Molecular Interactions that Enable Movement of the Lyme Disease Agent from the Tick Gut into the Hemolymph

Zhang, Lili; Zhang, Yue; Adusumilli, Sarojini; Liu, Lei; Narasimhan, Sukanya; Dai, Jianfeng; Zhao, Yang O.; Fikrig, Erol

doi:10.1371/journal.ppat.1002079

Cited by 62 publications

(60 citation statements)

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“…Recent research investigating borrelia-vector interactions have focused on inactivation of global regulators, individual genes, and replicons to advance our understanding of B. burgdorferi tick colonization and persistence and vector transmission mechanisms (1,4,7,18,(37)(38)(39)(40)(41)(42)(43)(44)(45)(46)(47)(48)(49)(50)(51)(52)(53)(54). The loss of BBA66 activity did not completely abolish the ability of B. burgdorferi to invade the host by tick bite (at least when more than 4 ticks/mouse fed to repletion), but mouse infectivity was significantly impaired.…”

Section: Discussionmentioning

confidence: 99%

Borrelia burgdorferi bba66 Gene Inactivation Results in Attenuated Mouse Infection by Tick Transmission

et al. 2013

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bThe impact of the Borrelia burgdorferi surface-localized immunogenic lipoprotein BBA66 on vector and host infection was evaluated by inactivating the encoding gene, bba66, and characterizing the mutant phenotype throughout the natural mouse-tickmouse cycle. The BBA66-deficient mutant isolate, Bb ⌬A66 , remained infectious in mice by needle inoculation of cultured organisms, but differences in spirochete burden and pathology in the tibiotarsal joint were observed relative to the parental wild-type (WT) strain. Ixodes scapularis larvae successfully acquired Bb ⌬A66 following feeding on infected mice, and the organisms persisted in these ticks through the molt to nymphs. A series of tick transmission experiments (n ‫؍‬ 7) demonstrated that the ability of Bb ⌬A66 -infected nymphs to infect laboratory mice was significantly impaired compared to that of mice fed upon by WT-infected ticks. trans-complementation of Bb ⌬A66 with an intact copy of bba66 restored the WT infectious phenotype in mice via tick transmission. These results suggest a role for BBA66 in facilitating B. burgdorferi dissemination and transmission from the tick vector to the mammalian host as part of the disease process for Lyme borreliosis.

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Section: Discussionmentioning

confidence: 99%

Borrelia burgdorferi bba66 Gene Inactivation Results in Attenuated Mouse Infection by Tick Transmission

et al. 2013

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“…In order for the bacterium to survive the change of the host ability to multiply in the new body, it must alter some of its proteins, and -by extension -its antigens [33][34][35][36]. This process takes time, which is estimated at several hours [37].…”

Section: Introductionmentioning

confidence: 99%

Prevalence of <i>Borrelia burgdorferi</i> in ticks removed from skin of people and circumstances of being bitten – research from the area of Poland, 2012–2014

Gałęziowska¹,

Rzymowska²,

Najda³

et al. 2018

Ann Agric Environ Med.

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Introduction. During feeding, the tick sucks blood from the host along with the pathogens that are in the blood, simultaneously exchanging its own pathogens with the host. Humans can also be a host. It is important to understand the most typical circumstances in which people might become infected with Borrelia burgdorferi. This knowledge will help to prepare health education programmes aimed at the prevention of Lyme disease and other tick-borne diseases. Objective. The aim of the study was to determine the percentage of ticks infected with Borrelia burgdorferi sensu lato, depending on the circumstances of getting bitten. Materials and method. The research material consisted of ticks acquired from people who had been bitten, and questionnaires completed by these people. 510 ticks were acquired from 257 females and 253 males. Following delivery of a tick for testing, the stage of its development was determined and a molecular assay of Borrelia burgdorferi DNA performed. Results. A positive result of the nested-PCR test was obtained in 78 ticks, which represents 15.30% of all ticks. The infected ticks were collected from male (41 ticks -52.56%) and female subjects (37 ticks -47.44%). The biggest number of infected ticks were collected in autumn (54 ticks -69.23%) and from people who had been into forests (44 ticks -56.41%). Among the people from whom the infected ticks were acquired, the dominating group included persons over 16 years of age (53 persons -67.95%) and children aged 0-5 years (16 persons -20.51%). One in four infected ticks were acquired from the southwestern (20 ticks -25.64%) and eastern regions of Poland (21 ticks -26.92%). Conclusion. Infestation of ticks infected with Lyme disease spirochete in this study proved to be variable and depend on the season, the area of tick attack and the region in Poland. The results of the study clearly show that ticks infected with Borrelia burgdorferi inhabit all regions of Poland. The results are consistent with National Institute of Hygiene data which indicates that Lyme disease cases are recorded in all regions of Poland.

