Carnosine attenuates the development of both type 2 diabetes and diabetic nephropathy in BTBR ob/ob mice

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Albrecht, Thomas ^a   Schilperoort, Maaike ^b   Zhang, Shiqi ^a   Braun, Jana D ^a   Qiu, Jiedong ^a   Rodriguez, Angelica ^a   Pastene, Diego O ^a   Krämer, Bernhard K ^a   Köppel, Hannes ^a   Baelde, Hans ^b   De Heer, Emile ^b   Altomare, Alessandra Anna ^c   Regazzoni, Luca ^c   Denisi, Alessandra ^c   Aldini, Giancarlo ^c   Van Den Born, Jacob ^d   Yard, Benito A ^a   Hauske, Sibylle J ^a  

^a MEDICAL FACULTY MANNHEIM HEIDELBERG UNIVERSITY   (Germany)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF MILAN   (Italy)

^d UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOACYL-HISTIDINE DIPEPTIDASE; ANTIDIABETIC AGENT; C PEPTIDE; CARNOSINE; DIPEPTIDASE; GLYCOSYLATED HEMOGLOBIN; INSULIN;

ALBUMINURIA; ANIMAL; BLOOD; DIABETIC NEPHROPATHY; DIET THERAPY; DISEASE MODEL; DRUG EFFECT; GENE EXPRESSION; GENETICS; GLOMERULUS; GLUCOSE BLOOD LEVEL; HUMAN; MALE; MESANGIUM; METABOLISM; MOUSE; MOUSE MUTANT; NON INSULIN DEPENDENT DIABETES MELLITUS; ORAL DRUG ADMINISTRATION; ORGAN SIZE; PATHOLOGY;

ADMINISTRATION, ORAL; ALBUMINURIA; ANIMALS; BLOOD GLUCOSE; C-PEPTIDE; CARNOSINE; DIABETES MELLITUS, TYPE 2; DIABETIC NEPHROPATHIES; DIPEPTIDASES; DISEASE MODELS, ANIMAL; GENE EXPRESSION; GLOMERULAR MESANGIUM; GLYCATED HEMOGLOBIN A; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; KIDNEY GLOMERULUS; MALE; MICE; MICE, OBESE; ORGAN SIZE;

EID: 85014891926     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep44492     Document Type: Article

References (57)

