Home LiteratureArticle Details
PMID: 9490720 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Vac8p, a vacuolar protein with armadillo repeats, functions in both vacuole inheritance and protein targeting from the cytoplasm to vacuole.

The Journal of cell biology ·Vol. 140 ·No. 5 ·1998-03-09 ·Pages 1063-74

Wang YX, Catlett NL, Weisman LS

Abstract

During each cell cycle, the yeast vacuole actively partitions between mother and daughter cells. This process requires actin, profilin, an unconventional myosin (Myo2p), and Vac8p. A mutant yeast strain, vac8, is defective in vacuole inheritance, specifically, in early vacuole migration. Vac8p is a 64-kD protein found on the vacuole membrane, a site consistent with its role in vacuole inheritance. Both myristoylation and palmitoylation are required for complete Vac8p localization. Interestingly, whereas myristoylation of Vac8p is not required for vacuole inheritance, palmitoylation is essential. Thus, palmitoylation appears to play a more direct role in vacuole inheritance. Most of the VAC8 sequence encodes 11 armadillo (Arm) repeats. Arm repeats are thought to mediate protein-protein interactions, and many Arm proteins have multiple functions. This is also true for Vac8p. In addition to its role in early vacuole inheritance, Vac8p is required to target aminopeptidase I from the cytoplasm to the vacuole. Mutant analysis demonstrates that Vac8p functions separately in these two processes. Vac8p cosediments with actin filaments. Vac8p is related to beta-catenin and plakoglobin, which connect a specific region of the plasma membrane to the actin cytoskeleton. In analogy, Vac8p may link the vacuole to actin during vacuole partitioning.

