Table of Contents
International Journal of Proteomics
Volume 2015, Article ID 782798, 17 pages
http://dx.doi.org/10.1155/2015/782798
Review Article

Human Urine Proteomics: Analytical Techniques and Clinical Applications in Renal Diseases

1Chronic Kidney Disease Research Center, Labbafinejad Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran
2Department of Basic Science, Faculty of Paramedical Sciences, Shahid Beheshti University of Medical Sciences, Tehran, Iran

Received 20 July 2015; Accepted 9 November 2015

Academic Editor: Petra Zürbig

Copyright © 2015 Shiva Kalantari et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Adachi, C. Kumar, Y. Zhang, J. V. Olsen, and M. Mann, “The human urinary proteome contains more than 1500 proteins, including a large proportion of membrane proteins,” Genome Biology, vol. 7, article R80, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. H. Husi, N. Stephens, A. Cronshaw et al., “Proteomic analysis of urinary upper gastrointestinal cancer markers,” PROTEOMICS—Clinical Applications, vol. 5, no. 5-6, pp. 289–299, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. V. C. Wasinger, M. Zeng, and Y. Yau, “Current status and advances in quantitative proteomic mass spectrometry,” International Journal of Proteomics, vol. 2013, Article ID 180605, 12 pages, 2013. View at Publisher · View at Google Scholar
  4. D. M. Good, V. Thongboonkerd, J. Novak et al., “Body fluid proteomics for biomarker discovery: lessons from the past hold the key to success in the future,” Journal of Proteome Research, vol. 6, no. 12, pp. 4549–4555, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Cui, P. J. Verroust, S. K. Moestrup, and E. I. Christensen, “Megalin/gp330 mediates uptake of albumin in renal proximal tubule,” American Journal of Physiology—Renal Fluid and Electrolyte Physiology, vol. 271, no. 4, pp. F900–F907, 1996. View at Google Scholar · View at Scopus
  6. T. Pisitkun, R.-F. Shen, and M. A. Knepper, “Identification and proteomic profiling of exosomes in human urine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 36, pp. 13368–13373, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Castagna, D. Cecconi, L. Sennels et al., “Exploring the hidden human urinary proteome via ligand library beads,” Journal of Proteome Research, vol. 4, no. 6, pp. 1917–1930, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. R. Pieper, C. L. Gatlin, A. M. McGrath et al., “Characterization of the human urinary proteome: a method for high-resolution display of urinary proteins on two-dimensional electrophoresis gels with a yield of nearly 1400 distinct protein spots,” Proteomics, vol. 4, no. 4, pp. 1159–1174, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. W. Sun, F. Li, S. Wu et al., “Human urine proteome analysis by three separation approaches,” Proteomics, vol. 5, no. 18, pp. 4994–5001, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. L. Wang, F. Li, W. Sun et al., “Concanavalin A-captured glycoproteins in healthy human urine,” Molecular and Cellular Proteomics, vol. 5, no. 3, pp. 560–562, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Ożgo, W. F. Skrzypczak, A. Herosimczyk, and A. Mazur, “Proteomika a fizjologia i patofizjologia nerek,” MedWet, vol. 63, pp. 1146–1150, 2007. View at Google Scholar
  12. B. Haraldsson and J. Sörensson, “Why do we not all have proteinuria? An update of our current understanding of the glomerular barrier,” News in Physiological Sciences, vol. 19, no. 1, pp. 7–10, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. A. B. Maunsbach, “Absorption of I125-labeled homologous albumin by rat kidney proximal tubule cells. A study of microperfused single proximal tubules by electron microscopic autoradiography and histochemistry, 1966,” Journal of the American Society of Nephrology, vol. 8, no. 2, pp. 323–351, 1997. View at Google Scholar · View at Scopus
  14. M. J. Burne, T. M. Osicka, and W. D. Comper, “Fractional clearance of high molecular weight proteins in conscious rats using a continuous infusion method,” Kidney International, vol. 55, no. 1, pp. 261–270, 1999. View at Publisher · View at Google Scholar · View at Scopus
  15. V. Batuman, P. J. Verroust, G. L. Navar et al., “Myeloma light chains are ligands for cubilin (gp280),” American Journal of Physiology—Renal Physiology, vol. 275, no. 2, pp. F246–F254, 1998. View at Google Scholar · View at Scopus
