Systems Approach to Mitotic Chromosome Motions

DOI: 10.4236/ojbiphy.2013.32017   PDF   HTML   XML   2,898 Downloads   5,482 Views   Citations


Recent experiments revealing possible nanoscale electrostatic interactions in force generation at kinetochores for chromosome motions have prompted speculation regarding possible models for interactions between positively charged molecules in kinetochores and negative charge on C-termini near the plus ends of microtubules. A clear picture of how kinetochores establish and maintain a dynamic coupling to microtubules for force generation during the complex motions of mitosis remains elusive. The molecular cell biology paradigm requires that specific molecules, or molecular geometries, for force generation be identified. However, it is possible to account for mitotic chromosome motions within a systems approach in terms of experimentally known cellular electric charge distributions interacting over nanometer distances.

Share and Cite:

L. Gagliardi, "Systems Approach to Mitotic Chromosome Motions," Open Journal of Biophysics, Vol. 3 No. 2, 2013, pp. 133-147. doi: 10.4236/ojbiphy.2013.32017.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] G. J. Guimaraes, Y. Dong, B. F. McEwen and J. G. De-Luca, “Kinetochore-Microtubule Attachment Relies on the Disordered N-Terminal Tail Domain of Hec1,” Current Biology, Vol. 18, No. 22, 2008, pp. 1778-1784. doi:10.1016/j.cub.2008.08.012
[2] S. A. Miller, M. L. Johnson and P. T. Stukenberg, “Kinetochore Attachments Require an Interaction between Unstructured Tails on Microtubules and Ndc80/Hec1,” Current Biology, Vol. 18, No. 22, 2008, pp. 1785-1791. doi:10.1016/j.cub.2008.11.007
[3] L. J. Gagliardi, “Electrostatic Force in Prometaphase, Metaphase, and Anaphase-A Chromosome Motions,” Physical Review E, Vol. 66, No. 1, 2002, Article ID: 011901.
[4] L. J. Gagliardi, “Electrostatic Force Generation in Chromosome Motions during Mitosis,” Journal of Electrostatics, Vol. 63, No. 3-4, 2005, pp. 309-327. doi:10.1016/j.elstat.2004.09.007
[5] R. B. Nicklas and D. F. Kubai, “Microtubules, Chromosome Movement, and Reorientation after Chromosomes Are Detached from the Spindle by Micromanipulation,” Chromosoma, Vol. 92, No. 4, 1985, pp. 313-324. doi:10.1007/BF00329815
[6] B. Alberts, D. Bray, J. Lewis, M. Raff, M. K. Roberts and J. D. Watson, “Molecular Biology of the Cell,” Garland Publishing Company, New York, 1994, p. 920.
[7] G. B. Benedek and F. M. H. Villars, “Physics: With Illustrative Examples from Medicine and Biology: Electricity and Magnetism,” Springer-Verlag, New York, 2000, p. 403.
[8] R. A. Steinhardt and M. Morisawa, “Changes in Intracellular pH of Physarum Plasmodium during the Cell Cycle and in Response to Starvation,” In: R. Nuccitelli and D. W. Deamer, Eds., Intracellular pH: Its Measurement, Regulation, and Utilization in Cellular Functions, Alan R. Liss, New York, 1982, pp. 361-374.
[9] C. Amirand, et al., “Intracellular pH in One-Cell Mouse Embryo Differs between Subcellular Compartments and Between Interphase and Mitosis,” Biology of Cell, Vol. 92, No. 6, 2000, pp. 409-419. doi:10.1016/S0248-4900(00)01080-7
[10] G. Schatten, T. Bestor, R. Balczon, J. Henson and H. Schatten, “Intracellular pH Shift Leads to Microtubule Assembly and Microtubule-Mediated Motility during Sea Urchin Fertilization: Correlations between Elevated Intracellular pH, Microtubule Activity and Depressed Intracellular pH and Microtubule Disassembly,” European Journal of Cell Bi-ology, Vol. 36, No. 1, 1985, pp. 116- 127.
