Ferroptosis precedes apoptosis to facilitate specific death signalling by fatty acids

Author:

Zupo Valerio1ORCID,Costantini Maria2ORCID,Aflalo Eliahu D.34,Levy Tom56ORCID,Chalifa-Caspi Vered7,Obayomi Olabiyi89,Mutalipassi Mirko1011ORCID,Ruocco Nadia12ORCID,Glaviano Francesca1ORCID,Somma Emanuele113ORCID,Nieri Paola147,Sagi Amir315

Affiliation:

1. Department of Ecosustainable Marine Biotechnology, Stazione Zoologica Anton Dohrn, Villa Dohrn, Ischia, Italy

2. Department of Ecosustainable Marine Biotechnology, Stazione Zoologica Anton Dohrn, Via Ammiraglio Ferdinando Acton, 55, 80133 Napoli, Italy

3. Department of Life Sciences, Ben-Gurion University of the Negev, PO Box 653, Beer-Sheva 8410501, Israel

4. Department of Life Sciences, Achva Academic College, Mobile Post, Shikmim 79800, Israel

5. Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine, Stanford, CA 94305, USA

6. Hopkins Marine Station, Institute for Stem Cell Biology and Regenerative Medicine, Stanford University, Pacific Grove, CA 93950, USA

7. Ilse Katz Institute for Nanoscale Science & Technology, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel

8. Interdepartmental Center of Marine Pharmacology, Pisa University, 56126 Pisa, Italy

9. Zuckerberg Institute for Water Research, J. Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben Gurion 84990, Israel

10. Department of Integrative Marine Ecology, Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Napoli, Italy

11. NBFC, National Biodiversity Future Center, Piazza Marina 61, 90133 Palermo, Italy

12. Department of Ecosustainable Marine Biotechnology, Stazione Zoologica Anton Dohrn, Calabria Marine Centre, C. da Torre Spaccata, Amendolara, Italy

13. Department of Life Science, University of Trieste, Via L. Giorgieri, 10, 34127 Trieste, Italy

14. Department of Pharmacy, Pisa University, 56126 Pisa, Italy

15. The National Institute for Biotechnology in the Negev, Ben-Gurion University of the Negev, PO Box 653, Beer-Sheva 8410501, Israel

Abstract

Cell death is physiologically induced by specific mediators. However, our power to trigger the process in selected cells is quite limited. The protandric shrimp Hippolyte inermis offers a possible answer. Here, we analyse a de novo transcriptome of shrimp post-larvae fed on diatoms. The sex ratio of diatom-fed shrimps versus shrimps fed on control diets was dramatically altered, demonstrating the disruption of the androgenic gland, and their transcriptome revealed key modifications in gene expression. A wide transcriptomic analysis, validated by real-time qPCR, revealed that ferroptosis represents the primary factor to re-shape the body of this invertebrate, followed by further apoptotic events, and our findings open biotechnological perspectives for controlling the destiny of selected tissues. Ferroptosis was detected here for the first time in a crustacean. In addition, this is the first demonstration of a noticeable effect prompted by an ingested food, deeply impacting the gene networks of a young metazoan, definitely determining its future physiology and sexual differentiation.

Funder

Israel Ministry of Science and Technology

Italian Ministry for Foreign Affairs

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Environmental Science,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine

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