Skip to content
BY-NC-ND 3.0 license Open Access Published by De Gruyter July 23, 2011

Solute-dependent activation of cell motility in strongly hypertonic solutions in Dictyostelium discoideum, human melanoma HTB-140 cells and walker 256 carcinosarcoma cells

  • Włodzimierz Korohoda EMAIL logo , Magdalena Kucia , Ewa Wybieralska , Magdalena Wianecka-Skoczeń , Agnieszka Waligórska , Justyna Drukała and Zbigniew Madeja

Abstract

Published data concerning the effects of hypertonicity on cell motility have often been controversial. The interpretation of results often rests on the premise that cell responses result from cell dehydration, i.e. osmotic effects. The results of induced hypertonicity on cell movement of Dictyostelium discoideum amoebae and human melanoma HTB-140 cells reported here show that: i) hypertonic solutions of identical osmolarity will either inhibit or stimulate cell movement depending on specific solutes (Na+ or K+, sorbitol or saccharose); ii) inhibition of cell motility by hypertonic solutions containing Na+ ions or carbohydrates can be reversed by the addition of calcium ions; iii) various cell types react differently to the same solutions, and iv) cells can adapt to hypertonic solutions. Various hypertonic solutions are now broadly used in medicine and to study modulation of gene expression. The observations reported suggest the need to examine whether the other responses of cells to hypertonicity can also be based on the solute-dependent cell responses besides cell dehydration due to the osmotic effects.

[1] Zischka, H., Oehme, F., Pintsch, T., Ott, A., Keller, H., Kellermann, J. and Schuster, S.C. Rearrangement of cortex proteins constitutes and osmoprotective mechanism in Dictyostelium. EMBO J. 18 (1999) 4241–4249. http://dx.doi.org/10.1093/emboj/18.15.424110.1093/emboj/18.15.4241Search in Google Scholar

[2] Erickson, G.R., Alexopoulos, L.G. and Guilak, F. Hyper-osmotic stress induces volume change and calcium transients in chondrocytes by transmembrane, phospholipids, and G-protein pathways. J. Biomech. 34 (2001) 1527–1535. http://dx.doi.org/10.1016/S0021-9290(01)00156-710.1016/S0021-9290(01)00156-7Search in Google Scholar

[3] Cai, Q., Michea, L., Andrews, P., Zhang, Z., Rocha, G., Dmitrieva, N. and Burg M.B. Rate of increase of osmolarity determined osmotic tolerance of mouse inner medullary epithelial cells. Am. J. Physiol. Renal Physiol. 283 (2002) F792–798. 10.1152/ajprenal.00046.2002Search in Google Scholar

[4] Mavrogonatou, E. and Kletsas, D. High osmolarity activates the G1 and G2 cell cycle checkpoints and affects the DNA integrity of nucleus pulposus intervertebral disc cells triggering an enhanced DNA repair response. DNA Repair (Amst) 8 (2009) 930–943. http://dx.doi.org/10.1016/j.dnarep.2009.05.00510.1016/j.dnarep.2009.05.005Search in Google Scholar

[5] Kerwin, A.J., Schinco, M.A., Tepas, J.J., Renfro, W.H., Vitarbo, E.A., and Muehlberger, M. The use of 23.4% hypertonic saline for the management of elevated intracranial pressure in patients with severe traumatic brain injury: A pilot study. J. Trauma 67 (2009) 277–282. http://dx.doi.org/10.1097/TA.0b013e3181acc72610.1097/TA.0b013e3181acc726Search in Google Scholar

[6] Loram, L., Horwitz, E. and Bentlley, A. Gender and site of injection do not influence intensity of hypertonic saline-induced muscle pain in healthy volunteers. Man Ther. 14 (2009) 526–530. http://dx.doi.org/10.1016/j.math.2008.09.00210.1016/j.math.2008.09.002Search in Google Scholar

