Immunochemically unreactive albumin in urine: fiction or reality?

References

• Bigazzi R, Bianchi S, Baldari D, Campese VM. Microalbuminuria predicts cardiovascular events and renal insufficiency in patients with essential hypertension. j Hypertens 1998;16:1325–1333.
   PubMed Web of Science ®Google Scholar
• Mogensen CE. Microalbuminuria, blood pressure and diabetic renal disease: origin and development of ideas. Diabetologia 1999;42:263–285.
   PubMed Web of Science ®Google Scholar
• Arnlöv J, Evans JC, Meigs JB, Wang TJ, Fox CS, Levy D et al. Low-grade albuminuria and incidence of cardiovascular disease events in nonhypertensive and nondiabetic individuals: the Framingham Heart Study. Circulation 2005;112:969–975.
   PubMed Web of Science ®Google Scholar
• Xu J, Knowler WC, Devereux RB, Yeh J, Umans JG, Begum M et al. Albuminuria within the “normal” range and risk of cardiovascular disease and death in American Indians: the Strong Heart Study. Am j Kidney Dis 2007;49:208–216.
   Web of Science ®Google Scholar
• Comper WD, Osicka TM, Jerums G. High prevalence of immuno-unreactive intact albumin in urine of diabetic patients. Am j Kidney Dis 2003;41:336–342.
   PubMedGoogle Scholar
• Yagame M, Suzuki D, Jinde K, Yano N, Naka R, Abe Y et al. Urinary albumin fragments as a new clinical parameter for the early detection of diabetic nephropathy. Intern Med 1995;34:463–468.
   Google Scholar
• Myers BD. Pathophysiology of proteinuria in diabetic glomerular disease. j Hypertens Suppl 1990;8:S41–S46.
   PubMedGoogle Scholar
• Miller WG, Bruns DE, Hortin GL, Sandberg S, Aakre KM, McQueen MJ et al.; National Kidney Disease Education Program-IFCC Working Group on Standardization of Albumin in Urine. Current issues in measurement and reporting of urinary albumin excretion. Clin Chem 2009;55:24–38.
   PubMed Web of Science ®Google Scholar
• Donadio E, Piccolomini F, Dimuccio V, Felicioli A, Balestreri E, Cianti R et al. Serum albumin fragmentation in end-stage renal disease patients–a pilot study. Clin Chem Lab Med 2009;47:1373–1379.
   PubMed Web of Science ®Google Scholar
• Seegmiller JC, Sviridov D, Larson TS, Borland TM, Hortin GL, Lieske JC. Comparison of urinary albumin quantification by immunoturbidimetry, competitive immunoassay, and protein-cleavage liquid chromatography-tandem mass spectrometry. Clin Chem 2009;55:1991–1994.
   Google Scholar
• Sviridov D, Drake SK, Hortin GL. Reactivity of urinary albumin (microalbumin) assays with fragmented or modified albumin. Clin Chem 2008;54:61–68.
   PubMed Web of Science ®Google Scholar
• Sviridov D, Hortin GL. Urine albumin measurement: effects of urine matrix constituents. Clin Chim Acta 2009;404:140–143.
   PubMed Web of Science ®Google Scholar
• Osicka TM, Panagiotopoulos S, Jerums G, Comper WD. Fractional clearance of albumin is influenced by its degradation during renal passage. Clin Sci 1997;93:557–564.
   Google Scholar
• Osicka TM, Comper WD. Protein degradation during renal passage in normal kidneys is inhibited in experimental albuminuria. Clin Sci 1997;93:65–72.
   Google Scholar
• Osicka TM, Houlihan CA, Chan JG, Jerums G, Comper WD. Albuminuria in patients with type 1 diabetes is directly linked to changes in the lysosome-mediated degradation of albumin during renal passage. Diabetes 2000;49:1579–1584.
