The relationship between mitochondrial shape and function and the cytoskeleton

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1757, Issue 5-6, 2006, Pages 692-699

  Anesti, Vasiliki ^a   Scorrano, Luca ^a  

^a VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

Author keywords

Cytoskeleton; Dynein; Fission; Fusion; Kinesin; Mitochondria; Motility; Trichoplein

Indexed keywords

CALCIUM ION; CYTOSKELETON PROTEIN;

APOPTOSIS; CELL DEATH; CELL ORGANELLE; CELL TRANSPORT; CYTOSKELETON; ENERGY CONVERSION; EUKARYOTIC CELL; HUMAN; MICROTUBULE; MITOCHONDRION; MORPHOLOGY; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ACTINS; ANIMALS; CYTOSKELETON; HUMANS; MICROFILAMENTS; MICROTUBULES; MITOCHONDRIA; MITOCHONDRIAL SWELLING; YEASTS;

EID: 33745601933     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2006.04.013     Document Type: Review

References (89)

1. V. Anesti, R. Baffa, L. Scorrano. Trichoplein, a novel coiled-coil protein, bridges intermediate filaments and mitochondria to block their movement (submitted for publication).
2. Aufderheide K. Mitochondrial associations with specific microtubular components of the cortex of Tetrahymena thermophila. I Cortical patterning of mitochondria. J. Cell Sci. 39 (1979) 299
3. Aufderheide K.J. Mitochondrial associations with specific microtubular components of the cortex of Tetrahymena thermophila. II. Response of the mitochondrial pattern to changes in the microtubule pattern. J. Cell Sci. 42 (1980) 247
4. Balish M.F., Moeller III E.F., and Coluccio L.M. Overlapping distribution of the 130- and 110-kDa myosin I isoforms on rat liver membranes. Arch. Biochem. Biophys. 370 (1999) 285
5. Bereiter-Hahn J., and Voth M. Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc. Res. Tech. 27 (1994) 198
6. Berger K.H., and Yaffe M.P. Mitochondrial distribution and inheritance. Experientia 52 (1996) 1111
7. Boldogh I.R., Ramcharan S.L., Yang H.C., and Pon L.A. 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 15 (2004) 3994
8. Boldogh I.R., Yang H.C., Nowakowski W.D., Karmon S.L., Hays L.G., Yates III J.R., and Pon L.A. Arp2/3 complex and actin dynamics are required for actin-based mitochondrial motility in yeast. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 3162
9. Breitenbach M., Laun P., and Gimona M. The actin cytoskeleton, RAS-cAMP signaling and mitochondrial ROS in yeast apoptosis. Trends Cell Biol. 15 (2005) 637
10. Bremer A., and Aebi U. The structure of the F-actin filament and the actin molecule. Curr. Opin. Cell Biol. 4 (1992) 20
11. Chan K.Y., and Bunt A.H. An association between mitochondria and microtubules in synaptosomes and axon terminals of cerebral cortex. J. Neurocytol. 7 (1978) 137
12. Chen H., Detmer S.A., Ewald A.J., Griffin E.E., Fraser S.E., and Chan D.C. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 160 (2003) 189
13. Chua B.T., Volbracht C., Tan K.O., Li R., Yu V.C., and Li P. Mitochondrial translocation of cofilin is an early step in apoptosis induction. Nat. Cell Biol. 5 (2003) 1083
14. Cipolat S., de Brito O.M., Dal Zilio B., and Scorrano L. OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 15927
15. Cleveland D.W. Microtubule MAPping. Cell 60 (1990) 701
16. Cleveland D.W., and Sullivan K.F. Molecular biology and genetics of tubulin. Annu. Rev. Biochem. 54 (1985) 331
17. Dalpe G., Mathieu M., Comtois A., Zhu E., Wasiak S., De Repentigny Y., Leclerc N., and Kothary R. Dystonin-deficient mice exhibit an intrinsic muscle weakness and an instability of skeletal muscle cytoarchitecture. Dev. Biol. 210 (1999) 367
18. Danial N.N., and Korsmeyer S.J. Cell death: critical control points. Cell 116 (2004) 205
19. De Vos K., Goossens V., Boone E., Vercammen D., Vancompernolle K., Vandenabeele P., Haegeman G., Fiers W., and Grooten J. The 55-kDa tumor necrosis factor receptor induces clustering of mitochondria through its membrane-proximal region. J. Biol. Chem. 273 (1998) 9673
