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Transcriptome profiling of male and female Ascaris lumbricoides reproductive tissues

BACKGROUND: Ascaris lumbricoides causes human ascariasis, the most prevalent helminth disease, infecting approximately 1 billion individuals globally. In 2019 the global disease burden was estimated to be 754,000 DALYs and resulted in 2090 deaths. In the absence of a vaccination strategy, treatment...

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Autores principales: Phuphisut, Orawan, Poodeepiyasawat, Akkarin, Yoonuan, Tippayarat, Watthanakulpanich, Dorn, Chotsiri, Palang, Reamtong, Onrapak, Mousley, Angela, Gobert, Geoffrey N., Adisakwattana, Poom
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9768952/
https://www.ncbi.nlm.nih.gov/pubmed/36539906
http://dx.doi.org/10.1186/s13071-022-05602-2
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author Phuphisut, Orawan
Poodeepiyasawat, Akkarin
Yoonuan, Tippayarat
Watthanakulpanich, Dorn
Chotsiri, Palang
Reamtong, Onrapak
Mousley, Angela
Gobert, Geoffrey N.
Adisakwattana, Poom
author_facet Phuphisut, Orawan
Poodeepiyasawat, Akkarin
Yoonuan, Tippayarat
Watthanakulpanich, Dorn
Chotsiri, Palang
Reamtong, Onrapak
Mousley, Angela
Gobert, Geoffrey N.
Adisakwattana, Poom
author_sort Phuphisut, Orawan
collection PubMed
description BACKGROUND: Ascaris lumbricoides causes human ascariasis, the most prevalent helminth disease, infecting approximately 1 billion individuals globally. In 2019 the global disease burden was estimated to be 754,000 DALYs and resulted in 2090 deaths. In the absence of a vaccination strategy, treatment of ascariasis has relied on anthelminthic chemotherapy, but drug resistance is a concern. The propensity for reinfection is also a major challenge to disease control; female worms lay up to 200,000 eggs daily, which contaminate surrounding environments and remain viable for years, resulting in high transmission rates. Understanding the molecular mechanisms of reproductive processes, including control of egg production, spermatogenesis, oogenesis and embryogenesis, will drive the development of new drugs and/or vaccine targets for future ascariasis control. METHODS: Transcriptome profiles of discrete reproductive and somatic tissue samples were generated from adult male and female worms using Illumina HiSeq with 2 × 150 bp paired-end sequencing. Male tissues included: testis germinal zone, testis part of vas deferens, seminal vesicle and somatic tissue. Female tissues included: ovary germinal zone, ovary part of the oviduct, uterus and somatic tissue. Differentially expressed genes (DEGs) were identified from the fragments per kilobases per million reads (FPKM) profiles. Hierarchical analysis was performed to identify tissue-specific genes. Furthermore, Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses were employed to identify significant terms and pathways for the DEGs. RESULTS: DEGs involved in protein phosphorylation and adhesion molecules were indicated to play a crucial role in spermatogenesis and fertilization, respectively. Those genes associated with the G-protein-coupled receptor (GPCR) signaling pathway and small GTPase-mediated signal transduction pathway play an essential role in cytoskeleton organization during oogenesis. Additionally, DEGs associated with the SMA genes and TGF-β signaling pathway are crucial in adult female embryogenesis. Some genes associated with particular biological processes and pathways that were identified in this study have been linked to defects in germline development, embryogenesis and reproductive behavior. In the enriched KEGG pathway analysis, Hippo signaling, oxytocin signaling and tight junction pathways were identified to play a role in Ascaris male and female reproductive systems. CONCLUSIONS: This study has provided comprehensive transcriptome profiles of discrete A. lumbricoides reproductive tissue samples, revealing the molecular basis of these functionally important tissues. The data generated from this study will provide fundamental knowledge on the reproductive biology of Ascaris and will inform future target identification for anti-ascariasis drugs and/or vaccines. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05602-2.
