Experimental type II diabetes and related models of impaired glucose metabolism differentially regulate glucose transporters at the proximal tubule brush border membrane

Experimental Physiology

Volumn 101, Issue 6, 2016, Pages 731-742

  Chichger, Havovi ^a   Cleasby, Mark E ^b   Srai, Surjit K ^c   Unwin, Robert J ^c   Debnam, Edward S ^c   Marks, Joanne ^c  

^a ANGLIA RUSKIN UNIVERSITY   (United Kingdom)

^b ROYAL VETERINARY COLLEGE   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; GLUCOSE TRANSPORTER; GLUCOSE TRANSPORTER 2; PHLORIZIN; PROTEIN KINASE C BETA; PROTEIN KINASE C BETA1; SODIUM GLUCOSE COTRANSPORTER 1; SODIUM GLUCOSE COTRANSPORTER 2; UNCLASSIFIED DRUG; PROTEIN KINASE C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRUSH BORDER; CONTROLLED STUDY; EXPERIMENTAL DIABETES MELLITUS; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCEMIC CONTROL; HYPERGLYCEMIA; IMPAIRED GLUCOSE TOLERANCE; INSULIN RESISTANCE; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE ABSORPTION; LIPID DIET; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; WESTERN BLOTTING; WESTERN DIET; ANIMAL; GLUCOSE BLOOD LEVEL; KIDNEY; MEMBRANE; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; BLOOD GLUCOSE; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DIET, HIGH-FAT; GLUCOSE; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; GLUCOSE TRANSPORTER TYPE 2; HYPERGLYCEMIA; INSULIN RESISTANCE; KIDNEY; KIDNEY TUBULES, PROXIMAL; MALE; MEMBRANES; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; SODIUM-GLUCOSE TRANSPORTER 1; SODIUM-GLUCOSE TRANSPORTER 2;

EID: 84966622082     PISSN: 09580670     EISSN: 1469445X     Source Type: Journal    
DOI: 10.1113/EP085670     Document Type: Article

References (55)

