Abstract
Ascidians form a widespread marine invertebrate group and are heterogeneous in terms of the taxonomic groups’ evolutionary lineages. The ascidian genomes lack significant homologies for rearranging genes of the vertebrate adoptive immunity. Genome analysis, gene sequencing, and transcriptional profiling have allowed us to disclose upregulation of innate immunity genes and cell labeling with riboprobes and antibodies has identified hemocyte types in tunic and pharynx inflammatory responses. Lymphocyte-like cells are stem cells and their immunocompetence has been proposed. Granulocyte types (compartment/morula cells) and hemocytes with large granules/vacuoles (compartment/morula cells) are mature cells expressing and releasing inflammatory components. LPS stimulates gene families of innate immune receptor homologs of the mammalian counterparts, as well as immune regulatory genes, during inflammatory responses. Proinflammatory components are involved in allogeneic reactions, and nonself and missing-self recognitions may be proposed. The findings on Ig-like domains contained in chitin-binding proteins (VCBPs) indicate the ancestral origin of vertebrate adaptive immunity and show that relevant genetic circuitry was already in place in the common ancestor of the protochordates and vertebrates. On the other hand, ascidians share with the other invertebrates the prophenoloxidase system that produces melanin and is involved in the inflammatory cytotoxic mechanism. The peroxinectin gene is also upregulated. Damage signals could be proinflammatory, but there are difficulties in assessing this that presumably could be examined during larva metamorphosis.
Findings indicate that genetic circuitries relevant for vertebrate innate immunity were already in place in the common ancestor of the protochordates and vertebrates.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Ajjan RA, Watson PF, Weetman AP (1996) Cytokines and thyroid function. Adv Neuroimmunol 6:359–386
Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4:499–511
Amparyup P, Sutthangkul J, Charoensapsri W et al (2012) Pattern recognition protein binds to lipopolysaccharide and β-1,3-glucan and activates shrimp prophenoloxidase system. J Biol Chem 287:10060–10069
Anderson RS (1971) Cellular responses to foreign bodies in the tunicate Mogula manhattensis (DeKay). Biol Bull 141:91–98
Arizza V, Parrinello D (2009) Inflammatory hemocytes in Ciona intestinalis innate immune response. Invertebr Surviv J 6:S58–S66
Arizza V, Cammarata M, Tomasino MC et al (1995) Phenoloxidase characterization in vacuolar hemocytes from the solitary ascidians Styela plicata. J Invertebr Pathol 66:297–302
Arizza V, Parrinello D, Cammarata M et al (2011) A lytic mechanism based on soluble phospholypases A2 (sPLA2) and β-galactoside specific lectins is exerted by Ciona intestinalis (ascidian) unilocular refractile hemocytes against K562 cell line and mammalian erythrocytes. Fish Shellfish Immunol 30:1014–1023
Armstrong PB (2010) Role of α2-macroglobulin in the immune responses of invertebrates. Invertebr Surviv J 7:165–180
Asea A, Rehli M, Kabingu E et al (2002) Novel signal transduction pathway utilized by extracellular HSP70: role of Toll-like receptor (TLR) 2 and TLR4. J Biol Chem 277:15028–15034
Ashley NT, Zachary M, Weil RJ et al (2012) Inflammation: mechanisms, costs, and natural variation. Annu Rev Ecol Evol Syst 43:385–406
Azumi K, De Santis R, De Tomaso AW et al (2003) Genomic analysis of immunity in a urochordate and the emergence of the vertebrate immune system: “waiting for Godot”. Immunogenetics 55:570–581
Azumi K, Sabau SV, Fujie M et al (2007) Gene expression profile during the life cycle of the urochordate Ciona intestinalis. Dev Biol 308:572–582
Anderson P (2010) Post-transcriptional regulons coordinate the initiation and resolution of inflammation. Nat Rev 10:24–35
Ballarin L (2008) Immunobiology of compound ascidians, with particular reference to Botryllus schlosseri: state of art. Invertebr Surviv J 5:54–74
Ballarin L, Cima F (1998) Phenoloxidase and cytotoxicity in the compound ascidian Botryllus schlosseri. Dev Comp Immunol 22:479–492
Ballarin L, Cima F (2005) Cytochemical properties of Botryllus schlosseri haemocytes: indications for morpho-functional characterisation. Eur J Histochem 49:255–264
Ballarin L, Zaniolo G (2007) Colony specificity in Botrylloides leachi. II. Cellular aspects of the non-fusion reaction. Invertebr Surviv J 4:38–44
Ballarin L, Cima F, Sabbadin A (1994) Phenoloxidase in the colonial ascidian Botryllus schlosseri (Urochordata, Ascidiacea). Anim Biol 3:41–48
Ballarin L, Cima F, Floreani M et al (2002) Oxidative stress induces cytotoxicity during rejection reaction in the compound ascidian Botryllus schlosseri. Comp Biochem Physiol 133C:411–418
Ballarin L, Cammarata M, Franchi N et al (2013) Routes in innate immunity evolution: galectins and rhamnose-binding lectins in ascidians. In: Kim S-K (ed) Marine proteins and peptides: biological activities and applications. John Wiley & Sons, Ltd, Hoboken
Barnum SR (2015) C4a: an anaphylatoxin in name only. J Innate Immun 7:333–339
Bartel Y, Bauer B, Steinle A (2013) Modulation of NK cell function by genetically coupled C-type lectin–like receptor/ligand pairs encoded in the human natural killer gene complex. Front Immunol 4:362. https://doi.org/10.3389/fimmu.2013.00362
Beck G, Habicht GS (1991) Purification and biochemical characterization of an invertebrate interleukin-1. Mol Immunol 28:577–584
Beck G, Vasta R, Marchalonis J, Habicht GS (1989a) Characterization of interleukin-1 activity in tunicates. Comp Biochem Physiol 92B:93–98
Beck G, O'Brien RF, Habicht GS (1989b) Invertebrate cytokines: the phylogenetic emergence of interleukin-1. BioEssays 11:62–67
Beck G, O'Brien RF, Habicht GS, Stillman DL, Cooper EL, Raftos DA (1993) Invertebrate cytokines. III: Invertebrate interleukin-1-like molecules stimulate phagocytosis by tunicate and echinoderm cells. Cell Immunol 146:284–299
Berná L, Alvarez-Valin F (2014) Evolutionary genomics of fast evolving tunicates. Genome Biol Evol 6:1724–1738
Bianchet MA, Ahmed H, Vasta GR, Amzel LM (2008) Structural aspects of lectin–ligand interactions. In: Vasta GR, Ahmed H (eds) Animal lectins: a functional view. CRC Press Taylor & Francis Group, England, pp 17–31
Bianchi ME (2007) DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 81:1–5
Bierhaus AJ, Chen B, Liliensiek B et al (2000) LPS and cytokine activated endothelium. Semin Thromb Hemost 26:571–587
Billack B (2006) Macrophage activation: role of Toll-like receptors, nitric oxide, and nuclear factor kappa B. Amer J Pharm Edu 70:102. PMC1637021
Bishop CD, Bates WR, Brandhorst BP (2001) Regulation of metamorphosis in ascidians involves NO/cGMP signaling and HSP90. J Exp Zool 289:374–384
Bobó J, Pál G, Cerkenak L et al (2016) The emerging roles of mannose-binding lectin–associated serine proteases (MASPs) in the lectin pathway of complement and beyond. Immunol Rev 274:98–111
Bock DG, MacIsaac HJ, Cristescu ME (2012) Multilocus genetic analyses differentiate between widespread and spatially restricted cryptic species in a model ascidian. Proc Roy Soc Lond B. https://doi.org/10.1098/rspb.2011.2610
Bodmer JL, Schneider P, Tschopp J (2002) The molecular architecture of the TNF superfamily. Trends Biochem Sci 27:19–26
Bonura A, Vizzini A, Salerno G et al (2009) Isolation and expression of a novel MBL-like collectin cDNA enhanced by LPS injection in the body wall of the ascidian Ciona intestinalis. Mol Immunol 46:2389–2394
Bonura A, Vizzini A, Salerno G, Parrinello D, Parrinello N, Longo V, Montana G, Colombo P (2010) Cloning and expression of a novel component of the CAP superfamily enhanced in the inflammatory response to LPS of the ascidian Ciona intestinalis. Cell Tissue Res 342(3):411–421
Borrego F, Masilamani M, Kabat J et al (2005) The cell biology of the human natural killer cell CD94/NKG2A inhibitory receptor. Mol Immunol 42:485–488
Botos I, Segal DM, Davies DR (2011) The structural biology of Toll-like receptors. Structure 19:447–495
Boyington JC, Riaz AN, Patamawenu A et al (1999) Structure of CD94 reveals a novel C-type lectin fold: implications for the NK cell–associated CD94/NKG2 receptors. Immunity 10:75–82
Brocker C, Thompson D, Matsumoto A et al (2010) Evolutionary divergence and functions of the human interleukin (IL) gene family. Hum Genomics 5:30–55
Brown GD, Gordon S (2001) Immune recognition. A new receptor for beta-glucans. Nature 413:36–37
Brown FD, Tiozzo S, Roux MM, Ishizuka K et al (2009) Early lineage specification of long-lived germline precursors in the colonial ascidian Botryllus schlosseri. Development 136:3485–3494
Buchmann K (2014) Evolution of innate immunity: clues from invertebrates via fish to mammals. Front Immunol 5:459. https://doi.org/10.3389/fimmu.2014.00459
