Cellular volume regulation by anoctamin 6: Ca2+, phospholipase A2 and osmosensing

Pflugers Archiv European Journal of Physiology

Volumn 468, Issue 2, 2016, Pages 335-349

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

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

Anoctamin 6; Apoptosis; Regulatory volume decrease; RVD; TMEM16F; Volume regulation; Volume regulated anion channel; VRAC

Indexed keywords

ANOCTAMIN 6; ARACHIDONIC ACID; CALCIUM ACTIVATED CHLORIDE CHANNEL; CALCIUM ION; COMPLEMENTARY DNA; LYSOPHOSPHOLIPID; MELITTIN; MEMBRANE PHOSPHOLIPID; PHOSPHOLIPASE A2; SMALL INTERFERING RNA; TRANSIENT RECEPTOR POTENTIAL CHANNEL; UNCLASSIFIED DRUG; VOLUME REGULATED CHLORIDE CHANNEL; CHLORIDE; PHOSPHOLIPID TRANSFER PROTEIN; TMEM16F PROTEIN, MOUSE;

ANIMAL CELL; ANION TRANSPORT; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL MEMBRANE; CELL SWELLING; CELL VOLUME; CONTROLLED STUDY; GENE SILENCING; HEK293 CELL LINE; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; MOUSE; NONHUMAN; OSMOLARITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCOTT SYNDROME; WHOLE CELL; ACTION POTENTIAL; ANIMAL; ANTAGONISTS AND INHIBITORS; CALCIUM SIGNALING; CELL CULTURE; CELL SIZE; CYTOLOGY; GENETICS; LYMPHOCYTE; METABOLISM; OOCYTE; OSMOREGULATION;

ACTION POTENTIALS; ANIMALS; CALCIUM SIGNALING; CELL SIZE; CELLS, CULTURED; CHLORIDES; HEK293 CELLS; HUMANS; LYMPHOCYTES; LYSOPHOSPHOLIPIDS; MICE; OOCYTES; OSMOREGULATION; PHOSPHOLIPASES A2; PHOSPHOLIPID TRANSFER PROTEINS;

EID: 84954369038     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-015-1739-8     Document Type: Article

References (55)