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“…In the tick, spirochetes reside primarily in the midgut until the introduction of the host blood meal. During tick feeding on a vertebrate host, spirochetes replicate, and a subset of the motile organisms cross the midgut epithelium into the hemocoel before reaching the salivary glands, where they subsequently are deposited into the host dermis (6)(7)(8). Once in the host, B. burgdorferi must migrate through the complex skin tissues, including some hematogenous dissemination, and eventually colonize distant tissues, where they often produce disease symptoms in certain hosts.…”

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confidence: 99%

Motor Rotation Is Essential for the Formation of the Periplasmic Flagellar Ribbon, Cellular Morphology, and Borrelia burgdorferi Persistence within Ixodes scapularis Tick and Murine Hosts

Sultan

Sekar

Zhao³

et al. 2015

Infect Immun

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c Borrelia burgdorferi must migrate within and between its arthropod and mammalian hosts in order to complete its natural enzootic cycle. During tick feeding, the spirochete transmits from the tick to the host dermis, eventually colonizing and persisting within multiple, distant tissues. This dissemination modality suggests that flagellar motor rotation and, by extension, motility are crucial for infection. We recently reported that a nonmotile flaB mutant that lacks periplasmic flagella is rod shaped and unable to infect mice by needle or tick bite. However, those studies could not differentiate whether motor rotation or merely the possession of the periplasmic flagella was crucial for cellular morphology and host persistence. Here, we constructed and characterized a motB mutant that is nonmotile but retains its periplasmic flagella. Even though ⌬motB bacteria assembled flagella, part of the mutant cell is rod shaped. Cryoelectron tomography revealed that the flagellar ribbons are distorted in the mutant cells, indicating that motor rotation is essential for spirochetal flat-wave morphology. The ⌬motB cells are unable to infect mice, survive in the vector, or migrate out of the tick. Coinfection studies determined that the presence of these nonmotile ⌬motB cells has no effect on the clearance of wild-type spirochetes during murine infection and vice versa. Together, our data demonstrate that while flagellar motor rotation is necessary for spirochetal morphology and motility, the periplasmic flagella display no additional properties related to immune clearance and persistence within relevant hosts. Borrelia burgdorferi, the Lyme disease spirochete, shuttles principally between the Ixodes ticks and a vertebrate host during its natural infection cycle (1-5). In the tick, spirochetes reside primarily in the midgut until the introduction of the host blood meal. During tick feeding on a vertebrate host, spirochetes replicate, and a subset of the motile organisms cross the midgut epithelium into the hemocoel before reaching the salivary glands, where they subsequently are deposited into the host dermis (6-8). Once in the host, B. burgdorferi must migrate through the complex skin tissues, including some hematogenous dissemination, and eventually colonize distant tissues, where they often produce disease symptoms in certain hosts. Subsequently, when a naive tick feeds on an infected reservoir host, spirochetes in the skin migrate into the arthropod to complete the enzootic cycle (3, 4, 9). During the spirochete's migration within and between the hosts, periplasmic flagellar motor rotation and, by extension, motility are thought to be crucial for infection (10, 11). Indeed, nonmotile, reduced-motility, or nonchemotactic mutant spirochetes were found to be attenuated in mouse infection (12)(13)(14). Additionally, our data indicate that B. burgdorferi remains constantly motile in the mouse dermis, even 2 years after needle inoculation (P. Sekar, R. M. Wooten, and M. A. Motaleb, unpublished results). In fact, this Lyme dise...

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Molecular Interactions that Enable Movement of the Lyme Disease Agent from the Tick Gut into the Hemolymph

Cited by 62 publications

References 35 publications

Borrelia burgdorferi bba66 Gene Inactivation Results in Attenuated Mouse Infection by Tick Transmission

Borrelia burgdorferi bba66 Gene Inactivation Results in Attenuated Mouse Infection by Tick Transmission

Prevalence of <i>Borrelia burgdorferi</i> in ticks removed from skin of people and circumstances of being bitten – research from the area of Poland, 2012–2014

Motor Rotation Is Essential for the Formation of the Periplasmic Flagellar Ribbon, Cellular Morphology, and Borrelia burgdorferi Persistence within Ixodes scapularis Tick and Murine Hosts

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