Effects of high-fat diet feeding on Znt8-null mice: Differences between β-cell and global knockout of Znt8

American Journal of Physiology - Endocrinology and Metabolism

Volumn 302, Issue 9, 2012, Pages

  Hardy, A B ^a   Wijesekara, N ^a   Genkin, I ^a   Prentice, K J ^a   Bhattacharjee, A ^a   Kong, D ^b   Chimienti, F ^c   Wheeler, M B ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Mellitech   (France)

Author keywords

Obesity; Slc30a8; Zinc transporter 8

Indexed keywords

BETA ACTIN; UNCLASSIFIED DRUG; ZINC TRANSPORTER; ZINC TRANSPORTER 8 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOLOGICAL ACTIVITY; BODY WEIGHT; CALORIC INTAKE; CONTROLLED STUDY; ELECTRON MICROSCOPY; FOOD INTAKE; GENOTYPE; GLUCOSE INTOLERANCE; HYPERGLYCEMIA; HYPERINSULINEMIA; IMMUNOHISTOCHEMISTRY; INSULIN RELEASE; INSULIN RESISTANCE; INSULIN SYNTHESIS; LIPID DIET; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; WEIGHT GAIN;

ANALYSIS OF VARIANCE; ANIMALS; BLOOD GLUCOSE; CATION TRANSPORT PROTEINS; DIET, HIGH-FAT; ENERGY INTAKE; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; MALE; MATCHED-PAIR ANALYSIS; MICE; MICE, KNOCKOUT; OBESITY; STRESS, PHYSIOLOGICAL; TISSUE DISTRIBUTION;

EID: 84860499114     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00448.2011     Document Type: Article

References (65)

