Emerging role of thiamine therapy for prevention and treatment of early-stage diabetic nephropathy
Rabbani, Naila and Thornalley, Paul J.. (2011) Emerging role of thiamine therapy for prevention and treatment of early-stage diabetic nephropathy. Diabetes, Obesity and Metabolism, Volume 13 (Number 7). pp. 577-583. ISSN 1462-8902Full text not available from this repository.
Official URL: http://dx.doi.org/10.1111/j.1463-1326.2011.01384.x
Thiamine supplementation may prevent and reverse early-stage diabetic nephropathy. This probably occurs by correcting diabetes-linked increased clearance of thiamine, maintaining activity and expression of thiamine pyrophosphate-dependent enzymes that help counter the adverse effects of high glucose concentrations-particularly transketolase. Evidence from experimental and clinical studies suggests that metabolism and clearance of thiamine is disturbed in diabetes leading to tissue-specific thiamine deficiency in the kidney and other sites of development of vascular complications. Thiamine supplementation prevented the development of early-stage nephropathy in diabetic rats and reversed increased urinary albumin excretion in patients with type 2 diabetes and microalbuminuria in two recent clinical trials. The thiamine monophosphate prodrug, Benfotiamine, whilst preventing early-stage development of diabetic nephropathy experimentally, has failed to produce similar clinical effect. The probable explanations for this are discussed. Further definitive trials for prevention of progression of early-stage diabetic nephropathy by thiamine are now required.
|Item Type:||Journal Article|
|Subjects:||R Medicine > RC Internal medicine
R Medicine > RM Therapeutics. Pharmacology
|Divisions:||Faculty of Medicine > Warwick Medical School > Metabolic and Vascular Health
Faculty of Medicine > Warwick Medical School
|Library of Congress Subject Headings (LCSH):||Vitamin B1 -- Therapeutic use, Vitamin therapy, Diabetic nephropathies -- Treatment, Diabetic nephropathies -- Prevention|
|Journal or Publication Title:||Diabetes, Obesity and Metabolism|
|Page Range:||pp. 577-583|
|Access rights to Published version:||Restricted or Subscription Access|
|References:||1. Nielsen SE, Sugaya T, Hovind P, Baba T, Parving HH, Rossing P. Urinary liver-type fatty acid-binding protein predicts progression to nephropathy in type 1 diabetic patients. Diabetes Care 2010; 33: 1320–1324. 2. Williams ME. Diabetic CKD/ESRD 2010: a progress report? Semin Dial 2010; 23: 129–133. 3. American Diabetes Association. Standards of medical care in diabetes— 2009. Diabetes Care 2009; 32: S13–61. 4. Bergmann AK, Sahai I, Falcone JF et al. Thiamine-responsive megaloblastic anemia: identification of novel compound heterozygotes and mutation update. J Pediatr 2009; 155: 888–892. 5. Fleming JC, Tartaglini E, Steinkamp MP, Schorderet DF, Cohen N, Neufeld EJ. The gene mutated in thiamine-responsive anaemia with diabetes and deafness (TRMA) encodes a functional thiamine transporter. Nat Genet 1999; 22: 305–308. 6. Labay V, Raz T, Baron D et al. Mutations in SLC19A2 cause thiamineresponsive megaloblastic anaemia associated with diabetes mellitus and deafness. Nat Genet 1999; 22: 300–304. 7. Diaz GA, Banikazemi M, Oishi K, Desnick RJ, Gelb BD. Mutations in a new gene encoding a thiamine transporter cause thiamine-responsive megaloblastic anaemia syndrome. Nat Genet 1999; 22: 309–312. 