The +TIP coordinating protein EB1 is highly dynamic and diffusive on microtubules, sensitive to GTP analog, ionic strength, and EB1 concentration

Cytoskeleton

Volumn 73, Issue 1, 2016, Pages 23-34

  Lopez, Benjamin J ^a   Valentine, Megan T ^a  

^a Santa Barbara   (United States)

Author keywords

Diffusion; EB1; Microtubule associated protein; Microtubules; TIRF

Indexed keywords

BINDING PROTEIN; END BINDING PROTEIN 1; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); GUANOSINE TRIPHOSPHATE DERIVATIVE; MICROTUBULE ASSOCIATED PROTEIN; PACLITAXEL; TUBULIN; UNCLASSIFIED DRUG; 5'-GUANYLYLMETHYLENEBISPHOSPHONATE; GUANOSINE TRIPHOSPHATE; MAPRE1 PROTEIN, HUMAN; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; BLEACHING; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DIFFUSION COEFFICIENT; DIMERIZATION; FLUORESCENCE MICROSCOPY; HUMAN; IN VITRO STUDY; IONIC STRENGTH; MICROTUBULE; MICROTUBULE ASSEMBLY; MOLECULAR CROWDING; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; QUANTITATIVE ANALYSIS; ANALOGS AND DERIVATIVES; METABOLISM; OSMOLARITY;

GUANOSINE TRIPHOSPHATE; HUMANS; MICROSCOPY, FLUORESCENCE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; OSMOLAR CONCENTRATION; PROTEIN BINDING;

EID: 84956637532     PISSN: 19493584     EISSN: 19493592     Source Type: Journal    
DOI: 10.1002/cm.21267     Document Type: Article

References (63)

