The angiopoietin-Tie2 pathway regulates Purkinje cell dendritic morphogenesis in a cell-autonomous manner

Robert Luck, Andromachi Karakatsani, Bhavin Shah, Geza Schermann, Heike Adler, Janina Kupke, Nathalie Tisch, Hyun-Woo Jeong, Michaela Kerstin Back, Florian Hetsch, Anna D'Errico, Michele De Palma, Ellen Wiedtke, Dirk Grimm, Amparo Acker-Palmer, Jakob von Engelhardt, Ralf H. Adams, Hellmut G. Augustin, Carmen Ruiz de Almodóvar

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Neuro-vascular communication is essential to synchronize central nervous system development. Here, we identify angiopoietin/Tie2 as a neuro-vascular signaling axis involved in regulating dendritic morphogenesis of Purkinje cells (PCs). We show that in the developing cerebellum Tie2 expression is not restricted to blood vessels, but it is also present in PCs. Its ligands angiopoietin-1 (Ang1) and angiopoietin-2 (Ang2) are expressed in neural cells and endothelial cells (ECs), respectively. PC-specific deletion of Tie2 results in reduced dendritic arborization, which is recapitulated in neural-specific Ang1-knockout and Ang2 full-knockout mice. Mechanistically, RNA sequencing reveals that Tie2-deficient PCs present alterations in gene expression of multiple genes involved in cytoskeleton organization, dendritic formation, growth, and branching. Functionally, mice with deletion of Tie2 in PCs present alterations in PC network functionality. Altogether, our data propose Ang/Tie2 signaling as a mediator of intercellular communication between neural cells, ECs, and PCs, required for proper PC dendritic morphogenesis and function.
Original languageEnglish
Article number109522
JournalCell Reports
Volume36
Issue number7
DOIs
Publication statusPublished - 17 Aug 2021
Externally publishedYes

Funding

We thank the Nikon Imaging Center, the Math-Clinic, and the INBC of the University of Heidelberg for their support. We thank Prof. Susan E. Quaggin for providing the Ang1 fl/fl mice (supported by the National Institutes of Health ( P30 DK114857 [PI-SEQ]), Prof. Barski for the Pcp2-Cre mice, and Prof. Dr. Hannah Monyer for the Nestin:Cre mice. We thank Andreas Fischer and Juan Rodriguez-Vita for their support with the IPA analysis. We thank Melanie Richter, Alberto Arenas Molina, Daniel Maeso Miguel, Philip Ruthig, and Yi Lien for technical assistance and Prof. Daniela Mauceri and the entire Ruiz de Almodovar lab for useful discussions. The authors gratefully acknowledge the data storage service SDS@hd supported by the Ministry of Science , Research and the Arts Baden-Württemberg (M.W.K.) and the German Research Foundation (DFG) through grant INST 35/1314-1 FUGG and INST 35/1503-1 FUGG . R.L. was supported by a Boehringer Ingelheim Fonds fellowship. This work was supported by the Schram Foundation and the Chica and Heinz Schaller Foundation , by research grants of the Deutsche Forschungsgemeinschaft (DFG) from FOR2325 (“Interactions at the Neurovascular Interface” [to C.R.d.A and R.H.A.]), by DFG grants from SFB1366 (“Vascular Control of Organ Function;” Project number 394046768-SFB 1366 ; [to C.R.d.A., R.H.A., and H.G.A.]), by funds from the Baden-Württemberg Stiftung special programme “Angioformatics Single Cell Platform” (to C.R.d.A. and to H.G.A.), and by the European Research Council Consolidator grant 864875 “OLI.VAS” (to C.R.d.A.) and ERC Advance Grant 787181 “Angiomature” (to H.G.A.). We thank the Nikon Imaging Center, the Math-Clinic, and the INBC of the University of Heidelberg for their support. We thank Prof. Susan E. Quaggin for providing the Ang1fl/fl mice (supported by the National Institutes of Health (P30 DK114857 [PI-SEQ]), Prof. Barski for the Pcp2-Cre mice, and Prof. Dr. Hannah Monyer for the Nestin:Cre mice. We thank Andreas Fischer and Juan Rodriguez-Vita for their support with the IPA analysis. We thank Melanie Richter, Alberto Arenas Molina, Daniel Maeso Miguel, Philip Ruthig, and Yi Lien for technical assistance and Prof. Daniela Mauceri and the entire Ruiz de Almodovar lab for useful discussions. The authors gratefully acknowledge the data storage service SDS@hd supported by the Ministry of Science, Research and the Arts Baden-W?rttemberg (M.W.K.) and the German Research Foundation (DFG) through grant INST 35/1314-1 FUGG and INST 35/1503-1 FUGG. R.L. was supported by a Boehringer Ingelheim Fonds fellowship. This work was supported by the Schram Foundation and the Chica and Heinz Schaller Foundation, by research grants of the Deutsche Forschungsgemeinschaft (DFG) from FOR2325 (?Interactions at the Neurovascular Interface? [to C.R.d.A and R.H.A.]), by DFG grants from SFB1366 (?Vascular Control of Organ Function;? Project number 394046768-SFB 1366; [to C.R.d.A. R.H.A. and H.G.A.]), by funds from the Baden-W?rttemberg Stiftung special programme ?Angioformatics Single Cell Platform? (to C.R.d.A. and to H.G.A.), and by the European Research Council Consolidator grant 864875 ?OLI.VAS? (to C.R.d.A.) and ERC Advance Grant 787181 ?Angiomature? (to H.G.A.). Conceptualization, R.L. and C.R.d.A.; methodology, R.L. M.K.M. F.H. A.D. and E.W.; software, G.S.; formal analysis, R.L. A.K. B.S. G.S. J.K. N.T. M.K.M. F.H. and A.D.; investigation, R.L. A.K. B.S. G.S. H.A. J.K. N.T. M.K.M. F.H. A.D. and E.W.; resources, M.D.P. D.G. A.A.P. J.v.E. H.G.A. and C.R.d.A.; writing ? original draft, R.L. and C.R.d.A.; writing ? review & editing, R.L. A.K. B.S. G.S. N.T. A.D. D.G. A.A.P. J.v.E. R.H.A. H.G.A. and C.R.d.A.; visualization, R.L. and C.R.d.A.; supervision, C.R.d.A.; funding acquisition, A.A.P. R.H.A. H.G.A. and C.R.d.A. The authors declare no competing interests. One or more of the authors of this paper self-identifies as a member of the LGBTQ+ community.

FundersFunder number
Ministry of Science, Research and the Arts Baden-W?
Nikon Imaging Center
Schram Foundation
National Institutes of Health
National Institute of Diabetes and Digestive and Kidney DiseasesP30DK114857
Baden-Württemberg Stiftung
European Research Council864875, 787181
Boehringer Ingelheim Fonds
Deutsche ForschungsgemeinschaftSFB1366, INST 35/1314-1 FUGG, INST 35/1503-1 FUGG, 394046768-SFB 1366
Universität Heidelberg
Ministerium für Wissenschaft, Forschung und Kunst Baden-Württemberg
International Permafrost Association
Chica and Heinz Schaller Foundation

    Fingerprint

    Dive into the research topics of 'The angiopoietin-Tie2 pathway regulates Purkinje cell dendritic morphogenesis in a cell-autonomous manner'. Together they form a unique fingerprint.

    Cite this