Human Miltons associate with mitochondria and induce microtubule-dependent remodeling of mitochondrial networks

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1803, Issue 5, 2010, Pages 564-574

  Koutsopoulos, Olga S ^a,d   Laine, David ^a   Osellame, Laura ^a   Chudakov, Dmitriy M ^b   Parton, Robert G ^c   Frazier, Ann E ^a   Ryan, Michael T ^a  

^a LA TROBE UNIVERSITY   (Australia)

^b SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Distribution; Milton; Mitochondria; Morphology; Trafficking

Indexed keywords

ADAPTOR PROTEIN; GREEN FLUORESCENT PROTEIN; KINESIN; PROTEIN MILTON1; PROTEIN MILTON2; PROTEIN MIRO; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL INTERACTION; CONTROLLED STUDY; MICROTUBULE; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CERCOPITHECUS AETHIOPS; CLONING, MOLECULAR; COS CELLS; HUMANS; IMMUNOPRECIPITATION; MICROSCOPY, FLUORESCENCE; MICROTUBULES; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NERVE TISSUE PROTEINS; RHO GTP-BINDING PROTEINS;

MAMMALIA;

EID: 77951938881     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2010.03.006     Document Type: Article

References (57)

1. Chan D.C. Mitochondria: dynamic organelles in disease, aging, and development. Cell 2006, 125:1241-1252.
2. Frazier A.E., Kiu C., Stojanovski D., Hoogenraad N.J., Ryan M.T. Mitochondrial morphology and distribution in mammalian cells. Biol. Chem. 2006, 387:1551-1558.
3. Frederick R.L., Shaw J.M. Moving mitochondria: establishing distribution of an essential organelle. Traffic 2007, 8:1668-1675.
4. Hoppins S., Lackner L., Nunnari J. The machines that divide and fuse mitochondria. Annu. Rev. Biochem. 2007, 76:751-780.
5. McBride H.M., Neuspiel M., Wasiak S. Mitochondria: more than just a powerhouse. Curr. Biol. 2006, 16:R551-R560.
6. Hoppins S., Nunnari J. The molecular mechanism of mitochondrial fusion. Biochim. Biophys. Acta 2009, 1793:20-26.
7. Stojanovski D., Rissler M., Pfanner N., Meisinger C. Mitochondrial morphology and protein import-a tight connection?. Biochim. Biophys. Acta 2006, 1763:414-421.
8. Nangaku M., Sato-Yoshitake R., Okada Y., Noda Y., Takemura R., Yamazaki H., Hirokawa N. KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell 1994, 79:1209-1220.
9. Tanaka Y., Kanai Y., Okada Y., Nonaka S., Takeda S., Harada A., Hirokawa N. Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 1998, 93:1147-1158.
10. Morris R.L., Hollenbeck P.J. Axonal transport of mitochondria along microtubules and F-actin in living vertebrate neurons. J. Cell Biol. 1995, 131:1315-1326.
11. Hollenbeck P.J., Saxton W.M. The axonal transport of mitochondria. J. Cell Sci. 2005, 118:5411-5419.
12. Knott A.B., Perkins G., Schwarzenbacher R., Bossy-Wetzel E. Mitochondrial fragmentation in neurodegeneration. Nat. Rev. Neurosci. 2008, 9:505-518.
13. Li Z., Okamoto K., Hayashi Y., Sheng M. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 2004, 119:873-887.
14. Verstreken P., Ly C.V., Venken K.J., Koh T.W., Zhou Y., Bellen H.J. Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 2005, 47:365-378.
15. Sung J.Y., Engmann O., Teylan M.A., Nairn A.C., Greengard P., Kim Y. WAVE1 controls neuronal activity-induced mitochondrial distribution in dendritic spines. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:3112-3116.
16. Campello S., Lacalle R.A., Bettella M., Manes S., Scorrano L., Viola A. Orchestration of lymphocyte chemotaxis by mitochondrial dynamics. J. Exp. Med. 2006, 203:2879-2886.
17. Quintana A., Schwindling C., Wenning A.S., Becherer U., Rettig J., Schwarz E.C., Hoth M. T cell activation requires mitochondrial translocation to the immunological synapse. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:14418-14423.
18. Cai Q., Gerwin C., Sheng Z.H. Syntabulin-mediated anterograde transport of mitochondria along neuronal processes. J. Cell Biol. 2005, 170:959-969.