1. Akita T, Okada Y (2011) Regulation of bradykinin-induced activation of volume-sensitive outwardly rectifying anion channels by Ca2+ nanodomains in mouse astrocytes. J Physiol 589:3909–3927
2. 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
3. Berridge MJ (2004) Conformational coupling: a physiological calcium entry mechanism. Sci STKE 2004:e33
4. Bessac BF, Fleig A (2007) TRPM7 channel is sensitive to osmotic gradients in human kidney cells. J Physiol 582:1073–1086
5. Brunner JD, Lim NK, Schenck S, Duerst A, Dutzler R (2014) X-ray structure of a calcium-activated TMEM16 lipid scramblase. Nature 516:207–212
6. Cruz-Rangel S, Gamba G, Ramos-Mandujano G, Pasantes-Morales H (2012) Influence of WNK3 on intracellular chloride concentration and volume regulation in HEK293 cells. Pflugers Arch 464:317–330
7. Dawson DC, Van Driessche W, Helman SI (1988) Osmotically induced basolateral K+ conductance in turtle colon: lidocaine-induced K+ channel noise. Am J Physiol 254:C165–C174
8. Ehlen HW, Chinenkova M, Moser M, Munter HM, Krause Y, Gross S, Brachvogel B, Wuelling M, Kornak U, Vortkamp A (2012) Inactivation of Anoctamin-6/Tmem16f, a regulator of phosphatidylserine scrambling in osteoblasts, leads to decreased mineral deposition in skeletal tissues. J Bone Miner Res 28:246–259
9. 29) cells by cAMP. Pflugers Arch 432:735–740
10. Forrest LR, Tavoulari S, Zhang YW, Rudnick G, Honig B (2007) Identification of a chloride ion binding site in Na+/Cl-dependent transporters. Proc Natl Acad Sci U S A 104:12761–12766
11. Grubb S, Poulsen KA, Juul CA, Kyed T, Klausen TK, Larsen EH, Hoffmann EK (2013) TMEM16F (anoctamin 6), an anion channel of delayed Ca2+ activation. J Gen Physiol 141:585–600
12. Harteneck C, Frenzel H, Kraft R (2007) N-(p-amylcinnamoyl)anthranilic acid (ACA): a phospholipase A(2) inhibitor and TRP channel blocker. Cardiovasc Drug Rev 25:61–75
13. Harteneck C, Gollasch M (2011) Pharmacological modulation of diacylglycerol-sensitive TRPC3/6/7 channels. Curr Pharm Biotechnol 12:35–41
14. Helix N, Strobaek D, Dahl BH, Christophersen P (2003) Inhibition of the endogenous volume-regulated anion channel (VRAC) in HEK293 cells by acidic di-aryl-ureas. J Membr Biol 196:83–94
15. Hoffmann EK, Lambert IH, Pedersen SF (2009) Physiology of cell volume regulation in vertebrates. Physiol Rev 89:193–277
16. Ishii T, Hashimoto T, Ohmori H (1996) Hypotonic stimulation induced Ca2+ release from IP3-sensitive internal stores in a green monkey kidney cell line. J Physiol 493:371–384
17. 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
18. Klausen TK, Bergdahl A, Hougaard C, Christophersen P, Pedersen SF, Hoffmann EK (2007) Cell cycle-dependent activity of the volume- and Ca2+-activated anion currents in Ehrlich lettre ascites cells. J Cell Physiol 210:831–842
19. 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 4:e611
20. Kunzelmann K, Tian Y, Martins JR, Faria D, Kongsuphol P, Ousingsawat J, Thevenod F, Roussa E, Rock JR, Schreiber R (2011) Anoctamins. Pflugers Arch 462:195–208
21. Lee MY, Song H, Nakai J, Ohkura M, Kotlikoff MI, Kinsey SP, Golovina VA, Blaustein MP (2006) Local subplasma membrane Ca2+ signals detected by a tethered Ca2+ sensor. Proc Natl Acad Sci U S A 103:13232–13237
22. Lehtonen JY, Kinnunen PK (1995) Phospholipase A2 as a mechanosensor. Biophys J 68:1888–1894
23. Lemonnier L, Prevarskaya N, Shuba Y, Vanden Abeele F, Nilius B, Mazurier J, Skryma R (2002) Ca2+ modulation of volume-regulated anion channels: evidence for colocalization with store-operated channels. FASEB J 16:222–224
24. Malvezzi M, Chalat M, Janjusevic R, Picollo A, Terashima H, Menon AK, Accardi A (2013) Ca(2+)-dependent phospholipid scrambling by a reconstituted TMEM16 ion channel. Nat Commun 4:2367
25. 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 U S A 108:18168–18172
26. McCarty NA, O'Neil RG (1992) Calcium signalling in volume regulation. Physiol Rev 72:1037–1061
27. Mohanty MJ, Ye M, Li X, Rossi NF (2001) Hypotonic swelling-induced Ca(2+) release by an IP(3)-insensitive Ca(2+) store. Am J Physiol Cell Physiol 281:C555–C562
