The Inflammatory Response of Urochordata: The Basic Process of the Ascidians’ Innate Immunity

  • Nicolò ParrinelloEmail author
  • Matteo Cammarata
  • Daniela Parrinello


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.


Ascidians Tunic Pharynx Hemocytes Evolution Toll-like receptors Galectins RBLs Collectins Complement Phenoloxidase Cytokines Allorecognition 


  1. Ajjan RA, Watson PF, Weetman AP (1996) Cytokines and thyroid function. Adv Neuroimmunol 6:359–386PubMedPubMedCentralGoogle Scholar
  2. Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4:499–511PubMedPubMedCentralGoogle Scholar
  3. 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 287:10060–10069PubMedPubMedCentralGoogle Scholar
  4. Anderson RS (1971) Cellular responses to foreign bodies in the tunicate Mogula manhattensis (DeKay). Biol Bull 141:91–98Google Scholar
  5. Arizza V, Parrinello D (2009) Inflammatory hemocytes in Ciona intestinalis innate immune response. Invertebr Surviv J 6:S58–S66Google Scholar
  6. Arizza V, Cammarata M, Tomasino MC et al (1995) Phenoloxidase characterization in vacuolar hemocytes from the solitary ascidians Styela plicata. J Invertebr Pathol 66:297–302Google Scholar
  7. 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 30:1014–1023PubMedPubMedCentralGoogle Scholar
  8. Armstrong PB (2010) Role of α2-macroglobulin in the immune responses of invertebrates. Invertebr Surviv J 7:165–180Google Scholar
  9. 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 277:15028–15034PubMedPubMedCentralGoogle Scholar
  10. Ashley NT, Zachary M, Weil RJ et al (2012) Inflammation: mechanisms, costs, and natural variation. Annu Rev Ecol Evol Syst 43:385–406Google Scholar
  11. 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 55:570–581PubMedPubMedCentralGoogle Scholar
  12. Azumi K, Sabau SV, Fujie M et al (2007) Gene expression profile during the life cycle of the urochordate Ciona intestinalis. Dev Biol 308:572–582PubMedPubMedCentralGoogle Scholar
  13. Anderson P (2010) Post-transcriptional regulons coordinate the initiation and resolution of inflammation. Nat Rev 10:24–35PubMedPubMedCentralGoogle Scholar
  14. Ballarin L (2008) Immunobiology of compound ascidians, with particular reference to Botryllus schlosseri: state of art. Invertebr Surviv J 5:54–74Google Scholar
  15. Ballarin L, Cima F (1998) Phenoloxidase and cytotoxicity in the compound ascidian Botryllus schlosseri. Dev Comp Immunol 22:479–492PubMedPubMedCentralGoogle Scholar
  16. Ballarin L, Cima F (2005) Cytochemical properties of Botryllus schlosseri haemocytes: indications for morpho-functional characterisation. Eur J Histochem 49:255–264PubMedPubMedCentralGoogle Scholar
  17. Ballarin L, Zaniolo G (2007) Colony specificity in Botrylloides leachi. II. Cellular aspects of the non-fusion reaction. Invertebr Surviv J 4:38–44Google Scholar
  18. Ballarin L, Cima F, Sabbadin A (1994) Phenoloxidase in the colonial ascidian Botryllus schlosseri (Urochordata, Ascidiacea). Anim Biol 3:41–48Google Scholar
  19. 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:411–418Google Scholar
  20. 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, HobokenGoogle Scholar
  21. Barnum SR (2015) C4a: an anaphylatoxin in name only. J Innate Immun 7:333–339PubMedPubMedCentralGoogle Scholar
  22. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Beck G, Habicht GS (1991) Purification and biochemical characterization of an invertebrate interleukin-1. Mol Immunol 28:577–584PubMedPubMedCentralGoogle Scholar
  24. Beck G, Vasta R, Marchalonis J, Habicht GS (1989a) Characterization of interleukin-1 activity in tunicates. Comp Biochem Physiol 92B:93–98Google Scholar
  25. Beck G, O'Brien RF, Habicht GS (1989b) Invertebrate cytokines: the phylogenetic emergence of interleukin-1. BioEssays 11:62–67PubMedPubMedCentralGoogle Scholar
  26. 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 146:284–299PubMedPubMedCentralGoogle Scholar
  27. Berná L, Alvarez-Valin F (2014) Evolutionary genomics of fast evolving tunicates. Genome Biol Evol 6:1724–1738PubMedPubMedCentralGoogle Scholar
  28. 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 17–31Google Scholar
  29. Bianchi ME (2007) DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 81:1–5PubMedPubMedCentralGoogle Scholar
  30. Bierhaus AJ, Chen B, Liliensiek B et al (2000) LPS and cytokine activated endothelium. Semin Thromb Hemost 26:571–587PubMedPubMedCentralGoogle Scholar
  31. Billack B (2006) Macrophage activation: role of Toll-like receptors, nitric oxide, and nuclear factor kappa B. Amer J Pharm Edu 70:102. PMC1637021Google Scholar
  32. Bishop CD, Bates WR, Brandhorst BP (2001) Regulation of metamorphosis in ascidians involves NO/cGMP signaling and HSP90. J Exp Zool 289:374–384PubMedPubMedCentralGoogle Scholar
  33. 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 274:98–111Google Scholar
  34. 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. PubMedPubMedCentralGoogle Scholar
  35. Bodmer JL, Schneider P, Tschopp J (2002) The molecular architecture of the TNF superfamily. Trends Biochem Sci 27:19–26PubMedPubMedCentralGoogle Scholar
  36. 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 46:2389–2394PubMedPubMedCentralGoogle Scholar
  37. 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):411–421PubMedPubMedCentralGoogle Scholar
  38. Borrego F, Masilamani M, Kabat J et al (2005) The cell biology of the human natural killer cell CD94/NKG2A inhibitory receptor. Mol Immunol 42:485–488PubMedPubMedCentralGoogle Scholar
  39. Botos I, Segal DM, Davies DR (2011) The structural biology of Toll-like receptors. Structure 19:447–495PubMedPubMedCentralGoogle Scholar
  40. 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 10:75–82PubMedPubMedCentralGoogle Scholar
  41. Brocker C, Thompson D, Matsumoto A et al (2010) Evolutionary divergence and functions of the human interleukin (IL) gene family. Hum Genomics 5:30–55PubMedPubMedCentralGoogle Scholar
  42. Brown GD, Gordon S (2001) Immune recognition. A new receptor for beta-glucans. Nature 413:36–37PubMedPubMedCentralGoogle Scholar
  43. 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 136:3485–3494PubMedPubMedCentralGoogle Scholar
  44. Buchmann K (2014) Evolution of innate immunity: clues from invertebrates via fish to mammals. Front Immunol 5:459. CrossRefPubMedPubMedCentralGoogle Scholar
  45. 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 221–347Google Scholar
  46. Calderwood SK, Murshid A, Gong J (2012) Heat shock proteins: conditional mediators of inflammation in tumor immunity. Front Immunol 3:75. CrossRefPubMedPubMedCentralGoogle Scholar
  47. Cambi A, Figdor CG (2003) Dual function of C-type lectin–like receptors in the immune system. Curr Opin Cell Biol 15:539–546PubMedPubMedCentralGoogle Scholar
  48. Cammarata M, Parrinello N (2009) The ascidian prophenoloxidase activating system. Invert Surv J 6:S67–S76Google Scholar
  49. 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 74:302–307PubMedPubMedCentralGoogle Scholar
