Cell volume regulatory ion transport in the regulation of cell migration

Contributions to Nephrology

Volumn 152, Issue , 2006, Pages 161-180

  Jakab, M ^a   Ritter, M ^a  

^a PARACELSUS MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); MEMBRANE PROTEIN; SODIUM PROTON EXCHANGE PROTEIN;

ANIMAL; CELL ADHESION; CELL MEMBRANE PERMEABILITY; CELL MOTION; CELL SIZE; CELL SURVIVAL; CYTOSKELETON; ELECTROLYTE BALANCE; HUMAN; ION TRANSPORT; METABOLISM; MOUSE; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL ADHESION; CELL MEMBRANE PERMEABILITY; CELL MOVEMENT; CELL SIZE; CELL SURVIVAL; CYTOSKELETON; HUMANS; ION TRANSPORT; MEMBRANE PROTEINS; MICE; SIGNAL TRANSDUCTION; SODIUM-HYDROGEN ANTIPORTER; SODIUM-POTASSIUM-EXCHANGING ATPASE; WATER-ELECTROLYTE BALANCE;

EID: 33750562162     PISSN: 03025144     EISSN: None     Source Type: Book Series    
DOI: 10.1159/000096322     Document Type: Review

References (136)

1. Stossel TP: On the crawling of animal cells. Science 1993;260:1086-1094.
2. Vicente-Manzanares M, Webb DJ, Horwitz AR: Cell migration at a glance. J Cell Sci 2005;118:4917-4919.
3. Anand-Apte B, Zetter B: Signaling mechanisms in growth factor-stimulated cell motility. Stem Cells 1997;15:259-267.
4. Bereiter-Hahn J: Mechanics of crawling cells. Med Eng Phys 2005;27:743-753.
5. Hartwig JH: The platelet: form and function. Semin Hematol 2006;43:S94-S100.
6. Singer SJ, Kupfer A: The directed migration of eukaryotic cells. Annu Rev Cell Biol 1986;2:337-365.
7. Cooper HM: Axon guidance receptors direct growth cone pathfinding: rivalry at the leading edge. Int J Dev Biol 2002;46:621-631.
8. Govek EE, Newey SE, Van Aelst L: The role of the Rho GTPases in neuronal development. Genes Dev 2005;19:1-49.
9. Luo L: Actin cytoskeleton regulation in neuronal morphogenesis and structural plasticity. Annu Rev Cell Dev Biol 2002;18:601-635.
10. Prieschl EE, Kulmburg PA, Baumruker T: The nomenclature of chemokines. Int Arch Allergy Immunol 1995;107:475-483.
11. Carlos TM, Harlan JM: Leukocyte-endothelial adhesion molecules. Blood 1994;84:2068-2101.
12. Seely AJ, Pascual JL, Christou NV: Science review: Cell membrane expression (connectivity) regulates neutrophil delivery, function and clearance. Crit Care 2003;7:291-307.
13. Lang F, Busch GL, Ritter M, Volkl H, Waldegger S, Gulbins E, Haussinger D: Functional significance of cell volume regulatory mechanisms. Physiol Rev 1998;78:247-306.
14. Lang F, Busch GL, Ritter M, Völkl H, Waldegger S, Gulbins E, Häussinger D: The functional significance of cell volume regulatory mechanisms. Physiol Rev 1998;78:1-60.
15. Bray D, White JG: Cortical flow in animal cells. Science 1989;239:883-888.
16. Egelhoff TT, Spudich JA: Molecular genetics of cell migration: dictyostelium as a model system. Trends Genet 1991;7:161-166.
17. Lee J, Ishihara A, Jacobson K: How do cells move along surfaces? Trends Cell Biol 1993;3:366-370.
18. Oster GF, Perelson AS: The physics of cell motility. J Cell Sci 1987;8(suppl):35-54.
19. Lauffenburger DA, Horwitz AF: Cell migration: a physically integrated molecular process. Cell 1996;84:359-369.
20. Mitchison TJ, Cramer LP: Actin-based cell motility and cell locomotion. Cell 1996;84:371-379.
21. Condeelis J: Life at the leading edge: the formation of cell protrusions. Annu Rev Cell Biol 1993;9:411-444.
22. Condeelis J: Understanding the cortex of crawling cells: insights from dictyostelium. Trends Cell Biol 1993;3:371-376.
