Hepatic kinome atlas: An in-depth identification of kinase pathways in liver fibrosis of humans and rodents.


Journal

Hepatology (Baltimore, Md.)
ISSN: 1527-3350
Titre abrégé: Hepatology
Pays: United States
ID NLM: 8302946

Informations de publication

Date de publication:
11 2022
Historique:
revised: 02 03 2022
received: 23 11 2021
accepted: 12 03 2022
pubmed: 22 3 2022
medline: 22 10 2022
entrez: 21 3 2022
Statut: ppublish

Résumé

Resolution of pathways that converge to induce deleterious effects in hepatic diseases, such as in the later stages, have potential antifibrotic effects that may improve outcomes. We aimed to explore whether humans and rodents display similar fibrotic signaling networks. We assiduously mapped kinase pathways using 340 substrate targets, upstream bioinformatic analysis of kinase pathways, and over 2000 random sampling iterations using the PamGene PamStation kinome microarray chip technology. Using this technology, we characterized a large number of kinases with altered activity in liver fibrosis of both species. Gene expression and immunostaining analyses validated many of these kinases as bona fide signaling events. Surprisingly, the insulin receptor emerged as a considerable protein tyrosine kinase that is hyperactive in fibrotic liver disease in humans and rodents. Discoidin domain receptor tyrosine kinase, activated by collagen that increases during fibrosis, was another hyperactive protein tyrosine kinase in humans and rodents with fibrosis. The serine/threonine kinases found to be the most active in fibrosis were dystrophy type 1 protein kinase and members of the protein kinase family of kinases. We compared the fibrotic events over four models: humans with cirrhosis and three murine models with differing levels of fibrosis, including two models of fatty liver disease with emerging fibrosis. The data demonstrate a high concordance between human and rodent hepatic kinome signaling that focalizes, as shown by our network analysis of detrimental pathways. Our findings establish a comprehensive kinase atlas for liver fibrosis, which identifies analogous signaling events conserved among humans and rodents.

Sections du résumé

BACKGROUND AND AIMS
Resolution of pathways that converge to induce deleterious effects in hepatic diseases, such as in the later stages, have potential antifibrotic effects that may improve outcomes. We aimed to explore whether humans and rodents display similar fibrotic signaling networks.
APPROACH AND RESULTS
We assiduously mapped kinase pathways using 340 substrate targets, upstream bioinformatic analysis of kinase pathways, and over 2000 random sampling iterations using the PamGene PamStation kinome microarray chip technology. Using this technology, we characterized a large number of kinases with altered activity in liver fibrosis of both species. Gene expression and immunostaining analyses validated many of these kinases as bona fide signaling events. Surprisingly, the insulin receptor emerged as a considerable protein tyrosine kinase that is hyperactive in fibrotic liver disease in humans and rodents. Discoidin domain receptor tyrosine kinase, activated by collagen that increases during fibrosis, was another hyperactive protein tyrosine kinase in humans and rodents with fibrosis. The serine/threonine kinases found to be the most active in fibrosis were dystrophy type 1 protein kinase and members of the protein kinase family of kinases. We compared the fibrotic events over four models: humans with cirrhosis and three murine models with differing levels of fibrosis, including two models of fatty liver disease with emerging fibrosis. The data demonstrate a high concordance between human and rodent hepatic kinome signaling that focalizes, as shown by our network analysis of detrimental pathways.
CONCLUSIONS
Our findings establish a comprehensive kinase atlas for liver fibrosis, which identifies analogous signaling events conserved among humans and rodents.

Identifiants

pubmed: 35313030
doi: 10.1002/hep.32467
pmc: PMC9489820
mid: NIHMS1790833
doi:

Substances chimiques

Receptor, Insulin EC 2.7.10.1
Protein Kinases EC 2.7.-
Collagen 9007-34-5
Serine 452VLY9402
Discoidin Domain Receptors EC 2.7.10.1
Threonine 2ZD004190S

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1376-1388

Subventions

Organisme : NIMH NIH HHS
ID : R01 MH121102
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG057598
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK121797
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH107487
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA177558
Pays : United States
Organisme : NIAAA NIH HHS
ID : P50 AA024333
Pays : United States

Informations de copyright

© 2022 The Authors. Hepatology published by Wiley Periodicals LLC on behalf of American Association for the Study of Liver Diseases.

