Dome1-JAK-STAT signaling between parasite and host integrates vector immunity and development

Vipin S. Rana; Chrysoula Kitsou; Shraboni Dutta; Michael H. Ronzetti; Min Zhang; Quentin Bernard; Alexis A. Smith; Julen Tomás-Cortázar; Xiuli Yang; Ming Jie Wu; Oleksandra Kepple; Weizhong Li; Jennifer E. Dwyer; Jaqueline Matias; Bolormaa Baljinnyam; Jonathan D. Oliver; Nallakkandi Rajeevan; Joao H.F. Pedra; Sukanya Narasimhan; Yan Wang; Ulrike Munderloh; Erol Fikrig; Anton Simeonov; Juan Anguita; Utpal Pal

doi:10.1126/science.abl3837

Dome1-JAK-STAT signaling between parasite and host integrates vector immunity and development

Vipin S. Rana, Chrysoula Kitsou, Shraboni Dutta, Michael H. Ronzetti, Min Zhang, Quentin Bernard, Alexis A. Smith, Julen Tomás-Cortázar, Xiuli Yang, Ming Jie Wu, Oleksandra Kepple, Weizhong Li, Jennifer E. Dwyer, Jaqueline Matias, Bolormaa Baljinnyam, Jonathan D. Oliver, Nallakkandi Rajeevan, Joao H.F. Pedra, Sukanya Narasimhan, Yan WangUlrike Munderloh, Erol Fikrig, Anton Simeonov, Juan Anguita, Utpal Pal

Environmental Health Sciences

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Abstract

Ancestral signaling pathways serve critical roles in metazoan development, physiology, and immunity. We report an evolutionary interspecies communication pathway involving a central Ixodes scapularis tick receptor termed Dome1, which acquired a mammalian cytokine receptor motif exhibiting high affinity for interferon-gamma (IFN-g). Host-derived IFN-g facilitates Dome1-mediated activation of the Ixodes JAK-STAT pathway. This accelerates tick blood meal acquisition and development while upregulating antimicrobial components. The Dome1-JAK-STAT pathway, which exists in most Ixodid tick genomes, regulates the regeneration and proliferation of gut cells-including stem cells-and dictates metamorphosis through the Hedgehog and Notch-Delta networks, ultimately affecting Ixodes vectorial competence. We highlight the evolutionary dependence of I. scapularis on mammalian hosts through cross-species signaling mechanisms that dually influence arthropod immunity and development.

Original language	English (US)
Article number	eabl3837
Journal	Science
Volume	379
Issue number	6628
DOIs	https://doi.org/10.1126/science.abl3837
State	Published - Jan 13 2023

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© 2023 American Association for the Advancement of Science. All rights reserved.

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Rana, V. S., Kitsou, C., Dutta, S., Ronzetti, M. H., Zhang, M., Bernard, Q., Smith, A. A., Tomás-Cortázar, J., Yang, X., Wu, M. J., Kepple, O., Li, W., Dwyer, J. E., Matias, J., Baljinnyam, B., Oliver, J. D., Rajeevan, N., Pedra, J. H. F., Narasimhan, S., ... Pal, U. (2023). Dome1-JAK-STAT signaling between parasite and host integrates vector immunity and development. Science, 379(6628), Article eabl3837. https://doi.org/10.1126/science.abl3837

Rana, VS, Kitsou, C, Dutta, S, Ronzetti, MH, Zhang, M, Bernard, Q, Smith, AA, Tomás-Cortázar, J, Yang, X, Wu, MJ, Kepple, O, Li, W, Dwyer, JE, Matias, J, Baljinnyam, B, Oliver, JD, Rajeevan, N, Pedra, JHF, Narasimhan, S, Wang, Y, Munderloh, U, Fikrig, E, Simeonov, A, Anguita, J & Pal, U 2023, 'Dome1-JAK-STAT signaling between parasite and host integrates vector immunity and development', Science, vol. 379, no. 6628, eabl3837. https://doi.org/10.1126/science.abl3837

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abstract = "Ancestral signaling pathways serve critical roles in metazoan development, physiology, and immunity. We report an evolutionary interspecies communication pathway involving a central Ixodes scapularis tick receptor termed Dome1, which acquired a mammalian cytokine receptor motif exhibiting high affinity for interferon-gamma (IFN-g). Host-derived IFN-g facilitates Dome1-mediated activation of the Ixodes JAK-STAT pathway. This accelerates tick blood meal acquisition and development while upregulating antimicrobial components. The Dome1-JAK-STAT pathway, which exists in most Ixodid tick genomes, regulates the regeneration and proliferation of gut cells-including stem cells-and dictates metamorphosis through the Hedgehog and Notch-Delta networks, ultimately affecting Ixodes vectorial competence. We highlight the evolutionary dependence of I. scapularis on mammalian hosts through cross-species signaling mechanisms that dually influence arthropod immunity and development.",

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AU - Zhang, Min

AU - Bernard, Quentin

AU - Smith, Alexis A.

AU - Tomás-Cortázar, Julen

AU - Yang, Xiuli

AU - Wu, Ming Jie

AU - Kepple, Oleksandra

AU - Li, Weizhong

AU - Dwyer, Jennifer E.

AU - Matias, Jaqueline

AU - Baljinnyam, Bolormaa

AU - Oliver, Jonathan D.

AU - Rajeevan, Nallakkandi

AU - Pedra, Joao H.F.

AU - Narasimhan, Sukanya

AU - Wang, Yan

AU - Munderloh, Ulrike

AU - Fikrig, Erol

AU - Simeonov, Anton

AU - Anguita, Juan

AU - Pal, Utpal

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N2 - Ancestral signaling pathways serve critical roles in metazoan development, physiology, and immunity. We report an evolutionary interspecies communication pathway involving a central Ixodes scapularis tick receptor termed Dome1, which acquired a mammalian cytokine receptor motif exhibiting high affinity for interferon-gamma (IFN-g). Host-derived IFN-g facilitates Dome1-mediated activation of the Ixodes JAK-STAT pathway. This accelerates tick blood meal acquisition and development while upregulating antimicrobial components. The Dome1-JAK-STAT pathway, which exists in most Ixodid tick genomes, regulates the regeneration and proliferation of gut cells-including stem cells-and dictates metamorphosis through the Hedgehog and Notch-Delta networks, ultimately affecting Ixodes vectorial competence. We highlight the evolutionary dependence of I. scapularis on mammalian hosts through cross-species signaling mechanisms that dually influence arthropod immunity and development.

AB - Ancestral signaling pathways serve critical roles in metazoan development, physiology, and immunity. We report an evolutionary interspecies communication pathway involving a central Ixodes scapularis tick receptor termed Dome1, which acquired a mammalian cytokine receptor motif exhibiting high affinity for interferon-gamma (IFN-g). Host-derived IFN-g facilitates Dome1-mediated activation of the Ixodes JAK-STAT pathway. This accelerates tick blood meal acquisition and development while upregulating antimicrobial components. The Dome1-JAK-STAT pathway, which exists in most Ixodid tick genomes, regulates the regeneration and proliferation of gut cells-including stem cells-and dictates metamorphosis through the Hedgehog and Notch-Delta networks, ultimately affecting Ixodes vectorial competence. We highlight the evolutionary dependence of I. scapularis on mammalian hosts through cross-species signaling mechanisms that dually influence arthropod immunity and development.

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Dome1-JAK-STAT signaling between parasite and host integrates vector immunity and development

Abstract

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