Reduced islet function contributes to impaired glucose homeostasis in fructose-fed mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 312, Issue 2, 2017, Pages E109-E116

  Asghar, Zeenat A ^a   Cusumano, Andrew ^a   Yan, Zihan ^a   Remedi, Maria S ^a   Moley, Kelle H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FRUCTOSE; GLUCAGON; GLUCOSE; GLUCOSE TRANSPORTER 5; INSULIN; CARBOHYDRATE DIET;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DIET RESTRICTION; DIETARY INTAKE; DYSLIPIDEMIA; EXPERIMENTAL HYPERGLYCEMIA; GLUCAGON RELEASE; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; HYPERINSULINEMIA; HYPERURICEMIA; IN VITRO STUDY; IN VIVO STUDY; INSULIN BLOOD LEVEL; INSULIN RELEASE; INSULIN RESISTANCE; MALE; MOUSE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET ALPHA CELL; PHENOTYPE; PRIORITY JOURNAL; UPREGULATION; ANIMAL; C57BL MOUSE; CARBOHYDRATE DIET; CELL CULTURE; DOWN REGULATION; DRUG EFFECTS; HOMEOSTASIS; METABOLISM; PHARMACOLOGY; PHYSIOLOGY;

ANIMALS; CELLS, CULTURED; DIETARY CARBOHYDRATES; DOWN-REGULATION; FRUCTOSE; GLUCOSE; GLUCOSE INTOLERANCE; HOMEOSTASIS; ISLETS OF LANGERHANS; MALE; MICE; MICE, INBRED C57BL;

EID: 85012082529     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00279.2016     Document Type: Article

References (53)

1. Allister EM, Robson-Doucette CA, Prentice KJ, Hardy AB, Sultan S, Gaisano HY, Kong D, Gilon P, Herrera PL, Lowell BB, Wheeler MB. UCP2 regulates the glucagon response to fasting and starvation. Diabetes 62: 1623-1633, 2013. doi:10.2337/db12-0981.
2. Andrikopoulos S, Blair AR, Deluca N, Fam BC, Proietto J. Evaluating the glucose tolerance test in mice. Am J Physiol Endocrinol Metab 295: E1323-E1332, 2008. doi:10.1152/ajpendo.90617.2008.
3. Asghar ZA, Thompson A, Chi M, Cusumano A, Scheaffer S, Al-Hammadi N, Saben JL, Moley KH. Maternal fructose drives placental uric acid production leading to adverse fetal outcomes. Sci Rep 6: 25091, 2016. doi:10.1038/srep25091.
4. Ben-Zvi D, Barrandon O, Hadley S, Blum B, Peterson QP, Melton DA. Angptl4 links _-cell proliferation following glucagon receptor inhibition with adipose tissue triglyceride metabolism. Proc Natl Acad Sci U S A 112: 15498-15503, 2015. doi:10.1073/pnas.1513872112.
5. Bordone L, Motta MC, Picard F, Robinson A, Jhala US, Apfeld J, McDonagh T, Lemieux M, McBurney M, Szilvasi A, Easlon EJ, Lin SJ, Guarente L. Sirt1 regulates insulin secretion by repressing UCP2 in pancreatic β cells. PLoS Biol 4: e31, 2006. doi:10.1371/journal.pbio.0040031.
6. Caton PW, Kieswich J, Yaqoob MM, Holness MJ, Sugden MC. Nicotinamide mononucleotide protects against pro-inflammatory cytokine-mediated impairment of mouse islet function. Diabetologia 54: 3083-3092, 2011. doi:10.1007/s00125-011-2288-0.
7. Chan KK, Chan JY, Chung KK, Fung KP. Inhibition of cell proliferation in human breast tumor cells by antisense oligonucleotides against facilitative glucose transporter 5. J Cell Biochem 93: 1134-1142, 2004. doi:10.1002/jcb.20270.
8. Chan SM, Sun RQ, Zeng XY, Choong ZH, Wang H, Watt MJ, Ye JM. Activation of PPARα ameliorates hepatic insulin resistance and steatosis in high fructose-fed mice despite increased endoplasmic reticulum stress. Diabetes 62: 2095-2105, 2013. doi:10.2337/db12-1397.
9. Chen YR, Lai YL, Lin SD, Li XT, Fu YC, Xu WC. SIRT1 interacts with metabolic transcriptional factors in the pancreas of insulin-resistant and calorie-restricted rats. Mol Biol Rep 40: 3373-3380, 2013. doi:10.1007/s11033-012-2412-3.
10. Curry DL, Curry KP, Gomez M. Fructose potentiation of insulin secretion. Endocrinology 91: 1493-1498, 1972. doi:10.1210/endo-91-6-1493.
