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1. In-Depth In Silico Search for Cuttlefish (Sepia officinalis) Antimicrobial Peptides Following Bacterial Challenge of Haemocytes

Author

Louis Benoist, Baptiste Houyvet, Joël Henry, Erwan Corre, Bruno Zanuttini, and Céline Zatylny-Gaudin

Subjects
antimicrobial peptide, haemocyte, Sepia officinalis, mollusc, challenge, in vitro, Biology (General), QH301-705.5
Abstract

Cuttlefish (Sepia officinalis) haemocytes are potential sources of antimicrobial peptides (AMPs). To study the immune response to Vibrio splendidus and identify new AMPs, an original approach was developed based on a differential transcriptomic study and an in-depth in silico analysis using multiple tools. Two de novo transcriptomes were retrieved from cuttlefish haemocytes following challenge by V. splendidus or not. A first analysis of the annotated transcripts revealed the presence of Toll/NF-κB pathway members, including newly identified factors such as So-TLR-h, So-IKK-h and So-Rel/NF-κB-h. Out of the eight Toll/NF-κB pathway members, seven were found up-regulated following V. splendidus challenge. Besides, immune factors involved in the immune response were also identified and up-regulated. However, no AMP was identified based on annotation or conserved pattern searches. We therefore performed an in-depth in silico analysis of unannotated transcripts based on differential expression and sequence characteristics, using several tools available like PepTraq, a homemade software program. Finally, five AMP candidates were synthesized. Among them, NF19, AV19 and GK28 displayed antibacterial activity against Gram-negative bacteria. Each peptide had a different spectrum of activity, notably against Vibrio species. GK28—the most active peptide—was not haemolytic, whereas NF19 and AV19 were haemolytic at concentrations between 50 and 100 µM, 5 to 10 times higher than their minimum inhibitory concentration.

Published
2020
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2. Omic Analysis of the

Author

Louis, Benoist, Erwan, Corre, Benoit, Bernay, Joel, Henry, and Céline, Zatylny-Gaudin

Subjects
Proteomics, Sepia, Proteome, Decapodiformes, Animals, Hematopoiesis
Abstract

Cephalopods, like other protostomes, lack an adaptive immune system and only rely on an innate immune system. The main immune cells are haemocytes (Hcts), which are able to respond to pathogens and external attacks. First reports based on morphological observations revealed that the white body (WB) located in the optic sinuses of cuttlefish was the origin of Hcts. Combining transcriptomic and proteomic analyses, we identified several factors known to be involved in haematopoiesis in vertebrate species in cuttlefish WB. Among these factors, members of the JAK-STAT signaling pathway were identified, some of them for the first time in a molluscan transcriptome and proteome. Immune factors, such as members of the Toll/NF-κB signaling pathway, pattern recognition proteins and receptors, and members of the oxidative stress responses, were also identified, and support an immune role of the WB. Both transcriptome and proteome analyses revealed that the WB harbors an intense metabolism concurrent with the haematopoietic function. Finally, a comparative analysis of the WB and Hct proteomes revealed many proteins in common, confirming previous morphological studies on the origin of Hcts in cuttlefish. This molecular work demonstrates that the WB is multifunctional and provides bases for haematopoiesis regulation in cuttlefish.

Published
2020

3. Omic Analysis of the Sepia officinalis White Body: New Insights into Multifunctionality and Haematopoiesis Regulation

Author

Benoit Bernay, Céline Zatylny-Gaudin, Louis Benoist, Erwan Corre, Joël Henry, Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), Université de Caen Normandie (UNICAEN), Normandie Université (NU)-Normandie Université (NU)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA), ABiMS - Informatique et bioinformatique = Analysis and Bioinformatics for Marine Science (FR2424), Station biologique de Roscoff (SBR), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Interactions Cellules Organismes Environnement (ICORE), Normandie Université (NU)-Normandie Université (NU)-CHU Caen, Normandie Université (NU)-Tumorothèque de Caen Basse-Normandie (TCBN)-Tumorothèque de Caen Basse-Normandie (TCBN), ABiMS - Informatique et bioinformatique = Analysis and Bioinformatics for Marine Science (ABIMS), Fédération de recherche de Roscoff (FR2424), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Station biologique de Roscoff (SBR), and Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)

