Natural Products as Lead Compounds for Sodium Glucose Cotransporter (SGLT) Inhibitors

Planta Medica

Volumn 83, Issue 12-13, 2017, Pages 985-993

  Blaschek, Wolfgang ^a  

^a UNIVERSITY OF KIEL   (Germany)

Author keywords

diabetes; flavonoids; gliflozins; Malus domestica; Phlorizin; Rosaceae; SGLT inhibitors

Indexed keywords

ALBIGLUTIDE; CANAGLIFLOZIN; DAPAGLIFLOZIN; DULAGLUTIDE; EMPAGLIFLOZIN; EXENDIN 4; FLAVONOID; GLUCOSE TRANSPORTER; HEMOGLOBIN A1C; IPRAGLIFLOZIN; LIRAGLUTIDE; LUSEOGLIFLOZIN; LUTEOLIN; METFORMIN; NATURAL PRODUCT; PHLORIZIN; POLYPHENOL; PRAMLINTIDE; QUERCETIN; RECOMBINANT HUMAN INSULIN; REMOGLIFLOZIN ETABONATE; SERGLIFLOZIN ETABONATE; SODIUM GLUCOSE COTRANSPORTER; SODIUM GLUCOSE COTRANSPORTER 1; SODIUM GLUCOSE COTRANSPORTER 1 INHIBITOR; SODIUM GLUCOSE COTRANSPORTER 2 INHIBITOR; SODIUM GLUCOSE COTRANSPORTER INHIBITOR; SOTAGLIFLOZIN; TOFOGLIFLOZIN; UNCLASSIFIED DRUG; UNINDEXED DRUG; BIOLOGICAL PRODUCT; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 2; INSULIN; SLC2A1 PROTEIN, HUMAN; SLC2A2 PROTEIN, HUMAN; SLC5A1 PROTEIN, HUMAN; SLC5A2 PROTEIN, HUMAN; SODIUM GLUCOSE COTRANSPORTER 2;

BIOSYNTHESIS; CHEMICAL COMPOSITION; CONCENTRATION RESPONSE; DIABETES CONTROL; DIARRHEA; ENZYME INHIBITION; EPIDEMIOLOGICAL DATA; FLATULENCE; GLOMERULUS FILTRATION; GLUCOGENESIS; GLUCOSE ABSORPTION; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE INTAKE; GLUCOSURIA; GLYCOGEN METABOLISM; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; MALABSORPTION; MEDICINAL PLANT; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; ORAL REHYDRATION THERAPY; PREGNANCY DIABETES MELLITUS; PROTEIN TRANSPORT; REVIEW; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DRUG EFFECTS; GLUCONEOGENESIS; KIDNEY; METABOLISM;

BIOLOGICAL PRODUCTS; BLOOD GLUCOSE; DIABETES MELLITUS, TYPE 2; GLUCONEOGENESIS; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; GLUCOSE TRANSPORTER TYPE 1; GLUCOSE TRANSPORTER TYPE 2; HUMANS; INSULIN; KIDNEY; SODIUM-GLUCOSE TRANSPORT PROTEINS; SODIUM-GLUCOSE TRANSPORTER 1; SODIUM-GLUCOSE TRANSPORTER 2;

EID: 85017460512     PISSN: 00320943     EISSN: 14390221     Source Type: Journal    
DOI: 10.1055/s-0043-106050     Document Type: Review

References (82)

