Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein)

Journal of Neuroscience

Volumn 23, Issue 7, 2003, Pages 2655-2664

  Stepanova, Tatiana ^a   Slemmer, Jenny ^b   Hoogenraad, Casper C ^a,b   Lansbergen, Gideon ^a   Dortland, Bjorn ^a   De Zeeuw, Chris I ^b   Grosveld, Frank ^a   Van Cappellen, Gert ^b   Akhmanova, Anna ^a   Galjart, Niels ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b ERASMUS UNIVERSITY ROTTERDAM   (Netherlands)

Author keywords

Cytoskeleton; Microtubule dynamics; Microtubule plus end tracking proteins; Microtubules; Neuronal differentiation; Neurons

Indexed keywords

CYTOPLASMIC LINKER PROTEIN 170; END BINDING PROTEIN 1; END BINDING PROTEIN 3; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; PLUS END TRACKING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; DENDRITE; GLIA CELL; GROWTH CONE; HUMAN; HUMAN CELL; MICROTUBULE; MICROTUBULE ASSEMBLY; MICROTUBULE ORGANIZING CENTER; MOUSE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN TRANSPORT;

EID: 0345701251     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-07-02655.2003     Document Type: Article

References (41)

1. Akhmanova A, Hoogenraad CC, Drabek K, Stepanova T, Dortland B, Verkerk T, Vermeulen W, Burgering BM, De Zeeuw CI, Grosveld F, Galjart N (2001) CLASPs are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 104:923-935.
2. Baas PW (1997) Microtubules and axonal growth. Curr Opin Cell Biol 9:29-36.
3. Baas PW, Ahmad FJ (1992) The plus ends of stable microtubules are the exclusive nucleating structures for microtubules in the axon. J Cell Biol 116:1231-1241.
4. Baas PW, Black MM (1990) Individual microtubules in the axon consist of domains that differ in both composition and stability. J Cell Biol 111:495-509.
5. Baas PW, Deitch JS, Black MM, Banker GA (1988) Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc Natl Acad Sci USA 85:8335-8339.
6. Baas PW, Black MM, Banker GA (1989) Changes in microtubule polarity orientation during the development of hippocampal neurons in culture. J Cell Biol 109:3085-3094.
7. Baas PW, Slaughter T, Brown A, Black MM (1991) Microtubule dynamics in axons and dendrites. J Neurosci Res 30:134-153.
8. Baas PW, Ahmad FJ, Pienkowski TP, Brown A, Black MM (1993) Sites of microtubule stabilization for the axon. J Neurosci 13:2177-2185.
9. Buck KB, Zheng JQ (2002) Growth cone turning induced by direct local modification of microtubule dynamics. J Neurosci 22:9358-9367.
10. Chang S, Svitkina TM, Borisy GG, Popov SV (1999) Speckle microscopic evaluation of microtubule transport in growing nerve processes. Nat Cell Biol 1:399-403.
11. Coquelle FM, Caspi M, Cordelieres FP, Dompierre JP, Dujardin DL, Koifman C, Martin P, Hoogenraad CC, Akhmanova A, Galjart N, De Mey JR, Reiner O (2002) LIS1, CLIP-170's key to the dynein/dynactin pathway. Mol Cell Biol 22:3089-3102.
12. de Hoop MJ, Meyn L, Dotti CG (1998) Culturing hippocampal neurons and astrocytes from fetal rat brain. In: Cell biology: a laboratory handbook, 2nd Ed (Celis JE, ed), pp 154-163. San Diego: Academic.
13. Dent EW, Callaway JL, Szebenyi G, Baas PW, Kalil K (1999) Reorganization and movement of microtubules in axonal growth cones and developing interstitial branches. J Neurosci 19:8894-8908.
14. De Zeeuw CI, Hoogenraad CC, Goedknegt E, Hertzberg E, Neubauer A, Grosveld F, Galjart N (1997) CLIP-115, a novel brain-specific cyloplasmic linker protein, mediates the localization of dendritic lamellar bodies. Neuron 19:1187-1199.
15. Dotti CG, Sullivan CA, Banker GA (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8:1454-1468.
16. Downing KH (2000) Structural basis for the interaction of tubulin with proteins and drugs that affect microtubule dynamics. Annu Rev Cell Dev Biol 16:89-111.
17. Ehrengruber MU, Lundstrom K, Schweitzer C, Heuss C, Schlesinger S, Gahwiler BH (1999) Recombinant Semliki Forest virus and Sindbis virus efficiently infect neurons in hippocampal slice cultures. Proc Natl Acad Sci USA 96:7041-7046.
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.
