A stomatin dimer modulates the activity of acid-sensing ion channels

EMBO Journal

Volumn 31, Issue 17, 2012, Pages 3635-3646

  Brand, Janko ^a,b   Smith, Ewan St J ^a   Schwefel, David ^a   Lapatsina, Liudmila ^a   Poole, Kate ^a   Omerbašić, Damir ^a   Kozlenkov, Alexey ^a   Behlke, Joachim ^a   Lewin, Gary R ^a   Daumke, Oliver ^a,c  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

ASIC; ion channel regulation; membrane trafficking; protein structure; stomatin family

Indexed keywords

ACID SENSING ION CHANNEL; ACID SENSING ION CHANNEL 3; DIMER; FLOTILLIN 1; LIGAND; PROHIBITIN; STOMATIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHANNEL GATING; CRYSTAL STRUCTURE; DIMERIZATION; HYDROPHOBICITY; MEMBRANE ELECTROPHYSIOLOGY; MEMBRANE STRUCTURE; MEMBRANE TRANSPORT; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; STRUCTURE ANALYSIS;

ACID SENSING ION CHANNELS; ANIMALS; BLOOD PROTEINS; CELLS, CULTURED; CHO CELLS; CRICETINAE; CRICETULUS; DIMERIZATION; FIBROBLASTS; HEK293 CELLS; HUMANS; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; PROTEIN STRUCTURE, TERTIARY; RATS;

EID: 84866133815     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.203     Document Type: Article

References (63)

