Immune responses of Aedes togoi, Anopheles paraliae and Anopheles lesteri against nocturnally subperiodic Brugia malayi microfilariae during migration from the midgut to the site of development

Watcharatip Dedkhad, Bruce M Christensen, Lyric C Bartholomay, Deepak Joshi, Chayanit Hempolchom, Atiporn Saeung

Lymphatic filariasis is a mosquito-borne disease caused by filarioid nematodes. A comparative understanding of parasite biology and host-parasite interactions can provide information necessary for developing intervention programmes for vector control. Here, to understand such interactions, we choose highly susceptible filariasis vectors (Aedes togoi and Anopheles lesteri) as well as Anopheles paraliae, which has lower susceptibility, infected them with nocturnally subperiodic (NSP) Brugia malayi microfilariae (mf) and studied the exsheathment, migration and innate immune responses among them. Mosquito-parasite relationships were systematically investigated from the time mf entered the midgut until they reached their development site in the thoracic musculature (12 time points). Results showed that exsheathment of B. malayi mf occurred in the midgut of all mosquito species and was completed within 24 h post-blood meal. The migration of B. malayi mf from the midgut to thoracic muscles of the highly susceptible mosquitoes Ae. togoi and An. lesteri was more rapid than in the low susceptibility mosquito, An. paraliae. Melanisation and degeneration, two distinct refractory phenotypes, of mf were found in the midgut, haemocoel and thoracic musculature of all mosquito species. Melanisation is a complex biochemical cascade that results in deposition of melanin pigment on a capsule around the worms. Also, some biological environments in the body are inhospitable to parasite development and cause direct toxicity that results in vacuolated or degenerated worms. Even though Ae. togoi is highly susceptible to B. malayi, melanisation responses against B. malayi mf were first noted in the haemocoel of Ae. togoi, followed by a degeneration process. In contrast, in An. lesteri and An. paraliae, the degeneration process occurred in the haemocoel and thoracic musculature prior to melanisation responses. This study provides a thorough description of the comparative pathobiology of responses of mosquitoes against the filarial worm B. malayi.