23. Borisy GG, Svitkina TM: Actin machinery: pushing the envelope. Curr Opin Cell Biol 2000;12:104-112.
24. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR: Cell migration: integrating signals from front to back. Science 2003;302:1704-1709.
25. Pollard TD, Borisy GG: Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003;112:453-465.
26. Gaffey CT, Mullins LJ: Ion fluxes during the action potential in Chara. J Physiol 1958;144:505-524.
27. Ghosh M, Song X, Mouneimne G, Sidani M, Lawrence DS, Condeelis JS: Cofilin promotes actin polymerization and defines the direction of cell motility. Science 2004;304:743-746.
28. Theriot JA, Mitchison TJ: Actin microfilament dynamics in locomoting cells. Nature 1991;352:126-131.
29. Small JV, Rohlfs A, Herzog M: Actin and cell movement. Symp Soc Exp Biol 1993;47:57-71.
30. Small JV, Herzog M, Anderson K: Actin filament organization in the fish keratocyte lamellipodium. J Cell Biol 1995;129:1275-1286.
31. Svitkina TM, Borisy GG: Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J Cell Biol 1999;145:1009-1026.
32. Verkman AS: More than just water channels: unexpected cellular roles of aquaporins. J Cell Sci 2005;118:3225-3232.
33. Ponti A, Machacek M, Gupton SL, Waterman-Storer CM, Danuser G: Two distinct actin networks drive the protrusion of migrating cells. Science 2004;305:1782-1786.
34. Jaffe AB, Hall A: Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 2005;21:247-269.
35. Aguado-Velasco C, Bretscher MS: Circulation of the plasma membrane in Dictyostelium. Mol Biol Cell 1999;10:4419-4427.
36. Oberleithner H, Giebisch G, Geibel J: Imaging the lamellipodium of migrating epithelial cells in vivo by atomic force microscopy. Pflugers Arch 1993:425:506-510.
37. Zaidel-Bar R, Ballestrem C, Kam Z, Geiger B: Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells. J Cell Sci 2003:116:4605-4613.
38. Chaves F, Tierno B, Xu D: Neutrophil volume distribution width: a new automated hematologic parameter for acute infection. Arch Pathol Lab Med 2006;130:378-380.
39. + ATPase on cell volume, intracellular pH and migration of human polymorphonuclear leucocytes. Br J Pharmacol 1998;124:627-638.
40. Rosengren S, Henson PM, Worthen GS: Migration-associated volume changes in neutrophils facilitate the migratory process in vitro. Am J Physiol 1994;267:C1623-C1632.
41. Borregaard N, Schwartz JH, Tauber AI: Proton secretion by stimulated neutrophils. Significance of hexose monophosphate shunt activity as source of electrons and protons for the respiratory burst. J Clin Invest 1984;74:455-459.
42. + exchange in human neutrophils: mechanism of activation by chemotactic factors. Biochem Biophys Res Commun 1984;122:755-762.
43. + exchange. J Physiol 2005;567:225-238.
44. Klein M, Seeger P, Schuricht B, Alper SL, Schwab A: Polarization of Na(+)/H(+) and Cl(-)/HCO(3)(-) exchangers in migrating renal epithelial cells. J Gen Physiol 2000;115:599-608.
45. Bereiter-Hahn J, Voth M: Ionic control of locomotion and shape of epithelial cells: II. Role of monovalent cations. Cell Motil Cytoskeleton 1988;10:528-536.
46. + exchanger in metastasis. Nat Rev Cancer 2005;5:786-795.
47. + exchanger-1 induces cytoskeletal changes involving reciprocal RhoA and Racl signaling, resulting in motility and invasion in MDA-MB-435 cells. Breast Cancer Res 2004;6:R616-R628.
48. Lagana A, Vadnais J, Le PU, Nguyen TN, Laprade R, Nabi IR, Noel J: Regulation of the formation of tumor cell pseudopodia by the Na(+)/H(+) exchanger NHE1. J Cell Sci 2000;113(pt 20): 3649-3662.
49. Schwab A: Function and spatial distribution of ion channels and transporters in cell migration. Am J Physiol Renal Physiol 2001;280:F739-F747.
50. 3-cotransport in migration of transformed renal epithelial cells. J Physiol 2005;568:445-458.
