STAS domain structure and function

Cellular Physiology and Biochemistry

Volumn 28, Issue 3, 2011, Pages 407-422

  Sharma, Alok K ^a   Rigby, Alan C ^a   Alper, Seth L ^a  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

Acyl carrier protein; Bicarbonate; Carbonic anhydrase; Guanine nucleotides; SLC26; Stressosome; Sulfate transporter and anti sigma factor antagonist domain; SulP

Indexed keywords

AMINO ACID; ANION; ANION TRANSPORT PROTEIN; BACTERIAL RNA; CARBOHYDRATE; GUANINE NUCLEOTIDE BINDING PROTEIN; HYDROCARBON; INOSITOL PHOSPHATE; LIPID; MEMBRANE PROTEIN; NUCLEOTIDASE; OXYGEN; PENDRIN; PHOSPHOPROTEIN; POLYPEPTIDE; PROTEIN SERINE THREONINE KINASE; RNA POLYMERASE; SCAFFOLD PROTEIN; STAS DOMAIN PROTEIN; SULFATE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VITAMIN;

ALPHA HELIX; AMINO ACID SEQUENCE; ANION TRANSPORT; BETA SHEET; ENZYME METABOLISM; GENE TARGETING; METABOLOME; MOLECULAR INTERACTION; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; SULFATE TRANSPORTER AND ANTI SIGMA FACTOR ANTAGONIST DOMAIN;

EID: 82255196445     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000335104     Document Type: Review

References (75)

