Intracellular pH as an electrostatic regulator of the spindle assembly checkpoint.
Main Article Content
Abstract
Experiments have shown that intracellular pH of many cells rises to a maximum at the onset of mitosis, subsequently decreasing 0.3 to 0.5 pH units by the end of mitosis. This result, and observations that tubulin net charge depends strongly on pH, may be significant for microtubule (MT) dynamics during mitosis. In vivo studies demonstrate that MT dynamics is sensitive to pH, with MT growth favored by higher pH values. Thus it seems likely that the shift from the dominance of mi- crotubule growth during prophase, and to a lesser extent during prometaphase, to a parity between MT polymerization and depolymerization during metaphase chromo- some oscillations is a consequence of a gradually decreasing intracellular pH during mitosis. A long-standing problem in the cell biology of mitosis concerns the operation of the spindle assembly checkpoint, a surveillance mechanism that delays anaphase-A onset until all chromosomes are attached to the spindle. When improper chromosome attachments persist into anaphase, chromosome segregation is defective and cells con- taining abnormal numbers of chromosomes can result leading to genetic diseases such as cancer. Here we propose that a consequence of relatively high intracellular pH near the metaphase-anaphase transition results in an anaphase-A delay that functions as the spindle assembly checkpoint.
Article Details
How to Cite
SHAIN, Daniel; GAGLIARDI, L. John.
Intracellular pH as an electrostatic regulator of the spindle assembly checkpoint..
Medical Research Archives, [S.l.], v. 2, n. 7, nov. 2015.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/368>. Date accessed: 27 dec. 2024.
Keywords
checkpoint, electrostatics
Section
Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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[30] Gagliardi LJ: Electrostatic force in prometaphase, metaphase, and anaphase- A chromosome motions. Phys Rev E 2002, 66. 011901-1 – 011901-8.
[31] Gagliardi LJ: Microscale electrostatics in mitosis. J. Electrostat. 2002, 54: 219-232.
[32] Gagliardi LJ, Shain DH: Is intracellular pH a clock for mitosis? Theor Biol Med Model 2013, 10:8.
[33] Gagliardi LJ, Shain DH: Chromosome congression explained by nano- scale electrostatics. Theor Biol Med Model 2014, 11:12.
[34] Maiato H, DeLuca J, Salmon ED, Earnshaw WC: The dynamic kinetochore microtubule interface. J Cell Sci 2004, 117:5461-5477.
[35] Hepler PK, Callaham DA: Free calcium increases in anaphase in stamen hair cells of Tradescantia. J Cell Biol 1987, 105:2137-2143.
[36] Zhang, DH, Callaham DA, Hepler PK: Regulation of anaphase chromo- some motions in Tradescantia stamen hair cells by calcium and related sig- nalling agents. J Cell Biol 1990, 111:171-182.
[37] Liu D, Vader G, Vromans MJ, Lampson MA, and Lens SM: Sensing chro- mosome bi-orientation by spatial separation of Aurora-B kinase from kine- tochore substrates. Science 2009, 323:1350-1353.
[38] Cheesman JM, Anderson S, Jwa M, Green EM, Kang J, Yates JR, Chan CS, Drubin DG, and Barnes G: Phospho-regulation of kinetochore microtubule at- tachments by the Aurora-kinase lpl1p. Cell 2002, 111:163-172.
[39] Yang Z, Kenny AE, Brito DA, Rieder CL: Cells satisfy the mitotic check- point in Taxol, and do so faster in concentrations that stabilize syntelic at- tachments. J Cell Biol 2009, 186:675-684.
[40] Khodjakov A and Rieder C Too much of a good thing (can be bad). Curr Biol 2009, 19:R1032.
[41] Nezi L and Musacchio A: Sister chromatid tension and the spindle as- sembly checkpoint. Curr Opin Cell biol 2009, 21:785-795.