11. DeBosch BJ, Chen Z, Finck BN, Chi M, Moley KH. Glucose transporter-8 (GLUT8) mediates glucose intolerance and dyslipidemia in high-fructose diet-fed male mice. Mol Endocrinol 27: 1887-1896, 2013. doi:10.1210/me.2013-1137.
12. Del Prato S, Marchetti P. Beta-and alpha-cell dysfunction in type 2 diabetes. Horm Metab Res 36: 775-781, 2004. doi:10.1055/s-2004-826163.
13. Douard V, Ferraris RP. Regulation of the fructose transporter GLUT5 in health and disease. Am J Physiol Endocrinol Metab 295: E227-E237, 2008. doi:10.1152/ajpendo.90245.2008.
14. Douard V, Ferraris RP. The role of fructose transporters in diseases linked to excessive fructose intake. J Physiol 591: 401-414, 2013. doi: 10.1113/jphysiol.2011.215731.
15. Dyer J, Wood IS, Palejwala A, Ellis A, Shirazi-Beechey SP. Expression of monosaccharide transporters in intestine of diabetic humans. Am J Physiol Gastrointest Liver Physiol 282: G241-G248, 2002. doi:10.1152/ajpgi.00310.2001.
16. Evans SA, Doblado M, Chi MM, Corbett JA, Moley KH. Facilitative glucose transporter 9 expression affects glucose sensing in pancreatic beta-cells. Endocrinology 150: 5302-5310, 2009. doi:10.1210/en.2009-0747.
17. Farhy LS, McCall AL. Optimizing reduction in basal hyperglucagonaemia to repair defective glucagon counterregulation in insulin deficiency. Diabetes Obes Metab 13, Suppl 1: 133-143, 2011. doi:10.1111/j.1463-1326.2011.01455.x.
18. Gabriely I, Hawkins M, Vilcu C, Rossetti L, Shamoon H. Fructose amplifies counterregulatory responses to hypoglycemia in humans. Diabetes 51: 893-900, 2002. doi:10.2337/diabetes.51.4.893.
19. Godoy A, Ulloa V, Rodríguez F, Reinicke K, Yañez AJ, García ML, Medina RA, Carrasco M, Barberis S, Castro T, Martínez F, Koch X, Vera JC, Poblete MT, Figueroa CD, Peruzzo B, Pérez F, Nualart F. Differential subcellular distribution of glucose transporters GLUT1-6 and GLUT9 in human cancer: ultrastructural localization of GLUT1 and GLUT5 in breast tumor tissues. J Cell Physiol 207: 614-627, 2006. doi:10.1002/jcp.20606.
20. Heimberg H, De Vos A, Pipeleers D, Thorens B, Schuit F. Differences in glucose transporter gene expression between rat pancreatic alpha-and beta-cells are correlated to differences in glucose transport but not in glucose utilization. J Biol Chem 270: 8971-8975, 1995. doi:10.1074/jbc.270.15.8971.
21. Johnson RJ, Perez-Pozo SE, Sautin YY, Manitius J, Sanchez-Lozada LG, Feig DI, Shafiu M, Segal M, Glassock RJ, Shimada M, Roncal C, Nakagawa T. Hypothesis: could excessive fructose intake and uric acid cause type 2 diabetes? Endocr Rev 30: 96-116, 2009. doi:10.1210/er.2008-0033.
22. Kawamori D, Kurpad AJ, Hu J, Liew CW, Shih JL, Ford EL, Herrera PL, Polonsky KS, McGuinness OP, Kulkarni RN. Insulin signaling in alpha cells modulates glucagon secretion in vivo. Cell Metab 9: 350-361, 2009. doi:10.1016/j.cmet.2009.02.007.
23. Kim J, Song G, Wu G, Bazer FW. Functional roles of fructose. Proc Natl Acad Sci U S A 109: E1619-E1628, 2012. doi:10.1073/pnas.1204298109.
24. Kuhre RE, Gribble FM, Hartmann B, Reimann F, Windeløv JA, Rehfeld JF, Holst JJ. Fructose stimulates GLP-1 but not GIP secretion in mice, rats, and humans. Am J Physiol Gastrointest Liver Physiol 306: G622-G630, 2014. doi:10.1152/ajpgi.00372.2013.
25. Kyriazis GA, Soundarapandian MM, Tyrberg B. Sweet taste receptor signaling in beta cells mediates fructose-induced potentiation of glucosestimulated insulin secretion. Proc Natl Acad Sci U S A 109: E524-E532, 2012. doi:10.1073/pnas.1115183109.
26. Lawrence JR, Gray CE, Grant IS, Ford JA, McIntosh WB, Dunnigan MG. The insulin response to intravenous fructose in maturity-onset diabetes mellitus and in normal subjects. Diabetes 29: 736-741, 1980. doi:10.2337/diab.29.9.736.
