Urochordate Immunity

  • Masaru Nonaka
  • Honoo Satake
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 708)


This chapter provides a short review of the immune system of urochordates, the closest living relative of vertebrates. Since adaptive immunity is a unique property of vertebrates, urochordates rely exclusively on innate immunity to recognize and eliminate pathogens. Here we discuss three immune systems of urochordates which show different evolutionary relationship with the vertebrate immune system. Urochordate Toll-like receptors (TLR) show a clear orthologous relationship with vertebrate counterparts, although they show unique characteristics most likely gained in the urochordate lineage. The urochordate complement system also shows orthologous relationship with the vertebrate complement system. From the structural and functional viewpoints, it seems to represent a more primitive state of the vertebrate complement system without any major deviation. In contrast, the allorecognition systems of urochordates show no evolutionary relationship with any invertebrate or vertebrate systems, suggesting that they were invented in the urochordate lineage.


Ement System Vertebrate Immune System Ciona Genome Histocompatibility Locus Middle Intestine 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 1.
    Flajnik MF, Kasahara M. Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat Rev Genet 2010; 11:47–59.PubMedCrossRefGoogle Scholar
  2. 2.
    Delsuc F, Brinkmann H, Chourrout D et al. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 2006; 439:965–968.PubMedCrossRefGoogle Scholar
  3. 3.
    Azumi K, De Santis R, De Tomaso A et al. Genomic analysis of immunity in a Urochordate and the emergence of the vertebrate immune system: “waiting for Godot”. Immunogenetics 2003; 55:570–581.PubMedCrossRefGoogle Scholar
  4. 4.
    Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol 2004; 4:4499–4511.CrossRefGoogle Scholar
  5. 5.
    Dunne A, O*#x2019;Neill LA. Adaptor usage and Toll-like receptor signaling specificity. FEBS Lett 2005; 579:3330–3335.PubMedCrossRefGoogle Scholar
  6. 6.
    Shimazu R, Akashi S, Ogata H et al. MD-2, a molecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4. J Exp Med 1999; 189:1777–1782.PubMedCrossRefGoogle Scholar
  7. 7.
    Matsuo A, Oshiumi H, Tsujita T et al. Teleost TLR22 recognizes RNA duplex to induce IFN and protect cells from birnaviruses. J Immunol 2008; 181:3474–3485.PubMedGoogle Scholar
  8. 8.
    Takano T, Kondo H, Hirono I et al. Molecular cloning and characterization of Toll-like receptor 9 in Japanese flounder, Paralichthys olivaceus. Mol Immunol 2007; 44:1845–1853.PubMedCrossRefGoogle Scholar
  9. 9.
    Yu Y, Zhong Q, Li C et al. Isolation and characterization of Toll-like receptor 9 in half-smooth tongue sole Cynoglossus semilaevis. Fish Shellfish Immunol 2009; 26:492–499.PubMedCrossRefGoogle Scholar
  10. 10.
    Ishii A, Matsuo A, Sawa H et al. Lamprey TLRs with properties distinct from those of the variable lymphocyte receptors. J Immunol 2007; 178:397–406.PubMedGoogle Scholar
  11. 11.
    Huang S, Yuan S, Guo L et al. Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity. Genome Res 2008; 18:1112–1126.PubMedCrossRefGoogle Scholar
  12. 12.
    Hibino T, Loza-Coll M, Messier C et al. The immune gene repertoire encoded in the purple sea urchin genome. Dev Biol 2006; 300:349–365.PubMedCrossRefGoogle Scholar
  13. 13.
    Davidson CR, Best NM, Francis JW et al. Toll-like receptor genes (TLRs) from Capitella capitata and Helobdella robusta (Annelida). Dev Comp Immunol 2008; 32:608–612.PubMedCrossRefGoogle Scholar
  14. 14.
    Bosch TC, Augustin R, Anton-Erxleben F et al. Uncovering the evolutionary history of innate immunity: the simple metazoan Hydra uses epithelial cells for host defence. Dev Comp Immunol 2009; 33:559–569.PubMedCrossRefGoogle Scholar
  15. 15.
    Sasaki N, Ogasawara M, Sekiguchi T et al. Toll-like receptors of the ascidian Ciona intestinalis: prototypes with hybrid functionalities of vertebrate Toll-like receptors. J Biol Chem 2009; 284:27336–27343.PubMedCrossRefGoogle Scholar
