Transcriptome profiling of male and female Ascaris lumbricoides reproductive tissues

Abstract 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, tr...

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Main Authors: Orawan Phuphisut, Akkarin Poodeepiyasawat, Tippayarat Yoonuan, Dorn Watthanakulpanich, Palang Chotsiri, Onrapak Reamtong, Angela Mousley, Geoffrey N. Gobert, Poom Adisakwattana
Format: Article
Language:English
Published: BMC 2022-12-01
Series:Parasites & Vectors
Subjects:
Online Access:https://doi.org/10.1186/s13071-022-05602-2
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author Orawan Phuphisut
Akkarin Poodeepiyasawat
Tippayarat Yoonuan
Dorn Watthanakulpanich
Palang Chotsiri
Onrapak Reamtong
Angela Mousley
Geoffrey N. Gobert
Poom Adisakwattana
author_facet Orawan Phuphisut
Akkarin Poodeepiyasawat
Tippayarat Yoonuan
Dorn Watthanakulpanich
Palang Chotsiri
Onrapak Reamtong
Angela Mousley
Geoffrey N. Gobert
Poom Adisakwattana
author_sort Orawan Phuphisut
collection DOAJ
description Abstract 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
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spelling doaj.art-1612e04a6f3443cc80444da1b0ab413f2022-12-25T12:06:46ZengBMCParasites & Vectors1756-33052022-12-0115111810.1186/s13071-022-05602-2Transcriptome profiling of male and female Ascaris lumbricoides reproductive tissuesOrawan Phuphisut0Akkarin Poodeepiyasawat1Tippayarat Yoonuan2Dorn Watthanakulpanich3Palang Chotsiri4Onrapak Reamtong5Angela Mousley6Geoffrey N. Gobert7Poom Adisakwattana8Department of Helminthology, Faculty of Tropical Medicine, Mahidol UniversityDepartment of Helminthology, Faculty of Tropical Medicine, Mahidol UniversityDepartment of Helminthology, Faculty of Tropical Medicine, Mahidol UniversityDepartment of Helminthology, Faculty of Tropical Medicine, Mahidol UniversityMahidol-Oxford Tropical Medicine Research Unit, Mahidol UniversityDepartment of Molecular Tropical Medicine and Genetics, Faculty of Tropical Medicine, Mahidol UniversitySchool of Biological Sciences, Queenʼs University BelfastSchool of Biological Sciences, Queenʼs University BelfastDepartment of Helminthology, Faculty of Tropical Medicine, Mahidol UniversityAbstract 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 Abstracthttps://doi.org/10.1186/s13071-022-05602-2Ascaris lumbricoidesGene expressionReproductive tissueRNA-SeqTranscriptomeTranscriptomics
spellingShingle Orawan Phuphisut
Akkarin Poodeepiyasawat
Tippayarat Yoonuan
Dorn Watthanakulpanich
Palang Chotsiri
Onrapak Reamtong
Angela Mousley
Geoffrey N. Gobert
Poom Adisakwattana
Transcriptome profiling of male and female Ascaris lumbricoides reproductive tissues
Parasites & Vectors
Ascaris lumbricoides
Gene expression
Reproductive tissue
RNA-Seq
Transcriptome
Transcriptomics
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 Ascaris lumbricoides
Gene expression
Reproductive tissue
RNA-Seq
Transcriptome
Transcriptomics
url https://doi.org/10.1186/s13071-022-05602-2
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