Intrinsic carnosine metabolism in the human kidney

Amino Acids

Volumn 47, Issue 12, 2015, Pages 2541-2550

  Peters, Verena ^a   Klessens, Celine Q F ^b   Baelde, Hans J ^b   Singler, Benjamin ^a   Veraar, Kimberley A M ^b   Zutinic, Ana ^b   Drozak, Jakub ^c   Zschocke, Johannes ^d   Schmitt, Claus P ^a   De Heer, Emile ^b  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF WARSAW   (Poland)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

Anserine; Carnosinase (CNDP1); Carnosine; Diabetic nephropathy; Metabolism

Indexed keywords

ANSERINE; BETA ALANINE; CARNOSINASE 1; CARNOSINE; CARNOSINE SYNTHASE; MESSENGER RNA; PROTEIN; TAURINE TRANSPORTER; UNCLASSIFIED DRUG; CARNOSINE SYNTHETASE; CARRIER PROTEIN; CNDP1 PROTEIN, HUMAN; DIPEPTIDASE; MEMBRANE PROTEIN; PEPTIDE SYNTHASE;

ANIMAL CELL; ARTICLE; CARNS GENE; CELL COMPARTMENTALIZATION; CLINICAL ARTICLE; CNDP1 GENE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME LOCALIZATION; ENZYME SYNTHESIS; GENE; GENE EXPRESSION; GLOMERULOSA CELL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDROLYSIS; IN VITRO STUDY; KIDNEY CORTEX; KIDNEY EPITHELIUM; KIDNEY METABOLISM; KIDNEY TUBULE CELL; NEPHRON; NONHUMAN; PATHOGENESIS; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; DIABETIC NEUROPATHY; EPITHELIUM CELL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; KIDNEY; KIDNEY TUBULE; METABOLISM;

ANSERINE; CARNOSINE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DIABETIC NEUROPATHIES; DIPEPTIDASES; ENDOTHELIAL CELLS; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; HYDROLYSIS; IMMUNOHISTOCHEMISTRY; KIDNEY; KIDNEY TUBULES; MEMBRANE GLYCOPROTEINS; MEMBRANE TRANSPORT PROTEINS; NEPHRONS; PEPTIDE SYNTHASES; PODOCYTES; RNA, MESSENGER;

EID: 84946491275     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-015-2045-7     Document Type: Article

References (48)