1. Everett LA, Glaser B, Beck JC, Idol JR, Buchs A, Heyman M, Adawi F, Hazani E, Nassir E, Baxevanis AD, Sheffield VC, Green ED: Pendred syndrome is caused by mutations in a putative sulphate transporter gene (PDS). Nat Genet 1997;17:411-422. (Pubitemid 27518389)
2. Hoglund P, Haila S, Socha J, Tomaszewski L, Saarialho-Kere U, Karjalainen-Lindsberg ML, Airola K, Holmberg C, de la Chapelle A, Kere J: Mutations of the down-regulated in adenoma (DRA) gene cause congenital chloride diarrhoea. Nat Genet 1996;14:316-319.
3. Mount DB, Romero MF: The SLC26 gene family of multifunctional anion exchangers. Pflugers Arch 2004;447:710-721. (Pubitemid 38241456)
4. Kere J: Overview of the SLC26 family and associated diseases. Novartis Found Symp 2006;273:2-11; disc. 11-18, 261-264.
5. Dorwart MR, Shcheynikov N, Yang D, Muallem S: The solute carrier 26 family of proteins in epithelial ion transport. Physiology 2008;23:104-114.
6. Price GD, Howitt SM: The cyanobacterial bicarbonate transporter bicA: Its physiological role and the implications of structural similarities with human SLC26 transporters. Biochem Cell Biol 2011;89:178-188.
7. Felce J, Saier MH Jr: Carbonic anhydrases fused to anion transporters of the sulP family: Evidence for a novel type of bicarbonate transporter. J Molec Microbiol Biotechnol 2004;8:169-176. (Pubitemid 41202240)
8. Aravind L, Koonin EV: The stas domain-a link between anion transporters and antisigma-factor antagonists. Curr Biol 2000;10:R53-55.
9. Campbell EA, Westblade LF, Darst SA: Regulation of bacterial RNA polymerase sigma factor activity: A structural perspective. Curr Opin Microbiol 2008;11:121-127.
10. Pasqualetto E, Aiello R, Gesiot L, Bonetto G, Bellanda M, Battistutta R: Structure of the cytosolic portion of the motor protein prestin and functional role of the STAS domain in SLC26/SulP anion transporters. J Molec Biol 2010;400:448-462.
11. Kovacs H, Comfort D, Lord M, Campbell ID, Yudkin MD: Solution structure of SpoIIAA, a phosphorylatable component of the system that regulates transcription factor sigmaf of Bacillus subtilis. Proc Natl Acad Sci USA 1998;95:5067-5071.
12. Seavers PR, Lewis RJ, Brannigan JA, Verschueren KH, Murshudov GN, Wilkinson AJ: Structure of the Bacillus cell fate determinant SpoIIAA in phosphorylated and unphosphorylated forms. Structure 2001;9:605-614. (Pubitemid 32695585)
13. Masuda S, Murakami KS, Wang S, Anders Olson C, Donigian J, Leon F, Darst SA, Campbell EA: Crystal structures of the ADP-and ATP-bound forms of the Bacillus anti-sigma factor SpoIIAB in complex with the anti-anti-sigma SpoIIAA. J Mol Biol 2004;340:941-956. (Pubitemid 38968693)
14. Najafi SM, Harris DA, Yudkin MD: The SpoIIAA protein of Bacillus subtilis has GTP-binding properties. J Bacteriol 1996;178:6632-6634. (Pubitemid 26374734)
15. Hecker M, Pane-Farre J, Volker U: Sigma b-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu Rev Microbiol 2007;61:215-236. (Pubitemid 350058207)
16. Marles-Wright J, Lewis RJ: The stressosome: Molecular architecture of a signalling hub. Biochem Soc Trans 2010;38:928-933.
17. Murray JW, Delumeau O, Lewis RJ: Structure of a nonheme globin in environmental stress signaling. Proc Natl Acad Sci USA 2005;102:17320-17325. (Pubitemid 41740864)
18. Kuo S, Demeler B, Haldenwang WG: The growth-promoting and stress response activities of the Bacillus subtilis GTP binding protein Obg are separable by mutation. J Bacteriol 2008;190:6625-6635.
19. Jurk M, Dorn M, Schmieder P: Blue flickers of hope: Secondary structure, dynamics, and putative dimerization interface of the blue-light receptor YtvA from Bacillus subtilis. Biochemistry 2011;50:8163-8171.
20. Avila-Perez M, Vreede J, Tang Y, Bende O, Losi A, Gartner W, Hellingwerf K: In vivo mutational analysis of YtvA from Bacillus subtilis: Mechanism of light activation of the general stress response. J Biol Chem 2009;284:24958-24964.
