Cl− channels in apoptosis

European Biophysics Journal

Volumn 45, Issue 7, 2016, Pages 599-610

  Wanitchakool, Podchanart ^a   Ousingsawat, Jiraporn ^a   Sirianant, Lalida ^a   MacAulay, Nanna ^b   Schreiber, Rainer ^a   Kunzelmann, Karl ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Anoctamin; Apoptosis; Ca2+ activated chloride channels; Cell death; CFTR; Chloride channel; LRRC8A; RVD; TMEM16A; TMEM16F; TMEM16J; TMEM16K; Volume regulation

Indexed keywords

ANOCTAMIN 10; ANOCTAMIN 6; ANOCTAMIN 9; CHLORIDE CHANNEL; CISPLATIN; COMPLEMENTARY DNA; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; GLUTATHIONE; LRRC8 CHANNEL; MEMBRANE PHOSPHOLIPID; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; LRRC8A PROTEIN, HUMAN; MEMBRANE PROTEIN; PHOSPHOLIPID TRANSFER PROTEIN; TMEM16F PROTEIN, HUMAN; WATER;

APOPTOSIS; CELL CULTURE; CELL DEATH; CELL SWELLING; CELL VOLUME; FLOW CYTOMETRY; HUMAN; IMMUNOPRECIPITATION; MEMBRANE CHANNEL; NONHUMAN; OOCYTE; PATCH CLAMP TECHNIQUE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; WATER PERMEABILITY; WESTERN BLOTTING; ANIMAL; CELL CYCLE; ELECTROPHYSIOLOGY; HCT 116 CELL LINE; HEK293 CELL LINE; METABOLISM; OSMOSIS; PERMEABILITY;

ANIMALS; APOPTOSIS; CELL CYCLE; CHLORIDE CHANNELS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; ELECTROPHYSIOLOGICAL PHENOMENA; HCT116 CELLS; HEK293 CELLS; HUMANS; MEMBRANE PROTEINS; OSMOSIS; PERMEABILITY; PHOSPHOLIPID TRANSFER PROTEINS; WATER;

EID: 84976291648     PISSN: 01757571     EISSN: 14321017     Source Type: Journal    
DOI: 10.1007/s00249-016-1140-3     Document Type: Review

References (69)