[7] Vinzenzi, R., Cepeda, L.A., Pirani, W.M., Sannomyia, P., Rocha-e-Silvia, M. and Cruz, R. Small volume resuscitation with 3% hypertonic saline solution decrease inflammatory response and attenuates end organ damage after controlled hemorrhagic shock. Am. J. Surg. 198 (2009) 407–414. http://dx.doi.org/10.1016/j.amjsurg.2009.01.01710.1016/j.amjsurg.2009.01.017Search in Google Scholar

[8] Burg, M.B., Kwon, E.D. and Kültz, D. Regulation of gene expression by hypertonicity. Annu. Rev. Physiol. 59 (1997) 437–455. http://dx.doi.org/10.1146/annurev.physiol.59.1.43710.1146/annurev.physiol.59.1.437Search in Google Scholar

[9] Maallem, S., Wierinckx, A., Lachuer, J., Kwon, M.H. and Tappaz, M.L. Gene expression profiling in brain following acute systemic hypertonicity: novel genes possibly involved in osmoadaptation. J. Neurochem 105 (2008) 1198–1211. http://dx.doi.org/10.1111/j.1471-4159.2008.05222.x10.1111/j.1471-4159.2008.05222.xSearch in Google Scholar

[10] Oster, G.F. and Perelson, A.S. The physics of cell motility. J. Cell Sci. Suppl.8 (1987) 35–54. Search in Google Scholar

[11] Fedier, A. and Keller, H.U. Suppression of bleb formation, locomotion, and polarity of Walker carcinosarcoma cells by hypertonic media correlates with cell volume reduction but not with changes in the F-actin content. Cell. Motil. Cytoskeleton 37 (1997) 326–337. http://dx.doi.org/10.1002/(SICI)1097-0169(1997)37:4<326::AID-CM4>3.0.CO;2-210.1002/(SICI)1097-0169(1997)37:4<326::AID-CM4>3.0.CO;2-2Search in Google Scholar

[12] Schachtschabel, D.O. and Foley, G.E. Serial cultivation of Ehrlich ascites tumor cells in hypertonic media. Exp. Cell Res. 70 (1972) 317–324. http://dx.doi.org/10.1016/0014-4827(72)90142-510.1016/0014-4827(72)90142-5Search in Google Scholar

[13] Korohoda, W. and Stockem, W. Experimentally induced destabilization of the cell membrane and cell surface activity in Amoeba proteus. Cytobiologie (Europ. J. Cell Biol.) 12 (1975) 93–110. Search in Google Scholar

[14] Erickson, G.R., Alexopoulos, L.G. and Guilak F. Hyper-osmotic stress induces volume change and calcium transients in chemocytes by transmembrane, phospholipids, and G-protein pathways. J. Biomech. 34 (2002) 1527–1535. http://dx.doi.org/10.1016/S0021-9290(01)00156-710.1016/S0021-9290(01)00156-7Search in Google Scholar

[15] Yoshida, K. and Inouye, K. Myosin II -dependent cylindrical protrusions induced by quinine in Dictystelium: antagonizing effects of actin polymerization at the leading edge. J. Cell Sci. 114 (2001) Pt 11 2155–2165. 10.1242/jcs.114.11.2155Search in Google Scholar

[16] Franz, C.M., Jones, G.E. and Ridley A.J. Cell migration in development and disease. Dev. Cell 2 (2002) 153–158. http://dx.doi.org/10.1016/S1534-5807(02)00120-X10.1016/S1534-5807(02)00120-XSearch in Google Scholar

[17] Stracke, M.L., Aznavoorian, S.A., Beckner, M.E., Liotta, L.A. and Schiffmann, E. Cell motility, a principal requirement for metastasis. EXS 59 (1991) 147–162. Search in Google Scholar

[18] Condeelis, J., Singer, R.H. and Segall, J.E. The great escape: When cancer cells hijack the genes for chemotaxis and motility. Annu. Rev. Cell. Dev. Biol. 21 (2005) 695–718. http://dx.doi.org/10.1146/annurev.cellbio.21.122303.12030610.1146/annurev.cellbio.21.122303.120306Search in Google Scholar PubMed

