Calcium-activated and apoptotic phospholipid scrambling induced by Ano6 can occur independently of Ano6 ion currents

Cell Death and Disease

Volumn 4, Issue 4, 2013, Pages

  Kmit, A ^a   Van Kruchten, R ^b   Ousingsawat, J ^a   Mattheij, N J A ^b   Senden Gijsbers, B ^c   Heemskerk, J W M ^b   Schreiber, R ^a   Bevers, E M ^b   Kunzelmann, K ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Ano6; Anoctamin 6; Ca2+ activated Cl channels; Phospholipid scrambling; TMEM16F

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; ANOCTAMIN 6 PROTEIN; CALCIUM; CASPASE 3; CATION; CHLORIDE; FAS LIGAND; IONOMYCIN; MEMBRANE PROTEIN; PHOSPHOLIPID; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; GENE MUTATION; HUMAN; HUMAN CELL; ION CURRENT; LYMPHOCYTE; PHOSPHOLIPID SCRAMBLING; PRIORITY JOURNAL; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCOTT SYNDROME; WESTERN BLOTTING;

APOPTOSIS; B-LYMPHOCYTES; BIPHENYL COMPOUNDS; BLOOD COAGULATION DISORDERS; CALCIUM; CALCIUM IONOPHORES; CHLORIDE CHANNELS; FAS LIGAND PROTEIN; HEK293 CELLS; HUMANS; ION TRANSPORT; IONOMYCIN; JURKAT CELLS; NITROPHENOLS; PATCH-CLAMP TECHNIQUES; PHOSPHOLIPID TRANSFER PROTEINS; PHOSPHOLIPIDS; PIPERAZINES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SULFONAMIDES;

EID: 84876925080     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.135     Document Type: Article

References (36)