1. Baron A, Deval E, Salinas M, Lingueglia E, Voilley N, Lazdunski M (2002) Protein kinase C stimulates the acid-sensing ion channel ASIC2a via the PDZ domain-containing protein PICK1. J Biol Chem 277: 50463-50468
2. Behlke J, Ristau O, Schonfeld HJ (1997) Nucleotide-dependent complex formation between the Escherichia coli chaperonins GroEL and GroES studied under equilibrium conditions. Biochemistry 36: 5149-5156
3. Boehm M, Nield J, Zhang P, Aro EM, Komenda J, Nixon PJ (2009) Structural and mutational analysis of band 7 proteins in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 191: 6425-6435
4. Boute N, Gribouval O, Roselli S, Benessy F, Lee H, Fuchshuber A, Dahan K, Gubler MC, Niaudet P, Antignac C (2000) NPHS2, encoding the glomerular protein podocin, is mutated in autoso-mal recessive steroid-resistant nephrotic syndrome. Nat Genet 24: 349-354
5. Browman DT, Hoegg MB, Robbins SM (2007) The SPFH domain-containing proteins: more than lipid raft markers. Trends Cell Biol 17: 394-402
6. Cadiou H, Studer M, Jones NG, Smith ES, Ballard A, McMahon SB, McNaughton PA (2007) Modulation of acid-sensing ion channel activity by nitric oxide. J Neurosci 27: 13251-13260
7. Chalfie M, Sulston J (1981) Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Dev Biol 82: 358-370
8. COLLABORATIVE COMPUTATIONAL PROJECT (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D 50: 760-763
9. Cueva JG, Mulholland A, Goodman MB (2007) Nanoscale organization of the MEC-4 DEG/ENaC sensory mechanotransduction channel in Caenorhabditis elegans touch receptor neurons. J Neurosci 27: 14089-14098
10. Deval E, Salinas M, Baron A, Lingueglia E, Lazdunski M (2004) ASIC2b-dependent regulation of ASIC3, an essential acid-sensing ion channel subunit in sensory neurons via the partner protein PICK-1. J Biol Chem 279: 19531-19539
11. Duggan A, Garcia-Anoveros J, Corey DP (2002) The PDZ domain protein PICK1 and the sodium channel BNaC1 interact and localize at mechanosensory terminals of dorsal root ganglion neurons and dendrites of central neurons. J Biol Chem 277: 5203-5208
12. Dundas J, Ouyang Z, Tseng J, Binkowski A, Turpaz Y, Liang J (2006) CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucleic Acids Res 34: W116-W118
13. Frick M, Bright NA, Riento K, Bray A, Merrified C, Nichols BJ (2007) Coassembly of flotillins induces formation of membrane microdomains, membrane curvature, and vesicle budding. Curr Biol 17: 1151-1156
14. Fricke B, Argent AC, Chetty MC, Pizzey AR, Turner EJ, Ho MM, Iolascon A, von DM, Stewart GW (2003) The 'stomatin' gene and protein in overhydrated hereditary stomatocytosis. Blood 102: 2268-2277
15. Frost A, Perera R, Roux A, Spasov K, Destaing O, Egelman EH, De CP, Unger VM (2008) Structural basis of membrane invagination by F-BAR domains. Cell 132: 807-817
16. Frost A, Unger VM, De CP (2009) The BAR domain superfamily: membrane-molding macromolecules. Cell 137: 191-196
17. Gallagher PG, Forget BG (1995) Structure, organization, and expression of the human band 7.2b gene, a candidate gene for hereditary hydrocytosis. J Biol Chem 270: 26358-26363
18. Garcia-Anoveros J, Samad TA, Zuvela-Jelaska L, Woolf CJ, Corey DP (2001) Transport and localization of the DEG/ENaC ion channel BNaC1alpha to peripheral mechanosensory terminals of dorsal root ganglia neurons. J Neurosci 21: 2678-2686
19. Gonzales EB, Kawate T, Gouaux E (2009) Pore architecture and ion sites in acid-sensing ion channels and P2X receptors. Nature 460: 599-604
20. Goodman MB, Ernstrom GG, Chelur DS, O'Hagan R, Yao CA, Chalfie M (2002) MEC-2 regulates C. elegans DEG/ENaC channels needed for mechanosensation. Nature 415: 1039-1042
21. Hruska-Hageman AM, Benson CJ, Leonard AS, Price MP, Welsh MJ (2004) PSD-95 and Lin-7b interact with acid-sensing ion channel-3 and have opposite effects on H\+-gated current. J Biol Chem 279: 46962-46968
22. Hu CD, Chinenov Y, Kerppola TK (2002) Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol Cell 9: 789-798
23. Huang M, Gu G, Ferguson EL, Chalfie M (1995) A stomatin-like protein necessary for mechanosensation in C. elegans. Nature 378: 292-295
24. Huber TB, Schermer B, Müller RU, Höhne M, Bartram M, Calixto A, Hagmann H, Reinhardt C, Koos F, Kunzelmann K, Shirokova E, Krautwurst D, Harteneck C, Simons M, Pavenstädt H, Kerjaschki D, Thiele C, Walz G, Chalfie M, Benzing T (2006) Podocin and MEC-2 bind cholesterol to regulate the activity of associated ion channels. Proc Natl Acad Sci USA 103: 17079-17086
25. Jasti J, Furukawa H, Gonzales EB, Gouaux E (2007) Structure of acid-sensing ion channel 1 at 1.9 A resolution and low pH. Nature 449: 316-323
26. Kabsch W (2010) XDS. Acta Crystallogr D Biol Crystallogr 66: 125-132
27. Kadurin I, Huber S, Grunder S (2009) A single conserved proline residue determines the membrane topology of stomatin. Biochem J 418: 587-594
28. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797
29. Kumar P, Ziegler A, Grahn A, Hee CS, Ziegler A (2010) Leaving the structural ivory tower, assisted by interactive 3D PDF. Trends Biochem Sci 35: 419-422
30. Lapatsina L, Brand J, Poole K, Daumke O, Lewin GR (2012a) Stomatin-domain proteins. Eur J Cell Biol 91: 240-245
31. Lapatsina L, Jira J, Smith ES, Poole K, Kozlenkov A, Bilbao D, Lewin GR, Heppenstall PA (2012b) Regulation of ASIC channels by a stomatin/STOML3 complex located in a mobile vesicle pool in sensory neurons. Open Biol 2: 120096
