Directly probing the mechanical properties of the spindle and its matrix

Journal of Cell Biology

Volumn 188, Issue 4, 2010, Pages 481-489

  Gatlin, Jesse C ^a,d   Matov, Alexandre ^a   Danuser, Gaudenz ^b,c   Mitchison, Timothy J ^c,d   Salmon, Edward D ^a,d  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d MARINE BIOLOGICAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; EMBRYO; METAPHASE; MICROTUBULE; MITOSIS SPINDLE; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; XENOPUS LAEVIS;

ANIMALS; BIOMECHANICS; CROSS-LINKING REAGENTS; MICROTUBULES; MITOTIC SPINDLE APPARATUS; NEEDLES; XENOPUS;

XENOPUS LAEVIS;

EID: 77149156379     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200907110     Document Type: Article

References (45)

1. Begg, D.A., and G.W. Ellis. 1979. Micromanipulation studies of chromosome movement. I. Chromosome-spindle attachment and the mechanical properties of chromosomal spindle fibers. J. Cell Biol. 82:528-541. doi:10.1083/jcb.82.2.528
2. Berg, H.C. 1983. Random Walks in Biology. Princeton University Press, Princeton, NJ. 142 pp.
3. Burbank, K.S., A.C. Groen, Z.E. Perlman, D.S. Fisher, and T.J. Mitchison. 2006. A new method reveals microtubule minus ends throughout the meiotic spindle. J. Cell Biol. 175:369-375. doi:10.1083/jcb.200511112
4. Burbank, K.S., T.J. Mitchison, and D.S. Fisher. 2007. Slide-and-cluster models for spindle assembly. Curr. Biol. 17:1373-1383. doi:10.1016/j.cub.2007.07.058
5. Chang, P., M.K. Jacobson, and T.J. Mitchison. 2004. Poly(ADP-ribose) is required for spindle assembly and structure. Nature. 432:645-649. doi:10.1038/nature03061
6. Desai, A., P.S. Maddox, T.J. Mitchison, and E.D. Salmon. 1998. Anaphase A chromosome movement and poleward spindle microtubule flux occur at similar rates in Xenopus extract spindles. J. Cell Biol. 141:703-713. doi:10.1083/jcb.141.3.703
7. Desai, A., A. Murray, T.J. Mitchison, and C.E. Walczak. 1999. The use of Xenopus egg extracts to study mitotic spindle assembly and function in vitro. In Mitosis and meiosis. Methods in Cell Biology, vol. 61. C.L. Rieder, L. Wilson, and P.T. Matsudaira, editors. Academic Press Inc., San Diego, CA. 385-412.
8. Dionne, M.A., L. Howard, and D.A. Compton. 1999. NuMA is a component of an insoluble matrix at mitotic spindle poles. Cell Motil. Cytoskeleton. 42:189-203. doi:10.1002/(SICI)1097-0169(1999)42:3〈189::AID-CM3〉3.0. CO;2-X
9. Dumont, S., and T.J. Mitchison. 2009. Compression regulates mitotic spindle length by a mechanochemical switch at the poles. Curr. Biol. 19:1086-1095. doi:10.1016/j.cub.2009.05.056
10. Fabian, L., X. Xia, D.V. Venkitaramani, K.M. Johansen, J. Johansen, D.J. Andrew, and A. Forer. 2007. Titin in insect spermatocyte spindle fibers associates with microtubules, actin, myosin and the matrix proteins skeletor, megator and chromator. J. Cell Sci. 120:2190-2204. doi:10.1242/jcs.03465
11. Ferenz, N.P., R. Paul, C. Fagerstrom, A. Mogilner, and P. Wadsworth. 2009. Dynein antagonizes eg5 by crosslinking and sliding antiparallel microtubules. Curr. Biol. 19:1833-1838. doi:10.1016/j.cub.2009.09.025
12. Gaetz, J., and T.M. Kapoor. 2004. Dynein/dynactin regulate metaphase spindle length by targeting depolymerizing activities to spindle poles. J. Cell Biol. 166:465-471. doi:10.1083/jcb.200404015
13. Gatlin, J.C., A. Matov, A.C. Groen, D.J. Needleman, T.J. Maresca, G. Danuser, T.J. Mitchison, and E.D. Salmon. 2009. Spindle fusion requires dyneinmediated sliding of oppositely oriented microtubules. Curr. Biol. 19:287-296. doi:10.1016/j.cub.2009.01.055