51. + channel. A prerequisite for migration of transformed Madin-Darby canine kidney focus cells. J Clin Invest 1994;93:1631-1636.
52. +-ATPases. J Biol Chem 1996;271:15963-15970.
53. + (equivalent) conductance in the plasma membrane of human neutrophils. Proc Natl Acad Sci USA 1991;88:10816-10820.
54. Nanda A, Grinstein S, Curnutte JT: Abnormal activation of H+ conductance in NADPH oxidase-defective neutrophils. Proc Natl Acad of Sci USA 1993;90:760-764.
55. Nanda A, Gukuskaya A, Tseng J, Grinstein S: Activation of vacuolar-type proton pumps by protein kinase C. Role in neutrophil pH regulation. J Biol Chem 1992;267:22740-22746.
56. Leung S, O'Donnell ME, Martinez A, Palfrey HC: Regulation by nerve growth factor and protein phosphorylation of Na/K/2Cl cotransport and cell volume in PC12 cells. J Biol Chem 1994;269:10581-10589.
57. Bray D, Money NP, Harlold FM, Bamburg JR: Responses of growth cones to changes in osmolality of the surrounding medium. J Cell Sci 1991:98:507-515.
58. + exchange: possible role of protein phosphorylation in lymphocyte volume regulation. J Cell Biol 1985;101:269-276.
59. Gallin EK, McKinney L: Monovalent ion transport and membrane potential changes during activation in phagocytic leukocytes. Curr Top Membr Transport 1990;35:127-152.
60. + channel. Proc Natl Acad Sci USA 1998;95:5378-5382.
61. + channel (cIK1) by protein kinase C. J Membr Biol 2002;187:71-79.
62. Schwab A, Reinhardt J, Schneider SW, Gassner B, Schuricht B: K(+) channel-dependent migration of fibroblasts and human melanoma cells. Cell Physiol Biochem 1999;9:126-132.
63. Levite M, Cahalon L, Peretz A, Hershkoviz R, Sobko A, Ariel A, Desai R, Attali B, Lider O: Extracellular K(+) and opening of voltage-gated potassium channels activate T cell integrin function: physical and functional association between Kv1.3 channels and betal integrins. J Exp Med 2000;191:1167-1176.
64. Hendriks R, Morest DK, Kaczmarek LK: Role in neuronal cell migration for high-threshold potassium currents in the chicken hindbrain. J Neurosci Res 1999;58:805-814.
65. + release during migration of transformed Madin-Darby canine kidney cells. Pflugers Arch 1996;433:71-76.
66. + channel activity in transformed Madin-Darby kidney cells. J Clin Invest 1993;92:218-223.
67. Schneider SW, Oberleithner H, Schillers H, Schwab A: Volume dynamics in migrating epithelial cells imaged with the atomic force microscopy. Pflugers Arch 1998;435(suppl):R61.
68. Schwab A, Gabriel K, Finsterwalder F, Folprecht G, Greger R, Kramer A, Oberleithner H: Polarized ion transport during migration of transformed Madin-Darby canine kidney cells. Pflugers Arch 1995;430:802-807.
69. Ritter M, Wöll E: Modification of cellular ion transport by Ha-ras oncogene expression: Stept towards malignant transformation. Cell Physiol Biochem 1996;6:245-270.
70. Brundage RA, Fogarty KE, Tuft RA, Fay FS: Calcium gradients underlying polarization and chemotaxis of eosinophils. Science 1991;254:703-706.
71. Menegazzi R, Busetto S, Dri P, Cramer R, Patriarca P: Chloride ion efflux regulate adherence, spreading, and respiratory burst of neutrophils stimulated by tumor necrosis factor-alpha (TNF) on biologic surfaces. J Cell Biol 1996;135:511-522.
72. Shimizu Y, Daniels RH, Elmore MA, Finnen MJ, Hill ME, Lackie JM: Agonist-stimulated Cl-efflux form human neutrophils. Biochem Pharmacol 1993;45:1743-1751.
73. Moreland JG, Davis AP, Bailey G, Nauseef WM, Lamb FS: Anion channels including CLC-3 are required for normal neutrophil oxidative function, phagocytosis, and transendothelial migration. J Biol Chem 2006;281:12277-12288.
