Cholesterol biosynthesis pathway intermediates and inhibitors regulate glucose-stimulated insulin secretion and secretory granule formation in pancreatic β-cells

Endocrinology

Volumn 151, Issue 10, 2010, Pages 4705-4716

  Tsuchiya, Miho ^a   Hosaka, Masahiro ^a   Moriguchi, Tomohisa ^a   Zhang, Shaojuan ^a   Suda, Masayuki ^a   Yokota Hashimoto, Hiromi ^a   Shinozuka, Kazuo ^a   Takeuchi, Toshiyuki ^a  

^a GUNMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GERANYLGERANYL PYROPHOSPHATE; GLUCOSE; INSULIN; LOW DENSITY LIPOPROTEIN RECEPTOR; MEVALONIC ACID; MEVINOLIN; SECRETOGRANIN II; SQUALENE; CHOLESTEROL; CHROMOGRANIN; ENZYME INHIBITOR; HYPOCHOLESTEROLEMIC AGENT; SECRETOGRANIN III;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; DENSITY GRADIENT; ENDOCYTOSIS; FRACTIONATION; INSULIN RELEASE; LIPID ANALYSIS; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION; RAT; SECRETORY GRANULE; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CELL MEMBRANE; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; SECRETION (PROCESS); SECRETORY VESICLE; WISTAR RAT;

ANIMALS; ANTICHOLESTEREMIC AGENTS; CELL MEMBRANE; CELLS, CULTURED; CHOLESTEROL; CHROMOGRANINS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; GLUCOSE; INSULIN; INSULIN-SECRETING CELLS; LOVASTATIN; METABOLIC NETWORKS AND PATHWAYS; MEVALONIC ACID; MICE; RATS; RATS, WISTAR; SECRETORY VESICLES; SQUALENE;

EID: 77957254197     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-0623     Document Type: Article

References (54)