20. De Vos K.J., Sable J., Miller K.E., and Sheetz M.P. Expression of phosphatidylinositol (4,5) bisphosphate-specific pleckstrin homology domains alters direction but not the level of axonal transport of mitochondria. Mol. Biol. Cell 14 (2003) 3636
21. DeGiorgis J.A., Reese T.S., and Bearer E.L. Association of a nonmuscle myosin II with axoplasmic organelles. Mol. Biol. Cell 13 (2002) 1046
22. Drubin D.G., Jones H.D., and Wertman K.F. Actin structure and function: roles in mitochondrial organization and morphogenesis in budding yeast and identification of the phalloidin-binding site. Mol. Biol. Cell 4 (1993) 1277
23. Duchen M.R. Mitochondria and calcium: from cell signalling to cell death. J. Physiol. 529 Pt. 1 (2000) 57-68
24. Ducret A., Nguyen M., Breckenridge D.G., and Shore G.C. The resident endoplasmic reticulum protein, BAP31, associates with {gamma}-actin and myosin B heavy chain: analysis by capillary liquid chromatography microelectrospray tandem MS. Eur. J. Biochem. 270 (2003) 342
25. Ebneth A., Godemann R., Stamer K., Illenberger S., Trinczek B., and Mandelkow E. Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J. Cell Biol. 143 (1998) 777
26. Fehrenbacher K.L., Boldogh I.R., and Pon L.A. A role for Jsn1p in recruiting the Arp2/3 complex to mitochondria in budding yeast. Mol. Biol. Cell 16 (2005) 5094
27. Fountoulakis M., Soumaka E., Rapti K., Mavroidis M., Tsangaris G., Maris A., Weisleder N., and Capetanaki Y. Alterations in the heart mitochondrial proteome in a desmin null heart failure model. J. Mol. Cell. Cardiol. 38 (2005) 461
28. Fuchs E. The cytoskeleton and disease: genetic disorders of intermediate filaments. Annu. Rev. Genet. 30 (1996) 197
29. Garcia M.L., and Cleveland D.W. Going new places using an old MAP: tau, microtubules and human neurodegenerative disease. Curr. Opin. Cell Biol. 13 (2001) 41
30. Gourlay C.W., and Ayscough K.R. The actin cytoskeleton: a key regulator of apoptosis and ageing?. Nat. Rev., Mol. Cell Biol. 6 (2005) 583
31. Gourlay C.W., Carpp L.N., Timpson P., Winder S.J., and Ayscough K.R. A role for the actin cytoskeleton in cell death and aging in yeast. J. Cell Biol. 164 (2004) 803
32. Green D.R., and Kroemer G. The pathophysiology of mitochondrial cell death. Science 305 (2004) 626
33. Heggeness M.H., Simon M., and Singer S.J. Association of mitochondria with microtubules in cultured cells. Proc. Natl. Acad. Sci. U. S. A. 75 (1978) 3863
34. Hermann G.J., and Shaw J.M. Mitochondrial dynamics in yeast. Annu. Rev. Cell Dev. Biol. 14 (1998) 265
35. Herrmann H., and Aebi U. Intermediate filaments: molecular structure, assembly mechanism, and integration into functionally distinct intracellular Scaffolds. Annu. Rev. Biochem. 73 (2004) 749
36. Hollenbeck P.J., and Saxton W.M. The axonal transport of mitochondria. J. Cell Sci. 118 (2005) 5411
37. Itoh T., Watabe A., Toh E., and Matsui Y. 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. 22 (2002) 7744
38. James D.I., Parone P.A., Mattenberger Y., and Martinou J.C. hFis1, a novel component of the mammalian mitochondrial fission machinery. J. Biol. Chem. 278 (2003) 36373
39. Kodama A., Lechler T., and Fuchs E. Coordinating cytoskeletal tracks to polarize cellular movements. J. Cell Biol. 167 (2004) 203
40. Koya R.C., Fujita H., Shimizu S., Ohtsu M., Takimoto M., Tsujimoto Y., and Kuzumaki N. Gelsolin inhibits apoptosis by blocking mitochondrial membrane potential loss and cytochrome c release. J. Biol. Chem. 275 (2000) 15343
41. Kusano H., Shimizu S., Koya R.C., Fujita H., Kamada S., Kuzumaki N., and Tsujimoto Y. Human gelsolin prevents apoptosis by inhibiting apoptotic mitochondrial changes via closing VDAC. Oncogene 19 (2000) 4807
42. La Jr. F.J. An association between microtubules and aligned mitochondria in Nephrotoma spermatocytes. Exp. Cell Res. 71 (1972) 325
43. Leterrier J.F., Rusakov D.A., Nelson B.D., and Linden M. Interactions between brain mitochondria and cytoskeleton: evidence for specialized outer membrane domains involved in the association of cytoskeleton-associated proteins to mitochondria in situ and in vitro. Microsc. Res. Tech. 27 (1994) 233
