piRNA pathway evolution beyond gonad context: Perspectives from apicomplexa and trypanosomatids

Horjales, S. - Li Calzi, M. - Francia, M. E. - Cayota, A. - Garcia-Silva, M. R.

Resumen:

piRNAs function as genome defense mechanisms against transposable elements insertions within germ line cells. Recent studies have unraveled that piRNA pathways are not limited to germ cells as initially reckoned, but are instead also found in non-gonadal somatic contexts. Moreover, these pathways have also been reported in bacteria, mollusks and arthropods, associated with safeguard of genomes against transposable elements, regulation of gene expression and with direct consequences in axon regeneration and memory formation. In this Perspective we draw attention to early branching parasitic protozoa, whose genome preservation is an essential function as in late eukaryotes. However, little is known about the defense mechanisms of these genomes. We and others have described the presence of putative PIWI-related machinery members in protozoan parasites. We have described the presence of a PIWI-like protein in Trypanosoma cruzi, bound to small non-coding RNAs (sRNAs) as cargo of secreted extracellular vesicles relevant in intercellular communication and host infection. Herein, we put forward the presence of members related to Argonaute pathways in both Trypanosoma cruzi and Toxoplasma gondii. The presence of PIWI-like machinery in Trypansomatids and Apicomplexa, respectively, could be evidence of an ancestral piRNA machinery that evolved to become more sophisticated and complex in multicellular eukaryotes. We propose a model in which ancient PIWI proteins were expressed broadly and had functions independent of germline maintenance. A better understanding of current and ancestral PIWI/piRNAs will be relevant to better understand key mechanisms of genome integrity conservation during cell cycle progression and modulation of host defense mechanisms by protozoan parasites.


Detalles Bibliográficos
2023
Argonautes (AGO)
PIWI
Toxoplasma
Trypanosoma
piRNA biogenesis
Ciencias Naturales y Exactas
Ciencias Biológicas
Bioquímica y Biología Molecular
Inglés
Institut Pasteur de Montevideo
IPMON en REDI
https://hdl.handle.net/20.500.12381/3253
https://doi.org/10.3389/fgene.2023.1129194
Acceso abierto
Reconocimiento 4.0 Internacional. (CC BY)
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author Horjales, S.
author2 Li Calzi, M.
Francia, M. E.
Cayota, A.
Garcia-Silva, M. R.
author2_role author
author
author
author
author_facet Horjales, S.
Li Calzi, M.
Francia, M. E.
Cayota, A.
Garcia-Silva, M. R.
author_role author
bitstream.checksum.fl_str_mv 2d6047b2c47a34748db9b1d0017b96da
95f0556c96d2bb964e5915aedcfbf564
bitstream.checksumAlgorithm.fl_str_mv MD5
MD5
bitstream.url.fl_str_mv https://redi.anii.org.uy/jspui/bitstream/20.500.12381/3253/2/license.txt
https://redi.anii.org.uy/jspui/bitstream/20.500.12381/3253/1/fgene-14-1129194.pdf
collection IPMON en REDI
dc.creator.none.fl_str_mv Horjales, S.
Li Calzi, M.
Francia, M. E.
Cayota, A.
Garcia-Silva, M. R.
dc.date.accessioned.none.fl_str_mv 2023-06-18T14:17:16Z
dc.date.available.none.fl_str_mv 2023-06-18T14:17:16Z
dc.date.issued.none.fl_str_mv 2023-02-03
dc.description.abstract.none.fl_txt_mv piRNAs function as genome defense mechanisms against transposable elements insertions within germ line cells. Recent studies have unraveled that piRNA pathways are not limited to germ cells as initially reckoned, but are instead also found in non-gonadal somatic contexts. Moreover, these pathways have also been reported in bacteria, mollusks and arthropods, associated with safeguard of genomes against transposable elements, regulation of gene expression and with direct consequences in axon regeneration and memory formation. In this Perspective we draw attention to early branching parasitic protozoa, whose genome preservation is an essential function as in late eukaryotes. However, little is known about the defense mechanisms of these genomes. We and others have described the presence of putative PIWI-related machinery members in protozoan parasites. We have described the presence of a PIWI-like protein in Trypanosoma cruzi, bound to small non-coding RNAs (sRNAs) as cargo of secreted extracellular vesicles relevant in intercellular communication and host infection. Herein, we put forward the presence of members related to Argonaute pathways in both Trypanosoma cruzi and Toxoplasma gondii. The presence of PIWI-like machinery in Trypansomatids and Apicomplexa, respectively, could be evidence of an ancestral piRNA machinery that evolved to become more sophisticated and complex in multicellular eukaryotes. We propose a model in which ancient PIWI proteins were expressed broadly and had functions independent of germline maintenance. A better understanding of current and ancestral PIWI/piRNAs will be relevant to better understand key mechanisms of genome integrity conservation during cell cycle progression and modulation of host defense mechanisms by protozoan parasites.