  16. E. I. Christensen and J. Gburek, “Protein reabsorption in renal proximal tubule—function and dysfunction in kidney pathophysiology,” Pediatric Nephrology, vol. 19, no. 7, pp. 714–721, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Afkarian, M. Bhasin, S. T. Dillon et al., “Optimizing a proteomics platform for urine biomarker discovery,” Molecular and Cellular Proteomics, vol. 9, no. 10, pp. 2195–2204, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Peng and S. P. Gygi, “Proteomics: the move to mixtures,” Journal of Mass Spectrometry, vol. 36, no. 10, pp. 1083–1091, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. V. Thongboonkerd, “Proteomics in nephrology: current status and future directions,” American Journal of Nephrology, vol. 24, no. 3, pp. 360–378, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Marimuthu, R. N. O'Meally, R. Chaerkady et al., “A comprehensive map of the human urinary proteome,” Journal of Proteome Research, vol. 10, no. 6, pp. 2734–2743, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. Q.-R. Li, K.-X. Fan, R.-X. Li et al., “A comprehensive and nonprefractionation on the protein level approach for the human urinary proteome: touching phosphorylation in urine,” Rapid Communications in Mass Spectrometry, vol. 24, no. 6, pp. 823–832, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. P. A. Gonzales, T. Pisitkun, J. D. Hoffert et al., “Large-scale proteomics and phosphoproteomics of urinary exosomes,” Journal of the American Society of Nephrology, vol. 20, no. 2, pp. 363–379, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Khan and N. H. Packer, “Simple urinary sample preparation for proteomic analysis,” Journal of Proteome Research, vol. 5, no. 10, pp. 2824–2838, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. V. Thongboonkerd, S. Chutipongtanate, and R. Kanlaya, “Systematic evaluation of sample preparation methods for gel-based human urinary proteomics: quantity, quality, and variability,” Journal of Proteome Research, vol. 5, no. 1, pp. 183–191, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. G. Gopalan, V. S. Rao, and V. V. Kakar, “An overview of urinary proteomics applications in human diseases,” International Journal of High Throughput Screening, vol. 1, pp. 183–192, 2010. View at Google Scholar
  26. H.-Y. Tang, L. A. Beer, and D. W. Speicher, “In-depth analysis of a plasma or serum proteome using a 4D protein profiling method,” Methods in Molecular Biology, vol. 728, pp. 47–67, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. N. S. Vasudev, R. E. Ferguson, D. A. Cairns, A. J. Stanley, P. J. Selby, and R. E. Banks, “Serum biomarker discovery in renal cancer using 2-DE and prefractionation by immunodepletion and isoelectric focusing; increasing coverage or more of the same?” Proteomics, vol. 8, no. 23-24, pp. 5074–5085, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. C.-L. Chen, T.-S. Lin, C.-H. Tsai et al., “Identification of potential bladder cancer markers in urine by abundant-protein depletion coupled with quantitative proteomics,” Journal of Proteomics, vol. 85, pp. 28–43, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Filip, K. Vougas, J. Zoidakis et al., “Comparison of depletion strategies for the enrichment of low-abundance proteins in urine,” PLoS ONE, vol. 10, no. 7, Article ID e0133773, 2015. View at Publisher · View at Google Scholar
  30. C.-M. Lu, Y.-J. Wu, C.-C. Chen et al., “Identification of low-abundance proteins via fractionation of the urine proteome with weak anion exchange chromatography,” Proteome Science, vol. 9, article 17, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. S. A. Beausoleil, M. Jedrychowski, D. Schwartz et al., “Large-scale characterization of HeLa cell nuclear phosphoproteins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 33, pp. 12130–12135, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. V. Thongboonkerd, T. Semangoen, and S. Chutipongtanate, “Enrichment of the basic/cationic urinary proteome using ion exchange chromatography and batch adsorption,” Journal of Proteome Research, vol. 6, no. 3, pp. 1209–1214, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. M. M. Kushnir, P. Mrozinski, A. L. Rockwood, and D. K. Crockett, “A depletion strategy for improved detection of human proteins from urine,” Journal of Biomolecular Techniques, vol. 20, no. 2, pp. 101–108, 2009. View at Google Scholar · View at Scopus
