Speculations on the Relationships of Two Botryllus Allo-Recognition Reactions—Colony Specificity and Resorption—To Vertebrate Histocompatibility

  • Irving L. Weissman
  • Virginia Scofield
  • Yasunori Saito
  • Heather Boyd
  • Baruch Rinkevich
Part of the Bodega Marine Laboratory Marine Science Series book series (BMSS)


The objective of this essay is to consider functions of the vertebrate major histocompatibility complex (MHC), especially in comparison to allorecognition in colonial tunicates. Elsewhere Burnet (1971), and our group (Scofield et al. 1982b) have provided some theoretical and experimental bases for making such a comparison.


Major Histocompatibility Complex Major Histocompatibility Complex Molecule Major Histocompatibility Complex Gene Germinal Vesicle Breakdown Major Histocompatibility Complex Polymorphism 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Babbitt, B. P., P. M. Allen, G. Matsueda, E. Haber and E. R. Unanue. 1985. Binding of immunogenic peptides to Ia histocompatibility molecules. Nature317: 359–361.PubMedCrossRefGoogle Scholar
  2. Berrill, N. J. 1935. Studies in tunicate development. IV. Asexual reproduction. Phil. Trans. R Soc. Lond. Biol. Sci.225: 327–379.CrossRefGoogle Scholar
  3. Bevan, M. J. 1977. Killer cells reactive to altered-self antigens can also be alloreactive. Proc. Natl. Acad. Sci. USA74: 2094–2098.PubMedCrossRefGoogle Scholar
  4. Bjorkman, P., M. A. Saper, B. Samraoui, W. S. Bennett, J. L. Strominger and D. C. Wiley. 1987. The foreign antigen binding site and T cell recognition of regions of Class I histocompatibility antigens. Nature329: 512–518.PubMedCrossRefGoogle Scholar
  5. Boyd, H. C., S. K. Brown, J. A. Harp and I. L. Weissman. 1986. Growth and sexual maturation of laboratory-cultured Monterey Botryllus schlosseri. Biol. Bull. 170: 91–109.CrossRefGoogle Scholar
  6. Bruce, H. M. 1959. An exteroceptive block to pregnancy in the mouse. Nature184: 105.PubMedCrossRefGoogle Scholar
  7. Burnet, F. M. 1971. “Self-recognition” in colonial marine forms and flowering plants in relation to the evolution of immunity. Nature 232:230–235.PubMedCrossRefGoogle Scholar
  8. Buss, L. W. 1981. Group living, competition, and the evolution of cooperation in a sessile invertebrate. Science213: 1012–1014.PubMedCrossRefGoogle Scholar
  9. Buss, L. W. 1982. Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc. Natl. Acad. Sci. USA79: 5337–5341.PubMedCrossRefGoogle Scholar
  10. Buss, L. W. and D. R. Green. 1985. Histoincompatibility in vertebrates: The relict hypothesis. Dey. Comp. Immunol9: 191–201.CrossRefGoogle Scholar
  11. Clayberger, C., P. Parham, J. Rothbard, D. S. Ludwig, G. K. Schoolnik and A. M. Krensky. 1987. HLA-A2 peptides can regulate cytolysis by human allogenic T lymphocytes. Nature330: 763–765.PubMedCrossRefGoogle Scholar
  12. Doherty, P. C., R. V. Blanden and R. M. Zinkernagel. 1976. Specificity of virusimmune effector T cells for H-2K or H-2D compatible interactions: Implications for H-antigen diversity. Transplant. Rev.29: 89–124.PubMedGoogle Scholar
  13. Fink, P. J. and M. J. Bevan. 1978. H-2 antigens of the thymus determine lymphocyte specificity. J. Exp. Med.148: 766–775.PubMedCrossRefGoogle Scholar
  14. Flajnik, M. F., J. F. Kaufman, P. Riegert and L. Du Pasquier. 1984. Identification of class I major histocompatibility complex encoded molecules in the amphibian Xenopus. Immunogenetics20: 433–442.CrossRefGoogle Scholar
  15. Grosberg, R. K. 1981. Competitive ability influences habitat choice in marine invertebrates. Nature290: 700–702.CrossRefGoogle Scholar
