Serum biomarkers for diagnosis and prediction of type 1 diabetes

Yi, Lian; Swensen, Adam C.; Qian, Wei -Jun

doi:10.1016/j.trsl.2018.07.009

Title: Serum biomarkers for diagnosis and prediction of type 1 diabetes

Journal Article · Wed Aug 01 00:00:00 EDT 2018 · Translational Research

DOI:https://doi.org/10.1016/j.trsl.2018.07.009· OSTI ID:1464493

Yi, Lian ^[1]; Swensen, Adam C. ^[1]; Qian, Wei -Jun ^[1]

Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

Here, Type 1 diabetes (T1D) culminates in the autoimmune destruction of the pancreatic β-cells, leading to insufficient production of insulin and development of hyperglycemia. Serum biomarkers including a combination of glucose, glycated molecules, c-peptide, and autoantibodies have been well established for the diagnosis of T1D. However, these molecules often mark a late stage of the disease when ~90% of the pancreatic insulin-producing β-cells have already been lost. With the prevalence of T1D increasing worldwide and because of the physical and psychological burden induced by this disease, there is a great need for prognostic biomarkers to predict T1D development or progression. This would allow us to identify individuals at high risk for early prevention and intervention. Therefore, considerable efforts have been dedicated to the understanding of disease etiology and the discovery of novel biomarkers in the last few decades. The advent of high-throughput and sensitive ‘-omics’ technologies for the study of proteins, nucleic acids, and metabolites have allowed large scale profiling of protein expression and gene changes in T1D patients relative to disease-free controls. In this review, we briefly discuss the classical diagnostic biomarkers of T1D but mainly focus on the novel biomarkers that are identified as markers of β-cell destruction and screened with the use of state-of-the-art ‘-omics’ technologies.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: DP3 DK110844; UC4 DK104167; AC05-76RL01830

OSTI ID:: 1464493

Report Number(s):: PNNL-SA-134879; PII: S1931524418301105

Journal Information:: Translational Research, Vol. 201; ISSN 1931-5244

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 29 works

Citation information provided by
Web of Science

References (131)

