Role of Kidney Biopsies for Biomarker Discovery in Diabetic Kidney Disease

National Kidney Foundation, 2012, KDOQI clinical practice guidelines for diabetes and CKD: 2012 update, Am J Kidney Dis, 60, 850, 10.1053/j.ajkd.2012.07.005 Steinke, 2005, The early natural history of nephropathy in Type 1 Diabetes: III. Predictors of 5-year urinary albumin excretion rate patterns in initially normoalbuminuric patients, Diabetes, 54, 2164, 10.2337/diabetes.54.7.2164 Perrin, 2010, Risk markers of future microalbuminuria and hypertension based on clinical and morphological parameters in young type 1 diabetes patients, Pediatr Diabetes, 11, 305, 10.1111/j.1399-5448.2009.00595.x Caramori, 2013, Renal lesions predict progression of diabetic nephropathy in type 1 diabetes, J Am Soc Nephrol, 24, 1175, 10.1681/ASN.2012070739 Bader, 1980, Structure and function of the kidney in diabetic glomerulosclerosis. Correlations between morphological and functional parameters, Pathol Res Pract, 167, 204, 10.1016/S0344-0338(80)80051-3 Gilbert, 1999, The tubulointerstitium in progressive diabetic kidney disease: more than an aftermath of glomerular injury?, Kidney Int, 56, 1627, 10.1046/j.1523-1755.1999.00721.x Phillips, 2002, Diabetic nephropathy: the central role of renal proximal tubular cells in tubulointerstitial injury, Histol Histopathol, 17, 247 Molitch, 2010, Development and progression of renal insufficiency with and without albuminuria in adults with type 1 diabetes in the diabetes control and complications trial and the epidemiology of diabetes interventions and complications study, Diabetes Care, 33, 1536, 10.2337/dc09-1098 Retnakaran, 2006, Risk factors for renal dysfunction in type 2 diabetes: U.K. Prospective Diabetes Study 74, Diabetes, 55, 1832, 10.2337/db05-1620 Parving, 2006, Prevalence and risk factors for microalbuminuria in a referred cohort of type II diabetic patients: a global perspective, Kidney Int, 69, 2057, 10.1038/sj.ki.5000377 Thomas, 2009, Nonalbuminuric renal impairment in type 2 diabetic patients and in the general population (national evaluation of the frequency of renal impairment cO-existing with NIDDM [NEFRON] 11), Diabetes Care, 32, 1497, 10.2337/dc08-2186 Perkins, 2003, Regression of microalbuminuria in type 1 diabetes, N Engl J Med, 348, 2285, 10.1056/NEJMoa021835 Forsblom, 1992, Predictive value of microalbuminuria in patients with insulin-dependent diabetes of long duration, BMJ, 305, 1051, 10.1136/bmj.305.6861.1051 Caramori, 2006, Enhancing the predictive value of urinary albumin for diabetic nephropathy, J Am Soc Nephrol, 17, 339, 10.1681/ASN.2005101075 Ju, 2015, Tissue transcriptome-driven identification of epidermal growth factor as a chronic kidney disease biomarker, Sci Transl Med, 7, 316ra193, 10.1126/scitranslmed.aac7071 Van, 2017, Insights into diabetic kidney disease using urinary proteomics and bioinformatics, J Am Soc Nephrol, 28, 1050, 10.1681/ASN.2016091018 Chung, 2015, microRNAs in diabetic kidney disease, 253 Simpson, 2016, MicroRNAs in diabetic nephropathy: from biomarkers to therapy, Curr Diab Rep, 16, 35, 10.1007/s11892-016-0724-8 Argyropoulos, 2015, Urinary microRNA profiling predicts the development of microalbuminuria in patients with type 1 diabetes, J Clin Med, 4, 1498, 10.3390/jcm4071498 Argyropoulos, 2013, Urinary microRNA profiling in the nephropathy of type 1 diabetes, PLoS One, 8, e54662, 10.1371/journal.pone.0054662 Caramori, 2015, Differential response to high glucose in skin fibroblasts of monozygotic twins discordant for type 1 diabetes, J Clin Endocrinol Metab, 100, E883, 10.1210/jc.2014-4467 Caramori, 2015, Differential gene expression in diabetic nephropathy in individuals with type 1 diabetes, J Clin Endocrinol Metab, 100, E876, 10.1210/jc.2014-4465 Reddy, 2015, Epigenetic mechanisms in diabetic complications and metabolic memory, Diabetologia, 58, 443, 10.1007/s00125-014-3462-y Mazzucco, 2002, Different