Stem cell proliferation and differentiation during larval metamorphosis of the model tapeworm Hymenolepis microstoma

Montagne, Jimena - Preza Pérez, Matías Facundo - Koziol, Uriel

Resumen:

Background: Tapeworm larvae cause important diseases in humans and domestic animals. During infection, the first larval stage undergoes a metamorphosis where tissues are formed de novo from a population of stem cells called germinative cells. This process is difficult to study for human pathogens, as these larvae are infectious and difficult to obtain in the laboratory. Methods: In this work, we analyzed cell proliferation and differentiation during larval metamorphosis in the model tapeworm Hymenolepis microstoma, by in vivo labelling of proliferating cells with the thymidine analogue 5 ethynyl-2′- deoxyuridine (EdU), tracing their differentiation with a suite of specific molecular markers for different cell types. Results: Proliferating cells are very abundant and fast-cycling during early metamorphosis: the total number of cells duplicates every ten hours, and the length of G2 is only 75 minutes. New tegumental, muscle and nerve cells differentiate from this pool of proliferating germinative cells, and these processes are very fast, as differentiation markers for neurons and muscle cells appear within 24 hours after exiting the cell cycle, and fusion of new cells to the tegumental syncytium can be detected after only 4 hours. Tegumental and muscle cells appear from early stages of metamorphosis (24 to 48 hours postinfection); in contrast, most markers for differentiating neurons appear later, and the detection of synapsin and neuropeptides correlates with scolex retraction. Finally, we identified populations of proliferating cells that express conserved genes associated with neuronal progenitors and precursors, suggesting the existence of tissue-specific lineages among germinative cells. Discussion: These results provide for the first time a comprehensive view of the development of new tissues during tapeworm larval metamorphosis, providing a framework for similar studies in human and veterinary pathogens.


Detalles Bibliográficos
2023
CSIC: I+D_2018_162
Differentiation
Stem cell
Neoblast
Cestode
Oncosphere
Metacestode
Tegument
NeuroD
Inglés
Universidad de la República
COLIBRI
https://hdl.handle.net/20.500.12008/43218
Acceso abierto
Licencia Creative Commons Atribución (CC - By 4.0)
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author Montagne, Jimena
author2 Preza Pérez, Matías Facundo
Koziol, Uriel
author2_role author
author
author_facet Montagne, Jimena
Preza Pérez, Matías Facundo
Koziol, Uriel
author_role author
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dc.contributor.filiacion.none.fl_str_mv Montagne Jimena, Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología.
Preza Pérez Matías Facundo, Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología.
Koziol Uriel, Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología.
dc.creator.none.fl_str_mv Montagne, Jimena
Preza Pérez, Matías Facundo
Koziol, Uriel
dc.date.accessioned.none.fl_str_mv 2024-03-20T13:50:09Z
dc.date.available.none.fl_str_mv 2024-03-20T13:50:09Z
dc.date.issued.none.fl_str_mv 2023
dc.description.abstract.none.fl_txt_mv Background: Tapeworm larvae cause important diseases in humans and domestic animals. During infection, the first larval stage undergoes a metamorphosis where tissues are formed de novo from a population of stem cells called germinative cells. This process is difficult to study for human pathogens, as these larvae are infectious and difficult to obtain in the laboratory. Methods: In this work, we analyzed cell proliferation and differentiation during larval metamorphosis in the model tapeworm Hymenolepis microstoma, by in vivo labelling of proliferating cells with the thymidine analogue 5 ethynyl-2′- deoxyuridine (EdU), tracing their differentiation with a suite of specific molecular markers for different cell types. Results: Proliferating cells are very abundant and fast-cycling during early metamorphosis: the total number of cells duplicates every ten hours, and the length of G2 is only 75 minutes. New tegumental, muscle and nerve cells differentiate from this pool of proliferating germinative cells, and these processes are very fast, as differentiation markers for neurons and muscle cells appear within 24 hours after exiting the cell cycle, and fusion of new cells to the tegumental syncytium can be detected after only 4 hours. Tegumental and muscle cells appear from early stages of metamorphosis (24 to 48 hours postinfection); in contrast, most markers for differentiating neurons appear later, and the detection of synapsin and neuropeptides correlates with scolex retraction. Finally, we identified populations of proliferating cells that express conserved genes associated with neuronal progenitors and precursors, suggesting the existence of tissue-specific lineages among germinative cells. Discussion: These results provide for the first time a comprehensive view of the development of new tissues during tapeworm larval metamorphosis, providing a framework for similar studies in human and veterinary pathogens.
dc.description.sponsorship.none.fl_txt_mv CSIC: I+D_2018_162
dc.format.extent.es.fl_str_mv 16 h.