   PubMed Web of Science ®Google Scholar
• Nakayama A, Sakatsume M, Kasama T, Kawara T, Gejyo F, Isobe M et al. Molecular heterogeneity of urinary albumin in glomerulonephritis: comparison of cardiovascular disease with albuminuria. Clin Chim Acta 2009;402:94–101.
   Google Scholar
• Norden AG, Sharratt P, Cutillas PR, Cramer R, Gardner SC, Unwin RJ. Quantitative amino acid and proteomic analysis: very low excretion of polypeptides >750 Da in normal urine. Kidney Int 2004;66:1994–2003.
   PubMed Web of Science ®Google Scholar
• Hilliard LM, Osicka TM, Clavant SP, Robinson PJ, Nikolic-Paterson DJ, Comper WD. Characterization of the urinary albumin degradation pathway in the isolated perfused rat kidney. j Lab Clin Med 2006;147:36–44.
   Google Scholar
• Peters H. All about albumin: biochemistry, genetics, and medical applications. San Diego, CA: Academic Press, 1996.
   Google Scholar
• Iwao Y, Hiraike M, Kragh-Hansen U, Mera K, Noguchi T, Anraku M et al. Changes of net charge and alpha-helical content affect the pharmacokinetic properties of human serum albumin. Biochim Biophys Acta 2007;1774:1582–1590.
   PubMed Web of Science ®Google Scholar
• Wiggins RC, Kshrisagar B, Kelsch RC, Wilson BS. Fragmentation and polymeric complexes of albumin in human urine. Clin Chim Acta 1985;149:155–163.
   Google Scholar
• Calzada-García JA, Pérez González MN, Benito-Andrés FJ, Morales García LJ, Cabezas JA, Sánchez-Bernal C. Evaluation of patterns of urinary proteins by SDS-PAGE in rats of different ages. Mech Ageing Dev 1996;87:1–13.
   Google Scholar
• Candiano G, Musante L, Bruschi M, Petretto A, Santucci L, Del Boccio P et al. Repetitive fragmentation products of albumin and alpha1-antitrypsin in glomerular diseases associated with nephrotic syndrome. j Am Soc Nephrol 2006;17:3139–3148.
   PubMed Web of Science ®Google Scholar
• Maunsbach AB. Absorption of I-125-labeled homologous albumin by rat kidney proximal tubule cells. A study of microperfused single proximal tubules by electron microscopic autoradiography and histochemistry. j Ultrastruct Res 1966;15:197–241.
   PubMedGoogle Scholar
• Christensen EI, Nielsen S, Moestrup SK, Borre C, Maunsbach AB, de Heer E et al. Segmental distribution of the endocytosis receptor gp330 in renal proximal tubules. Eur j Cell Biol 1995;66:349–364.
   PubMed Web of Science ®Google Scholar
• Kshirsagar B, Wilson B, Wiggins RC. Polymeric complexes and fragments of albumin in normal human plasma. Clin Chim Acta 1984;143:265–273.
   PubMed Web of Science ®Google Scholar
• Burne MJ, Panagiotopoulos S, Jerums G, Comper WD. Alterations in renal degradation of albumin in early experimental diabetes in the rat: a new factor in the mechanism of albuminuria. Clin Sci 1998;95:67–72.
   Google Scholar
• Osicka TM, Yu Y, Panagiotopoulos S, Clavant SP, Kiriazis Z, Pike RN et al. Prevention of albuminuria by aminoguanidine or ramipril in streptozotocin-induced diabetic rats is associated with the normalization of glomerular protein kinase C. Diabetes 2000;49:87–93.
   PubMed Web of Science ®Google Scholar
• Olbricht CJ, Geissinger B. Renal hypertrophy in streptozotocin diabetic rats: role of proteolytic lysosomal enzymes. Kidney Int 1992;41:966–972.
   Google Scholar
• Myers BD, Winetz JA, Chui F, Michaels AS. Mechanisms of proteinuria in diabetic nephropathy: a study of glomerular barrier function. Kidney Int 1982;21:633–641.
