The kinesin KIF1C and microtubule plus ends regulate podosome dynamics in macrophages

Molecular Biology of the Cell

Volumn 17, Issue 6, 2006, Pages 2811-2823

  Kopp, Petra ^a   Lammers, Reiner ^b   Aepfelbacher, Martin ^c   Woehlke, Günther ^a   Rudel, Thomas ^d   Machuy, Nikolaus ^d   Steffen, Walter ^e   Linder, Stefan ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^e HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATE; DYNEIN ADENOSINE TRIPHOSPHATASE; KINESIN; MYOSIN IIA; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; TUBULIN;

ARTICLE; CELL FATE; CELL MIGRATION; CONTROLLED STUDY; CYTOSKELETON; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HYDROLYSIS; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; MACROPHAGE; MASS SPECTROMETRY; MICROTUBULE; MONOCYTE; MUTAGENESIS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION;

EID: 33744724934     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-11-1010     Document Type: Article

References (44)

1. Babb, S. G., Matsudaira, P., Sato, M., Correia, I., and Lim, S. S. (1997). Fimbrin in podosomes of monocyte-derived osteoclasts. Cell Motil. Cytoskeleton. 37, 308-325.
2. Bershadsky, A., Balaban, N. Q., and Geiger, B. (2003). Adhesion-dependent cell mechanosensitivity. Annu. Rev. Cell Dev. Biol. 19, 677-695.
3. Buccione, R., Orth, J., and McNiven, M. (2004). Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Mol. Cell. Biol. 5, 647-657.
4. Burns, S., Thrasher, A. J., Blundell, M. P., Machesky, L., and Jones, G. E. (2001). Configuration of human dendritic cell cytoskeleton by Rho GTPases, the WAS protein, and differentiation. Blood 98, 1142-1149.
5. Destaing, O., Saltel, F., Geminard, J. C., Jurdic, P., and Bard, F. (2003). Podosomes display actin turnover and dynamic self-organization in osteoclasts expressing actin-green fluorescent protein. Mol. Biol. Cell 14, 407-416.
6. Destaing, O., Saltel, F., Gillquin, B., Chabadel, A., Khochbin, S., Ory, S., and Jurdic, P. (2005). A novel Rho-mDia2-HDAC6 pathway controls podosome patterning through microtubule acetylation in osteoclasts. J. Cell Sci. 118, 2901-2911.
7. Dorner, C., Ciossek, T., Müller, S., Møller, N., Ullrich, A., and Lammers, R. (1998). Characterization of KIF1C, a new kinesin-like protein involved in vesicle transport from the Golgi apparatus to the endoplasmic reticulum. J. Biol. Chem. 273, 20267-20275.
8. Dorner, C., Ullrich, A., Häring, H., and Lammers, R. (1999). The kinesin-like motor protein KIF1C occurs in intact cells as a dimer and associates with proteins of the 14-3-3 family. J. Biol. Chem. 274, 33654-33660.
9. Evans, J., Correia, I., Krasavina, O., Watson, N., and Matsudaira, P. (2003). Macrophage podosomes assemble at the leading lamella by growth and fragmentation. J. Cell Biol. 161, 697-705.
10. Galjart, N. (2005). CLIPs and CLASPs and cellular dynamics. Nat. Rev. Mol. Cell. Biol. 6, 487-498.
11. Gavazzi, I., Nermut, M. V., and Marchisio, P. C. (1989). Ultrastructure and gold-immunolabelling of cell-substratum adhesions (podosomes) in RSV-transformed BHK cells. J. Cell Sci. 94, 85-99.
12. Goode, B., Drubin, D., and Barnes, G. (2000). Functional cooperation between the microtubule and actin cytoskeletons. Curr. Opin. Cell Biol. 12, 63-71.
13. Gundersen, G. G., Gomes, E. R., and Wen, Y. (2004). Cortical control of microtubule stability and polarization. Curr. Opin. Cell Biol. 16, 106-112.
14. Honegger, A. M., Dull, T. J., Felder, S., Van Obberghen, E., Bellot, F., Szapary, D., Schmidt, A., Ullrich, A., and Schlessinger, J. (1987). Point mutation in the ATP binding site of EGF receptor abolishes protein-tyrosine kinase activity and alters cellular routing. Cell 51, 199-209.
15. Huang, J., Brady, S., Richards, B., Stenoien, D., Resau, J., Copeland, N., and Jenkins, N. (1999). Direct interaction of microtubule- and actin-based transport motors. Nature 397, 267-270.
16. Ingold, A. L., Cohn, S., and Scholey, J. (1988). Inhibition of kinesin-driven microtubule motility by monoclonal antibodies to kinesin heavy chains. J. Cell Biol. 107, 2657-2667.
17. Kanehisa, J., Yamanaka, T., Dio, S., Turksen, K., Heersche, J., Aubin, F., and Takeuchi, H. (1990). A band of F-actin containing podosomes is involved in bone resorption by osteoclasts. Bone 11, 287-293.
18. Kaverina, I., Krylyshkina, O., and Small, J. (1999). Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J. Cell Biol. 146, 1033-1043.
19. Kaverina, I., Krylyshkina, O., and Small, J. (2002). Regulation of substrate adhesion dynamics during cell motility. Int. J. Biochem. Cell Biol. 34, 746-761.
