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PMID: 9234686 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

EH domain proteins Pan1p and End3p are components of a complex that plays a dual role in organization of the cortical actin cytoskeleton and endocytosis in Saccharomyces cerevisiae.

Molecular and cellular biology ·Vol. 17 ·No. 8 ·1997-08-00 ·Pages 4294-304

Tang HY, Munn A, Cai M

Abstract

Several proteins from diverse organisms have been shown to share a region of sequence homology with the mammalian epidermal growth factor receptor tyrosine kinase substrate Eps15. Included in this new protein family, termed EH domain proteins, are two yeast proteins, Pan1p and End3p. We have shown previously that Pan1p is required for normal organization of the actin cytoskeleton and that it associates with the actin patches on the cell cortex. End3p has been shown by others to be an important factor in the process of endocytosis. End3p is also known to be required for the organization of the actin cytoskeleton. Here we report that Pan1p and End3p act as a complex in vivo. Using the pan1-4 mutant which we isolated and characterized previously, the END3 gene was identified as a suppressor of pan1-4 when overexpressed. Suppression of the pan1-4 mutation by multicopy END3 required the presence of the mutant Pan1p protein. Coimmunoprecipitation and two-hybrid protein interaction experiments indicated that Pan1p and End3p associate with each other. The localization of Pan1p to the cortical actin cytoskeleton became weakened in the end3 mutant at the permissive temperature and undetectable at the restrictive temperature, suggesting that End3p may be important for proper localization of Pan1p to the cortical actin cytoskeleton. The finding that the pan1-4 mutant was defective in endocytosis as severely as the end3 mutant under nonpermissive conditions supports the notion that the association between Pan1p and End3p is of physiological relevance. Together with results of earlier reports, these results provide strong evidence suggesting that Pan1p and End3p are the components of a complex that has essential functions in both the organization of cell membrane-associated actin cytoskeleton and the process of endocytosis.