MeSH Terms
Actins/metabolism Acylation Amino Acid Sequence Animals Biological Transport Cytoplasm/metabolism Fungal Proteins/chemistry,genetics,isolation & purification,metabolism Intracellular Membranes/metabolism Lipoproteins/chemistry,genetics,isolation & purification,metabolism Membrane Proteins/chemistry,genetics,isolation & purification,metabolism Molecular Sequence Data Myristic Acids/metabolism Palmitic Acids/metabolism Proteins/metabolism Saccharomyces cerevisiae Saccharomyces cerevisiae Proteins Sequence Analysis Vacuoles/metabolism Vesicular Transport Proteins
Chemicals
Actins Fungal Proteins Lipoproteins Membrane Proteins Myristic Acids Palmitic Acids Proteins Saccharomyces cerevisiae Proteins VAC8 protein, S cerevisiae Vesicular Transport Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Wang Y X
Department of Biochemistry, University of Iowa, Iowa City, Iowa 52242, USA.
Catlett N L
Weisman L S
References (65)
65 references, click to expand
  1. Fatty acylation of alpha z. Effects of palmitoylation and myristoylation on alpha z signaling.
    J Biol Chem. 1995 Apr 21;270(16):9667-75 PMID: 7536745
  2. Characterization of new vacuolar segregation mutants, isolated by screening for loss of proteinase B self-activation.
    Eur J Cell Biol. 1996 Nov;71(3):237-47 PMID: 8929562
  3. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  4. Mitochondrial inheritance: cell cycle and actin cable dependence of polarized mitochondrial movements in Saccharomyces cerevisiae.
    Cell Motil Cytoskeleton. 1997;37(3):199-210 PMID: 9227850
  5. Sec6, Sec8, and Sec15 are components of a multisubunit complex which localizes to small bud tips in Saccharomyces cerevisiae.
    J Cell Biol. 1995 Jul;130(2):299-312 PMID: 7615633
  6. A homolog of the armadillo protein in Drosophila (plakoglobin) associated with E-cadherin.
    Science. 1991 Nov 29;254(5036):1359-61 PMID: 1962194
  7. Yeast synaptobrevin homologs are modified posttranslationally by the addition of palmitate.
    Proc Natl Acad Sci U S A. 1995 Jun 20;92(13):5987-91 PMID: 7597066
  8. Genetic and phenotypic overlap between autophagy and the cytoplasm to vacuole protein targeting pathway.
    J Biol Chem. 1996 Jul 26;271(30):17621-4 PMID: 8663607
  9. Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase.
    Anal Biochem. 1991 Feb 1;192(2):262-7 PMID: 1852137
  10. A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector.
    Gene. 1987;60(2-3):237-43 PMID: 3327750
  11. A versatile transcriptional effector of Wingless signaling.
    Cell. 1997 May 2;89(3):321-3 PMID: 9150130
  12. Fatty acyl-coenzyme A is required for budding of transport vesicles from Golgi cisternae.
    Cell. 1989 Oct 6;59(1):95-102 PMID: 2790961
  13. A heterodimer of thioredoxin and I(B)2 cooperates with Sec18p (NSF) to promote yeast vacuole inheritance.
    J Cell Biol. 1997 Jan 27;136(2):299-306 PMID: 9015301
  14. The GTPase Ypt7p of Saccharomyces cerevisiae is required on both partner vacuoles for the homotypic fusion step of vacuole inheritance.
    EMBO J. 1995 Nov 1;14(21):5258-70 PMID: 7489715
  15. Metabolic instability and constitutive endocytosis of STE6, the a-factor transporter of Saccharomyces cerevisiae.
    Mol Biol Cell. 1994 Nov;5(11):1185-98 PMID: 7865884
  16. Yeast Srp1p has homology to armadillo/plakoglobin/beta-catenin and participates in apparently multiple nuclear functions including the maintenance of the nucleolar structure.
    Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6880-4 PMID: 8041713
  17. Palmitoylation of a G protein alpha i subunit requires membrane localization not myristoylation.
    J Biol Chem. 1994 Dec 9;269(49):30898-903 PMID: 7983022
  18. The 25 kDa synaptosomal-associated protein SNAP-25 is the major methionine-rich polypeptide in rapid axonal transport and a major substrate for palmitoylation in adult CNS.
    J Neurosci. 1992 Dec;12(12):4634-41 PMID: 1281490
  19. Aminopeptidase I is targeted to the vacuole by a nonclassical vesicular mechanism.
    J Cell Biol. 1997 Jul 14;138(1):37-44 PMID: 9214379
  20. Organelle inheritance.
    Cell. 1996 Feb 9;84(3):395-400 PMID: 8608593
  21. Cell adhesion - spreading frontiers, intricate insights.
    Trends Cell Biol. 1997 Mar;7(3):107-10 PMID: 17708918
  22. The alpha-subunits of G-proteins G12 and G13 are palmitoylated, but not amidically myristoylated.
    FEBS Lett. 1994 Feb 14;339(1-2):160-4 PMID: 8313967
  23. Mutants of Saccharomyces cerevisiae that block intervacuole vesicular traffic and vacuole division and segregation.
    Proc Natl Acad Sci U S A. 1990 Feb;87(3):1076-80 PMID: 1689059
  24. vac2: a yeast mutant which distinguishes vacuole segregation from Golgi-to-vacuole protein targeting.
    EMBO J. 1991 Jul;10(7):1741-8 PMID: 2050111
  25. Partial constitutive activation of pheromone responses by a palmitoylation-site mutant of a G protein alpha subunit in yeast.
    Biochemistry. 1996 Nov 26;35(47):14806-17 PMID: 8942643
  26. Binding of acylated peptides and fatty acids to phospholipid vesicles: pertinence to myristoylated proteins.
    Biochemistry. 1993 Oct 5;32(39):10436-43 PMID: 8399188
  27. Characterization of the Saccharomyces Golgi complex through the cell cycle by immunoelectron microscopy.
    Mol Biol Cell. 1992 Jul;3(7):789-803 PMID: 1381247
  28. Protein lipidation in cell signaling.
    Science. 1995 Apr 14;268(5208):221-5 PMID: 7716512
  29. Vac7p, a novel vacuolar protein, is required for normal vacuole inheritance and morphology.
    Mol Cell Biol. 1997 Dec;17(12):6847-58 PMID: 9372916
  30. Thioredoxin is required for vacuole inheritance in Saccharomyces cerevisiae.
    J Cell Biol. 1996 Mar;132(5):787-94 PMID: 8603912
  31. Homotypic vacuole fusion requires Sec17p (yeast alpha-SNAP) and Sec18p (yeast NSF).
