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      Gene expression profiles of antigenic proteins of third stage larvae of the zoonotic nematode Anisakis pegreffii in response to temperature conditions Translated title: Profils d’expression génique des protéines antigéniques des larves du troisième stade du nématode zoonotique Anisakis pegreffii en réponse aux conditions de température

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          Anisakis pegreffii, a recognised etiological agent of human anisakiasis, is a parasite of homeothermic hosts at the adult stage and of ectothermic hosts at the third larval stage. Among distinct factors, temperature appears to be crucial in affecting parasite hatching, moulting and to modulate parasite-host interaction. In the present study, we investigated the gene transcripts of proteins having an antigenic role among excretory secretory products (ESPs) (i.e., a Kunitz-type trypsin inhibitor , A.peg-1; a glycoprotein, A.peg-7; and the myoglobin, A.peg-13) after 24 h, in A. pegreffii larvae maintained in vitro, under controlled temperature conditions. Temperatures were 37 °C and 20 °C, resembling respectively homeothermic and ectothermic hosts conditions, and 7 °C, the cold stress condition post mortem of the fish host. Primers of genes coding for these ESPs to be used in quantitative real-time PCR were newly designed, and qRT-PCR conditions developed. Expression profiles of the genes A.peg-1 and A.peg-13 were significantly up-regulated at 20 °C and 37 °C, with respect to the control (larvae kept at 2 °C for 24 h). Conversely, transcript profiles of A.peg-7 did not significantly change among the chosen temperature conditions. In accordance with the observed transcript profiles, sodium dodecyl sulfate–polyacrylamide gel electrophoresis (SDS-PAGE) revealed the presence of the three target ESPs at 37 °C, while only A.peg-13 was observed at 7 °C. The results suggest that temperature conditions do regulate the gene expression profiles of A.peg-1 and A.peg-13 in A. pegreffii larvae. However, regulation of the glycoprotein A.peg-7 is likely to be related to other factors such as the host’s immune response.

          Translated abstract

          Anisakis pegreffii, reconnu comme agent étiologique de l’anisakiase humaine, est un parasite d’hôtes homéothermes au stade adulte et d’hôtes ectothermes au troisième stade larvaire. Parmi les facteurs distincts, la température semble être cruciale pour l’éclosion des parasites, la mue et pour moduler l’interaction parasite-hôte. Dans la présente étude, nous avons étudié les transcrits géniques de protéines ayant un rôle antigénique parmi les produits de sécrétion excréteurs (PSE) (y compris un inhibiteur de la trypsine de type Kunitz, A.peg-1 ; une glycoprotéine, A.peg-7 ; et la myoglobine, A.peg-13) après 24 h, chez des larves de A. pegreffii maintenues in vitro dans des conditions de température contrôlées. Les températures étaient de 37 °C et 20 °C, ressemblant respectivement à la condition des hôtes homéothermes et ectothermes, et 7 °C, température de stress post mortem de l’hôte poisson. Des amorces de gènes codant pour ces PSE, pour utilisation dans la PCR quantitative en temps réel, ont été spécialement conçues et des conditions de qRT-PCR ont été développées. Les profils d’expression des gènes A.peg-1 et A.peg-13 étaient nettement régulés à la hausse à 20 °C et à 37 °C par rapport au contrôle (les larves ont été conservées à 2 °C pendant 24 h). Inversement, les profils de transcription de A.peg-7 n’ont pas changé de manière significative parmi les conditions de température choisies. Conformément aux profils de transcription observés, la SDS-PAGE a révélé la présence des trois PSE cibles à 37 °C, alors que seul A.peg-13 a été observé à 7 °C. Les résultats obtenus suggèrent que les conditions de température régulent le profil d’expression des gènes de A.peg-1 et A.peg-13 chez les larves d’ A. pegreffii. Cependant, la régulation de la glycoprotéine A.peg-7 est probablement liée à d’autres facteurs tels que la réponse immunitaire de l’hôte.

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          Most cited references 60

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          Anisakiasis and Gastroallergic Reactions Associated with Anisakis pegreffii Infection, Italy

          Human cases of gastric anisakiasis caused by the zoonotic parasite Anisakis pegreffii are increasing in Italy. The disease is caused by ingestion of larval nematodes in lightly cooked or raw seafood. Because symptoms are vague and serodiagnosis is difficult, the disease is often misdiagnosed and cases are understimated.
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            Genetic and morphological approaches distinguish the three sibling species of the Anisakis simplex species complex, with a species designation as Anisakis berlandi n. sp. for A. simplex sp. C (Nematoda: Anisakidae).