Type I Diabetes Mellitus Flier, Jeffrey S.; Underhill, Lisa H.; Eisenbarth, George S. New England Journal of Medicine, Vol. 314, Issue 21 https://doi.org/10.1056/NEJM198605223142106	journal	May 1986
Targeted immune interventions for type 1 diabetes: not as easy as it looks! Rigby, Mark R.; Ehlers, Mario R. Current Opinion in Endocrinology & Diabetes and Obesity, Vol. 21, Issue 4 https://doi.org/10.1097/MED.0000000000000075	journal	January 2014
Epidemiology of Type 1 Diabetes Maahs, David M.; West, Nancy A.; Lawrence, Jean M. Endocrinology and Metabolism Clinics of North America, Vol. 39, Issue 3 https://doi.org/10.1016/j.ecl.2010.05.011	journal	September 2010
Type 1 diabetes mellitus Katsarou, Anastasia; Gudbjörnsdottir, Soffia; Rawshani, Araz Nature Reviews Disease Primers, Vol. 3, Issue 1 https://doi.org/10.1038/nrdp.2017.16	journal	March 2017
Factors affecting the level of burden of caregivers of children with type 1 diabetes Kobos, Ewa; Imiela, Jacek Applied Nursing Research, Vol. 28, Issue 2 https://doi.org/10.1016/j.apnr.2014.09.008	journal	May 2015
Perceived family burden and emotional distress: similarities and differences between mothers and fathers of children with type 1 diabetes in a population-based study Haugstvedt, Anne; Wentzel-Larsen, Tore; Rokne, Berit Pediatric Diabetes, Vol. 12, Issue 2 https://doi.org/10.1111/j.1399-5448.2010.00661.x	journal	February 2011
Proteomic Technologies for the Discovery of Type 1 Diabetes Biomarkers Zhi, Wenbo; Purohit, Sharad; Carey, Colleen Journal of Diabetes Science and Technology, Vol. 4, Issue 4 https://doi.org/10.1177/193229681000400431	journal	July 2010
-Cell Mass and Turnover in Humans: Effects of obesity and aging Saisho, Y.; Butler, A. E.; Manesso, E. Diabetes Care, Vol. 36, Issue 1 https://doi.org/10.2337/dc12-0421	journal	August 2012
Current Concepts on the Pathogenesis of Type 1 Diabetes—Considerations for Attempts to Prevent and Reverse the Disease Atkinson, Mark A.; von Herrath, Matthias; Powers, Alvin C. Diabetes Care, Vol. 38, Issue 6 https://doi.org/10.2337/dc15-0144	journal	May 2015
Diabetes Antibody Standardization Program: evaluation of assays for autoantibodies to glutamic acid decarboxylase and islet antigen-2 Törn, C.; Mueller, P. W.; Schlosser, M. Diabetologia, Vol. 51, Issue 5 https://doi.org/10.1007/s00125-008-0967-2	journal	March 2008
Diabetes Antibody Standardization Program: evaluation of assays for insulin autoantibodies Schlosser, M.; Mueller, P. W.; Törn, C. Diabetologia, Vol. 53, Issue 12 https://doi.org/10.1007/s00125-010-1915-5	journal	September 2010
Diabetes Antibody Standardization Program: Table 1: First evaluation of assays for autoantibodies to IA-2β Schlosser, Michael; Mueller, Patricia W.; Achenbach, Peter Diabetes Care, Vol. 34, Issue 11 https://doi.org/10.2337/dc11-1161	journal	September 2011
Diabetes Antibody Standardization Program: First Proficiency Evaluation of Assays for Autoantibodies to Zinc Transporter 8 Lampasona, Vito; Schlosser, Michael; Mueller, Patricia W. Clinical Chemistry, Vol. 57, Issue 12 https://doi.org/10.1373/clinchem.2011.170662	journal	December 2011
Guidelines and Recommendations for Laboratory Analysis in the Diagnosis and Management of Diabetes Mellitus Sacks, David B.; Bruns, David E.; Goldstein, David E. Clinical Chemistry, Vol. 48, Issue 3 https://doi.org/10.1093/clinchem/48.3.436	journal	March 2002
Seroconversion to Multiple Islet Autoantibodies and Risk of Progression to Diabetes in Children Ziegler, Anette G.; Rewers, Marian; Simell, Olli JAMA, Vol. 309, Issue 23 https://doi.org/10.1001/jama.2013.6285	journal	June 2013
Normal weight promotes remission and low number of islet antibodies prolong the duration of remission in Type 1 diabetes Scholin, A.; Torn, C.; Nystrom, L. Diabetic Medicine, Vol. 21, Issue 5 https://doi.org/10.1111/j.1464-5491.2004.01175.x	journal	May 2004
A Practical Review of C-Peptide Testing in Diabetes Leighton, Emma; Sainsbury, Christopher AR; Jones, Gregory C. Diabetes Therapy, Vol. 8, Issue 3 https://doi.org/10.1007/s13300-017-0265-4	journal	May 2017
Preserved C-peptide levels in overweight or obese compared with underweight children upon diagnosis of type 1 diabetes mellitus Yu, Hyeoh Won; Lee, Yun Jeong; Cho, Won Im Annals of Pediatric Endocrinology & Metabolism, Vol. 20, Issue 2 https://doi.org/10.6065/apem.2015.20.2.92	journal	January 2015
C-Peptide Is the Appropriate Outcome Measure for Type 1 Diabetes Clinical Trials to Preserve -Cell Function: Report of an ADA Workshop, 21-22 October 2001 Palmer, J. P.; Fleming, G. A.; Greenbaum, C. J. Diabetes, Vol. 53, Issue 1 https://doi.org/10.2337/diabetes.53.1.250	journal	December 2003
Disease-associated Autoimmunity and Prevention of Insulin-dependent Diabetes Mellitus Knip, Mikael Annals of Medicine, Vol. 29, Issue 5 https://doi.org/10.3109/07853899708999375	journal	January 1997
Prediction of Type 1 Diabetes in the General Population Knip, M.; Korhonen, S.; Kulmala, P. Diabetes Care, Vol. 33, Issue 6 https://doi.org/10.2337/dc09-1040	journal	May 2010
Predicting Type 1 Diabetes Using Biomarkers Bonifacio, Ezio Diabetes Care, Vol. 38, Issue 6 https://doi.org/10.2337/dc15-0101	journal	May 2015
Primary islet autoantibody at initial seroconversion and autoantibodies at diagnosis of type 1 diabetes as markers of disease heterogeneity: ILONEN et al. Ilonen, Jorma; Lempainen, Johanna; Hammais, Anna Pediatric Diabetes, Vol. 19, Issue 2 https://doi.org/10.1111/pedi.12545	journal	June 2017
