Non-muscle myosin II drives critical steps of nematocyst morphogenesis

Summary: Nematocysts are generated by secretion of proteins into a post-Golgi compartment. They consist of a capsule that elongates into a long tube, which is coiled inside the capsule matrix and expelled during its nano-second discharge deployed for prey capture. The driving force for discharge is...

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Main Authors: Niharika Garg, Urška Knez Štibler, Björn Eismann, Moritz Mercker, Bruno Gideon Bergheim, Anna Linn, Patrizia Tuchscherer, Ulrike Engel, Stefan Redl, Anna Marciniak-Czochra, Thomas W. Holstein, Michael W. Hess, Suat Özbek
Format: Article
Language:English
Published: Elsevier 2023-03-01
Series:iScience
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Online Access:http://www.sciencedirect.com/science/article/pii/S2589004223003681
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author Niharika Garg
Urška Knez Štibler
Björn Eismann
Moritz Mercker
Bruno Gideon Bergheim
Anna Linn
Patrizia Tuchscherer
Ulrike Engel
Stefan Redl
Anna Marciniak-Czochra
Thomas W. Holstein
Michael W. Hess
Suat Özbek
author_facet Niharika Garg
Urška Knez Štibler
Björn Eismann
Moritz Mercker
Bruno Gideon Bergheim
Anna Linn
Patrizia Tuchscherer
Ulrike Engel
Stefan Redl
Anna Marciniak-Czochra
Thomas W. Holstein
Michael W. Hess
Suat Özbek
author_sort Niharika Garg
collection DOAJ
description Summary: Nematocysts are generated by secretion of proteins into a post-Golgi compartment. They consist of a capsule that elongates into a long tube, which is coiled inside the capsule matrix and expelled during its nano-second discharge deployed for prey capture. The driving force for discharge is an extreme osmotic pressure of 150 bar. The complex processes of tube elongation and invagination under these biomechanical constraints have so far been elusive. Here, we show that a non-muscle myosin II homolog (HyNMII) is essential for nematocyst formation in Hydra. In early nematocysts, HyNMII assembles to a collar around the neck of the protruding tube. HyNMII then facilitates tube outgrowth by compressing it along the longitudinal axis as evidenced by inhibitor treatment and genetic knockdown. In addition, live imaging of a NOWA::NOWA-GFP transgenic line, which re-defined NOWA as a tube component facilitating invagination, allowed us to analyze the impact of HyNMII on tube maturation.
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spelling doaj.art-e05575fc96794958a18a8f48ca0106a62023-03-11T04:20:19ZengElsevieriScience2589-00422023-03-01263106291Non-muscle myosin II drives critical steps of nematocyst morphogenesisNiharika Garg0Urška Knez Štibler1Björn Eismann2Moritz Mercker3Bruno Gideon Bergheim4Anna Linn5Patrizia Tuchscherer6Ulrike Engel7Stefan Redl8Anna Marciniak-Czochra9Thomas W. Holstein10Michael W. Hess11Suat Özbek12University of Heidelberg, Centre for Organismal Studies, Department of Molecular Evolution and Genomics, Im Neuenheimer Feld 230, 69120 Heidelberg, GermanyUniversity of Heidelberg, Centre for Organismal Studies, Department of Molecular Evolution and Genomics, Im Neuenheimer Feld 230, 69120 Heidelberg, GermanyUniversity of Heidelberg, Centre for Organismal Studies, Department of Molecular Evolution and Genomics, Im Neuenheimer Feld 230, 69120 Heidelberg, GermanyInstitute for Applied Mathematics, Interdisciplinary Center for Scientific Computing, Heidelberg University, Im Neuenheimer Feld 205, 69120 Heidelberg, GermanyUniversity of Heidelberg, Centre for Organismal Studies, Department of Molecular Evolution and Genomics, Im Neuenheimer Feld 230, 69120 Heidelberg, GermanyUniversity of Heidelberg, Centre for Organismal Studies, Department of Molecular Evolution and Genomics, Im Neuenheimer Feld 230, 69120 Heidelberg, GermanyUniversity of Heidelberg, Centre for Organismal Studies, Department of Molecular Evolution and Genomics, Im Neuenheimer Feld 230, 69120 Heidelberg, GermanyUniversity of Heidelberg, Centre for Organismal Studies, Department of Molecular Evolution and Genomics, Im Neuenheimer Feld 230, 69120 Heidelberg, Germany; Nikon Imaging Center at the University of Heidelberg, Bioquant, Heidelberg University, 69120 Heidelberg, GermanyInstitute of Neuroanatomy, Medical University of Innsbruck, Müllerstrasse 59, 6020 Innsbruck, Austria; Institute of Zoology, University of Innsbruck, Technikerstrasse 25, 6020 Innsbruck, AustriaInstitute for Applied Mathematics, Interdisciplinary Center for Scientific Computing, Heidelberg University, Im Neuenheimer Feld 205, 69120 Heidelberg, GermanyUniversity of Heidelberg, Centre for Organismal Studies, Department of Molecular Evolution and Genomics, Im Neuenheimer Feld 230, 69120 Heidelberg, GermanyInstitute of Histology and Embryology, Medical University of Innsbruck, Müllerstrasse 59, 6020 Innsbruck, AustriaUniversity of Heidelberg, Centre for Organismal Studies, Department of Molecular Evolution and Genomics, Im Neuenheimer Feld 230, 69120 Heidelberg, Germany; Corresponding authorSummary: Nematocysts are generated by secretion of proteins into a post-Golgi compartment. They consist of a capsule that elongates into a long tube, which is coiled inside the capsule matrix and expelled during its nano-second discharge deployed for prey capture. The driving force for discharge is an extreme osmotic pressure of 150 bar. The complex processes of tube elongation and invagination under these biomechanical constraints have so far been elusive. Here, we show that a non-muscle myosin II homolog (HyNMII) is essential for nematocyst formation in Hydra. In early nematocysts, HyNMII assembles to a collar around the neck of the protruding tube. HyNMII then facilitates tube outgrowth by compressing it along the longitudinal axis as evidenced by inhibitor treatment and genetic knockdown. In addition, live imaging of a NOWA::NOWA-GFP transgenic line, which re-defined NOWA as a tube component facilitating invagination, allowed us to analyze the impact of HyNMII on tube maturation.http://www.sciencedirect.com/science/article/pii/S2589004223003681Cell biologyDevelopmental biology
spellingShingle Niharika Garg
Urška Knez Štibler
Björn Eismann
Moritz Mercker
Bruno Gideon Bergheim
Anna Linn
Patrizia Tuchscherer
Ulrike Engel
Stefan Redl
Anna Marciniak-Czochra
Thomas W. Holstein
Michael W. Hess
Suat Özbek
Non-muscle myosin II drives critical steps of nematocyst morphogenesis
iScience
Cell biology
Developmental biology
title Non-muscle myosin II drives critical steps of nematocyst morphogenesis
title_full Non-muscle myosin II drives critical steps of nematocyst morphogenesis
title_fullStr Non-muscle myosin II drives critical steps of nematocyst morphogenesis
title_full_unstemmed Non-muscle myosin II drives critical steps of nematocyst morphogenesis
title_short Non-muscle myosin II drives critical steps of nematocyst morphogenesis
title_sort non muscle myosin ii drives critical steps of nematocyst morphogenesis
topic Cell biology
Developmental biology
url http://www.sciencedirect.com/science/article/pii/S2589004223003681
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