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 4

Expression of iafgp is developmentally regulated and induced by cold and A. phagocytophilum.

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Expression of iafgp is developmentally regulated and induced by cold and...
(A) The expression of iafgp is developmentally regulated in I. scapularis ticks. Total RNA from unfed larvae (n = 10), unfed nymphs (n = 10), unfed adult males (n = 10 ticks), and unfed adult females (n = 10) was prepared in triplicate and the amount of iafgp transcripts was quantified by QRT-PCR and normalized to tick beta-actin. Error bars indicate + SD from the mean. (B) The expression of iafgp in nymphs is induced by cold temperatures. Total RNA from nymphs incubated at different temperatures (23°C, 10°C, 4°C, and 0°C) was prepared, and the iafgp transcript levels were quantified by QRT-PCR. Each circle represents 1 individual tick. The differences in iafgp levels at 4°C and 0°C in comparison with 23°C is significant (P < 0.05, Student’s t test). (C) Total RNA from uninfected nymphs (white circles) and A. phagocytophilum–infected nymphs (black circles) incubated at different temperatures (23°C, 10°C, 4°C, and 0°C) was prepared, and transcript levels of iafgp were quantified by QRT-PCR. Levels of iafgp were normalized to tick beta-actin. Each circle represents 1 individual tick. The elevated levels of iafgp transcripts in A. phagocytophilum–infected nymphs in comparison with the uninfected controls is significant at all tested temperatures (P < 0.05, Student’s t test). Horizontal lines in panels B and C indicate average of the readings from independent ticks.