patterns of renal damage in type 2 diabetes mellitus: a multicentric study on 393 biopsies, Am J Kidney Dis, 39, 713, 10.1053/ajkd.2002.31988 Kidney Disease, 2013, KDIGO 2012 clinical practice guideline for the evaluation and management of chronic kidney disease. Chapter 1: Definition and classification of CKD, Kidney Int Suppl, 3, 19 Kidney Disease, 2013, Improving Global Outcomes (KDIGO) CKD Work Group. KDIGO 2012 clinical practice guideline for the evaluation and management of chronic kidney disease. Chapter 2: Definition, identification, and prediction of CKD progression, Kidney Int Suppl, 3, 63 National Kidney Foundation, 2007, KDOQI clinical practice guidelines and clinical practice recommendations for diabetes and chronic kidney disease, Am J Kidney Dis, 49, S12 Bell, 2015, End-stage renal disease and survival in people with diabetes: a national database linkage study, QJM, 108, 127, 10.1093/qjmed/hcu170 Caramori, 2003, Low glomerular filtration rate in normoalbuminuric type 1 diabetic patients: an indicator of more advanced glomerular lesions, Diabetes, 52, 1036, 10.2337/diabetes.52.4.1036 Porrini, 2015, Non-proteinuric pathways in loss of renal function in patients with type 2 diabetes, Lancet Diabetes Endocrinol, 3, 382, 10.1016/S2213-8587(15)00094-7 Pagtalunan, 1997, Podocyte loss and progressive glomerular injury in type II diabetes, J Clin Invest, 99, 342, 10.1172/JCI119163 Tonneijck, 2017, Glomerular hyperfiltration in diabetes: mechanisms, clinical significance, and treatment, J Am Soc Nephrol, 28, 1023, 10.1681/ASN.2016060666 Magee, 2009, Is hyperfiltration associated with the future risk of developing diabetic nephropathy? A meta-analysis, Diabetologia, 52, 691, 10.1007/s00125-009-1268-0 Ruggenenti, 2012, Glomerular hyperfiltration and renal disease progression in type 2 diabetes, Diabetes Care, 35, 2061, 10.2337/dc11-2189 Mauer, 2015, Glomerular structural-functional relationship models of diabetic nephropathy are robust in type 1 diabetic patients, Nephrol Dial Transpl, 30, 918, 10.1093/ndt/gfu279 Mauer, 1984, Structural-functional relationships in diabetic nephropathy, J Clin Invest, 74, 1143, 10.1172/JCI111523 Drummond, 2002, The early natural history of nephropathy in type 1 diabetes: II. Early renal structural changes in type 1 diabetes, Diabetes, 51, 1580, 10.2337/diabetes.51.5.1580 Beisswenger, 2005, Susceptibility to diabetic nephropathy is related to dicarbonyl and oxidative stress, Diabetes, 54, 3274, 10.2337/diabetes.54.11.3274 Beisswenger, 2013, Early progression of diabetic nephropathy correlates with methylglyoxal-derived advanced glycation end products, Diabetes Care, 36, 3234, 10.2337/dc12-2689 Beisswenger, 2014, Detection of diabetic nephropathy from advanced glycation endproducts (AGEs) differs in plasma and urine, and is dependent on the method of preparation, Amino Acids, 46, 311, 10.1007/s00726-013-1533-x Saulnier, 2016, Advanced glycation end products predict loss of renal function and correlate with lesions of diabetic kidney disease in American Indians with type 2 diabetes, Diabetes, 65, 3744, 10.2337/db16-0310 Uslu, 2005, Serum cystatin C and urinary enzymes as screening markers of renal dysfunction in diabetic patients, J Nephrol, 18, 559 Wheelock, 2017, Plasma bradykinin and early diabetic nephropathy lesions in type 1 diabetes mellitus, PLoS One, 12, e0180964, 10.1371/journal.pone.0180964 Fufaa, 2016, Structural predictors of loss of renal function in American Indians with type 2 diabetes, Clin J Am Soc Nephrol, 11, 254, 10.2215/CJN.05760515 Pavkov, 2016, Tumor necrosis factor receptors 1 and 2 are associated with early glomerular lesions in type 2 diabetes, Kidney Int, 89, 226, 10.1038/ki.2015.278 Wheelock, 2017, White blood cell fractions correlate with lesions of diabetic kidney disease and predict loss of kidney function in type 2 diabetes [published online July 18, 2017], Nephrol Dial Transplant, 10.1093/ndt/gfx303 