[19] Yamaguchi, H. and Condeelis, J. Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim. Biophys. Acta 1773 (2007) 642–652. http://dx.doi.org/10.1016/j.bbamcr.2006.07.00110.1016/j.bbamcr.2006.07.001Search in Google Scholar PubMed PubMed Central

[20] Varani, J. Control of cell motility during tissue invasion. In: Kaiser, H.E. and Nasir, A. editors. Selected Aspects of Cancer progression: Metastasis, Apoptosis and Immune Response. Springer Sci. Buisness Media BV (2008) 11–19. Search in Google Scholar

[21] Korohoda, W., Madeja, Z. and Sroka, J. Diverse chemotactic responses of Dictyostelium discoideum amoebae in the developing (temporal) and stationary (spatial) concentration gradients of folic acid, cAMP, Ca(2+) and Mg(2+). Cell Motil. Cytoskeleton 53 (2002) 1–25. http://dx.doi.org/10.1002/cm.1005210.1002/cm.10052Search in Google Scholar PubMed

[22] Waligórska, A., Wianecka-Skoczeń, M. and Korohoda, W. Motile activities of Dictyostelium discoideum differ from those in Protista or vertebrate animal cells. Folia Biol. (Kraków) 55 (2007) 87–93. http://dx.doi.org/10.3409/17349160778149262310.3409/173491607781492623Search in Google Scholar PubMed

[23] Sroka, J., Kamiński, R., Michalik, M., Madeja, Z., Przestalski, S. and Korohoda, W. The effect of triethyllead on the motile activity of Walker 256 carcinosarcoma cells. Cell. Mol. Biol. Lett. 9 (2004) 15–30. Search in Google Scholar

[24] Bereiter-Hahn, J. and Kajstura, J. Scanning microfluorometric measurement of TRITC-phalloidin labelled F-actin. Dependence of F-actin content on density of normal and transformed cells. Histochemistry 90 (1988) 271–276. http://dx.doi.org/10.1007/BF0049597010.1007/BF00495970Search in Google Scholar PubMed

[25] Kajstura, J. and Bereiter-Hahn, J. Scanning microfluorometric measurement of immunofluorescently labelled microtubules in cultured cells. Dependence of microtubule content on cell density. Histochemistry 88 (1987) 53–55. http://dx.doi.org/10.1007/BF0049016710.1007/BF00490167Search in Google Scholar PubMed

[26] Waligórska, A., Wianecka-Skoczeń, M., Nowak, P. and Korohoda, W. Some difficulties in research into cell motile activity under isotropic conditions. Folia Biol (Krakow) 55 (2007) 9–16. http://dx.doi.org/10.3409/17349160778000639910.3409/173491607780006399Search in Google Scholar

[27] Korohoda, W. and Madeja, Z. Contact of sarcoma cells with aligned fibroblasts accelerates their displacement: computer — assisted analysis of tumor cell locomotion in coculture. Biochem. Cell. Biol. 75 (1997) 263–276. http://dx.doi.org/10.1139/o97-04910.1139/o97-049Search in Google Scholar

[28] Erickson, C.A. and Nuccitelli, R. Embryonic fibroblast motility and orientation can be influenced by physiological electric fields. J. Cell Biol. 98 (1984) 296–307. http://dx.doi.org/10.1083/jcb.98.1.29610.1083/jcb.98.1.296Search in Google Scholar

[29] Wójciak-Stothard, B., Madeja, Z., Korohoda, W., Curtis, A.S.G. and Wilkinson, H. Activation of macrophage-like cells by multiple grooved substrata. Topographical control of cell behaviour. Cell Biol. Int. 19 (1995) 485–490. http://dx.doi.org/10.1006/cbir.1995.109210.1006/cbir.1995.1092Search in Google Scholar

[30] Gail, M. Time lapse studies on the motility of fibroblasts in tissue culture. In: Ciba Found. Symp.14, (Porter, R., Fitzsimons, D.W. Eds.) Locomotion of Tissue Cells. Elsevier, Excperta Medica, North-Holland, Amsterdam, London, New York, (1973) 287–310. Search in Google Scholar