8. Valerio G, Franzese A, Poggi V, Tenore A. Long-term follow-up of diabetes in two patients with thiamine-responsive megaloblastic anemia syndrome. Diabetes Care 1998; 21: 38–41. 9. Rajgopal A, Edmondnson A, Goldman ID, Zhao RB. SLC19A3 encodes a second thiamine transporter ThTr2. Biochim Biophys Acta Mol Basis Dis 2001; 1537: 175–178. 10. Matherly LH. Molecular and cellular biology of the human reduced folate carrier. Prog Nucleic Acid Res Mol Biol 2001; 67: 131–162. 11. Zhao R, Gao F, Goldman ID. Reduced folate carrier transports thiamine monophosphate: an alternative route for thiamine delivery into mammalian cells. Am J Physiol Cell Physiol 2002; 282: C1512–1517. 12. Zhao RB, Gao F, Wang YH, Diaz GA, Gelb BD, Goldman ID. Impact of the reduced folate carrier on the accumulation of active thiamin metabolites in murine leukemia cells. J Biol Chem 2001; 276: 1114–1118. 13. Lindhurst MJ, Fiermonte G, Song S et al. Knockout of Slc25a19 causes mitochondrial thiamine pyrophosphate depletion, embryonic lethality, CNS malformations, and anemia. PNAS 2006; 103: 15927–15932. 14. Kang J, Samuels DC. The evidence that the DNC (SLC25A19) is not the mitochondrial deoxyribonucleotide carrier. Mitochondrion 2008; 8: 103–108. 15. Said HM, Balamurugan K, Subramanian VS, Marchant JS. Expression and functional contribution of hTHTR-2 in thiamin absorption in human intestine. Am J Physiol Gastrointest Liver Physiol 2004; 286: G491–498. 16. Dutta B, Huang W, Molero M et al. Cloning of the human thiamine transporter, a member of the folate transporter family. J Biol Chem 1999; 274: 31925–31929. 17. Reidling JC, Subramanian VS, Dudeja PK, Said HM. Expression and promoter analysis of SLC19A2 in the human intestine. Biochim Biophys Acta 2002; 1561: 180–187. 18. Eudy JD, Spiegelstein O, Barber RC, Wlodarczyk BJ, Talbot J, Finnell RH. Identification and characterization of the human and mouse SLC19A3 gene: a novel member of the reduced folate family of micronutrient transporter genes. Mol Genet Metab 2000; 71: 581–590. 19. Dolce V, Fiermonte G, Runswick MJ, Palmieri F, Walker JE. The human mitochondrial deoxynucleotide carrier and its role in the toxicity of nucleoside antivirals. Proc Natl Acad Sci USA 2001; 98: 2284–2288. 20. Gastaldi G, Coya E, Verri A, Laforenza U, Faelli A, Rindi G. Transport of thiamin in rat renal brush border membrane vesicles. Kidney Int 2002; 57: 2043–2054. 21. Trippett TM, Garcia S, Manova K et al. Localization of a human reduced folate carrier protein in the mitochondrial as well as the cell membrane of leukemia cells. Cancer Res 2001; 61: 1941–1947. 22. Zhao R, Gao F, Wang Y, Diaz GA, Gelb BD, Goldman ID. Impact of the reduced folate carrier on the accumulation of active thiamin metabolites in murine leukemia cells. J Biol Chem 2001; 276: 1114–1118. 23. Babaei-Jadidi R, Karachalias N, Kupich C, Ahmed N, Thornalley PJ. High dose thiamine therapy counters dyslipidaemia in streptozotocin-induced diabetic rats. Diabetologia 2004; 47: 2235–2246. 24. Chin E, Zhou J, Bondy C. Anatomical and developmental patterns of facilitative glucose transporter gene-expression in the rat kidney. J Clin Invest 1993; 91: 1810–1815. 25. Tallaksen CME, Bohmer T, Karlsen J, Bell H. Determination of thiamin and its phosphate esters in human blood, plasma, and urine. Vitam Coenzymes 1997; 279(Pt I): 67–74. 26. Morshed KM, Ross DM, McMartin KE. Folate transport proteins mediate the bidirectional transport of 5-methyltetrahydrofolate in cultured human proximal tubule cells. J Nutr 1997; 127: 1137–1147. 