A novel approach for the analysis of longitudinal profiles reveals delayed progression to type 1 diabetes in a subgroup of multiple-islet-autoantibody-positive children Endesfelder, David; Hagen, Michael; Winkler, Christiane Diabetologia, Vol. 59, Issue 10 https://doi.org/10.1007/s00125-016-4050-0	journal	July 2016
Reversion of β-Cell Autoimmunity Changes Risk of Type 1 Diabetes: TEDDY Study Vehik, Kendra; Lynch, Kristian F.; Schatz, Desmond A. Diabetes Care, Vol. 39, Issue 9 https://doi.org/10.2337/dc16-0181	journal	June 2016
Islet Autoantibodies and Type 1 Diabetes: Does the Evidence Support Screening? Calderon, Boris; Sacks, David B. Clinical Chemistry, Vol. 60, Issue 3 https://doi.org/10.1373/clinchem.2013.212381	journal	March 2014
Mature high-affinity immune responses to (pro)insulin anticipate the autoimmune cascade that leads to type 1 diabetes Achenbach, Peter; Koczwara, Kerstin; Knopff, Annette Journal of Clinical Investigation, Vol. 114, Issue 4 https://doi.org/10.1172/JCI200421307	journal	August 2004
Clinical Applications of Diabetes Antibody Testing Bingley, Polly J. The Journal of Clinical Endocrinology & Metabolism, Vol. 95, Issue 1 https://doi.org/10.1210/jc.2009-1365	journal	January 2010
Autoimmune Markers in Diabetes Winter, William E.; Schatz, Desmond A. Clinical Chemistry, Vol. 57, Issue 2 https://doi.org/10.1373/clinchem.2010.148205	journal	February 2011
Novel Biomarkers in Type 1 Diabetes Jin, Yulan; She, Jin-Xiong The Review of Diabetic Studies, Vol. 9, Issue 4 https://doi.org/10.1900/RDS.2012.9.224	journal	January 2012
Prediction and Pathogenesis in Type 1 Diabetes Ziegler, Anette-G.; Nepom, Gerald T. Immunity, Vol. 32, Issue 4 https://doi.org/10.1016/j.immuni.2010.03.018	journal	April 2010
Primary Human and Rat β-Cells Release the Intracellular Autoantigens GAD65, IA-2, and Proinsulin in Exosomes Together With Cytokine-Induced Enhancers of Immunity Cianciaruso, Chiara; Phelps, Edward A.; Pasquier, Miriella Diabetes, Vol. 66, Issue 2 https://doi.org/10.2337/db16-0671	journal	November 2016
High-throughput Functional Genomics Identifies Regulators of Primary Human Beta Cell Proliferation Robitaille, Karine; Rourke, Jillian L.; McBane, Joanne E. Journal of Biological Chemistry, Vol. 291, Issue 9 https://doi.org/10.1074/jbc.M115.683912	journal	February 2016
Identification of proliferative and mature β-cells in the islets of Langerhans Bader, Erik; Migliorini, Adriana; Gegg, Moritz Nature, Vol. 535, Issue 7612 https://doi.org/10.1038/nature18624	journal	July 2016
Citrullinated Glucose-Regulated Protein 78 Is an Autoantigen in Type 1 Diabetes Rondas, Dieter; Crèvecoeur, Inne; D’Hertog, Wannes Diabetes, Vol. 64, Issue 2 https://doi.org/10.2337/db14-0621	journal	September 2014
Compensatory Islet Response to Insulin Resistance Revealed by Quantitative Proteomics El Ouaamari, Abdelfattah; Zhou, Jian-Ying; Liew, Chong Wee Journal of Proteome Research, Vol. 14, Issue 8 https://doi.org/10.1021/acs.jproteome.5b00587	journal	June 2015
Proteomic Analysis of Disease Stratified Human Pancreas Tissue Indicates Unique Signature of Type 1 Diabetes Burch, Tanya C.; Morris, Margaret A.; Campbell-Thompson, Martha PLOS ONE, Vol. 10, Issue 8 https://doi.org/10.1371/journal.pone.0135663	journal	August 2015
Proteomic profiling of human islets collected from frozen pancreata using laser capture microdissection Zhang, Lina; Lanzoni, Giacomo; Battarra, Matteo Journal of Proteomics, Vol. 150 https://doi.org/10.1016/j.jprot.2016.09.002	journal	January 2017
Comparative quantitative proteomic analysis of disease stratified laser captured microdissected human islets identifies proteins and pathways potentially related to type 1 diabetes Nyalwidhe, Julius O.; Grzesik, Wojciech J.; Burch, Tanya C. PLOS ONE, Vol. 12, Issue 9 https://doi.org/10.1371/journal.pone.0183908	journal	September 2017
Nanodroplet processing platform for deep and quantitative proteome profiling of 10–100 mammalian cells Zhu, Ying; Piehowski, Paul D.; Zhao, Rui Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03367-w	journal	February 2018
MicroRNA Expression in Alpha and Beta Cells of Human Pancreatic Islets Klein, Dagmar; Misawa, Ryosuke; Bravo-Egana, Valia PLoS ONE, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pone.0055064	journal	January 2013
Enhanced Detection of Low Abundance Human Plasma Proteins Using a Tandem IgY12-SuperMix Immunoaffinity Separation Strategy Qian, Wei-Jun; Kaleta, David T.; Petritis, Brianne O. Molecular & Cellular Proteomics, Vol. 7, Issue 10 https://doi.org/10.1074/mcp.M800008-MCP200	journal	July 2008
Depletion of Abundant Plasma Proteins and Limitations of Plasma Proteomics Tu, Chengjian; Rudnick, Paul A.; Martinez, Misti Y. Journal of Proteome Research, Vol. 9, Issue 10 https://doi.org/10.1021/pr100646w	journal	October 2010
Human Plasma Proteome Analysis by Multidimensional Chromatography Prefractionation and Linear Ion Trap Mass Spectrometry Identification Jin, Wen-Hai; Dai, Jie; Li, Su-Jun Journal of Proteome Research, Vol. 4, Issue 2 https://doi.org/10.1021/pr049761h	journal	April 2005
Discovery and Validation of Serum Protein Changes in Type 1 Diabetes Patients Using High Throughput Two Dimensional Liquid Chromatography-Mass Spectrometry and Immunoassays Zhi, Wenbo; Sharma, Ashok; Purohit, Sharad Molecular & Cellular Proteomics, Vol. 10, Issue 11 https://doi.org/10.1074/mcp.M111.012203	journal	September 2011
