Porin Expression Profiles in Haemaphysalis longicornis Infected With Babesia microti

The porin gene is widely disseminated in various organisms and has a pivotal role in the regulation of pathogen infection in blood-sucking arthropods. However, to date, information on the porin gene from the Haemaphysalis longicornis tick, an important vector of human and animal diseases, remains un...

Full description

Bibliographic Details
Main Authors: Weiqing Zheng, Rika Umemiya-Shirafuji, Qian Zhang, Kiyoshi Okado, Paul Franck Adjou Moumouni, Hiroshi Suzuki, Haiying Chen, Mingming Liu, Xuenan Xuan
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-05-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fphys.2020.00502/full
id doaj-6a73a456f1af4c23874e6795b7a9d101
record_format Article
collection DOAJ
language English
format Article
sources DOAJ
author Weiqing Zheng
Weiqing Zheng
Rika Umemiya-Shirafuji
Qian Zhang
Kiyoshi Okado
Paul Franck Adjou Moumouni
Hiroshi Suzuki
Haiying Chen
Mingming Liu
Xuenan Xuan
spellingShingle Weiqing Zheng
Weiqing Zheng
Rika Umemiya-Shirafuji
Qian Zhang
Kiyoshi Okado
Paul Franck Adjou Moumouni
Hiroshi Suzuki
Haiying Chen
Mingming Liu
Xuenan Xuan
Porin Expression Profiles in Haemaphysalis longicornis Infected With Babesia microti
Frontiers in Physiology
Haemaphysalis longicornis
tick
Babesia microti
protozoan parasite
porin
expression profiles
author_facet Weiqing Zheng
Weiqing Zheng
Rika Umemiya-Shirafuji
Qian Zhang
Kiyoshi Okado
Paul Franck Adjou Moumouni
Hiroshi Suzuki
Haiying Chen
Mingming Liu
Xuenan Xuan
author_sort Weiqing Zheng
title Porin Expression Profiles in Haemaphysalis longicornis Infected With Babesia microti
title_short Porin Expression Profiles in Haemaphysalis longicornis Infected With Babesia microti
title_full Porin Expression Profiles in Haemaphysalis longicornis Infected With Babesia microti
title_fullStr Porin Expression Profiles in Haemaphysalis longicornis Infected With Babesia microti
title_full_unstemmed Porin Expression Profiles in Haemaphysalis longicornis Infected With Babesia microti
title_sort porin expression profiles in haemaphysalis longicornis infected with babesia microti
publisher Frontiers Media S.A.
series Frontiers in Physiology
issn 1664-042X
publishDate 2020-05-01
description The porin gene is widely disseminated in various organisms and has a pivotal role in the regulation of pathogen infection in blood-sucking arthropods. However, to date, information on the porin gene from the Haemaphysalis longicornis tick, an important vector of human and animal diseases, remains unknown. In this study, we identified the porin gene from H. longicornis and evaluated its expression levels in Babesia microti-infected and -uninfected H. longicornis ticks at developmental stages. We also analyzed porin functions in relation to both tick blood feeding and Babesia infection and the relationship between porin and porin-related apoptosis genes such as B-cell lymphoma (Bcl), cytochrome complex (Cytc), caspase 2 (Cas2), and caspase 8 (Cas8). The coding nucleotide sequence of H. longicornis porin cDNA was found to be 849 bp in length and encoded 282 amino acids. Domain analysis showed the protein to contain six determinants of voltage gating and two polypeptide binding sites. Porin mRNA levels were not significantly different between 1-day-laid and 7-day-laid eggs. In the nymphal stage, higher porin expression levels were found in unfed, 12-h-partially-fed (12 hPF), 1-day-partially-fed (1 dPF), 2 dPF nymphs and nymphs at 0 day post-engorgement (0 dAE) vs. nymphs at 2 dAE. Cytc and Cas2 mRNA levels were higher in 2 dPF nymphs in contrast to nymphs at 2 dAE. Porin expression levels appeared to be higher in the infected vs. uninfected nymphs during blood feeding except at 1 dPF and 0–1 dAE. Especially, the highest B. microti burden negatively affected porin mRNA levels in both nymphs and female adults. Porin knockdown affected body weight and Babesia infection levels and significantly downregulated the expression levels of Cytc and Bcl in H. longicornis female ticks. In addition, this study showed that infection levels of the B. microti Gray strain in nymphal and female H. longicornis peaked at or around engorgement from blood feeding to post engorgement. Taken together, the research conducted in this study suggests that H. longicornis porin might interfere with blood feeding and B. microti infection.
topic Haemaphysalis longicornis
tick
Babesia microti
protozoan parasite
porin
expression profiles
url https://www.frontiersin.org/article/10.3389/fphys.2020.00502/full
work_keys_str_mv AT weiqingzheng porinexpressionprofilesinhaemaphysalislongicornisinfectedwithbabesiamicroti
