Home LiteratureArticle Details
PMID: 8682864 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Synthetic lethality screen identifies a novel yeast myosin I gene (MYO5): myosin I proteins are required for polarization of the actin cytoskeleton.

The Journal of cell biology ·Vol. 133 ·No. 6 ·1996-06-00 ·Pages 1277-91

Goodson HV, Anderson BL, Warrick HM, Pon LA, Spudich JA

Abstract

The organization of the actin cytoskeleton plays a critical role in cell physiology in motile and nonmotile organisms. Nonetheless, the function of the actin based motor molecules, members of the myosin superfamily, is not well understood. Deletion of MYO3, a yeast gene encoding a "classic" myosin I, has no detectable phenotype. We used a synthetic lethality screen to uncover genes whose functions might overlap with those of MYO3 and identified a second yeast myosin 1 gene, MYO5. MYO5 shows 86 and 62% identity to MYO3 across the motor and non-motor regions. Both genes contain an amino terminal motor domain, a neck region containing two IQ motifs, and a tail domain consisting of a positively charged region, a proline-rich region containing sequences implicated in ATP-insensitive actin binding, and an SH3 domain. Although myo5 deletion mutants have no detectable phenotype, yeast strains deleted for both MYO3 and MYO5 have severe defects in growth and actin cytoskeletal organization. Double deletion mutants also display phenotypes associated with actin disorganization including accumulation of intracellular membranes and vesicles, cell rounding, random bud site selection, sensitivity to high osmotic strength, and low pH as well as defects in chitin and cell wall deposition, invertase secretion, and fluid phase endocytosis. Indirect immunofluorescence studies using epitope-tagged Myo5p indicate that Myo5p is localized at actin patches. These results indicate that MYO3 and MYO5 encode classical myosin I proteins with overlapping functions and suggest a role for Myo3p and Myo5p in organization of the actin cytoskeleton of Saccharomyces cerevisiae.