   PubMed Web of Science ®Google Scholar
• Scandling JD, Black VM, Deen WM, Myers BD. Glomerular permselectivity in healthy and nephrotic humans. Adv Nephrol Necker Hosp 1992;21:159–176.
   PubMedGoogle Scholar
• Gekle M, Mildenberger S, Freudinger R, Schwerdt G, Silbernagl S. Albumin endocytosis in OK cells: dependence on actin and microtubules and regulation by protein kinases. Am j Physiol 1997;272:F668–F677.
   Google Scholar
• Koya D, Lee IK, Ishii H, Kanoh H, King GL. Prevention of glomerular dysfunction in diabetic rats by treatment with d-alpha-tocopherol. j Am Soc Nephrol 1997;8:426–435.
   PubMed Web of Science ®Google Scholar
• Derubertis FR, Craven PA. Activation of protein kinase C in glomerular cells in diabetes. Mechanisms and potential links to the pathogenesis of diabetic glomerulopathy. Diabetes 1994;43:1–8.
   PubMed Web of Science ®Google Scholar
• Han HJ, Koh HJ, Park SH. A signaling pathway for stimulation of Na+ uptake induced by angiotensin II in primary cultured rabbit renal proximal tubule cells. j Vet Med Sci 1999;61:135–141.
   Google Scholar
• Radons J, Biewusch U, Grässel S, Geuze HJ, Hasilik A. Distinctive inhibition of the lysosomal targeting of lysozyme and cathepsin D by drugs affecting pH gradients and protein kinase C. Biochem j 1994;302 (Pt 2):581–586.
   Google Scholar
• Gewert K, Tapper H, Nauclér C, Sundler R. Dexamethasone downregulates lysosomal secretion in mouse macrophages: involvement of signaling through protein kinase C. j Inflamm 1995;47:115–125.
   Google Scholar
• Hilliard LM, Russo LM, Comper WD. Hypertension-mediated albuminuria is associated with reduced lysosomal activity in the kidney and the heart. Am j Nephrol 2009;29:454–464.
   Google Scholar
• Russo LM, Comper WD, Osicka TM. Mechanism of albuminuria associated with cardiovascular disease and kidney disease. Kidney Int Suppl 2004;92:S67–S68.
   Google Scholar
• Russo LM, Osicka TM, Brammar GC, Candido R, Jerums G, Comper WD. Renal processing of albumin in diabetes and hypertension in rats: possible role of TGF-beta1. Am j Nephrol 2003;23:61–70.
   Google Scholar
• Russo LM, Brammar GC, Jerums G, Comper WD, Osicka TM. The effect of ramipril on albumin excretion in diabetes and hypertension: the role of increased lysosomal activity and decreased transforming growth factor-beta expression. j Hypertens 2003;21:419–428.
   Google Scholar
• Russo LM, Osicka TM, Bonnet F, Jerums G, Comper WD. Albuminuria in hypertension is linked to altered lysosomal activity and TGF-beta1 expression. Hypertension 2002;39:281–286.
   Google Scholar
• Ling H, Vamvakas S, Busch G, Dämmrich J, Schramm L, Lang F et al. Suppressing role of transforming growth factor-beta 1 on cathepsin activity in cultured kidney tubule cells. Am j Physiol 1995;269:F911–F917.
   PubMed Web of Science ®Google Scholar
• Schenk O, Ling H, Sebeková K, Vamvakas S, Heidland A. High-glucose media enhance the responsiveness of tubular cells to growth promoters: effect on lysosomal cathepsins and protein degradation. Miner Electrolyte Metab 1998;24:254–260.
   Google Scholar
• Gekle M, Knaus P, Nielsen R, Mildenberger S, Freudinger R, Wohlfarth V et al. Transforming growth factor-beta1 reduces megalin- and cubilin-mediated endocytosis of albumin in proximal-tubule-derived opossum kidney cells. j Physiol (Lond) 2003;552:471–481.
