Saturated fatty acids alter the late secretory pathway by modulating membrane properties

Traffic

Volumn 14, Issue 12, 2013, Pages 1228-1241

  Payet, Laurie Anne ^a   Pineau, Ludovic ^b   Snyder, Ellen C R ^a   Colas, Jenny ^a   Moussa, Ahmed ^c   Vannier, Brigitte ^a   Bigay, Joelle ^d   Clarhaut, Jonathan ^e   Becq, Frédéric ^a   Berjeaud, Jean Marc ^a   Vandebrouck, Clarisse ^a   Ferreira, Thierry ^a  

^a UNIVERSITÉ DE POITIERS   (France)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c Abdelmalek Essaadi University   (Morocco)

^d INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^e POITIERS UNIVERSITY HOSPITAL   (France)

Author keywords

Arf GAP1; Loose lipid packing; Protein trafficking; trans Golgi network; Type 2 diabetes; Vesicular budding

Indexed keywords

CERAMIDE; PHOSPHOLIPID; SATURATED FATTY ACID;

ARTICLE; BIOSYNTHESIS; CELL MEMBRANE; CELL STRUCTURE; CELL SURFACE; CONTROLLED STUDY; GENETIC TRANSCRIPTION; GENOME; INTRACELLULAR MEMBRANE; LIPID STORAGE; LIPOTOXICITY; MAMMAL CELL; NONHUMAN; NUTRIENT; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SECRETORY PATHWAY; SECRETORY VESICLE; TRANS GOLGI NETWORK; UNFOLDED PROTEIN RESPONSE; YEAST;

ARF-GAP1; LOOSE LIPID PACKING; PROTEIN TRAFFICKING; TRANS-GOLGI NETWORK; TYPE 2 DIABETES; VESICULAR BUDDING;

CELL MEMBRANE; CERAMIDES; FATTY ACIDS; PHOSPHOLIPIDS; SACCHAROMYCES CEREVISIAE; SECRETORY PATHWAY; TRANS-GOLGI NETWORK; TRANSPORT VESICLES; UNFOLDED PROTEIN RESPONSE;

EID: 84887610278     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12117     Document Type: Article

References (51)

