Renalase is a novel tissue and serological biomarker in pancreatic ductal adenocarcinoma

Dysregulated expression of the secretory protein renalase can promote pancreatic ductal adenocarcinoma (PDAC) growth in animal models. We characterized renalase expression in premalignant and malignant PDAC tissue and investigated whether plasma renalase levels corresponded to clinical PDAC characte...

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Veröffentlicht in:PloS one 2021-09, Vol.16 (9), p.e0250539
Hauptverfasser: Gao, Yasheen, Wang, Melinda, Guo, Xiaojia, Hu, Joanna, Chen, Tian-Min, Finn, Sade M B, Lacy, Jill, Kunstman, John W, Cha, Charles H, Bellin, Melena D, Robert, Marie E, Desir, Gary V, Gorelick, Fred S
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creator Gao, Yasheen
Wang, Melinda
Guo, Xiaojia
Hu, Joanna
Chen, Tian-Min
Finn, Sade M B
Lacy, Jill
Kunstman, John W
Cha, Charles H
Bellin, Melena D
Robert, Marie E
Desir, Gary V
Gorelick, Fred S
description Dysregulated expression of the secretory protein renalase can promote pancreatic ductal adenocarcinoma (PDAC) growth in animal models. We characterized renalase expression in premalignant and malignant PDAC tissue and investigated whether plasma renalase levels corresponded to clinical PDAC characteristics. Renalase immunohistochemistry was used to determine the presence and distribution of renalase in normal pancreas, chronic pancreatitis, PDAC precursor lesions, and PDAC tissues. Associations between pretreatment plasma renalase and PDAC clinical status were assessed in patients with varied clinical stages of PDAC and included tumor characteristics, surgical resection in locally advanced/borderline resectable PDAC, and overall survival. Data were retrospectively obtained and correlated using non-parametric analysis. Little to no renalase was detected by histochemistry in the normal pancreatic head in the absence of abdominal trauma. In chronic pancreatitis, renalase immunoreactivity localized to peri-acinar spindle-shaped cells in some samples. It was also widely present in PDAC precursor lesions and PDAC tissue. Among 240 patients with PDAC, elevated plasma renalase levels were associated with worse tumor characteristics, including greater angiolymphatic invasion (80.0% vs. 58.1%, p = 0.012) and greater node positive disease (76.5% vs. 56.5%, p = 0.024). Overall survival was worse in patients with high plasma renalase levels with median follow-up of 27.70 months vs. 65.03 months (p < 0.001). Renalase levels also predicted whether patients with locally advanced/borderline resectable PDAC underwent resection (AUC 0.674; 95%CI 0.42-0.82, p = 0.04). Overall tissue renalase was increased in both premalignant and malignant PDAC tissues compared to normal pancreas. Elevated plasma renalase levels were associated with advanced tumor characteristics, decreased overall survival, and reduced resectability in patients with locally advanced/borderline resectable PDAC. These studies show that renalase levels are increased in premalignant pancreatic tissues and that its levels in plasma correspond to the clinical behavior of PDAC.
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We characterized renalase expression in premalignant and malignant PDAC tissue and investigated whether plasma renalase levels corresponded to clinical PDAC characteristics. Renalase immunohistochemistry was used to determine the presence and distribution of renalase in normal pancreas, chronic pancreatitis, PDAC precursor lesions, and PDAC tissues. Associations between pretreatment plasma renalase and PDAC clinical status were assessed in patients with varied clinical stages of PDAC and included tumor characteristics, surgical resection in locally advanced/borderline resectable PDAC, and overall survival. Data were retrospectively obtained and correlated using non-parametric analysis. Little to no renalase was detected by histochemistry in the normal pancreatic head in the absence of abdominal trauma. In chronic pancreatitis, renalase immunoreactivity localized to peri-acinar spindle-shaped cells in some samples. It was also widely present in PDAC precursor lesions and PDAC tissue. Among 240 patients with PDAC, elevated plasma renalase levels were associated with worse tumor characteristics, including greater angiolymphatic invasion (80.0% vs. 58.1%, p = 0.012) and greater node positive disease (76.5% vs. 56.5%, p = 0.024). Overall survival was worse in patients with high plasma renalase levels with median follow-up of 27.70 months vs. 65.03 months (p &lt; 0.001). Renalase levels also predicted whether patients with locally advanced/borderline resectable PDAC underwent resection (AUC 0.674; 95%CI 0.42-0.82, p = 0.04). Overall tissue renalase was increased in both premalignant and malignant PDAC tissues compared to normal pancreas. Elevated plasma renalase levels were associated with advanced tumor characteristics, decreased overall survival, and reduced resectability in patients with locally advanced/borderline resectable PDAC. These studies show that renalase levels are increased in premalignant pancreatic tissues and that its levels in plasma correspond to the clinical behavior of PDAC.