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First published online August 4, 2005
Journal of Experimental Biology 208, 3211-3218 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01756

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A chemotactic response facilitates mosquito salivary gland infection by malaria sporozoites

Mayumi Akaki and James A. Dvorak^*

Biochemical and Biophysical Parasitology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, 12735 Twinbrook Parkway, Bethesda, MD 20892-8132, USA

View larger version (22K): [in a new window]   Fig. 1. (A) Schematic diagram of the custom-built chamber used for studies of sporozoite chemotaxis. a, 18 mmx18 mm coverglass; b, 9 mmx18 mm coverglass. (B) Diagram of the mathematical procedure used to analyze the direction of sporozoite movement calculated as tangency angle . Movement directed to the bottom of the figure is defined as 90°.

View larger version (84K): [in a new window]   Fig. 2. Sporozoite transport through the hemolymph in mosquito wing veins. Arrows show the progress of a sporozoite (green) floating passively through a peripheral vein (upper images, 0–2 s) and subsequently through a larger central vein (bottom images, 2.64–4.64 s). Asterisks indicate a sporozoite apparently caught in a wing vein constriction. The number at the lower left in each frame is the time (s) at which the image was recorded. Scale bar, 100 µm.

View larger version (67K): [in a new window]   Fig. 3. Representative examples of sporozoite motility in assay medium. (A) Circular gliding motion. X–Y maximum projection of five time-lapse images acquired over a period 21 s, artificially colored as green (the first four frames) and yellow (the last frame). The white arrows indicate the direction of rotation of the two sporozoites. (B) Attached waving motion. X–Y maximum projection of four time-lapse images acquired over a 32 s period, artificially colored as red, cyan, green and yellow, respectively. Scale bars, 5 µm.

View larger version (79K): [in a new window]   Fig. 4. Representative examples of the effects of salivary gland homogenate on sporozoite motility. (A) Random sporozoite motility in Matrigel. (B) Directed sporozoite motility in the presence of salivary gland homogenate. X–Y (upper left), X-time (bottom), and Y-time (upper right) maximum projections of 60 time-lapse images acquired over a 318 s period. The yellow outlined arrows show the directions of sporozoite movement (green). To highlight the influence of time on sporozoite direction, the yellow broken lines indicating the starting and ending points of a sporozoite moving in X–Y space were projected into both X- and Y-time space to demonstrate the influence of time on motility. The solid yellow arrow in B indicates the relative position of the salivary gland homogenate.

View larger version (12K): [in a new window]   Fig. 5. Effects of sample preparation temperature on sporozoite motility. Sporozoites in Matrigel were exposed at 4°C for 40 min and transferred to the chamber at 20°C at time 0. The graph is a summary of 240 time-lapse images acquired over a 21 min period. Migration area of sporozoites in each image was normalized to sporozoite number.

View larger version (100K): [in a new window]   Fig. 6. Sporozoite motility in the absence of salivary gland homogenate. (A) Salivary gland-derived sporozoites. (B) Oocyst- and hemolymph-derived sporozoites. The images represent X–Y maximum projections of 50 time-lapse images acquired over a 265 s period. The yellow outlined arrows show the direction of sporozotie movement (green). Scale bars, 50 µm.

View larger version (105K): [in a new window]   Fig. 7. The effects of salivary gland treatment on sporozoite motility. Sporozoite motility in the presence of (A) unheated or (B) heated salivary gland homogenate. X–Y maximum projections of 106 time-lapse images acquired over a 561 s period. The yellow outlined arrows show the direction of sporozoite movement (green). The yellow solid arrows points to the relative position of the unheated or heated salivary gland homogenate. The white arrows point to fluorescent beads (b). Scale bars, 50 µm.

View larger version (79K): [in a new window]   Fig. 8. The effects of the site of origin of sporozoites on motility in the presence of salivary gland homogenate. (A) Salivary gland-derived sporozoites. (B) Oocyst- and hemolymph-derived sporozoites. The images represent X–Y maximum projections of 140 time-lapse images acquired over a 742 s period. The yellow outlined arrows show the direction of sporozotie movement (green). The yellow solid arrows indicate the relative position of the salivary gland homogenate. The white arrows indicate fluorescent beads (b). Scale bars, 50 µm.