  34. V. Thongboonkerd, “Current status of renal and urinary proteomics: ready for routine clinical application,” Nephrology Dialysis Transplantation, vol. 25, no. 1, pp. 11–16, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Decramer, A. G. de Peredo, B. Breuil et al., “Urine in clinical proteomics,” Molecular and Cellular Proteomics, vol. 7, no. 10, pp. 1850–1862, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Jia and L. Zhang, “Advance in proteomics research and application,” Journal of Animal and Veterinary Advances, vol. 11, no. 20, pp. 3812–3817, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Dihazi, “The urinary proteomics: a tool to discover new and potent biomarkers for kidney damage,” Journal of the International Federation of Clinical Chemistry and Laboratory Medicine, vol. 20, no. 1, pp. 82–91, 2009. View at Google Scholar
  38. J. M. González-Buitrago, L. Ferreira, and I. Lorenzo, “Urinary proteomics,” Clinica Chimica Acta, vol. 375, no. 1-2, pp. 49–56, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. M. M. Camacho-Carvcajal, B. Wollscheid, R. Aebersold, V. Steimle, and W. W. A. Schamel, “Two-dimensional Blue Native/SDS gel electrophoresiss of multi-protein complexes from whole cellular lysates: a proteomics approach,” Molecular and Cellular Proteomics, vol. 3, no. 2, pp. 176–182, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. I. Neverova and J. E. Van Eyk, “Role of chromatographic techniques in proteomic analysis,” Journal of Chromatography B: Analytical Technologies in the Biomedical and Life Sciences, vol. 815, no. 1-2, pp. 51–63, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. T. Niwa, “Biomarker discovery for kidney diseases by mass spectrometry,” Journal of Chromatography B, vol. 870, no. 2, pp. 148–153, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. M. G. Janech, J. R. Raymond, and J. M. Arthur, “Proteomics in renal research,” The American Journal of Physiology—Renal Physiology, vol. 292, no. 2, pp. F501–F512, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. P. Rossing, “The changing epidemiology of diabetic microangiopathy in type 1 diabetes,” Diabetologia, vol. 48, no. 8, pp. 1439–1444, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. G. Soldatos and M. E. Cooper, “Diabetic nephropathy: important pathophysiologic mechanisms,” Diabetes Research and Clinical Practice, vol. 82, no. 1, pp. S75–S79, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Soggiu, C. Piras, L. Bonizzi, H. A. Hussein, S. Pisanu, and P. Roncada, “A discovery-phase urine proteomics investigation in type 1 diabetes,” Acta Diabetologica, vol. 49, no. 6, pp. 453–464, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Kalantari, D. Rutishauser, S. Samavat et al., “Urinary prognostic biomarkers and classification of IgA nephropathy by high resolution mass spectrometry coupled with liquid chromatography,” PLoS ONE, vol. 8, no. 12, Article ID e80830, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. B. Xin, D. Pu, S. X. Xiong, and G. H. Wang, “On-line separation and detection of peptides by capillary electrophoresis/electrospray FT-ICR-MS,” Chinese Chemical Letters, vol. 14, pp. 191–194, 2003. View at Google Scholar
  48. D. Fliser, J. Novak, V. Thongboonkerd et al., “Advances in urinary proteome analysis and biomarker discovery,” Journal of the American Society of Nephrology, vol. 18, no. 4, pp. 1057–1071, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. Z. Liu, Z. Yuan, and Q. Zhao, “SELDI-TOF-MS proteomic profiling of serum, urine, and amniotic fluid in neural tube defects,” PLoS ONE, vol. 9, no. 7, Article ID e103276, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Siwy, A. Vlahou, L. U. Zimmerli, P. Zürbig, and E. Schiffer, “Clinical proteomics: current techniques and potential applications in the elderly,” Maturitas, vol. 68, no. 3, pp. 233–244, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. H. Mischak, E. Schiffer, P. Zürbig, M. Dakna, and J. Metzger, “Urinary proteome analysis using capillary electrophoresis coupled to mass spectrometry: a powerful tool in clinical diagnosis, prognosis and therapy evaluation,” Journal of Medical Biochemistry, vol. 28, no. 4, pp. 223–234, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. G. A. Müller, C. A. Müller, and H. Dihazi, “Clinical proteomics—on the long way from bench to bedside?” Nephrology Dialysis Transplantation, vol. 22, no. 5, pp. 1297–1300, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Albalat, H. Mischak, and W. Mullen, “Urine proteomics in clinical applications: technologies, principal considerations and clinical implementation,” Prilozi, vol. 32, pp. 44–45, 2011. View at Google Scholar