14. Goshima, G., R. Wollman, N. Stuurman, J.M. Scholey, and R.D. Vale. 2005. Length control of the metaphase spindle. Curr. Biol. 15:1979-1988. doi:10.1016/j.cub.2005.09.054
15. Heald, R., R. Tournebize, T. Blank, R. Sandaltzopoulos, P. Becker, A. Hyman, and E. Karsenti. 1996. Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature. 382:420-425. doi:10.1038/382420a0
16. Itabashi, T., J. Takagi, Y. Shimamoto, H. Onoe, K. Kuwana, I. Shimoyama, J. Gaetz, T.M. Kapoor, and S. Ishiwata. 2009. Probing the mechanical architecture of the vertebrate meiotic spindle. Nat. Methods. 6:167-172. doi:10.1038/nmeth.1297
17. Kapoor, T.M., and T.J. Mitchison. 2001. Eg5 is static in bipolar spindles relative to tubulin: evidence for a static spindle matrix. J. Cell Biol. 154:1125-1133. doi:10.1083/jcb.200106011
18. Lince-Faria, M., S. Maffini, B. Orr, Y. Ding, C.E. Cláudia Florindo, C.E. Sunkel, A. Tavares, J. Johansen, K.M. Johansen, and H. Maiato. 2009. Spatiotemporal control of mitosis by the conserved spindle matrix protein Megator. J. Cell Biol. 184:647-657. doi:10.1083/jcb.200811012
19. Maddox, P.S., B. Moree, J.C. Canman, and E.D. Salmon. 2003a. Spinning disk confocal microscope system for rapid high-resolution, multi-mode, fluorescence speckle microscopy and green fluorescent protein imaging in living cells. Methods Enzymol. 360:597-617. doi:10.1016/S0076-6879(03)60130-8
20. Maddox, P., A. Straight, P. Coughlin, T.J. Mitchison, and E.D. Salmon. 2003b. Direct observation of microtubule dynamics at kinetochores in Xenopus extract spindles: implications for spindle mechanics. J. Cell Biol. 162: 377-382. doi:10.1083/jcb.200301088
21. Matos, I., A.J. Pereira, M. Lince-Faria, L.A. Cameron, E.D. Salmon, and H. Maiato. 2009. Synchronizing chromosome segregation by flux-dependent force equalization at kinetochores. J. Cell Biol. 186:11-26. doi:10.1083/jcb.200904153
22. Merdes, A., R. Heald, K. Samejima, W.C. Earnshaw, and D.W. Cleveland. 2000. Formation of spindle poles by dynein/dynactin-dependent transport of NuMA. J. Cell Biol. 149:851-862. doi:10.1083/jcb.149.4.851
23. Mitchison, T.J., P. Maddox, J. Gaetz, A. Groen, M. Shirasu, A. Desai, E.D. Salmon, and T.M. Kapoor. 2005. Roles of polymerization dynamics, opposed motors, and a tensile element in governing the length of Xenopus extract meiotic spindles. Mol. Biol. Cell. 16:3064-3076. doi:10.1091/mbc.E05-02- 0174
24. Miyamoto, D.T., Z.E. Perlman, K.S. Burbank, A.C. Groen, and T.J. Mitchison. 2004. The kinesin Eg5 drives poleward microtubule flux in Xenopus laevis egg extract spindles. J. Cell Biol. 167:813-818. doi:10.1083/jcb.200407126
25. Mogilner, A., R. Wollman, G. Civelekoglu-Scholey, and J. Scholey. 2006. Modeling mitosis. Trends Cell Biol. 16:88-96. doi:10.1016/j.tcb.2005.12. 007
26. Murray, A.W. 1991. Cell cycle extracts. Methods Cell Biol. 36:581-605. doi:10.1016/S0091-679X(08)60298-8
27. Nicklas, R.B., and C.A. Staehly. 1967. Chromosome micromanipulation. I. The mechanics of chromosome attachment to the spindle. Chromosoma. 21:1-16. doi:10.1007/BF00330544
28. Nicklas, R.B., D.F. Kubai, and T.S. Hays. 1982. Spindle microtubules and their mechanical associations after micromanipulation in anaphase. J. Cell Biol. 95:91-104. doi:10.1083/jcb.95.1.91
29. Perrin, F. 1934. Mouvement brownien d'un ellipsoide - I. Dispersion diélectrique pour des molécules ellipsoidales. J. Phys. Radium. 5:497-511. doi:10.1051/jphysrad:01934005010049700