   Google Scholar
• Russo LM, del Re E, Brown D, Lin HY. Evidence for a role of transforming growth factor (TGF)-beta1 in the induction of postglomerular albuminuria in diabetic nephropathy: amelioration by soluble TGF-beta type II receptor. Diabetes 2007;56:380–388.
   PubMed Web of Science ®Google Scholar
• Brooks WW, Bing OH, Robinson KG, Slawsky MT, Chaletsky DM, Conrad CH. Effect of angiotensin-converting enzyme inhibition on myocardial fibrosis and function in hypertrophied and failing myocardium from the spontaneously hypertensive rat. Circulation 1997;96:4002–4010.
   PubMed Web of Science ®Google Scholar
• Brilla CG, Janicki JS, Weber KT. Cardioreparative effects of lisinopril in rats with genetic hypertension and left ventricular hypertrophy. Circulation 1991;83:1771–1779.
   PubMed Web of Science ®Google Scholar
• Terawaki H, Yoshimura K, Hasegawa T, Matsuyama Y, Negawa T, Yamada K et al. Oxidative stress is enhanced in correlation with renal dysfunction: examination with the redox state of albumin. Kidney Int 2004;66:1988–1993.
   PubMed Web of Science ®Google Scholar
• Candiano G, Musante L, Petretto A, Bruschi M, Santucci L, Urbani A et al. Proteomics of plasma and urine in primary nephrotic syndrome in children. Contrib Nephrol 2008;160:17–28.
   Web of Science ®Google Scholar
• Hellin JL, Bech-Serra JJ, Moctezuma EL, Chocron S, Santin S, Madrid A et al. Very low-molecular-mass fragments of albumin in the plasma of patients with focal segmental glomerulosclerosis. Am j Kidney Dis 2009;54:871–880.
   Google Scholar
• Cochran A, Dong L, Edelman LS, Roberts WL, Ballard J, Privette A et al. Microalbuminuria in acute burn injury. j Burn Care Res 2008;29:176–179.
   Google Scholar
• Sviridov D, Owen WE, Roberts WL, Edelman LS, Drake SK, Hortin GL. Proteinuria without albuminuria: urinary protein excretion by a subset of patients with burn injuries. Clin Chim Acta 2009;403:42–46.
   Google Scholar
• Markó L, Szigeti N, Szabó Z, Böddi K, Takátsy A, Ludány A et al. Potential urinary biomarkers of disease activity in Crohn’s disease. Scand j Gastroenterol 2010;45:1440–1448.
   PubMed Web of Science ®Google Scholar
• Mahmud N, McDonald GS, Kelleher D, Weir DG. Microalbuminuria correlates with intestinal histopathological grading in patients with inflammatory bowel disease. Gut 1996;38:99–103.
   PubMed Web of Science ®Google Scholar
• Mahmud N, O’Connell MA, Stinson J, Goggins MG, Weir DG, Kelleher D. Tumour necrosis factor-alpha and microalbuminuria in patients with inflammatory bowel disease. Eur j Gastroenterol Hepatol 1995;7:215–219.
   PubMed Web of Science ®Google Scholar
• Sakata S, Atassi MZ. Immunochemistry of serum albumin. X. Five major antigenic sites of human serum albumin are extrapolated from bovine albumin and confirmed by synthetic peptides. Mol Immunol 1980;17:139–142.
   PubMed Web of Science ®Google Scholar
• Brinkman JW, Bakker SJ, Gansevoort RT, Hillege HL, Kema IP, Gans RO et al. Which method for quantifying urinary albumin excretion gives what outcome? A comparison of immunonephelometry with HPLC. Kidney Int Suppl 2004;S69–S75.
   Google Scholar
• Markó L, Molnár GA, Wagner Z, Böddi K, Koszegi T, Szabó Z et al. Measurement of the modification and interference rate of urinary albumin detected by size-exclusion HPLC. Physiol Meas 2009;30:1137–1150.