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Auteurs

Justin F Creeden (JF)

Department of Neurosciences, University of Toledo College of Medicine and Life Sciences, Toledo, Ohio, USA.

Zachary A Kipp (ZA)

Department of Pharmacology and Nutritional Sciences, University of Kentucky College of Medicine, Lexington, Kentucky, USA.

Mei Xu (M)

Department of Pharmacology and Nutritional Sciences, University of Kentucky College of Medicine, Lexington, Kentucky, USA.

Robert M Flight (RM)

Department of Molecular & Cellular Biochemistry, University of Kentucky, Lexington, Kentucky, USA.
Markey Cancer Center, University of Kentucky, Lexington, Kentucky, USA.
Resource Center for Stable Isotope Resolved Metabolomics, University of Kentucky, Lexington, Kentucky, USA.

Hunter N B Moseley (HNB)

Department of Molecular & Cellular Biochemistry, University of Kentucky, Lexington, Kentucky, USA.
Markey Cancer Center, University of Kentucky, Lexington, Kentucky, USA.
Resource Center for Stable Isotope Resolved Metabolomics, University of Kentucky, Lexington, Kentucky, USA.
Institute for Biomedical Informatics, University of Kentucky, Lexington, Kentucky, USA.
Center for Clinical and Translational Science, University of Kentucky, Lexington, Kentucky, USA.

Genesee J Martinez (GJ)

Department of Pharmacology and Nutritional Sciences, University of Kentucky College of Medicine, Lexington, Kentucky, USA.

Wang-Hsin Lee (WH)

Department of Pharmacology and Nutritional Sciences, University of Kentucky College of Medicine, Lexington, Kentucky, USA.

Khaled Alganem (K)

Department of Neurosciences, University of Toledo College of Medicine and Life Sciences, Toledo, Ohio, USA.

Ali S Imami (AS)

Department of Neurosciences, University of Toledo College of Medicine and Life Sciences, Toledo, Ohio, USA.

Megan R McMullen (MR)

Department of Inflammation and Immunity, Cleveland Clinic, Cleveland, Ohio, USA.

Sanjoy Roychowdhury (S)

Department of Inflammation and Immunity, Cleveland Clinic, Cleveland, Ohio, USA.

Atta M Nawabi (AM)

Division of Transplant and Hepatobiliary, Department of Surgery, The University of Kansas Medical Center, Kansas City, Kansas, USA.

Jennifer A Hipp (JA)

Strata Oncology, Ann Arbor, Michigan, USA.

Samir Softic (S)

Department of Pharmacology and Nutritional Sciences, University of Kentucky College of Medicine, Lexington, Kentucky, USA.
Department of Pediatrics, University of Kentucky, Lexington, Kentucky, USA.

Steven A Weinman (SA)

Department of Internal Medicine and Liver Center, University of Kansas Medical Center, Kansas City, Kansas, USA.

Robert McCullumsmith (R)

Department of Neurosciences, University of Toledo College of Medicine and Life Sciences, Toledo, Ohio, USA.
Neurosciences Institute, ProMedica, Toledo, Ohio, USA.

Laura E Nagy (LE)

Department of Inflammation and Immunity, Cleveland Clinic, Cleveland, Ohio, USA.
Department of Gastroenterology and Hepatology, Center for Liver Disease Research, Cleveland Clinic, Cleveland, Ohio, USA.
Department of Molecular Medicine, Case Western Reserve University, Cleveland, Ohio, USA.

Terry D Hinds (TD)

Department of Pharmacology and Nutritional Sciences, University of Kentucky College of Medicine, Lexington, Kentucky, USA.
Markey Cancer Center, University of Kentucky, Lexington, Kentucky, USA.
Barnstable Brown Diabetes Center, University of Kentucky College of Medicine, Lexington, Kentucky, USA.

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