Localized expression and inhibition effect of miR-184 on blood digestion and oviposition in Haemaphysalis longicornis (Acari: Ixodidae)

Abstract Background The hard tick Haemaphysalis longicornis (Ixodidae) is widely distributed in East Asia, China, Australia and New Zealand. It can transmit many infectious pathogens, including the causative agents of human rickettsiosis, bovine theileriosis, bovine babesiosis and canine babesiosis....

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Main Authors: Muhammad Irfan Malik, Mohsin Nawaz, Yanan Wang, Houshuang Zhang, Jie Cao, Yongzhi Zhou, Ibrahim A. Hassan, Md. Nazrul Islam, Muhammad Naveed Anwar, Jinlin Zhou
Format: Article
Language:English
Published: BMC 2019-10-01
Series:Parasites & Vectors
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13071-019-3754-7
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author Muhammad Irfan Malik
Mohsin Nawaz
Yanan Wang
Houshuang Zhang
Jie Cao
Yongzhi Zhou
Ibrahim A. Hassan
Md. Nazrul Islam
Muhammad Naveed Anwar
Jinlin Zhou
author_facet Muhammad Irfan Malik
Mohsin Nawaz
Yanan Wang
Houshuang Zhang
Jie Cao
Yongzhi Zhou
Ibrahim A. Hassan
Md. Nazrul Islam
Muhammad Naveed Anwar
Jinlin Zhou
author_sort Muhammad Irfan Malik
collection DOAJ
description Abstract Background The hard tick Haemaphysalis longicornis (Ixodidae) is widely distributed in East Asia, China, Australia and New Zealand. It can transmit many infectious pathogens, including the causative agents of human rickettsiosis, bovine theileriosis, bovine babesiosis and canine babesiosis. Therefore, a greater understanding of H. longicornis biology might aid in the development of more effective control measures against the tick and tick-borne pathogens. Methods We analyzed the expression of miR-184 in different developmental stages and various tissues of H. longicornis using real-time PCR (qRT-PCR). Antagomir (Ant-184) was used to knock-down miR-184, whilst Ms-Ant and non-injected ticks were used as the negative and blank controls, respectively. We used online software tools (RNAhybrid and TargetScan) to predict the putative target genes of miR-184. Results The expression of miR-184 was highest in unfed nymphs and lowest in unfed larvae. The tissue distribution of miR-184 showed abundant expression in the midgut. To investigate the probable roles of miR-184, antagomir (Ant-184) was used to knock-down miR-184 (t (4) = 12.32, P = 0.0002). After inhibiting miR-184, other biological factors were examined in each group. The engorged body weight was significantly reduced in the treated group (Ant-184) in contrast to control groups (t (22) = 2.19, P = 0.0388). The mean duration of the egg-laying days was significantly increased (33.5 ± 1.91) and the number of eggs (t (10) = 3.147, P = 0.0137), and egg mass (t (10) = 3.4472, P = 0.0063) were significantly reduced in the treated group. During oviposition, eggs were monitored and in half of the ticks of the Ant-184 group the eggs were completely desiccated, lacked embryo development and did not hatch. We analyzed the expression of Vg proteins (Vg1, Vg2, Vg3) in semi-engorged ticks, engorged ticks, ticks at day 2 after engorgement and egg stage in Ant-184, non-injected and Ms-Ant groups, and found significant variation. Conclusions This study provides information on the role of miR-184 in H. longicornis ticks. The data suggest that miR-184 targets Vg proteins and affects blood digestion and oviposition.
