Insects in anthelminthics research: Lady beetle-derived harmonine affects survival, reproduction and stem cell proliferation of Schistosoma mansoni
Natural products have moved into the spotlight as possible sources for new drugs in the treatment of helminth infections including schistosomiasis. Surprisingly, insect-derived compounds have largely been neglected so far in the search for novel anthelminthics, despite the generally recognized high...
Saved in:
| Published in | PLoS neglected tropical diseases Vol. 13; no. 3; p. e0007240 |
|---|---|
| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.03.2019
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
Cover
Loading…
| Abstract | Natural products have moved into the spotlight as possible sources for new drugs in the treatment of helminth infections including schistosomiasis. Surprisingly, insect-derived compounds have largely been neglected so far in the search for novel anthelminthics, despite the generally recognized high potential of insect biotechnology for drug discovery. This motivated us to assess the antischistosomal capacity of harmonine, an antimicrobial alkaloid from the harlequin ladybird Harmonia axyridis that raised high interest in insect biotechnology in recent years. We observed remarkably pleiotropic effects of harmonine on physiological, cellular, and molecular processes in adult male and female Schistosoma mansoni at concentrations as low as 5 μM in vitro. This included tegumental damage, gut dilatation, dysplasia of gonads, a complete stop of egg production at 10 μM, and increased production of abnormally shaped eggs at 5 μM. Motility was reduced with an EC50 of 8.8 μM and lethal effects occurred at 10-20 μM within 3 days of culture. Enzyme inhibition assays revealed acetylcholinesterase (AChE) as one potential target of harmonine. To assess possible effects on stem cells, which represent attractive anthelminthic targets, we developed a novel in silico 3D reconstruction of gonads based on confocal laser scanning microscopy of worms after EdU incorporation to allow for quantification of proliferating stem cells per organ. Harmonine significantly reduced the number of proliferating stem cells in testes, ovaries, and also the number of proliferating parenchymal neoblasts. This was further supported by a downregulated expression of the stem cell markers nanos-1 and nanos-2 in harmonine-treated worms revealed by quantitative real-time PCR. Our data demonstrate a multifaceted antischistosomal activity of the lady beetle-derived compound harmonine, and suggest AChE and stem cell genes as possible targets. Harmonine is the first animal-derived alkaloid detected to have antischistosomal capacity. This study highlights the potential of exploiting insects as a source for the discovery of anthelminthics. |
|---|---|
| AbstractList | Natural products have moved into the spotlight as possible sources for new drugs in the treatment of helminth infections including schistosomiasis. Surprisingly, insect-derived compounds have largely been neglected so far in the search for novel anthelminthics, despite the generally recognized high potential of insect biotechnology for drug discovery. This motivated us to assess the antischistosomal capacity of harmonine, an antimicrobial alkaloid from the harlequin ladybird Harmonia axyridis that raised high interest in insect biotechnology in recent years. We observed remarkably pleiotropic effects of harmonine on physiological, cellular, and molecular processes in adult male and female Schistosoma mansoni at concentrations as low as 5 μM in vitro. This included tegumental damage, gut dilatation, dysplasia of gonads, a complete stop of egg production at 10 μM, and increased production of abnormally shaped eggs at 5 μM. Motility was reduced with an EC50 of 8.8 μM and lethal effects occurred at 10-20 μM within 3 days of culture. Enzyme inhibition assays revealed acetylcholinesterase (AChE) as one potential target of harmonine. To assess possible effects on stem cells, which represent attractive anthelminthic targets, we developed a novel in silico 3D reconstruction of gonads based on confocal laser scanning microscopy of worms after EdU incorporation to allow for quantification of proliferating stem cells per organ. Harmonine significantly reduced the number of proliferating stem cells in testes, ovaries, and also the number of proliferating parenchymal neoblasts. This was further supported by a downregulated expression of the stem cell markers nanos-1 and nanos-2 in harmonine-treated worms revealed by quantitative real-time PCR. Our data demonstrate a multifaceted antischistosomal activity of the lady beetle-derived compound harmonine, and suggest AChE and stem cell genes as possible targets. Harmonine is the first animal-derived alkaloid detected to have antischistosomal capacity. This study highlights the potential of exploiting insects as a source for the discovery of anthelminthics. Natural products have moved into the spotlight as possible sources for new drugs in the treatment of helminth infections including schistosomiasis. Surprisingly, insect-derived compounds have largely been neglected so far in the search for novel anthelminthics, despite the generally recognized high potential of insect biotechnology for drug discovery. This motivated us to assess the antischistosomal capacity of harmonine, an antimicrobial alkaloid from the harlequin ladybird Harmonia axyridis that raised high interest in insect biotechnology in recent years. We observed remarkably pleiotropic effects of harmonine on physiological, cellular, and molecular processes in adult male and female Schistosoma mansoni at concentrations as low as 5 μM in vitro . This included tegumental damage, gut dilatation, dysplasia of gonads, a complete stop of egg production at 10 μM, and increased production of abnormally shaped eggs at 5 μM. Motility was reduced with an EC50 of 8.8 μM and lethal effects occurred at 10–20 μM within 3 days of culture. Enzyme inhibition assays revealed acetylcholinesterase (AChE) as one potential target of harmonine. To assess possible effects on stem cells, which represent attractive anthelminthic targets, we developed a novel in silico 3D reconstruction of gonads based on confocal laser scanning microscopy of worms after EdU incorporation to allow for quantification of proliferating stem cells per organ. Harmonine significantly reduced the number of proliferating stem cells in testes, ovaries, and also the number of proliferating parenchymal neoblasts. This was further supported by a downregulated expression