Peptide serum markers in islet autoantibody-positive children von Toerne, Christine; Laimighofer, Michael; Achenbach, Peter Diabetologia, Vol. 60, Issue 2 https://doi.org/10.1007/s00125-016-4150-x	journal	November 2016
Application of Proteomics in the Discovery of Candidate Protein Biomarkers in a Diabetes Autoantibody Standardization Program Sample Subset Metz, Thomas O.; Qian, Wei-Jun; Jacobs, Jon M. Journal of Proteome Research, Vol. 7, Issue 2 https://doi.org/10.1021/pr700606w	journal	February 2008
Serum proteomics reveals systemic dysregulation of innate immunity in type 1 diabetes Zhang, Qibin; Fillmore, Thomas L.; Schepmoes, Athena A. The Journal of Experimental Medicine, Vol. 210, Issue 1 https://doi.org/10.1084/jem.20111843	journal	December 2012
Serum Proteomes Distinguish Children Developing Type 1 Diabetes in a Cohort With HLA-Conferred Susceptibility Moulder, Robert; Bhosale, Santosh D.; Erkkilä, Timo Diabetes, Vol. 64, Issue 6 https://doi.org/10.2337/db14-0983	journal	January 2015
Temporal expression profiling of plasma proteins reveals oxidative stress in early stages of Type 1 Diabetes progression Liu, Chih-Wei; Bramer, Lisa; Webb-Robertson, Bobbie-Jo Journal of Proteomics, Vol. 172 https://doi.org/10.1016/j.jprot.2017.10.004	journal	February 2018
Protein labeling by iTRAQ: A new tool for quantitative mass spectrometry in proteome research Wiese, Sebastian; Reidegeld, Kai A.; Meyer, Helmut E. PROTEOMICS, Vol. 7, Issue 3 https://doi.org/10.1002/pmic.200600422	journal	February 2007
Tandem Mass Tags: A Novel Quantification Strategy for Comparative Analysis of Complex Protein Mixtures by MS/MS Thompson, Andrew; Schäfer, Jürgen; Kuhn, Karsten Analytical Chemistry, Vol. 75, Issue 8 https://doi.org/10.1021/ac0262560	journal	April 2003
Revisiting biomarker discovery by plasma proteomics Geyer, Philipp E.; Holdt, Lesca M.; Teupser, Daniel Molecular Systems Biology, Vol. 13, Issue 9 https://doi.org/10.15252/msb.20156297	journal	September 2017
ER Stress in Pancreatic Cells: The Thin Red Line Between Adaptation and Failure Eizirik, D. L.; Cnop, M. Science Signaling, Vol. 3, Issue 110 https://doi.org/10.1126/scisignal.3110pe7	journal	February 2010
Endoplasmic Reticulum Stress and the Inflammatory Basis of Metabolic Disease Hotamisligil, Gökhan S. Cell, Vol. 140, Issue 6 https://doi.org/10.1016/j.cell.2010.02.034	journal	March 2010
Serological Proteome Analysis (SERPA) as a tool for the identification of new candidate autoantigens in type 1 diabetes Massa, Ornella; Alessio, Massimo; Russo, Lucia Journal of Proteomics, Vol. 82 https://doi.org/10.1016/j.jprot.2013.02.030	journal	April 2013
Recognition of Posttranslationally Modified GAD65 Epitopes in Subjects With Type 1 Diabetes McGinty, J. W.; Chow, I. -T.; Greenbaum, C. Diabetes, Vol. 63, Issue 9 https://doi.org/10.2337/db13-1952	journal	April 2014
Posttranslational Modification of HLA-DQ Binding Islet Autoantigens in Type 1 Diabetes van Lummel, M.; Duinkerken, G.; van Veelen, P. A. Diabetes, Vol. 63, Issue 1 https://doi.org/10.2337/db12-1214	journal	October 2013
HLA-dependent autoantibodies against post-translationally modified collagen type II in type 1 diabetes mellitus Strollo, R.; Rizzo, P.; Spoletini, M. Diabetologia, Vol. 56, Issue 3 https://doi.org/10.1007/s00125-012-2780-1	journal	November 2012
Antibodies to post-translationally modified insulin as a novel biomarker for prediction of type 1 diabetes in children Strollo, Rocky; Vinci, Chiara; Napoli, Nicola Diabetologia, Vol. 60, Issue 8 https://doi.org/10.1007/s00125-017-4296-1	journal	May 2017
Discovery of Phosphorylated Peripherin as a Major Humoral Autoantigen in Type 1 Diabetes Mellitus Doran, Todd M.; Morimoto, Jumpei; Simanski, Scott Cell Chemical Biology, Vol. 23, Issue 5 https://doi.org/10.1016/j.chembiol.2016.04.006	journal	May 2016
The insulin A-chain epitope recognized by human T cells is posttranslationally modified Mannering, Stuart I.; Harrison, Leonard C.; Williamson, Nicholas A. The Journal of Experimental Medicine, Vol. 202, Issue 9 https://doi.org/10.1084/jem.20051251	journal	October 2005
eIF2α phosphorylation is pathognomonic for immunogenic cell death Bezu, Lucillia; Sauvat, Allan; Humeau, Juliette Cell Death & Differentiation, Vol. 25, Issue 8 https://doi.org/10.1038/s41418-017-0044-9	journal	January 2018
Pharmacological Inhibition of Protein Lipidation Ganesan, Lakshmi; Levental, Ilya The Journal of Membrane Biology, Vol. 248, Issue 6 https://doi.org/10.1007/s00232-015-9835-4	journal	August 2015
Glycated albumin: a potential biomarker in diabetes Freitas, Priscila Aparecida Correa; Ehlert, Lethicia Rozales; Camargo, Joíza Lins Archives of Endocrinology and Metabolism, Vol. 61, Issue 3 https://doi.org/10.1590/2359-3997000000272	journal	June 2017
Pathogenic CD4 T cells in type 1 diabetes recognize epitopes formed by peptide fusion Delong, T.; Wiles, T. A.; Baker, R. L. Science, Vol. 351, Issue 6274 https://doi.org/10.1126/science.aad2791	journal	February 2016
The role of inflammation in insulitis and β-cell loss in type 1 diabetes Eizirik, Décio L.; Colli, Maikel L.; Ortis, Fernanda Nature Reviews Endocrinology, Vol. 5, Issue 4 https://doi.org/10.1038/nrendo.2009.21	journal	April 2009