19. Frederick R.L., McCaffery J.M., Cunningham K.W., Okamoto K., Shaw J.M. Yeast Miro GTPase, Gem1p, regulates mitochondrial morphology via a novel pathway. J. Cell Biol. 2004, 167:87-98.
20. Santama N., Er C.P., Ong L.L., Yu H. Distribution and functions of kinectin isoforms. J. Cell Sci. 2004, 117:4537-4549.
21. Stowers R.S., Megeath L.J., Gorska-Andrzejak J., Meinertzhagen I.A., Schwarz T.L. Axonal transport of mitochondria to synapses depends on milton, a novel Drosophila protein. Neuron 2002, 36:1063-1077.
22. Wozniak M.J., Melzer M., Dorner C., Haring H.U., Lammers R. The novel protein KBP regulates mitochondria localization by interaction with a kinesin-like protein. BMC Cell Biol. 2005, 6:35.
23. Kang J.S., Tian J.H., Pan P.Y., Zald P., Li C., Deng C., Sheng Z.H. Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation. Cell 2008, 132:137-148.
24. Li Y., Lim S., Hoffman D., Aspenstrom P., Federoff H.J., Rempe D.A. HUMMR, a hypoxia- and HIF-1alpha-inducible protein, alters mitochondrial distribution and transport. J. Cell Biol. 2009, 185:1065-1081.
25. Weihofen A., Thomas K.J., Ostaszewski B.L., Cookson M.R., Selkoe D.J. Pink1 forms a multiprotein complex with Miro and Milton, linking Pink1 function to mitochondrial trafficking. Biochemistry 2009, 48:2045-2052.
26. Iyer S.P., Akimoto Y., Hart G.W. Identification and cloning of a novel family of coiled-coil domain proteins that interact with O-GlcNAc transferase. J. Biol. Chem. 2003, 278:5399-5409.
27. Beck M., Brickley K., Wilkinson H.L., Sharma S., Smith M., Chazot P.L., Pollard S., Stephenson F.A. Identification, molecular cloning, and characterization of a novel GABAA receptor-associated protein, GRIF-1. J. Biol. Chem. 2002, 277:30079-30090.
28. Kirk E., Chin L.S., Li L. GRIF1 binds Hrs and is a new regulator of endosomal trafficking. J. Cell Sci. 2006, 119:4689-4701.
29. Gilbert S.L., Zhang L., Forster M.L., Anderson J.R., Iwase T., Soliven B., Donahue L.R., Sweet H.O., Bronson R.T., Davisson M.T., Wollmann R.L., Lahn B.T. Trak1 mutation disrupts GABA(A) receptor homeostasis in hypertonic mice. Nat. Genet. 2006, 38:245-250.
30. Grishin A., Li H., Levitan E.S., Zaks-Makhina E. Identification of gamma-aminobutyric acid receptor-interacting factor 1 (TRAK2) as a trafficking factor for the K+ channel Kir2.1. J. Biol. Chem. 2006, 281:30104-30111.
31. Brickley K., Smith M.J., Beck M., Stephenson F.A. GRIF-1 and OIP106, members of a novel gene family of coiled-coil domain proteins: association in vivo and in vitro with kinesin. J. Biol. Chem. 2005, 280:14723-14732.
32. Smith M.J., Pozo K., Brickley K., Stephenson F.A. Mapping the GRIF-1 binding domain of the kinesin, KIF5C, substantiates a role for GRIF-1 as an adaptor protein in the anterograde trafficking of cargoes. J. Biol. Chem. 2006, 281:27216-27228.
33. Fransson S., Ruusala A., Aspenstrom P. The atypical Rho GTPases Miro-1 and Miro-2 have essential roles in mitochondrial trafficking. Biochem. Biophys. Res. Commun. 2006, 344:500-510.
34. Macaskill A.F., Rinholm J.E., Twelvetrees A.E., Arancibia-Carcamo I.L., Muir J., Fransson A., Aspenstrom P., Attwell D., Kittler J.T. Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 2009, 61:541-555.
35. Wang X., Schwarz T.L. The mechanism of Ca2+-dependent regulation of kinesin-mediated mitochondrial motility. Cell 2009, 136:163-174.
36. Guo X., Macleod G.T., Wellington A., Hu F., Panchumarthi S., Schoenfield M., Marin L., Charlton M.P., Atwood H.L., Zinsmaier K.E. The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses. Neuron 2005, 47:379-393.
37. Russo G.J., Louie K., Wellington A., Macleod G.T., Hu F., Panchumarthi S., Zinsmaier K.E. Drosophila Miro is required for both anterograde and retrograde axonal mitochondrial transport. J. Neurosci. 2009, 29:5443-5455.
