cell Biol. 1995 Oct;131(1):69–80. doi: 10.1083/jcb.131.1.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Drubin D. G., Mulholland J., Zhu Z. M., Botstein D. Homology of a yeast actin-binding protein to signal transduction proteins and myosin-I. Nature. 1990 Jan 18;343(6255):288–290. doi: 10.1038/343288a0. [DOI] [PubMed] [Google Scholar]
  13. Dulic V., Egerton M., Elguindi I., Raths S., Singer B., Riezman H. Yeast endocytosis assays. Methods Enzymol. 1991;194:697–710. doi: 10.1016/0076-6879(91)94051-d. [DOI] [PubMed] [Google Scholar]
  14. Fazioli F., Minichiello L., Matoskova B., Wong W. T., Di Fiore P. P. eps15, a novel tyrosine kinase substrate, exhibits transforming activity. Mol Cell Biol. 1993 Sep;13(9):5814–5828. doi: 10.1128/mcb.13.9.5814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gammie A. E., Kurihara L. J., Vallee R. B., Rose M. D. DNM1, a dynamin-related gene, participates in endosomal trafficking in yeast. J Cell Biol. 1995 Aug;130(3):553–566. doi: 10.1083/jcb.130.3.553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gascón S., Neumann N. P., Lampen J. O. Comparative study of the properties of the purified internal and external invertases from yeast. J Biol Chem. 1968 Apr 10;243(7):1573–1577. [PubMed] [Google Scholar]
  17. Geli M. I., Riezman H. Role of type I myosins in receptor-mediated endocytosis in yeast. Science. 1996 Apr 26;272(5261):533–535. doi: 10.1126/science.272.5261.533. [DOI] [PubMed] [Google Scholar]
  18. Gottlieb T. A., Ivanov I. E., Adesnik M., Sabatini D. D. Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J Cell Biol. 1993 Feb;120(3):695–710. doi: 10.1083/jcb.120.3.695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Govindan B., Bowser R., Novick P. The role of Myo2, a yeast class V myosin, in vesicular transport. J Cell Biol. 1995 Mar;128(6):1055–1068. doi: 10.1083/jcb.128.6.1055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hemmaplardh D., Morgan E. H. Transferrin uptake and release by reticulocytes treated with proteolytic enzymes and neuraminidase. Biochim Biophys Acta. 1976 Mar 19;426(3):385–398. doi: 10.1016/0005-2736(76)90384-9. [DOI] [PubMed] [Google Scholar]
  21. Herman P. K., Emr S. D. Characterization of VPS34, a gene required for vacuolar protein sorting and vacuole segregation in Saccharomyces cerevisiae. Mol Cell Biol. 1990 Dec;10(12):6742–6754. doi: 10.1128/mcb.10.12.6742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Herzog V., Farquhar M. G. Use of electron-opaque tracers for studies on endocytosis and membrane recycling. Methods Enzymol. 1983;98:203–225. doi: 10.1016/0076-6879(83)98150-8. [DOI] [PubMed] [Google Scholar]
  23. Hewlett L. J., Prescott A. R., Watts C. The coated pit and macropinocytic pathways serve distinct endosome populations. J Cell Biol. 1994 Mar;124(5):689–703. doi: 10.1083/jcb.124.5.689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ho M. N., Hill K. J., Lindorfer M. A., Stevens T. H. Isolation of vacuolar membrane H(+)-ATPase-deficient yeast mutants; the VMA5 and VMA4 genes are essential for assembly and activity of the vacuolar H(+)-ATPase. J Biol Chem. 1993 Jan 5;268(1):221–227. [PubMed] [Google Scholar]
  25. Holtzman D. A., Yang S., Drubin D. G. Synthetic-lethal interactions identify two novel genes, SLA1 and SLA2, that control membrane cytoskeleton assembly in Saccharomyces cerevisiae. J Cell Biol. 1993 Aug;122(3):635–644. doi: 10.1083/jcb.122.3.635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Jansen R. P., Dowzer C., Michaelis C., Galova M., Nasmyth K. Mother cell-specific HO expression in budding yeast depends on the unconventional myosin myo4p and other cytoplasmic proteins. Cell. 1996 Mar 8;84(5):687–697. doi: 10.1016/s0092-8674(00)81047-8. [DOI] [PubMed] [Google Scholar]
  27. Johnston G. C., Prendergast J. A., Singer R. A. The Saccharomyces cerevisiae MYO2 gene encodes an essential myosin for vectorial transport of vesicles. J Cell Biol. 1991 May;113(3):539–551. doi: 10.1083/jcb.113.3.539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Karin M., Mintz B. Receptor-mediated endocytosis of transferrin in developmentally totipotent mouse teratocarcinoma stem cells. J Biol Chem. 1981 Apr 10;256(7):3245–3252. [PubMed] [Google Scholar]