Burighel P, Cloney RA (1997) Urochordata: ascidiacea. In: Harrison FW, Ruppert EE (eds) Microscopic anatomy of invertebrates, vol 15. Wiley-Liss Inc, New York, pp 221–347
Calderwood SK, Murshid A, Gong J (2012) Heat shock proteins: conditional mediators of inflammation in tumor immunity. Front Immunol 3:75. https://doi.org/10.3389/fimmu.2012.00075
Cambi A, Figdor CG (2003) Dual function of C-type lectin–like receptors in the immune system. Curr Opin Cell Biol 15:539–546
Cammarata M, Parrinello N (2009) The ascidian prophenoloxidase activating system. Invert Surv J 6:S67–S76
Cammarata M, Arizza V, Parrinello N et al (1997) Phenoloxidase-dependent cytotoxic mechanism in ascidian (Styela plicata) hemocytes active against erythrocytes and K562 cells. Eur J Cell Biol 74:302–307
Cammarata M, Arizza V, Savona B et al (1999) Prophenoloxidase in the hemocyte of Phallusia mamillata. Anim Biol 8:15–17
Cammarata M, Arizza V, Cianciolo C et al (2008) The prophenoloxidase system is activated during the tunic inflammatory reaction of Ciona intestinalis. Cell Tissue Res 333:481–492
Cammarata M, Parisi M, Benenati G, Vasta G, Parrinello N (2014) A rhamnose-binding lectin from sea bass (Dicentrarchus labrax) plasma agglutinates and opsonizes pathogenic bacteria. Dev Comp Immunol 44:332–340
Cannon JP, Haire RN, Litman GW (2002) Identification of diversified genes that contain immunoglobulin-like variable regions in a protochordate. Nat Immunol 3(12):1200–1207
Cannon JP, Haire RN, Schnitker N, Mueller MG, Litman GW (2004) Individual protochordates have unique immune-type receptor repertoires. Curr Biol 14(12):R465–R466
Caputi L, Andreakis N, Mastrototaro F et al (2007) Cryptic speciation in a model invertebrate chordate. PNAS 104:9364–9369
Cerenius L, Lee BL, Söderhäll K (2008) The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol 29:263–271
Cha IS, Segovia del Castillo C, Nho SW et al (2011) Innate immune response in the hemolymph of an ascidian, Halocynthia roretzi, showing soft tunic syndrome, using label-free quantitative proteomics. Dev Comp Immunol 35:809–816
Chaga OY (1980) Ortho-diphenoloxidase system of ascidians. Tsitologia 22:619–625
Chambon J-P, Soule J, Pomies P et al (2002) Tail regression in Ciona intestinalis (prochordate) involves a Caspase dependent apoptosis event associated with ERK activation. Development 129:3105–3114
Chambon JP, Nakayama A, Takamura K et al (2007) ERK-and JNK-signalling regulate gene networks that stimulate metamorphosis and apoptosis in tail tissues of ascidian tadpoles. Development 134:1203–1219
Cima F, Perin A, Burighel P et al (2001) Morphofunctional characterisation of haemocytes of the compound ascidian Botrylloides leachi (Tunicata, Ascidiacea). Acta Zool 82:261–274
Cima F, Basso G, Ballarin L (2003) Apoptosis and phosphatidylserine-mediated recognition during the take-over phase of the colonial life-cycle in the ascidian Botryllus schlosseri. Cell Tissue Res 312:369–376
Cima F, Sabbadin A, Ballarin L (2004) Cellular aspects of allorecognition in the compound ascidian Botryllus schlosseri. Dev Comp Immunol 28:881–889
Cima F, Manni L, Basso G et al (2010) Hovering between death and life: natural apoptosis and phagocytes in the blastogenetic cycle of the colonial ascidian Botryllus schlosseri. Dev Comp Immunol 34:272–285
Cima F, Franchi N, Ballarin L (2016) Origin and function of tunicate hemocytes. In: Malagoli D (ed) The evolution of the immune system. Elsevier, London, pp 29–49
Cloney RA (1982) Ascidian larvae and the events of metamorphosis. Am Zool 22:817–826
Cloney RA, Grimm LM (1970) Transcellular emigration of blood cells during ascidian metamorphosis. Z Zellforsch 107:157–173
Comes S, Locascio A, Silvestre F et al (2007) Regulatory roles of nitric oxide during larval development and metamorphosis in Ciona intestinalis. Dev Biol 306:772–784
Cooper EL (1992) Overview of immunoevolution. Boll Zool 59:119–128
Cooper EL (2009) Putative stem cell origins in solitary tunicates. In: Rinkevich B, Matranga V (eds) Stem cells in marine organisms. Springer, Netherlands, pp 21–32
Cooper EL (2016) Commentary: blurring borders: innate immunity with adaptive features. Front Microbiol 7:358. https://doi.org/10.3389/fmicb.2016.00358
Cooper EL, Parrinello N (2001) Immunodefense in tunicates: cells and molecules. In: Sawada H, Yokosawa H, Lambert CC (eds) The biology of ascidians. Springer, Tokio, pp 383–394
Corey DM, Rosental B, Kowarsky M et al (2016) Developmental cell death programs license cytotoxic cells to eliminate histocompatible partners. Proc Natl Acad Sci U S A 113:6520–6525
Coscia MR, Giacomelli S, Oreste U (2011) Toll-like receptors: an overview from invertebrates to vertebrates. Invert Surv J 8:210–226
Cummings RD, McEver RP (2009) C-type lectins. In: Varki A, Cummings RD, Esko JD et al (eds) Essentials of glycobiology, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor. Chapter 31
Cummings RD, Schnaar RL, Esko JD et al. (2017) Principles of glycan recognition. In: Varki A, Cummings RD, Esko JD et al (eds) Essentials of glycobiology. 3rd edn. Cold Spring Harbor Laboratory Press Chapter 29. https://doi.org/10.1101/glycobiology.3e.029
Davidson B, Swalla BJ (2002) A molecular analysis of ascidian metamorphosis reveals activation of an innate immune response. Develop 129:4739–4751
De Barros CM, Andrade LR, Allodi S, Viskov C et al (2007) The hemolymph of the ascidian styela plicata (Chordata–Tunicata) contains heparin inside basophil-like cells and a unique sulfated galactoglucan in the plasma. J Biol Chem 282:1615–1626
De Leo G (1992) Ascidian hemocytes and their involvement in defence reactions. Boll Zool 59:195–213
Deck JD, Hay ED, Revel J-P (1966) Fine structure and origin of the tunic of Perophora viridis. J Morphol 120:267–280
Dehal P, Satou Y, Campbell RK et al (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2167
De Leo G, Parrinello N, Parrinello D et al (1997) Encapsulation response of Ciona intestinalis (Ascidiacea) to intratunic erythrocyte injection. J Invertebr Pathol 69:14–23
de Leo G, Parrinello N, Parrinello D, Cassara’ G, di Bella MA (1996) Encapsulation response of Ciona intestinalis (Ascidiacea) to intratunical erythrocyte injection. J Invertebr Pathol 67(3):205–212
Delsuc F, Brinkmann H, Chourrout D et al (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965–968
Delsuc F, Tsagkogeorga G, Lartillot N, Philippe H (2008) Additional molecular support for the new chordate phylogeny. Genesis 46:592–594
Di Bella MA, Cassarà G, Russo D et al (1998) Cellular components and tunic architecture of the solitary ascidian Styela canopus (Stolidobranchiata, Styelidae). Tissue Cell 30:352–359
Di Bella MA, Carbone MC, De Leo G (2005) Aspects of cell production in mantle tissue of Ciona intestinalis L. (Tunicata, Ascidiacea). Micron 36:477–481
Di Bella MA, Carbone MC, D’Amato M et al (2009) The identification and localization of two intermediate filament proteins in the tunic of Styela plicata (Tunicata, Styelidae). Tissue Cell 41:381–389
Di Bella MA, Fedders H, De Leo G et al (2011) Localization of antimicrobial peptides in the tunic of Ciona intestinalis (Ascidiacea, Tunicata) and their involvement in local inflammatory-like reactions. Results Immunol 1:70–75
Di Bella MA, Carbone MC, De Leo G (2015) Ultrastructural aspects of naturally occurring wound in the tunic of two ascidians: Ciona intestinalis and Styela plicata (Tunicata). Micron 69:6–14
Di Bella MA, De Leo G (2000) Hemocyte migration during Inflammatory-like reaction of Ciona intestinalis (Tunicata, Ascidiacea). J Invertebr Pathol 76(2):105–111
Di Giammartino DC, Nishida K, Manley JL (2011) Mechanisms and consequences of alternative polyadenylation. Mol Cell 43:853–866
Dinarello CA (2007) Historical review of cytokines. Eur J Immunol 37:S34–S45
Dinasarapu AR, Chandrasekhar A, Fujita T et al (2013) Mannose/mannan-binding lectin. UCSD Molecule 2:8–18. https://doi.org/10.1155/2016/1245049
Dishaw LJ, Giacomelli S, Melillo D, Zucchetti I, Haire RN, Natale L, Russo NA, De Santis R, Litman GW, Pinto MR (2011) A role for variable region-containing chitin-binding proteins (VCBPs) in host gut-bacteria interactions. Proc Natl Acad Sci 108(40):16747–16752
Dishaw LJ, Leigh B, Cannon JP et al (2016) Gut immunity in a protochordate involves a secreted immunoglobulin-type mediator binding host chitin and bacteria. Nat Commun 7:10617
Donaghy L, Hong HK, Park KI et al (2017) Flow cytometric characterization of hemocytes of the solitary ascidian, Halocynthia roretzi. Fish Shellfish Immunol 66:289–299
Dong B, Liu F, Gao H et al (2009) CDNA cloning and gene expression pattern following bacterial challenge of peroxinectin in Chinese shrimp Fenneropenaeus chinensis. Mol Biol Rep 36:2333–2339
Drickamer K, Fadden AJ (2002) Genomic analysis of C-type lectins. Biochem Soc Symp 69:59–72
Drickamer K, Taylor ME (2015) Recent insights into structures and functions of C-type lectins in the immune system. Curr Opin Struct Biol 34:26–34
