Controlled and stochastic retention concentrates dynein at microtubule ends to keep endosomes on track

EMBO Journal

Volumn 30, Issue 4, 2011, Pages 652-664

  Schuster, Martin ^a   Kilaru, Sreedhar ^a   Ashwin, Peter ^a   Lin, Congping ^a   Severs, Nicholas J ^b   Steinberg, Gero ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

dynein; EB1; endosome motility; membrane trafficking; microtubules

Indexed keywords

BINDING PROTEIN; DYNACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; GREEN FLUORESCENT PROTEIN; KINESIN; KINESIN 3; PROTEIN EB1; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; ENDOSOME; GENOTYPE; MATHEMATICAL MODEL; MICROTUBULE; NONHUMAN; NUCLEAR PORE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; STOCHASTIC MODEL; USTILAGO MAYDIS;

AMINO ACID SEQUENCE; BIOLOGICAL TRANSPORT; DYNEINS; ENDOSOMES; FUNGAL PROTEINS; MICROTUBULES; MODELS, BIOLOGICAL; MODELS, THEORETICAL; ORGANISMS, GENETICALLY MODIFIED; OSMOLAR CONCENTRATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; SEQUENCE HOMOLOGY, AMINO ACID; STOCHASTIC PROCESSES; USTILAGO;

FUNGI;

EID: 79951809345     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.360     Document Type: Article

References (74)

