Evidence of the role of tick subolesin in gene expression

Fuente, José de la; Maritz-Olivier, Christine; Naranjo, Victoria; Ayoubi, Patricia; Nijhof, Ard M.; Almazán, Consuelo; Canales, Mario; Lastra, José Manuel Pérez de la; Galindo, Ruth C.; Blouin, Edmour F.; Gortázar, Christian; Jongejan, Frans; Kocan, Katherine M.

doi:10.1186/1471-2164-9-372

Cited by 83 publications

(89 citation statements)

References 30 publications

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“…Although subolesin and akirin function as transcription regulatory factors and should therefore be located in cell nuclei (14,(56)(57)(58)63), the results shown herein suggest, as did previous experiments (25), that at least for tick subolesin, the protein is also present in the cell cytoplasm. This result agrees with the hypothesized role for tick subolesin in different pathways that help to provide an understanding of the effect of gene knockdown by RNAi and vaccination (13,14).…”

Section: Discussionsupporting

confidence: 73%

Anaplasma phagocytophilum Inhibits Apoptosis and Promotes Cytoskeleton Rearrangement for Infection of Tick Cells

et al. 2013

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dAnaplasma phagocytophilum causes human granulocytic anaplasmosis. Infection with this zoonotic pathogen affects gene expression in both the vertebrate host and the tick vector, Ixodes scapularis. Here, we identified new genes, including spectrin alpha chain or alpha-fodrin (CG8) and voltage-dependent anion-selective channel or mitochondrial porin (T2), that are involved in A. phagocytophilum infection/multiplication and the tick cell response to infection. The pathogen downregulated the expression of CG8 in tick salivary glands and T2 in both the gut and salivary glands to inhibit apoptosis as a mechanism to subvert host cell defenses and increase infection. In the gut, the tick response to infection through CG8 upregulation was used by the pathogen to increase infection due to the cytoskeleton rearrangement that is required for pathogen infection. These results increase our understanding of the role of tick genes during A. phagocytophilum infection and multiplication and demonstrate that the pathogen uses similar strategies to establish infection in both vertebrate and invertebrate hosts.T icks are ectoparasites of animals and humans and are considered to be the most important arthropod vector of pathogens in some regions (1). Ixodes scapularis Say (Acari: Ixodidae) is an important vector of pathogens that infect and cause disease in humans and domestic animals in the United States. Anaplasma phagocytophilum (Rickettsiales: Anaplasmataceae), the focus of this study, is the causative agent of human, canine, and equine granulocytic anaplasmosis and tick-borne fever of ruminants (2, 3).A. phagocytophilum is an intracellular bacterium that infects vertebrate host neutrophils, where it multiplies within a parasitophorous vacuole, thus evading host defenses while inhibiting apoptosis and promoting cytoskeleton rearrangement for infection and multiplication (4-8). Tick-A. phagocytophilum interactions are not as well characterized as those between pathogen and vertebrate hosts (4). While A. phagocytophilum has been shown to infect I. scapularis gut cells (9) and salivary glands (10), the developmental cycle of this pathogen has not been described in ticks. Tick proteins such as Salp16, subolesin, antifreeze glycoprotein IAFGP, and alpha1-3-fucosyltransferease were differentially regulated and required for A. phagocytophilum infection of I. scapularis (10-20). Activation of heat shock proteins and other stress response proteins in ticks and cultured tick cells in response to A. phagocytophilum infection was also characterized by proteomics and transcriptomics analyses (21).The overall goal of our research is to characterize molecular interactions at the vector-pathogen interface and develop vaccines for the control of tick infestations and pathogen infection/transmission. Our hypothesis is that tick genes differentially expressed in response to pathogen infection would include those involved in pathogen infection, multiplication, and transmission, as well as in the tick protective response to infection. In this researc...

