Infection-derived lipids elicit an immune deficiency circuit in arthropods

Dana K. Shaw, Xiaowei Wang, Lindsey J. Brown, Adela S. Oliva Chávez, Kathryn E. Reif, Alexis A. Smith, Alison J. Scott, Erin E. McClure, Vishant M. Boradia, Holly L. Hammond, Eric J. Sundberg, Greg A. Snyder, Lei Liu, Kathleen DePonte, Margarita Villar, Massaro W. Ueti, José de la Fuente, Robert K. Ernst, Utpal Pal, Erol Fikrig and Joao H. F. Pedra ()
Additional contact information
Dana K. Shaw: University of Maryland School of Medicine
Xiaowei Wang: University of Maryland School of Medicine
Lindsey J. Brown: University of Maryland School of Medicine
Adela S. Oliva Chávez: University of Maryland School of Medicine
Kathryn E. Reif: Animal Disease Research Unit, Agriculture Research Service
Alexis A. Smith: Virginia-Maryland Regional College of Veterinary Medicine, University of Maryland
Alison J. Scott: University of Maryland School of Dentistry
Erin E. McClure: University of Maryland School of Medicine
Vishant M. Boradia: University of Maryland School of Medicine
Holly L. Hammond: University of Maryland School of Medicine
Eric J. Sundberg: Institute of Human Virology, University of Maryland School of Medicine
Greg A. Snyder: Institute of Human Virology, University of Maryland School of Medicine
Lei Liu: Section of Infectious Diseases, Yale University School of Medicine
Kathleen DePonte: Section of Infectious Diseases, Yale University School of Medicine
Margarita Villar: SaBio. Instituto de Investigación en Recursos Cinegéticos IREC, CSIC-UCLM-JCCM
Massaro W. Ueti: Animal Disease Research Unit, Agriculture Research Service
José de la Fuente: SaBio. Instituto de Investigación en Recursos Cinegéticos IREC, CSIC-UCLM-JCCM
Robert K. Ernst: University of Maryland School of Medicine
Utpal Pal: Virginia-Maryland Regional College of Veterinary Medicine, University of Maryland
Erol Fikrig: Section of Infectious Diseases, Yale University School of Medicine
Joao H. F. Pedra: University of Maryland School of Medicine

Nature Communications, 2017, vol. 8, issue 1, 1-13

Abstract: Abstract The insect immune deficiency (IMD) pathway resembles the tumour necrosis factor receptor network in mammals and senses diaminopimelic-type peptidoglycans present in Gram-negative bacteria. Whether unidentified chemical moieties activate the IMD signalling cascade remains unknown. Here, we show that infection-derived lipids 1-palmitoyl-2-oleoyl-sn-glycero-3-phosphoglycerol (POPG) and 1-palmitoyl-2-oleoyl diacylglycerol (PODAG) stimulate the IMD pathway of ticks. The tick IMD network protects against colonization by three distinct bacteria, that is the Lyme disease spirochete Borrelia burgdorferi and the rickettsial agents Anaplasma phagocytophilum and A. marginale. Cell signalling ensues in the absence of transmembrane peptidoglycan recognition proteins and the adaptor molecules Fas-associated protein with a death domain (FADD) and IMD. Conversely, biochemical interactions occur between x-linked inhibitor of apoptosis protein (XIAP), an E3 ubiquitin ligase, and the E2 conjugating enzyme Bendless. We propose the existence of two functionally distinct IMD networks, one in insects and another in ticks.

Date: 2017
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DOI: 10.1038/ncomms14401

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