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      Tracking of Borrelia afzelii Transmission from Infected Ixodes ricinus Nymphs to Mice

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          Abstract

          Quantitative and microscopic tracking of Borrelia afzelii transmission from infected Ixodes ricinus nymphs has shown a transmission cycle different from that of Borrelia burgdorferi and Ixodes scapularis. Borrelia afzelii organisms are abundant in the guts of unfed I. ricinus nymphs, and their numbers continuously decrease during feeding.

          ABSTRACT

          Quantitative and microscopic tracking of Borrelia afzelii transmission from infected Ixodes ricinus nymphs has shown a transmission cycle different from that of Borrelia burgdorferi and Ixodes scapularis. Borrelia afzelii organisms are abundant in the guts of unfed I. ricinus nymphs, and their numbers continuously decrease during feeding. Borrelia afzelii spirochetes are present in murine skin within 1 day of tick attachment. In contrast, spirochetes were not detectable in salivary glands at any stage of tick feeding. Further experiments demonstrated that tick saliva is not essential for B. afzelii infectivity, the most important requirement for successful host colonization being a change in expression of outer surface proteins that occurs in the tick gut during feeding. Spirochetes in vertebrate mode are then able to survive within the host even in the absence of tick saliva. Taken together, our data suggest that the tick gut is the decisive organ that determines the competence of I. ricinus to vector B. afzelii. We discuss possible transmission mechanisms of B. afzelii spirochetes that should be further tested in order to design effective preventive and therapeutic strategies against Lyme disease.

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          Most cited references40

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          Of ticks, mice and men: understanding the dual-host lifestyle of Lyme disease spirochaetes.

          In little more than 30 years, Lyme disease, which is caused by the spirochaete Borrelia burgdorferi, has risen from relative obscurity to become a global public health problem and a prototype of an emerging infection. During this period, there has been an extraordinary accumulation of knowledge on the phylogenetic diversity, molecular biology, genetics and host interactions of B. burgdorferi. In this Review, we integrate this large body of information into a cohesive picture of the molecular and cellular events that transpire as Lyme disease spirochaetes transit between their arthropod and vertebrate hosts during the enzootic cycle.
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            An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks.

            Over 8000 expressed sequence tags from six different salivary gland cDNA libraries from the tick Ixodes scapularis were analyzed. These libraries derive from feeding nymphs infected or not with the Lyme disease agent, Borrelia burgdorferi, from unfed adults, and from adults feeding on a rabbit for 6-12 h, 18-24 h, and 3-4 days. Comparisons of the several libraries led to identification of several significantly differentially expressed transcripts. Additionally, over 500 new predicted protein sequences are described, including several novel gene families unique to ticks; no function can be presently ascribed to most of these novel families. Among the housekeeping-associated transcripts, we highlight those enzymes associated with post translation modification of amino acids, particularly those forming sulfotyrosine, hydroxyproline, and carboxyl-glutamic acid. Results support the hypothesis that gene duplication, most possibly including genome duplications, is a major player in tick evolution.
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              Induction of an outer surface protein on Borrelia burgdorferi during tick feeding.

              Lyme disease spirochetes, Borrelia burgdorferi sensu lato, are maintained in zoonotic cycles involving ticks and small mammals. In unfed ticks, the spirochetes produce one outer surface protein, OspA, but not OspC. During infection in mammals, immunological data suggest that the spirochetes have changed their surface, now expressing OspC but little or no OspA. We find by in vitro growth experiments that this change is regulated in part by temperature; OspC is produced by spirochetes at 32-37 degrees C but not at 24 degrees C. Furthermore, spirochetes in the midgut of ticks that have fully engorged on mice now have OspC on their surface. Thus two environmental cues, an increase in temperature and tick feeding, trigger a major alteration of the spirochetal outer membrane. This rapid synthesis of OspC by spirochetes during tick feeding may play an essential role in the capacity of these bacteria to successfully infect mammalian hosts, including humans, when transmitted by ticks.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                Infect Immun
                Infect. Immun
                iai
                iai
                IAI
                Infection and Immunity
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                0019-9567
                1098-5522
                25 March 2019
                21 May 2019
                June 2019
                21 May 2019
                : 87
                : 6
                : e00896-18
                Affiliations
                [a ]Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Ceske Budejovice, Czech Republic
                [b ]Faculty of Science, University of South Bohemia, Ceske Budejovice, Czech Republic
                [c ]Department of Pathology, Charles University, Medical Faculty and Charles University Hospital, Plzen, Czech Republic
                Yale University School of Medicine
                Author notes
                Address correspondence to Radek Sima, sima@ 123456paru.cas.cz .

                Citation Pospisilova T, Urbanova V, Hes O, Kopacek P, Hajdusek O, Sima R. 2019. Tracking of Borrelia afzelii transmission from infected Ixodes ricinus nymphs to mice. Infect Immun 87:e00896-18. https://doi.org/10.1128/IAI.00896-18.

                Author information
                https://orcid.org/0000-0002-5058-4476
                Article
                00896-18
                10.1128/IAI.00896-18
                6529662
                30910791
                4b9708cc-8fc8-48d9-9f22-e94331be2bbd
                Copyright © 2019 Pospisilova et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 20 December 2018
                : 14 January 2019
                : 14 March 2019
                Page count
                Figures: 7, Tables: 1, Equations: 0, References: 45, Pages: 13, Words: 7940
                Funding
                Funded by: European Commission (EC), https://doi.org/10.13039/501100000780;
                Award ID: 602272
                Award Recipient : Award Recipient : Award Recipient :
                Funded by: Ministerstvo Školství, Mládeže a Tělovýchovy (MŠMT), https://doi.org/10.13039/501100001823;
                Award ID: CZ.02.1.01/0.0/0.0/16_019/0000759
                Award Recipient : Award Recipient : Award Recipient :
                Funded by: Grantová Agentura České Republiky (GAČR), https://doi.org/10.13039/501100001824;
                Award ID: 17-27393S
                Award Recipient : Award Recipient :
                Funded by: Grantová Agentura České Republiky (GAČR), https://doi.org/10.13039/501100001824;
                Award ID: 17-27386S
                Award Recipient : Award Recipient :
                Funded by: Grantová Agentura České Republiky (GAČR), https://doi.org/10.13039/501100001824;
                Award ID: 18-01832S
                Award Recipient :
                Categories
                Bacterial Infections
                Custom metadata
                June 2019

                Infectious disease & Microbiology
                borrelia,borrelia afzelii,ixodes ricinus,lyme disease,tick-borne pathogens,transmission

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