Clasp-mediated microtubule bundling regulates persistent motility and contact repulsion in Drosophila macrophages in vivo

Journal of Cell Biology

Volumn 189, Issue 4, 2010, Pages 681-689

  Stramer, Brian ^a,b   Moreira, Severina ^b   Millard, Tom ^b,c   Evans, Iwan ^d   Huang, Chieh Yin ^a   Sabet, Ola ^d   Milner, Martin ^e   Dunn, Graham ^a   Martin, Paul ^b   Wood, Will ^d  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d University of Bath   (United Kingdom)

^e UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BINDING PROTEIN; FLUORESCENT DYE; SPASTIN;

ARTICLE; CELL COMMUNICATION; CELL MOTILITY; CELL POLARITY; DEPOLYMERIZATION; DROSOPHILA MELANOGASTER; IN VIVO STUDY; MACROPHAGE MIGRATION; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; REGULATORY MECHANISM;

ADENOSINE TRIPHOSPHATASES; ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MICROFILAMENTS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES;

DROSOPHILA MELANOGASTER;

EID: 77952335884     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200912134     Document Type: Article

References (41)

1. Abercrombie, M., and J.E. Heaysman. 1953. Observations on the social behaviour of cells in tissue culture. I. Speed of movement of chick heart fibroblasts in relation to their mutual contacts. Exp. Cell Res. 5:111-131. doi:10.1016/0014-4827(53)90098-6
2. Abercrombie, M., and J.E. Heaysman. 1954. Observations on the social behaviour of cells in tissue culture. II. Monolayering of fibroblasts. Exp. Cell Res. 6:293-306. doi:10.1016/0014-4827(54)90176-7
3. Brand, A. 1995. GFP in Drosophila. Trends Genet. 11:324-325. doi:10.1016/ S0168-9525(00)89091-89095
4. Brückner, K., L. Kockel, P. Duchek, C.M. Luque, P. Rørth, and N. Perrimon. 2004. The PDGF/VEGF receptor controls blood cell survival in Drosophila. Dev. Cell. 7:73-84. doi:10.1016/j.devcel.2004.06.007 (Pubitemid 39172689)
5. Buck, K.B., and J.Q. Zheng. 2002. Growth cone turning induced by direct local modification of microtubule dynamics. J. Neurosci. 22:9358-9367.
6. Carmona-Fontaine, C., H.K. Matthews, S. Kuriyama, M. Moreno, G.A. Dunn, M. Parsons, C.D. Stern, and R. Mayor. 2008. Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature. 456:957-961. doi:10.1038/nature07441
7. Diamantopoulos, G.S., F. Perez, H.V. Goodson, G. Batelier, R. Melki, T.E. Kreis, and J.E. Rickard. 1999. Dynamic localization of CLIP-170 to microtubule plus ends is coupled to microtubule assembly. J. Cell Biol. 144:99-112. doi:10.1083/jcb.144.1.99
8. Doyle, A.D., F.W. Wang, K. Matsumoto, and K.M. Yamada. 2009. One-dimensional topography underlies three-dimensional fibrillar cell migration. J. Cell Biol. 184:481-490. doi:10.1083/jcb.200810041
9. Dutta, D., J.W. Bloor, M. Ruiz-Gomez, K. VijayRaghavan, and D.P. Kiehart. 2002. Real-time imaging of morphogenetic movements in Drosophila using Gal4-UAS-driven expression of GFP fused to the actin-binding domain of moesin. Genesis. 34:146-151. doi:10.1002/gene.10113
10. Glaven, J.A., I. Whitehead, S. Bagrodia, R. Kay, and R.A. Cerione. 1999. The Dbl-related protein, Lfc, localizes to microtubules and mediates the activation of Rac signaling pathways in cells. J. Biol. Chem. 274:2279-2285. doi:10.1074/jbc.274.4.2279 (Pubitemid 29061383)
11. Gloushankova, N.A., M.F. Krendel, N.O. Alieva, E.M. Bonder, H.H. Feder, J.M. Vasiliev, and I.M. Gelfand. 1998. Dynamics of contacts between lamellae of fibroblasts: essential role of the actin cytoskeleton. Proc. Natl. Acad. Sci. USA. 95:4362-4367. doi:10.1073/pnas.95.8.4362