20. Krylyshkina, O., Anderson, K., Kaverina, I., Upmann, I., Manstein, D., Small, J., and Toomre, D. (2003). Nanometer targeting of microtubules to focal adhesions. J. Cell Biol. 161, 853-859.
21. Krylyshkina, O., Kaverina, I., Kranewitter, W., Steffen, W., Alonso, M., Cross, R., and Small, J. (2002). Modulation of substrate adhesion dynamics via microtubule targeting requires kinesin-1. J. Cell Biol. 156, 349-359.
22. Lawrence, C. J., et al. (2004). A standardized kinesin nomenclature. J. Cell Biol. 167, 19-22.
23. Limouze, J., Straight, A. F., Mitchison, T., and Sellers, J. F. (2004). Specificity of blebbistatin, an inhibitor of myosin II. J. Muscle Res. Cell Motil. 25, 337-341.
24. Linder, S., and Aepfelbacher, M. (2003). Podosomes: adhesion hot-spots of invasive cells. Trends Cell Biol. 13, 376-385.
25. Linder, S., Hufner, K., Wintergerst, U., and Aepfelbacher, M. (2000). Microtubule-dependent formation of podosomal adhesion structures in primary human macrophages. J. Cell Sci. 113, 4165-4176.
26. Linder, S., and Kopp, P. (2005). Podosomes at a glance. J. Cell Sci. 118, 2079-2082.
27. Linder, S., Nelson, D., Weiss, M., and Aepfelbacher, M. (1999). Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages. Proc. Natl. Acad. Sci. USA 96, 9648-9653.
28. Louie, R. K., Bahmanyar, S., Siemers, K. A., Votin, V., Chang, P., Stearns, T., Nelson, W. J., and Barth, A. I. (2004). Adenomatous polyposis coli and EB1 localize in close proximity of the mother centriole and EB1 is a functional component of centrosomes. J. Cell Sci. 117, 1117-1128.
29. Machuy, N., Thiede, B., Rajalingam, K., Dimmler, C., Thieck, O., Meyer, T. F., and Rudel, T. (2005). A global approach combining proteome analysis and phenotypic screening with RNA interference yields novel apoptosis regulators. Mol. Cell Proteomics 4, 44-55.
30. Marchisio, P. C., D'Urso, N., Comoglio, P. M., Giancotti, F. G., and Tarone, G. (1988). Vanadate-treated baby hamster kidney fibroblasts show cytoskeleton and adhesion patterns similar to their Rous sarcoma virus-transformed counterparts. J. Cell. Biochem. 37, 151-159.
31. Miki, H., Setou, M., Kaneshiro, K., and Hirokawa, N. (2001). All kinesin superfamily protein, KIF, genes in mouse and human. Proc. Natl. Acad. Sci. USA 98, 7004-7011.
32. Morris, R., and Scholey, J. (1997). Heterotrimeric Kinesin-II is required for the assembly of motile 9+2 ciliary axonemes on sea urchin embryos. J. Cell Biol. 138, 1009-1022.
33. Nakajima, K., Takei, Y., Tanaka, Y., Nakagawa, T., Nakata, T., Noda, Y., Setou, M., and Hirokawa, N. (2002). Molecular motor KIF1C is not essential for mouse survival and motor-dependent retrograde Golgi apparatus-to-endoplasmic reticulum transport. Mol. Cell. Biol. 22, 866-873.
34. Nakata, T., and Hirokawa, N. (1995). Point mutation of adenosine triphosphate-binding motif generated rigor kinesin that selectively blocks anterograde lysosome membrane transport. J. Cell Biol. 131, 1039-1053.
35. Osiak, A.-E., Zenner, G., and Linder, S. (2005). Subconfluent endothelial cells form podosomes downstream of cytokine and RhoGTPase signaling. Exp. Cell Res. 307, 342-353.
36. Rodriguez, O. C., Schaefer, A., Mandato, C., Forscher, P., Bement, W., and Waterman-Storer, C. (2003). Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat. Cell Biol. 5, 599-609.
37. Sack, S., Kull, F. J., and Mandelkow, E. (1999). Motor proteins of the kinesin family. Structures, variations, and nucleotide binding sites. Eur. J. Biochem. 262, 1-11.
38. Salmon, W. C., Adams, M. C., and Waterman-Storer, C. M. (2002). Dual-wavelength fluorescent speckle microscopy reveals coupling of microtubule and actin movements in migrating cells. J. Cell Biol. 158, 31-37.
39. Schliwa, M., Ezzell, R. M., and Euteneuer, U. (1984). erythro-9-[3-(2-Hydroxynonyl)]adenine is an effective inhibitor of cell motility and actin assembly. Proc. Natl. Acad. Sci. USA 81, 6044-6048.
40. Schliwa, M., and Woehlke, G. (2003). Molecular motors. Nature 422, 759-765.
41. Small, J. V., Geiger, B., Kaverina, I., and Bershadsky, A. (2002). How do microtubules guide migrating cells? Nat. Rev. Mol. Cell. Biol. 3, 957-964.
42. Steffen, W., Karki, S., Vaughan, K. T., Vallee, R. B., Holzbaur, E.L.F., Weiss, D. G., and Kuznetsov, S. A. (1997). The involvement of the intermediate chain of cytoplasmic dynein in binding the motor complex to membranous organelles of Xenopus oocytes. Mol. Biol. Cell 8, 2077-2088.
43. Watters, J. W., Dewar, K., Lehoczky, J., Boyartchuk, V., and Dietrich, W. F. (2001). Kif1C, a kinesin-like motor protein, mediates mouse macrophage resistance to anthrax lethal factor. Curr. Biol. Bull. 11, 1503-1511.
44. Zhao, C., et al. (2001). Charcot-Marie-Tooth disease type 2A caused by mutation in a microtubule motor KIF1Bβ. Cell 105, 587-597.