Echinodermata: the Complex Immune System in Echinoderms
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Echinodermata: The Complex Immune System in Echinoderms L. Courtney Smith, Vincenzo Arizza, Megan A. Barela Hudgell, Gianpaolo Barone, Andrea G. Bodnar, Katherine M. Buckley, Vincenzo Cunsolo, Nolwenn M. Dheilly, Nicola Franchi, Sebastian D. Fugmann, Ryohei Furukawa, Jose Garcia-Arraras, John H. Henson, Taku Hibino, Zoe H. Irons, Chun Li, Cheng Man Lun, Audrey J. Majeske, Matan Oren, Patrizia Pagliara, Annalisa Pinsino, David A. Raftos, Jonathan P. Rast, Bakary Samasa, Domenico Schillaci, Catherine S. Schrankel, Loredana Stabili, Klara Stensväg, and Elisse Sutton Echinoderm Life History and Phylogeny Echinoderms are benthic marine invertebrates living in communities ranging from shallow nearshore waters to the abyssal depths. Often members of this phylum are top predators or herbivores that shape and/or control the ecological characteristics All co-authors contributed equally to this chapter and are listed in alphabetical order. L. C. Smith (*) · M. A. Barela Hudgell · K. M. Buckley Department of Biological Sciences, George Washington University, Washington, DC, USA e-mail: [email protected] V. Arizza · G. Barone · D. Schillaci Department of Biological, Chemical and Pharmaceutical Sciences and Technologies (STEBICEF), University of Palermo, Palermo, Italy A. G. Bodnar Bermuda Institute of Ocean Sciences, St. George’s Island, Bermuda Gloucester Marine Genomics Institute, Gloucester, MA, USA V. Cunsolo Department of Chemical Sciences, University of Catania, Catania, Italy N. M. Dheilly School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY, USA N. Franchi Department of Biology, University of Padova, Padua, Italy © Springer International Publishing AG, part of Springer Nature 2018 409 E. L. Cooper (ed.), Advances in Comparative Immunology, https://doi.org/10.1007/978-3-319-76768-0_13 410 L. C. Smith et al. of their habitats. Five classes are defined within echinoderms: Crinoidea (sea lilies and feather stars), Ophiuroidea (brittle stars), Asteroidea (sea stars and sea daisies), Holothuroidea (sea cucumbers), and Echinoidea (sea urchins and sand dollars) (Fig. 1a–e). As a consequence of rapid divergence that occurred shortly after the origin of the echinoderm phyla, which emerged an estimated 570 million years ago (Pisani et al. 2012), the phylogenetic relationships among the classes have been dif- ficult to establish, and vary depending on the data set and phylogenetic methods (Fig. 1f) (Janies et al. 2011). Crinoids are unequivocally the basal group, whereas the monophyly of asteroids and ophiuroids remains in debate. The Echinodermata and Hemichordata phyla constitute the Ambulacraria, which is the basal group S. D. Fugmann Department of Biomedical Sciences and the Chang Gung Immunology Consortium, Chang Gung Memorial Hospital, Chang Gung University, Tao-Yuan City, Taiwan R. Furukawa Department of Biology, Research and Education Center for Natural Sciences, Keio University, Kanagawa, Japan J. Garcia-Arraras Department of Biology, University of Puerto Rico, San Juan, Puerto Rico J. H. Henson · Z. H. Irons · B. Samasa Department of Biology, Dickinson College, Carlisle, PA, USA T. Hibino Faculty of Education, Saitama University, Saitama, Japan C. Li Marbio, UiT The Arctic University of Norway, Forskningsparken, Tromsø, Norway C. M. Lun Department of Biological Sciences, George Washington University, Washington, DC, USA Virus-Cell Interaction Section, HIV Dynamics and Replication Program, Center for Cancer Research, National Cancer Institute, Frederick, MD, USA A. J. Majeske Department of Biology, University of Puerto Rico at Mayagüez, Mayagüez, Puerto Rico M. Oren Department of Biological Sciences, George Washington University, Washington, DC, USA Department of Molecular Biology, Ariel University, Ariel, Israel P. Pagliara Department of Biological and Environmental Sciences and Technologies, University of Salento, Lecce, Italy A. Pinsino Consiglio Nazionale delle Ricerche, Istituto di Biomedicina e Immunologia Molecolare “A. Monroy”, Palermo, Italy D. A. Raftos · E. Sutton Department of Biological Sciences, Macquarie University, Sydney, NSW, Australia Echinodermata: The Complex Immune System in Echinoderms 411 within the deuterostome lineage (Blair and Hedges 2005) and sister to the chordates (Fig. 1g). The nearly 8000 extant echinoderms (from the Greek, meaning “spiny skin”) share several aspects of life cycle and body plan. Most echinoderm species develop indirectly through a dispersal-stage planktonic larva, which exhibits bilat- eral symmetry and swims and feeds through the activities of surface cilia and the ciliary band. Metamorphosis occurs when the larva descends to the benthos from the littoral zone and everts