Subdued, a TMEM16 family Ca2+-activated Cl- channel in Drosophila melanogaster with an unexpected role in host defense

eLife

Volumn 2013, Issue 2, 2013, Pages

  Wong, Xiu Ming ^a   Younger, Susan ^a   Peters, Christian J ^a   Jan, Yuh Nung ^a   Jan, Lily Y ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ACTIVATED CHLORIDE CHANNEL; SUBDUED CHANNEL; TMEM16A CHANNEL; TMEM16B CHANNEL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLONY FORMING UNIT; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ELECTROPHYSIOLOGY; FEEDING; FEMALE; HOST RESISTANCE; HUMAN; HUMAN CELL; INTESTINE INFECTION; MEMBRANE PERMEABILITY; NONHUMAN; ORTHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SERRATIA INFECTION;

DROSOPHILA MELANOGASTER; MAMMALIA; SERRATIA MARCESCENS; VERTEBRATA;

EID: 84887386469     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.00862.001     Document Type: Article

References (39)

1. Bernsel A, Viklund H, Hennerdal A, Elofsson A. 2009. TOPCONS: consensus prediction of membrane protein topology. Nucleic Acids Res 37:W465-8. doi: 10.1093/nar/gkp363.
2. Billig GM, Pal B, Fidzinski P, Jentsch TJ. 2011. Ca2+-activated Cl-currents are dispensable for olfaction. Nat Neurosci 14:763-9. doi: 10.1038/nn.2821.
3. Bonnay F, Cohen-Berros E, Hoffmann M, Kim SY, Boulianne GL, Hoffmann JA, et al. 2013. big bang gene modulates gut immune tolerance in Drosophila. Proc Natl Acad Sci USA 110:2957-62. doi: 10.1073/pnas.1221910110.
4. Bulley S, Neeb ZP, Burris SK, Bannister JP, Thomas-Gatewood CM, Jangsangthong W, et al. 2012. TMEM16A/ANO1 channels contribute to the myogenic response in cerebral arteries. Circ Res 111:1027-36. doi: 10.1161/CIRCRESAHA.112.277145.
5. Caputo A, Caci E, Ferrera L, Pedemonte N, Barsanti C, Sondo E, et al. 2008. TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science 322:590-4. doi: 10.1126/science.1163518.
6. Chien LT, Zhang ZR, Hartzell HC. 2006. Single Cl-channels activated by Ca2+ in Drosophila S2 cells are mediated by bestrophins. J Gen Physiol 128:247-59. doi: 10.1085/jgp.200609581.
7. Chintapalli VR, Wang J, Dow JA. 2007. Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet 39:715-20. doi: 10.1038/ng2049.
8. Cho H, Yang YD, Lee J, Lee B, Kim T, Jang Y, et al. 2012. The calcium-activated chloride channel anoctamin 1 acts as a heat sensor in nociceptive neurons. Nat Neurosci 15:1015-21. doi: 10.1038/nn.3111.
9. Cronin SJ, Nehme NT, Limmer S, Liegeois S, Pospisilik JA, Schramek D, et al. 2009. Genome-wide RNAi screen identifies genes involved in intestinal pathogenic bacterial infection. Science 325:340-3. doi: 10.1126/science.1173164.
10. Flyg C, Kenne K, Boman HG. 1980. Insect pathogenic properties of Serratia marcescens: phage-resistant mutants with a decreased resistance to Cecropia immunity and a decreased virulence to Drosophila. J Gen Microbiol 120:173-81.
11. Fromm J, Lautner S. 2007. Electrical signals and their physiological significance in plants. Plant Cell Environ 30:249-57. doi: 10.1111/j.1365-3040.2006.01614.x.
12. Ha EM, Lee KA, Park SH, Kim SH, Nam HJ, Lee HY, et al. 2009. Regulation of DUOX by the Galphaq-phospholipase Cbeta-Ca2+ pathway in Drosophila gut immunity. Dev Cell 16:386-97. doi: 10.1016/j.devcel.2008.12.015.
13. Ha EM, Oh CT, Bae YS, Lee WJ. 2005. A direct role for dual oxidase in Drosophila gut immunity. Science 310:847-50. doi: 10.1126/science.1117311.
14. Hortsch M, Margolis B. 2003. Septate and paranodal junctions: kissing cousins. Trends Cell Biol 13:557-61. doi: 10.1016/j.tcb.2003.09.004.
15. Huang F, Zhang H, Wu M, Yang H, Kudo M, Peters CJ, et al. 2012a. Calcium-activated chloride channel TMEM16A modulates mucin secretion and airway smooth muscle contraction. Proc Natl Acad Sci USA 109:16354-9. doi: 10.1073/pnas.1214596109.
16. Huang WC, Xiao S, Huang F, Harfe BD, Jan YN, Jan LY. 2012b. Calcium-activated chloride channels (CaCCs) regulate action potential and synaptic response in hippocampal neurons. Neuron 74:179-92. doi: 10.1016/j.neuron.2012.01.033.
17. Hwang SJ, Blair PJ, Britton FC, O'Driscoll KE, Hennig G, Bayguinov YR, et al. 2009. Expression of anoctamin 1/TMEM16A by interstitial cells of Cajal is fundamental for slow wave activity in gastrointestinal muscles. J Physiol 587:4887-904. doi: 10.1113/jphysiol.2009.176198.