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0250539</identifier><identifier>PMID: 34587190</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acids ; Adenocarcinoma ; Adult ; Aged ; Aged, 80 and over ; Analysis ; Animal growth ; Animal models ; Antibodies ; Antigens ; Biological markers ; Biology and Life Sciences ; Biomarkers ; Biomarkers, Tumor - blood ; Cancer ; Carcinoma, Pancreatic Ductal - blood ; Carcinoma, Pancreatic Ductal - mortality ; Carcinoma, Pancreatic Ductal - pathology ; Case-Control Studies ; Diagnosis ; Female ; Gastrointestinal cancer ; Gene Expression Regulation, Neoplastic ; Genetic aspects ; Histochemistry ; Humans ; Immunohistochemistry ; Kidney cancer ; Labeling ; Laboratories ; Lesions ; Male ; Medical prognosis ; Medicine ; Medicine and Health Sciences ; Middle Aged ; Monoamine Oxidase - blood ; Neoplasm Grading ; Pancreas ; Pancreatic cancer ; Pancreatic Neoplasms - blood ; Pancreatic Neoplasms - mortality ; Pancreatic Neoplasms - pathology ; Pancreatitis ; Parametric analysis ; Patients ; Plasma ; Precursors ; Prognosis ; Prospective Studies ; Retrospective Studies ; Surgery ; Survival ; Survival Analysis ; Tissues ; Trauma ; Tumors ; Up-Regulation ; Veterans ; Young Adult</subject><ispartof>PloS one, 2021-09, Vol.16 (9), p.e0250539</ispartof><rights>COPYRIGHT 2021 Public Library of Science</rights><rights>This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication: https://creativecommons.org/publicdomain/zero/1.0/ (the “License”). 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We characterized renalase expression in premalignant and malignant PDAC tissue and investigated whether plasma renalase levels corresponded to clinical PDAC characteristics. Renalase immunohistochemistry was used to determine the presence and distribution of renalase in normal pancreas, chronic pancreatitis, PDAC precursor lesions, and PDAC tissues. Associations between pretreatment plasma renalase and PDAC clinical status were assessed in patients with varied clinical stages of PDAC and included tumor characteristics, surgical resection in locally advanced/borderline resectable PDAC, and overall survival. Data were retrospectively obtained and correlated using non-parametric analysis. Little to no renalase was detected by histochemistry in the normal pancreatic head in the absence of abdominal trauma. In chronic pancreatitis, renalase immunoreactivity localized to peri-acinar spindle-shaped cells in some samples. It was also widely present in PDAC precursor lesions and PDAC tissue. Among 240 patients with PDAC, elevated plasma renalase levels were associated with worse tumor characteristics, including greater angiolymphatic invasion (80.0% vs. 58.1%, p = 0.012) and greater node positive disease (76.5% vs. 56.5%, p = 0.024). Overall survival was worse in patients with high plasma renalase levels with median follow-up of 27.70 months vs. 65.03 months (p &lt; 0.001). Renalase levels also predicted whether patients with locally advanced/borderline resectable PDAC underwent resection (AUC 0.674; 95%CI 0.42-0.82, p = 0.04). Overall tissue renalase was increased in both premalignant and malignant PDAC tissues compared to normal pancreas. Elevated plasma renalase levels were associated with advanced tumor characteristics, decreased overall survival, and reduced resectability in patients with locally advanced/borderline resectable PDAC. These studies show that renalase levels are increased in premalignant pancreatic tissues and that its levels in plasma correspond to the clinical behavior of PDAC.</description><subject>Acids</subject><subject>Adenocarcinoma</subject><subject>Adult</subject><subject>Aged</subject><subject>Aged, 80 and over</subject><subject>Analysis</subject><subject>Animal growth</subject><subject>Animal models</subject><subject>Antibodies</subject><subject>Antigens</subject><subject>Biological markers</subject><subject>Biology and Life Sciences</subject><subject>Biomarkers</subject><subject>Biomarkers, Tumor - blood</subject><subject>Cancer</subject><subject>Carcinoma, Pancreatic Ductal - blood</subject><subject>Carcinoma, Pancreatic Ductal - mortality</subject><subject>Carcinoma, Pancreatic Ductal - pathology</subject><subject>Case-Control Studies</subject><subject>Diagnosis</subject><subject>Female</subject><subject>Gastrointestinal cancer</subject><subject>Gene Expression Regulation, Neoplastic</subject><subject>Genetic aspects</subject><subject>Histochemistry</subject><subject>Humans</subject><subject>Immunohistochemistry</subject><subject>Kidney cancer</subject><subject>Labeling</subject><subject>Laboratories</subject><subject>Lesions</subject><subject>Male</subject><subject>Medical prognosis</subject><subject>Medicine</subject><subject>Medicine and Health Sciences</subject><subject>Middle Aged</subject><subject>Monoamine Oxidase - blood</subject><subject>Neoplasm Grading</subject><subject>Pancreas</subject><subject>Pancreatic cancer</subject><subject>Pancreatic Neoplasms - blood</subject><subject>Pancreatic Neoplasms - mortality</subject><subject>Pancreatic