Islet cholesterol accumulation due to loss of ABCA1 leads to impaired exocytosis of insulin granules

Diabetes

Volumn 60, Issue 12, 2011, Pages 3186-3196

  Kruit, Janine K ^a   Wijesekara, Nadeeja ^a   Manning Fox, Jocelyn E ^b   Dai, Xiao Qing ^b   Brunham, Liam R ^a   Searle, Gavin J ^b   Morgan, Garry P ^c   Costin, Adam J ^c   Tang, Renmei ^a   Bhattacharjee, Alpana ^a   Johnson, James D ^d   Light, Peter E ^b   Marsh, Brad J ^c   MacDonald, Patrick E ^b   Verchere, C Bruce ^a   Hayden, Michael R ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER A1; ION CHANNEL; PROINSULIN; SYNAPTOBREVIN 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM TRANSPORT; CELL MEMBRANE; CELL STRUCTURE; CELL ULTRASTRUCTURE; CHOLESTEROL METABOLISM; CONTROLLED STUDY; ELECTRON MICROSCOPY; EXOCYTOSIS; GOLGI COMPLEX; INSULIN RELEASE; LIPID RAFT; MEMBRANE STRUCTURE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PATCH CLAMP; PRIORITY JOURNAL;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BLOTTING, WESTERN; CALCIUM; CALCIUM CHANNELS; CELL LINE; CELL LINE, TUMOR; CELL MEMBRANE; CHOLESTEROL; ELECTROPHYSIOLOGY; EXOCYTOSIS; GLUCOSE INTOLERANCE; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION;

EID: 82255164672     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db11-0081     Document Type: Article

References (50)