[31] Sroka, J., Kordecka, A., Włosiak, P., Madeja, Z. and Korohoda, W. Separation methods for isolation of human polymorphonuclear leukocytes affect their motile activity. Eur. J. Cell Biol. 88 (2009) 531–539. http://dx.doi.org/10.1016/j.ejcb.2009.05.00510.1016/j.ejcb.2009.05.005Search in Google Scholar

[32] Kruyt, H.R. and Overbeek, J.T.G. An Introduction to Physical Chemistry. W. Heinemann Ltd: London and Tonbridge; 1960. Search in Google Scholar

[33] Barrow, G.M. Physical Chemistry, McGraw-Hill New York, 1961. Search in Google Scholar

[34] Katchalsky, A. and Curran, P.F. Nonequilibrium thermodynamics in biophysics. Harvard University Press, Cambridge, Massachusetts, (1965) 1–248. 10.4159/harvard.9780674494121Search in Google Scholar

[35] Szydłowska, H., Zasporowska, E., Kuszlik-Jochym, K., Korohoda. W. and Branny, J. Membranolytic activity of detergents as studiem with cell viability tests. Folia Histochem. Cytochem. 16 (1978) 69–78. Search in Google Scholar

[36] Ling, G.N. A Physical Theory of the Living State. The Association Induction Hypothesis. Blaisdell Publ. Co. New York; 1962. Search in Google Scholar

[37] Van Duijn, B., Vogelzang, S.A., Ypey, D.L., Van der Molen, L.G. and Van Haastert, P.J. Normal chemotaxis in Dictyostelium discoideum cells with a depolarized plasma membrane potential. J. Cell Sci. 95 (1990) (Pt 1) 177–183. 10.1242/jcs.95.1.177Search in Google Scholar

[38] Wessels, D., Titus, M. and Soll, D.R. A Dictyostelium myosin I plays a crucial role in regulating the frequency of pseudopods formed on the substratum. Cell Motil. Cytoskeleton 33 (1996) 64–79. http://dx.doi.org/10.1002/(SICI)1097-0169(1996)33:1<64::AID-CM7>3.0.CO;2-I10.1002/(SICI)1097-0169(1996)33:1<64::AID-CM7>3.0.CO;2-ISearch in Google Scholar

[39] Stracke, M.L., Aznavoornian, S.A., Beckner, M.E., Liotta, L.A. and Schiffmann E. Cell motility, a principal requirement for metastasis. EXS 59 (1991) 147–162. Search in Google Scholar

[40] Quiñones, L.G. and Garcia-Castro, I. Characterization of human melanoma cell lines according to their migratory properties in vitro. In Vitro Cell. Dev. Biol. Anim. 40 (2004) 35–42. http://dx.doi.org/10.1290/1543-706X(2004)40<35:COHMCL>2.0.CO;210.1290/1543-706X(2004)40<35:COHMCL>2.0.CO;2Search in Google Scholar

[41] Lewis, L., Barrandon, Y., Green, H. and Albrecht-Buehler, G. The reorganization of microtubules and microfilaments in differentiating keratinocytes. Differentiation 36 (1987) 228–233. http://dx.doi.org/10.1111/j.1432-0436.1987.tb00197.x10.1111/j.1432-0436.1987.tb00197.xSearch in Google Scholar

[42] Blasé, C., Becker, D., Kappel, S. and Bereiter-Hahn, J. Microfilament dynamics during HaCat cell volume regulations. Eur. J. Cell Biol. 88 (2009) 131–139. http://dx.doi.org/10.1016/j.ejcb.2008.10.00310.1016/j.ejcb.2008.10.003Search in Google Scholar

[43] Schmitz, H.D. and Bereiter-Hahn, J. GFP associates with microfilaments in fixed cells. Histochem. Cell Biol. 116 (2001) 89–94. Search in Google Scholar