MeSH Terms
Actins/metabolism Cytoskeletal Proteins Cytoskeleton/metabolism Endocytosis/genetics Fungal Proteins/genetics,metabolism Genes, Fungal/genetics Genetic Complementation Test Mating Factor Peptides/metabolism Saccharomyces cerevisiae/cytology,genetics,metabolism Saccharomyces cerevisiae Proteins Sequence Homology, Amino Acid Suppression, Genetic
Chemicals
Actins Cytoskeletal Proteins END3 protein, S cerevisiae Fungal Proteins Peptides Saccharomyces cerevisiae Proteins Mating Factor
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Tang H Y
Institute of Molecular and Cell Biology, National University of Singapore, Singapore.
Munn A
Cai M
References (50)
50 references, click to expand
  1. Signal-dependent membrane protein trafficking in the endocytic pathway.
    Annu Rev Cell Biol. 1993;9:129-61 PMID: 8280459
  2. The role of clathrin, adaptors and dynamin in endocytosis.
    Curr Opin Cell Biol. 1994 Aug;6(4):538-44 PMID: 7986531
  3. Recruitment of epidermal growth factor and transferrin receptors into coated pits in vitro: differing biochemical requirements.
    Mol Biol Cell. 1993 Jul;4(7):715-27 PMID: 8400457
  4. Endocytosis and degradation of the yeast uracil permease under adverse conditions.
    J Biol Chem. 1994 Apr 1;269(13):9833-41 PMID: 8144575
  5. A novel genetic system to detect protein-protein interactions.
    Nature. 1989 Jul 20;340(6230):245-6 PMID: 2547163
  6. Translation initiation requires the PAB-dependent poly(A) ribonuclease in yeast.
    Cell. 1992 Sep 18;70(6):961-73 PMID: 1339314
  7. Yeast endocytosis assays.
    Methods Enzymol. 1991;194:697-710 PMID: 2005817
  8. Actin and fimbrin are required for the internalization step of endocytosis in yeast.
    EMBO J. 1993 Jul;12(7):2855-62 PMID: 8335001
  9. eps15, a novel tyrosine kinase substrate, exhibits transforming activity.
    Mol Cell Biol. 1993 Sep;13(9):5814-28 PMID: 7689153
  10. Endocytosis and lysosomal targeting of epidermal growth factor receptors are mediated by distinct sequences independent of the tyrosine kinase domain.
    J Biol Chem. 1995 Mar 3;270(9):4325-33 PMID: 7876194
  11. Endocytosis of growth factor receptors.
    Bioessays. 1993 Jun;15(6):375-82 PMID: 8395172
  12. The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants.
    EMBO J. 1994 Jul 15;13(14):3261-71 PMID: 8045256
  13. Clathrin, adaptors, and sorting.
    Annu Rev Cell Biol. 1990;6:151-71 PMID: 2177341
  14. Recruitment of epidermal growth factor receptors into coated pits requires their activated tyrosine kinase.
    J Cell Biol. 1995 Apr;129(1):47-54 PMID: 7698994
  15. Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane.
    J Cell Biol. 1994 Apr;125(2):381-91 PMID: 8163554
  16. To shape a cell: an inquiry into the causes of morphogenesis of microorganisms.
    Microbiol Rev. 1990 Dec;54(4):381-431 PMID: 2128368
  17. In vitro mutagenesis and plasmid shuffling: from cloned gene to mutant yeast.
    Methods Enzymol. 1991;194:302-18 PMID: 2005795
  18. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
    Genetics. 1989 May;122(1):19-27 PMID: 2659436
  19. 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):9530-4 PMID: 7568168
  20. Receptor signalling and the regulation of endocytic membrane transport.
    Curr Opin Cell Biol. 1996 Aug;8(4):549-56 PMID: 8791448
  21. 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):4897-914 PMID: 8756649
  22. Purification of tropomyosin from Saccharomyces cerevisiae and identification of related proteins in Schizosaccharomyces and Physarum.
    Proc Natl Acad Sci U S A. 1989 Jan;86(1):90-3 PMID: 2643110
  23. Yeast endocytosis.
    Trends Cell Biol. 1993 Aug;3(8):273-7 PMID: 14731746
  24. The yeast Pan2 protein is required for poly(A)-binding protein-stimulated poly(A)-nuclease activity.
    J Biol Chem. 1996 Jan 5;271(1):432-8 PMID: 8550599
  25. 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):373-86 PMID: 7929582
  26. The Saccharomyces cerevisiae MYO2 gene encodes an essential myosin for vectorial transport of vesicles.
    J Cell Biol. 1991 May;113(3):539-51 PMID: 2016335
  27. A novel fluorescence-activated cell sorter-based screen for yeast endocytosis mutants identifies a yeast homologue of mammalian eps15.
    J Cell Biol. 1996 Dec;135(6 Pt 1):1485-500 PMID: 8978817
  28. 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):635-44 PMID: 8335689
  29. Yeast actin-binding proteins: evidence for a role in morphogenesis.
    J Cell Biol. 1988 Dec;107(6 Pt 2):2551-61 PMID: 3060468
  30. Multifunctional yeast high-copy-number shuttle vectors.
    Gene. 1992 Jan 2;110(1):119-22 PMID: 1544568
  31. Stoichiometric interaction of the epidermal growth factor receptor with the clathrin-associated protein complex AP-2.
    J Biol Chem. 1995 Jan 13;270(2):619-25 PMID: 7822287
  32. Two yeast mutants defective in endocytosis are defective in pheromone response.
    Cell. 1986 Aug 1;46(3):355-64 PMID: 3524852
  33. The tyrosine kinase substrate eps15 is constitutively associated with the plasma membrane adaptor AP-2.
    J Cell Biol. 1995 Dec;131(6 Pt 2):1831-8 PMID: 8557749
  34. Purification of profilin from Saccharomyces cerevisiae and analysis of profilin-deficient cells.
    J Cell Biol. 1990 Jan;110(1):105-14 PMID: 2404021
  35. 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):1721-42 PMID: 8590801
  36. Calcium-independent calmodulin requirement for endocytosis in yeast.
    EMBO J. 1994 Dec 1;13(23):5539-46 PMID: 7988551
  37. 5-Fluoroorotic acid as a selective agent in yeast molecular genetics.
    Methods Enzymol. 1987;154:164-75 PMID: 3323810
  38. 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):1023-37 PMID: 7841519
  39. Membrane dynamics in endocytosis.
    Cell. 1996 Jan 12;84(1):13-21 PMID: 8548817
  40. Receptor tyrosine kinases and their targets.
    Curr Opin Genet Dev. 1994 Feb;4(1):5-14 PMID: 8193540
  41. Analyzing protein-protein interactions using two-hybrid system.
    Methods Enzymol. 1995;254:241-63 PMID: 8531690
  42. The Saccharomyces cerevisiae BAR1 gene encodes an exported protein with homology to pepsin.
    Proc Natl Acad Sci U S A. 1988 Jan;85(1):55-9 PMID: 3124102
  43. Association of epidermal growth factor receptors with coated pit adaptins via a tyrosine phosphorylation-regulated mechanism.
    J Biol Chem. 1995 Mar 17;270(11):6320-7 PMID: 7534311
  44. 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 PMID: 8380177
  45. 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 PMID: 8381123
  46. Eps15 is a component of clathrin-coated pits and vesicles and is located at the rim of coated pits.
    J Biol Chem. 1996 Nov 15;271(46):28727-30 PMID: 8910509
  47. Melatonin madness.
    Cell. 1995 Dec 29;83(7):1059-62 PMID: 8548792
  48. MDP1, a Saccharomyces cerevisiae gene involved in mitochondrial/cytoplasmic protein distribution, is identical to the ubiquitin-protein ligase gene RSP5.
    Genetics. 1997 Mar;145(3):595-603 PMID: 9055070
  49. Regulation of inositol transport in Saccharomyces cerevisiae involves inositol-induced changes in permease stability and endocytic degradation in the vacuole.
    J Biol Chem. 1995 Feb 10;270(6):2525-34 PMID: 7852314
  50. Nucleotide sequence and analysis of the centromeric region of yeast chromosome IX.
    Yeast. 1995 Jan;11(1):61-78 PMID: 7762303
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1997-08-00
Pages
4294-304
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC232282
Subset
IM
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