dc.identifier.citation.es.fl_str_mv Horjales S, Li Calzi M, Francia ME, Cayota A and Garcia-Silva MR (2023), piRNA pathway evolution beyond gonad context: Perspectives from apicomplexa and trypanosomatids. Front. Genet. 14:1129194. doi: 10.3389/fgene.2023.1129194
dc.identifier.doi.none.fl_str_mv https://doi.org/10.3389/fgene.2023.1129194
dc.identifier.uri.none.fl_str_mv https://hdl.handle.net/20.500.12381/3253
dc.language.iso.none.fl_str_mv eng
dc.publisher.es.fl_str_mv Frontiers Media
dc.rights.es.fl_str_mv Acceso abierto
dc.rights.license.none.fl_str_mv Reconocimiento 4.0 Internacional. (CC BY)
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
dc.source.es.fl_str_mv Frontiers in Genetics
dc.source.none.fl_str_mv reponame:IPMON en REDI
instname:Institut Pasteur de Montevideo
instacron:Institut Pasteur de Montevideo
dc.subject.anii.none.fl_str_mv Ciencias Naturales y Exactas
Ciencias Biológicas
Bioquímica y Biología Molecular
dc.subject.es.fl_str_mv Argonautes (AGO)
PIWI
Toxoplasma
Trypanosoma
piRNA biogenesis
dc.title.none.fl_str_mv piRNA pathway evolution beyond gonad context: Perspectives from apicomplexa and trypanosomatids
dc.type.es.fl_str_mv Artículo
dc.type.none.fl_str_mv info:eu-repo/semantics/article
dc.type.version.es.fl_str_mv Publicado
dc.type.version.none.fl_str_mv info:eu-repo/semantics/publishedVersion
description piRNAs function as genome defense mechanisms against transposable elements insertions within germ line cells. Recent studies have unraveled that piRNA pathways are not limited to germ cells as initially reckoned, but are instead also found in non-gonadal somatic contexts. Moreover, these pathways have also been reported in bacteria, mollusks and arthropods, associated with safeguard of genomes against transposable elements, regulation of gene expression and with direct consequences in axon regeneration and memory formation. In this Perspective we draw attention to early branching parasitic protozoa, whose genome preservation is an essential function as in late eukaryotes. However, little is known about the defense mechanisms of these genomes. We and others have described the presence of putative PIWI-related machinery members in protozoan parasites. We have described the presence of a PIWI-like protein in Trypanosoma cruzi, bound to small non-coding RNAs (sRNAs) as cargo of secreted extracellular vesicles relevant in intercellular communication and host infection. Herein, we put forward the presence of members related to Argonaute pathways in both Trypanosoma cruzi and Toxoplasma gondii. The presence of PIWI-like machinery in Trypansomatids and Apicomplexa, respectively, could be evidence of an ancestral piRNA machinery that evolved to become more sophisticated and complex in multicellular eukaryotes. We propose a model in which ancient PIWI proteins were expressed broadly and had functions independent of germline maintenance. A better understanding of current and ancestral PIWI/piRNAs will be relevant to better understand key mechanisms of genome integrity conservation during cell cycle progression and modulation of host defense mechanisms by protozoan parasites.