[11] M. W. Kirschner, “Implications of Treadmilling for the Stability and Polarity of Actin and Tubulin Polymers in Vivo,” Journal of Cell Biology, Vol. 86, No. 1, 1980, pp. 330-334. doi:10.1083/jcb.86.1.330
[12] M. De Brabander, G. Geuens and R. Nuydens, “Microtubule Stability and Assembly in Living Cells: The Influence of Metabolic Inhibitors, Taxol and pH,” Cold Spring Harbor Symposia on Quantitative Biology, Vol. 46, 1982, pp. 227-240. doi:10.1101/SQB.1982.046.01.026
[13] W. J. Deery and B. R. Brinkley, “Cytoplasmic Microtubule Assembly—Disassembly from Endogenous Tubulin in a Brij-Lysed Cell Model,” Journal of Cell Biology, Vol. 96, No. 6, 1983, pp. 1631-1641. doi:10.1083/jcb.96.6.1631
[14] J. B. Olmsted and G. G. Borisy, “Characterization of Microtubule Assembly in Porcine Brain Extracts by Viscometry,” Biochemistry, Vol. 12, No. 21, 1973, pp. 4282-4289. doi:10.1021/bi00745a037
[15] M. V. Sataric, J. A. Tuszyński and R. B. Zakula, “Kink-like Excitations as an Energy Transfer Mechanism in Microtubules,” Physical Review E, Vol. 48, No. 1, 1993, pp. 589-597. doi:10.1103/PhysRevE.48.589
[16] J. A. Brown and J. A. Tuszyński, “Dipole Interactions in Axonal Microtubules as a Mechanism of Signal Propagation,” Physical Review E, Vol. 56, No. 5, 1997, pp. 5834-5840. doi:10.1103/PhysRevE.56.5834
[17] N. A. Baker, D. Sept, S. Joseph, M. J. Holst and J. A. McCammon, “Elec-trostatics of Nanosystems: Applications to Microtubules and the Ribosome,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 98, No. 18, 2001, pp. 10037-10041. doi:10.1073/pnas.181342398
[18] J. A. Tuszyński, J. A. Brown and P. Hawrylak, “Dielectric Polarization, Electrical Conduction, Information Processing and Quantum Computation in Microtubules: Are They Plausible?” Philosophical Transactions of the Royal Society of London, Vol. A356, No. 1743, 1998, pp. 1897-1926.
[19] J. A. Tuszyński, S. Hameroff, M. V. Sataric, B. Trpisová, and M. L. A. Nip, “Ferroelectric Behavior in Microtubule Dipole Lattices: Implications for Information Processing, Signaling and Assembly/Disassembly,” Journal of Theoretical Biology, Vol. 174, No. 4, 1995, pp. 371-380. doi:10.1006/jtbi.1995.0105
[20] D. Sackett, “pH-Induced Conformational Changes in the Carboxy Terminal Tails of Tubulin,” Presented at the Banff Workshop Molecular Biophysics of the Cytoskeleton, Banff, 25-30 August 1997.
[21] J. A. Tuszyński, J. A. Brown, E. J. Carpenter and E. Crawford, “Electrostatic Properties of Tubulin and Microtubules,” In: J. M. Crowley, Ed., Proceedings of the Electrostatics Society of America and Institute of Electrostatics Japan, Laplacian Press, Morgan Hill, 2002, pp. 41-50.
