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Feeding by Amblyomma maculatum (Acari: Ixodidae) enhances Rickettsia parkeri (Rickettsiales: Rickettsiaceae) infection in the skin.
J. Med. Entomol.
PUBLISHED: 08-15-2014
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Rickettsia parkeri Luckman (Rickettsiales: Rickettsiaceae), a member of the spotted fever group of Rickettsia, is the tick-borne causative agent of a newly recognized, eschar-associated rickettsiosis. Because of its relatively recent designation as a pathogen, few studies have examined the pathogenesis of transmission of R. parkeri to the vertebrate host. To further elucidate the role of tick feeding in rickettsial infection of vertebrates, nymphal Amblyomma maculatum Koch (Acari: Ixodidae) were fed on C3H/HeJ mice intradermally inoculated with R. parkeri (Portsmouth strain). The ticks were allowed to feed to repletion, at which time samples were taken for histopathology, immunohistochemistry (IHC), quantitative polymerase chain reaction (qPCR) for rickettsial quantification, and reverse transcriptase polymerase chain reaction (RT-PCR) for expression of Itgax, Mcp1, and Il1beta. The group of mice that received intradermal inoculation of R. parkeri with tick feeding displayed significant increases in rickettsial load and IHC staining, but not in cytokine expression, when compared with the group of mice that received intradermal inoculation of R. parkeri without tick feeding. Tick feeding alone was associated with histopathologic changes in the skin, but these changes, and particularly vascular pathology, were more pronounced in the skin of mice inoculated previously with R. parkeri and followed by tick feeding. The marked differences in IHC staining and qPCR for the R. parkeri with tick feeding group strongly suggest an important role for tick feeding in the early establishment of rickettsial infection in the skin.
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Growth of Rickettsia felis in Drosophila melanogaster S2 cells.
Vector Borne Zoonotic Dis.
PUBLISHED: 02-18-2014
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Rickettsia felis is an obligate, intracellular, Gram-negative bacterium and a member of the transitional group rickettsiae. This bacterium has been shown to grow in vitro in amphibian, tick, and mosquito cell lines. Here, we present data to show the growth of R. felis strain LSU in Drosophila melanogaster S2 cells, an embryonic, hemocytic cell line with phagocytic properties. R. felis LSU was isolated from Ixodes scapularis E6 (ISE6) cells and used to infect S2 cells, grown at 25°C. By 19 days postinfection, the S2 cells were 100% infected with R. felis as determined by Acridine Orange and Diff-Quik staining. A species-specific R. felis qPCR assay was used to demonstrate that the kinetics associated with the S2 cell culture infection involved a lag/adaptation phase, followed by continued growth to 20 days postinfection. Moreover, R. felis organisms were observed in the S2 cells using transmission electron microscopy and a polyclonal antibody against spotted fever rickettsiae. The ability to use D. melanogaster S2 cells for growing rickettsial agents is a useful tool owing to the ease of manipulation of the S2 cultures and the wide-ranging possibility of Drosophila resources available for future studies.
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Novel identification of Dermacentor variabilis Arp2/3 complex and its role in rickettsial infection of the arthropod vector.
PLoS ONE
PUBLISHED: 01-01-2014
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Tick-borne spotted fever group (SFG) Rickettsia species must be able to infect both vertebrate and arthropod host cells. The host actin-related protein 2/3 (Arp2/3) complex is important in the invasion process and actin-based motility for several intracellular bacteria, including SFG Rickettsia in Drosophila and mammalian cells. To investigate the role of the tick Arp2/3 complex in tick-Rickettsia interactions, open reading frames of all subunits of the protein including Arp2, Arp3, ARPC1, ARPC2, ARPC3, ARPC4, and ARPC5 were identified from Dermacentor variabilis. Amino acid sequence analysis showed variation (ranging from 25-88%) in percent identity compared to the corresponding subunits of the complex from Drosophila melanogaster, Mus musculus, Homo sapiens, and Saccharomyces cerevisiae. Potential ATP binding sites were identified in D. variabilis (Dv) Arp2 and Arp3 subunits as well as five putative WD (Trp-Asp) motifs which were observed in DvARPC1. Transcriptional profiles of all subunits of the DvArp2/3 complex revealed greater mRNA expression in both Rickettsia-infected and -uninfected ovary compared to midgut and salivary glands. In response to R. montanensis infection of the tick ovary, the mRNA level of only DvARPC4 was significantly upregulated compared to uninfected tissues. Arp2/3 complex inhibition bioassays resulted in a decrease in the ability of R. montanensis to invade tick tissues with a significant difference in the tick ovary, indicating a role for the Arp2/3 complex in rickettsial invasion of tick cells. Characterization of tick-derived molecules associated with rickettsial infection is imperative in order to better comprehend the ecology of tick-borne rickettsial diseases.
