Bordetella parapertussis is a human pathogen that causes
whooping cough. The increasing incidence of B. parapertussis has been attributed to the lack of cross protection induced by
pertussis vaccines. It was previously shown that B. parapertussis is able to avoid bacterial killing by polymorphonuclear leukocytes (PMN) if specific opsonic
antibodies are not present at the site of interaction. Here, we evaluated the outcome of B. parapertussis innate interaction with human macrophages, a less aggressive type of cell and a known reservoir of many persistent pathogens. The results showed that in the absence of
opsonins,
O antigen allows B. parapertussis to inhibit phagolysosomal fusion and to remain alive inside macrophages. The
O antigen targets B. parapertussis to
lipid rafts that are retained in the membrane of phagosomes that do not undergo lysosomal maturation. Forty-eight hours after
infection, wild-type B. parapertussis bacteria but not the
O antigen-deficient mutants were found colocalizing with
lipid rafts and alive in nonacidic compartments. Taken together, our data suggest that in the absence of opsonic
antibodies, B. parapertussis survives inside macrophages by preventing phagolysosomal maturation in a
lipid raft- and
O antigen-dependent manner. Two days after
infection, about 15% of macrophages were found loaded with live bacteria inside
flotillin-enriched phagosomes that had access to nutrients provided by the host cell recycling pathway, suggesting the development of an intracellular
infection.
IgG opsonization drastically changed this interaction, inducing efficient bacterial killing. These results highlight the need for B. parapertussis opsonic
antibodies to induce bacterial clearance and prevent the eventual establishment of cellular reservoirs of this pathogen.