AT weiqingzheng porinexpressionprofilesinhaemaphysalislongicornisinfectedwithbabesiamicroti
AT rikaumemiyashirafuji porinexpressionprofilesinhaemaphysalislongicornisinfectedwithbabesiamicroti
AT qianzhang porinexpressionprofilesinhaemaphysalislongicornisinfectedwithbabesiamicroti
AT kiyoshiokado porinexpressionprofilesinhaemaphysalislongicornisinfectedwithbabesiamicroti
AT paulfranckadjoumoumouni porinexpressionprofilesinhaemaphysalislongicornisinfectedwithbabesiamicroti
AT hiroshisuzuki porinexpressionprofilesinhaemaphysalislongicornisinfectedwithbabesiamicroti
AT haiyingchen porinexpressionprofilesinhaemaphysalislongicornisinfectedwithbabesiamicroti
AT mingmingliu porinexpressionprofilesinhaemaphysalislongicornisinfectedwithbabesiamicroti
AT xuenanxuan porinexpressionprofilesinhaemaphysalislongicornisinfectedwithbabesiamicroti
_version_ 1724630021513936896
spelling doaj-6a73a456f1af4c23874e6795b7a9d1012020-11-25T03:17:47ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2020-05-011110.3389/fphys.2020.00502534845Porin Expression Profiles in Haemaphysalis longicornis Infected With Babesia microtiWeiqing Zheng0Weiqing Zheng1Rika Umemiya-Shirafuji2Qian Zhang3Kiyoshi Okado4Paul Franck Adjou Moumouni5Hiroshi Suzuki6Haiying Chen7Mingming Liu8Xuenan Xuan9National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, JapanThe Collaboration Unit for Field Epidemiology of State Key Laboratory for Infectious Disease Prevention and Control, Jiangxi Provincial Key Laboratory of Animal-origin and Vector-Borne Diseases, Nanchang Center for Disease Control and Prevention, Nanchang, ChinaNational Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, JapanThe Ophthalmology Department, The Second Affiliated Hospital of Nanchang University, Nanchang, ChinaNational Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, JapanNational Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, JapanNational Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, JapanThe Collaboration Unit for Field Epidemiology of State Key Laboratory for Infectious Disease Prevention and Control, Jiangxi Provincial Key Laboratory of Animal-origin and Vector-Borne Diseases, Nanchang Center for Disease Control and Prevention, Nanchang, ChinaNational Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, JapanNational Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, JapanThe porin gene is widely disseminated in various organisms and has a pivotal role in the regulation of pathogen infection in blood-sucking arthropods. However, to date, information on the porin gene from the Haemaphysalis longicornis tick, an important vector of human and animal diseases, remains unknown. In this study, we identified the porin gene from H. longicornis and evaluated its expression levels in Babesia microti-infected and -uninfected H. longicornis ticks at developmental stages. We also analyzed porin functions in relation to both tick blood feeding and Babesia infection and the relationship between porin and porin-related apoptosis genes such as B-cell lymphoma (Bcl), cytochrome complex (Cytc), caspase 2 (Cas2), and caspase 8 (Cas8). The coding nucleotide sequence of H. longicornis porin cDNA was found to be 849 bp in length and encoded 282 amino acids. Domain analysis showed the protein to contain six determinants of voltage gating and two polypeptide binding sites. Porin mRNA levels were not significantly different between 1-day-laid and 7-day-laid eggs. In the nymphal stage, higher porin expression levels were found in unfed, 12-h-partially-fed (12 hPF), 1-day-partially-fed (1 dPF), 2 dPF nymphs and nymphs at 0 day post-engorgement (0 dAE) vs. nymphs at 2 dAE. Cytc and Cas2 mRNA levels were higher in 2 dPF nymphs in contrast to nymphs at 2 dAE. Porin expression levels appeared to be higher in the infected vs. uninfected nymphs during blood feeding except at 1 dPF and 0–1 dAE. Especially, the highest B. microti burden negatively affected porin mRNA levels in both nymphs and female adults. Porin knockdown affected body weight and Babesia infection levels and significantly downregulated the expression levels of Cytc and Bcl in H. longicornis female ticks. In addition, this study showed that infection levels of the B. microti Gray strain in nymphal and female H. longicornis peaked at or around engorgement from blood feeding to post engorgement. Taken together, the research conducted in this study suggests that H. longicornis porin might interfere with blood feeding and B. microti infection.https://www.frontiersin.org/article/10.3389/fphys.2020.00502/fullHaemaphysalis longicornistickBabesia microtiprotozoan parasiteporinexpression profiles