[2] Rattani A, Vinod PK, Godwin J, Tachibana-Konwalski K, Wolna M, Malum- bres M, Novák B, Nasmyth K: Dependency of the spindle assembly checkpoint on Cdk1 renders the anaphase transition irreversible. Curr Biol 2014, 24:630- 637.
[3] Kamenz J, Hauf S: Slow checkpoint activation kinetics as a safety device in anaphase. Curr Biol 2014, 24:646-651.
[4] Kops Geert: Cell division: SACing the anaphase problem. Curr Biol 2014, 24:R224-226.
[5] Alberts B, Bray D, Lewis J, Raff M, Roberts MK, Watson JD: Molecular Biology of the Cell. New York: Garland Publishing Company; 1994:921.
[6] Gagliardi LJ: Electrostatic force generation in chromosome motions dur- ing mitosis. J Electrostat 2005, 63:309-327.
[7] Amirand C et al.: Intracellular pH in one-cell mouse embryo differs be- tween subcellular compartments and between interphase and mitosis. Biol Cell 2000, 92:409-419.
[8] Steinhardt RA, Morisawa M: Changes in intracellular pH of Physarum Plasmodium during the cell cycle and in response to starvation. In Intra- cellular pH: Its Measurement, Regulation, and Utilization in Cellular Functions. Edited by Nuccitelli R, Deamer DW. New York: Alan R. Liss Publishing Com- pany; 1982:361-374.
[9] Schatten G, Bestor T, Balczon R, Henson J, Schatten H: Intracellular pH shift leads to microtubule assembly and microtubule-mediated motility dur- ing sea urchin fertilization: Correlations between elevated intracellular pH and microtubule activity and depressed intracellular pH and microtubule dis- assembly. Eur J Cell Biol 1985, 36: 116-127.
[10] Kirschner MW: Implications of treadmilling for the stability and polarity of actin and tubulin polymers in vivo. J Cell Biol 1980, 86: 330-334.
[11] Deery WJ, Brinkley BR: Cytoplasmic microtubule assembly – disassem- bly from endogenous tubulin in a Brij – lysed cell model. J Cell Biol 1983, 96: 1631-1641.
[12] Olmsted JB, Borisy GG: Characterization of microtubule assembly in porcine brain extracts by viscometry. Biochem 1973, 12: 4282-4289.
[13] Jordan-Lloyd D, Shore A: The Chemistry of Proteins. London: J.A. Churchill Publishing Company; 1938.
[14] Pauling L: The adsorption of water by proteins. J Am Chem Soc 1945, 67: 555-557.
[15] Toney MF, Howard JN, Richer J, Borges GL, Gordon JG, Melroy OR, Wiesler DG, Yee D, Sorensen L: Voltage-dependent ordering of water molecules at an electrode-electrolyte interface. Nature 1994, 368: 444-446.
[16] Teschke, O, Ceotto, G, De Souza EF: Interfacial water dielectric permittiv- ity profile measurements using atomic force spectroscopy. Phys Rev E 2001, 64: 011605-1 – 011605-10.
[17] Gagliardi LJ: Electrostatic Considerations in Mitosis. Bloomington, IN: iU-
niverse Publishing Company; 2009.
[18] Gagliardi LJ, Shain DH: Polar electrostatic forces drive poleward chro-
mosome motions. Cell Division 2014, 9:5.
[19] Sataric ́ MV, Tuszyn ́ ski JA, Z ̆ akula RB: Kinklike excitations as an energy-
transfer mechanism in microtubules. Phys Rev E 1993, 48: 589-597.
[20] Brown JA, Tuszyn ́ski JA: Dipole interactions in axonal microtubules as
a mechanism of signal propagation. Phys Rev E 1997, 56: 5834-5340.
[21] Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA: Electrostatics of nanosystems: Applications to microtubules and the ribosome. Proc Natl Acad Sci 2001, 98: 10037-10041.