Du Clos TW (2013) Pentraxins: structure, function, and role in inflammation. ISRN Inflamm 2013:1–22
Du Pasquier L (2004) Innate immunity in early chordates and the appearance of adaptive immunity. C R Biol 327:591–601
Di Meo S, Reed TT, Venditti P et al (2016) Role of ROS and RNS sources in physiological and pathological conditions. Oxidative Med Cell Longev 2016:1–44
East L, Isacke CM (2002) The mannose receptor family. Biochim Biophys Acta 1572:364–386
Elkon R, Ugalde AP, Agami R (2013) Alternative cleavage and polyadenylation: extent, regulation and function. Nat Rev Genet 14:496–506
Elliot MR, Ravochandran KS (2010) Clearance of apoptotic cells: implications in health and diseases. J Cell Biol 189:1059–1070
Endean R (1961) The test of the ascidian, Phallusia mammillata. Quart J Microsc Sci 102:107–117
Ermak TH (1975a) Cell proliferation in the ascidian Styela clava: an autoradiographic and electron microscopic investigation emphasizing cell renewal in the digestive tract of this and fourteen other species of ascidians. PhD Diss – Univ Cal, San Diego
Ermak TH (1975b) An autoradiographic demonstration of blood cell renewal in Styela clava (Urochordata: Ascidiacea). Experientia 31:837–838
Ermak TH (1976) The hematogenic tissues of tunicates. In: Wright RK, Cooper EL (eds) Phylogeny of thymus and bone marrow-bursa cells. Elsevier, Amsterdam, pp 45–56
Ermak TH (1982) The renewing cell populations of ascidians. Am Zool 22:795–805
Esposito R, D’Aniello S, Squarzoni P et al (2012) New insights into the evolution of metazoan tyrosinase gene family. PLoS One 74:1–10
Ewan R, Huxley-Jones J, Mould AP et al (2005) The integrins of the urochordate Ciona intestinalis provide novel insights into the molecular evolution of the vertebrate integrin family. BMC Evol Biol 5:1–18
Fedders H, Leippe M (2008) A reverse search for antimicrobial peptides in Ciona intestinalis: identification of a gene family expressed in hemocytes and evaluation of activity. Dev Comp Immunol 32:286–298
Fox PL (2015) Discovery and investigation of the GAIT translational control system. RNA 21:615–618
Franchi N, Ballarin L (2014) Preliminary characterization of complement in a colonial tunicate: C3, Bf and inhibition of C3 opsonic activity by compstatin. Dev Comp Immunol 46(2):430–438
Franchi N, Ballarin L (2016) Cytotoxic cells of compound ascidians. In: Ballarin L, Cammarata M (eds) Lessons in immunity: from single-cell organisms to mammals. Elsevier, London, pp 193–203
Franchi N, Ballarin L (2017) Morula cells as key hemocytes of the lectin pathway of complement activation in the colonial tunicate Botryllus schlosseri. Fish Shellfish Immunol 63:157–164
Fugmann SD (2010) The origins of the RAG genes—from transposition to V(D)J recombination. Semin Immunol 22:10–16
Fugmann SD, Messier C, Novack LA et al (2006) An ancient evolutionary origin of the Rag1/2 gene locus. Proc Natl Acad Sci U S A 103:3728–3733
Fujikawa T, Munakata T, S-i K et al (2010) Stress response in the ascidian Ciona intestinalis: transcriptional profiling of genes for the heat shock protein 70 chaperone system under heat stress and endoplasmic reticulum stress. Cell Stress Chaperones 15:193–204
Fujita H, Sawano F (1979) Fine structural localization of endogenous peroxidase in the endostyle of ascidians, Ciona intestinalis. A part of phylogenetic studies of the thyroid gland. Arch Histol Jpn 42:319–326
Fujita T, Endo Y, Nonaka M (2004a) Primitive complement system—recognition and activation. Mol Immunol 41:103–111
Fujita T, Matsushita M, Endo Y (2004b) The lectin–complement pathway—its role in innate immunity and evolution. Immunol Rev 198:346–353
Fuke MT (1980) “Contact reaction” between xenogeneic or allogeneic celomic cells of solitary ascidians. Biol Bull 158:304–315
Futosi K, Fodor S, Mócsai A (2013) Neutrophil cell surface receptors and their intracellular signal transduction pathways. Int Immunopharmacol 17:638–650
Gallucci S, Matzinger P (2001) Danger signals: SOS to the immune system. Curr Opin Immunol 13:114–119
Gasparini F, Franchi N, Spolaore B et al (2008) Novel rhamnose-binding lectins from the colonial ascidian Botryllus schlosseri. Dev Comp Immunol 32:1177–1191
Giacomelli S, Melillo D, Lambris JD et al (2012) Immune competence of the Ciona intestinalis pharynx: complement system-mediate activity. Fish Shellfish Immunol 33:946–952
Gibbs GM, Roelants K, O’Bryan MK (2008) The CAP superfamily: cysteine-rich secretory proteins, antigen 5, and pathogenesis-related 1 proteins—roles in reproduction, cancer, and immune defense. Endocr Rev 29:865–897
Gijtenbeel TBH, Inghuis GR (2009) Signalling through C-type lectin receptors: shaping immune responses. Nat Rev Immunol 9:465–479
Goetz FW, Planas JV, MacKenzie S (2004) Tumor necrosis factors. Dev Comp Immunol 28:487–497
Green PL, Nair SV, Raftos DA (2003) Secretion of a collectin-like protein in tunicates enhanced during inflammatory responses. Dev Comp Immunol 27:3–9
Gu C, Wu L, Li X (2013) IL-17 family: cytokines, receptors and signaling. Cytokine 64:477–485
Guilliams M, Ginhoux F, Jakubzick C et al (2014) Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat Rev Immunol 14:571–578
Gupta G, Surolia A (2007) Collectins: sentinels of innate immunity. BioEssays 29:452–464
Hansen JD, Vojtech LN, Laing KJ (2011) Sensing disease and danger: a survey of vertebrate PRRs and their origins. Dev Comp Immunol 35:886–897
Hata S, Azumi K, Yokosawa H (1998) Ascidian phenoloxidase: its release from hemocytes, isolation, characterization and physiological roles. Comp Biochem Physiol 119:769–776
Hibino T, Loza-Coll M, Messier C et al (2006) The immune gene repertoire encoded in the purple sea urchin genome. Dev Biol 300:349–365
Hirose E (2009) Ascidian tunic cells: morphology and functional diversity of free cells outside the epidermis. Invertebr Biol 128:83–96
Hirose E, Ishii T, Saito Y, Taneda Y (1994) Phagocytic activity of tunic cells in the colonial ascidian Aplidium yamazii (Polyclinidae, Aplousobranchia). Zool Sci 11:203–208
Hirsiger S, Simmen H-P, Werner CML et al (2012) Danger signals activating the immune response after trauma. Mediators Inflamm 315941:10. https://doi.org/10.1155/2012/315941
Houzelstein D, Goncalves IR, Fadden AJ et al (2004) Phylogenetic analysis of the vertebrate galectin family. Mol Biol Evol 21:1177–1187
Hoving JC, Wilson GJ, Brown GD (2014) Signalling C-type lectin receptors, microbial recognition and immunity. Cell Microbiol 16:185–194
Hsu PI, Liu CH, Tseng DY et al (2006) Molecular cloning and characterisation of peroxinectin, a cell adhesion molecule, from the giant freshwater prawn Macrobrachium rosenbergii. Fish Shellfish Immunol 21:1–10
Huang S, Yuan S, Guo L et al (2008) Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity. Genome Res 18:1112–1126
Hughes TK, Smith EM, Chin R et al (1990) Interaction of immunoactive monokines (interleukin 1 and tumor necrosis factor) in the bivalve mollusc Mytilus edulis. Proc Natl Acad Sci U S A 87:4426–4429
Huminiecki L, Goldovsky L, Freilich S et al (2009) Emergence, development and diversification of the TGF-b signalling pathway within the animal kingdom. BMC Evol Biol 3:9–28
Idriss TH, Naismith JH (2000) TNF alpha and the TNF receptor superfamily: structure function relationship(s). Microsc Res Tech 1:184–195
Immesberger A, Burmester T (2004) Putative phenoloxidases in the tunicate Ciona intestinalis and the origin of the arthropod hemocyanin superfamily. J Comp Physiol B 174:169–180
Inoue J, Ishida T, Tsukamoto N et al (2000) Tumor necrosis factor receptor–associated factor (TRAF) family: adapter proteins that mediate cytokine signaling. Exp Cell Res 254:142–144
Ip EWK, Takahashi K, Ezekowitz AR et al (2009) Mannose-binding lectin and innate immunity. Immunol Rev 230:9–21
Iwanaga S, Lee BL (2005) Recent advances in the innate immunity of invertebrate animals. J Biochem Mol Biol 38:128–150
Jackson AD, Smith VJ, Peddie CM (1993) In vitro phenoloxidase activity in the blood of Ciona intestinalis and other ascidians. Dev Comp Immunol 17:97–108
Janeway CA Jr, Travers P, Walport M et al (2001) Immunobiology: the immune system in health and disease. Receptors of the innate immune system, 5th edn. Garland Science, New York. Available from: https://www.ncbi.nlm.nih.gov/books/NBK27110/
Jensen LE, Whitehead AS (2001) IRAK1b, a novel alternative splice variant of interleukin-1 receptor associated kinase (IRAK), mediates interleukin-1 signaling and has prolonged stability. J Biol Chem 276:29037–29044
Ji X, Azumi K, Sasaki M, Nonaka M (1997) Ancient origin of the complement lectin pathway revealed by molecular cloning of mannan binding protein-associated serine protease from a urochordate, the Japanese ascidian, Halocynthia roretzi. Proc Natl Acad Sci 94(12):6340–6345
Jiang Y, Doolittle RF (2003) The evolution of vertebrate blood coagulation as viewed from a comparison of puffer fish and sea squirt genomes. Proc Natl Acad Sci U S A 100:7527–7532
