Glycocapture-assisted global quantitative proteomics (gagQP) reveals multiorgan responses in serum toxicoproteome.

Blood is an ideal window for viewing our health and disease status. Because blood circulates throughout the entire body and carries secreted, shed, and excreted signature proteins from every organ and tissue type, it is thus possible to use the blood proteome to achieve a comprehensive assessment of multiple-organ physiology and pathology. To date, the blood proteome has been frequently examined for diseases of individual organs; studies on compound insults impacting multiple organs are, however, elusive. We believe that a characterization of peripheral blood for organ-specific proteins affords a powerful strategy to allow early detection, staging, and monitoring of diseases and their treatments at a whole-body level. In this paper we test this hypothesis by examining a mouse model of acetaminophen (APAP)-induced hepatic and extra-hepatic toxicity. We used a glycocapture-assisted global quantitative proteomics (gagQP) approach to study serum proteins and validated our results using Western blot. We discovered in mouse sera both hepatic and extra-hepatic organ-specific proteins. From our validation, it was determined that selected organ-specific proteins had changed their blood concentration during the course of toxicity development and recovery. Interestingly, the peak responding time of proteins specific to different organs varied in a time-course study. The collected molecular information shed light on a complex, dynamic, yet interweaving, multiorgan-enrolled APAP toxicity. The developed technique as well as the identified protein markers is translational to human studies. We hope our work can broaden the utility of blood proteomics in diagnosis and research of the whole-body response to pathogenic cues.

[1]  Eric D. Dodds,et al.  Gas-phase dissociation of glycosylated peptide ions. , 2012, Mass spectrometry reviews.

[2]  Brad T. Sherman,et al.  DAVID-WS: a stateful web service to facilitate gene/protein list analysis , 2012, Bioinform..

[3]  J. Hallén Troponin for the Estimation of Infarct Size: What Have We Learned? , 2012, Cardiology.

[4]  Gilbert S Omenn,et al.  SRM targeted proteomics in search for biomarkers of HCV‐induced progression of fibrosis to cirrhosis in HALT‐C patients , 2012, Proteomics.

[5]  Zhaojing Meng,et al.  Targeted mass spectrometry approaches for protein biomarker verification. , 2011, Journal of proteomics.

[6]  Ruedi Aebersold,et al.  Mass Spectrometry Based Glycoproteomics—From a Proteomics Perspective* , 2010, Molecular & Cellular Proteomics.

[7]  S. S. Dadarkar,et al.  Phenotypic and genotypic assessment of concomitant drug‐induced toxic effects in liver, kidney and blood , 2010, Journal of applied toxicology : JAT.

[8]  M. Luster,et al.  Blood gene expression markers to detect and distinguish target organ toxicity , 2010, Molecular and Cellular Biochemistry.

[9]  W. Waring,et al.  Delayed onset of acute renal failure after significant paracetamol overdose: A case series , 2010, Human & experimental toxicology.

[10]  Amanda G. Paulovich,et al.  An Automated and Multiplexed Method for High Throughput Peptide Immunoaffinity Enrichment and Multiple Reaction Monitoring Mass Spectrometry-based Quantification of Protein Biomarkers* , 2009, Molecular & Cellular Proteomics.

[11]  Eric E Schadt,et al.  Multi-tissue coexpression networks reveal unexpected subnetworks associated with disease. , 2009 .

[12]  Christoph H Borchers,et al.  A Human Proteome Detection and Quantitation Project* , 2009, Molecular & Cellular Proteomics.

[13]  M. Passero,et al.  Estimating Radiation Risk from Computed Tomography Scanning , 2009, Lung.

[14]  Sandhya Rani,et al.  Human Protein Reference Database—2009 update , 2008, Nucleic Acids Res..

[15]  B. Anderson Paracetamol (Acetaminophen): mechanisms of action , 2008, Paediatric anaesthesia.

[16]  A. Dorner,et al.  Use of ex vivo systems for biomarker discovery. , 2008, Current opinion in pharmacology.

[17]  Ruedi Aebersold,et al.  The protein information and property explorer: an easy-to-use, rich-client web application for the management and functional analysis of proteomic data , 2008, Bioinform..

[18]  B Alex Merrick,et al.  Gene expression response in target organ and whole blood varies as a function of target organ injury phenotype , 2008, Genome Biology.

[19]  B. Hendriks,et al.  Multiple effects of acetaminophen and p38 inhibitors: Towards pathway toxicology , 2008, FEBS letters.

[20]  S. Hanash,et al.  Mining the plasma proteome for cancer biomarkers , 2008, Nature.

[21]  D. Mendrick,et al.  Genomic and genetic biomarkers of toxicity. , 2008, Toxicology.

