Chronic increase of urea leads to carbamylated proteins accumulation in tissues in a mouse model of CKD

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Pietrement, Christine ^a,b   Gorisse, Laëtitia ^b   Jaisson, Stéphane ^a,b   Gillery, Philippe ^a,b  

^a REIMS UNIVERSITY HOSPITAL   (France)

^b UNIVERSITÉ DE REIMS CHAMPAGNE ARDENNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CARBAMYLATED PROTEIN; COLLAGEN; HOMOCITRULLINE; PEPTIDES AND PROTEINS; SCLEROPROTEIN; UNCLASSIFIED DRUG; UREA;

ACUTE KIDNEY FAILURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CARBAMOYLATION; CHRONIC KIDNEY DISEASE; CHRONIC KIDNEY FAILURE; CONTROLLED STUDY; FEMALE; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN CONTENT; PROTEIN MODIFICATION;

ANIMALS; CARBAMATES; COLLAGEN; DISEASE MODELS, ANIMAL; EXTRACELLULAR MATRIX; FEMALE; KINETICS; MICE; ORGAN SPECIFICITY; PROTEINS; RENAL INSUFFICIENCY, CHRONIC; UREMIA;

EID: 84891771440     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082506     Document Type: Article

References (51)

1. Baynes JW, Thorpe SR (2000) Glycoxidation and lipoxidation in atherogenesis. Free Radic Biol Med 28: 1708-1716. doi:10.1016/S0891-5849(00) 00228-8. PubMed: 10946212.
2. Witko-Sarsat V, Nguyen-Khoa T, Jungers P, Drüeke TB, Descamps-Latscha B (1999) Advanced oxidation protein products as a novel molecular basis of oxidative stress in uraemia. Nephrol Dial Transplant 14 Suppl 1: 76-78. doi:10.1093/ndt/14.1.76. PubMed: 10048460.
3. Drüeke TB, Massy ZA (2010) Atherosclerosis in CKD: differences from the general population. Nat Rev Nephrol 6: 723-735. doi:10.1038/nrneph.2010.143. PubMed: 20978469.
4. Go AS, Chertow GM, Fan D, McCulloch CE, Hsu CY (2004) Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med 351: 1296-1305. doi:10.1056/NEJMoa041031. PubMed: 15385656.
5. Remuzzi G, Bertani T (1998) Pathophysiology of progressive nephropathies. N Engl J Med 339: 1448-1456. doi:10.1056/NEJM199811123392007. PubMed: 9811921.
6. Siew ED, Ikizler TA (2010) Insulin resistance and protein energy metabolism in patients with advanced chronic kidney disease. Semin Dial 23: 378-382. doi:10.1111/j.1525-139X.2010.00763.x. PubMed: 20701717.
7. Priyadarshi A, Shapiro JI (2006) Erythropoietin resistance in the treatment of the anemia of chronic renal failure. Semin Dial 19: 273-278. doi:10.1111/j.1525-139X.2006.00172.x. PubMed: 16893403.
8. Pugh-Clarke K, Donlon S, McCann M (2010) CE: continuing education article. Prevention of infection in patients with chronic kidney disease part 1: application of infection control principles to the renal care environment. J Ren Care 36: 191-198. doi:10.1111/j.1755-6686.2010.00203.x. PubMed: 20969737.
9. Longenecker JC, Coresh J, Powe NR, Levey AS, Fink NE et al. (2002) Traditional cardiovascular disease risk factors in dialysis patients compared with the general population: the CHOICE Study. J Am Soc Nephrol 13: 1918-1927. doi:10.1097/01.ASN.0000019641.41496.1E. PubMed: 12089389.
10. Gillery P, Jaisson S (2013) Post-translational modification derived products (PTMDPs): toxins in chronic diseases? Clin Chem Lab Med: 1-6. doi:10.1515/cclm-2012-0880. PubMed: 23454717.