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spelling pubmed-97689522022-12-22 Transcriptome profiling of male and female Ascaris lumbricoides reproductive tissues Phuphisut, Orawan Poodeepiyasawat, Akkarin Yoonuan, Tippayarat Watthanakulpanich, Dorn Chotsiri, Palang Reamtong, Onrapak Mousley, Angela Gobert, Geoffrey N. Adisakwattana, Poom Parasit Vectors Research BACKGROUND: Ascaris lumbricoides causes human ascariasis, the most prevalent helminth disease, infecting approximately 1 billion individuals globally. In 2019 the global disease burden was estimated to be 754,000 DALYs and resulted in 2090 deaths. In the absence of a vaccination strategy, treatment of ascariasis has relied on anthelminthic chemotherapy, but drug resistance is a concern. The propensity for reinfection is also a major challenge to disease control; female worms lay up to 200,000 eggs daily, which contaminate surrounding environments and remain viable for years, resulting in high transmission rates. Understanding the molecular mechanisms of reproductive processes, including control of egg production, spermatogenesis, oogenesis and embryogenesis, will drive the development of new drugs and/or vaccine targets for future ascariasis control. METHODS: Transcriptome profiles of discrete reproductive and somatic tissue samples were generated from adult male and female worms using Illumina HiSeq with 2 × 150 bp paired-end sequencing. Male tissues included: testis germinal zone, testis part of vas deferens, seminal vesicle and somatic tissue. Female tissues included: ovary germinal zone, ovary part of the oviduct, uterus and somatic tissue. Differentially expressed genes (DEGs) were identified from the fragments per kilobases per million reads (FPKM) profiles. Hierarchical analysis was performed to identify tissue-specific genes. Furthermore, Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses were employed to identify significant terms and pathways for the DEGs. RESULTS: DEGs involved in protein phosphorylation and adhesion molecules were indicated to play a crucial role in spermatogenesis and fertilization, respectively. Those genes associated with the G-protein-coupled receptor (GPCR) signaling pathway and small GTPase-mediated signal transduction pathway play an essential role in cytoskeleton organization during oogenesis. Additionally, DEGs associated with the SMA genes and TGF-β signaling pathway are crucial in adult female embryogenesis. Some genes associated with particular biological processes and pathways that were identified in this study have been linked to defects in germline development, embryogenesis and reproductive behavior. In the enriched KEGG pathway analysis, Hippo signaling, oxytocin signaling and tight junction pathways were identified to play a role in Ascaris male and female reproductive systems. CONCLUSIONS: This study has provided comprehensive transcriptome profiles of discrete A. lumbricoides reproductive tissue samples, revealing the molecular basis of these functionally important tissues. The data generated from this study will provide fundamental knowledge on the reproductive biology of Ascaris and will inform future target identification for anti-ascariasis drugs and/or vaccines. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05602-2. BioMed Central 2022-12-20 /pmc/articles/PMC9768952/ /pubmed/36539906 http://dx.doi.org/10.1186/s13071-022-05602-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Phuphisut, Orawan
Poodeepiyasawat, Akkarin
Yoonuan, Tippayarat
Watthanakulpanich, Dorn
Chotsiri, Palang
Reamtong, Onrapak
Mousley, Angela
Gobert, Geoffrey N.
Adisakwattana, Poom
Transcriptome profiling of male and female Ascaris lumbricoides reproductive tissues
title Transcriptome profiling of male and female Ascaris lumbricoides reproductive tissues
title_full Transcriptome profiling of male and female Ascaris lumbricoides reproductive tissues
title_fullStr Transcriptome profiling of male and female Ascaris lumbricoides reproductive tissues
title_full_unstemmed Transcriptome profiling of male and female Ascaris lumbricoides reproductive tissues
title_short Transcriptome profiling of male and female Ascaris lumbricoides reproductive tissues
title_sort transcriptome profiling of male and female ascaris lumbricoides reproductive tissues
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9768952/
https://www.ncbi.nlm.nih.gov/pubmed/36539906
http://dx.doi.org/10.1186/s13071-022-05602-2
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