The spatial organization of centrosome-attached and free microtubules in 3T3 fibroblasts

Tsitologiya

Volumn 50, Issue 11, 2008, Pages 936-946

  Alieva, I B ^a   Borisy, G G ^b   Vorobjev, I A ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Centrosome; Centrosome attached microtubules; Free microtubules; The microtubule system organization; Videomicroscopy

Indexed keywords

EID: 59449106291     PISSN: 00413771     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (113)

1. Russian source
2. Russian source
3. Russian source
4. Russian source
5. Russian source
6. Russian source
7. Abercrombie M. 1978. Fibroblasts. J. Clin. Pathol. Suppl. 12 : 1-6.
8. Akhmanova A., Hoogenraad C. C, Drabek K., Stepanova T., Dortland B., Verkerk T., Vermeulen W., Burgering B. M., De Zee- uw C.I., 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.
9. Alberts B., Bray D., Lewis J., Raff M., Roberts K., Watson J. D. 2002. The cytoskeleton. In: Molecular biology of the cell. New York: Garland. 375-388.
10. Antin P.B., Forry-Schaudies S., Friedman T. M., Taps- cott S. J., Holtzer H. 1981. Taxol induces postmitotic myoblasts to assemble interdigitating microtubule-myosin arrays that exclude actin filaments. J. Cell Biol. 90 : 300-308.
11. Baas P. W., Black M. M., Banker G. A. 1989. Changes in microtubule polarity orientation during the development of hippocampal neurons in culture. J. Cell Biol. 109 : 3085-3094.
12. Baas P. W., Deitch J. S., Black M. M., Banker G. A. 1988. Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc. Nat. Acad. Sci. USA. 85 : 8335-8339.
13. Baas P. W., Slaughter T., Brown A., Black M. M. 1991. Microtubule dynamics in axons and dendrites. J. Neurosci. Res. 30 : 134-153.
14. Bacallao R., Antony C., Dotti C., Karsenti E., Stelzer E. H., Simons K. 1989. The subcellular organization of Madin-Darby canine kidney cells during the formation of a polarized epithelium. J. Cell Biol. 109 : 2817-2832.
15. Bartolini F., Gundersen G. G. 2006. Generation of noncentro- somal microtubule arrays. J. Cell Sci. 119 : 4155-4163.
16. Becker B. E., Cassimeris L. 2005. Cytoskeleton: microtubules born on the run. Curr. Biol. 15 : 551-554.
17. Bershadsky A. D., Ballestrem C., Carramusa L., Zilberman Y., Gilquin B., Khochbin S., Alexandrova A. Y., Verkhovsky A. B., Shemesh T., Kozlov M. M. 2006. Assembly and mechanosensory function of focal adhesions: experiments and models. Eur. J. Cell Biol. 85 : 165-173.
18. Bornens M. 2002. Centrosome composition and microtubule anchoring mechanisms. Curr. Opin. Cell Biol. 14 : 25-34.
19. Bre M. H, Kreis T. E., Karsenti E. 1987. Control of microtubule nucleation and stability in Madin-Darby canine kidney cells: the occurrence of noncentrosomal, stable detyrosinated microtubules. J. Cell Biol. 105 : 1283-1296.
20. Brodsky I. B., Burakov A. V., Nadezhdina E. S. 2007. Microtubules' interaction with cell cortex is required for their radial organization, but not for centrosome positioning. Cell Motil. Cytoskeleton. 50 : 1-11.
21. Buynard E., Zaal K.J., Ralston E. 2005. Reorganization of microtubule nucleation during muscle differentiation. Cell Motil. Cytoskeleton. 60 : 1-13.
22. Burton P. R., Paige J. L. 1981. Polarity of axoplasmic microtubules in the olfactory nerve of the frog. Proc. Nat. Acad. Sci. USA. 78 : 3269-3273.
