Sodium-glucose cotransport

Current Opinion in Nephrology and Hypertension

Volumn 24, Issue 5, 2015, Pages 463-469

  Poulsen, Søren Brandt ^a,b   Fenton, Robert A ^a   Rieg, Timo ^b,c  

^a AARHUS UNIVERSITY   (Denmark)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Blood pressure; Colon; Dapagliflozin; Diabetic nephropathy; Glucagon like peptide 1; Phlorizin

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUCAGON LIKE PEPTIDE 2; GLUCOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; LEPTIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; PROTEIN KINASE WNK; PROTEIN SERINE THREONINE KINASE; RETINOSCHISIN; SODIUM GLUCOSE COTRANSPORTER 1; SODIUM GLUCOSE COTRANSPORTER 2; SODIUM GLUCOSE COTRANSPORTER INHIBITOR; STAT3 PROTEIN; UNCLASSIFIED DRUG; ANTIDIABETIC AGENT; GLUCOSE BLOOD LEVEL; SODIUM; SODIUM GLUCOSE COTRANSPORTER;

DIABETES MELLITUS; ENZYME REGULATION; GLUCOSE ABSORPTION; GLYCEMIC CONTROL; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; GLUCOSE BLOOD LEVEL; KIDNEY; METABOLISM;

ANIMALS; BLOOD GLUCOSE; GLUCOSE; HUMANS; HYPOGLYCEMIC AGENTS; KIDNEY; SODIUM; SODIUM-GLUCOSE TRANSPORT PROTEINS;

EID: 84942584748     PISSN: 10624821     EISSN: 14736543     Source Type: Journal    
DOI: 10.1097/MNH.0000000000000152     Document Type: Review

References (79)

