The anterior esophageal region of Schistosoma japonicum is a secretory organ
Abstract Background The esophagus of blood-feeding schistosomes has been largely neglected although its posterior portion was designated as a gland decades ago. However, we recently showed it plays a pivotal role in blood processing. It is clearly demarcated into anterior and posterior compartments,...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2014-12-01
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| Series: | Parasites & Vectors |
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| Online Access: | https://doi.org/10.1186/s13071-014-0565-8 |
| _version_ | 1797811660004524032 |
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| author | Xiao Hong Li Meg Stark Gillian M Vance Jian Ping Cao R Alan Wilson |
| author_facet | Xiao Hong Li Meg Stark Gillian M Vance Jian Ping Cao R Alan Wilson |
| author_sort | Xiao Hong Li |
| collection | DOAJ |
| description | Abstract Background The esophagus of blood-feeding schistosomes has been largely neglected although its posterior portion was designated as a gland decades ago. However, we recently showed it plays a pivotal role in blood processing. It is clearly demarcated into anterior and posterior compartments, both surrounded by a mass of cell bodies. Feeding movies revealed that erythrocytes accumulate in the anterior compartment before entering the posterior, indicating that a distinct process is executed there. We therefore investigated ultrastructural aspects and possible functions of the anterior region. Methods The heads of adult Schistosoma japonicum were detached and prepared for both transmission and scanning electron microscopy to define the detailed ultrastructure of the anterior esophagus. Cryosections of heads were also prepared for immunocytochemistry and confocal microscopy to define the pattern of intrinsic host antibody binding in the anterior esophageal lining. Results The anterior syncytial lining of the esophagus is highly extended by long, thin corrugations of cytoplasm projecting towards the lumen. Strikingly in the male worm, the tips of the corrugations are further expanded by numerous threads of cytoplasm, producing a spaghetti-like appearance in the central lumen. Flattened, pitted cytoplasmic plates are interspersed in the tangled mass of threads. Abundant, morphologically distinct light vesicles of varied size and contents are manufactured in the cell bodies, from where they traffic through cytoplasmic connections to the corrugations and out to the tips. Clusters of vesicles accumulate in expanded tips in males, together with occasional mitochondria whilst females have more mitochondria but fewer vesicles. The membranous contents of light vesicles are secreted mainly from the tips, but also from the sides of the corrugations. They coat the surfaces and then form organised self-adherent membrane figures when shed into the lumen. Host antibody binds strongly in a characteristic pattern to the anterior esophageal lining indicating that the secretions are highly immunogenic. Conclusions We suggest that the anterior esophageal region is an independent secretory organ. The contents of light vesicles are released into the esophageal lumen via the tips of corrugation to interact with incoming blood. Our immediate task is to establish their composition and role in blood processing. |
| first_indexed | 2024-03-13T07:26:58Z |
| format | Article |
| id | doaj.art-050cac19968a478990aff280200bcba1 |
| institution | Directory Open Access Journal |
| issn | 1756-3305 |
| language | English |
| last_indexed | 2024-03-13T07:26:58Z |
| publishDate | 2014-12-01 |
| publisher | BMC |
| record_format | Article |
| series | Parasites & Vectors |
| spelling | doaj.art-050cac19968a478990aff280200bcba12023-06-04T11:19:32ZengBMCParasites & Vectors1756-33052014-12-017111210.1186/s13071-014-0565-8The anterior esophageal region of Schistosoma japonicum is a secretory organXiao Hong Li0Meg Stark1Gillian M Vance2Jian Ping Cao3R Alan Wilson4National Institute of Parasitic Diseases, Chinese Center for Disease Control and PreventionCytometry Laboratory, Department of Biology, University of YorkCentre for Immunology and Infection, Department of Biology, University of YorkNational Institute of Parasitic Diseases, Chinese Center for Disease Control and PreventionCentre for Immunology and Infection, Department of Biology, University of YorkAbstract Background The esophagus of blood-feeding schistosomes has been largely neglected although its posterior portion was designated as a gland decades ago. However, we recently showed it plays a pivotal role in blood processing. It is clearly demarcated into anterior and posterior compartments, both surrounded by a mass of cell bodies. Feeding movies revealed that erythrocytes accumulate in the anterior compartment before entering the posterior, indicating that a distinct process is executed there. We therefore investigated ultrastructural aspects and possible functions of the anterior region. Methods The heads of adult Schistosoma japonicum were detached and prepared for both transmission and scanning electron microscopy to define the detailed ultrastructure of the anterior esophagus. Cryosections of heads were also prepared for immunocytochemistry and confocal microscopy to define the pattern of intrinsic host antibody binding in the anterior esophageal lining. Results The anterior syncytial lining of the esophagus is highly extended by long, thin corrugations of cytoplasm projecting towards the lumen. Strikingly in the male worm, the tips of the corrugations are further expanded by numerous threads of cytoplasm, producing a spaghetti-like appearance in the central lumen. Flattened, pitted cytoplasmic plates are interspersed in the tangled mass of threads. Abundant, morphologically distinct light vesicles of varied size and contents are manufactured in the cell bodies, from where they traffic through cytoplasmic connections to the corrugations and out to the tips. Clusters of vesicles accumulate in expanded tips in males, together with occasional mitochondria whilst females have more mitochondria but fewer vesicles. The membranous contents of light vesicles are secreted mainly from the tips, but also from the sides of the corrugations. They coat the surfaces and then form organised self-adherent membrane figures when shed into the lumen. Host antibody binds strongly in a characteristic pattern to the anterior esophageal lining indicating that the secretions are highly immunogenic. Conclusions We suggest that the anterior esophageal region is an independent secretory organ. The contents of light vesicles are released into the esophageal lumen via the tips of corrugation to interact with incoming blood. Our immediate task is to establish their composition and role in blood processing.https://doi.org/10.1186/s13071-014-0565-8EsophagusVesicleTransmission electron microscopyScanning electron microscopyAntibody localisationSchistosoma japonicum |
| spellingShingle | Xiao Hong Li Meg Stark Gillian M Vance Jian Ping Cao R Alan Wilson The anterior esophageal region of Schistosoma japonicum is a secretory organ Parasites & Vectors Esophagus Vesicle Transmission electron microscopy Scanning electron microscopy Antibody localisation Schistosoma japonicum |
| title | The anterior esophageal region of Schistosoma japonicum is a secretory organ |
| title_full | The anterior esophageal region of Schistosoma japonicum is a secretory organ |
| title_fullStr | The anterior esophageal region of Schistosoma japonicum is a secretory organ |
| title_full_unstemmed | The anterior esophageal region of Schistosoma japonicum is a secretory organ |
| title_short | The anterior esophageal region of Schistosoma japonicum is a secretory organ |
| title_sort | anterior esophageal region of schistosoma japonicum is a secretory organ |
| topic | Esophagus Vesicle Transmission electron microscopy Scanning electron microscopy Antibody localisation Schistosoma japonicum |
| url | https://doi.org/10.1186/s13071-014-0565-8 |
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