of the stem cell markers nanos-1 and nanos-2 in harmonine-treated worms revealed by quantitative real-time PCR. Our data demonstrate a multifaceted antischistosomal activity of the lady beetle-derived compound harmonine, and suggest AChE and stem cell genes as possible targets. Harmonine is the first animal-derived alkaloid detected to have antischistosomal capacity. This study highlights the potential of exploiting insects as a source for the discovery of anthelminthics. Natural compounds represent one of the richest sources for the discovery of new active compounds against diseases such as cancer or infections, including helminth infections that cause the highest disease burden in tropical countries. Surprisingly, insects have been almost completely neglected with respect to anthelminthics discovery although they represent the most species-rich class of animals known on earth, producing a wide spectrum of compounds with biological activities. In insect biotechnology, the harlequin ladybird Harmonia axyridis raised high interest being a rich source of antimicrobial compounds such as the alkaloid harmonine. Harmonine is thought to act as a chemical weapon keeping otherwise detrimental microsporidia in the beetle under control. Testing the antiparasitic potential of harmonine against adult Schistosoma mansoni , one of the most harmful helminths worldwide, resulted in multifaceted negative effects. The compound damaged tissues essential for survival and reproduction of schistosomes (tegument, intestine, gonads) and also affected stem-cell proliferation. Furthermore, we obtained first evidence for acetylcholinesterase as one potential molecular target, which was partially inhibited by harmonine. This is the first time to proof a direct effect of a defined insect-derived compound on a helminth parasite, a finding that will encourage further studies to explore insects as sources of novel anthelminthics. Natural products have moved into the spotlight as possible sources for new drugs in the treatment of helminth infections including schistosomiasis. Surprisingly, insect-derived compounds have largely been neglected so far in the search for novel anthelminthics, despite the generally recognized high potential of insect biotechnology for drug discovery. This motivated us to assess the antischistosomal capacity of harmonine, an antimicrobial alkaloid from the harlequin ladybird Harmonia axyridis that raised high interest in insect biotechnology in recent years. We observed remarkably pleiotropic effects of harmonine on physiological, cellular, and molecular processes in adult male and female Schistosoma mansoni at concentrations as low as 5 [mu]M in vitro. This included tegumental damage, gut dilatation, dysplasia of gonads, a complete stop of egg production at 10 [mu]M, and increased production of abnormally shaped eggs at 5 [mu]M. Motility was reduced with an EC50 of 8.8 [mu]M and lethal effects occurred at 10-20 [mu]M within 3 days of culture. Enzyme inhibition assays revealed acetylcholinesterase (AChE) as one potential target of harmonine. To assess possible effects on stem cells, which represent attractive anthelminthic targets, we developed a novel in silico 3D reconstruction of gonads based on confocal laser scanning microscopy of worms after EdU incorporation to allow for quantification of proliferating stem cells per organ. Harmonine significantly reduced the number of proliferating stem cells in testes, ovaries, and also the number of proliferating parenchymal neoblasts. This was further supported by a downregulated expression of the stem cell markers nanos-1 and nanos-2 in harmonine-treated worms revealed by quantitative real-time PCR. Our data demonstrate a multifaceted antischistosomal activity of the lady beetle-derived compound harmonine, and suggest AChE and stem cell genes as possible targets. Harmonine is the first animal-derived alkaloid detected to have antischistosomal capacity. This study highlights the potential of exploiting insects as a source for the discovery of anthelminthics. |
| Audience | Academic |
| Author | Thomas, Laura Haeberlein, Simone Hahnel, Steffen R Vilcinskas, Andreas Grünweller, Arnold Hardt, Martin Kellershohn, Josina Grevelding, Christoph G Hartmann, Roland K |
| AuthorAffiliation | 2 Institute of Pharmaceutical Chemistry, Philipps University, Marburg, Germany University of Würzburg, GERMANY 3 Biomedical Research Center Seltersberg—Imaging Unit, Justus Liebig University, Giessen, Germany 4 Institute for Insect Biotechnology, Justus Liebig University, Giessen, Germany 1 Institute of Parasitology, BFS, Justus Liebig University, Giessen, Germany |
| AuthorAffiliation_xml | – name: 2 Institute of Pharmaceutical Chemistry, Philipps University, Marburg, Germany – name: University of Würzburg, GERMANY – name: 3 Biomedical Research Center Seltersberg—Imaging Unit, Justus Liebig University, Giessen, Germany – name: 4 Institute for Insect Biotechnology, Justus Liebig University, Giessen, Germany – name: 1 Institute of Parasitology, BFS, Justus Liebig University, Giessen, Germany |
| Author_xml | – sequence: 1 givenname: Josina surname: Kellershohn fullname: Kellershohn, Josina organization: Institute of Parasitology, BFS, Justus Liebig University, Giessen, Germany – sequence: 2 givenname: Laura orcidid: 0000-0002-9551-3743 surname: Thomas fullname: Thomas, Laura organization: Institute of Pharmaceutical Chemistry, Philipps University, Marburg, Germany – sequence: 3 givenname: Steffen R surname: Hahnel fullname: Hahnel, Steffen R organization: Institute of Parasitology, BFS, Justus Liebig University, Giessen, Germany – sequence: 4 givenname: Arnold surname: Grünweller fullname: Grünweller, Arnold organization: Institute of Pharmaceutical Chemistry, Philipps University, Marburg, Germany – sequence: 5 givenname: Roland K surname: Hartmann fullname: Hartmann, Roland K organization: Institute of Pharmaceutical Chemistry, Philipps University, Marburg, Germany – sequence: 6 givenname: Martin surname: Hardt fullname: Hardt, Martin organization: Biomedical Research Center Seltersberg-Imaging Unit, Justus Liebig University, Giessen, Germany – sequence: 7 givenname: Andreas orcidid: 0000-0001-8276-4968 surname: Vilcinskas fullname: Vilcinskas, Andreas organization: Institute for Insect Biotechnology, Justus Liebig University, Giessen, Germany – sequence: 8 givenname: Christoph G surname: Grevelding fullname: Grevelding, Christoph G organization: Institute of Parasitology, BFS, Justus Liebig University, Giessen, Germany – sequence: 9 givenname: Simone orcidid: 0000-0002-1932-9696 surname: Haeberlein fullname: Haeberlein, Simone organization: Institute of Parasitology, BFS, Justus Liebig University, Giessen, Germany |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30870428$$D View this record in MEDLINE/PubMed |