1. Gross, J. L.et al. Diabetic nephropathy: diagnosis, prevention, and treatment. Diabetes Care 28, 164-176 (2005).
2. Bergrem, H. & Leivestad, T. Diabetic nephropathy and end-stage renal failure: the Norwegian story. Adv Ren Replace Ther 8, 4-12 (2001).
3. Gaede, P., Lund-Andersen, H., Parving, H. H. & Pedersen, O. Effect of a multifactorial intervention on mortality in type 2 diabetes. N Engl J Med 358, 580-591 (2008).
4. Krolewski, M., Eggers, P. W. & Warram, J. H. Magnitude of end-stage renal disease in IDDM: a 35 year follow-up study. Kidney Int 50, 2041-2046 (1996).
5. Schena, F. P. & Gesualdo, L. Pathogenetic mechanisms of diabetic nephropathy. J Am Soc Nephrol 16, S30-33 (2005).
6. Janssen, B.et al. Carnosine as a protective factor in diabetic nephropathy: association with a leucine repeat of the carnosinase gene CNDP1. Diabetes 54, 2320-2327 (2005).
7. Riedl, E.et al. A CTG polymorphism in the CNDP1 gene determines the secretion of serum carnosinase in Cos-7 transfected cells. Diabetes 56, 2410-2413 (2007).
8. Hipkiss, A. R.et al. Pluripotent protective effects of carnosine, a naturally occurring dipeptide. Ann N Y Acad Sci 854, 37-53 (1998).
9. Peters, V.et al. Carnosine treatment in combination with ACE inhibition in diabetic rats. Regul Pept 194-195, 36-40 (2014).
10. Riedl, E.et al. Carnosine prevents apoptosis of glomerular cells and podocyte loss in STZ diabetic rats. Cell Physiol Biochem 28, 279-288 (2011).
11. Hudkins, K. L.et al. BTBR Ob/Ob mutant mice model progressive diabetic nephropathy. J Am Soc Nephrol 21, 1533-1542 (2010).
12. Pichaiwong, W.et al. Reversibility of structural and functional damage in a model of advanced diabetic nephropathy. J Am Soc Nephrol 24, 1088-1102 (2013).
13. Clee, S. M., Nadler, S. T. & Attie, A. D. Genetic and genomic studies of the BTBR ob/ob mouse model of type 2 diabetes. Am J Ther 12, 491-498 (2005).
14. Flowers, J. B.et al. Abdominal obesity in BTBR male mice is associated with peripheral but not hepatic insulin resistance. Am J Physiol Endocrinol Metab 292, E936-945 (2007).
15. Drel, V. R.et al. The leptin-deficient (ob/ob) mouse: a new animal model of peripheral neuropathy of type 2 diabetes and obesity. Diabetes 55, 3335-3343 (2006).
16. Gembardt, F.et al. The SGLT2 inhibitor empagliflozin ameliorates early features of diabetic nephropathy in BTBR ob/ob type 2 diabetic mice with and without hypertension. Am J Physiol Renal Physiol 307, 317-325 (2014).
17. Sullivan, T.et al. In DIABETOLOGIA. S19-S19 (Springer 233 Spring St, New York, Ny 10013 USA).
18. Regazzoni, L.et al. A carnosine intervention study in overweight human volunteers: bioavailability and reactive carbonyl species sequestering effect. Scientific reports 6, 27224 (2016).
19. Lee, Y. T., Hsu, C. C., Lin, M. H., Liu, K. S. & Yin, M. C. Histidine and carnosine delay diabetic deterioration in mice and protect human low density lipoprotein against oxidation and glycation. Eur J Pharmacol 513, 145-150 (2005).
20. Soliman, K., Mohamed, A. & Mewally, N. Attenuation of some metabolic deteriorations induced by diabetes mellitus using carnosine. Journal of Applied Sciences 7, 2252-2260 (2007).
21. Sauerhofer, S.et al. L-carnosine, a substrate of carnosinase-1, influences glucose metabolism. Diabetes 56, 2425-2432 (2007).
22. Jappar, D., Hu, Y. & Smith, D. E. Effect of dose escalation on the in vivo oral absorption and disposition of glycylsarcosine in wildtype and Pept1 knockout mice. Drug Metab Dispos 39, 2250-2257 (2011).
23. Boldyrev, A. A., Aldini, G. & Derave, W. Physiology and pathophysiology of carnosine. Physiol Rev 93, 1803-1845 (2013).
24. Sjoholm, A. Histaminergic regulation of pancreatic beta-cell replication and insulin secretion. Biochem Biophys Res Commun 214, 224-229 (1995).
25. McClenaghan, N. H., Barnett, C. R., O'Harte, F. P. & Flatt, P. R. Mechanisms of amino acid-induced insulin secretion from the glucose-responsive BRIN-BD11 pancreatic B-cell line. J Endocrinol 151, 349-357 (1996).
26. Dunne, M. J., Yule, D. I., Gallacher, D. V. & Petersen, O. H. Effects of alanine on insulin-secreting cells: patch-clamp and single cell intracellular Ca2+ measurements. Biochim Biophys Acta 1055, 157-164 (1990).
27. L'Amoreaux, W. J.et al. Taurine regulates insulin release from pancreatic beta cell lines. J Biomed Sci 17 Suppl 1, S11 (2010).
28. Jessen, H. Taurine and beta-alanine transport in an established human kidney cell line derived from the proximal tubule. Biochim Biophys Acta 1194, 44-52 (1994).
29. Di Gialleonardo, V.et al. 11C-hydroxytryptophan uptake and metabolism in endocrine and exocrine pancreas. J Nucl Med 53, 1755-1763 (2012).
30. Otani, H., Okumura, A., Nagai, K. & Okumura, N. Colocalization of a carnosine-splitting enzyme, tissue carnosinase (CN2)/ cytosolic non-specific dipeptidase 2 (CNDP2), with histidine decarboxylase in the tuberomammillary nucleus of the hypothalamus. Neurosci Lett 445, 166-169 (2008).
31. Nagai, K.et al. Possible role of L-carnosine in the regulation of blood glucose through controlling autonomic nerves. Exp Biol Med (Maywood) 228, 1138-1145 (2003).