MeSH Terms
Actins/analysis Amino Acid Sequence Base Sequence Cell Membrane/ultrastructure Chitin/analysis Cloning, Molecular Cytoskeleton/chemistry DNA, Fungal/genetics Endocytosis Fungal Proteins/analysis,genetics,physiology Genes, Fungal/genetics Genes, Lethal/genetics Genetic Complementation Test Glycoside Hydrolases/metabolism Molecular Sequence Data Myosin Type I Myosins/analysis,genetics,physiology Organelles/ultrastructure Phenotype Saccharomyces cerevisiae/cytology,genetics,growth & development Saccharomyces cerevisiae Proteins Sequence Analysis, DNA Sequence Deletion Sequence Homology, Amino Acid beta-Fructofuranosidase
Chemicals
Actins DNA, Fungal Fungal Proteins MYO5 protein, S cerevisiae Saccharomyces cerevisiae Proteins Chitin Glycoside Hydrolases beta-Fructofuranosidase Myosin Type I Myosins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Goodson H V
Department of Biochemistry, Stanford University, CA 94305, USA.
Anderson B L
Warrick H M
Pon L A
Spudich J A
References (58)
58 references, click to expand
  1. Myosin IB null mutants of Dictyostelium exhibit abnormalities in motility.
    Cell Motil Cytoskeleton. 1991;20(4):301-15 PMID: 1666340
  2. Disruption of the actin cytoskeleton in budding yeast results in formation of an aberrant cell wall.
    Microbiology. 1995 Apr;141 ( Pt 4):891-9 PMID: 7773392
  3. Use of a screen for synthetic lethal and multicopy suppressee mutants to identify two new genes involved in morphogenesis in Saccharomyces cerevisiae.
    Mol Cell Biol. 1991 Mar;11(3):1295-305 PMID: 1996092
  4. Regulation of cortical actin cytoskeleton assembly during polarized cell growth in budding yeast.
    J Cell Biol. 1995 Feb;128(4):599-615 PMID: 7860633
  5. Actin and fimbrin are required for the internalization step of endocytosis in yeast.
    EMBO J. 1993 Jul;12(7):2855-62 PMID: 8335001
  6. Chitin synthesis and localization in cell division cycle mutants of Saccharomyces cerevisiae.
    Mol Cell Biol. 1983 May;3(5):922-30 PMID: 6223209
  7. Immunofluorescence methods for yeast.
    Methods Enzymol. 1991;194:565-602 PMID: 2005809
  8. Localization and specificity of the phospholipid and actin binding sites on the tail of Acanthamoeba myosin IC.
    J Cell Biol. 1992 Jun;117(6):1241-9 PMID: 1607386
  9. Review: cell wall assembly in yeast.
    Yeast. 1994 Jul;10(7):851-69 PMID: 7985414
  10. Actin structure and function: roles in mitochondrial organization and morphogenesis in budding yeast and identification of the phalloidin-binding site.
    Mol Biol Cell. 1993 Dec;4(12):1277-94 PMID: 8167410
  11. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product.
    Mol Cell Biol. 1985 Dec;5(12):3610-6 PMID: 3915782
  12. Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane.
    J Cell Biol. 1994 Apr;125(2):381-91 PMID: 8163554
  13. Myosin-I.
    Annu Rev Physiol. 1991;53:653-81 PMID: 2042976
  14. Genetic analysis of mutants of Saccharomyces cerevisiae resistant to the herbicide sulfometuron methyl.
    Genetics. 1985 Jan;109(1):21-35 PMID: 3881312
  15. Acanthamoeba myosin. I. Isolation from Acanthamoeba castellanii of an enzyme similar to muscle myosin.
    J Biol Chem. 1973 Jul 10;248(13):4682-90 PMID: 4268863
  16. Phenotypic analysis of temperature-sensitive yeast actin mutants.
    Cell. 1985 Feb;40(2):405-16 PMID: 3967297
  17. Beta-D-fructofuranoside fructohydrolase from yeast.
    Methods Enzymol. 1975;42:504-11 PMID: 237205
  18. Phylogenetic analysis of the myosin superfamily.
    Cell Motil Cytoskeleton. 1993;24(4):215-23 PMID: 8477454
  19. Motor proteins 2: myosin.
    Protein Profile. 1995;2(12):1323-1423 PMID: 8665326
  20. Classical mutagenesis techniques.
    Methods Enzymol. 1991;194:273-81 PMID: 2005792
  21. Molecular evolution of the myosin family: relationships derived from comparisons of amino acid sequences.
    Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):659-63 PMID: 8421702
  22. Actin-dependent mitochondrial motility in mitotic yeast and cell-free systems: identification of a motor activity on the mitochondrial surface.
    J Cell Biol. 1995 Jul;130(2):345-54 PMID: 7615636
  23. Single-step purification of shuttle vectors from yeast for high frequency back-transformation into E. coli.
    Nucleic Acids Res. 1990 Sep 11;18(17):5319 PMID: 2205843
  24. Osmotic stress and the yeast cytoskeleton: phenotype-specific suppression of an actin mutation.
    J Cell Biol. 1992 Aug;118(3):561-71 PMID: 1639843
  25. Dictyostelium myosin I double mutants exhibit conditional defects in pinocytosis.
    J Cell Biol. 1995 Dec;131(5):1205-21 PMID: 8522584
  26. The unconventional myosin encoded by the myoA gene plays a role in Dictyostelium motility.
    Mol Biol Cell. 1993 Feb;4(2):233-46 PMID: 8382977
  27. Autoradiographic study of mannan incorporation into the growing cell walls of Saccharomyces cerevisiae.