1. Almaca J, Tian Y, AlDehni F, Ousingsawat J, Kongsuphol P, Rock JR, Harfe BD, Schreiber R, Kunzelmann K (2009) TMEM16 proteins produce volume regulated chloride currents that are reduced in mice lacking TMEM16A. J Biol Chem 284:28571–28578
2. Barriere H, Poujeol C, Tauc M, Blasi JM, Counillon L, Poujeol P (2001) CFTR modulates programmed cell death by decreasing intracellular pH in Chinese hamster lung fibroblasts. Am J Physiol 281:C810–C824
3. − currents in primary cultures of mouse nephron. Am J Physiol Ren Physiol 284:F796–F811
4. Billet A, Hanrahan JW (2013) The secret life of CFTR as a calcium-activated chloride channel. J Physiol 591:5273–5278
5. Braunstein GM, Roman RM, Clancy JP, Kudlow BA, Taylor AL, Shylonsky VG, Jovov B, Peter K, Jilling T, Ismailov II et al (2001) Cystic fibrosis transmembrane conductance regulator facilitates ATP release by stimulating a separate ATP release channel for autocrine control of cell volume regulation. J Biol Chem 276:6621–6630
6. + channels in apoptosis. J Membr Biol 209:3–20
7. Gawenis LR, Franklin CL, Simpson JE, Palmer BA, Walker NM, Wiggins TM, Clarke LL (2003) cAMP inhibition of murine intestinal Na/H exchange requires CFTR-mediated cell shrinkage of villus epithelium. Gastroenterology 125:1148–1163
8. Gottlieb RA, Dosanjh A (1996) Mutant cystic fibrosis transmembrane conductance regulator inhibits acidification and apoptosis in C127 cells: possible relevance to cystic fibrosis. Proc Natl Acad Sci USA 93:3587–3591
9. Grassme H, Jendrossek V, Riehle A, von Kurthy G, Berger J, Schwarz H, Weller M, Kolesnick R, Gulbins E (2003) Host defense against Pseudomonas aeruginosa requires ceramide-rich membrane rafts. Nat Med 9:322–330
10. 2+ activation. J Gen Physiol 141:585–600
11. Gulbins E, Jekle A, Ferlinz K, Grassme H, Lang F (2000) Physiology of apoptosis. Am J Physiol Ren Physiol 279:F605–F615
12. Hammer C, Wanitchakool P, Sirianant L, Papiol S, Monnheimer M, Faria D, Ousingsawat J, Schramek N, Schmitt C, Margos G et al (2015) A coding variant of ANO10, affecting volume regulation of macrophages, is associated with Borrelia seropositivity. Mol Med 21:26–37
13. Hudson VM (2001) Rethinking cystic fibrosis pathology: the critical role of abnormal reduced glutathione (GSH) transport caused by CFTR mutation. Free Radic Biol Med 30:1440–1461
14. − channel in cisplatin-induced apoptosis in human epidermoid cancer cells. J Membr Biol 205:139–145
15. Jentsch TJ (2016) VRACs and other ion channels and transporters in the regulation of cell volume and beyond. Nat Rev Mol Cell Biol 17:293–307
16. Jentsch TJ, Lutter D, Planells-Cases R, Ullrich F, Voss FK (2015) VRAC: molecular identification as LRRC8 heteromers with differential functions. Pflugers Arch 468:385–393
17. Jungas T, Motta I, Duffieux F, Fanen P, Stoven V, Ojcius DM (2002) Glutathione levels and BAX activation during apoptosis due to oxidative stress in cells expressing wild-type and mutant cystic fibrosis transmembrane conductance regulator. J Biol Chem 277:27912–27918
18. Juul CA, Grubb S, Poulsen KA, Kyed T, Hashem N, Lambert IH, Larsen EH, Hoffmann EK (2014) Anoctamin 6 differs from VRAC and VSOAC but is involved in apoptosis and supports volume regulation in the presence of Ca. Pflugers Arch 466:1899–1910
19. 2+-activated anion currents in Ehrlich Lettre ascites cells. J Cell Physiol 210:831–842
20. Kmit A, van Kruchten R, Ousingsawat J, Mattheij NJ, Senden-Gijsbers B, Heemskerk JW, Bevers EM, Kunzelmann K (2013) Calcium-activated and apoptotic phospholipid scrambling induced by Ano6 can occur independently of Ano6 ion currents. Cell Death Dis 25(4):e611
21. Kondratskyi A, Kondratska K, Skryma R, Prevarskaya N (2015) Ion channels in the regulation of apoptosis. Biochim Biophys Acta 1848:2532–2546
22. König J, Schreiber R, Mall M, Kunzelmann K (2002) No evidence for inhibition of ENaC through CFTR mediated release of ATP. Biochim Biophys Acta 1565:17–28
23. Kunzelmann K, Nilius B, Owsianik G, Schreiber R, Ousingsawat J, Sirianant L, Wanitchakool P, Bevers EM, Heemskerk JW (2014) Molecular functions of anoctamin 6 (TMEM16F): a chloride channel, cation channel or phospholipid scramblase? Pflügers Arch 466:407–414
24. 2+ signals: a common theme for TMEM16, Ist2, and TMC. Pflügers Arch 468:475–490