Jimbo M, Usui R, Sakai R et al (2007) Purification, cloning and characterization of egg lectins from the teleost Tribolodon brandti. Comp Biochem Physiol 147B:164–171
Johansson MW, Lind MI, Holmblad T et al (1995) Peroxinectin, a novel cell adhesion protein from crayfish blood. Biochem Biophys Res Commun 216:1079–1087
Jouault T, Abed-El Behi ME, Martínez-Esparza M et al (2006) Specific recognition of Candida albicans by macrophages requires galectin-3 to discriminate Saccharomyces cerevisiae and needs association with TLR2 for signaling. J Immunol 177:4679–4687
Johansson MW (1999) Cell adhesion molecules in invertebrate immunity. Dev Comp Immunol 23:303–315
Johansson MW, Söderhäll K (1989) A cell adhesion factor from crayfish haemocytes has degranulating activity towards crayfish granular cells. Insect Biochem 19(2):183–190
Kamesh N, Aradhyam GK, Manoj N (2008) The repertoire of G protein-coupled receptors in the sea squirt Ciona intestinalis. BMC Evol Biol 8:129 doi:10.1186/1471-2148-8-129://www.biomedcentral.com/1471-2148/8/129
Kaczmarek A, Vandenabeele P, Krysko DV (2013) Necroptosis: the release of damage-associated molecular patterns and its physiological relevance. Immunity 38:209–223
Karpova AY, Ronco LV, Howley PM (2001) Functional characterization of interferon regulatory factor 3a (IRF3a), an alternative splice isoform of IRF3. Mol Cell Biol 21:4169–4176
Kawamura K, Sunanaga T (2010) Hemoblasts in colonial tunicates: are they stem cells or tissue-restricted progenitor cells? Develop Growth Differ 52:69–76
Kawashima A, Yamazaki K, Hara T et al (2013) Demonstration of innate immune responses in the thyroid gland: potential to sense danger and a possible trigger for autoimmune reactions. Thyroid 23:477–487
Kelley J, Walter L, Trowsdale J (2015) Comparative genomics of natural killer cell receptor gene clusters. PLoS Genet 1(2):e27. https://doi.org/10.1371/journal.pgen.0010027
Kelly KL, Cooper EL, Raftos DA (1992) In vitro allogeneic cytotoxicity in the solitary urochordate Styela clava. J Exp Zool 262:202–208
Kenjo A, Takahashi M, Matsushita M et al (2001) Cloning and characterization of novel ficolins from the solitary ascidian Halocynthia roretzi. J Biol Chem 276:19959–19965
Kerrigan AM, Brown GD (2009) C-type lectins and phagocytosis. Immunobiology 214:562–575
Khalturin K, Becker M, Rinkevich B, Bosch TCG (2003) Urochordates and the origin of natural killer cells: identification of a CD94/NKR-P1-related receptor in blood cells of Botryllus. PNAS 100:622–627
Kirkitadze M, Barlow P (2001) Structure and flexibility of the multiple domain proteins that regulate complement activation. Immunol Rev 180:146–161
Klebanoff JS (2005) Myeloperoxidase: friend and foe. J Leukoc Biol 77:598–625
Klyosov AA (2008) Galectins and their functions in plain language. In: Klyosov AA, Witczak ZJ, Platt D (eds) Galectins. Wiley & Sons, Hoboken, pp 9–32
Kobayashi M, Johansson MW, Söderhäll K (1990) The 76 kDa cell adhesion factor from crayfish haemocytes promotes encapsulation in vitro. Cell Tissue Res 260:113–118
Koh TJ, DiPietro LA (2011) Inflammation and wound healing: the role of the macrophage. Expert Rev Mol Med 13:e23. https://doi.org/10.1017/S1462399411001943
Kondos SC, Hatfaludi T, Voskoboinik I et al (2010) The structure and function of mammalian membrane-attack complex/perforin-like proteins. Tissue Antigens 76:341–351
Kono H, Rock KL (2008) How dying cells alert the immune system to danger. Nat Rev Immunol 8:279–289
Konrad MW (2016) Blood circulation in the ascidian tunicate Corella inflata (Corellidae). Wang L (ed) PeerJ 4:2771. https://doi.org/10.7717/peerj.2771
Kvell K, Cooper E, Engelmann P, Bovari J, Nemeth P (2007) Blurring borders: innate immunity with adaptive features. Clin Dev Immunol 2007:83671. https://doi.org/10.1155/2007/83671
Laird DJ, De Tomaso AW, Weissman IL (2005) Stem cells are units of natural selection in a colonial ascidian. Cell 123:1351–1360
Lauzon RJ, Ishizuka KJ, Weissman IL (1992) A cyclical, developmentally-regulated death phenomenon in a colonial urochordate. Dev Dyn 1941:71–83
Lauzon RJ, Brown C, Kerr L, Tiozzo S (2013) Phagocyte dynamics in a highly regenerative urochordate: insights into development and host defense Devel. Biol 374:357–373
Lemaitre B, Hoffmann J (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25:697–743
Levasseur A, Pontarotti P (2011) The role of duplications in the evolution of genomes highlights the need for evolutionary-based approaches in comparative genomics. Biol Direct 6:11. https://doi.org/10.1186/2F1745-6150-6-11
Li MO, Wan YY, Sanjabi S et al (2006) Transforming growth factor-b regulation of immune responses. Annu Rev Immunol 24:99–146
Li K, Fazekasova H, Wang N et al (2011) Expression of complement components, receptors and regulators by human dendritic cells. Mol Immunol 48:1121–1127
Linger RM, Keating AK, Earp HS, Graham DK (2008) TAM receptor tyrosine kinases: biologic functions, signaling, and potential therapeutic targeting in human cancer. Adv Cancer Res 100:35–83
Liu Y, Wang Y, Yamakuchi M et al (2001) Upregulation of Toll-like receptor 2 gene expression in macrophage response to peptidoglycan and high concentration of lipopolysaccharide is involved in NF-κB activation. Infect Immun 69:2788–2796
Liu CH, Cheng W, Chen JC (2005) The peroxinectin of white shrimp Litopenaeus vannamei is synthesised in the semi-granular and granular cells, and its transcription is up-regulated with Vibrio alginolyticus infection. Fish Shellfish Immunol 18:431–444
Liu CH, Yeh SP, Hsu PY, Cheng W (2007) Peroxinectin gene transcription of the giant freshwater prawn Macrobrachium rosenbergii under intrinsic, immunostimulant, and chemotherapeutant influences. Fish Shellfish Immunol 22:408–417
Liu FT, Hsu DK, Yang RY et al (2008) Galectins in regulation of inflammation and immunity. In: Klyosov AA, Witczak ZJ, Platt D (eds) Galectins. Wiley & Sons, Hoboken, pp 97–114
Liu FT, Yang RY, Hsu DK (2012) Galectins in acute and chronic inflammation. Ann N Y Acad Sci 1253:80–91
Locksley RM, Killeen N, Lenardo MJ (2001) The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104:487–501
López-Botet M, Carretero M, Pérez-Villar J et al (1997) The CD94/NKG2 C-type lectin receptor complex: involvement in NK cell-mediated recognition of HLA class I molecules. Immunol Rev 16:175–185
Lubbers R, van Essen MF, van Kooten C et al (2017) Production of complement components by cells of the immune system. Clin Exp Immunol 188:183–194
Lohr J, Knoechel B, Wang JJ, Villarino AV, Abbas AK (2006) Role of IL-17 and regulatory T lymphocytes in a systemic autoimmune disease. J Exp Med 203:2785–2791
MacKenzie S, Planas JV, Goetz FW (2003) LPS-stimulated expression of a tumor necrosis factor-alpha mRNA in primary trout monocytes and in vitro differentiated macrophages. Dev Comp Immunol 27:393–400
Mak TW, Saunders ME (2006) Innate immunity. In: Mak TW, Saunders ME (eds) The immune response. Basic and clinical principles. Elsevier Academic Press, Burligton MA USA, pp 69–92
Mantovani A, Biswas SK, Galdiero MR et al (2013) Macrophage plasticity and polarization in tissue repair and remodelling. J Pathol 229:176–185
Marino R, Pinto MR, Cotelli F, Lamia CL, De Santis R (1998) The hsp70 protein is involved in the acquisition of gamete self-sterility in the ascidian Ciona intestinalis. Development 125:899–907
Marino R, Kimura Y, DeSantis R et al (2002) Complement in urochordates: cloning and characterization of two C3-like genes in the ascidian Ciona intestinalis. Immunogenetics 53:1055–1064
Marshall ASJ, Gordon S (2004) C-type lectins on the macrophage cell surface—recent findings. Eur J Immunol 34:18–24
Martchenko M, Levitin A, Hogues H, Nantel A, Whiteway M (2007) Transcriptional rewiring of fungal galactose-metabolism circuitry. Curr Biol: CB 17(12). https://doi.org/10.1016/j.cub.2007.05.017
Massagué J, Gomis RR (2006) The logic of TGF-b signaling. FEBS Lett 580:2811–2820
Matsumoto J, Nakamoto C, Fujiwara S et al (2001) A novel C-type lectin regulating cell growth, cell adhesion and cell differentiation of the multipotent epithelium in budding tunicates. Development 128:3339–3347
Matsushita M, Fujita T (2001) Ficolins and the lectin complement pathway. Immunol Rev 180:78–85
Matsushita M, Endo Y, Fujita T (1998) MASP1 (MBL-associated serine protease 1). Immunobiology 199:340–347
Matsushita M, Endo Y, Fujita T (2000) Cutting edge: complement-activating complex of ficolin and mannose-binding lectin–associated serine protease. J Immunol 164:2281–2284
Matzinger P (1994) Tolerance, danger, and the extended family. Annu Rev Immunol 12:991–1045
Matzinger P (2002) The danger model: a renewed sense of self. Science 296:301–305
McKitrick TR, De Tomaso AW (2010) Molecular mechanisms of allorecognition in a basal chordate. Semin Immunol 22(1). https://doi.org/10.1016/j.smim.2009.12.001.