   PubMedGoogle Scholar
• Brinkman JW, de Zeeuw D, Duker JJ, Gansevoort RT, Kema IP, Hillege HL et al. Falsely low urinary albumin concentrations after prolonged frozen storage of urine samples. Clin Chem 2005;51:2181–2183.
   PubMed Web of Science ®Google Scholar
• Osicka TM, Comper WD. Characterization of immunochemically nonreactive urinary albumin. Clin Chem 2004;50:2286–2291.
   PubMed Web of Science ®Google Scholar
• Bertolatus JA, Hunsicker LG. Glomerular sieving of anionic and neutral bovine albumins in proteinuric rats. Kidney Int 1985;28:467–476.
   Google Scholar
• Greive KA, Eppel GA, Reeve S, Smith AI, Jerums G, Comper WD. Immuno-unreactive albumin excretion increases in streptozotocin diabetic rats. Am j Kidney Dis 2001;38:144–152.
   Google Scholar
• Comper WD, Jerums G, Osicka TM. Differences in urinary albumin detected by four immunoassays and high-performance liquid chromatography. Clin Biochem 2004;37:105–111.
   PubMed Web of Science ®Google Scholar
• Osicka TM, MacIsaac RJ, Jerums G, Comper WD. High prevalence of immunounreactive albumin in urine from diabetic patients with a low glomerular filtration rate and normoalbuminuria. Diabetes Care 2004;27:1515.
   Google Scholar
• Comper WD, Osicka TM, Clark M, MacIsaac RJ, Jerums G. Earlier detection of microalbuminuria in diabetic patients using a new urinary albumin assay. Kidney Int 2004;65:1850–1855.
   PubMed Web of Science ®Google Scholar
• Markó L, Cseh J, Kószegi T, Szabó Z, Molnár GA, Mohás M et al. Storage at -80 degrees C decreases the concentration of HPLC-detected urinary albumin: possible mechanisms and implications. j Nephrol 2009;22:397–402.
   PubMed Web of Science ®Google Scholar
• Brinkman JW, de Zeeuw D, Lambers Heerspink HJ, Gansevoort RT, Kema IP, de Jong PE et al. Apparent loss of urinary albumin during long-term frozen storage: HPLC vs immunonephelometry. Clin Chem 2007;53:1520–1526.
   PubMed Web of Science ®Google Scholar
• Singh R, Crow FW, Babic N, Lutz WH, Lieske JC, Larson TS et al. A liquid chromatography-mass spectrometry method for the quantification of urinary albumin using a novel 15N-isotopically labeled albumin internal standard. Clin Chem 2007;53:540–542.
   Google Scholar
• Babic N, Larson TS, Grebe SK, Turner ST, Kumar R, Singh RJ. Application of liquid chromatography-mass spectrometry technology for early detection of microalbuminuria in patients with kidney disease. Clin Chem 2006;52:2155–2157.
   Google Scholar
• Shaikh A, Seegmiller JC, Borland TM, Burns BE, Ladwig PM, Singh RJ et al. Comparison between immunoturbidimetry, size-exclusion chromatography, and LC-MS to quantify urinary albumin. Clin Chem 2008;54:1504–1510.
   PubMed Web of Science ®Google Scholar
• Seegmiller JC, Barnidge DR, Burns BE, Larson TS, Lieske JC, Kumar R. Quantification of urinary albumin by using protein cleavage and LC-MS/MS. Clin Chem 2009;55:1100–1107.
   Google Scholar
• Whicher JT, Ritchie RF, Johnson AM, Baudner S, Bienvenu J, Blirup-Jensen S et al. New international reference preparation for proteins in human serum (RPPHS). Clin Chem 1994;40:934–938.
   PubMed Web of Science ®Google Scholar
• Zegers I, Keller T, Schreiber W, Sheldon J, Albertini R, Blirup-Jensen S et al. Characterization of the new serum protein reference material ERM-DA470k/IFCC: value assignment by immunoassay. Clin Chem 2010;56:1880–1888.