  50. Cammarata M, Arizza V, Savona B et al (1999) Prophenoloxidase in the hemocyte of Phallusia mamillata. Anim Biol 8:15–17Google Scholar
  51. 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 333:481–492PubMedPubMedCentralGoogle Scholar
  52. 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 44:332–340PubMedPubMedCentralGoogle Scholar
  53. Cannon JP, Haire RN, Litman GW (2002) Identification of diversified genes that contain immunoglobulin-like variable regions in a protochordate. Nat Immunol 3(12):1200–1207PubMedGoogle Scholar
  54. Cannon JP, Haire RN, Schnitker N, Mueller MG, Litman GW (2004) Individual protochordates have unique immune-type receptor repertoires. Curr Biol 14(12):R465–R466PubMedPubMedCentralGoogle Scholar
  55. Caputi L, Andreakis N, Mastrototaro F et al (2007) Cryptic speciation in a model invertebrate chordate. PNAS 104:9364–9369PubMedPubMedCentralGoogle Scholar
  56. Cerenius L, Lee BL, Söderhäll K (2008) The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol 29:263–271PubMedPubMedCentralGoogle Scholar
  57. 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 35:809–816PubMedPubMedCentralGoogle Scholar
  58. Chaga OY (1980) Ortho-diphenoloxidase system of ascidians. Tsitologia 22:619–625Google Scholar
  59. 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 129:3105–3114PubMedPubMedCentralGoogle Scholar
  60. 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 134:1203–1219PubMedPubMedCentralGoogle Scholar
  61. Cima F, Perin A, Burighel P et al (2001) Morphofunctional characterisation of haemocytes of the compound ascidian Botrylloides leachi (Tunicata, Ascidiacea). Acta Zool 82:261–274Google Scholar
  62. 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 312:369–376PubMedPubMedCentralGoogle Scholar
  63. Cima F, Sabbadin A, Ballarin L (2004) Cellular aspects of allorecognition in the compound ascidian Botryllus schlosseri. Dev Comp Immunol 28:881–889PubMedPubMedCentralGoogle Scholar
  64. 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 34:272–285PubMedPubMedCentralGoogle Scholar
  65. 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 29–49Google Scholar
  66. Cloney RA (1982) Ascidian larvae and the events of metamorphosis. Am Zool 22:817–826Google Scholar
  67. Cloney RA, Grimm LM (1970) Transcellular emigration of blood cells during ascidian metamorphosis. Z Zellforsch 107:157–173PubMedPubMedCentralGoogle Scholar
  68. Comes S, Locascio A, Silvestre F et al (2007) Regulatory roles of nitric oxide during larval development and metamorphosis in Ciona intestinalis. Dev Biol 306:772–784PubMedPubMedCentralGoogle Scholar
  69. Cooper EL (1992) Overview of immunoevolution. Boll Zool 59:119–128Google Scholar
  70. Cooper EL (2009) Putative stem cell origins in solitary tunicates. In: Rinkevich B, Matranga V (eds) Stem cells in marine organisms. Springer, Netherlands, pp 21–32Google Scholar
  71. Cooper EL (2016) Commentary: blurring borders: innate immunity with adaptive features. Front Microbiol 7:358. CrossRefPubMedPubMedCentralGoogle Scholar
  72. 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 383–394Google Scholar
  73. 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 113:6520–6525PubMedPubMedCentralGoogle Scholar
  74. Coscia MR, Giacomelli S, Oreste U (2011) Toll-like receptors: an overview from invertebrates to vertebrates. Invert Surv J 8:210–226Google Scholar
  75. 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 31Google Scholar
  76. 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.
  77. Davidson B, Swalla BJ (2002) A molecular analysis of ascidian metamorphosis reveals activation of an innate immune response. Develop 129:4739–4751Google Scholar
  78. 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 282:1615–1626PubMedPubMedCentralGoogle Scholar
  79. De Leo G (1992) Ascidian hemocytes and their involvement in defence reactions. Boll Zool 59:195–213Google Scholar
  80. Deck JD, Hay ED, Revel J-P (1966) Fine structure and origin of the tunic of Perophora viridis. J Morphol 120:267–280PubMedPubMedCentralGoogle Scholar
  81. Dehal P, Satou Y, Campbell RK et al (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2167PubMedPubMedCentralGoogle Scholar
  82. De Leo G, Parrinello N, Parrinello D et al (1997) Encapsulation response of Ciona intestinalis (Ascidiacea) to intratunic erythrocyte injection. J Invertebr Pathol 69:14–23PubMedPubMedCentralGoogle Scholar
  83. 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):205–212Google Scholar
  84. Delsuc F, Brinkmann H, Chourrout D et al (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965–968PubMedPubMedCentralGoogle Scholar
  85. Delsuc F, Tsagkogeorga G, Lartillot N, Philippe H (2008) Additional molecular support for the new chordate phylogeny. Genesis 46:592–594PubMedPubMedCentralGoogle Scholar
  86. 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 30:352–359PubMedPubMedCentralGoogle Scholar
  87. Di Bella MA, Carbone MC, De Leo G (2005) Aspects of cell production in mantle tissue of Ciona intestinalis L. (Tunicata, Ascidiacea). Micron 36:477–481PubMedPubMedCentralGoogle Scholar
  88. 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 41:381–389PubMedPubMedCentralGoogle Scholar
  89. 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 1:70–75PubMedPubMedCentralGoogle Scholar
  90. 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 69:6–14PubMedPubMedCentralGoogle Scholar
  91. Di Bella MA, De Leo G (2000) Hemocyte migration during Inflammatory-like reaction of Ciona intestinalis (Tunicata, Ascidiacea). J Invertebr Pathol 76(2):105–111PubMedPubMedCentralGoogle Scholar
  92. Di Giammartino DC, Nishida K, Manley JL (2011) Mechanisms and consequences of alternative polyadenylation. Mol Cell 43:853–866PubMedPubMedCentralGoogle Scholar
  93. Dinarello CA (2007) Historical review of cytokines. Eur J Immunol 37:S34–S45PubMedPubMedCentralGoogle Scholar
  94. Dinasarapu AR, Chandrasekhar A, Fujita T et al (2013) Mannose/mannan-binding lectin. UCSD Molecule 2:8–18. CrossRefGoogle Scholar
  95. 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):16747–16752PubMedPubMedCentralGoogle Scholar
  96. 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 7:10617PubMedPubMedCentralGoogle Scholar
  97. Donaghy L, Hong HK, Park KI et al (2017) Flow cytometric characterization of hemocytes of the solitary ascidian, Halocynthia roretzi. Fish Shellfish Immunol 66:289–299PubMedPubMedCentralGoogle Scholar
  98. 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 36:2333–2339PubMedPubMedCentralGoogle Scholar
  99. Drickamer K, Fadden AJ (2002) Genomic analysis of C-type lectins. Biochem Soc Symp 69:59–72Google Scholar
  100. Drickamer K, Taylor ME (2015) Recent insights into structures and functions of C-type lectins in the immune system. Curr Opin Struct Biol 34:26–34PubMedPubMedCentralGoogle Scholar
  101. Du Clos TW (2013) Pentraxins: structure, function, and role in inflammation. ISRN Inflamm 2013:1–22Google Scholar