1. Vallon V. The mechanisms and therapeutic potential of SGLT2 inhibitors in diabetes mellitus. Annu Rev Med 2015; 66:255-270. doi: 10.1146/annurevmed-051013-110046. [Epub ahead of print]
2. Gallo LA, Wright EM, Vallon V. Probing SGLT2 as a therapeutic target for diabetes: basic physiology and consequences. Diabetes Vasc Dis Re 2015; 12:78-89. 3.
3. Gorboulev V, Schurmann A, Vallon V, et al. Na+-D-glucose cotransporter SGLT1 is pivotal for intestinal glucose-Absorption and glucose-dependent incretin secretion. Diabetes 2012; 61:187-196. This study is first that d escribed the phenotype of the SGLT1 knockout mouse. 4.
4. Rieg T, Masuda T, Gerasimova M, et al. Increase in SGLT1-mediated transport explains renal glucose reabsorption during genetic and pharmacological SGLT2 inhibiti on in euglycemia. Am J Physiol Renal Physiol 2014; 306: F188-F193. This study described renal glucose handling in SGLT1/SGLT2 double knockout mice.
5. Wright EM, Loo DDF, Hirayama BA. Biology of human sodium glucose transporters. Physiol Rev 2011; 91:733-794.
6. Dyer J, Merediz EFC, Salmon KSH, et al. Molecular characterisation of carbohydrate digestion and absorption in equine small intestine. Equine Vet J 2002; 34:349-358.
7. Zhao FQ, Zheng YC, Wall EH, McFadden TB. Cloning and expression of bovine sodium/glucose cotransporters. J Dairy Sci 2005; 88:182-194.
8. Herrmann J, Schroder B, Klinger S, et al. Segmental diversity of electrogenic glucose transport characteristics in the small intestin es of weaned pigs. Comp Biochem Physiol A Mol Integr Physiol 2012; 163:161-169.
9. Batchelor DJ, Al-Rammahi M, Moran AW, et al. Sodium/glucose cotransporter-1, sweet receptor, and disaccharidase expression in the intestine of the domestic dog and cat: two species of different dietary habit. Am J Physiol Regul Integr Comp Physiol 2011; 300:R67-R75.
10. Muscher-Banse AS, Piechotta M, Schrooder B, Breves G. Modulation of intestinal glucose transport in response to reduced nitrogen supply in young goats. J Animal Sci 2012; 90:4995-5004.
11. Moran AW, Al-Rammahi M, Zhang C, et al. Sweet taste receptor expression in ruminant intestine and its activation by artificial sweeteners to regulate glucose absorption. J Dairy Sci 2014; 97:4955-4972.
12. Yang CB, Albin DM, Wang ZR, et al. Apical Na+-D-glucose cotransporter 1 (SGLT1) activity and protein abundance are expressed along the jejunal cryptvillus axis in the neonatal pig. Am J Physiol Gastrointest Liver Physiol 2011; 300:G60-G70.
13. Vrhova c I, Balen Eror D, Klessen D, et al. Localizations of Na+-d-glucose cotransporters SGLT1 and SGLT2 in human kidney and of SGLT1 in human small intestine, liver, lung, and heart. Pflügers Arch 2014. doi: 10.1007/s00424-014-1619-7. [Epub ahead of print] This study uses thoroughly evaluated SGLT1 and SGLT2 antibodies to characterize their expression in human tissue.
14. Vallon V, Platt KA, Cunard R, et al. SGLT2 mediates glucose reabsorption in the early proximal tubule. J Am Soc Nephrol 2011; 22:104-112. This study first described the phenotype of the SGLT2 knockout mouse.
15. Vallon V, Thomson SC. Renal function in diabetic disease models: the tubular system in the pathophysiology of the diabetic kidney. Annu Rev Physiol 2012; 74:351-375.
16. Ferraris RP, Diamond J. Regulation of intestinal sugar transport. Physiol Rev 1997; 77:257-302.
17. Dyer J, Hosie KB, Shirazi-Beechey SP. Nutrient regulation of human intestinal sugar transporter (SGLT1) expression. Gut 1997; 41:56-59.
18. Shirazi-Beechey SP,Gribble SM,Wood IS,et al. Dietary-regulation of the intestinal sodium-dependent glucose cotransporter (SGLT1 Biochem Soc Trans 1994, 22, 655-658.
19. Ferraris RP, Vinnakota RR. Intestinal nutrient transport in genetically obese mice. Am J Clin Nutr 1995; 62:540-546.
20. Fisher RB, Gardner ML. A diurnal rhythm in the absorption of glucose and water by isolated rat small intestine. J Physiol 1976; 254:821-825.
21. Corpe CP, Burant CF. Hexose transporter expression in rat small intestine: effect of diet on diurnal variations. Am J Physiol Gastrointest Liver Physiol 1996; 271:G211-G216.