1. Alemzadeh R, Holshouser S, Massey P, Koontz J. Chronic suppression of insulin by diazoxide alters the activities of key enzymes regulating hepatic gluconeogenesis in Zucker rats. Eur J Endocrinol 146: 871-879, 2002.
2. Alemzadeh R, Jacobs W, Pitukcheewanont P. Antiobesity effect of diazoxide in obese Zucker rats. Metabolism 45: 334-341, 1996.
3. Alemzadeh R, Langley G, Upchurch L, Smith P, Slonim AE. Beneficial effect of diazoxide in obese hyperinsulinemic adults. J Clin Endocrinol Metab 83: 1911-1915, 1998.
4. Alemzadeh R, Slonim AE, Zdanowicz MM, Maturo J. Modification of insulin resistance by diazoxide in obese Zucker rats. Endocrinology 133: 705-712, 1993.
5. Asakawa A, Inui A, Yuzuriha H, Ueno N, Katsuura G, Fujimiya M, Fujino MA, Niijima A, Meguid MM, Kasuga M. Characterization of the effects of pancreatic polypeptide in the regulation of energy balance. Gastroenterology 124: 1325-1336, 2003.
6. 2+ concentration, Slc39 (ZiP) and metallothionein gene expression in primary pancreatic islet (beta)-cells. J Biol Chem 2011.
7. Boden G. Role of fatty acids in the pathogenesis of insulin resistance and NIDDM. Diabetes 46: 3-10, 1997.
8. Bozym RA, Chimienti F, Giblin LJ, Gross GW, Korichneva I, Li Y, Libert S, Maret W, Parviz M, Frederickson CJ, Thompson RB. Free zinc ions outside a narrow concentration range are toxic to a variety of cells in vitro. Exp Biol Med (Maywood) 235: 741-750, 2010.
9. Cauchi S, Nead KT, Choquet H, Horber F, Potoczna N, Balkau B, Marre M, Charpentier G, Froguel P, Meyre D. The genetic susceptibility to type 2 diabetes may be modulated by obesity status: implications for association studies. BMC Med Genet 9: 45, 2008.
10. Chimienti F, Devergnas S, Pattou F, Schuit F, Garcia-Cuenca R, Vandewalle B, Kerr-Conte J, Van Lommel L, Grunwald D, Favier A, Seve M. In vivo expression and functional characterization of the zinc transporter ZnT8 in glucose-induced insulin secretion. J Cell Sci 119: 4199-4206, 2006.
11. Choi D, Cai EP, Schroer SA, Wang L, Woo M. Vhl is required for normal pancreatic fj-cell function and the maintenance of beta cell mass with age in mice. Lab Invest 91: 527-538, 2011.
12. Cui Y, Huang L, Elefteriou F, Yang G, Shelton JM, Giles JE, Oz OK, Pourbahrami T, Lu CY, Richardson JA, Karsenty G, Li C. Essential role of STAT3 in body weight and glucose homeostasis. Mol Cell Biol 24: 258-269, 2004.
13. Deltour L, Leduque P, Blume N, Madsen O, Dubois P, Jami J, Bucchini D. Differential expression of the two nonallelic proinsulin genes in the developing mouse embryo. Proc Natl Acad Sci USA 90: 527-531, 1993.
14. Deltour L, Montagutelli X, Guenet JL, Jami J, Paldi A. Tissue- and developmental stage-specific imprinting of the mouse proinsulin gene, Ins2. Dev Biol 168: 686-688, 1995.
15. Formigari A, Irato P, Santon A. Zinc, antioxidant systems and metallothionein in metal mediated-apoptosis: biochemical and cytochemical aspects. Comp Biochem Physiol C Toxicol Pharmacol 146: 443-459, 2007.
16. Fu A, Ng AC, Depatie C, Wijesekara N, He Y, Wang GS, Bardeesy N, Scott FW, Touyz RM, Wheeler MB, Screaton RA. Loss of Lkb1 in adult beta cells increases beta cell mass and enhances glucose tolerance in mice. Cell Metab 10: 285-295, 2009.
17. Gannon M, Shiota C, Postic C, Wright CV, Magnuson M. Analysis of the Cre-mediated recombination driven by rat insulin promoter in embryonic and adult mouse pancreas. Genesis 26: 139-142, 2000.
