Abstract
Nowadays, biologists can explore the cell at the nanometre level. They discover an unsuspected world, amazingly overcrowded, complex and heterogeneous, in which water, also, is complex and heterogeneous. In the cell, statistical phenomena, such as diffusion, long considered as the main transport for water soluble substances, must be henceforth considered as inoperative to orchestrate cell activity. Results at this level are not yet numerous enough to give an exact representation of the cell machinery; however, they are sufficient to cease reasoning in terms of statistics (diffusion, law of mass action, pH, etc.) and encourage cytologists and biochemists to prospect thoroughly the huge panoply of the biophysical properties of macromolecule-water associations at the nanometre level. Our main purpose, here, is to discuss some of the more common misinterpretations due to the ignorance of these properties, and expose briefly the bases for a better approach of the cell machinery. Giorgio Careri, who demonstrated the correlation between proton currents at the surface of lysozyme and activity of this enzyme was one of the pioneers of this approach.
Similar content being viewed by others
Notes
Organization of water into H-bonded linear chains of molecules has been often referred as “ice-like” water: indeed, this structure observed in the common Ih-ice is not present in all the types of ice.
References
Goodsell, D.S.: Inside a living cell. Trends Biochem. Sci. 16, 203–206 (1991)
Goodsell, D.S. (ed.): The Machinery of Life, 2nd edn. Springer, New York (2009)
Porter, K.R.: The cytoplasmic matrix and the integration of cellular function. Proc. of a Conference sponsored by Fogarty Internatl. Center, Natl. Institutes of Health. J. Cell Biol. 99, 1–248 (1984)
Porter K.R.: The cytomatrix: a short history of its study. J. Cell Biol. 99, 3–14 (1984)
Zierold, K.: The determination of wet weight concentrations of elements in freeze-dried cryosections from biological cells. Scanning Electron Microsc. 2, 713–724 (1986)
Mentré, P. (ed.): Coquille d’hydratation des macromolécules, eau “ liée ” et eau “ structurée ”. In: L’eau dans la cellule. Une interface hétérogène et dynamique des macromolécules, pp. 65–82. Masson-Dunod, Paris (1995)
Mentré, P., Hui Bon Hoa, G.: The effects of high hydrostatic pressures on living cells: a consequence of the properties of macomolecules and macromolecule-associated water. Int. Rev. Cytol. 201, 1–84 (2001)
Klotz, I.M.: Water. In: Kasha, M., Pullman, B. (eds.) Horizons in Biochemistry. Albert Szent-Györgyi dedicatory volume, pp. 523–550. Academic, New York (1962)
Mentré, P.: An introduction to “Water in the cell”: tamed hydra? In: Water in the Cell (Mentré, P. guest ed.). Cell. Mol. Biol. 47, 709–715 (2001)
Leitner, D.M., Gruebele, M., Havenith, M.: Solvation dynamics of biomolecules: modeling and terahertz experiments. HFSP J. 2, 314–323 (2008)
Cameron, I.L., Fullerton, G.D.: Non-bulk like water on cellular interfaces. In: Pollack, G. (ed.) Water and the Cell, pp. 315–323. Springer, Heidelberg (2006)
Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K., Walter, P. (eds): Molecular motors. In: Molecular Biology of the Cell, 4th ed., pp. 949–968. Garland Science, New York (2002)
Lasek, R.J., Garner, J.A., Brady, S.T.: Axonal transport of the cytoplasmic matrix. J. Cell Biol. 99, 212s–221s (1984)
Matveev, V.V.: Protoreaction of protoplasm. In: Water in the Cell (Mentré, P., ed.). Cell. Mol. Biol. 51, 715–723 (2005)
Troshin, A.S. (ed.): The protoplasm as a colloidal system. In: Problems of Cell Permeability, pp. 57–73 (1956). Translated from Russian by Widdas, W.F., Pergamon, Oxford (1966)
Troshin, A.S.: Do live cells have osmotic properties? In: Problems of Cell Permeability, pp. 30–56 (1956). Translated from Russian by Widdas, W.F., Pergamon, Oxford (1966)
Mentré, P. (ed.): L’eau dans la cellule. Une interface hétérogène et dynamique des macromolécules, p. 292. Masson-Dunod (1995)
