Anaplasma phagocytophilum induces Ixodes scapularis ticks to express an antifreeze glycoprotein gene that enhances their survival in the cold

Neelakanta, Girish; Sultana, Hameeda; Fish, Durland; Anderson, John F.; Fikrig, Erol

doi:10.1172/jci42868

Cited by 182 publications

(204 citation statements)

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“…IAFGP, the I. scapularis antifreeze glycoprotein, is induced by ticks in the presence of A. phagocytophilum (26), and silencing iafgp impairs A. phagocytophilum colonization of the gut. Independently, we demonstrated IAFGP to inhibit biofilm formation among Gram-positive pathogens such as S. aureus (25).…”

Section: Discussionmentioning

confidence: 99%

“…However, unique physical characteristics and previously determined molecular evidence suggest the absence of peptidoglycan from A. phagocytophilum (62)(63)(64), which would nullify any effect IAFGP (or P1) would have on A. phagocytophilum. Our earlier work described the role for elevated levels of IAFGP, upon A. phagocytophilum infection of Ixodes ticks, to protect ticks from the cold environment (26). Therefore, IAFGP aids Anaplasma in two manners: by increasing the ability of ticks to survive in the winter and therefore indirectly increasing the chance of Anaplasma transmission to mice, and by altering the tick microbiomes and their associated biofilms, thereby enhancing its colonization within the tick vector.…”

Section: Discussionmentioning

confidence: 99%

“…IAFGP, a secreted I. scapularis antifreeze glycoprotein, was recently determined to inhibit bacterial biofilm formation (25). The expression of iafgp is induced by cold exposure and A. phagocytophilum infection (26). The qRT PCR demonstrated that iafgp is highly induced in the tick gut by the presence of A. phagocytophilum (26), and silencing iafgp expression by RNAi diminishes the A. phagocytophilum burden in tick guts (Fig.…”

Section: The Peritrophic Matrix Is Essential For Colonization Of the mentioning

confidence: 98%

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Pathogen-mediated manipulation of arthropod microbiota to promote infection

Abraham

Liu

Jutras

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Arthropods transmit diverse infectious agents; however, the ways microbes influence their vector to enhance colonization are poorly understood.Ixodes scapularisticks harbor numerous human pathogens, includingAnaplasma phagocytophilum,the agent of human granulocytic anaplasmosis. We now demonstrate thatA. phagocytophilummodifies theI. scapularismicrobiota to more efficiently infect the tick.A. phagocytophiluminduces ticks to expressIxodes scapularisantifreeze glycoprotein (iafgp), which encodes a protein with several properties, including the ability to alter bacterial biofilm formation. IAFGP thereby perturbs the tick gut microbiota, which influences the integrity of the peritrophic matrix and gut barrier—critical obstacles forAnaplasmacolonization. Mechanistically, IAFGP binds the terminald-alanine residue of the pentapeptide chain of bacterial peptidoglycan, resulting in altered permeability and the capacity of bacteria to form biofilms. These data elucidate the molecular mechanisms by which a human pathogen appropriates an arthropod antibacterial protein to alter the gut microbiota and more effectively colonize the vector.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: The Peritrophic Matrix Is Essential For Colonization Of the mentioning

confidence: 98%

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Pathogen-mediated manipulation of arthropod microbiota to promote infection

Abraham

Liu

Jutras

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…An interesting study on I. scapularis showed that A. phagocytophilum promotes cold tolerance through an antifreeze glycoprotein [148]. In the absence of this antifreeze glycoprotein, the survival rate of ticks after exposure to extremely cold temperature and the infection level of A. phagocytophilum following exposure was reduced.…”

Section: Understanding Tick-pathogen Interaction Through Rnaimentioning

confidence: 99%

RNA Interference – A Powerful Functional Analysis Tool for Studying Tick Biology and its Control

