Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells

Autores
De Rossi, María Cecilia; Wetzler, Diana E.; Benseñor, Lorena; De Rossi, María Emilia; Sued, Raquel Mariela; Rodríguez, Daniela; Gelfand, Vladimir; Bruno, Luciana; Levi, Valeria
Año de publicación
2017
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Background: Intracellular transport requires molecular motors that step along
cytoskeletal filaments actively dragging cargoes through the crowded cytoplasm. Here,
we explore the interplay of the opposed polarity motors kinesin-1 and cytoplasmic
dynein during peroxisome transport along microtubules in Drosophila S2 cells.
Methods: We used single particle tracking with nanometer accuracy and millisecond
time resolution to extract quantitative information on the bidirectional motion of
organelles. The transport performance was studied in cells expressing a slow chimeric
plus-end directed motor or the kinesin heavy chain. We also analyzed the influence of
peroxisomes membrane fluidity in methyl--ciclodextrin treated cells. The experimental
data was also confronted with numerical simulations of two well-established tug of war
scenarios.
SC
Results and conclusions: The velocity distributions of retrograde and anterograde
peroxisomes showed a multimodal pattern suggesting that multiple motor teams drive
transport in either direction. The chimeric motors interfered with the performance of
anterograde transport and also reduced the speed of the slowest retrograde team. In
addition, increasing the fluidity of peroxisomes membrane decreased the speed of the
slowest anterograde and retrograde teams.
General Significance: Our results support the existence of a crosstalk between
opposed-polarity motor teams. Moreover, the slowest teams seem to mechanically
communicate with each other through the membrane to trigger transport.
Fil: De Rossi, María Cecilia. Universidad de Buenos Aires; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Wetzler, Diana E.. Universidad de Buenos Aires; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Benseñor, Lorena. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: De Rossi, María Emilia. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires; Argentina
Fil: Sued, Raquel Mariela. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Cálculo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Rodríguez, Daniela. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Cálculo; Argentina
Fil: Gelfand, Vladimir. Northwestern University; Estados Unidos
Fil: Bruno, Luciana. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires; Argentina
Fil: Levi, Valeria. Universidad de Buenos Aires; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Materia
Single Particle Tracking
Molecular Motors
Intracellular Transport
Drosophila S2 Cells
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/47901
Acceder
id CONICETDig_5305e32743cf88866f3f97a01282c47a
oai_identifier_str oai:ri.conicet.gov.ar:11336/47901
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cellsDe Rossi, María CeciliaWetzler, Diana E.Benseñor, LorenaDe Rossi, María EmiliaSued, Raquel MarielaRodríguez, DanielaGelfand, VladimirBruno, LucianaLevi, ValeriaSingle Particle TrackingMolecular MotorsIntracellular TransportDrosophila S2 Cellshttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Background: Intracellular transport requires molecular motors that step along<br />cytoskeletal filaments actively dragging cargoes through the crowded cytoplasm. Here,<br />we explore the interplay of the opposed polarity motors kinesin-1 and cytoplasmic<br />dynein during peroxisome transport along microtubules in Drosophila S2 cells.<br />Methods: We used single particle tracking with nanometer accuracy and millisecond<br />time resolution to extract quantitative information on the bidirectional motion of<br />organelles. The transport performance was studied in cells expressing a slow chimeric<br />plus-end directed motor or the kinesin heavy chain. We also analyzed the influence of<br />peroxisomes membrane fluidity in methyl--ciclodextrin treated cells. The experimental<br />data was also confronted with numerical simulations of two well-established tug of war<br />scenarios.<br />SC<br />Results and conclusions: The velocity distributions of retrograde and anterograde<br />peroxisomes showed a multimodal pattern suggesting that multiple motor teams drive<br />transport in either direction. The chimeric motors interfered with the performance of<br />anterograde transport and also reduced the speed of the slowest retrograde team. In<br />addition, increasing the fluidity of peroxisomes membrane decreased the speed of the<br />slowest anterograde and retrograde teams.<br />General Significance: Our results support the existence of a crosstalk between<br />opposed-polarity motor teams. Moreover, the slowest teams seem to mechanically<br />communicate with each other through the membrane to trigger transport.Fil: De Rossi, María Cecilia. Universidad de Buenos Aires; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Wetzler, Diana E.. Universidad de Buenos Aires; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Benseñor, Lorena. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: De Rossi, María Emilia. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires; ArgentinaFil: Sued, Raquel Mariela. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Cálculo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Rodríguez, Daniela. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Cálculo; ArgentinaFil: Gelfand, Vladimir. Northwestern University; Estados UnidosFil: Bruno, Luciana. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires; ArgentinaFil: Levi, Valeria. Universidad de Buenos Aires; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaElsevier Science2017-09info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/47901De Rossi, María Cecilia; Wetzler, Diana E.; Benseñor, Lorena; De Rossi, María Emilia; Sued, Raquel Mariela; et al.; Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells; Elsevier Science; Biochimica et Biophysica Acta- General Subjects; 9-20170304-4165CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/http://linkinghub.elsevier.com/retrieve/pii/S0304416517302933info:eu-repo/semantics/altIdentifier/doi/10.1016/j.bbagen.2017.09.009info:eu-repo/semantics/altIdentifier/url/https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5796658/info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:46:31Zoai:ri.conicet.gov.ar:11336/47901instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 09:46:31.943CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells
title Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells
spellingShingle Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells
De Rossi, María Cecilia
Single Particle Tracking
Molecular Motors
Intracellular Transport
Drosophila S2 Cells
title_short Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells
title_full Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells
title_fullStr Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells
title_full_unstemmed Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells
title_sort Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells
dc.creator.none.fl_str_mv De Rossi, María Cecilia
Wetzler, Diana E.
