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.
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References
Ballarin L, Cima F, Sabbadin A (1995) Morula cells and histocompatibility in the colonial ascidian Botryllus schlosseri. Zool Sci 12:757–764
Cima F, Sabbadin A, Ballarin L (1995) Cellular aspects of allorecognition in the compound ascidian Botryllus schlosseri. Dev Comp Immunol 28:881–889
De Santo RS, Dudley PL (1969) Ultramicroscopic filaments in the ascidian Botryllus schlosseri (Pallas) and their possible role in ampullar contractions. J Ultrastruct Res 28:259–274
Ermak TH (1982) The renewing cell populations of ascidians. Am Zool 22:795–805
Hirose E (2003) Colonial allorecognition, hemolytic rejection, and viviparity in botryllid ascidians. Zool Sci 20:387–394
Hirose E, Saito Y, Watanabe H (1990) Allogeneic rejection induced by cut surface contact in the compound ascidian, Botrylloides simodensis. Invertebr Reprod Dev 17:159–164
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 64:23–34
Katow H, Watanabe H (1980) Fine structure of fusion reaction in compound ascidian Botryllus primigenus Oka. Dev Biol 76:1–14
Kawamura K, Fujiwara S (1995) Cellular and molecular characterization of transdifferentiation in the process of morphallaxis of budding tunicates. Semin Cell Biol 6:117–126
Milkman R, Byrne S (1961) Recent observations on Botryllus schlosseri. Biol Bull 121:169–221
Oka H, Watanabe H (1957) Vascular budding, a new type of budding in Botryllus. Biol Bull 112:225–240
Oka H, Watanabe H (1959) Vascular budding in Botrylloides. Biol Bull 117:340–346
Pérèz JM (1958) Ascidies reeoltées sur les côtes Méditerranéennes d’Israel. Bull Rec Counc Isr Sect B Zool 7:143–150
Rinkevich B (2005) Rejection patterns in botryllid ascidians immunity: the first tier of allorecognition. Can J Zool 83:101–121
Rinkevich B, Saito Y (1992) Self-nonself recognition in the colonial protochordate Botryllus schlosseri from Mutsu Bay, Japan. Zool Sci 9:983–988
Rinkevich B, Weissman IL (1992) Incidents of rejection and indifference in Fu/HC incompatible protochordate colonies. J Exp Zool 263:105–111
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 39:197–212
Rinkevich B, Lilker-Levav T, Goren M (1994) Allorecognition/xenorecognition responses in Botrylloides (Ascidiacea) subpopulations from the Mediterranean coast of Israel. J Exp Zool 270:302–313
Rinkevich B, Shlemberg Z, Fishelson L (1995) Whole-body protochordate regeneration from totipotent blood cells. Proc Natl Acad Sci USA 92:7695–7699
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 1–9
Rinkevich B, Tartakover S, Gershon H (1998) Contribution of morula cells to allogeneic responses in the colonial urochordate Botryllus schlosseri. Mar Biol 131:227–236
Sabbadin A, Zaniolo G, Ballarin L (1992) Genetic and cytological aspects of histocompatibility in ascidians. Boll Zool 59:167–173
Saito Y, Hirose E, Watanabe H (1994) Allorecognition in compound ascidians. Int J Dev Biol 38:237–247
Tanaka K (1973) Allogeneic inhibition in a composed ascidian, Botryllus primigenus Oka. II. Cellular and humoral responses in “nonfusion” reaction. Cell Immunol 7:427–443
Tanaka K, Watanabe H (1973) Allogeneic inhibition in a compound ascidian, Botryllus primigenus Oka. I. Processes and features of “nonfusion” reaction. Cell Immunol 7:410–426
Taneda Y, Saito Y, Watanabe H (1985) Self or nonself discrimination in ascidians. Zool Sci 2:433–442
Watanabe H, Taneda Y (1982) Self or non-self recognition in compound ascidians. Am Zool 22:775–782
Watkins MJ (1958) Regeneration of buds in Botryllus. Biol Bull 112:147–152
Watson JM, Scofield VL (1989) Amyloid deposits in the rejection lesions of Botrylloides leachi. J Cell Chem S13:68
Weissman IL, Saito Y, Rinkevich B (1990) Allorecognition histocompatibility in a protochordate species: Is the relationship to MHC semantic or structural? Immunol Rev 113:227–241
Zaniolo G (1981) Histology of the ascidian Botryllus schlosseri tunic: in particular, the test cells. Boll Zool 48:169–178
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 442–444
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.
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Communicated by O. Kinne, Oldendorf/Luhe
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Simon-Blecher, N., Hanania, J., Achituv, Y. et al. Fine structure of naive and allogeneic challenged ampullae in Botrylloides subpopulation I from the Mediterranean coast of Israel. Marine Biology 148, 987–996 (2006). https://doi.org/10.1007/s00227-005-0147-6
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DOI: https://doi.org/10.1007/s00227-005-0147-6