27. Rindi G, Laforenza U. Thiamine intestinal transport and related issues: recent aspects. PSEBM 2000; 224: 246–255. 28. Laforenza U, Patrini C, Alvisi C, Faelli A, Licandro A, Rindi G. Thiamine uptake in human intestinal biopsy specimens, including observations from a patient with acute thiamine deficiency. Am J Clin Nutr 1997; 66: 320–326. 29. European Food Safety Authority. Scientific opinion of the panel on food additives and nutrient sources added to food (ANS) on a request from the Commission on benfotiamine, thiamine monophosphate chloride and thiamine pyrophosphate chloride, as sources of vitamin B1. EFSA J 2008; 864: 1–31. 30. Finglas PM. Thiamin. Int J Vitam Nutr Res 1993; 63: 270–274. 31. Tasevska N, Runswick SA, McTaggart A, Bingham SA. Twenty-four-hour urinary thiamine as a biomarker for the assessment of thiamine intake. Eur J Clin Nutr 2007; 62: 1139–1147. 32. Patrini C, Laforenza U, Gastaldi G, Verri A, Ferrari G, Rindi G. Effects of insulin on thiamine intestinal transport in rat everted jejunal sacs. J Physiol (Lond) 1996; 493: 100S–101S. 33. Thornalley PJ, Babaei-Jadidi R, Al Ali H et al. High prevalence of low plasma thiamine concentration in diabetes linked to marker of vascular disease. Diabetologia 2007; 50: 2164–2170. 34. Rabbani N, Shahzad Alam S, Riaz S et al. High dose thiamine therapy for patients with type 2 diabetes and microalbuminuria: a pilot randomised, double-blind, placebo-controlled study. Diabetologia 2009; 52: 208–212. 35. AntonySunil A, Babaei-Jadidi R, Rabbani N et al. Increased thiamine transporter contents of red blood cells and peripheral blood mononuclear leukocytes in type 1 and type 2 diabetic patients. Diabetes 2007; 56: A609. 36. Larkin JR, Thornalley PJ. High glucose causes a decrease in expression of thiamine transporters in human proximal tubule epithelial cells in vitro. Diabetologia 2008; 51: 219. 37. Babaei-Jadidi R, Karachalias N, Ahmed N, Battah S, Thornalley PJ. Prevention of incipient diabetic nephropathy by high dose thiamine and Benfotiamine. Diabetes 2003; 52: 2110–2120. 38. Patrini C, Griziotti A, Ricciardi L. Obese individuals as thiamin storers. Int J Obes 2004; 28: 920–924. 39. Weber W, Kewitz H. Determination of thiamine in human plasma and its pharmacokinetics. Eur J Clin Pharmacol 1985; 28: 213–219. 40. Ariaey-Nejad MR, Balaghi M, Baker EM, Sauberlich HE. Thiamin metabolism in man. Am J Clin Nutr 1970; 23: 764–778. 41. Weber W, Nitz M, Looby M. Nonlinear kinetics of the thiamine cation in humans—saturation of nonrenal clearance and tubular reabsorption. J Pharmacokinet Biopharm 1990; 18: 501–523. 42. Bellazzi R, Guglielmann R, Ironi L, Patrini C A. Hybrid input-output approach to model metabolic systems: an application to intracellular thiamine kinetics. J Biomed Inform 2001; 34: 221–248. 43. Perkins BA, Ficociello LH, Ostrander BE et al. Microalbuminuria and the risk for early progressive renal function decline in type 1 diabetes. J Am Soc Nephrol 2007; 18: 1353–1361. 44. AntonySunil A, Perkins B, Krolewski A, Rabbani N, Thornalley PJ. Thiamine status and risk of early renal function decline in type 1 diabetic patients. Diabetologia 2008; 51: S98. 45. Xue M, Qian Q, Adaikalakoteswari A, Rabbani N, Babaei-Jadidi R, Thornalley PJ. Activation of NF-E2-related factor-2 reverses biochemical dysfunction of endothelial cells induced by hyperglycemia linked to vascular disease. Diabetes 2008; 57: 2809–2817. 