12. Halfon, M.S., S. Gisselbrecht, J. Lu, B. Estrada, H. Keshishian, and A.M. Michelson. 2002. New fluorescent protein reporters for use with the Drosophila Gal4 expression system and for vital detection of balancer chromosomes. Genesis. 34:135-138. doi:10.1002/gene.10136
13. Jankovics, F., and D. Brunner. 2006. Transiently reorganized microtubules are essential for zippering during dorsal closure in Drosophila melanogaster. Dev. Cell. 11:375-385. doi:10.1016/j.devcel.2006.07.014 (Pubitemid 44283946)
14. Janson, M.E., M.E. de Dood, and M. Dogterom. 2003. Dynamic instability of microtubules is regulated by force. J. Cell Biol. 161:1029-1034. doi:10.1083/jcb.200301147
15. Kaverina, I., O. Krylyshkina, and J.V. Small. 1999. Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J. Cell Biol. 146:1033-1044. doi:10.1083/jcb.146.5.1033 (Pubitemid 29430445)
16. Kiger, A.A., B. Baum, S. Jones, M.R. Jones, A. Coulson, C. Echeverri, and N. Perrimon. 2003. A functional genomic analysis of cell morphology using RNA interference. J. Biol. 2:27. doi:10.1186/1475-4924-2-27
17. Krendel, M., F.T. Zenke, and G.M. Bokoch. 2002. Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat. Cell Biol. 4:294-301. doi:10.1038/ncb773
18. Laan, L., J. Husson, E.L. Munteanu, J.W. Kerssemakers, and M. Dogterom. 2008. Force-generation and dynamic instability of microtubule bundles. Proc. Natl. Acad. Sci. USA. 105:8920-8925. doi:10.1073/pnas.0710311105
19. Lee, H., U. Engel, J. Rusch, S. Scherrer, K. Sheard, and D. Van Vactor. 2004. The microtubule plus end tracking protein Orbit/MAST/CLASP acts downstream of the tyrosine kinase Abl in mediating axon guidance. Neuron. 42:913-926. doi:10.1016/j.neuron.2004.05.020
20. Millard, T.H., and P. Martin. 2008. Dynamic analysis of filopodial interactions during the zippering phase of Drosophila dorsal closure. Development. 135:621-626. doi:10.1242/dev.014001
21. Omelchenko, T., E. Fetisova, O. Ivanova, E.M. Bonder, H. Feder, J.M. Vasiliev, and I.M. Gelfand. 2001. Contact interactions between epitheliocytes and fibroblasts: formation of heterotypic cadherin-containing adhesion sites is accompanied by local cytoskeletal reorganization. Proc. Natl. Acad. Sci. USA. 98:8632-8637. doi:10.1073/pnas.151247698
22. Paladi, M., and U. Tepass. 2004. Function of Rho GTPases in embryonic blood cell migration in Drosophila. J. Cell Sci. 117:6313-6326. doi:10.1242/jcs.01552 (Pubitemid 40214559)
23. Perez, F., G.S. Diamantopoulos, R. Stalder, and T.E. Kreis. 1999. CLIP-170 high-lights growing microtubule ends in vivo. Cell. 96:517-527. doi:10.1016/ S0092-8674(00)80656-X
24. Rajnicek, A.M., L.E. Foubister, and C.D. McCaig. 2006. Growth cone steering by a physiological electric field requires dynamic microtubules, microfilaments and Rac-mediated filopodial asymmetry. J. Cell Sci. 119:1736-1745. doi:10.1242/jcs.02897
25. Ren, Y., R. Li, Y. Zheng, and H. Busch. 1998. Cloning and characterization of GEF-H1, a microtubule-associated guanine nucleotide exchange factor for Rac and Rho GTPases. J. Biol. Chem. 273:34954-34960. doi:10.1074/jbc.273.52.34954 (Pubitemid 29028193)
26. Rogers, S.L., U. Wiedemann, N. Stuurman, and R.D. Vale. 2003. Molecular requirements for actin-based lamella formation in Drosophila S2 cells. J. Cell Biol. 162:1079-1088. doi:10.1083/jcb.200303023