  54. M. M. Nilsen, K.-E. Uleberg, E. A. M. Janssen, J. P. A. Baak, O. K. Andersen, and A. Hjelle, “From SELDI-TOF MS to protein identification by on-chip elution,” Journal of Proteomics, vol. 74, no. 12, pp. 2995–2998, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. C. Ibáñez, C. Simó, V. García-Cañas, A. Cifuentes, and M. Castro-Puyana, “Metabolomics, peptidomics and proteomics applications of capillary electrophoresis-mass spectrometry in Foodomics: a review,” Analytica Chimica Acta, vol. 802, pp. 1–13, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. H. Mischak, J. J. Coon, J. Novak, E. M. Weissinger, J. P. Schanstra, and A. F. Dominiczak, “Capillary electrophoresis-mass spectrometry as a powerful tool in biomarker discovery and clinical diagnosis: an update of recent developments,” Mass Spectrometry Reviews, vol. 28, no. 5, pp. 703–724, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. J. Wu, Y.-D. Chen, and W. Gu, “Urinary proteomics as a novel tool for biomarker discovery in kidney diseases,” Journal of Zhejiang University: Science B, vol. 11, no. 4, pp. 227–237, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. C. Simó, A. Cifuentes, and V. Kašička, “Capillary electrophoresis-mass spectrometry for peptide analysis: target-based approaches and proteomics/ peptidomics strategies,” Methods in Molecular Biology, vol. 984, pp. 139–151, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Hu, J. A. Loo, and D. T. Wong, “Human body fluid proteome analysis,” Proteomics, vol. 6, no. 23, pp. 6326–6353, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. P. Díez, N. Dasilva, M. González-González et al., “Data analysis strategies for protein microarrays,” Microarrays, vol. 1, pp. 64–83, 2012. View at Google Scholar
  61. R. Chen and M. Snyder, “Yeast proteomics and protein microarrays,” Journal of Proteomics, vol. 73, no. 11, pp. 2147–2157, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. W. Ruige and Y. S. Fung, “Microfluidic chip-capillary electrophoresis device for the determination of urinary metabolites and proteins,” Bioanalysis, vol. 7, pp. 907–922, 2015. View at Google Scholar
  63. W. P. Guo, Z. B. Rong, Y. H. Li, Y. S. Fung, G. Q. Gao, and Z. M. Cai, “Microfluidic chip capillary electrophoresis coupled with electrochemiluminescence for enantioseparation of racemic drugs using central composite design optimization,” Electrophoresis, vol. 34, no. 20-21, pp. 2962–2969, 2013. View at Publisher · View at Google Scholar · View at Scopus
  64. C.-C. Lin, C.-C. Tseng, T.-K. Chuang, D.-S. Lee, and G.-B. Lee, “Urine analysis in microfluidic devices,” Analyst, vol. 136, no. 13, pp. 2669–2688, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. J. R. Wiśniewski, A. Zougman, N. Nagaraj, and M. Mann, “Universal sample preparation method for proteome analysis,” Nature Methods, vol. 6, no. 5, pp. 359–362, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. Y. Yu, M.-J. Suh, P. Sikorski, K. Kwon, K. E. Nelson, and R. Pieper, “Urine sample preparation in 96-well filter plates for quantitative clinical proteomics,” Analytical Chemistry, vol. 86, no. 11, pp. 5470–5477, 2014. View at Publisher · View at Google Scholar · View at Scopus
  67. Y. Lyutvinskiy, H. Yang, D. Rutishauser, and R. A. Zubarev, “In silico instrumental response correction improves precision of label-free proteomics and accuracy of proteomics-based predictive models,” Molecular and Cellular Proteomics, vol. 12, no. 8, pp. 2324–2331, 2013. View at Publisher · View at Google Scholar · View at Scopus
  68. S. Samavat, S. Kalantari, M. Nafar et al., “Diagnostic urinary proteome profile for immunoglobulin a nephropathy,” Iranian Journal of Kidney Diseases, vol. 9, pp. 239–248, 2015. View at Google Scholar
  69. S. Kalantari, M. Nafar, D. Rutishauser et al., “Predictive urinary biomarkers for steroid-resistant and steroid-sensitive focal segmental glomerulosclerosis using high resolution mass spectrometry and multivariate statistical analysis,” BMC Nephrology, vol. 15, no. 1, article 141, 2014. View at Publisher · View at Google Scholar · View at Scopus
  70. S. Kalantari, M. Nafar, S. Samavat, M. Rezaei-Tavirani, D. Rutishauser, and R. Zubarev, “Urinary prognostic biomarkers in patients with focal segmental glomerulosclerosis,” Nephro-Urology Monthly, vol. 6, no. 2, Article ID e16806, 2014. View at Publisher · View at Google Scholar · View at Scopus
