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Cyclosporin A Suspends Transplantation Reactions in the Marine Sponge Microciona prolifera¹

Clarissa Sabella^*,, Ellen Faszewski^*,, Lisa Himic^*,, Katherine M. Colpitts, Jane Kaltenbach^*,, Max M. Burger^*, and Xavier Fernàndez-Busquets^2,*,¶

^* Marine Biological Laboratory, Woods Hole, MA 02543; Mount Holyoke College, South Hadley, MA 01075; Wheelock College, Boston, MA 02215; Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland; and ^¶ Bioengineering Institute of Catalonia, and Nanoscience and Nanotechnology Institute, Barcelona Science Park, University of Barcelona, Barcelona, Spain

Sponges are the simplest extant animals but nevertheless possess self-nonself recognition that rivals the specificity of the vertebrate MHC. We have used dissociated cell assays and grafting techniques to study tissue acceptance and rejection in the marine sponge Microciona prolifera. Our data show that allogeneic, but not isogeneic, cell contacts trigger cell death and an increased expression of cell adhesion and apoptosis markers in cells that accumulate in graft interfaces. Experiments investigating the possible existence of immune memory in sponges indicate that faster second set reactions are nonspecific. Among the different cellular types, gray cells have been proposed to be the sponge immunocytes. Fluorescence confocal microscopy results from intact live grafts show the migration of autofluorescent gray cells toward graft contact zones and the inhibition of gray cell movements in the presence of nontoxic concentrations of cyclosporin A. These results suggest that cell motility is an important factor involved in sponge self/nonself recognition. Communication between gray cells in grafted tissues does not require cell contact and is carried by an extracellular diffusible marker. The finding that a commonly used immunosuppressor in human transplantation such as cyclosporin A blocks tissue rejection in marine sponges indicates that the cellular mechanisms for regulating this process in vertebrates might have appeared at the very start of metazoan evolution.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ This work was supported by grant 2005-SGR00037 from the Generalitat de Catalunya, Sweden.

² Address correspondence and reprint requests to Dr. Xavier Fernàndez-Busquets, Bioengineering Institute of Catalonia, Barcelona Science Park, Josep Samitier 1-5, Barcelona E08028, Spain. E-mail address: xfernandez_busquets{at}ub.edu

³ Abbreviations used in this paper: ECM, extracellular matrix; AF, aggregation factor; CMFDA, 5-chloromethylfluorescein diacetate; CsA, cyclosporin A.

⁴ The online version of this article contains supplemental material.

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