[22] R. Heald, R. Tournebize, T. Blank, R. Sandaltzopoulos, P. Becker, A. Hyman and E. Karsenti, “Self-Organization of Microtubules into Bipolar Spindles around Artificial Chromosomes in Xenopus Egg Extracts,” Nature, Vol. 382, 1996, pp. 420-425. doi:10.1038/382420a0
[23] H. C. Joshi, M. J. Palacios, L. McNamara, D. W. Cleveland, “γ-Tubulin Is a Centrosomal Protein Required for Cell Cycle-Dependent Microtubule Nucleation,” Nature, Vol. 356, 1992, pp. 80-83. doi:10.1038/356080a0
[24] L. J. Gagliardi, “Microscale Electrostatics in Mitosis,” Journal of Electrostatics, Vol. 54, No. 3-4, 2002, pp. 219- 232. doi:10.1016/S0304-3886(01)00155-3
[25] S. Hormeno, et al., “Single Centrosome Manipulation Reveals Its Electric Charge and Associated Dynamic Structure,” Biophysical Journal, Vol. 97, No. 4, 2009, pp. 1022-1030. doi:10.1016/j.bpj.2009.06.004
[26] Y. H. Song and E. Mandelkow, “The Anatomy of Flagellar Microtubules: Polarity, Seam, Junctions, and Lattice,” Journal of Cell Biology, Vol. 128, No. 1, 1995, pp. 81-94. doi:10.1083/jcb.128.1.81
[27] C. Ciferri, et al., “Implications for Kinetochore-Micro- tubule Attachment from the Structure of an Engineered Ndc80 Complex,” Cell, Vol. 133, No. 3, 2008, pp. 427- 439. doi:10.1016/j.cell.2008.03.020
[28] S. Westermann, et al., “Formation of a Dynamic Kinetochore-Microtubule Interface through Assembly of the Dam1 Ring Complex,” Molecular Cell, Vol. 17, No. 2, 2005, pp. 277-290. doi:10.1016/j.molcel.2004.12.019
[29] D. Jordan-Lloyd and A. Shore, “The Chemistry of Proteins,” J. A. Churchill Publishing Company, London, 1938.
[30] L. Pauling, “The Adsorption of Water by Proteins,” Jour- nal of American Chemical Society, Vol. 67, No. 4, 1945, pp. 555-557. doi:10.1021/ja01220a017
[31] M. F. Toney, J. N. Howard, J. Richer, G. L. Borges, J. G. Gordon, O. R. Melroy, D. G. Wiesler, D. Yee and L. Sorensen, “Voltage-Dependent Ordering of Water Molecules at an Electrode-Electrolyte Interface,” Nature, Vol. 368, 1994, pp. 444-446. doi:10.1038/368444a0
[32] R. C. Weisenberg, “Microtubule Formation in Vitro in Solutions Containing Low Calcium Concentrations,” Science, Vol. 177, No. 4054, 1972, pp. 1104-1105. doi:10.1126/science.177.4054.1104
[33] G. G. Borisy and J. B. Olmsted, “Nucleated Assembly of Microtubules in Porcine Brain Extracts,” Science, Vol. 177, No. 4055, 1972, pp. 1196-1197. doi:10.1126/science.177.4055.1196
[34] B. Alberts, D. Bray, J. Lewis, M. Raff, M. K. Roberts and J. D. Watson, “Molecular Biology of the Cell,” Garland Publishing Company, New York, 1994, p. 930.
[35] G. B. Benedek and F. M. H. Villars, “Physics: With Illustrative Examples from Medicine and Biology: Electricity and Magnetism,” Springer-Verlag, New York, 2000, p. 400.
[36] J. O. Bockris and A. K. N. Reddy, “Modern Electrochemistry,” Plenum Press, New York, 1977. doi:10.1007/978-1-4613-4136-9
[37] O. Teschke, G. Ceotto and E. F. de Souza, “Interfacial Water Dielectric Permittivity Profile Measurements Using Atomic Force Microscopy,” Physical Review E, Vol. 64, No. 1, 2001, Article ID: 011605.
[38] G. H. Pollack, “Cells, Gels and the Engines of Life,” Ebner and Sons Publishers, Seattle, 2001, p. 69.