Pollack, G.H.: Cells, Gels and the Engines of Life. A New, Unifying Approach to Cell Function. Ebner, Seattle (2001)
Pollack, G.H., Cameron, I.L., Wheatley, D.N. (ed.): Water and the Cell. Springer, New York (2006)
Chaplin, M.: http://www.lsbu.ac.uk/water/ (2009)
Schrödinger, E. (ed.): What is Life? The Physical Aspects of the Living Cell (1944)
Ling, G.N.: Solute exclusion by polymer and protein-dominated water: correlation with results of nuclear magnetic resonance (NMR) and calorimetric studies and their significance for the understanding of the physical state of water in living cells. Scanning Microsc. 2, 871–884 (1988)
Hofmeister, F: Zur Lehre von der Wirkung der Salze. Arch. Exp. Pathol. Pharmakol. 24, 247–260 (1888)
Ling, G.N.: A Physical Theory of the Living State: The Association-Induction Hypothesis, pp. 1–680. Blaisdell Waltham (1962)
Ling, G.N. (ed.): In Search of the Physical Basis of Life. Plenum, New York (1984)
Ling, G.N. (ed.): The membrane pump theory. In: A Revolution in the Physiology of the Living Cell, pp. 9–30. Krieger, Malabar (1992)
Wiggins, P., MacClement, B.A.E.: Two states of water found in hydrophobic clefts: their possible contribution to mechanism of action of pumps and other enzymes. Int. Rev. Cytol. 108, 249–304 (1987)
Wiggins, P., Van Ryn, R.T.: Changes in ionic selectivity with changes in density in gels and cells. Biophys. J. 58, 585–596 (1987)
Chen, X., Flores, S.C., Lim, S.M., Zhang, Y., Yang, T., Kherb, J., Cremer, P.: Specific anion effects on water structure adjacent to protein monolayers. Langmuir 26, 16447–16454 (2010)
Zhang, Y., Cremer P.S.: Interactions between macromolecules and ions: the Hofmeister series. Curr. Opinions Chem. Biol. 10, 658–663 (2006)
Glasstone, S. (ed.): Electrochemistry. In: Textbook of Physical Chemistry, pp. 884–1043. MacMillan, London (1948)
Simson, J.A.V., Spicer, S.S.: Selective subcellular localization of cations with variants of the potassium (pyro)antimonate technique. J. Histochem. Cytochem. 23, 575–598 (1975)
Mentré, P., Halpern, S.: Localization by pyroantimonate method and electron probe microanalysis of calcium and sodium in skeletal muscle of mouse. J. Histochem. Cytochem. 36, 55–64 (1988)
Mentré, P.: Taking into account the cell water properties for the cytochemical detection of cations: embedding into melamine after pyroantimonate fixation. In: Vasilescu, D., Jaz, J., Packer, L., Pullman, B. (eds.) Water and Ions in Biomolecular Systems. Proceed. 5th Unesco Internatl. Conf., pp. 287–294. Birkhäuser, Basel (1990)
Mentré, P.: Preservation of the diffusible cations for SIMS microscopy. I. A problem related to the state of water in the cell. Biol. Cell. 74, 19–30 (1992)
Mentré, P. Halpern, S.: Application of the pyroantimonate method and electron probe microanalysis to the study of glycogen metabolism in liver. Scanning Microsc. 3, 495–504 (1989)
Mentré, P. (ed.): Transports au sein de la cellule. In: L’eau dans la cellule. Une interface hétérogène et dynamique des macromolécules, pp. 207–233. Masson-Dunod, Paris (1995)
Berridge, M.J., Galone A.: Cytosolic oscillators. FASEB J. 2, 3074–3082 (1988)
Rasmussen, H.: The cycling of calcium as an intracellular messenger. Sci. Am. 261, 66–73 (1989)
Swann, K., Ozil, J.P.: Dynamics of the calcium signal that triggers mammalian egg activation: Int. Rev. Cytol. 152, 183–222 (1994)
Rand, R.P.: Raising water to new heights. Science 256, 618 (1992)
Colombo, M.F., Rau, D.C., Parsegian, V.A.: Protein solvation in allosteric regulation: a water effect on hemoglobin? Science 256, 655–659 (1992)
Teissié, J., Prats, M., Soucaille, P., Tocanne, J.F.: Evidence for conduction of protons along the interface between water and a polar lipid monolayer. Proc. Natl. Acad. Sci. U.S.A. 82, 3217–3221 (1985)
Kell, D.B.: On the functional proton current pathway of electron transport phosphorylation. An electrodic view. Biochim. Biophys. Acta 549, 55–99 (1979).