1. Adelmann K, Frey D, Riedl E, Koeppel H, Pfister F, Peters V, Schmitt CP, Sternik P, Hofmann S, Zentgraf HW, Navis G, van den Born J, Bakker SJ, Kramer BK, Yard BA, Hauske SJ (2012) Different conformational forms of serum carnosinase detected by a newly developed sandwich ELISA for the measurements of carnosinase concentrations. Amino Acid 43:143-151. doi: 10.1007/s00726-012-1244-8
2. Aldini G, Facino RM, Beretta G, Carini M (2005) Carnosine and related dipeptides as quenchers of reactive carbonyl species: from structural studies to therapeutic perspectives. BioFactors 24:77-87
3. Alhamdani MS, Al-Azzawie HF, Abbas FK (2007) Decreased formation of advanced glycation end-products in peritoneal fluid by carnosine and related peptides. Perit Dial Int 27:86-89
4. Ansurudeen I, Sunkari VG, Grunler J, Peters V, Schmitt CP, Catrina SB, Brismar K, Forsberg EA (2012) Carnosine enhances diabetic wound healing in the db/db mouse model of type 2 diabetes. Amino Acid 43:127-134. doi: 10.1007/s00726-012-1269-z
5. Babizhayev MA, Lankin VZ, Savel'Yeva EL, Deyev AI, Yegorov YE (2013) Diabetes mellitus: novel insights, analysis and interpretation of pathophysiology and complications management with imidazole-containing peptidomimetic antioxidants. Recent Pat Drug Deliv Formul 7:216-256
6. Baek SH, Noh AR, Kim KA, Akram M, Shin YJ, Kim ES, Yu SW, Majid A, Bae ON (2014) Modulation of mitochondrial function and autophagy mediates carnosine neuroprotection against ischemic brain damage. Stroke 45:2438-2443. doi: 10.1161/STROKEAHA.114.005183
7. Baelde HJ, Eikmans M, Doran PP, Lappin DW, de Heer E, Bruijn JA (2004) Gene expression profiling in glomeruli from human kidneys with diabetic nephropathy. Am J Kidney Dis 43:636-650
8. Baelde HJ, Eikmans M, Lappin DW, Doran PP, Hohenadel D, Brinkkoetter PT, van der Woude FJ, Waldherr R, Rabelink TJ, de Heer E, Bruijn JA (2007) Reduction of VEGF-A and CTGF expression in diabetic nephropathy is associated with podocyte loss. Kidney Int 71:637-645. doi: 10.1038/sj.ki.5002101
9. Barski OA, Xie Z, Baba SP, Sithu SD, Agarwal A, Cai J, Bhatnagar A, Srivastava S (2013) Dietary carnosine prevents early atherosclerotic lesion formation in apolipoprotein E-null mice. Arterioscler Thromb Vasc Biol 33:1162-1170. doi: 10.1161/ATVBAHA.112.300572
10. Bex T, Chung W, Baguet A, Stegen S, Stautemas J, Achten E, Derave W (2014) Muscle carnosine loading by beta-alanine supplementation is more pronounced in trained vs. untrained muscles. J Appl Physiol 116:204-209. doi: 10.1152/japplphysiol.01033.2013
11. Boldyrev AA (1993) Does carnosine possess direct antioxidant activity? Int J Biochem 25:1101-1107
12. Boldyrev A, Bulygina E, Leinsoo T, Petrushanko I, Tsubone S, Abe H (2004) Protection of neuronal cells against reactive oxygen species by carnosine and related compounds. Comp Biochem Physiol B Biochem Mol Biol 137:81-88
13. Boldyrev AA, Aldini G, Derave W (2013) Physiology and pathophysiology of carnosine. Physiol Rev 93:1803-1845. doi: 10.1152/physrev.00039.2012
14. Budzen S, Rymaszewska J (2013) The biological role of carnosine and its possible applications in medicine. Adv Clin Exp Med Off Organ Wroc Med Uni 22:739-744
15. Chesney RW, Han X, Patters AB (2010) Taurine and the renal system. J Biomed Sci 17(Suppl 1):S4. doi: 10.1186/1423-0127-17-S1-S4
16. Daniel RL, Osbaldeston NJ, McCormack JG (1992) Activation by anserine and inhibition by carnosine of Ca(2+)-uptake by mammalian mitochondria. Biochem Soc Trans 20:131S
17. Drozak J, Veiga-da-Cunha M, Vertommen D, Stroobant V, Van Schaftingen E (2010) Molecular identification of carnosine synthase as ATP-grasp domain-containing protein 1 (ATPGD1). J Biol Chem 285:9346-9356. doi: 10.1074/jbc.M109.095505
