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Immune Reactions in the Vertebrates' Closest Relatives, the Urochordates

  • Konstantin Khalturin
  • Ulrich Kürn
  • Thomas C. G. Bosch
Part of the Nucleic Acids and Molecular Biology book series (NUCLEIC, volume 21)

Currently existing urochordates (sea squirts) and vertebrates diverged in evolution around 570 million years (myr) ago. Phylogenetic analyses based on molecular data provide compelling evidence that these animals are the closest living relatives of vertebrates. Urochordares, therefore, are of critical importance for understanding the origin of vertebrate immune system. For a number of species a large body of molecular data is now available. An extensive EST project and the draft genome sequences of Ciona intestinalis and C. savignyi allow rapid “in silico” searches for immunorelevant molecules. Recent data convincingly demonstrate that urochordates possess nearly full repertoire of vertebrate innate immune system, but totally lack most of the components of an adaptive immunity such as MHC, TCRs and antibodies. In this review we show that knowledge of immunity in lower vertebrate and invertebrate species is now rapidly increasing. Elucidating the details of the origin of the immune systems from a comparative point of view in vertebrate's closest relatives, may finally lead to a better understanding of our own immune system.

Keywords

Antimicrobial Peptide Adaptive Immune System Membrane Cofactor Protein Close Living Relative Vertebrate Immune System 
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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References

