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PMID: 22119524 Published · ppublish English Journal Article Research Support, American Recovery and Reinvestment Act Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Role for cER and Mmr1p in anchorage of mitochondria at sites of polarized surface growth in budding yeast.

Current biology : CB ·Vol. 21 ·No. 23 ·2011-12-06 ·Pages 1994-9

Swayne TC, Zhou C, Boldogh IR, Charalel JK, McFaline-Figueroa JR, Thoms S, Yang C, Leung G, McInnes J, Erdmann R, Pon LA

Abstract

Mitochondria accumulate at neuronal and immunological synapses and yeast bud tips and associate with the ER during phospholipid biosynthesis, calcium homeostasis, and mitochondrial fission. Here we show that mitochondria are associated with cortical ER (cER) sheets underlying the plasma membrane in the bud tip and confirm that a deletion in YPT11, which inhibits cER accumulation in the bud tip, also inhibits bud tip anchorage of mitochondria. Time-lapse imaging reveals that mitochondria are anchored at specific sites in the bud tip. Mmr1p, a member of the DSL1 family of tethering proteins, localizes to punctate structures on opposing surfaces of mitochondria and cER sheets underlying the bud tip and is recovered with isolated mitochondria and ER. Deletion of MMR1 impairs bud tip anchorage of mitochondria without affecting mitochondrial velocity or cER distribution. Deletion of the phosphatase PTC1 results in increased Mmr1p phosphorylation, mislocalization of Mmr1p, defects in association of Mmr1p with mitochondria and ER, and defects in bud tip anchorage of mitochondria. These findings indicate that Mmr1p contributes to mitochondrial inheritance as a mediator of anchorage of mitochondria to cER sheets in the yeast bud tip and that Ptc1p regulates Mmr1p phosphorylation, localization, and function.