18. Hipkiss AR, Brownson C, Carrier MJ (2001) Carnosine, the anti-ageing, anti-oxidant dipeptide, may react with protein carbonyl groups. Mech Ageing Dev 122:1431-1445
19. Hobart LJ, Seibel I, Yeargans GS, Seidler NW (2004) Anti-crosslinking properties of carnosine: significance of histidine. Life Sci 75:1379-1389. doi: 10.1016/j.lfs.2004.05.002
20. Hou WC, Chen HJ, Lin YH (2003) Antioxidant peptides with Angiotensin converting enzyme inhibitory activities and applications for Angiotensin converting enzyme purification. J Agric Food Chem 51:1706-1709. doi: 10.1021/jf0260242
21. Janssen B, Hohenadel D, Brinkkoetter P, Peters V, Rind N, Fischer C, Rychlik I, Cerna M, Romzova M, de Heer E, Baelde H, Bakker SJ, Zirie M, Rondeau E, Mathieson P, Saleem MA, Meyer J, Koppel H, Sauerhoefer S, Bartram CR, Nawroth P, Hammes HP, Yard BA, Zschocke J, van der Woude FJ (2005) Carnosine as a protective factor in diabetic nephropathy: association with a leucine repeat of the carnosinase gene CNDP1. Diabetes 54:2320-2327
22. Jessen H (1994) Taurine and beta-alanine transport in an established human kidney cell line derived from the proximal tubule. Biochim Biophys Acta 1194:44-52
23. Jessen H, Sheikh MI (1991) Renal transport of taurine in luminal membrane vesicles from rabbit proximal tubule. Biochim Biophys Acta 1064:189-198
24. Kohen R, Yamamoto Y, Cundy KC, Ames BN (1988) Antioxidant activity of carnosine, homocarnosine, and anserine present in muscle and brain. Proc Natl Acad Sci USA 85:3175-3179
25. Liu QR, Lopez-Corcuera B, Nelson H, Mandiyan S, Nelson N (1992) Cloning and expression of a cDNA encoding the transporter of taurine and beta-alanine in mouse brain. Proc Natl Acad Sci USA 89:12145-12149
26. Margolis FL, Grillo M (1984) Carnosine, homocarnosine and anserine in vertebrate retinas. Neurochem Int 6:207-209
27. Margolis FL, Grillo M, Hempstead J, Morgan JI (1987) Monoclonal antibodies to mammalian carnosine synthetase. J Neurochem 48:593-600
28. Mooyaart AL, van Valkengoed IG, Shaw PK, Peters V, Baelde HJ, Rabelink TJ, Bruijn JA, Stronks K, de Heer E (2009) Lower frequency of the 5/5 homozygous CNDP1 genotype in South Asian Surinamese. Diabetes Res Clin Pract 85:272-278. doi: 10.1016/j.diabres.2009.06.001
29. Mozdzan M, Szemraj J, Rysz J, Nowak D (2005) Antioxidant properties of carnosine re-evaluated with oxidizing systems involving iron and copper ions. Basic Clin Pharmacol Toxicol 96:352-360. doi: 10.1111/j.1742-7843.2005.pto-03.x
30. Nakagawa K, Ueno A, Nishikawa Y (2006) Interactions between carnosine and captopril on free radical scavenging activity and angiotensin-converting enzyme activity in vitro. Yakugaku Zasshi 126:37-42
31. Negre-Salvayre A, Coatrieux C, Ingueneau C, Salvayre R (2008) Advanced lipid peroxidation end products in oxidative damage to proteins. Potential role in diseases and therapeutic prospects for the inhibitors. Br J Pharmacol 153:6-20. doi: 10.1038/sj.bjp.0707395
32. Peters V, Kebbewar M, Jansen EW, Jakobs C, Riedl E, Koeppel H, Frey D, Adelmann K, Klingbeil K, Mack M, Hoffmann GF, Janssen B, Zschocke J, Yard BA (2010) Relevance of allosteric conformations and homocarnosine concentration on carnosinase activity. Amino Acid 38:1607-1615. doi: 10.1007/s00726-009-0367-z
33. Peters V, Jansen EE, Jakobs C, Riedl E, Janssen B, Yard BA, Wedel J, Hoffmann GF, Zschocke J, Gotthardt D, Fischer C, Koppel H (2011) Anserine inhibits carnosine degradation but in human serum carnosinase (CN1) is not correlated with histidine dipeptide concentration. Clin Chim Acta 412:263-267. doi: 10.1016/j.cca.2010.10.016
34. Peters V, Schmitt CP, Zschocke J, Gross ML, Brismar K, Forsberg E (2012) Carnosine treatment largely prevents alterations of renal carnosine metabolism in diabetic mice. Amino Acid 42:2411-2416. doi: 10.1007/s00726-011-1046-4