22. Tavakkolizadeh A, Berger UV, Shen KR, et al. Diurnal rhythmicity in intestinal SGLT-1 function, V-max, and mRNA expression topog raphy. Am J Physiol Gastrointest Liver Physiol 2001; 280:G209-G215.
23. Pan XY, Terada T, Okuda M, Inui KI. The diurnal rhythm of the intestinal transporters SGLT1 and PEPT1 is regulated by the f eeding conditions in rats. J Nutr 2004; 134:2211-2215.
24. Pan X, Hussain MM. Clock is important for food and circadian regulation of macronutrient absorption in mice. J Lipid Res 2009; 50:1800-1813.
25. Mate A, Barfull A, Hermosa AM, et al. Regulation of sodium-glucose cotransporter SGLT1 in the intestine of hypertensive rats. Am J Physiol Regul Integr Comp Physiol 2006; 291:R760-767.
26. Grefner NM, Gromova LV, Gruzdkov AA, Komissarchik I. The interaction between SGLT1 or GLUT2 glucose transporter and the cytoskeleton in the enterocyte as well as Caco2 cell during hexose absorption. Tsi tologiia 2014; 56:749-757. This work suggested colocalization of the SGLT1 and GLUT2 and actin, as well as actin and a-tubulin, which suggests that elements of the cytoskeleton participate in the translocation of glucose transporters to t he apical cell membrane.
27. Ikari A, Harada H, Takagi K. Role of actin in the cAMP-dependent activation of sodium/glucose cotransporter in renal epithelial cells. Biochim Biophys Acta Biomemb 2005; 1711:20-24.
28. Elvira B, Honisch S, Almilaji A, et al. Up-regulation of Na+-coupled glucose transporter SGLT1 by caveolin-1. Biochim Biophys Acta Biomemb 2013; 1828:2394-2398.
29. Zhuang Z, Marshansky V, Breton S, Brown D. Is caveolin involved in normal proximal tubule function? Presence in model PT systems but absence in situ. Am J Physiol Renal Physiol 2011; 300:F199-F206.
30. Hirsch JR, Loo DDF, Wright EM. Regulation of Na+/glucose cotransporter expression by protein kinases in Xenopus laevis oocytes. J Biol Chem 1996; 271:14740-14746.
31. Wright EM, Hirsch JR, L oo DDF, Zampighi GA. Regulation of Na+/glucose cotransporters. J Exp Biol 1997; 200:287-293.
32. Subramanian S, Glitz P, Kipp H, et al. Protein kinase-A affects sorting and conformation of the sodium-dependent glucose co-transporter SGLT1. J Cell Biochem 2009; 106:444-452.
33. Ghezzi C, Wright EM. Regulation of the human Na+-dependent glucose cotransporter hSGLT2. Am J Physiol Cell Physiol 2012; 303:C348-C354. One of the limited studies describing the regulation of human SGLT2.
34. Aschenbach JR, Borau T, Gabel G. Glucose uptake via SGLT-1 is stimulated by beta(2)-Adrenoceptors in the ruminal epithelium of sheep. J Nutr 2002; 132:1254-1257.
35. Ishikawa Y, Eguchi T, Ishida H. Mechanism of beta-Adrenergic agon istinduced transmural transport of glucose in rat small intestine: regulation of phosphorylation of SGLT1 controls the function. Biochim Biophys Acta 1997; 1357:306-318.
36. Castaneda-Sceppa C, Subramanian S, Castaneda F. Protein kinase C mediated intracellular signaling pathways are involved in the regulation of sodium-dependent glucose co-transporter SGLT1 activity. J Cell Biochem 2010; 109:1109-1117.
37. Veyhl M, Wagner CA, Gorboulev V, et al. Downregulation of the Na+-Dglucose cotransporter SGLT1 by protein RS1 (RSC1A1) is dependent on dynamin and protein kinase C. J Memb Biol 2003; 196:71-81.
38. Vayro S, Silverman M. PKC regulates turnover rate of rabbit intestinal Na+glucose transporter expressed in COS-7 cells. Am J Physiol Cell Physiol 1999; 276:C1053-C1060.
39. Osswald C, Baumgarten K, Stumpel F, et al. Mice without the regulator gene Rsc1A1 exhibit increased Na+-(D)-glucose cotransport in small intestine and develop obesity. Mol Cell Biol 2005; 25:78-87.
40. Reinhardt J, Veyhl M, Wagner K, et al. Cloning and characterization of the transport modifier RS1 from rabbit which was previously assumed to be specific for Na+-D-glucose cotransport. Biochim Biophys Acta 1999; 1417:131-143.
41. Pakladok T, Hosseinzadeh Z, Alesutan I, Lang F. Stimulation of the Na+coupled glucose transporter SGLT1 by B-RAF. Biochem Biophys Res Commun 2012; 427:689-693.
