Advertisement

Marine Biology

, Volume 148, Issue 5, pp 987–996 | Cite as

Fine structure of naive and allogeneic challenged ampullae in Botrylloides subpopulation I from the Mediterranean coast of Israel

  • N. Simon-Blecher
  • J. Hanania
  • Y. Achituv
  • B. Rinkevich
Research Article
  • 63 Downloads

Abstract

The external peripheral termini of vasculature in botryllid ascidians (ampullae) are important in the expression of effector mechanisms during histocompatibility reactions. We study here morphological changes to the microstructure during allorecognition in Botrylloides subpopulation I (SP1) from the Mediterranean coast of Israel, where special giant ampullae, called megaloampullae are developed hours after first allogeneic challenge. The basal part of each naive ampulla consists of a sheath of continuous squamous epithelial cells (1 μm×20 μm). At the tip of the ampullae, about 130 epithelial cells become columnar with wide apical pads (15 μm×5–10 μm), that contain electron-opaque “adhesive vesicles”. Foci of crystallizations were observed within the vesicles of some columnar cells. Ampullar epithelial cells develop internal folds that support tight attachments between circulating blood cells (most of them are pigment cells) and ampullar epithelium. During the histoincompatibility process, the tunic peripheral edge at the interaction area becomes highly convoluted. Filaments (up to 1.16 μm) accumulate in the interaction tunic matrix. Some of these filaments encircle destructed cells. Fragmented cell membranes are also found next to the reacting ampullae. The most characteristic feature of the Botrylloides SP1 rejection reaction is dilation of the ampullae. The ampullar epithelium becomes “curly” when megaloampullae are formed. Within the curly region, about 30% of the squamous epithelial cells are further stretched, up to 33 μm in length. Some additional mechanisms are suggested to explain the fast increase (up to seven times) in ampullar width that is recorded within a few hours from the first allogeneic contact.

Keywords

Columnar Cell Mediterranean Coast Squamous Epithelial Cell Circulate Blood Cell Rejection Process 
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.

Notes

Acknowledgements

The study was supported by the US–Israel Binational Science Foundation and by the Israel Science Foundation (456/01). N.S.-B. was a doctoral fellow of the Charles Clore Foundation. This study is part of N.S.-B.’s PhD dissertation at Bar-Ilan University.