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Gene expression of tissue-specific molecules in ex vivo Dermacentor variabilis (Acari: Ixodidae) during rickettsial exposure.
J. Med. Entomol.
PUBLISHED: 11-05-2013
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Ticks serve as both vectors and the reservoir hosts capable of transmitting spotted fever group Rickettsia by horizontal and vertical transmission. Persistent maintenance of Rickettsia species in tick populations is dependent on the specificity of the tick and Rickettsia relationship that limits vertical transmission of particular Rickettsia species, suggesting host-derived mechanisms of control. Tick-derived molecules are differentially expressed in a tissue-specific manner in response to rickettsial infection; however, little is known about tick response to specific rickettsial species. To test the hypothesis that tissue-specific tick-derived molecules are uniquely responsive to rickettsial infection, a bioassay to characterize the tick tissue-specific response to different rickettsial species was used. Whole organs of Dermacentor variabilis (Say) were exposed to either Rickettsia montanensis or Rickettsia amblyommii, two Rickettsia species common, or absent, in field-collected D. variabilis, respectively, for 1 and 12 h and harvested for quantitative real time-polymerase chain reaction assays of putative immune-like tick-derived factors. The results indicated that tick genes are differently expressed in a temporal and tissue-specific manner. Genes encoding glutathione S-transferase 1 (dvgst1) and Kunitz protease inhibitor (dvkpi) were highly expressed in midgut, and rickettsial exposure downregulated the expression of both genes. Two other genes encoding glutathione S-transferase 2 (dvgst2) and beta-thymosin (dvpbeta-thy) were highly expressed in ovary, with dvbeta-thy expression significantly downregulated in ovaries exposed to R. montanensis, but not R. amblyommii, at 12-h postexposure, suggesting a selective response. Deciphering the tissue-specific molecular interactions between tick and Rickettsia will enhance our understanding of the key mechanisms that mediate rickettsial infection in ticks.
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Dissemination of bloodmeal acquired Rickettsia felis in cat fleas, Ctenocephalides felis.
Parasit Vectors
PUBLISHED: 04-17-2013
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BACKGROUND: Cat fleas, Ctenocephalides felis, are known biological vectors for Rickettsia felis. Rickettsial transmission can be vertical via transovarial transmission within a flea population, as well as horizontal between fleas through a bloodmeal. The previously undescribed infection kinetics of bloodmeal-acquired R. felis in cat fleas provides insight into the R. felis-flea interaction. FINDINGS: In the present study, dissemination of R. felis in previously uninfected cat fleas fed an R. felis-infected bloodmeal was investigated. At weekly intervals for 28 days, rickettsial propagation, accumulation, and dissemination in gut epithelial cells, specifically in the hindgut and the specialized cells in the neck region of midgut, were observed on paraffin sections of infected cat fleas by immunofluorescence assay (IFA) and confirmed by PCR detection of R. felis 17-kDa antigen gene. IFA results demonstrate ingested rickettsiae in vacuoles during early infection of the gut; lysosomal activity, indicated by lysosome marker staining of freshly-dissected gut, suggests the presence of phagolysosome-associated vacuoles. Subsequent to infection in the gut, rickettsiae spread to the hemocoel and other tissues including reproductive organs. Densely-packed rickettsiae forming mycetome-like structures were observed in the abdomen of infected male cat fleas during late infection. Ultrastructural analysis by transmission electron microscopy (TEM) confirmed the presence and infection characteristics of Rickettsia including rickettsial destruction in the phagolysosome, rickettsial division, and accumulation in the flea gut. CONCLUSIONS: This study intimately profiles R. felis dissemination in cat fleas and further illuminates the mechanisms of rickettsial transmission in nature.