11. Jaisson S, Pietrement C, Gillery P (2011) Carbamylation-derived products: bioactive compounds and potential biomarkers in chronic renal failure and atherosclerosis. Clin Chem 57: 1499-1505. doi: 10.1373/clinchem.2011.163188. PubMed: 21768218.
12. Roxborough HE, Young IS (1995) Carbamylation of proteins and atherogenesis in renal failure. Med Hypotheses 45: 125-128. doi: 10.1016/0306-9877(95)90059-4. PubMed: 8531833.
13. Kraus LM, Kraus AP (2001) Carbamoylation of amino acids and proteins in uremia. Kidney Int Suppl 78: S102-S107. PubMed: 11168993.
14. Sirpal S (2009) Myeloperoxidase-mediated lipoprotein carbamylation as a mechanistic pathway for atherosclerotic vascular disease. Clin Sci (Lond) 116: 681-695. doi:10.1042/CS20080322. PubMed: 19323651.
15. Wang Z, Nicholls SJ, Rodriguez ER, Kummu O, Hörkkö S et al. (2007) Protein carbamylation links inflammation, smoking, uremia and atherogenesis. Nat Med 13: 1176- 1184. doi:10.1038/nm1637. PubMed: 17828273.
16. Roberts JM, Veres PR, Cochran AK, Warneke C, Burling IR et al. (2011) Isocyanic acid in the atmosphere and its possible link to smoke-related health effects. Proc Natl Acad Sci U S A 108: 8966-8971. doi: 10.1073/pnas.1103352108. PubMed: 21576489.
17. Apostolov EO, Ray D, Savenka AV, Shah SV, Basnakian AG (2010) Chronic uremia stimulates LDL carbamylation and atherosclerosis. J Am Soc Nephrol 21: 1852-1857. doi:10.1681/ASN.2010040365. PubMed: 20947625.
18. Holzer M, Gauster M, Pfeifer T, Wadsack C, Fauler G et al. (2011) Protein carbamylation renders high-density lipoprotein dysfunctional. Antioxid Redox Signal 14: 2337-2346. doi:10.1089/ars.2010.3640. PubMed: 21235354.
19. Ok E, Basnakian AG, Apostolov EO, Barri YM, Shah SV (2005) Carbamylated low density lipoprotein induces death of endothelial cells: a link to atherosclerosis in patients with kidney disease. Kidney Int 68: 173-178. doi:10.1111/j.1523-1755.2005.00391.x. PubMed: 15954906.
20. Garnotel R, Sabbah N, Jaisson S, Gillery P (2004) Enhanced activation of and increased production of matrix metalloproteinase-9 by human blood monocytes upon adhering to carbamylated collagen. FEBS Lett 563: 13-16. doi:10.1016/S0014-5793(04)00233-9. PubMed: 15063715.
21. Jaisson S, Larreta-Garde V, Bellon G, Hornebeck W, Garnotel R et al. (2007) Carbamylation differentially alters type I collagen sensitivity to various collagenases. Matrix Biol 26: 190-196. doi:10.1016/j.matbio.2006.10.008. PubMed: 17156988.
22. Jaisson S, Lorimier S, Ricard-Blum S, Sockalingum GD, Delevallée-Forte C et al. (2006) Impact of carbamylation on type I collagen conformational structure and its ability to activate human polymorphonuclear neutrophils. Chem Biol 13: 149-159. doi:10.1016/j.chembiol. 2005.11.005. PubMed: 16492563.
23. Koeth RA, Kalantar-Zadeh K, Wang Z, Fu X, Tang WH et al. (2013) Protein Carbamylation Predicts Mortality in ESRD. J Am Soc Nephrol, 24: 853-61. doi:10.1681/ASN.2012030254. PubMed: 23431074.