1. Petersen C. Analyse des Phloridzins. Ann Acad Sci Fr: 1835; 15 178
2. Zemplen G. Bognar R. Synthese des natürlichen Phlorrhizins. Chem Ber: 1942; 75 1040
3. De Koninck L. Observations sur les proprieties febrifuges de las phloridzine. Bull Soc Med Gand: 1836; 1 75 110
4. Von Mering J. Über künstlichen Diabetes. Centralbl Med Wiss: 1886; 22 531
5. Stiles P. G. Lusk G. On the action of phlorizin. Am J Physiol: 1903; 10 61 79
6. Chassis H. Jolliffe N. Smith H. The action of phlorizin on the excretion of glucose, xylose, sucrose, creatinine, and urea by man. J Clin Invest: 1933; 12 1083 1089
7. Crane R. K. Miller D. Bihler I. The Restrictions on possible Mechanisms of intestinal active Transport of Sugars. In: Kleinzeller A. Kotyk A. eds. Intestinal Absorption. London Academic Press: 1961; 439 449
8. Alvarado F. C. Crane R. K. Phlorizine as a competitive inhibitor of the active transport of sugars by hamster small intestine in vitro. Biochim Biophys Acta: 1962; 56 170 172
9. Vick H. D. Deidrich D. F. Reevaluation of renal tubular glucose transport inhibition by phlorizin analogs. Am J Physiol: 1973; 224 552 557
10. + -dependent hexose transport in a cultured line of porcine kidney cells. Am J Physiol: 1982; 242 C94 C101
11. Lee W. S. Wells R. G. Hediger M. A. The high affinity Na/glucose cotransporter: reevaluation and distribution of expression. J Biol Chem: 1994; 268 12032 12039
12. Ehrenkranz J. RL. Lewis N. G. Kahn C. R. Roth J. Phlorizin: a review. Diabetes Metab Res Rev: 2005; 21 31 38
13. + -glucose cotransporters, may provide a novel approach to treating diabetes. Diabetes: 1999; 48 1794 1800
14. Katsuno K. Fujimori Y. Takemura Y. Hiratochi M. Itoh F. Komatsu Y. Fujikura H. Isaji M. Sergliflozin, a novel selective inhibitor of low-affinity sodium glucose cotransporter (SGLT2), validates the critical role of SGLT2 in renal glucose reabsorption and modulates plasma glucose level. J Pharmacol Exp Ther: 2007; 320 323 330
15. Fujimori Y. Katsuno K. Nakashima I. Ishikawa-Takemura Y. Fujikura H. Isaji M. Remogliflozin etabonate, in a novel category of selective low-affinity sodium glucose cotransporter (SGLT2) inhibitors, exhibits antidiabetic efficacy in rodent models. J Pharmacol Exp Ther: 2008; 327 268 276
16. Link J. T. Sorensen B. K. A method for preparing C-glycosides related to phlorizin. Tetrahedron Lett: 2000; 41 9213 9217
17. Meng W. Ellsworth B. A. Nirschl A. A. McCann P. J. Patel M. Girotra R. N. Wu G. Sher P. M. Morrison E. P. Biller S. A. Zahler R. Deshpande P. P. Pullockaran A. Hagan D. L. Morgan N. Taylor J. R. Obermeier M. T. Humphreys W. G. Khanna A. Discenza L. Robertson J. G. Wang A. Han S. Wetterau J. R. Janovitz E. B. Flint O. P. Whaley J. M. Washburn W. N. Discovery of dapagliflozin: A potent, selective renal sodium-dependent glucose cotransporter 2 (SGLT2) inhibitor for the treatment of type 2 diabetes. J Med Chem: 2008; 51 1145 1149
18. Nomura S. Sasamaki S. Hongu M. Kawanishi E. Koga Y. Sakamoto T. Yamamoto Y. Ueta K. Kimata H. Nakayama K. Tsuda-Tsukimoto M. Discovery of canagliflozin, a novel C-glucoside with thiophene ring, as sodium-dependent glucose cotransporter 2 inhibitor for the treatment of type 2 diabetes mellitus. J Med Chem: 2010; 53 6355 6360
19. Grampler R. Thomas L. Eckhardt M. Himmelsbach F. Sauer A. Sharp D. E. Bakker R. A. Mark M. Klein T. Eickelmann P. Empagliflozin, a novel selective sodium glucose cotransporter-2 (SGLT-2) inhibitor: Characterisation and comparison with other SGLT-2 inhibitors. Diabetes Obes Metab: 2012; 14 83 90
20. Mudaliar S. Polidori D. Zambrowicz B. Henry R. R. Sodium-glucose cotransporter inhibitors: effects on renal and intestinal glucose transport. Diabetes Care: 2015; 38 2344 2353
21. Lapuerta P. Zambrowicz B. Strumph P. Sands A. Development of sotagliflozin, a dual sodium-dependent glucose transporter 1/2 inhibitor. Diab Vasc Dis Res: 2015; 12 101 110