  102. Du Pasquier L (2004) Innate immunity in early chordates and the appearance of adaptive immunity. C R Biol 327:591–601PubMedPubMedCentralGoogle Scholar
  103. 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 2016:1–44Google Scholar
  104. East L, Isacke CM (2002) The mannose receptor family. Biochim Biophys Acta 1572:364–386PubMedPubMedCentralGoogle Scholar
  105. Elkon R, Ugalde AP, Agami R (2013) Alternative cleavage and polyadenylation: extent, regulation and function. Nat Rev Genet 14:496–506PubMedPubMedCentralGoogle Scholar
  106. Elliot MR, Ravochandran KS (2010) Clearance of apoptotic cells: implications in health and diseases. J Cell Biol 189:1059–1070Google Scholar
  107. Endean R (1961) The test of the ascidian, Phallusia mammillata. Quart J Microsc Sci 102:107–117Google Scholar
  108. 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 DiegoGoogle Scholar
  109. Ermak TH (1975b) An autoradiographic demonstration of blood cell renewal in Styela clava (Urochordata: Ascidiacea). Experientia 31:837–838Google Scholar
  110. 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 45–56Google Scholar
  111. Ermak TH (1982) The renewing cell populations of ascidians. Am Zool 22:795–805Google Scholar
  112. Esposito R, D’Aniello S, Squarzoni P et al (2012) New insights into the evolution of metazoan tyrosinase gene family. PLoS One 74:1–10Google Scholar
  113. 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 5:1–18Google Scholar
  114. 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 32:286–298PubMedPubMedCentralGoogle Scholar
  115. Fox PL (2015) Discovery and investigation of the GAIT translational control system. RNA 21:615–618PubMedPubMedCentralGoogle Scholar
  116. 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):430–438PubMedPubMedCentralGoogle Scholar
  117. 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 193–203Google Scholar
  118. 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 63:157–164Google Scholar
  119. Fugmann SD (2010) The origins of the RAG genes—from transposition to V(D)J recombination. Semin Immunol 22:10–16PubMedPubMedCentralGoogle Scholar
  120. 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 103:3728–3733PubMedPubMedCentralGoogle Scholar
  121. 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 15:193–204PubMedPubMedCentralGoogle Scholar
  122. 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 42:319–326PubMedPubMedCentralGoogle Scholar
  123. Fujita T, Endo Y, Nonaka M (2004a) Primitive complement system—recognition and activation. Mol Immunol 41:103–111PubMedPubMedCentralGoogle Scholar
  124. Fujita T, Matsushita M, Endo Y (2004b) The lectin–complement pathway—its role in innate immunity and evolution. Immunol Rev 198:346–353Google Scholar
  125. Fuke MT (1980) “Contact reaction” between xenogeneic or allogeneic celomic cells of solitary ascidians. Biol Bull 158:304–315Google Scholar
  126. Futosi K, Fodor S, Mócsai A (2013) Neutrophil cell surface receptors and their intracellular signal transduction pathways. Int Immunopharmacol 17:638–650PubMedPubMedCentralGoogle Scholar
  127. Gallucci S, Matzinger P (2001) Danger signals: SOS to the immune system. Curr Opin Immunol 13:114–119PubMedPubMedCentralGoogle Scholar
  128. Gasparini F, Franchi N, Spolaore B et al (2008) Novel rhamnose-binding lectins from the colonial ascidian Botryllus schlosseri. Dev Comp Immunol 32:1177–1191PubMedPubMedCentralGoogle Scholar
  129. Giacomelli S, Melillo D, Lambris JD et al (2012) Immune competence of the Ciona intestinalis pharynx: complement system-mediate activity. Fish Shellfish Immunol 33:946–952PubMedPubMedCentralGoogle Scholar
  130. 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 29:865–897PubMedPubMedCentralGoogle Scholar
  131. Gijtenbeel TBH, Inghuis GR (2009) Signalling through C-type lectin receptors: shaping immune responses. Nat Rev Immunol 9:465–479Google Scholar
  132. Goetz FW, Planas JV, MacKenzie S (2004) Tumor necrosis factors. Dev Comp Immunol 28:487–497PubMedPubMedCentralGoogle Scholar
  133. Green PL, Nair SV, Raftos DA (2003) Secretion of a collectin-like protein in tunicates enhanced during inflammatory responses. Dev Comp Immunol 27:3–9PubMedPubMedCentralGoogle Scholar
  134. Gu C, Wu L, Li X (2013) IL-17 family: cytokines, receptors and signaling. Cytokine 64:477–485PubMedPubMedCentralGoogle Scholar
  135. Guilliams M, Ginhoux F, Jakubzick C et al (2014) Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat Rev Immunol 14:571–578PubMedPubMedCentralGoogle Scholar
  136. Gupta G, Surolia A (2007) Collectins: sentinels of innate immunity. BioEssays 29:452–464PubMedPubMedCentralGoogle Scholar
  137. Hansen JD, Vojtech LN, Laing KJ (2011) Sensing disease and danger: a survey of vertebrate PRRs and their origins. Dev Comp Immunol 35:886–897PubMedPubMedCentralGoogle Scholar
  138. Hata S, Azumi K, Yokosawa H (1998) Ascidian phenoloxidase: its release from hemocytes, isolation, characterization and physiological roles. Comp Biochem Physiol 119:769–776Google Scholar
  139. Hibino T, Loza-Coll M, Messier C et al (2006) The immune gene repertoire encoded in the purple sea urchin genome. Dev Biol 300:349–365PubMedPubMedCentralGoogle Scholar
  140. Hirose E (2009) Ascidian tunic cells: morphology and functional diversity of free cells outside the epidermis. Invertebr Biol 128:83–96Google Scholar
  141. Hirose E, Ishii T, Saito Y, Taneda Y (1994) Phagocytic activity of tunic cells in the colonial ascidian Aplidium yamazii (Polyclinidae, Aplousobranchia). Zool Sci 11:203–208Google Scholar
  142. Hirsiger S, Simmen H-P, Werner CML et al (2012) Danger signals activating the immune response after trauma. Mediators Inflamm 315941:10. CrossRefGoogle Scholar
  143. Houzelstein D, Goncalves IR, Fadden AJ et al (2004) Phylogenetic analysis of the vertebrate galectin family. Mol Biol Evol 21:1177–1187Google Scholar
  144. Hoving JC, Wilson GJ, Brown GD (2014) Signalling C-type lectin receptors, microbial recognition and immunity. Cell Microbiol 16:185–194PubMedPubMedCentralGoogle Scholar
  145. 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 21:1–10PubMedPubMedCentralGoogle Scholar
  146. 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 18:1112–1126PubMedPubMedCentralGoogle Scholar
  147. 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 87:4426–4429PubMedPubMedCentralGoogle Scholar
  148. 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 3:9–28Google Scholar
  149. Idriss TH, Naismith JH (2000) TNF alpha and the TNF receptor superfamily: structure function relationship(s). Microsc Res Tech 1:184–195Google Scholar
  150. Immesberger A, Burmester T (2004) Putative phenoloxidases in the tunicate Ciona intestinalis and the origin of the arthropod hemocyanin superfamily. J Comp Physiol B 174:169–180PubMedPubMedCentralGoogle Scholar
  151. 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 254:142–144Google Scholar