  29. Kilmartin J. V., Adams A. E. Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccharomyces. J Cell Biol. 1984 Mar;98(3):922–933. doi: 10.1083/jcb.98.3.922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kübler E., Riezman H. Actin and fimbrin are required for the internalization step of endocytosis in yeast. EMBO J. 1993 Jul;12(7):2855–2862. doi: 10.1002/j.1460-2075.1993.tb05947.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kübler E., Schimmöller F., Riezman H. Calcium-independent calmodulin requirement for endocytosis in yeast. EMBO J. 1994 Dec 1;13(23):5539–5546. doi: 10.1002/j.1460-2075.1994.tb06891.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lamaze C., Schmid S. L. The emergence of clathrin-independent pinocytic pathways. Curr Opin Cell Biol. 1995 Aug;7(4):573–580. doi: 10.1016/0955-0674(95)80015-8. [DOI] [PubMed] [Google Scholar]
  33. Lemmon S., Lemmon V. P., Jones E. W. Characterization of yeast clathrin and anticlathrin heavy-chain monoclonal antibodies. J Cell Biochem. 1988 Apr;36(4):329–340. doi: 10.1002/jcb.240360403. [DOI] [PubMed] [Google Scholar]
  34. Liu H., Bretscher A. Characterization of TPM1 disrupted yeast cells indicates an involvement of tropomyosin in directed vesicular transport. J Cell Biol. 1992 Jul;118(2):285–299. doi: 10.1083/jcb.118.2.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Mueller S. C., Branton D. Identification of coated vesicles in Saccharomyces cerevisiae. J Cell Biol. 1984 Jan;98(1):341–346. doi: 10.1083/jcb.98.1.341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Mulholland J., Preuss D., Moon A., Wong A., Drubin D., Botstein D. Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane. J Cell Biol. 1994 Apr;125(2):381–391. doi: 10.1083/jcb.125.2.381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Munn A. L., Riezman H. Endocytosis is required for the growth of vacuolar H(+)-ATPase-defective yeast: identification of six new END genes. J Cell Biol. 1994 Oct;127(2):373–386. doi: 10.1083/jcb.127.2.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Munn A. L., Stevenson B. J., Geli M. I., Riezman H. end5, end6, and end7: mutations that cause actin delocalization and block the internalization step of endocytosis in Saccharomyces cerevisiae. Mol Biol Cell. 1995 Dec;6(12):1721–1742. doi: 10.1091/mbc.6.12.1721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Murphy R. F., Jorgensen E. D., Cantor C. R. Kinetics of histone endocytosis in Chinese hamster ovary cells. A flow cytofluorometric analysis. J Biol Chem. 1982 Feb 25;257(4):1695–1701. [PubMed] [Google Scholar]
  40. Nasmyth K. Regulating the HO endonuclease in yeast. Curr Opin Genet Dev. 1993 Apr;3(2):286–294. doi: 10.1016/0959-437x(93)90036-o. [DOI] [PubMed] [Google Scholar]
  41. Nelson H., Nelson N. Disruption of genes encoding subunits of yeast vacuolar H(+)-ATPase causes conditional lethality. Proc Natl Acad Sci U S A. 1990 May;87(9):3503–3507. doi: 10.1073/pnas.87.9.3503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Novick P., Botstein D. Phenotypic analysis of temperature-sensitive yeast actin mutants. Cell. 1985 Feb;40(2):405–416. doi: 10.1016/0092-8674(85)90154-0. [DOI] [PubMed] [Google Scholar]
  43. Ottosen P. D., Courtoy P. J., Farquhar M. G. Pathways followed by membrane recovered from the surface of plasma cells and myeloma cells. J Exp Med. 1980 Jul 1;152(1):1–19. doi: 10.1084/jem.152.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Parton R. G., Joggerst B., Simons K. Regulated internalization of caveolae. J Cell Biol. 1994 Dec;127(5):1199–1215. doi: 10.1083/jcb.127.5.1199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Payne G. S., Baker D., van Tuinen E., Schekman R. Protein transport to the vacuole and receptor-mediated endocytosis by clathrin heavy chain-deficient yeast. J Cell Biol. 1988 May;106(5):1453–1461. doi: 10.1083/jcb.106.5.1453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Payne G. S., Hasson T. B., Hasson M. S., Schekman R. Genetic and biochemical characterization of clathrin-deficient Saccharomyces cerevisiae. Mol Cell Biol. 1987 Nov;7(11):3888–3898. doi: 10.1128/mcb.7.11.3888. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Payne G. S., Schekman R. A test of clathrin function in protein secretion and cell growth. Science. 1985 Nov 29;230(4729):1009–1014. doi: 10.1126/science.2865811. [DOI] [PubMed] [Google Scholar]
