An Atlas for Schistosoma mansoni Organs and Life-Cycle Stages Using Cell Type-Specific Markers and Confocal Microscopy (2024)

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      An Atlas for Schistosoma mansoni Organs and Life-Cycle Stages Using Cell Type-Specific Markers and Confocal Microscopy (1)

      Author(s):

      James J. Collins III 1 ,

      Ryan S. King 1 ,

      Alexis Cogswell 2 ,

      David L. Williams 2 ,

      Phillip A. Newmark 1 , *

      Editor(s):

      Matty Knight

      Publication date (Electronic): 8 March 2011

      Journal: PLoS Neglected Tropical Diseases

      Publisher: Public Library of Science

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Schistosomiasis (bilharzia) is a tropical disease caused by trematode parasites ( Schistosoma) that affects hundreds of millions of people in the developing world. Currently only a single drug (praziquantel) is available to treat this disease, highlighting the importance of developing new techniques to study Schistosoma. While molecular advances, including RNA interference and the availability of complete genome sequences for two Schistosoma species, will help to revolutionize studies of these animals, an array of tools for visualizing the consequences of experimental perturbations on tissue integrity and development needs to be made widely available. To this end, we screened a battery of commercially available stains, antibodies and fluorescently labeled lectins, many of which have not been described previously for analyzing schistosomes, for their ability to label various cell and tissue types in the cercarial stage of S. mansoni. This analysis uncovered more than 20 new markers that label most cercarial tissues, including the tegument, the musculature, the protonephridia, the secretory system and the nervous system. Using these markers we present a high-resolution visual depiction of cercarial anatomy. Examining the effectiveness of a subset of these markers in S. mansoni adults and miracidia, we demonstrate the value of these tools for labeling tissues in a variety of life-cycle stages. The methodologies described here will facilitate functional analyses aimed at understanding fundamental biological processes in these parasites.

          Author Summary

          Schistosomes are parasitic flatworms that infect hundreds of millions of people worldwide. The development of genomic resources and recent application of functional genomic tools (e.g., global gene expression studies, inhibition of gene expression by RNA interference, and transgenesis) hold the promise of revolutionizing the study of schistosome biology. These advances necessitate the introduction of molecular markers for examining the consequences of manipulating schistosome genes. In this manuscript we report the use of several cell type-specific markers and confocal microscopy for visualizing various schistosome tissues in a variety of life-cycle stages. Our analysis provides an atlas of the major organ systems in three different life-cycle stages in these important parasites. The tools and methodologies reported here are widely available and can be readily adopted by researchers interested in more detailed studies of these organisms. We anticipate that these resources will be particularly useful for detailed phenotypic characterization following gene inhibition or over-expression studies.

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          The global status of schistosomiasis and its control.

          L Chitsulo, D Engels, A Montresor (2000)

          Schistosomiasis is being successfully controlled in many countries but remains a major public health problem, with an estimated 200 million people infected, mostly in Africa. Few countries in this region have undertaken successful and sustainable control programmes. The construction of water schemes to meet the power and agricultural requirements for development have lead to increasing transmission, especially of Schistosoma mansoni. Increasing population and movement have contributed to increased transmission and introduction of schistosomiasis to new areas. Most endemic countries are among the least developed whose health systems face difficulties to provide basic care at the primary health level. Constraints to control include, the lack of political commitment and infrastructure for public health interventions. Another constraint is that available anti-schistosomal drugs are expensive and the cost of individual treatment is a high proportion of the per capita drug budgets. There is need for increased support for schistosomiasis control in the most severely affected countries.

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            The Schistosoma japonicum genome reveals features of host-parasite interplay.

            (2009)

            Schistosoma japonicum is a parasitic flatworm that causes human schistosomiasis, which is a significant cause of morbidity in China and the Philippines. Here we present a draft genomic sequence for the worm. The genome provides a global insight into the molecular architecture and host interaction of this complex metazoan pathogen, revealing that it can exploit host nutrients, neuroendocrine hormones and signalling pathways for growth, development and maturation. Having a complex nervous system and a well-developed sensory system, S. japonicum can accept stimulation of the corresponding ligands as a physiological response to different environments, such as fresh water or the tissues of its intermediate and mammalian hosts. Numerous proteases, including cercarial elastase, are implicated in mammalian skin penetration and haemoglobin degradation. The genomic information will serve as a valuable platform to facilitate development of new interventions for schistosomiasis control.

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              Invertebrate synapsins: a single gene codes for several isoforms in Drosophila.

              Bert R.E. Klagges, Gertrud Heimbeck, Tanja A. Godenschwege (1996)

              Vertebrate synapsins constitute a family of synaptic proteins that participate in the regulation of neurotransmitter release. Information on the presence of synapsin homologs in invertebrates has been inconclusive. We have now cloned a Drosophila gene coding for at least two inferred proteins that both contain a region with 50% amino acid identity to the highly conserved vesicle- and actin-binding "C" domain of vertebrate synapsins. Within the C domain coding sequence, the positions of two introns have been conserved exactly from fly to human. The positions of three additional introns within this domain are similar. The Drosophila synapsin gene (Syn) is widely expressed in the nervous system of the fly. The gene products are detected in all or nearly all conventional synaptic terminals. A single amber (UAG) stop codon terminates the open reading frame (ORF1) of the most abundant transcript of the Syn gene 140 amino acid codons downstream of the homology domain. Unexpectedly, the stop codon is followed by another 443 in-frame amino acid codons (ORF2). Using different antibodies directed against ORF1 or ORF2, we demonstrate that in the adult fly small and large synapsin isoforms are generated. The small isoforms are only recognized by antibodies against ORF1; the large isoforms bind both kinds of antibodies. We suggest that the large synapsin isoform in Drosophila may be generated by UAG read-through. Implications of such an unconventional mechanism for the generation of protein diversity from a single gene are discussed.

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                Author and article information

                Contributors

                : Role: Editor

                Journal

                Journal ID (nlm-ta): PLoS Negl Trop Dis

                Journal ID (publisher-id): plos

                Journal ID (pmc): plosntds

                Title: PLoS Neglected Tropical Diseases

                Publisher: Public Library of Science (San Francisco, USA )

                ISSN (Print): 1935-2727

                ISSN (Electronic): 1935-2735

                Publication date Collection: March 2011

                Publication date (Electronic): 8 March 2011

                Volume: 5

                Issue: 3

                Electronic Location Identifier: e1009

                Affiliations

                [1 ]Howard Hughes Medical Institute, Department of Cell and Developmental Biology, Neuroscience Program, University of Illinois at Urbana-Champaign, Urbana, Illinois, United States of America

                [2 ]Department of Immunology/Microbiology, Rush University Medical Center, Chicago, Illinois, United States of America

                Biomedical Research Institute, United States of America

                Author notes

                Conceived and designed the experiments: JJC RSK PAN. Performed the experiments: JJC RSK AC. Analyzed the data: JJC RSK PAN. Contributed reagents/materials/analysis tools: AC DLW. Wrote the paper: JJC RSK PAN.

                Article

                Publisher ID: PNTD-D-10-00126

                DOI: 10.1371/journal.pntd.0001009

                PMC ID: 3050934

                PubMed ID: 21408085

                SO-VID: ffcb206d-6afc-4860-b60c-3ae4dd3e883d

                Copyright © Collins et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History

                Date received : 28 October 2010

                Date accepted : 15 December 2010

                Page count

                Pages: 17

                Categories

                Subject: Research Article

                Subject: Biology

                Subject: Zoology

                Subject: Helminthology

                Subject: Parasitology


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