27. Li JM, Wang W, Fan CY, Wang MX, Zhang X, Hu QH, Kong LD. Quercetin Preserves β-Cell Mass and Function in Fructose-Induced Hyperinsulinemia through Modulating Pancreatic Akt/FoxO1 Activation. Evid Based Complement Alternat Med 2013: 303902, 2013. doi:10.1155/2013/303902.
28. Li M, Dean ED, Zhao L, Nicholson WE, Powers AC, Chen W. Glucagon receptor inactivation leads to _-cell hyperplasia in zebrafish. J Endocrinol 227: 93-103, 2015. doi:10.1530/JOE-15-0284.
29. Liu Z, Kim W, Chen Z, Shin YK, Carlson OD, Fiori JL, Xin L, Napora JK, Short R, Odetunde JO, Lao Q, Egan JM. Insulin and glucagon regulate pancreatic α-cell proliferation. PLoS One 6: e16096, 2011. doi:10.1371/journal.pone.0016096.
30. Lu H, Koshkin V, Allister EM, Gyulkhandanyan AV, Wheeler MB. Molecular and metabolic evidence for mitochondrial defects associated with beta-cell dysfunction in a mouse model of type 2 diabetes. Diabetes 59: 448-459, 2010. doi:10.2337/db09-0129.
31. Marroqui L, Masini M, Merino B, Grieco FA, Millard I, Dubois C, Quesada I, Marchetti P, Cnop M, Eizirik DL. Pancreatic α Cells are Resistant to Metabolic Stress-induced Apoptosis in Type 2 Diabetes. EBioMedicine 2: 378-385, 2015. doi:10.1016/j.ebiom.2015.03.012.
32. Mitchell T, Johnson MS, Ouyang X, Chacko BK, Mitra K, Lei X, Gai Y, Moore DR, Barnes S, Zhang J, Koizumi A, Ramanadham S, Darley-Usmar VM. Dysfunctional mitochondrial bioenergetics and oxidative stress in Akita(+/Ins2)-derived β-cells. Am J Physiol Endocrinol Metab 305: E585-E599, 2013. doi:10.1152/ajpendo.00093.2013.
33. Montgomery MK, Fiveash CE, Braude JP, Osborne B, Brown SH, Mitchell TW, Turner N. Disparate metabolic response to fructose feeding between different mouse strains. Sci Rep 5: 18474, 2015. doi:10.1038/srep18474.
34. Monzavi-Karbassi B, Hine RJ, Stanley JS, Ramani VP, Carcel-Trullols J, Whitehead TL, Kelly T, Siegel ER, Artaud C, Shaaf S, Saha R, Jousheghany F, Henry-Tillman R, Kieber-Emmons T. Fructose as a carbon source induces an aggressive phenotype in MDA-MB-468 breast tumor cells. Int J Oncol 37: 615-622, 2010. doi:10.3892/ijo_00000710.
35. Paquot N, Schneiter P, Jéquier E, Gaillard R, Lefèbvre PJ, Scheen A, Tappy L. Effects of ingested fructose and infused glucagon on endogenous glucose production in obese NIDDM patients, obese non-diabetic subjects, and healthy subjects. Diabetologia 39: 580-586, 1996. doi:10.1007/BF00403305.
36. Pokrywczynska M, Flisinski M, Jundzill A, Krzyzanowska S, Brymora A, Deptula A, Bodnar M, Kloskowski T, Stefanska A, Marszalek A, Manitius J, Drewa T. Impact of fructose diet and renal failure on the function of pancreatic islets. Pancreas 43: 801-808, 2014. doi:10.1097/MPA.0000000000000111.
37. Raskin P, Unger RH. Hyperglucagonemia and its suppression. Importance in the metabolic control of diabetes. N Engl J Med 299: 433-436, 1978. doi:10.1056/NEJM197808312990901.
38. Roncal-Jimenez CA, Lanaspa MA, Rivard CJ, Nakagawa T, Sanchez-Lozada LG, Jalal D, Andres-Hernando A, Tanabe K, Madero M, Li N, Cicerchi C, Mc Fann K, Sautin YY, Johnson RJ. Sucrose induces fatty liver and pancreatic inflammation in male breeder rats independent of excess energy intake. Metabolism 60: 1259-1270, 2011. doi:10.1016/j.metabol.2011.01.008.
39. Saben JL, Asghar Z, Rhee JS, Drury A, Scheaffer S, Moley KH. Excess Maternal Fructose Consumption Increases Fetal Loss and Impairs Endometrial Decidualization in Mice. Endocrinology 157: 956-968, 2016. doi:10.1210/en.2015-1618.
