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. 2011 May 25;16(3):412–430. doi: 10.2478/s11658-011-0015-y

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 1,✉, Magdalena Kucia 1,2, Ewa Wybieralska 1, Magdalena Wianecka-Skoczeń 1, Agnieszka Waligórska 1,3, Justyna Drukała 1, Zbigniew Madeja 1
PMCID: PMC6275904  PMID: 21614489

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.

Key words: Cell motility activation, Hypertonicity, Solute-dependent, Membrane interaction

Full Text

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Abbreviations used

BSS

balanced salt solution

CME

coefficient of movement efficiency

EGTA

ethylene glycol bis(β-aminoethyl ether)-N,N-tetraacetic acid

HTB-140

human melanoma cell line

SEM

standard error of the mean

TRITC

tetramethyl rhodamine iso-thiocyanate

References

  • 1.Zischka H., Oehme F., Pintsch T., Ott A., Keller H., Kellermann J., Schuster S.C. Rearrangement of cortex proteins constitutes and osmoprotective mechanism in Dictyostelium. EMBO J. 1999;18:4241–4249. doi: 10.1093/emboj/18.15.4241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Erickson G.R., Alexopoulos L.G., Guilak F. Hyper-osmotic stress induces volume change and calcium transients in chondrocytes by transmembrane, phospholipids, and G-protein pathways. J. Biomech. 2001;34:1527–1535. doi: 10.1016/S0021-9290(01)00156-7. [DOI] [PubMed] [Google Scholar]
  • 3.Cai Q., Michea L., Andrews P., Zhang Z., Rocha G., Dmitrieva N., Burg M.B. Rate of increase of osmolarity determined osmotic tolerance of mouse inner medullary epithelial cells. Am. J. Physiol. Renal Physiol. 2002;283:F792–798. doi: 10.1152/ajprenal.00046.2002. [DOI] [PubMed] [Google Scholar]
  • 4.Mavrogonatou E., 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. 2009;8:930–943. doi: 10.1016/j.dnarep.2009.05.005. [DOI] [PubMed] [Google Scholar]
  • 5.Kerwin A.J., Schinco M.A., Tepas J.J., Renfro W.H., Vitarbo E.A., 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. 2009;67:277–282. doi: 10.1097/TA.0b013e3181acc726. [DOI] [PubMed] [Google Scholar]
  • 6.Loram L., Horwitz E., Bentlley A. Gender and site of injection do not influence intensity of hypertonic saline-induced muscle pain in healthy volunteers. Man Ther. 2009;14:526–530. doi: 10.1016/j.math.2008.09.002. [DOI] [PubMed] [Google Scholar]
  • 7.Vinzenzi R., Cepeda L.A., Pirani W.M., Sannomyia P., Rocha-e-Silvia M., 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. 2009;198:407–414. doi: 10.1016/j.amjsurg.2009.01.017. [DOI] [PubMed] [Google Scholar]
  • 8.Burg M.B., Kwon E.D., Kültz D. Regulation of gene expression by hypertonicity. Annu. Rev. Physiol. 1997;59:437–455. doi: 10.1146/annurev.physiol.59.1.437. [DOI] [PubMed] [Google Scholar]
  • 9.Maallem S., Wierinckx A., Lachuer J., Kwon M.H., Tappaz M.L. Gene expression profiling in brain following acute systemic hypertonicity: novel genes possibly involved in osmoadaptation. J. Neurochem. 2008;105:1198–1211. doi: 10.1111/j.1471-4159.2008.05222.x. [DOI] [PubMed] [Google Scholar]
  • 10.Oster G.F., Perelson A.S. The physics of cell motility. J. Cell Sci. 1987;Suppl.8:35–54. doi: 10.1242/jcs.1987.supplement_8.3. [DOI] [PubMed] [Google Scholar]
  • 11.Fedier A., 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. 1997;37:326–337. doi: 10.1002/(SICI)1097-0169(1997)37:4<326::AID-CM4>3.0.CO;2-2. [DOI] [PubMed] [Google Scholar]