  71. M. Nafar, S. Kalantari, S. Samavat, M. Rezaei-Tavirani, D. Rutishuser, and R. A. Zubarev, “The novel diagnostic biomarkers for focal segmental glomerulosclerosis,” International Journal of Nephrology, vol. 2014, Article ID 574261, 10 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  72. J. Cox, M. Y. Hein, C. A. Luber, I. Paron, N. Nagaraj, and M. Mann, “Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ,” Molecular and Cellular Proteomics, vol. 13, no. 9, pp. 2513–2526, 2014. View at Publisher · View at Google Scholar · View at Scopus
  73. K. A. Neilson, N. A. Ali, S. Muralidharan et al., “Less label, more free: approaches in label-free quantitative mass spectrometry,” Proteomics, vol. 11, no. 4, pp. 535–553, 2011. View at Publisher · View at Google Scholar · View at Scopus
  74. S. Nahnsen, C. Bielow, K. Reinert, and O. Kohlbacher, “Tools for label-free peptide quantification,” Molecular and Cellular Proteomics, vol. 12, no. 3, pp. 549–556, 2013. View at Publisher · View at Google Scholar · View at Scopus
  75. L. Su, R. Zhou, C. Liu et al., “Urinary proteomics analysis for sepsis biomarkers with iTRAQ labeling and two-dimensional liquid chromatography-tandem mass spectrometry,” Journal of Trauma and Acute Care Surgery, vol. 74, no. 3, pp. 940–945, 2013. View at Publisher · View at Google Scholar · View at Scopus
  76. M. T. Davis, C. S. Spahr, M. D. McGinley et al., “Towards defining the urinary proteome using liquid chromatography-tandem mass spectrometry II. Limitations of complex mixture analyses,” Proteomics, vol. 1, no. 1, pp. 108–117, 2001. View at Publisher · View at Google Scholar · View at Scopus
  77. H. Mischak, J. P. A. Ioannidis, A. Argiles et al., “Implementation of proteomic biomarkers: making it work,” European Journal of Clinical Investigation, vol. 42, no. 9, pp. 1027–1036, 2012. View at Publisher · View at Google Scholar · View at Scopus
  78. B. Jim, M. Ghanta, A. Qipo et al., “Dysregulated nephrin in diabetic nephropathy of type 2 diabetes: a cross sectional study,” PLoS ONE, vol. 7, no. 5, Article ID e36041, 2012. View at Publisher · View at Google Scholar · View at Scopus
  79. P. Zürbig, G. Jerums, P. Hovind et al., “Urinary proteomics for early diagnosis in diabetic nephropathy,” Diabetes, vol. 61, no. 12, pp. 3304–3313, 2012. View at Publisher · View at Google Scholar · View at Scopus
  80. A. Lewandowicz, M. Bakun, R. Kohutnicki et al., “Changes in urine proteome accompanying diabetic nephropathy progression,” Polskie Archiwum Medycyny Wewnetrznej, vol. 125, pp. 27–38, 2015. View at Google Scholar
  81. J. Barratt and J. Feehally, “IgA nephropathy,” Journal of the American Society of Nephrology, vol. 16, no. 7, pp. 2088–2097, 2005. View at Publisher · View at Google Scholar · View at Scopus
  82. B. A. Julian, S. Wittke, M. Haubitz et al., “Urinary biomarkers of IgA nephropathy and other IgA-associated renal diseases,” World Journal of Urology, vol. 25, no. 5, pp. 467–476, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. M. T. Rocchetti, M. Papale, A. M. d'Apollo et al., “Association of urinary laminin G-like 3 and free K light chains with disease activity and histological injury in IgA nephropathy,” Clinical Journal of the American Society of Nephrology, vol. 8, no. 7, pp. 1115–1125, 2013. View at Publisher · View at Google Scholar · View at Scopus
  84. B. A. Julian, S. Wittke, J. Novak et al., “Electrophoretic methods for analysis of urinary polypeptides in lgA-associated renal diseases,” Electrophoresis, vol. 28, no. 23, pp. 4469–4483, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. S. Zhao, R. Li, X. Cai et al., “The application of SILAC mouse in human body fluid proteomics analysis reveals protein patterns associated with IgA nephropathy,” Evidence-Based Complementary and Alternative Medicine, vol. 2013, Article ID 275390, 10 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  86. K. Mucha, M. Bakun, R. Jaźwiec et al., “Complement components, proteolysis-related, and cell communication-related proteins detected in urine proteomics are associated with IgA nephropathy,” Polskie Archiwum Medycyny Wewnetrznej, vol. 124, no. 7-8, pp. 380–386, 2014. View at Google Scholar · View at Scopus
  87. V. D. D'Agati, F. J. Kaskel, and R. J. Falk, “Focal segmental glomerulosclerosis,” The New England Journal of Medicine, vol. 365, no. 25, pp. 2398–2411, 2011. View at Publisher · View at Google Scholar · View at Scopus