  1. Ammerman JW, Fuhrman JA, Hagstrom A, Azam F (1984) Bacterioplankton growth in seawater. 1. Growth kinetics and cellular characteristics in seawater cultures. Mar Ecol Prog Ser 18:31–39CrossRefGoogle Scholar
  2. Arai M, Suzuki-Koike M, Ohtake S, Ohba H, Tanaka K, Chiba J (2001) Common cell-surface antigens functioning in self-recognition reactions by both somatic cells and gametes in the solitary ascidian Halocynthia roretzi. Microbiol Immunol 45:857–866PubMedGoogle Scholar
  3. Azumi K, Yokosawa H, Ishi S (1990a) Haolcyamines: novel antimicrobial tetrapeptide-like substances isolated from the hemocytes of the solitary ascidian Halocynthia roretzi. Biochemistry 29:156–165CrossRefGoogle Scholar
  4. Azumi K, Yokosawa H, Ishii S (1990b) Presence of 3, 4-dihydroxyphenylalanine containing peptides in hemocytes of the ascidian Halocynthia roretzi. Experientia 46:1020–1023CrossRefGoogle Scholar
  5. Azumi K, Yoshimizu M, Suzuki S, Ezura Y, Yokosawa H (1990c) Inhibitory effect of halocyamine, an antimicrobial substance from ascidian hemocytes, on the growth of fish viruses and marine-bacteria. Experientia 46:1066–1068PubMedCrossRefGoogle Scholar
  6. Azumi K, De Santis R, De Tomaso A, Rigoutsos I, Yoshizaki F, Pinto MR, et al (2003) Genomic analysis of immunity in a Urochordate and the emergence of the vertebrate immune system: ‘waiting for Godot’. Immunogenetics 55:570–581PubMedCrossRefGoogle Scholar
  7. Ban S, Harada Y, Yokosawa H, Sawada H (2005) Highly polymorphic vitelline-coat protein HaVC80 from the ascidian, Halocynthia aurantium: structural analysis and involvement in self/nonself recognition during fertilization. Dev Biol 286:440–451PubMedCrossRefGoogle Scholar
  8. Bancroft FW (1903) Variation and fusion of colonies in compound ascidians. Proc Calif Acad Sci 3:137–186Google Scholar
  9. Davidson B, Swalla BJ (2002) A molecular analysis of ascidian metamorphosis reveals activation of an innate immune response. Development 129:4739–4751PubMedCrossRefGoogle Scholar
  10. De Tomaso AW, Weissman IL (2003) Initial characterization of a protochordate histocompatibility locus. Immunogenetics 55:480–490PubMedCrossRefGoogle Scholar
  11. De Tomaso AW, Nyholm SV, Palmeri KJ, Ishizuka KJ, Ludington WB, Mitchel K, Weissman IL (2005) Isolation and characterization of a protochordate histocompatibility locus. Nature 438:454–459PubMedCrossRefGoogle Scholar
  12. Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, DeTomaso A, Davidson B, Di Gregorio A, Gelpke M, Goodstein DM, et al (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2167PubMedCrossRefGoogle Scholar
  13. Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965–968PubMedCrossRefGoogle Scholar
  14. Endo Y, Nonaka M, Saiga H, Kakinuma Y, Matsushita A, Takahashi M, Matsushita M, Fujita F (2003) Origin of mannose-binding lectin-associated serine protease (MASP)-1 and MASP-3 involved in the lectin complement pathway traced back to the invertebrate, Amphioxus. J Immunol 170:4701–4707PubMedGoogle Scholar
  15. Fujita T (2002) Evolution of the lectin-complement pathway and its role in innate immunity. Nat Rev Immunol 2:346–353PubMedCrossRefGoogle Scholar
  16. Hirose E (2003) Colonial allorecognition, hemolytic rejection, and viviparity in botryllid ascidians. Zool Sci 20:387–394PubMedCrossRefGoogle Scholar
  17. Janeway CA Jr, et al (2005) Immunobiology: the immune system in health and disease, 6th edn. Garland, New YorkGoogle Scholar
  18. Jang W, Kim K, Lee Y, Nam M, Lee I (2002) Halocidin: a new antimicrobial peptide from hemocytes of the solitary tunicate, Halocynthia aurantium. FEBS Lett 521:81–86PubMedCrossRefGoogle Scholar
  19. Kawamura K, Fujita H, Nakauchi M (1989) Concanavalin A modifies allo-specific sperm-egg interactions in the ascidian, Ciona intestinalis. Develop Growth Differ 31:493–501CrossRefGoogle Scholar
  20. Kenjo A, Takahashi M, Matsushita M, Endo Y, Nakata M, Mizuochi T, Fujita T (2001) Cloning and characterization of novel ficolins from the solitary ascidian, Halocynthia roretzi. J Biol Chem 276:19959–19965PubMedCrossRefGoogle Scholar
  21. Khalturin K, Bosch TCG (2007) Self/nonself discrimination at the basis of chordate evolution: limits on molecular conservation. Curr Opin Immunol 19:4–9PubMedCrossRefGoogle Scholar
  22. 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. Proc Natl Acad Sci USA 100:622–627PubMedCrossRefGoogle Scholar
  23. Khalturin K, Pancer Z, Cooper MD, Bosch TCG (2004) Recognition strategies in the innate immune system of ancestral chordates. Mol Immunol 41:1077–1087PubMedCrossRefGoogle Scholar
  24. Khalturin K, Kurn U, Pinnow N, Bosch TCG (2005) Towards a molecular code for individuality in the absence of MHC: screening for individually variable genes in the urochordate Ciona intestinalis. Dev Comp Immunol 29:759–773PubMedCrossRefGoogle Scholar
  25. Klein J (2006) The grapes of incompatibility. Dev Cell 10:2–4PubMedCrossRefGoogle Scholar
  26. Kürn U, Sommer F, Hemmrich G, Bosch TCG, Khalturin K (2006) Allorecognition in urochordates: identification of a highly variable complement receptor-like protein expressed in follicle cells of Ciona. Dev Comp Immunol 31:360–371PubMedCrossRefGoogle Scholar
  27. Kürn U, Sommer F, Bosch TC, Khalturin K (2007) In the urochordate Ciona intestinalis zona pellucida domain proteins vary among individuals. Dev Comp Immunol doi:10.1016/j.dci.2007.03.011Google Scholar
  28. Lambert G (2005) Ecology and natural history of protochordates. Can J Zool 83:34–50CrossRefGoogle Scholar
  29. Lee I, Cho Y, Lehrer R (1997a) Effects of pH and salinity on the antimicrobial properties of clavanins. Infect Immun 65:2898–2903PubMedGoogle Scholar
  30. Lee I, Zhao C, Cho Y, Harwig S, Cooper E, Lehrer R (1997b) Clavanins, helical antimicrobial peptides from tunicate hemocytes. FEBS Lett 400:158–162PubMedCrossRefGoogle Scholar