23. Chabin-Brion K., Marceiller J., Perez F., Settegrana C., Drechou A., Durand G., Pouës C. 2001. The Golgi is a microtubule-or- ganizing organelle. Mol. Biol. Cell. 12 : 2047-2060.
24. Chan J., Calder G. M., Doonan J. H., Lloyd C. W. 2003. EB1 reveals mobile microtubule nucleation sites in Arabidopsis. Nat. Cell Biol. 5 : 967-971.
25. Chen J., Kanai Y., Cowan N. J., Hirokawa N. 1992. Projection domains of MAP2 and tau determine spacings between microtubules in dendrites and axons. Nature. 360 : 674-677.
26. Connolly J. A., Kiosses B. W., Kalnins V. I. 1986. Centrioles are lost as embryonic myoblasts fuse into myotubes in vitro. Eur. J. Cell Biol. 39 : 341-345.
27. Cramer E. M., Norol F., Guichard J., Breton-Gorius J., Vain- chenker W., Massé J.-M., Debili N. 1997. Ultrastructure of platelet formation by human megakaryocytes cultured with the Mp 1 ligand. Blood. 89 : 2336-2346.
28. Cytrynbaum E., Rodionov V., Mogilner A. 2004. Computational model of dynein-dependent self-organization of microtubule asters. J. Cell Sci. 117 : 1381-1397.
29. D'Addario M., Arora P. D., Ellen R. P., McCulloch C. A. G. 2003. Regulation of tension-induced mechanotranscriptional signals by the microtubule network in fibroblasts. J. Biol. Chem. 278 : 53 090-53 097.
30. Dammermann A., Merdes A. 2002. Assembly of centrosomal proteins and microtubule organization depends on PCM-1. J. Cell Biol. 159 : 255-266.
31. Daub H., Gevaert K., Vandekerckhove J., Sobel A., Hall A. 2001. Rac/Cdc42 and p65PAK regulate the microtubule-destabili- zing protein stathmin through phosphorylation at serine 16. J. Biol. Chem. 276 : 1677-1680.
32. De Brabander M., Geuens G., Nuydens R., Willebrords R., Aerts F., De Mey J. 1986. Microtubule dynamics during the cell cycle: the effects of taxol and nocodazole on the microtubule system of Pt K2 cells at different stages of the mitotic cycle. Int. Rev. Cytol. 101 : 215-274.
33. Delgehyr N., Sillibourne J., Bornens M. 2005. Microtubule nucleation and anchoring at the centrosome are independent processes linked by ninein function. J. Cell Sci. 118: 1565- 1575.
34. Desai A., Mitchison T. J. 1997. Microtubule polymerization dynamics. Annu. Rev. Cell. Develop. Biol. 13 : 83-117.
35. Doxsey S. 2001. Re-evaluating centrosome function. Nat. Rev. Mol. Cell Biol. 2 : 688-698.
36. Efimov A., Kharitonov A., Efimova N., Loncarek J., Miller P.M., AndreyevaN., Gleeson P., Galjart N., Maia A.R.R., McLeod 1. X., Yates J. R., Ill, Maiato H, Khodjakov A., Akhmano- va A., Kaverina I. 2007. Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network. Develop. Cell. 12 : 917-930.
37. Etienne-Manneville S., Hall A. 2001. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell. 106 : 489-498.
38. Fuchs E., Karakesisoglou I. 2001. Bridging cytoskeletal intersections. Genes Develop. 15 : 1-14.
39. Fukata M., Watanabe T., Noritake J., Nakagawa M., Yamaga M., Kuroda S., Matsuura Y., Iwamatsu A., Perez F., Kaibuchi K. 2002. Racl and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell. 109 : 873-885.
40. Gilbert T., Le Bivic A., Quaroni A., Rodriguez-Boulan E. 1991. Microtubular organization and its involvement in the biogenetic pathways of plasma membrane proteins in Caco-2 intestinal epithelial cells. J. Cell Biol. 113 : 275-288.