  48. Pearse B. M., Crowther R. A. Structure and assembly of coated vesicles. Annu Rev Biophys Biophys Chem. 1987;16:49–68. doi: 10.1146/annurev.bb.16.060187.000405. [DOI] [PubMed] [Google Scholar]
  49. Raths S., Rohrer J., Crausaz F., Riezman H. end3 and end4: two mutants defective in receptor-mediated and fluid-phase endocytosis in Saccharomyces cerevisiae. J Cell Biol. 1993 Jan;120(1):55–65. doi: 10.1083/jcb.120.1.55. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Ren R., Mayer B. J., Cicchetti P., Baltimore D. Identification of a ten-amino acid proline-rich SH3 binding site. Science. 1993 Feb 19;259(5098):1157–1161. doi: 10.1126/science.8438166. [DOI] [PubMed] [Google Scholar]
  51. Rieder S. E., Banta L. M., Köhrer K., McCaffery J. M., Emr S. D. Multilamellar endosome-like compartment accumulates in the yeast vps28 vacuolar protein sorting mutant. Mol Biol Cell. 1996 Jun;7(6):985–999. doi: 10.1091/mbc.7.6.985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Robinson J. S., Klionsky D. J., Banta L. M., Emr S. D. Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol Cell Biol. 1988 Nov;8(11):4936–4948. doi: 10.1128/mcb.8.11.4936. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Rose M. D., Novick P., Thomas J. H., Botstein D., Fink G. R. A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene. 1987;60(2-3):237–243. doi: 10.1016/0378-1119(87)90232-0. [DOI] [PubMed] [Google Scholar]
  54. Rothberg K. G., Heuser J. E., Donzell W. C., Ying Y. S., Glenney J. R., Anderson R. G. Caveolin, a protein component of caveolae membrane coats. Cell. 1992 Feb 21;68(4):673–682. doi: 10.1016/0092-8674(92)90143-z. [DOI] [PubMed] [Google Scholar]
  55. Rothberg K. G., Ying Y. S., Kolhouse J. F., Kamen B. A., Anderson R. G. The glycophospholipid-linked folate receptor internalizes folate without entering the clathrin-coated pit endocytic pathway. J Cell Biol. 1990 Mar;110(3):637–649. doi: 10.1083/jcb.110.3.637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Russo P., Kalkkinen N., Sareneva H., Paakkola J., Makarow M. A heat shock gene from Saccharomyces cerevisiae encoding a secretory glycoprotein. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8857–8857. doi: 10.1073/pnas.89.18.8857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Sachs A. B., Deardorff J. A. Translation initiation requires the PAB-dependent poly(A) ribonuclease in yeast. Cell. 1992 Sep 18;70(6):961–973. doi: 10.1016/0092-8674(92)90246-9. [DOI] [PubMed] [Google Scholar]
  58. Sandvig K., van Deurs B. Endocytosis without clathrin. Trends Cell Biol. 1994 Aug;4(8):275–277. doi: 10.1016/0962-8924(94)90211-9. [DOI] [PubMed] [Google Scholar]
  59. Schumacher C., Knudsen B. S., Ohuchi T., Di Fiore P. P., Glassman R. H., Hanafusa H. The SH3 domain of Crk binds specifically to a conserved proline-rich motif in Eps15 and Eps15R. J Biol Chem. 1995 Jun 23;270(25):15341–15347. doi: 10.1074/jbc.270.25.15341. [DOI] [PubMed] [Google Scholar]
  60. Seaman M. N., Burd C. G., Emr S. D. Receptor signalling and the regulation of endocytic membrane transport. Curr Opin Cell Biol. 1996 Aug;8(4):549–556. doi: 10.1016/s0955-0674(96)80034-2. [DOI] [PubMed] [Google Scholar]
  61. Sheetz M. P., Dai J. Modulation of membrane dynamics and cell motility by membrane tension. Trends Cell Biol. 1996 Mar;6(3):85–89. doi: 10.1016/0962-8924(96)80993-7. [DOI] [PubMed] [Google Scholar]
