Self-DNA Exposure Induces Developmental Defects and Germline DNA Damage Response in <i>Caenorhabditis elegans</i>

All organisms, from bacteria to mammals, sense and respond to foreign nucleic acids to fight infections in order to survive and preserve genome integrity across generations. The innate immune system is an evolutionarily conserved defence strategy. Complex organisms have developed various cellular pr...

Full description

Bibliographic Details
Main Authors: Marcello Germoglio, Adele Adamo, Guido Incerti, Fabrizio Cartenì, Silvia Gigliotti, Aurora Storlazzi, Stefano Mazzoleni
Format: Article
Language:English
Published: MDPI AG 2022-02-01
Series:Biology
Subjects:
Online Access:https://www.mdpi.com/2079-7737/11/2/262
_version_ 1797482614974578688
author Marcello Germoglio
Adele Adamo
Guido Incerti
Fabrizio Cartenì
Silvia Gigliotti
Aurora Storlazzi
Stefano Mazzoleni
author_facet Marcello Germoglio
Adele Adamo
Guido Incerti
Fabrizio Cartenì
Silvia Gigliotti
Aurora Storlazzi
Stefano Mazzoleni
author_sort Marcello Germoglio
collection DOAJ
description All organisms, from bacteria to mammals, sense and respond to foreign nucleic acids to fight infections in order to survive and preserve genome integrity across generations. The innate immune system is an evolutionarily conserved defence strategy. Complex organisms have developed various cellular processes to respond to and recognise not only infections, i.e., pathogen-associated molecular patterns (PAMPs), but also to sense injury and tissue dysfunctions, i.e., damage-associated molecular patterns (DAMPs). Mis-localized self-DNA can be sensed as DAMP by specific DNA-sensing pathways, and self-DNA chronic exposure can be detrimental to the organisms. Here, we investigate the effects of dietary delivered self-DNA in the nematode <i>Caenorhabditis elegans</i>. The hermaphrodite worms were fed on <i>Escherichia coli</i> genomic libraries: a <i>C. elegans</i> library (self) and a legume (<i>Medicago truncatula</i>) library (non-self). We show that the self-library diet affects embryogenesis, larval development and gametogenesis. DNA damage and activation of p53/CEP-1-dependent apoptosis occur in gonadal germ cells. Studies of self-DNA exposure in this model organism were not pursued up to now. The genetic tractability of <i>C. elegans</i> will help to identify the basic molecular pathways involved in such mechanisms. The specificity of the adverse effects associated with a self-DNA enriched diet suggests applications in biological pest control approaches.
first_indexed 2024-03-09T22:34:57Z
format Article
id doaj.art-8bed91b603d34179b8e72c1a79f23acf
institution Directory Open Access Journal
issn 2079-7737
language English
last_indexed 2024-03-09T22:34:57Z
publishDate 2022-02-01
publisher MDPI AG
record_format Article
series Biology
spelling doaj.art-8bed91b603d34179b8e72c1a79f23acf2023-11-23T18:50:32ZengMDPI AGBiology2079-77372022-02-0111226210.3390/biology11020262Self-DNA Exposure Induces Developmental Defects and Germline DNA Damage Response in <i>Caenorhabditis elegans</i>Marcello Germoglio0Adele Adamo1Guido Incerti2Fabrizio Cartenì3Silvia Gigliotti4Aurora Storlazzi5Stefano Mazzoleni6Institute of Biosciences and BioResources, National Research Council, Via Pietro Castellino 111, 80131 Napoli, ItalyInstitute of Biosciences and BioResources, National Research Council, Via Pietro Castellino 111, 80131 Napoli, ItalyDepartment of Agri-Food, Animal and Environmental Sciences (DI4A), University of Udine, 33100 Udine, ItalyDepartment of Agricultural Sciences, Università degli Studi di Napoli Federico II, 80055 Portici, ItalyInstitute of Biosciences and BioResources, National Research Council, Via Pietro Castellino 111, 80131 Napoli, ItalyInstitute of Biosciences and