Rickettsial pathogen uses arthropod tryptophan pathway metabolites to evade reactive oxygen species in tick cells

Dahmani, Mustapha; Anderson, John F.; Sultana, Hameeda; Neelakanta, Girish

doi:10.1111/cmi.13237

Cited by 15 publications

(31 citation statements)

References 56 publications

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“…In malaria, XA is present in the gut of Anopheles mosquitos and is known to induce gametogenesis of P. falciparum [9]. It has recently been shown that XA supported the growth of a tick-borne pathogen, Anaplasma phagocytophilum, in tick cells by inhibition of tryptophan dioxygenase activity [41]. However, it remains unknown whether this metabolite is present in the tick midgut [10].…”

Section: Discussionmentioning

confidence: 99%

Differential expression of calcium-dependent protein kinase 4, tubulin tyrosine ligase, and methyltransferase by xanthurenic acid-induced Babesia bovis sexual stages

Hussein

Johnson²,

Taus

et al. 2021

Parasites Vectors

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Background Babesia bovis is one of the most significant tick-transmitted pathogens of cattle worldwide. Babesia bovis parasites have a complex lifecycle, including development within the mammalian host and tick vector. Each life stage has developmental forms that differ in morphology and metabolism. Differentiation between these forms is highly regulated in response to changes in the parasite’s environment. Understanding the mechanisms by which Babesia parasites respond to environmental changes and the transmission cycle through the biological vector is critically important for developing bovine babesiosis control strategies. Results In this study, we induced B. bovis sexual stages in vitro using xanthurenic acid and documented changes in morphology and gene expression. In vitro induced B. bovis sexual stages displayed distinctive protrusive structures and surface ruffles. We also demonstrated the upregulation of B. bovis calcium-dependent protein kinase 4 (cdpk4), tubulin-tyrosine ligase (ttl), and methyltransferase (mt) genes by in vitro induced sexual stages and during parasite development within tick midguts. Conclusions Similar to other apicomplexan parasites, it is likely that B. bovis upregulated genes play a vital role in sexual reproduction and parasite transmission. Herein, we document the upregulation of cdpk4, ttl, and mt genes by both B. bovis in vitro induced sexual stages and parasites developing in the tick vector. Understanding the parasite's biology and identifying target genes essential for sexual reproduction will enable the production of non-transmissible live vaccines to control bovine babesiosis. Graphical abstract

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Section: Discussionmentioning

confidence: 99%

Differential expression of calcium-dependent protein kinase 4, tubulin tyrosine ligase, and methyltransferase by xanthurenic acid-induced Babesia bovis sexual stages

Hussein

Johnson²,

Taus

et al. 2021

Parasites Vectors

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“…Villar and colleagues reported that the presence of A. phagocytophilum leads to overrepresentation of proteins involved in blood digestion and lipid absorption in ticks [ 9 ]. Several other recent studies from our and other groups provide strong evidence that A. phagocytophilum modulates several signaling pathways in ticks for its survival, colonization, and transmission to the vertebrate host [ 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 ].…”

Section: Introductionmentioning

confidence: 93%

Rickettsial Pathogen Perturbs Tick Circadian Gene to Infect the Vertebrate Host

Khanal

Taank

Anderson

et al. 2022

IJMS

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Ixodes scapularis is a medically important tick that transmits several microbes to humans, including rickettsial pathogen Anaplasma phagocytophilum. In nature, these ticks encounter several abiotic factors including changes in temperature, humidity, and light. Many organisms use endogenously generated circadian pathways to encounter abiotic factors. In this study, we provide evidence for the first time to show that A. phagocytophilum modulates the arthropod circadian gene for its transmission to the vertebrate host. We noted a circadian oscillation in the expression of arthropod clock, bmal1, period and timeless genes when ticks or tick cells were exposed to alternate 12 h light: 12 h dark conditions. Moreover, A. phagocytophilum significantly modulates the oscillation pattern of expression of these genes. In addition, increased levels of clock and bmal1 and decreased expression of Toll and JAK/STAT pathway immune genes such as pelle and jak, respectively, were noted during A. phagocytophilum transmission from ticks to the vertebrate host. RNAi-mediated knockdown of clock gene expression in ticks resulted in the reduced expression of jak and pelle that increased bacterial transmission from ticks to the murine host. Furthermore, clock-deficient ticks fed late and had less engorgement weights. These results indicate an important role for circadian modulation of tick gene expression that is critical for arthropod blood feeding and transmission of pathogens from vector to the vertebrate host.

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“…The observation of inhibition of OATPs that significantly reduced viral replication in tick cells suggests a possible anti-viral role for these molecules ( Taank et al., 2018 ). More recent studies showed that A. phagocytophilum uses tick OATPs and tryptophan pathway metabolism to inhibit build-up of reactive oxygen species that is toxic to bacterial replication ( Dahmani et al., 2020 ). In addition, we noted that A. phagocytophilum regulate tick OATPs through microRNA133 ( Ramasamy et al., 2020 ).…”

Section: Organic Anion Transporting Polypeptides(oatps)mentioning

confidence: 99%

Tick Saliva and Salivary Glands: What Do We Know So Far on Their Role in Arthropod Blood Feeding and Pathogen Transmission

Neelakanta

Sultana

2022

Front. Cell. Infect. Microbiol.

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Ticks are blood-sucking arthropods that have developed myriad of strategies to get a blood meal from the vertebrate host. They first attach to the host skin, select a bite site for a blood meal, create a feeding niche at the bite site, secrete plethora of molecules in its saliva and then starts feeding. On the other side, host defenses will try to counter-attack and stop tick feeding at the bite site. In this constant battle between ticks and the host, arthropods successfully pacify the host and completes a blood meal and then replete after full engorgement. In this review, we discuss some of the known and emerging roles for arthropod components such as cement, salivary proteins, lipocalins, HSP70s, OATPs, and extracellular vesicles/exosomes in facilitating successful blood feeding from ticks. In addition, we discuss how tick-borne pathogens modulate(s) these components to infect the vertebrate host. Understanding the biology of arthropod blood feeding and molecular interactions at the tick-host interface during pathogen transmission is very important. This information would eventually lead us in the identification of candidates for the development of transmission-blocking vaccines to prevent diseases caused by medically important vector-borne pathogens.

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Rickettsial pathogen uses arthropod tryptophan pathway metabolites to evade reactive oxygen species in tick cells

Cited by 15 publications

References 56 publications

Differential expression of calcium-dependent protein kinase 4, tubulin tyrosine ligase, and methyltransferase by xanthurenic acid-induced Babesia bovis sexual stages

Differential expression of calcium-dependent protein kinase 4, tubulin tyrosine ligase, and methyltransferase by xanthurenic acid-induced Babesia bovis sexual stages

Rickettsial Pathogen Perturbs Tick Circadian Gene to Infect the Vertebrate Host

Tick Saliva and Salivary Glands: What Do We Know So Far on Their Role in Arthropod Blood Feeding and Pathogen Transmission

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