High T-helper-1 cytokines but low T-helper-3 cytokines, inflammatory cytokines and chemokines in children with high risk of developing type 1 diabetes Stechova, Katerina; Bohmova, Kristyna; Vrabelova, Zuzana Diabetes/Metabolism Research and Reviews, Vol. 23, Issue 6 https://doi.org/10.1002/dmrr.718	journal	January 2007
Children With Islet Autoimmunity and Enterovirus Infection Demonstrate a Distinct Cytokine Profile Yeung, W. -C. G.; Al-Shabeeb, A.; Pang, C. N. I. Diabetes, Vol. 61, Issue 6 https://doi.org/10.2337/db11-0264	journal	April 2012
Serum CXCL1 concentrations are elevated in type 1 diabetes mellitus, possibly reflecting activity of anti-islet autoimmune activity Takahashi, Kazuma; Ohara, Mio; Sasai, Takayoshi Diabetes/Metabolism Research and Reviews, Vol. 27, Issue 8 https://doi.org/10.1002/dmrr.1257	journal	November 2011
Large-Scale Discovery and Validation Studies Demonstrate Significant Reductions in Circulating Levels of IL8, IL-1Ra, MCP-1, and MIP-1β in Patients With Type 1 Diabetes Purohit, Sharad; Sharma, Ashok; Hopkins, Diane The Journal of Clinical Endocrinology & Metabolism, Vol. 100, Issue 9 https://doi.org/10.1210/JC.2015-1388	journal	September 2015
Serum cytokines as biomarkers of disease and clues to pathogenesis Mack, Cara L. Hepatology, Vol. 46, Issue 1 https://doi.org/10.1002/hep.21793	journal	January 2007
The Role of Biomarkers in the Diagnosis and Risk Stratification of Acute Graft-versus-Host Disease: A Systematic Review Ali, Alaa M.; DiPersio, John F.; Schroeder, Mark A. Biology of Blood and Marrow Transplantation, Vol. 22, Issue 9 https://doi.org/10.1016/j.bbmt.2016.04.022	journal	September 2016
Dual and opposing roles of the unfolded protein response regulated by IRE1 and XBP1 in proinsulin processing and insulin secretion Lee, A. -H.; Heidtman, K.; Hotamisligil, G. S. Proceedings of the National Academy of Sciences, Vol. 108, Issue 21 https://doi.org/10.1073/pnas.1105564108	journal	May 2011
Elevations in the Fasting Serum Proinsulin–to–C-Peptide Ratio Precede the Onset of Type 1 Diabetes Sims, Emily K.; Chaudhry, Zunaira; Watkins, Renecia Diabetes Care, Vol. 39, Issue 9 https://doi.org/10.2337/dc15-2849	journal	July 2016
Proinsulin levels and the proinsulin:c-peptide ratio complement autoantibody measurement for predicting type 1 diabetes Truyen, I.; De Pauw, P.; Jørgensen, P. N. Diabetologia, Vol. 48, Issue 11 https://doi.org/10.1007/s00125-005-1959-0	journal	October 2005
Identification of Tetraspanin-7 as a Target of Autoantibodies in Type 1 Diabetes McLaughlin, Kerry A.; Richardson, Carolyn C.; Ravishankar, Aarthi Diabetes, Vol. 65, Issue 6 https://doi.org/10.2337/db15-1058	journal	March 2016
Islet Cell Surface Antibodies from Insulin-dependent Diabetics Bind Specifically to Pancreatic B Cells Van De Winkel, M.; Smets, G.; Gepts, W. Journal of Clinical Investigation, Vol. 70, Issue 1 https://doi.org/10.1172/JCI110601	journal	July 1982
Circulating Reg1α Proteins and Autoantibodies to Reg1α Proteins as Biomarkers of β-Cell Regeneration and Damage in Type 1 Diabetes Astorri, E.; Guglielmi, C.; Bombardieri, M. Hormone and Metabolic Research, Vol. 42, Issue 13 https://doi.org/10.1055/s-0030-1267206	journal	October 2010
Pancreatic duodenal homeobox 1 protein is a novel β-cell-specific autoantigen for type I diabetes Li, Shi-Wu; Koya, Vijay; Li, Yi Laboratory Investigation, Vol. 90, Issue 1 https://doi.org/10.1038/labinvest.2009.116	journal	November 2009
Selective Autoantibody Production against CCL3 Is Associated with Human Type 1 Diabetes Mellitus and Serves As a Novel Biomarker for Its Diagnosis Shehadeh, Naim; Pollack, Shirly; Wildbaum, Gizi The Journal of Immunology, Vol. 182, Issue 12 https://doi.org/10.4049/jimmunol.0803348	journal	June 2009
Identification of a common autoantigenic epitope of protein disulfide isomerase, golgin-160 and voltage-gated potassium channel in type 1 diabetes Fierabracci, Alessandra; Saura, Francesca Diabetes Research and Clinical Practice, Vol. 88, Issue 2 https://doi.org/10.1016/j.diabres.2010.01.018	journal	May 2010
Amylase -2A Autoantibodies: Novel Marker of Autoimmune Pancreatitis and Fulminant Type 1 Diabetes Endo, T.; Takizawa, S.; Tanaka, S. Diabetes, Vol. 58, Issue 3 https://doi.org/10.2337/db08-0493	journal	November 2008
Autoantibodies to calcium channels in type 1 diabetes mediate autonomic dysfunction by different mechanisms in colon and bladder and are neutralized by antiidiotypic antibodies Wan, En-Chi; Gordon, Tom P.; Jackson, Michael W. Journal of Autoimmunity, Vol. 31, Issue 1 https://doi.org/10.1016/j.jaut.2008.03.004	journal	August 2008
A novel impedance-based cellular assay for the detection of anti-calcium channel autoantibodies in type 1 diabetes Jackson, Michael W.; Gordon, Tom P. Journal of Immunological Methods, Vol. 361, Issue 1-2 https://doi.org/10.1016/j.jim.2010.07.005	journal	September 2010
Autoantibodies against aminoacyl-tRNA synthetase: novel diagnostic marker for type 1 diabetes mellitus Park, Sang Gyu; Park, Ho Seon; Jeong, In-Kyong Biomarkers, Vol. 15, Issue 4 https://doi.org/10.3109/13547501003777823	journal	January 2010
Autoimmunity to two forms of glutamate decarboxylase in insulin-dependent diabetes mellitus. Kaufman, D. L.; Erlander, M. G.; Clare-Salzler, M. Journal of Clinical Investigation, Vol. 89, Issue 1 https://doi.org/10.1172/JCI115573	journal	January 1992
Molecular Cloning of Phogrin, a Protein-tyrosine Phosphatase Homologue Localized to Insulin Secretory Granule Membranes Wasmeier, Christina; Hutton, John C. Journal of Biological Chemistry, Vol. 271, Issue 30 https://doi.org/10.1074/jbc.271.30.18161	journal	July 1996