  16. 16.
    Volanakis JE. Overview of the complement system. In: Volanakis JE, Frank MM, eds. The Human Complement System in Health and Disease. New York: Marcel Dekker, Inc., 1998:9–32.Google Scholar
  17. 17.
    Kimura A, Sakaguchi E, Nonaka M. Multi-component complement system of Cnidaria: C3, Bf and MASP genes expressed in the endodermal tissues of a sea anemone, Nematostella vectensis. Immunobiology 2009;214:165–178.PubMedCrossRefGoogle Scholar
  18. 18.
    Nonaka M, Kimura A. Genomic view of the evolution of the complement system. Immunogenetics 2006; 58:701–713.PubMedCrossRefGoogle Scholar
  19. 19.
    Nonaka M, Azumi K, Ji X et al. Opsonic complement component C3 in the solitary ascidian, Halocynthia roretzi. J Immunol 1999; 162:387–391.PubMedGoogle Scholar
  20. 20.
    Marino R, Kimura Y, De Santis R et al. Complement in urochordates: cloning and characterization of two C3-like genes in the ascidian Ciona intestinalis. Immunogenetics 2002; 53:1055–1064.PubMedCrossRefGoogle Scholar
  21. 21.
    Yoshizaki FY, Ikawa S, Satake M et al. Structure and the evolutionary implication of the triplicated complementfactor B genes of aurochordateascidian, Cionaintestinalis. Immunogenetics 2005; 56:930–942.PubMedCrossRefGoogle Scholar
  22. 22.
    Ji X, Azumi K, Sasaki M et al. 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 USA 1997; 94:6340–6345.PubMedCrossRefGoogle Scholar
  23. 23.
    Bonura A, Vizzini A, Salerno G et al. 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 2009; 46:2389–2394.PubMedCrossRefGoogle Scholar
  24. 24.
    Kenjo A, Takahashi M, Matsushita M et al. Cloning and characterization of novel ficolins from the solitary ascidian, Halocynthia roretzi. J Biol Chem 2001; 276:19959–19965.PubMedCrossRefGoogle Scholar
  25. 25.
    Miyazawa S, Azumi K, Nonaka M. Cloning and characterization of integrin alpha subunits from the solitary ascidian, Halocynthia roretzi. J Immunol 2001; 166:1710–1715.PubMedGoogle Scholar
  26. 26.
    Miyazawa S, Nonaka M. Characterization of novel ascidian beta integrins as primitive complement receptor subunits. Immunogenetics 2004; 55:836–844.PubMedCrossRefGoogle Scholar
  27. 27.
    Sekine H, Kenjo A, Azumi K et al. An ancient lectin-dependent complement system in an ascidian: novel lectin isolated from the plasma of the solitary ascidian, Halocynthia roretzi. J Immunol 2001; 167:4504–4510.PubMedGoogle Scholar
  28. 28.
    Pinto MR, Chinnici CM, Kimura Y et al. CiC3-la-mediated chemotaxis in the deuterostome invertebrate Ciona intestinalis (Urochordata). J Immunol 2003; 171:5521–5528.PubMedGoogle Scholar
  29. 29.
    McKitrick TR, De Tomaso AW. Molecular mechanisms of allorecognition in a basal chordate. Semin Immunol 2009; 22:34–38.PubMedCrossRefGoogle Scholar
  30. 30.
    Harada Y, Sawada H. Allorecognition mechanisms during ascidian fertilization. Int J Dev Biol 2008; 52:637–645.PubMedCrossRefGoogle Scholar
  31. 31.
    De Tomaso AW, Nyholm SV, Palmeri KJ et al. Isolation and characterization of a protochordate histocompatibility locus. Nature 2005; 438:454–459.PubMedCrossRefGoogle Scholar
  32. 32.
    Nyholm SV, Passegue E, Ludington WB et al fester, A candidate allorecognition receptor from a primitive chordate. Immunity 2006; 25:163–173.PubMedCrossRefGoogle Scholar
  33. 33.
    Harada Y, Takagaki Y, Sunagawa M et al. Mechanism of self-sterility in a hermaphroditic chordate. Science 2008; 320:548–550.PubMedCrossRefGoogle Scholar
  34. 34.
    Sawada H, Tanaka E, Ban S et al. Self nonself recognition in ascidian fertilization: vitelline coat protein HrVC70 is a candidate allorecognition molecule. Proc Natl Acad Sci USA 2004; 101:15615–15620.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Department of Biological Sciences, Graduate School of ScienceThe University of TokyoHongoJapan
  2. 2.Suntory Institute for Bioorganic ResearchMishimaJapan

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