eu_rights_str_mv openAccess
format article
id IPMON_961c8f66f67e35ab1e1f68fe182baadc
identifier_str_mv Horjales S, Li Calzi M, Francia ME, Cayota A and Garcia-Silva MR (2023), piRNA pathway evolution beyond gonad context: Perspectives from apicomplexa and trypanosomatids. Front. Genet. 14:1129194. doi: 10.3389/fgene.2023.1129194
instacron_str Institut Pasteur de Montevideo
institution Institut Pasteur de Montevideo
instname_str Institut Pasteur de Montevideo
language eng
network_acronym_str IPMON
network_name_str IPMON en REDI
oai_identifier_str oai:redi.anii.org.uy:20.500.12381/3253
publishDate 2023
reponame_str IPMON en REDI
repository.mail.fl_str_mv msarroca@pasteur.edu.uy
repository.name.fl_str_mv IPMON en REDI - Institut Pasteur de Montevideo
repository_id_str 9421_2
rights_invalid_str_mv Reconocimiento 4.0 Internacional. (CC BY)
Acceso abierto
spelling Reconocimiento 4.0 Internacional. (CC BY)Acceso abiertoinfo:eu-repo/semantics/openAccess2023-06-18T14:17:16Z2023-06-18T14:17:16Z2023-02-03Horjales S, Li Calzi M, Francia ME, Cayota A and Garcia-Silva MR (2023), piRNA pathway evolution beyond gonad context: Perspectives from apicomplexa and trypanosomatids. Front. Genet. 14:1129194. doi: 10.3389/fgene.2023.1129194https://hdl.handle.net/20.500.12381/3253https://doi.org/10.3389/fgene.2023.1129194piRNAs function as genome defense mechanisms against transposable elements insertions within germ line cells. Recent studies have unraveled that piRNA pathways are not limited to germ cells as initially reckoned, but are instead also found in non-gonadal somatic contexts. Moreover, these pathways have also been reported in bacteria, mollusks and arthropods, associated with safeguard of genomes against transposable elements, regulation of gene expression and with direct consequences in axon regeneration and memory formation. In this Perspective we draw attention to early branching parasitic protozoa, whose genome preservation is an essential function as in late eukaryotes. However, little is known about the defense mechanisms of these genomes. We and others have described the presence of putative PIWI-related machinery members in protozoan parasites. We have described the presence of a PIWI-like protein in Trypanosoma cruzi, bound to small non-coding RNAs (sRNAs) as cargo of secreted extracellular vesicles relevant in intercellular communication and host infection. Herein, we put forward the presence of members related to Argonaute pathways in both Trypanosoma cruzi and Toxoplasma gondii. The presence of PIWI-like machinery in Trypansomatids and Apicomplexa, respectively, could be evidence of an ancestral piRNA machinery that evolved to become more sophisticated and complex in multicellular eukaryotes. We propose a model in which ancient PIWI proteins were expressed broadly and had functions independent of germline maintenance. A better understanding of current and ancestral PIWI/piRNAs will be relevant to better understand key mechanisms of genome integrity conservation during cell cycle progression and modulation of host defense mechanisms by protozoan parasites.engFrontiers MediaFrontiers in Geneticsreponame:IPMON en REDIinstname:Institut Pasteur de Montevideoinstacron:Institut Pasteur de MontevideoArgonautes (AGO)PIWIToxoplasmaTrypanosomapiRNA biogenesisCiencias Naturales y ExactasCiencias BiológicasBioquímica y Biología MolecularpiRNA pathway evolution beyond gonad context: Perspectives from apicomplexa and trypanosomatidsArtículoPublicadoinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleInstitut Pasteur de Montevideo//Ciencias Naturales y Exactas/Ciencias Biológicas/Bioquímica y Biología MolecularHorjales, S.Li Calzi, M.Francia, M. E.Cayota, A.Garcia-Silva, M. R.LICENSElicense.txtlicense.txttext/plain; charset=utf-85334https://redi.anii.org.uy/jspui/bitstream/20.500.12381/3253/2/license.txt2d6047b2c47a34748db9b1d0017b96daMD52ORIGINALfgene-14-1129194.pdffgene-14-1129194.pdfpiRNA pathway evolution beyond gonad context: Perspectives from apicomplexa and trypanosomatidsapplication/pdf1607069https://redi.anii.org.uy/jspui/bitstream/20.500.12381/3253/1/fgene-14-1129194.pdf95f0556c96d2bb964e5915aedcfbf564MD5120.500.12381/32532023-06-18 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://pasteur.uy/https://redi.anii.org.uy/oai/requestmsarroca@pasteur.edu.uyUruguayopendoar:9421_22023-06-18T14:17:17IPMON en REDI - Institut Pasteur de Montevideofalse
spellingShingle piRNA pathway evolution beyond gonad context: Perspectives from apicomplexa and trypanosomatids
Horjales, S.
Argonautes (AGO)
PIWI
Toxoplasma
Trypanosoma
piRNA biogenesis
Ciencias Naturales y Exactas
Ciencias Biológicas
Bioquímica y Biología Molecular
status_str publishedVersion
title piRNA pathway evolution beyond gonad context: Perspectives from apicomplexa and trypanosomatids
title_full piRNA pathway evolution beyond gonad context: Perspectives from apicomplexa and trypanosomatids
title_fullStr piRNA pathway evolution beyond gonad context: Perspectives from apicomplexa and trypanosomatids
title_full_unstemmed piRNA pathway evolution beyond gonad context: Perspectives from apicomplexa and trypanosomatids
title_short piRNA pathway evolution beyond gonad context: Perspectives from apicomplexa and trypanosomatids
title_sort piRNA pathway evolution beyond gonad context: Perspectives from apicomplexa and trypanosomatids
topic Argonautes (AGO)
PIWI
Toxoplasma
Trypanosoma
piRNA biogenesis
Ciencias Naturales y Exactas
Ciencias Biológicas
Bioquímica y Biología Molecular
url https://hdl.handle.net/20.500.12381/3253
https://doi.org/10.3389/fgene.2023.1129194