41. Hagan I. M. 1998. The fission yeast microtubule cytoskeleton. Review. J. Cell Sci. 1ll : 1603-1612.
42. Heald R., Tournebize R., Habermann A., Karsenti E., Hyman A. A. 1997. Spindle assembly in Xenopus egg extracts: respective roles of centrosomes and microtubule self-organization. J. Cell Biol. 138 : 615-628.
43. Heidemann S. R., Landers J. M., Hamborg M. A. 1981. Polarity orientation of axonal microtubules. J. Cell Biol. 91 : 661-665.
44. Hill C. S., Duran S., Lin Z. X, Weber K., Holtzer H. 1986. Titin and myosin, but not desmin, are linked during myofibrillogenesis in postmitotic mononucleated myoblasts. J. Cell Biol. 103 : 2185-2196.
45. Hoogenraad C. C., Akhmanova A., Howell S. A., Dortland B., De Zeeuw C.L, Willemsen R., Visser P., Grosveld F., Galjart N. 2001. Mammalian Golgi-associated Bicaudal-D2 functions in the dynein-dynactin pathway by interacting with these complexes. EMBO J. 20 : 4041-4054.
46. Horton A. C, Ehlers M. D. 2003. Dual modes of endoplasmic reticulum-to-Golgi transport in dendrites revealed by live-cell imaging. J. Neurosci. 23 : 6188-6199.
47. Howard J., Hyman A. A. 2003. Dynamics and mechanics of the microtubule plus end. Nature. 422 : 753-758.
48. Ishizaki T., Morishima Y., Okamoto M., Furuyashiki T., Ka- to T., Narumiya S. 2001. Coordination of microtubules and the ac- tin cytoskeleton by the Rho effector mDial. Nat. Cell Biol. 3 : 8-14.
49. Jaffe A. B., Hall A. 2005. Rho GTRases: biochemistry and biology. Annu. Rev. Cell Develop. Biol. 21 : 247-269.
50. Janson M. E., Setty T. G., Paoletti A., Tran P. T. 2005. Efficient formation of bipolar microtubule bundles requires microtubu- le-bound gamma-tubulin complexes. J. Cell Biol. 169 : 297-308.
51. Karsenti E., KobayashiS., Mitchison T., Kirschner M. 1984. Role of the centrosome in organizing the interphase microtubule array: properties of cytoplasts containing or lacking centrosomes. J. Cell Biol. 98 : 1763-1776.
52. Kaverina I., Krylyshkina O., Small J. V. 1999. Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J. Cell Biol. 146 : 1033-1044.
53. Kaverina 1., Rottner K., Small J. V. 1998. Targeting, capture, and stabilization of microtubules at early focal adhesions. J. Cell Biol. 142 : 181-190.
54. Keating T. J., Borisy G. G. 1999. Centrosomal and non-centro- somal microtubules. Biol. Cell. 91 : 321-329.
55. Keating T. J., Peloquin J. G., Rodionov V. I., Momcilovic D., Borisy G. G. 1997. Microtubule release from the centrosome. Proc. Nat. Acad. Sci. USA. 94 : 5078-5083.
56. KitaK., Wittmann T., Nathkel.S., Waterman-Storer C. M. 2006. Adenomatous polyposis coli on microtubule plus ends in cell extensions can promote microtubule net growth with or without EB1. Mol. Biol. Cell. 17 : 2331-2345.
57. Knop M., Pereira G., Schiebel E. 1999. Microtubule organization by the budding yeast spindle pole body. Review. Biol. Cell. 91 : 291-304.
58. Komarova Y. A., Vorobjev I. A., Borisy G. G. 2002. Life cycle of MTs: persistent growth in the cell interior; asymmetric transition fraquencies and effects of cell boundary. J. Cell Sci. 115 : 3517- 3539.
59. Krendel M., Osterweil E. K., Mooseker M. S. 2007. Myosin IE interacts with synaptojanin-1 and dynamin and is involved in endocytosis. FEBS Lett. 581 : 644-650.