1. Aguilar-Salinas CA, Rojas R, Gómez-Pérez FJ, Mehta R, Franco A, Olaiz G & Rull JA (2005). The metabolic syndrome: a concept hard to define. Arch Med Res 36, 223-231.
2. Ait-Omar A, Monteiro-Sepulveda M, Poitou C, Le Gall M, Cotillard A, Gilet J, Garbin K, Houiller A, Château D, Lacombe A, Veyrie N, Hugol D, Tordjman J, Magnan C, Serradas P, Clément K, Leturque A & Brot-Laroche E (2011). GLUT2 accumulation in enterocyte apical and intracellular membranes: a study in morbidly obese human subjects and ob/ob and high-fat-fed mice. Diabetes 60, 2598-2607.
3. Albertoni Borghese MF, Majowicz MP, Ortiz MC, del Rosario Passalacqua M, Sterin Speziale NB & Vidal NA (2009). Expression and activity of SGLT2 in diabetes induced by streptozotocin: relationship with the lipid environment. Nephron Physiol 112, p45-p52.
4. AlSaraj F, McDermott JH, Cawood T, McAteer S, Ali M, Tormey W, Cockburn BN & Sreenan S (2009). Prevalence of the metabolic syndrome in patients with diabetes mellitus. Ir J Med Sci 178, 309-313.
5. 2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest 119, 573-581.
6. +-glucose cotransporter inhibitor T-1095. Br J Pharmacol 132, 578-586.
7. Barcelona S, Menegaz D & Díez-Sampedro A (2012). Mouse SGLT3a generates proton-activated currents but does not transport sugar. Am J Physiol Cell Physiol 302, C1073-C1082.
8. Barfuss DW & Schafer JA (1981). Differences in active and passive glucose transport along the proximal nephron. Am J Physiol Renal Physiol 241, F322-F332.
9. Bayol SA, Simbi BH & Stickland NC (2005). A maternal cafeteria diet during gestation and lactation promotes adiposity and impairs skeletal muscle development and metabolism in rat offspring at weaning. J Physiol 567, 951-961.
10. Boot-Handford RP & Heath H (1981). The effect of dietary fructose and diabetes on the rat kidney. Br J Exp Pathol 62, 398-406.
11. Bradford MM (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
12. Brown GK (2000). Glucose transporters: structure, function and consequences of deficiency. J Inherit Metab Dis 23, 237-246.
13. Cramer SC, Pardridge WM, Hirayama BA & Wright EM (1992). Colocalization of GLUT2 glucose transporter, sodium/glucose cotransporter, and γ-glutamyl transpeptidase in rat kidney with double-peroxidase immunocytochemistry. Diabetes 41, 766-770.
14. Debnam ES & Unwin RJ (1996). Hyperglycemia and intestinal and renal glucose transport: implications for diabetic renal injury. Kidney Int 50, 1101-1109.
15. Diez-Sampedro A, Hirayama BA, Osswald C, Gorboulev V, Baumgarten K, Volk C, Wright EM & Koepsell H (2003). A glucose sensor hiding in a family of transporters. Proc Natl Acad Sci USA 100, 11753-11758.
16. Dluhy RG & McMahon GT (2008). Intensive glycemic control in the ACCORD and ADVANCE trials. N Engl J Med 358, 2630-2633.
17. Duckworth W, Abraira C, Moritz T, Reda D, Emanuele N, Reaven PD, Zieve FJ, Marks J, Davis SN, Hayward R, Warren SR, Goldman S, McCarren M, Vitek ME, Henderson WG & Huang GD; VADT Investigators (2009). Glucose control and vascular complications in veterans with type 2 diabetes. N Engl J Med 360, 129-139.
18. Feraille E, Marsy S, Barlet-Bas C, Rousselot M, Cheval L, Favre H & Doucet A (1995). Insulin unresponsiveness of tubular monovalent cation transport during fructose-induced hypertension in rats. Clin Sci (Lond) 88, 293-299.
19. Fulgoni V 3rd (2008). High-fructose corn syrup: everything you wanted to know, but were afraid to ask. Am J Clin Nutr 88, 1715S.
20. Gai Z, Hiller C, Chin SH, Hofstetter L, Stieger B, Konrad D & Kullak-Ublick GA (2014). Uninephrectomy augments the effects of high fat diet induced obesity on gene expression in mouse kidney. Biochim Biophys Acta 1842, 1870-1878.
21. Goestemeyer AK, Marks J, Srai SK, Debnam ES & Unwin RJ (2007). GLUT2 protein at the rat proximal tubule brush border membrane correlates with protein kinase C (PKC)-βl and plasma glucose concentration. Diabetologia 50, 2209-2217.
22. Goto Y, Kakizaki M & Masaki N (1976). Production of spontaneous diabetic rats by repetition of selective breeding. Tohoku J Exp Med 119, 85-90.
23. Han S, Hagan DL, Taylor JR, Xin L, Meng W, Biller SA, Wetterau JR, Washburn WN & Whaley JM (2008). Dapagliflozin, a selective SGLT2 inhibitor, improves glucose homeostasis in normal and diabetic rats. Diabetes 57, 1723-1729.
24. Hu FB, Manson JE, Stampfer MJ, Colditz G, Liu S, Solomon CG & Willett WC (2001). Diet, lifestyle, and the risk of type 2 diabetes mellitus in women. N Engl J Med 345, 790-797.
25. Huggett AS & Nixon DA (1957). Use of glucose oxidase, peroxidase, and O-dianisidine in determination of blood and urinary glucose. Lancet 273, 368-370.
26. +/d-glucose cotransporters SGLT1 and SGLT2. Am J Physiol Cell Physiol 300, C14-C21.
27. Inoue S, Honma K, Mochizuki K, Goda T (2015). Induction of histone H3K4 methylation at the promoter, enhance, and transcribed regions of the Si and Sglt1 genes in rat jejunum in response to a high-starch/low-fat diet. Nutrition 31, 366-372.
28. Jang HJ, Kokrashvili Z, Theodorakis MJ, Carlson OD, Kim BJ, Zhou J, Kim HH, Xu X, Chan SL, Juhaszova M, Bernier M, Mosinger B, Margolskee RF & Egan JM (2007). Gut-expressed gustducin and taste receptors regulate secretion of glucagon-like peptide-1. Proc Natl Acad Sci USA 104, 15069-15074.