22. Vallon V. The mechanisms and therapeutic potential of SGLT2 inhibitors in diabetes mellitus. Annu Rev Med: 2015; 66 255 270
23. Song P. Onishi A. Koepsell H. Vallon V. Sodium glucose cotransporter SGLT1 as a therapeutic target in diabetes mellitus. Expert Opin Ther Targets: 2016; 20 1109 1125
24. Madaan T. Akhtar M. Abul Najmi S. K. Sodium glucose cotransporter 2 (SGLT2) inhibitors: Current status and future perspective. Eur J Pharm Sci: 2016; 93 244 252
25. Koepsell H. The Na+-D-Glucose cotransporters SGLT1 and SGLT2 are targets for the treatment of diabetes and cancer. Pharmacol Ther: 2017; 170 148 165
26. Cefalu W. T. ed. Standards of Medical Care in Diabetes - 2016. Diabetes Care: 2016; 39 S1 S112
27. Marín-Peñalver J. J. Martín-Timón I. Sevillano-Collantes C. del Cañizo-Gómez F. J. Update on the treatment of type 2 diabetes mellitus. World J Diabetes: 2016; 7 354 395
28. World Health Organization Global Report on Diabetes 2016. Geneva World Health Organization: 2016
29. Gururaj Setty S. Crasto W. Jarvis J. Khunti K. Davies M. J. New insulins and newer insulin regimens: a review of their role in improving glycaemic control in patients with diabetes. Postgrad Med J: 2016; 92 152 164
30. Bennett W. L. Maruthur N. M. Singh S. Segal J. B. Wilson L. M. Chatterjee R. Marinpopoulos S. S. Puhan M. A. Ranasinghe P. Block L. Nocholson W. K. Hutfless S. Bass E. B. Bolen S. Comparative effectiveness and safety of medications for type 2 diabetes: an update including new drugs and 2-drug combinations. Ann Intern Med: 2011; 154 602 613
31. + /glucose co-transporter. Nature: 1987; 330 379 381
32. + /proline cotransporters. Proc Natl Acad Sci: 1989; 86 5748 5752
33. + /glucose cotransporter SGLT1. J Biol Chem: 1996; 271 1925 1934
34. Turk E. Wright E. M. Membrane topology motifs in the SGLT (1996) cotransporter family. J Membr Biol: 1997; 159 1 20
35. +: glucose coupling ratio for the human SGLT1 cotransporter. Biophys J: 1995; 69 2405 2414
36. + /glucose cotransporter (SGLT1) currents and fluxes. J Membr Biol: 1998; 162 101 106
37. Wright E. M. Loo D. DF. Hirayama B. A. Biology of human sodium glucose transporters. Physiol Rev: 2011; 91 733 794
38. World Health Organization The treatment of diarrhea, a manual for physicians and other senior health workers. Geneva World Health Organization: 2005
39. Loo D. D. Wright E. M. Zeuthen T. Water pumps. J Physiol: 2002; 542 53 60
40. + /glucose cotransport. Biophys J: 2004; 86 125 133
41. Erokhova L. Horner A. Ollinger N. Siligan C. Pohl P. The sodium glucose cotransporter SGLT1 is an extremely efficient facilitator of passive water transport. J Biol Chem: 2016; 291 9712 9720
42. Preuss H. G. Basics of renal anatomy and physiology. Clin Lab Med: 1993; 13 1 11
43. Vallon V. The proximal tubule in the pathophysiology of the diabetic kidney. Am J Physiol Regul Integr Comp Physiol: 2011; 300 R1009 R1022
44. DeFronzo R. A. Hompesch M. Kasichayanula S. Liu X. Hong Y. Pfister M. Morrow L. A. Leslie B. R. Boulton D. W. Ching A. LaCreta F. P. Griffen S. C. Characterization of renal glucose reabsorption in response to dapagliflozin in healthy subjects and subjects with type 2 diabetes. Diabetes Care: 2013; 36 3169 3176
45. Gallo L. A. Wright E. M. Vallon V. Probing SGLT2 as a therapeutic target for diabetes: Basic physiology and consequences. Diab Vasc Dis Res: 2015; 12 78 89
46. Liu J. Lee T. W. DeFronzo R. A. Why do SGLT2 inhibitors inhibit only 30-50% of renal glucose reabsorption in humans? Diabetes: 2012; 61 2199 2204
47. Rosenstock J. Jelaska A. Frappin G. Salsali A. Kim G. Woerle H. J. Broedl U. C. Improved glucose control with weight loss, lower insulin doses, and no increased hypoglycemia with empagliflozin added to titrated multiple daily injections of insulin in obese inadequately controlled type 2 diabetes. Diabetes Care: 2014; 37 1815 1823
