Unpacking the intricacies of Rickettsia–vector interactions

Laukaitis, Hanna J; Macaluso, Kevin R.

doi:10.1016/j.pt.2021.05.008

Cited by 18 publications

(19 citation statements)

References 100 publications

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“…In the current study, after >300 days in culture, both strains of M. leprae were able to replicate in MFP, suggesting that non-propagative culture still allows for maintenance of viable bacilli. Ticks can maintain obligate intracellular bacterial populations for an extended life cycle, sometimes up to two years, and transovarially transmit bacteria to their progeny (Laukaitis and Macaluso, 2021). The isolation and cultivation of the M. chelonae complex bacilli in tick cells derived from eggs of field-caught ticks (Palomar et al, 2019) supports the current in vitro studies demonstrating Mycobacterium persistence in tick cells which is consistent with the previous study (Ferreira et al, 2018), M. leprae does not show sustainable growth in ISE6 cells.…”

Section: Discussionsupporting

confidence: 86%

“…Ticks are effective vectors for transmitting a variety of diseasecausing agents, including numerous obligate intracellular bacteria (Laukaitis and Macaluso, 2021). These data indicate that Amblyomma ticks infected with M. leprae can successfully transmit the organisms both vertically and horizontally, making it possible for them to transfer the organisms to other hosts in subsequent blood meals.…”

Section: Discussionmentioning

confidence: 94%

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Mycobacterium leprae Infection in Ticks and Tick-Derived Cells

et al. 2021

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Leprosy is a zoonosis in the southern United States involving humans and wild armadillos. The majority of patients presenting with zoonotic strains of Mycobacterium leprae note extensive outdoor activity but only rarely report any history of direct contact with wild armadillos. Whether M. leprae is transmitted to new vertebrate hosts through the environment independently or with the aid of other organisms, e.g., arthropod vectors, is a fundamental question in leprosy transmission. The objectives of this study were to assess the potential for ticks to transmit M. leprae and to test if viable M. leprae can be maintained in tick-derived cells. To evaluate tick transmission, nymphal Amblyomma maculatum ticks were injected with isolated M. leprae. Infection and transmission were assessed by qPCR. Ticks infected as nymphs harbored M. leprae through vertical transmission events (nymph to adult and adult to progeny); and, horizontal transmission of M. leprae to a vertebrate host was observed. Mycobacterium leprae DNA was detected in multiple tick life cycle stages. Likewise, freshly isolated M. leprae (Thai-53) was used to infect a tick-derived cell line, and enumeration and bacterial viability were assessed at individual time points for up to 49 days. Evaluations of the viability of long-term cultured M. leprae (Thai-53 and Br4923) were also assessed in a mouse model. Tick-derived cells were able to maintain viable M. leprae over the 49-day course of infection and M. leprae remained infectious within tick cells for at least 300 days. The results of this study suggest that ticks themselves might serve as a vector for the transmission of M. leprae and that tick cells are suitable for maintenance of viable M. leprae for an extended period of time.

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Section: Discussionsupporting

confidence: 86%

Section: Discussionmentioning

confidence: 94%

Mycobacterium leprae Infection in Ticks and Tick-Derived Cells

et al. 2021

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“…Placed in the transitional group of Rickettsia, R. felis contains genetic and biological characteristics of both tick-associated spotted fever group (SFG) and insect-associated typhus group Rickettsia [35]. As obligate intracellular bacteria, arthropods often serve as both reservoirs and vectors of Rickettsia [36]. The most well-studied vector for R. felis is the common cat flea, which supports both vertical and horizontal transmission mechanisms [1].…”

Section: Plos Neglected Tropical Diseasesmentioning

confidence: 99%

The role of cofeeding arthropods in the transmission of Rickettsia felis

et al. 2022

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Rickettsia felis is an emerging etiological agent of rickettsioses worldwide. The cosmopolitan cat flea (Ctenocephalides felis) is the primary vector of R. felis, but R. felis has also been reported in other species of hematophagous arthropods including ticks and mosquitoes. Canines can serve as a bacteremic host to infect fleas under laboratory conditions, yet isolation of R. felis from the blood of a vertebrate host in nature has not been realized. Cofeeding transmission is an efficient mechanism for transmitting rickettsiae between infected and uninfected fleas; however, the mechanism of transmission among different orders and classes of arthropods is not known. The potential for R. felis transmission between infected fleas and tick (Dermacentor variabilis) and mosquito (Anopheles quadrimaculatus) hosts was examined via cofeeding bioassays. Donor cat fleas infected with R. felis transmitted the agent to naïve D. variabilis nymphs via cofeeding on a rat host. Subsequent transstadial transmission of R. felis from the engorged nymphs to the adult ticks was observed with reduced prevalence in adult ticks. Using an artificial host system, An. quadrimaculatus exposed to a R. felis-infected blood meal acquired rickettsiae and maintained infection over 12 days post-exposure (dpe). Similar to ticks, mosquitoes were able to acquire R. felis while cofeeding with infected cat fleas on rats infection persisting in the mosquito for up to 3 dpe. The results indicate R. felis-infected cat fleas can transmit rickettsiae to both ticks and mosquitoes via cofeeding on a vertebrate host, thus providing a potential avenue for the diversity of R. felis-infected arthropods in nature.