44. Li J., Li Q., Xie C., Zhou H., Wang Y., Zhang N., Shao H., Chan S.C., Peng X., Lin S.C., and Han J. {beta}-actin is required for mitochondria clustering and ROS generation in TNF-induced, caspase-independent cell death. J. Cell Sci. 117 (2004) 4673
45. Linden M., Nelson B.D., and Leterrier J.F. The specific binding of the microtubule-associated protein 2 (MAP2) to the outer membrane of rat brain mitochondria. Biochem. J. 261 (1989) 167
46. Linden M., Nelson B.D., Loncar D., and Leterrier J.F. Studies on the interaction between mitochondria and the cytoskeleton. J. Bioenerg. Biomembr. 21 (1989) 507
47. Mandelkow E.M., Thies E., Trinczek B., Biernat J., and Mandelkow E. MARK/PAR1 kinase is a regulator of microtubule-dependent transport in axons. J. Cell Biol. 167 (2004) 99
48. McConnell S.J., and Yaffe M.P. Nuclear and mitochondrial inheritance in yeast depends on novel cytoplasmic structures defined by the MDM1 protein. J. Cell Biol. 118 (1992) 385
49. McConnell S.J., and Yaffe M.P. Intermediate filament formation by a yeast protein essential for organelle inheritance. Science 260 (1993) 687
50. McNiven M.A. Dynamin: a molecular motor with pinchase action. Cell 94 (1998) 151
51. Miki H., Setou M., Kaneshiro K., and Hirokawa N. All kinesin superfamily protein, KIF, genes in mouse and human. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 7004
52. Milner D.J., Mavroidis M., Weisleder N., and Capetanaki Y. Desmin cytoskeleton linked to muscle mitochondrial distribution and respiratory function. J. Cell Biol. 150 (2000) 1283
53. Moritz M., and Agard D.A. Gamma-tubulin complexes and microtubule nucleation. Curr. Opin. Struct. Biol. 11 (2001) 174
54. Morris R.L., and Hollenbeck P.J. Axonal transport of mitochondria along microtubules and F-actin in living vertebrate neurons. J. Cell Biol. 131 (1995) 1315
55. Mose-Larsen P., Bravo R., Fey S.J., Small J.V., and Celis J.E. Putative association of mitochondria with a subpopulation of intermediate-sized filaments in cultured human skin fibroblasts. Cell 31 (1982) 681
56. Nangaku M., Sato-Yoshitake R., Okada Y., Noda Y., Takemura R., Yamazaki H., and Hirokawa N. KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell 79 (1994) 1209
57. Nguyen M., Breckenridge D.G., Ducret A., and Shore G.C. Caspase-resistant BAP31 inhibits fas-mediated apoptotic membrane fragmentation and release of cytochrome c from mitochondria. Mol. Cell. Biol. 20 (2000) 6731
58. Nishizawa M., Izawa I., Inoko A., Hayashi Y., Nagata K., Yokoyama T., Usukura J., and Inagaki M. Identification of trichoplein, a novel keratin filament-binding protein. J. Cell Sci. 118 (2005) 1081
59. Nogales E. Structural insights into microtubule function. Annu. Rev. Biochem. 69 (2000) 277
60. Orrenius S., Zhivotovsky B., and Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat. Rev., Mol. Cell Biol. 4 (2003) 552
61. Pereira A.J., Dalby B., Stewart R.J., Doxsey S.J., and Goldstein L.S. Mitochondrial association of a plus end-directed microtubule motor expressed during mitosis in Drosophila. J. Cell Biol. 136 (1997) 1081
62. Puthalakath H., Huang D.C., O'Reilly L.A., King S.M., and Strasser A. The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol. Cell 3 (1999) 287
63. Raff E.C. Genetics of microtubule systems. J. Cell Biol. 99 (1984) 1
64. Raine C.S., Ghetti B., and Shelanski M.L. On the association between microtubules and mitochondria within axons. Brain Res. 34 (1971) 389
65. Reipert S., Steinbock F., Fischer I., Bittner R.E., Zeold A., and Wiche G. Association of mitochondria with plectin and desmin intermediate filaments in striated muscle. Exp. Cell Res. 252 (1999) 479
66. Rintoul G.L., Filiano A.J., Brocard J.B., Kress G.J., and Reynolds I.J. Glutamate decreases mitochondrial size and movement in primary forebrain neurons. J. Neurosci. 23 (2003) 7881