Krolewski, 2014, Early progressive renal decline precedes the onset of microalbuminuria and its progression to macroalbuminuria, Diabetes Care, 37, 226, 10.2337/dc13-0985 Looker, 2015, Biomarkers of rapid chronic kidney disease progression in type 2 diabetes, Kidney Int, 88, 888, 10.1038/ki.2015.199 Gohda, 2012, Circulating TNF receptors 1 and 2 predict stage 3 CKD in type 1 diabetes, J Am Soc Nephrol, 23, 516, 10.1681/ASN.2011060628 Pavkov, 2015, Elevation of circulating TNF receptors 1 and 2 increases the risk of end-stage renal disease in American Indians with type 2 diabetes, Kidney Int, 87, 812, 10.1038/ki.2014.330 Looker, 2017, Reading the tree leaves-how to enrich clinical trials of diabetic kidney disease, Kidney Int, 92, 23, 10.1016/j.kint.2017.03.042 Vielhauer, 2005, Renal cell-expressed TNF receptor 2, not receptor 1, is essential for the development of glomerulonephritis, J Clin Invest, 115, 1199, 10.1172/JCI200523348 Locksley, 2001, The TNF and TNF receptor superfamilies: integrating mammalian biology, Cell, 104, 487, 10.1016/S0092-8674(01)00237-9 Mauer, 2009, Renal and retinal effects of enalapril and losartan in type 1 diabetes, N Engl J Med, 361, 40, 10.1056/NEJMoa0808400 Horie, 1997, Immunohistochemical colocalization of glycoxidation products and lipid peroxidation products in diabetic renal glomerular lesions. Implication for glycoxidative stress in the pathogenesis of diabetic nephropathy, J Clin Invest, 100, 2995, 10.1172/JCI119853 Zhou, 2004, Advanced glycation end-products induce connective tissue growth factor-mediated renal fibrosis predominantly through transforming growth factor beta-independent pathway, Am J Pathol, 165, 2033, 10.1016/S0002-9440(10)63254-3 Wolkow, 2008, Association of urinary inflammatory markers and renal decline in microalbuminuric type 1 diabetics, J Am Soc Nephrol, 19, 789, 10.1681/ASN.2007050556 Titan, 2012, Urinary MCP-1 and RBP: independent predictors of renal outcome in macroalbuminuric diabetic nephropathy, J Diabetes Complications, 26, 546, 10.1016/j.jdiacomp.2012.06.006 Verhave, 2013, Clinical value of inflammatory urinary biomarkers in overt diabetic nephropathy: a prospective study, Diabetes Res Clin Pract, 101, 333, 10.1016/j.diabres.2013.07.006 Tomita, 2012, The kallikrein-kinin system in diabetic nephropathy, Kidney Int, 81, 733, 10.1038/ki.2011.499 Merchant, 2013, Plasma kininogen and kininogen fragments are biomarkers of progressive renal decline in type 1 diabetes, Kidney Int, 83, 1177, 10.1038/ki.2013.8 Ahluwalia, 1996, Involvement of bradykinin B1 receptors in the polymorphonuclear leukocyte accumulation induced by IL-1 beta in vivo in the mouse, J Immunol, 156, 269, 10.4049/jimmunol.156.1.269 Bockmann, 2000, Kinins and kinin receptors: importance for the activation of leukocytes, J Leukoc Biol, 68, 587, 10.1189/jlb.68.5.587 Furchgott, 1989, Endothelium-derived relaxing and contracting factors, FASEB J, 3, 2007, 10.1096/fasebj.3.9.2545495 Hong, 1980, Effect of bradykinin and thrombin on prostacyclin synthesis in endothelial cells from calf and pig aorta and human umbilical cord vein, Thromb Res, 18, 787, 10.1016/0049-3848(80)90201-7 Tong, 2004, White blood cell count is associated with macro- and microvascular complications in Chinese patients with type 2 diabetes, Diabetes Care, 27, 216, 10.2337/diacare.27.1.216 Vozarova, 2002, High white blood cell count is associated with a worsening of insulin sensitivity and predicts the development of type 2 diabetes, Diabetes, 51, 455, 10.2337/diabetes.51.2.455 Lim, 2012, Inflammation in diabetic nephropathy, Mediators Inflamm, 2012, 146154, 10.1155/2012/146154 Pertynska-Marczewska, 2004, Advanced glycation end products upregulate angiogenic and pro-inflammatory cytokine production in human monocyte/macrophages, Cytokine, 28, 35, 10.1016/j.cyto.2004.06.006 Shurtz-Swirski, 2001, Involvement of peripheral polymorphonuclear leukocytes in oxidative stress