Meager A, Wadhwa M (2013) An overview of cytokine regulation of inflammation and immunity. In: eLS. John Wiley & Sons Ltd, Chichester
Medzhitov R (2008) Origin and physiological roles of inflammation. Nature 454:428–435
Melillo D, Sfyroera G, De Santis R et al (2006) First identification of a chemotactic receptor in an invertebrate species: structural and functional characterization of Ciona intestinalis C3a receptor. J Immunol 177:4132–4140
Menin A, Ballarin L (2010) Immunomodulatory molecules in the compound ascidian Botryllus schlosseri: evidence from conditioned media. Dev Comp Immunol 34:272–285
Menin A, Del Favero M, Cima F et al (2005) Release of phagocytosis-stimulating factor(s) by morula cells in a colonial ascidian. Mar Biol 148:225–230
Merle NS, Church SE, Fremeaux-Bacchi V et al (2015a) Complement system part I—molecular mechanisms of activation and regulation. Front Immunol 6:262. https://doi.org/10.3389/fimmu.2015.00262
Merle NS, Noe R, Halbwachs-Mecarelli L et al (2015b) Complement system part II: role in immunity. Front Immunol 6:257. https://doi.org/10.3389/fimmu.2015.00257
Metchnikoff E (1887) Sur la lutte des cellules de l'organisme contre l’invasion des microbes. Ann Inst Pasteur 1:321–345
Michel ML, Mendes-da-Cruz D, Keller AC et al (2008) Critical role of ROR-gammat in a new thymic pathway leading to IL-17-producing invariant NKT cell differentiation. Proc Natl Acad Sci U S A 105:19845–19850
Miyazawa S, Nonaka M (2004) Characterization of novel ascidian beta integrins as primitive complement receptor subunits. Immunogenetics 55:836–844
Miyazawa S, Azumi K, Nonaka M (2001) Cloning and characterization of integrin a subunits from the solitary ascidian, Halocynthia roretzi. J Immunol 166:1710–1715
Mogensen TH (2009) Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 22:240–273
Moodley Y, Rigby P, Bundell C et al (2003) Macrophage recognition and phagocytosis of apoptotic fibroblasts is critically dependent on fibroblast-derived thrombospondin 1 and CD36. Am J Pathol 162:771–779
Moreno E, Yan M, Basler K (2002) Evolution of TNF signaling mechanisms: JNK-dependent apoptosis triggered by Eiger, the Drosophila homolog of the TNF superfamily. Curr Biol 12:1263–1268
Nair SV, Pearce S, Green PL et al (2000) A collectin-like protein from tunicates. Comp Biochem Physiol 125B:279–289
Nair SV, Ramsden A, Raftos DA (2005) Ancient origins: complement in invertebrates. Invertebr Surviv J 2:114–123
Nappi AJ, Ottaviani E (2000) Cytotoxicity and cytotoxic molecules in invertebrates. BioEssays 22:469–480
Nappi AJ, Vass E (1993) Melanogenesis and the generation of cytotoxic molecules during insect cellular immune reactions. Pigment Cell Res 6:117–126
Nesargikar PN, Spiller B, Chavez R (2012) The complement system: history, pathways, cascade and inhibitors. Eur J Microbiol Immunol 2:103–111
Nesmelova IV, Dings RPM, Mayo KH (2008) Understanding galectin structure. Function relationships to design effective antagonists. In: Klyosov AA, Witczak ZJ, Platt D (eds) Galectins. Wiley & Sons, Hoboken, pp 33–70
Nonaka M (2014) Evolution of the complement system. In: Anderluh G, Gilbert R (eds) MACPF/CDC proteins—agents of defence, attack and invasion. Subcellular biochemistry, vol 80. Springer, Dordrecht, pp 31–43. https://doi.org/10.1007/978-94-017-8881-6
Nonaka M, Azumi K (1999) Opsonic complement system of the solitary ascidian Halocynthia roretzi. Dev Comp Immunol 23:421–427
Nonaka M, Kimura A (2006) Genomic view of the evolution of the complement system. Immunogenetics 58:701–713
Nonaka M, Satake H (2010) Urochordate immunity. In: Söderhall K (ed) Invertebrate immunity. Landes Bioscience and Springer Science, Boston, pp 302–310
Nonaka M, Yoshizaki F (2004) Primitive complement system of invertebrates. Immunol Rev 198:203–215
Nonaka M, Azumi K, Ji X et al (1999) Opsonic complement component C3 in the solitary ascidian Halocynthia roretzi. J Immunol 162:387–391
Norling LV, Perretti M, Cooper D (2009) Endogenous galectins and the control of the host inflammatory response. J Endocrinol 201:169–184
Nydam ML, Harrison RG (2007) Genealogical relationships within and among shallow-water Ciona species (Ascidiacea). Mar Biol 151:1839–1847
Nydam ML, Harrison RG (2011) Introgression despite substantial divergence in a broadcast spawning marine invertebrate. Evolution 65:429–442
Nydam ML, Hoang TA, Shanley KM, De Tomaso AW (2013) Molecular evolution of a polymorphic HSP40-like protein encoded in the histocompatibility locus of an invertebrate chordate. Dev Comp Immunol 41(2):128–136
Ogasawara M, Di Lauro R, Satoh N (1999) Ascidian homologs of mammalian thyroid peroxidase genes are expressed in the thyroid-equivalent region of the endostyle. J Exp Zool 285:158–169
Ogawa T, Watanabe M, Naganuma T, Muramoto K (2011) Diversified carbohydrate-binding lectins from marine resources. J Amino Acids 2011:838914, 20. https://doi.org/10.4061/2011/838914
Oren M, Douek J, Fishelson Z et al (2007) Identification of immune relevant genes in histoincompatible rejecting colonies of the tunicate Botryllus schlosseri. Dev Comp Immunol 31:889–902
Oren M, Escande M-l, Paz G et al (2008) Urochordate histoincompatible interactions activate vertebrate-like coagulation system components. PLoS One:3. https://doi.org/10.1371/journal.pone.0003123
Oren M, Paz G, Douek J et al (2013) Marine invertebrates cross phyla comparisons reveal highly conserved immune machinery. Immunobiology 218:484–495
Ottaviani E, Franchini A, Cassanelli S et al (1995) Cytokines and invertebrate immune responses. Biol Cell 85:87–91
Ottaviani E, Franchini A, Kletsas D et al (1996) Presence and role of cytokines and growth factors in invertebrates. Ital J Zool 63:317–323
Pancer Z, Gershon H, Rinkevich B (1995) Cloning of a urochordate cDNA featuring mammalian short consensus repeats (SCR) of complement-control protein superfamily. Comp Biochem Physiol 111B:625–632
Pancer Z, Diehl-Seifert B, Rinkevich B et al (1997) A novel tunicate (Botryllus schlosseri) putative C-type lectin features an immunoglobulin domain. DNA Cell Biol 16:801–806
Pandolfi F, Altamura S, Frosali S, Conti P (2016) Key role of DAMP in inflammation, cancer, and tissue repair. Clin Ther 38:1017–1028
Pappu R, Ramirez-Carrozzi V, Ota N et al (2010) The IL-17 family cytokines in immunity and disease. J Clin Immunol 30:185–195
Parker JS, Mizuguchi K, Gay NJ (2001) A family of proteins related to Spätzle, the Toll receptor ligand, are encoded in the Drosophila genome. Proteins 45:71–80
Parrinello N (1981) The reaction of Ciona intestinalis L. to subcuticular erythrocyte and protein injection. Dev Comp Immunol 5:105–110
Parrinello N (1995) Humoral and cellular lectins of ascidians. J Mar Biotechnol 3:29–34
Parrinello N (1996) Cytotoxic activity of tunicates hemocytes. In: Cellular, biochemical and molecular aspects of invertebrate immunology. Müller WEG, Rinkevich B (eds). Progress in molecular and subcellular biology, Springer, Berlin, pp 190–217
Parrinello N, Patricolo E (1984) Inflammatory-like reaction in the tunic of Ciona intestinalis (Tunicata). II. Capsule components. Biol Bull 167:238–250
Parrinello N, Patricolo E, Canicatti C (1984) Inflammatory-like reaction in the tunic of Ciona intestinalis (Tunicata). I. Encapsulation and tissue injury. Biol Bull 167:229–237
Parrinello N, De Leo G, Di Bella MA (1990) Fine structural observations of granulocytes involved in the tunic inflammatory-like reaction of Ciona intestinalis (Tunicata). J Invertebr Pathol 56:181–189
Parrinello N, Cammarata M, Lipari L et al (1995) Sphingomyelin inhibition of Ciona intestinalis hemocytes assayed against sheep erythrocytes. Dev Comp Immunol 19:31–41