18. Gu G, Dubauskaite J, Melton DA. Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 129: 2447-2457, 2002.
19. 2+ channel. J Biol Chem 281: 9361-9372, 2006.
20. + channels in alpha- and beta-cells of mouse and human islets. J Biol Chem 284: 30441-30452, 2009.
21. + currents. Mol Endocrinol 21: 765-773, 2007.
22. Kahn SE, Hull RL, Utzschneider KM. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 444: 840-846, 2006.
23. Kambe T, Narita H, Yamaguchi-Iwai Y, Hirose J, Amano T, Sugiura N, Sasaki R, Mori K, Iwanaga T, Nagao M. Cloning and characterization of a novel mammalian zinc transporter, zinc transporter 5, abundantly expressed in pancreatic beta cells. J Biol Chem 277: 19049-19055, 2002.
24. Keller MP, Choi Y, Wang P, Davis DB, Rabaglia ME, Oler AT, Stapleton DS, Argmann C, Schueler KL, Edwards S, Steinberg HA, Chaibub Neto E, Kleinhanz R, Turner S, Hellerstein MK, Schadt EE, Yandell BS, Kendziorski C, Attie AD. A gene expression network model of type 2 diabetes links cell cycle regulation in islets with diabetes susceptibility. Genome Res 18: 706-716, 2008.
25. Kim BJ, Kim YH, Kim S, Kim JW, Koh JY, Oh SH, Lee MK, Kim KW, Lee MS. Zinc as a paracrine effector in pancreatic islet cell death. Diabetes 49: 367-372, 2000.
26. Kin T, O'Gorman D, Schroeder A, Onderka C, Richer B, Rosichuk S, Zhai X, Shapiro AM. Human islet distribution program for basic research at a single center. Transplant Proc 43: 3195-3197, 2011.
27. Kizelsztein P, Govorko D, Komarnytsky S, Evans A, Wang Z, Cefalu WT, Raskin I. 20-Hydroxyecdysone decreases weight and hyperglycemia in a diet-induced obesity mice model. Am J Physiol Endocrinol Metab 296: E433-E439, 2009.
28. Koshkin V, Dai FF, Robson-Doucette CA, Chan CB, Wheeler MB. Limited mitochondrial permeabilization is an early manifestation of palmitate-induced lipotoxicity in pancreatic beta-cells. J Biol Chem 283: 7936-7948, 2008.
29. Kubota N, Terauchi Y, Tobe K, Yano W, Suzuki R, Ueki K, Takamoto I, Satoh H, Maki T, Kubota T, Moroi M, Okada-Iwabu M, Ezaki O, Nagai R, Ueta Y, Kadowaki T, Noda T. Insulin receptor substrate 2 plays a crucial role in beta cells and the hypothalamus. J Clin Invest 114: 917-927, 2004.
30. Lamotte L, Jackerott M, Bucchini D, Jami J, Joshi RL, Deltour L. Knock-in of diphteria toxin A chain gene at Ins2 locus: effects on islet development and localization of Ins2 expression in the brain. Transgenic Res 13: 463-473, 2004.
31. Lee JY, Ristow M, Lin X, White MF, Magnuson MA, Hennighausen L. RIP-Cre revisited, evidence for impairments of pancreatic beta-cell function. J Biol Chem 281: 2649-2653, 2006.
32. Lee SC, Robson-Doucette CA, Wheeler MB. Uncoupling protein 2 regulates reactive oxygen species formation in islets and influences susceptibility to diabetogenic action of streptozotocin. J Endocrinol 203: 33-43, 2009.
33. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, Dong HW, Dougherty JG, Duncan BJ, Ebbert AJ, Eichele G, Estin LK, Faber C, Facer BA, Fields R, Fischer SR, Fliss TP, Frensley C, Gates SN, Glattfelder KJ, Halverson KR, Hart MR, Hohmann JG, Howell MP, Jeung DP, Johnson RA, Karr PT, Kawal R, Kidney JM, Knapik RH, Kuan CL, Lake JH, Laramee AR, Larsen KD, Lau C, Lemon TA, Liang AJ, Liu Y, Luong LT, Michaels J, Morgan JJ, Morgan RJ, Mortrud MT, Mosqueda NF, Ng LL, Ng R, Orta GJ, Overly CC, Pak TH, Parry SE, Pathak SD, Pearson OC, Puchalski RB, Riley ZL, Rockett HR, Rowland SA, Royall JJ, Ruiz MJ, Sarno NR, Schaffnit K, Shapovalova NV, Sivisay T, Slaughterbeck CR, Smith SC, Smith KA, Smith BI, Sodt AJ, Stewart NN, Stumpf KR, Sunkin SM, Sutram M, Tam A, Teemer CD, Thaller C, Thompson CL, Varnam LR, Visel A, Whitlock RM, Wohnoutka PE, Wolkey CK, Wong VY, Wood M, Yaylaoglu MB, Young RC, Youngstrom BL, Yuan XF, Zhang B, Zwingman TA, Jones AR. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445: 168-176, 2007.
