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PMID: 11248049 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Arp2/3 complex and actin dynamics are required for actin-based mitochondrial motility in yeast.

Boldogh IR, Yang HC, Nowakowski WD, Karmon SL, Hays LG, Yates JR, Pon LA

Abstract

The Arp2/3 complex is implicated in actin polymerization-driven movement of Listeria monocytogenes. Here, we find that Arp2p and Arc15p, two subunits of this complex, show tight, actin-independent association with isolated yeast mitochondria. Arp2p colocalizes with mitochondria. Consistent with this result, we detect Arp2p-dependent formation of actin clouds around mitochondria in intact yeast. Cells bearing mutations in ARP2 or ARC15 genes show decreased velocities of mitochondrial movement, loss of all directed movement and defects in mitochondrial morphology. Finally, we observe a decrease in the velocity and extent of mitochondrial movement in yeast in which actin dynamics are reduced but actin cytoskeletal structure is intact. These results support the idea that the movement of mitochondria in yeast is actin polymerization driven and that this movement requires Arp2/3 complex.

MeSH Terms
Actin-Related Protein 2 Actin-Related Protein 3 Actins/metabolism Cytoskeletal Proteins Fungal Proteins/metabolism Membrane Proteins/metabolism Mitochondria/metabolism,physiology Potassium Chloride/metabolism,pharmacology Saccharomyces cerevisiae/drug effects,metabolism
Chemicals
Actin-Related Protein 2 Actin-Related Protein 3 Actins Cytoskeletal Proteins Fungal Proteins Membrane Proteins Potassium Chloride
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Boldogh I R
Department of Anatomy and Cell Biology, Columbia University, New York, NY 10032, USA.
Yang H C
Nowakowski W D
Karmon S L
Hays L G
Yates J R
Pon L A
References (36)
36 references, click to expand
  1. 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
  2. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes.
    J Cell Biol. 1989 Oct;109(4 Pt 1):1597-608 PMID: 2507553
  3. Requirement of yeast fimbrin for actin organization and morphogenesis in vivo.
    Nature. 1991 Dec 5;354(6352):404-8 PMID: 1956405
  4. Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane.
    J Cell Biol. 1994 Apr;125(2):381-91 PMID: 8163554
  5. 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
  6. Immunofluorescence localization of the unconventional myosin, Myo2p, and the putative kinesin-related protein, Smy1p, to the same regions of polarized growth in Saccharomyces cerevisiae.
    J Cell Biol. 1994 May;125(4):825-42 PMID: 8188749
  7. Purification of a cortical complex containing two unconventional actins from Acanthamoeba by affinity chromatography on profilin-agarose.
    J Cell Biol. 1994 Oct;127(1):107-15 PMID: 7929556
  8. Yeast mitochondria contain ATP-sensitive, reversible actin-binding activity.
    Mol Biol Cell. 1994 Jul;5(7):807-18 PMID: 7812049
  9. 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
  10. 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
  11. Asymmetric accumulation of Ash1p in postanaphase nuclei depends on a myosin and restricts yeast mating-type switching to mother cells.
    Cell. 1996 Mar 8;84(5):699-709 PMID: 8625408
  12. Synthetic lethality screen identifies a novel yeast myosin I gene (MYO5): myosin I proteins are required for polarization of the actin cytoskeleton.
    J Cell Biol. 1996 Jun;133(6):1277-91 PMID: 8682864
  13. The Saccharomyces cerevisiae actin-related protein Arp2 is involved in the actin cytoskeleton.
    J Cell Biol. 1996 Jul;134(1):117-32 PMID: 8698808
  14. Fission yeast Sop2p: a novel and evolutionarily conserved protein that interacts with Arp3p and modulates profilin function.
    EMBO J. 1996 Dec 2;15(23):6426-37 PMID: 8978670
  15. Actin polymerization is induced by Arp2/3 protein complex at the surface of Listeria monocytogenes.
    Nature. 1997 Jan 16;385(6613):265-9 PMID: 9000076
  16. Structure, subunit topology, and actin-binding activity of the Arp2/3 complex from Acanthamoeba.
    J Cell Biol. 1997 Jan 27;136(2):331-43 PMID: 9015304
  17. The yeast gene, MDM20, is necessary for mitochondrial inheritance and organization of the actin cytoskeleton.
    J Cell Biol. 1997 Apr 7;137(1):141-53 PMID: 9105043
  18. High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A.
    J Cell Biol. 1997 Apr 21;137(2):399-416 PMID: 9128251
  19. The complex containing actin-related proteins Arp2 and Arp3 is required for the motility and integrity of yeast actin patches.
    Curr Biol. 1997 Jul 1;7(7):519-29 PMID: 9210376
  20. Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA.
    Science. 1997 Jul 18;277(5324):383-7 PMID: 9219698
  21. 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
  22. The human Arp2/3 complex is composed of evolutionarily conserved subunits and is localized to cellular regions of dynamic actin filament assembly.
    J Cell Biol. 1997 Jul 28;138(2):375-84 PMID: 9230079
  23. Unconventional myosins in cell movement, membrane traffic, and signal transduction.
    Science. 1998 Jan 23;279(5350):527-33 PMID: 9438839
  24. Corequirement of specific phosphoinositides and small GTP-binding protein Cdc42 in inducing actin assembly in Xenopus egg extracts.
    J Cell Biol. 1998 Mar 9;140(5):1125-36 PMID: 9490725
  25. Interaction between mitochondria and the actin cytoskeleton in budding yeast requires two integral mitochondrial outer membrane proteins, Mmm1p and Mdm10p.
    J Cell Biol. 1998 Jun 15;141(6):1371-81 PMID: 9628893
  26. Interaction of human Arp2/3 complex and the Listeria monocytogenes ActA protein in actin filament nucleation.
    Science. 1998 Jul 3;281(5373):105-8 PMID: 9651243
  27. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae.
    Yeast. 1998 Jul;14(10):953-61 PMID: 9717241
  28. The yeast V159N actin mutant reveals roles for actin dynamics in vivo.
    J Cell Biol. 1998 Sep 7;142(5):1289-99 PMID: 9732289
  29. Localization of ASH1 mRNA particles in living yeast.
    Mol Cell. 1998 Oct;2(4):437-45 PMID: 9809065
  30. 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
  31. Tyrosine phosphorylation is required for actin-based motility of vaccinia but not Listeria or Shigella.
    Curr Biol. 1999 Jan 28;9(2):89-92 PMID: 10021367
  32. Reconstitution of actin-based motility of Listeria and Shigella using pure proteins.
    Nature. 1999 Oct 7;401(6753):613-6 PMID: 10524632
  33. A retention mechanism for distribution of mitochondria during cell division in budding yeast.
    Curr Biol. 1999 Oct 7;9(19):1111-4 PMID: 10531006
  34. Endocytic vesicles move at the tips of actin tails in cultured mast cells.
    Nat Cell Biol. 1999 May;1(1):72-4 PMID: 10559868
  35. Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae.
    J Cell Biol. 1984 Mar;98(3):934-45 PMID: 6365931
  36. Getting started with yeast.
    Methods Enzymol. 1991;194:3-21 PMID: 2005794
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2001-03-13
Pages
3162-7
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC30624
Subset
IM
Grants
NIGMS NIH HHS · R01 GM045735 · United States
NCI NIH HHS · P30CA13696 · United States
NIGMS NIH HHS · GM45735 · United States
NCRR NIH HHS · S10RR10506 · United States
NCI NIH HHS · P30 CA013696 · United States
NCRR NIH HHS · RR11832 · United States
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