28. Murakami M, Kudo I (2002) Phospholipase A2. J Biochem 131:285–292
29. 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
30. Nilius B, Eggermont J, Voets T, Buyse G, Manolopoulos V, Droogmans G (1997) Properties of volume-regulated anion channels in mammalian cells. Prog Biophys Mol Biol 68:69–119
31. Nilius B, Eggermont J, Voets T, Droogmans G (1996) Volume-activated Cl-channels. Gen Pharmacol 27:1131–1140
32. Nilius B, Oike M, Zahradnik I, Droogmans G (1994) Activation of a Cl-current by hypotonic volume increase in human endothelial cells. J Gen Physiol 103:787–805
33. Okada Y (2006) Cell volume-sensitive chloride channels: phenotypic properties and molecular identity. Contrib Nephrol 152:9–24
34. Ousingsawat J, Martins JR, Schreiber R, Rock JR, Harfe BD, Kunzelmann K (2009) Loss of TMEM16A causes a defect in epithelial Ca2+ dependent chloride transport. J Biol Chem 284:28698–28703
35. 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
36. Pedemonte N, Galietta LJ (2014) Structure and function of TMEM16 proteins (anoctamins). Physiol Rev 94:419–459
37. Pedersen S, Lambert IH, Thoroed SM, Hoffmann EK (2000) Hypotonic cell swelling induces translocation of the alpha isoform of cytosolic phospholipase A2 but not the gamma isoform in Ehrlich ascites tumor cells. Eur J Biochem 267:5531–5539
38. Pedersen SF, Nilius B (2007) Transient receptor potential channels in mechanosensing and cell volume regulation. Methods Enzymol 428:183–207
39. Pedersen SF, Poulsen KA, Lambert IH (2006) Roles of phospholipase A2 isoforms in swelling- and melittin-induced arachidonic acid release and taurine efflux in NIH3T3 fibroblasts. Am J Physiol Cell Physiol 291:C1286–C1296
40. Preston GM, Carroll TP, Guggino WB, Agre P (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256:385–387
41. 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
42. Sabirov RZ, Prenen J, Tomita T, Droogmans G, Nilius B (2000) Reduction of ionic strength activates single volume-regulated anion channels (VRAC) in endothelial cells. Pflugers Arch 439:315–320
43. 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. Pflugers Arch 467:1203–1213
44. Shimizu T, Iehara T, Sato K, Fujii T, Sakai H, Okada Y (2013) TMEM16F is a component of a Ca2+-activated Cl-channel but not a volume-sensitive outwardly rectifying Cl-channel. Am J Physiol Cell Physiol 304:C748–C759
45. Strange K, Emma F, Jackson PS (1996) Cellular and molecular physiology of volume-sensitive anion channels. Am J Physiol 270:C711–C730
46. Suzuki J, Umeda M, Sims PJ, Nagata S (2010) Calcium-dependent phospholipid scrambling by TMEM16F. Nature 468:834–838
47. Szteyn K, Schmid E, Nurbaeva MK, Yang W, Munzer P, Kunzelmann K, Lang F, Shumilina E (2012) Expression and functional significance of the Ca-activated Cl(−) channel ANO6 in dendritic cells. Cell Physiol Biochem 30:1319–1332
48. Thoroed SM, Lauritzen L, Lambert IH, Hansen HS, Hoffmann EK (1997) Cell swelling activates phospholipase A2 in Ehrlich ascites tumor cells. J Membr Biol 160:47–58
49. Tian Y, Schreiber R, Kunzelmann K (2012) Anoctamins are a family of Ca2+ activated Cl-channels. J Cell Sci 125:4991–4998
50. 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 U S A 96:5298–5303
51. 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
52. Yang H, Kim A, David T, Palmer D, Jin T, Tien J, Huang F, Cheng T, Coughlin SR, Jan YN, Jan LY (2012) TMEM16F forms a Ca(2+)-activated cation channel required for lipid scrambling in platelets during blood coagulation. Cell 151:111–122
53. Yoo J, Cui Q (2009) Curvature generation and pressure profile modulation in membrane by lysolipids: insights from coarse-grained simulations. Biophys J 97:2267–2276
54. Yu K, Whitlock JM, Lee K, Ortlund EA, Yuan CY, and Hartzell HC (2015) Identification of a lipid scrambling domain in ANO6/TMEM16F. Elife. 4. doi: 10
55. Zholos A, Beck B, Sydorenko V, Lemonnier L, Bordat P, Prevarskaya N, Skryma R (2005) Ca(2+)- and volume-sensitive chloride currents are differentially regulated by agonists and store-operated Ca2+ entry. J Gen Physiol 125:197–211