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dc.identifier.citation.es.fl_str_mv Montagne, J, Preza Pérez, M y Koziol, U. "Stem cell proliferation and differentiation during larval metamorphosis of the model tapeworm Hymenolepis microstoma". Frontiers in Cellular and Infection Microbiology. [en línea] 2023, 13: 1286190. 16 h. DOI: 10.3389/fcimb.2023.1286190.
dc.identifier.doi.none.fl_str_mv 10.3389/fcimb.2023.1286190
dc.identifier.issn.none.fl_str_mv 2235-2988
dc.identifier.uri.none.fl_str_mv https://hdl.handle.net/20.500.12008/43218
dc.language.iso.none.fl_str_mv en
eng
dc.publisher.es.fl_str_mv Frontiers
dc.relation.ispartof.es.fl_str_mv Frontiers in Cellular and Infection Microbiology, 2023, 13: 1286190.
dc.rights.license.none.fl_str_mv Licencia Creative Commons Atribución (CC - By 4.0)
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
dc.source.none.fl_str_mv reponame:COLIBRI
instname:Universidad de la República
instacron:Universidad de la República
dc.subject.es.fl_str_mv Differentiation
Stem cell
Neoblast
Cestode
Oncosphere
Metacestode
Tegument
NeuroD
dc.title.none.fl_str_mv Stem cell proliferation and differentiation during larval metamorphosis of the model tapeworm Hymenolepis microstoma
dc.type.es.fl_str_mv Artículo
dc.type.none.fl_str_mv info:eu-repo/semantics/article
dc.type.version.none.fl_str_mv info:eu-repo/semantics/publishedVersion
description Background: Tapeworm larvae cause important diseases in humans and domestic animals. During infection, the first larval stage undergoes a metamorphosis where tissues are formed de novo from a population of stem cells called germinative cells. This process is difficult to study for human pathogens, as these larvae are infectious and difficult to obtain in the laboratory. Methods: In this work, we analyzed cell proliferation and differentiation during larval metamorphosis in the model tapeworm Hymenolepis microstoma, by in vivo labelling of proliferating cells with the thymidine analogue 5 ethynyl-2′- deoxyuridine (EdU), tracing their differentiation with a suite of specific molecular markers for different cell types. Results: Proliferating cells are very abundant and fast-cycling during early metamorphosis: the total number of cells duplicates every ten hours, and the length of G2 is only 75 minutes. New tegumental, muscle and nerve cells differentiate from this pool of proliferating germinative cells, and these processes are very fast, as differentiation markers for neurons and muscle cells appear within 24 hours after exiting the cell cycle, and fusion of new cells to the tegumental syncytium can be detected after only 4 hours. Tegumental and muscle cells appear from early stages of metamorphosis (24 to 48 hours postinfection); in contrast, most markers for differentiating neurons appear later, and the detection of synapsin and neuropeptides correlates with scolex retraction. Finally, we identified populations of proliferating cells that express conserved genes associated with neuronal progenitors and precursors, suggesting the existence of tissue-specific lineages among germinative cells. Discussion: These results provide for the first time a comprehensive view of the development of new tissues during tapeworm larval metamorphosis, providing a framework for similar studies in human and veterinary pathogens.
eu_rights_str_mv openAccess
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identifier_str_mv Montagne, J, Preza Pérez, M y Koziol, U. "Stem cell proliferation and differentiation during larval metamorphosis of the model tapeworm Hymenolepis microstoma". Frontiers in Cellular and Infection Microbiology. [en línea] 2023, 13: 1286190. 16 h. DOI: 10.3389/fcimb.2023.1286190.
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10.3389/fcimb.2023.1286190
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repository.mail.fl_str_mv mabel.seroubian@seciu.edu.uy
repository.name.fl_str_mv COLIBRI - Universidad de la República
repository_id_str 4771
rights_invalid_str_mv Licencia Creative Commons Atribución (CC - By 4.0)
spelling Montagne Jimena, Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología.Preza Pérez Matías Facundo, Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología.Koziol Uriel, Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología.2024-03-20T13:50:09Z2024-03-20T13:50:09Z2023Montagne, J, Preza Pérez, M y Koziol, U. "Stem cell proliferation and differentiation during larval metamorphosis of the model tapeworm Hymenolepis microstoma". Frontiers in Cellular and Infection Microbiology. [en línea] 2023, 13: 1286190. 