[39] S. P. Alexander and C. L. Rieder, “Chromosome Motion during Attachment to the Vertebrate Spindle: Initial Saltatory-Like Behavior of Chromosomes and Quantitative Analysis of Force Production by Nascent Kinetochore Fibers,” The Journal of Cell Biology, Vol. 113, No. 4, 1991, pp. 805-815. doi:10.1083/jcb.113.4.805
[40] R. Stracke, K. J. Bohm, L. Wollweber, J. A. Tuszynski and E. Unger, “Analysis of the Migration Behaviour of Single Microtubules in Electric Fields,” Biochemical and Biophysical Research Communications, Vol. 293, No. 1, 2002, pp. 602-609.
[41] C. L. Rieder, “The Formation, Structure, and Composition of the Mammaliam Kinetochore and Kinetochore Fiber,” International Review of Cytology, Vol. 79, 1982, pp. 1-58. doi:10.1016/S0074-7696(08)61672-1
[42] G. Civelekoglu-Scholey, D. J. Sharp, A. Mogilner and J. M. Scholey, “Model of Chromosome Motility in Drosophila Embryos: Adaptation of a General Mechanism for Rapid Mitosis,” Biophysical Journal, Vol. 90, No. 11, 2006, pp. 3966-3982. doi:10.1529/biophysj.105.078691
[43] E. L. Grishchuk et al., “The Dam1 Ring Binds Microtubules Strongly Enough to Be a Processive as Well as Energy-Efficient Coupler for Chromosome Motion,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 105, No. 40, 2008, pp. 15423-15428. doi:10.1073/pnas.0807859105
[44] J. R. McIntosh, et al., “Kinetochore-Microtubule Interactions Visualized by EM Tomagraphy,” The 47th Annual Meeting of the American Society for Cell Biology, Washington DC, 1-5 December 2007.
[45] D. J. Griffiths, “Introduction to Electrodynamics,” Prentice-Hall Publishing Company, Upper Saddle River, 1999, p. 75.
[46] S. A. Schelkunoff, “Electromagnetic Fields,” Blaisdell Publishing Company, New York, 1963, p. 29.
[47] C. L. Rieder and S. P. Alexander, “Kinetochores Are Transported Poleward along a Single Astral Microtubule during Chromosomes Attachment to the Spindle in Newt Lung Cells,” The Journal of Cell Biology, Vol. 110, No. 1, 1990, pp. 81-95. doi:10.1083/jcb.110.1.81
[48] A. Grancell and P. K. Sorger, “Chromosome Movement: Kinetochores Motor Along,” Current Biology, Vol. 8, No. 11, 1998, pp. R382-R385. doi:10.1016/S0960-9822(98)70243-X
[49] L. J. Gagliardi, “Induced Electrostatic Charge in Pole-ward Motion of Chromosomes during Mitosis,” Journal of Electrostatics, Vol. 66, No. 3-4, 2008, pp. 147-155. doi:10.1016/j.elstat.2007.11.002
[50] C. L. Rieder, E. A. Davison and L. C. W. Jensen, “Oscillatory Movements of Monooriented Chromosomes and Their Position Relative to the Spindle Pole Result from the Ejection Properties of the Aster and Half-Spindle,” The Journal of Cell Biology, Vol. 103, No. 2, 1986, pp. 581-591. doi:10.1083/jcb.103.2.581
[51] B. Alberts, D. Bray, J. Lewis, M. Raff, M. K. Roberts and J. D. Watson, “Molecular Biology of the Cell,” Garland Publishing Company, New York, 1994, p. 926.
[52] T. S. Hays and E. D. Salmon, “Poleward Force at Kinetochores in Metaphase Depends on the Number of Kinetochore Microtubules,” The Journal of Cell Biology, Vol. 110, No. 2, 1990, pp. 391-404. doi:10.1083/jcb.110.2.391
[53] H. Maiato, J. DeLuca, E. D. Salmon and W. C. Earnshaw, “The Dynamic Kinetochore-Microtubule Interface,” Journal of Cell Science, Vol. 117, Part 23, 2004, pp. 5461- 5477. doi:10.1242/jcs.01536
[54] L. J. Gagliardi, “Electrostatic Considerations in Mitosis,” iUniverse Publishing Company, Bloomington, 2009.