67. Rizzuto R., Bernardi P., and Pozzan T. Mitochondria as all-round players of the calcium game. J. Physiol. 529 Pt. 1 (2000) 37-47
68. Schliwa M., and Woehlke G. Molecular motors. Nature 422 (2003) 759
69. Schwarzer C., Barnikol-Watanabe S., Thinnes F.P., and Hilschmann N. Voltage-dependent anion-selective channel (VDAC) interacts with the dynein light chain Tctex1 and the heat-shock protein PBP74. Int. J. Biochem. Cell Biol. 34 (2002) 1059
70. Scorrano L. Proteins that fuse and fragment mitochondria in apoptosis: con-fissing a deadly con-fusion?. J. Bioenerg. Biomembr. 37 (2005) 165
71. Shaw J.M., and Nunnari J. Mitochondrial dynamics and division in budding yeast. Trends Cell Biol. 12 (2002) 178
72. Simon V.R., Karmon S.L., and Pon L.A. Mitochondrial inheritance: cell cycle and actin cable dependence of polarized mitochondrial movements in Saccharomyces cerevisiae. Cell Motil. Cytoskeleton 37 (1997) 199
73. Simon V.R., Swayne T.C., and Pon L.A. Actin-dependent mitochondrial motility in mitotic yeast and cell-free systems: identification of a motor activity on the mitochondrial surface. J. Cell Biol. 130 (1995) 345
74. Smirnova E., Griparic L., Shurland D.L., and van der Bliek A.M. Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 12 (2001) 2245
75. Smith D.S., Jarlfors U., and Cayer M.L. Structural cross-bridges between microtubules and mitochondria in central axons of an insect (Periplaneta americana). J. Cell Sci. 27 (1977) 255
76. Stowers R.S., Megeath L.J., Gorska-Andrzejak J., Meinertzhagen I.A., and Schwarz T.L. Axonal transport of mitochondria to synapses depends on milton, a novel Drosophila protein. Neuron 36 (2002) 1063
77. Tanaka Y., Kanai Y., Okada Y., Nonaka S., Takeda S., Harada A., and Hirokawa N. Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 93 (1998) 1147
78. Toh B.H., Lolait S.J., Mathy J.P., and Baum R. Association of mitochondria with intermediate filaments and of polyribosomes with cytoplasmic actin. Cell Tissue Res. 211 (1980) 163
79. Vale R.D. The molecular motor toolbox for intracellular transport. Cell 112 (2003) 467
80. Varadi A., Johnson-Cadwell L.I., Cirulli V., Yoon Y., Allan V.J., and Rutter G.A. Cytoplasmic dynein regulates the subcellular distribution of mitochondria by controlling the recruitment of the fission factor dynamin-related protein-1. J. Cell Sci. 117 (2004) 4389
81. Varadi A., Tsuboi T., and Rutter G.A. Myosin Va transports dense core secretory vesicles in pancreatic MIN6 beta-cells. Mol. Biol. Cell 16 (2005) 2670
82. Weir B.A., and Yaffe M.P. Mmd1p, a novel, conserved protein essential for normal mitochondrial morphology and distribution in the fission yeast Schizosaccharomyces pombe. Mol. Biol. Cell 15 (2004) 1656
83. Weisleder N., Taffet G.E., and Capetanaki Y. Bcl-2 overexpression corrects mitochondrial defects and ameliorates inherited desmin null cardiomyopathy. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 769
84. Welte M.A. Bidirectional transport along microtubules. Curr. Biol. 14 (2004) R525-R537
85. Wozniak M.J., Melzer M., Dorner C., Haring H.U., and Lammers R. The novel protein KBP regulates mitochondria localization by interaction with a kinesin-like protein. BMC Cell Biol. 6 (2005) 35
86. Yaffe M.P., Harata D., Verde F., Eddison M., Toda T., and Nurse P. Microtubules mediate mitochondrial distribution in fission yeast. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 11664
87. Yaffe M.P., Stuurman N., and Vale R.D. Mitochondrial positioning in fission yeast is driven by association with dynamic microtubules and mitotic spindle poles. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 11424
88. Yi M., Weaver D., and Hajnoczky G. Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J. Cell Biol. 167 (2004) 661
89. Zhu Y., Swanson B.J., Wang M., Hildeman D.A., Schaefer B.C., Liu X., Suzuki H., Mihara K., Kappler J., and Marrack P. Constitutive association of the proapoptotic protein Bim with Bcl-2-related proteins on mitochondria in T cells. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 7681