Toxoplasma gondii Manipulates Expression of Host Long Noncoding RNA during Intracellular Infection

Menard, Kayla L.; Haskins, Breanne E.; Colombo, Anthony P.; Denkers, Eric Y.

doi:10.1038/s41598-018-33274-5

Title: Toxoplasma gondii Manipulates Expression of Host Long Noncoding RNA during Intracellular Infection

Journal Article · 08 October 2018 · Scientific Reports

DOI: https://doi.org/10.1038/s41598-018-33274-5 · OSTI ID:1624429

Menard, Kayla L. ^[1]; Haskins, Breanne E. ^[2]; Colombo, Anthony P. ^[3]; Denkers, Eric Y. ^[2]

Univ. of New Mexico, Albuquerque, NM (United States). Dept. of Biology and Center for Evolutionary and Theoretical Immunology; DOE/OSTI
Univ. of New Mexico, Albuquerque, NM (United States). Dept. of Biology and Center for Evolutionary and Theoretical Immunology
Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)

Long noncoding RNA (lncRNA) are non-protein-coding transcripts greater than 200 nucleotides that regulate gene expression. The field of transcriptomics is only beginning to understand the role of lncRNA in host defense. Little is known about the role of lncRNA in the response to infection by intracellular pathogens such as Toxoplasma gondii. Using a microarray, we examined the differential expression of 35,923 lncRNAs and 24,881 mRNAs in mouse bone-marrow-derived macrophages during infection with high- and low-virulence T. gondii strains. We found that 1,522 lncRNA molecules were differentially regulated during infection with the high-virulence Type I strain, versus 528 with the less-virulent Type II strain. Of these lncRNAs, 282 were co-regulated with a nearby or overlapping mRNA–including approximately 60 mRNAs with immune-related functions. We validated the microarray for 4 lncRNAs and 4 mRNAs using qRT-PCR. Using deletion strains of T. gondii, we found that the secretory kinase ROP16 controls upregulation of lncRNAs Csf1-lnc and Socs2-lnc, demonstrating that the parasite directly manipulates host lncRNA expression. Given the number of regulated lncRNAs and the magnitude of the expression changes, we hypothesize that these molecules constitute both an additional regulatory layer in the host response to infection and a target for manipulation by T. gondii.

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Research Organization:: Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: NA0003525

OSTI ID:: 1624429

Journal Information:: Scientific Reports, Journal Name: Scientific Reports Journal Issue: 1 Vol. 8; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Acute Toxoplasmosis Leads to Lethal Overproduction of Th1 Cytokines Mordue, Dana G.; Monroy, Fernando; La Regina, Marie The Journal of Immunology, Vol. 167, Issue 8 https://doi.org/10.4049/jimmunol.167.8.4574	journal	October 2001
Toxoplasma gondii Interferes with Lipopolysaccharide-Induced Mitogen-Activated Protein Kinase Activation by Mechanisms Distinct from Endotoxin Tolerance Kim, Leesun; Butcher, Barbara A.; Denkers, Eric Y. The Journal of Immunology, Vol. 172, Issue 5 https://doi.org/10.4049/jimmunol.172.5.3003	journal	February 2004
Production of IL-12 by Macrophages Infected with Toxoplasma gondii Depends on the Parasite Genotype Robben, Paul M.; Mordue, Dana G.; Truscott, Steven M. The Journal of Immunology, Vol. 172, Issue 6 https://doi.org/10.4049/jimmunol.172.6.3686	journal	March 2004
p38 MAPK Autophosphorylation Drives Macrophage IL-12 Production during Intracellular Infection Kim, Leesun; Rio, Laura Del; Butcher, Barbara A. The Journal of Immunology, Vol. 174, Issue 7 https://doi.org/10.4049/jimmunol.174.7.4178	journal	March 2005
Toxoplasma gondii Genotype Determines MyD88-Dependent Signaling in Infected Macrophages Kim, Leesun; Butcher, Barbara A.; Lee, Chiang W. The Journal of Immunology, Vol. 177, Issue 4 https://doi.org/10.4049/jimmunol.177.4.2584	journal	August 2006
Dendritic Cells Expressing Plasmacytoid Marker PDCA-1 Are Trojan Horses during Toxoplasma gondii Infection Bierly, Allison L.; Shufesky, William J.; Sukhumavasi, Woraporn The Journal of Immunology, Vol. 181, Issue 12 https://doi.org/10.4049/jimmunol.181.12.8485	journal	December 2008