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spelling doaj.art-e0b9d571055f4201b430a7959ea43d922022-12-21T18:59:11ZengBMCParasites & Vectors1756-33052019-10-011211810.1186/s13071-019-3754-7Localized expression and inhibition effect of miR-184 on blood digestion and oviposition in Haemaphysalis longicornis (Acari: Ixodidae)Muhammad Irfan Malik0Mohsin Nawaz1Yanan Wang2Houshuang Zhang3Jie Cao4Yongzhi Zhou5Ibrahim A. Hassan6Md. Nazrul Islam7Muhammad Naveed Anwar8Jinlin Zhou9Key Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, Chinese Academy of Agricultural SciencesKey Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, Chinese Academy of Agricultural SciencesKey Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, Chinese Academy of Agricultural SciencesKey Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, Chinese Academy of Agricultural SciencesKey Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, Chinese Academy of Agricultural SciencesKey Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, Chinese Academy of Agricultural SciencesKey Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, Chinese Academy of Agricultural SciencesKey Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, Chinese Academy of Agricultural SciencesKey Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, Chinese Academy of Agricultural SciencesKey Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, Chinese Academy of Agricultural SciencesAbstract Background The hard tick Haemaphysalis longicornis (Ixodidae) is widely distributed in East Asia, China, Australia and New Zealand. It can transmit many infectious pathogens, including the causative agents of human rickettsiosis, bovine theileriosis, bovine babesiosis and canine babesiosis. Therefore, a greater understanding of H. longicornis biology might aid in the development of more effective control measures against the tick and tick-borne pathogens. Methods We analyzed the expression of miR-184 in different developmental stages and various tissues of H. longicornis using real-time PCR (qRT-PCR). Antagomir (Ant-184) was used to knock-down miR-184, whilst Ms-Ant and non-injected ticks were used as the negative and blank controls, respectively. We used online software tools (RNAhybrid and TargetScan) to predict the putative target genes of miR-184. Results The expression of miR-184 was highest in unfed nymphs and lowest in unfed larvae. The tissue distribution of miR-184 showed abundant expression in the midgut. To investigate the probable roles of miR-184, antagomir (Ant-184) was used to knock-down miR-184 (t (4) = 12.32, P = 0.0002). After inhibiting miR-184, other biological factors were examined in each group. The engorged body weight was significantly reduced in the treated group (Ant-184) in contrast to control groups (t (22) = 2.19, P = 0.0388). The mean duration of the egg-laying days was significantly increased (33.5 ± 1.91) and the number of eggs (t (10) = 3.147, P = 0.0137), and egg mass (t (10) = 3.4472, P = 0.0063) were significantly reduced in the treated group. During oviposition, eggs were monitored and in half of the ticks of the Ant-184 group the eggs were completely desiccated, lacked embryo development and did not hatch. We analyzed the expression of Vg proteins (Vg1, Vg2, Vg3) in semi-engorged ticks, engorged ticks, ticks at day 2 after engorgement and egg stage in Ant-184, non-injected and Ms-Ant groups, and found significant variation. Conclusions This study provides information on the role of miR-184 in H. longicornis ticks. The data suggest that miR-184 targets Vg proteins and affects blood digestion and oviposition.http://link.springer.com/article/10.1186/s13071-019-3754-7Haemaphysalis longicornismiR-184VitellogeninBlood digestionOviposition
spellingShingle Muhammad Irfan Malik
Mohsin Nawaz
Yanan Wang
Houshuang Zhang
Jie Cao
Yongzhi Zhou
Ibrahim A. Hassan
Md. Nazrul Islam
Muhammad Naveed Anwar
Jinlin Zhou
Localized expression and inhibition effect of miR-184 on blood digestion and oviposition in Haemaphysalis longicornis (Acari: Ixodidae)
Parasites & Vectors
Haemaphysalis longicornis
miR-184
Vitellogenin
Blood digestion
Oviposition
title Localized expression and inhibition effect of miR-184 on blood digestion and oviposition in Haemaphysalis longicornis (Acari: Ixodidae)
title_full Localized expression and inhibition effect of miR-184 on blood digestion and oviposition in Haemaphysalis longicornis (Acari: Ixodidae)
title_fullStr Localized expression and inhibition effect of miR-184 on blood digestion and oviposition in Haemaphysalis longicornis (Acari: Ixodidae)
title_full_unstemmed Localized expression and inhibition effect of miR-184 on blood digestion and oviposition in Haemaphysalis longicornis (Acari: Ixodidae)
title_short Localized expression and inhibition effect of miR-184 on blood digestion and oviposition in Haemaphysalis longicornis (Acari: Ixodidae)
title_sort localized expression and inhibition effect of mir 184 on blood digestion and oviposition in haemaphysalis longicornis acari ixodidae
topic Haemaphysalis longicornis
miR-184
Vitellogenin
Blood digestion
Oviposition
url http://link.springer.com/article/10.1186/s13071-019-3754-7
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