34. Lemaire K, Ravier MA, Schraenen A, Creemers JW, Van de Plas R, Granvik M, Van Lommel L, Waelkens E, Chimienti F, Rutter GA, Gilon P, In't Veld PA, Schuit FC. Insulin crystallization depends on zinc transporter ZnT8 expression, but is not required for normal glucose homeostasis in mice. Proc Natl Acad Sci USA 106: 14872-14877, 2009.
35. Lustig RH, Greenway F, Velasquez-Mieyer P, Heimburger D, Schumacher D, Smith D, Smith W, Soler N, Warsi G, Berg W, Maloney J, Benedetto J, Zhu W, Hohneker J. A multicenter, randomized, double-blind, placebo-controlled, dose-finding trial of a long-acting formulation of octreotide in promoting weight loss in obese adults with insulin hypersecretion. Int J Obes (Lond) 30: 331-341, 2006.
36. Michael J, Carroll R, Swift HH, Steiner DF. Studies on the molecular organization of rat insulin secretory granules. J Biol Chem 262: 16531-16535, 1987.
37. Murgia C, Devirgiliis C, Mancini E, Donadel G, Zalewski P, Perozzi G. Diabetes-linked zinc transporter ZnT8 is a homodimeric protein expressed by distinct rodent endocrine cell types in the pancreas and other glands. Nutr Metab Cardiovasc Dis 19: 431-439, 2009.
38. Ng MC, Park KS, Oh B, Tam CH, Cho YM, Shin HD, Lam VK, Ma RC, So WY, Cho YS, Kim HL, Lee HK, Chan JC, Cho NH. Implication of genetic variants near TCF7L2, SLC30A8, HHEX, CDKAL1, CDKN2A/B, IGF2BP2, and FTO in type 2 diabetes and obesity in 6,719 Asians. Diabetes 57: 2226-2233, 2008.
39. Nicolson TJ, Bellomo EA, Wijesekara N, Loder MK, Baldwin JM, Gyulkhandanyan AV, Koshkin V, Tarasov AI, Carzaniga R, Kronen-berger K, Taneja TK, da Silva Xavier G. Libert S, Froguel P, Scharfmann R, Stetsyuk V, Ravassard P, Parker H, Gribble FM, Reimann F, Sladek R, Hughes SJ, Johnson PR, Masseboeuf M, Burcelin R, Baldwin SA, Liu M, Lara-Lemus R, Arvan P, Schuit FC, Wheeler MB, Chimienti F, Rutter GA. Insulin storage and glucose homeostasis in mice null for the granule zinc transporter ZnT8 and studies of the type 2 diabetes-associated variants. Diabetes 58: 2070-2083, 2009.
40. Odeleye OE, de Courten M, Pettitt DJ, Ravussin E. Fasting hyperin-sulinemia is a predictor of increased body weight gain and obesity in Pima Indian children. Diabetes 46: 1341-1345, 1997.
41. Omori S, Tanaka Y, Takahashi A, Hirose H, Kashiwagi A, Kaku K, Kawamori R, Nakamura Y, Maeda S. Association of CDKAL1, IGF2BP2, CDKN2A/B, HHEX, SLC30A8, and KCNJ11 with susceptibility to type 2 diabetes in a Japanese population. Diabetes 57: 791-795, 2008.
42. Oprescu AI, Bikopoulos G, Naassan A, Allister EM, Tang C, Park E, Uchino H, Lewis GF, Fantus IG, Rozakis-Adcock M, Wheeler MB, Giacca A. Free fatty acid-induced reduction in glucose-stimulated insulin secretion: evidence for a role of oxidative stress in vitro and in vivo. Diabetes 56: 2927-2937, 2007.
43. Overbeck S, Uciechowski P, Ackland ML, Ford D, Rink L. Intracel-lular zinc homeostasis in leukocyte subsets is regulated by different expression of zinc exporters ZnT-1 to ZnT-9. J Leukoc Biol 83: 368-380, 2008.