27. Rogers, S.L., U. Wiedemann, U. Häcker, C. Turck, and R.D. Vale. 2004. Drosophila RhoGEF2 associates with microtubule plus ends in an EB1-dependent manner. Curr. Biol. 14:1827-1833. doi:10.1016/j.cub.2004.09.078
28. Siegrist, S.E., and C.Q. Doe. 2007. Microtubule-induced cortical cell polarity. Genes Dev. 21:483-496. doi:10.1101/gad.1511207
29. Small, J.V., B. Geiger, I. Kaverina, and A. Bershadsky. 2002. How do microtubules guide migrating cells? Nat. Rev. Mol. Cell Biol. 3:957-964. doi:10.1038/nrm971
30. Sousa, A., R. Reis, P. Sampaio, and C.E. Sunkel. 2007. The Drosophila CLASP homologue, Mast/Orbit regulates the dynamic behaviour of interphase microtubules by promoting the pause state. Cell Motil. Cytoskeleton. 64:605-620. doi:10.1002/cm.20208 (Pubitemid 47106165)
31. Stramer, B., and W. Wood. 2009. Chemotaxis: inflammation and wound healing in Drosophila embryos. In Chemotaxis: methods and protocols. Methods in Molecular Biology, Vol. 571. T. Jin and D. Hereld, editors. Humana Press Inc., Totowa, NJ. 137-149.
32. Stramer, B., W. Wood, M.J. Galko, M.J. Redd, A. Jacinto, S.M. Parkhurst, and P. Martin. 2005. Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration. J. Cell Biol. 168:567-573. doi:10.1083/jcb.200405120 (Pubitemid 40271022)
33. Stramer, B., M. Winfield, T. Shaw, T.H. Millard, S. Woolner, and P. Martin. 2008. Gene induction following wounding of wild-type versus macrophage-deficient Drosophila embryos. EMBO Rep. 9:465-471. doi:10.1038/embor.2008.34
34. Trotta, N., G. Orso, M.G. Rossetto, A. Daga, and K. Broadie. 2004. The hereditary spastic paraplegia gene, spastin, regulates microtubule stability to modulate synaptic structure and function. Curr. Biol. 14:1135-1147. doi:10.1016/j.cub.2004.06.058
35. van Horck, F.P., M.R. Ahmadian, L.C. Haeusler, W.H. Moolenaar, and O. Kranenburg. 2001. Characterization of p190RhoGEF, a RhoA-specific guanine nucleotide exchange factor that interacts with microtubules. J. Biol. Chem. 276:4948-4956. doi:10.1074/jbc.M003839200
36. Williamson, T., P.R. Gordon-Weeks, M. Schachner, and J. Taylor. 1996. Microtubule reorganization is obligatory for growth cone turning. Proc. Natl. Acad. Sci. USA. 93:15221-15226. doi:10.1073/pnas.93.26.15221
37. Wood, W., and A. Jacinto. 2007. Drosophila melanogaster embryonic haemocytes: masters of multitasking. Nat. Rev. Mol. Cell Biol. 8:542-551. doi:10.1038/nrm2202
38. Wood, W., C. Faria, and A. Jacinto. 2006. Distinct mechanisms regulate hemocyte chemotaxis during development and wound healing in Drosophila melanogaster. J. Cell Biol. 173:405-416. doi:10.1083/jcb.200508161
39. Zanet, J., B. Stramer, T. Millard, P. Martin, F. Payre, and S. Plaza. 2009. Fascin is required for blood cell migration during Drosophila embryogenesis. Development. 136:2557-2565. doi:10.1242/dev.036517
40. Zhou, F.Q., J. Zhou, S. Dedhar, Y.H. Wu, and W.D. Snider. 2004. NGF-induced axon growth is mediated by localized inactivation of GSK-3beta and functions of the microtubule plus end binding protein APC. Neuron. 42:897-912. doi:10.1016/j.neuron.2004.05.011
41. Zumbrunn, J., K. Kinoshita, A.A. Hyman, and I.S. Näthke. 2001. Binding of the adenomatous polyposis coli protein to microtubules increases microtubule stability and is regulated by GSK3 beta phosphorylation. Curr. Biol. 11:44-49. doi:10.1016/S0960-9822(01)00002-1 (Pubitemid 32062715)