Dermacentor variabilis: Resistance to ticks acquired by mast cell-deficient and other strains of mice

denHollander, Neal; Allen, John R.

doi:10.1016/0014-4894(85)90069-4

Cited by 31 publications

(24 citation statements)

References 16 publications

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“…The present study reconciles the apparent discrepancy between guinea pigs and mice in the cellular components each requires for acquired tick resistance (17,(21)(22)(23)(24)(25) and illuminates a nonredundant role for basophils in protective immunity to ectoparasites. The acquisition of tick resistance is associated with reduced pathogen transmission from infected ticks (12)(13)(14)(15), and therefore our findings may provide new avenues toward the development of novel control strategies for tick infestations and tick-borne diseases.…”

Section: Figuresupporting

confidence: 72%

“…Alternatively, antigen/antibody-stimulated basophils may function as activators of mast cells that in turn produce effector molecules against ticks. A previous study using mice infested with another tick species, Dermacentor variabilis, demonstrated that mast cells were not essential for acquired tick resistance (24). To our knowledge, the contribution of mast cells to tick resistance has not been reported in other animal species, including guinea pigs.…”

Section: Discussionmentioning

confidence: 63%

“…Instead, one research group suggests that mast cells in place of basophils are important for acquired immunity to ticks in mice, based on the observation that mast cell-deficient mice failed to acquire tick resistance and that basophils were not detected in tick-feeding sites (21)(22)(23). On the other hand, another group showed that the same strain of mast cell-deficient mice developed resistance to another tick species (24,25). Thus, the mechanism underlying acquired immunity to ticks, including the differential roles played by basophils and mast cells, and the influence of genetic background of both ticks and hosts remain to be clarified.…”

Section: Introductionmentioning

confidence: 99%

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Selective ablation of basophils in mice reveals their nonredundant role in acquired immunity against ticks

Wada¹,

Ishiwata²,

Koseki³

et al. 2010

J. Clin. Invest.

278

354

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Ticks are ectoparasitic arthropods that can transmit a variety of microorganisms to humans and animals during blood feeding, causing serious infectious disorders, including Lyme disease. Acaricides are pharmacologic agents that kill ticks. The emergence of acaricide-resistant ticks calls for alternative control strategies for ticks and tick-borne diseases. Many animals develop resistance to ticks after repeated infestations, but the nature of this acquired anti-tick immunity remains poorly understood. Here we investigated the cellular and molecular mechanisms underlying acquired resistance to Haemaphysalis longicornis ticks in mice and found that antibodies were required, as was IgFc receptor expression on basophils but not on mast cells. The infiltration of basophils at tick-feeding sites occurred during the second, but not the first, tick infestation. To assess the requirement for basophil infiltration to acquired tick resistance, mice expressing the human diphtheria toxin receptor under the control of the mast cell protease 8 (Mcpt8) promoter were generated. Diphtheria toxin administration to these mice selectively ablated basophils. Diphtheria toxin-mediated basophil depletion before the second tick infestation resulted in loss of acquired tick resistance. These data provide the first clear evidence, to our knowledge, that basophils play an essential and nonredundant role in antibody-mediated acquired immunity against ticks, which may suggest new strategies for controlling tick-borne diseases.

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Section: Figuresupporting

confidence: 72%

Section: Discussionmentioning

confidence: 63%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Selective ablation of basophils in mice reveals their nonredundant role in acquired immunity against ticks

Wada¹,

Ishiwata²,

Koseki³

et al. 2010

J. Clin. Invest.

278

354

View full text Add to dashboard Cite

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“…Further experiments showed that both mast cells and IgE were implicated in the manifestation of resistance (Matsuda et al 1990) and that the in®ltrating eosinophils in collaboration with mast cells seemed to contribute considerably to disturbances in ticks (rejection or loss of weight; Ushio et al 1993). DenHollander and Allen (1985) also used WBB6F1-W/ W v mice infested with larvae of Dermacentor variabilis ticks and concluded that a de®ciency in tissue mast cells had only a minor eect on the expression of resistance to ticks. Steeves and Allen (1990) showed the presence of basophils in the skin of resistant WBB6F1-W/W v mice infested with larvae of D. variabilis.…”

Section: Introductionmentioning

confidence: 99%

Susceptibility of BALB/c mice to nymphs and larvae of Ixodes ricinus after modulation of IgE production with anti-interleukin-4 or anti-interferon-γ monoclonal antibodies