1. Dannies PS 1999 Protein hormone storage in secretory granules: mechanisms for concentration and sorting. Endocr Rev 20:3-21
2. Dhanvantari S, Loh YP 2000 Lipid raft association of carboxypeptidase E is necessary for its function as a regulated secretory pathway sorting receptor. J Biol Chem 275:29887-22993
3. Wang R, Hosaka M, Han L, Yokota-Hashimoto H, Suda M, Mitsushima D, Torii S, Takeuchi T 2006 Molecular probes for sensing the cholesterol composition of subcellular organelle membranes. Biochim Biophys Acta 1761:1169-1181
4. Pfrieger FW 2003 Role of cholesterol in synapse formation and function. Biochim Biophys Acta 1610:271-280
5. Nelson DL, Cox MM 2005 Lipid biosynthesis. In: Lehninger's principles of biochemistry. 4th ed. New York: W. H. Freeman; 787-832
6. Kowluru A 2003 Regulatory roles for small G proteins in the pancreatic β-cell: lessons from models of impaired insulin secretion. Am J Physiol Endocrinol Metab 285:E669-E684
7. Takai Y, Sasaki T, Matozaki T 2001 Small GTP-binding proteins. Physiol Rev 81:153-208
8. Yaekura K, Julyan R, Wicksteed BL, Hays LB, Alarcon C, Sommers S, Poitout V, Baskin DG, Wang Y, Philipson LH, Rhodes CJ 2003 Insulin secretory deficiency and glucose intolerance in Rab3A null mice. J Biol Chem 278:9715-9721
9. Kasai K, Fujita T, Gomi H, Izumi T 2008 Docking is not a prerequisite but a temporal constraint for fusion of secretory granules. Traffic 9:1191-1203
10. Nevins AK, Thurmond DC 2005 A direct interaction between Cdc42 and vesicle-associated membrane protein 2 regulates SNARE-dependent insulin exocytosis. J Biol Chem 280:1944-1952
11. McDonald P, Veluthakal R, Kaur H, Kowluru A 2007 Biologically active lipids promote trafficking and membrane association of Rac1 in insulin-secreting INS 832/13 cells. Am J Physiol Cell Physiol 292: C1216-1220
12. Veluthakal R, Kaur H, Goalstone M, Kowluru A 2007 Dominantnegative alpha-subunit of farnesyl- and geranyltransferase inhibits glucose-stimulated, but not KCl-stimulated, insulin secretion in INS 832/13 cells. Diabetes 56:204-210
13. Bretscher MS, Munro S 1993 Cholesterol and the Golgi apparatus. Science 261:1280-1281
14. Simons K, Ikonen E 2000 How cells handle cholesterol. Science 290:1721-1726
15. Lodish H, Berk A, Matsudaira P, Kaiser CA, Krieger M, Scott MP, Zipursky SL, Darnell J 2004 Biomembranes and cell architecture. In: Molecular cell biology. 5th ed. New York: Scientific American Press; 147-157
16. Hosaka M, Suda M, Sakai Y, Izumi T, Watanabe T, Takeuchi T 2004 Sercretogranin III binds to cholesterol in the secretory granule membrane as an adapter for chromogranin A. J Biol Chem 279: 3627-3634
17. Arnaoutova I, Smith AM, Coates LC, Sharpe JC, Dhanvantari S, Snell CR, Birch NP, Loh YP 2003 The prohormone processing enzyme PC3 is a lipid raft-associated transmembrane protein. Biochemistry 42:10445-10455
18. Blázquez M, Thiele C, Huttner WB, Docherty K, Shennan KIJ 2000 Involvement of the membrane lipid bilayer in sorting prohormone convertase 2 into the regulated secretory pathway. Biochem J 349: 843-852
19. Assadi M, Sharpe JC, Snell C, Loh YP 2004 The C-terminus of prohormone convertase 2 is sufficient and necessary for Raft association and sorting to the regulated secretory pathway. Biochemistry 43:7798-7807
20. Takeuchi T, Hosaka M 2008 Sorting mechanism of peptide hormones and biogenesis mechanism of secretory granules by secretogranin III, a cholesterol-binding protein, in endocrine cells. Curr Diabetes Rev 4:31-38
21. Gondré-Lewis MC, Petrache HI, Wassif CA, Harries D, Parsegian A, Porter FD, Loh YP 2006 Abnormal sterols in cholesterol-deficiency diseases cause secretory granule malformation and decreased membrane curvature. J Cell Sci 119:1876-1885
22. Moriguchi T, Hosaka M, Yosinari A, Ozaki A, Takeuchi T, Shinozuka K 2009 Cholesterol analogs labeled with novel silylated fluorescent compounds. Chem Lett 38:966-967
23. Sawada Y, Zhang B, Okajima F, Izumi T, Takeuchi T 2001 Parathyroid hormone-related protein increases pancreatic β-cellspecific functions in well-differentiated cells. Mol Cell Endocrinol 182:265-275
24. Ridsdale A, Denis M, Gougeon PY, Ngsee JK, Presley JF, Zha X 2006 Cholesterol is required for efficient endoplasmic reticulumto-Golgi transport of secretory membrane proteins. Mol Biol Cell 17:1593-1605
25. Lee J, Lee I, Park C, Kang WK 2006 Lovastatin-induced RhoA modulation and its effect on senescence in prostate cancer cells. Biochem Biophys Res Commun 339:748-754
26. Brusselmans K, Timmermans L, Van de Sande T, Van Veldhoven PP, Guan G, Shechter I, Claessens F, Verhoeven G, Swinnen JV 2007 Squalene synthase, a determinant of Raft-associated cholesterol and modulator of cancer cell proliferation. J Biol Chem 282:18777-18785
27. Proksch GJ, Bonderman DP 1978 A water-soluble cholesterol derivative for use in augmenting serum control materials. Clin Chem 24:1924-1926
28. Massy ZA, Guijarro C, Oda H, Kasiske BL, Keane WF, O'Donnell MP 1999 Importance of geranylgeranyl pyrophosphate for mesangial cell DNA synthesis. Kidney Int Suppl 71:80-83