    J Bacteriol. 1974 Jan;117(1):265-9 PMID: 4587607
  28. Unconventional myosins.
    Curr Opin Cell Biol. 1992 Feb;4(1):27-35 PMID: 1558751
  29. Genetic evidence that Acanthamoeba myosin I is a true myosin.
    Proc Natl Acad Sci U S A. 1986 Jul;83(13):4655-9 PMID: 3014500
  30. Yeast mitochondria contain ATP-sensitive, reversible actin-binding activity.
    Mol Biol Cell. 1994 Jul;5(7):807-18 PMID: 7812049
  31. Identification and molecular characterization of a yeast myosin I.
    Cell Motil Cytoskeleton. 1995;30(1):73-84 PMID: 7728870
  32. 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
  33. Novel myosins.
    Trends Cell Biol. 1991 Aug;1(2-3):50-6 PMID: 14731566
  34. Inhibition of contractile vacuole function in vivo by antibodies against myosin-I.
    Nature. 1993 Oct 28;365(6449):841-3 PMID: 8413668
  35. Organelle-cytoskeletal interactions: actin mutations inhibit meiosis-dependent mitochondrial rearrangement in the budding yeast Saccharomyces cerevisiae.
    Mol Biol Cell. 1995 Oct;6(10):1381-96 PMID: 8573793
  36. 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
  37. Yeast actin-binding proteins: evidence for a role in morphogenesis.
    J Cell Biol. 1988 Dec;107(6 Pt 2):2551-61 PMID: 3060468
  38. Multifunctional yeast high-copy-number shuttle vectors.
    Gene. 1992 Jan 2;110(1):119-22 PMID: 1544568
  39. Order of events in the yeast secretory pathway.
    Cell. 1981 Aug;25(2):461-9 PMID: 7026045
  40. Endocytosis in yeast: several of the yeast secretory mutants are defective in endocytosis.
    Cell. 1985 Apr;40(4):1001-9 PMID: 3886157
  41. Purification of profilin from Saccharomyces cerevisiae and analysis of profilin-deficient cells.
    J Cell Biol. 1990 Jan;110(1):105-14 PMID: 2404021
  42. Effects of null mutations and overexpression of capping protein on morphogenesis, actin distribution and polarized secretion in yeast.
    J Cell Biol. 1992 Dec;119(5):1151-62 PMID: 1447293
  43. The actin binding site in the tail domain of Dictyostelium myosin IC (myoC) resides within the glycine- and proline-rich sequence (tail homology region 2).
    FEBS Lett. 1994 Apr 4;342(2):197-202 PMID: 8143877
  44. Requirement of yeast fimbrin for actin organization and morphogenesis in vivo.
    Nature. 1991 Dec 5;354(6352):404-8 PMID: 1956405
  45. The GPQ-rich segment of Dictyostelium myosin IB contains an actin binding site.
    Biochemistry. 1994 Mar 1;33(8):2322-8 PMID: 8117689
  46. ATPase activities and actin-binding properties of subfragments of Acanthamoeba myosin IA.
    J Biol Chem. 1986 Dec 25;261(36):17156-62 PMID: 2946692
  47. Alteration of a yeast SH3 protein leads to conditional viability with defects in cytoskeletal and budding patterns.
    Mol Cell Biol. 1993 Aug;13(8):5070-84 PMID: 8336735
  48. Identification of MYO4, a second class V myosin gene in yeast.
    J Cell Sci. 1994 Apr;107 ( Pt 4):1055-64 PMID: 8056830
  49. Nucleotide sequence of the yeast ILV2 gene which encodes acetolactate synthase.
    Nucleic Acids Res. 1985 Jun 11;13(11):4011-27 PMID: 2989783
  50. Binding of myosin I to membrane lipids.
    Nature. 1989 Aug 17;340(6234):565-8 PMID: 2770861
  51. myoA of Aspergillus nidulans encodes an essential myosin I required for secretion and polarized growth.
    J Cell Biol. 1995 Feb;128(4):577-87 PMID: 7860631
  52. Yeast myosin heavy chain mutant: maintenance of the cell type specific budding pattern and the normal deposition of chitin and cell wall components requires an intact myosin heavy chain gene.
    Cell Motil Cytoskeleton. 1990;17(4):301-8 PMID: 2076546
  53. Sequence, expression pattern, intracellular localization, and targeted disruption of the Dictyostelium myosin ID heavy chain isoform.
    J Biol Chem. 1993 Jul 15;268(20):14981-90 PMID: 8325874
  54. Molecular motors, membrane movements and physiology: emerging roles for myosins.
    Curr Opin Cell Biol. 1995 Aug;7(4):587-94 PMID: 7495580
  55. Generation and characterization of Dictyostelium cells deficient in a myosin I heavy chain isoform.
    J Cell Biol. 1990 Jun;110(6):1955-64 PMID: 2141028
  56. Characterization of TPM1 disrupted yeast cells indicates an involvement of tropomyosin in directed vesicular transport.
    J Cell Biol. 1992 Jul;118(2):285-99 PMID: 1629236
  57. 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):485-95 PMID: 7891662
  58. Genetic analysis of the yeast cytoskeleton.
    Annu Rev Genet. 1987;21:259-84 PMID: 3327466
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1996-06-00
Pages
1277-91
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2120899
Subset
IM
Grants
NIGMS NIH HHS · 5T32 GM07367 · United States
NIGMS NIH HHS · GM40509 · United States
NIGMS NIH HHS · GM45735 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]