60. Krendel M., Zenke F. T., Bokoch G. M. 2002. Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat. Cell Biol. 4 : 294-301.
61. Kroboth K, Newton I. P., Kita K, Dikovskaya D., Zumbrunn J., Waterman-Storer C. M., Nathke I. S. 2007. Lack of adenomatous polyposis coli protein correlates with a decrease in cell migration and overall changes in microtubule stability. Mol. Biol. Cell. 18 : 910-918.
62. Luders J., Stearns T. 2007. Microtubule- organizing centres: a re-evaluation. Nat. Rev. Mol. Cell Biol. 8 : 161-167.
63. Malikov V., Cytrynbaum E. N., Kashina A., Mogilner A., Rodionov V. 2005. Centering of a radial microtubule array by translocation along microtubules spontaneously nucleated in the cytoplasm. Nat. Cell Biol. 7 : 1213-1218.
64. Malikov V., Kashina A., Rodionov V. 2004. Cytoplasmic dynein nucleates microtubules to organize them into radial arrays in vivo. Mol. Biol. Cell. 15 : 2742-2749.
65. Maly I. V., Borisy G. G. 2002. Self-organization of treadmilling microtubules into a polar array. Trends Cell Biol. 12 : 462- 465.
66. Maniotis A., Schliwa M., 1991. Microsurgical removal of centrosomes blocks cell reproduction and centriole generation in BSC-1 cells. Cell. 67 : 495-504.
67. Mcintosh J. R., Euteneuer U. 1984. Tubulin hooks as probes for microtubule polarity: an analysis of the method and an evaluation of data on microtubule polarity in the mitotic spindle. J. Cell Biol. 98 : 525-533.
68. McNiven M. A., Porter K. R. 1988. Organization of microtubules in centrosome-free cytoplasm. J. Cell Biol. 106 : 1593-1605.
69. Mikhailov A. V., Gundersen G. G. 1995. Centripetal transport of microtubules in motile cells. Cell Motil. Cytoskeleton. 32 : 173-186.
70. Mimori-Kiyosue Y., Grigoriev I., Lansbergen G., Sasaki H., Matsui C., Severin F., Galjart N., Grosveld F., Vorobiev I., Tsukita S., Akhmanova A. 2005. CLASP 1 and CLASP2 bind to EB1 and regulate microtubule plus end dynamics at the cell cortex. J. Cell Biol. 68 : 141-153.
71. Mogensen M. M. 2004. Microtubule organizing centers in polarized epithelial cells. In: Centrosomes in development and disease. Weinheim: Wiley-VCH Verlag GmbH & Co., KGaA. 299- 319.
72. Mogensen M. M., Mackie J.B., Doxsey S.J., Stearns T., Tucker J. B. 1997. Centrosomal deployment of gamma-tubulin and pericentrin: evidence for a microtubule-nucleating domain and a minus-end docking domain in certain mouse epithelial cells. Cell Motil. Cytoskeleton. 36 : 276-290.
73. Mogensen M. M., Malik A., Piel M., Bouckson-Castaing V., Bornens M. 2000. Microtubule minus-end anchorage at centrosomal and non-centrosomal sites: the role of ninein. J. Cell Sci. 113 : 3013-3023.
74. Mogensen M. M., Tucker J. B., MackieJ.B., Prescott A. R., Nathke I. S. 2002. The adenomatous polyposis coli protein unambiguously localizes to microtubule plus ends and is involved in establishing parallel arrays of microtubule bundles in highly polarized epithelial cells. J. Cell Biol. 157 : 1041 - 1048.
75. Moritz M., Agard D. 2001. G-tubulin complexes and microtubule nucleation. Curr. Opin. Struct. Biol. 11 : 174-181.
76. Moritz M., Braunfeld M. B., Guenebaut V., Heuser J., Agard D. A. 2000. Structure of the gamma-tubulin ring complex: a template for microtubule nucleation. Nat. Cell Biol. 2 : 365-370.