  88. B. Bose and D. Cattran, “Glomerular diseases: FSGS,” Clinical Journal of the American Society of Nephrology, vol. 9, no. 3, pp. 626–632, 2014. View at Publisher · View at Google Scholar · View at Scopus
  89. C. Kitiyakara, J. B. Kopp, and P. Eggers, “Trends in the epidemiology of focal segmental glomerulosclerosis,” Seminars in Nephrology, vol. 23, no. 2, pp. 172–182, 2003. View at Publisher · View at Google Scholar · View at Scopus
  90. H.-A. Shui, T.-H. Huang, S.-M. Ka, P.-H. Chen, Y.-F. Lin, and A. Chen, “Urinary proteome and potential biomarkers associated with serial pathogenesis steps of focal segmental glomerulosclerosis,” Nephrology Dialysis Transplantation, vol. 23, no. 1, pp. 176–185, 2008. View at Publisher · View at Google Scholar · View at Scopus
  91. R. P. Woroniecki, T. N. Orlova, N. Mendelev et al., “Urinary proteome of steroid-sensitive and steroid-resistant idiopathic nephrotic syndrome of childhood,” American Journal of Nephrology, vol. 26, no. 3, pp. 258–267, 2006. View at Publisher · View at Google Scholar · View at Scopus
  92. M. Zhao, M. Li, X. Li, C. Shao, J. Yin, and Y. Gao, “Dynamic changes of urinary proteins in a focal segmental glomerulosclerosis rat model,” Proteome Science, vol. 12, article 42, 2014. View at Publisher · View at Google Scholar · View at Scopus
  93. T. Wu, C. Xie, H. W. Wang et al., “Elevated urinary VCAM-1, P-selectin, soluble TNF receptor-1, and CXC chemokine ligand 16 in multiple murine lupus strains and human lupus nephritis,” Journal of Immunology, vol. 179, no. 10, pp. 7166–7175, 2007. View at Publisher · View at Google Scholar · View at Scopus
  94. M. Suzuki, K. Wiers, E. B. Brooks et al., “Initial validation of a novel protein biomarker panel for active pediatric lupus nephritis,” Pediatric Research, vol. 65, no. 5, pp. 530–536, 2009. View at Publisher · View at Google Scholar · View at Scopus
  95. R. F. Rosa, K. Takei, N. C. Araújo, S. M. A. Loduca, J. C. M. Szajubok, and W. H. Chahade, “Monocyte chemoattractant-1 as a urinary biomarker for the diagnosis of activity of lupus nephritis in Brazilian patients,” The Journal of Rheumatology, vol. 39, no. 10, pp. 1948–1954, 2012. View at Publisher · View at Google Scholar · View at Scopus
  96. Z. Xuejing, T. Jiazhen, L. Jun, X. Xiangqing, Y. Shuguang, and L. Fuyou, “Urinary TWEAK level as a marker of lupus nephritis activity in 46 cases,” Journal of Biomedicine and Biotechnology, vol. 2012, Article ID 359647, 7 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  97. P. Lee, H. Peng, T. Gelbart, L. Wang, and E. Beutler, “Regulation of hepcidin transcription by interleukin-1 and interleukin-6,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 6, pp. 1906–1910, 2005. View at Publisher · View at Google Scholar · View at Scopus
  98. K. Mosley, F. W. K. Tam, R. J. Edwards, J. Crozier, C. D. Pusey, and L. Lightstone, “Urinary proteomic profiles distinguish between active and inactive lupus nephritis,” Rheumatology, vol. 45, no. 12, pp. 1497–1504, 2006. View at Publisher · View at Google Scholar · View at Scopus
  99. J. C. Oates, S. Varghese, A. M. Bland et al., “Prediction of urinary protein markers in lupus nephritis,” Kidney International, vol. 68, no. 6, pp. 2588–2592, 2005. View at Publisher · View at Google Scholar · View at Scopus
  100. W. Sui, R. Zhang, J. Chen et al., “Comparative proteomic analysis of membranous nephropathy biopsy tissues using quantitative proteomics,” Experimental and Therapeutic Medicine, vol. 9, no. 3, pp. 805–810, 2015. View at Publisher · View at Google Scholar · View at Scopus
  101. L. H. Beck Jr. and D. J. Salant, “Membranous nephropathy: forms models to man,” Journal of Clinical Investigation, vol. 124, no. 6, pp. 2307–2314, 2014. View at Publisher · View at Google Scholar · View at Scopus
  102. L. H. Beck Jr. and D. J. Salant, “Membranous nephropathy: recent travels and new roads ahead,” Kidney International, vol. 77, no. 9, pp. 765–770, 2010. View at Publisher · View at Google Scholar · View at Scopus
  103. H. H.-Y. Ngai, W.-H. Sit, P.-P. Jiang, R.-J. Xu, J. M.-F. Wan, and V. Thongboonkerd, “Serial changes in urinary proteome profile of membranous nephropathy: implications for pathophysiology and biomarker discovery,” Journal of Proteome Research, vol. 5, no. 11, pp. 3038–3047, 2006. View at Publisher · View at Google Scholar · View at Scopus