16 h. DOI: 10.3389/fcimb.2023.1286190.2235-2988https://hdl.handle.net/20.500.12008/4321810.3389/fcimb.2023.1286190Background: Tapeworm larvae cause important diseases in humans and domestic animals. During infection, the first larval stage undergoes a metamorphosis where tissues are formed de novo from a population of stem cells called germinative cells. This process is difficult to study for human pathogens, as these larvae are infectious and difficult to obtain in the laboratory. Methods: In this work, we analyzed cell proliferation and differentiation during larval metamorphosis in the model tapeworm Hymenolepis microstoma, by in vivo labelling of proliferating cells with the thymidine analogue 5 ethynyl-2′- deoxyuridine (EdU), tracing their differentiation with a suite of specific molecular markers for different cell types. Results: Proliferating cells are very abundant and fast-cycling during early metamorphosis: the total number of cells duplicates every ten hours, and the length of G2 is only 75 minutes. New tegumental, muscle and nerve cells differentiate from this pool of proliferating germinative cells, and these processes are very fast, as differentiation markers for neurons and muscle cells appear within 24 hours after exiting the cell cycle, and fusion of new cells to the tegumental syncytium can be detected after only 4 hours. Tegumental and muscle cells appear from early stages of metamorphosis (24 to 48 hours postinfection); in contrast, most markers for differentiating neurons appear later, and the detection of synapsin and neuropeptides correlates with scolex retraction. Finally, we identified populations of proliferating cells that express conserved genes associated with neuronal progenitors and precursors, suggesting the existence of tissue-specific lineages among germinative cells. Discussion: These results provide for the first time a comprehensive view of the development of new tissues during tapeworm larval metamorphosis, providing a framework for similar studies in human and veterinary pathogens.Submitted by Pintos Natalia (nataliapintosmvd@gmail.com) on 2024-03-19T18:24:44Z No. of bitstreams: 2 license_rdf: 24251 bytes, checksum: 71ed42ef0a0b648670f707320be37b90 (MD5) 10.3389.fcimb.2023.1286190.pdf: 18744139 bytes, checksum: 811063ab89bb037ad9f1eb7583b6f5b9 (MD5)Approved for entry into archive by Faget Cecilia (lfaget@fcien.edu.uy) on 2024-03-20T11:55:15Z (GMT) No. of bitstreams: 2 license_rdf: 24251 bytes, checksum: 71ed42ef0a0b648670f707320be37b90 (MD5) 10.3389.fcimb.2023.1286190.pdf: 18744139 bytes, checksum: 811063ab89bb037ad9f1eb7583b6f5b9 (MD5)Made available in DSpace by Luna Fabiana (fabiana.luna@seciu.edu.uy) on 2024-03-20T13:50:09Z (GMT). No. of bitstreams: 2 license_rdf: 24251 bytes, checksum: 71ed42ef0a0b648670f707320be37b90 (MD5) 10.3389.fcimb.2023.1286190.pdf: 18744139 bytes, checksum: 811063ab89bb037ad9f1eb7583b6f5b9 (MD5) Previous issue date: 2023CSIC: I+D_2018_16216 h.application/pdfenengFrontiersFrontiers in Cellular and Infection Microbiology, 2023, 13: 1286190.Las obras depositadas en el Repositorio se rigen por la Ordenanza de los Derechos de la Propiedad Intelectual de la Universidad de la República.(Res. Nº 91 de C.D.C. de 8/III/1994 – D.O. 7/IV/1994) y por la Ordenanza del Repositorio Abierto de la Universidad de la República (Res. Nº 16 de C.D.C. de 07/10/2014)info:eu-repo/semantics/openAccessLicencia Creative Commons Atribución (CC - By 4.0)DifferentiationStem cellNeoblastCestodeOncosphereMetacestodeTegumentNeuroDStem cell proliferation and differentiation during larval metamorphosis of the model tapeworm Hymenolepis microstomaArtículoinfo:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionreponame:COLIBRIinstname:Universidad de la Repúblicainstacron:Universidad de la RepúblicaMontagne, JimenaPreza Pérez, Matías FacundoKoziol, UrielLICENSElicense.txtlicense.txttext/plain; charset=utf-84267http://localhost:8080/xmlui/bitstream/20.500.12008/43218/5/license.txt6429389a7df7277b72b7924fdc7d47a9MD55CC-LICENSElicense_urllicense_urltext/plain; charset=utf-844http://localhost:8080/xmlui/bitstream/20.500.12008/43218/2/license_urla0ebbeafb9d2ec7cbb19d7137ebc392cMD52license_textlicense_texttext/html; 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- Universidad de la Repúblicafalse
spellingShingle Stem cell proliferation and differentiation during larval metamorphosis of the model tapeworm Hymenolepis microstoma
Montagne, Jimena
Differentiation
Stem cell
Neoblast
Cestode
Oncosphere
Metacestode
Tegument
NeuroD
status_str publishedVersion
title Stem cell proliferation and differentiation during larval metamorphosis of the model tapeworm Hymenolepis microstoma
title_full Stem cell proliferation and differentiation during larval metamorphosis of the model tapeworm Hymenolepis microstoma
title_fullStr Stem cell proliferation and differentiation during larval metamorphosis of the model tapeworm Hymenolepis microstoma
title_full_unstemmed Stem cell proliferation and differentiation during larval metamorphosis of the model tapeworm Hymenolepis microstoma
title_short Stem cell proliferation and differentiation during larval metamorphosis of the model tapeworm Hymenolepis microstoma
title_sort Stem cell proliferation and differentiation during larval metamorphosis of the model tapeworm Hymenolepis microstoma
topic Differentiation
Stem cell
Neoblast
Cestode
Oncosphere
Metacestode
Tegument
NeuroD
url https://hdl.handle.net/20.500.12008/43218