Differential gene expression in Anopheles stephensi following infection with drug-resistant Plasmodium yoelii

Abstract Background The transmission of drug-resistant parasites by the mosquito may be influenced by the altered biological fitness of drug-resistant parasites and different immune reactions or metabolic change in the mosquito. At this point, little is known about the variations in mosquito immunit...

Full description

Bibliographic Details
Main Authors: Jingru Zhang, Jiacheng Huang, Feng Zhu, Jian Zhang
Format: Article
Language:English
Published: BMC 2017-08-01
Series:Parasites & Vectors
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13071-017-2326-y
_version_ 1818519591686504448
author Jingru Zhang
Jiacheng Huang
Feng Zhu
Jian Zhang
author_facet Jingru Zhang
Jiacheng Huang
Feng Zhu
Jian Zhang
author_sort Jingru Zhang
collection DOAJ
description Abstract Background The transmission of drug-resistant parasites by the mosquito may be influenced by the altered biological fitness of drug-resistant parasites and different immune reactions or metabolic change in the mosquito. At this point, little is known about the variations in mosquito immunity and metabolism when mosquitoes are infected with drug-resistant parasites. To understand the differential gene expression in Anopheles following infection with drug-resistant Plasmodium, we conducted a genome-wide transcriptomic profiling analysis of Anopheles stephensi following feeding on mice with drug-resistant or drug-sensitive P. yoelii, observed changes in gene expression profiles and identified transcripts affected by the drug-resistant parasite. Results To study the impact of drug-resistant Plasmodium infections on An. stephensi gene transcription, we analyzed the three major transition stages of Plasmodium infections: at 24 h and 13 and 19 days after blood-feeding. Six cDNA libraries (R-As24h, R-As13d, R-As19d,S-As24h, S-As13dand S-As19d) were constructed, and RNA sequencing was subsequently performed. In total, approximately 50.1 million raw reads, 47.9 million clean reads and 7.18G clean bases were obtained. Following differentially expressed gene (DEG) analysis, GO enrichment analysis of DEGs, and functional classification by KEGG, we showed that the variations in gene expression in An. stephensi infected by the drug-resistant P. yoelii NSM occurred mainly at 13 days after blood meal during sporozoite migration through the hemolymph. The differentially expressed genes included those functioning in some important immune reaction and iron metabolism pathways, such as pattern recognition receptors, regulators of the JNK pathway, components of the phagosome pathway, regulators of the melanization response, activators of complement reactions, insulin signaling cascade members, oxidative stress and detoxification proteins. Conclusions Our study shows that drug-resistant P. yoelii NSM has an impact on the transcript abundance levels of An.stephensi mostly at 13 days after blood meal during sporozoite migration through the hemolymph and that most differentially expressed genes were downregulated. Our results highlight the need for a better understanding of selective pressures from these differentially expressed genes of the drug-resistant Plasmodium in the mosquito and the different transmission patterns of drug-resistant Plasmodium by Anopheles.
first_indexed 2024-12-11T01:26:14Z
format Article
id doaj.art-3633d743c70d4f4cbb7942d7926a8dec
institution Directory Open Access Journal
issn 1756-3305
language English
last_indexed 2024-12-11T01:26:14Z
publishDate 2017-08-01
publisher BMC
record_format Article
series Parasites & Vectors