48. Nauck M. A. Update on developments with SGLT2 inhibitors in the management of type 2 diabetes. Drug Des Devel Ther: 2014; 8 1335 1380
49. Blevins T. Combination therapy for patients with uncontrolled type 2 diabetes mellitus: Adding empagliflozin to pioglitazone or pioglitazone plus metformin. Expert Opin Drug Saf: 2015; 14 789 793
50. DeFronzo R. A. Lewin A. Patel S. Liu D. Kaste R. Woerle H. J. Broedl U. C. Combination of empagliflozin and linagliptin as second-line therapy in subjects with type 2 diabetes inadequately controlled on metformin. Diabetes Care: 2015; 38 384 393
51. Kushner P. Benefits/risks of sodium-glucose co-transporter 2 inhibitor canagliflozin in women for the treatment of type 2 diabetes. Women's Health (Lond): 2016; 12 379 388
52. Nyirjesy P. Sobel J. D. Fung A. Mayer C. Capuano G. Way K. Usiskin K. Genital mycotic infections with canagliflozin, a sodium glucose co-transporter 2 inhibitor, in patients with type 2 diabetes mellitus: a pooled analysis of clinical studies. Curr Med Res Opin: 2014; 30 1109 1119
53. Campbell J. E. Drucker D. J. Pharmacology, physiology, and mechanisms of incretin hormone action. Cell Metab: 2013; 17 819 837
54. Spreckley E. Murphy K. G. The L-cell in nutritional sensing and the regulation of appetite. Front Nutr: 2015; 2 23
55. Zambrowicz B. Freiman J. Brown P. M. Frazier K. S. Turnage A. Bronner J. Ruff D. Shadoan M. Banks P. Mseeh F. Rawlins D. B. Goodwin N. C. Mabon R. Harrison B. A. Wilson A. Sands A. Powell D. R. LX4211, a dual SGLT1/SGLT2 inhibitor, improved glycemic control in patients with type 2 diabetes in a randomized, placebo-controlled trial. Clin Pharmacol Ther: 2012; 92 158 169
56. Rosenstock J. Cefalu W. T. Lapuerta P. Zambrowicz B. Ogbaa I. Banks P. Sands A. Greater dose-ranging effects on A1C levels than on glucosuria with LX4211, a dual inhibitor of SGLT1 and SGLT2, in patients with type 2 diabetes on metformin monotherapy. Diabetes Care: 2015; 38 431 438
57. Sands A. T. Zambrowicz B. P. Rosenstock J. Lapuerta P. Bode B. W. Garg S. K. Buse J. B. Banks P. Heptulla R. Rendell M. Cefalu W. T. Strumph P. Sotagliflozin, a dual SGLT1 and SGLT2 inhibitor, as adjunct therapy to insulin in type 1 diabetes. Diabetes Care: 2015; 38 1181 1188
58. Gosch C. Halbwirth H. Stich K. Phloridzin: biosynthesis, distribution and physiological relevance in plants. Phytochem: 2010; 71 838 843
59. Hilt P. Schieber A. Yildirim C. Arnold G. Klaiber I. Conrad J. Carle R. Detection of phloridzin in strawberries (Fragaria x ananassa Duch.) by HPLC-PDA-MS/MS and NMR spectroscopy. J Agric Food Chem: 2003; 51 2896 2899
60. Hvattum E. Determination of phenolic compounds in rose hip (Rosa canina) using liquid chromatography coupled to electrospray ionization tandem mass spectrometry and diode-array detection. Rapid Commun Mass Spectrom: 2002; 16 655 662
61. Gosch C. Halbwirth H. Schneider B. Hölscher D. Stich K. Cloning and heterologous expression of glycosyltransferases from Malus x domestica and Pyrus communis, which convert phloretin to phloretin 2′-O-glucoside (phloridzin). Plant Sci: 2010; 178 299 306
62. Schulze C. Bangert A. Kottra G. Geillinger K. E. Schwanck B. Vollert H. Blaschek W. Daniel H. Inhibition of the intestinal sodium-coupled glucose transporter 1 (SGLT1) by extracts and polyphenols from apple reduces postprandial blood glucose levels in mice and humans. Mol Nutr Food Res: 2014; 57 1795 1808
63. Day A. J. Gee J. M. DuPont M. S. Johnson I. T. Williamson G. Absorption of quercetin-3-glucoside and quercetin-4-glucoside in the rat small intestine: the role of lactase phlorizin hydrolase and the sodium-dependent glucose transporter. Biochem Pharmacol: 2003; 65 1199 1206