  31. Lee IH, Cho Y, Lehrer RI (1997c) Styelins, broad spectrum antimicrobial peptides from the solitary tunicate, Styela clava. Comp Biochem Physiol 118B:515–521Google Scholar
  32. Lee I, Lee Y, Kim C, Hong C, Menzel LT, Boo L, Pohl J, Sherman M, Waring A, Lehrer R (2001a) Dicynthaurin: an antimicrobial peptide from hemocytes of the solitary tunicate, Halocynthia aurantium. Biochim Biophys Acta 1527:141–148PubMedGoogle Scholar
  33. Lee I, Zhao C, Nguyen T, Menzel L, Waring A, Sherman M, Lehrer R (2001b) Clavaspirin, an antimicrobial and hemolytic peptide from Styela clava. J Peptide Res 58:445–456CrossRefGoogle Scholar
  34. Liszewski MK, Post TW, Atkinson JP (1991) Membrane cofactor protein (MCP or CD46): newest member of the regulators of complement activation gene cluster. Annu Rev Immunol 9:431–455PubMedCrossRefGoogle Scholar
  35. Magor BG, De Tomaso A, Rinkevich B, Weissman IL (1999) Allorecognition in colonial tunicates: protection against predatory cell lineages? Immunol Rev 167:69–79PubMedCrossRefGoogle Scholar
  36. Marino R, Kimura Y, De Santis R, Lambris JD, Pinto MR (2002) Complement in urochordates: cloning and characterization of two C3-like genes in the ascidian Ciona intestinalis. Immunogenetics, 53:1055–1064PubMedCrossRefGoogle Scholar
  37. Menzel L, Lee I, Sjostrand B, Lehrer R (2002) Immunolocalization of clavanins in Styela clava hemocytes. Dev Comp Immunol 26:505–515PubMedCrossRefGoogle Scholar
  38. Murabe N, Hoshi M (2002) Re-examination of sibling cross-sterility in the ascidian, Ciona intestinalis: genetic background of the self-sterility. Zool Sci 19:527–538PubMedCrossRefGoogle Scholar
  39. Naranjo SA, Carballo JL, Garcia-Gomez G (1996) Effects of environmental stress on ascidian populations in Algeciras Bay (southern Spain). Possible marine bioindicators? Mar Ecol Prog Ser 144:119–131CrossRefGoogle Scholar
  40. Natsuume-Sakai S, Kaidoh T, Nonaka M, Takahashi M (1980) Structural polymorphism of murine C4 and its linkage to H-2. J Immunol 1980 124:2714–2720PubMedGoogle Scholar
  41. Nonaka M, Kimura A (2006) Genomic view of the evolution of the complement system. Immunogenetics 58:701–713PubMedCrossRefGoogle Scholar
  42. Nonaka M, Yoshizaki F (2004) Primitive complement system of invertebrates. Immunol Rev 198:203–215PubMedCrossRefGoogle Scholar
  43. Oka H, Watanabe H (1957) Colony specificity in compound ascidians as tested by fusion experiments (a preliminary report). Proc Jpn Acad 33:657–659Google Scholar
  44. Oka K, Watanabe H (1960) Problems of colony specificity in compound ascidians. Bull Mar Biol Stn Asamushi 10:153–155Google Scholar
  45. Parrinello N, Cammarata M, Arizza V (1996) Univacuolar refractile hemocytes from the tunicate Ciona intestinalis are cytotoxic for mammalian erythrocytes in vitro. Biol Bull 190:418–425PubMedCrossRefGoogle Scholar
  46. Reddy AL, Bryan B, Hildemann WH (1975) Integumentary allograft versus autograft reactions in Ciona intestinalis: a protochordate species of solitary tunicate. Immunogenetics 1:584–590CrossRefGoogle Scholar
  47. Sahu A, Lambris JD (2001) Structure and biology of complement protein C3, a connecting link between innate and acquired immunity. Immunol Rev 180:35–48PubMedCrossRefGoogle Scholar
  48. Saito Y, Hirose E, Watanabe H (1994) Allorecognition in compound ascidians. Int J Dev Biol 38:237–247PubMedGoogle Scholar
  49. Satou Y, Yamada L, Mochizuki Y, Takatori N, Kawashima T, Sasaki A, Hamaguchi M, Awazu S, Yagi K, Sasakura Y, Nakayama A, Ishikawa H, Inaba K, Satoh N (2002) A cDNA resource from the basal chordate Ciona intestinalis. Genesis 33:153–154PubMedCrossRefGoogle Scholar
  50. Sawada H (2002) Ascidian sperm lysin system. Zool Sci 19:139–151PubMedCrossRefGoogle Scholar
  51. Sawada H, Tanaka E, Ban S, Yamasaki C, Fujino J, Ooura K, et al (2004) Self/nonself recognition in ascidian fertilization: vitelline coat protein HrVC70 is a candidate allorecognition molecule. Proc Natl Acad Sci USA 101:15615–15620PubMedCrossRefGoogle Scholar
  52. Scofield VL, Schlumpberger JM, West LA, Weissman IL (1982) Protochordate allorecognition is controlled by a MHC-like gene system. Nature 295:499–502PubMedCrossRefGoogle Scholar
  53. Sekine H, Kenjo A, Azumi K, Ohi G, Takahashi M, Kasukawa R, Ichikawa N, Nakata M, Mizuochi T, Matsushita M, Endo Y, Fujita T (2001) An ancient lectin-dependent complement system in an ascidian: novel lectin isolated from the plasma of the solitary ascidian, Halocynthia roretzi. J Immunol 167:4504–4510PubMedGoogle Scholar
  54. Taylor SW, Kammerer B, Bayer E (1997) New perspectives in the chemistry and biochemistry of the tunichromes and related compounds. Chem Rev 97:333–346PubMedCrossRefGoogle Scholar
  55. Tincu JA, Taylor SW (2004) Antimicrobial peptides from marine invertebrates. Antimicrob Agents Chemother 48:3645–3654PubMedCrossRefGoogle Scholar
  56. Tincu JA, Craig AG, Taylor SW (2000) Plicatamide: a lead to the biosynthetic origins of the tunichromes? Biochem Biophys Res Commun 270:421–424PubMedCrossRefGoogle Scholar
  57. Tincu JA, Menzel LP, Azimov R, Sands J, Hong T, Waring AJ, Taylor SW, Lehrer RI (2003) Plicatamide, an antimicrobial octapeptide from Styela plicata hemocytes. J Biol Chem 278:13546–13553PubMedCrossRefGoogle Scholar
  58. Vanderpuye OA, Labarrere CA, McIntyre JA (1992) The complement system in human reproduction. Am J Reprod Immunol 27:145–155PubMedGoogle Scholar
  59. Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415:389–395PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  • Konstantin Khalturin
    • 1
  • Ulrich Kürn
    • 1
  • Thomas C. G. Bosch
    • 1
  1. 1.Zoological InstituteChristian-Albrechts-UniversityKielGermany

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