24. Tang WHW, Shrestha K, Wang Z, Borowski AG, Troughton RW et al. (2013) Protein Carbamylation in Chronic Systolic Heart Failure: Relationship With Renal Impairment and Adverse Long-Term Outcomes. J Card Fail, 19: 219-24. doi:10.1016/j.cardfail.2013.02.001. PubMed: 23582087.
25. Berg AH, Drechsler C, Wenger J, Buccafusca R, Hod T et al. (2013) Carbamylation of serum albumin as a risk factor for mortality in patients with kidney failure. Sci Transl Med 5: 175ra129. PubMed: 23467560.
26. Kraus LM, Gaber L, Handorf CR, Marti HP, Kraus AP Jr. (2001) Carbamoylation of glomerular and tubular proteins in patients with kidney failure: a potential mechanism of ongoing renal damage. Swiss Med Wkly 131: 139-134. PubMed: 11416886.
27. Collins AJ (2003) Cardiovascular mortality in end-stage renal disease. Am J Med Sci 325: 163-167. doi:10.1097/00000441-200304000-00002. PubMed: 12695721.
28. Foley RN, Parfrey PS (1998) Cardiovascular disease and mortality in ESRD. J Nephrol 11: 239-245. PubMed: 9831236.
29. Foley RN, Parfrey PS, Sarnak MJ (1998) Epidemiology of cardiovascular disease in chronic renal disease. J Am Soc Nephrol 9: S16-S23. PubMed: 11443763.
30. Parfrey PS, Foley RN (1999) The clinical epidemiology of cardiac disease in chronic renal failure. J Am Soc Nephrol 10: 1606-1615. PubMed: 10405218.
31. Sarnak MJ, Levey AS, Schoolwerth AC, Coresh J, Culleton B et al. (2003) Kidney disease as a risk factor for development of cardiovascular disease: a statement from the American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention. Circulation 108: 2154-2169. doi:10.1161/01.CIR. 0000095676.90936.80. PubMed: 14581387.
32. Sugiyama S, Okada Y, Sukhova GK, Virmani R, Heinecke JW et al. (2001) Macrophage myeloperoxidase regulation by granulocyte macrophage colony-stimulating factor in human atherosclerosis and implications in acute coronary syndromes. Am J Pathol 158: 879-891. doi:10.1016/S0002-9440(10)64036-9. PubMed: 11238037.
33. Kraus LM, Elberger AJ, Handorf CR, Pabst MJ, Kraus AP Jr (1994) Urea-derived cyanate forms epsilon-amino-carbamoyl-lysine (homocitrulline) in leukocyte proteins in patients with end-stage renal disease on peritoneal dialysis. J Lab Clin Med 123: 882-891. PubMed: 8201267.
34. Gross ML, Piecha G, Bierhaus A, Hanke W, Henle T et al. (2011) Glycated and carbamylated albumin are more "nephrotoxic" than unmodified albumin in the amphibian kidney. Am J Physiol Renal Physiol 301: F476-F485. doi:10.1152/ajprenal.00342.2010. PubMed: 21367923.
35. Shaykh M, Pegoraro AA, Mo W, Arruda JA, Dunea G et al. (1999) Carbamylated proteins activate glomerular mesangial cells and stimulate collagen deposition. J Lab Clin Med 133: 302-308. doi: 10.1016/S0022-2143(99)90086-0. PubMed: 10072262.
36. Mun KC, Golper TA (2000) Impaired biological activity of erythropoietin by cyanate carbamylation. Blood Purif 18: 13-17. doi: 10.1159/000014403. PubMed: 10686438.
37. Hörkkö S, Huttunen K, Korhonen T, Kesäniemi YA (1994) Decreased clearance of lowdensity lipoprotein in patients with chronic renal failure. Kidney Int 45: 561-570. doi:10.1038/ki.1994.73. PubMed: 8164446.
38. Maizel J, Six I, Slama M, Tribouilloy C, Sevestre H et al. (2009) Mechanisms of aortic and cardiac dysfunction in uremic mice with aortic calcification. Circulation 119: 306-313. doi:10.1161/CIRCULATIONAHA.108.797407. PubMed: 19118252.
