© The Rockefeller University Press,
0021-9525/1997//1 $5.00
The Journal of Cell Biology, Volume 139, Number 1,
, 1997 1-12
Elasticity and Structure of Eukaryote Chromosomes Studied by Micromanipulation and Micropipette Aspiration
Bahram Houchmandzadeh*,
,
John F. Marko
,
,
Didier Chatenay
,||, and
Albert Libchaber
,¶
* Centre National de la Recherche Scientifique (CNRS), Laboratoire de Spectrométrie Physique, 38402 Saint-Martin-d'Hères Cedex, France;
Center for Studies in Physics and Biology, The Rockefeller University, New York 10021-6399;
Department of Physics, The University of Illinois at Chicago, Chicago, Illinois 60607-7059; || Université Louis Pasteur, CNRS, Institut de Physique, 67000 Strasbourg, France; and ¶ NEC Research Institute, Princeton, New Jersey 08540
The structure of mitotic chromosomes in cultured newt lung cells was investigated by a quantitative study of their deformability, using micropipettes. Metaphase chromosomes are highly extensible objects that return to their native shape after being stretched up to 10 times their normal length. Larger deformations of 10 to 100 times irreversibly and progressively transform the chromosomes into a "thin filament," parts of which display a helical organization. Chromosomes break for elongations of the order of 100 times, at which time the applied force is around 100 nanonewtons. We have also observed that as mitosis proceeds from nuclear envelope breakdown to metaphase, the native chromosomes progressively become more flexible. (The elastic Young modulus drops from 5,000 ± 1,000 to 1,000 ± 200 Pa.) These observations and measurements are in agreement with a helix-hierarchy model of chromosome structure. Knowing the Young modulus allows us to estimate that the force exerted by the spindle on a newt chromosome at anaphase is roughly one nanonewton.
1. Abbreviation used in this paper: NEB, nuclear envelope breakdown.
Address all correspondence to Bahram Houchmandzadeh, CNRS, Laboratorie de Spectrométrie Physique, BP 57, 38402 Saint-Martin-d'Hères Cedex, France. Tel.: (33) 476 51 44 27. Fax: (33) 476 51 45 44. E-mail: bahram{at}coucou.ujf-grenoble.fr
We warmly thank M. Elbaum who developed the micromanipulation set-up, and S. Childress, M. Goulian, T. Hirano, H. Macgregor, W. Marshall, P. Moens, Y. Rabin, E. Siggia, and J. Swedlow for many helpful discussions.

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
This article has been cited by other articles:
-
Ribeiro, S. A., Gatlin, J. C., Dong, Y., Joglekar, A., Cameron, L., Hudson, D. F., Farr, C. J., McEwen, B. F., Salmon, E. D., Earnshaw, W. C., Vagnarelli, P.
(2009). Condensin Regulates the Stiffness of Vertebrate Centromeres. Mol. Biol. Cell
20: 2371-2380
[Abstract]
[Full Text]
-
Liu, J., Desai, A., Onuchic, J. N., Hwa, T.
(2008). An integrated mechanobiochemical feedback mechanism describes chromosome motility from prometaphase to anaphase in mitosis. Proc. Natl. Acad. Sci. USA
105: 13752-13757
[Abstract]
[Full Text]
-
Raj, A., Peskin, C. S.
(2006). The influence of chromosome flexibility on chromosome transport during anaphase A. Proc. Natl. Acad. Sci. USA
103: 5349-5354
[Abstract]
[Full Text]
-
Pope, L. H., Xiong, C., Marko, J. F.
(2006). Proteolysis of Mitotic Chromosomes Induces Gradual and Anisotropic Decondensation Correlated with a Reduction of Elastic Modulus and Structural Sensitivity to Rarely Cutting Restriction Enzymes. Mol. Biol. Cell
17: 104-113
[Abstract]
[Full Text]
-
Cytrynbaum, E. N., Sommi, P., Brust-Mascher, I., Scholey, J. M., Mogilner, A.
(2005). Early Spindle Assembly in Drosophila Embryos: Role of a Force Balance Involving Cytoskeletal Dynamics and Nuclear Mechanics. Mol. Biol. Cell
16: 4967-4981
[Abstract]
[Full Text]
-
Maniotis, A. J., Valyi-Nagy, K., Karavitis, J., Moses, J., Boddipali, V., Wang, Y., Nunez, R., Setty, S., Arbieva, Z., Bissell, M. J., Folberg, R.
(2005). Chromatin Organization Measured by AluI Restriction Enzyme Changes with Malignancy and Is Regulated by the Extracellular Matrix and the Cytoskeleton. Am. J. Pathol.
166: 1187-1203
[Abstract]
[Full Text]
-
Dahl, K. N., Kahn, S. M., Wilson, K. L., Discher, D. E.
(2004). The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of a molecular shock absorber. J. Cell Sci.
117: 4779-4786
[Abstract]
[Full Text]
-
Marcy, Y., Prost, J., Carlier, M.-F., Sykes, C.