40. Samuel VT, Beddow SA, Iwasaki T, Zhang XM, Chu X, Still CD, Gerhard GS, Shulman GI. Fasting hyperglycemia is not associated with increased expression of PEPCK or G6Pc in patients with Type 2 Diabetes. Proc Natl Acad Sci U S A 106: 12121-12126, 2009. doi:10.1073/pnas.0812547106.
41. Sato Y, Ito T, Udaka N, Kanisawa M, Noguchi Y, Cushman SW, Satoh S. Immunohistochemical localization of facilitated-diffusion glucose transporters in rat pancreatic islets. Tissue Cell 28: 637-643, 1996. doi:10.1016/S0040-8166(96)80067-X.
42. Seino Y, Ogata H, Maekawa R, Izumoto T, Iida A, Harada N, Miki T, Seino S, Inagaki N, Tsunekawa S, Oiso Y, Hamada Y. Fructose induces glucose-dependent insulinotropic polypeptide, glucagon-like peptide-1 and insulin secretion: Role of adenosine triphosphate-sensitive K(+) channels. J Diabetes Investig 6: 522-526, 2015. doi:10.1111/jdi.12356.
43. Spaeth JM, Hunter CS, Bonatakis L, Guo M, French CA, Slack I, Hara M, Fisher SE, Ferrer J, Morrisey EE, Stanger BZ, Stein R. The FOXP1, FOXP2 and FOXP4 transcription factors are required for islet alpha cell proliferation and function in mice. Diabetologia 58: 1836-1844, 2015. doi:10.1007/s00125-015-3635-3.
44. Steenberg VR, Jensen SM, Pedersen J, Madsen AN, Windeløv JA, Holst B, Quistorff B, Poulsen SS, Holst JJ. Acute disruption of glucagon secretion or action does not improve glucose tolerance in an insulindeficient mouse model of diabetes. Diabetologia 59: 363-370, 2016. doi:10.1007/s00125-015-3794-2.
45. Stuart CA, Howell ME, Yin D. Overexpression of GLUT5 in diabetic muscle is reversed by pioglitazone. Diabetes Care 30: 925-931, 2007. doi:10.2337/dc06-1788.
46. Sussman KE, Vaughan GD, Timmer RF. An in vitro method for studying insulin secretion in the perfused isolated rat pancreas. Metabolism 15: 466-476, 1966. doi:10.1016/0026-0495(66)90089-8.
47. Tappy L, Lê KA. Metabolic effects of fructose and the worldwide increase in obesity. Physiol Rev 90: 23-46, 2010. doi:10.1152/physrev.00019.2009.
48. Teff KL, Elliott SS, Tschöp M, Kieffer TJ, Rader D, Heiman M, Townsend RR, Keim NL, D'Alessio D, Havel PJ. Dietary fructose reduces circulating insulin and leptin, attenuates postprandial suppression of ghrelin, and increases triglycerides in women. J Clin Endocrinol Metab 89: 2963-2972, 2004. doi:10.1210/jc.2003-031855.
49. Unger RH. Role of glucagon in the pathogenesis of diabetes: the status of the controversy. Metabolism 27: 1691-1709, 1978. doi:10.1016/0026-0495(78)90291-3.
50. Vasu S, Moffett RC, McClenaghan NH, Flatt PR. Differential molecular and cellular responses of GLP-1 secreting L-cells and pancreatic alpha cells to glucotoxicity and lipotoxicity. Exp Cell Res 336: 100-108, 2015. doi:10.1016/j.yexcr.2015.05.022.
51. Wang H, Sun RQ, Zeng XY, Zhou X, Li S, Jo E, Molero JC, Ye JM. Restoration of autophagy alleviates hepatic ER stress and impaired insulin signalling transduction in high fructose-fed male mice. Endocrinology 156: 169-181, 2015. doi:10.1210/en.2014-1454.
52. Wang MY, Yan H, Shi Z, Evans MR, Yu X, Lee Y, Chen S, Williams A, Philippe J, Roth MG, Unger RH. Glucagon receptor antibody completely suppresses type 1 diabetes phenotype without insulin by disrupting a novel diabetogenic pathway. Proc Natl Acad Sci U S A 112: 2503-2508, 2015. doi:10.1073/pnas.1424934112.
53. Yoon KH, Ko SH, Cho JH, Lee JM, Ahn YB, Song KH, Yoo SJ, Kang MI, Cha BY, Lee KW, Son HY, Kang SK, Kim HS, Lee IK, Bonner-Weir S. Selective beta-cell loss and alpha-cell expansion in patients with type 2 diabetes mellitus in Korea. J Clin Endocrinol Metab 88: 2300-2308, 2003. doi:10.1210/jc.2002-020735.