Sphingosine-1-phosphate is a novel regulator of cystic fibrosis transmembrane conductance regulator (CFTR) activity

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Malik, Firhan A ^a   Meissner, Anja ^a,b   Semenkov, Illya ^a   Molinski, Steven ^a,c   Pasyk, Stan ^a,c   Ahmadi, Saumel ^a,c   Bui, Hai H ^d   Bear, Christine E ^a,c   Lidington, Darcy ^a,e   Bolz, Steffen Sebastian ^a,e,f  

^a UNIVERSITY OF TORONTO   (Canada)

^b INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^c HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^d ELI LILLY AND COMPANY   (United States)

^e ST MICHAEL'S HOSPITAL   (Canada)

^f UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; FORSKOLIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; IODIDE; LYSOPHOSPHOLIPID; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYSTIC FIBROSIS; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME MECHANISM; ENZYME REGULATION; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CELL LINE; GENETICS; HAMSTER; HUMAN; METABOLISM; MUTATION;

CRICETINAE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CELL LINE; CRICETINAE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; HUMANS; IODIDES; LYSOPHOSPHOLIPIDS; MICE; MICE, INBRED C57BL; MUTATION; RECEPTORS, LYSOSPHINGOLIPID; SIGNAL TRANSDUCTION; SPHINGOSINE;

EID: 84937950714     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0130313     Document Type: Article

References (40)