(2004). Forces generated during actin-based propulsion: A direct measurement by micromanipulation. Proc. Natl. Acad. Sci. USA
101: 5992-5997
[Abstract]
[Full Text]
-
Belmont, A. S.
(2002). Mitotic chromosome scaffold structure: New approaches to an old controversy. Proc. Natl. Acad. Sci. USA
99: 15855-15857
[Full Text]
-
Poirier, M. G., Marko, J. F.
(2002). From the Cover: Mitotic chromosomes are chromatin networks without a mechanically contiguous protein scaffold. Proc. Natl. Acad. Sci. USA
99: 15393-15397
[Abstract]
[Full Text]
-
Machado, C., Andrew, D. J.
(2000). D-Titin: A Giant Protein with Dual Roles in Chromosomes and Muscles. JCB
151: 639-652
[Abstract]
[Full Text]
-
Balliet, J. W., Gendron, K., Bates, P.
(2000). Mutational Analysis of the Subgroup A Avian Sarcoma and Leukosis Virus Putative Fusion Peptide Domain. J. Virol.
74: 3731-3739
[Abstract]
[Full Text]
-
Lupi, R., Corda, D., Di Girolamo, M.
(2000). Endogenous ADP-ribosylation of the G Protein beta Subunit Prevents the Inhibition of Type 1 Adenylyl Cyclase. J. Biol. Chem.
275: 9418-9424
[Abstract]
[Full Text]
-
Poirier, M., Eroglu, S., Chatenay, D., Marko, J. F.
(2000). Reversible and Irreversible Unfolding of Mitotic Newt Chromosomes by Applied Force. Mol. Biol. Cell
11: 269-276
[Abstract]
[Full Text]
-
Vorobjev, I., Rodionov, V., Maly, I., Borisy, G.
(1999). Contribution of plus and minus end pathways to microtubule turnover. J. Cell Sci.
112: 2277-2289
[Abstract]
-
Nguyen, H., Gruber, D, Bulinski, J.
(1999). Microtubule-associated protein 4 (MAP4) regulates assembly, protomer-polymer partitioning and synthesis of tubulin in cultured cells. J. Cell Sci.
112: 1813-1824
[Abstract]
-
Storrie, B., White, J., Rottger, S., Stelzer, E. H.K., Suganuma, T., Nilsson, T.
(1998). Recycling of Golgi-resident Glycosyltransferases through the ER Reveals a Novel Pathway and Provides an Explanation for Nocodazole-induced Golgi Scattering. JCB
143: 1505-1521
[Abstract]
[Full Text]
-
Ostashevsky, J.
(1998). A Polymer Model for the Structural Organization of Chromatin Loops and Minibands in Interphase Chromosomes. Mol. Biol. Cell
9: 3031-3040
[Abstract]
[Full Text]
-
Shirai, Y., Kashiwagi, K., Yagi, K., Sakai, N., Saito, N.
(1998). Distinct Effects of Fatty Acids on Translocation of {gamma}- and {varepsilon}-Subspecies of Protein Kinase C. JCB
143: 511-521
[Abstract]
[Full Text]
-
Tan, S., Sagara, Y., Liu, Y., Maher, P., Schubert, D.
(1998). The Regulation of Reactive Oxygen Species Production during Programmed Cell Death. JCB
141: 1423-1432
[Abstract]
[Full Text]
-
Waters, J. C., Chen, R.-H., Murray, A. W., Salmon, E.D.
(1998). Localization of Mad2 to Kinetochores Depends on Microtubule Attachment, Not Tension. JCB
141: 1181-1191
[Abstract]
[Full Text]
-
Sartorius, C. A., Lu, B. D., Acakpo-Satchivi, L., Jacobsen, R. P., Byrnes, W. C., Leinwand, L. A.
(1998). Myosin Heavy Chains IIa and IId Are Functionally Distinct in the Mouse. JCB
141: 943-953
[Abstract]
[Full Text]
-
Machado, C., Sunkel, C. E., Andrew, D. J.
(1998). Human Autoantibodies Reveal Titin as a Chromosomal Protein. JCB
141: 321-333
[Abstract]
[Full Text]
-
Damico, R. L., Crane, J., Bates, P.
(1998). Receptor-triggered membrane association of a model retroviral glycoprotein. Proc. Natl. Acad. Sci. USA
95: 2580-2585
[Abstract]
[Full Text]
-
Ungermann, C., Nichols, B. J., Pelham, H. R.B., Wickner, W.
(1998). A Vacuolar v-t-SNARE Complex, the Predominant Form In Vivo and on Isolated Vacuoles, Is Disassembled and Activated for Docking and Fusion. JCB
140: 61-69
[Abstract]
[Full Text]
-
Hyman, A, Karsenti, E
(1998). The role of nucleation in patterning microtubule networks. J. Cell Sci.
111: 2077-2083
[Abstract]