35. Peters V, Riedl E, Braunagel M, Hoger S, Hauske S, Pfister F, Zschocke J, Lanthaler B, Benck U, Hammes HP, Kramer BK, Schmitt CP, Yard BA, Koppel H (2014) Carnosine treatment in combination with ACE inhibition in diabetic rats. Regul Pept. doi: 10.1016/j.regpep.2014.09.005
36. Pfister F, Riedl E, Wang Q, vom Hagen F, Deinzer M, Harmsen MC, Molema G G, Yard B, Feng Y, Hammes HP (2011) Oral carnosine supplementation prevents vascular damage in experimental diabetic retinopathy. Cell Physiol Biochem 28:125-136. doi: 10.1159/000331721
37. Riedl E, Koeppel H, Pfister F, Peters V, Sauerhoefer S, Sternik P, Brinkkoetter P, Zentgraf H, Navis G, Henning RH, Van Den Born J, Bakker SJ, Janssen B, van der Woude FJ, Yard BA (2010) N-glycosylation of carnosinase influences protein secretion and enzyme activity: implications for hyperglycemia. Diabetes 59:1984-1990. doi: 10.2337/db09-0868
38. Riedl E, Pfister F, Braunagel M, Brinkkotter P, Sternik P, Deinzer M, Bakker SJ, Henning RH, van den Born J, Kramer BK, Navis G, Hammes HP, Yard B, Koeppel H (2011) Carnosine prevents apoptosis of glomerular cells and podocyte loss in STZ diabetic rats. Cell Physiol Biochem 28:279-288. doi: 10.1159/000331740
39. Sauerhofer S, Yuan G, Braun GS, Deinzer M, Neumaier M, Gretz N, Floege J, Kriz W, van der Woude F, Moeller MJ (2007) L-carnosine, a substrate of carnosinase-1, influences glucose metabolism. Diabetes 56:2425-2432. doi: 10.2337/db07-0177
40. Schönherr J (2002) Analysis of products of animal origin in feeds by determination of carnosine and related dipeptides by high-performance liquid chromatography. J Agric Food Chem 50:1945-1950
41. Tanida M, Shen J, Kubomura D, Nagai K (2010) Effects of anserine on the renal sympathetic nerve activity and blood pressure in urethane-anesthetized rats. Physiol Res 59:177-185
42. Teufel M, Roggentin P, Schauer R (1989) Properties of sialidase isolated from Actinomyces viscosus DSM 43798. Biol Chem Hoppe Seyler 370:435-443
43. Teufel M, Saudek V, Ledig JP, Bernhardt A, Boularand S, Carreau A, Cairns NJ, Carter C, Cowley DJ, Duverger D, Ganzhorn AJ, Guenet C, Heintzelmann B, Laucher V, Sauvage C, Smirnova T (2003) Sequence identification and characterization of human carnosinase and a closely related non-specific dipeptidase. J Biol Chem 278:6521-6531. doi: 10.1074/jbc.M209764200
44. Veiga-da-Cunha M, Chevalier N, Stroobant V, Vertommen D, Van Schaftingen E (2014) Metabolite proofreading in carnosine and homocarnosine synthesis: molecular identification of PM20D2 as beta-alanyl-lysine dipeptidase. J Biol Chem 289:19726-19736. doi: 10.1074/jbc.M114.576579
45. Vistoli G, Orioli M, Pedretti A, Regazzoni L, Canevotti R, Negrisoli G, Carini M, Aldini G (2009) Design, synthesis, and evaluation of carnosine derivatives as selective and efficient sequestering agents of cytotoxic reactive carbonyl species. Chem Med Chem 4:967-975. doi: 10.1002/cmdc.200800433
46. Weins A, Schwarz K, Faul C, Barisoni L, Linke WA, Mundel P (2001) Differentiation- and stress-dependent nuclear cytoplasmic redistribution of myopodin, a novel actin-bundling protein. J Cell Biol 155:393-404. doi: 10.1083/jcb.200012039
47. Yay A, Akkus D, Yapislar H, Balcioglu E, Sonmez M, Ozdamar S (2014) Antioxidant effect of carnosine treatment on renal oxidative stress in streptozotocin-induced diabetic rats. Biotech Histochem. doi: 10.3109/10520295.2014.913811
48. Zhang X, Song L, Cheng X, Yang Y, Luan B, Jia L, Xu F, Zhang Z (2011) Carnosine pretreatment protects against hypoxia-ischemia brain damage in the neonatal rat model. Eur J Pharmacol 667:202-207. doi: 10.1016/j.ejphar.2011.06.003