[55] P. K. Hepler and D. A. Callaham “Free Calcium Increases in Anaphase in Stamen Hair Cells of Tradescantia,” The Journal of Cell Biology, Vol. 105, No. 5, 1987, pp. 2137-2143. doi:10.1083/jcb.105.5.2137
[56] P. K. Hepler, “Regulation of Anaphase Spindle Microtubule Structure in Stamen Hair Cells of Tradescantia by Calcium and Related Agents,” In: J. S. Hyams and B. R. Brinkley, Eds., Mitosis: Molecules and Mechanisms, Academic Press, San Diego, 1989, pp. 241-271.
[57] D. H. Zhang, D. A. Callaham and P. K. Hepler, “Regulation of Anaphase Chromosome Motion in Tradescantia Stamen Hair Cells by Calcium and Related Signalling Agents,” The Journal of Cell Biology, Vol. 111, No. 1, 1990, pp. 171-182. doi:10.1083/jcb.111.1.171
[58] E. D. Salmon and R. R. Segall, “Calcium-Labile Mitotic Spindles Isolated from Sea Urchin Eggs (Lytechinus variegatus),” The Journal of Cell Biology, Vol. 86, No. 2, 1980, pp. 355-365. doi:10.1083/jcb.86.2.355
[59] D. P. Kiehart, “Studies on the in Vivo Sensitivity of Spindle Microtubules to Calcium Ions and Evidence for a Vesicular Calcium-Sequestereing System,” The Journal of Cell Biology, Vol. 88, No. 3, 1981, pp. 604-617. doi:10.1083/jcb.88.3.604
[60] W. Z. Cande, “Physiology of Chromosome Movement in Lysed Cell Models,” In: H. G. Schweiger, Ed., International Cell Biology, Springer Publishing Company, Berlin, 1981, pp. 382-391.
[61] J. B. Olmsted and G. G. Borisy, “Ionic and Nucleotide Requirements for Microtubule Polymerization in Vitro,” Biochemistry, Vol. 14, No. 13, 1975, pp. 2996-3005. doi:10.1021/bi00684a032
[62] R. B. Nicklas, “Chromosome Movement: Current Models and Experiments on Living Cells,” In: S. Inoue and R. E. Stephens, Eds., Molecules and Cell Movement, Raven Press, New York, 1975, pp. 97-117.
[63] R. B. Nicklas, “Chromosomes and Kinetochores Do More in Mitosis than Previously Thought,” In: J. P. Gustafson, R. Appels and R. J. Kaufman, Eds., Chromosome Structure and Function, Plenum Publishing Company, New York, 1987, pp. 53-74.
[64] E. D. Salmon, “Spindle Microtubules: Thermodynamics of in Vivo Assembly and Role in Chromosome Movement,” Annals of the New York Academy of Sciences, Vol. 253, 1975, pp. 383-406. doi:10.1111/j.1749-6632.1975.tb19216.x
[65] E. D. Salmon, “Microtubule Dynamics and Chromosome Movement,” In: J. S. Hyams and B. R. Brinkley, Eds., Mitosis: Molecules and Mechanisms, Academic Press, San Diego, 1989, pp. 119-181.
[66] S. L. Wolfe, “Molecular and Cellular Biology,” Wadsworth Publishing Company, Belmont, 1993, p. 425.
[67] H. Diebler, G. Eigen, G. Ilgenfritz, G. Maass and R. Winkler, “Kinetics and Mechanism of Reactions of Main Group Metal Ions with Biological Carriers,” Pure and Applied Chemistry, Vol. 20, No. 1, 1969, pp. 93-116. doi:10.1351/pac196920010093

comments powered by Disqus

Copyright © 2020 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.