  152. Ip EWK, Takahashi K, Ezekowitz AR et al (2009) Mannose-binding lectin and innate immunity. Immunol Rev 230:9–21PubMedPubMedCentralGoogle Scholar
  153. Iwanaga S, Lee BL (2005) Recent advances in the innate immunity of invertebrate animals. J Biochem Mol Biol 38:128–150PubMedPubMedCentralGoogle Scholar
  154. Jackson AD, Smith VJ, Peddie CM (1993) In vitro phenoloxidase activity in the blood of Ciona intestinalis and other ascidians. Dev Comp Immunol 17:97–108Google Scholar
  155. 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: Google Scholar
  156. 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 276:29037–29044PubMedPubMedCentralGoogle Scholar
  157. 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):6340–6345PubMedPubMedCentralGoogle Scholar
  158. 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 100:7527–7532PubMedPubMedCentralGoogle Scholar
  159. 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:164–171Google Scholar
  160. Johansson MW, Lind MI, Holmblad T et al (1995) Peroxinectin, a novel cell adhesion protein from crayfish blood. Biochem Biophys Res Commun 216:1079–1087PubMedPubMedCentralGoogle Scholar
  161. 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 177:4679–4687PubMedPubMedCentralGoogle Scholar
  162. Johansson MW (1999) Cell adhesion molecules in invertebrate immunity. Dev Comp Immunol 23:303–315Google Scholar
  163. Johansson MW, Söderhäll K (1989) A cell adhesion factor from crayfish haemocytes has degranulating activity towards crayfish granular cells. Insect Biochem 19(2):183–190Google Scholar
  164. 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:// Scholar
  165. Kaczmarek A, Vandenabeele P, Krysko DV (2013) Necroptosis: the release of damage-associated molecular patterns and its physiological relevance. Immunity 38:209–223Google Scholar
  166. Karpova AY, Ronco LV, Howley PM (2001) Functional characterization of interferon regulatory factor 3a (IRF3a), an alternative splice isoform of IRF3. Mol Cell Biol 21:4169–4176PubMedPubMedCentralGoogle Scholar
  167. Kawamura K, Sunanaga T (2010) Hemoblasts in colonial tunicates: are they stem cells or tissue-restricted progenitor cells? Develop Growth Differ 52:69–76Google Scholar
  168. 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 23:477–487PubMedPubMedCentralGoogle Scholar
  169. Kelley J, Walter L, Trowsdale J (2015) Comparative genomics of natural killer cell receptor gene clusters. PLoS Genet 1(2):e27. CrossRefGoogle Scholar
  170. Kelly KL, Cooper EL, Raftos DA (1992) In vitro allogeneic cytotoxicity in the solitary urochordate Styela clava. J Exp Zool 262:202–208PubMedPubMedCentralGoogle Scholar
  171. Kenjo A, Takahashi M, Matsushita M et al (2001) Cloning and characterization of novel ficolins from the solitary ascidian Halocynthia roretzi. J Biol Chem 276:19959–19965PubMedPubMedCentralGoogle Scholar
  172. Kerrigan AM, Brown GD (2009) C-type lectins and phagocytosis. Immunobiology 214:562–575PubMedPubMedCentralGoogle Scholar
  173. 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 100:622–627PubMedGoogle Scholar
  174. Kirkitadze M, Barlow P (2001) Structure and flexibility of the multiple domain proteins that regulate complement activation. Immunol Rev 180:146–161PubMedGoogle Scholar
  175. Klebanoff JS (2005) Myeloperoxidase: friend and foe. J Leukoc Biol 77:598–625PubMedPubMedCentralGoogle Scholar
  176. Klyosov AA (2008) Galectins and their functions in plain language. In: Klyosov AA, Witczak ZJ, Platt D (eds) Galectins. Wiley & Sons, Hoboken, pp 9–32Google Scholar
  177. Kobayashi M, Johansson MW, Söderhäll K (1990) The 76 kDa cell adhesion factor from crayfish haemocytes promotes encapsulation in vitro. Cell Tissue Res 260:113–118Google Scholar
  178. Koh TJ, DiPietro LA (2011) Inflammation and wound healing: the role of the macrophage. Expert Rev Mol Med 13:e23. CrossRefPubMedPubMedCentralGoogle Scholar
  179. Kondos SC, Hatfaludi T, Voskoboinik I et al (2010) The structure and function of mammalian membrane-attack complex/perforin-like proteins. Tissue Antigens 76:341–351PubMedPubMedCentralGoogle Scholar
  180. Kono H, Rock KL (2008) How dying cells alert the immune system to danger. Nat Rev Immunol 8:279–289PubMedPubMedCentralGoogle Scholar
  181. Konrad MW (2016) Blood circulation in the ascidian tunicate Corella inflata (Corellidae). Wang L (ed) PeerJ 4:2771. PubMedPubMedCentralGoogle Scholar
  182. Kvell K, Cooper E, Engelmann P, Bovari J, Nemeth P (2007) Blurring borders: innate immunity with adaptive features. Clin Dev Immunol 2007:83671. Google Scholar
  183. Laird DJ, De Tomaso AW, Weissman IL (2005) Stem cells are units of natural selection in a colonial ascidian. Cell 123:1351–1360PubMedPubMedCentralGoogle Scholar
  184. Lauzon RJ, Ishizuka KJ, Weissman IL (1992) A cyclical, developmentally-regulated death phenomenon in a colonial urochordate. Dev Dyn 1941:71–83Google Scholar
  185. Lauzon RJ, Brown C, Kerr L, Tiozzo S (2013) Phagocyte dynamics in a highly regenerative urochordate: insights into development and host defense Devel. Biol 374:357–373Google Scholar
  186. Lemaitre B, Hoffmann J (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25:697–743PubMedPubMedCentralGoogle Scholar
  187. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  188. Li MO, Wan YY, Sanjabi S et al (2006) Transforming growth factor-b regulation of immune responses. Annu Rev Immunol 24:99–146PubMedPubMedCentralGoogle Scholar
  189. Li K, Fazekasova H, Wang N et al (2011) Expression of complement components, receptors and regulators by human dendritic cells. Mol Immunol 48:1121–1127PubMedPubMedCentralGoogle Scholar
  190. 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 100:35–83PubMedPubMedCentralGoogle Scholar
  191. 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 69:2788–2796PubMedPubMedCentralGoogle Scholar
  192. 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 18:431–444PubMedPubMedCentralGoogle Scholar
  193. 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 22:408–417PubMedPubMedCentralGoogle Scholar
  194. 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 97–114Google Scholar
  195. Liu FT, Yang RY, Hsu DK (2012) Galectins in acute and chronic inflammation. Ann N Y Acad Sci 1253:80–91PubMedPubMedCentralGoogle Scholar
  196. Locksley RM, Killeen N, Lenardo MJ (2001) The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104:487–501PubMedPubMedCentralGoogle Scholar
  197. 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 16:175–185Google Scholar
  198. Lubbers R, van Essen MF, van Kooten C et al (2017) Production of complement components by cells of the immune system. Clin Exp Immunol 188:183–194Google Scholar
  199. 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 203:2785–2791PubMedPubMedCentralGoogle Scholar
  200. 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 27:393–400PubMedPubMedCentralGoogle Scholar
  201. 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 69–92Google Scholar
