Microtubule acetylation regulates dynamics of KIF1C-powered vesicles and contact of microtubule plus ends with podosomes

European Journal of Cell Biology

Volumn 93, Issue 10-12, 2014, Pages 424-437

  Bhuwania, Ridhirama ^a   Castro Castro, Antonio ^b,c   Linder, Stefan ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b INSTITUT CURIE   (France)

^c CNRS   (France)

Author keywords

KIF1C; Kinesin; Macrophage; MEC 17; Microtubule acetylation; Podosomes

Indexed keywords

ACYLTRANSFERASE; ALPHA TUBULIN; KINESIN; MEMBRANE PROTEIN; PROTEIN KIF1C; PROTEIN MEC 17; PROTEOME; SMALL INTERFERING RNA; TUBACIN; UNCLASSIFIED DRUG; ANILIDE; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID; KIF1C PROTEIN, HUMAN; MEC17 PROTEIN, HUMAN; TUBULIN;

ACETYLATION; ACTIN FILAMENT; ARTICLE; CELL ADHESION; CELL FUNCTION; CELL ORGANELLE; CELL VACUOLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MACROPHAGE; MICROTUBULE; MOLECULAR DYNAMICS; PODOSOME; PROTEIN MODIFICATION; REGULATORY MECHANISM; CELL SURFACE; GENETICS; METABOLISM; PRIMARY CELL CULTURE; TRANSPORT VESICLE;

ACETYLATION; ACETYLTRANSFERASES; ACTIN CYTOSKELETON; ANILIDES; CELL SURFACE EXTENSIONS; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; KINESIN; MACROPHAGES; MICROTUBULES; PRIMARY CELL CULTURE; RNA, SMALL INTERFERING; TRANSPORT VESICLES; TUBULIN;

EID: 84920604951     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2014.07.006     Document Type: Article

References (68)