Parrinello N, Cammarata M, Vazzana M et al (2001) Immunological activity of ascidian hemocytes. In: Sawada H, Yokosawa H, Lambert CC (eds) The biology of ascidians. Springer, Tokyo, pp 395–401
Parrinello N, Arizza V, Chinnici C et al (2003) Phenoloxidases in ascidian hemocytes: characterization of the pro-phenoloxidase activating system. Comp Biochem Physiol B Biochem Mol Biol 135B:583–591
Parrinello N, Arizza V, Cammarata M et al (2007) Inducible lectins with galectin properties and human IL1alpha epitopes opsonize yeast during the inflammatory response of the ascidian Ciona intestinalis. Cell Tissue Res 329:379–390
Parrinello N, Vizzini A, Arizza V et al (2008) Enhanced expression of a cloned and sequenced Ciona intestinalis TNF alpha like (CiTNF alpha) gene during the LPS-induced inflammatory response. Cell Tissue Res 334:305–317
Parrinello N, Vizzini A, Salerno G et al (2010) Inflamed adult pharynx tissues and swimming larva of Ciona intestinalis share CiTNFα-producing cells. Cell Tissue Res 341:299–311
Parrinello D, Sanfratello MA, Vizzini A et al (2015a) Ciona intestinalis galectin (CiLgals-a and CiLgals-b) genes are differentially expressed in endostyle zones and challenged by LPS. Fish Shellfish Immunol 42:171–176
Parrinello D, Sanfratello MA, Vizzini A, Cammarata M (2015b) The expression of an immune-related phenoloxidase gene is modulated in Ciona intestinalis ovary, test cells, embryos and larva. J Exp Zool B Mol Dev Evol 324B:141–151
Parrinello N, Cammarata M, Parrinello D et al (2016) Inflammatory response of the ascidian Ciona intestinalis. In: Ballarin L, Cammarata M (eds) Lessons in immunity: from single-cell organisms to mammals. Elsevier, London, pp 177–192
Parrinello D, Sanfratello MA, Vizzini A et al (2017) The Ciona intestinalis immune-related galectin genes (CiLgals-a andCiLgals-b) are expressed by the gastric epithelium. Fish Shellfish Immunol 62:24–30
Parrinello D, Sanfratello MA, Parisi MG et al (2018) In the ovary of Ciona intestinalis (type A), immune-related galectin and phenoloxidase genes are differentially expressed by the follicle accessory cells. Fish Shellfish Immunol 72:452–458
Pérez-Portela R, Bishop JDD, Davis AR et al (2009) Phylogeny of the families Pyuridae and Styelidae (Stolidobranchiata, Ascidiacea) inferred from mitochondrial and nuclear DNA sequences. Mol Phylogenet Evol 50:560–570
Petersen JK (2007) Ascidian suspension feeding. J Exp Mar Biol Ecol 342:127–137
Pineda MC, Turon X, López-Legentil S (2012) Stress levels over time in the introduced ascidian Styela plicata: the effects of temperature and salinity variations on hsp70 gene expression. Cell Stress Chaperones 17:435–444
Pinto MR, Chinnici CM, Kimura Y et al (2003) CiC3-1 mediated chemotaxis in the deuterostome invertebrate Ciona intestinalis (Urochordata). J Immunol 171:5521–5528
Poget SF, Legge GB, Proctor MR et al (1999) The structure of a tunicate C-type lectin from Polyandrocarpa misakiensis complexed with D-galactose. J Mol Biol 290:867–879
Pradeu T, Cooper EL (2012) The danger theory: 20 years later. Front Immunol Hypoth Theory 3:287, 1 https://doi.org/10.3389/fimmu.2012.00287
Prasobh R, Manoj N, Kelso J (2009) The repertoire of heterotrimeric G proteins and RGS proteins in Ciona intestinalis. PLoS One 4(10):e7349
Peddie CM, Smith VJ (1993) In vitro spontaneous cytotoxic activity against mammalian target cells by the hemocytes of the solitary ascidian,Ciona intestinalis. J Exp Zool 267(6):616–623
Peddie CM, Smith VJ (1995) Lymphocyte-like’cells in ascidians: precursors for vertebrate lymphocytes? Fish Shellfish Immunol 5:613–629
Quesenberry MS, Ahmed H, Elola MT et al (2003) Diverse lectin repertoires in tunicates mediate broad recognition and effector innate immune responses. Integr Comp Biol 43:323–330
Rabinovich G (2002) Role of galectins in inflammatory and immunomodulatory processes. Biochim Biophys Acta Gen Subj 1572(2–3):274–284
Rabinovich GA, Croci DO (2012) Regulatory circuits mediated by lectin–glycan interactions in autoimmunity and cancer. Immunity 36:322–335
Rabinovich GA, Gruppi A (2005) Galectins as immunoregulators during infectious processes: from microbial invasion to the resolution of the disease. Parasite Immunol 27(4):103–114
Raftos D (1996a) Interactions of tunicate immunomodulatory proteins with mammalians cells. Immunol Cell Biol 74:26–31
Raftos DA (1996b) Adoptive transfer of alloimmune memory in the solitary tunicate, Styela plicata. J Exp Zool 274:310
Raftos DA, Cooper EL (1991) Proliferation of lymphocyte-like cells from the solitary tunicate, Styela clava, in response to allogeneic stimuli. J Exp Zool 260:391–400
Raftos DA, Tait NN, Briscoe DA (1987a) Allograft rejection and alloimmune memory in the solitary urochordate, Styela plicata. Dev Comp Immunol 11:343–351
Raftos DA, Tait NN, Briscoe DA (1987b) Cellular basis of allograft rejection in the solitary urochordate, Styela plicata. Dev Comp Immunol 11:713–725
Raftos DA, Briscoe DA, Tait NN (1988) The mode of recognition of allogeneic tissue in the solitary urochordate Styela plicata. Transplantation 45:1123–1126
Raftos DA, Stillman DL, Cooper EL (1991a) Interleukin-2 and phytohemagglutinin stimulate proliferation of tunicate cells. Immunol Cell Biol 69:225–234
Raftos DA, Cooper EL, Habicht GS et al (1991b) Invertebrate citokines: tunicate cell proliferation stimulated by an interleukin 1–like molecule. Proc Natl Acad Sci 88:9518–9522
Raftos D, Green P, Mahajan D et al (2001) Collagenous lectins in tunicates and the proteolytic activation of complement. Adv Exp Med Biol 484:229–236
Raftos DA, Nair SV, Robbins J et al (2002) A complement component C3–like protein from the tunicate, Styela plicata. Dev Comp Immunol 26:307–312
Raftos DA, Robbins J, Newton RA et al (2003) A complement component C3a–like stimulates chemotaxis by hemocytes from an invertebrate chordate—the tunicate, Pyura stolonifera. Comp Biochem Physiol 134A:377–386
Raftos DA, Fabbro M, Nair SV (2004) Exocytosis of a complement component C3–like protein by tunicate hemocytes. Dev Comp Immunol 28:181–190
Rast JP, Smith LC, Loza-Coll M, Hibino T, Litman GW (2006) Genomic insights into the immune system of the sea urchin. Science 314:952–956
Reddy AL, Bryan B, Hidelmann WH (1975) Integumentary allograft versus autograft reactions in Ciona intestinalis: a protochordate species of solitary tunicate. Immunogenetics 1:584–590
Reynold JM, Dong C (2013) Toll-like receptor regulation of effector T lymphocyte function. Trends Immunol 34:511–519
Rinkevich B (2002) The colonial urochordate Botryllus schlosseri: from stem cells and natural tissue transplantation to issues in evolutionary ecology. Bioessays 24:730–740
Rinkevich B (2005) Rejection pattern in botryllid ascidian immunity: the first tier of allorecognition. Can J Zool 83:101–121
Rinkevich B, Rabinowitz C (1993) In vitro culture of blood cells from the colonial protochordate Botryllus schlosseri. In Vitro Cell Dev Biol Anim 29:79–85
Rinkevich B, Weissman IL (1987) A long-term study on fused subclones in the ascidian Botryllus schlosseri: the resorption phenomenon (Protochordata: Tunicata). J Zool (Lond) 213:717–733
Rinkevich B, Weissman IL (1992) Allogeneic resorption in colonial protochordates—consequences of nonself recognition. Dev Comp Immunol 16:275–286
Rinkevich B, Tartakover S, Gershon H (1998) Contribution of morula cells to allogeneic responses in the colonial urochordate Botryllus schlosseri. Mar Biol 131:227–236
Rinkevich Y, Douek J, Haber O, Rinkevich B, Reshef R (2007) Urochordate whole body regeneration inaugurates a diverse innate immune signaling profile. Dev Biol 312(1):131–146
Rinkevich B, Douek J, Rabinowitz C, Paz G (2012) The candidate FuHC gene in B. schlosseri (Urochordata) and ascidians’ historecognition—an oxymoron? Dev Comp Immunol 36:718–772