    EMBO J. 1996 Jul 1;15(13):3296-305 PMID: 8670830
  32. beta-Catenin associates with the actin-bundling protein fascin in a noncadherin complex.
    J Cell Biol. 1996 Sep;134(5):1271-81 PMID: 8794867
  33. Pendulin, a Drosophila protein with cell cycle-dependent nuclear localization, is required for normal cell proliferation.
    J Cell Biol. 1995 Jun;129(6):1491-507 PMID: 7790350
  34. Vacuolar segregation to the bud of Saccharomyces cerevisiae: an analysis of morphology and timing in the cell cycle.
    J Gen Microbiol. 1991 Oct;137(10):2447-54 PMID: 1770360
  35. Docking of yeast vacuoles is catalyzed by the Ras-like GTPase Ypt7p after symmetric priming by Sec18p (NSF).
    J Cell Biol. 1997 Jan 27;136(2):307-17 PMID: 9015302
  36. Covalent binding of fatty acid to the transferrin receptor in cultured human cells.
    J Biol Chem. 1981 May 25;256(10):4715-8 PMID: 6262300
  37. Lipid-modified, cysteinyl-containing peptides of diverse structures are efficiently S-acylated at the plasma membrane of mammalian cells.
    J Cell Biol. 1996 Aug;134(3):647-60 PMID: 8707845
  38. Actin and myosin function in directed vacuole movement during cell division in Saccharomyces cerevisiae.
    J Cell Biol. 1996 Dec;135(6 Pt 1):1535-49 PMID: 8978821
  39. Fatty acylation promotes fusion of transport vesicles with Golgi cisternae.
    J Cell Biol. 1990 Apr;110(4):955-61 PMID: 2324202
  40. Sec18p (NSF)-driven release of Sec17p (alpha-SNAP) can precede docking and fusion of yeast vacuoles.
    Cell. 1996 Apr 5;85(1):83-94 PMID: 8620540
  41. Genetic interactions between KAR2 and SEC63, encoding eukaryotic homologues of DnaK and DnaJ in the endoplasmic reticulum.
    Mol Biol Cell. 1993 Nov;4(11):1145-59 PMID: 8305736
  42. Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants.
    Mol Biol Cell. 1992 Dec;3(12):1389-402 PMID: 1493335
  43. The dynamic role of palmitoylation in signal transduction.
    Trends Biochem Sci. 1995 May;20(5):181-7 PMID: 7610481
  44. A polybasic domain allows nonprenylated Ras proteins to function in Saccharomyces cerevisiae.
    J Biol Chem. 1994 Aug 26;269(34):21540-6 PMID: 8063791
  45. Intervacuole exchange in the yeast zygote: a new pathway in organelle communication.
    Science. 1988 Jul 29;241(4865):589-91 PMID: 3041591
  46. Cell cycle control of morphogenesis in budding yeast.
    Curr Opin Genet Dev. 1995 Feb;5(1):17-23 PMID: 7749320
  47. Receptor regulation of G-protein palmitoylation.
    Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2800-4 PMID: 8146194
  48. Cytoskeleton-membrane interactions.
    Curr Opin Cell Biol. 1996 Feb;8(1):56-65 PMID: 8791403
  49. Cytoplasm-to-vacuole targeting and autophagy employ the same machinery to deliver proteins to the yeast vacuole.
    Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12304-8 PMID: 8901576
  50. Molecular cloning and amino acid sequence of human plakoglobin, the common junctional plaque protein.
    Proc Natl Acad Sci U S A. 1989 Jun;86(11):4027-31 PMID: 2726765
  51. Molecular characterization of VAC1, a gene required for vacuole inheritance and vacuole protein sorting.
    J Biol Chem. 1992 Jan 5;267(1):618-23 PMID: 1730622
  52. Myristylation and palmitylation of Src family members: the fats of the matter.
    Cell. 1994 Feb 11;76(3):411-3 PMID: 8313462
  53. Molecular analysis of the armadillo locus: uniformly distributed transcripts and a protein with novel internal repeats are associated with a Drosophila segment polarity gene.
    Genes Dev. 1989 Jan;3(1):96-113 PMID: 2707602
  54. ER membrane protein complex required for nuclear fusion.
    J Cell Biol. 1996 Feb;132(4):499-509 PMID: 8647883
  55. Homotypic vacuolar fusion mediated by t- and v-SNAREs.
    Nature. 1997 May 8;387(6629):199-202 PMID: 9144293
  56. Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway.
    J Cell Biol. 1995 Nov;131(3):591-602 PMID: 7593182
  57. A Sec63p-BiP complex from yeast is required for protein translocation in a reconstituted proteoliposome.
    J Cell Biol. 1993 Dec;123(6 Pt 1):1355-63 PMID: 8253836
  58. Cysteines 153 and 154 of transmembrane transforming growth factor-alpha are palmitoylated and mediate cytoplasmic protein association.
    J Biol Chem. 1996 Nov 8;271(45):28502-8 PMID: 8910478
  59. Aminopeptidase I of Saccharomyces cerevisiae is localized to the vacuole independent of the secretory pathway.
    J Cell Biol. 1992 Oct;119(2):287-99 PMID: 1400574
  60. Transport of a large oligomeric protein by the cytoplasm to vacuole protein targeting pathway.
    J Cell Biol. 1997 May 5;137(3):609-18 PMID: 9151668
  61. A repeating amino acid motif shared by proteins with diverse cellular roles.
    Cell. 1994 Mar 11;76(5):789-91 PMID: 7907279
  62. Multiple classes of yeast mutants are defective in vacuole partitioning yet target vacuole proteins correctly.
    Mol Biol Cell. 1996 Sep;7(9):1375-89 PMID: 8885233
  63. A genetic and structural analysis of the yeast Vps15 protein kinase: evidence for a direct role of Vps15p in vacuolar protein delivery.
    EMBO J. 1991 Dec;10(13):4049-60 PMID: 1756716
  64. Failure to myristoylate the alpha subunit of Gz is correlated with an inhibition of palmitoylation and membrane attachment, but has no affect on phosphorylation by protein kinase C.
    J Biol Chem. 1994 Feb 11;269(6):4571-6 PMID: 8308028
  65. Fatty acylation is important but not essential for Saccharomyces cerevisiae RAS function.
    Mol Cell Biol. 1987 Jul;7(7):2344-51 PMID: 3302674
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1998-03-09
Pages
1063-74
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2132703
Subset
IM
Grants
NIGMS NIH HHS · GM50403 · 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: product@genelibs.com