1. Akella J.S., Wloga D., Kim J., Starostina N.G., Lyons-Abbott S., Morrissette N.S., Dougan S.T., Kipreos E.T., Gaertig J. MEC-17 is an alpha-tubulin acetyltransferase. Nature 2010, 467:218-222.
2. Akisaka T., Yoshida H., Takigawa T. Differential distribution of posttranslationally modified microtubules in osteoclasts. J. Histochem. Cytochem. 2011, 59:630-638.
3. Asthana J., Kapoor S., Mohan R., Panda D. Inhibition of HDAC6 deacetylase activity increases its binding with microtubules and suppresses microtubule dynamic instability in MCF-7 cells. J. Biol. Chem. 2013, 288:22516-22526.
4. Benado A., Nasagi-Atiya Y., Sagi-Eisenberg R. Protein trafficking in immune cells. Immunobiology 2009, 214:403-421.
5. Bhuwania R., Cornfine S., Fang Z., Krüger M., Luna E.J., Linder S. Supervillin couples myosin-dependent contractility to podosomes and enables their turnover. J. Cell Sci. 2012, 125:2300-2314.
6. Biosse Duplan M., Zalli D., Stephens S., Zenger S., Neff L., Oelkers J.M., Lai F.P., Horne W., Rottner K., Baron R. Microtubule dynamic instability controls podosome patterning in osteoclasts through EB1, cortactin, and Src. Mol. Cell. Biol. 2014, 34:16-29.
7. Block M.R., Badowski C., Millon-Fremillon A., Bouvard D., Bouin A.P., Faurobert E., Gerber-Scokaert D., Planus E., Albiges-Rizo C. Podosome-type adhesions and focal adhesions, so alike yet so different. Eur. J. Cell Biol. 2008, 87:491-506.
8. Bohm K.J., Stracke R., Baum M., Zieren M., Unger E. Effect of temperature on kinesin-driven microtubule gliding and kinesin ATPase activity. FEBS Lett. 2000, 466:59-62.
9. Bouchet-Marquis C., Zuber B., Glynn A.M., Eltsov M., Grabenbauer M., Goldie K.N., Thomas D., Frangakis A.S., Dubochet J., Chrétien D. Visualization of cell microtubules in their native state. Biol. Cell 2007, 99:45-53.
10. Burton P.R. Luminal material in microtubules of frog olfactory axons: structure and distribution. J. Cell Biol. 1984, 99:520-528.
11. Castro-Castro A., Janke C., Montagnac G., Paul-Gilloteaux P., Chavrier P. ATAT1/MEC-17 acetyltransferase and HDAC6 deacetylase control a balance of acetylation of alpha-tubulin and cortactin and regulate MT1-MMP trafficking and breast tumor cell invasion. Eur. J. Cell Biol. 2012, 91:950-960.
12. Cervero P., Panzer L., Linder S. Podosome reformation in macrophages: assays and analysis. Methods Mol. Biol. 2013, 1046:97-121.
13. Chen W.T. Proteases associated with invadopodia, and their role in degradation of extracellular matrix. Enzym. Protein 1996, 49:59-71.
14. Cornfine S., Himmel M., Kopp P., El Azzouzi K., Wiesner C., Krüger M., Rudel T., Linder S. The kinesin KIF9 and reggie/flotillin proteins regulate matrix degradation by macrophage podosomes. Mol. Biol. Cell 2011, 22:202-215.
15. Destaing O., Saltel F., Géminard J.C., Jurdic P., Bard F. Podosomes display actin turnover and dynamic self-organization in osteoclasts expressing actin-green fluorescent protein. Mol. Biol. Cell 2003, 14:407-416.
16. Destaing O., Saltel F., Gilquin B., Chabadel A., Khochbin S., Ory S., Jurdic P. A novel Rho-mDia2-HDAC6 pathway controls podosome patterning through microtubule acetylation in osteoclasts. J. Cell Sci. 2005, 118:2901-2911.
17. Dorner C., Ciossek T., Müller S., Møller P.H., Ullrich A., Lammers R. Characterization of KIF1C, a new kinesin-like protein involved in vesicle transport from the Golgi apparatus to the endoplasmic reticulum. J. Biol. Chem. 1998, 273:20267-20275.
18. Dunn S., Morrison E.E., Liverpool T.B., Molina-París C., Cross R.A., Alonso M.C., Peckham M. Differential trafficking of Kif5c on tyrosinated and detyrosinated microtubules in live cells. J. Cell Sci. 2008, 121:1085-1095.
19. Etienne-Manneville S. Microtubules in cell migration. Annu. Rev. Cell Dev. Biol. 2013, 29:471-499.
20. Evans J.G., Correia I., Krasavina O., Watson N., Matsudaira P. Macrophage podosomes assemble at the leading lamella by growth and fragmentation. J. Cell Biol. 2003, 161:697-705.
21. Franker M.A., Hoogenraad C.C. Microtubule-based transport - basic mechanisms, traffic rules and role in neurological pathogenesis. J. Cell Sci. 2013, 126:2319-2329.
