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Development of the indirect flight muscles of Aedes aegypti, a main arbovirus vector

BACKGROUND: Flying is an essential function for mosquitoes, required for mating and, in the case of females, to get a blood meal and consequently function as a vector. Flight depends on the action of the indirect flight muscles (IFMs), which power the wings beat. No description of the development of...

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Autores principales: Celestino-Montes, Antonio, Hernández-Martínez, Salvador, Rodríguez, Mario Henry, Cázares-Raga, Febe Elena, Vázquez-Calzada, Carlos, Lagunes-Guillén, Anel, Chávez-Munguía, Bibiana, Rubio-Miranda, José Ángel, Hernández-Cázares, Felipe de Jesús, Cortés-Martínez, Leticia, Hernández-Hernández, Fidel de la Cruz
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8394598/
https://www.ncbi.nlm.nih.gov/pubmed/34445959
http://dx.doi.org/10.1186/s12861-021-00242-8
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author Celestino-Montes, Antonio
Hernández-Martínez, Salvador
Rodríguez, Mario Henry
Cázares-Raga, Febe Elena
Vázquez-Calzada, Carlos
Lagunes-Guillén, Anel
Chávez-Munguía, Bibiana
Rubio-Miranda, José Ángel
Hernández-Cázares, Felipe de Jesús
Cortés-Martínez, Leticia
Hernández-Hernández, Fidel de la Cruz
author_facet Celestino-Montes, Antonio
Hernández-Martínez, Salvador
Rodríguez, Mario Henry
Cázares-Raga, Febe Elena
Vázquez-Calzada, Carlos
Lagunes-Guillén, Anel
Chávez-Munguía, Bibiana
Rubio-Miranda, José Ángel
Hernández-Cázares, Felipe de Jesús
Cortés-Martínez, Leticia
Hernández-Hernández, Fidel de la Cruz
author_sort Celestino-Montes, Antonio
collection PubMed
description BACKGROUND: Flying is an essential function for mosquitoes, required for mating and, in the case of females, to get a blood meal and consequently function as a vector. Flight depends on the action of the indirect flight muscles (IFMs), which power the wings beat. No description of the development of IFMs in mosquitoes, including Aedes aegypti, is available. METHODS: A. aegypti thoraces of larvae 3 and larvae 4 (L3 and L4) instars were analyzed using histochemistry and bright field microscopy. IFM primordia from L3 and L4 and IFMs from pupal and adult stages were dissected and processed to detect F-actin labelling with phalloidin-rhodamine or TRITC, or to immunodetection of myosin and tubulin using specific antibodies, these samples were analyzed by confocal microscopy. Other samples were studied using transmission electron microscopy. RESULTS: At L3–L4, IFM primordia for dorsal-longitudinal muscles (DLM) and dorsal–ventral muscles (DVM) were identified in the expected locations in the thoracic region: three primordia per hemithorax corresponding to DLM with anterior to posterior orientation were present. Other three primordia per hemithorax, corresponding to DVM, had lateral position and dorsal to ventral orientation. During L3 to L4 myoblast fusion led to syncytial myotubes formation, followed by myotendon junctions (MTJ) creation, myofibrils assembly and sarcomere maturation. The formation of Z-discs and M-line during sarcomere maturation was observed in pupal stage and, the structure reached in teneral insects a classical myosin thick, and actin thin filaments arranged in a hexagonal lattice structure. CONCLUSIONS: A general description of A. aegypti IFM development is presented, from the myoblast fusion at L3 to form myotubes, to sarcomere maturation at adult stage. Several differences during IFM development were observed between A. aegypti (Nematoceran) and Drosophila melanogaster (Brachyceran) and, similitudes with Chironomus sp. were observed as this insect is a Nematoceran, which is taxonomically closer to A. aegypti and share the same number of larval stages. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12861-021-00242-8.
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spelling pubmed-83945982021-08-30 Development of the indirect flight muscles of Aedes aegypti, a main arbovirus vector Celestino-Montes, Antonio Hernández-Martínez, Salvador Rodríguez, Mario Henry Cázares-Raga, Febe Elena Vázquez-Calzada, Carlos Lagunes-Guillén, Anel Chávez-Munguía, Bibiana Rubio-Miranda, José Ángel Hernández-Cázares, Felipe de Jesús Cortés-Martínez, Leticia Hernández-Hernández, Fidel de la Cruz BMC Dev Biol Research Article BACKGROUND: Flying is an essential function for mosquitoes, required for mating and, in the case of females, to get a blood meal and consequently function as a vector. Flight depends on the action of the indirect flight muscles (IFMs), which power the wings beat. No description of the development of IFMs in mosquitoes, including Aedes aegypti, is available. METHODS: A. aegypti thoraces of larvae 3 and larvae 4 (L3 and L4) instars were analyzed using histochemistry and bright field microscopy. IFM primordia from L3 and L4 and IFMs from pupal and adult stages were dissected and processed to detect F-actin labelling with phalloidin-rhodamine or TRITC, or to immunodetection of myosin and tubulin using specific antibodies, these samples were analyzed by confocal microscopy. Other samples were studied using transmission electron microscopy. RESULTS: At L3–L4, IFM primordia for dorsal-longitudinal muscles (DLM) and dorsal–ventral muscles (DVM) were identified in the expected locations in the thoracic region: three primordia per hemithorax corresponding to DLM with anterior to posterior orientation were present. Other three primordia per hemithorax, corresponding to DVM, had lateral position and dorsal to ventral orientation. During L3 to L4 myoblast fusion led to syncytial myotubes formation, followed by myotendon junctions (MTJ) creation, myofibrils assembly and sarcomere maturation. The formation of Z-discs and M-line during sarcomere maturation was observed in pupal stage and, the structure reached in teneral insects a classical myosin thick, and actin thin filaments arranged in a hexagonal lattice structure. CONCLUSIONS: A general description of A. aegypti IFM development is presented, from the myoblast fusion at L3 to form myotubes, to sarcomere maturation at adult stage. Several differences during IFM development were observed between A. aegypti (Nematoceran) and Drosophila melanogaster (Brachyceran) and, similitudes with Chironomus sp. were observed as this insect is a Nematoceran, which is taxonomically closer to A. aegypti and share the same number of larval stages. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12861-021-00242-8. BioMed Central 2021-08-26 /pmc/articles/PMC8394598/ /pubmed/34445959 http://dx.doi.org/10.1186/s12861-021-00242-8 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Celestino-Montes, Antonio
Hernández-Martínez, Salvador
Rodríguez, Mario Henry
Cázares-Raga, Febe Elena
Vázquez-Calzada, Carlos
Lagunes-Guillén, Anel
Chávez-Munguía, Bibiana
Rubio-Miranda, José Ángel
Hernández-Cázares, Felipe de Jesús
Cortés-Martínez, Leticia
Hernández-Hernández, Fidel de la Cruz
Development of the indirect flight muscles of Aedes aegypti, a main arbovirus vector
title Development of the indirect flight muscles of Aedes aegypti, a main arbovirus vector
title_full Development of the indirect flight muscles of Aedes aegypti, a main arbovirus vector
title_fullStr Development of the indirect flight muscles of Aedes aegypti, a main arbovirus vector
title_full_unstemmed Development of the indirect flight muscles of Aedes aegypti, a main arbovirus vector
title_short Development of the indirect flight muscles of Aedes aegypti, a main arbovirus vector
title_sort development of the indirect flight muscles of aedes aegypti, a main arbovirus vector
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8394598/
https://www.ncbi.nlm.nih.gov/pubmed/34445959
http://dx.doi.org/10.1186/s12861-021-00242-8
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