[22]  J. Perrone,et al.  Acetaminophen-induced nephrotoxicity: Pathophysiology, clinical manifestations, and management , 2008, Journal of Medical Toxicology.

[23]  J. Ozer,et al.  The current state of serum biomarkers of hepatotoxicity. , 2008, Toxicology.

[24]  C. Liew,et al.  The peripheral-blood transcriptome: new insights into disease and risk assessment. , 2007, Trends in molecular medicine.

[25]  H. Yamada,et al.  Evaluation of human hepatocyte chimeric mice as a model for toxicological investigation using panomic approaches--effect of acetaminophen on the expression profiles of proteins and endogenous metabolites in liver, plasma and urine. , 2007, The Journal of toxicological sciences.

[26]  Jennifer J. Kohler,et al.  Chemical methods for glycoprotein discovery. , 2007, Current opinion in chemical biology.

[27]  J. Uetrecht,et al.  Idiosyncratic drug reactions: current understanding. , 2007, Annual review of pharmacology and toxicology.

[28]  L. Hood,et al.  Shotgun Glycopeptide Capture Approach Coupled with Mass Spectrometry for Comprehensive Glycoproteomics *S , 2007, Molecular & Cellular Proteomics.

[29]  K. Egerer,et al.  Circulating proteasomes are functional and have a subtype pattern distinct from 20S proteasomes in major blood cells. , 2006, Clinical chemistry.

[30]  J. Sanders,et al.  Matricellular Hevin Regulates Decorin Production and Collagen Assembly* , 2006, Journal of Biological Chemistry.

[31]  K. Tomer,et al.  Alterations in the Rat Serum Proteome during Liver Injury from Acetaminophen Exposure , 2006, Journal of Pharmacology and Experimental Therapeutics.

[32]  Leigh Anderson,et al.  Quantitative Mass Spectrometric Multiple Reaction Monitoring Assays for Major Plasma Proteins* , 2006, Molecular & Cellular Proteomics.

[33]  A. Dorner,et al.  Transcriptional profiling of peripheral blood cells in clinical pharmacogenomic studies. , 2006, Pharmacogenomics.

[34]  Y. Yıldırım,et al.  Labeling of acetaminophen with I-131 and biodistribution in rats. , 2006, Chemical & pharmaceutical bulletin.

[35]  Eric W. Deutsch,et al.  The PeptideAtlas project , 2005, Nucleic Acids Res..

[36]  R. Townsend,et al.  Use of proteomic methods to identify serum biomarkers associated with rat liver toxicity or hypertrophy. , 2005, Clinical chemistry.

[37]  Marcus B Smolka,et al.  Dynamic Changes in Protein-Protein Interaction and Protein Phosphorylation Probed with Amine-reactive Isotope Tag*S , 2005, Molecular & Cellular Proteomics.

[38]  D. Harrison,et al.  Regulation of Xanthine Oxidoreductase Protein Expression by Hydrogen Peroxide and Calcium , 2005, Arteriosclerosis, thrombosis, and vascular biology.

[39]  H. Cui,et al.  In Vivo Mechanisms of Tissue-Selective Drug Toxicity: Effects of Liver-Specific Knockout of the NADPH-Cytochrome P450 Reductase Gene on Acetaminophen Toxicity in Kidney, Lung, and Nasal Mucosa , 2005, Molecular Pharmacology.

[40]  N. Kaplowitz,et al.  Serum alanine aminotransferase in skeletal muscle diseases , 2005, Hepatology.

[41]  K. Dalhoff,et al.  Alpha‐fetoprotein is a predictor of outcome in acetaminophen‐induced liver injury , 2005, Hepatology.

[42]  Darryl B. Hardie,et al.  Mass spectrometric quantitation of peptides and proteins using Stable Isotope Standards and Capture by Anti-Peptide Antibodies (SISCAPA). , 2004, Journal of proteome research.

[43]  R. Watson,et al.  Pathophysiology, Homeostasis and Nursing , 2003 .

[44]  P. Shannon,et al.  Cytoscape: a software environment for integrated models of biomolecular interaction networks. , 2003, Genome research.

[45]  Jeffrey B. Gross,et al.  Timing of New Black Box Warnings and Withdrawals for Prescription Medications , 2003 .

[46]  M. Paulsson,et al.  SC1/Hevin , 2003, The Journal of Biological Chemistry.

[47]  N. Anderson,et al.  The Human Plasma Proteome , 2002, Molecular & Cellular Proteomics.

[48]  A. Woolf,et al.  2001 Annual report of the American Association of Poison Control Centers Toxic Exposure Surveillance System. , 2002, The American journal of emergency medicine.