spelling doaj.art-3633d743c70d4f4cbb7942d7926a8dec2022-12-22T01:25:30ZengBMCParasites & Vectors1756-33052017-08-0110111010.1186/s13071-017-2326-yDifferential gene expression in Anopheles stephensi following infection with drug-resistant Plasmodium yoeliiJingru Zhang0Jiacheng Huang1Feng Zhu2Jian Zhang3Department of Pathobiology, the Third Military Medical UniversityStudents brigade 5, The Third Military Medical UniversityDepartment of Pathobiology, the Third Military Medical UniversityDepartment of Pathobiology, the Third Military Medical UniversityAbstract Background The transmission of drug-resistant parasites by the mosquito may be influenced by the altered biological fitness of drug-resistant parasites and different immune reactions or metabolic change in the mosquito. At this point, little is known about the variations in mosquito immunity and metabolism when mosquitoes are infected with drug-resistant parasites. To understand the differential gene expression in Anopheles following infection with drug-resistant Plasmodium, we conducted a genome-wide transcriptomic profiling analysis of Anopheles stephensi following feeding on mice with drug-resistant or drug-sensitive P. yoelii, observed changes in gene expression profiles and identified transcripts affected by the drug-resistant parasite. Results To study the impact of drug-resistant Plasmodium infections on An. stephensi gene transcription, we analyzed the three major transition stages of Plasmodium infections: at 24 h and 13 and 19 days after blood-feeding. Six cDNA libraries (R-As24h, R-As13d, R-As19d,S-As24h, S-As13dand S-As19d) were constructed, and RNA sequencing was subsequently performed. In total, approximately 50.1 million raw reads, 47.9 million clean reads and 7.18G clean bases were obtained. Following differentially expressed gene (DEG) analysis, GO enrichment analysis of DEGs, and functional classification by KEGG, we showed that the variations in gene expression in An. stephensi infected by the drug-resistant P. yoelii NSM occurred mainly at 13 days after blood meal during sporozoite migration through the hemolymph. The differentially expressed genes included those functioning in some important immune reaction and iron metabolism pathways, such as pattern recognition receptors, regulators of the JNK pathway, components of the phagosome pathway, regulators of the melanization response, activators of complement reactions, insulin signaling cascade members, oxidative stress and detoxification proteins. Conclusions Our study shows that drug-resistant P. yoelii NSM has an impact on the transcript abundance levels of An.stephensi mostly at 13 days after blood meal during sporozoite migration through the hemolymph and that most differentially expressed genes were downregulated. Our results highlight the need for a better understanding of selective pressures from these differentially expressed genes of the drug-resistant Plasmodium in the mosquito and the different transmission patterns of drug-resistant Plasmodium by Anopheles.http://link.springer.com/article/10.1186/s13071-017-2326-yDifferential gene expressionAnophelesDrug-resistant Plasmodium
spellingShingle Jingru Zhang
Jiacheng Huang
Feng Zhu
Jian Zhang
Differential gene expression in Anopheles stephensi following infection with drug-resistant Plasmodium yoelii
Parasites & Vectors
Differential gene expression
Anopheles
Drug-resistant Plasmodium
title Differential gene expression in Anopheles stephensi following infection with drug-resistant Plasmodium yoelii
title_full Differential gene expression in Anopheles stephensi following infection with drug-resistant Plasmodium yoelii
title_fullStr Differential gene expression in Anopheles stephensi following infection with drug-resistant Plasmodium yoelii
title_full_unstemmed Differential gene expression in Anopheles stephensi following infection with drug-resistant Plasmodium yoelii
title_short Differential gene expression in Anopheles stephensi following infection with drug-resistant Plasmodium yoelii
title_sort differential gene expression in anopheles stephensi following infection with drug resistant plasmodium yoelii
topic Differential gene expression
Anopheles
Drug-resistant Plasmodium
url http://link.springer.com/article/10.1186/s13071-017-2326-y
work_keys_str_mv AT jingruzhang differentialgeneexpressioninanophelesstephensifollowinginfectionwithdrugresistantplasmodiumyoelii
AT jiachenghuang differentialgeneexpressioninanophelesstephensifollowinginfectionwithdrugresistantplasmodiumyoelii
AT fengzhu differentialgeneexpressioninanophelesstephensifollowinginfectionwithdrugresistantplasmodiumyoelii
AT jianzhang differentialgeneexpressioninanophelesstephensifollowinginfectionwithdrugresistantplasmodiumyoelii