1. Yang YD, Cho H, Koo JY, Tak MH, Cho Y, Shim WS et al. TMEM16A confers receptoractivated calcium-dependent chloride conductance. Nature 2008; 455: 1210-1215.
2. Schroeder BC, Cheng T, Jan YN, Jan LY. Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell 2008; 134: 1019-1029.
3. Caputo A, Caci E, Ferrera L, Pedemonte N, Barsanti C, Sondo E et al. TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science 2008; 322: 590-594.
4. Tian Y, Schreiber R, Kunzelmann K. Anoctamins are a family of Ca2 activated Cl-channels. J Cell Sci 2012; 125: 4991-4998.
5. Ferrera L, Caputo A, Galietta LJ. TMEM16A protein: a new identity for Ca(2)-dependent Cl channels. Physiology. 2010; 25: 357-363.
6. Billig GM, Pá l B, Fidzinski P, Jentsch TJ. Ca2-activated Cl-currents are dispensable for olfaction. Nature Neurosci 2011; 14: 763-769.
7. Kunzelmann K, Kongsuphol P, Aldehni F, Tian Y, Ousingsawat J, Warth R et al. Bestrophin and TMEM16 -Ca2 activated Cl-channels with different functions. Cell Calcium 2009; 46: 233-241.
8. Yang H, Kim A, David T, Palmer D, Jin T, Tien J et al. TMEM16F forms a Ca(2)-activated cation channel required for lipid scrambling in platelets during blood coagulation. Cell 2012; 151: 111-122.
9. Martins JR, Faria D, Kongsuphol P, Reisch B, Schreiber R, Kunzelmann K. Anoctamin 6 is an essential component of the outwardly rectifying chloride channel. Proc Natl Acad Sci USA 2011; 108: 18168-18172.
10. Almaca J, Tian Y, Aldehni F, Ousingsawat J, Kongsuphol P, Rock JR et al. TMEM16 proteins produce volume regulated chloride currents that are reduced in mice lacking TMEM16A. J Biol Chem 2009; 284: 28571-28578.
11. Hanzu FA, Gasa R, Bulur N, Lybaert P, Gomis R, Malaisse WJ et al. Expression of TMEM16A and SLC4A4 in human pancreatic islets. Cell Physiol Biochem 2012; 29: 61-64.
12. Owsianik G, Prenen J, Hermans C, Eggermont J, Nilius B. Functional characterization of TMEM16 anion channels. FASEB J (Abstract) 2010; 608: 12.
13. Yu K, Duran C, Qu Z, Cui YY, Hartzell HC. Explaining calcium-dependent gating of anoctamin-1 chloride channels requires a revised topology. Circ Res 2012; 110: 990-999.
14. Suzuki J, Umeda M, Sims PJ, Nagata S. Calcium-dependent phospholipid scrambling by TMEM16F. Nature 2010; 468: 834-838.
15. Bevers EM, Williamson PL. Phospholipid scramblase: an update. FEBS Lett. 2010; 584: 2724-2730.
16. Heemskerk JW, Bevers EM, Lindhout T. Platelet activation and blood coagulation. Thromb Haemost 2002; 88: 186-193.
17. Castoldi E, Collins PW, Williamson PL, Bevers EM. Compound heterozygosity for 2 novel TMEM16F mutations in a patient with Scott syndrome. Blood 2011; 117: 4399-4400.
18. Munnix IC, Harmsma M, Giddings JC, Collins PW, Feijge MA, Comfurius P et al. Storemediated calcium entry in the regulation of phosphatidylserine exposure in blood cells from Scott patients. Thromb Haemost 2003; 89: 687-695.
19. Williamson P, Christie A, Kohlin T, Schlegel RA, Comfurius P, Harmsma M et al. Phospholipid scramblase activation pathways in lymphocytes. Biochemistry 2001; 40: 8065-8072.
20. de la Fuente R, NamkungW,Mills A, Verkman AS. Small molecule screen identifies inhibitors of a human intestinal calcium activated chloride channel. Mol Pharmacol 2007; 73: 758-768.
21. Hartzell HC, Putzier I, Arreola J. Calcium-activated chloride channels. Annu Rev Physiol 2005; 67: 719-758.
22. Namkung W, Thiagarajah JR, Phuan PW, Verkman AS. Inhibition of Ca2-activated Clchannels by gallotannins as a possible molecular basis for health benefits of red wine and green tea. FASEB J 2010; 24: 4178-4186.
23. Taylor SR, Gonzalez-Begne M, Dewhurst S, Chimini G, Higgins CF, Melvin JE et al. Sequential shrinkage and swelling underlie P2X7-stimulated lymphocyte phosphatidylserine exposure and death. J Immunol 2008; 180: 300-308.
24. Schoenwaelder SM, Yuan Y, Josefsson EC, White MJ, Yao Y, Mason KD et al. Two distinct pathways regulate platelet phosphatidylserine exposure and procoagulant function. Blood 2009; 114: 663-666.
25. Szabo I, Lepple-Wienhues A, Kaba KN, Zoratti M, Gulbins E, Lang F. Tyrosine kinasedependent activation of a chloride channel in CD95-induced apoptosis in T lymphocytes. Proc Natl Acad Sci USA 1998; 95: 6169-6174.
26. Kunzelmann K, Pavenstádt H, Greger R. Properties and regulation of chloride channels in cystic fibrosis and normal airway epithelial cells. Pflügers Arch 1989; 415: 172-182.
27. Aguirre A, Shoji KF, Saez JC, Henriquez M, Quest AF. FasL-triggered death of Jurkat cells requires caspase 8-induced, ATP-dependent cross-talk between Fas and the purinergic receptor P2X(7). J Cell Physiol 2013; 228: 485-493.
28. Szteyn K, Schmid E, Nurbaeva MK, Yang W, Münzer P, Kunzelmann K et al. Expression and functional significance of the ca-activated Cl(-) channel ANO6 in dendritic cells. Cell Physiol Biochem 2012; 30: 1319-1332.
29. Blazer-Yost BL, Blacklock BJ, Flaig S, Bacallao RL, Gattone VH. Lysophosphatidic acid is a modulator of cyst growth in autosomal dominant polycystic kidney disease. Cell Physiol Biochem 2011; 28: 1255-1264.
30. Kunzelmann K, Schreiber R, Kmit A, Jantarajit W, Martins JR, Faria D et al. Expression and function of epithelial anoctamins. Exp Physiol 2012; 97: 184-192.
31. Kunzelmann K, Tian Y, Martins JR, Faria D, Kongsuphol P, Ousingsawat J et al. Anoctamins. Pflugers Arch. 2011; 462: 195-208.
32. Schreiber R, Uliyakina I, Kongsuphol P, Warth R, Mirza M, Martins JR et al. Expression and function of epithelial anoctamins. J Biol Chem 2010; 285: 7838-7845.
33. Segawa K, Suzuki J, Nagata S. Constitutive exposure of phosphatidylserine on viable cells. Proc Natl Acad Sci USA 2011; 108: 19246-19251.
34. Ousingsawat J, Martins JR, Schreiber R, Rock JR, Harfe BD, Kunzelmann K. Loss of TMEM16A causes a defect in epithelial Ca2 dependent chloride transport. J Biol Chem 2009; 284: 28698-28703.
35. Heemskerk JW, Willems GM, Rook MB, Sage SO. Ragged spiking of free calcium in ADPstimulated human platelets: regulation of puff-like calcium signals in vitro and ex vivo. J Physiol 2001; 535: 625-635.
36. Barro Soria R, Aldehni F, Almaça J, Witzgall R, Schreiber R, Kunzelmann K. ER localized bestrophin1 acts as a counter-ion channel to activate Ca2 dependent ion channels TMEM16A and SK4. Pflügers Arch 2009; 459: 485-497.