Volume regulation of murine T lymphocytes relies on voltage-dependent and two-pore domain potassium channels

Biochimica et Biophysica Acta - Biomembranes

Volumn 1808, Issue 8, 2011, Pages 2036-2044

  Bobak, Nicole ^a   Bittner, Stefan ^a   Andronic, Joseph ^b   Hartmann, Susanne ^b   Mühlpfordt, Friederike ^b   Schneider Hohendorf, Tilman ^a   Wolf, Karen ^b   Schmelter, Carsten ^b   Göbel, Kerstin ^a   Meuth, Patrick ^a   Zimmermann, Heiko ^c,d   Döring, Frank ^b   Wischmeyer, Erhard ^b   Budde, Thomas ^a   Wiendl, Heinz ^a   Meuth, Sven G ^a   Sukhorukov, Vladimir L ^b  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c FRAUNHOFER INSTITUTE FOR BIOMEDICAL ENGINEERING   (Germany)

^d SAARLAND UNIVERSITY   (Germany)

Author keywords

Cell volumetry; K2P channels; Osmotic stress; Potassium channel; Regulatory volume decrease; T lymphocyte

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM ACTIVATED POTASSIUM CHANNEL KCA3.1; POTASSIUM CHANNEL; POTASSIUM CHANNEL BLOCKING AGENT; POTASSIUM CHANNEL K2P; POTASSIUM CHANNEL KV1.3; POTASSIUM CHANNEL TASK1; POTASSIUM CHANNEL TASK2; POTASSIUM CHANNEL TASK3; POTASSIUM CHANNEL TRESK; QUINIDINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL VOLUME; CONTROLLED STUDY; GENE INACTIVATION; HOMEOSTASIS; MOUSE; NONHUMAN; OSMOREGULATION; OSMOTIC STRESS; PRIORITY JOURNAL; T LYMPHOCYTE; WILD TYPE;

ANIMALS; CELL SIZE; CELLS, CULTURED; HYPOTONIC SOLUTIONS; KV1.3 POTASSIUM CHANNEL; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS; POTASSIUM CHANNELS, TANDEM PORE DOMAIN; SALINE SOLUTION, HYPERTONIC; T-LYMPHOCYTES; TIME FACTORS; WATER-ELECTROLYTE BALANCE;

MURINAE;

EID: 79958131026     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.04.013     Document Type: Article

References (48)

