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PMID: 19116310 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

PTC1 is required for vacuole inheritance and promotes the association of the myosin-V vacuole-specific receptor complex.

Molecular biology of the cell ·Vol. 20 ·No. 5 ·2009-03-00 ·Pages 1312-23

Jin Y, Taylor Eves P, Tang F, Weisman LS

Abstract

Organelle inheritance occurs during cell division. In Saccharomyces cerevisiae, inheritance of the vacuole, and the distribution of mitochondria and cortical endoplasmic reticulum are regulated by Ptc1p, a type 2C protein phosphatase. Here we show that PTC1/VAC10 controls the distribution of additional cargoes moved by a myosin-V motor. These include peroxisomes, secretory vesicles, cargoes of Myo2p, and ASH1 mRNA, a cargo of Myo4p. We find that Ptc1p is required for the proper distribution of both Myo2p and Myo4p. Surprisingly, PTC1 is also required to maintain the steady-state levels of organelle-specific receptors, including Vac17p, Inp2p, and Mmr1p, which attach Myo2p to the vacuole, peroxisomes, and mitochondria, respectively. Furthermore, Vac17p fused to the cargo-binding domain of Myo2p suppressed the vacuole inheritance defect in ptc1Delta cells. These findings suggest that PTC1 promotes the association of myosin-V with its organelle-specific adaptor proteins. Moreover, these observations suggest that despite the existence of organelle-specific receptors, there is a higher order regulation that coordinates the movement of diverse cellular components.

MeSH Terms
Biological Transport/genetics,physiology Cell Division/physiology Mutation, Missense Myosin Heavy Chains/analysis,metabolism Myosin Type V/analysis,metabolism Peroxisomes/metabolism Phosphoprotein Phosphatases/genetics,metabolism,physiology Protein Phosphatase 2 Receptors, Cell Surface/metabolism Saccharomyces cerevisiae/genetics,metabolism,ultrastructure Saccharomyces cerevisiae Proteins/analysis,genetics,metabolism,physiology Secretory Vesicles/metabolism Vacuoles/metabolism,ultrastructure Vesicular Transport Proteins/metabolism
Chemicals
MYO2 protein, S cerevisiae Receptors, Cell Surface Saccharomyces cerevisiae Proteins VAC17 protein, S cerevisiae Vesicular Transport Proteins PTC1 protein, S cerevisiae Phosphoprotein Phosphatases Protein Phosphatase 2 Myosin Type V Myosin Heavy Chains
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Jin Yui
Life Sciences Institute, Department of Cell and Developmental Biology, University of Michigan, Ann Arbor, MI 48109-2216, USA.
Taylor Eves P
Tang Fusheng
Weisman Lois S
References (80)
80 references, click to expand
  1. Myosin-V: head to tail.
    Cell Mol Life Sci. 1999 Oct 15;56(3-4):233-42 PMID: 11212351
  2. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae.
    Yeast. 1998 Jul;14(10):953-61 PMID: 9717241
  3. She2p is a novel RNA-binding protein that recruits the Myo4p-She3p complex to ASH1 mRNA.
    EMBO J. 2000 Dec 1;19(23):6592-601 PMID: 11101531
  4. Heat stress activates the yeast high-osmolarity glycerol mitogen-activated protein kinase pathway, and protein tyrosine phosphatases are essential under heat stress.
    Eukaryot Cell. 2002 Apr;1(2):163-73 PMID: 12455951
  5. Maintaining peroxisome populations: a story of division and inheritance.
    Annu Rev Cell Dev Biol. 2007;23:321-44 PMID: 17506702
  6. The YHR076w gene encodes a type 2C protein phosphatase and represents the seventh PP2C gene in budding yeast.
    FEBS Lett. 2002 Sep 11;527(1-3):323-5 PMID: 12220683
  7. A role for actin, Cdc1p, and Myo2p in the inheritance of late Golgi elements in Saccharomyces cerevisiae.
    J Cell Biol. 2001 Apr 2;153(1):47-62 PMID: 11285273
  8. Inheritance of the endoplasmic reticulum and Golgi apparatus.
    Curr Opin Cell Biol. 2002 Aug;14(4):496-9 PMID: 12383802
  9. A type V myosin (Myo2p) and a Rab-like G-protein (Ypt11p) are required for retention of newly inherited mitochondria in yeast cells during cell division.