46. Cheng JZ, Yang YS, Singh SP et al. Two distinct 4-hydroxynonenal metabolizing glutathione S-transferase isozymes are differentially expressed in human tissues. Biochem Biophys Res Commun 2001; 282: 1268–1274. 47. Thornalley PJ, Qian Q, Rabbani N. Prevention of dicarbonyl stress induced by hyperglycaemia in microvascular endoethelial cells by sulforaphane. Diabetologia 2008; 51: 1301. 48. Hammes H-P, Du X, Edelstein D et al. Benfotiamine blocks three major pathways of hyperglycemic damage and prevents experimental diabetic retinopathy. Nat Med 2003; 9: 294–299.49. Karachalias N, Babaei-Jadidi R, Rabbani N, Thornalley P. Increased protein damage in renal glomeruli, retina, nerve, plasma and urine and its prevention by thiamine and benfotiamine therapy in a rat model of diabetes. Diabetologia 2010; 53: 1506–1516. 50. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001; 414: 813–820. 51. Brady JA, Rock CL, Horneffer MR. Thiamin status, diuretic medications, and the management of congestive heart failure. J Am Diet Assoc 1995; 95: 541–544. 52. Soh Y, Song BJ, Jeng JJ, Kallarakal AT. Critical role of Arg(433) in rat transketolase activity as probed by site-directed mutagenesis. Biochem J 1998; 333: 367–372. 53. Lapsys NM, Layfield R, Baker E et al. Chromosomal location of the human transketolase gene. Cytogenet Cell Genet 1992; 61: 274–275. 54. Freedman BI, Bowden DW, Rich SS et al. Genome-wide linkage scans for renal function and albuminuria in type 2 diabetes mellitus: the Diabetes Heart Study. Diabet Med 2008; 25: 268–276. 55. Pacal L, Tomandl J, Tanhauserova V et al. Thiamine levels and transketolase genetic variants as modifiers of progression of diabetic nephropathy. Diabetologia 2009; 52: 1079. 56. Balakumar P, Chakkarwar VA, Singh M. Ameliorative effect of combination of benfotiamine and fenofibrate in diabetes-induced vascular endothelial dysfunction and nephropathy in the rat. Mol Cell. Biochem 2009; 320: 149–162. 57. Rabbani N, Alam S, Riaz S et al. Thiamine in diabetic nephropathy: a novel treatment modality? Reply to Alkhalaf A, Kleefstra N, Groenier KH et al. [letter]. Diabetologia 2009; 52: 1214–1216. 58. Araki Si, Haneda M, Koya D et al. Reduction in microalbuminuria as an integrated indicator for renal and cardiovascular risk reduction in patients with type 2 diabetes. Diabetes 2007; 56: 1727–1730. 59. Sihag B, Meena B, Agrawal R, Meel J, Sirohi P, Bishnoi P. High dose thiamine therapy for patients with type 2 diabetes andmicroalbuminuria: a randomised, double-blind placebo-controlled study. Diabetes Obes Metab 2010; 12: 87–88. 60. Alkhalaf A, Klooster A, van Oeveren W et al. A double-blind, randomized, placebo-controlled clinical trial on benfotiamine treatment in patients with diabetic nephropathy. Diabetes Care 2010; 33: 1598–1601. 61. Satchell S, Tooke J. What is the mechanism of microalbuminuria in diabetes: a role for the glomerular endothelium? Diabetologia 2008; 51: 714–725. 62. Kim D, Nam H. The effect of benfotiamine on endothelial function in patients with type 2 diabetes mellitus. Diabetologia 2006; 49: 1202. 63. Du X, Edelstein D, Brownlee M. Oral benfotiamine plus α-lipoic acid normalises complication-causing pathways in type 1 diabetes. Diabetologia 2008; 51: 1930–1932. 64. Ascher E, Gade PV, Hingorani A et al. Thiamine reverses hyperglycemiainduced dysfunction in cultured endothelial cells. Surgery 2001; 130: 851–858. 