1. Bolz SS, Vogel L, Sollinger D, Derwand R, Boer C, Pitson SM, et al. Sphingosine kinase modulates microvascular tone and myogenic responses through activation of RhoA/Rho kinase. Circulation. 2003; 108: 342-347. PMID: 12847068
2. Lidington D, Peter BF, Meissner A, Kroetsch JT, Pitson SM, Pohl U, et al. The phosphorylation motif at serine 225 governs the localization and function of sphingosine kinase 1 in resistance arteries. Arterioscler Thromb Vasc Biol. 2009; 29: 1916-1922. doi: 10.1161/ATVBAHA.109.194803 PMID: 19729605
3. Lim M, Choi SK, Cho YE, Yeon SI, Kim EC, Ahn DS, et al. The role of sphingosine kinase 1/sphingosine- 1-phosphate pathway in the myogenic tone of posterior cerebral arteries. PLoS One. 2012; 7: e35177. doi: 10.1371/journal.pone.0035177 PMID: 22532844
4. Lidington D, Schubert R, Bolz SS. Capitalizing on diversity: an integrative approach towards the multiplicity of cellular mechanisms underlying myogenic responsiveness. Cardiovasc Res. 2013; 97: 404-412. doi: 10.1093/cvr/cvs345 PMID: 23180720
5. Peter BF, Lidington D, Harada A, Bolz HJ, Vogel L, Heximer S, et al. Role of sphingosine-1-phosphate phosphohydrolase 1 in the regulation of resistance artery tone. Circ Res. 2008; 103: 315-324. doi: 10. 1161/CIRCRESAHA.108.173575 PMID: 18583713
6. Meissner A, Yang J, Kroetsch JT, Sauvé M, Dax H, Momen A, et al. Tumor Necrosis Factor-α-Mediated Downregulation of the Cystic Fibrosis Transmembrane Conductance Regulator Drives Pathological Sphingosine-1-Phosphate Signaling in a Mouse Model of Heart Failure. Circulation. 2012; 125: 2739-2750. doi: 10.1161/CIRCULATIONAHA.111.047316 PMID: 22534621
7. Levine YC, Li GK, Michel T. Agonist-modulated regulation of AMP-activated protein kinase (AMPK) in endothelial cells. Evidence for an AMPK-> Rac1 -> Akt-> endothelial nitric-oxide synthase pathway. J Biol Chem. 2007; 282: 20351-20364. PMID: 17519230
8. Kimura T, Tomura H, Sato K, Ito M, Matsuoka I, Im DS, et al. Mechanism and role of high density lipoprotein- induced activation of AMP-activated protein kinase in endothelial cells. J Biol Chem. 2010; 285: 4387-4397. doi: 10.1074/jbc.M109.043869 PMID: 20018878
9. Wilkinson DJ, Strong TV, Mansoura MK, Wood DL, Smith SS, Collins FS, et al. CFTR activation: additive effects of stimulatory and inhibitory phosphorylation sites in the R domain. Am J Physiol. 1997; 273: L127-L133. PMID: 9252549
10. Kongsuphol P, Cassidy D, Hieke B, Treharne KJ, Schreiber R, Mehta A, et al. Mechanistic insight into control of CFTR by AMPK. J Biol Chem. 2009; 284: 5645-5653. doi: 10.1074/jbc.M806780200 PMID: 19095655
11. Steinberg GR, Kemp BE. AMPK in Health and Disease. Physiol Rev. 2009; 89: 1025-1078. doi: 10. 1152/physrev.00011.2008 PMID: 19584320
12. Carling D, Sanders MJ, Woods A. The regulation of AMP-activated protein kinase by upstream kinases. Int J Obes (Lond). 2008; 32 Suppl 4: S55-S59.
13. Suter M, Riek U, Tuerk R, Schlattner U, Wallimann T, Neumann D. Dissecting the role of 5'-AMP for allosteric stimulation, activation, and deactivation of AMP-activated protein kinase. J Biol Chem. 2006; 281: 32207-32216. PMID: 16943194
14. Spiegel S, Milstien S. Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat Rev Mol Cell Biol. 2003; 4: 397-407. PMID: 12728273
15. van Doorninck JH, French PJ, Verbeek E, Peters RH, Morreau H, Bijman J, et al. A mouse model for the cystic fibrosis delta F508 mutation. EMBO J. 1995; 14: 4403-4411. PMID: 7556083
16. Hoefer J, Azam MA, Kroetsch JT, Leong-Poi H, Momen MA, Voigtlaender-Bolz J, et al. Sphingosine-1- phosphate-dependent activation of p38 MAPK maintains elevated peripheral resistance in heart failure through increased myogenic vasoconstriction. Circ Res. 2010; 107: 923-933. doi: 10.1161/ CIRCRESAHA.110.226464 PMID: 20671234
17. Sharma M, Benharouga M, Hu W, Lukacs GL. Conformational and temperature-sensitive stability defects of the delta F508 cystic fibrosis transmembrane conductance regulator in post-endoplasmic reticulum compartments. J Biol Chem. 2001; 276: 8942-8950. PMID: 11124952
18. Wellhauser L, Kim Chiaw P, Pasyk S, Li C, Ramjeesingh M, Bear CE. A small-molecule modulator interacts directly with deltaPhe508-CFTR to modify its ATPase activity and conformational stability. Mol Pharmacol. 2009; 75: 1430-1438. doi: 10.1124/mol.109.055608 PMID: 19339490
19. Yu W, Kim Chiaw P, Bear CE. Probing conformational rescue induced by a chemical corrector of F508del-cystic fibrosis transmembrane conductance regulator (CFTR) mutant. J Biol Chem. 2011; 286: 24714-24725. doi: 10.1074/jbc.M111.239699 PMID: 21602569
20. Pasyk S, Li C, Ramjeesingh M, Bear CE. Direct interaction of a small-molecule modulator with G551DCFTR, a cystic fibrosis-causing mutation associated with severe disease. Biochem J. 2009; 418: 185-190. doi: 10.1042/BJ20081424 PMID: 18945216