  • 12.Schachtschabel D.O., Foley G.E. Serial cultivation of Ehrlich ascites tumor cells in hypertonic media. Exp. Cell Res. 1972;70:317–324. doi: 10.1016/0014-4827(72)90142-5. [DOI] [PubMed] [Google Scholar]
  • 13.Korohoda W., Stockem W. Experimentally induced destabilization of the cell membrane and cell surface activity in Amoeba proteus. Cytobiologie (Europ. J. Cell Biol.) 1975;12:93–110. [Google Scholar]
  • 14.Erickson G.R., Alexopoulos L.G., Guilak F. Hyper-osmotic stress induces volume change and calcium transients in chemocytes by transmembrane, phospholipids, and G-protein pathways. J. Biomech. 2002;34:1527–1535. doi: 10.1016/S0021-9290(01)00156-7. [DOI] [PubMed] [Google Scholar]
  • 15.Yoshida K., Inouye K. Myosin II -dependent cylindrical protrusions induced by quinine in Dictystelium: antagonizing effects of actin polymerization at the leading edge. J. Cell Sci. 2001;114:Pt 11 2155–2165. doi: 10.1242/jcs.114.11.2155. [DOI] [PubMed] [Google Scholar]
  • 16.Franz C.M., Jones G.E., Ridley A.J. Cell migration in development and disease. Dev. Cell. 2002;2:153–158. doi: 10.1016/S1534-5807(02)00120-X. [DOI] [PubMed] [Google Scholar]
  • 17.Stracke M.L., Aznavoorian S.A., Beckner M.E., Liotta L.A., Schiffmann E. Cell motility, a principal requirement for metastasis. EXS. 1991;59:147–162. doi: 10.1007/978-3-0348-7494-6_10. [DOI] [PubMed] [Google Scholar]
  • 18.Condeelis J., Singer R.H., Segall J.E. The great escape: When cancer cells hijack the genes for chemotaxis and motility. Annu. Rev. Cell. Dev. Biol. 2005;21:695–718. doi: 10.1146/annurev.cellbio.21.122303.120306. [DOI] [PubMed] [Google Scholar]
  • 19.Yamaguchi H., Condeelis J. Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim. Biophys. Acta. 2007;1773:642–652. doi: 10.1016/j.bbamcr.2006.07.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 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.
  • 21.Korohoda W., Madeja Z., 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. 2002;53:1–25. doi: 10.1002/cm.10052. [DOI] [PubMed] [Google Scholar]
  • 22.Waligórska A., Wianecka-Skoczeń M., Korohoda W. Motile activities of Dictyostelium discoideum differ from those in Protista or vertebrate animal cells. Folia Biol. (Kraków) 2007;55:87–93. doi: 10.3409/173491607781492623. [DOI] [PubMed] [Google Scholar]
  • 23.Sroka J., Kamiński R., Michalik M., Madeja Z., Przestalski S., Korohoda W. The effect of triethyllead on the motile activity of Walker 256 carcinosarcoma cells. Cell. Mol. Biol. Lett. 2004;9:15–30. [PubMed] [Google Scholar]
  • 24.Bereiter-Hahn J., Kajstura J. Scanning microfluorometric measurement of TRITC-phalloidin labelled F-actin. Dependence of F-actin content on density of normal and transformed cells. Histochemistry. 1988;90:271–276. doi: 10.1007/BF00495970. [DOI] [PubMed] [Google Scholar]
  • 25.Kajstura J., Bereiter-Hahn J. Scanning microfluorometric measurement of immunofluorescently labelled microtubules in cultured cells. Dependence of microtubule content on cell density. Histochemistry. 1987;88:53–55. doi: 10.1007/BF00490167. [DOI] [PubMed] [Google Scholar]
  • 26.Waligórska A., Wianecka-Skoczeń M., Nowak P., Korohoda W. Some difficulties in research into cell motile activity under isotropic conditions. Folia Biol (Krakow) 2007;55:9–16. doi: 10.3409/173491607780006399. [DOI] [PubMed] [Google Scholar]