65. Berrone E, Beltramo E, Solimine C, Ape AU, Porta M. Regulation of intracellular glucose and polyol pathway by thiamine and benfotiamine in vascular cells cultured in high glucose. J Biol Chem 2006; 281: 9307–9313. 66. LaSelva M, Beltramo E, Pagnozzi F et al. Thiamine corrects delayed replication and decreases production of lactate and advanced glycation endproducts in bovine retinal and human umbilical vein endothelial cells cultured under high glucose conditions. Diabetologia 1997; 39: 1263–1268. 67. Beltramo E, Berrone E, Buttiglieri S, Porta M. Thiamine and benfotiamine prevent increased apoptosis in endothelial cells and pericytes cultured in high glucose. Diabetes Metab Res Rev 2004; 20: 330–336. 68. Arora S, Lidor A, Abularrage CJ et al. Thiamine (vitamin B-1) improves endothelium-dependent vasodilatation in the presence of hyperglycemia. Ann Vasc Surg 2006; 20: 653–658. 69. Potter DR, Jiang J, Damiano ER. The recovery time course of the endothelial cell glycocalyx in vivo and its implications in vitr o. Circ Res 2009; 104: 1318–1325. 70. van Balkom BWM, Savelkoul PJM, Markovich D et al. The role of putative phosphorylation sites in the targeting and shuttling of the aquaporin-2 water channel. J Biol Chem 2002; 277: 41473–41479. 71. Zelenina M, Zelenin S, Bondar AA, Brismar H, Aperia A. Water permeability of aquaporin-4 is decreased by protein kinase C and dopamine. Am J Physiol Renal Physiol 2002; 283: F309–318. 72. Shindo H, Okamoto K, Totsu J. Transport of organic compounds through biological membranes. I. Accumulative uptake of S-benzoylthiamine by human erythrocytes. Chem Pharm Bull 1967; 15: 295–302. 73. Volvert ML, Seyen S, Piette M et al. Benfotiamine, a synthetic S-acyl thiamine derivative, has different mechanisms of action and a different pharmacological profile than lipid-soluble thiamine disulfide derivatives. BMC Pharmacol 2008; 8: 10. 74. Ziems M, Netzel M, Bitsch I. Biokinetic of S-benzoylthiamine-Omonophosphate in human. Vitam Addit Hum Anim Nutr 1997;194–199. 75. Thornalley PJ, Babaei-Jadidi R. Prevention of microvascular complications of diabetes by high dose S-benzoylthiamine monophosphate (benfotiamine): mechanism of thiamine delivery into cells. Diabetologia 2005; 48: A377. 76. Wakabayashi Y. Purification and properties of porcine thiamine pyrophosphokinase. Vitamins 1978; 52: 223–236. 77. Thornalley PJ. The potential role of thiamine (vitamin B1) in diabetic complications. Curr Diabetes Res 2005; 1: 287–298. 78. Heinze T, Weber W. Determination of thiamine (vitamin B1) in maternal blood during normal pregnancies and pregnancies with intrauterine growth retardation. Z Ernahrungswiss 1990; 29: 39–46. 79. Kohda Y, Shirakawa H, Yamane K et al. Prevention of incipient diabetic cardiomyopathy by high-dose thiamine. J Toxicol Sci 2008; 33: 459–472. 80. Ceylan-Isik AF, Wu S, Li Q, Li SY, Ren J. High-dose benfotiamine rescues cardiomyocyte contractile dysfunction in streptozotocin-induced diabetes mellitus. J Appl Physiol 2006; 100: 150–156. 81. Karachalias N, Babaei-Jadidi R, Rabbani N, Thornalley PJ. Prevention of decline in glycaemic control in streptozotocin-induced diabetic rats by thiamine but not by benfotiamine. Diabetic Med 2010; 27(Suppl. 1): 74. 82. Bakker SJL, Hoogeveen EK, Nijpels G et al. The association of dietary fibres with glucose is partly explained by concomitant intake of thiamine: the Hoorn study. Diabetologia 1998; 41: 1168–1175 [abstract].|
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