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“…Vitellogenin C is a molecule synthesized in the fat body of insects, transported through the hemolymph until reaching female ovaries, where it is then taken up by oocytes. During vitellogenesis, it is responsible for enhancing yolk protein synthesis required for proper embryogenesis by maturing oocytes (Laukaitis and Macaluso, 2021). Indeed, Vitellogenin C levels were found to be approximately 9-fold higher in females compared with males (McIntosh et al, 2016).…”

Section: Vitellogenin Cmentioning

confidence: 99%

“…A vaccine targeting both flea fitness and pathogen competence is an attractive choice requiring the identification of flea proteins/metabolites with a dual effect. Even though recent developments in vector and pathogen omics have advanced the understanding of the genetic factors and molecular pathways involved at the tickpathogen interface, leading to discovery of candidate protective antigens (de la Fuente et al, 2007a;de la Fuente et al, 2007b), only a few studies have focused on the interaction between fleas and flea-borne pathogens (Dreher-Lesnick et al, 2010;Brown, 2019;Bland et al, 2020;Danchenko et al, 2021;Laukaitis and Macaluso, 2021).…”

Section: Introductionmentioning

confidence: 99%

Using Proteomic Approaches to Unravel the Response of Ctenocephalides felis felis to Blood Feeding and Infection With Bartonella henselae

André

Neupane

Lappin

et al. 2022

Front. Cell. Infect. Microbiol.

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Among the Ctenocephalides felis felis-borne pathogens, Bartonella henselae, the main aetiological agent of cat scratch disease (CSD), is of increasing comparative biomedical importance. Despite the importance of B. henselae as an emergent pathogen, prevention of the diseases caused by this agent in cats, dogs and humans mostly relies on the use of ectoparasiticides. A vaccine targeting both flea fitness and pathogen competence is an attractive choice requiring the identification of flea proteins/metabolites with a dual effect. Even though recent developments in vector and pathogen -omics have advanced the understanding of the genetic factors and molecular pathways involved at the tick-pathogen interface, leading to discovery of candidate protective antigens, only a few studies have focused on the interaction between fleas and flea-borne pathogens. Taking into account the period of time needed for B. henselae replication in flea digestive tract, the present study investigated flea-differentially abundant proteins (FDAP) in unfed fleas, fleas fed on uninfected cats, and fleas fed on B. henselae-infected cats at 24 hours and 9 days after the beginning of blood feeding. Proteomics approaches were designed and implemented to interrogate differentially expressed proteins, so as to gain a better understanding of proteomic changes associated with the initial B. henselae transmission period (24 hour timepoint) and a subsequent time point 9 days after blood ingestion and flea infection. As a result, serine proteases, ribosomal proteins, proteasome subunit α-type, juvenile hormone epoxide hydrolase 1, vitellogenin C, allantoinase, phosphoenolpyruvate carboxykinase, succinic semialdehyde dehydrogenase, glycinamide ribotide transformylase, secreted salivary acid phosphatase had high abundance in response of C. felis blood feeding and/or infection by B. henselae. In contrast, high abundance of serpin-1, arginine kinase, ribosomal proteins, peritrophin-like protein, and FS-H/FSI antigen family member 3 was strongly associated with unfed cat fleas. Findings from this study provide insights into proteomic response of cat fleas to B. henselae infected and uninfected blood meal, as well as C. felis response to invading B. henselae over an infection time course, thus helping understand the complex interactions between cat fleas and B. henselae at protein levels.

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Unpacking the intricacies of Rickettsia–vector interactions

Cited by 18 publications

References 100 publications

Mycobacterium leprae Infection in Ticks and Tick-Derived Cells

Mycobacterium leprae Infection in Ticks and Tick-Derived Cells

The role of cofeeding arthropods in the transmission of Rickettsia felis

Using Proteomic Approaches to Unravel the Response of Ctenocephalides felis felis to Blood Feeding and Infection With Bartonella henselae

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