  62. Shortle D., Novick P., Botstein D. Construction and genetic characterization of temperature-sensitive mutant alleles of the yeast actin gene. Proc Natl Acad Sci U S A. 1984 Aug;81(15):4889–4893. doi: 10.1073/pnas.81.15.4889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Singer B., Riezman H. Detection of an intermediate compartment involved in transport of alpha-factor from the plasma membrane to the vacuole in yeast. J Cell Biol. 1990 Jun;110(6):1911–1922. doi: 10.1083/jcb.110.6.1911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Sivadon P., Bauer F., Aigle M., Crouzet M. 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. 1995 Feb 20;246(4):485–495. doi: 10.1007/BF00290452. [DOI] [PubMed] [Google Scholar]
  65. Smythe E., Carter L. L., Schmid S. L. Cytosol- and clathrin-dependent stimulation of endocytosis in vitro by purified adaptors. J Cell Biol. 1992 Dec;119(5):1163–1171. doi: 10.1083/jcb.119.5.1163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Stevens T., Esmon B., Schekman R. Early stages in the yeast secretory pathway are required for transport of carboxypeptidase Y to the vacuole. Cell. 1982 Sep;30(2):439–448. doi: 10.1016/0092-8674(82)90241-0. [DOI] [PubMed] [Google Scholar]
  67. Tan P. K., Davis N. G., Sprague G. F., Payne G. S. Clathrin facilitates the internalization of seven transmembrane segment receptors for mating pheromones in yeast. J Cell Biol. 1993 Dec;123(6 Pt 2):1707–1716. doi: 10.1083/jcb.123.6.1707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Tang H. Y., Cai M. The EH-domain-containing protein Pan1 is required for normal organization of the actin cytoskeleton in Saccharomyces cerevisiae. Mol Cell Biol. 1996 Sep;16(9):4897–4914. doi: 10.1128/mcb.16.9.4897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Vida T. A., Emr S. D. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol. 1995 Mar;128(5):779–792. doi: 10.1083/jcb.128.5.779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Voss H., Tamames J., Teodoru C., Valencia A., Sensen C., Wiemann S., Schwager C., Zimmermann J., Sander C., Ansorge W. Nucleotide sequence and analysis of the centromeric region of yeast chromosome IX. Yeast. 1995 Jan;11(1):61–78. doi: 10.1002/yea.320110109. [DOI] [PubMed] [Google Scholar]
  71. Wang Y. X., Zhao H., Harding T. M., Gomes de Mesquita D. S., Woldringh C. L., Klionsky D. J., Munn A. L., Weisman L. S. Multiple classes of yeast mutants are defective in vacuole partitioning yet target vacuole proteins correctly. Mol Biol Cell. 1996 Sep;7(9):1375–1389. doi: 10.1091/mbc.7.9.1375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. West M. A., Bretscher M. S., Watts C. Distinct endocytotic pathways in epidermal growth factor-stimulated human carcinoma A431 cells. J Cell Biol. 1989 Dec;109(6 Pt 1):2731–2739. doi: 10.1083/jcb.109.6.2731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Willingham M. C., Pastan I. H. Transit of epidermal growth factor through coated pits of the Golgi system. J Cell Biol. 1982 Jul;94(1):207–212. doi: 10.1083/jcb.94.1.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Wong W. T., Schumacher C., Salcini A. E., Romano A., Castagnino P., Pelicci P. G., Di Fiore P. P. A protein-binding domain, EH, identified in the receptor tyrosine kinase substrate Eps15 and conserved in evolution. Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9530–9534. doi: 10.1073/pnas.92.21.9530. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  76. Yu H., Chen J. K., Feng S., Dalgarno D. C., Brauer A. W., Schreiber S. L. Structural basis for the binding of proline-rich peptides to SH3 domains. Cell. 1994 Mar 11;76(5):933–945. doi: 10.1016/0092-8674(94)90367-0. [DOI] [PubMed] [Google Scholar]
  77. Zoladek T., Vaduva G., Hunter L. A., Boguta M., Go B. D., Martin N. C., Hopper A. K. Mutations altering the mitochondrial-cytoplasmic distribution of Mod5p implicate the actin cytoskeleton and mRNA 3' ends and/or protein synthesis in mitochondrial delivery. Mol Cell Biol. 1995 Dec;15(12):6884–6894. doi: 10.1128/mcb.15.12.6884. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES