Environmental Constraints Guide Migration of Malaria Parasites during Transmission

Janina Kristin Hellmann, Sylvia Münter, Mikhail Kudryashev, Simon Schulz, Kirsten Heiss,
Ann-Kristin Müller, Kai Matuschewski, Joachim P. Spatz, Ulrich S. Schwarz, Friedrich Frischknecht

PLoS Pathogens 7:e1002080 (2011)

Migrating cells are guided in complex environments mainly by
chemotaxis or structural cues presented by the surrounding
tissue. During transmission of malaria, parasite motility in the skin
is important for Plasmodium sporozoites to reach the blood
circulation. Here we show that sporozoite migration varies in
different skin environments the parasite encounters at the arbitrary
sites of the mosquito bite. In order to systematically examine how
sporozoite migration depends on the structure of the environment, we
studied it in micro-fabricated obstacle arrays. The trajectories
observed in vivo and in vitro closely resemble each other suggesting
that structural constraints can be sufficient to guide Plasmodium
sporozoites in complex environments. Sporozoite speed in different
environments is optimized for migration and correlates with
persistence length and dispersal. However, this correlation breaks
down in mutant sporozoites that show adhesion impairment due to the
lack of TRAP-like protein (TLP) on their surfaces. This may explain
their delay in infecting the host. The flexibility of sporozoite
adaption to different environments and a favorable speed for optimal
dispersal ensures efficient host switching during malaria
transmission.