30. Pickett-Heaps, J., and A. Forer. 2009. Mitosis: spindle evolution and the matrix model. Protoplasma. 235:91-99. doi:10.1007/s00709-009-0030-2
31. Qi, H., U. Rath, D. Wang, Y.Z. Xu, Y. Ding, W. Zhang, M.J. Blacketer, M.R. Paddy, J. Girton, J. Johansen, and K.M. Johansen. 2004. Megator, an essential coiled-coil protein that localizes to the putative spindle matrix during mitosis in Drosophila. Mol. Biol. Cell. 15:4854-4865. doi:10.1091/mbc.E04-07-0579
32. Sawin, K.E., and T.J. Mitchison. 1991. Poleward microtubule flux mitotic spindles assembled in vitro. J. Cell Biol. 112:941-954. doi:10.1083/jcb.112.5.941
33. Scholey, J.M., G.C. Rogers, and D.J. Sharp. 2001. Mitosis, microtubules, and the matrix. J. Cell Biol. 154:261-266. doi:10.1083/jcb.200101097
34. Sharp, D.J., K.R. Yu, J.C. Sisson, W. Sullivan, and J.M. Scholey. 1999. Antagonistic microtubule-sliding motors position mitotic centrosomes in Drosophila early embryos. Nat. Cell Biol. 1:51-54. doi:10.1038/9025
35. Tanenbaum, M.E., L. Macůrek, N. Galjart, and R.H. Medema. 2008. Dynein, Lis1 and CLIP-170 counteract Eg5-dependent centrosome separation during bipolar spindle assembly. EMBO J. 27:3235-3245. doi:10.1038/emboj.2008. 242
36. Tsai, M.Y., S. Wang, J.M. Heidinger, D.K. Shumaker, S.A. Adam, R.D. Goldman, and Y. Zheng. 2006. A mitotic lamin B matrix induced by RanGTP required for spindle assembly. Science. 311:1887-1893. doi:10.1126/science. 1122771
37. Uteng, M., C. Hentrich, K. Miura, P. Bieling, and T. Surrey. 2008. Poleward transport of Eg5 by dynein-dynactin in Xenopus laevis egg extract spindles. J. Cell Biol. 182:715-726. doi:10.1083/jcb.200801125
38. Valentine, M.T., Z.E. Perlman, T.J. Mitchison, and D.A. Weitz. 2005. Mechanical properties of Xenopus egg cytoplasmic extracts. Biophys. J. 88:680-689. doi:10.1529/biophysj.104.048025
39. Varga, V., J. Helenius, K. Tanaka, A.A. Hyman, T.U. Tanaka, and J. Howard. 2006. Yeast kinesin-8 depolymerizes microtubules in a length-dependent manner. Nat. Cell Biol. 8:957-962. doi:10.1038/ncb1462
40. Walczak, C.E., and R. Heald. 2008. Mechanisms of mitotic spindle assembly and function. Int. Rev. Cytol. 265:111-158. doi:10.1016/S0074-7696(07) 65003-7
41. Walker, D.L., D. Wang, Y. Jin, U. Rath, Y. Wang, J. Johansen, and K.M. Johansen. 2000. Skeletor, a novel chromosomal protein that redistributes during mitosis provides evidence for the formation of a spindle matrix. J. Cell Biol. 151:1401-1412. doi:10.1083/jcb.151.7.1401
42. Waterman-Storer, C., A. Desai, and E.D. Salmon. 1999. Fluorescent speckle microscopy of spindle microtubule assembly and motility in living cells. Methods Cell Biol. 61:155-173. doi:10.1016/S0091-679X(08)61980-9
43. Yang, G., A. Matov, and G. Danuser. 2005. Reliable tracking of large scale dense antiparallel particle motion for fluorescence live cell imaging. Proc. IEEE Comput. Soc. Conf. Comput. Vis. Pattern Recognit. 2005:138-146. doi:10.1109/CVPR.2005.519
44. Yang, G., B.R. Houghtaling, J. Gaetz, J.Z. Liu, G. Danuser, and T.M. Kapoor. 2007. Architectural dynamics of the meiotic spindle revealed by single-fluorophore imaging. Nat. Cell Biol. 9:1233-1242. doi:10.1038/ncb1643
45. Yang, G., L.A. Cameron, P.S. Maddox, E.D. Salmon, and G. Danuser. 2008. Regional variation of microtubule flux reveals microtubule organization in the metaphase meiotic spindle. J. Cell Biol. 182:631-639. doi:10.1083/jcb.200801105