A multi-adenylate cyclase regulator at the flagellar tip controls African trypanosome transmission

Sabine Bachmaier (), Giacomo Giacomelli, Estefanía Calvo-Alvarez, Larissa Rezende Vieira, Jan Abbeele, Aris Aristodemou, Esben Lorentzen, Matt K. Gould, Ana Brennand, Jean-William Dupuy, Ignasi Forné, Axel Imhof, Marc Bramkamp, Didier Salmon, Brice Rotureau and Michael Boshart ()
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Sabine Bachmaier: Ludwig-Maximilians-University Munich (LMU)
Giacomo Giacomelli: Ludwig-Maximilians-University Munich (LMU), 82152 Martinsried and Institute for General Microbiology, Kiel University
Estefanía Calvo-Alvarez: Université de Paris, INSERM U1201, Trypanosome Cell Biology Unit, Trypanosome Transmission Group
Larissa Rezende Vieira: Federal University of Rio de Janeiro
Jan Abbeele: Institute of Tropical Medicine Antwerp
Aris Aristodemou: Ludwig-Maximilians-University Munich (LMU)
Esben Lorentzen: Aarhus University
Matt K. Gould: Ludwig-Maximilians-University Munich (LMU)
Ana Brennand: Ludwig-Maximilians-University Munich (LMU)
Jean-William Dupuy: Plateforme Protéome
Ignasi Forné: Ludwig-Maximilians-University Munich
Axel Imhof: Ludwig-Maximilians-University Munich
Marc Bramkamp: Ludwig-Maximilians-University Munich (LMU), 82152 Martinsried and Institute for General Microbiology, Kiel University
Didier Salmon: Federal University of Rio de Janeiro
Brice Rotureau: Université de Paris, INSERM U1201, Trypanosome Cell Biology Unit, Trypanosome Transmission Group
Michael Boshart: Ludwig-Maximilians-University Munich (LMU)

Nature Communications, 2022, vol. 13, issue 1, 1-17

Abstract: Abstract Signaling from ciliary microdomains controls developmental processes in metazoans. Trypanosome transmission requires development and migration in the tsetse vector alimentary tract. Flagellar cAMP signaling has been linked to parasite social motility (SoMo) in vitro, yet uncovering control of directed migration in fly organs is challenging. Here we show that the composition of an adenylate cyclase (AC) complex in the flagellar tip microdomain is essential for tsetse salivary gland (SG) colonization and SoMo. Cyclic AMP response protein 3 (CARP3) binds and regulates multiple AC isoforms. CARP3 tip localization depends on the cytoskeletal protein FLAM8. Re-localization of CARP3 away from the tip microdomain is sufficient to abolish SoMo and fly SG colonization. Since intrinsic development is normal in carp3 and flam8 knock-out parasites, AC complex-mediated tip signaling specifically controls parasite migration and thereby transmission. Participation of several developmentally regulated receptor-type AC isoforms may indicate the complexity of the in vivo signals perceived.

Date: 2022
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DOI: 10.1038/s41467-022-33108-z

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