1. F. Lang, G.L. Busch, M. Ritter, H. Völkl, S. Waldegger, E. Gulbins, and D. Häussinger Functional significance of cell volume regulatory mechanisms Physiol. Rev. 78 1998 247 306 (Pubitemid 28070981)
2. F. Lang, G.L. Busch, and H. Völkl The diversity of volume regulatory mechanisms Cell. Physiol. Biochem. 8 1998 1 45 (Pubitemid 28044155)
3. E.K. Hoffmann, I.H. Lambert, and S.F. Pedersen Physiology of cell volume regulation in vertebrates Physiol. Rev. 89 2009 193 277
4. M.D. Cahalan, and K.G. Chandy The functional network of ion channels in T lymphocytes Immunol. Rev. 231 2009 59 87
5. S. Grinstein, C.A. Clarke, A. Dupre, and A. Rothstein Volume-induced increase of anion permeability in human lymphocytes J. Gen. Physiol. 80 1982 801 823 (Pubitemid 13202189)
6. R.S. Lewis, P.E. Ross, and M.D. Cahalan Chloride channels activated by osmotic stress in T lymphocytes J. Gen. Physiol. 101 1993 801 826 (Pubitemid 23175827)
7. M.D. Cahalan, H. Wulff, and K.G. Chandy Molecular properties and physiological roles of ion channels in the immune system J. Clin. Immunol. 21 2001 235 252 (Pubitemid 32652595)
8. C. Deutsch, and L.Q. Chen Heterologous expression of specific K + channels in T lymphocytes: functional consequences for volume regulation Proc. Natl. Acad. Sci. U. S. A. 90 1993 10036 10040 (Pubitemid 23328246)
9. S.C. Lee, M. Price, M.B. Prystowsky, and C. Deutsch Volume response of quiescent and interleukin 2-stimulated T-lymphocytes to hypotonicity Am. J. Physiol. 254 1988 C286 C296
10. S. Grinstein, and J.D. Smith Calcium-independent cell volume regulation in human lymphocytes. Inhibition by charybdotoxin J. Gen. Physiol. 95 1990 97 120 (Pubitemid 20030339)
11. 2+ induces charybdotoxin- sensitive membrane potential changes in rat lymphocytes Am. J. Physiol. 257 1989 C197 C206
12. R. Khanna, M.C. Chang, W.J. Joiner, L.K. Kaczmarek, and L.C. Schlichter hSK4/hIK1, a calmodulin-binding KCa channel in human T lymphocytes. Roles in proliferation and volume regulation J. Biol. Chem. 274 1999 14838 14849
13. 2+ signalling induced by osmotic shock in human T lymphocytes Exp. Cell Res. 215 1994 211 222
14. 2+ influx pathways mediated by swelling or stores depletion in mouse thymocytes J. Gen. Physiol. 106 1995 415 444
15. + channel in T cells J. Biol. Chem. 267 1992 20971 20979
16. R.S. Lewis, and M.D. Cahalan Subset-specific expression of potassium channels in developing murine T lymphocytes Science 239 1988 771 775 (Pubitemid 18070930)
17. M.D. Cahalan, and K.G. Chandy Ion channels in the immune system as targets for immunosuppression Curr. Opin. Biotechnol. 8 1997 749 756 (Pubitemid 27517253)
18. 2+-inhibited cation (MIC) channels J. Gen. Physiol. 119 2002 487 507 (Pubitemid 34522292)
19. T. Numata, T. Shinizu, and Y. Okada TRPM7 is a stretch- and swelling-activated cation channel involved in volume regulation in human epithelial cells Am. J. Physiol. Cell Physiol. 292 2007 C460 C467
20. J.J. García, R. Sánchez Olea, and H. Pasantes-Morales Taurine release associated to volume regulation in rabbit lymphocytes J. Cell. Biochem. 45 1991 207 212
21. V.L. Sukhorukov, D. Imes, M.W. Woellhaf, J. Andronic, M. Kiesel, R. Shirakashi, U. Zimmermann, and H. Zimmermann Pore size of swelling-activated channels for organic osmolytes in Jurkat lymphocytes, probed by differential polymer exclusion Biochim. Biophys. Acta 1788 2009 1841 1850
22. M. Kiesel, R. Reuss, J. Endter, D. Zimmermann, H. Zimmermann, R. Shirakashi, E. Bamberg, U. Zimmermann, and V.L. Sukhorukov Swelling-activated pathways in human T-lymphocytes studies by cell volumetry and electrorotation Biophys. J. 90 2006 4720 4729 (Pubitemid 43830916)
23. 2P5.1 potassium channels in multiple sclerosis Ann. Neurol. 68 2010 58 69
24. S.G. Meuth, S. Bittner, P. Meuth, O.J. Simon, T. Budde, and H. Wiendl TWIK-related acid-sensitive K + channel 1 (TASK1) and TASK3 critically influence T lymphocyte effector functions J. Biol. Chem. 283 2008 14559 14570
25. I.I. Pottosin, E. Bonales-Alatorre, G. Valencia-Cruz, M.L. Mendoza-Magaña, and O.R. Dobrovinskaya TRESK-like potassium channels in leukemic T cells Pflugers Arch. 456 2008 1037 1048
26. v1.3 channels mediate potassium efflux in the early phase of apoptosis in Jurkat T lymphocytes Am. J. Physiol. Cell Physiol. 297 2009 C1544 C1553
27. + channel in mouse B cells as TREK-2 Am. J. Physiol. Cell Physiol. 297 2009 C188 C197
28. + channels constitute a significant component of background potassium currents in murine dorsal root ganglion neurones J. Physiol. 15 2007 867 879 (Pubitemid 350278721)
