Fasciola gigantica: Ultrastructure and cytochemistry of tegumental secretory activity and extracellular vesicle formation in juvenile flukes migrating in mouse liver.

Fasciola gigantica, the predominant cause of fasciolosis in tropical regions, is a major cause of economic loss to the global farming community and is also recognised as a significant human pathogen. The surface tegument of the fluke, situated as it is at the host-parasite interface, is a metabolically active and highly dynamic secretory organ mainly concerned with ensuring the survival of the parasite in a hostile immunological and physiochemical environment. The period of migration of the juvenile fluke through the hepatic parenchyma of the host is critical in establishing a mutually sustainable host-parasite relationship, but due to technical difficulties has been inadequately investigated. Here, the tegument of migrating juvenile F. gigantica collected from the hepatic parenchyma of experimentally infected mice 4 and 7 weeks after infection was examined by conventional transmission electron microscopy (TEM) and by cytochemistry using the periodic acid-thiocarbohydrazine-osmium (PATCO) and Ruthenium Red methods. T1 secretory bodies in the surface syncytium maintain the surface glycocalyx by exocytosis in response to sloughing of immunocomplex as the fluke encounters the effectors of host immunity. Their bounding plasma membranes engender a superficial zone of microvilli which appear to give rise to detached tubules and extracellular vesicles. These may have a role in host-parasite communication and immunomodulation. T2 secretory bodies in the tegument contain stable glycoprotein, and their main contribution may be to preadapt the apical surface for changes in the physicochemical environment when the fluke enters the bile ducts. A novel type of tegumental cell, termed T3, has been described in the sub-syncytial zone. T3 secretory bodies may contribute to the syncytial proteome or spine formation in the growing juvenile flukes. The surface secretory activity in migrating juvenile flukes may offer a battery of stage-specific soluble and membrane-associated molecular products with potential for therapeutic exploitation.