74. Kim MJ, Cheng G, Agrawal DK: Cl-channels are expressed in human normal monocytes: a functional role in migration, adhesion and volume change. Clin Exp Immunol 2004;138:453-459.
75. Mao JW, Wang LW, Sun XR, Zhu LY, Li P, Zhong P, Nie SH, Jacob T, Chen LX: Volume-activated Cl-current in migrated nasopharyngeal carcinoma cells. Sheng Li Xue Bao 2004;56:525-530.
76. Mao JW, Wang LW, Jacob T, Sun XR, Li H, Zhu LY, Li P, Zhong P, Nie SH, Chen LX: Involvement of regulatory volume decrease in the migration of nasopharyngeal carcinoma cells. Cell Res 2005;15:371-378.
77. Zierler S, Kerschbaum HH: Blockade of chloride conductance antagonizes PMA-induced ramifi-cation in the murine microglial cell line, BV-2. Brain Res 2005;1039:162-170.
78. Ransom CB, O'Neal JT, Sontheimer H: Volume-activated chloride currents contribute to the resting conductance and invasive migration of human glioma cells. J Neurosci 2001;21:7674-7683.
79. Soroceanu L, Manning TJ Jr, Sontheimer H: Modulation of glioma cell migration and invasion using Cl(-) and K(+) ion channel blockers. J Neurosci 1999;19:5942-5954.
80. McFerrin MB, Sontheimer H: A role for ion channels in glioma cell invasion. Neuron Glia Biol 2006;2:39-49.
81. Bennett JS: Structure and function of the platelet integrin alphaIIbbeta3. J Clin Invest 2005;115:3363-3369.
82. Furst J, Botta G, Saino S, Dopinto S, Gandini R, Dossena S, Vezzoli V, Rodighiero S, Bazzini C, Garavaglia ML, Meyer G, Jakab M, Ritter M, Wappl-Kornherr E, Paulmichl M: The ICln interactome. Acta Physiol 2006;187:43-49.
83. Larkin D, Murphy D, Reilly DF, Cahill M, Sattler E, Harriott P, Cahill DJ, Moran N: ICln, a novel integrin alphaIIbbeta3-associated protein, functionally regulates platelet activation. J Biol Chem 2004;279:27286-27293.
84. Furst J, Gschwentner M, Ritter M, Botta G, Jakab M, Mayer M, Garavaglia L, Bazzini C, Rodighiero S, Meyer G, Eichmuller S, Woll E, Paulmichl M: Molecular and functional aspects of anionic channels activated during regulatory volume decrease in mammalian cells. Pflugers Arch 2002;444:1-25.
85. Jakab M, Grundbichler M, Benicky J, Ravasio A, Chwatal S, Schmidt S, Strbak V, Fürst J, Paulmichl M, Ritter M: Glucose induces anion conductance and cytosol to membrane transposition of ICln in INS-1E rat insulinoma cells. Cell Physiol Biochem 2006;18:21-34.
86. Ritter M, Ravasio A, Jakab M, Chwatal S, Furst J, Laich A, Gschwentner M, Signorelli S, Burtscher C, Eichmuller S, Paulmichl M: Cell swelling stimulates cytosol to membrane transposition of ICln. J Biol Chem 2003;278:50163-50174.
87. Mandeville JTH, Ghosh RN, Maxfield FR: Intracellular calcium levels correlate with speed and persistent forward motion in migrating neutrophils. Biophys J 1995;68:1207-1217.
88. Ritter M: Cell volume regulatory ion transport in cell migration. Contrib Nephrol 1998;123:135-157.
89. 2+. Trends Cell Biol 1993;3:386-391.
90. i and cell shape, polarity, and locomotion by InsP3, DAG, and protein kinase C in newt eosinophils. J Cell Biol 1994;127:489-503.
91. Hahn K, DeBiasio R, Taylor L: Patterns of elevated free calcium and calmodulin activation in living cells. Nature 1992;359:736-738.
92. 2+ distribution in migrating transformed epithelial cells. Pflugers Arch 1997;434:70-76.
93. 2+ fluctuations. J Neurobiol 1998;37:110-130.
94. 2+ entry into Mardin-Darby canine kidney-focus (MDCK-F) cells. Pflugers Arch 1994;426:95-100.