Subjects
0301 basic medicine, Cuttlefish, Innate immune system, 030102 biochemistry & molecular biology, white body, sepia officinalis, General Chemistry, Biology, haematopoiesis, Acquired immune system, Biochemistry, [SDV.IMM.II]Life Sciences [q-bio]/Immunology/Innate immunity, Cell biology, JAK-STAT pathway, Transcriptome, [SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology, 03 medical and health sciences, Haematopoiesis, 030104 developmental biology, Immune system, mollusc, Proteome, Sepia
Abstract

International audience; Cephalopods, like other protostomes, lack an adaptive immune system and only rely on an innate immune system. The main immune cells are haemocytes (Hcts), which are able to respond to pathogens and external attacks. First reports based on morphological observations revealed that the white body (WB) located in the optic sinuses of cuttlefish was the origin of Hcts. Combining transcriptomic and proteomic analyses, we identified several factors known to be involved in haematopoiesis in vertebrate species in cuttlefish WB. Among these factors, members of the JAK-STAT signaling pathway were identified, some of them for the first time in a molluscan transcriptome and proteome. Immune factors, such as members of the Toll/NF-κB signaling pathway, pattern recognition proteins and receptors, and members of the oxidative stress responses, were also identified, and support an immune role of the WB. Both transcriptome and proteome analyses revealed that the WB harbors an intense metabolism concurrent with the haematopoietic function. Finally, a comparative analysis of the WB and Hct proteomes revealed many proteins in common, confirming previous morphological studies on the origin of Hcts in cuttlefish. This molecular work demonstrates that the WB is multifunctional and provides bases for haematopoiesis regulation in cuttlefish

Published
2020
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4. Crustacean cardioactive peptides: Expression, localization, structure, and a possible involvement in regulation of egg-laying in the cuttlefish Sepia officinalis

Author

Maxime Endress, Jimmy Rangama, Jérôme Leprince, Benoit Bernay, Joël Henry, Anne-Gaëlle Lafont, Benjamin Lefranc, Arnaud Bondon, Gildas Le Corguillé, Louis Benoist, Alexandre Leduc, Erwan Corre, Céline Zatylny-Gaudin, Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), Université de Caen Normandie (UNICAEN), Normandie Université (NU)-Normandie Université (NU)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA), ABiMS - Informatique et bioinformatique = Analysis and Bioinformatics for Marine Science (ABIMS), Fédération de recherche de Roscoff (FR2424), Station biologique de Roscoff (SBR), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Station biologique de Roscoff (SBR), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Différenciation et communication neuronale et neuroendocrine (DC2N), Université de Rouen Normandie (UNIROUEN), Normandie Université (NU)-Normandie Université (NU)-Institut National de la Santé et de la Recherche Médicale (INSERM), Interactions Cellules Organismes Environnement (ICORE), Normandie Université (NU)-Normandie Université (NU)-CHU Caen, Normandie Université (NU)-Tumorothèque de Caen Basse-Normandie (TCBN)-Tumorothèque de Caen Basse-Normandie (TCBN), Centre de recherche sur les Ions, les MAtériaux et la Photonique (CIMAP - UMR 6252), Normandie Université (NU)-Normandie Université (NU)-École Nationale Supérieure d'Ingénieurs de Caen (ENSICAEN), Normandie Université (NU)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche sur les Matériaux Avancés (IRMA), Normandie Université (NU)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université de Rouen Normandie (UNIROUEN), Normandie Université (NU)-Institut national des sciences appliquées Rouen Normandie (INSA Rouen Normandie), Institut National des Sciences Appliquées (INSA)-Normandie Université (NU)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université de Rouen Normandie (UNIROUEN), Institut National des Sciences Appliquées (INSA)-Normandie Université (NU)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS), Institut des Sciences Chimiques de Rennes (ISCR), Université de Rennes (UR)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Ecole Nationale Supérieure de Chimie de Rennes (ENSCR)-Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Université de Caen Normandie (UNICAEN), Normandie Université (NU)-Normandie Université (NU), ABiMS - Informatique et bioinformatique = Analysis and Bioinformatics for Marine Science (FR2424), CHU Caen, Normandie Université (NU)-Tumorothèque de Caen Basse-Normandie (TCBN)-Normandie Université (NU)-Tumorothèque de Caen Basse-Normandie (TCBN)-Université de Caen Normandie (UNICAEN), Normandie Université (NU), Centre National de la Recherche Scientifique (CNRS)-École Nationale Supérieure d'Ingénieurs de Caen (ENSICAEN), Normandie Université (NU)-Normandie Université (NU)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université de Caen Normandie (UNICAEN), Centre National de la Recherche Scientifique (CNRS)-Institut de Chimie du CNRS (INC)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Ecole Nationale Supérieure de Chimie de Rennes (ENSCR)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA), and Jonchère, Laurent