Careri, G., Giansanti, A., Rupley J.A.: Proton percolation on hydrated lysozyme powder. Proc. Natl. Acad. Sci. U.S.A. 83, 6810–6814 (1986)
Paddock, M.L., McPherson, P.H., Feher, G., Okamura, M.Y.: Pathway of proton transfer in bacterial reaction centers: replacement of serine-L223 by alanine inhibits electron and proton transfers associated with reduction of quinone to dihydroquinone. Proc. Natl. Acad. Sci. U.S.A. 87, 6803–6807 (1990)
Wikström, M., Verkhovsky, M.I., Hummer, G.: Water-gated mechanism of proton translocation by cytochrome c oxidase. Biochim. Biophys. Acta 1604, 61–65 (2003)
Yin, H., Feng, G., Clore, G.M., Hummer, G., Rasaiah, J.C.: Water in the polar and nonpolar cavities of the protein interleukin-1β. J. Phys. Chem., B. 114, 16290–16297 (2010)
Careri, G., Geraci, M., Giansanti, A., Rupley J.A.: Protonic conduction of hydrated lysozyme powders at megahertz frequencies. Proc. Natl. Acad. Sci. U.S.A. 82, 5342–5346 (1985)
Careri, G., Consolini, G., Bruni F.: Proton conductivity in hydrated proteins. Evidence for percolation. In: Vasilescu, D., Jaz, J., Packer, L., Pullman, B. (eds.) Water and Ions in Biomolecular Systems. Proceed. 5th Unesco Internatl. Conf., pp. 165–170. Birkhäuser, Basel (1990)
Careri, G., Peyrard, M.: Physical aspects of the weakly hydrated protein surface. In: Water in the Cell (Mentré, P. ed.). Cell Mol. Biol. 47, 745–756 (2001)
Albrecht-Buelher, G.: In defense of “nonmolecular” biology. Int. Rev. Cytol. 120, 191–241 (1990)
Mentré, P. (ed.): L’eau, une interface hétérogène et dynamique des macromolecules. In: L’eau dans la cellule. Une interface hétérogène et dynamique des macromolécules, pp. 268–275. Masson Dunod, Paris (1995)
Robinson, C.R., Sligar, S.G.: Hydrostatic and osmotic pressure as tools to study macromolecular recognition. Methods Enzymol. 259, 395–427 (1995)
Bloom, K., Yeh, E.: Tension management in the kinetochore. Curr. Biol. 20, 1040–1048 (2010)
Jibu, M., Hagan, S., Hameroff, S.R., Pribram, K.H., Yasue, K.: Quantum optical coherence in cytoskeletal microtubules: implications for brain function. Biosystems 32, 195–209 (1994)
Hameroff, S.R., Penrose, R. (eds.): Orchestrated reduction of quantum coherence in brain microtubules: a model for consciousness? In: Toward a Science of Consciousness—The First Tucson Discussions and Debates, pp. 507–540. Cambridge, MIT (1996)
Albrecht-Buelher, G.: Cellular infrared detector appears to be contained in the centrosome. Cell Motil. Cytoskelet. 27, 262–271 (1994)
Nihonyanagi, S., Yamaguchi, S., Tahara, T.: Water hydrogen bond structure near highly charged interfaces is not like ice. J. Am. Chem. Soc. 132, 6867–6869 (2010)
Mentré, P.: Organization and properties of water in cell system. In: Greppin, H., Penel, C., Broughton, W.J., Strasser R. (eds.) Integrated Plant Systems, pp. 3–22. University of Geneva, Geneva (2000)
Acknowledgement
I am very grateful towards Dr. Yolène Thomas for her encouragements.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mentré, P. Water in the orchestration of the cell machinery. Some misunderstandings: a short review. J Biol Phys 38, 13–26 (2012). https://doi.org/10.1007/s10867-011-9225-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10867-011-9225-9