1. Kusminski C, Shetty S, Orci L, Unger R, Scherer P. Diabetes and apoptosis: lipotoxicity. Apoptosis 2009;14:1484-1495.
2. Sabin MA, De Hora M, Holly JMP, Hunt LP, Ford AL, Williams SR, Baker JS, Retallick CJ, Crowne EC, Shield JPH. Fasting nonesterified fatty acid profiles in childhood and their relationship with adiposity, insulin sensitivity, and lipid levels. Pediatrics 2007;120:e1426-e1433.
3. Hagman DK, Hays LB, Parazzoli SD, Poitout V. Palmitate inhibits insulin gene expression by altering PDX-1 nuclear localization and reducing MafA expression in isolated rat islets of langerhans. J Biol Chem 2005;280:32413-32418.
4. Diakogiannaki E, Morgan NG. Differential regulation of the ER stress response by long-chain fatty acids in the pancreatic beta-cell. Biochem Soc Trans 2008;36:959-962.
5. Dey D, Mukherjee M, Basu D, Datta M, Roy SS, Bandyopadhyay A, Bhattacharya S. Inhibition of insulin receptor gene expression and insulin signaling by fatty acid: interplay of PKC isoforms therein. Cell Physiol Biochem 2005;16:217-228.
6. Alkhateeb H, Chabowski A, Glatz JFC, Luiken JFP, Bonen A. Two phases of palmitate-induced insulin resistance in skeletal muscle: impaired GLUT4 translocation is followed by a reduced GLUT4 intrinsic activity. Am J Physiol: Endocrinol Metab 2007;293:E783-E793.
7. Tsuchiya Y, Hatakeyama H, Emoto N, Wagatsuma F, Matsushita S, Kanzaki M. Palmitate-induced down-regulation of sortilin and impaired GLUT4 trafficking in C2C12 myotubes. J Biol Chem 2010;285:34371-34381.
8. Boslem E, MacIntosh G, Preston AM, Bartley C, Busch AK, Fuller M, Laybutt DR, Meikle PJ, Biden TJ. A lipidomic screen of palmitate-treated MIN6 beta-cells links sphingolipid metabolites with endoplasmic reticulum (ER) stress and impaired protein trafficking. Biochem J 2011;435:267-276.
9. Holland WL, Summers SA. Sphingolipids, insulin resistance, and metabolic disease: new insights from in vivo manipulation of sphingolipid metabolism. Endocr Rev 2008;29:381-402.
10. Busch AK, Gurisik E, Cordery DV, Sudlow M, Denyer GS, Laybutt DR, Hughes WE, Biden TJ. Increased fatty acid desaturation and enhanced expression of stearoyl coenzyme a desaturase protects pancreatic {beta}-cells from lipoapoptosis. Diabetes 2005;54:2917-2924.
11. Pineau L, Colas J, Dupont S, Beney L, Fleurat-Lessard P, Berjeaud JM, Berges T, Ferreira T. Lipid-induced ER stress: synergistic effects of sterols and saturated fatty acids. Traffic 2009;10:673-690.
12. Borradaile NM, Han X, Harp JD, Gale SE, Ory DS, Schaffer JE. Disruption of endoplasmic reticulum structure and integrity in lipotoxic cell death. J Lipid Res 2006;47:2726-2737.
13. Pineau L, Ferreira T. Lipid-induced ER stress in yeast and beta cells: parallel trails to a common fate. FEMS Yeast Res 2010;10:1035-1045.
14. Maedler K, Oberholzer J, Bucher P, Spinas GA, Donath MY. Monounsaturated fatty acids prevent the deleterious effects of palmitate and high glucose on human pancreatic beta-cell turnover and function. Diabetes 2003;52:726-733.
15. Karki S, Chakrabarti P, Huang G, Wang H, Farmer SR, Kandror KV. The Multi-Level Action of Fatty Acids on Adiponectin Production by Fat Cells. PLoS ONE 2011;6:e28146.
16. Ferreira T, Regnacq M, Alimardani P, Moreau-Vauzelle C, Berges T. Lipid dynamics in yeast under haem-induced unsaturated fatty acid and / or sterol depletion. Biochem J 2004;378:899-908.
17. Pineau L, Bonifait L, Berjeaud JM, Alimardani-Theuil P, Berges T, Ferreira T. A lipid-mediated quality control process in the Golgi apparatus in yeast. Mol Biol Cell 2008;19:807-821.
18. Deguil J, Pineau L, Rowland Snyder EC, Dupont S, Beney L, Gil A, Frapper G, Ferreira T. Modulation of lipid-induced ER stress by fatty acid shape. Traffic 2011;12:349-362.
19. Songer JA, Munson M. Sec6p anchors the assembled exocyst complex at sites of secretion. Mol Biol Cell 2009;20:973-982.
20. Hsu VW, Yang J-S. Mechanisms of COPI vesicle formation. FEBS Lett 2009;583:3758-3763.
21. Stefan N, Peter A, Cegan A, Staiger H, Machann J, Schick F, Claussen C, Fritsche A, Häring H-U, Schleicher E. Low hepatic stearoyl-CoA desaturase 1 activity is associated with fatty liver and insulin resistance in obese humans. Diabetologia 2008;51:648-656.
22. Lyons TJ, Villa NY, Regalla LM, Kupchak BR, Vagstad A, Eide DJ. Metalloregulation of yeast membrane steroid receptor homologs. Proc Natl Acad Sci USA 2004;101:5506-5511.
23. Yamauchi T, Kamon J, Ito Y, Tsuchida A, Yokomizo T, Kita S, Sugiyama T, Miyagishi M, Hara K, Tsunoda M, Murakami K, Ohteki T, Uchida S, Takekawa S, Waki H, et al. Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 2003;423:762-769.
24. Ghosh AK, Ramakrishnan G, Rajasekharan R. YLR099C (ICT1) encodes a soluble acyl-CoA-dependent lysophosphatidic acid acyltransferase responsible for enhanced phospholipid synthesis on organic solvent stress in Saccharomyces cerevisiae. J Biol Chem 2008;283:9768-9775.
