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Polychaetes As Annelid Models to Study Ecoimmunology of Marine Organisms

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Polychaetes As Annelid Models to Study Ecoimmunology of Marine Organisms Journal of Marine Science and Technology, Vol. 22, No. 1, pp. 9-14 (2014) 9 DOI: 10.6119/JMST-013-0718-1 POLYCHAETES AS ANNELID MODELS TO STUDY ECOIMMUNOLOGY OF MARINE ORGANISMS Virginie Cuvillier-Hot, Céline Boidin-Wichlacz, and Aurélie Tasiemski Key words: Marine annelids, invertebrates, ecological immunology. Innate immunity which constituted the most ancient first line of immune protection is vital for invertebrate host defense and has become conserved through the animal kingdom. Even if ABSTRACT invertebrates lack such critical elements of adaptive immunity Annelids are among the first coelomates and are therefore as antibodies and lymphocytes, they can resist infections and of special phylogenetic interest. They constitute an important also transmit lethal diseases to vertebrates, without necessarily part of the biomass of the seashore, estuaries, fresh water and being affected. Components that participate in innate immune terrestrial soils. Moreover, they occupy a central position in responses include humoral factors found in body fluids the trophic networks, as a major food source for fishes, birds (phenoloxidases, clotting factors, complement factors, lectins, and terrestrial fauna. Among Annelids, the large majority of protease inhibitors, antimicrobial peptides…) and cells that polychaetes is restricted to the marine domain. This report kill invading pathogens by using phagocytic or cytotoxic gives an overview of the immune strategies developed by systems. polychaetes to fight pathogens. The potential and interest to Annelids belonging to the lophotrochozoan group are primi- use these worms as biomarkers to monitor the influence of tive coelomates that have developed both cellular and humoral environmental perturbation on the immunity of marine or- immunity against pathogens. Ringed worms constitute an ganisms is discussed. important part of the biomass of the seashore, estuaries, fresh water and terrestrial soils. Moreover, they occupy a central position in the trophic network, as a major food source for I. INTRODUCTION fishes, birds and terrestrial fauna. Among Annelids, the large The field of immunology classically examines the physio- majority of polychaetes is restricted to the marine domain logical and molecular processes underpinning host defense whereas oligochaetes and leeches can be terrestrial semi or against pathogens and is usually conducted on laboratory fully aquatic in freshwater or more rarely in seawater. models under optimal conditions i.e. in the absence of natural This report gives an overview of the immune strategies pathogens. The role and the regulation of immune effector used by polychaetes to fight pathogens. The potential and systems under the constraints imposed by life history and interest for the use of polychaetes as biomarkers to study the ecology came into focus ten years ago. This emerging field influence of environmental perturbation on the immunity of called ecological immunology or ecoimmunology is concerned marine organisms is discussed. Special interest is accorded with decorticating the microevolutionary processes that create to species of economic importance and/or used in ecotoxi- and maintain variation in immune effector systems and the cological studies and bioaccumulation assays. coordinated host response to pathogens. Immune reactions For understanding immune processes, it is necessary to have been showed to be influenced to various degrees by en- briefly review Annelids’ anatomy. Annelids are characterized vironmental factors such as anthropogenic pollution. by the presence of two compartment containing circulating Invertebrates appear as attractive subjects to study ecoim- cells: (i) the blood system with hemocytes, the implication of munology because of the simple mechanisms underpinning this compartment in immunity has been studied in leeches their innate immune systems and their amenability to physio- only and (ii) the coelom that contains several coelomocytes logical manipulations in the context of life history and ecology. populations playing functions in immune defense. 1. The Cellular Immune Response of Polychaetes Paper submitted 08/01/12; revised 10/30/12; accepted 07/18/13. Author for correspondence: Aurélie Tasiemski (e-mail: [email protected]). Cellular immunity includes various mechanisms such as University of Lille1-CNRS UMR8198, GEPV, Eco immunology of Marine cytotoxicity, phagocytosis and the encapsulation process Annelids group, Villeneuve d’Ascq, France. which leads to the elimination of foreign bodies bigger than 10 Journal of Marine Science and Technology, Vol. 22, No. 1 (2014) Septic injury Environment Microorganisms Tegument Coelomic liquide G1 cells G2 cells G3 cells = NK like MPII Melanisation Cytotoxicity Phagocytosis AMP production Lysozyme Fig. 1. Hypothetical scheme of the putative immune response of Hediste diversicolor. Cellular immunity (melanisation, phagocytosis, cytotoxicity) implicates three types of granulocytes, G1, G2 and G3. Humoral immunity is based on the release from these cells of active substances such as antimicrobial molecules (AMPs, MPII and lysozyme) into the coelomic liquid. bacteria. As for Arthropods and Molluscs, three major cell To date, G3 have been observed in Nereididae only. types were structurally characterized in the coelomic liquid of Annelids [14]. The clear differentiation in the structure 1) Phagocytosis of Annelid coelomocytes is associated with their function: In polychaetes, active phagocytosis occurs in the battle hyaline cells participate in the melanization/encapsulation against bacteria. Experimentally, this process is observed by processes, granular coelomocytes called ‘granulocytes’ exert injecting into the coelomic cavity either small particles or phagocytic and cytotoxic activities, eleocytes constitute the labelled bacteria, which are taken up by endocytosis and functional equivalent of the fat body of insects. The cellular stored in the vacuoles of the coelomic cells. This uptake is part of the immune system plays a central role in defense usually linked with the induction of an oxidative burst of against all types of threats. It helps bacterial clearing but also metabolism. Production of highly reactive oxygen radicals finishes the work in all defense mechanisms (as well as in the represents an effective way of destroying engulfed bacteria. In current cell) through waste removal. Moreover, it is the sole Nereidae and Arenicolidae, granular coelomocytes through effective barrier against pathogens of large size, especially their phagocytic system, are associated with the clearance of parasites, via cytotoxicity and encapsulation. The proportion bacteria from the coelom [8]. In H. diversicolor, after injec- of cells exerting cytotoxic and/or phagocytic activities is thus tion of radiolabelled Vibrio alginolyticus, a progressive de- an important criterion that can be measured to monitor the crease of the radioactivity of the coelomic fluid together with a impact of environment on individual immunocompetence. reduction of the number of granulocytes is observed whereas Immune cell integrity can also be an interesting parameter. In the number of eleocytes does not change [12]. Contact of lungworm, the negative impact of nanoparticules trapped in isolated coelomocytes with yeast cells show that small foreign sediments was evidenced by measuring the lysosomal mem- bodies are phagocytosed by G2 granulocytes (Fig. 2A), as brane stability of coelomocytes [13]. confirmed by electron microscopy observations [11]. In the In Hediste diversicolor, three subtypes of granulocytes free living polychaete Eurythoe complanata, the contamina- were described (Fig. 1), first from ultrastructural observations tion of the environment by copper can be assessed through its and later with the aid of monoclonal antibodies [22-24]. Type immune negative impact measured as phagocytosis impair- 1 granulocytes (G1) observed also in Arenicolidae, are large ment, replacing ineffective classical biochemical markers and fusiform cells. Type 2 granulocytes (G2) observed in [17]. Arenicolidae, Nereididae, and Terebellidae [8] posses abun- dant phagocytic vacuoles and are numerically more important 2) Encapsulation than G1. G2 may be related to the hyaline cell type described The encapsulation process has been extensively studied in in leeches, earthworms and non-annelid species of inverte- H. diversicolor in an experimental form (implantation of latex brates. Type 3 granulocytes (G3) are small cells and numerous, beads, [23]) and in a natural context (reactions against dif- with a high nucleoplasmic ratio and a few rounded granules. ferent natural coelomic parasites, [23]). Cooperation between V. Cuvillier-Hot et al.: Ecoimmunology of Marine Annelids 11 A B G3 G2 G1 G3 G2 10 µm 10 µm C D G3 G1 G3 G2 10 µm 10 µm Fig. 2. Immune functions of isolated Hediste diversicolor granulocytes. A- G2 cells are able to engulf foreign particles (here yeast cell pointed by the arrow); B- in the presence of L-DOPA, G2 and G3 cells release compounds that generate melanine (arrow); C- G3 cells exert cytotoxic activity against foreign cells (here coelomocyte from Eisenia fetida, colored with neutral red) by tightly adhering to the foreign surface and releasing pore-forming proteins; D- all three types of granulocytes degranulate in presence of bacterial motifs such as LPS (arrows point released gran- ules). different coelomocyte populations (except eleocytes) was The study of graft rejection has highlighted the role of cell observed
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