[49]  K. Muldrew,et al.  Determination of acetaminophen-protein adducts in mouse liver and serum and human serum after hepatotoxic doses of acetaminophen using high-performance liquid chromatography with electrochemical detection. , 2002, Drug metabolism and disposition: the biological fate of chemicals.

[50]  G. Gores,et al.  Mechanisms of hepatotoxicity. , 2002, Toxicological sciences : an official journal of the Society of Toxicology.

[51]  R. Aebersold,et al.  Quantitative profiling of differentiation-induced microsomal proteins using isotope-coded affinity tags and mass spectrometry , 2001, Nature Biotechnology.

[52]  A. Dell,et al.  Glycoprotein Structure Determination by Mass Spectrometry , 2001, Science.

[53]  Simon C Watkins,et al.  Actin-containing sera from patients with adult respiratory distress syndrome are toxic to sheep pulmonary endothelial cells. , 2000, American journal of respiratory and critical care medicine.

[54]  J. Mestecky,et al.  Role of nuclear factor-κ B in the expression by tumor necrosis factor-α of the human polymeric immunoglobulin receptor (pIgR ) gene , 2000, Immunogenetics.

[55]  T. Litovitz,et al.  1997 annual report of the American Association of Poison Control Centers Toxic Exposure Surveillance System. , 1998, The American journal of emergency medicine.

[56]  Steven D. Cohen,et al.  Selective protein arylation and acetaminophen-induced hepatotoxicity. , 1997, Drug metabolism reviews.

[57]  N. Tygstrup,et al.  Expression of liver-specific functions in rat hepatocytes following sublethal and lethal acetaminophen poisoning. , 1996, Journal of hepatology.

[58]  S. D. Cohen,et al.  Acetaminophen-arylated proteins are detected in hepatic subcellular fractions and numerous extra-hepatic tissues in CD-1 and C57B1/6J mice. , 1996, Toxicology.

[59]  Steven D. Cohen,et al.  Immunohistochemical localization of acetaminophen in target tissues of the CD-1 mouse: correspondence of covalent binding with toxicity. , 1995, Fundamental and applied toxicology : official journal of the Society of Toxicology.

[60]  M. Csete,et al.  Vicodin-induced fulminant hepatic failure. , 1993, Anesthesiology.

[61]  A. Varki,et al.  Biological roles of oligosaccharides: all of the theories are correct , 1993, Glycobiology.

[62]  K. Taketa a-Fetoprotein: Reevaluation , 2005 .

[63]  Steven D. Cohen,et al.  Extrahepatic Lesions Induced by Acetaminophen in the Mouse , 1987, Toxicologic pathology.

[64]  R Heywood,et al.  Target organ toxicity. , 1981, Toxicology letters.

[65]  J R Gillette,et al.  Acetaminophen-induced hepatotoxicity. , 1981, Life sciences.

[66]  E. N. Wardle,et al.  Circulating lysosomal enzymes and acute hepatic necrosis. , 1981, Journal of clinical pathology.

[67]  G. Murphy,et al.  Quantitation of prostate-specific antigen in serum by a sensitive enzyme immunoassay. , 1980, Cancer research.

[68]  B B Brodie,et al.  Acetaminophen-induced hepatic necrosis. I. Role of drug metabolism. , 1973, The Journal of pharmacology and experimental therapeutics.

[69]  T. Boyer,et al.  Acetaminophen-induced hepatic necrosis and renal failure. , 1971, JAMA.

[70]  E. M. Boyd,et al.  Liver necrosis from paracetamol. , 1966, British journal of pharmacology and chemotherapy.

[71]  G. Tortora,et al.  Principles of Anatomy and Physiology , 1911, Buffalo Medical Journal.

[72]  Joseph Zaia,et al.  Historical overview of glycoanalysis. , 2010, Methods in molecular biology.

[73]  B. Merrick The plasma proteome, adductome and idiosyncratic toxicity in toxicoproteomics research. , 2008, Briefings in functional genomics & proteomics.

[74]  R. Aebersold,et al.  A uniform proteomics MS/MS analysis platform utilizing open XML file formats , 2005, Molecular systems biology.

[75]  C. Mothersill,et al.  Bystander and other delayed effects and multi-organ involvement and failure following high dose exposure to ionising radiation , 2005 .

[76]  J. Mestecky,et al.  Role of nuclear factor-kappaB in the expression by tumor necrosis factor-alpha of the human polymeric immunoglobulin receptor (plgR) gene. , 2000, Immunogenetics.

[77]  K. Taketa Alpha-fetoprotein: reevaluation in hepatology. , 1990, Hepatology.

[78]  M. Burke Hepatic function tests. , 1974, Geriatrics.