[22] Tuszyn ́ski JA, Brown JA, Hawrylak P: Dielectric polarization, electrical conduction, information processing and quantum computation in microtubules. Are they plausible? Phil Trans R Soc (London) 1998, A356: 1897-1926.
[23] Tuszyn ́ski JA, Brown JA, Carpenter EJ, Crawford, E, Nip MLA: Electro- static Properties of Tubulin and Microtubules. In ESA-IEJ Joint Symposium on Electrostatics. Edited by Crowley JM. CA: Laplacian Press; 2002:41-50.
[24] Tuszyn ́ ski JA, Hameroff S, Sataric ́ MV, Trpisová B, Nip MLA: Ferroelectric behavior in microtubule dipole lattices: Implications for information process- ing, signaling, and assembly/disassembly. J Theoretical Biol 1995, 174: 371- 380.
[25] Sackett D: pH-induced conformational changes in the carboxy-terminal tails of tubulin. Banff, Alberta, Canada: Presented at the Banff Workshop Molecular Biophysics of the Cytoskeleton; August 25-30, 1997.
[26] Alberts B, Bray D, Lewis J, Raff M, Roberts MK, Watson JD: Molecular Biology of the Cell. New York: Garland Publishing Company; 1994:1041.
[27] Westerman S, et al.: Formation of dynamic kinetochore-microtubule in- terface through assembly of the Dam1 ring complex. Mol Cell 2005, 17:277- 290.
[28] Weisenberg RC: Microtubule formation in vitro in solutions containing low calcium concentrations. Science 1972, 177:1104-1105.
[29] Borisy GG, Olmsted JB: Nucleated assembly of microtubules in porcine brain extracts. Science 1972, 177: 1196-1197.
[30] Gagliardi LJ: Electrostatic force in prometaphase, metaphase, and anaphase- A chromosome motions. Phys Rev E 2002, 66. 011901-1 – 011901-8.
[31] Gagliardi LJ: Microscale electrostatics in mitosis. J. Electrostat. 2002, 54: 219-232.
[32] Gagliardi LJ, Shain DH: Is intracellular pH a clock for mitosis? Theor Biol Med Model 2013, 10:8.
[33] Gagliardi LJ, Shain DH: Chromosome congression explained by nano- scale electrostatics. Theor Biol Med Model 2014, 11:12.
[34] Maiato H, DeLuca J, Salmon ED, Earnshaw WC: The dynamic kinetochore microtubule interface. J Cell Sci 2004, 117:5461-5477.
[35] Hepler PK, Callaham DA: Free calcium increases in anaphase in stamen hair cells of Tradescantia. J Cell Biol 1987, 105:2137-2143.
[36] Zhang, DH, Callaham DA, Hepler PK: Regulation of anaphase chromo- some motions in Tradescantia stamen hair cells by calcium and related sig- nalling agents. J Cell Biol 1990, 111:171-182.
[37] Liu D, Vader G, Vromans MJ, Lampson MA, and Lens SM: Sensing chro- mosome bi-orientation by spatial separation of Aurora-B kinase from kine- tochore substrates. Science 2009, 323:1350-1353.
[38] Cheesman JM, Anderson S, Jwa M, Green EM, Kang J, Yates JR, Chan CS, Drubin DG, and Barnes G: Phospho-regulation of kinetochore microtubule at- tachments by the Aurora-kinase lpl1p. Cell 2002, 111:163-172.
[39] Yang Z, Kenny AE, Brito DA, Rieder CL: Cells satisfy the mitotic check- point in Taxol, and do so faster in concentrations that stabilize syntelic at- tachments. J Cell Biol 2009, 186:675-684.
[40] Khodjakov A and Rieder C Too much of a good thing (can be bad). Curr Biol 2009, 19:R1032.
[41] Nezi L and Musacchio A: Sister chromatid tension and the spindle as- sembly checkpoint. Curr Opin Cell biol 2009, 21:785-795.