1. Abenza JF, Pantazopoulou A, Rodriguez JM, Galindo A, Penalva MA (2009) Long-distance movement of Aspergillus nidulans early endosomes on microtubule tracks. Traffic 10: 57-75
2. Adamikova L, Straube A, Schulz I, Steinberg G (2004) Calcium signaling is involved in dynein-dependent microtubule organization. Mol Biol Cell 15: 1969-1980 (Pubitemid 38401843)
3. Akhmanova A, Steinmetz MO (2008) Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nature Rev 9: 309-322 (Pubitemid 351430849)
4. Ally S, Jolly AL, Gelfand VI (2008) Motor-cargo release: CaMKII as a traffic cop. Nat Cell Biol 10: 3-5
5. Andersson TP, Svensson SP, Karlsson AM (2003) Regulation of melanosome movement by MAP kinase. Pigment Cell Res 16: 215-221 (Pubitemid 36597057)
6. Ashwin P, Lin C, Steinberg G (2010) Queueing induced by bidirectional motor motion near the end of a microtubule. Phys Rev E 82: 051907
7. Becht P, Konig J, Feldbrugge M (2006) The RNA-binding protein Rrm4 is essential for polarity in Ustilago maydis and shuttles along microtubules. J Cell Sci 119: 4964-4973 (Pubitemid 46017809)
8. Bloom GS, Wagner MC, Pfister KK, Brady ST (1988) Native structure and physical properties of bovine brain kinesin and identification of the ATP-binding subunit polypeptide. Biochemistry 27: 3409-3416
9. Bottin A, Kämper J, Kahmann R (1996) Isolation of a carbon source-regulated gene from Ustilago maydis. Mol Gen Genet 253: 342-352 (Pubitemid 27023192)
10. Cai D, Verhey KJ, Meyhöfer E (2007) Tracking single kinesin molecules in the cytoplasm of mammalian cells. Biophys J 92: 4137-4144 (Pubitemid 46910529)
11. Chevalier-Larsen E, Holzbaur EL (2006) Axonal transport and neurodegenerative disease. Biochim Biophys Acta 1762: 1094-1108 (Pubitemid 44750577)
12. Chowdhury D, Schadschneider A, Nishinari K (2005) Physics of transport and traffic phenomena in biology: from molecular motors and cells to organisms. Phy Life Rev 2: 318-352 (Pubitemid 41762628)
13. Deacon SW, Nascimento A, Serpinskaya AS, Gelfand VI (2005) Regulation of bidirectional melanosome transport by organelle bound MAP kinase. Curr Biol 15: 459-463 (Pubitemid 40323533)
14. Fuchs U, Hause G, Schuchardt I, Steinberg G (2006) Endocytosis is essential for pathogenic development in the corn smut fungus Ustilago maydis. Plant Cell 18: 2066-2081 (Pubitemid 44260197)
15. Gazzola M, Burckhardt CJ, Bayati B, Engelke M, Greber UF, Koumoutsakos P (2009) A stochastic model for microtubule motors describes the in vivo cytoplasmic transport of human adenovirus. PLoS Comput Biol 5: e1000623
16. Gross SP (2004) Hither and yon: a review of bi-directional microtubule-based transport. Phys Biol 1: R1-R11
17. Hammond JW, Cai D, Blasius TL, Li Z, Jiang Y, Jih GT, Meyhofer E, Verhey KJ (2009) Mammalian Kinesin-3 motors are dimeric in vivo and move by processive motility upon release of autoinhibition. PLoS Biol 7: e72
18. Han G, Liu B, Zhang J, Zuo W, Morris NR, Xiang X (2001) The Aspergillus cytoplasmic dynein heavy chain and NUDF localize to microtubule ends and affect microtubule dynamics. Curr Biol 11: 719-724 (Pubitemid 32418170)
19. Hendricks AG, Perlson E, Ross JL, Schroeder III HW, Tokito M, Holzbaur EL (2010) Motor coordination via a tug-of-war mechanism drives bidirectional vesicle transport. Curr Biol 20: 697-702
20. Hoepfner S, Severin F, Cabezas A, Habermann B, Runge A, Gillooly D, Stenmark H, Zerial M (2005) Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B. Cell 121: 437-450 (Pubitemid 40692303)
21. Holliday R (1974) Ustilago maydis. In Handbook of Genetics, King RC (ed) Vol. 1, pp 575-595. New York: Plenum Press
22. Honnappa S, Okhrimenko O, Jaussi R, Jawhari H, Jelesarov I, Winkler FK, Steinmetz MO (2006) Key interaction modes of dynamic +TIP networks. Mol Cell 23: 663-671 (Pubitemid 44292557)
23. Hough LE, Schwabe A, Glaser MA, McIntosh JR, Betterton MD (2009) Microtubule depolymerization by the Kinesin-8 motor Kip3p: a mathematical model. Biophys J 96: 3050-3064
24. Howe CL, Mobley WC (2005) Long-distance retrograde neurotrophic signaling. Curr Opin Neurobiol 15: 40-48 (Pubitemid 40249960)