  104. I. M. Rood, M. L. Merchant, D. W. Wilkey et al., “Increased expression of lysosome membrane protein 2 in glomeruli of patients with idiopathic membranous nephropathy,” Proteomics, vol. 15, no. 21, pp. 3722–3730, 2015. View at Publisher · View at Google Scholar
  105. P. Ruggenenti, C. Chiurchiu, V. Brusegan et al., “Rituximab in idiopathic membranous nephropathy: a one-year prospective study,” Journal of the American Society of Nephrology, vol. 14, no. 7, pp. 1851–1857, 2003. View at Publisher · View at Google Scholar · View at Scopus
  106. M. V. Irazabal, A. Eirin, J. Lieske et al., “Low-and high-molecular-weight urinary proteins as predictors of response to rituximab in patients with membranous nephropathy: a prospective study,” Nephrology Dialysis Transplantation, vol. 28, no. 1, pp. 137–146, 2013. View at Publisher · View at Google Scholar · View at Scopus
  107. R. L. Mehta, J. A. Kellum, S. V. Shah et al., “Acute kidney injury network: report of an initiative to improve outcomes in acute kidney injury,” Critical Care, vol. 11, article R31, 2007. View at Publisher · View at Google Scholar · View at Scopus
  108. S. Herget-Rosenthal, J. Metzger, A. Albalat, V. Bitsika, and H. Mischak, “Proteomic biomarkers for the early detection of acute kidney injury,” Prilozi, vol. 33, pp. 27–48, 2012. View at Google Scholar
  109. M. T. Nguyen, G. F. Ross, C. L. Dent, and P. Devarajan, “Early prediction of acute renal injury using urinary proteomics,” American Journal of Nephrology, vol. 25, no. 4, pp. 318–326, 2005. View at Publisher · View at Google Scholar · View at Scopus
  110. M. T. Nguyen, C. L. Dent, G. F. Ross et al., “Urinary aprotinin as a predictor of acute kidney injury after cardiac surgery in children receiving aprotinin therapy,” Pediatric Nephrology, vol. 23, no. 8, pp. 1317–1326, 2008. View at Publisher · View at Google Scholar · View at Scopus
  111. J. Metzger, T. Kirsch, E. Schiffer et al., “Urinary excretion of twenty peptides forms an early and accurate diagnostic pattern of acute kidney injury,” Kidney International, vol. 78, no. 12, pp. 1252–1262, 2010. View at Publisher · View at Google Scholar · View at Scopus
  112. F. Aregger, C. Pilop, D. E. Uehlinger et al., “Urinary proteomics before and after extracorporeal circulation in patients with and without acute kidney injury,” Journal of Thoracic and Cardiovascular Surgery, vol. 139, no. 3, pp. 692–700, 2010. View at Publisher · View at Google Scholar · View at Scopus
  113. F. Aregger, D. E. Uehlinger, J. Witowski et al., “Identification of IGFBP-7 by urinary proteomics as a novel prognostic marker in early acute kidney injury,” Kidney International, vol. 85, no. 4, pp. 909–919, 2014. View at Publisher · View at Google Scholar · View at Scopus
  114. M. Bell, A. Larsson, P. Venge, R. Bellomo, and J. Mårtensson, “Assessment of cell-cycle arrest biomarkers to predict early and delayed acute kidney injury,” Disease Markers, vol. 2015, Article ID 158658, 9 pages, 2015. View at Publisher · View at Google Scholar
  115. Y. Zhang, Y. Zhang, J. Adachi et al., “MAPU: max-planck unified database of organellar, cellular, tissue and body fluid proteomes,” Nucleic Acids Research, vol. 35, supplement 1, pp. D771–D779, 2007. View at Publisher · View at Google Scholar · View at Scopus
  116. S.-J. Li, M. Peng, H. Li et al., “Sys-BodyFluid: a systematical database for human body fluid proteome research,” Nucleic Acids Research, vol. 37, supplement 1, pp. D907–D912, 2009. View at Publisher · View at Google Scholar · View at Scopus
  117. J. Siwy, W. Mullen, I. Golovko, J. Franke, and P. Zürbig, “Human urinary peptide database for multiple disease biomarker discovery,” Proteomics—Clinical Applications, vol. 5, no. 5-6, pp. 367–374, 2011. View at Publisher · View at Google Scholar · View at Scopus
  118. T. M. Shiju, V. Mohan, M. Balasubramanyam, and P. Viswanathan, “Soluble CD36 in plasma and urine: a plausible prognostic marker for diabetic nephropathy,” Journal of Diabetes and its Complications, vol. 29, pp. 400–406, 2015. View at Publisher · View at Google Scholar · View at Scopus
  119. J. Ma, X. Chen, J.-S. Li et al., “Upregulation of podocyte-secreted angiopoietin-like-4 in diabetic nephropathy,” Endocrine, vol. 49, no. 2, pp. 373–384, 2014. View at Publisher · View at Google Scholar · View at Scopus
  120. A. Caseiro, A. Barros, R. Ferreira et al., “Pursuing type 1 diabetes mellitus and related complications through urinary proteomics,” Translational Research, vol. 163, no. 3, pp. 188–199, 2014. View at Publisher · View at Google Scholar · View at Scopus