  202. Mantovani A, Biswas SK, Galdiero MR et al (2013) Macrophage plasticity and polarization in tissue repair and remodelling. J Pathol 229:176–185PubMedPubMedCentralGoogle Scholar
  203. 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 125:899–907PubMedPubMedCentralGoogle Scholar
  204. 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 53:1055–1064PubMedPubMedCentralGoogle Scholar
  205. Marshall ASJ, Gordon S (2004) C-type lectins on the macrophage cell surface—recent findings. Eur J Immunol 34:18–24PubMedPubMedCentralGoogle Scholar
  206. Martchenko M, Levitin A, Hogues H, Nantel A, Whiteway M (2007) Transcriptional rewiring of fungal galactose-metabolism circuitry. Curr Biol: CB 17(12). PubMedPubMedCentralGoogle Scholar
  207. Massagué J, Gomis RR (2006) The logic of TGF-b signaling. FEBS Lett 580:2811–2820PubMedPubMedCentralGoogle Scholar
  208. 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 128:3339–3347PubMedPubMedCentralGoogle Scholar
  209. Matsushita M, Fujita T (2001) Ficolins and the lectin complement pathway. Immunol Rev 180:78–85PubMedPubMedCentralGoogle Scholar
  210. Matsushita M, Endo Y, Fujita T (1998) MASP1 (MBL-associated serine protease 1). Immunobiology 199:340–347PubMedPubMedCentralGoogle Scholar
  211. Matsushita M, Endo Y, Fujita T (2000) Cutting edge: complement-activating complex of ficolin and mannose-binding lectin–associated serine protease. J Immunol 164:2281–2284PubMedPubMedCentralGoogle Scholar
  212. Matzinger P (1994) Tolerance, danger, and the extended family. Annu Rev Immunol 12:991–1045PubMedPubMedCentralGoogle Scholar
  213. Matzinger P (2002) The danger model: a renewed sense of self. Science 296:301–305PubMedPubMedCentralGoogle Scholar
  214. McKitrick TR, De Tomaso AW (2010) Molecular mechanisms of allorecognition in a basal chordate. Semin Immunol 22(1). PubMedPubMedCentralGoogle Scholar
  215. Meager A, Wadhwa M (2013) An overview of cytokine regulation of inflammation and immunity. In: eLS. John Wiley & Sons Ltd, ChichesterGoogle Scholar
  216. Medzhitov R (2008) Origin and physiological roles of inflammation. Nature 454:428–435PubMedPubMedCentralGoogle Scholar
  217. 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 177:4132–4140PubMedPubMedCentralGoogle Scholar
  218. Menin A, Ballarin L (2010) Immunomodulatory molecules in the compound ascidian Botryllus schlosseri: evidence from conditioned media. Dev Comp Immunol 34:272–285Google Scholar
  219. 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 148:225–230Google Scholar
  220. Merle NS, Church SE, Fremeaux-Bacchi V et al (2015a) Complement system part I—molecular mechanisms of activation and regulation. Front Immunol 6:262. CrossRefPubMedPubMedCentralGoogle Scholar
  221. Merle NS, Noe R, Halbwachs-Mecarelli L et al (2015b) Complement system part II: role in immunity. Front Immunol 6:257. CrossRefPubMedPubMedCentralGoogle Scholar
  222. Metchnikoff E (1887) Sur la lutte des cellules de l'organisme contre l’invasion des microbes. Ann Inst Pasteur 1:321–345Google Scholar
  223. 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 105:19845–19850PubMedPubMedCentralGoogle Scholar
  224. Miyazawa S, Nonaka M (2004) Characterization of novel ascidian beta integrins as primitive complement receptor subunits. Immunogenetics 55:836–844PubMedPubMedCentralGoogle Scholar
  225. Miyazawa S, Azumi K, Nonaka M (2001) Cloning and characterization of integrin a subunits from the solitary ascidian, Halocynthia roretzi. J Immunol 166:1710–1715PubMedPubMedCentralGoogle Scholar
  226. Mogensen TH (2009) Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 22:240–273PubMedPubMedCentralGoogle Scholar
  227. 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 162:771–779PubMedPubMedCentralGoogle Scholar
  228. 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 12:1263–1268PubMedPubMedCentralGoogle Scholar
  229. Nair SV, Pearce S, Green PL et al (2000) A collectin-like protein from tunicates. Comp Biochem Physiol 125B:279–289Google Scholar
  230. Nair SV, Ramsden A, Raftos DA (2005) Ancient origins: complement in invertebrates. Invertebr Surviv J 2:114–123Google Scholar
  231. Nappi AJ, Ottaviani E (2000) Cytotoxicity and cytotoxic molecules in invertebrates. BioEssays 22:469–480PubMedPubMedCentralGoogle Scholar
  232. Nappi AJ, Vass E (1993) Melanogenesis and the generation of cytotoxic molecules during insect cellular immune reactions. Pigment Cell Res 6:117–126PubMedPubMedCentralGoogle Scholar
  233. Nesargikar PN, Spiller B, Chavez R (2012) The complement system: history, pathways, cascade and inhibitors. Eur J Microbiol Immunol 2:103–111Google Scholar
  234. 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 33–70Google Scholar
  235. 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. CrossRefGoogle Scholar
  236. Nonaka M, Azumi K (1999) Opsonic complement system of the solitary ascidian Halocynthia roretzi. Dev Comp Immunol 23:421–427PubMedPubMedCentralGoogle Scholar
  237. Nonaka M, Kimura A (2006) Genomic view of the evolution of the complement system. Immunogenetics 58:701–713PubMedPubMedCentralGoogle Scholar
  238. Nonaka M, Satake H (2010) Urochordate immunity. In: Söderhall K (ed) Invertebrate immunity. Landes Bioscience and Springer Science, Boston, pp 302–310Google Scholar
  239. Nonaka M, Yoshizaki F (2004) Primitive complement system of invertebrates. Immunol Rev 198:203–215PubMedPubMedCentralGoogle Scholar
  240. Nonaka M, Azumi K, Ji X et al (1999) Opsonic complement component C3 in the solitary ascidian Halocynthia roretzi. J Immunol 162:387–391PubMedPubMedCentralGoogle Scholar
  241. Norling LV, Perretti M, Cooper D (2009) Endogenous galectins and the control of the host inflammatory response. J Endocrinol 201:169–184PubMedPubMedCentralGoogle Scholar
  242. Nydam ML, Harrison RG (2007) Genealogical relationships within and among shallow-water Ciona species (Ascidiacea). Mar Biol 151:1839–1847Google Scholar
  243. Nydam ML, Harrison RG (2011) Introgression despite substantial divergence in a broadcast spawning marine invertebrate. Evolution 65:429–442PubMedPubMedCentralGoogle Scholar
  244. 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):128–136PubMedPubMedCentralGoogle Scholar
  245. 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 285:158–169PubMedPubMedCentralGoogle Scholar
  246. Ogawa T, Watanabe M, Naganuma T, Muramoto K (2011) Diversified carbohydrate-binding lectins from marine resources. J Amino Acids 2011:838914, 20. Google Scholar
  247. 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 31:889–902PubMedPubMedCentralGoogle Scholar
  248. Oren M, Escande M-l, Paz G et al (2008) Urochordate histoincompatible interactions activate vertebrate-like coagulation system components. PLoS One:3. PubMedPubMedCentralGoogle Scholar
  249. Oren M, Paz G, Douek J et al (2013) Marine invertebrates cross phyla comparisons reveal highly conserved immune machinery. Immunobiology 218:484–495PubMedPubMedCentralGoogle Scholar
