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A Galectin of Unique Domain Organization from Hemocytes of the Eastern Oyster (Crassostrea virginica) Is a Receptor for the Protistan Parasite Perkinsus marinus^1,2

Center of Marine Biotechnology, University of Maryland Biotechnology Institute, Baltimore, MD 21202

Invertebrates display effective innate immune responses for defense against microbial infection. However, the protozoan parasite Perkinsus marinus causes Dermo disease in the eastern oyster Crassostrea virginica and is responsible for catastrophic damage to shellfisheries and the estuarine environment in North America. The infection mechanisms remain unclear, but it is likely that, while filter feeding, the healthy oysters ingest P. marinus trophozoites released to the water column by the infected neighboring individuals. Inside oyster hemocytes, trophozoites resist oxidative killing, proliferate, and spread throughout the host. However, the mechanism(s) for parasite entry into the hemocyte are unknown. In this study, we show that oyster hemocytes recognize P. marinus via a novel galectin (C. virginica galectin (CvGal)) of unique structure. The biological roles of galectins have only been partly elucidated, mostly encompassing embryogenesis and indirect roles in innate and adaptive immunity mediated by the binding to endogenous ligands. CvGal recognized a variety of potential microbial pathogens and unicellular algae, and preferentially, Perkinsus spp. trophozoites. Attachment and spreading of hemocytes to foreign surfaces induced localization of CvGal to the cell periphery, its secretion and binding to the plasma membrane. Exposure of hemocytes to Perkinsus spp. trophozoites enhanced this process further, and their phagocytosis could be partially inhibited by pretreatment of the hemocytes with anti-CvGal Abs. The evidence presented indicates that CvGal facilitates recognition of selected microbes and algae, thereby promoting phagocytosis of both potential infectious challenges and phytoplankton components, and that P. marinus subverts the host’s immune/feeding recognition mechanism to passively gain entry into the hemocytes.

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 National Institutes of Health Grant R01 GM070589-01, National Oceanic and Atmospheric Administration Grant NA05NMF4571243, and National Science Foundation Grant IOB 0618409.

² The sequence presented in this article has been submitted to GenBank under accession number DQ779197.

³ Address correspondence and reprint requests to Dr. Gerardo R. Vasta, Center of Marine Biotechnology, University of Maryland Biotechnology Institute, 701 East Pratt Street, Baltimore, MD 21202. E-mail address: vasta{at}umbi.umd.edu

⁴ Abbreviations used in this paper: CvGal, Crassostrea virginica galectin; CRD, carbohydrate recognition domain; ASW, artificial sea water; UTR, untranslated region; GalNAc, N-acetyl-D-galactosamine; GlcNAc, N-acetyl-D-glucosamine; LacNAc, N-acetyllactosamine; TDG, thiodigalactose; PFA, paraformaldehyde; HBS, HEPES-buffered saline; N-J, neighbor-joining.

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