42. Rexhepaj R,Artunc F,Metzger M,et al. PI3-kinase-dependent electrogenic intestinal transport of glucose and amino acids Pflugers Arch 2007 453, 863-870.
43. Kempe DS, S iraskar G, Frohlich H, et al. Regulation of renal tubular glucose reabsorption by Akt2/PKB beta. Am J Physiol Renal Physiol 2010; 298:F1113-F1117.
44. Hosseinzadeh Z, Bhavsar SK, Shojaiefard M, et al. Stimulation of the glucose carrier SGLT1 by JAK2. Biochem Biophys Res Commun 2011; 408:208-213.
45. Alesutan I, Sopjani M, Dermaku-Sopjani M, et al. Upregulation of Na+-coupl ed glucose transporter SGLT1 by Tau tubulin kinase 2. Cell Physiol Biochem 2012; 30:458-465.
46. Lee GH, Proenca R, Montez JM, et al. Abnormal splicing of the leptin receptor in diabetic mice. Nature 1996; 379:632-635.
47. Lostao MP, Urdaneta E, Martinez-Anso E, et al. Presence of leptin receptors in rat small intestine and leptin effect on sugar absorption. FEBS Lett 1998; 423:302-306.
48. Yara ndi SS, Hebbar G, Sauer CG, et al. Diverse roles of leptin in the gastrointestinal tract: modulation of motility, absorption, growth, and inflammation. Nutrition 2011; 27:269-275.
49. Cammisotto PG, Levy E, Bukowiecki LJ, Bendayan M. Cross-talk between adipose and gastric leptins for the control of food intake and energy metabolism. Progr Histochem Cytochem 2010; 45:143-200.
50. Doming uez Rieg JD, Chirasani V, Koepsell H, et al. Regulation of intestinal SGLT1 by catestatin in hyperleptinemic type 2 diabetic mice. FASEB J 2015; 29:A970.9.
51. Ducroc R, Guilmeau S, Akas hi K, et al. Luminal leptin induces rapid inhibition of active intestinal absorption of glucose mediated by sodium-glucose cotransporter Diabetes 2005; 54:348-354.
52. Tavernier A, Cavin JB, Le Gall M, et al. Intestinal deletion of leptin signaling alters activity of nutrient transporters and delayed the onset of obesity in mice. FASEB J 2014; 28:4100-4110.
53. Barrenetxe J, Sainz N, Barber A, Lostao MP. Involvement of PKC and PKA in the inhibitory effect of leptin on intestinal galactose absorption. Biochem Biophys Res Commun 2004; 317:717-721.
54. Elvira B, Blecua M, Luo D, et al. SPAK-sensitive regulation of glucose transporter SGLT1. J Memb Biol 2014; 247:1191-1197. This study reports that in oocytes, coexpression of SPAK and SGLT1 decreases SGLT1 plasma membrane abun dance.
55. Pasham V, Pathare G, Fajol A, et al. OSR1-sensitive small intestinal Na+ transport. Am J Physiol Gastrointest Liver Physiol 2012; 303:G1212-G1219.
56. Sopjani M, Bhavsar SK, Fraser S, et al. Regulation of Na+-coupled glucose carrier SGLT1 by AMP-Activated protein kinase. Mol Memb Biol 2010; 27:137-144.
57. Artunc F, Rexhepaj R, Volkl H, et a l. Impaired intestinal and renal glucose transport in PDK-1 hypomorphic mice. Am J Physiol Regul Integr Comp Physiol 2006; 291:R1533-R1538.
58. Shojaiefard M, Strutz-Seebohm N, Tavare JM, et al. Regulation of the Na+ , glucose cotransporter by PIKfyve and the serum and glucocorticoid inducible kinase SGK1. Biochem Biophys Res Commun 2007; 359: 843-847.
59. Grahammer F, Henke G, Sandu C, e t al. Intestinal function of gene-targeted mice lacking serum-And glucocorticoid-inducible kinase 1. Am J Physiol Gastrointest Liver Physiol 2006; 290:G1114-G1123.
60. Sandu C, Rexhepaj R, Grahammer F, et al. Decreased intestinal glucose transport in the sgk3-knockout mouse. Pflugers Arch 2005; 451:437-444.
61. Dieter M, PalmadaM, Rajama nickam J, et al. Regulation of glucose transporter SGLT1 by ubiquitin ligase Nedd4-2 and kinases SGK1, SGK3, and PKB. Obesity Res 2004; 12:862-870.
62. Feric M, Zhao B, Hoffert JD, et al. Large-scale phosphoproteomic analysis of membrane proteins in renal proximal and distal tubule. Am J Physiol Cell Physiol 2011; 300:C755-C770.
63. Nakamura N, Matsui T, Ishibashi Y, Yamagishi S. Insulin s timulates SGLT2-mediated tubular glucose absorption via oxidative stress generation. Diabetol Metab Syndr 2015; 7:48. This study demonstrates that insulin stimulates SGLT2-mediated glucose entry into cultured proximal tubular cells v ia oxidative stress generation.