19. He Y, Yu W, Baas PW (2002) Microtubule reconfiguration during axonal retraction induced by nitric oxide. J Neurosci 22:5982-5991.
20. Hoogenraad CC, Akhmanova A, Grosveld F, De Zeeuw CI, Galjart N (2000) Functional analysis of CLIP-115 and its binding to microtubules. J Cell Sci 113:2285-2297.
21. Hoogenraad CC, Koekkoek B, Akhmanova A, Krugers H, Dortland B, Miedema M, van Alphen A, Kistler WM, Jaegle M, Koutsourakis M, Van Camp N, Verhoye M, van der Linden A, Kaverina I, Grosveld F, De Zeeuw CI, Galjart N (2002) Targeted mutation of Cyln2 in the Williams syndrome critical region links CLIP-115 haploinsufficiency to neurodevelopmental abnormalities in mice. Nat Genet 32:116-127.
22. Komarova YA, Vorobjev IA, Borisy GG (2002a) Life cycle of MTs: persistent growth in the cell interior, asymmetric transition frequencies and effects of the cell boundary. J Cell Sci 115:3527-3539.
23. Komarova YA, Akhmanova AS, Kojima S, Galjart N, Borisy GG (2002b) Cytoplasmic linker proteins promote microtubule rescue in vivo. J Cell Biol 159:589-599.
24. Lundstrom K, Rotmann D, Hermann D, Schneider EM, Ehrengruber MU (2001a) Novel mutant Semliki Forest virus vectors: gene expression and localization studies in neuronal cells. Histochem Cell Biol 115:83-91.
25. Lundstrom K, Schweitzer C, Rotmann D, Hermann D, Schneider EM, Ehrengruber MU (2001b) Semliki Forest virus vectors: efficient vehicles for in vitro and in vivo gene delivery. FEBS Lett 504:99-103.
26. Mimori-Kiyosue Y, Shiina N, Tsukita S (2000a) Adenomatous polyposis coli (APC) protein moves along microtubules and concentrates at their growing ends in epithelial cells. J Cell Biol 148:505-518.
27. Mimori-Kiyosue Y, Shiina N, Tsukita S (2000b) The dynamic behavior of the APC-binding protein EB1 on the distal ends of microtubules. Curr Biol 10:865-868.
28. Morrison EE, Moncur PM, Askham JM (2002) EB1 identifies sites of microtubule polymerisation during neurite development. Brain Res Mol Brain Res 98:145-152.
29. Nakagawa H, Koyama K, Murata Y, Morito M, Akiyama T, Nakamura Y (2000) EB3, a novel member of the EB1 family preferentially expressed in the central nervous system, binds to a CNS-specific APC homologue. Oncogene 19:210-216.
30. Perez F, Diamantopoulos GS, Stalder R, Kreis TE (1999) CLIP-170 highlights growing microtubule ends in vivo. Cell 96:517-527.
31. Pierre P, Pepperkok R, Kreis TE (1994) Molecular characterization of two functional domains of CLIP-170 in vivo. J Cell Sci 107:1909-1920.
32. Rickard JE, Kreis TE (1991) Binding of pp170 to microtubules is regulated by phosphorylation. J Biol Chem 266:17597-17605.
33. Rogers SL, Rogers GC, Sharp DJ, Vale RD (2002) Drosophila EB1 is important for proper assembly, dynamics, and positioning of the mitotic spindle. J Cell Biol 158:873-884.
34. Schuyler SC, Pellman D (2001) Microtubule "plus-end-tracking proteins": the end is just the beginning. Cell 105:421-424.
35. Su LK, Qi Y (2001) Characterization of human MAPRE genes and their proteins. Genomics 71:142-149.
36. Terada S, Kinjo M, Hirokawa N (2000) Oligomeric tubulin in large transporting complex is transported via kinesin in squid giant axons. Cell 103:141-155.
37. Tirnauer JS, Grego S, Salmon ED, Mitchison TJ (2002) EB1-microtubule interactions in Xenopus egg extracts: role of EB1 in microtubule stabilization and mechanisms of targeting to microtubules. Mol Biol Cell 13:3614-3626.
38. Valetti C, Wetzel DM, Schrader M, Hasbani MJ, Gill SR, Kreis TE, Schroer TA (1999) Role ofdynactin in endocytic traffic: effects of dynamitin overexpression and colocalization with CLIP-170. Mol Biol Cell 10:4107-4120.
39. Vaughan KT, Tynan SH, Faulkner NE, Echeverri CJ, Vallee RB (1999) Colocalization of cytoplasmic dynein with dynactin and CLIP-170 at microtubule distal ends. J Cell Sci 112:1437-1447.
40. Glued to microtubule plus ends in organelle transport. J Cell Biol 158:305-319.
41. Yu W, Baas PW (1994) Changes in microtubule number and length during axon differentiation. J Neurosci 14:2818-2829.