  121. I. Zubiri, M. Posada-Ayala, A. Sanz-Maroto et al., “Diabetic nephropathy induces changes in the proteome of human urinary exosomes as revealed by label-free comparative analysis,” Journal of Proteomics, vol. 96, pp. 92–102, 2014. View at Publisher · View at Google Scholar · View at Scopus
  122. K. Inoue, J. Wada, J. Eguchi et al., “Urinary Fetuin-A is a novel marker for diabetic nephropathy in type 2 diabetes identified by lectin microarray,” PLoS ONE, vol. 8, no. 10, Article ID e77118, 2013. View at Publisher · View at Google Scholar · View at Scopus
  123. B. Surin, E. Sachon, J.-P. Rougier et al., “LG3 fragment of endorepellin is a possible biomarker of severity in IgA nephropathy,” Proteomics, vol. 13, no. 1, pp. 142–152, 2013. View at Publisher · View at Google Scholar · View at Scopus
  124. J. Lopez-Hellin, C. Cantarell, L. Jimeno et al., “A form of apolipoprotein A-I is found specifically in relapses of focal segmental glomerulosclerosis following transplantation,” American Journal of Transplantation, vol. 13, no. 2, pp. 493–500, 2013. View at Publisher · View at Google Scholar · View at Scopus
  125. N. Piyaphanee, Q. Ma, O. Kremen et al., “Discovery and initial validation of α1-B glycoprotein fragmentation as a differential urinary biomarker in pediatric steroid-resistant nephrotic syndrome,” Proteomics—Clinical Applications, vol. 5, no. 5-6, pp. 334–342, 2011. View at Publisher · View at Google Scholar · View at Scopus
  126. E. O. Honkanen, A.-M. Teppo, and C. Grönhagen-Riska, “Decreased urinary excretion of vascular endothelial growth factor in idiopathic membranous glomerulonephritis,” Kidney International, vol. 57, no. 6, pp. 2343–2349, 2000. View at Publisher · View at Google Scholar · View at Scopus
  127. A. J. W. Branten, P. W. du Buf-Vereijken, I. S. Klasen et al., “Urinary excretion of beta2-microglobulin and IgG predict prognosis in idiopathic membranous nephropathy: a validation study,” Journal of the American Society of Nephrology, vol. 16, no. 1, pp. 169–174, 2005. View at Publisher · View at Google Scholar · View at Scopus
  128. T. Nakatsue, H. Koike, G. D. Han et al., “Nephrin and podocin dissociate at the onset of proteinuria in experimental membranous nephropathy,” Kidney International, vol. 67, no. 6, pp. 2239–2253, 2005. View at Publisher · View at Google Scholar · View at Scopus
  129. C. R. Parikh, J. Mishra, H. Thiessen-Philbrook et al., “Urinary IL-18 is an early predictive biomarker of acute kidney injury after cardiac surgery,” Kidney International, vol. 70, no. 1, pp. 199–203, 2006. View at Publisher · View at Google Scholar · View at Scopus
  130. W. K. Han, G. Wagener, Y. Zhu, S. Wang, and H. T. Lee, “Urinary biomarkers in the early detection of acute kidney injury after cardiac surgery,” Clinical Journal of the American Society of Nephrology, vol. 4, no. 5, pp. 873–882, 2009. View at Publisher · View at Google Scholar · View at Scopus
  131. J. Mishra, C. Dent, R. Tarabishi et al., “Neutrophil gelatinase-associated lipocalin (NGAL) as a biomarker for acute renal injury after cardiac surgery,” The Lancet, vol. 365, no. 9466, pp. 1231–1238, 2005. View at Publisher · View at Google Scholar · View at Scopus
  132. V. S. Vaidya, V. Ramirez, T. Ichimura, N. A. Bobadilla, and J. V. Bonventre, “Urinary kidney injury molecule-1: a sensitive quantitative biomarker for early detection of kidney tubular injury,” The American Journal of Physiology—Renal Physiology, vol. 290, no. 2, pp. F517–F529, 2006. View at Publisher · View at Google Scholar · View at Scopus
  133. G. Ramesh, C. D. Krawczeski, J. G. Woo, Y. Wang, and P. Devarajan, “Urinary netrin-1 is an early predictive biomarker of acute kidney injury after cardiac surgery,” Clinical Journal of the American Society of Nephrology, vol. 5, no. 3, pp. 395–401, 2010. View at Publisher · View at Google Scholar · View at Scopus
  134. P. Devarajan, C. D. Krawczeski, M. T. Nguyen, T. Kathman, Z. Wang, and C. R. Parikh, “Proteomic identification of early biomarkers of acute kidney injury after cardiac surgery in children,” American Journal of Kidney Diseases, vol. 56, no. 4, pp. 632–642, 2010. View at Publisher · View at Google Scholar · View at Scopus
  135. L. E. Morales-Buenrostro, O. I. Salas-Nolasco, J. Barrera-Chimal et al., “Hsp72 is a novel biomarker to predict acute kidney injury in critically ill patients,” PLoS ONE, vol. 9, no. 10, Article ID e109407, 2014. View at Publisher · View at Google Scholar