Christe

Rutti

Brossard

1998

Parasitology Research

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BALB/c mice infested three times with nymphs or larvae of Ixodes ricinus ticks do not acquire resistance as assessed by evaluation of both tick attachment and the weight of engorged nymphs or larvae. Tick challenge causes a gradual increase in total IgE antibody production from the first to the third infestation. Anti-tick IgG antibodies are never detected. When the mice are treated with anti-interleukin-4 (anti-IL-4) or anti-interferon-gamma (anti-IFN-gamma) monoclonal antibodies (mAbs) 1 day before each infestation, they produce fewer or more IgE antibodies, respectively. No effect is observed on IgG antibodies. In IL-4-deficient mice, no IgE or IgG antibody is produced. However, these treatments and the use of IL-4-deficient mice have no negative effect on either tick attachment or the weight of engorged nymphs or larvae. Treatment with anti-IL-4 mAb and the use of IL-4-deficient mice inhibits and abolishes the switching of IgE, respectively, but these are apparently not sufficient to shift the response toward Th1 cells.

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“…In addition to guinea pigs, tick immunity has been described in cattle and rabbits. [3][4][5][6][7] While some have reported anti-tick immunity in mice, 8 others have reported that it did not occur. 9 Wikel and others have recently reported that BALB/c mice repeatedly infested with pathogen-free Ixodes scapularis ticks failed to become infected when subsequently infested with Borrelia burgdorferi-infected ticks, even though mean weights of fed ticks and percentage reaching repletion did not indicate development of acquired resistance.…”

mentioning

confidence: 99%

Prevention of Borrelia burgdorferi transmission in guinea pigs by tick immunity.

Nazario¹,

Das²,

Silva

et al. 1998

The American Journal of Tropical Medicine and Hygiene

104

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Abstract. We examined the effect of repeated infestation of guinea pigs with Ixodes scapularis on the capacity of ticks to transmit Borrelia burgdorferi infection. Repeated challenges with nymphs or larvae lead to a reduction in duration of nymphal tick attachment and weight of recovered ticks consistent with the development of tick immunity. Only one of 18 I. scapularis-immune guinea pigs challenged with B. burgdorferi-infected nymphal ticks became infected, whereas 10 of 18 naive guinea pigs similarly challenged became infected. We conclude that tick immunity interferes with borrelial transmission.Ticks are the most common vector transmitting diseases to humans in the United States. 1 The ixodids, also called hard-bodied ticks, have a complex life cycle involving egg, larval, nymphal, and adult stages. Development of the later three stages requires ingestion of blood. The prolonged period of feeding, 48-96 hr for larvae and nymphs, allows an immune response to develop in certain hosts against tick components. Trager first observed that repeated feeding of larvae or nymphs of Dermacentor sp. upon guinea pigs resulted in tick immunity. 2 Tick immunity is the capacity of previously exposed hosts to interfere with tick feeding and development. A reduction in tick weight, duration of attachment, number of ticks feeding, size of egg mass, and molting success are parameters to measure immunity. In addition to guinea pigs, tick immunity has been described in cattle and rabbits. [3][4][5][6][7] While some have reported anti-tick immunity in mice, 8 others have reported that it did not occur. 9 Wikel and others have recently reported that BALB/c mice repeatedly infested with pathogen-free Ixodes scapularis ticks failed to become infected when subsequently infested with Borrelia burgdorferi-infected ticks, even though mean weights of fed ticks and percentage reaching repletion did not indicate development of acquired resistance. 10 Development of tick immunity involves the interactions of tick antigens with host antibodies, T cells, B cells, mast cells, and basophils. 11 Langerhans' cells in the skin process and present tick antigens to lymphocytes that develop into sensitized lymphocytes and plasma cells secreting antibodies of various isotypes; among these are tissue-binding or homocytotropic antibodies. Antibodies bound to mast cells and basophils through their Fc receptors recognize tick antigens and induce degranulation resulting in development of microvesicles at the attachment site. Also contributing to the various manifestations of tick immunity are the multiple lymphokines, monokines, and chemokines released at the site of attachment. Basophil accumulation at tick attachment sites characterizes the immune reaction termed cutaneous basophil hypersensitivity, 12, 13 although the relative role of this reaction compared with the various other immunoreactants in producing the elements of tick immunity is not well defined, and may vary in different host species.The present paper evaluates the response of guinea pigs t...

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Dermacentor variabilis: Resistance to ticks acquired by mast cell-deficient and other strains of mice

Cited by 31 publications

References 16 publications

Selective ablation of basophils in mice reveals their nonredundant role in acquired immunity against ticks

Selective ablation of basophils in mice reveals their nonredundant role in acquired immunity against ticks

Susceptibility of BALB/c mice to nymphs and larvae of Ixodes ricinus after modulation of IgE production with anti-interleukin-4 or anti-interferon-γ monoclonal antibodies

Prevention of Borrelia burgdorferi transmission in guinea pigs by tick immunity.

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