Abstract
Small rodents serve as reservoir hosts for tick-borne pathogens, such as the spirochetes causing Lyme disease. Whether natural coinfections with other macroparasites alter the success of tick feeding, antitick immunity, and the host's reservoir competence for tick-borne pathogens remains to be determined. In a parasitological survey of wild mice in Berlin, Germany, approximately 40% of Ixodes ricinus-infested animals simultaneously harbored a nematode of the genus Heligmosomoides. We therefore aimed to analyze the immunological impact of the nematode/tick coinfection as well as its effect on the tick-borne pathogen Borrelia afzelii. Hosts experimentally coinfected with Heligmosomoides polygyrus and larval/nymphal I. ricinus ticks developed substantially stronger systemic type 2 T helper cell (Th2) responses, on the basis of the levels of GATA-3 and interleukin-13 expression, than mice infected with a single pathogen. During repeated larval infestations, however, anti-tick Th2 reactivity and an observed partial immunity to tick feeding were unaffected by concurrent nematode infections. Importantly, the strong systemic Th2 immune response in coinfected mice did not affect susceptibility to tick-borne B. afzelii. An observed trend for decreased local and systemic Th1 reactivity against B. afzelii in coinfected mice did not result in a higher spirochete burden, nor did it facilitate bacterial dissemination or induce signs of immunopathology. Hence, this study indicates that strong systemic Th2 responses in nematode/tick-coinfected house mice do not affect the success of tick feeding and the control of the causative agent of Lyme disease.
Highlights
Ticks are the most important arthropod vectors of pathogens in temperate regions of the Northern Hemisphere
To examine whether the expected strong Th2 immune responses associated with intestinal nematode infections interfere with, first, the experimental host’s development of antitick immunity and, second, the control of tick-borne pathogens, we established an experimental model of coinfection in inbred laboratory mice, compared susceptibility to tick feeding and to tick-borne infection with Lyme disease (LD) spirochetes, and evaluated local and systemic immune responses
Small rodents serve as reservoir hosts for several tick-borne pathogens in Europe, and the I. ricinus tick is the vector for the agents of
Summary
Ticks are the most important arthropod vectors of pathogens in temperate regions of the Northern Hemisphere. To examine whether the expected strong Th2 immune responses associated with intestinal nematode infections interfere with, first, the experimental host’s development of antitick immunity (measured by means of determination of tick-specific cytokine responses and the success of repeated tick feeding) and, second, the control of tick-borne pathogens, we established an experimental model of coinfection in inbred laboratory mice, compared susceptibility to tick feeding and to tick-borne infection with LD spirochetes, and evaluated local and systemic immune responses. We show that (i) H. polygyrus and I. ricinus frequently parasitize wild Apodemus mice in Berlin; (ii) local anti-I. ricinus immune responses in laboratory house mice are not altered by a concurrent nematode infection, despite the induction of extraordinarily high systemic Th2 responses by nematode/tick coinfections; (iii) the nematode infection does not alter the feeding success of pathogen-free tick larvae and spirochete-infected nymphs or the development of partial immunity toward repeated tick infestations; and (iv) the nematode coinfection does not affect the tick-borne transmission, replication, and dissemination of B. afzelii spirochetes in house mice
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