64. Day A. J. Canada F. J. Diaz J. C. Kroon P. A. McLauchlan R. Faulds C. B. Plumb G. W. Morgan M. R. Williamson G. Dietary flavonoid and isoflavone glycosides are hydrolysed by the lactase site of lactase phlorizin hydrolase. FEBS Lett: 2000; 468 166 170
65. Schwank B. Behrendt M. Naim H. Y. Blaschek W. Deglycosylation of individual flavonoids and flavonoid containing plant extracts by purified human intestinal lactase-phlorizin hydrolase (LPH). Planta Med: 2011; 77 PA22
66. Kwon O. Eck P. Chen S. Corpe C. P. Lee J. Kruhlak M. Levine M. Inhibition of the intestinal glucose transporter GLUT2 by flavonoids. FASEB J: 2007; 21 366 377
67. Johnston K. L. Clifford M. N. Morgan L. M. Possible role for apple juice phenolic compounds in the acute modification of glucose tolerance and gastrointestinal hormone secretion in humans. J Sci Food Agric: 2002; 82 1800 1805
68. Shirosaki M. Koyama T. Yazawa K. Apple leaf extract as a potential candidate for suppressing postprandial elevation of the blood glucose level. J Nutr Sci Vitaminol: 2012; 58 63 67
69. Powell D. R. Smith M. Greer J. Harris A. LX4211 increases serum glucagon-like peptide 1 and peptide YY levels by reducing sodium/glucose cotransporter 1 (SGLT1)-mediated absorption of intestinal glucose. J Pharmacol Exp Ther: 2013; 345 250 259
70. Makarova E. Gornas P. Konrade I. Tirzite D. Cirule H. Pugajeva I. Seglina D. Dambrova M. Acute anti-hyperglycaemic effects of an unripe apple preparation containing phlorizin im healthy volunteers: a preliminary study. J Sci Food Agric: 2015; 95 560 568
71. + -glucose cotransporter (SGLT) inhibitory flavonoids from the roots of Sophora flavescens. Bioorg Med Chem: 2007; 15 3445 3449
72. Yang J. Yang X. Wang C. Lin Q. Mei Z. Zhao P. Sodium-glucose-linked transporter 2 inhibitors from Sophora flavescens. Med Chem Res: 2015; 24 1265 1271
73. Goto T. Horita M. Nagai H. Nagatomo S. Nishida N. Matsuura Y. Nagaoka S. Tirliroside, a glycosidic flavonoid, inhibits carbohydrate digestion and glucose absorption in the gastrointestinal tract. Mol Nutr Food Res: 2012; 56 435 445
74. Manach C. Williamson G. Morand C. Scalbert A. Remesy C. Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am J Clin Nutr: 2005; 81 230S 242S
75. Walgren R. A. Lin J. T. Kinne R. K. Walle T. Cellular uptake of dietary flavonoid quercetin 4′- β -glucoside by sodium-dependent glucose transporter SGLT1. J Pharmacol Exp Ther: 2000; 294 837 843
76. Wolffram S. Blöck M. Ader P. Quercetin-3-glucoside is transported by the glucose carrier SGLT1 across the brush border membrane of rat small intestine. J Nutr: 2002; 132 630 635
77. + /glucose transporter when expressed in Xenopus laevis oocytes, but effectively inhibit electrogenic glucose uptake. J Pharmacol Exp Ther: 2007; 322 829 835
78. Ader P. Blöck M. Pietzsch S. Wolffram S. Interaction of quercetin glucosides with the intestinal sodium/glucose co-transporter (SGLT-1). Cancer Lett: 2001; 162 175 180
79. Cermak R. Landgraf S. Wolffram S. Quercetin glucosides inhibit glucose uptake into brush-border-membrane vesicles of porcine jejunum. Br J Nutr: 2004; 91 849 855
80. Schulze C. Bangert A. Schwanck B. Vollert H. Blaschek W. Daniel H. Extracts and flavonoids from onion inhibit the intestinal sodium-coupled glucose transporter 1 (SGLT1) in vitro but show no anti-hyperglycaemic effects in vivo in normoglycaemic mice and human volunteers. J Funct Foods: 2015; 18 117 128
81. Snoussi C. Ducroc R. Hamdaoui M. H. Dhaouadi K. Abaidi H. Cluzeaud F. Nazaret C. Le Gall M. Bado A. Green tea decoction improves glucose tolerance and reduces weight gain of rats fed normal and high-fat diet. J Nutr Biochem: 2014; 25 557 564
82. Arai H. Hirasawa Y. Rahman A. Kusumawati I. Zaini N. C. Sato S. Aoyama C. Takeo J. Morita H. Alstiphyllanines E-H, picraline and ajmaline-type alkaloids from Alstonia macrophylla inhibiting sodium glucose cotransporter. Bioorg Med Chem: 2010; 18 2152 2158