Effects of selected blood-derived factors on innate immunity in the human body louse

Abstract

Background: The human body louse (Pediculus humanus humanus) is a host-specific hematophagous ectoparasite that frequently infests populations experiencing a breakdown of hygienic conditions. Body lice are also vectors for several bacterial human pathogens, including Bartonella quintana, the agent of trench fever. However, the factors that influence immunity and infection in body lice are poorly understood. Human infection with B. quintana is associated with alcoholism and homelessness and can coincide with elevated circulating levels of the cytokine IL-10 and the inflammatory marker neopterin. Hematophagous arthropods are capable of responding physiologically and immunologically to a variety of biomolecules present in the blood of their hosts. Therefore, we sought to investigate whether ingestion of alcohol, its metabolic product acetaldehyde, IL-10 or neopterin could affect innate immunity and infection in the body louse.

Methods: Groups of lice were provisioned multiple blood meals containing physiological concentrations of alcohol, acetaldehyde, IL-10 or neopterin, and expression of six previously identified immunity-related genes (Defensin 1, Defensin 2, Prophenoloxidase, Hemocytin, Noduler and Dual Oxidase) was examined by qRT-PCR.

Results: Alcohol, acetaldehyde and IL-10 had no significant effects on gene expression relative to blood-fed controls while ingestion of neopterin significantly downregulated expression of Defensin 1 and Defensin 2. Nonetheless, ingestion of neopterin concurrent with B. quintana had no significant effect on the load of infection, indicating that neopterin-induced repression of Defensin expression is insufficient to reduce resistance to the pathogen.

Conclusions: Our findings demonstrate that the immune system of body lice can be affected by factors present in the blood of their human hosts and suggest potential conservation of the function of some immune molecules from human host to ectoparasite. Further, the discord between the effects of neopterin on immunity-related gene expression and B. quintana load highlights the complexity of the regulation of pathogen infection in the louse vector.

Keywords: Bartonella quintana; IL-10; acetaldehyde; ethanol; immunity; infection.