Anaplasma phagocytophilum induces Ixodes scapularis ticks to express an antifreeze glycoprotein gene that enhances their survival in the cold
Girish Neelakanta, … , John F. Anderson, Erol Fikrig
Girish Neelakanta, … , John F. Anderson, Erol Fikrig
Published August 25, 2010
Citation Information: J Clin Invest. 2010;120(9):3179-3190. https://doi.org/10.1172/JCI42868.
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Research Article

Anaplasma phagocytophilum induces Ixodes scapularis ticks to express an antifreeze glycoprotein gene that enhances their survival in the cold

Abstract

In the United States, Ixodes scapularis ticks overwinter in the Northeast and Upper Midwest and transmit the agent of human granulocytic anaplasmosis, Anaplasma phagocytophilum, among other pathogens. We now show that the presence of A. phagocytophilum in I. scapularis ticks increases their ability to survive in the cold. We identified an I. scapularis antifreeze glycoprotein, designated IAFGP, and demonstrated via RNAi knockdown studies the importance of IAFGP for the survival of I. scapularis ticks in a cold environment. Transfection studies also show that IAFGP increased the viability of yeast cells subjected to cold temperature. Remarkably, A. phagocytophilum induced the expression of iafgp, thereby increasing the cold tolerance and survival of I. scapularis. These data define a molecular basis for symbiosis between a human pathogenic bacterium and its arthropod vector and delineate what we believe to be a new pathway that may be targeted to alter the life cycle of this microbe and its invertebrate host.

Authors

Girish Neelakanta, Hameeda Sultana, Durland Fish, John F. Anderson, Erol Fikrig

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Figure 5

Silencing of iafgp by RNAi reduces survival of ticks at cold temperatures.

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Silencing of iafgp by RNAi reduces survival of ticks at cold temperature...
(A) QRT-PCR showing reduced iafgp mRNA levels in iafgp-dsRNA–injected uninfected ticks compared with the mock-dsRNA control. (B) Survival of mock-dsRNA–injected and iafgp-dsRNA–injected ticks at the LT50 time point. (C) Mobility (in cm) by mock-dsRNA–injected and iafgp-dsRNA–injected ticks at LT50 time point (–20°C, 25 min). (A–C) White circles represent mock-dsRNA–injected ticks, and white triangles represent iafgp-dsRNA–injected ticks. QRT-PCR showing reduced iafgp mRNA levels (D) and A. phagocytophilum burden (E) in mock-injected (black circles) and iafgp-dsRNA–injected (black triangles) ticks partially fed (48 hours) on A. phagocytophilum–infected mice. (F) Survival percentage at –20°C, 50-minute time point of mock-dsRNA–injected (black circles) and iafgp-dsRNA–injected (black triangles) ticks partially fed (48 hours) on A. phagocytophilum–infected mice. Each circle in A, C, D, and E represents 1 individual tick, and each circle in B and F represents 1 independent experiment with 10 ticks/group/experiment. Statistics in A, D, and E were performed using 2-tailed Student’s t test and in B, C, and F using Mann-Whitney U test. n = 60 (C) for both mock and iafgp-dsRNA ticks. Horizontal lines in A, D, and E represent average and in B, C, and F represent median of the readings from independent experiments/ticks.