21. Schmidt A, Hughes LK, Cai Z, Mendes F, Li H, Sheppard DN, et al. Prolonged treatment of cells with genistein modulates the expression and function of the cystic fibrosis transmembrane conductance regulator. Br J Pharmacol. 2008; 153: 1311-1323. doi: 10.1038/sj.bjp.0707663 PMID: 18223673
22. French PJ, van Doorninck JH, Peters RH, Verbeek E, Ameen NA, Marino CR, et al. A delta F508 mutation in mouse cystic fibrosis transmembrane conductance regulator results in a temperature-sensitive processing defect in vivo. J Clin Invest. 1996; 98: 1304-1312. PMID: 8823295
23. Lukacs GL, Chang XB, Bear C, Kartner N, Mohamed A, Riordan JR, et al. The delta F508 mutation decreases the stability of cystic fibrosis transmembrane conductance regulator in the plasma membrane. Determination of functional half-lives on transfected cells. J Biol Chem. 1993; 268: 21592-21598. PMID: 7691813
24. Denning GM, Anderson MP, Amara JF, Marshall J, Smith AE, Welsh MJ. Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature. 1992; 358: 761-764. PMID: 1380673
25. Yatomi Y, Igarashi Y, Yang L, Hisano N, Qi R, Asazuma N, et al. Sphingosine 1-phosphate, a bioactive sphingolipid abundantly stored in platelets, is a normal constituent of human plasma and serum. J Biochem. 1997; 121: 969-973. PMID: 9192741
26. Cheng SH, Rich DP, Marshall J, Gregory RJ, Welsh MJ, Smith AE. Phosphorylation of the R domain by cAMP-dependent protein kinase regulates the CFTR chloride channel. Cell. 1991; 66: 1027-1036. PMID: 1716180
27. Luz S, Cihil KM, Brautigan DL, Amaral MD, Farinha CM, Swiatecka-Urban A. LMTK2-mediated phosphorylation regulates CFTR endocytosis in human airway epithelial cells. J Biol Chem. 2014; 289: 15080-15093. doi: 10.1074/jbc.M114.563742 PMID: 24727471
28. Pasyk S, Molinski S, Ahmadi S, Ramjeesingh M, Huan LJ, Chin S, et al. The major cystic fibrosis causing mutation exhibits defective propensity for phosphorylation. Proteomics. 2015; 15: 447-461. doi: 10. 1002/pmic.201400218 PMID: 25330774
29. Picciotto MR, Cohn JA, Bertuzzi G, Greengard P, Nairn AC. Phosphorylation of the cystic fibrosis transmembrane conductance regulator. J Biol Chem. 1992; 267: 12742-12752. PMID: 1377674
30. Seibert FS, Linsdell P, Loo TW, Hanrahan JW, Clarke DM, Riordan JR. Disease-associated mutations in the fourth cytoplasmic loop of cystic fibrosis transmembrane conductance regulator compromise biosynthetic processing and chloride channel activity. J Biol Chem. 1996; 271: 15139-15145. PMID: 8662892
31. Chappe V, Hinkson DA, Zhu T, Chang XB, Riordan JR, Hanrahan JW. Phosphorylation of protein kinase C sites in NBD1 and the R domain control CFTR channel activation by PKA. J Physiol. 2003; 548: 39-52. PMID: 12588899
32. Hallows KR, Raghuram V, Kemp BE, Witters LA, Foskett JK. Inhibition of cystic fibrosis transmembrane conductance regulator by novel interaction with the metabolic sensor AMP-activated protein kinase. J Clin Invest. 2000; 105: 1711-1721. PMID: 10862786
33. Bannykh SI, Bannykh GI, Fish KN, Moyer BD, Riordan JR, Balch WE. Traffic pattern of cystic fibrosis transmembrane regulator through the early exocytic pathway. Traffic. 2000; 1: 852-870. PMID: 11208075
34. DalemansW, Hinnrasky J, Slos P, Dreyer D, Fuchey C, Pavirani A, et al. Immunocytochemical analysis reveals differences between the subcellular localization of normal and delta Phe508 recombinant cystic fibrosis transmembrane conductance regulator. Exp Cell Res. 1992; 201: 235-240. PMID: 1377133
35. Gee HY, Noh SH, Tang BL, Kim KH, Lee MG. Rescue of ΔF508-CFTR trafficking via a GRASP-dependent unconventional secretion pathway. Cell. 2011; 146: 746-760. doi: 10.1016/j.cell.2011.07.021 PMID: 21884936
36. Pedemonte N, Tomati V, Sondo E, Galietta LJ. Influence of cell background on pharmacological rescue of mutant CFTR. Am J Physiol Cell Physiol. 2010; 298: C866-C874. doi: 10.1152/ajpcell.00404.2009 PMID: 20053923
37. Wang Y, Bartlett MC, Loo TW, Clarke DM. Specific rescue of cystic fibrosis transmembrane conductance regulator processing mutants using pharmacological chaperones. Mol Pharmacol. 2006; 70: 297-302. PMID: 16624886
38. van Goor F, Straley KS, Cao D, González J, Hadida S, Hazlewood A, et al. Rescue of DeltaF508-CFTR trafficking and gating in human cystic fibrosis airway primary cultures by small molecules. Am J Physiol Lung Cell Mol Physiol. 2006; 290: L1117-L1130. PMID: 16443646
39. Bigaud M, Guerini D, Billich A, Bassilana F, Brinkmann V. Second generation S1P pathway modulators: research strategies and clinical developments. Biochim Biophys Acta. 2014; 1841: 745-758. doi: 10. 1016/j.bbalip.2013.11.001 PMID: 24239768
40. Yang J, Hossein Noyan-Ashraf M, Meissner A, Voigtlaender-Bolz J, Kroetsch JT, Foltz W, et al. Proximal Cerebral Arteries Develop Myogenic Responsiveness in Heart Failure via Tumor Necrosis Factor- α-Dependent Activation of Sphingosine-1-Phosphate Signaling. Circulation. 2012; 126: 196-206. doi: 10.1161/CIRCULATIONAHA.111.039644 PMID: 22668972