  • 27.Korohoda W., Madeja Z. Contact of sarcoma cells with aligned fibroblasts accelerates their displacement: computer — assisted analysis of tumor cell locomotion in coculture. Biochem. Cell. Biol. 1997;75:263–276. doi: 10.1139/o97-049. [DOI] [PubMed] [Google Scholar]
  • 28.Erickson C.A., Nuccitelli R. Embryonic fibroblast motility and orientation can be influenced by physiological electric fields. J. Cell Biol. 1984;98:296–307. doi: 10.1083/jcb.98.1.296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Wójciak-Stothard B., Madeja Z., Korohoda W., Curtis A.S.G., Wilkinson H. Activation of macrophage-like cells by multiple grooved substrata. Topographical control of cell behaviour. Cell Biol. Int. 1995;19:485–490. doi: 10.1006/cbir.1995.1092. [DOI] [PubMed] [Google Scholar]
  • 30.Gail M. Time lapse studies on the motility of fibroblasts in tissue culture. In: Porter R., Fitzsimons D.W., editors. Locomotion of Tissue Cells. Excperta Medica, North-Holland, Amsterdam, London, New York: Elsevier; 1973. pp. 287–310. [Google Scholar]
  • 31.Sroka J., Kordecka A., Włosiak P., Madeja Z., Korohoda W. Separation methods for isolation of human polymorphonuclear leukocytes affect their motile activity. Eur. J. Cell Biol. 2009;88:531–539. doi: 10.1016/j.ejcb.2009.05.005. [DOI] [PubMed] [Google Scholar]
  • 32.Kruyt H.R., Overbeek J.T.G. An Introduction to Physical Chemistry. London and Tonbridge: W. Heinemann Ltd; 1960. [Google Scholar]
  • 33.Barrow, G.M. Physical Chemistry, McGraw-Hill New York, 1961.
  • 34.Katchalsky A., Curran P.F. Nonequilibrium thermodynamics in biophysics. Cambridge, Massachusetts: Harvard University Press; 1965. pp. 1–248. [Google Scholar]
  • 35.Szydłowska H., Zasporowska E., Kuszlik-Jochym K., Korohoda W., Branny J. Membranolytic activity of detergents as studiem with cell viability tests. Folia Histochem. Cytochem. 1978;16:69–78. [PubMed] [Google Scholar]
  • 36.Ling G.N. A Physical Theory of the Living State. The Association Induction Hypothesis. New York: Blaisdell Publ. Co.; 1962. [Google Scholar]
  • 37.Van Duijn B., Vogelzang S.A., Ypey D.L., Van der Molen L.G., Van Haastert P.J. Normal chemotaxis in Dictyostelium discoideum cells with a depolarized plasma membrane potential. J. Cell Sci. 1990;95(Pt1):177–183. doi: 10.1242/jcs.95.1.177. [DOI] [PubMed] [Google Scholar]
  • 38.Wessels D., Titus M., Soll D.R. A Dictyostelium myosin I plays a crucial role in regulating the frequency of pseudopods formed on the substratum. Cell Motil. Cytoskeleton. 1996;33:64–79. doi: 10.1002/(SICI)1097-0169(1996)33:1<64::AID-CM7>3.0.CO;2-I. [DOI] [PubMed] [Google Scholar]
  • 39.Stracke M.L., Aznavoornian S.A., Beckner M.E., Liotta L.A., Schiffmann E. Cell motility, a principal requirement for metastasis. EXS. 1991;59:147–162. doi: 10.1007/978-3-0348-7494-6_10. [DOI] [PubMed] [Google Scholar]
  • 40.Quiñones L.G., Garcia-Castro I. Characterization of human melanoma cell lines according to their migratory properties in vitro. In Vitro Cell. Dev. Biol. Anim. 2004;40:35–42. doi: 10.1290/1543-706X(2004)40<35:COHMCL>2.0.CO;2. [DOI] [PubMed] [Google Scholar]