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Horizontal transmission of Rickettsia felis between cat fleas, Ctenocephalides felis.
Mol. Ecol.
PUBLISHED: 10-04-2011
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Rickettsia felis is a rickettsial pathogen primarily associated with the cat flea, Ctenocephalides felis. Although laboratory studies have confirmed that R. felis is maintained by transstadial and transovarial transmission in C. felis, distinct mechanisms of horizontal transmission of R. felis among cat fleas are undefined. Based on the inefficient vertical transmission of R. felis by cat fleas and the detection of R. felis in a variety of haematophagous arthropods, we hypothesize that R. felis is horizontally transmitted between cat fleas. Towards testing this hypothesis, flea transmission of R. felis via a bloodmeal was assessed weekly for 4 weeks. Rhodamine B was used to distinguish uninfected recipient and R. felis-infected donor fleas in a rickettsial horizontal transmission bioassay, and quantitative real-time PCR assay was used to measure transmission frequency; immunofluorescence assay also confirmed transmission. Female fleas acquired R. felis infection more readily than male fleas after feeding on a R. felis-infected bloodmeal for 24 h (69.3% and 43.3%, respectively) and both Rickettsia-uninfected recipient male and female fleas became infected with R. felis after cofeeding with R. felis-infected donor fleas (3.3-40.0%). Distinct bioassays were developed to further determine that R. felis was transmitted from R. felis-infected to uninfected fleas during cofeeding and copulation. Vertical transmission of R. felis by infected fleas was not demonstrated in this study. The demonstration of horizontal transmission of R. felis between cat fleas has broad implications for the ecology of R. felis rickettsiosis.
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Isolation of a rickettsial pathogen from a non-hematophagous arthropod.
PLoS ONE
PUBLISHED: 01-25-2011
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Rickettsial diversity is intriguing in that some species are transmissible to vertebrates, while others appear exclusive to invertebrate hosts. Of particular interest is Rickettsia felis, identifiable in both stored product insect pests and hematophagous disease vectors. To understand rickettsial survival tactics in, and probable movement between, both insect systems will explicate the determinants of rickettsial pathogenicity. Towards this objective, a population of Liposcelis bostrychophila, common booklice, was successfully used for rickettsial isolation in ISE6 (tick-derived cells). Rickettsiae were also observed in L. bostrychophila by electron microscopy and in paraffin sections of booklice by immunofluorescence assay using anti-R. felis polyclonal antibody. The isolate, designated R. felis strain LSU-Lb, resembles typical rickettsiae when examined by microscopy. Sequence analysis of portions of the Rickettsia specific 17-kDa antigen gene, citrate synthase (gltA) gene, rickettsial outer membrane protein A (ompA) gene, and the presence of the R. felis plasmid in the cell culture isolate confirmed the isolate as R. felis. Variable nucleotide sequences from the isolate were obtained for R. felis-specific pRF-associated putative tldD/pmbA. Expression of rickettsial outer membrane protein B (OmpB) was verified in R. felis (LSU-Lb) using a monoclonal antibody. Additionally, a quantitative real-time PCR assay was used to identify a significantly greater median rickettsial load in the booklice, compared to cat flea hosts. With the potential to manipulate arthropod host biology and infect vertebrate hosts, the dual nature of R. felis provides an excellent model for the study of rickettsial pathogenesis and transmission. In addition, this study is the first isolation of a rickettsial pathogen from a non-hematophagous arthropod.
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Acquisition of Rickettsia felis by cat fleas during feeding.
Vector Borne Zoonotic Dis.