95. Omann GM, Porasik MM, Sklar LA: Oscillating actin polymerization/ depolymerization responses in human polymorhonuclear leucocytes. J Biol Chem 1989;264:16355-16358.
96. Downey GP, Grinstei S, Sue-A-Quan A, Czaban B, Chan CK: Volume regulation in leukocytes: requirement for an intact cytoskeleton. J Cell Physiol 1995;163:96-104.
97. Wenzel-Seifert K, Lentzen H, Aktories K, Seifert R: Complex regulation of human neutrophil activation by actin filaments: dihydrocytochalasin B and botulinum C2 toxin uncover the existence of multiple cation entry pathways. J Leukoc Biol 1997:61:703-711.
98. + antiport: assessment of effects on intracellular pH. EMBO J 1993;12:5209-5218.
99. + antiporter. Analysis of phosphorylation and subcellular localization. J Biol Chem 1994;269:8741-8748.
100. Hsu LS, Becker EL: Volume changes induced in rabbit polymorphonuclear leukocytes by chemotactic factor and cytochalasin B. Am J Pathol 1975;81:1-14.
101. Ritter M, Wöll E, Häusslinger D, Lang F: Effects of bradykinin on cell volume and intracellular pH in NIH 3T3 fibroblasts expressing the ras oncogene. FEBS Lett 1992;307:367-370.
102. +-exchanger in NIH 3T3 fibroblasts expressing the Ha-ras oncogene requires stimulated calcium influx and is associated with rearrangement of the actin cytoskeleton. Eur J Cell Biol 1997;72:222-228.
103. Ritter M, Fuerst J, Woll E, Chwatal S, Gschwentner M, Lang F, Deetjen P, Paulmichl M: Na(+)/H(+)exchangers: linking osmotic dysequilibrium to modified cell function. Cell Physiol Biochem 2001;11:1-18.
104. + channel modulation of actin cytoskeleton and cell volume. Pflugers Arch 1999;438:330-337.
105. 2+ transport across the plasma membrane for cell migration. Cell Physiol Biochem 2005;16:119-126.
106. Kaneider NC, Egger P, Wiedermann FJ, Ritter M, Woll E, Wiedermann CJ: Involvement of cyclic adenosine monophosphate-dependent protein kinase A and pertussis toxin-sensitive G proteins in the migratory response of human CD14+ mononuclear cells to katacalcin. J Bone Miner Res 2002;17:1872-1882.
107. + exchange in Caco-2 cells by a mechanism which is dependent on F-actin. J Biol Chem 1992;267:956-962.
108. Cantiello HF, Prat AG, Bonventre JV, Cunningham CC, Hartwig JH, Ausiello DA: Actin-binding protein contributes to cell volume regulatory ion channel activation in melanoma cells. J Biol Chem 1993;268:4596-4599.
109. Okada Y: Volume expansion-sensing outward-rectifier Cl- channel: fresh start to the molecular identity and volume sensor. Am J Physiol 1997;273:C755-C789.
110. Simchowitz S, Bibb JA: Functional analysis of the modes of anion transport in neutrophils and hL-60 cells. Annu Rev Physiol 1990;52:381-397.
111. Jessen F, Hoffmann EK: Activation of the Na-K-2Cl cotransport system by reorganization of the actin filaments in ehrlich ascites tumor cells. Biochim Biophys Acta 1992;1110:199-201.
112. Matthews JB, Smith JA, Tally KJ, Awtrey CS, Nguyen H, Rich J, Madara JL: Na-K-2Cl cotransport in intestinal epithelial cells. Influence of chloride efflux and F-action on regulation of cotransporter activity and bumetanide binding. J Biol Chem 1994;269:15703-15709.
113. Vriens J, Janssens A, Prenen J, Nilius B, Wondergem R: TRPV channels and modulation by hepatocyte growth factor/scatter factor in human hepatoblastoma (HepG2) cells. Cell Calcium 2004;36:19-28.
114. Liu X, Bandyopadhyay BB, Nakamoto T, Singh BB, Liedtke W, Melvin JE, Ambudkar IS: A role for AQP5 in activation of TRPV4 by hypotonicity: concerted involvement of AQP5 and TRPV4 in regulation of cell volume recovery. J Biol Chem 2006;281:15485-15495.