| BookMark | eNptkttq3DAQhk1JaQ7tG5TWUCi96G51sOx1Lgoh9BBY6EXbazGWRrGCLG0leyHP0ReunGzCbol0IaH555Nm9J8WRz54LIrXlCwpb-inmzBFD2658aNeEkIaVpFnxQltuViwhoujvf1xcZrSDSGiFSv6ojjmZNWQiq1Oir9XPqEaU2l9CX7s0Q02L1alMmJCiKo_L9egb8sOcXS40BjtFnXZQxyCtx5LMOaOkKa4tVtwH3PmJgY9qdGGmarLNOJQKnSuzAFnDUa4iwVT_lS9TWNIYYByAJ8y82Xx3IBL-Gq3nhW_v375dfl9sf7x7eryYr1QNavGBeemNrls1po6DxAtaU23wq6BVnUUNDYdFw1ZKV4RouqWtwy6uhUVqzWFhp8Vb--5GxeS3PUzScYE45Q2os2Kq3uFDnAjN9EOEG9lACvvDkK8lhBHqxxKBkgqYWhtqKoaLUBzhURQjoxhq1Rmfd7dNnUDaoV-jOAOoIcRb3t5HbayrnjdCJIBH3aAGP5MmEY52DQ3FTyGKb87fzedlassffef9OnqdqpryAVYb0K-V81QeZF9wgVnYmYtn1DlqXGwKnvS2Hx-kPB-L6FHcGOfgpvmH0-HwupeqGJIKaJ5bAYlcvb4w6vl7HG583hOe7PfyMekB1Pzf9TZ_SI |
| CitedBy_id | crossref_primary_10_1371_journal_pntd_0010661 crossref_primary_10_3390_ph15020119 crossref_primary_10_1371_journal_ppat_1008213 crossref_primary_10_3389_fpara_2024_1394407 crossref_primary_10_1039_D0MD00062K crossref_primary_10_1080_07391102_2020_1850363 crossref_primary_10_1007_s00216_021_03230_w crossref_primary_10_1038_s41598_023_35765_6 crossref_primary_10_3389_fimmu_2021_599014 crossref_primary_10_1038_s41598_023_36826_6 crossref_primary_10_3390_antibiotics9100664 crossref_primary_10_1016_j_vetpar_2024_110244 crossref_primary_10_1016_j_pestbp_2020_104561 |
| Cites_doi | 10.1016/j.cbi.2017.01.020 10.1371/journal.pntd.0002865 10.1517/17460441.2.S1.S53 10.3390/molecules20021872 10.1016/j.fct.2018.04.029 10.1007/s00436-004-1241-2 10.1016/0014-4894(84)90042-0 10.1371/journal.pntd.0002336 10.1017/S0031182099006174 10.1645/0022-3395(2000)086[1125:TCIASM]2.0.CO;2 10.4269/ajtmh.1994.51.83 10.1111/j.1476-5381.1966.tb01845.x 10.1016/j.ijpddr.2014.09.006 10.1007/s00436-008-1080-7 10.1007/s10158-007-0059-x 10.3109/13880209.2011.615842 10.3390/toxins7114758 10.1146/annurev.micro.56.012302.160854 10.1016/j.pt.2017.05.008 10.1006/expr.1995.1152 10.1186/1471-2164-8-181 10.1016/j.ijpara.2010.01.007 10.1110/ps.8.12.2553 10.1186/s40249-018-0444-1 10.1016/j.molbiopara.2014.06.002 10.1517/17460441.2.S1.S35 10.1021/ci900491t 10.1007/BF00930846 10.1039/C5OB00461F 10.1016/j.molbiopara.2005.01.019 10.1016/j.ijpara.2006.06.007 10.1007/s00436-017-5476-0 10.1126/science.1234032 10.1096/fj.01-0683fje 10.1111/1744-7917.12159 10.1038/srep31150 10.1016/j.cbi.2010.03.007 10.1186/1472-6750-3-18 10.1016/j.lfs.2007.03.008 10.3109/13880209.2012.661741 10.3389/fgene.2014.00170 10.7554/eLife.35449 10.1098/rsbl.2011.0760 10.1098/rsbl.2013.0006 10.1017/S0031182000046394 10.1186/2041-9139-5-10 10.1111/jnc.13856 10.1016/j.bmcl.2012.05.103 10.1111/j.1476-5381.1972.tb08145.x 10.1590/0037-8682-0241-2016 10.1006/meth.2001.1262 10.1007/s12639-014-0516-5 10.1038/nature11924 10.1002/cbdv.201000163 10.1073/pnas.0609708104 10.1242/jcs.34.1.173 10.1016/0006-2952(61)90145-9 10.1016/j.ijpara.2006.01.007 10.1371/journal.pntd.0004994 10.1016/j.gde.2016.06.010 10.1016/0035-9203(71)90070-8 10.4269/ajtmh.1994.50.281 10.1016/0166-6851(94)00058-U 10.1007/s10555-011-9339-3 10.1038/s41598-018-21781-4 10.1021/np200906s 10.1186/s13071-016-1615-1 10.1016/j.ijpara.2016.03.004 10.1515/znc-2000-1-214 10.1097/QCO.0b013e328318978f |
| ContentType | Journal Article |
| Copyright | COPYRIGHT 2019 Public Library of Science 2019 Kellershohn et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2019 Kellershohn et al 2019 Kellershohn et al |
| Copyright_xml | – notice: COPYRIGHT 2019 Public Library of Science – notice: 2019 Kellershohn et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: 2019 Kellershohn et al 2019 Kellershohn et al |
| DBID | NPM AAYXX CITATION 3V. 7QL 7SS 7T2 7T7 7U9 7X7 7XB 88E 8C1 8FD 8FI 8FJ 8FK ABUWG AFKRA AZQEC BENPR C1K CCPQU DWQXO F1W FR3 FYUFA GHDGH H94 H95 H97 K9. L.G M0S M1P M7N P64 PIMPY PQEST PQQKQ PQUKI PRINS 7X8 5PM DOA |
| DOI | 10.1371/journal.pntd.0007240 |
| DatabaseName | PubMed CrossRef ProQuest Central (Corporate) Bacteriology Abstracts (Microbiology B) Entomology Abstracts (Full archive) Health and Safety Science Abstracts (Full archive) Industrial and Applied Microbiology Abstracts (Microbiology A) Virology and AIDS Abstracts Health & Medical Complete (ProQuest Database) ProQuest Central (purchase pre-March 2016) Medical Database (Alumni Edition) Public Health Database (Proquest) Technology Research Database Hospital Premium Collection Hospital Premium Collection (Alumni Edition) ProQuest Central (Alumni) (purchase pre-March 2016) ProQuest Central (Alumni) ProQuest Central ProQuest Central Essentials AUTh Library subscriptions: ProQuest Central Environmental Sciences and Pollution Management ProQuest One Community College ProQuest Central ASFA: Aquatic Sciences and Fisheries Abstracts Engineering Research Database Health Research Premium Collection Health Research Premium Collection (Alumni) AIDS and Cancer Research Abstracts Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality ProQuest Health & Medical Complete (Alumni) Aquatic Science & Fisheries Abstracts (ASFA) Professional Health & Medical Collection (Alumni Edition) PML(ProQuest Medical Library) Algology Mycology and Protozoology Abstracts (Microbiology C) Biotechnology and BioEngineering Abstracts Publicly Available Content Database ProQuest One Academic Eastern Edition (DO NOT USE) ProQuest One Academic ProQuest One Academic UKI Edition ProQuest Central China MEDLINE - Academic PubMed Central (Full Participant titles) Directory of Open Access Journals |
| DatabaseTitle | PubMed CrossRef Publicly Available Content Database Aquatic Science & Fisheries Abstracts (ASFA) Professional Technology Research Database ProQuest Central Essentials ProQuest Health & Medical Complete (Alumni) ProQuest Central (Alumni Edition) ProQuest One Community College ProQuest Central China Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality Environmental Sciences and Pollution Management ProQuest Central Health Research Premium Collection Health and Medicine Complete (Alumni Edition) ProQuest Central Korea Bacteriology Abstracts (Microbiology B) Algology Mycology and Protozoology Abstracts (Microbiology C) AIDS and Cancer Research Abstracts Health & Safety Science Abstracts Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources Industrial and Applied Microbiology Abstracts (Microbiology A) ProQuest Medical Library (Alumni) ProQuest Public Health Virology and AIDS Abstracts ProQuest One Academic Eastern Edition ProQuest Hospital Collection Health Research Premium Collection (Alumni) ProQuest Hospital Collection (Alumni) Biotechnology and BioEngineering Abstracts Entomology Abstracts ProQuest Health & Medical Complete ProQuest Medical Library ProQuest One Academic UKI Edition ASFA: Aquatic Sciences and Fisheries Abstracts Engineering Research Database ProQuest One Academic ProQuest Central (Alumni) MEDLINE - Academic |