21. Tang Y, Cao Z, Livoti E, Krauss U, Jaeger KE, Gartner W, Losi A: Interdomain signalling in the blue-light sensing and GTP-binding protein YtvA: A mutagenesis study uncovering the importance of specific protein sites. Photochem Photobiol Sci 2010;9:47-56.
22. Buttani V, Gartner W, Losi A: NTPbinding properties of the blue-light receptor YtvA and effects of the E105l mutation. Eur Biophys J 2007;36:831-839. (Pubitemid 350092513)
23. Losi A: Flavin-based blue-light photosensors: A photobiophysics update. Photochem Photobiol 2007;83:1283-1300. (Pubitemid 350132622)
24. Buttani V, Losi A, Polverini E, Gartner W: Blue news: NTP binding properties of the blue-light sensitive YtvA protein from Bacillus subtilis. FEBS Lett 2006;580:3818-3822. (Pubitemid 43946872)
25. Nakasone Y, Hellingwerf KJ: On the binding of BODIPY-GTP by the photosensory protein YtvA from the common soil bacterium Bacillus subtilis. Photochem Photobiol 2011;87:542-547.
26. Herrou J, Crosson S: Function, structure and mechanism of bacterial photosensory LOV proteins. Nat Rev Microbiol 2011:9:713-723.
27. Price GD, Woodger FJ, Badger MR, Howitt SM, Tucker L: Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proc Natl Acad Sci USA 2004;101:18228-18233. (Pubitemid 40054102)
28. Shelden MC, Howitt SM, Price GD: Membrane topology of the cyanobacterial bicarbonate transporter, BicA, a member of the SulP (SLC26A) family. Molec Membr Biol 2011;27:12-23.
29. Zolotarev AS, Unnikrishnan M, Shmukler BE, Clark JS, Vandorpe DH, Grigorieff N, Rubin EJ, Alper SL: Increased sulfate uptake by E. Coli overexpressing the Slc26-related SulP protein RV1739c from Mycobacterium tuberculosis. Comp Biochem Physiol 2008;149:255-266.
30. Sharma AK, Ye L, Baer CE, Shanmugasundaram K, Alber T, Alper SL, Rigby AC: Solution structure of the guanine nucleotide-binding STAS domain of Slc26-related SulP protein RV1739c from Mycobacterium tuberculosis. J Biol Chem 2011;286:8534-8544.
31. Babu M, Greenblatt JF, Emili A, Strynadka NC, Reithmeier RA, Moraes TF: Structure of a Slc26 anion transporter STAS domain in complex with acyl carrier protein: Implications for E. Coli YchM in fatty acid metabolism. Structure 2010;18:1450-1462.
32. Compton EL, Karinou E, Naismith JH, Gabel F, Javelle A: Low resolution structure of a bacterial Slc26 transporter reveals dimeric stoichiometry and mobile intracellular domains. J Biol Chem 2011;286:27058-27067.
33. Nishimori I, Minakuchi T, Vullo D, Scozzafava A, Innocenti A, Supuran CT: Carbonic anhydrase inhibitors. Cloning, characterization, and inhibition studies of a new beta-carbonic anhydrase from Mycobacterium tuberculosis. J Med Chem 2009;52:3116-3120.
34. Du L, Sanchez C, Chen M, Edwards DJ, Shen B: The biosynthetic gene cluster for the antitumor drug bleomycin from Streptomyces verticillus atcc15003 supporting functional interactions between nonribosomal peptide synthetases and a polyketide synthase. Chem Biol 2000;7:623-642.
35. Lai JR, Koglin A, Walsh CT: Carrier protein structure and recognition in polyketide and nonribosomal peptide biosynthesis. Biochem 2006;45:14869-14879. (Pubitemid 44937000)
36. Fitzpatrick KL, Tyerman SD, Kaiser BN: Molybdate transport through the plant sulfate transporter Shst1. FEBS Lett 2008;582:1508-1513.
37. Ye H, Zhang XQ, Broughton S, Westcott S, Wu D, Lance R, Li C: A nonsense mutation in a putative sulphate transporter gene results in low phytic acid in barley. Funct Integr Genom 2011;11:103-110.
38. Davidian JC, Kopriva S: Regulation of sulfate uptake and assimilation-the same or not the same? Molec Plant 2010;3:314-325.
39. Buchner P, Takahashi H, Hawkesford MJ: Plant sulphate transporters: Coordination of uptake, intracellular and long-distance transport. J Exp Botany 2004;55:1765-1773. (Pubitemid 39123310)
40. Shibagaki N, Grossman AR: The role of the STAS domain in the function and biogenesis of a sulfate transporter as probed by random mutagenesis. J Biol Chem 2006;281:22964-22973.