25. Lang F, Hoffmann EK (2012) Role of ion transport in control of apoptotic cell death. Compr Physiol 2:2037–2061
26. Lang F, Foller M, Lang K, Lang P, Ritter M, Vereninov A, Szabo I, Huber SM, Gulbins E (2007) Cell volume regulatory ion channels in cell proliferation and cell death. Methods Enzymol 428:209–225
27. − channel is involved in cisplatin resistance of cancer cells. J Cell Physiol 211:513–521
28. L’hoste S, Chargui A, Belfodil R, Corcelle E, Duranton C, Rubera I, Poujeol C, Mograbi B, Tauc M, Poujeol P (2010) CFTR mediates apoptotic volume decrease and cell death by controlling glutathione efflux and ROS production in cultured mice proximal tubules. Am J Physiol Ren Physiol 298:F435–F453
29. L’hoste S, Chargui A, Belfodil R, Duranton C, Rubera I, Mograbi B, Poujeol C, Tauc M, Poujeol P (2009) CFTR mediates cadmium-induced apoptosis through modulation of ROS level in mouse proximal tubule cells. Free Radic Biol Med 46:1017–1031
30. Linsdell P, Hanrahan JW (1998) Glutathione permeability of CFTR. Am J Physiol 275:C323–C326
31. Maeno E, Ishizaki Y, Kanaseki T, Hazama A, Okada Y (2000) Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis. Proc Natl Acad Sci USA 97:9487–9492
32. Maisonneuve P, Marshall BC, Knapp EA, Lowenfels AB (2013) Cancer risk in cystic fibrosis: a 20-year nationwide study from the United States. J Natl Cancer Inst 105:122–129
33. Martins JR, Faria D, Kongsuphol P, Reisch B, Schreiber R, Kunzelmann K (2011) Anoctamin 6 is an essential component of the outwardly rectifying chloride channel. Proc Natl Acad Sci USA 108:18168–18172
34. Milenkovic A, Brandl C, Milenkovic VM, Jendrike T, Sirianant L, Wanitchakool P, Zimmermann S, Reif CM, Horling F, Schrewe H et al (2015) Bestrophin1 is the volume-regulated anion channel in mouse sperm and human retinal pigment epithelium. Proc Natl Acad Sci USA 112:E2630–E2639
35. Namkung W, Finkbeiner WE, Verkman AS (2010) CFTR-adenylyl cyclase I association is responsible for UTP activation of CFTR in well-differentiated primary human bronchial cell cultures. Mol Biol Cell 21:2639–2648
36. Namkung W, Phuan PW, Verkman AS (2011) TMEM16A inhibitors reveal TMEM16A as a minor component of CaCC conductance in airway and intestinal epithelial cells. J Biol Chem 286:2365–2374
37. Nilius B (2004) Is the volume-regulated anion channel VRAC a “water-permeable” channel? Neurochem Res 29:3–8
38. Noe J, Petrusca D, Rush N, Deng P, VanDemark M, Berdyshev E, Gu Y, Smith P, Schweitzer K, Pilewsky J et al (2009) CFTR regulation of intracellular pH and ceramides is required for lung endothelial cell apoptosis. Am J Respir Cell Mol Biol 41:314–323
39. Okada Y, Shimizu T, Maeno E, Tanabe S, Wang X, Takahashi N (2006) Volume-sensitive chloride channels involved in apoptotic volume decrease and cell death. J Membr Biol 209:21–29
40. Okiyoneda T, Barriere H, Bagdany M, Rabeh WM, Du K, Hohfeld J, Young JC, Lukacs GL (2010) Peripheral protein quality control removes unfolded CFTR from the plasma membrane. Science 329:805–810
41. Ousingsawat J, Wanitchakool P, Kmit A, Romao AM, Jantarajit W, Schreiber S, Kunzelmann K (2015) Anoctamin 6 mediates effects essential for innate immunity downstream of P2X7-receptors in macrophages. Nat Commun 6:6245
42. Pedersen SF, Klausen TK, Nilius B (2015) The identification of VRAC (volume regulated anion channel): an amazing Odyssey. Acta Physiol (Oxf) 213:868–881
43. Planells-Cases R, Lutter D, Guyader C, Gerhards NM, Ullrich F, Elger DA, Kucukosmanoglu A, Xu G, Voss FK, Reincke SM et al (2015) Subunit composition of VRAC channels determines substrate specificity and cellular resistance to Pt-based anti-cancer drugs. EMBO J 34:2993–3008
44. Poulsen KA, Andersen EC, Hansen CF, Klausen TK, Hougaard C, Lambert IH, Hoffmann EK (2010) Deregulation of apoptotic volume decrease and ionic movements in multidrug-resistant tumor cells: role of chloride channels. Am J Physiol Cell Physiol 298:C14–C25
45. Qiu Z, Dubin AE, Mathur J, Tu B, Reddy K, Miraglia LJ, Reinhardt J, Orth AP, Patapoutian A (2014) SWELL1, a plasma membrane protein, is an essential component of volume-regulated anion channel. Cell 157:447–458
46. Rottner M, Tual-Chalot S, Mostefai HA, Andriantsitohaina R, Freyssinet JM, Martinez MC (2011) Increased oxidative stress induces apoptosis in human cystic fibrosis cells. PLoS One 6:e24880