  • 41.Lewis L., Barrandon Y., Green H., Albrecht-Buehler G. The reorganization of microtubules and microfilaments in differentiating keratinocytes. Differentiation. 1987;36:228–233. doi: 10.1111/j.1432-0436.1987.tb00197.x. [DOI] [PubMed] [Google Scholar]
  • 42.Blasé C., Becker D., Kappel S., Bereiter-Hahn J. Microfilament dynamics during HaCat cell volume regulations. Eur. J. Cell Biol. 2009;88:131–139. doi: 10.1016/j.ejcb.2008.10.003. [DOI] [PubMed] [Google Scholar]
  • 43.Schmitz H.D., Bereiter-Hahn J. GFP associates with microfilaments in fixed cells. Histochem. Cell Biol. 2001;116:89–94. doi: 10.1007/s004180100293. [DOI] [PubMed] [Google Scholar]
  • 44.Crowe J.H., Whittam M.A., Chapman D., Crowe L.M. Interactions of phospholipids monolayers with carbohydrates. Biochim. Biophys. Acta. 1984;769:151–159. doi: 10.1016/0005-2736(84)90018-X. [DOI] [PubMed] [Google Scholar]
  • 45.Clegg J.S., Gallo J., Gordon E. Some structural, biochemical and biophysical characteristics of L-929 cells growing in the presence of hyperosmotic sorbitol concentration. Exp. Cell Res. 1986;163:35–46. doi: 10.1016/0014-4827(86)90556-2. [DOI] [PubMed] [Google Scholar]
  • 46.Rand R.P., Parsegian V.A., Rau D.C. Intracellular osmotic action. Cell. Mol. Life Sci. 2000;57:1018–1032. doi: 10.1007/PL00000742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47.Dall’Asta V., Bussolati O., Sala R., Parolari A., Alamanni F., Biglioli P., Gazzol G.C. Amino acids are compatible osmolytes for volume recovery after hypertonic shrinkage in vascular endothelial cells. Am. J. Physiol. 1999;276:C865–872. doi: 10.1152/ajpcell.1999.276.4.C865. [DOI] [PubMed] [Google Scholar]
  • 48.Schaffer S., Takahashi K., Azuma J. Role of osmoregulation in the actions of taurine. Amino Acids. 2000;19:527–546. doi: 10.1007/s007260070004. [DOI] [PubMed] [Google Scholar]
  • 49.Schuster S.C., Noegel A.N., Oehme F., Gerisch G., Simon M.I. The hybrid histone kinase Dok A is part of the osmotic response system of Dictyostelium. EMBO J. 1996;15:3880–3889. [PMC free article] [PubMed] [Google Scholar]
  • 50.Steck T.L., Chiaraviglio L., Meredith S. Osmotic homeostasis in Dictyostelium discoideyn: excretion of amino acids and ingested solutes. J. Eukaryot. Microbiol. 1997;44:503–510. doi: 10.1111/j.1550-7408.1997.tb05731.x. [DOI] [PubMed] [Google Scholar]
  • 51.Guthrie H.D., Liu J., Crister J.K. Osmotic tolerance limits and effects of osmoprotectants on motility of bovine spermatozoa. Biol. Reprod. 2002;67:1811–1816. doi: 10.1095/biolreprod67.6.1811. [DOI] [PubMed] [Google Scholar]
  • 52.Heilbrunn L.V., Daugherty K. The action of sodium, potassium, calcium and magnesium ions on the plasmagel of Amoeba proteus. Physiol. Zool. 1932;5:254–274. [Google Scholar]
  • 53.Thiel M., Buessecker F., Eberhardt K., Chouker A., Setzer F., Kreimeier U., Arforst K.E., Peter K., Messmer K. Effects of hypertonic saline on expression of human polymorphonuclear leukocyte adhesion molecules. J. Leukoc. Biol. 2001;70:261–273. [PubMed] [Google Scholar]
  • 54.Bryszewska M., 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. 1988;943:485–492. doi: 10.1016/0005-2736(88)90381-1. [DOI] [PubMed] [Google Scholar]
  • 55.Wyckoff J.B., Segall J.E., Condeelis J.S. The collection of the motile population of cells from a living tumor. Cancer Res. 2000;60:5401–5404. [PubMed] [Google Scholar]

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