32. Leonard AS, Yermolaieva O, Hruska-Hageman A, Askwith CC, Price MP, Wemmie JA, Welsh MJ (2003) cAMP-dependent protein kinase phosphorylation of the acid-sensing ion channel-1 regulates its binding to the protein interacting with C-kinase-1. Proc Natl Acad Sci USA 100: 2029-2034
33. Leslie AG (2006) The integration of macromolecular diffraction data. Acta Crystallogr D Biol Crystallogr 62: 48-57
34. Lumpkin EA, Marshall KL, Nelson AM (2010) The cell biology of touch. J Cell Biol 191: 237-248
35. Mairhofer M, Steiner M, Salzer U, Prohaska R (2009) Stomatin-like protein-1 interacts with stomatin and is targeted to late endo-somes. J Biol Chem 284: 29218-29229
36. Martinez-Salgado C, Benckendorff AG, Chiang LY, Wang R, Milenkovic N, Wetzel C, Hu J, Stucky CL, Parra MG, Mohandas N, Lewin GR (2007) Stomatin and sensory neuron mechanotrans-duction. J Neurophysiol 98: 3802-3808
37. O'Hagan R, Chalfie M, Goodman MB (2005) The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals. Nat Neurosci 8: 43-50
38. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326
39. Owczarek CM, Treutlein HR, Portbury KJ, Gulluyan LM, Kola I, Hertzog PJ (2001) A novel member of the STOMATIN/EPB72/mec-2 family, stomatin-like 2 (STOML2), is ubiquitously expressed and localizes to HSA chromosome 9p13.1. Cytogenet Cell Genet 92: 196-203
40. Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJ, Evans PR, McMahon HT (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303: 495-499
41. Poole K, Lechner SG, Lewin GR (2011) The molecular and genetic basis of touch. In The Handbook of Touch, Hertenstein MJ, Weiss SJ (eds) pp 59-84. New York, USA: Springer Publications
42. Price MP, Thompson RJ, Eshcol JO, Wemmie JA, Benson CJ (2004) Stomatin modulates gating of acid-sensing ion channels. J Biol Chem 279: 53886-53891
43. Salzer U, Ahorn H, Prohaska R (1993) Identification of the phos-phorylation site on human erythrocyte band 7 integral membrane protein: implications for a monotopic protein structure. Biochim Biophys Acta 1151: 149-152
44. Schrödinger LLC (2003) The PyMOL Molecular Graphics System. Version 1.4.1
45. Seidel G, Prohaska R (1998) Molecular cloning of hSLP-1, a novel human brain-specific member of the band 7/MEC-2 family similar to Caenorhabditis elegans UNC-24. Gene 225: 23-29
46. Shimada A, Niwa H, Tsujita K, Suetsugu S, Nitta K, Hanawa-Suetsugu K, Akasaka R, Nishino Y, Toyama M, Chen L, Liu ZJ, Wang BC, Yamamoto M, Terada T, Miyazawa A, Tanaka A, Sugano S, Shirouzu M, Nagayama K, Takenawa T et al (2007) Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 129: 761-772
47. Smith ES, Lewin GR (2009) Nociceptors: a phylogenetic view. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 195: 1089-1106
48. Smith ES, Zhang X, Cadiou H, McNaughton PA (2007) Proton binding sites involved in the activation of acid-sensing ion channel ASIC2a. Neurosci Lett 426: 12-17
49. Snyers L, Umlauf E, Prohaska R (1998) Oligomeric nature of the integral membrane protein stomatin. J Biol Chem 273: 17221-17226
50. Snyers L, Umlauf E, Prohaska R (1999a) Association of stomatin with lipid-protein complexes in the plasma membrane and the endocytic compartment. Eur J Cell Biol 78: 802-812
51. Snyers L, Umlauf E, Prohaska R (1999b) Cysteine 29 is the major palmitoylation site on stomatin. FEBS Lett 449: 101-104
52. Steinkellner G, Rader R, Thallinger GG, Kratky C, Gruber K (2009) VASCo: computation and visualization of annotated protein surface contacts. BMC Bioinformatics 10: 32
53. Stewart GW, Hepworth-Jones BE, Keen JN, Dash BC, Argent AC, Casimir CM (1992) Isolation of cDNA coding for an ubiquitous membrane protein deficient in high Na +, low K + stomatocytic erythrocytes. Blood 79: 1593-1601
54. Tanaka H, Kato K, Yamashita E, Sumizawa T, Zhou Y, Yao M, Iwasaki K, Yoshimura M, Tsukihara T (2009) The structure of rat liver vault at 3.5 angstrom resolution. Science 323: 384-388
55. Tatsuta T, Model K, Langer T (2005) Formation of membrane-bound ring complexes by prohibitins in mitochondria. Mol Biol Cell 16: 248-259
56. Umlauf E, Csaszar E, Moertelmaier M, Schuetz GJ, Parton RG, Prohaska R (2004) Association of stomatin with lipid bodies. J Biol Chem 279: 23699-23709
57. Umlauf E, Mairhofer M, Prohaska R (2006) Characterization of the stomatin domain involved in homo-oligomerization and lipid raft association. J Biol Chem 281: 23349-23356
58. Unfried I, Entler B, Prohaska R (1995) The organization of the gene (EPB72) encoding the human erythrocyte band 7 integral membrane protein (protein 7.2b). Genomics 30: 521-528
59. Vagin A, Teplyakov A (1997) MOLREP: an automated program for molecular replacement. J Appl Cryst 30: 1022-1025
60. Wetzel C, Hu J, Riethmacher D, Benckendorff A, Harder L, Eilers A, Moshourab R, Kozlenkov A, Labuz D, Caspani O, Erdmann B, Machelska H, Heppenstall PA, Lewin GR (2007) A stomatin-domain protein essential for touch sensation in the mouse. Nature 445: 206-209
61. Whitmore L, Wallace BA (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res 32: W668-W673
62. Yokoyama H, Fujii S, Matsui I (2008) Crystal structure of a core domain of stomatin from Pyrococcus horikoshii Illustrates a novel trimeric and coiled-coil fold. J Mol Biol 376: 868-878
63. Zhu Y Paszty C, Turetsky T, Tsai S, Kuypers FA, Lee G, Cooper P, Gallagher PG, Stevens ME, Rubin E, Mohandas N, Mentzer WC (1999) Stomatocytosis is absent in 'stomatin'-deficient murine red blood cells. Blood 93: 2404-2410