PUBLISHED: 01-09-2011
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Evidence for horizontal routes of transmission for Rickettsia felis has come from detection of R. felis infection in vertebrates and multiple blood-feeding arthropods; however, infection of cat fleas, Ctenocephalides felis, during blood feeding has not been demonstrated. In this study, the ability of cat fleas to acquire R. felis through an infectious blood meal with subsequent vertical transmission was examined. Utilizing an artificial feeding system, Rickettsia-naive fleas were exposed to R. felis-infected blood meals and monitored for subsequent infection at weekly intervals for 4 weeks. At 7 days postexposure (dpe) ~52% of fleas successfully acquired rickettsiae and R. felis DNA; rickettsial transcript and DNA was detected in cat flea feces. Quantitative real-time polymerase chain reaction determined that both the R. felis infection load and R. felis infection density was significantly greater in fleas assessed at later time points. Although a persistent R. felis infection was detected in adult fleas, R. felis infection was not observed in F(1) progeny. This study demonstrates that cat fleas are able to acquire R. felis infection from an infectious blood meal and will serve as a model to examine R. felis transmission between arthropod and vertebrate hosts.
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Development of microsatellites for genetic analyses and population assignment of the cat flea (Siphonaptera: Pulicidae).
J. Med. Entomol.
PUBLISHED: 12-24-2010
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Cat fleas, Ctenocephalidesfelis (Bouché) (Siphonaptera: Pulicidae), are common ectoparasites of companion animals that negatively impact their hosts directly by causing dermatitis and blood loss during feeding and indirectly through the potential transmission of disease causing agents. We isolated and characterized seven novel microsatellite loci from a partial genomic library of the cat flea enriched for di-, tri-, and tetranucleotide repeats. We screened these loci in cat fleas from two laboratory colonies and one wild-caught population collected at a temporary animal shelter (Parker coliseum) in Baton Rouge, LA. Six loci were polymorphic, with two to 15 alleles per locus and an average observed heterozygosity of 0.21 across populations. Although the two laboratory cat flea colonies were isolated from each other for many years, they did not significantly differ in their genotypic composition. The cat flea population from Parker coliseum was genetically different from the laboratory colonies, but also showed high degrees of inbreeding. Multilocus genotypes of the polymorphic loci were sufficient to assign over 85% of cat fleas to their population of origin. Genetic markers for flea population identity will allow further studies to examine the origins and movement of cat fleas with important genetic traits such as insecticide resistance or pathogen susceptibility. The use of microsatellites also could determine if there are host-specific strains of cat fleas and add insight into the development of the different subspecies of C. felis.
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Interaction of Rickettsia felis with histone H2B facilitates the infection of a tick cell line.
Microbiology (Reading, Engl.)
PUBLISHED: 06-17-2010
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Haematophagous arthropods are the primary vectors in the transmission of Rickettsia, yet the molecular mechanisms mediating the rickettsial infection of arthropods remain elusive. This study utilized a biotinylated protein pull-down assay together with LC-MS/MS to identify interaction between Ixodes scapularis histone H2B and Rickettsia felis. Co-immunoprecipitation of histone with rickettsial cell lysate demonstrated the association of H2B with R. felis proteins, including outer-membrane protein B (OmpB), a major rickettsial adhesin molecule. The rickettsial infection of tick ISE6 cells was reduced by approximately 25 % via RNA-mediated H2B-depletion or enzymic treatment of histones. The interaction of H2B with the rickettsial adhesin OmpB suggests a role for H2B in mediating R. felis internalization into ISE6 cells.
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Attenuated Francisella asiatica iglC mutant induces protective immunity to francisellosis in tilapia.