41. Shibagaki N, Grossman AR: Binding of cysteine synthase to the STAS domain of sulfate transporter and its regulatory consequences. J Biol Chem 2010;285:25094-25102.
42. Ito T CB, King KA, Zalewski CK, Muskett J, Chattaraj P, Shawker T, Reynolds JC, Butman JA, Brewer CC, Wangemann P, Alper SL, Griffith AJ: SLC26A4 and phenotypes associated with enlargment of the vestibular aqueduct (EVA); Cell Physiol Biochem 2011;28:545-552.
43. Hastbacka J, Kerrebrock A, Mokkala K, Clines G, Lovett M, Kaitila I, de la Chapelle A, Lander ES: Identification of the finnish founder mutation for diastrophic dysplasia (DTD). Eur J Hum Genet 1999;7:664-670. (Pubitemid 29424057)
44. Liu XZ, Ouyang XM, Xia XJ, Zheng J, Pandya A, Li F, Du LL, Welch KO, Petit C, Smith RJ, Webb BT, Yan D, Arnos KS, Corey D, Dallos P, Nance WE, Chen ZY: Prestin, a cochlear motor protein, is defective in non-syndromic hearing loss. Hum Molec Genet 2003;12:1155-1162. (Pubitemid 36622147)
45. Zheng J, Shen W, He DZ, Long KB, Madison LD, Dallos P: Prestin is the motor protein of cochlear outer hair cells. Nature 2000;405:149-155. (Pubitemid 30313525)
46. Minor JS, Tang HY, Pereira FA, Alford RL: DNA sequence analysis of SLC26A5, encoding prestin, in a patient-control cohort: Identification of fourteen novel DNA sequence variations. PloS One 2009;4:e5762.
47. Dawson PA, Russell CS, Lee S, McLeay SC, van Dongen JM, Cowley DM, Clarke LA, Markovich D: Urolithiasis and hepatotoxicity are linked to the anion transporter Sat1 in mice. J Clin Invest 2010;120:706-712.
48. Jiang Z, Asplin JR, Evan AP, Rajendran VM, Velazquez H, Nottoli TP, Binder HJ, Aronson PS: Calcium oxalate urolithiasis in mice lacking anion transporter Slc26a6. Nat Genet 2006;38:474-478.
49. Xu J, Song P, Miller ML, Borgese F, Barone S, Riederer B, Wang Z, Alper SL, Forte JG, Shull GE, Ehrenfeld J, Seidler U, Soleimani M: Deletion of the chloride transporter Slc26a9 causes loss of tubulovesicles in parietal cells and impairs acid secretion in the stomach. Proc Natl Acad Sci USA 2008;105:17955-17960.
50. Xu J, Song P, Nakamura S, Miller M, Barone S, Alper SL, Riederer B, Bonhagen J, Arend LJ, Amlal H, Seidler U, Soleimani M: Deletion of the chloride transporter Slc26a7 causes distal renal tubular acidosis and impairs gastric acid secretion. J Biol Chem 2009;284:29470-29479.
51. Toure A, Lhuillier P, Gossen JA, Kuil CW, Lhote D, Jegou B, Escalier D, Gacon G: The testis anion transporter 1 (Slc26a8) is required for sperm terminal differentiation and male fertility in the mouse. Hum Molec Genet 2007;16:1783-1793. (Pubitemid 47244526)
52. Chernova MN, Jiang L, Shmukler BE, Schweinfest CW, Blanco P, Freedman SD, Stewart AK, Alper SL: Acute regulation of the SLC26A3 congenital chloride diarrhoea anion exchanger (DRA) expressed in Xenopus oocytes. J Physiol 2003;549:3-19. (Pubitemid 36626394)
53. Rouached H, Berthomieu P, El Kassis E, Cathala N, Catherinot V, Labesse G, Davidian JC, Fourcroy P: Structural and functional analysis of the C-terminal STAS (sulfate transporter and anti-sigma antagonist) domain of the Arabidopsis thaliana sulfate transporter Sultr1.2. J Biol Chem 2005;280:15976-15983. (Pubitemid 40616721)
54. Sali A, Potterton L, Yuan F, van Vlijmen H, Karplus M: Evaluation of comparative protein modeling by modeller. Proteins 1995;23:318-326.
55. Toure A, Morin L, Pineau C, Becq F, Dorseuil O, Gacon G: Tat1, a novel sulfate transporter specifically expressed in human male germ cells and potentially linked to Rho GTPase signaling. J Biol Chem 2001;276:20309-20315.
56. Lamprecht G, Heil A, Baisch S, Lin-Wu E, Yun CC, Kalbacher H, Gregor M, Seidler U: The down regulated in adenoma (DRA) gene product binds to the second PDZ domain of the NHE3 kinase regulatory protein (E3KARP), potentially linking intestinal Cl-/HCO3-exchange to Na+/H+ exchange. Biochem 2002;41:12336-12342.