77. Moritz M., Zheng Y, Alberts B. M., Oegema K. 1998. Recruitment of the gamma-tubulin ring complex to Drosophila salt-stripped centrosome scaffolds. J. Cell Biol. 142 : 775-786.
78. Moss D.K., Bellett G., Carter J. M., Liovic M., Keynton J., Prescott A. R., Lane E. B., Mogensen M. M. 2007. Ninein is released from the centrosome and moves bi-directionally along microtubules. J. Cell Sci. 120 : 3064-3074.
79. Musch A. 2004. Microtubule organization and function in epithelial cells. Traffic. 5 : 1-9.
80. Nedelec F.J., Surrey T., Maggs A. C, Leibler S. 1997. Self- organization of microtubules and motors. Nature. 389 : 305-308.
81. Oegema K., Wiese C, Martin O. C, Milligan R. A., Iwamatsu A., Mitchison T. J., Zheng Y. 1999. Characterization of two related Drosophila gamma-tubulin complexes that differ in their ability to nucleate microtubules. J. Cell Biol. 144 : 721-733.
82. Overly C. C, Rieff H. I., Hollenbeck P. J. 1996. Organelle motility and metabolism in axons vs dendrites of cultured hippocampal neurons. J. Cell Sci. 109 : 971-980.
83. Palazzo A. F., Joseph H.L., Chen Y. J., Dujardin D. L., Alberts A. S, Pfister K.K, Vallee R. B., Gundersen G. G. 2001. Cdc42, dynein, and dynactin regulate MTOC reorientation independent of Rho-regulated microtubule stabilization. Curr. Biol. 11 : 1536-1541.
84. Patuzzi R. 1998. Exponential onset and recovery of temporary threshold shift after loud sound: evidence for long-term inactivation of mechano-electrical transduction channels. Hear Res. 125 : 17-38.
85. Penman G. A., Leung L., Nathke 1. S. 2005. The adenomatous polyposis coli protein (APC) exists in two distinct soluble complexes with different functions. J. Cell Sci. 118 : 4741-4750.
86. Pizon V., Gerbal F., Diaz C. C, Karsenti E. 2005. Microtubu- le-dependent transport and organization of sarcomeric myosin during skeletal muscle differentiation. EMBO J. 24 : 3781-3792.
87. Quintyne N. J., Gill S. R., Eckley D. M., CregoC.L., Comp- ton D. A., Schroer T. A. 1999. Dynactin is required for microtubule anchoring at centrosomes. J. Cell Biol. 147 : 321-334.
88. Quintyne N. J., Schroer T. A. 2002. Distinct cell cycle-dependent roles for dynactin and dynein at centrosomes. J. Cell Biol. 159 : 245-254.
89. Reilein A., Nelson W. J. 2005. APC is a component of an organizing template for cortical microtubule networks. Nat. Cell Biol. 7 : 463-473.
90. Reilein A., Yamada S., Nelson W. J. 2005. Self-organization of an acentrosomal microtubule network at the basal cortex of polarized epithelial cells. J. Cell Biol. 171 : 845-855.
91. Rodionov V. I., Borisy G. G. 1997. Self-centring activity of cytoplasm. Nature. 386 : 170-173.
92. Rodionov V. I., Hope A. J., Svitkina T. M., Borisy G. G. 1998. Functional coordination of microtubule-based and actin-based motility in melanophores. Curr. Biol. 8 : 165-168.
93. Rodionov V. I., Lim S, Gelfand V. I., Borisy G. G. 1994. Microtubule dynamic in fish melanofores. J. Cell Biol. 126 : 1455-1464.
94. Rodionov V., Nadezhdina E., Borisy G. 1999. Centrosomal control of microtubule dynamics. Proc. Nat. Acad. Sci. USA. 96 : 115-120.
95. Rodriguez O. C, Schaefer A. W., Mandato C. A., Forscher P., Bement W. M., Waterman-Storer C. M. 2003. Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat. Cell Biol. 5 : 599-609.