29. Junien C & Nathanielsz P (2007). Report on the IASO Stock Conference 2006: early and lifelong environmental epigenomic programming of metabolic syndrome, obesity and type II diabetes. Obes Rev 8, 487-502.
30. Lee EY, Kaneko S, Jutabha P, Zhang X, Seino S, Jomori T, Anzai N & Miki T (2015a). Distinct action of the α-glucosidase inhibitor miglitol on SGLT3, enteroendocrine cells, and GLP1 secretion. J Endocrinol 224, 205-214.
31. Lee JW, Chou CL & Knepper MA (2015b). Deep sequencing in microdissected renal tubules identifies nephron segment-specific transcriptomes. J Am Soc Nephrol 26, 2669-2677.
32. Li X, Staszewski L, Xu H, Durick K, Zoller M & Adler E (2002). Human receptors for sweet and umami taste. Proc Natl Acad Sci USA 99, 4692-4696.
33. Liu JJ, Lee T & DeFronzo RA (2012). Why do SGLT2 inhibitors inhibit only 30-50% of renal glucose reabsorption in humans? Diabetes 61, 2199-2204.
34. Mace OJ, Affleck J, Patel N & Kellett GL (2007). Sweet taste receptors in rat small intestine stimulate glucose absorption through apical GLUT2. J Physiol 582, 379-392.
35. Mace OJ, Lister N, Morgan E, Shepherd E, Affleck J, Helliwell P, Bronk JR, Kellett GL, Meredith D, Boyd R, Pieri M, Bailey PD, Pettcrew R & Foley D (2009). An energy supply network of nutrient absorption coordinated by calcium and T1R taste receptors in rat small intestine. J Physiol 587, 195-210.
36. Marks J, Carvou NJ, Debnam ES, Srai SK & Unwin RJ (2003). Diabetes increases facilitative glucose uptake and GLUT2 expression at the rat proximal tubule brush border membrane. J Physiol 553, 137-145.
37. Mattes RD & Popkin BM (2009). Nonnutritive sweetener consumption in humans: effects on appetite and food intake and their putative mechanisms. Am J Clin Nutr 89, 1-14.
38. Moeller SM, Fryhofer SA, Osbahr AJ 3rd & Robinowitz CB; Council on Science and Public Health, American Medical Association (2009). The effects of high fructose syrup. J Am Coll Nutr 28, 619-626.
39. Noll C, Lacraz G, Ehses J, Coulhaud J, Bailbe D, Paul J, Portha B, Homo-Delarche F & Janel N (2011). Early reduction of circulating homocysteine levels in Goto-Kakizaki rat, a spontaneous nonobese model of type 2 diabetes. Biochim Biophys Acta 1812, 699-702.
40. 2 tension in the renal cortex but causes hypoxia in the renal medulla in anaesthetized control and diabetic rats. Am J Physiol Renal Physiol 309, F227-F234.
41. Pal A, Rhoads DB & Tavakkoli A (2015). Foregut exclusion disrupts intestinal glucose sensing and alters portal nutrient and hormonal milieu. Diabetes 64, 1941-1950.
42. Parker HE, Habib AM, Rogers GJ, Gribble FM & Reimann F (2009). Nutrient-dependent secretion of glucose-dependent insulinotropic polypeptide from primary murine K cells. Diabetologia 52, 289-298.
43. Pepino MY, Tiemann CD, Patterson BW, Wice BM & Klein S (2013). Sucralose affects glycemic and hormonal responses to an oral glucose load. Diabetes Care 36, 2530-2535.
44. Phillips AO, Steadman R, Morrisey K, Martin J, Eynstone L & Williams JD (1997). Exposure of human renal proximal tubular cells to glucose leads to accumulation of type IV collagen and fibronectin by decreased degradation. Kidney Int 52, 973-984.
45. Poulsen SB, Fenton RA & Rieg T (2015). Sodium-glucose cotransport. Curr Opin Nephrol Hypertens 24, 463-469.
46. Rahmoune H, Thompson PW, Ward JM, Smith CD, Hong G & Brown J (2005). Glucose transporters in human renal proximal tubular cells isolated from the urine of patients with non-insulin-dependent diabetes. Diabetes 54, 3427-3434.
47. Rajkumar P, Aisenberg WH, Acres OW, Protzko RJ & Pluznick JL (2014). Identification and characterization of novel renal sensory receptors. PLoS ONE 9, e111053.
48. Rieg T, Masuda T, Gerasimova M, Mayoux E, Platt K, Powell DR, Thomson SC, Koepsell H & Vallon V (2014). Increase in SGLT1-mediated transport explains renal glucose reabsorption during genetic and pharmacological SGLT2 inhibition in euglycemia. Am J Physiol Renal Physiol 306, F188-F193.
49. Rothwell NJ & Stock MJ (1979). Regulation of energy balance in two models of reversible obesity in the rat. J Comp Physiol Psychol 93, 1024-1034.
50. Suez J, Korem T, Zeevi D, Zilberman-Schapira G, Thaiss CA, Maza O, Israeli D, Zmora N, Gilad S, Weinberger A, Kuperman Y, Harmelin A, Kolodkin-Gal I, Shapiro H, Halpern Z, Segal E & Elinav E (2014). Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature 514, 181-186.
51. Tobin V, Le Gall M, Fioramonti X, Stolarczyk E, Blazquez AG, Klein C, Prigent M, Serradas P, Cuif MH, Magnan C, Leturque A & Brot-Laroche E (2008). Insulin internalizes GLUT2 in the enterocytes of healthy but not insulin-resistant mice. Diabetes 57, 555-562.
52. Turner RJ & Silverman M (1977). Sugar uptake into brush border vesicles from normal human kidney. Proc Natl Acad Sci USA 74, 2825-2829.
53. Vallon V, Rose M, Gerasimova M, Satriano J, Platt KA, Koepsell H, Cunard R, Sharma K, Thomson SC & Rieg T (2013). Knockout of Na-glucose transporter SGLT2 attenuates hyperglycemia and glomerular hyperfiltration but not kidney growth or injury in diabetes mellitus. Am J Physiol Renal Physiol 304, F156-F167.
54. +-glucose cotransporters. Am J Physiol Renal Physiol 280, F10-F18.
55. Yang Q (2010). Gain weight by "going diet?" Artificial sweeteners and the neurobiology of sugar cravings: Neuroscience 2010. Yale J Biol Med 83, 101-108.