  250. Ottaviani E, Franchini A, Cassanelli S et al (1995) Cytokines and invertebrate immune responses. Biol Cell 85:87–91PubMedPubMedCentralGoogle Scholar
  251. Ottaviani E, Franchini A, Kletsas D et al (1996) Presence and role of cytokines and growth factors in invertebrates. Ital J Zool 63:317–323Google Scholar
  252. 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:625–632Google Scholar
  253. 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 16:801–806PubMedPubMedCentralGoogle Scholar
  254. Pandolfi F, Altamura S, Frosali S, Conti P (2016) Key role of DAMP in inflammation, cancer, and tissue repair. Clin Ther 38:1017–1028PubMedPubMedCentralGoogle Scholar
  255. Pappu R, Ramirez-Carrozzi V, Ota N et al (2010) The IL-17 family cytokines in immunity and disease. J Clin Immunol 30:185–195PubMedPubMedCentralGoogle Scholar
  256. 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 45:71–80PubMedPubMedCentralGoogle Scholar
  257. Parrinello N (1981) The reaction of Ciona intestinalis L. to subcuticular erythrocyte and protein injection. Dev Comp Immunol 5:105–110Google Scholar
  258. Parrinello N (1995) Humoral and cellular lectins of ascidians. J Mar Biotechnol 3:29–34Google Scholar
  259. 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 190–217Google Scholar
  260. Parrinello N, Patricolo E (1984) Inflammatory-like reaction in the tunic of Ciona intestinalis (Tunicata). II. Capsule components. Biol Bull 167:238–250Google Scholar
  261. Parrinello N, Patricolo E, Canicatti C (1984) Inflammatory-like reaction in the tunic of Ciona intestinalis (Tunicata). I. Encapsulation and tissue injury. Biol Bull 167:229–237Google Scholar
  262. 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 56:181–189PubMedPubMedCentralGoogle Scholar
  263. Parrinello N, Cammarata M, Lipari L et al (1995) Sphingomyelin inhibition of Ciona intestinalis hemocytes assayed against sheep erythrocytes. Dev Comp Immunol 19:31–41PubMedPubMedCentralGoogle Scholar
  264. 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 395–401Google Scholar
  265. 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:583–591Google Scholar
  266. 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 329:379–390PubMedPubMedCentralGoogle Scholar
  267. 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 334:305–317PubMedPubMedCentralGoogle Scholar
  268. 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 341:299–311PubMedPubMedCentralGoogle Scholar
  269. 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 42:171–176PubMedPubMedCentralGoogle Scholar
  270. 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:141–151Google Scholar
  271. 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 177–192Google Scholar
  272. 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 62:24–30PubMedPubMedCentralGoogle Scholar
  273. 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 72:452–458PubMedPubMedCentralGoogle Scholar
  274. 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 50:560–570PubMedPubMedCentralGoogle Scholar
  275. Petersen JK (2007) Ascidian suspension feeding. J Exp Mar Biol Ecol 342:127–137Google Scholar
  276. 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 17:435–444PubMedPubMedCentralGoogle Scholar
  277. Pinto MR, Chinnici CM, Kimura Y et al (2003) CiC3-1 mediated chemotaxis in the deuterostome invertebrate Ciona intestinalis (Urochordata). J Immunol 171:5521–5528PubMedPubMedCentralGoogle Scholar
  278. 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 290:867–879PubMedPubMedCentralGoogle Scholar
  279. Pradeu T, Cooper EL (2012) The danger theory: 20 years later. Front Immunol Hypoth Theory 3:287, 1
  280. Prasobh R, Manoj N, Kelso J (2009) The repertoire of heterotrimeric G proteins and RGS proteins in Ciona intestinalis. PLoS One 4(10):e7349PubMedPubMedCentralGoogle Scholar
  281. 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):616–623PubMedPubMedCentralGoogle Scholar
  282. Peddie CM, Smith VJ (1995) Lymphocyte-like’cells in ascidians: precursors for vertebrate lymphocytes? Fish Shellfish Immunol 5:613–629Google Scholar
  283. 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 43:323–330PubMedPubMedCentralGoogle Scholar
  284. Rabinovich G (2002) Role of galectins in inflammatory and immunomodulatory processes. Biochim Biophys Acta Gen Subj 1572(2–3):274–284Google Scholar
  285. Rabinovich GA, Croci DO (2012) Regulatory circuits mediated by lectin–glycan interactions in autoimmunity and cancer. Immunity 36:322–335PubMedPubMedCentralGoogle Scholar
  286. Rabinovich GA, Gruppi A (2005) Galectins as immunoregulators during infectious processes: from microbial invasion to the resolution of the disease. Parasite Immunol 27(4):103–114PubMedPubMedCentralGoogle Scholar
  287. Raftos D (1996a) Interactions of tunicate immunomodulatory proteins with mammalians cells. Immunol Cell Biol 74:26–31PubMedPubMedCentralGoogle Scholar
  288. Raftos DA (1996b) Adoptive transfer of alloimmune memory in the solitary tunicate, Styela plicata. J Exp Zool 274:310Google Scholar
  289. Raftos DA, Cooper EL (1991) Proliferation of lymphocyte-like cells from the solitary tunicate, Styela clava, in response to allogeneic stimuli. J Exp Zool 260:391–400PubMedPubMedCentralGoogle Scholar
  290. Raftos DA, Tait NN, Briscoe DA (1987a) Allograft rejection and alloimmune memory in the solitary urochordate, Styela plicata. Dev Comp Immunol 11:343–351PubMedPubMedCentralGoogle Scholar
  291. Raftos DA, Tait NN, Briscoe DA (1987b) Cellular basis of allograft rejection in the solitary urochordate, Styela plicata. Dev Comp Immunol 11:713–725PubMedPubMedCentralGoogle Scholar
  292. Raftos DA, Briscoe DA, Tait NN (1988) The mode of recognition of allogeneic tissue in the solitary urochordate Styela plicata. Transplantation 45:1123–1126PubMedPubMedCentralGoogle Scholar
  293. Raftos DA, Stillman DL, Cooper EL (1991a) Interleukin-2 and phytohemagglutinin stimulate proliferation of tunicate cells. Immunol Cell Biol 69:225–234PubMedPubMedCentralGoogle Scholar
  294. 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 88:9518–9522PubMedPubMedCentralGoogle Scholar
  295. Raftos D, Green P, Mahajan D et al (2001) Collagenous lectins in tunicates and the proteolytic activation of complement. Adv Exp Med Biol 484:229–236PubMedPubMedCentralGoogle Scholar
  296. Raftos DA, Nair SV, Robbins J et al (2002) A complement component C3–like protein from the tunicate, Styela plicata. Dev Comp Immunol 26:307–312PubMedPubMedCentralGoogle Scholar
  297. 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:377–386Google Scholar
  298. Raftos DA, Fabbro M, Nair SV (2004) Exocytosis of a complement component C3–like protein by tunicate hemocytes. Dev Comp Immunol 28:181–190PubMedGoogle Scholar
  299. Rast JP, Smith LC, Loza-Coll M, Hibino T, Litman GW (2006) Genomic insights into the immune system of the sea urchin. Science 314:952–956PubMedPubMedCentralGoogle Scholar