Subjects
Central Nervous System, Male, 0301 basic medicine, Cuttlefish, Sepia, animal structures, Oviposition, Neuropeptide, Zoology, Context (language use), Oviducts, Sepia officinalis, [SDV.BDLR.RS]Life Sciences [q-bio]/Reproductive Biology/Sexual reproduction, 03 medical and health sciences, Endocrinology, Animals, Tissue Distribution, Amino Acid Sequence, 14. Life underwater, Peptide sequence, [SDV.BDLR.RS] Life Sciences [q-bio]/Reproductive Biology/Sexual reproduction, biology, Reproduction, egg-laying, Neuropeptides, CCAPs, fungi, Decapodiformes, Gene Expression Regulation, Developmental, biology.organism_classification, NMR, Cephalopod, [SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology, 030104 developmental biology, Oviparity, [SDV.BA.ZI] Life Sciences [q-bio]/Animal biology/Invertebrate Zoology, Oocytes, Oviduct, Female, Animal Science and Zoology, Sequence Alignment, Free nerve ending
Abstract

International audience; The cuttlefish (Sepia officinalis) is a cephalopod mollusk distributed on the western European coast, in the West African Ocean and in the Mediterranean Sea. On the Normandy coast (France), cuttlefish is a target species of professional fishermen, so its reproduction strategy is of particular interest in the context of stock management. Egg-laying, which is coastal, is controlled by several types of regulators among which neuropeptides. The cuttlefish neuropeptidome was recently identified by Zatylny-Gaudin et al. (2016). Among the 38 neuropeptide families identified, some were significantly overexpressed in egg-laying females as compared to mature males. This study is focused on crustacean cardioactive peptides (CCAPs), a highly expressed neuropeptide family strongly suspected of being involved in the control of egg-laying. We investigated the functional and structural characterization and tissue mapping of CCAPs, as well as the expression patterns of their receptors. CCAPs appeared to be involved in oocyte transport through the oviduct and in mechanical secretion of capsular products. Immunocytochemistry revealed that the neuropeptides were localized throughout the central nervous system (CNS) and in the nerve endings of the glands involved in egg-capsule synthesis and secretion, i.e. the oviduct gland and the main nidamental glands. The CCAP receptor was expressed in these glands and in the subesophageal mass of the CNS. Multiple sequence alignments revealed a high level of conservation of CCAP protein precursors in Sepia officinalis and Loligo pealei, two cephalopod decapods. Primary sequences of CCAPs from the two species were fully conserved, and cryptic peptides detected in the nerve endings were also partially conserved, suggesting biological activity that remains unknown for the time being.

Published
2018
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