References

  1. Ballarin L, Cima F, Sabbadin A (1995) Morula cells and histocompatibility in the colonial ascidian Botryllus schlosseri. Zool Sci 12:757–764CrossRefGoogle Scholar
  2. Cima F, Sabbadin A, Ballarin L (1995) Cellular aspects of allorecognition in the compound ascidian Botryllus schlosseri. Dev Comp Immunol 28:881–889CrossRefGoogle Scholar
  3. De Santo RS, Dudley PL (1969) Ultramicroscopic filaments in the ascidian Botryllus schlosseri (Pallas) and their possible role in ampullar contractions. J Ultrastruct Res 28:259–274CrossRefPubMedCentralGoogle Scholar
  4. Ermak TH (1982) The renewing cell populations of ascidians. Am Zool 22:795–805CrossRefGoogle Scholar
  5. Hirose E (2003) Colonial allorecognition, hemolytic rejection, and viviparity in botryllid ascidians. Zool Sci 20:387–394CrossRefPubMedCentralGoogle Scholar
  6. Hirose E, Saito Y, Watanabe H (1990) Allogeneic rejection induced by cut surface contact in the compound ascidian, Botrylloides simodensis. Invertebr Reprod Dev 17:159–164CrossRefGoogle Scholar
  7. Katow H, Watanabe H (1978) Fine structure and possible role of ampullae on tunic supply and attachment in a compound ascidian, Botryllus primigenus Oka. J Ultrastruct Res 64:23–34CrossRefPubMedCentralGoogle Scholar
  8. Katow H, Watanabe H (1980) Fine structure of fusion reaction in compound ascidian Botryllus primigenus Oka. Dev Biol 76:1–14CrossRefPubMedCentralGoogle Scholar
  9. Kawamura K, Fujiwara S (1995) Cellular and molecular characterization of transdifferentiation in the process of morphallaxis of budding tunicates. Semin Cell Biol 6:117–126CrossRefPubMedCentralGoogle Scholar
  10. Milkman R, Byrne S (1961) Recent observations on Botryllus schlosseri. Biol Bull 121:169–221Google Scholar
  11. Oka H, Watanabe H (1957) Vascular budding, a new type of budding in Botryllus. Biol Bull 112:225–240CrossRefGoogle Scholar
  12. Oka H, Watanabe H (1959) Vascular budding in Botrylloides. Biol Bull 117:340–346CrossRefGoogle Scholar
  13. Pérèz JM (1958) Ascidies reeoltées sur les côtes Méditerranéennes d’Israel. Bull Rec Counc Isr Sect B Zool 7:143–150Google Scholar
  14. Rinkevich B (2005) Rejection patterns in botryllid ascidians immunity: the first tier of allorecognition. Can J Zool 83:101–121CrossRefGoogle Scholar
  15. Rinkevich B, Saito Y (1992) Self-nonself recognition in the colonial protochordate Botryllus schlosseri from Mutsu Bay, Japan. Zool Sci 9:983–988Google Scholar
  16. Rinkevich B, Weissman IL (1992) Incidents of rejection and indifference in Fu/HC incompatible protochordate colonies. J Exp Zool 263:105–111CrossRefPubMedCentralGoogle Scholar
  17. Rinkevich B, Shlemberg Z, Lilker-Levav T, Goren M, Fishelson L (1993) Life history characteristics of Botrylloides (Tunicata) populations in Akko Bay, Mediterranean coast of Israel. Israel J Zool 39:197–212Google Scholar
  18. Rinkevich B, Lilker-Levav T, Goren M (1994) Allorecognition/xenorecognition responses in Botrylloides (Ascidiacea) subpopulations from the Mediterranean coast of Israel. J Exp Zool 270:302–313CrossRefGoogle Scholar
  19. Rinkevich B, Shlemberg Z, Fishelson L (1995) Whole-body protochordate regeneration from totipotent blood cells. Proc Natl Acad Sci USA 92:7695–7699CrossRefPubMedCentralGoogle Scholar
  20. Rinkevich B, Shlemberg Z, Fishelson L (1996) Survival budding processes in the colonial tunicate Botrylloides from the Mediterranean Sea: the role of totipotent blood cells. In: Maramorosch K, Loeb MJ (eds) Invertebrate cell culture: looking towards the 21st century. In Vitro Society Press, Charlotte, NC, pp 1–9Google Scholar
  21. Rinkevich B, Tartakover S, Gershon H (1998) Contribution of morula cells to allogeneic responses in the colonial urochordate Botryllus schlosseri. Mar Biol 131:227–236CrossRefGoogle Scholar
  22. Sabbadin A, Zaniolo G, Ballarin L (1992) Genetic and cytological aspects of histocompatibility in ascidians. Boll Zool 59:167–173CrossRefGoogle Scholar
  23. Saito Y, Hirose E, Watanabe H (1994) Allorecognition in compound ascidians. Int J Dev Biol 38:237–247PubMedPubMedCentralGoogle Scholar
  24. Tanaka K (1973) Allogeneic inhibition in a composed ascidian, Botryllus primigenus Oka. II. Cellular and humoral responses in “nonfusion” reaction. Cell Immunol 7:427–443CrossRefPubMedCentralGoogle Scholar
  25. Tanaka K, Watanabe H (1973) Allogeneic inhibition in a compound ascidian, Botryllus primigenus Oka. I. Processes and features of “nonfusion” reaction. Cell Immunol 7:410–426CrossRefPubMedCentralGoogle Scholar
  26. Taneda Y, Saito Y, Watanabe H (1985) Self or nonself discrimination in ascidians. Zool Sci 2:433–442Google Scholar
  27. Watanabe H, Taneda Y (1982) Self or non-self recognition in compound ascidians. Am Zool 22:775–782CrossRefGoogle Scholar
  28. Watkins MJ (1958) Regeneration of buds in Botryllus. Biol Bull 112:147–152CrossRefGoogle Scholar
  29. Watson JM, Scofield VL (1989) Amyloid deposits in the rejection lesions of Botrylloides leachi. J Cell Chem S13:68Google Scholar
  30. Weissman IL, Saito Y, Rinkevich B (1990) Allorecognition histocompatibility in a protochordate species: Is the relationship to MHC semantic or structural? Immunol Rev 113:227–241CrossRefPubMedCentralGoogle Scholar
  31. Zaniolo G (1981) Histology of the ascidian Botryllus schlosseri tunic: in particular, the test cells. Boll Zool 48:169–178CrossRefGoogle Scholar
  32. Zaniolo G, Ballarin L (2001) Colony specificity in Botrylloides leachi (Savigny): preliminary reports. In: Swada H, Yokosawa H, Lambert CC (eds) The biology of ascidians. Springer, Tokyo, pp 442–444CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • N. Simon-Blecher
    • 1
    • 2
  • J. Hanania
    • 1
  • Y. Achituv
    • 1
  • B. Rinkevich
    • 2
  1. 1.Faculty of Life SciencesBar Ilan UniversityRamat GanIsrael
  2. 2.National Institute of OceanographyIsrael Oceanography and Limnological ResearchHaifaIsrael

Personalised recommendations