1. Brunham LR, Kruit JK, Verchere CB, Hayden MR. Cholesterol in islet dysfunction and type 2 diabetes. J Clin Invest 2008;118:403-408 (Pubitemid 351206525)
2. Adiels M, Olofsson SO, Taskinen MR, Borén J. Diabetic dyslipidaemia. Curr Opin Lipidol 2006;17:238-246 (Pubitemid 43786057)
3. von Eckardstein A, Schulte H, Assmann G. Risk for diabetes mellitus in middle-aged Caucasian male participants of the PROCAMstudy: implications for the definition of impaired fasting glucose by the American Diabetes Association. Prospective Cardiovascular Münster. J Clin Endocrinol Metab 2000;85:3101-3108
4. Hermans MP, Ahn SA, Rousseau MF. log(TG)/HDL-C is related to both residual cardiometabolic risk and β-cell function loss in type 2 diabetes males. Cardiovasc Diabetol 2010;9:88
5. Brunham LR, Kruit JK, Pape TD, et al. Beta-cell ABCA1 influences insulin secretion, glucose homeostasis and response to thiazolidinedione treatment. Nat Med 2007;13:340-347 (Pubitemid 46376682)
6. Kruit JK, Kremer PH, Dai L, et al. Cholesterol efflux via ATP-binding cassette transporter A1 (ABCA1) and cholesterol uptake via the LDL receptor influences cholesterol-induced impairment of beta cell function in mice. Diabetologia 2010;53:1110-1119
7. Hao M, Head WS, Gunawardana SC, Hasty AH, Piston DW. Direct effect of cholesterol on insulin secretion: a novel mechanism for pancreatic betacell dysfunction. Diabetes 2007;56:2328-2338 (Pubitemid 47358240)
8. Cnop M, Hannaert JC, Grupping AY, Pipeleers DG. Low density lipoprotein can cause death of islet beta-cells by its cellular uptake and oxidative modification. Endocrinology 2002;143:3449-3453 (Pubitemid 34925718)
9. Peyot ML, Pepin E, Lamontagne J, et al. Beta-cell failure in diet-induced obese mice stratified according to body weight gain: secretory dysfunction and altered islet lipid metabolism without steatosis or reduced beta-cell mass. Diabetes 2010;59:2178-2187
10. Drew BG, Duffy SJ, Formosa MF, et al. High-density lipoprotein modulates glucose metabolism in patients with type 2 diabetes mellitus. Circulation 2009;119:2103-2111
11. Vergeer M, Brunham LR, Koetsveld J, et al. Carriers of loss-of-function mutations in ABCA1 display pancreatic beta-cell dysfunction. Diabetes Care 2010;33:869-874
12. Brunham LR, Singaraja RR, Duong M, et al. Tissue-specific roles of ABCA1 influence susceptibility to atherosclerosis. Arterioscler Thromb Vasc Biol 2009;29:548-554
13. Wijesekara N, Dai FF, Hardy AB, et al. Beta cell-specific Znt8 deletion in mice causes marked defects in insulin processing, crystallisation and secretion. Diabetologia 2010;53:1656-1668
14. Johnson JD, Ahmed NT, Luciani DS, et al. Increased islet apoptosis in Pdx1+/- mice. J Clin Invest 2003;111:1147-1160 (Pubitemid 36519932)
15. Dai XQ, Kolic J, Marchi P, Sipione S, Macdonald PE. SUMOylation regulates Kv2.1 and modulates pancreatic beta-cell excitability. J Cell Sci 2009;122:775-779
16. Pigeau GM, Kolic J, Ball BJ, et al. Insulin granule recruitment and exocytosis is dependent on p110gamma in insulinoma and human beta-cells. Diabetes 2009;58:2084-2092
17. Marsh BJ, Volkmann N, McIntosh JR, Howell KE. Direct continuities between cisternae at different levels of the Golgi complex in glucose-stimulated mouse islet beta cells. Proc Natl Acad Sci U S A 2004;101:5565-5570 (Pubitemid 38481196)
18. Berglund ED, Li CY, Poffenberger G, et al. Glucose metabolism in vivo in four commonly used inbred mouse strains. Diabetes 2008;57:1790-1799
19. Rorsman P, Renström E. Insulin granule dynamics in pancreatic beta cells. Diabetologia 2003;46:1029-1045 (Pubitemid 37041234)
20. Lee AK, Yeung-Yam-Wah V, Tse FW, Tse A. Cholesterol elevation impairs glucose-stimulated Ca2+ signaling in mouse pancreatic {beta}-cells. Endocrinology 2011;152:3351-3361
21. Barg S, Eliasson L, Renström E, Rorsman P. A subset of 50 secretory granules in close contact with L-type Ca2+ channels accounts for firstphase insulin secretion in mouse beta-cells. Diabetes 2002;51(Suppl. 1):S74-S82 (Pubitemid 34761498)
22. Xia F, Gao X, Kwan E, et al. Disruption of pancreatic beta-cell lipid rafts modifies Kv2.1 channel gating and insulin exocytosis. J Biol Chem 2004;279:24685-24691 (Pubitemid 38725336)
23. Takahashi N, Kishimoto T, Nemoto T, Kadowaki T, Kasai H. Fusion pore dynamics and insulin granule exocytosis in the pancreatic islet. Science 2002;297:1349-1352 (Pubitemid 34913173)
24. Smukler SR, Tang L, Wheeler MB, Salapatek AM. Exogenous nitric oxide and endogenous glucose-stimulated beta-cell nitric oxide augment insulin release. Diabetes 2002;51:3450-3460 (Pubitemid 35403449)