  16. Grosberg, R. K. 1982. Ecological, genetical and developmental factors regulating life history variation within a population of the colonial ascidian Botryllus schlossen (Pallas) Savigny. Ph.D. dissertation. Yale University.Google Scholar
  17. Grosberg, R. K. and J. F. Quinn. 1986. The genetic control and consequences of kin recognition by the larvae of a colonial marine invertebrate. Nature322: 456–459.CrossRefGoogle Scholar
  18. Guillet, J.-G., M.-Z. Lai, T. J. Briner, S. Buus, A. Sette, H. M. Grey, J. A. Smith and M. L. Gefter. 1987 Immunological self, nonself discrimination. Science235: 865–870.PubMedCrossRefGoogle Scholar
  19. Harp, J. A., C. B. Tsuchida, I. L. Weissman and V. Scofield. 1987. Auroreactive blood cells and programmed cell death in growth and development of protochordates. J. Exp. Zool (In press).Google Scholar
  20. Howard, J. 1984. Presentation at a symposium/course entitled “Evolution and immunity,” August 1984, Hopkins Marine Station, Pacific Grove, California.Google Scholar
  21. Isakovic, K., S. B. Smith, and B. H. Waksman. 1965. Role of the thymus in tolerance. I. Tolerance to bovine gamma globulin in thymectomized, irradiated rats grafted with thymus from tolerant donars. J. Exp. Med.122: 1103–1123.PubMedCrossRefGoogle Scholar
  22. Karakashian, S. and R. Milkman 1967. Colony fusion compatibility types in Botryllus schlossen. BioL Bull. 133: 473.Google Scholar
  23. Klein, J. 1975. Biology of the Mouse Histocompatibility-2 Complex. Springer, New York.Google Scholar
  24. Maryanski, J. L., P. Pala, G. Corradin, B. R. Jordan and J.-C. Cerottini. 1986. H-2-restricted cytolytic T cells specific for HLA can recognize a synthetic HLA peptide. Nature324: 578–579.PubMedCrossRefGoogle Scholar
  25. Milkman, R. 1967. Genetic and developmental studies on Botryllus schlossen. Biol. Bull. 132: 229–243.CrossRefGoogle Scholar
  26. Mukai, H. and H. Watanabe. 1976. Relation between sexual and a sexual reproduction in the compound ascidian, Botryllus primigenus. Sci. Rep. Fac. Educ. Gunma Univ.25: 61–79.Google Scholar
  27. Oka, H. and H. Watanabe. 1957. Colony-specificity in compound ascidians as tested by fusion experiments. Proc. Jpn. Acad.33: 657–659.Google Scholar
  28. Raviola, E. and M. J. Karnovsky. 1972. Evidence for a blood-thymus barrier using electron-opaque tracers. J. Exp. Med136: 466–498.PubMedCrossRefGoogle Scholar
  29. Rinkevich, B. and I. L. Weissman. 1987a. A long-term study on fused subclones of a compound ascidian. The resorption phenomenon. J. Zool.213: 717–733.CrossRefGoogle Scholar
  30. Rinkevich, B. and I. L. Weissman. 1987b. Chimeras in colonial invertebrates: a synergistic symbiosis or somatic-and germ-cell parasitism? Symbiosis4: 117–134.Google Scholar
  31. Rinkevich, B. and I. L. Weissman. 1987c. The fate of Botrylluslarvae cosettled nearby parental colonies: beneficial or deleterious consequences? BioL Bull. 173: 474–488.CrossRefGoogle Scholar
  32. Sabbadin, A. 1960. Ulteriori notizie sull’allevamento e sulla biologia dei Botrilli in condizioni di laboratorio. Arch. Ocean. Limn.12: 97–107.Google Scholar
  33. Saito, Y. and H. Watanabe. 1982. Colony specificity in the compound ascidian, Botryllus scalars. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 58: 105–108.CrossRefGoogle Scholar
  34. Schlumpberger, J. M., I. L. Weissman and V. L. Scofield. 1984. Monoclonal antibodies developed against Botryllusblood cell antigens bind to cells of distinct lineages during embryonic development. J. Exp. Zool229: 205–213.CrossRefGoogle Scholar