32. Nagai, K.et al. Role of L-carnosine in the control of blood glucose, blood pressure, thermogenesis, and lipolysis by autonomic nerves in rats: involvement of the circadian clock and histamine. Amino Acids 43, 97-109 (2012).
33. Weil, E. J.et al. Podocyte detachment and reduced glomerular capillary endothelial fenestration promote kidney disease in type 2 diabetic nephropathy. Kidney Int. 82, 1010-1017 (2012).
34. Tobar, A.et al. Proximal tubular hypertrophy and enlarged glomerular and proximal tubular urinary space in obese subjects with proteinuria. PLoS One 8, e75547 (2013).
35. Sasson, A. N. & Cherney, D. Z. Renal hyperfiltration related to diabetes mellitus and obesity in human disease. World J Diabetes 3, 1-6 (2012).
36. Menini, S., Iacobini, C., Ricci, C., Blasetti Fantauzzi, C. & Pugliese, G. Protection from diabetes-induced atherosclerosis and renal disease by D-carnosine-octylester: effects of early vs late inhibition of advanced glycation end-products in Apoe-null mice. Diabetologia 58, 845-853 (2015).
37. Mason, R. M. & Wahab, N. A. Extracellular matrix metabolism in diabetic nephropathy. J Am Soc Nephrol 14, 1358-1373 (2003).
38. Bispo, V. S., de Arruda Campos, I. P., Di Mascio, P. & Medeiros, M. H. Structural Elucidation of a Carnosine-Acrolein Adduct and its Quantification in Human Urine Samples. Sci. Rep. 6, 19348 (2016).
39. Baba, S. P.et al. Role of aldose reductase in the metabolism and detoxification of carnosine-acrolein conjugates. J. Biol. Chem. 288, 28163-28179 (2013).
40. Carini, M., Aldini, G., Beretta, G., Arlandini, E. & Facino, R. M. Acrolein-sequestering ability of endogenous dipeptides: characterization of carnosine and homocarnosine/acrolein adducts by electrospray ionization tandem mass spectrometry. J. Mass Spectrom. 38, 996-1006 (2003).
41. Kehrer, J. P. & Biswal, S. S. The molecular effects of acrolein. Toxicol Sci 57, 6-15 (2000).
42. Suzuki, D. & Miyata, T. Carbonyl stress in the pathogenesis of diabetic nephropathy. Intern Med 38, 309-314 (1999).
43. Orioli, M., Aldini, G., Benfatto, M. C., Facino, R. M. & Carini, M. HNE Michael adducts to histidine and histidine-containing peptides as biomarkers of lipid-derived carbonyl stress in urines: LC-MS/MS profiling in Zucker obese rats. Anal. Chem. 79, 9174-9184 (2007).
44. Feroe, A. G., Attanasio, R. & Scinicariello, F. Acrolein metabolites, diabetes and insulin resistance. Environ. Res. 148, 1-6 (2016).
45. Koppel, H.et al. L-carnosine inhibits high-glucose-mediated matrix accumulation in human mesangial cells by interfering with TGF-beta production and signalling. Nephrology, dialysis, transplantation: official publication of the European Dialysis and Transplant Association - European Renal Association 26, 3852-3858 (2011).
46. Nagasawa, T., Yonekura, T., Nishizawa, N. & Kitts, D. D. In vitro and in vivo inhibition of muscle lipid and protein oxidation by carnosine. Molecular and cellular biochemistry 225, 29-34 (2001).
47. Rashid, I., van Reyk, D. M. & Davies, M. J. Carnosine and its constituents inhibit glycation of low-density lipoproteins that promotes foam cell formation in vitro. FEBS letters 581, 1067-1070 (2007).
48. Hipkiss, A. R. & Chana, H. Carnosine protects proteins against methylglyoxal-mediated modifications. Biochemical and biophysical research communications 248, 28-32 (1998).
49. Hyland, P., Duggan, O., Hipkiss, A., Barnett, C. & Barnett, Y. The effects of carnosine on oxidative DNA damage levels and in vitro lifespan in human peripheral blood derived CD4+ T cell clones. Mechanisms of ageing and development 121, 203-215 (2000).
50. Abbasoglu, L.et al. Beneficial effects of taurine and carnosine in experimental ischemia/reperfusion injury in testis. Pediatric surgery international 28, 1125-1131 (2012).
51. Kurata, H.et al. Renoprotective effects of l-carnosine on ischemia/reperfusion-induced renal injury in rats. The Journal of pharmacology and experimental therapeutics 319, 640-647 (2006).
52. Yay, A.et al. Antioxidant effect of carnosine treatment on renal oxidative stress in streptozotocin-induced diabetic rats. Biotechnic & histochemistry: official publication of the Biological Stain Commission 89, 552-557 (2014).
53. Everaert, I.et al. Low plasma carnosinase activity promotes carnosinemia after carnosine ingestion in humans. Am J Physiol Renal Physiol 302, F1537-1544 (2012).
54. Peters, V.et al. Intrinsic carnosine metabolism in the human kidney. Amino Acids, 1-10 (2015).
55. Lambers Heerspink, H. J.et al. Comparison of different measures of urinary protein excretion for prediction of renal events. J Am Soc Nephrol 21, 1355-1360 (2010).
56. Keller, B. O., Sui, J., Young, A. B. & Whittal, R. M. Interferences and contaminants encountered in modern mass spectrometry. Analytica chimica acta 627, 71-81 (2008).
57. Levin, J. R., Serlin, R. C. & Seaman, M. A. A controlled, powerful multiple-comparison strategy for several situations. Psychological Bulletin 115, 153-159 (1994).