Influenza A virus replicates productively in primary human kidney cells and induces factors and mechanisms related to regulated cell death and renal pathology observed in virus-infected patients

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Abstract

Introduction

Influenza A virus (IAV) infection can cause the often-lethal acute respiratory distress syndrome (ARDS) of the lung. Concomitantly, acute kidney injury (AKI) is frequently noticed during IAV infection, correlating with an increased mortality. The aim of this study was to elucidate the interaction of IAV with human kidney cells and, thereby, to assess the mechanisms underlying IAV-mediated AKI.

Methods

To investigate IAV effects on nephron cells we performed infectivity assays with human IAV, as well as with human isolates of either low or highly pathogenic avian IAV. Also, transcriptome and proteome analysis of IAV-infected primary human distal tubular kidney cells (DTC) was performed. Furthermore, the DTC transcriptome was compared to existing transcriptomic data from IAV-infected lung and trachea cells.

Results

We demonstrate productive replication of all tested IAV strains on primary and immortalized nephron cells. Comparison of our transcriptome and proteome analysis of H1N1-type IAV-infected human primary distal tubular cells (DTC) with existing data from H1N1-type IAV-infected lung and primary trachea cells revealed enrichment of specific factors responsible for regulated cell death in primary DTC, which could be targeted by specific inhibitors.

Discussion

IAV not only infects, but also productively replicates on different human nephron cells. Importantly, multi-omics analysis revealed regulated cell death as potential contributing factor for the clinically observed kidney pathology in influenza.

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Most cited references 93

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Trimmomatic: a flexible trimmer for Illumina sequence data

Anthony M. Bolger, Marc Lohse, Bjoern Usadel (2014)

Motivation: Although many next-generation sequencing (NGS) read preprocessing tools already existed, we could not find any tool or combination of tools that met our requirements in terms of flexibility, correct handling of paired-end data and high performance. We have developed Trimmomatic as a more flexible and efficient preprocessing tool, which could correctly handle paired-end data. Results: The value of NGS read preprocessing is demonstrated for both reference-based and reference-free tasks. Trimmomatic is shown to produce output that is at least competitive with, and in many cases superior to, that produced by other tools, in all scenarios tested. Availability and implementation: Trimmomatic is licensed under GPL V3. It is cross-platform (Java 1.5+ required) and available at http://www.usadellab.org/cms/index.php?page=trimmomatic Contact: usadel@bio1.rwth-aachen.de Supplementary information: Supplementary data are available at Bioinformatics online.

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Cytoscape is an open source software project for integrating biomolecular interaction networks with high-throughput expression data and other molecular states into a unified conceptual framework. Although applicable to any system of molecular components and interactions, Cytoscape is most powerful when used in conjunction with large databases of protein-protein, protein-DNA, and genetic interactions that are increasingly available for humans and model organisms. Cytoscape's software Core provides basic functionality to layout and query the network; to visually integrate the network with expression profiles, phenotypes, and other molecular states; and to link the network to databases of functional annotations. The Core is extensible through a straightforward plug-in architecture, allowing rapid development of additional computational analyses and features. Several case studies of Cytoscape plug-ins are surveyed, including a search for interaction pathways correlating with changes in gene expression, a study of protein complexes involved in cellular recovery to DNA damage, inference of a combined physical/functional interaction network for Halobacterium, and an interface to detailed stochastic/kinetic gene regulatory models.

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KEGG: kyoto encyclopedia of genes and genomes.

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KEGG (Kyoto Encyclopedia of Genes and Genomes) is a knowledge base for systematic analysis of gene functions, linking genomic information with higher order functional information. The genomic information is stored in the GENES database, which is a collection of gene catalogs for all the completely sequenced genomes and some partial genomes with up-to-date annotation of gene functions. The higher order functional information is stored in the PATHWAY database, which contains graphical representations of cellular processes, such as metabolism, membrane transport, signal transduction and cell cycle. The PATHWAY database is supplemented by a set of ortholog group tables for the information about conserved subpathways (pathway motifs), which are often encoded by positionally coupled genes on the chromosome and which are especially useful in predicting gene functions. A third database in KEGG is LIGAND for the information about chemical compounds, enzyme molecules and enzymatic reactions. KEGG provides Java graphics tools for browsing genome maps, comparing two genome maps and manipulating expression maps, as well as computational tools for sequence comparison, graph comparison and path computation. The KEGG databases are daily updated and made freely available (http://www. genome.ad.jp/kegg/).

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Author and article information

Contributors

Benjamin Koch: URI : https://loop.frontiersin.org/people/1803560Role: Role: Role: Role: Role: Role: Role: Role:

Mahmoud Shehata: URI : https://loop.frontiersin.org/people/1883066Role: Role: Role: Role: Role:

Christin Müller-Ruttloff: URI : https://loop.frontiersin.org/people/2618991Role: Role: Role: Role:

Shady A. Gouda: Role: Role: Role: Role: Role:

Nils Wetzstein: Role: Role:

Sammy Patyna: Role: Role:

Anica Scholz: URI : https://loop.frontiersin.org/people/2666661Role: Role: Role:

Tobias Schmid: URI : https://loop.frontiersin.org/people/701798Role: Role: Role:

Ursula Dietrich: URI : https://loop.frontiersin.org/people/2670495Role: Role: Role:

Christian Münch: Role: Role: Role: Role:

John Ziebuhr: URI : https://loop.frontiersin.org/people/40174Role: Role: Role:

Helmut Geiger: Role: Role: Role:

Luis Martinez-Sobrido: URI : https://loop.frontiersin.org/people/340837Role: Role:

Patrick C. Baer: URI : https://loop.frontiersin.org/people/841790Role: Role: Role:

Ahmed Mostafa: URI : https://loop.frontiersin.org/people/473991Role: Role: Role: Role: Role: Role:

Stephan Pleschka: URI : https://loop.frontiersin.org/people/519155Role: Role: Role: Role: Role: Role:

Journal

Journal ID (nlm-ta): Front Cell Infect Microbiol

Journal ID (iso-abbrev): Front Cell Infect Microbiol

Journal ID (publisher-id): Front. Cell. Infect. Microbiol.

Title: Frontiers in Cellular and Infection Microbiology

Publisher: Frontiers Media S.A.

ISSN (Electronic): 2235-2988

Publication date (Electronic): 25 March 2024

Publication date Collection: 2024

Volume: 14

Electronic Location Identifier: 1363407

Affiliations

[1] ¹ Department of Internal Medicine 4, Nephrology, University Hospital, Goethe University Frankfurt , Frankfurt am Main, Germany

[2] ² Center of Scientific Excellence for Influenza Viruses, National Research Centre (NRC) , Cairo, Egypt

[3] ³ Institute of Medical Virology, Justus Liebig University Giessen , Giessen, Germany

[4] ⁴ German Center for Infection Research (DZIF), Partner Site Giessen , Giessen, Germany

[5] ⁵ Institute for Biochemistry II, Goethe University Frankfurt , Frankfurt am Main, Germany

[6] ⁶ Department of Internal Medicine 2, Infectious Diseases, Goethe University Frankfurt , Frankfurt am Main, Germany

[7] ⁷ Institute of Biochemistry I, Goethe University Frankfurt , Frankfurt am Main, Germany

[8] ⁸ Institute for Tumor Biology and Experimental Therapy, Georg-Speyer-Haus , Frankfurt am Main, Germany

[9] ⁹ Frankfurt Cancer Institute (FCI) , Frankfurt am Main, Germany

[10] ¹⁰ Cardio-Pulmonary Institute , Frankfurt am Main, Germany

[11] ¹¹ Texas Biomedical Research Institute, Disease Intervention & Prevention (DIP) and Host Pathogen Interactions (HPI) Programs , San Antonio, TX, United States

Author notes

Edited by: Chen Zhao, Fudan University, China

Reviewed by: Norberto Gonzalez-Juarbe, J. Craig Venter Institute (La Jolla), United States

Li Xing, Shanxi University, China

Amie J. Eisfeld, University of Wisconsin-Madison, United States

*Correspondence: Benjamin Koch, B.Koch@ 123456med.uni-frankfurt.de ; Stephan Pleschka, stephan.pleschka@ 123456viro.med.uni-giessen.de

†These authors share last authorship

Article

DOI: 10.3389/fcimb.2024.1363407

PMC ID: 10999593

PubMed ID: 38590437

SO-VID: 61cb4863-c042-4749-9794-9eec46ccd440

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 30 December 2023

Date accepted : 29 February 2024

Page count

Figures: 6, Tables: 0, Equations: 0, References: 93, Pages: 16, Words: 8249

Funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. The research was funded in part by the University Hospital Frankfurt am Main, a postdoctoral fellowship of the Justus-Liebig University, Giessen, Germany (Just’Us to AM), and the NRC internal project (TT110801 to AM). Furthermore, the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) funded collaborative research center SFB1021 (TP C01 to StP) and the German Ministry for Education and Research (BMBF) funded German Center for Infection Research, partner site Giessen, Germany (DZIF, TTU 01.806 to SP and JZ). The research was also funded by the Alexander von Humboldt Foundation with a Georg Forster Research Fellowship (MS). StP is a member of the German FluResearchNet, a nationwide research network on zoonotic influenza. Research on influenza in the LM-S laboratory is partially supported by the R01AI145332 and R01AI141607 grants from the National Institute of Health (NIH); by the Center for Research on Influenza Pathogenesis and Transmission (CRIPT), one of the National Institute of Allergy and Infectious Diseases (NIAID)-funded Centers of Excellence for Influenza Research and Response (CEIRR; contract No. 75N93021C00014); and by the American Lung Association. The funders had no role in study design, data collection/analysis, decision to publish, or preparation of the manuscript.

Custom metadata

section-in-acceptance Virus and Host

ScienceOpen disciplines: Infectious disease & Microbiology

Keywords: influenza a virus,acute kidney injury,distal tubular cells,transcriptomics,proteomics,regulated cell death

Data availability:

ScienceOpen disciplines: Infectious disease & Microbiology

Keywords: influenza a virus, acute kidney injury, distal tubular cells, transcriptomics, proteomics, regulated cell death

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Influenza A virus replicates productively in primary human kidney cells and induces factors and mechanisms related to regulated cell death and renal pathology observed in virus-infected patients

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Abstract

Introduction

Methods

Results

Discussion

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Karger: Nephrology

Most cited references 93

Trimmomatic: a flexible trimmer for Illumina sequence data

Cytoscape: a software environment for integrated models of biomolecular interaction networks.

KEGG: kyoto encyclopedia of genes and genomes.

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