64. Lee YJ,Kim MO,Ryu JM,Han HJ. Regulation of SGLT expression and localization through Epac/PKA-dependent caveolin-1 and F-Actin activation in renal proximal tubule cells. Biochim Biophy s Acta Mol Cell Res 2012 1823 971-982.
65. Maldonado-Cervantes MI, Galicia OG, Moreno-Jaime B, et al. Autocrine modulation of glucose transporter SGLT2 by IL-6 and TNF-Alpha in LLCPK1 cells. J Physio l Biochem 2012; 68:411-420.
66. Panchapakesan U, Pegg K, Gross S, et al. Effects of SGLT2 inhibition in human kidney proximal tubular cells-renoprotection in diabetic nephropathy? PLos One 2013; 8:e54442.
67. Zapata-Morales JR, Galicia-Cruz OG, Franco M, Morales FMY. Hypoxiainducible factor-1 alpha (HIF-1 alpha) protein diminishes sodium glucose transport 1 (SGLT1) and SGLT2 protein expression in renal epit helial tubular cells (LLC-PK1) under hypoxia. J Biol Chem 2014; 289: 346-357. In this work, it was shown that HIF-1a mediates changes in mRNA and protein expression of SGLT1 and SGLT2 in LLC-PK1 cell monolayers under low O2 concentrations.
68. Tabatabai NM, Blumenthal SS, Lewand DL, Petering DH. Mouse kidney expresses mRNA of four highly related sodium-glucose cotransporters: regulation by cadmium. Kidney Int 2003; 64:1320-1330.
69. Kothinti RK, Blodgett AB, Petering DH, Tabatabai NM. Cadmium downregulation of kidney Sp1 binding to mouse SGLT1 and SGLT2 gene promoters: possible reaction of cadmium with the zinc finger domain of Sp1. Toxicol Appl Pha rmacol 2010; 244:254-262.
70. Vallon V, Rose M, Gerasimova M, et al. Knockout of Na-glucose transporter SGLT2 attenuates hyperglycemia and glomerular hyperfiltration but not kidney growth or injury i n diabetes mellitus. Am J Physiol Renal Physiol 2013; 304:F156-F167.
71. Brouwers B, Pruniau VP, Cauwelier EJ, et al. Phlorizin pretreatment reduces acute renal toxicity in a mouse model for dia betic nephropathy. J Biol Chem 2013; 288:27200-27207.
72. Albertoni Borghese MF, Majowicz MP, Ortiz MC, et al. Expression and activity of SGLT2 in diabetes induced by streptozotocin: relationshi p with the lipid environment. Nephron Physiol 2009; 112:45-52.
73. Debnam ES, Smith MW, Sharp PA, et al. The effects of streptozotocin diabetes on sodium-glucose transporter (SGLT1) expression an d function in rat jejunal and ileal villus-Attached enterocytes. Pflugers Arch 1995; 430:151-159.
74. Vallon V, Gerasimova M, Rose MA, et al. SGLT2 inhibitor empagliflozin reduces renal growth and albuminuria in proportion to hyperglycemia and prevents glomerular hyperfiltration in diabetic Akita mice. Am J Physiol Renal Phys iol 2014; 306:F194-F204. This study uses the Akita mouse model of type 1 diabetes mellitus to evaluate the beneficial effects of empagliflozin. Results show that empagliflozin attenuates/prevents hyperglycemia, glomerular hyperfiltration, hypertension and kidney growth.
75. Komala MG, Panchapakesan U, Pollock C, Mather A. Sodium glucose cotransporter 2 and the diabetic kidney. Curr Opin Nephrol Hypertens 2013; 22:113-119.
76. Vallon V. The proximal tubule in the pathophysiology of the diabetic kidney. Am J Physiol Reg I 2011; 300:R1009-R1022.
77. Zambrowicz B, Lapuerta P, Strumph P, et al. LX4211 therapy reduces postprandial glucose levels in patients with type 2 diabetes mellitus and renal impairment despite low urinary glucose excretion. Clin Ther 2015; 37:71-82. This clinical trial shows that postprandial glucose levels were main t ained in patients with an estimated GFR of less than 45 ml/min/1.73m2 despite the expected reduction in urinary glucose excretion suggesting that dual SGLT1/2 inhibition could prove useful for the treatment of patients with type 2 diabetes mellitus and im paired renal function.
78. Henry RR, Rosenstock J, Edelman S, et al. Exploring the potential of the SGLT2 inhibitor dapagliflozin in type 1 diabetes: a randomized, double-blind, placebo-controlled pilot study. Di abetes Care 2015; 38:412-419.
79. Shibazaki T, Tomae M, Ishikawa-Takemura Y, et al. KGA-2727, a novel selective inhibitor of a high-Affinity sodium glucose cotransporter (SGLT1), exhibits antidiabeti c efficacy in rodent models. J Pharmacol Exp Ther 2012; 342:288-296.