Utilization of an intron located polyadenlyation site resulted in four novel glutamate decarboxylase transcripts Liu, Haixiong; Wang, Zhiqiang; Li, Shifeng Molecular Biology Reports, Vol. 36, Issue 6 https://doi.org/10.1007/s11033-008-9337-x	journal	August 2008
Differential Splicing of the IA-2 mRNA in Pancreas and Lymphoid Organs as a Permissive Genetic Mechanism for Autoimmunity Against the IA-2 Type 1 Diabetes Autoantigen Diez, J.; Park, Y.; Zeller, M. Diabetes, Vol. 50, Issue 4 https://doi.org/10.2337/diabetes.50.4.895	journal	April 2001
Evaluation of Polymorphic Splicing in the Mechanism of the Association of the Insulin Gene With Diabetes Marchand, L.; Polychronakos, C. Diabetes, Vol. 56, Issue 3 https://doi.org/10.2337/db06-0402	journal	February 2007
Novel fusion proteins in the analysis of diabetes-associated autoantibodies to GAD65 and IA-2 Zavialov, Anton; Ankelo, Matti; Westerlund-Karlsson, Annette Journal of Immunological Methods, Vol. 246, Issue 1-2 https://doi.org/10.1016/S0022-1759(00)00303-3	journal	December 2000
Novel Diabetes Autoantibodies and Prediction of Type 1 Diabetes Wenzlau, Janet M.; Hutton, John C. Current Diabetes Reports, Vol. 13, Issue 5 https://doi.org/10.1007/s11892-013-0405-9	journal	July 2013
The Origin of Circulating Free DNA van der Vaart, Maniesh; Pretorius, Piet J. Clinical Chemistry, Vol. 53, Issue 12 https://doi.org/10.1373/clinchem.2007.092734	journal	December 2007
Characterization of the release and biological significance of cell-free DNA from breast cancer cell lines Wang, Wei; Kong, Peng; Ma, Ge Oncotarget, Vol. 8, Issue 26 https://doi.org/10.18632/oncotarget.17858	journal	May 2017
Nucleic acid biomarkers of β cell stress and death in type 1 diabetes Syed, Farooq; Evans-Molina, Carmella Current Opinion in Endocrinology & Diabetes and Obesity, Vol. 23, Issue 4 https://doi.org/10.1097/MED.0000000000000261	journal	January 2016
β Cell death and dysfunction during type 1 diabetes development in at-risk individuals Herold, Kevan C.; Usmani-Brown, Sahar; Ghazi, Tara Journal of Clinical Investigation, Vol. 125, Issue 3 https://doi.org/10.1172/JCI78142	journal	February 2015
Detection of cell death in diabetes using differentially methylated circulating DNA Akirav, E. M.; Lebastchi, J.; Galvan, E. M. Proceedings of the National Academy of Sciences, Vol. 108, Issue 47 https://doi.org/10.1073/pnas.1111008108	journal	November 2011
Identification of tissue-specific cell death using methylation patterns of circulating DNA Lehmann-Werman, Roni; Neiman, Daniel; Zemmour, Hai Proceedings of the National Academy of Sciences, Vol. 113, Issue 13 https://doi.org/10.1073/pnas.1519286113	journal	March 2016
Analysis of β-Cell Death in Type 1 Diabetes by Droplet Digital PCR Usmani-Brown, Sahar; Lebastchi, Jasmin; Steck, Andrea K. Endocrinology, Vol. 155, Issue 9 https://doi.org/10.1210/en.2014-1150	journal	September 2014
Elevations in Circulating Methylated and Unmethylated Preproinsulin DNA in New-Onset Type 1 Diabetes Fisher, Marisa M.; Watkins, Renecia A.; Blum, Janice Diabetes, Vol. 64, Issue 11 https://doi.org/10.2337/db15-0430	journal	July 2015
Immune Therapy and -Cell Death in Type 1 Diabetes Lebastchi, J.; Deng, S.; Lebastchi, A. H. Diabetes, Vol. 62, Issue 5 https://doi.org/10.2337/db12-1207	journal	February 2013
Circulating Differentially Methylated Amylin DNA as a Biomarker of β-Cell Loss in Type 1 Diabetes Olsen, John A.; Kenna, Lauren A.; Spelios, Michael G. PLOS ONE, Vol. 11, Issue 4 https://doi.org/10.1371/journal.pone.0152662	journal	April 2016
Innate Immune Activity Is Detected Prior to Seroconversion in Children With HLA-Conferred Type 1 Diabetes Susceptibility Kallionpaa, H.; Elo, L. L.; Laajala, E. Diabetes, Vol. 63, Issue 7 https://doi.org/10.2337/db13-1775	journal	February 2014
Risk of Type 1 Diabetes Progression in Islet Autoantibody-Positive Children Can Be Further Stratified Using Expression Patterns of Multiple Genes Implicated in Peripheral Blood Lymphocyte Activation and Function Jin, Y.; Sharma, A.; Bai, S. Diabetes, Vol. 63, Issue 7 https://doi.org/10.2337/db13-1716	journal	March 2014
A Type I Interferon Transcriptional Signature Precedes Autoimmunity in Children Genetically at Risk for Type 1 Diabetes Ferreira, R. C.; Guo, H.; Coulson, R. M. R. Diabetes, Vol. 63, Issue 7 https://doi.org/10.2337/db13-1777	journal	February 2014
Peripheral Blood Monocyte Gene Expression Profile Clinically Stratifies Patients With Recent-Onset Type 1 Diabetes Irvine, Katharine M.; Gallego, Patricia; An, Xiaoyu Diabetes, Vol. 61, Issue 5 https://doi.org/10.2337/db11-1549	journal	March 2012
MicroRNA expression profiles and type 1 diabetes mellitus: systematic review and bioinformatic analysis Assmann, Taís S.; Recamonde-Mendoza, Mariana; De Souza, Bianca M. Endocrine Connections, Vol. 6, Issue 8 https://doi.org/10.1530/EC-17-0248	journal	November 2017
Pancreas-enriched miRNAs are altered in the circulation of subjects with diabetes: a pilot cross-sectional study Seyhan, Attila A.; Nunez Lopez, Yury O.; Xie, Hui Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep31479	journal	August 2016
Circulating miRNA Profiles in Patients with Metabolic Syndrome Karolina, Dwi Setyowati; Tavintharan, Subramaniam; Armugam, Arunmozhiarasi The Journal of Clinical Endocrinology & Metabolism, Vol. 97, Issue 12 https://doi.org/10.1210/jc.2012-1996	journal	December 2012