47. Rubera I, Duranton C, Melis N, Cougnon M, Mograbi B, Tauc M (2013) Role of CFTR in oxidative stress and suicidal death of renal cells during cisplatin-induced nephrotoxicity. Cell Death Dis 4:e817
48. Schreiber R, Faria D, Skryabin BV, Rock JR, Kunzelmann K (2014) Anoctamins support calcium-dependent chloride secretion by facilitating calcium signaling in adult mouse intestine. Pflügers Arch 467:1203–1213
49. Shen MR, Droogmans G, Eggermont J, Voets T, Ellory JC, Nilius B (2000) Differential expression of volume-regulated anion channels during cell cycle progression of human cervical cancer cells. J Physiol 529(Pt 2):385–394
50. − channel. Am J Physiol Cell Physiol 304:C748–C759
51. 2+, phospholipase A2, osmosensing. Pflügers Arch 468:335–349
52. Sirianant L, Wanitchakool P, Ousingsawat J, Benedetto R, Zormpa A, Cabrita I, Schreiber R, Kunzelmann K (2016) Non-essential contribution of LRRC8A to volume regulation. Pflügers Arch 468:805–816
53. Sorensen BH, Thorsteinsdottir UA, Lambert IH (2014) Acquired cisplatin resistance in humane ovarian cancer A2780 cells correlates with shift in taurine homeostasis and ability to volume regulate. Am J Physiol Cell Physiol 307:C1071–C1080
54. Suzuki J, Umeda M, Sims PJ, Nagata S (2010) Calcium-dependent phospholipid scrambling by TMEM16F. Nature 468:834–838
55. Syeda R, Qiu Z, Dubin AE, Murthy SE, Florendo MN, Mason DE, Mathur J, Cahalan SM, Peters EC, Montal M et al (2016) LRRC8 proteins form volume-regulated anion channels that sense ionic strength. Cell 164:499–511
56. Szabo I, Lepple-Wienhues A, Kaba KN, Zoratti M, Gulbins E, Lang F (1998) Tyrosine kinase-dependent activation of a chloride channel in CD95-induced apoptosis in T lymphocytes. Proc Natl Acad Sci USA 95:6169–6174
57. Tait SW, Oberst A, Quarato G, Milasta S, Haller M, Wang R, Karvela M, Ichim G, Yatim N, Albert ML et al (2013) Widespread mitochondrial depletion via mitophagy does not compromise necroptosis. Cell Rep 5:878–885
58. − channels. J Cell Sci 125:4991–4998
59. Uramoto H, Okada T, Okada Y (2012) Protective role of cardiac CFTR activation upon early reperfusion against myocardial infarction. Cell Physiol Biochem 30:1023–1038
60. Valverde MA, O’Briens JA, Sepulveda FV, Ratcliff RA, Evans MJ, Colledge WH (1995) Impaired cell volume regulation in intestinal crypt epithelia of cystic fibrosis. Proc Natl Acad Sci 92:9038–9041
61. Vitzthum C, Clauss WG, Fronius M (2015) Mechanosensitive activation of CFTR by increased cell volume and hydrostatic pressure but not shear stress. Biochim Biophys Acta 1848:2942–2951
62. Voets T, Droogmans G, Raskin G, Eggermont J, Nilius B (1999) Reduced intracellular ionic strength as the initial trigger for activation of endothelial volume-regulated anion channels. Proc Natl Acad Sci USA 96:5298–5303
63. Voss FK, Ullrich F, Munch J, Lazarow K, Lutter D, Mah N, Andrade-Navarro MA, von Kries JP, Stauber T, Jentsch TJ (2014) Identification of LRRC8 heteromers as an essential component of the volume-regulated anion channel VRAC. Science 344:634–638
64. Wanitchakool P, Wolf L, Koehl G, Sirianant L, Gaumann A, Schreiber R, Duvvuri U, Kunzelmann K (2014) Role of anoctamins in cancer and apoptosis. Philos Trans R Soc Lond B Biol Sci 369:20130096
65. Yang H, Kim A, David T, Palmer D, Jin T, Tien J, Huang F, Cheng T, Coughlin SR, Jan YN et al (2012) TMEM16F forms a Ca(2+)-activated cation channel required for lipid scrambling in platelets during blood coagulation. Cell 151:111–122
66. Yu H, Zeidan YH, Wu BX, Jenkins RW, Flotte TR, Hannun YA, Virella-Lowell I (2009) Defective acid sphingomyelinase pathway with Pseudomonas aeruginosa infection in cystic fibrosis. Am J Respir Cell Mol Biol 41:367–375
67. Zampighi GA, Kreman M, Boorer KJ, Loo DD, Bezanilla F, Chandy G, Hall JE, Wright EM (1995) A method for determining the unitary functional capacity of cloned channels and transporters expressed in Xenopus laevis oocytes. J Membr Biol 148:65–78
68. +-coupled cotransporters of glucose (SGLT1) and of iodide (NIS). The dependence of substrate size studied at high resolution. J Physiol 570:485–499
69. Zhang WK, Wang D, Duan Y, Loy MM, Chan HC, Huang P (2010) Mechanosensitive gating of CFTR. Nat Cell Biol 12:507–512