Vaccine
PUBLISHED: 02-22-2010
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Francisella asiatica is a Gram-negative, facultative intracellular bacteria that causes fish francisellosis. Fish francisellosis is a severe sub-acute to chronic granulomatous disease with high mortalities and high infectivity rates in cultured and wild fish. To date, there is no approved vaccine for this widespread emergent disease. The goal of this study was to characterize the efficacy of a defined F. asiatica mutant (?iglC) as a live attenuated vaccine against subsequent immersion challenge with the wild-type (WT) organism. In previous work, the ?iglC was found to be attenuated upon intraperitoneal injection and immersion challenges. In vitro, the ?iglC exhibited reduced growth in tilapia head-kidney derived macrophages, and was significantly attenuated (p<0.001) as demonstrated by cytopathogenic and apoptosis assays. In this study, the ?iglC was tested to determine its ability to protect tilapia against challenge with high doses (lethal dose 80) of WT bacteria. Naïve tilapia vaccinated by immersion with a suspension of the ?iglC and subsequently challenged with WT F. asiatica were protected (90% mean percent survival) from the lethal challenges. F. asiatica-specific antibodies produced in response to immunization with the ?iglC were subsequently found to protect naïve tilapia against high-dose F. asiatica challenge in passive immunization experiments. Significant protection (p<0.001) was obtained when fish were passively immunized and challenged with 10(4) and 10(5)CFU/fish of WT F. asiatica; but not when challenged with 10(6)CFU/fish. This is the first report of a defined live attenuated strain providing protection against F. asiatica in fish.
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Proteomic analysis of Rickettsia parkeri strain portsmouth.
Infect. Immun.
PUBLISHED: 09-21-2009
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Rickettsia parkeri, a recently recognized pathogen of human, is one of several Rickettsia spp. in the United States that causes a spotted fever rickettsiosis. To gain insights into its biology and pathogenesis, we applied the proteomics approach to establish a two-dimensional gel proteome reference map and combined this technique with cell surface biotinylation to identify surface-exposed proteins of a low-passage isolate of R. parkeri obtained from a patient. We identified 91 proteins by matrix-assisted laser desorption ionization-tandem time of flight mass spectrometry. Of these, 28 were characterized as surface proteins, including virulence-related proteins (e.g., outer membrane protein A [OmpA], OmpB, beta-peptide, and RickA). Two-dimensional immunoblotting with serum from the R. parkeri-infected index patient was utilized to identify the immunoreactive proteins as potential targets for diagnosis and vaccine development. In addition to the known rickettsial antigens, OmpA and OmpB, we identified translation initiation factor 2, cell division protein FtsZ, and cysteinyl-tRNA synthetase as immunoreactive proteins. The proteome map with corresponding cell surface protein analysis and antigen detection will facilitate a better understanding of the mechanisms of rickettsial pathogenesis.
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Ecology of Rickettsia felis: a review.
J. Med. Entomol.
PUBLISHED: 08-04-2009
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It has been two decades since the first description of Rickettsia felis, and although a nearly cosmopolitan distribution is now apparent, much of the ecology of this unique microorganism remains unresolved. The cat flea, Ctenocephalides felis, is currently the only known biological vector of R. felis; however, molecular evidence of R. felis in other species of fleas as well as in ticks and mites suggests a variety of arthropod hosts. Studies examining the transmission of R. felis using colonized cat fleas have shown stable vertical transmission but not horizontal transmission. Likewise, serological and molecular tools have been used to detect R. felis in a number of vertebrate hosts, including humans, in the absence of a clear mechanism of horizontal transmission. Considered an emerging flea-borne rickettsiosis, clinical manifestation of R. felis infection in humans, including, fever, rash, and headache is similar to other rickettsial diseases. Recent advances toward further understanding the ecology of R. felis have been facilitated by stable R. felis-infected cat flea colonies, several primary flea isolates and sustained maintenance of R. felis in cell culture systems, and highly sensitive quantitative molecular assays. Here, we provide a synopsis of R. felis including the known distribution and arthropods infected; transmission mechanisms; current understanding of vertebrate infection and human disease; and the tools available to further examine R. felis.
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An insight into the sialotranscriptome of the cat flea, Ctenocephalides felis.