115. Verkman AS: Aquaporins in endothelia. Kidney Int 2006;69:1120-1123.
116. Webb DJ, Donais K, Whitmore LA, Thomas SM, Turner CE, Parsons JT, Horwitz AF: FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat Cell Biol 2004;6:154-161.
117. van Buul JD, Hordijk PL: Signaling in leukocyte transendothelial migration. Arterioscler Thromb Vasc Biol 2004;24:824-833.
118. Small JV, Anderson K, Rottner K: Actin and the coordination of protrusion, attachment and retraction in cell crawling. Biosci Rep 1996;16:351-368.
119. Beningo KA, Dembo M, Kaverina I, Small JV, Wang YL: Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. J Cell Biol 2001;153:881-888.
120. Lawson MA, Maxfield FR: Ca(2+)- and calcineurin-dependent recycling of an integrin to the front of migrating neutrophils. Nature 1995;377:75-79.
121. Demaurex N, Downey GP, Waddell TK, Grinstein S: Intracellular pH regulation during spreading of human neutrophils. J Cell Biol 1996;133:1391-1402.
122. Ingber DE, Prusty D, Frangioni JV, Cragoe EJJ, Lechene C, Schwartz MA: Control of intracellular pH and growth by fibronectin in capillary endothelial cells. J Cell Biol 1990;110:1803-1811.
123. Schwartz MA, Both G, Lechene C: Effect of cell spreading on cytoplasmic pH in normal and transformed fibroblasts. Proc Natl Acad Sci USA 1989;1989:4525-4529.
124. Schwartz MA, ingber DE, Lawrence M, Springer TA, Lechene C: Multiple integrins share the ability to induce elevation of intracellular pH. Exp Cell Res 1991;195:533-535.
125. Schwartz MA, Lechene C, Ingber DE: Insoluble fibronectin activates the Na/H antiporter by clustering immobilizing integrin o5β, independent of cell shape. Proc Natl Acad Sci USA 1991;88:7849-7853.
126. Tominaga T, Barber DL: Na-H exchange acts downstream of RhoA to regulate integrin-induced cell adhesion and spreading. Mol Biol Cell 1998;9:2287-2303.
127. Denker SP, Barber DL: Cell migration requires both ion translocation and cytoskeletal anchoring by the Na-H exchanger NHE1. J Cell Biol 2002;159:1087-1096.
128. Denker SP, Huang DC, Orlowski J, Furthmayr H, Barber DL: Direct binding of the Na-H exchanger NHE1 to ERM proteins regulates the cortical cytoskeleton and cell shape independently of H(+) translocation. Mol Cell 2000;6:1425-1436.
129. + exchanger (NHE1) creates acidic microenvironments leading to hyaluronidase-2 and cathepsin B activation and breast tumor cell invasion. J Biol Chem 2004;279:26991-27007.
130. Pedersen SF: The Na(+)/H(+) exchanger NHE1 in stress-induced signal transduction: implications for cell proliferation and cell death. Pflugers Arch 2006;452:249-259.
131. Tilly BC, Edixhoven ML, Tertoolen LGJ, Morii N, Narumiya S, de Jonge HR: Activation of the osmosensitive chloride conductance involves the p21rho signalling cascade and is accompanied by a transient reorganization of the F-actin cytoskeleton. Mol Biol Cell 1996;7:1419-1427.
132. Walsh KB, Zhang J: Regulation of cardiac volume-sensitive chloride channel by focal adhesion kinase and Src kinase. Am J Physiol Heart Circ Physiol 2005;289:H2566-H2574.
133. Melmed Rn, Karanian PJ, Berlin Rd: Control of cell volume in the J774 macrophage by micro-tubule disassembly and cyclic AMP. J Cell Biol 1981;90:761-768.
134. Schwab A: Ion channels and transporters on the move. News Physiol Sci 2001;16:29-33.
135. Schwab A, Wulf A, Schulz C, Kessler W, Nechyporuk-Zloy V, Romer M, Reinhardt J, Weinhold D, Dieterich P, Stock C, Hebert SC: Subcellular distribution of calcium-sensitive potassium channels (IK1) in migrating cells. J Cell Physiol 2006;206:86-94.
136. Schneider SW, Pagel P, Rotsch C, Danker T, Oberleithner H, Radmacher M, Schwab A: Volume dynamics in migrating epithelial cells measured with atomic force microscopy. Pflugers Arch 2000;439:297-303.