BioResources, National Research Council, Via Pietro Castellino 111, 80131 Napoli, ItalyDepartment of Agricultural Sciences, Università degli Studi di Napoli Federico II, 80055 Portici, ItalyAll organisms, from bacteria to mammals, sense and respond to foreign nucleic acids to fight infections in order to survive and preserve genome integrity across generations. The innate immune system is an evolutionarily conserved defence strategy. Complex organisms have developed various cellular processes to respond to and recognise not only infections, i.e., pathogen-associated molecular patterns (PAMPs), but also to sense injury and tissue dysfunctions, i.e., damage-associated molecular patterns (DAMPs). Mis-localized self-DNA can be sensed as DAMP by specific DNA-sensing pathways, and self-DNA chronic exposure can be detrimental to the organisms. Here, we investigate the effects of dietary delivered self-DNA in the nematode <i>Caenorhabditis elegans</i>. The hermaphrodite worms were fed on <i>Escherichia coli</i> genomic libraries: a <i>C. elegans</i> library (self) and a legume (<i>Medicago truncatula</i>) library (non-self). We show that the self-library diet affects embryogenesis, larval development and gametogenesis. DNA damage and activation of p53/CEP-1-dependent apoptosis occur in gonadal germ cells. Studies of self-DNA exposure in this model organism were not pursued up to now. The genetic tractability of <i>C. elegans</i> will help to identify the basic molecular pathways involved in such mechanisms. The specificity of the adverse effects associated with a self-DNA enriched diet suggests applications in biological pest control approaches.https://www.mdpi.com/2079-7737/11/2/262<i>Caenorhabditis elegans</i>self-DNAgermlineapoptosisnematode
spellingShingle Marcello Germoglio
Adele Adamo
Guido Incerti
Fabrizio Cartenì
Silvia Gigliotti
Aurora Storlazzi
Stefano Mazzoleni
Self-DNA Exposure Induces Developmental Defects and Germline DNA Damage Response in <i>Caenorhabditis elegans</i>
Biology
<i>Caenorhabditis elegans</i>
self-DNA
germline
apoptosis
nematode
title Self-DNA Exposure Induces Developmental Defects and Germline DNA Damage Response in <i>Caenorhabditis elegans</i>
title_full Self-DNA Exposure Induces Developmental Defects and Germline DNA Damage Response in <i>Caenorhabditis elegans</i>
title_fullStr Self-DNA Exposure Induces Developmental Defects and Germline DNA Damage Response in <i>Caenorhabditis elegans</i>
title_full_unstemmed Self-DNA Exposure Induces Developmental Defects and Germline DNA Damage Response in <i>Caenorhabditis elegans</i>
title_short Self-DNA Exposure Induces Developmental Defects and Germline DNA Damage Response in <i>Caenorhabditis elegans</i>
title_sort self dna exposure induces developmental defects and germline dna damage response in i caenorhabditis elegans i
topic <i>Caenorhabditis elegans</i>
self-DNA
germline
apoptosis
nematode
url https://www.mdpi.com/2079-7737/11/2/262
work_keys_str_mv AT marcellogermoglio selfdnaexposureinducesdevelopmentaldefectsandgermlinednadamageresponseinicaenorhabditiselegansi
AT adeleadamo selfdnaexposureinducesdevelopmentaldefectsandgermlinednadamageresponseinicaenorhabditiselegansi
AT guidoincerti selfdnaexposureinducesdevelopmentaldefectsandgermlinednadamageresponseinicaenorhabditiselegansi
AT fabriziocarteni selfdnaexposureinducesdevelopmentaldefectsandgermlinednadamageresponseinicaenorhabditiselegansi
AT silviagigliotti selfdnaexposureinducesdevelopmentaldefectsandgermlinednadamageresponseinicaenorhabditiselegansi
AT aurorastorlazzi selfdnaexposureinducesdevelopmentaldefectsandgermlinednadamageresponseinicaenorhabditiselegansi
AT stefanomazzoleni selfdnaexposureinducesdevelopmentaldefectsandgermlinednadamageresponseinicaenorhabditiselegansi