25. Ingold AL, Cohn SA, Scholey JM (1988) Inhibition of kinesin-driven microtubule motility by monoclonal antibodies to kinesin heavy chains. J Cell Biol 107: 2657-2667
26. Joglekar AP, Salmon ED, Bloom KS (2008) Counting kinetochore protein numbers in budding yeast using genetically encoded fluorescent proteins. Methods Cell Biol 85: 127-151
27. Kerssemakers JW, Munteanu EL, Laan L, Noetzel TL, Janson ME, Dogterom M (2006) Assembly dynamics of microtubules at molecular resolution. Nature 442: 709-712 (Pubitemid 44215328)
28. King SM (2000) The dynein microtubule motor. Biochim Biophys Acta 1496: 60-75
29. Klumpp S, Lipowsky R (2005) Cooperative cargo transport by several molecular motors. Proc Natl Acad Sci USA 102: 17284-17289 (Pubitemid 41740858)
30. Kumar S, Lee IH, Plamann M (2000) Cytoplasmic dynein ATPase activity is regulated by dynactin-dependent phosphorylation. J Biol Chem 275: 31798-31804
31. Lenz JH, Schuchardt I, Straube A, Steinberg G (2006) A dynein loading zone for retrograde endosome motility at microtubule plus-ends. EMBO J 25: 2275-2286 (Pubitemid 44012211)
32. Ligon LA, Shelly SS, Tokito M, Holzbaur EL (2003) The microtubule plus-end proteins EB1 and dynactin have differential effects on microtubule polymerization. Mol Biol Cell 14: 1405-1417 (Pubitemid 36547410)
33. Lomakin AJ, Semenova I, Zaliapin I, Kraikivski P, Nadezhdina E, Slepchenko BM, Akhmanova A, Rodionov V (2009) CLIP-170-dependent capture of membrane organelles by microtubules initiates minus-end directed transport. Dev Cell 17: 323-333
34. Miaczynska M, Pelkmans L, Zerial M (2004) Not just a sink: endosomes in control of signal transduction. Curr Opin Cell Biol 16: 400-406 (Pubitemid 38903146)
35. Müller MJ, Klumpp S, Lipowsky R (2008) Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors. Proc Natl Acad Sci USA 105: 4609-4614 (Pubitemid 351753794)
36. Müller MJ, Klumpp S, Lipowsky R (2010) Bidirectional transport by molecular motors: enhanced processivity and response to external forces. Biophysical J 98: 2610-2618
37. Münsterkötter M, Steinberg G (2007) The fungus Ustilago maydis and humans share disease-related proteins that are not found in Saccharomyces cerevisiae. BMC Genomics 8: 473
38. Okada Y, Hirokawa N (1999) A processive single-headed motor: kinesin superfamily protein KIF1A. Science 283: 1152-1157
39. Patterson GH, Lippincott-Schwartz J (2002) A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297: 1873-1877 (Pubitemid 35024347)
40. Peñalva MA (2010) Endocytosis in filamentous fungi: Cinderella gets her reward. Curr Opin Microbiol 13: 1-9
41. Porter ME, Scholey JM, Stemple DL, Vigers GP, Vale RD, Sheetz MP, McIntosh JR (1987) Characterization of the microtubule movement produced by sea urchin egg kinesin. J Biol Chem 262: 2794-2802
42. Rabut G, Doye V, Ellenberg J (2004) Mapping the dynamic organization of the nuclear pore complex inside single living cells. Nat Cell Biol 6: 1114-1121 (Pubitemid 39468013)
43. Ray S, Meyhöfer E, Milligan RA, Howard J (1993) Kinesin follows the microtubule's protofilament axis. J Cell Biol 121: 1083-1093 (Pubitemid 23154269)
44. Reck-Peterson SL, Yildiz A, Carter AP, Gennerich A, Zhang N, Vale RD (2006) Single-molecule analysis of dynein processivity and stepping behavior. Cell 126: 335-348 (Pubitemid 44092968)
45. Schnitzer MJ, Block SM (1997) Kinesin hydrolyses one ATP per 8-nm step. Nature 388: 386-390 (Pubitemid 27334818)
46. Schroer TA (2004) Dynactin. Annu Rev Cell Dev Biol 20: 759-779
47. Schuchardt I, Assmann D, Thines E, Schuberth C, Steinberg G (2005) Myosin-V, Kinesin-1, and Kinesin-3 cooperate in hyphal growth of the fungus Ustilago maydis. Mol Biol Cell 16: 5191-5201
48. Severs NJ (2007) Freeze-fracture electron microscopy. Nat Protoc 2: 547-576
49. Soppina V, Rai AK, Ramaiya AJ, Barak P, Mallik R (2009) Tug-of-war between dissimilar teams of microtubule motors regulates transport and fission of endosomes. Proc Natl Acad Sci USA 106: 19381-19386
50. Spellig T, Bottin A, Kahmann R (1996) Green fluorescent protein (GFP) as a new vital marker in the phytopathogenic fungus Ustilago maydis. Mol Gen Genet 252: 503-509
