Stem cell proliferation and differentiation during larval metamorphosis of the model tapeworm Hymenolepis microstoma
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.
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) |
_version_ | 1807522808146690048 |
---|---|
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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collection | COLIBRI |
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. |
dc.format.mimetype.es.fl_str_mv | application/pdf |
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 |
format | article |
id | COLIBRI_8602cd86cd381bdbed9238890a642f4b |
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. 2235-2988 10.3389/fcimb.2023.1286190 |
instacron_str | Universidad de la República |
institution | Universidad de la República |
instname_str | Universidad de la República |
language | eng |
language_invalid_str_mv | en |
network_acronym_str | COLIBRI |
network_name_str | COLIBRI |
oai_identifier_str | oai:colibri.udelar.edu.uy:20.500.12008/43218 |
publishDate | 2023 |
reponame_str | COLIBRI |
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 |