Benseñor, Lorena
De Rossi, María Emilia
Sued, Raquel Mariela
Rodríguez, Daniela
Gelfand, Vladimir
Bruno, Luciana
Levi, Valeria
author De Rossi, María Cecilia
author_facet De Rossi, María Cecilia
Wetzler, Diana E.
Benseñor, Lorena
De Rossi, María Emilia
Sued, Raquel Mariela
Rodríguez, Daniela
Gelfand, Vladimir
Bruno, Luciana
Levi, Valeria
author_role author
author2 Wetzler, Diana E.
Benseñor, Lorena
De Rossi, María Emilia
Sued, Raquel Mariela
Rodríguez, Daniela
Gelfand, Vladimir
Bruno, Luciana
Levi, Valeria
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Single Particle Tracking
Molecular Motors
Intracellular Transport
Drosophila S2 Cells
topic Single Particle Tracking
Molecular Motors
Intracellular Transport
Drosophila S2 Cells
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Background: Intracellular transport requires molecular motors that step along<br />cytoskeletal filaments actively dragging cargoes through the crowded cytoplasm. Here,<br />we explore the interplay of the opposed polarity motors kinesin-1 and cytoplasmic<br />dynein during peroxisome transport along microtubules in Drosophila S2 cells.<br />Methods: We used single particle tracking with nanometer accuracy and millisecond<br />time resolution to extract quantitative information on the bidirectional motion of<br />organelles. The transport performance was studied in cells expressing a slow chimeric<br />plus-end directed motor or the kinesin heavy chain. We also analyzed the influence of<br />peroxisomes membrane fluidity in methyl--ciclodextrin treated cells. The experimental<br />data was also confronted with numerical simulations of two well-established tug of war<br />scenarios.<br />SC<br />Results and conclusions: The velocity distributions of retrograde and anterograde<br />peroxisomes showed a multimodal pattern suggesting that multiple motor teams drive<br />transport in either direction. The chimeric motors interfered with the performance of<br />anterograde transport and also reduced the speed of the slowest retrograde team. In<br />addition, increasing the fluidity of peroxisomes membrane decreased the speed of the<br />slowest anterograde and retrograde teams.<br />General Significance: Our results support the existence of a crosstalk between<br />opposed-polarity motor teams. Moreover, the slowest teams seem to mechanically<br />communicate with each other through the membrane to trigger transport.
Fil: De Rossi, María Cecilia. Universidad de Buenos Aires; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Wetzler, Diana E.. Universidad de Buenos Aires; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Benseñor, Lorena. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: De Rossi, María Emilia. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires; Argentina
Fil: Sued, Raquel Mariela. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Cálculo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Rodríguez, Daniela. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Cálculo; Argentina
Fil: Gelfand, Vladimir. Northwestern University; Estados Unidos
Fil: Bruno, Luciana. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires; Argentina
Fil: Levi, Valeria. Universidad de Buenos Aires; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
description Background: Intracellular transport requires molecular motors that step along<br />cytoskeletal filaments actively dragging cargoes through the crowded cytoplasm. Here,<br />we explore the interplay of the opposed polarity motors kinesin-1 and cytoplasmic<br />dynein during peroxisome transport along microtubules in Drosophila S2 cells.<br />Methods: We used single particle tracking with nanometer accuracy and millisecond<br />time resolution to extract quantitative information on the bidirectional motion of<br />organelles. The transport performance was studied in cells expressing a slow chimeric<br />plus-end directed motor or the kinesin heavy chain. We also analyzed the influence of<br />peroxisomes membrane fluidity in methyl--ciclodextrin treated cells. The experimental<br />data was also confronted with numerical simulations of two well-established tug of war<br />scenarios.<br />SC<br />Results and conclusions: The velocity distributions of retrograde and anterograde<br />peroxisomes showed a multimodal pattern suggesting that multiple motor teams drive<br />transport in either direction. The chimeric motors interfered with the performance of<br />anterograde transport and also reduced the speed of the slowest retrograde team. In<br />addition, increasing the fluidity of peroxisomes membrane decreased the speed of the<br />slowest anterograde and retrograde teams.<br />General Significance: Our results support the existence of a crosstalk between<br />opposed-polarity motor teams. Moreover, the slowest teams seem to mechanically<br />communicate with each other through the membrane to trigger transport.
publishDate 2017
dc.date.none.fl_str_mv 2017-09
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/47901
De Rossi, María Cecilia; Wetzler, Diana E.; Benseñor, Lorena; De Rossi, María Emilia; Sued, Raquel Mariela; et al.; Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells; Elsevier Science; Biochimica et Biophysica Acta- General Subjects; 9-2017
0304-4165
CONICET Digital
CONICET
url http://hdl.handle.net/11336/47901
identifier_str_mv De Rossi, María Cecilia; Wetzler, Diana E.; Benseñor, Lorena; De Rossi, María Emilia; Sued, Raquel Mariela; et al.; Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells; Elsevier Science; Biochimica et Biophysica Acta- General Subjects; 9-2017
0304-4165
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/http://linkinghub.elsevier.com/retrieve/pii/S0304416517302933
info:eu-repo/semantics/altIdentifier/doi/10.1016/j.bbagen.2017.09.009
info:eu-repo/semantics/altIdentifier/url/https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5796658/
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv Elsevier Science
publisher.none.fl_str_mv Elsevier Science
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.070432

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