18. Kline D. 1988. Calcium-dependent events at fertilization of the frog egg: injection of a calcium buffer blocks ion channel opening, exocytosis, and formation of pronuclei. Dev Biol 126:346-61. doi: 10.1016/0012-1606(88)90145-5.
19. Kramer J, Hawley RS. 2003. The spindle-associated transmembrane protein Axs identifies a membranous structure ensheathing the meiotic spindle. Nat Cell Biol 5:261-3. doi: 10.1038/ncb944.
20. Kuraishi T, Binggeli O, Opota O, Buchon N, Lemaitre B. 2011. Genetic evidence for a protective role of the peritrophic matrix against intestinal bacterial infection in Drosophila melanogaster. Proc Natl Acad Sci USA 108:15966-71. doi: 10.1073/pnas.1105994108.
21. Lalonde MR, Kelly ME, Barnes S. 2008. Calcium-activated chloride channels in the retina. Channels (Austin) 2:252-60. doi: 10.4161/chan.2.4.6704.
22. Large WA, Wang Q. 1996. Characteristics and physiological role of the Ca(2+)-activated Cl-conductance in smooth muscle. Am J Physiol 271:C435-54.
23. Lemaitre B, Hoffmann J. 2007. The host defense of Drosophila melanogaster. Annu Rev Immunol 25:697-743. doi: 10.1146/annurev.immunol.25.022106.141615.
24. Manoury B, Tamuleviciute A, Tammaro P. 2010. TMEM16A/anoctamin 1 protein mediates calcium-activated chloride currents in pulmonary arterial smooth muscle cells. J Physiol 588:2305-14. doi: 10.1113/jphysiol.2010.189506.
25. Miledi R, Parker I. 1984. Chloride current induced by injection of calcium into Xenopus oocytes. J Physiol 357:173-83.
26. Namkung W, Phuan PW, Verkman AS. 2011. TMEM16A inhibitors reveal TMEM16A as a minor component of calcium-activated chloride channel conductance in airway and intestinal epithelial cells. J Biol Chem 286:2365-74. doi: 10.1074/jbc.M110.175109.
27. Nehme NT, Liegeois S, Kele B, Giammarinaro P, Pradel E, Hoffmann JA, et al. 2007. A model of bacterial intestinal infections in Drosophila melanogaster. PLOS Pathog 3:e173. doi: 10.1371/journal.ppat.0030173.
28. Parks AL, Cook KR, Belvin M, Dompe NA, Fawcett R, Huppert K, et al. 2004. Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat Genet 36:288-92. doi: 10.1038/ng1312.
29. Pifferi S, Dibattista M, Menini A. 2009. TMEM16B induces chloride currents activated by calcium in mammalian cells. Pflugers Arch 458:1023-38. doi: 10.1007/s00424-009-0684-9.
30. Qu Z, Hartzell HC. 2000. Anion permeation in Ca(2+)-activated Cl(-) channels. J Gen Physiol 116:825-44. doi: 10.1085/jgp.116.6.825.
31. Rock JR, O'Neal WK, Gabriel SE, Randell SH, Harfe BD, Boucher RC, et al. 2009. Transmembrane protein 16A (TMEM16A) is a Ca2+-regulated Cl-secretory channel in mouse airways. J Biol Chem 284:14875-80. doi: 10.1074/jbc.C109.000869.
32. Romanenko VG, Catalan MA, Brown DA, Putzier I, Hartzell HC, Marmorstein AD, et al. 2010. Tmem16A encodes the Ca2+-activated Cl-channel in mouse submandibular salivary gland acinar cells. J Biol Chem 285:12990-3001. doi: 10.1074/jbc.M109.068544.
33. Schroeder BC, Cheng T, Jan YN, Jan LY. 2008. Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell 134:1019-29. doi: 10.1016/j.cell.2008.09.003.
34. Shiina T, Tazawa M. 1987. Ca2+-activated Cl-channel in plasmalemma of Nitellopsis obtusa. Journal of Membrane Biology 99:137-46. doi: 10.1007/BF01871233.
35. Stohr H, Heisig JB, Benz PM, Schoberl S, Milenkovic VM, Strauss O, et al. 2009. TMEM16B, a novel protein with calcium-dependent chloride channel activity, associates with a presynaptic protein complex in photoreceptor terminals. J Neurosci 29:6809-18. doi: 10.1523/JNEUROSCI.5546-08.2009.
36. Tepass U, Tanentzapf G, Ward R, Fehon R. 2001. Epithelial cell polarity and cell junctions in Drosophila. Annu Rev Genet 35:747-84. doi: 10.1146/annurev.genet.35.102401.091415.
37. Wolf W, Kilic A, Schrul B, Lorenz H, Schwappach B, Seedorf M. 2012. Yeast Ist2 recruits the endoplasmic reticulum to the plasma membrane and creates a ribosome-free membrane microcompartment. PLOS ONE 7:e39703. doi: 10.1371/journal.pone.0039703.
38. Yang H, Kim A, David T, Palmer D, Jin T, Tien J, et al. 2012. TMEM16F forms a Ca2+-activated cation channel required for lipid scrambling in platelets during blood coagulation. Cell 151:111-22. doi: 10.1016/j.cell.2012.07.036.
39. Yang YD, Cho H, Koo JY, Tak MH, Cho Y, Shim WS, et al. 2008. TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature 455:1210-5. doi: 10.1038/nature07313.