29. Lerner EC, Qian Y, Hamilton AD, Sebti SM 1995 Disruption of oncogenic K-Ras4B processing and signaling by a potent geranylgeranyltransferase I inhibitor. J Biol Chem 270:26770-26773
30. Finder JD, Litz JL, Blaskovich MA, McGuire TF, Qian Y, Hamilton AD, Davies P, Sebti SM 1997 Inhibition of protein geranylgeranylation causes a superinduction of nitric-oxide synthase-2 by inter-leukin-1β in vascular smooth muscle cells. J Biol Chem 272:13484-13488
31. Grimmer S, Iversen TG, van Deurs B, Sandvig K 2000 Endosome to Golgi transport of ricin is regulated by cholesterol. Mol Biol Cell 11:4205-4216
32. Saito E, Wachi H, Sato F, Seyama Y 2008 7-Ketocholesterol, a major oxysterol, promotes Pi-induced vascular calcification in cultured smooth muscle cells. J Atheroscler Thromb 15:130-137
33. Gomi H, Mizutani S, Kasai K, Itohara S, Izumi T 2005 Granuphilin molecularly docks insulin granules to the fusion machinery. J Cell Biol 171:99-109
34. Stechly L, Morelle W, Dessein AF, André S, Grard G, Trinel D, Dejonghe MJ, Leteurtre E, Drobecq H, Trugnan G, Gabius HJ, Huet G 2009 Galectin-4-regulated delivery of glycoproteins to the brush border membrane of enterocyte-like cells. Traffic 10:438-450
35. Wang Y, Thiele C, Huttner WB 2000 Cholesterol is required for the formation of regulated and constitutive secretory vesicles from the trans-Golgi network. Traffic 1:952-962
36. Han L, Suda M, Tsuzuki K, Wang R, Ohe Y, Hirai H, Watanabe T, Takeuchi T, Hosaka M 2008 A large form of secretogranin III functions as a sorting receptor for chromogranin A aggregates in C12 cells. Mol Endocrinol 22:1935-1949
37. Thiele C, Hannah MJ, Fahrenholz F, Huttner WB 2000 Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat Cell Biol 2:42-49
38. Huang J, Feigenson GW 1999 A microscopic interaction model of maximum solubility of cholesterol in lipid bilayers. Biophys J 76: 2142-2157 (Pubitemid 29266367)
39. Wei S, Lee TS, Zhu M, Gu C, Wang Y, Zhu Y, Shyy JY 2006 Statins activate AMP-activated protein kinase in vitro and in vivo. Circulation 114:2655-2662
40. Viollet B, Mounier R, Leclerc J, Yazigi A, Foretz M, Andreelli F 2007 Targeting AMP-activated protein kinase as a novel therapeutic approach for the treatment of metabolic disorders. Diabetes Metab 33:395-402
41. Okazaki Y, Eto K, Yamashita T, Okamoto M, Ohsugi M, Noda M, Terauchi Y, Ueki K, Kadowaki T 2010 Decreased insulin secretion and accumulation of triglyceride in β cells overexpressing a dominant-negative form of AMP-activated protein kinase. Endocr J 57:141-152
42. Cole SL, Grudzien A, Manhart IO, Kelly BL, Oakley H, Vassar R 2005 Statins cause intracellular accumulation of amyloid precursor protein, β-secretase-cleaved fragments, and amyloid β-peptide via an isoprenoid-dependent mechanism. J Biol Chem 280:18755-18770
43. Chugh A, Ray A, Gupta JB 2003 Squalene epoxidase as a hypocholesterolemic drug target revisited. Prog Lipid Res 42:37-50
44. Xia F, Xie L, Mihic A, Gao X, Chen Y, Gaisano HY, Tsushima RG 2008 Inhibition of cholesterol biosynthesis impairs insulin secretion and voltage-gated calcium channel function in pancreatic β-cells. Endocrinology 149:5136-5145
45. Tanaka T, Tatsuno I, Uchida D, Moroo I, Morio H, Nakamura S, Noguchi Y, Yasuda T, Kitagawa M, Saito Y, Hirai A 2000 Geranylgeranyl-pyrophosphate, an isoprenoid of mevalonate cascade, is a critical compound for rat primary cultured cortical neurons to protect the cell death induced by 3-hydroxy-3-methylglutaryl-CoA reductase inhibition. J Neurosci 20:2852-2859
46. Salaün C, James DJ, Chamberlain LH 2004 Lipid rafts and the regulation of exocytosis. Traffic 5:255-264
47. Tooze SA, Martens GJM, Huttner WB 2001 Secretory granule biogenesis: rafting to the SNARE. Trends Cell Biol 11:16-22
48. Chamberlain LH, Burgoyne RD, Gould GW 2001 SNARE proteins are highly enriched in lipid rafts in PC12 cells: Implications for the spatial control of exocytosis. Proc Natl Acad Sci USA 98:5619-5624
49. Ohara-Imaizumi M, Nishiwaki C, Kikuta T, Kumakura K, Nakamichi Y, Nagamatsu S 2004 Site of docking and fusion of insulin secretory granules in live MIN6 β-cells analyzed by TATconjugated anti-syntaxin 1 antibody and total internal reflection fluorescence microscopy. J Biol Chem 279:8403-8408
50. Hosaka M, Watanabe T, Sakai Y, Uchiyama Y, Takeuchi T 2002 Identification of a chromograninAdomain that mediates binding to secretogranin III and targeting to secretory granules in pituitary cells and pancreatic β-cells. Mol Biol Cell 13:3388-3399
51. Cool DR, Normant E, Shen F, Chen HC, Pannell L, Zhang Y, Loh YP 1997 Carboxypeptidase E is a regulated secretory pathway sorting receptor: genetic obliteration leads to endocrine disorders in Cpe(fat) mice. Cell 88:73-83
52. Hosaka M, Watanabe T, Sakai Y, Kato T, Takeuchi T 2005 Interaction between secretogranin III and carboxypeptidase E facilitates prohormone sorting within secretory granules. J Cell Sci 118:4785-4795
53. Farsad K, De Camilli P 2003 Mechanisms of membrane deformation. Curr Opin Cell Biol 15:372-381
54. Horton JD, Goldstein JL, BrownMS 2002 SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 109:1125-1131