            Numerous specimens of the 3 sibling species of the Anisakis simplex species complex (A. pegreffii, A. simplex (senso stricto)), and A. simplex sp. C) recovered from cetacean species stranded within the known geographical ranges of these nematodes were studied morphologically and genetically. The genetic characterization was performed on diagnostic allozymes and sequences analysis of nuclear (internal transcribed spacer [ITS] of ribosomal [r]DNA) and mitochondrial (mitochondrial [mt]DNA cox2 and rrnS) genes. These markers showed (1) the occurrence of sympatry of the 2 sibling species A. pegreffii and A. simplex sp. C in the same individual host, the pilot whale, Globicephala melas Traill, from New Zealand waters; (2) the identification of specimens of A. pegreffii in the striped dolphin, Stenella coeruleoalba (Meyen), from the Mediterranean Sea; and (3) the presence of A. simplex (s.s.) in the pilot whale and the minke whale, Balaenoptera acutorostrata Lacépède, from the northeastern Atlantic waters. No F1 hybrids were detected among the 3 species using the nuclear markers. The phylogenetic inference, obtained by maximum parsimony (MP) analysis of separate nuclear (ITS rDNA region), combined mitochondrial (mtDNA cox2 and rrnS) sequences datasets, and by concatenated analysis obtained at both MP and Bayesian inference (BI) of the sequences datasets at the 3 studied genes, resulted in a similar topology. They were congruent in depicting the existence of the 3 species as distinct phylogenetic lineages, and the tree topologies support the finding that A. simplex (s.s.), A. pegreffii, and A. berlandi n. sp. (= A. simplex sp. C) represent a monophyletic group. The morphological and morphometric analyses revealed the presence of morphological features that differed among the 3 biological species. Morphological analysis using principal component analysis, and Procrustes analysis, combining morphological and genetic datasets, showed the specimens clustering into 3 well-defined groups. Nomenclatural designation and formal description are given for A. simplex species C: the name Anisakis berlandi n. sp. is proposed. Key morphological diagnostic traits are as follows between A. berlandi n. sp. and A. simplex (s.s.): ventriculus length, tail shape, tail length/total body length ratio, and left spicule length/total body length ratio; between A. berlandi n. sp. and A. pegreffii: ventriculus length and plectane 1 width/plectane 3 width ratio; and between A. simplex (s.s.) and A. pegreffii: ventriculus length, left and right spicule length/total body length ratios, and tail length/total body length ratio. Ecological data pertaining to the geographical ranges and host distribution of the 3 species are updated.
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              Sweet preferences of MGL: carbohydrate specificity and function.

              C-type lectins play important roles in both innate and adaptive immune responses. In contrast to the mannose- or fucose-specific C-type lectins DC-SIGN and mannose receptor, the galactose-type lectins, of which only macrophage galactose-type lectin (MGL) is found within the immune system, are less well known. MGL is selectively expressed by immature dendritic cells and macrophages with elevated levels on tolerogenic or alternatively activated subsets. Human MGL has an exclusive specificity for rare terminal GalNAc structures, which are revealed on the tumor-associated mucin MUC1 and CD45 on effector T cells. These findings implicate MGL in the homeostatic control of adaptive immunity. We discuss here the functional similarities and differences between MGL orthologs and compare MGL to its closest homolog, the liver-specific asialoglycoprotein receptor (ASGP-R).

                Author and article information

                EDP Sciences
                23 August 2019
                : 26
                : ( publisher-idID: parasite/2019/01 )
                [1 ] Department of Public Health and Infectious Diseases, Section of Parasitology, and “Umberto I” Academic Hospital “Sapienza – University of Rome” P.le Aldo Moro, 5 00185 Rome Italy
                [2 ] Department of Ecological and Biological Sciences, Tuscia University Viale dell’Università s/n 01100 Viterbo Italy
                [3 ] Department of Experimental Medicine, “Sapienza-University of Rome” P.le Aldo Moro, 5 00185 Rome Italy
                Author notes
                parasite190080 10.1051/parasite/2019055
                © M. Palomba et al., published by EDP Sciences, 2019

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                Page count
                Figures: 6, Tables: 2, Equations: 0, References: 66, Pages: 12
                Research Article


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