miR-375 gene dosage in pancreatic β-cells: implications for regulation of β-cell mass and biomarker development Latreille, Mathieu; Herrmanns, Karolin; Renwick, Neil Journal of Molecular Medicine, Vol. 93, Issue 10 https://doi.org/10.1007/s00109-015-1296-9	journal	May 2015
miRNA-375 a Sensor of Glucotoxicity Is Altered in the Serum of Children with Newly Diagnosed Type 1 Diabetes Marchand, Lucien; Jalabert, Audrey; Meugnier, Emmanuelle Journal of Diabetes Research, Vol. 2016 https://doi.org/10.1155/2016/1869082	journal	January 2016
Profiling of circulating microRNAs in children with recent onset of type 1 diabetes Erener, Suheda; Marwaha, Ashish; Tan, Rusung JCI Insight, Vol. 2, Issue 4 https://doi.org/10.1172/jci.insight.89656	journal	February 2017
Diabetes-Associated MicroRNAs in Pediatric Patients With Type 1 Diabetes Mellitus: A Cross-Sectional Cohort Study Osipova, Julia; Fischer, Dagmar-Christiane; Dangwal, Seema The Journal of Clinical Endocrinology & Metabolism, Vol. 99, Issue 9 https://doi.org/10.1210/jc.2013-3868	journal	September 2014
Circulating miR-375 as a Biomarker of β-Cell Death and Diabetes in Mice Erener, Suheda; Mojibian, Majid; Fox, Jessica K. Endocrinology, Vol. 154, Issue 2 https://doi.org/10.1210/en.2012-1744	journal	January 2013
The Association Between Circulating Levels of miRNA-181a and Pancreatic Beta Cells Dysfunction via SMAD7 in Type 1 Diabetic Children and Adolescents: miRNA-181a and Pancreatic Beta Cells Dysfunction Nabih, Enas Samir; Andrawes, Nevine Gamal Journal of Clinical Laboratory Analysis, Vol. 30, Issue 5 https://doi.org/10.1002/jcla.21928	journal	February 2016
Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells Valadi, Hadi; Ekström, Karin; Bossios, Apostolos Nature Cell Biology, Vol. 9, Issue 6 https://doi.org/10.1038/ncb1596	journal	May 2007
Beta cell extracellular vesicle miR-21-5p cargo is increased in response to inflammatory cytokines and serves as a biomarker of type 1 diabetes Lakhter, Alexander J.; Pratt, Rachel E.; Moore, Rachel E. Diabetologia, Vol. 61, Issue 5 https://doi.org/10.1007/s00125-018-4559-5	journal	February 2018
Plasma-derived exosome characterization reveals a distinct microRNA signature in long duration Type 1 diabetes Garcia-Contreras, Marta; Shah, Sanket H.; Tamayo, Alejandro Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-05787-y	journal	July 2017
Age- and Islet Autoimmunity–Associated Differences in Amino Acid and Lipid Metabolites in Children at Risk for Type 1 Diabetes Pflueger, Maren; Seppänen-Laakso, Tuulikki; Suortti, Tapani Diabetes, Vol. 60, Issue 11 https://doi.org/10.2337/db10-1652	journal	October 2011
Metabolic profiling of type 1 diabetes mellitus in children and adolescents: a case–control study Bervoets, Liene; Massa, Guy; Guedens, Wanda Diabetology & Metabolic Syndrome, Vol. 9, Issue 1 https://doi.org/10.1186/s13098-017-0246-9	journal	June 2017
Metabolomics Makes a Mark: Early Changes Associated With Autoimmune Diabetes Leslie, R. David; Beyan, Huriya Diabetes, Vol. 60, Issue 11 https://doi.org/10.2337/db11-1177	journal	October 2011
Circulating sphingolipid biomarkers in models of type 1 diabetes Fox, Todd E.; Bewley, Maria C.; Unrath, Kellee A. Journal of Lipid Research, Vol. 52, Issue 3 https://doi.org/10.1194/jlr.M010595	journal	March 2011
Decreased Cord-Blood Phospholipids in Young Age-at-Onset Type 1 Diabetes La Torre, D.; Seppanen-Laakso, T.; Larsson, H. E. Diabetes, Vol. 62, Issue 11 https://doi.org/10.2337/db13-0215	journal	August 2013
Dysregulation of lipid and amino acid metabolism precedes islet autoimmunity in children who later progress to type 1 diabetes Orešič, Matej; Simell, Satu; Sysi-Aho, Marko Journal of Experimental Medicine, Vol. 205, Issue 13 https://doi.org/10.1084/jem.20081800	journal	December 2008
Cord Serum Lipidome in Prediction of Islet Autoimmunity and Type 1 Diabetes Orešič, Matej; Gopalacharyulu, Peddinti; Mykkänen, Juha Diabetes, Vol. 62, Issue 9 https://doi.org/10.2337/db13-0159	journal	April 2013
Advances in targeted proteomics and applications to biomedical research Shi, Tujin; Song, Ehwang; Nie, Song PROTEOMICS, Vol. 16, Issue 15-16 https://doi.org/10.1002/pmic.201500449	journal	August 2016
Molecular aspects of diabetes mellitus: Resistin, microRNA, and exosome Saeedi Borujeni, Mohammad Javad; Esfandiary, Ebrahim; Taheripak, Gholamreza Journal of Cellular Biochemistry, Vol. 119, Issue 2 https://doi.org/10.1002/jcb.26271	journal	August 2017
Circulating Endothelial Microparticles in Diabetes Mellitus Tramontano, A. F.; Lyubarova, R.; Tsiakos, J. Mediators of Inflammation, Vol. 2010 https://doi.org/10.1155/2010/250476	journal	January 2010
Phosphopeptidomics Reveals Differential Phosphorylation States and Novel SxE Phosphosite Motifs of Neuropeptides in Dense Core Secretory Vesicles Lietz, Christopher B.; Toneff, Thomas; Mosier, Charles Journal of The American Society for Mass Spectrometry, Vol. 29, Issue 5 https://doi.org/10.1007/s13361-018-1915-0	journal	March 2018
Impaired immune phenotype of circulating endothelial-derived microparticles in patients with metabolic syndrome and diabetes mellitus Berezin, A. E.; Kremzer, A. A.; Samura, T. A. Journal of Endocrinological Investigation, Vol. 38, Issue 8 https://doi.org/10.1007/s40618-015-0273-z	journal	April 2015

