Caspase-1 participates in apoptosis of salivary glands in Rhipicephalus haemaphysaloides

Yu, Xinmao; Zhou, Yongzhi; Cao, Jie; Zhang, Houshuang; Gong, Haiyan; Zhou, Jinlin

doi:10.1186/s13071-017-2161-1

Cited by 23 publications

(19 citation statements)

References 67 publications

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“…During feeding, the SGs undergo marked changes. These include increased protein synthesis as well as induction of apoptotic and autophagic responses (30,37). In addition, the size of the type 2 and 3 acini increases in comparison to that of type 1 acini during tick blood feeding (29).…”

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confidence: 99%

Dissecting Flavivirus Biology in Salivary Gland Cultures from Fed and UnfedIxodes scapularis(Black-Legged Tick)

Grabowski¹,

Nilsson²,

Fischer

et al. 2019

mBio

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The Ixodes scapularis tick transmits a number of pathogens, including tick-borne flaviviruses (TBFVs). In the United States, confirmed human infections with the Powassan virus (POWV) TBFV have a fatality rate of ∼10% and are increasing in incidence. Tick salivary glands (SGs) serve as an organ barrier to TBFV transmission, and little is known regarding the location of TBFV infection in SGs from fed ticks. Previous studies showed I. scapularis vanin (VNN) involved with TBFV infection of I. scapularis ISE6 embryonic cells, suggesting a potential role for this gene. The overall goal of this study was to use SG cultures to compare data on TBFV biology in SGs from fully engorged, replete (fed) ticks and from unfed ticks. TBFV multiplication was higher in SGs from fed ticks than in those from unfed ticks. Virus-like particles were observed only in granular acini of SGs from unfed ticks. The location of TBFV infection of SGs from fed ticks was observed in cells lining lobular ducts and trachea but not observed in acini. Transcript knockdown of VNN decreased POWV multiplication in infected SG cultures from both fed and unfed ticks. This work was the first to identify localization of TBFV multiplication in SG cultures from a fed tick and a tick transcript important for POWV multiplication in the tick SG, an organ critical for TBFV transmission. This research exemplifies the use of SG cultures in deciphering TBFV biology in the tick and as a translational tool for screening and identifying potential tick genes as potential countermeasure targets. IMPORTANCE Tick-borne flaviviruses (TBFVs) are responsible for more than 15,000 human disease cases each year, and Powassan virus lineage 2 (POWV-L2) deer tick virus has been a reemerging threat in North America over the past 20 years. Rapid transmission of TBFVs in particular emphasizes the importance of preventing tick bites, the difficulty in developing countermeasures to prevent transmission, and the importance of understanding TBFV infection in tick salivary glands (SGs). Tick blood feeding is responsible for phenomenal physiological changes and is associated with changes in TBFV multiplication within the tick and in SGs. Using SG cultures from Ixodes scapularis female ticks, the primary aims of this study were to identify cellular localization of virus-like particles in acini of infected SGs from fed and unfed ticks, localization of TBFV infection in infected SGs from fed ticks, and a tick transcript (with associated metabolic function) involved in POWV-L2 infection in SG cultures.

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confidence: 99%

Dissecting Flavivirus Biology in Salivary Gland Cultures from Fed and UnfedIxodes scapularis(Black-Legged Tick)

Grabowski¹,

Nilsson²,

Fischer

et al. 2019

mBio

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“…On the other hand, autophagy is another pathway leading to apoptosis, with activity involvement of CPs, but controlled by ATG4 and ATG8. Recently, Yu et al (44) succeeded to identify two ATG8s. It is well known that caspase 1 plays a major role in salivary gland apoptosis of R. haemaphysaloides 3-4 days after tick attachment.…”

Section: Ticksmentioning

confidence: 99%

“…Although the investigators performed silencing RNAi technique to knock out the genes encoding caspases 1 and 8, they still observed apoptosis, but delayed. Accordingly, the investigators suggested that salivary gland apoptosis of R. haemaphysaloides is affected by both pathways; genes encoding caspases and ATGs (44) .…”

Section: Ticksmentioning

confidence: 99%

Expression of cysteine proteinases and cystatins in parasites and use of cysteine proteinase inhibitors in parasitic diseases. Part II: Arthropods