  300. Reddy AL, Bryan B, Hidelmann WH (1975) Integumentary allograft versus autograft reactions in Ciona intestinalis: a protochordate species of solitary tunicate. Immunogenetics 1:584–590Google Scholar
  301. Reynold JM, Dong C (2013) Toll-like receptor regulation of effector T lymphocyte function. Trends Immunol 34:511–519Google Scholar
  302. Rinkevich B (2002) The colonial urochordate Botryllus schlosseri: from stem cells and natural tissue transplantation to issues in evolutionary ecology. Bioessays 24:730–740PubMedGoogle Scholar
  303. Rinkevich B (2005) Rejection pattern in botryllid ascidian immunity: the first tier of allorecognition. Can J Zool 83:101–121Google Scholar
  304. Rinkevich B, Rabinowitz C (1993) In vitro culture of blood cells from the colonial protochordate Botryllus schlosseri. In Vitro Cell Dev Biol Anim 29:79–85Google Scholar
  305. 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) 213:717–733Google Scholar
  306. Rinkevich B, Weissman IL (1992) Allogeneic resorption in colonial protochordates—consequences of nonself recognition. Dev Comp Immunol 16:275–286PubMedPubMedCentralGoogle Scholar
  307. Rinkevich B, Tartakover S, Gershon H (1998) Contribution of morula cells to allogeneic responses in the colonial urochordate Botryllus schlosseri. Mar Biol 131:227–236Google Scholar
  308. 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):131–146PubMedPubMedCentralGoogle Scholar
  309. 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 36:718–772PubMedPubMedCentralGoogle Scholar
  310. 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 32:1099–1104Google Scholar
  311. Robinson JM (2008) Reactive oxygen species in phagocytic leukocytes. Histochem Cell Biol 130:281–297PubMedPubMedCentralGoogle Scholar
  312. 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 64:1–12PubMedPubMedCentralGoogle Scholar
  313. Rybakin V, Clemen CS (2005) Coronin proteins as multifunctional regulators of the cytoskeleton and membrane trafficking. BioEssays 27:625–632PubMedPubMedCentralGoogle Scholar
  314. Sano H, Hsu DK, Apgar JR et al (2003) Critical role of galectin-3 in phagocytosis by macrophages. J Clin Invest 112:389–397PubMedPubMedCentralGoogle Scholar
  315. Sasaki N, Ogasawara M, Sekiguchi T et al (2009) Toll-like receptors of the ascidian Ciona intestinalis. J Biol Chem 284:27336–27343PubMedPubMedCentralGoogle Scholar
  316. Satake H, Sasaki N (2010) Comparative overview of Toll-like receptors in lower animals. Zool Sci 27:154–161PubMedPubMedCentralGoogle Scholar
  317. Satake H, Sekiguchi T (2012) Toll-like receptors of deuterostome invertebrates. Front Immunol 3:34. CrossRefPubMedPubMedCentralGoogle Scholar
  318. Satake M, Kawazoe Y, Kasuya A (2003) Hemocytes of Ciona intestinalis express multiple genes involved in innate immune host defense. Biochem Biophys Res Commun 302:207–218PubMedPubMedCentralGoogle Scholar
  319. Sato S, Nieminen J (2004) Seeing strangers or announcing “danger”: galectin-3 in two models of innate immunity. Glycoconj J 19:583–591Google Scholar
  320. 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 159:1611–1619Google Scholar
  321. Satoh N, Satau Y, Davidson B, Levine M (2003) Ciona intestinalis: an emerging model for whole-genome analyses. Trends Genet 19:376–381PubMedPubMedCentralGoogle Scholar
  322. 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 34:2863–2873PubMedPubMedCentralGoogle Scholar
  323. Scofield VL, Nagashima LS (1983) Morphology and genetics of rejection reactions between oozooids from the tunicate Botryllus schlosseri. Biol Bull 165:733–744PubMedPubMedCentralGoogle Scholar
  324. 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 167:4504–4510PubMedPubMedCentralGoogle Scholar
  325. Shaw LM, Olsen BR (1991) FACIT collagens: diverse molecular bridges in extracellular matrices. Trends Biochem Sci 16:191–194PubMedPubMedCentralGoogle Scholar
  326. Shi Y, Massagué J (2003) Mechanisms of TGF-b signaling from cell membrane to the nucleus. Cell 113:685–700PubMedPubMedCentralGoogle Scholar
  327. 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 302:207–218PubMedPubMedCentralGoogle Scholar
  328. Shirae M, Saito Y (2000) A comparison of hemocytes and their phenoloxidase activity among botryllid ascidians. Zool Sci 17:881–891Google Scholar
  329. 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 197:188–197PubMedPubMedCentralGoogle Scholar
  330. 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) 32:1380–1389Google Scholar
  331. Silerova M, Prochazkova P, Joskova R et al (2006) Comparative study of the CCFlike pattern recognition protein in different lumbricid species. Dev Comp Immunol 30:765–771PubMedPubMedCentralGoogle Scholar
  332. Silva MT, Correia-Neves M (2012) Neutrophils and macrophages: the main partners of phagocyte cell systems. Front Immunol 3:174. CrossRefPubMedPubMedCentralGoogle Scholar
  333. Sim RB, Laich A (2000) Serine proteases of the complement system. Biochem Soc Trans 28:545–550PubMedPubMedCentralGoogle Scholar
  334. 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 34:59–68PubMedPubMedCentralGoogle Scholar
  335. Smith VJ, Söderhäll K (1991) A comparison of phenoloxidase activity in the blood of marine invertebrates. Dev Comp Immunol 15:251–261PubMedPubMedCentralGoogle Scholar
  336. Smith LC, Azumi K, Nonaka M (1999) Complement systems in invertebrates. The ancient alternative and lectin pathways. Immunopharmacology 42:107–120PubMedPubMedCentralGoogle Scholar
  337. Söderhäll K, Cerenius L (1998) Role of prophenoxidase-activating system in invertebrate immunity. Curr Opin Immunol 10:23–28Google Scholar
  338. Springer SA, Gagneux P (2013) Glycan evolution in response to collaboration, conflict, and constraint. J Biol Chem 288:6904–6911PubMedPubMedCentralGoogle Scholar
  339. 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 25:353–363PubMedPubMedCentralGoogle Scholar
  340. Suzuki MM, Nishikawa T, Bird A (2005) Genomic approaches reveal unexpected genetic divergence within Ciona intestinalis. J Mol Evol 61:627–635PubMedPubMedCentralGoogle Scholar
  341. Swalla BJ, Smith AB (2008) Deciphering deuterostome phylogeny: molecular, morphological and paleontological perspectives. Philos Trans R Soc 363B:1557–1568Google Scholar
  342. Takeda K, Akira S (2005) Toll-like receptors in innate immunity. Int Immunol 17:1–14PubMedPubMedCentralGoogle Scholar
  343. Taketa DA, De Tomaso AW (2015) Botryllus schlosseri Allorecognition: Tackling the enigma. Dev Comp Immunol 48:254–265Google Scholar
  344. Tarallo R, Sordino P (2004) Time course of programmed cell death in Ciona intestinalis in relation to mitotic activity and MAPK signaling. Dev Dyn 230:251–262PubMedPubMedCentralGoogle Scholar
  345. Tecchio C, Micheletti A, Cassatella MA (2014) Neutrophil-derived cytokines: facts beyond expression. Front Immunol | Molecular Innate Immunity 5:508. CrossRefPubMedPubMedCentralGoogle Scholar
  346. 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 1770:617–629PubMedPubMedCentralGoogle Scholar
  347. 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 10:203–212PubMedPubMedCentralGoogle Scholar