Cited By (2)

Fetal malnutrition-induced catch up failure is caused by elevated levels of miR-322 in rats Nemoto, Takahiro; Kakinuma, Yoshihiko Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-58392-x	journal	January 2020
The role of proteomics in assessing beta-cell dysfunction and death in type 1 diabetes Nakayasu, Ernesto S.; Qian, Wei-Jun; Evans-Molina, Carmella Expert Review of Proteomics, Vol. 16, Issue 7 https://doi.org/10.1080/14789450.2019.1634548	journal	June 2019

Similar Records

Serum biomarkers for diagnosis and prediction of type 1 diabetes

Journal Article · Thu Nov 01 00:00:00 EDT 2018 · Translational Research · OSTI ID:1464493

Yi, Lian; Swensen, Adam C.; Qian, Wei-Jun

Systematic review of type 1 diabetes biomarkers reveals regulation in circulating proteins related to complement, lipid metabolism, and immune response

Journal Article · Thu Sep 21 00:00:00 EDT 2023 · Clinical Proteomics · OSTI ID:1464493

Sarkar, Soumyadeep; Elliott, Emily C.; Henry, Hayden R.; +9 more

Plasma protein biomarkers predict the development of persistent autoantibodies and type 1 diabetes 6 months prior to the onset of autoimmunity

Journal Article · Sat Jul 01 00:00:00 EDT 2023 · Cell Reports Medicine · OSTI ID:1464493

Nakayasu, Ernesto S.; Bramer, Lisa M.; Ansong, Charles; +22 more

Related Subjects

60 APPLIED LIFE SCIENCES

Title: Serum biomarkers for diagnosis and prediction of type 1 diabetes

Citation Formats

References (131)

Cited By (2)

Similar Records

Related Subjects