29. D.K. Mulkey, E.M. Talley, R.L. Stornetta, A.R. Siegel, G.H. West, X. Chen, N. Sen, A.M. Mistry, P.G. Guyenet, and D.A. Bayliss TASK channels determine pH sensitivity in select respiratory neurons but do not contribute to central respiratory chemosensitivity J. Neurosci. 19 2007 4049 4058
30. H. Barriere, R. Belfodil, I. Rubera, M. Tauc, F. Lesage, C. Poujeol, N. Guy, J. Barhanin, and P. Poujeol Role of TASK2 potassium channels regarding volume regulation in primary cultures of mouse proximal tubules J. Gen. Physiol. 122 2003 177 190 (Pubitemid 37064683)
31. A.D. Lúcio, R.A. Santos, and O.N. Mesquita Measurements and modeling of water transport and osmoregulation in a single kidney cell using optical tweezers and videomicroscopy Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 68 2003 041906
32. S. Grinstein, A. Rothstein, B. Sarkadi, and E.W. Gelfand Responses of lymphocytes to anisotonic media: volume-regulating behavior Am. J. Physiol. 246 1984 C204 C215
33. Ca1: a potential immunosuppressant Proc. Natl. Acad. Sci. U. S. A. 97 2000 8151 8156 (Pubitemid 30460788)
34. S.G. Meuth, M.I. Aller, T. Munsch, T. Schuhmacher, T. Seidenbecher, P. Meuth, C. Kleinschnitz, H.C. Pape, H. Wiendl, W. Wisden, and T. Budde The contribution of TWIK-related acid-sensitive K+-containing channels to the function of dorsal lateral geniculate thalamocortical relay neurons Mol. Pharmacol. 69 2006 1468 1476
35. + channels as targets for specific immunomodulation Trends Pharmacol. Sci. 25 2004 280 289 (Pubitemid 38553830)
36. G.A. Gutman, K.G. Chandy, S. Grissmer, M. Lazdunski, D. McKinnon, L.A. Pardo, G.A. Robertson, B. Rudy, M.C. Sanguinetti, W. Stühmer, and X. Wang International Union of Pharmacology. LIII. Nomenclature and molecular relationships of voltage-gated potassium channels Pharmacol. Rev. 57 2005 473 508 (Pubitemid 43036437)
37. H. Barriere, R. Belfodil, I. Rubera, M. Tauc, F. Lesage, C. Poujeol, N. Guy, J. Barhanin, and P. Poujeol Role of TASK2 potassium channels regarding volume regulation in primary cultures of mouse proximal tubules J. Gen. Physiol. 122 2003 177 190 (Pubitemid 37064683)
38. S. L'Hoste, M. Poet, C. Duranton, R. Belfodil, H. é Barriere, I. Rubera, M. Tauc, C. Poujeol, J. Barhanin, and P. Poujeol Role of TASK2 in the control of apoptotic volume decrease in proximal kidney cells J. Biol. Chem. 282 2007 36692 36703
39. T.G. Cooper, and C.H. Yeung Involvement of potassium and chloride channels and other transporters in volume regulation by spermatozoa Curr. Pharm. Des. 13 2007 3222 3230 (Pubitemid 350201698)
40. + channel TASK-2 (KCNK5) by changes in cell volume J. Biol. Chem. 276 2001 43166 43174
41. + conductance activated during regulatory volume decrease. The channels in Ehrlich cells and their possible molecular counterpart Comp. Biochem. Physiol. A Mol. Integr. Physiol. 130 2001 565 575 (Pubitemid 32972006)
42. + channels in the human leukemic T cell line, Jurkat FEBS Lett. 469 2000 192 202
43. P. Launay, H. Cheng, S. Srivatsan, R. Penner, A. Fleig, and J.P. Kinet TRPM4 regulates calcium oscillations after T cell activation Science 306 2004 1374 1377 (Pubitemid 39532514)
44. A. Beck, M. Kolisek, L.A. Bagley, A. Fleig, and R. Penner Nicotinic acid adenine dinucleotide phosphate and cyclic ADP-ribose regulate TRPM2 channels in T lymphocytes FASEB J. 20 2006 962 964
45. V.L. Sukhorukov, R. Reuss, D. Zimmermann, C. Held, K.J. Müller, M. Kiesel, P. Gessner, A. Steinbach, W.A. Schenk, E. Bamberg, and U. Zimmermann Surviving high-intensity field pulses: strategies for improving robustness and performance of electrotransfection and electrofusion J. Membr. Biol. 206 2005 187 201 (Pubitemid 43199137)
46. V.L. Sukhorukov, R. Reuss, J. Endter, S. Fehrmann, A. Katsen-Globa, P. Geβner, A. Steinbach, K.J. Müller, A. Karpas, U. Zimmermann, and H. Zimmermann A biophysical approach to the optimisation of dendritic-tumour cell electrofusion Biochem. Biophys. Res. Commun. 346 2006 829 839
47. R. Shirakashi, R. Reuss, J. Ludwig, F. Ehrhart, U. Zimmermann, and V.L. Sukhorukov Introduction of lyo- and cryoprotective carbohydrates into mammalian cells through swelling-activated channels Trans. Japan Soc. Mech. Eng. B71 2005 901 907 (Pubitemid 40749602)
48. S.M. Zeisberger, J.C. Schulz, M. Mairhofer, P. Ponsaerts, G. Wouters, D. Doerr, A. Katsen-Globa, M. Ehrbar, J. Hescheler, S.P. Hoerstrup, A.H. Zisch, A. Kolbus, and H. Zimmermann Biological and physicochemical characterization of a serum- and xeno-free chemically defined cryopreservation procedure for adult human progenitor cells Cell Transplant. 2010 doi:10.3727/096368910X547426