Comparative transcriptomics reveal a novel tardigrade-specific DNA-binding protein induced in response to ionizing radiation

Author:

Anoud Marwan12,Delagoutte Emmanuelle1,Helleu Quentin1,Brion Alice1,Duvernois-Berthet Evelyne3ORCID,As Marie1,Marques Xavier14,Lamribet Khadija1,Senamaud-Beaufort Catherine5ORCID,Jourdren Laurent5ORCID,Adrait Annie6,Heinrich Sophie78,Toutirais Geraldine9,Hamlaoui Sahima10,Gropplero Giacomo11,Giovannini Ilaria1213,Ponger Loic1,Geze Marc4,Blugeon Corinne5ORCID,Couté Yohann6ORCID,Guidetti Roberto1213ORCID,Rebecchi Lorena1213,Giovannangeli Carine1,De Cian Anne1ORCID,Concordet Jean-Paul1ORCID

Affiliation:

1. Département AVIV, MNHN, CNRS UMR7196, INSERM U1154

2. Université Paris-Saclay

3. Département AVIV, MNHN, CNRS UMR7221

4. CeMIM, MNHN, CNRS UMR7245

5. Génomique ENS, Institut de Biologie de l’ENS (IBENS), Ecole Normale Supérieure, CNRS, INSERM, Université PSL

6. Univ. Grenoble Alpes, INSERM, CEA, UA13 BGE, CNRS, CEA

7. Institut Curie, Inserm U1021-CNRS UMR 3347, Université Paris-Saclay, Université PSL

8. Plateforme RADEXP, Institut Curie

9. Plateforme technique de Microscopie Electronique, MNHN

10. Département AVIV MNHN, UMR7245

11. MMBM, Institut Curie, CNRS UMR168

12. Department of Life Sciences, University of Modena and Reggio Emilia

13. NBFC, National Biodiversity Future Center

Abstract

Tardigrades are microscopic animals renowned for their ability to withstand extreme conditions, including high doses of ionizing radiation (IR). To better understand their radio-resistance, we first characterized induction and repair of DNA double- and single-strand breaks after exposure to IR in the model species Hypsibius exemplaris. Importantly, we found that the rate of single-strand breaks induced was roughly equivalent to that in human cells, suggesting that DNA repair plays a predominant role in tardigrades’ radio-resistance. To identify novel tardigrade-specific genes involved, we next conducted a comparative transcriptomics analysis across three different species. In all three species, many DNA repair genes were among the most strongly overexpressed genes alongside a novel tardigrade-specific gene, which we named Tardigrade DNA damage Response 1 (TDR1). We found that TDR1 protein interacts with DNA and forms aggregates at high concentration suggesting it may condensate DNA and preserve chromosome organization until DNA repair is accomplished. Remarkably, when expressed in human cells, TDR1 improved resistance to Bleomycin, a radiomimetic drug. Based on these findings, we propose that TDR1 is a novel tardigrade-specific gene conferring resistance to IR. Our study sheds light on mechanisms of DNA repair helping cope with high levels of DNA damage inflicted by IR.

Funder

Sorbonne Université

Agence Nationale de la Recherche

Publisher

eLife Sciences Publications, Ltd

Cited by 1 articles. 订阅此论文施引文献 订阅此论文施引文献,注册后可以免费订阅5篇论文的施引文献,订阅后可以查看论文全部施引文献

1. Surviving extreme radiation;eLife;2024-07-04

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