96. Rodriguez-Boulan E., Kreitzer G., Musch A. 2005. Organization of vesicular trafficking in epithelia. Nat. Rev. Mol. Cell Biol. 6 : 233-247.
97. Samejima I., Lourenco P. C, Snaith H. A., Sawin K. E. 2005. Fission yeast mto2p regulates microtubule nucleation by the centro- somin-related protein mtolp. Mol. Biol. Cell. 16 : 3040-3051.
98. Signor D., Scholey J.M. 2000. Microtubule-based transport along axons, dendrites and axonemes. Essays Biochem. 35 : 89-102.
99. SmallJ. V., Geiger B., Kaverina I., Bershadsky A. D. 2002. How do microtubules guide migrating cells? Nat. Rev. Mol. Cell Biol. 3 : 957-964.
100. Surrey T, Nedelec F., Leibler S., Karsenti E. 2001. Physical properties determining self-organization of motors and microtubules. Science. 292 : 1167-1171.
101. Tassin A. M., Maro B., Bornens M. 1985. Fate of microtubule- organizing centers during myogenesis in vitro. J. Cell Biol. 100 : 35-46.
102. Tsvetkov A. S., Samsonov A., Akhmanova A., Galjart N., Popov S. V. 2007. Microtubule-binding proteins CLASP1 and CLASP2 interact with actin filaments. Cell Motil. Cytoskeleton. 64 : 519-530.
103. Uetake Y, Terada Y., Matuliene J., Kuriyama R. 2004. Interaction of Cep l35 with a p50 dynactin subunit in mammalian centrosomes. Cell Motil. Cytoskeleton. 58 : 53-66.
104. Venkatram S., Jennings J. L., Link A., Gould K. L. 2005. Mto2p, a novel fission yeast protein required for cytoplasmic microtubule organization and anchoring of the cytokinetic actin ring. Mol. Biol. Cell. 16 : 3052-3063.
105. Vorobjev I. A., Alieva I. B., Grigoriev I. S., Borisy G. G. 2003. Microtubule dynamics in living cells: direct analysis in the internal cytoplasm. Cell Biol. Int. 27 : 9-29.
106. Vorobjev I. A., Chentsov Yu. S. 1982. Centrioles in the cell cycle. I. Epithelial cells. J. Cell Biol. 93 : 938-949.
107. Vorobjev I., Malikov V., Rodionov V. 2001. Self-organization of a radial microtubule array by dynein-dependent nucleation of microtubules. Proc. Nat. Acad. Sci. USA. 98 : 10 160-10 165.
108. Vorobjev I. A., Svitkina T. M, Borisy G. G. 1997. Cytoplasmic assembly of microtubules in cultured cells. J. Cell Sci. 110: 2635- 2645.
109. Wadsworth P. 1999. Regional regulation of microtubule dynamics in polarized, motile cells. Cell Motil. Cytoskeleton. 42 : 48-59.
110. Wallar B. J., Alberts A. S. 2003. The formins: active scaffolds that remodel the cytoskeleton. Review. Trends Cell Biol. 13:435-446.
111. Waterman-Storer C. M., Worthylake R. A., Liu B. P., Burridge K., Salmon E. D. 1999. Microtubule growth activates Racl to promote lamellipodial protrusion in fibroblasts. Nat. Cell Biol. 1 : 45-50.
112. Yan L. Y., Huang J. C, Zhu Z. Y., Lei Z. L., Shi L. H., Nan C L., Zhao Z. J., OuyangY.C, Song X. F., Sun Q. Y., Chen D. Y. 2006. NuMA distribution and microtubule configuration in rabbit oocytes and cloned embryos. Reproduction. 132 : 869-876.
113. Yu W., Ahmad F. J., Baas P. W. 1994. Microtubule fragmentatir and partitioning in the axon during collateral branch formation. J. Neurosci. 14 : 5872-5884.