MeSH Terms
Cytokinesis/physiology Endoplasmic Reticulum/metabolism Mitochondria/metabolism,physiology Mitochondrial Proteins/metabolism Protein Phosphatase 2/metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism Saccharomycetales/growth & development,metabolism Sequence Deletion/genetics Time-Lapse Imaging rab GTP-Binding Proteins/genetics,metabolism
Chemicals
Mitochondrial Proteins Mmr1 protein, S cerevisiae Saccharomyces cerevisiae Proteins Ypt11 protein, S cerevisiae PTC1 protein, S cerevisiae Protein Phosphatase 2 rab GTP-Binding Proteins
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Swayne Theresa C
Department of Pathology and Cell Biology, Columbia University College of Physicians and Surgeons, New York, NY 10032, USA.
Zhou Chun
Boldogh Istvan R
Charalel Joseph K
McFaline-Figueroa José Ricardo
Thoms Sven
Yang Christine
Leung Galen
McInnes Joseph
Erdmann Ralf
Pon Liza A
References (33)
33 references, click to expand
  1. Ptc1p regulates cortical ER inheritance via Slt2p.
    EMBO J. 2006 Oct 4;25(19):4413-22 PMID: 16977319
  2. A protein complex containing Mdm10p, Mdm12p, and Mmm1p links mitochondrial membranes and DNA to the cytoskeleton-based segregation machinery.
    Mol Biol Cell. 2003 Nov;14(11):4618-27 PMID: 13679517
  3. T cell activation requires mitochondrial translocation to the immunological synapse.
    Proc Natl Acad Sci U S A. 2007 Sep 4;104(36):14418-23 PMID: 17726106
  4. The myosin-related motor protein Myo2 is an essential mediator of bud-directed mitochondrial movement in yeast.
    J Cell Biol. 2011 Aug 8;194(3):473-88 PMID: 21807878
  5. 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
  6. 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
  7. Live cell imaging of mitochondrial movement along actin cables in budding yeast.
    Curr Biol. 2004 Nov 23;14(22):1996-2004 PMID: 15556861
  8. A retention mechanism for distribution of mitochondria during cell division in budding yeast.
    Curr Biol. 1999 Oct 7;9(19):1111-4 PMID: 10531006
  9. PhosphoPep--a database of protein phosphorylation sites in model organisms.
    Nat Biotechnol. 2008 Dec;26(12):1339-40 PMID: 19060867
  10. 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
  11. Regulation of mitochondrial morphology and inheritance by Mdm10p, a protein of the mitochondrial outer membrane.
    J Cell Biol. 1994 Sep;126(6):1361-73 PMID: 8089171
  12. Synapses in the central nervous system.
    J Biophys Biochem Cytol. 1956 Jul 25;2(4 Suppl):193-202 PMID: 13357542
  13. An ER-mitochondria tethering complex revealed by a synthetic biology screen.
    Science. 2009 Jul 24;325(5939):477-81 PMID: 19556461
  14. Proteomic analysis of the yeast mitochondrial outer membrane reveals accumulation of a subclass of preproteins.
    Mol Biol Cell. 2006 Mar;17(3):1436-50 PMID: 16407407
  15. Association between the endoplasmic reticulum and mitochondria of yeast facilitates interorganelle transport of phospholipids through membrane contact.
    Eur J Biochem. 1999 Sep;264(2):545-53 PMID: 10491102
  16. ER tubules mark sites of mitochondrial division.
    Science. 2011 Oct 21;334(6054):358-62 PMID: 21885730
  17. Mitochondria on the move.
    Trends Cell Biol. 2007 Oct;17(10):502-10 PMID: 17804238
  18. PTC1 is required for vacuole inheritance and promotes the association of the myosin-V vacuole-specific receptor complex.
    Mol Biol Cell. 2009 Mar;20(5):1312-23 PMID: 19116310
  19. Multiple pathways influence mitochondrial inheritance in budding yeast.
    Genetics. 2008 Feb;178(2):825-37 PMID: 18245340
  20. Mitofusin 2 tethers endoplasmic reticulum to mitochondria.
    Nature. 2008 Dec 4;456(7222):605-10 PMID: 19052620
  21. 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
  22. Structural organization of the endoplasmic reticulum.
    EMBO Rep. 2002 Oct;3(10):944-50 PMID: 12370207
  23. Bioinformatic and comparative localization of Rab proteins reveals functional insights into the uncharacterized GTPases Ypt10p and Ypt11p.
    Mol Cell Biol. 2006 Oct;26(19):7299-317 PMID: 16980630
  24. Mitochondrial protein sorting: differentiation of beta-barrel assembly by Tom7-mediated segregation of Mdm10.
    J Biol Chem. 2006 Aug 11;281(32):22819-26 PMID: 16760475
  25. 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
  26. Mechanisms of polarized growth and organelle segregation in yeast.
    Annu Rev Cell Dev Biol. 2004;20:559-91 PMID: 15473852
  27. Mitochondrial quality control during inheritance is associated with lifespan and mother-daughter age asymmetry in budding yeast.
    Aging Cell. 2011 Oct;10(5):885-95 PMID: 21726403
  28. 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
  29. Dsl1p, an essential component of the Golgi-endoplasmic reticulum retrieval system in yeast, uses the same sequence motif to interact with different subunits of the COPI vesicle coat.
    J Biol Chem. 2003 Dec 19;278(51):51722-34 PMID: 14504276
  30. 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
  31. 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
  32. A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature.
    J Cell Biol. 2011 Apr 18;193(2):333-46 PMID: 21502358
  33. Protein phosphatases in MAPK signalling: we keep learning from yeast.
    Mol Microbiol. 2005 Oct;58(1):6-16 PMID: 16164545
Article Info
Journal
Current biology : CB
Abbr.
Curr Biol
ISSN
1879-0445
Published
2011-12-06
Epub
2011-00-23
Pages
1994-9
Language
English
Region
England
NLM ID
9107782
PMCID
PMC3237857
Subset
IM
Grants
NIGMS NIH HHS · R01 GM045735 · United States
NIGMS NIH HHS · GM45735S1 · United States
NIA NIH HHS · F31 AG034835 · United States
NIGMS NIH HHS · GM45735 · United States
NIA NIH HHS · 1 F31 AG034835 · United States
NIGMS NIH HHS · GM096445 · United States
NIGMS NIH HHS · R01 GM045735-15S1 · United States
NCI NIH HHS · P30 CA13696 · United States
NIGMS NIH HHS · R01 GM096445-01 · United States
NIGMS NIH HHS · R01 GM045735-15 · United States
NIGMS NIH HHS · R01 GM096445 · United States
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