| DatabaseTitleList | PubMed MEDLINE - Academic Publicly Available Content Database |
| Database_xml | – sequence: 1 dbid: DOA name: DOAJ Directory of Open Access Journals url: https://www.doaj.org/ sourceTypes: Open Website – sequence: 2 dbid: NPM name: PubMed url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 3 dbid: BENPR name: AUTh Library subscriptions: ProQuest Central url: https://www.proquest.com/central sourceTypes: Aggregation Database |
| DeliveryMethod | fulltext_linktorsrc |
| Discipline | Medicine Chemistry |
| DocumentTitleAlternate | Pleiotropic antischistosomal effects of harmonine |
| EISSN | 1935-2735 |
| Editor | Brehm, Klaus |
| Editor_xml | – sequence: 1 givenname: Klaus surname: Brehm fullname: Brehm, Klaus |
| EndPage | e0007240 |
| ExternalDocumentID | 2252311759 oai_doaj_org_article_2ae045f16f1c47d5ad3ce0513e22e9cc A581353258 10_1371_journal_pntd_0007240 30870428 |
| Genre | Journal Article |
| GeographicLocations | Germany |
| GeographicLocations_xml | – name: Germany |
| GroupedDBID | --- 123 29O 2WC 3V. 53G 5VS 7X7 88E 8C1 8FI 8FJ AAFWJ ABDBF ABUWG ACGFO ACIHN ACPRK ADBBV ADRAZ AEAQA AENEX AFKRA AFPKN AFRAH AHMBA ALIPV ALMA_UNASSIGNED_HOLDINGS AOIJS BAWUL BCNDV BENPR BPHCQ BVXVI BWKFM CCPQU CS3 DIK DU5 E3Z EAP EAS EBD ECGQY EMOBN ESX F5P FPL FYUFA GROUPED_DOAJ GX1 H13 HMCUK HYE IAO IHR IHW IPNFZ ITC KQ8 M1P M48 M~E NPM O5R O5S OK1 P2P PGMZT PIMPY PQQKQ PROAC PSQYO PV9 RIG RNS RPM RZL SV3 TR2 TUS UKHRP WOQ AAYXX CITATION 7QL 7SS 7T2 7T7 7U9 7XB 8FD 8FK AZQEC C1K DWQXO F1W FR3 H94 H95 H97 K9. L.G M7N P64 PQEST PQUKI PRINS 7X8 5PM AAPBV ABPTK |
| ID | FETCH-LOGICAL-c624t-33f6f07229f6666a5909fb8eb7a9cb1ade7b35708c3400c69392ab695426d1a73 |
| IEDL.DBID | RPM |
| ISSN | 1935-2735 1935-2727 |
| IngestDate | Sun May 07 16:29:03 EDT 2023 Thu Sep 05 15:38:58 EDT 2024 Tue Sep 17 21:28:06 EDT 2024 Fri Jun 28 05:36:06 EDT 2024 Thu Oct 10 16:36:05 EDT 2024 Thu Feb 22 23:35:21 EST 2024 Fri Feb 02 04:02:21 EST 2024 Tue Aug 20 22:10:03 EDT 2024 Thu Sep 12 19:10:51 EDT 2024 Sat Sep 28 08:40:40 EDT 2024 |
| IsDoiOpenAccess | true |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 3 |
| Language | English |
| License | 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. Creative Commons Attribution License |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c624t-33f6f07229f6666a5909fb8eb7a9cb1ade7b35708c3400c69392ab695426d1a73 |
| Notes | new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 The authors have declared that no competing interests exist. |
| ORCID | 0000-0002-9551-3743 0000-0002-1932-9696 0000-0001-8276-4968 |
| OpenAccessLink | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6436750/ |
| PMID | 30870428 |
| PQID | 2252311759 |
| PQPubID | 1436337 |
| ParticipantIDs | plos_journals_2252311759 doaj_primary_oai_doaj_org_article_2ae045f16f1c47d5ad3ce0513e22e9cc pubmedcentral_primary_oai_pubmedcentral_nih_gov_6436750 proquest_miscellaneous_2193167508 proquest_journals_2252311759 gale_infotracmisc_A581353258 gale_infotracacademiconefile_A581353258 gale_healthsolutions_A581353258 crossref_primary_10_1371_journal_pntd_0007240 pubmed_primary_30870428 |
| PublicationCentury | 2000 |
| PublicationDate | 2019-03-01 |
| PublicationDateYYYYMMDD | 2019-03-01 |
| PublicationDate_xml | – month: 03 year: 2019 text: 2019-03-01 day: 01 |
| PublicationDecade | 2010 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States – name: San Francisco – name: San Francisco, CA USA |
| PublicationTitle | PLoS neglected tropical diseases |
| PublicationTitleAlternate | PLoS Negl Trop Dis |
| PublicationYear | 2019 |
| Publisher | Public Library of Science Public Library of Science (PLoS) |
| Publisher_xml | – name: Public Library of Science – name: Public Library of Science (PLoS) |
| References | CD Dettman (ref24) 1989; 76 R Arnon (ref36) 1999; 8 I Popiel (ref50) 1984; 58 CR Röhrich (ref7) 2012; 8 NC Nagel (ref12) 2015; 13 S Hahnel (ref32) 2014; 5 IN Mwangi (ref20) 2014; 4 DJ Newman (ref1) 2012; 75 S Xiao (ref52) 2000; 86 M Camacho (ref55) 1995; 81 A Vilcinskas (ref6) 2015; 22 DA Denham (ref63) 1971; 65 S Beckmann (ref31) 2010; 40 AK Jones (ref56) 2002; 16 U Koziol (ref45) 2014; 5 JJ Collins 3rd (ref44) 2013; 494 CV Kramer (ref61) 2014 A Vilcinskas (ref10) 2013; 340 H Schmidtberg (ref5) 2013; 9 Y Wang (ref43) 2007; 104 R Kaminsky (ref53) 2008; 103 P McCusker (ref46) 2016; 10 BR Giri (ref66) 2017; 116 WR Lee (ref75) 2015; 7 GL Ellman (ref29) 1961; 7 RH Neves (ref30) 2005; 95 B Wang (ref42) 2018; 7 GR Mair (ref48) 2000; 121 FR Melek (ref70) 2012; 50 MJ Doenhoff (ref17) 2008; 21 AW Cheever (ref16) 1994; 50 E Bueding (ref35) 1972; 46 BE Barker LR (ref58) 1966; 26 GN Bentley (ref38) 2005; 141 JM Fitzpatrick (ref59) 2006; 36 T Gegner (ref8) 2018; 8 CG Grevelding (ref23) 1995; 71 LE Paraoanu (ref68) 2007; 80 JJ Van Hellemond (ref49) 2006; 36 H You (ref57) 2016; 9 ref34 R Gönnert (ref22) 1955; 6 ref33 J de Moraes (ref3) 2011; 8 PJ Keeling (ref9) 2002; 56 DA Erasmus (ref47) 1973; 67 S Hahnel (ref28) 2013; 7 BJ Neves (ref2) 2015; 20 AG Hegazi (ref74) 2000; 55 SS Botros (ref18) 2007; 2 D Landgraf (ref67) 2010; 187 H You (ref37) 2017; 22 B Ramirez (ref25) 2007; 2 M Waisberg (ref60) 2007; 8 GR Wendt (ref64) 2016; 40 AH Mohamed (ref4) 2016; 40 J Wang (ref65) 2016; 46 O Imamura (ref69) 2017; 140 KJ Livak (ref27) 2001; 25 Z Lu (ref39) 2016; 6 AM Glauert (ref51) 1978; 34 MDS Regueira-Neto (ref73) 2018; 119 D Cioli (ref21) 2014; 195 PG Fallon (ref19) 1994; 51 F Ponchel (ref26) 2003; 3 HB Weng (ref14) 2018; 7 AM Prugh (ref41) 2017; 266 JA Hartsel (ref62) 2012; 22 FJ Verheggen (ref11) 2017; 5 AP Robertson (ref54) 2007; 7 PJ Hotez (ref15) 2014; 8 J Sopkova-de Oliveira Santos (ref40) 2010; 50 N Orsolic (ref76) 2012; 31 EA Hassan (ref72) 2016; 49 F Kenyon (ref13) 2017; 33 MH Mona (ref71) 2012; 50 |