22. Gu Z., Noss E.H., Hsu V.W., Brenner M.B. Integrins traffic rapidly via circular dorsal ruffles and macropinocytosis during stimulated cell migration. J. Cell Biol. 2011, 193:61-70.
23. Haggarty S.J., Koeller K.M., Wong J.C., Grozinger C.M., Schreiber S.L. Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:4389-4394.
24. Hammond J.W., Huang C.F., Kaech S., Jacobson C., Banker G., Verhey K.J. Posttranslational modifications of tubulin and the polarized transport of kinesin-1 in neurons. Mol. Biol. Cell 2010, 21:572-583.
25. Hoepfner S., Severin F., Cabezas A., Habermann B., Runge A., Gillooly D., Stenmark H., Zerial M. Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B. Cell 2005, 121:437-450.
26. Howes S.C., Alushin G.M., Shida T., Nachury M.V., Nogales E. Effects of tubulin acetylation and tubulin acetyltransferase binding on microtubule structure. Mol. Biol. Cell 2014, 25:257-266.
27. Hubbert C., Guardiola A., Shao R., Kawaguchi Y., Ito A., Nixon A., Yoshida M., Wang X.F., Yao T.P. HDAC6 is a microtubule-associated deacetylase. Nature 2002, 417:455-458.
28. Janke C., Bulinski J.C. Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions. Nat. Rev. Mol. Cell Biol. 2011, 12:773-786.
29. Kalebic N., Sorrentino S., Perlas E., Bolasco G., Martinez C., Heppenstall P.A. alphaTAT1 is the major alpha-tubulin acetyltransferase in mice. Nat. Commun. 2013, 4:1962.
30. Kaverina I., Krylyshkina O., Small J.V. Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J. Cell Biol. 1999, 146:1033-1044.
31. Kaverina I., Rottner K., Small J.V. Targeting, capture, and stabilization of microtubules at early focal adhesions. J. Cell Biol. 1998, 142:181-190.
32. Kopp P., Lammers R., Aepfelbacher M., Woehlke G., Rudel T., Machuy N., Steffen W., Linder S. The kinesin KIF1C and microtubule plus ends regulate podosome dynamics in macrophages. Mol. Biol. Cell 2006, 17:2811-2823.
33. Krylyshkina O., Kaverina I., Kranewitter W., Steffen W., Alonso M.C., Cross R.A., Small J.V. Modulation of substrate adhesion dynamics via microtubule targeting requires kinesin-1. J. Cell Biol. 2002, 156:349-359.
34. Lansbergen G., Akhmanova A. Microtubule plus end: a hub of cellular activities. Traffic 2006, 7:499-507.
35. Linder S. The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol. 2007, 17:107-117.
36. Linder S., Higgs H., Hufner K., Schwarz K., Pannicke U., Aepfelbacher M. The polarization defect of Wiskott-Aldrich syndrome macrophages is linked to dislocalization of the Arp2/3 complex. J. Immunol. 2000, 165:221-225.
37. Linder S., Hüfner K., Wintergerst U., Aepfelbacher M. Microtubule-dependent formation of podosomal adhesion structures in primary human macrophages. J. Cell Sci. 2000, 113(Pt 23):4165-4176.
38. Linder S., Nelson D., Weiss M., Aepfelbacher M. Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:9648-9653.
39. Linder S., Wiesner C., Himmel M. Degrading devices: invadosomes in proteolytic cell invasion. Annu. Rev. Cell Dev. Biol. 2011, 27:185-211.
40. Luxenburg C., Winograd-Katz S., Addadi L., Geiger B. Involvement of actin polymerization in podosome dynamics. J. Cell Sci. 2012, 125:1666-1672.
41. Manneville J.B., Jehanno M., Etienne-Manneville S. Dlg1 binds GKAP to control dynein association with microtubules, centrosome positioning, and cell polarity. J. Cell Biol. 2010, 191:585-598.
42. North B.J., Marshall B.L., Borra M.T., Denu J.M., Verdin E. The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Mol. Cell 2003, 11:437-444.
43. Paturle-Lafanechère L., Eddé B., Denoulet P., Van Dorsselaer A., Mazarguil H., Le Caer J.P., Wehland J., Job D. Characterization of a major brain tubulin variant which cannot be tyrosinated. Biochemistry 1991, 30:10523-10528.
44. Purev E., Neff L., Horne W.C., Baron R. c-Cbl and Cbl-b act redundantly to protect osteoclasts from apoptosis and to displace HDAC6 from beta-tubulin, stabilizing microtubules and podosomes. Mol. Biol. Cell 2009, 20:4021-4030.
45. Reed N.A., Cai D., Blasius T.L., Jih G.T., Meyhofer E., Gaertig J., Verhey K.J. Microtubule acetylation promotes kinesin-1 binding and transport. Curr. Biol. 2006, 16:2166-2172.