39. Quinn RP, Price GB, Ellis JM, Makinodan T (1973) Catabolic half-lives of immunoglobulin and albumin as a function of age in mice. J Gerontol 28: 257-264. doi:10.1093/geronj/28.3.257. PubMed: 4709642.
40. Wynckel A, Randoux C, Millart H, Desroches C, Gillery P et al. (2000) Kinetics of carbamylated haemoglobin in acute renal failure. Nephrol Dial Transplant 15: 1183-1188. doi:10.1093/ndt/15.8.1183. PubMed: 10910442.
41. Sell DR, Lane MA, Johnson WA, Masoro EJ, Mock OB et al. (1996) Longevity and the genetic determination of collagen glycoxidation kinetics in mammalian senescence. Proc Natl Acad Sci U S A 93: 485-490. doi:10.1073/pnas.93.1.485. PubMed: 8552666.
42. El-Gamal D, Holzer M, Gauster M, Schicho R, Binder V et al. (2012) Cyanate is a novel inducer of endothelial icam-1 expression. Antioxid Redox Signal 16: 129-137. doi:10.1089/ars.2011.4090. PubMed: 21838543.
43. Francis AA, Pierce GN (2011) An integrated approach for the mechanisms responsible for atherosclerotic plaque regression. Exp Clin Cardiol 16: 77-86. PubMed: 22065938.
44. Himmelfarb J, Stenvinkel P, Ikizler TA, Hakim RM (2002) The elephant in uremia: oxidant stress as a unifying concept of cardiovascular disease in uremia. Kidney Int 62: 1524- 1538. doi:10.1046/j.1523-1755.2002.00600.x. PubMed: 12371953.
45. Kalantar-Zadeh K, Block G, Humphreys MH, Kopple JD (2003) Reverse epidemiology of cardiovascular risk factors in maintenance dialysis patients. Kidney Int 63: 793-808. doi:10.1046/j.1523-1755.2003.00803.x. PubMed: 12631061.
46. Liu Y, Coresh J, Eustace JA, Longenecker JC, Jaar B et al. (2004) Association between cholesterol level and mortality in dialysis patients: role of inflammation and malnutrition. JAMA 291: 451-459. doi:10.1001/jama.291.4.451. PubMed: 14747502.
47. Hazen SL (2004) Myeloperoxidase and plaque vulnerability. Arterioscler Thromb Vasc Biol 24: 1143-1146. doi:10.1161/01.ATV.0000135267.82813.52. PubMed: 15237089.
48. Rudolph TK, Wipper S, Reiter B, Rudolph V, Coym A et al. (2012) Myeloperoxidase deficiency preserves vasomotor function in humans. Eur Heart J 33: 1625-1634. doi:10.1093/eurheartj/ehr193. PubMed: 21724624.
49. Sugiyama S, Kugiyama K, Aikawa M, Nakamura S, Ogawa H et al. (2004) Hypochlorous acid, a macrophage product, induces endothelial apoptosis and tissue factor expression: involvement of myeloperoxidase-mediated oxidant in plaque erosion and thrombogenesis. Arterioscler Thromb Vasc Biol 24: 1309-1314. doi: 10.1161/01.ATV.0000131784.50633.4f. PubMed: 15142860.
50. Vita JA, Brennan ML, Gokce N, Mann SA, Goormastic M et al. (2004) Serum myeloperoxidase levels independently predict endothelial dysfunction in humans. Circulation 110: 1134-1139. doi: 10.1161/01.CIR.0000140262.20831.8F. PubMed: 15326065.
51. Jaisson S, Gorisse L, Pietrement C, Gillery P (2012) Quantification of plasma homocitrulline using hydrophilic interaction liquid chromatography (HILIC) coupled to tandem mass spectrometry. Anal Bioanal Chem 402: 1635-1641. doi:10.1007/s00216-011-5619-6. PubMed: 22160237.