   PubMed Web of Science ®Google Scholar
• Comper WD, Jerums G, Osicka TM. Differences in urinary albumin detected by four immunoassays and high-performance liquid chromatography. Clin Biochem 2004;37:105–111.
   PubMed Web of Science ®Google Scholar
• Giampietro O, Penno G, Clerico A, Cruschelli L, Lucchetti A, Nannipieri M et al. Which method for quantifying “microalbuminuria” in diabetics? Comparison of several immunological methods (immunoturbidimetric assay, immunonephelometric assay, radioimmunoassay and two semiquantitative tests) for measurement of albumin in urine. Acta Diabetol 1992;28:239–245.
   PubMedGoogle Scholar
• Roberts WL, Calcote CB, Cook CB, Gordon DL, Moore ML, Moore S et al. Comparison of four commercial urinary albumin (microalbumin) methods: implications for detecting diabetic nephropathy using random urine specimens. Clin Chim Acta 1998;273:21–33.
   PubMed Web of Science ®Google Scholar
• Agarwal R. On the nature of proteinuria with acute renal injury in patients with chronic kidney disease. Am j Physiol Renal Physiol 2005;288:F265–F271.
   PubMed Web of Science ®Google Scholar
• Curry S, Mandelkow H, Brick P, Franks N. Crystal structure of human serum albumin complexed with fatty acid reveals an asymmetric distribution of binding sites. Nat Struct Biol 1998;5:827–835.
   PubMed Web of Science ®Google Scholar
• Sviridov D, Meilinger B, Drake SK, Hoehn GT, Hortin GL. Coelution of other proteins with albumin during size-exclusion HPLC: Implications for analysis of urinary albumin. Clin Chem 2006;52:389–397.
   PubMedGoogle Scholar
• Clavant SP, Sastra SA, Osicka TM, Comper WD. The analysis and characterisation of immuno-unreactive urinary albumin in healthy volunteers. Clin Biochem 2006;39:143–151.
   PubMedGoogle Scholar
• Bakker SJ, Gansevoort RT, de Zeeuw D. Albuminuria: what can we expect from the determination of nonimmunoreactive albumin? Curr Hypertens Rep 2009;11:111–117.
   Google Scholar
• Magliano DJ, Polkinghorne KR, Barr EL, Su Q, Chadban SJ, Zimmet PZ et al. HPLC-detected albuminuria predicts mortality. j Am Soc Nephrol 2007;18:3171–3176.
   Google Scholar
• McQueen MJ, Gerstein HC, Pogue J, Mann JF, Yusuf S. Reevaluation by high-performance liquid chromatography: clinical significance of microalbuminuria in individuals at high risk of cardiovascular disease in the Heart Outcomes Prevention Evaluation (HOPE) Study. Am j Kidney Dis 2006;48:889–896.
   Google Scholar
• Wang Z, Hoy WE, Nicol JL, Wang Z, Su Q, Atkins RC et al. Predictive value of nephelometric and high-performance liquid chromatography assays of urine albumin for mortality in a high-risk Aboriginal population. Am j Kidney Dis 2008;52:672–682.
   Google Scholar
• Halimi JM, Buchler M, Al-Najjar A, Laouad I, Chatelet V, Marlière JF et al. Urinary albumin excretion and the risk of graft loss and death in proteinuric and non-proteinuric renal transplant recipients. Am j Transplant 2007;7:618–625.
   PubMed Web of Science ®Google Scholar
• Caramori ML, Fioretto P, Mauer M. The need for early predictors of diabetic nephropathy risk: is albumin excretion rate sufficient? Diabetes 2000;49:1399–1408.
   PubMed Web of Science ®Google Scholar
• Fioretto P, Steffes MW, Sutherland DE, Mauer M. Sequential renal biopsies in insulin-dependent diabetic patients: structural factors associated with clinical progression. Kidney Int 1995;48:1929–1935.
   PubMed Web of Science ®Google Scholar