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Expression of Long Non-Coding RNAs by Human Retinal Müller Glial Cells Infected with Clonal and Exotic Virulent Toxoplasma gondii Non-Coding RNA, Vol. 5, Issue 4 https://doi.org/10.3390/ncrna5040048	journal	September 2019
Additional file 10 of Full-length transcriptome analysis and identification of transcript structures in Eimeria necatrix from different developmental stages by single-molecule real-time sequencing Gao, Yang; Suding, Zeyang; Wang, Lele figshare https://doi.org/10.6084/m9.figshare.16689729.v1	dataset	January 2021
Additional file 11 of Full-length transcriptome analysis and identification of transcript structures in Eimeria necatrix from different developmental stages by single-molecule real-time sequencing Gao, Yang; Suding, Zeyang; Wang, Lele figshare https://doi.org/10.6084/m9.figshare.16689732	dataset	January 2021
Additional file 12 of Full-length transcriptome analysis and identification of transcript structures in Eimeria necatrix from different developmental stages by single-molecule real-time sequencing Gao, Yang; Suding, Zeyang; Wang, Lele figshare https://doi.org/10.6084/m9.figshare.16689735	image	January 2021
Additional file 13 of Full-length transcriptome analysis and identification of transcript structures in Eimeria necatrix from different developmental stages by single-molecule real-time sequencing Gao, Yang; Suding, Zeyang; Wang, Lele figshare https://doi.org/10.6084/m9.figshare.16689741.v1	dataset	January 2021
Additional file 14 of Full-length transcriptome analysis and identification of transcript structures in Eimeria necatrix from different developmental stages by single-molecule real-time sequencing Gao, Yang; Suding, Zeyang; Wang, Lele figshare https://doi.org/10.6084/m9.figshare.16689744	dataset	January 2021
Additional file 1 of Full-length transcriptome analysis and identification of transcript structures in Eimeria necatrix from different developmental stages by single-molecule real-time sequencing Gao, Yang; Suding, Zeyang; Wang, Lele figshare https://doi.org/10.6084/m9.figshare.16689747	image	January 2021
Additional file 2 of Full-length transcriptome analysis and identification of transcript structures in Eimeria necatrix from different developmental stages by single-molecule real-time sequencing Gao, Yang; Suding, Zeyang; Wang, Lele figshare https://doi.org/10.6084/m9.figshare.16689750.v1	image	January 2021
Additional file 3 of Full-length transcriptome analysis and identification of transcript structures in Eimeria necatrix from different developmental stages by single-molecule real-time sequencing Gao, Yang; Suding, Zeyang; Wang, Lele figshare https://doi.org/10.6084/m9.figshare.16689753	image	January 2021
Additional file 4 of Full-length transcriptome analysis and identification of transcript structures in Eimeria necatrix from different developmental stages by single-molecule real-time sequencing Gao, Yang; Suding, Zeyang; Wang, Lele figshare https://doi.org/10.6084/m9.figshare.16689756.v1	dataset	January 2021
Additional file 5 of Full-length transcriptome analysis and identification of transcript structures in Eimeria necatrix from different developmental stages by single-molecule real-time sequencing Gao, Yang; Suding, Zeyang; Wang, Lele figshare https://doi.org/10.6084/m9.figshare.16689759	dataset	January 2021
Additional file 6 of Full-length transcriptome analysis and identification of transcript structures in Eimeria necatrix from different developmental stages by single-molecule real-time sequencing Gao, Yang; Suding, Zeyang; Wang, Lele figshare https://doi.org/10.6084/m9.figshare.16689762.v1	image	January 2021
Additional file 7 of Full-length transcriptome analysis and identification of transcript structures in Eimeria necatrix from different developmental stages by single-molecule real-time sequencing Gao, Yang; Suding, Zeyang; Wang, Lele figshare https://doi.org/10.6084/m9.figshare.16689765.v1	dataset	January 2021
Additional file 8 of Full-length transcriptome analysis and identification of transcript structures in Eimeria necatrix from different developmental stages by single-molecule real-time sequencing Gao, Yang; Suding, Zeyang; Wang, Lele figshare https://doi.org/10.6084/m9.figshare.16689768.v1	dataset	January 2021
Additional file 9 of Full-length transcriptome analysis and identification of transcript structures in Eimeria necatrix from different developmental stages by single-molecule real-time sequencing Gao, Yang; Suding, Zeyang; Wang, Lele figshare https://doi.org/10.6084/m9.figshare.16689771.v1	dataset	January 2021
lncRedibly versatile: biochemical and biological functions of long noncoding RNAs Shields, Emily J.; Petracovici, Ana F.; Bonasio, Roberto Biochemical Journal, Vol. 476, Issue 7 https://doi.org/10.1042/bcj20180440	journal	April 2019
Long Non-Coding RNAs in the Regulation of Gene Expression: Physiology and Disease Fernandes, Juliane; Acuña, Stephanie; Aoki, Juliana Non-Coding RNA, Vol. 5, Issue 1 https://doi.org/10.3390/ncrna5010017	journal	February 2019

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