PLoS ONE
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Saliva of hematophagous arthropods contains a diverse mixture of compounds that counteracts host hemostasis. Immunomodulatory and antiinflammatory components are also found in these organisms saliva. Blood feeding evolved at least ten times within arthropods, providing a scenario of convergent evolution for the solution of the salivary potion. Perhaps because of immune pressure from hosts, the salivary proteins of related organisms have considerable divergence, and new protein families are often found within different genera of the same family or even among subgenera. Fleas radiated with their vertebrate hosts, including within the mammal expansion initiated 65 million years ago. Currently, only one flea species-the rat flea Xenopsylla cheopis-has been investigated by means of salivary transcriptome analysis to reveal salivary constituents, or sialome. We present the analysis of the sialome of cat flea Ctenocephaides felis.
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Rickettsia parkeri infection in domestic dogs, Southern Louisiana, USA, 2011.
Emerging Infect. Dis.
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The association between companion animals and tick-borne rickettsial disease has long been recognized and can be essential to the emergence of rickettsioses. We tested whole blood from dogs in temporary shelters by using PCR for rickettsial infections. Of 93 dogs, 12 (13%) were positive for Rickettsia parkeri, an emerging tick-borne rickettsiosis.
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Susceptibility of inbred mice to Rickettsia parkeri.
Infect. Immun.
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Rickettsia parkeri, a member of the spotted fever group Rickettsia, is the causative agent of American boutonneuse fever in humans. Despite the increased recognition of human cases, limited information is available regarding the infection of invertebrate and vertebrate hosts for this emerging tick-borne disease. Toward the development of a viable transmission model and to further characterize the pathology associated with R. parkeri infection, inbred mouse strains (A/J, BALB/c, C3H/HeJ, and C3H/HeN) were intravenously and intradermally inoculated with 10(5) low-passage-number R. parkeri (Portsmouth strain), and infection, gross pathology, and histopathology were scored. Additionally, a quantitative real-time PCR (qPCR) was performed to estimate rickettsial load in heart, lung, spleen, and liver tissues of infected mice at 19 days postinoculation. Of the A/J, BALB/c, and C3H/HeN mice, none displayed universal pathology consistent with sustained infection. Compared to age-matched control mice, the intravenously inoculated C3H/HeJ mice exhibited marked facial edema and marked splenomegaly upon gross examination, while the intradermally inoculated mice developed characteristic eschar-like lesions. The C3H/HeJ mice also exhibited the greatest concentrations of rickettsial DNA from heart, lung, liver, and spleen samples when examined by qPCR. The similarity of the pathology of human disease and sustained infection suggests that the C3H/HeJ strain of mice is a promising candidate for subsequent experiments to examine the tick transmission, dissemination, and pathology of R. parkeri rickettsiosis.
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Molecular characterization and tissue-specific gene expression of Dermacentor variabilis ?-catenin in response to rickettsial infection.
Insect Mol. Biol.
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Alpha catenin is a cytoskeleton protein that acts as a regulator of actin rearrangement by forming an E-cadherin adhesion complex. In Dermacentor variabilis, a putative ?-catenin (Dv?-catenin) was previously identified as differentially regulated in ovaries of ticks chronically infected with Rickettsia montanensis. To begin characterizing the role(s) of Dv?-catenin during rickettsial infection, the full-length Dv?-catenin cDNA was cloned and analysed. Comparative sequence analysis demonstrates a 3069-bp cDNA with a 2718-bp open reading frame with a sequence similar to Ixodes scapularis?-catenin. A portion of Dv?-catenin is homologous to the vinculin-conserved domain containing a putative actin-binding region and ?-catenin-binding and -dimerization regions. Quantitative reverse-transcription PCR analysis demonstrated that Dv?-catenin is predominantly expressed in tick ovaries and is responsive to tick feeding. The tissue-specific gene expression analysis of ticks exposed to Rickettsia demonstrates that Dv?-catenin expression was significantly downregulated 12 h after exposure to R. montanensis, but not in Rickettsia amblyommii-exposed ovaries, compared with Rickettsia-unexposed ticks. Studying tick-derived molecules associated with rickettsial infection will provide a better understanding of the transmission dynamics of tick-borne rickettsial diseases.
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