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Section: Discussionsupporting

confidence: 73%

Anaplasma phagocytophilum Inhibits Apoptosis and Promotes Cytoskeleton Rearrangement for Infection of Tick Cells

et al. 2013

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“…Tick subolesin was shown to be an intracellular protein evolutionary conserved in invertebrate and vertebrate organisms (de la Fuente et al 2006b;Galindo et al 2009). Recent results suggest that subolesin is involved in regulation of gene expression, modulation of feeding, and tick reproduction and development (de la Fuente et al 2006a(de la Fuente et al , 2008bGalindo et al 2009). …”

Section: Introductionmentioning

confidence: 99%

Conservation and immunogenicity of the mosquito ortholog of the tick-protective antigen, subolesin

et al. 2009

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The control of arthropod vectors of pathogens that affect human and animal health is important for the eradication of vector-borne diseases. The ortholog of the tick-protective antigen, subolesin, was identified in Aedes albopictus and found to have conserved epitopes in ticks and mosquitoes. RNA interference with the tick and mosquito double-stranded RNA in three tick species resulted in significant gene knockdown and decreased tick weight and/or survival. Feeding Anopheles atroparvus, Aedes caspius, and Culex pipiens female mosquitoes on an A. albopictus subolesin hyperimmune serum resulted in 11 +/- 5% to 29 +/- 6% survival inhibition when compared to controls fed on preimmune serum. Feeding sand flies, Phlebotomus perniciosus, on antimosquito subolesin ortholog protein antibodies inhibited female survival and the number of larvae and adults obtained after hatching by 28 +/- 22% and 16 +/- 3%, respectively, when compared to controls. Vaccination with tick and mosquito subolesin ortholog proteins significantly reduced Ixodes scapularis tick infestation and weight in a similar way. However, vaccination with the recombinant mosquito subolesin ortholog antigen did not protect against Amblyomma americanum and Rhipicephalus sanguineus tick infestations. Collectively, these preliminary results provided the first evidence that development of vaccines may be possible for control of multiple arthropod vectors using subolesin orthologs but suggested that multiple antigens may be required to produce an effective vaccine.

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“…The mechanism of dsRNA-induced RNAi in ticks should be refined to contribute to a better understanding and utilization of this genetic approach in this species 35,36 . The extent of off-target effects of RNAi in ticks is also an important question that needs to be fully addressed 14,27 . Finally, RNAi will most likely provide comprehensive contributions to the study of tick gene regulation and systems biology and the tick-pathogen interface and may have an impact on the development of vaccines to control tick infestations and the transmission of tick-borne pathogens.…”

Section: Discussionmentioning

confidence: 99%

RNA Interference in Ticks

Kocan

Blouin

Fuente

2011

JoVE

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Ticks are obligate hematophagous ectoparasites of wild and domestic animals and humans, and are considered to be second worldwide to mosquitoes as vectors of human diseases 1 and the most important vectors affecting cattle industry worldwide 2 . Ticks are classified in the subclass Acari, order Parasitiformes, suborder Ixodida and are distributed worldwide from Arctic to tropical regions 3 . Despite efforts to control tick infestations, these ectoparasites remain a serious problem for human and animal health 4,5 .RNA interference (RNAi) 6 is a nucleic acid-based reverse genetic approach that involves disruption of gene expression in order to determine gene function or its effect on a metabolic pathway. Small interfering RNAs (siRNAs) are the effector molecules of the RNAi pathway that is initiated by double-stranded RNA (dsRNA) and results in a potent sequence-specific degradation of cytoplasmic mRNAs containing the same sequence as the dsRNA trigger [7][8][9] . Post-transcriptional gene silencing mechanisms initiated by dsRNA have been discovered in all eukaryotes studied thus far, and RNAi has been rapidly developed in a variety of organisms as a tool for functional genomics studies and other applications 10

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Evidence of the role of tick subolesin in gene expression

Cited by 83 publications

References 30 publications

Anaplasma phagocytophilum Inhibits Apoptosis and Promotes Cytoskeleton Rearrangement for Infection of Tick Cells

Anaplasma phagocytophilum Inhibits Apoptosis and Promotes Cytoskeleton Rearrangement for Infection of Tick Cells

Conservation and immunogenicity of the mosquito ortholog of the tick-protective antigen, subolesin

RNA Interference in Ticks

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