| References_xml | – volume: 266 start-page: 38 year: 2017 ident: ref41 article-title: Effects of organophosphates on the regulation of mesenchymal stem cell proliferation and differentiation publication-title: Chemico-biological interactions doi: 10.1016/j.cbi.2017.01.020 contributor: fullname: AM Prugh – volume: 8 start-page: e2865 issue: 7 year: 2014 ident: ref15 article-title: The global burden of disease study 2010: interpretation and implications for the neglected tropical diseases. publication-title: PLoS neglected tropical diseases doi: 10.1371/journal.pntd.0002865 contributor: fullname: PJ Hotez – volume: 2 start-page: S53 issue: s1 year: 2007 ident: ref25 article-title: Schistosomes: challenges in compound screening. publication-title: Expert opinion on drug discovery doi: 10.1517/17460441.2.S1.S53 contributor: fullname: B Ramirez – volume: 20 start-page: 1872 issue: 2 year: 2015 ident: ref2 article-title: Natural products as leads in schistosome drug discovery publication-title: Molecules (Basel, Switzerland). doi: 10.3390/molecules20021872 contributor: fullname: BJ Neves – volume: 119 start-page: 215 year: 2018 ident: ref73 article-title: Antitrypanosomal, antileishmanial and cytotoxic activities of Brazilian red propolis and plant resin of Dalbergia ecastaphyllum (L) Taub. publication-title: Food and chemical toxicology: an international journal published for the British Industrial Biological Research Association doi: 10.1016/j.fct.2018.04.029 contributor: fullname: MDS Regueira-Neto – volume: 95 start-page: 43 issue: 1 year: 2005 ident: ref30 article-title: A new description of the reproductive system of Schistosoma mansoni (Trematoda: Schistosomatidae) analyzed by confocal laser scanning microscopy publication-title: Parasitology research doi: 10.1007/s00436-004-1241-2 contributor: fullname: RH Neves – volume: 58 start-page: 254 issue: 3 year: 1984 ident: ref50 article-title: Schistosoma mansoni: ultrastructure of adults from mice treated with oxamniquine publication-title: Experimental parasitology doi: 10.1016/0014-4894(84)90042-0 contributor: fullname: I Popiel – volume: 7 start-page: e2336 issue: 7 year: 2013 ident: ref28 article-title: Whole-organ isolation approach as a basis for tissue-specific analyses in Schistosoma mansoni publication-title: PLoS neglected tropical diseases doi: 10.1371/journal.pntd.0002336 contributor: fullname: S Hahnel – volume: 121 start-page: 163 issue: Pt 2 year: 2000 ident: ref48 article-title: A confocal microscopical study of the musculature of adult Schistosoma mansoni publication-title: Parasitology doi: 10.1017/S0031182099006174 contributor: fullname: GR Mair – volume: 86 start-page: 1125 issue: 5 year: 2000 ident: ref52 article-title: Tegumental changes in adult Schistosoma mansoni harbored in mice treated with artemether publication-title: The Journal of parasitology doi: 10.1645/0022-3395(2000)086[1125:TCIASM]2.0.CO;2 contributor: fullname: S Xiao – volume: 51 start-page: 83 issue: 1 year: 1994 ident: ref19 article-title: Drug-resistant schistosomiasis: resistance to praziquantel and oxamniquine induced in Schistosoma mansoni in mice is drug specific publication-title: The American journal of tropical medicine and hygiene doi: 10.4269/ajtmh.1994.51.83 contributor: fullname: PG Fallon – volume: 26 start-page: 656 issue: 3 year: 1966 ident: ref58 article-title: The possible role of acetylcholine in Schistosoma mansoni publication-title: Br J Pharmacol Chemother doi: 10.1111/j.1476-5381.1966.tb01845.x contributor: fullname: BE Barker LR – volume: 4 start-page: 296 issue: 3 year: 2014 ident: ref20 article-title: Praziquantel sensitivity of Kenyan Schistosoma mansoni isolates and the generation of a laboratory strain with reduced susceptibility to the drug publication-title: International journal for parasitology Drugs and drug resistance doi: 10.1016/j.ijpddr.2014.09.006 contributor: fullname: IN Mwangi – ident: ref34 – volume: 103 start-page: 931 issue: 4 year: 2008 ident: ref53 article-title: Identification of the amino-acetonitrile derivative monepantel (AAD 1566) as a new anthelmintic drug development candidate publication-title: Parasitology research doi: 10.1007/s00436-008-1080-7 contributor: fullname: R Kaminsky – volume: 7 start-page: 209 issue: 4 year: 2007 ident: ref54 article-title: Ion-channels on parasite muscle: pharmacology and physiology. publication-title: Invertebrate neuroscience: IN doi: 10.1007/s10158-007-0059-x contributor: fullname: AP Robertson – volume: 50 start-page: 490 issue: 4 year: 2012 ident: ref70 article-title: Screening of marine extracts for schistosomicidal activity in vitro. Isolation of the triterpene glycosides echinosides A and B with potential activity from the sea cucumbers Actinopyga echinites and Holothuria polii publication-title: Pharmaceutical biology doi: 10.3109/13880209.2011.615842 contributor: fullname: FR Melek – volume: 7 start-page: 4758 issue: 11 year: 2015 ident: ref75 article-title: The protective effect of bee venom on fibrosis causing inflammatory diseases publication-title: Toxins doi: 10.3390/toxins7114758 contributor: fullname: WR Lee – volume: 56 start-page: 93 year: 2002 ident: ref9 article-title: Microsporidia: biology and evolution of highly reduced intracellular parasites publication-title: Annual review of microbiology doi: 10.1146/annurev.micro.56.012302.160854 contributor: fullname: PJ Keeling – volume: 33 start-page: 669 issue: 9 year: 2017 ident: ref13 article-title: Worm control in livestock: bringing science to the field publication-title: Trends in parasitology doi: 10.1016/j.pt.2017.05.008 contributor: fullname: F Kenyon – volume: 81 start-page: 584 issue: 4 year: 1995 ident: ref55 article-title: Schistosoma: rate of glucose import is altered by acetylcholine interaction with tegumental acetylcholine receptors and acetylcholinesterase publication-title: Experimental parasitology doi: 10.1006/expr.1995.1152 contributor: fullname: M Camacho – volume: 8 start-page: 181 year: 2007 ident: ref60 article-title: Microarray analysis of gene expression induced by sexual contact in Schistosoma mansoni publication-title: BMC genomics doi: 10.1186/1471-2164-8-181 contributor: fullname: M Waisberg – volume: 40 start-page: 521 issue: 5 year: 2010 ident: ref31 article-title: Imatinib has a fatal impact on morphology, pairing stability and survival of adult Schistosoma mansoni in vitro publication-title: International journal for parasitology doi: 10.1016/j.ijpara.2010.01.007 contributor: fullname: S Beckmann – volume: 8 start-page: 2553 issue: 12 year: 1999 ident: ref36 article-title: Acetylcholinesterase of Schistosoma mansoni—functional correlates. Contributed in honor of Professor Hans Neurath's 90th birthday publication-title: Protein science: a publication of the Protein Society doi: 10.1110/ps.8.12.2553 contributor: fullname: R Arnon – volume: 7 start-page: 67 issue: 1 year: 2018 ident: ref14 article-title: Innovation in neglected tropical disease drug discovery and development publication-title: Infectious diseases of poverty doi: 