44. Pecioska S, Zillikens MC, Henneman P, Snijders PJ, Oostra BA, van Duijn CM, Aulchenko YS. Association between type 2 diabetes loci and measures of fatness. PLoS One 5: e8541, 2010.
45. Pound LD, Sarkar SA, Benninger RK, Wang Y, Suwanichkul A, Shadoan MK, Printz RL, Oeser JK, Lee CE, Piston DW, McGuinness OP, Hutton JC, Powell DR, O'Brien RM. Deletion of the mouse Slc30a8 gene encoding zinc transporter-8 results in impaired insulin secretion. Biochem J 421: 371-376, 2009.
46. Reaven GM, Hollenbeck C, Jeng CY, Wu MS, Chen YD. Measurement of plasma glucose, free fatty acid, lactate, and insulin for 24 h in patients with NIDDM. Diabetes 37: 1020-1024, 1988.
47. Robson-Doucette CA, Sultan S, Allister EM, Wikstrom JD, Koshkin V, Bhatacharjee A, Prentice KJ, Sereda SB, Shirihai OS, Wheeler MB. Beta-cell uncoupling protein 2 regulates reactive oxygen species production, which influences both insulin and glucagon secretion. Diabetes 60: 2710-2719, 2011.
48. Saxena R, Voight BF, Lyssenko V, Burtt NP, de Bakker PI, Chen H, Roix JJ, Kathiresan S, Hirschhorn JN, Daly MJ, Hughes TE, Groop L, Altshuler D, Almgren P, Florez JC, Meyer J, Ardlie K, Bengtsson Bostrom K, Isomaa B, Lettre G, Lindblad U, Lyon HN, Melander O, Newton-Cheh C, Nilsson P, Orho-Melander M, Rastam L, Speliotes EK, Taskinen MR, Tuomi T, Guiducci C, Berglund A, Carlson J, Gianniny L, Hackett R, Hall L, Holmkvist J, Laurila E, Sjogren M, Sterner M, Surti A, Svensson M, Tewhey R, Blumenstiel B, Parkin M, Defelice M, Barry R, Brodeur W, Camarata J, Chia N, Fava M, Gibbons J, Handsaker B, Healy C, Nguyen K, Gates C, Sougnez C, Gage D, Nizzari M, Gabriel SB, Chirn GW, Ma Q, Parikh H, Richardson D, Ricke D, Purcell S. Genome-wide association analysis identifies loci for type 2 diabetes and triglyceride levels. Science 316: 1331-1336, 2007.
49. Scott DA, Fisher AM. The insulin and the zinc content of normal and diabetic pancreas. J Clin Invest 17: 725-728, 1938.
50. Scott LJ, Mohlke KL, Bonnycastle LL, Willer CJ, Li Y, Duren WL, Erdos MR, Stringham HM, Chines PS, Jackson AU, Prokunina-Olsson L, Ding CJ, Swift AJ, Narisu N, Hu T, Pruim R, Xiao R, Li XY, Conneely KN, Riebow NL, Sprau AG, Tong M, White PP, Hetrick KN, Barnhart MW, Bark CW, Goldstein JL, Watkins L, Xiang F, Saramies J, Buchanan TA, Watanabe RM, Valle TT, Kinnunen L, Abecasis GR, Pugh EW, Doheny KF, Bergman RN, Tuomilehto J, Collins FS, Boehnke M. A genome-wide association study of type 2 diabetes in Finns detects multiple susceptibility variants. Science 316: 1341-1345, 2007.
51. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest 116: 1793-1801, 2006.
52. Sladek R, Rocheleau G, Rung J, Dina C, Shen L, Serre D, Boutin P, Vincent D, Belisle A, Hadjadj S, Balkau B, Heude B, Charpentier G, Hudson TJ, Montpetit A, Pshezhetsky AV, Prentki M, Posner BI, Balding DJ, Meyre D, Polychronakos C, Froguel P. A genome-wide association study identifies novel risk loci for type 2 diabetes. Nature 445: 881-885, 2007.
53. Smidt K, Pedersen SB, Brock B, Schmitz O, Fisker S, Bendix J, Wogensen L, Rungby J. Zinc-transporter genes in human visceral and subcutaneous adipocytes: lean versus obese. Mol Cell Endocrinol 264: 68-73, 2007.