25. Kwan EP, Gaisano HY. Glucagon-like peptide 1 regulates sequential and compound exocytosis in pancreatic islet beta-cells. Diabetes 2005;54:2734-2743 (Pubitemid 41233597)
26. MacDonald PE, Obermüller S, Vikman J, Galvanovskis J, Rorsman P, Eliasson L. Regulated exocytosis and kiss-and-run of synaptic-like microvesicles in INS-1 and primary rat beta-cells. Diabetes 2005;54:736-743 (Pubitemid 40322076)
27. Ladinsky MS, Wu CC, McIntosh S, McIntosh JR, Howell KE. Structure of the Golgi and distribution of reporter molecules at 20 degrees C reveals the complexity of the exit compartments. Mol Biol Cell 2002;13:2810-2825
28. Eliasson L, Abdulkader F, Braun M, Galvanovskis J, Hoppa MB, Rorsman P. Novel aspects of the molecular mechanisms controlling insulin secretion. J Physiol 2008;586:3313-3324 (Pubitemid 352003868)
29. Lang T. SNARE proteins and 'membrane rafts'. J Physiol 2007;585:693-698
30. Chamberlain LH, Burgoyne RD, Gould GW. SNARE proteins are highly enriched in lipid rafts in PC12 cells: implications for the spatial control of exocytosis. Proc Natl Acad Sci U S A 2001;98:5619-5624 (Pubitemid 32435691)
31. Pike LJ, Casey L. Cholesterol levels modulate EGF receptor-mediated signaling by altering receptor function and trafficking. Biochemistry 2002;41:10315-10322 (Pubitemid 34856457)
32. Zhuang L, Lin J, Lu ML, Solomon KR, Freeman MR. Cholesterol-rich lipid rafts mediate Akt-regulated survival in prostate cancer cells. Cancer Res 2002;62:2227-2231 (Pubitemid 34411694)
33. Paila YD, Chattopadhyay A. Membrane cholesterol in the function and organization of G-protein coupled receptors. Subcell Biochem 2010;51:439-466
34. Navratil AM, Bliss SP, Roberson MS. Membrane rafts and GnRH receptor signaling. Brain Res 2010;1364:53-61
35. Chen YG. Endocytic regulation of TGF-beta signaling. Cell Res 2009;19:58-70
36. Gerin I, Dolinsky VW, Shackman JG, et al. LXRbeta is required for adipocyte growth, glucose homeostasis, and beta cell function. J Biol Chem 2005;280:23024-23031 (Pubitemid 40861694)
37. Flowers JB, Rabaglia ME, Schueler KL, et al. Loss of stearoyl-CoA desaturase-1 improves insulin sensitivity in lean mice but worsens diabetes in leptindeficient obese mice. Diabetes 2007;56:1228-1239 (Pubitemid 46715602)
38. Ishikawa M, Iwasaki Y, Yatoh S, et al. Cholesterol accumulation and diabetes in pancreatic beta-cell-specific SREBP-2 transgenic mice: a new model for lipotoxicity. J Lipid Res 2008;49:2524-2534
39. Churchward MA, Coorssen JR. Cholesterol, regulated exocytosis and the physiological fusion machine. Biochem J 2009;423:1-14
40. Chang J, Kim SA, Lu X, Su Z, Kim SK, Shin YK. Fusion step-specific influence of cholesterol on SNARE-mediated membrane fusion. Biophys J 2009;96:1839-1846
41. Murray DH, Tamm LK. Clustering of syntaxin-1A in model membranes is modulated by phosphatidylinositol 4,5-bisphosphate and cholesterol. Biochemistry 2009;48:4617-4625
42. Tong J, Borbat PP, Freed JH, Shin YK. A scissors mechanism for stimulation of SNARE-mediated lipid mixing by cholesterol. Proc Natl Acad Sci U S A 2009;106:5141-5146
43. Churchward MA, Rogasevskaia T, Höfgen J, Bau J, Coorssen JR. Cholesterol facilitates the native mechanism of Ca2+-triggered membrane fusion. J Cell Sci 2005;118:4833-4848 (Pubitemid 41646391)
44. Rickman C, Medine CN, Dun AR, et al. t-SNARE protein conformations patterned by the lipid microenvironment. J Biol Chem 2010;285:13535-13541
45. Sturek JM, Castle JD, Trace AP, et al. An intracellular role for ABCG1-mediated cholesterol transport in the regulated secretory pathway of mouse pancreatic beta cells. J Clin Invest 2010;120:2575-2589
46. Wang N, Lan D, Chen W, Matsuura F, Tall AR. ATP-binding cassette transporters G1 and G4 mediate cellular cholesterol efflux to high-density lipoproteins. Proc Natl Acad Sci U S A 2004;101:9774-9779 (Pubitemid 38869312)
47. Barg S, Ma X, Eliasson L, et al. Fast exocytosis with few Ca(2+) channels in insulin-secreting mouse pancreatic B cells. Biophys J 2001;81:3308-3323 (Pubitemid 33111478)
48. Hansen GH, Niels-Christiansen LL, Thorsen E, Immerdal L, Danielsen EM. Cholesterol depletion of enterocytes. Effect on the Golgi complex and apical membrane trafficking. J Biol Chem 2000;275:5136-5142 (Pubitemid 30108916)
49. Ying M, Grimmer S, Iversen TG, Van Deurs B, Sandvig K. Cholesterol loading induces a block in the exit of VSVG from the TGN. Traffic 2003;4:772-784 (Pubitemid 37361857)
50. Orsó E, Broccardo C, Kaminski WE, et al. Transport of lipids from Golgi to plasma membrane is defective in Tangier disease patients and Abc1-deficient mice. Nat Genet 2000;24:192-196 (Pubitemid 30094724)