46. Rey M., Irondelle M., Waharte F., Lizarraga F., Chavrier P. HDAC6 is required for invadopodia activity and invasion by breast tumor cells. Eur. J. Cell Biol. 2011, 90:128-135.
47. Rid R., Schiefermeier N., Grigoriev I., Small J.V., Kaverina I. The last but not the least: the origin and significance of trailing adhesions in fibroblastic cells. Cell Motil. Cytoskeleton 2005, 61:161-171.
48. Schliwa M., Woehlke G. Molecular motors. Nature 2003, 422:759-765.
49. Schoumacher M., Goldman R.D., Louvard D., Vignjevic D.M. Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia. J. Cell Biol. 2010, 189:541-556.
50. Seitz A., Kojima H., Oiwa K., Mandelkow E.M., Song Y.H., Mandelkow E. Single-molecule investigation of the interference between kinesin, tau and MAP2c. EMBO J. 2002, 21:4896-4905.
51. Shida T., Cueva J.G., Xu Z., Goodman M.B., Nachury M.V. The major alpha-tubulin K40 acetyltransferase alphaTAT1 promotes rapid ciliogenesis and efficient mechanosensation. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:21517-21522.
52. Siegrist S.E., Doe C.Q. Microtubule-induced cortical cell polarity. Genes Dev. 2007, 21:483-496.
53. Sirajuddin M., Rice L.M., Vale R.D. Regulation of microtubule motors by tubulin isotypes and post-translational modifications. Nat. Cell Biol. 2014, 16:335-344.
54. Steffen A., Le Dez G., Poincloux R., Recchi C., Nassoy P., Rottner K., Galli T., Chavrier P. MT1-MMP-dependent invasion is regulated by TI-VAMP/VAMP7. Curr. Biol. 2008, 18:926-931.
55. Stehbens S., Wittmann T. Targeting and transport: how microtubules control focal adhesion dynamics. J. Cell Biol. 2012, 198:481-489.
56. Stephenson F.A. Revisiting the TRAK family of proteins as mediators of GABAA receptor trafficking. Neurochem. Res. 2013, [Epub ahead of print].
57. Sung H.H., Telley I.A., Papadaki P., Ephrussi A., Surrey T., Rørth P. Drosophila ensconsin promotes productive recruitment of Kinesin-1 to microtubules. Dev. Cell 2008, 15:866-876.
58. Takeda S., Yamazaki H., Seog D.H., Kanai Y., Terada S., Hirokawa N. Kinesin superfamily protein 3 (KIF3) motor transports fodrin-associating vesicles important for neurite building. J. Cell Biol. 2000, 148:1255-1265.
59. Tran A.D., Marmo T.P., Salam A.A., Che S., Finkelstein E., Kabarriti R., Xenias H.S., Mazitschek R., Hubbert C., Kawaguchi Y., Sheetz M.P., Yao T.P., Bulinski J.C. HDAC6 deacetylation of tubulin modulates dynamics of cellular adhesions. J. Cell Sci. 2007, 120:1469-1479.
60. Verhey K.J., Hammond J.W. Traffic control: regulation of kinesin motors. Nat. Rev. Mol. Cell Biol. 2009, 10:765-777.
61. Walter W.J., Beranek V., Fischermeier E., Diez S. Tubulin acetylation alone does not affect kinesin-1 velocity and run length in vitro. PLoS ONE 2012, 7:e42218.
62. Wang Y., McNiven M.A. Invasive matrix degradation at focal adhesions occurs via protease recruitment by a FAK-p130Cas complex. J. Cell Biol. 2012, 196:375-385.
63. Wickström S.A., Fässler R. Regulation of membrane traffic by integrin signaling. Trends Cell Biol. 2011, 21:266-273.
64. Wiesner C., El Azzouzi K., Linder S. A specific subset of RabGTPases controls cell surface exposure of MT1-MMP, extracellular matrix degradation and three-dimensional invasion of macrophages. J. Cell Sci. 2013, 126:2820-2833.
65. Wiesner C., Faix J., Himmel M., Bentzien F., Linder S. KIF5B and KIF3A/KIF3B kinesins drive MT1-MMP surface exposure, CD44 shedding, and extracellular matrix degradation in primary macrophages. Blood 2010, 116:1559-1569.
66. Wloga D., Gaertig J. Post-translational modifications of microtubules. J. Cell Sci. 2010, 123:3447-3455.
67. Wu B., Decourt B., Zabidi M.A., Wuethrich L.T., Kim W.H., Zhou Z., MacIsaac K., Suter D.M. Microtubule-mediated Src tyrosine kinase trafficking in neuronal growth cones. Mol. Biol. Cell 2008, 19:4611-4627.
68. Zhang X., Yuan Z., Zhang Y., Yong S., Salas-Burgos A., Koomen J., Olashaw N., Parsons J.T., Yang X.J., Dent S.R., Yao T.P., Lane W.S., Seto E. HDAC6 modulates cell motility by altering the acetylation level of cortactin. Mol. Cell 2007, 27:197-213.