54. Steinthorsdottir V, Thorleifsson G, Reynisdottir I, Benediktsson R, Jonsdottir T, Walters GB, Styrkarsdottir U, Gretarsdottir S, Emilsson V, Ghosh S, Baker A, Snorradottir S, Bjarnason H, Ng MC, Hansen T, Bagger Y, Wilensky RL, Reilly MP, Adeyemo A, Chen Y, Zhou J, Gudnason V, Chen G, Huang H, Lashley K, Doumatey A, So WY, Ma RC, Andersen G, Borch-Johnsen K, Jorgensen T, van Vliet-Ostaptchouk JV, Hofker MH, Wijmenga C, Christiansen C, Rader DJ, Rotimi C, Gurney M, Chan JC, Pedersen O, Sigurdsson G, Gulcher JR, Thorsteinsdottir U, Kong A, Stefansson K. A variant in CDKAL1 influences insulin response and risk of type 2 diabetes. Nat Genet 39: 770-775, 2007.
55. Takeuchi F, Serizawa M, Yamamoto K, Fujisawa T, Nakashima E, Ohnaka K, Ikegami H, Sugiyama T, Katsuya T, Miyagishi M, Na-kashima N, Nawata H, Nakamura J, Kono S, Takayanagi R, Kato N. Confirmation of multiple risk Loci and genetic impacts by a genome-wide association study of type 2 diabetes in the Japanese population. Diabetes 58: 1690-1699, 2009.
56. Tamaki M, Fujitani Y, Uchida T, Hirose T, Kawamori R, Watada H. Downregulation of ZnT8 expression in pancreatic b-cells of diabetic mice. Islets 1: 124-128, 2009.
57. Timpson NJ, Lindgren CM, Weedon MN, Randall J, Ouwehand WH, Strachan DP, Rayner NW, Walker M, Hitman GA, Doney AS, Palmer CN, Morris AD, Hattersley AT, Zeggini E, Frayling TM, McCarthy MI. Adiposity-related heterogeneity in patterns of type 2 diabetes susceptibility observed in genome-wide association data. Diabetes 58: 505-510, 2009.
58. Wang L, Liu Y, Yan Lu S, Nguyen KT, Schroer SA, Suzuki A, Mak TW, Gaisano H, Woo M. Deletion of Pten in pancreatic ss-cells protects against deficient ss-cell mass and function in mouse models of type 2 diabetes. Diabetes 59: 3117-3126, 2010.
59. Webster RJ, Warrington NM, Beilby JP, Frayling TM, Palmer LJ. The longitudinal association of common susceptibility variants for type 2 diabetes and obesity with fasting glucose level and BMI. BMC Med Genet 11: 140, 2010.
60. Wellen KE, Hotamisligil GS. Inflammation, stress, diabetes. J Clin Invest 115: 1111-1119, 2005.
61. Wenzlau JM, Juhl K, Yu L, Moua O, Sarkar SA, Gottlieb P, Rewers M, Eisenbarth GS, Jensen J, Davidson HW, Hutton JC. The cation efflux transporter ZnT8 (Slc30A8) is a major autoantigen in human type 1 diabetes. Proc Natl Acad Sci USA 104: 17040-17045, 2007.
62. Wicksteed B, Brissova M, Yan W, Opland DM, Plank JL, Reinert RB, Dickson LM, Tamarina NA, Philipson LH, Shostak A, Bernal-Mizrachi E, Elghazi L, Roe MW, Labosky PA, Myers MM Jr, Gannon M, Powers AC, Dempsey PJ. Conditional gene targeting in mouse pancreatic (beta)-cells: analysis of ectopic Cre transgene expression in the brain. Diabetes 59: 3090-3098 2010.
63. Wijesekara N, Dai FF, Hardy AB, Giglou PR, Bhattacharjee A, Koshkin V, Chimienti F, Gaisano HY, Rutter GA, Wheeler MB. Beta cell-specific Znt8 deletion in mice causes marked defects in insulin processing, crystallisation and secretion. Diabetologia 53: 1656-1668, 2010.
64. Wu Y, Li H, Loos RJ, Yu Z, Ye X, Chen L, Pan A, Hu FB, Lin X. Common variants in CDKAL1, CDKN2A/B, IGF2BP2, SLC30A8, and HHEX/IDE genes are associated with type 2 diabetes and impaired fasting glucose in a Chinese Han population. Diabetes 57: 2834-2842, 2008.
65. Zeggini E, Weedon MN, Lindgren CM, Frayling TM, Elliott KS, Lango H, Timpson NJ, Perry JR, Rayner NW, Freathy RM, Barrett JC, Shields B, Morris AP, Ellard S, Groves CJ, Harries LW, Marchini JL, Owen KR, Knight B, Cardon LR, Walker M, Hitman GA, Morris AD, Doney AS, McCarthy MI, Hattersley AT. Replication of genome-wide association signals in UK samples reveals risk loci for type 2 diabetes. Science 316: 1336-1341, 2007.