51. Steinberg G (1997) A kinesin-like mechanoenzyme from the zygomycete Syncephalastrum racemosum shares biochemical similarities with conventional kinesin from Neurospora crassa. Eur J Cell Biol 73: 124-131
52. Steinberg G (2007) On the move: endosomes in fungal growth and pathogenicity. Nat Rev Microbiol 5: 309-316
53. Steinberg G, Perez-Martin J (2008) Ustilago maydis, a new fungal model system for cell biology. Trends Cell Biol 18: 61-67
54. Steinberg G, Schliwa M (1996) Characterization of the biophysical and motility properties of kinesin from the fungus Neurospora crassa. J Biol Chem 271: 7516-7521 (Pubitemid 26107026)
55. Steinberg G, Schliwa M, Lehmler C, Bölker M, Kahmann R, McIntosh JR (1998) Kinesin from the plant pathogenic fungus Ustilago maydis is involved in vacuole formation and cytoplasmic migration. J Cell Sci 111: 2235-2246 (Pubitemid 28403528)
56. Straube A, Brill M, Oakley BR, Horio T, Steinberg G (2003) Microtubule organization requires cell cycle-dependent nucleation at dispersed cytoplasmic sites: polar and perinuclear microtubule organizing centers in the plant pathogen Ustilago maydis. Mol Biol Cell 14: 642-657 (Pubitemid 36237022)
57. Straube A, Enard W, Berner A, Wedlich-Söldner R, Kahmann R, Steinberg G (2001) A split motor domain in a cytoplasmic dynein. EMBO J 20: 5091-5100 (Pubitemid 32910905)
58. Theisen U, Straube A, Steinberg G (2008) Dynamic rearrangement of nucleoporins during fungal 'open' Mitosis. Mol Biol Cell 19: 1230-1240
59. Tilney LG, Bryan J, Bush DJ, Fujiwara K, Mooseker MS, Murphy DB, Snyder DH (1973) Microtubules: evidence for 13 protofilaments. J Cell Biol 59: 267-275
60. Ulbrich MH, Isacoff EY (2007) Subunit counting in membranebound proteins. Nat Methods 4: 319-321
61. Vale RD, Reese TS, Sheetz M (1985) Identification of a novel forcegenerating protein, kinesin, involved in microtubule-based motility. Cell 42: 39-50 (Pubitemid 16237554)
62. Valetti C, Wetzel DM, Schrader M, Hasbani MJ, Gill SR, Kreis TE, Schroer TA (1999) Role of dynactin in endocytic traffic: effects of dynamitin overexpression and colocalization with CLIP-170. Mol Biol Cell 10: 4107-4120
63. Vallee RB, Williams JC, Varma D, Barnhart LE (2004) Dynein: an ancient motor protein involved in multiple modes of transport. J Neurobiol 58: 189-200 (Pubitemid 38173717)
64. Vaughan KT (2005) Microtubule plus ends, motors, and traffic of Golgi membranes. Biochim Biophys Acta 1744: 316-324
65. Vaughan PS, Miura P, Henderson M, Byrne B, Vaughan KT (2002) A role for regulated binding of p150(Glued) to microtubule plus ends in organelle transport. J Cell Biol 158: 305-319
66. Wang Z, Khan S, Sheetz MP (1995) Single cytoplasmic dynein molecule movements: characterization and comparison with kinesin. Biophys J 69: 2011-2023
67. Wedlich-Söldner R, Bölker M, Kahmann R, Steinberg G (2000) A putative endosomal t-SNARE links exo- and endocytosis in the phytopathogenic fungus Ustilago maydis. EMBO J 19: 1974-1986 (Pubitemid 30237573)
68. Wedlich-Söldner R, Schulz I, Straube A, Steinberg G (2002b) Dynein supports motility of endoplasmic reticulum in the fungus Ustilago maydis. Mol Biol Cell 13: 965-977 (Pubitemid 34250358)
69. Wedlich-Söldner R, Straube A, Friedrich MW, Steinberg G (2002a) A balance of KIF1A-like kinesin and dynein organizes early endosomes in the fungus Ustilago maydis. EMBO J 21: 2946-2957 (Pubitemid 34670379)
70. Welte MA (2004) Bidirectional transport along microtubules. Curr Biol 14: R525-R537
71. Welte MA, Gross SP (2008) Molecular motors: a traffic cop within? HFSP J 2: 178-182
72. Xiang X (2003) LIS1 at the microtubule plus end and its role in dynein-mediated nuclear migration. J Cell Biol 160: 289-290
73. Zhang J, Li S, Fischer R, Xiang X (2003) Accumulation of cytoplasmic dynein and dynactin at microtubule plus ends in Aspergillus nidulans is kinesin dependent. Mol Biol Cell 14: 1479-1488
74. Zhang J, Zhuang L, Lee Y, Abenza JF, Peñalva MA, Xiang X (2010) The microtubule plus-end localization of Aspergillus dynein is important for dynein-early-endosome interaction but not for dynein ATPase activation. J Cell Sci 123: 3596-3604