Roberts S, Gueguen Y, De Lorgeril J et al (2008) Rapid accumulation of an interleukin 17 homolog transcript in Crassostrea gigas hemocytes following bacterial exposure. Dev Comp Immunol 32:1099–1104
Robinson JM (2008) Reactive oxygen species in phagocytic leukocytes. Histochem Cell Biol 130:281–297
Rubinstein N, Ilarregui JM, Toscano MA, Rabinovich GA (2004) The role of galectins in the initiation, amplification and resolution of the inflammatory response. Tissue Antigens 64:1–12
Rybakin V, Clemen CS (2005) Coronin proteins as multifunctional regulators of the cytoskeleton and membrane trafficking. BioEssays 27:625–632
Sano H, Hsu DK, Apgar JR et al (2003) Critical role of galectin-3 in phagocytosis by macrophages. J Clin Invest 112:389–397
Sasaki N, Ogasawara M, Sekiguchi T et al (2009) Toll-like receptors of the ascidian Ciona intestinalis. J Biol Chem 284:27336–27343
Satake H, Sasaki N (2010) Comparative overview of Toll-like receptors in lower animals. Zool Sci 27:154–161
Satake H, Sekiguchi T (2012) Toll-like receptors of deuterostome invertebrates. Front Immunol 3:34. https://doi.org/10.3389/fimmu.2012
Satake M, Kawazoe Y, Kasuya A (2003) Hemocytes of Ciona intestinalis express multiple genes involved in innate immune host defense. Biochem Biophys Res Commun 302:207–218
Sato S, Nieminen J (2004) Seeing strangers or announcing “danger”: galectin-3 in two models of innate immunity. Glycoconj J 19:583–591
Sato A, Satoh N, Bishop JDD (2012) Field identification of ‘types’ A and B of the ascidian Ciona intestinalis in a region of sympatry. Mar Biol 159:1611–1619
Satoh N, Satau Y, Davidson B, Levine M (2003) Ciona intestinalis: an emerging model for whole-genome analyses. Trends Genet 19:376–381
Schmitz F, Mages J, Heit A et al (2004) Transcriptional activation induced in macrophages by Toll-like receptor (TLR) ligands: from expression profiling to a model of TLR signalling. Eur J Immunol 34:2863–2873
Scofield VL, Nagashima LS (1983) Morphology and genetics of rejection reactions between oozooids from the tunicate Botryllus schlosseri. Biol Bull 165:733–744
Sekine H, Kenjo A, Azumi K et al (2001) An ancient lectin-dependent complement system in an ascidian: novel lectin isolated from the plasma of the solitary ascidian, Halocynthia roretzi. J Immunol 167:4504–4510
Shaw LM, Olsen BR (1991) FACIT collagens: diverse molecular bridges in extracellular matrices. Trends Biochem Sci 16:191–194
Shi Y, Massagué J (2003) Mechanisms of TGF-b signaling from cell membrane to the nucleus. Cell 113:685–700
Shida K, Terajima D, Uchino R et al (2003) Hemocytes of Ciona intestinalis express multiple genes involved in innate immune host defense. Biochem Biophys Res Commun 302:207–218
Shirae M, Saito Y (2000) A comparison of hemocytes and their phenoloxidase activity among botryllid ascidians. Zool Sci 17:881–891
Shirae M, Hirose E, Saito Y (1999) Behavior of hemocytes in the allorejection reaction in two compound ascidians, Botryllus scalaris and Symplegma reptans. Biol Bull 197:188–197
Sidney LE, Branch MJ, Dunphy SE et al (2014) Concise review: evidence for CD34 as a common marker for diverse progenitors. Stem Cells (Dayton, Ohio) 32:1380–1389
Silerova M, Prochazkova P, Joskova R et al (2006) Comparative study of the CCFlike pattern recognition protein in different lumbricid species. Dev Comp Immunol 30:765–771
Silva MT, Correia-Neves M (2012) Neutrophils and macrophages: the main partners of phagocyte cell systems. Front Immunol 3:174. https://doi.org/10.3389/fimmu.2012.00174
Sim RB, Laich A (2000) Serine proteases of the complement system. Biochem Soc Trans 28:545–550
Skjoedt MO, Palarasah Y, Rasmussen K et al (2010) Two mannose-binding lectin homologues and an MBL-associated serine protease are expressed in the gut epithelia of the urochordate species Ciona intestinalis. Dev Comp Immunol 34:59–68
Smith VJ, Söderhäll K (1991) A comparison of phenoloxidase activity in the blood of marine invertebrates. Dev Comp Immunol 15:251–261
Smith LC, Azumi K, Nonaka M (1999) Complement systems in invertebrates. The ancient alternative and lectin pathways. Immunopharmacology 42:107–120
Söderhäll K, Cerenius L (1998) Role of prophenoxidase-activating system in invertebrate immunity. Curr Opin Immunol 10:23–28
Springer SA, Gagneux P (2013) Glycan evolution in response to collaboration, conflict, and constraint. J Biol Chem 288:6904–6911
Sritunyalucksana K, Wongsuebsantati K, Johansson MW et al (2001) Peroxinectin, a cell adhesive protein associated with the proPO system from the black tiger shrimp, Penaeus monodon. Dev Comp Immunol 25:353–363
Suzuki MM, Nishikawa T, Bird A (2005) Genomic approaches reveal unexpected genetic divergence within Ciona intestinalis. J Mol Evol 61:627–635
Swalla BJ, Smith AB (2008) Deciphering deuterostome phylogeny: molecular, morphological and paleontological perspectives. Philos Trans R Soc 363B:1557–1568
Takeda K, Akira S (2005) Toll-like receptors in innate immunity. Int Immunol 17:1–14
Taketa DA, De Tomaso AW (2015) Botryllus schlosseri Allorecognition: Tackling the enigma. Dev Comp Immunol 48:254–265
Tarallo R, Sordino P (2004) Time course of programmed cell death in Ciona intestinalis in relation to mitotic activity and MAPK signaling. Dev Dyn 230:251–262
Tecchio C, Micheletti A, Cassatella MA (2014) Neutrophil-derived cytokines: facts beyond expression. Front Immunol | Molecular Innate Immunity 5:508. https://doi.org/10.3389/fimmu.2014.00508
Terada T, Watanabe Y, Tateno H, Naganuma T, Ogawa T, Muramoto K, Kamiya H (2007) Structural characterization of a rhamnose binding glycoprotein (lectin) from Spanish mackerel (Scomberomorous niphonius) eggs. Biochim Biophys Acta 1770:617–629
Terajima D, Yamada S, Uchino R et al (2003) Identification and sequence of seventy-nine new transcripts expressed in hemocytes of Ciona intestinalis, three of which may be involved in characteristic cell–cell communication. DNA Res 10:203–212
Thornqvist PO, Johansson MW, Söderhäll K (1994) Opsonic activity of cell adhesion protein and b-1,3-glucan-binding proteins from two crustaceans. Dev Comp Immunol 18:3–12
Trapani MR, Sanfratello MA, Mangano V et al (2015) Phenoloxidases of different sizes are modulated by LPS inoculation into Ciona intestinalis tunic and pharynx. Inv Surv J 12:75–81
Trepels T, Zeiher AM, Fichtlscherer S (2006) The endothelium and inflammation. Endothelium 13:423–429
Tu Q, Cameron RA, Worley KC, Gibbs RA, Davidson EH (2012) Gene structure in the seaurchin Strongylocentrotus purpuratus based on transcriptome analysis. Genome Res 22:2079–2087
Turner MW (2003) The role of mannose-binding lectin in health and disease. Mol Immunol 40:423–429
Vabulas RM, Hmad-Nejad P, Ghose S et al (2002) HSP70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J Biol Chem 277:15107–15112
Valanne S, Wang J-H, Rämet M (2011) The Drosophila Toll signaling pathway. J Immunol 186:649–656
Van Lookeren Campagne M, Weismann C, Brown EJ (2007) Macrophage complement receptors and pathogen clearance. Lit Rev Cell Microbiol 9:2095–2102
Vanlangenakker N, Vanden Berghe T, Vandenabeele P (2012) Many stimuli pull the necrotic trigger, an overview. Cell Death Differ 19:75–86
Varki A, Acids SRS (2009) In: Varki A, Cummings RD, Esko JD et al (eds) Essentials of glycobiology, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor Chapter 14
Vasta GR (2012) Galectins as pattern recognition receptors: structure, function, and evolution, current topics in innate immunity II. Lambris JD, Hajishengallis G (eds) Adv Exp Med Biol 946:21–36
Vasta GR, Hunt JC, Marchalonis JJ et al (1986) Galactosyl-binding lectins from the tunicate Didemnum candidum. Purification and physicochemical characterization. J Biol Chem 261:9174–9181
