The role of complement in the tick cellular immune defense against the entomopathogenic fungus Metarhizium robertsii

Fiorotti, Jéssica; Urbanová, Veronika; Gôlo, Patrícia Silva; Bittencourt, Vânia Rita Elias Pinheiro; Kopáček, Petr

doi:10.1016/j.dci.2021.104234

Cited by 15 publications

(10 citation statements)

References 54 publications

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“…This specific and discriminatory role was proposed for TEP-1 in B. glabrata ( 56 ), and is supported by previous studies in arthropods, where unique TEPs are involved in clearing specific pathogens ( 33 , 54 , 77 , 91 – 96 ). The susceptibility trait of snails to schistosomes may not necessarily correlate to susceptibility to other pathogens, and it would be interesting to compare TEPs responses to various other pathogens or immune stressors.…”

Section: Discussionsupporting

confidence: 81%

Molecular characterization of thioester-containing proteins in Biomphalaria glabrata and their differential gene expression upon Schistosoma mansoni exposure

et al. 2022

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Schistosomiasis is a disease caused by trematode parasites of the genus Schistosoma that affects approximately 200 million people worldwide. Schistosomiasis has been a persistent problem in endemic areas as there is no vaccine available, currently used anti-helmintic medications do not prevent reinfection, and most concerning, drug resistance has been documented in laboratory and field isolates. Thus, alternative approaches to curtail this human disease are warranted. Understanding the immunobiology of the obligate intermediate host of these parasites, which include the freshwater snail Biomphalaria glabrata, may facilitate the development of novel methods to stop or reduce transmission to humans. Molecules from the thioester-containing protein (TEP) superfamily have been shown to be involved in immunological functions in many animals including corals and humans. In this study we identified, characterized, and compared TEP transcripts and their expression upon S. mansoni exposure in resistant and susceptible strains of B. glabrata snails. Results showed the expression of 11 unique TEPs in B. glabrata snails. These transcripts present high sequence identity at the nucleotide and putative amino acid levels between susceptible and resistant strains. Further analysis revealed differences in several TEPs’ constitutive expression levels between resistant and susceptible snail strains, with C3-1, C3-3, and CD109 having higher constitutive expression levels in the resistant (BS90) strain, whereas C3-2 and TEP-1 showed higher constitutive expression levels in the susceptible (NMRI) strain. Furthermore, TEP-specific response to S. mansoni miracidia exposure reiterated their differential expression, with resistant snails upregulating the expression of both TEP-4 and TEP-3 at 2 h and 48 h post-exposure, respectively. Further understanding the diverse TEP genes and their functions in invertebrate animal vectors will not only expand our knowledge in regard to this ancient family of immune proteins, but also offer the opportunity to identify novel molecular targets that could aid in the efforts to develop control methods to reduce schistosomiasis transmission.

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Section: Discussionsupporting

confidence: 81%

Molecular characterization of thioester-containing proteins in Biomphalaria glabrata and their differential gene expression upon Schistosoma mansoni exposure

et al. 2022

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“…Following microbial infection, tick hemocytes execute cell-mediated responses including phagocytosis, encapsulation, and nodulation, clearing microbes from the system (3)(4)(5)(6). The humoral arm of the tick immune system produces soluble effector molecules that activate the complement pathway, prophenoloxidase pathway, and melanization cascade and produce reactive oxygen and nitrogen species (7)(8)(9)(10)(11). Hemocytes also secrete effectors that eventually activate humoral responses (9,12).…”

Section: Introductionmentioning

confidence: 99%

Rickettsia parkeri hijacks tick hemocytes to manipulate cellular and humoral transcriptional responses

et al. 2023

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IntroductionBlood-feeding arthropods rely on robust cellular and humoral immunity to control pathogen invasion and replication. Tick hemocytes produce factors that can facilitate or suppress microbial infection and pathogenesis. Despite the importance of hemocytes in regulating microbial infection, understanding of their basic biology and molecular mechanisms remains limited.MethodsHere we combined histomorphology and functional analysis to identify five distinct phagocytic and non-phagocytic hemocyte populations circulating within the Gulf Coast tick Amblyomma maculatum.Results and discussionDepletion of phagocytic hemocytes using clodronate liposomes revealed their function in eliminating bacterial infection. We provide the first direct evidence that an intracellular tick-borne pathogen, Rickettsia parkeri, infects phagocytic hemocytes in Am. maculatum to modify tick cellular immune responses. A hemocyte-specific RNA-seq dataset generated from hemocytes isolated from uninfected and R. parkeri-infected partially blood-fed ticks generated ~40,000 differentially regulated transcripts, >11,000 of which were immune genes. Silencing two differentially regulated phagocytic immune marker genes (nimrod B2 and eater-two Drosophila homologs), significantly reduced hemocyte phagocytosis.ConclusionTogether, these findings represent a significant step forward in understanding how hemocytes regulate microbial homeostasis and vector competence.

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“…The reduced survival of CLD-depleted ticks following bacterial challenge further highlights the critical role of hemocytes in maintaining immune responses in ticks, consistent with immune impairments following CLD depletion seen in mosquitoes and Drosophila (32-33). While ours is the first functional validation of phagocytic hemocytes by CLD depletion in ticks, two studies used alternative approaches to inhibit hemocyte function and demonstrated reduced survival in ticks following bacterial challenge (6, 11). The outcome of our experiments and similar reports in other organisms highlight the functional conservation of these immune cells in invertebrates.…”

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Rickettsia parkeriHijacks Tick Hemocytes to Manipulate Cellular and Humoral Transcriptional Responses

Adegoke

Ribeiro

Brown

et al. 2022

Preprint

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Blood-feeding arthropods rely on robust cellular and humoral immunity to control pathogen invasion and replication. Tick hemocytes produce factors that can facilitate or suppress microbial infection and pathogenesis. Despite the importance of hemocytes in regulating microbial infection, understanding of their basic biology and molecular mechanisms remains limited. Here we combined histomorphology and functional analysis to identify five distinct phagocytic and non-phagocytic hemocyte populations circulating within the Gulf Coast tick Amblyomma maculatum. Depletion of phagocytic hemocytes using clodronate liposomes revealed their function in eliminating bacterial infection. We provide the first direct evidence that an intracellular tick-borne pathogen, Rickettsia parkeri, infects phagocytic hemocytes in Am. maculatum to modify tick cellular immune responses. A massive RNA-seq dataset generated from hemocytes isolated from uninfected and R. parkeri-infected partially blood-fed ticks generated ~40,000 differentially regulated transcripts, >11,000 of which were immune genes. Silencing two differentially regulated phagocytic immune marker genes (nimrod B2 and eater) significantly reduced hemocyte phagocytosis. Together, these findings represent a significant step forward in understanding how hemocytes regulate microbial homeostasis and vector competence.

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The role of complement in the tick cellular immune defense against the entomopathogenic fungus Metarhizium robertsii

Cited by 15 publications

References 54 publications

Molecular characterization of thioester-containing proteins in Biomphalaria glabrata and their differential gene expression upon Schistosoma mansoni exposure

Molecular characterization of thioester-containing proteins in Biomphalaria glabrata and their differential gene expression upon Schistosoma mansoni exposure

Rickettsia parkeri hijacks tick hemocytes to manipulate cellular and humoral transcriptional responses

Rickettsia parkeriHijacks Tick Hemocytes to Manipulate Cellular and Humoral Transcriptional Responses

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