    Mol Biol Cell. 2004 Sep;15(9):3994-4002 PMID: 15215313
  10. Transcriptional profiling of the protein phosphatase 2C family in yeast provides insights into the unique functional roles of Ptc1.
    J Biol Chem. 2006 Nov 17;281(46):35057-69 PMID: 16973600
  11. Global analysis of protein localization in budding yeast.
    Nature. 2003 Oct 16;425(6959):686-91 PMID: 14562095
  12. Ptc1p regulates cortical ER inheritance via Slt2p.
    EMBO J. 2006 Oct 4;25(19):4413-22 PMID: 16977319
  13. Genomic screen for vacuolar protein sorting genes in Saccharomyces cerevisiae.
    Mol Biol Cell. 2002 Jul;13(7):2486-501 PMID: 12134085
  14. 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
  15. The cyclin-dependent kinase Cdk1 directly regulates vacuole inheritance.
    Dev Cell. 2008 Sep;15(3):478-485 PMID: 18804442
  16. Organelle targeting of myosin XI is mediated by two globular tail subdomains with separate cargo binding sites.
    J Biol Chem. 2007 Jul 13;282(28):20593-602 PMID: 17500056
  17. Myo4p is a monomeric myosin with motility uniquely adapted to transport mRNA.
    J Cell Biol. 2007 Sep 24;178(7):1193-206 PMID: 17893244
  18. Zebrafish melanophilin facilitates melanosome dispersion by regulating dynein.
    Curr Biol. 2007 Oct 23;17(20):1721-34 PMID: 17919909
  19. She3p binds to the rod of yeast myosin V and prevents it from dimerizing, forming a single-headed motor complex.
    J Biol Chem. 2008 Mar 14;283(11):6906-14 PMID: 18175803
  20. Ypt11 functions in bud-directed transport of the Golgi by linking Myo2 to the coatomer subunit Ret2.
    Curr Biol. 2008 Jul 8;18(13):987-91 PMID: 18595704
  21. Regulated degradation of a class V myosin receptor directs movement of the yeast vacuole.
    Nature. 2003 Mar 6;422(6927):87-92 PMID: 12594460
  22. Dynamics and inheritance of the endoplasmic reticulum.
    J Cell Sci. 2004 Jun 15;117(Pt 14):2871-8 PMID: 15197242
  23. Widespread cytoplasmic mRNA transport in yeast: identification of 22 bud-localized transcripts using DNA microarray analysis.
    Proc Natl Acad Sci U S A. 2003 Sep 30;100(20):11429-34 PMID: 13679573
  24. The sliding theory of cytoplasmic streaming: fifty years of progress.
    J Plant Res. 2007 Jan;120(1):31-43 PMID: 17252175
  25. The myosin motor, Myo4p, binds Ash1 mRNA via the adapter protein, She3p.
    Proc Natl Acad Sci U S A. 2000 May 9;97(10):5273-8 PMID: 10792032
  26. Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier.
    Science. 2000 Oct 13;290(5490):341-4 PMID: 11030653
  27. Ptc1, a type 2C Ser/Thr phosphatase, inactivates the HOG pathway by dephosphorylating the mitogen-activated protein kinase Hog1.
    Mol Cell Biol. 2001 Jan;21(1):51-60 PMID: 11113180
  28. The UCS domain protein She4p binds to myosin motor domains and is essential for class I and class V myosin function.
    Curr Biol. 2003 Apr 29;13(9):715-24 PMID: 12725728
  29. Polarized growth and organelle segregation in yeast: the tracks, motors, and receptors.
    J Cell Biol. 2003 Mar 17;160(6):811-6 PMID: 12642608
  30. Two yeast forkhead genes regulate the cell cycle and pseudohyphal growth.
    Nature. 2000 Jul 6;406(6791):90-4 PMID: 10894548
  31. She2p, a novel RNA-binding protein tethers ASH1 mRNA to the Myo4p myosin motor via She3p.
    EMBO J. 2000 Oct 16;19(20):5514-24 PMID: 11032818
  32. Mother cell-specific HO expression in budding yeast depends on the unconventional myosin myo4p and other cytoplasmic proteins.
    Cell. 1996 Mar 8;84(5):687-97 PMID: 8625407
  33. Pushing for answers: is myosin V directly involved in moving mitochondria?
    J Cell Biol. 2008 Apr 7;181(1):15-8 PMID: 18391069
  34. Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway.