and inflammation in type 2 diabetic patients, Diabetes Care, 24, 104, 10.2337/diacare.24.1.104 Inker, 2017, Filtration markers as predictors of ESRD and mortality: individual participant data meta-analysis, Clin J Am Soc Nephrol, 12, 69, 10.2215/CJN.03660316 Schardijn, 1987, Beta 2-microglobulin: its significance in the evaluation of renal function, Kidney Int, 32, 635, 10.1038/ki.1987.255 Zhou, 2016, Are urinary tubular injury markers useful in chronic kidney disease? A systematic review and meta analysis, PLoS One, 11, e0167334, 10.1371/journal.pone.0167334 Nauta, 2011, Glomerular and tubular damage markers are elevated in patients with diabetes, Diabetes Care, 34, 975, 10.2337/dc10-1545 Papale, 2010, Urine proteome analysis may allow noninvasive differential diagnosis of diabetic nephropathy, Diabetes Care, 33, 2409, 10.2337/dc10-0345 Rebholz, 2017, Risk of ESRD and mortality associated with change in filtration markers, Am J Kidney Dis, 70, 551, 10.1053/j.ajkd.2017.04.025 Mise, 2016, Prognostic value of tubulointerstitial lesions, urinary N-acetyl-beta-d-glucosaminidase, and urinary beta2-microglobulin in patients with type 2 diabetes and biopsy-proven diabetic nephropathy, Clin J Am Soc Nephrol, 11, 593, 10.2215/CJN.04980515 Sabbisetti, 2014, Blood kidney injury molecule-1 is a biomarker of acute and chronic kidney injury and predicts progression to ESRD in type I diabetes, J Am Soc Nephrol, 25, 2177, 10.1681/ASN.2013070758 Coca, 2017, Plasma biomarkers and kidney function decline in early and established diabetic kidney disease, J Am Soc Nephrol, 28, 2786, 10.1681/ASN.2016101101 Baker, 2017, Tissue-specific microRNA expression patterns in four types of kidney disease, J Am Soc Nephrol, 28, 2985, 10.1681/ASN.2016121280 Bijkerk, 2015, Circulating microRNAs associate with diabetic nephropathy and systemic microvascular damage and normalize after simultaneous pancreas-kidney transplantation, Am J Transplant, 15, 1081, 10.1111/ajt.13072 Bhatt, 2016, Mini-review: emerging roles of microRNAs in the pathophysiology of renal diseases, Am J Physiol Renal Physiol, 310, F109, 10.1152/ajprenal.00387.2015 Ko, 2013, Cytosine methylation changes in enhancer regions of core pro-fibrotic genes characterize kidney fibrosis development, Genome Biol, 14, R108, 10.1186/gb-2013-14-10-r108 Siegfried, 1999, DNA methylation represses transcription in vivo, Nat Genet, 22, 203, 10.1038/9727 Yang, 2016, A study on the correlation between MTHFR promoter methylation and diabetic nephropathy, Am J Transl Res, 8, 4960 Aldemir, 2017, The association between methylation levels of targeted genes and albuminuria in patients with early diabetic kidney disease, Ren Fail, 39, 597, 10.1080/0886022X.2017.1358180 Leung, 2017, Could MRI be used to image kidney fibrosis? A review of recent advances and remaining barriers, Clin J Am Soc Nephrol, 12, 1019, 10.2215/CJN.07900716 Li, 2017, Recent advances in magnetic resonance imaging assessment of renal fibrosis, Adv Chronic Kidney Dis, 24, 150, 10.1053/j.ackd.2017.03.005 Zhao, 2014, Assessment of renal fibrosis in chronic kidney disease using diffusion-weighted MRI, Clin Radiol, 69, 1117, 10.1016/j.crad.2014.06.011 Inoue, 2011, Noninvasive evaluation of kidney hypoxia and fibrosis using magnetic resonance imaging, J Am Soc Nephrol, 22, 1429, 10.1681/ASN.2010111143 Ogawa, 1990, Brain magnetic resonance imaging with contrast dependent on blood oxygenation, Proc Natl Acad Sci U S A, 87, 9868, 10.1073/pnas.87.24.9868 Muthupillai, 1995, Magnetic resonance elastography by direct visualization of propagating acoustic strain waves, Science, 269, 1854, 10.1126/science.7569924 Lee, 2012, MR elastography in renal transplant patients and correlation with renal allograft biopsy: a feasibility study, Acad Radiol, 19, 834, 10.1016/j.acra.2012.03.003 Morrell, 2017, Magnetic resonance imaging of the fibrotic kidney, J Am Soc Nephrol, 28, 2564, 10.1681/ASN.2016101089