Abaza

2018

Parasitologists United Journal

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Most of the cysteine proteases (CPs) expressed by ectoparasites belong to the papain-like superfamily (clan CA, family C1) and are associated with the physiological events during different developmental life stages. Cathepsins, legumains/asparaginyl endopeptidases and caspases (clan CA, family C1, C13 and C14, respectively) play a major role in mosquito biology. There is accumulating evidence that CPs expressed by arthropods may play a role in clinical presentations of some transmitted parasitic disease, e.g. babesiosis. During blood meals, salivary glands secrete bioactive substances, including CPs, to exert several pharmacological properties that assist ectoparasites to evade host defense responses and to induce inflammatory reactions. Furthermore, they play an important role in extracellular and intracellular proteins degradation as well as their processing. In this regard, cystatins (CYSs) were found to inhibit insect CPs suggesting its use as targets for control of mites and ticks. The present review aims to identify different CPs expressed in ectoparasites, the main vectors of several endemic diseases such as malaria, babesiosis, Chagas' and Lyme disease. Meanwhile, it highlights different CYSs that could be used as biological insecticides to control diseases transmitted by mites and ticks.

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“…Although relatively well known in many organisms, information about caspases in ticks is scarce [33][34][35]. Since the roles of caspases in apoptosis are well known in animals, we postulated they might have a similar role in ticks [33][34][35][36]. However, in ticks and tick-borne diseases, the roles of caspases are poorly understood.…”

Section: Introductionmentioning

confidence: 97%

Initiator and executioner caspases in salivary gland apoptosis of Rhipicephalus haemaphysaloides

Wang

Tuerdi

et al. 2020

Parasites Vectors

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Background: Apoptosis is fundamental in maintaining cell balance in multicellular organisms, and caspases play a crucial role in apoptosis pathways. It is reported that apoptosis plays an important role in tick salivary gland degeneration. Several different caspases have been found in ticks, but the interactions between them are currently unknown. Here, we report three new caspases, isolated from the salivary glands of the tick Rhipicephalus haemaphysaloides. Methods: The full-length cDNA of the RhCaspases 7, 8 and 9 genes were obtained by transcriptome, and RhCaspases 7, 8 and 9 were expressed in E. coli; after protein purification and immunization in mice, specific polyclonal antibodies (PcAb) were created in response to the recombinant protein. Reverse-transcription quantitative PCR (RT-qPCR) and western blot were used to detect the existence of RhCaspases 7, 8 and 9 in ticks. TUNEL assays were used to determine the apoptosis level in salivary glands at different feeding times after gene silencing. The interaction between RhCaspases 7, 8 and 9 were identified by co-transfection assays. Results: The transcription of apoptosis-related genes in R. haemaphysaloides salivary glands increased significantly after tick engorgement. Three caspase-like molecules containing conserved caspase domains were identified and named RhCaspases 7, 8 and 9. RhCaspase8 and RhCaspase9 contain a long pro-domain at their N-terminals. An RT-qPCR assay demonstrated that the transcription of these three caspase genes increased significantly during the engorged periods of the tick developmental stages (engorged larval, nymph, and adult female ticks). Transcriptional levels of RhCaspases 7, 8 and 9 in salivary glands increased more significantly than other tissues post-engorgement. RhCaspase9-RNAi treatment significantly inhibited tick feeding. In contrast, knockdown of RhCaspase7 and RhCas-pase8 had no influence on tick feeding. Compared to the control group, apoptosis levels were significantly reduced after interfering with RhCaspase 7, 8 and 9 expressions. Co-transfection assays showed RhCaspase7 was cleaved by RhCaspases 8 and 9, demonstrating that RhCaspases 8 and 9 are initiator caspases and RhCaspase7 is an executioner caspase. Conclusions: To the best of our knowledge, this is the first study to identify initiator and executioner caspases in ticks, confirm the interaction among them, and associate caspase activation with tick salivary gland degeneration.

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Caspase-1 participates in apoptosis of salivary glands in Rhipicephalus haemaphysaloides

Cited by 23 publications

References 67 publications

Dissecting Flavivirus Biology in Salivary Gland Cultures from Fed and UnfedIxodes scapularis(Black-Legged Tick)

Dissecting Flavivirus Biology in Salivary Gland Cultures from Fed and UnfedIxodes scapularis(Black-Legged Tick)

Expression of cysteine proteinases and cystatins in parasites and use of cysteine proteinase inhibitors in parasitic diseases. Part II: Arthropods

Initiator and executioner caspases in salivary gland apoptosis of Rhipicephalus haemaphysaloides

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