10.1186/s40249-018-0444-1 contributor: fullname: HB Weng – volume: 195 start-page: 23 issue: 1 year: 2014 ident: ref21 article-title: Schistosomiasis control: praziquantel forever? publication-title: Molecular and biochemical parasitology doi: 10.1016/j.molbiopara.2014.06.002 contributor: fullname: D Cioli – volume: 2 start-page: S35 issue: s1 year: 2007 ident: ref18 article-title: Praziquantel resistance publication-title: Expert opinion on drug discovery doi: 10.1517/17460441.2.S1.S35 contributor: fullname: SS Botros – volume: 50 start-page: 422 issue: 3 year: 2010 ident: ref40 article-title: Virtual screening discovery of new acetylcholinesterase inhibitors issued from CERMN chemical library publication-title: Journal of chemical information and modeling doi: 10.1021/ci900491t contributor: fullname: J Sopkova-de Oliveira Santos – volume: 76 start-page: 183 issue: 2 year: 1989 ident: ref24 article-title: Enhanced efficacy of the paddling method for schistosome infection of rodents by a four-step pre-soaking procedure publication-title: Parasitology research doi: 10.1007/BF00930846 contributor: fullname: CD Dettman – volume: 13 start-page: 5139 issue: 18 year: 2015 ident: ref12 article-title: Efficient synthesis of (R)-harmonine—the toxic principle of the multicolored Asian lady beetle (Harmonia axyridis). publication-title: Organic & biomolecular chemistry doi: 10.1039/C5OB00461F contributor: fullname: NC Nagel – volume: 141 start-page: 119 issue: 1 year: 2005 ident: ref38 article-title: Expression and comparative functional characterisation of recombinant acetylcholinesterase from three species of Schistosoma publication-title: Molecular and biochemical parasitology doi: 10.1016/j.molbiopara.2005.01.019 contributor: fullname: GN Bentley – volume: 36 start-page: 1081 issue: 10–11 year: 2006 ident: ref59 article-title: Dioecious Schistosoma mansoni express divergent gene repertoires regulated by pairing publication-title: International journal for parasitology doi: 10.1016/j.ijpara.2006.06.007 contributor: fullname: JM Fitzpatrick – volume: 116 start-page: 1947 issue: 7 year: 2017 ident: ref66 article-title: Molecular characterization and expression profile of nanos in Schistosoma japonicum and its influence on the expression several mammalian stem cell factors publication-title: Parasitology research doi: 10.1007/s00436-017-5476-0 contributor: fullname: BR Giri – volume: 340 start-page: 862 issue: 6134 year: 2013 ident: ref10 article-title: Invasive harlequin ladybird carries biological weapons against native competitors publication-title: Science (New York, NY). doi: 10.1126/science.1234032 contributor: fullname: A Vilcinskas – volume: 6 start-page: 33 issue: 1 year: 1955 ident: ref22 article-title: Schistosomiasis-Studien. II. Über die Eibildung bei Schistosoma mansoni und das Schicksal der Eier im Wirtsorganismus publication-title: Zeitschrift fur Tropenmedizin und Parasitologie contributor: fullname: R Gönnert – volume: 22 issue: 9 year: 2017 ident: ref37 article-title: Acetylcholinesterase and nicotinic acetylcholine receptors in schistosomes and other parasitic helminths publication-title: Molecules (Basel, Switzerland). contributor: fullname: H You – volume: 16 start-page: 441 issue: 3 year: 2002 ident: ref56 article-title: Molecular characterization of an acetylcholinesterase implicated in the regulation of glucose scavenging by the parasite Schistosoma publication-title: FASEB journal: official publication of the Federation of American Societies for Experimental Biology doi: 10.1096/fj.01-0683fje contributor: fullname: AK Jones – volume: 22 start-page: 313 issue: 3 year: 2015 ident: ref6 article-title: Evolutionary ecology of microsporidia associated with the invasive ladybird Harmonia axyridis publication-title: Insect science doi: 10.1111/1744-7917.12159 contributor: fullname: A Vilcinskas – volume: 6 start-page: 31150 year: 2016 ident: ref39 article-title: Schistosome sex matters: a deep view into gonad-specific and pairing-dependent transcriptomes reveals a complex gender interplay publication-title: Scientific reports doi: 10.1038/srep31150 contributor: fullname: Z Lu – volume: 187 start-page: 115 issue: 1–3 year: 2010 ident: ref67 article-title: Acetylcholine as a possible signaling molecule in embryonic stem cells: studies on survival, proliferation and death publication-title: Chemico-biological interactions doi: 10.1016/j.cbi.2010.03.007 contributor: fullname: D Landgraf – volume: 3 start-page: 18 year: 2003 ident: ref26 article-title: Real-time PCR based on SYBR-Green I fluorescence: an alternative to the TaqMan assay for a relative quantification of gene rearrangements, gene amplifications and micro gene deletions publication-title: BMC biotechnology doi: 10.1186/1472-6750-3-18 contributor: fullname: F Ponchel – ident: ref33 – volume: 80 start-page: 2375 issue: 24–25 year: 2007 ident: ref68 article-title: Expression and possible functions of the cholinergic system in a murine embryonic stem cell line publication-title: Life sciences doi: 10.1016/j.lfs.2007.03.008 contributor: fullname: LE Paraoanu – volume: 50 start-page: 1144 issue: 9 year: 2012 ident: ref71 article-title: Antischistosomal effect of holothurin extracted from some Egyptian sea cucumbers publication-title: Pharmaceutical biology doi: 10.3109/13880209.2012.661741 contributor: fullname: MH Mona – volume: 5 start-page: 170 year: 2014 ident: ref32 article-title: Gonad RNA-specific qRT-PCR analyses identify genes with potential functions in schistosome reproduction such as SmFz1 and SmFGFRs publication-title: Frontiers in genetics doi: 10.3389/fgene.2014.00170 contributor: fullname: S Hahnel – volume: 7 year: 2018 ident: ref42 article-title: Stem cell heterogeneity drives the parasitic life cycle of Schistosoma mansoni publication-title: eLife doi: 10.7554/eLife.35449 contributor: fullname: B Wang – volume: 8 start-page: 308 issue: 2 year: 2012 ident: ref7 article-title: Harmonine, a defence compound from the harlequin ladybird, inhibits mycobacterial growth and demonstrates multi-stage antimalarial activity publication-title: Biology letters doi: 10.1098/rsbl.2011.0760 contributor: fullname: CR Röhrich – volume: 9 start-page: 20130006 issue: 3 year: 2013 ident: ref5 article-title: A switch from constitutive chemical defence to inducible innate immune responses in the invasive ladybird Harmonia axyridis publication-title: Biology letters doi: 10.1098/rsbl.2013.0006 contributor: fullname: H Schmidtberg – volume: 5 issue: 156 year: 2017 ident: ref11 article-title: Behavioral and immunological features promoting the invasive