1. Akhmanova A, Hoogenraad CC. 2005. Microtubule plus-end-tracking proteins: mechanisms and functions. Curr Opin Cell Biol 17:47-54.
2. Akhmanova A, Steinmetz MO. 2008. Tracking the ends: A dynamic protein network controls the fate of microtubule tips. Nat Rev Mol Cell Biol 9:309-322.
3. Akhmanova A, Steinmetz MO. 2011. Microtubule end binding: EBs sense the guanine nucleotide state. Curr Biol 21:R283-R285.
4. Ali MY, Krementsova EB, Kennedy GG, Mahaffy R, Pollard TD, Trybus KM, Warshaw DM. 2007. Myosin Va maneuvers through actin intersections and diffuses along microtubules. Proc Natl Acad Sci USA 104:4332-4336.
5. Berg HC 1993. Random Walks in Biology. Princeton, New Jersey: Princeton University Press.
6. Bieling P, Kandels-Lewis S, Telley IA, van Dijk J, Janke C, Surrey T. 2008. CLIP-170 tracks growing microtubule ends by dynamically recognizing composite EB1/tubulin-binding sites. J Cell Biol 183:1223-1233.
7. Bieling P, Laan L, Schek H, Munteanu EL, Sandblad L, Dogterom M, Brunner D, Surrey T. 2007. Reconstitution of a microtubule plus-end tracking system in vitro. Nature 450:1100-1105.
8. Bruening-Richardson A, Langford KJ, Ruane P, Lee T, Askham JM, Morrison EE. 2011. EB1 is required for spindle symmetry in mammalian mitosis. PLoS One 6:1-23.
9. Bu W, Su L-K. 2003. Characterization of functional domains of human EB1 family proteins. J Biol Chem 278:49721-49731.
10. Buey RM, Mohan R, Leslie K, Walzthoeni T, Missimer JH, Menzel A, Bjelic S, Bargsten K, Grigoriev I, Smal I, et al. 2011. Insights into EB1 structure and the role of its C-terminal domain for discriminating microtubule tips from the lattice. Mol Biol Cell 22:2912-2923.
11. Butner KA, Kirschner MW. 1991. Tau protein binds to microtubules through a flexible array of distributed weak sites. J Cell Biol 115:717-730.
12. Cooper JR, Wordeman L. 2009. The diffusive interaction of microtubule binding proteins. Curr Opin Cell Biol 21:68-73.
13. Crocker JC, Grier DG. 1996. Methods of digital video microscopy for colloidal studies. J Colloid Interface Sci 179:298-310.
14. Dixit RRJ, Goldman YE, Holzbaur EL. 2008. Differential regulation of dynein and kinesin motor proteins by tau. Science 319:1086-1089.
15. Dong X, Liu FF, Sun L, Liu M, Li DW, Su D, Zhu ZM, Dong JT, Fu L, Zhou J. 2010. Oncogenic function of microtubule end-binding protein I in breast cancer. J Pathol 220:361-369.
16. Einstein A. 1905. Über die von der molekularkinetischen Theorie der Wärme geforderte Bewegung von in ruhenden Flüssigkeiten suspendierten Teilchen. Annalen Der Physik 322:549-560.
17. Forth S, Hsia KC, Shimamoto Y, Kapoor TM. 2014. Asymmetric friction of nonmotor MAPs can lead to their directional motion in active microtubule networks. Cell 157:13.
18. Gao Y, Kilfoil ML. 2009. Accurate detection and complete tracking of large populations of featuresin three dimensions. Opt Express 17:4685-4704.
19. Glotzer M. 2009. The 3Ms of central spindle assembly: microtubules, motors and MAPs. Nat Rev 10:9-20.
20. Goode B, Feinstein S. 1994. Identification of a novel microtubule binding and assembly domain in the developmentally regulated inter-repeat region of tau. J Cell Biol 124:769-782.
21. Goutelle S, Maurin M, Rougier F, Barbaut X, Bourguignon L, Ducher M, Maire P. 2008. The Hill equation: a review of its capabilities in pharmacological modelling. Fundamental Clin Pharmacol 22:633-648.
22. Hayashi I, Ikura M. 2003. Crystal structure of the amino-terminal microtubule-binding domain of end-binding protein 1 (EB1). J Biol Chem 278:36430-36434.
23. Helenius J, Brouhard G, Kalaidzidis Y, Diez S, Howard J. 2006. The depolymerizing kinesin MCAK uses lattice diffusion to rapidly target microtubule ends. Nature 441:115-119.
24. Hill AV. 1910. The possible effects of the aggregation of the molecules of haemoglobin on its dissociation curves. J Physiol 40:iv-vii.
25. Hinrichs MH, Jalal A, Brenner B, Mandelkow E, Kumar S, Scholz T. 2012. Tau protein diffuses along the microtubule lattice. J Biol Chem 287:38559-38568.
26. Hoenger A, Thormählen M, Diaz-Avalos R, Doerhoefer M, Goldie KN, Müller J, Mandelkow E. 2000. A new look at the microtubule binding patterns of dimeric kinesins1. J Mol Biol 297:1087-1103.
27. Honnappa S, Gouveia SM, Weisbrich A, Damberger FF, Bhavesh NS, Jawhari H, Grigoriev I, van Rijssel FJA, Buey RM, Lawera A, et al. 2009. An EB1-binding motif acts as a microtubule tip localization signal. Cell 138:366-376.
28. Honnappa S, John CM, Kostrewa D, Winkler FK, Steinmetz MO. 2005. Structural insights into the EB1-APC interaction. EMBO J 24:261-269.
29. Hyman A, Drechsel D, Kellogg D, Salser S, Sawin K, Steffen P, Wordeman L, Mitchison T. 1991. Preparation of modified tubulins. Methods Enzymol 196:478-485.
30. Hyman AA, Salser S, Drechsel DN, Unwin N, Mitchison TJ. 1992. Role of GTP hydrolysis in microtubule dynamics: information from a slowly hydrolyzable analogue, GMPCPP. Mol Biol Cell 3:1155-1167.
31. Kawaguchi K, Ishiwata Si. 2001. Nucleotide-dependent single- to double-headed binding of kinesin. Science 291:667-669.
32. Kim MJ, Yun HS, Hong EH, Lee SJ, Baek JH, Lee CW, Yim JH, Kim JS, Park JK, Um HD, et al. 2013. Depletion of end-binding protein 1 (EB1) promotes apoptosis of human non-small-cell lung cancer cells via reactive oxygen species and Bax-mediated mitochondrial dysfunction. Cancer Lett 339:15-24.