38. Saotome M., Safiulina D., Szabadkai G., Das S., Fransson A., Aspenstrom P., Rizzuto R., Hajnoczky G. Bidirectional Ca2+-dependent control of mitochondrial dynamics by the Miro GTPase. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:20728-20733.
39. Sambrook J., Russell D.V. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, Cold Spring Horbor, New York.
40. Johnston A.J., Hoogenraad J., Dougan D.A., Truscott K.N., Yano M., Mori M., Hoogenraad N.J., Ryan M.T. Insertion and assembly of human tom7 into the preprotein translocase complex of the outer mitochondrial membrane. J. Biol. Chem. 2002, 277:42197-42204.
41. Stojanovski D., Koutsopoulos O.S., Okamoto K., Ryan M.T. Levels of human Fis1 at the mitochondrial outer membrane regulate mitochondrial morphology. J. Cell Sci. 2004, 117:1201-1210.
42. Yano M., Hoogenraad N., Terada K., Mori M. Identification and functional analysis of human Tom22 for protein import into mitochondria. Mol. Cell. Biol. 2000, 20:7205-7213.
43. Harlow E., Lane D. Using Antibodies: A Laboratory Manual 1999, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
44. Tyynismaa H., Sembongi H., Bokori-Brown M., Granycome C., Ashley N., Poulton J., Jalanko A., Spelbrink J.N., Holt I.J., Suomalainen A. Twinkle helicase is essential for mtDNA maintenance and regulates mtDNA copy number. Hum. Mol. Genet. 2004, 13:3219-3227.
45. Schagger H., von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100kDa. Anal. Biochem. 1987, 166:368-379.
46. Kanazawa M., Yano M., Namchai C., Yamamoto S., Ohtake A., Takayanagi M., Mori M., Niimi H. Visualization of mitochondria with green fluorescent protein in cultured fibroblasts from patients with mitochondrial diseases. Biochem. Biophys. Res. Commun. 1997, 239:580-584.
47. Perkins G., Bossy-Wetzel E., Ellisman M.H. New insights into mitochondrial structure during cell death. Exp. Neurol. 2009, 218:183-192.
48. Glater E.E., Megeath L.J., Stowers R.S., Schwarz T.L. Axonal transport of mitochondria requires milton to recruit kinesin heavy chain and is light chain independent. J. Cell Biol. 2006, 173:545-557.
49. Kremer B.E., Haystead T., Macara I.G. Mammalian septins regulate microtubule stability through interaction with the microtubule-binding protein MAP4. Mol. Biol. Cell 2005, 16:4648-4659.
50. Shcherbo D., Merzlyak E.M., Chepurnykh T.V., Fradkov A.F., Ermakova G.V., Solovieva E.A., Lukyanov K.A., Bogdanova E.A., Zaraisky A.G., Lukyanov S., Chudakov D.M. Bright far-red fluorescent protein for whole-body imaging. Nat. Methods 2007, 4:741-746.
51. Karbowski M., Lee Y.J., Gaume B., Jeong S.Y., Frank S., Nechushtan A., Santel A., Fuller M., Smith C.L., Youle R.J. Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J. Cell Biol. 2002, 159:931-938.
52. Knowles M.K., Guenza M.G., Capaldi R.A., Marcus A.H. Cytoskeletal-assisted dynamics of the mitochondrial reticulum in living cells. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:14772-14777.
53. Gurskaya N.G., Verkhusha V.V., Shcheglov A.S., Staroverov D.B., Chepurnykh T.V., Fradkov A.F., Lukyanov S., Lukyanov K.A. Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light. Nat. Biotechnol. 2006, 24:461-465.
54. MacAskill A.F., Brickley K., Stephenson F.A., Kittler J.T. GTPase dependent recruitment of Grif-1 by Miro1 regulates mitochondrial trafficking in hippocampal neurons. Mol. Cell. Neurosci. 2009, 40:301-312.
55. Bowes T., Gupta R.S. Novel mitochondrial extensions provide evidence for a link between microtubule-directed movement and mitochondrial fission. Biochem. Biophys. Res. Commun. 2008, 376:40-45.
56. Navratil M., Terman A., Arriaga E.A. Giant mitochondria do not fuse and exchange their contents with normal mitochondria. Exp. Cell Res. 2008, 314:164-172.
57. Webber E., Li L., Chin L.S. Hypertonia-associated protein Trak1 is a novel regulator of endosome-to-lysosome trafficking. J. Mol. Biol. 2008, 382:638-651.