57. Rossmann H, Jacob P, Baisch S, Hassoun R, Meier J, Natour D, Yahya K, Yun C, Biber J, Lackner KJ, Fiehn W, Gregor M, Seidler U, Lamprecht G: The Cftr associated protein Cap70 interacts with the apical Cl-/HCO3-exchanger DRA in rabbit small intestinal mucosa. Biochem 2005;44:4477-4487. (Pubitemid 40403990)
58. Lohi H, Lamprecht G, Markovich D, Heil A, Kujala M, Seidler U, Kere J: Isoforms of SLC26A6 mediate anion transport and have functional PDZ interaction domains. Am J Physiol Cell Physiol 2003;284:C769-779. (Pubitemid 36237529)
59. Li C, Naren AP: Analysis of CFTR interactome in the macromolecular complexes. Methods Mol Biol 2011;741:255-270.
60. Ko SB, Shcheynikov N, Choi JY, Luo X, Ishibashi K, Thomas PJ, Kim JY, Kim KH, Lee MG, Naruse S, Muallem S: A molecular mechanism for aberrant Cftrdependent HCO3-transport in cystic fibrosis. EMBO J 2002;21:5662-5672. (Pubitemid 35315266)
61. Ko SB, Zeng W, Dorwart MR, Luo X, Kim KH, Millen L, Goto H, Naruse S, Soyombo A, Thomas PJ, Muallem S: Gating of Cftr by the STAS domain of SLC26 transporters. Nat Cell Biol 2004;6:343-350. (Pubitemid 38584824)
62. Dorwart MR, Shcheynikov N, Baker JM, Forman-Kay JD, Muallem S, Thomas PJ: Congenital chloride-losing diarrhea causing mutations in the STAS domain result in misfolding and mistrafficking of SLC26A3. J Biol Chem 2008;283:8711-8722.
63. Wang Y, Soyombo AA, Shcheynikov N, Zeng W, Dorwart M, Marino CR, Thomas PJ, Muallem S: Slc26a6 regulates Cftr activity in vivo to determine pancreatic duct HCO3-secretion: Relevance to cystic fibrosis. EMBO J 2006;25:5049-5057. (Pubitemid 44658523)
64. Avella M, Borgese F, Ehrenfeld J: Characterization of the l683P mutation of SLC26A9 in Xenopus oocytes. Biochim Biophys Acta 2011;1810:577-583.
65. Chang MH, Plata C, Sindic A, Ranatunga WK, Chen AP, Zandi-Nejad K, Chan KW, Thompson J, Mount DB, Romero MF: SLC26A9 is inhibited by the R-region of the cystic fibrosis transmembrane conductance regulator via the STAS domain. J Biol Chem 2009;284:28306-28318.
66. Shcheynikov N, Yang D, Wang Y, Zeng W, Karniski LP, So I, Wall SM, Muallem S: The Slc26a4 transporter functions as an electroneutral Cl-/I-/HCO3-exchanger: Role of Slc26a4 and Slc26a6 in I-and HCO3-secretion and in regulation of Cftr in the parotid duct. J Physiol 2008;586:3813-3824.
67. Homma K, Miller KK, Anderson CT, Sengupta S, Du GG, Aguinaga S, Cheatham M, Dallos P, Zheng J: Interaction between Cftr and prestin (Slc26a5). Biochim Biophys Acta 2010;1798:1029-1040.
68. Bai JP, Surguchev A, Ogando Y, Song L, Bian S, Santos-Sacchi J, Navaratnam D: Prestin surface expression and activity are augmented by interaction with MAP1S, a microtubule-associated protein. J Biol Chem 2010;285:20834-20843.
69. Sengupta S, Miller KK, Homma K, Edge R, Cheatham MA, Dallos P, Zheng J: Interaction between the motor protein prestin and the transporter protein VAPA. Biochim Biophys Acta 2010;1803:796-804.
70. Zheng J, Anderson CT, Miller KK, Cheatham M, Dallos P: Identifying components of the hair-cell interactome involved in cochlear amplification. BMC Genomics 2009;10:127.
71. Marcotti W, Johnson SL, Kros CJ: A transiently expressed SK current sustains and modulates action potential activity in immature mouse inner hair cells. J Physiol 2004;560:691-708. (Pubitemid 39530111)
72. Wang Y, Guo N, Nathans J: The role of frizzled3 and frizzled6 in neural tube closure and in the planar polarity of innerear sensory hair cells. J Neurosci 2006;26:2147-2156. (Pubitemid 44699023)
73. Legendre K, Safieddine S, Kussel-Andermann P, Petit C, El-Amraoui A: Alpha2-betaV spectrin bridges the plasma membrane and cortical lattice in the lateral wall of the auditory outer hair cells. J Cell Sci 2008;121:3347-3356.
74. Humphrey W, Dalke A, Schulten K: Vmd: Visual molecular dynamics. J Molec Graphics 1996;14:33-38, 27-38. (Pubitemid 26152973)
75. Koradi R, Billeter M, Wuthrich K: Molmol: A program for display and analysis of macromolecular structures. J Molec Graphics 1996;14:51-55, 29-32. (Pubitemid 26152976)