the adult rudiment into a juvenile with five spines and five tube feet. Most adults share the characteristics of a radial body plan with pen- tameral symmetry, a rigid calcite endoskeleton, and a water vascular system that functions as a hydraulic mechanism for tube foot extension and locomotion, sensory activity (including responses to light/dark (Ullrich-Lüter et al. 2011), and food cap- ture (Hyman 1955). Early Evidence for Echinoderm Immune Responses Allograft Rejection Defines an Innate Immune System in Echinoderms For centuries, the prevailing theory was that animals without backbones lacked immune systems. Invertebrates infected with pathogens either recovered or were deleted from the gene pool, and populations remained at steady state as a conse- quence of a large number of offspring. When this assumption was first challenged, the most straightforward strategy to identify immune responses in echinoderms was to use allograft rejection experiments designed to determine whether individuals could differentiate between self and nonself. When skin allografts and autografts were transplanted among individuals of the sea star Dermasterias imbricata, allografts were always rejected, whereas autografts were accepted and healed into the grafted site (Fig. 2a, b) (Hildemann and Dix 1972; Karp and Hildemann 1976). J. P. Rast Sunnybrook Research Institute, University of Toronto, Toronto, ON, Canada Department of Immunology, University of Toronto, Toronto, ON, Canada Department of Pathology and Laboratory Medicine, Emory University School of Medicine, Atlanta, GA, USA C. S. Schrankel Department of Immunology, University of Toronto, Toronto, ON, Canada Marine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA, USA L. Stabili National Research Council, Institute for Coastal Marine Environment, Taranto, Italy K. Stensväg Norwegian College of Fishery Science, Faculty of Biosciences, Fisheries and Economics, UiT The Arctic University of Norway, Breivika, Tromsø, Norway 412 L. C. Smith et al. Similar experiments using body wall transplants demonstrated that nonself- recognition mechanisms are also present in the white sea urchin Lytechinus pictus (Coffaro and Hinegardner 1977). Although the kinetics of the second-set allograft rejections are significantly faster than the first-set rejections in this species, the kinetics of first-set versus third-party rejections are identical, suggesting a lack of specific immune memory (Fig. 2c) (Smith and Davidson 1992). This demonstrated that echinoderms have an immune system that is efficient for host protection, but that it functions with innate mechanisms in the absence of adaptive capabilities. Foreign Particles Are Cleared Rapidly from the Coelomic Cavity The use of allograft rejection to demonstrate immune capabilities in echinoderms, albeit effective, is an artificial experimental approach. Unlike the well-established systems in colonial tunicates and hydroids (Nydam and DeTomaso 2011; Rosengarten and Nicotra 2011; Taketa and DeTomaso 2015), natural allografts do not occur in echinoderms. As an alternative approach to assess nonself recognition capacity, echinoderms have been evaluated for their abilities to clear foreign parti- cles and cells injected into their coelomic cavity. A wide range of particles and molecules have been employed in these studies, including foreign proteins, T4 bac- teriophage, carbon particles, carmine, Sephadex, and latex beads, which are all cleared effectively (reviewed in Smith and Davidson (1994)). In response to injec- tion with sheep red blood cells (RBCs), the sea cucumber Holothuroidea polii clears these cells within 8 days, which correlates with the appearance of dark brown bod- ies in the coelomic cavity (Canicatti and D’Ancona 1989). These bodies are consis- tent with aggregates of hemoglobin from the RBCs encapsulated by coelomocytes that have activated phenoloxidase activity and melanin production. In the sea urchin Strongylocentrotus nudus, intracoelomic injection of sheep RBCs is followed by the production of reactive oxygen intermediates (Ito et al. 1992). Furthermore, the rate of RBC phagocytosis is increased as a consequence of preincubation or opsoniza- tion with Strongylocentrotus nudus coelomic fluid (CF). Echinoderms also respond to foreign cells from other species within the phylum, and the injection of coelomo- cytes from the sea urchin Arbacia punctulata into the sea star Asterias forbesi results in the swift clearance of the sea urchin cells and corresponds to a transient decrease in the sea star coelomocytes (Reinisch and Bang 1971). A more Fig. 1 (continued) Patiria miniata. (e) The Ophiuroidea are represented by the brittle star Amphiura filiformis. (Reprinted from Arnone et al. (2015).) (f) There are two possible relationships among the