    Cell. 1980 Aug;21(1):205-15 PMID: 6996832
  35. The peroxisomal membrane protein Inp2p is the peroxisome-specific receptor for the myosin V motor Myo2p of Saccharomyces cerevisiae.
    Dev Cell. 2006 May;10(5):587-600 PMID: 16678774
  36. Participation of XPB/Ptr8p, a component of TFIIH, in nucleocytoplasmic transport of mRNA in fission yeast.
    Genes Cells. 2007 Jan;12(1):35-47 PMID: 17212653
  37. Organelles on the move: insights from yeast vacuole inheritance.
    Nat Rev Mol Cell Biol. 2006 Apr;7(4):243-52 PMID: 16607287
  38. The yeast kinesin-related protein Smy1p exerts its effects on the class V myosin Myo2p via a physical interaction.
    Mol Biol Cell. 2000 Feb;11(2):691-702 PMID: 10679024
  39. Ypt32p and Mlc1p bind within the vesicle binding region of the class V myosin Myo2p globular tail domain.
    Mol Microbiol. 2008 Mar;67(5):1051-66 PMID: 18221262
  40. A myosin from a higher plant has structural similarities to class V myosins.
    J Mol Biol. 1994 Jun 17;239(4):591-7 PMID: 8006972
  41. Dephosphorylation of cyclin-dependent kinases by type 2C protein phosphatases.
    Genes Dev. 1999 Nov 15;13(22):2946-57 PMID: 10580002
  42. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications.
    Nat Biotechnol. 2002 Jan;20(1):87-90 PMID: 11753368
  43. Yeast Nap1-binding protein Nbp2p is required for mitotic growth at high temperatures and for cell wall integrity.
    Genetics. 2003 Oct;165(2):517-29 PMID: 14573466
  44. Crystal structure of the protein serine/threonine phosphatase 2C at 2.0 A resolution.
    EMBO J. 1996 Dec 16;15(24):6798-809 PMID: 9003755
  45. The role of the proteins Kar9 and Myo2 in orienting the mitotic spindle of budding yeast.
    Curr Biol. 2000 Nov 30;10(23):1497-506 PMID: 11114516
  46. Suppressors of a Saccharomyces cerevisiae pkc1 mutation identify alleles of the phosphatase gene PTC1 and of a novel gene encoding a putative basic leucine zipper protein.
    Genetics. 1995 Dec;141(4):1275-85 PMID: 8601473
  47. Complex formation with Ypt11p, a rab-type small GTPase, is essential to facilitate the function of Myo2p, a class V myosin, in mitochondrial distribution in Saccharomyces cerevisiae.
    Mol Cell Biol. 2002 Nov;22(22):7744-57 PMID: 12391144
  48. Dual prenylation is required for Rab protein localization and function.
    Mol Biol Cell. 2003 May;14(5):1852-67 PMID: 12802060
  49. Monomeric myosin V uses two binding regions for the assembly of stable translocation complexes.
    Proc Natl Acad Sci U S A. 2007 Dec 11;104(50):19778-83 PMID: 18056806
  50. The COOH-terminal domain of Myo2p, a yeast myosin V, has a direct role in secretory vesicle targeting.
    J Cell Biol. 1999 Nov 15;147(4):791-808 PMID: 10562281
  51. When the stress of your environment makes you go HOG wild.
    Science. 2004 Nov 26;306(5701):1511-2 PMID: 15567851
  52. Vac8p, an armadillo repeat protein, coordinates vacuole inheritance with multiple vacuolar processes.
    Traffic. 2006 Oct;7(10):1368-77 PMID: 16824055
  53. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization.
    Mol Biol Cell. 1998 Dec;9(12):3273-97 PMID: 9843569
  54. Genome-wide expression analysis of NAP1 in Saccharomyces cerevisiae.
    Biochem Biophys Res Commun. 2003 Jun 20;306(1):5-9 PMID: 12788058
  55. 'Should I stay or should I go?': myosin V function in organelle trafficking.
    Biol Cell. 2007 Aug;99(8):411-23 PMID: 17635110
  56. Identification of an organelle-specific myosin V receptor.
    J Cell Biol. 2003 Mar 17;160(6):887-97 PMID: 12642614
  57. Nbp2 targets the Ptc1-type 2C Ser/Thr phosphatase to the HOG MAPK pathway.
    EMBO J. 2004 Jan 28;23(2):302-11 PMID: 14685261
  58. Sharing the wealth: peroxisome inheritance in budding yeast.
    Biochim Biophys Acta. 2006 Dec;1763(12):1669-77 PMID: 17005268
  59. Slac2-c (synaptotagmin-like protein homologue lacking C2 domains-c), a novel linker protein that interacts with Rab27, myosin Va/VIIa, and actin.