[44] Crowe, J.H., Whittam, M.A., Chapman, D. and Crowe, L.M. Interactions of phospholipids monolayers with carbohydrates. Biochim. Biophys. Acta 769 (1984) 151–159. http://dx.doi.org/10.1016/0005-2736(84)90018-X10.1016/0005-2736(84)90018-XSearch in Google Scholar

[45] Clegg, J.S., Gallo, J. and Gordon, E. Some structural, biochemical and biophysical characteristics of L-929 cells growing in the presence of hyperosmotic sorbitol concentration. Exp. Cell Res. 163 (1986) 35–46. http://dx.doi.org/10.1016/0014-4827(86)90556-210.1016/0014-4827(86)90556-2Search in Google Scholar

[46] Rand, R.P., Parsegian, V.A. and Rau, D.C. Intracellular osmotic action. Cell. Mol. Life Sci. 57 (2000) 1018–1032. http://dx.doi.org/10.1007/PL0000074210.1007/PL00000742Search in Google Scholar

[47] Dall’Asta, V., Bussolati, O., Sala, R., Parolari, A., Alamanni, F., Biglioli, P. and Gazzol G.C. Amino acids are compatible osmolytes for volume recovery after hypertonic shrinkage in vascular endothelial cells. Am. J. Physiol. 276 (1999) C865–872. 10.1152/ajpcell.1999.276.4.C865Search in Google Scholar

[48] Schaffer, S., Takahashi, K. and Azuma J. Role of osmoregulation in the actions of taurine. Amino Acids 19 (2000) 527–546. http://dx.doi.org/10.1007/s00726007000410.1007/s007260070004Search in Google Scholar

[49] Schuster, S.C., Noegel, A.N., Oehme, F., Gerisch, G. and Simon, M.I. The hybrid histone kinase Dok A is part of the osmotic response system of Dictyostelium. EMBO J. 15 (1996) 3880–3889. Search in Google Scholar

[50] Steck, T.L., Chiaraviglio, L. and Meredith, S. Osmotic homeostasis in Dictyostelium discoideyn: excretion of amino acids and ingested solutes. J. Eukaryot. Microbiol. 44 (1997) 503–510. http://dx.doi.org/10.1111/j.1550-7408.1997.tb05731.x10.1111/j.1550-7408.1997.tb05731.xSearch in Google Scholar

[51] Guthrie, H.D., Liu, J. and Crister, J.K. Osmotic tolerance limits and effects of osmoprotectants on motility of bovine spermatozoa. Biol. Reprod. 67 (2002) 1811–1816. http://dx.doi.org/10.1095/biolreprod67.6.181110.1095/biolreprod67.6.1811Search in Google Scholar

[52] Heilbrunn, L.V. and Daugherty, K. The action of sodium, potassium, calcium and magnesium ions on the plasmagel of Amoeba proteus. Physiol. Zool. 5 (1932) 254–274. Search in Google Scholar

[53] Thiel, M., Buessecker, F, Eberhardt, K, Chouker, A., Setzer, F., Kreimeier, U., Arforst, K.E., Peter, K. and Messmer K. Effects of hypertonic saline on expression of human polymorphonuclear leukocyte adhesion molecules. J. Leukoc. Biol. 70 (2001) 261–273. Search in Google Scholar

[54] Bryszewska, M. and Epand, R.M. Effects of sugar alcohols and disaccharides in inducing the hexagonal phase and altering membrane properties: implications for diabetes mellitus. Biochim. Biophys. Acta 943 (1988) 485–492. http://dx.doi.org/10.1016/0005-2736(88)90381-110.1016/0005-2736(88)90381-1Search in Google Scholar

[55] Wyckoff, J.B., Segall, J.E. and Condeelis, J.S. The collection of the motile population of cells from a living tumor. Cancer Res. 60 (2000) 5401–5404. Search in Google Scholar

Published Online: 2011-7-23
Published in Print: 2011-9-1

© 2011 University of Wrocław, Poland

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

Downloaded on 21.5.2024 from https://www.degruyter.com/document/doi/10.2478/s11658-011-0015-y/html
Scroll to top button