25. Riekhof WR, Wu J, Jones JL, Voelker DR. Identification and characterization of the major lysophosphatidylethanolamine Acyltransferase in Saccharomyces cerevisiae. J Biol Chem 2007;282:28344-28352.
26. Gijón MA, Riekhof WR, Zarini S, Murphy RC, Voelker DR. Lysophospholipid acyltransferases and arachidonate recycling in human neutrophils. J Biol Chem 2008;283:30235-30245.
27. Guo L, Zhou D, Pryse KM, Okunade AL, Su X. Fatty acid 2-hydroxylase mediates diffusional mobility of Raft-associated lipids, GLUT4 level, and lipogenesis in 3T3-L1 adipocytes. J Biol Chem 2010;285:25438-25447.
28. Dickson RC, Sumanasekera C, Lester RL. Functions and metabolism of sphingolipids in Saccharomyces cerevisiae. Prog Lipid Res 2006;45:447-465.
29. Surma MA, Klose C, Simons K. Lipid-dependent protein sorting at the trans-Golgi network. Biochim Biophys Acta: Mol Cell Biol Lipids 2012;1821:1059-1067.
30. Summers SA. Ceramides in insulin resistance and lipotoxicity. Prog Lipid Res 2006;45:42-72.
31. Guenther GG, Peralta ER, Rosales KR, Wong SY, Siskind LJ, Edinger AL. Ceramide starves cells to death by downregulating nutrient transporter proteins. Proc Natl Acad Sci USA 2008;105:17402-17407.
32. Chung N, Mao C, Heitman J, Hannun YA, Obeid LM. Phytosphingosine as a specific inhibitor of growth and nutrient import in Saccharomyces cerevisiae. J Biol Chem 2001;276:35614-35621.
33. Skrzypek MS, Nagiec MM, Lester RL, Dickson RC. Inhibition of amino acid transport by sphingoid long chain bases in Saccharomyces cerevisiae. J Biol Chem 1998;273:2829-2834.
34. Dickson RC. Thematic review series: sphingolipids: New insights into sphingolipid metabolism and function in budding yeast. J Lipid Res 2008;49:909-921.
35. Welsch CA, Roth LW, Goetschy JF, Movva NR. Genetic, biochemical, and transcriptional responses of Saccharomyces cerevisiae to the novel immunomodulator FTY720 largely mimic those of the natural sphingolipid phytosphingosine. J Biol Chem 2004;279:36720-36731.
36. Schneiter R, Brugger B, Sandhoff R, Zellnig G, Leber A, Lampl M, Athenstaedt K, Hrastnik C, Eder S, Daum G, Paltauf F, Wieland FT, Kohlwein SD. Electrospray ionization tandem mass spectrometry (ESI-MS/MS) analysis of the lipid molecular species composition of yeast subcellular membranes reveals acyl chain-based sorting/remodeling of distinct molecular species en route to the plasma membrane. J Cell Biol 1999;146:741-754.
37. Robinson M, Poon PP, Schindler C, Murray LE, Kama R, Gabriely G, Singer RA, Spang A, Johnston GC, Gerst JE. The Gcs1 Arf-GAP mediates Snc1, 2 v-SNARE retrieval to the Golgi in yeast. Mol Biol Cell 2006;17:1845-1858.
38. Poon PP, Nothwehr SF, Singer RA, Johnston GC. The Gcs1 and Age2 ArfGAP proteins provide overlapping essential function for transport from the yeast trans-Golgi network. J Cell Biol 2001;155:1239-1250.
39. Bigay J, Casella JF, Drin G, Mesmin B, Antonny B. ArfGAP1 responds to membrane curvature through the folding of a lipid packing sensor motif. EMBO J 2005;24:2244-2253.
40. Preston A, Gurisik E, Bartley C, Laybutt D, Biden T. Reduced endoplasmic reticulum (ER)-to-Golgi protein trafficking contributes to ER stress in lipotoxic mouse beta cells by promoting protein overload. Diabetologia 2009;52:2369-2373.
41. Lang F, Ullrich S, Gulbins E. Ceramide formation as a target in beta-cell survival and function. Expert Opin Ther Targets 2011;15:1061-1071.
42. Lupi R, Dotta F, Marselli L, Del Guerra S, Masini M, Santangelo C, Patané G, Boggi U, Piro S, Anello M, Bergamini E, Mosca F, Di Mario U, Del Prato S, Marchetti P. Prolonged exposure to free fatty acids has cytostatic and pro-apoptotic effects on human pancreatic islets. Diabetes 2002;51:1437-1442.
43. Antonny B. Membrane deformation by protein coats. Curr Opin Cell Biol 2006;18:386-394.
44. Marchal C, Dupre S, Urban-Grimal D. Casein kinase I controls a late step in the endocytic trafficking of yeast uracil permease. J Cell Sci 2002;115:217-226.
45. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003;4:249-264.
46. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001;98:5116-5121.
47. Stewart JCM. Colorimetric determination of phospholipids with ammonium ferrothiocyanate. Anal Biochem 1980;104:10-14.
48. Cox JS, Walter P. A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 1996;87:391-404.
49. Nalaskowski MM, Fliegert R, Ernst O, Brehm MA, Fanick W, Windhorst S, Lin H, Giehler S, Hein J, Lin YN, Mayr GW. Human inositol 1, 4, 5-trisphosphate 3-kinase isoform B (IP3KB) is a nucleocytoplasmic shuttling protein specifically enriched at cortical actin filaments and at invaginations of the nuclear envelope. J Biol Chem 2011;286:4500-4510.
50. Glauert AM, Lewis PR. Biological Specimen Preparation for Transmission Electron Microscopy. USA: Princeton University Press, Princeton, New Jersey; 1998.
51. Poon PP, Cassel D, Huber I, Singer RA, Johnston GC. Expression, analysis, and properties of yeast ADP-ribosylation factor (ARF) GTPase activating proteins (GAPs) Gcs1 and Glo3. Methods Enzymol 2001;329:317-324.