    J Biol Chem. 2002 Nov 8;277(45):43096-103 PMID: 12221080
  60. Direct interaction between a myosin V motor and the Rab GTPases Ypt31/32 is required for polarized secretion.
    Mol Biol Cell. 2008 Oct;19(10):4177-87 PMID: 18653471
  61. The class V myosin motor protein, Myo2, plays a major role in mitochondrial motility in Saccharomyces cerevisiae.
    J Cell Biol. 2008 Apr 7;181(1):119-30 PMID: 18391073
  62. Localization and anchoring of mRNA in budding yeast.
    Curr Biol. 1999 Jun 3;9(11):569-78 PMID: 10359695
  63. Mitochondrial inheritance in budding yeast.
    Traffic. 2001 Jun;2(6):368-74 PMID: 11389764
  64. Heterologous HIS3 marker and GFP reporter modules for PCR-targeting in Saccharomyces cerevisiae.
    Yeast. 1997 Sep 15;13(11):1065-75 PMID: 9290211
  65. Tropomyosin-containing actin cables direct the Myo2p-dependent polarized delivery of secretory vesicles in budding yeast.
    J Cell Biol. 1998 Dec 28;143(7):1931-45 PMID: 9864365
  66. 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
  67. Molecular mechanisms of pigment transport in melanophores.
    Pigment Cell Res. 1999 Oct;12(5):283-94 PMID: 10541038
  68. Myo4p and She3p are required for cortical ER inheritance in Saccharomyces cerevisiae.
    J Cell Biol. 2003 Dec 22;163(6):1255-66 PMID: 14691136
  69. Mitochondrial inheritance is delayed in Saccharomyces cerevisiae cells lacking the serine/threonine phosphatase PTC1.
    Mol Biol Cell. 1998 Apr;9(4):917-30 PMID: 9529388
  70. Regulated phosphorylation of budding yeast's essential myosin V heavy chain, Myo2p.
    Mol Biol Cell. 2006 Apr;17(4):1812-21 PMID: 16467380
  71. Mmr1p is a mitochondrial factor for Myo2p-dependent inheritance of mitochondria in the budding yeast.
    EMBO J. 2004 Jul 7;23(13):2520-30 PMID: 15201867
  72. The YCR079w gene confers a rapamycin-resistant function and encodes the sixth type 2C protein phosphatase in Saccharomyces cerevisiae.
    FEMS Yeast Res. 2007 Mar;7(2):209-15 PMID: 17002782
  73. Palmitoylation plays a role in targeting Vac8p to specific membrane subdomains.
    Traffic. 2006 Oct;7(10):1378-87 PMID: 16978392
  74. Identification of an organelle receptor for myosin-Va.
    Nat Cell Biol. 2002 Apr;4(4):271-8 PMID: 11887186
  75. Myosin V orientates the mitotic spindle in yeast.
    Nature. 2000 Aug 31;406(6799):1013-5 PMID: 10984058
  76. Protein phosphatases in MAPK signalling: we keep learning from yeast.
    Mol Microbiol. 2005 Oct;58(1):6-16 PMID: 16164545
  77. Apg13p and Vac8p are part of a complex of phosphoproteins that are required for cytoplasm to vacuole targeting.
    J Biol Chem. 2000 Aug 18;275(33):25840-9 PMID: 10837477
  78. Two distinct regions in a yeast myosin-V tail domain are required for the movement of different cargoes.
    J Cell Biol. 2000 Aug 7;150(3):513-26 PMID: 10931864
  79. 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
  80. Vac8p, a vacuolar protein with armadillo repeats, functions in both vacuole inheritance and protein targeting from the cytoplasm to vacuole.
    J Cell Biol. 1998 Mar 9;140(5):1063-74 PMID: 9490720
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1939-4586
DOI
10.1091/mbc.e08-09-0954
Published
2009-03-00
Epub
2008-00-30
Pages
1312-23
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC2649272
Subset
IM
Grants
NIGMS NIH HHS · R01 GM062261 · United States
NIGMS NIH HHS · R37 GM062261 · United States
NIGMS NIH HHS · GM62261 · United States
External Links
PubMed source DOI: 10.1091/mbc.e08-09-0954 PMC Full Text View journal details
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