Neoplasms - pathology</subject><subject>Pancreatitis</subject><subject>Parametric analysis</subject><subject>Patients</subject><subject>Plasma</subject><subject>Precursors</subject><subject>Prognosis</subject><subject>Prospective Studies</subject><subject>Retrospective Studies</subject><subject>Surgery</subject><subject>Survival</subject><subject>Survival Analysis</subject><subject>Tissues</subject><subject>Trauma</subject><subject>Tumors</subject><subject>Up-Regulation</subject><subject>Veterans</subject><subject>Young 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Advanced Technologies &amp; Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gao, Yasheen</au><au>Wang, Melinda</au><au>Guo, Xiaojia</au><au>Hu, Joanna</au><au>Chen, Tian-Min</au><au>Finn, Sade M B</au><au>Lacy, Jill</au><au>Kunstman, John W</au><au>Cha, Charles H</au><au>Bellin, Melena D</au><au>Robert, Marie E</au><au>Desir, Gary V</au><au>Gorelick, Fred S</au><au>Su, Gloria H.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Renalase is a novel tissue and serological biomarker in pancreatic ductal adenocarcinoma</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2021-09-29</date><risdate>2021</risdate><volume>16</volume><issue>9</issue><spage>e0250539</spage><pages>e0250539-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Dysregulated expression of the secretory protein renalase can promote pancreatic ductal adenocarcinoma (PDAC) growth in animal models. We characterized renalase expression in premalignant and malignant PDAC tissue and investigated whether plasma renalase levels corresponded to clinical PDAC characteristics. Renalase immunohistochemistry was used to determine the presence and distribution of renalase in normal pancreas, chronic pancreatitis, PDAC precursor lesions, and PDAC tissues. Associations between pretreatment plasma renalase and PDAC clinical status were assessed in patients with varied clinical stages of PDAC and included tumor characteristics, surgical resection in locally advanced/borderline resectable PDAC, and overall survival. Data were retrospectively obtained and correlated using non-parametric analysis. Little to no renalase was detected by histochemistry in the normal pancreatic head in the absence of abdominal trauma. In chronic pancreatitis, renalase immunoreactivity localized to peri-acinar spindle-shaped cells in some samples. It was also widely present in PDAC precursor lesions and PDAC tissue. Among 240 patients with PDAC, elevated plasma renalase levels were associated with worse tumor characteristics, including greater angiolymphatic invasion (80.0% vs. 58.1%, p = 0.012) and greater node positive disease (76.5% vs. 56.5%, p = 0.024). Overall survival was worse in patients with high plasma renalase levels with median follow-up of 27.70 months vs. 65.03 months (p &lt; 0.001). Renalase levels also predicted whether patients with locally advanced/borderline resectable PDAC underwent resection (AUC 0.674; 95%CI 0.42-0.82, p = 0.04). Overall tissue renalase was increased in both premalignant and malignant PDAC tissues compared to normal pancreas. Elevated plasma renalase levels were associated with advanced tumor characteristics, decreased overall survival, and reduced resectability in patients with locally advanced/borderline resectable PDAC. These studies show that renalase levels are increased in premalignant pancreatic tissues and that its levels in plasma correspond to the clinical behavior of PDAC.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>34587190</pmid><doi>10.1371/journal.pone.0250539</doi><tpages>e0250539</tpages><orcidid>https://orcid.org/0000-0001-8293-6803</orcidid><orcidid>https://orcid.org/0000-0002-2618-4173</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1932-6203
ispartof PloS one, 2021-09, Vol.16 (9), p.e0250539
issn 1932-6203
1932-6203
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source MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS); PubMed Central; Free Full-Text Journals in Chemistry
subjects Acids
Adenocarcinoma
Adult
Aged
Aged, 80 and over
Analysis
Animal growth
Animal models
Antibodies
Antigens
Biological markers
Biology and Life Sciences
Biomarkers
Biomarkers, Tumor - blood
Cancer
Carcinoma, Pancreatic Ductal - blood
Carcinoma, Pancreatic Ductal - mortality
Carcinoma, Pancreatic Ductal - pathology
Case-Control Studies
Diagnosis
Female
Gastrointestinal cancer
Gene Expression Regulation, Neoplastic
Genetic aspects
Histochemistry
Humans
Immunohistochemistry
Kidney cancer
Labeling
Laboratories
Lesions
Male
Medical prognosis
Medicine
Medicine and Health Sciences
Middle Aged
Monoamine Oxidase - blood
Neoplasm Grading
Pancreas
Pancreatic cancer
Pancreatic Neoplasms - blood
Pancreatic Neoplasms - mortality
Pancreatic Neoplasms - pathology
Pancreatitis
Parametric analysis
Patients
Plasma
Precursors
Prognosis
Prospective Studies
Retrospective Studies
Surgery
Survival
Survival Analysis
Tissues
Trauma
Tumors
Up-Regulation
Veterans
Young Adult
title Renalase is a novel tissue and serological biomarker in pancreatic ductal adenocarcinoma
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