Galay¹,

Umemiya‐Shirafuji²,

MasamiMochizuki³

et al. 2016

RNA Interference

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Ticks (Acari: Ixodida) are blood-sucking arthropods globally recognized as vectors of numerous diseases. They are primarily responsible for the transmission of various pathogens, including viruses, rickettsiae, and blood parasites of animals. Ticks are second to mosquitoes in terms of disease transmission to humans. The continuous emergence of tick-borne diseases and acaricide resistance of ticks necessitates the development of new and more effective control agents and strategies; therefore, understanding of different aspects of tick biology and their interaction with pathogens is very crucial in developing effective control strategies. RNA interference (RNAi) has been widely used in the area of tick research as a versatile reverse genetic tool to elucidate the functions of various tick proteins. During the past decade, numerous studies on ticks utilized RNAi to evaluate potentially key tick proteins involved in blood feeding, reproduction, evasion of host immune response, interaction with pathogens, and pathogen transmission that may be targeted for tick and pathogen control. This chapter reviewed the application of RNAi in tick research over the past decade, focusing on the impact of this technique in the advancement of knowledge on tick and pathogen biology.

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“…Since then, AFPs have been described in diverse taxa including terrestrial arthropods (Duman, 1977: Duman, 2001Tyshenko et al, 1997;Andorfer and Duman, 2000;Duman et al, 2004;Graham and Davies, 2005;Neelakanta et al, 2010), bacteria and fungi (Duman and Olsen, 1993;Sun et al, 1995;Yamashita et al, 2002;Gilbert et al, 2005) and plants (Griffith et al, 1992;Urrutia et al, 1992;Hon et al, 1994;Duman, 1994;Smallwood et al, 1999;Griffith and Yaish, 2004). Antifreeze proteins lower the non-colligative freezing point of water without depressing the melting point.…”

Section: Introductionmentioning

confidence: 99%

Antifreeze proteins in the primary urine of larvae of the beetle Dendroides canadensis (Latreille)

Nickell

Sass

Verleye

et al. 2013

Journal of Experimental Biology

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SUMMARYTo avoid freezing while overwintering beneath the bark of fallen trees, Dendroides canadensis (Coleoptera: Pyrochroidae) larvae produce a family of antifreeze proteins (DAFPs) that are transcribed in specific tissues and have specific compartmental fates. DAFPs and associated thermal hysteresis activity (THA) have been shown previously in hemolymph and midgut fluid, but the presence of DAFPs has not been explored in primary urine, a potentially important site that can contain endogenous icenucleating compounds that could induce freezing. A maximum mean THA of 2.65±0.33°C was observed in primary urine of wintercollected D. canadensis larvae. THA in primary urine increased significantly through autumn, peaked in the winter and decreased through spring to levels of 0.2-0.3°C in summer, in a pattern similar to that of hemolymph and midgut fluid. THA was also found in hindgut fluid and excreted rectal fluid, suggesting that these larvae not only concentrate AFPs in the hindgut, but also excrete AFPs from the rectal cavity. Based on dafp transcripts isolated from Malpighian tubule epithelia, cDNAs were cloned and sequenced, identifying the presence of transcripts encoding 24 DAFP isoforms. Six of these Malpighian tubule DAFPs were known previously, but 18 are new. We also provide functional evidence that DAFPs can inhibit ice nucleators present in insect primary urine. This is potentially critical because D. canadensis larvae die if frozen, and therefore ice formation in any body fluid, including the urine, would be lethal.

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Anaplasma phagocytophilum induces Ixodes scapularis ticks to express an antifreeze glycoprotein gene that enhances their survival in the cold

Cited by 182 publications

References 72 publications

Pathogen-mediated manipulation of arthropod microbiota to promote infection

Pathogen-mediated manipulation of arthropod microbiota to promote infection

RNA Interference – A Powerful Functional Analysis Tool for Studying Tick Biology and its Control

Antifreeze proteins in the primary urine of larvae of the beetle Dendroides canadensis (Latreille)

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