  35. Scofield, V. L. and L. S. Nagashima. 1983. Morphology and genetics of rejection reactions between oozooids from the tunicate Botryllus schlossen. Biol. Bull. 165: 733–744.CrossRefGoogle Scholar
  36. Scofield, V. L. and I. L. Weissman. 1981. Allorecognition in biological systems. Dey. Comp. Immunol.5 (suppl. 1): 23–28.CrossRefGoogle Scholar
  37. Scofield, V. L., J. M. Schlumpberger and I. L. Weissman. 1982a. Colony specificity in the colonial tunicate Botryllusand the origins of vertebrate immunity. Am. Zool.22: 783–794.Google Scholar
  38. Scofield, V. L., J. M. Schlumpberger, L. A. West and I. L. Weissman. 1982b. Protochordate allorecognition is controlled by a MHC-like gene system. Nature295: 499–502.CrossRefGoogle Scholar
  39. Simonsen, M. 1967. The clonal selection hypothesis evaluated by grafted cells reacting against their hosts. Cold Spring Harbor Symp. Quant. Biol.32: 517–523.Google Scholar
  40. Singh, P. B., R. E. Brown and B. Roser. 1987. MHC antigens in urine as olfactory recognition cues. Nature327: 161–164.PubMedCrossRefGoogle Scholar
  41. Taneda, Y., Y. Saito and H. Watanabe. 1985. Self or non-self discrimination in ascidians. Zool. Sci.2: 433–442.Google Scholar
  42. Townsend, A. R. M., J. Rothbard, F. M. Gotch, G. Bahadur, D. Wraith and A. J. McMichael. 1986. The epitopes of influenza nucleoprotein recognized by cytotoxic T lymphocytes can be defined with short synthetic peptides. Cell44: 959–968.PubMedCrossRefGoogle Scholar
  43. Watanabe, H. 1962. Further studies on the regulation in fused colonies in Botryllus primigenus(Ascidiae compositae). Sci. Rep. Tokyo Kyoiku Daigaku Sert. B.10: 253–284.Google Scholar
  44. Yamazaki, K., E. A. Boyse, V. Miké, H. T. Thaler, B. J. Mathieson, J. Abbott, J. Boyse, Z. A. Zayas and L. Thomas. 1976. Control of mating preferences in mice by genes in the major histocompatibility complex. J. Exp. Med.144: 1324–1335.PubMedCrossRefGoogle Scholar
  45. Yamazaki, K., M. Yamaguchi, P. W. Andrews, B. Peake and E. A. Boyse. 1978. Mating preferences of F2 segregants of crosses between MHC-congenic mouse strains. Immunogenetics6: 253–259.CrossRefGoogle Scholar
  46. Yamazaki, K., M. Yamaguchi, L. Baranoski, J. Bard, E. A. Boyse and L. Thomas. 1979. Recognition among mice: Evidence from the use of a Y-maze differentially scented by congenic mice of different major histocompatibility types. J. Exp. Med150: 755–760.PubMedCrossRefGoogle Scholar
  47. Yamazaki, K., G. K. Beauchamp, C. J. Wysocki, J. Bard, L. Thomas and E. A. Boyse. 1983. Recognition of H-2 types in relation to the blocking of pregnancy in mice. Science221: 186–188.PubMedCrossRefGoogle Scholar
  48. Yamazaki, K., G. K. Beauchamp, O. Matsuzaki, D. Kupniewski, J. Bard, L. Thomas and E. A. Boyse. 1986. Influence of a genetic difference confined to mutation of H-2K on the incidence of pregnancy block in mice. Proc. Natl. Acad. Sci. USA83: 740–741.PubMedCrossRefGoogle Scholar
  49. Zinkernagel, R. M., G. N. Callahan, A. Althage, S. Cooper, P. A. Klein and J. Klein. 1978. On the thymus in the differentiation of “H-2 self-recognition” by T cells: Evidence for dual recognition? J. Exp. Med147: 882–896.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1988

Authors and Affiliations

  • Irving L. Weissman
    • 1
  • Virginia Scofield
    • 1
  • Yasunori Saito
    • 1
  • Heather Boyd
    • 1
  • Baruch Rinkevich
    • 1
  1. 1.Laboratory of Experimental Oncology Department of PathologyStanford University School of MedicineStanfordUSA

Personalised recommendations