Vasta GR, Quesenberry MS, Ahmed H et al (1999) C-type lectins and galectins mediate innate and adaptive immune functions: their roles in the complement activation pathway. Dev Comp Immunol 23:401–420
Vasta GR, Ahmed H, Odom EW (2004) Structural and functional diversity of lectin repertoires in invertebrates, protochordates and ectothermic vertebrates. Curr Opin Struct Biol 14:617–630
Vasta GR, Ahmed H, Nita-Lazar M et al (2012) Galectins as self/non-self recognition receptors in innate and adaptive immunity: an unresolved paradox. Front Immunol 3:199. https://doi.org/10.3389/fimmu.2012.00199
Vestweber D, Blanks JE (1999) Mechanisms that regulate the function of the selectins and their ligands. Physiol Rev 79:181–213
Vizzini A, Arizza V, Cervello M et al (2001) Identification of type I and IX collagens in the ascidian Ciona intestinalis. In: Sawada H, Yokosawa H, Lambert CC (eds) The biology of ascidians. Springer, Tokyo, pp 402–407
Vizzini A, Arizza V, Cervello M et al (2002) Cloning and expression of a type IX–like collagen in tissues of the ascidian Ciona intestinalis. Biochim Biophys Acta 1577:38–44
Vizzini A, Pergolizzi M, Vazzana M et al (2008) FACIT collagen (1alpha-chain) is expressed by hemocytes and epidermis during the inflammatory response of the ascidian Ciona intestinalis. Dev Comp Immunol 32:682–692
Vizzini A, Parrinello D, Sanfratello MA et al (2012) Inducible galectins are expressed in the inflamed pharynx of the ascidian Ciona intestinalis. Fish Shellfish Immunol 32:101–109
Vizzini A, Parrinello D, Sanfratello MA et al (2013a) Ciona intestinalis peroxinectin is a novel component of the peroxidase–cyclooxygenase gene superfamily upregulated by LPS. Dev Comp Immunol 41:59–67
Vizzini A, Bonura A, Parrinello D et al (2013b) LPS challenge regulates gene expression and tissue localization of a Ciona intestinalis gene through an alternative polyadenylation mechanism. PLoS One 8:63235
Vizzini A, Parrinello D, Sanfratello MA et al (2015a) Upregulated transcription of phenoloxidase genes in the pharynx and endostyle of Ciona intestinalis in response to LPS. J Invertebr Pathol 126:6–11
Vizzini A, Di Falco F, Parrinello D et al (2015b) Ciona intestinalis interleukin 17-like genes expression is upregulated by LPS challenge. Dev Comp Immunol 48:129–137
Vizzini A, Di Falco F, Parrinello D et al (2016a) Transforming growth factor b (CiTGF-b) gene expression is induced in the inflammatory reaction of Ciona intestinalis. Dev Comp Immunol 55:102–110
Vizzini A, Bonura A, Longo V et al (2016b) LPS injection reprograms the expression and the 3' UTR of a CAP gene by alternative polyadenylation and the formation of a GAIT element in Ciona intestinalis. Mol Immunol 77:174–183
Vizzini A, Parisi MG, Cardinale L et al (2017) Evolution of Ciona intestinalis tumor necrosis factor alpha (CiTNFα): polymorphism, tissues expression, and 3D modeling. Dev Comp Immunol 67:107–116
Voogdt CGP, van Putten JPM (2016) The evolution of the Toll-like receptor system. In: Malagoli D (ed) The evolution of the immune system. Conservation and diversification. Acad Press, London, pp 311–330
Voskoboynik A, Rinkevich B, Weiss A et al (2004) Macrophage involvement for successful degeneration of apoptotic organs in the colonial urochordate Botryllus schlosseri. J Exp Biol 207:2409–2416
Voskoboynik A, Soen Y, Rinkevich Y et al (2008) Identification of the endostyle as a stem cell niche in a colonial chordate. Cell Stem Cell 3:456–464
Voskoboynik A, Neff NF, Sahoo D et al (2013a) The genome sequence of the colonial chordate, Botryllus schlosseri. elife 2:00569
Voskoboynik A, Newman AM, Corey DM et al (2013b) Identification of a colonial chordate histocompatibility gene. Science 341(6144). https://doi.org/10.1126/science.1238036
Vyas K, Chaudhuri S, Leaman DW et al (2009) Genome-wide polysome profiling reveals an inflammation-responsive post-transcriptional operon in gamma interferon-activated monocytes. Mol Cell Biol 29:458–470
Wada H, Matsumoto N, Maenaka K et al (2004) The inhibitory NK cell receptor CD94/NKG2A and the activating receptor CD94/NKG2C bind the top of HLA-E through mostly shared but partly distinct sets of HLA-E residues. Eur J Immunol 34:81–90
Wada S, Hamada M, Satoh N (2006) A genomewide analysis of genes for the heat shock protein 70 chaperone system in the ascidian Ciona intestinalis. Cell Stress Chaperones 11:23–33
Wallis R (2007) Interactions between mannose-binding lectin and MASPs during complement activation by the lectin pathway. Immunobiology 212:289–299
Wang J, Slungaard A (2006) Role of eosinophil peroxidase in host defense and disease pathology. Arch Biochem Biophys 15:256–260
Wang KS, Frank DA, Ritz J (2000) Interleukin-2 enhances the response of natural killer cells to interleukin-12 through up-regulation of the interleukin-12 receptor and STAT4. Blood 95:3183–3190
Ward-Kavanagh L, Lin WW, Šedý JS et al (2016) The TNF receptor superfamily in costimulating and coinhibitory responses. Immunity 44:1005–1019
Weaver CT, Hatton RD, Mangan PR et al (2007) IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol 25:821–852
Weissman I (2000) Stem cells: units of development, review units of regeneration, and units in evolution. Cell 100:157–168
Wright RK, Cooper EL (1983) Inflammatory reactions of the protochordata. Am Zool 23:205–211
Wu S-Z, Huang X-D, Li Q, He M-X (2013) Interleukin-17 in pearl oyster (Pinctada fucata): molecular cloning and functional characterization. Fish Shellfish Immunol 34(5):1050–1056
Wynn TA, Vannella KM (2016) Macrophages in tissue repair, regeneration, and fibrosis. Immunity 44:450–462
Yousef GM, Diamandis EP (2003) An overview of the kallikrein gene families in humans and other species: emerging candidate tumour markers. Clin Biochem 36:443–452
Yu Y, Yuan S, Yi Y, Huang H et al (2007) Molecular and biochemical characterization of galectin from amphioxus: primitive galectin of chordates participated in the infection processes. Glycobiology 17:774–783
Zanoni I, Ostuni R, Marek LR et al (2011) CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 147:868–880
Zederbauer M, Furtmuller PG, Bellei M et al (2007a) Distruption of the aspartate to heme ester linkage in human myeloperoxidase: impact on ligand binding, redox chemistry and interconversion of redox intermediates. J Biol Chem 282:17041–17052
Zederbauer M, Furtmuller PG, Ganster B et al (2007b) Manipulating the vinyl–sulfonium bond in human myeloperoxidase: impact on compound I formation and reduction by halides and thiocyanate. Biochem Biophys Res Commun 356:450–456
Zelensky AN, Gready JE (2005) The C-type lectin–like domain superfamily. FEBS J 272:6179–6217
Zhang X, Luan W, Jin S et al (2008) A novel tumor necrosis factor ligand superfamily member (CsTL) from Ciona savignyi: molecular identification and expression analysis. Dev Comp Immunol 32:1362–1373
Zhang X, Angkasekwinai P, Dong C et al (2011) Structure and function of interleukin-17 family cytokines. Protein Cell 2:26–40
Zucchetti I, Marino R, Pinto MR et al (2008) CiCD94-1, an ascidian multipurpose C-type lectin–like receptor expressed in Ciona intestinalis hemocytes and larval neural structures. Differentiation 76:267–283
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer International Publishing AG, part of Springer Nature
About this chapter
Cite this chapter
Parrinello, N., Cammarata, M., Parrinello, D. (2018). The Inflammatory Response of Urochordata: The Basic Process of the Ascidians’ Innate Immunity. In: Cooper, E. (eds) Advances in Comparative Immunology. Springer, Cham. https://doi.org/10.1007/978-3-319-76768-0_15
Download citation
DOI: https://doi.org/10.1007/978-3-319-76768-0_15
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-76767-3
Online ISBN: 978-3-319-76768-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)