  348. 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 18:3–12PubMedPubMedCentralGoogle Scholar
  349. 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 12:75–81Google Scholar
  350. Trepels T, Zeiher AM, Fichtlscherer S (2006) The endothelium and inflammation. Endothelium 13:423–429PubMedPubMedCentralGoogle Scholar
  351. Tu Q, Cameron RA, Worley KC, Gibbs RA, Davidson EH (2012) Gene structure in the seaurchin Strongylocentrotus purpuratus based on transcriptome analysis. Genome Res 22:2079–2087PubMedPubMedCentralGoogle Scholar
  352. Turner MW (2003) The role of mannose-binding lectin in health and disease. Mol Immunol 40:423–429PubMedPubMedCentralGoogle Scholar
  353. 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 277:15107–15112PubMedPubMedCentralGoogle Scholar
  354. Valanne S, Wang J-H, Rämet M (2011) The Drosophila Toll signaling pathway. J Immunol 186:649–656PubMedPubMedCentralGoogle Scholar
  355. Van Lookeren Campagne M, Weismann C, Brown EJ (2007) Macrophage complement receptors and pathogen clearance. Lit Rev Cell Microbiol 9:2095–2102Google Scholar
  356. Vanlangenakker N, Vanden Berghe T, Vandenabeele P (2012) Many stimuli pull the necrotic trigger, an overview. Cell Death Differ 19:75–86PubMedPubMedCentralGoogle Scholar
  357. 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 14Google Scholar
  358. 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 946:21–36Google Scholar
  359. Vasta GR, Hunt JC, Marchalonis JJ et al (1986) Galactosyl-binding lectins from the tunicate Didemnum candidum. Purification and physicochemical characterization. J Biol Chem 261:9174–9181PubMedPubMedCentralGoogle Scholar
  360. 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 23:401–420PubMedPubMedCentralGoogle Scholar
  361. Vasta GR, Ahmed H, Odom EW (2004) Structural and functional diversity of lectin repertoires in invertebrates, protochordates and ectothermic vertebrates. Curr Opin Struct Biol 14:617–630PubMedPubMedCentralGoogle Scholar
  362. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  363. Vestweber D, Blanks JE (1999) Mechanisms that regulate the function of the selectins and their ligands. Physiol Rev 79:181–213PubMedPubMedCentralGoogle Scholar
  364. 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 402–407Google Scholar
  365. 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 1577:38–44PubMedPubMedCentralGoogle Scholar
  366. 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 32:682–692PubMedPubMedCentralGoogle Scholar
  367. 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 32:101–109PubMedPubMedCentralGoogle Scholar
  368. 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 41:59–67PubMedPubMedCentralGoogle Scholar
  369. 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 8:63235Google Scholar
  370. 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 126:6–11PubMedPubMedCentralGoogle Scholar
  371. 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 48:129–137PubMedPubMedCentralGoogle Scholar
  372. 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 55:102–110PubMedPubMedCentralGoogle Scholar
  373. 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 77:174–183PubMedPubMedCentralGoogle Scholar
  374. 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 67:107–116PubMedPubMedCentralGoogle Scholar
  375. 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 311–330Google Scholar
  376. 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 207:2409–2416PubMedPubMedCentralGoogle Scholar
  377. 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 3:456–464PubMedPubMedCentralGoogle Scholar
  378. Voskoboynik A, Neff NF, Sahoo D et al (2013a) The genome sequence of the colonial chordate, Botryllus schlosseri. elife 2:00569Google Scholar
  379. Voskoboynik A, Newman AM, Corey DM et al (2013b) Identification of a colonial chordate histocompatibility gene. Science 341(6144). PubMedPubMedCentralGoogle Scholar
  380. 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 29:458–470PubMedPubMedCentralGoogle Scholar
  381. 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 34:81–90PubMedPubMedCentralGoogle Scholar
  382. 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 11:23–33PubMedPubMedCentralGoogle Scholar
  383. Wallis R (2007) Interactions between mannose-binding lectin and MASPs during complement activation by the lectin pathway. Immunobiology 212:289–299PubMedPubMedCentralGoogle Scholar
  384. Wang J, Slungaard A (2006) Role of eosinophil peroxidase in host defense and disease pathology. Arch Biochem Biophys 15:256–260Google Scholar
  385. 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 95:3183–3190PubMedPubMedCentralGoogle Scholar
  386. Ward-Kavanagh L, Lin WW, Šedý JS et al (2016) The TNF receptor superfamily in costimulating and coinhibitory responses. Immunity 44:1005–1019PubMedPubMedCentralGoogle Scholar
  387. 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 25:821–852PubMedPubMedCentralGoogle Scholar
  388. Weissman I (2000) Stem cells: units of development, review units of regeneration, and units in evolution. Cell 100:157–168PubMedPubMedCentralGoogle Scholar
  389. Wright RK, Cooper EL (1983) Inflammatory reactions of the protochordata. Am Zool 23:205–211Google Scholar
  390. 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):1050–1056PubMedGoogle Scholar
  391. Wynn TA, Vannella KM (2016) Macrophages in tissue repair, regeneration, and fibrosis. Immunity 44:450–462PubMedPubMedCentralGoogle Scholar
  392. Yousef GM, Diamandis EP (2003) An overview of the kallikrein gene families in humans and other species: emerging candidate tumour markers. Clin Biochem 36:443–452PubMedPubMedCentralGoogle Scholar
  393. 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 17:774–783PubMedPubMedCentralGoogle Scholar
  394. Zanoni I, Ostuni R, Marek LR et al (2011) CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 147:868–880PubMedPubMedCentralGoogle Scholar
  395. 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 282:17041–17052PubMedPubMedCentralGoogle Scholar
  396. 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 356:450–456PubMedPubMedCentralGoogle Scholar
  397. Zelensky AN, Gready JE (2005) The C-type lectin–like domain superfamily. FEBS J 272:6179–6217PubMedPubMedCentralGoogle Scholar
  398. 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 32:1362–1373PubMedPubMedCentralGoogle Scholar
  399. Zhang X, Angkasekwinai P, Dong C et al (2011) Structure and function of interleukin-17 family cytokines. Protein Cell 2:26–40PubMedPubMedCentralGoogle Scholar
  400. 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 76:267–283PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Nicolò Parrinello
    • 1
    Email author
  • Matteo Cammarata
    • 1
  • Daniela Parrinello
    • 1
  1. 1.Department of Earth and Marine Science, Marine Immunobiology LaboratoryUniversity of PalermoPalermoItaly

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