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PloS one2024; 19(2); e0298039; doi: 10.1371/journal.pone.0298039

Gene co-expression network analysis reveal core responsive genes in Parascaris univalens tissues following ivermectin exposure.

Abstract: Anthelmintic resistance in equine parasite Parascaris univalens, compromises ivermectin (IVM) effectiveness and necessitates an in-depth understanding of its resistance mechanisms. Most research, primarily focused on holistic gene expression analyses, may overlook vital tissue-specific responses and often limit the scope of novel genes. This study leveraged gene co-expression network analysis to elucidate tissue-specific transcriptional responses and to identify core genes implicated in the IVM response in P. univalens. Adult worms (n = 28) were exposed to 10-11 M and 10-9 M IVM in vitro for 24 hours. RNA-sequencing examined transcriptional changes in the anterior end and intestine. Differential expression analysis revealed pronounced tissue differences, with the intestine exhibiting substantially more IVM-induced transcriptional activity. Gene co-expression network analysis identified seven modules significantly associated with the response to IVM. Within these, 219 core genes were detected, largely expressed in the intestinal tissue and spanning diverse biological processes with unspecific patterns. After 10-11 M IVM, intestinal tissue core genes showed transcriptional suppression, cell cycle inhibition, and ribosomal alterations. Interestingly, genes PgR028_g047 (sorb-1), PgB01_g200 (gmap-1) and PgR046_g017 (col-37 & col-102) switched from downregulation at 10-11 M to upregulation at 10-9 M IVM. The 10-9 M concentration induced expression of cuticle and membrane integrity core genes in the intestinal tissue. No clear core gene patterns were visible in the anterior end after 10-11 M IVM. However, after 10-9 M IVM, the anterior end mostly displayed downregulation, indicating disrupted transcriptional regulation. One interesting finding was the non-modular calcium-signaling gene, PgR047_g066 (gegf-1), which uniquely connected 71 genes across four modules. These genes were enriched for transmembrane signaling activity, suggesting that PgR047_g066 (gegf-1) could have a key signaling role. By unveiling tissue-specific expression patterns and highlighting biological processes through unbiased core gene detection, this study reveals intricate IVM responses in P. univalens. These findings suggest alternative drug uptake of IVM and can guide functional validations to further IVM resistance mechanism understanding.
Copyright: © 2024 Dube et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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Publication Date: 2024-02-15 PubMed ID: 38359071PubMed Central: PMC10868809DOI: 10.1371/journal.pone.0298039Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The study investigates the resistance mechanisms of the equine parasite, Parascaris univalens, towards the common anthelmintic drug ivermectin (IVM) by exploring tissue-specific transcriptional responses and identifying critical genes involved.

Research Methodology

  • P. univalens (adult worms, n = 28) were exposed to two various concentrations of IVM (10-11 M & 10-9 M) in a controlled lab setting over a 24-hour period.
  • Post-exposure, the researchers utilized RNA-sequencing to observe transcriptional changes in two specific worm tissues: the anterior end and the intestine.
  • Upon analyzing differential expression, they detected pronounced tissue differences, noting greater IVM-induced transcriptional activity in the intestinal tissue compared to the anterior end.

Findings

  • Through gene co-expression network analysis, the researchers identified seven modules that exhibited significant associations with IVM response.
  • Within these modules, 219 core genes were found, most of which exhibited expression in the intestinal tissue and were involved in diverse biological processes.
  • When exposed to the lower concentration of IVM (10-11M), these intestinal core genes showed a decrease in transcription activity, cell cycle inhibition, and changes in the ribosomal structure.
  • However, certain genes (PgR028_g047, PgB01_g200, and PgR046_g017) displayed behavior contrary to the general pattern, switching from downregulation to upregulation when the IVM concentration was increased to 10-9 M.
  • Under higher IVM concentration (10-9M), core genes associated with cuticle and membrane integrity exhibited enhanced expression in the intestinal tissue. No consistent patterns were observed in the anterior end under 10-11M IVM; however, it mainly showed downregulation after exposure to 10-9M IVM.
  • Another unique discovery was the calcium-signaling gene, PgR047_g066 (gegf-1), which was found to connect with 71 other genes across four different modules. These connected genes were generally enriched for transmembrane signaling activity, suggesting a critical signaling role for the PgR047_g066 (gegf-1) gene.

Conclusion

  • The study highlights tissue-specific expression patterns in response to IVM, thus shedding light on the complexities of IVM responses in P. univalens.
  • The findings indicate potential alternate methods of drug uptake of IVM by the parasite, promising to guide further research into functional validation and understanding resistance mechanisms.

Cite This Article

APA
Dube F, Delhomme N, Martin F, Hinas A, Åbrink M, Svärd S, Tydén E. (2024). Gene co-expression network analysis reveal core responsive genes in Parascaris univalens tissues following ivermectin exposure. PLoS One, 19(2), e0298039. https://doi.org/10.1371/journal.pone.0298039

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 19
Issue: 2
Pages: e0298039
PII: e0298039

Researcher Affiliations

Dube, Faruk
  • Department of Animal Biosciences, Swedish University of Agricultural Sciences, Uppsala, Sweden.
Delhomme, Nicolas
  • Umeå Plant Science Centre (UPSC), Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå, Sweden.
Martin, Frida
  • Department of Animal Biosciences, Swedish University of Agricultural Sciences, Uppsala, Sweden.
Hinas, Andrea
  • Department of Cell and Molecular Biology, Uppsala University, Uppsala Sweden.
Åbrink, Magnus
  • Department of Animal Biosciences, Swedish University of Agricultural Sciences, Uppsala, Sweden.
Svärd, Staffan
  • Department of Cell and Molecular Biology, Uppsala University, Uppsala Sweden.
Tydén, Eva
  • Department of Animal Biosciences, Swedish University of Agricultural Sciences, Uppsala, Sweden.

MeSH Terms

  • Horses / genetics
  • Animals
  • Ivermectin / pharmacology
  • Anthelmintics / pharmacology
  • Gene Expression Regulation
  • Gene Expression Profiling
  • Ascaridoidea / genetics
  • Drug Resistance / genetics

Conflict of Interest Statement

The authors have declared that no competing interests exist.

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Citations

This article has been cited 1 times.
  1. Yu Y, Dong H, Zhao Q, Zhu S, Wang H, Yao Y, Huang W, Han H. Combined transcriptome and whole genome sequencing analyses reveal candidate drug-resistance genes of Eimeria tenella. iScience 2025 Jan 17;28(1):111592.
    doi: 10.1016/j.isci.2024.111592pubmed: 39811641google scholar: lookup
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