33. Komarova Y, De Groot CO, Grigoriev I, Gouveia SM, Munteanu EL, Schober JM, Honnappa S, Buey RM, Hoogenraad CC, Dogterom M, et al. 2009. Mammalian end binding proteins control persistent microtubule growth. J Cell Biol 184:691-706.
34. Kronja I, Kruljac-Letunic A, Caudron-Herger M, Bieling P, Karsenti E. 2009. XMAP215-EB1 interaction is required for proper spindle assembly and chromosome segregation in xenopus egg extract. Mol Biol Cell 20:2684-2696.
35. Leduc C, Padberg-Gehle K, Varga V, Helbing D, Diez S, Howard J. 2012. Molecular crowding creates traffic jams of kinesin motors on microtubules. Proc Natl Acad Sci USA 109:6100-6105.
36. Liu M, Yang S, Wang Y, Zhu H, Yan S, Zhang W, Quan L, Bai J, Xu N. 2009. EB1 acts as an oncogene via activating beta-catenin/TCF pathway to promote cellular growth and inhibit apoptosis. Mol Carcinogen 48:212-219.
37. Lopez BJ, Valentine MT. 2014. Mechanical effects of EB1 on microtubules depend on GTP hydrolysis state and presence of paclitaxel. Cytoskeleton 71:530-541.
38. Lu HL, Ali MY, Bookwalter CS, Warshaw DM, Trybus KM. 2009. Diffusive movement of processive kinesin-1 on microtubules. Traffic 10:1429-1438.
39. Makrides V, Massie MR, Feinstein SC, Lew J. 2004. Evidence for two distinct binding sites for tau on microtubules. Proc Natl Acad Sci USA 101:6746-6751.
40. Makrides V, Shen TE, Bhatia R, Smith BL, Thimm J, Lal R, Feinstein SC. 2003. Microtubule-dependent oligomerization of tau: implications for physiological tau function and tauopathies. J Biol Chem 278:33298-33304.
41. Mandelkow E, Mandelkow E-M. 1995. Microtubules and microtubule-associated proteins. Curr Opin Cell Biol 7:72-81.
42. Maurer SP, Bieling P, Cope J, Hoenger A, Surrey T. 2011. GTPγS microtubules mimic the growing microtubule end structure recognized by end-binding proteins (EBs). Proc Natl Acad Sci USA 108:3988-3993.
43. Maurer SP, Cade NI, Bohner G, Gustafsson N, Boutant E, Surrey T. 2014. EB1 accelerates two conformational transitions important for microtubule maturation and dynamics. Curr Biol 24:372-384.
44. McVicker DP, Hoeprich GJ, Thompson AR, Berger CL. 2014. Tau interconverts between diffusive and stable populations on the microtubule surface in an isoform and lattice specific manner. Cytoskeleton 71:184-194.
45. Miller HP, Wilson L, Leslie W, John JC. 2010. Preparation of Microtubule Protein and Purified Tubulin from Bovine Brain by Cycles of Assembly and Disassembly and Phosphocellulose Chromatography. Methods in Cell Biology, Vol. 95. Academic Press. Chapter 1, pp 2-15.
46. Minoura I, Katayama E, Sekimoto K, Muto E. 2010. One-dimensional brownian motion of charged nanoparticles along microtubules: a model system for weak binding interactions. Biophys J 98:1589-1597.
47. Muto E, Sakai H, Kaseda K. 2005. Long-range cooperative binding of kinesin to a microtubule in the presence of ATP. J Cell Biol 168:691-696.
48. Nishigaki R, Osaki M, Hiratsuka M, Toda T, Murakami K, Jeang KT, Ito H, Inoue T, Oshimura M. 2005. Proteomic identification of differentially-expressed genes in human gastric carcinomas. Proteomics 5:3205-3213.
49. Phillips GN. 1997. Structure and dynamics of green fluorescent protein. Curr Opin Struct Biol 7:821-827.
50. Schek IIIHT, Gardner MK, Cheng J, Odde DJ, Hunt AJ. 2007. Microtubule Assembly Dynamics at the Nanoscale. Curr Biol 17:1445-1455.
51. Schuyler SC, Pellman D. 2001. Microtubule "plus-end-tracking proteins": the end is just the beginning. Cell 105:421-424.
52. Seetapun D, Castle Brian T, McIntyre Alistair J, Tran Phong T, Odde DJ. 2012. Estimating the microtubule GTP cap size in vivo. Curr Biol 22:1681-1687.
53. Sen I, Veprintsev D, Akhmanova A, Steinmetz MO. 2013. End binding proteins are obligatory dimers. PLoS One 8:7.
54. Skube SB, Chaverri JM, Goodson HV. 2010. Effect of GFP tags on the localization of EB1 and EB1 fragments in vivo. Cytoskeleton 67:12.
55. Snyder JP, Nettles JH, Cornett B, Downing KH, Nogales E. 2001. The binding conformation of Taxol in β-tubulin: a model based on electron crystallographic density. Proc Natl Acad Sci USA 98:5312-5316.
56. Stypula-Cyrus Y, Mutyal NN, Dela Cruz M, Kunte DP, Radosevich AJ, Wali R, Roy HK, Backman V. 2014. End-binding protein 1 (EB1) up-regulation is an early event in colorectal carcinogenesis. FEBS Lett 588:829-835.
57. Toso RJ, Jordan MA, Farrell KW, Matsumoto B, Wilson L. 1993. Kinetic stabilization of microtubule dynamic instability in vitro by vinblastine. Biochemistry 32:1285-1293.
58. Valentine MT, Kaplan PD, Thota D, Crocker JC, Gisler T, Prud'homme RK, Beck M, Weitz DA. 2001. Investigating the microenvironments of inhomogeneous soft materials with multiple particle tracking. Phys Rev E 64:061506.
59. Vaughan KT. 2005. TIP maker and TIP marker; EB1 as a master controller of microtubule plus ends. J Cell Biol 171:197-200.
60. Zacharias DA, Violin JD, Newton AC, Tsien RY. 2002. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296:913-916.
61. Zanic M, Stear JH, Hyman AA, Howard J. 2009. EB1 Recognizes the nucleotide state of tubulin in the microtubule lattice. PLoS One 4:1-5.
62. Zhu ZQC, Gupta KK, Slabbekoorn AR, Paulson BA, Folker ES, Goodson HV. 2009. Interactions between EB1 and microtubules: dramatic effect of affinity tags and evidence for cooperative behavior. J Biol Chem 284:32651-32661.
63. Zimmermann D, Motaal BA, von Voithenberg LV, Schliwa M, Okten Z. 2011. Diffusion of myosin V on microtubules: a fine-tuned interaction for which E-hooks are dispensable. PLoS One 6:10.