performance of the harlequin ladybird Harmonia axyridis publication-title: Frontiers in Ecology and Evolution contributor: fullname: FJ Verheggen – volume: 67 start-page: 165 issue: 2 year: 1973 ident: ref47 article-title: A comparative study of the reproductive system of mature, immature and "unisexual" female Schistosoma mansoni publication-title: Parasitology doi: 10.1017/S0031182000046394 contributor: fullname: DA Erasmus – volume: 5 start-page: 10 issue: 1 year: 2014 ident: ref45 article-title: The unique stem cell system of the immortal larva of the human parasite Echinococcus multilocularis publication-title: EvoDevo doi: 10.1186/2041-9139-5-10 contributor: fullname: U Koziol – volume: 140 start-page: 231 issue: 2 year: 2017 ident: ref69 article-title: Donepezil promotes differentiation of neural stem cells into mature oligodendrocytes at the expense of astrogenesis publication-title: Journal of neurochemistry doi: 10.1111/jnc.13856 contributor: fullname: O Imamura – volume: 22 start-page: 4593 issue: 14 year: 2012 ident: ref62 article-title: Re-engineering aryl methylcarbamates to confer high selectivity for inhibition of Anopheles gambiae versus human acetylcholinesterase publication-title: Bioorganic & medicinal chemistry letters doi: 10.1016/j.bmcl.2012.05.103 contributor: fullname: JA Hartsel – volume: 46 start-page: 480 issue: 3 year: 1972 ident: ref35 article-title: Inhibition by metrifonate and dichlorvos of cholinesterases in schistosomes publication-title: British journal of pharmacology doi: 10.1111/j.1476-5381.1972.tb08145.x contributor: fullname: E Bueding – volume: 49 start-page: 752 issue: 6 year: 2016 ident: ref72 article-title: In vitro antischistosomal activity of venom from the Egyptian snake Cerastes cerastes publication-title: Revista da Sociedade Brasileira de Medicina Tropical doi: 10.1590/0037-8682-0241-2016 contributor: fullname: EA Hassan – volume: 25 start-page: 402 issue: 4 year: 2001 ident: ref27 article-title: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method publication-title: Methods (San Diego, Calif). doi: 10.1006/meth.2001.1262 contributor: fullname: KJ Livak – volume: 40 start-page: 390 issue: 2 year: 2016 ident: ref4 article-title: Effect of bee venom or proplis on molecular and parasitological aspects of Schistosoma mansoni infected mice publication-title: Journal of parasitic diseases: official organ of the Indian Society for Parasitology doi: 10.1007/s12639-014-0516-5 contributor: fullname: AH Mohamed – volume: 494 start-page: 476 issue: 7438 year: 2013 ident: ref44 article-title: Adult somatic stem cells in the human parasite Schistosoma mansoni publication-title: Nature doi: 10.1038/nature11924 contributor: fullname: JJ Collins 3rd – volume: 8 start-page: 548 issue: 3 year: 2011 ident: ref3 article-title: Evaluation of the in vitro activity of dermaseptin 01, a cationic antimicrobial peptide, against Schistosoma mansoni. publication-title: Chemistry & biodiversity doi: 10.1002/cbdv.201000163 contributor: fullname: J de Moraes – volume: 104 start-page: 5901 issue: 14 year: 2007 ident: ref43 article-title: Nanos function is essential for development and regeneration of planarian germ cells publication-title: Proceedings of the National Academy of Sciences of the United States of America doi: 10.1073/pnas.0609708104 contributor: fullname: Y Wang – volume: 34 start-page: 173 year: 1978 ident: ref51 article-title: The mechansim of antibody-dependent, eosinophil-mediated damage to schistosomula of Schistosoma mansoni in vitro: a study by phase-contrast and electron microscopy publication-title: Journal of cell science doi: 10.1242/jcs.34.1.173 contributor: fullname: AM Glauert – volume: 7 start-page: 88 year: 1961 ident: ref29 article-title: A new and rapid colorimetric determination of acetylcholinesterase activity publication-title: Biochemical pharmacology doi: 10.1016/0006-2952(61)90145-9 contributor: fullname: GL Ellman – volume: 36 start-page: 691 issue: 6 year: 2006 ident: ref49 article-title: Functions of the tegument of schistosomes: clues from the proteome and lipidome publication-title: International journal for parasitology doi: 10.1016/j.ijpara.2006.01.007 contributor: fullname: JJ Van Hellemond – start-page: Cd000053 issue: 8 year: 2014 ident: ref61 article-title: Drugs for treating urinary schistosomiasis publication-title: The Cochrane database of systematic reviews contributor: fullname: CV Kramer – volume: 10 start-page: e0004994 issue: 9 year: 2016 ident: ref46 article-title: Stimulating neoblast-like cell proliferation in juvenile Fasciola hepatica supports growth and progression towards the adult phenotype in vitro publication-title: PLoS neglected tropical diseases doi: 10.1371/journal.pntd.0004994 contributor: fullname: P McCusker – volume: 40 start-page: 95 year: 2016 ident: ref64 article-title: 3rd. Schistosomiasis as a disease of stem cells publication-title: Current opinion in genetics & development doi: 10.1016/j.gde.2016.06.010 contributor: fullname: GR Wendt – volume: 65 start-page: 696 issue: 5 year: 1971 ident: ref63 article-title: The effect of metrifonate in vitro on Schistosoma haematobium and S. mansoni adults publication-title: Transactions of the Royal Society of Tropical Medicine and Hygiene doi: 10.1016/0035-9203(71)90070-8 contributor: fullname: DA Denham – volume: 50 start-page: 281 issue: 3 year: 1994 ident: ref16 article-title: Kinetics of egg production and egg excretion by Schistosoma mansoni and S. japonicum in mice infected with a single pair of worms publication-title: The American journal of tropical medicine and hygiene doi: 10.4269/ajtmh.1994.50.281 contributor: fullname: AW Cheever – volume: 71 start-page: 269 issue: 2 year: 1995 ident: ref23 article-title: The female-specific W1 sequence of the Puerto Rican strain of Schistosoma mansoni occurs in both genders of a Liberian strain publication-title: Molecular and biochemical parasitology doi: 10.1016/0166-6851(94)00058-U contributor: fullname: CG Grevelding – volume: 31 start-page: 173 issue: 1–2 year: 2012 ident: ref76 article-title: Bee venom in cancer therapy publication-title: Cancer metastasis reviews doi: 10.1007/s10555-011-9339-3 contributor: fullname: N Orsolic – volume: 8 start-page: 3600 issue: 1 year: 2018 ident: ref8 article-title: Population-specific expression of antimicrobial peptides conferring pathogen resistance in the invasive ladybird Harmonia axyridis publication-title: Scientific reports doi: 10.1038/s41598-018-21781-4 contributor: fullname: T Gegner – volume: 75 start-page: 311 issue: 3 year: 2012 ident: ref1 article-title: Natural products as sources of new drugs over the 30 years from 1981 to 2010 publication-title: Journal of natural products doi: 10.1021/np200906s contributor: fullname: DJ Newman – volume: 9 start-page: 328 issue: 1 year: 2016 ident: ref57 article-title: Functional characterisation of Schistosoma japonicum acetylcholinesterase publication-title: Parasites & vectors doi: 10.1186/s13071-016-1615-1 contributor: fullname: H You – volume: 46 start-page: 405 issue: 7 year: 2016 ident: ref65 article-title: Identification of new markers for the Schistosoma mansoni vitelline lineage publication-title: International journal for parasitology doi: 10.1016/j.ijpara.2016.03.004 contributor: fullname: J Wang – volume: 55 start-page: 70 issue: 1–2 year: 2000 ident: ref74 article-title: Chemical composition and antimicrobial activity of European propolis publication-title: Zeitschrift fur Naturforschung C, Journal of biosciences doi: 10.1515/znc-2000-1-214 contributor: fullname: AG Hegazi – volume: 21 start-page: 659 issue: 6 year: 2008 ident: ref17 article-title: Praziquantel: mechanisms of action, resistance and new derivatives for schistosomiasis publication-title: Current opinion in infectious diseases doi: 10.1097/QCO.0b013e328318978f contributor: fullname: MJ Doenhoff |
| SSID | ssj0059581 |
| Score | 2.3836935 |
| Snippet | Natural products have moved into the spotlight as possible sources for new drugs in the treatment of helminth infections including schistosomiasis.... |
| SourceID | plos doaj pubmedcentral proquest gale crossref pubmed |
| SourceType | Open Website Open Access Repository Aggregation Database Index Database |
| StartPage | e0007240 |
| SubjectTerms | Acetylcholinesterase Alkaloids Anthelmintics Antimicrobial agents Backup software Biology and Life Sciences Biotechnology Cancer therapies Care and treatment Cell culture Cell proliferation Cell survival Cells Chemical properties Chemistry Confocal microscopy Control DNA Drug discovery Dysplasia Egg production Eggs Enzymes Gene expression Genes Gonads Human blood fluke Immune system Insects Ladybugs Lasers Lethal effects Medicine and Health Sciences Metabolites Microscopy Natural products Novels Nucleotide sequence Ovaries Parasites Parasitology PCR Peptides Pharmaceuticals Physical Sciences Physiological aspects Physiological effects Praziquantel Proliferation Research and Analysis Methods Scanning microscopy Scanning transmission electron microscopy Schistosoma mansoni Schistosomiasis Stem cell research Stem cell transplantation Stem cells Survival Testing Tropical diseases Worms |
| SummonAdditionalLinks | – databaseName: Directory of Open Access Journals dbid: DOA link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1Lj9MwELZQD4gLYnltlwWMhMSFsEkcxzW3BbFaEMsFVtpb5MdYrbRNKtKuxO_gDzNjp1WDVuLCtXaceubzeCae-czYa1fnEOgOQKhsnlW6MLjmZJHVGI1IpaVSguqdL77V55fVlyt5tXfVF-WEJXrgJLiT0gB6HaGoQ-Eq5aXxwgEiSUBZgnYuWt9CboOpZIOllvF6UvROqOKqVEPRnFDFyaCjd6t27Ym9UJX04WNvU4rc_TsLPVldd_1t7uffWZR729LZA3Z_8Cf5aZrHAbsD7UN292I4MX_Efn9ue0rY4IuWoxDncL1ctDHHnQ88P_P3_Kvxv7gFQNxkHiF5A54TpTV9qgVuUsoH7zdoVhCYbzkxYUaiWFQqjuo5sUFzOgPgK7oFKEDCFe8C_-4ipXHfLQ1fGio1Wzxml2effnw8z4aLGDJXl9U6EyLUAQVV6oDRTm2kznWwM7DKaGcL40FZIVU-cwJNgqs1Ol3G1lri9u8Lo8QTNmm7Fg4ZV0oGZXU-CyWg72ZsAG9dAa70El8wm7Jsq4lmlfg2mnjopjBOSSJtSHPNoLkp-0Dq2vUltuz4A2KoGTDU_AtDU_aSlN2k0tPdmm9OEUVCilLi33oTe9CqR2U7MxQv4KSIP2vU83jUE1erGzUfEqC2c-kbtKfoYqMTp_HJLchub361a6ZBKTmuhW6DfRDmBQZ-OY7-NGFyJw8ifKSweMrUCK0jgY1b2sU80oyjr0qDHv0PCT9j99DT1Cl575hN1j838By9ubV9ERfuH1IwSb0 priority: 102 providerName: Directory of Open Access Journals – databaseName: Health & Medical Complete (ProQuest Database) dbid: 7X7 link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV3db9MwELegSMDLBONjHQOMhMQLYYldxzUvaExMAzFeYFLfIn_SSmtSlhaJv4N_mDvHDQuaeK0dN_H9fL6z735HyEtb5j5gDUA_MXk2UYWGNSeKrARvREglpOSY73z2pTw9n3yaiVk6cGtTWOVWJ0ZF7RqLZ-SHgDswRWCzU-9WPzKsGoW3q6mExk1yq2BgTACe5ax3uIQSsUgp2CiYd8VkSp3jsjhMknqzqtcOOQwlw-OPK1tTZPDv9fRoddG01xmh_8ZSXtmcTu6RnWRV0qMOBvfJDV_vkjvH22Juu-T2WbpDf0B-f6xbDOGgi5rCtM79xXJRx6h3mph_5m_pZ-1-UeM9IClzANKf3lEkucbDW091FwRC2w0oGoDqa4rcmJE6FsQMozqK_NAUbwXoCusCBd8hjTaBfrWR5LhtlpouNSafLR6S85MP345Ps1SaIbMlm6wzzkMZYNKYCuD_lFqoXAUz9UZqZU2hnZeGC5lPLQclYUsFZpg2pRJgELhCS_6IjOqm9nuESimCNCqfBubBmtMmeGds4S1zAv5gOibZVirVqmPgqOI1nATPpZveCqVYJSmOyXsUXd8X-bPjD83l9yotx4ppD7ZsKMpQ2Il0QjtuPegn7hnzytoxeY6Cr7pk1F4LVEeAKC44E_Bar2IP1AMgeKtTOgN8FDJqDXoeDHqC5O2geQ_Btf2WtvqLdHhyC7jrm1_0zTgohsvVvtlAH4B8Aa5gDqM_7vDZzwdSQKKjPCZygNzBhA1b6sU8Eo-D9YqD7v__tZ6Qu2BVqi5Q74CM1pcb_xQst7V5FpfnH2hxREs priority: 102 providerName: ProQuest – databaseName: Scholars Portal Journals: Open Access dbid: M48 link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV1Lj9MwELaWIiEuiPd2WcBISFzIKonjuEZCaEGsFkS5QKW9RX5uK7VJadoV-zv4w8w4DxFUDlxrx21mPo9n6plvCHlp8th57AHoMh1HmUwU7DmeRDlEI1xILgTDeufp1_x8ln2-4BcHpOvZ2gqw3hvaYT-p2WZ58vPH9TvY8G9D1waRdA-drMutRT5CAafUDXIzzViGmJ9m_b0Clzy0LQWvBSuxGG-L6f61yuCwCpz-veUerZdVvc8t_Tu78o_j6uwuudP6mfS0AcY9cuDK--TWtL1Jf0B-fSprTOSgi5KCcOduuVqUIfedtvw_8zf0i7LXVDsHeIosQPXKWYpU1_gXrqOqSQWh9Q7MDQD2NUWGzEAgC8qGVS1FlmiKdwN0jd2BvGvwRitPv5lAdVxXK0VXCkvQFg_J7Ozj9w_nUdugITJ5mm0jxnzuQVCp9BAF5YrLWHo9cVooaXSirBOacRFPDANTYXIJzpjSueTgFthECfaIjMqqdIeECsG90DKe-NSBT6e0d1abxJnUcviCyZhEnSaKdcPDUYTLOAHxSyPSAjVXtJobk_eorn4usmiHD6rNZdFuyiJVDjxan-Q-MZmwXFlmHFgp5tLUSWPG5Dkqu2hKUntbUJwCihhnKYef9SrMQHyCso1qixrgpZBXazDzeDATdrEZDB8ioLp3qQuws-B6g3Mn4ckOZPuHX_TDuCgmzZWu2sEcgHkCAWEMqz9uMNnLA4kgMVweEzFA60Bgw5FyMQ_04-DD4qJH_6mRJ-Q2OJuyyd87JqPtZueegkO31c_CHv0NBxtMjg priority: 102 providerName: Scholars Portal |
| Title | Insects in anthelminthics research: Lady beetle-derived harmonine affects survival, reproduction and stem cell proliferation of Schistosoma mansoni |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/30870428 https://www.proquest.com/docview/2252311759 https://search.proquest.com/docview/2193167508 https://pubmed.ncbi.nlm.nih.gov/PMC6436750 https://doaj.org/article/2ae045f16f1c47d5ad3ce0513e22e9cc http://dx.doi.org/10.1371/journal.pntd.0007240 |
| Volume | 13 |
| hasFullText | 1 |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3Pb9MwFLa2Ik27IH6vMIqRkLiQNonjOOa2VZsGotMETOotsh2bVmqTaG2R-Dv4h3nPSSqCduKSQ-24id_37M_xe58JeWfS0Do8A9AmOgwSGSnwOR4FKaxGuJBcCIb5zrPr9Oo2-Tzn8wPCu1wYH7Rv9HJcrtbjcrnwsZX12ky6OLHJzWwKsyjw3HBySA4FY90SvRl-ueT-ZFIgJphsFYs2X46JaNKaZ1yX2wKFCwVMZ8fkCEXxcOnQm5q8gv9-nB7Uq2pzHwn9N5byr8np8hF52LJKetY8_WNyYMsn5GjW7ps_Jb8_lRsM26DLkkJXLuxqvSx9pDtt1X4WH-kXVfyi2lpAT1AAMH_agqKwNX6wtVQ1gR90s4PBBeD5gaIeppeLBdNCqwVFTWiKOwG0xrOAnG3QRStHvxkvbLyp1oquFSacLZ-R28uL79OroD2OITBpnGwDxlzqoM9i6WDNkyouQ-l0ZrVQ0uhIFVZoxkWYGQYDg0klUC-lU8mBBBSREuw5GZRVaU8IFYI7oWWYudgCg1Pa2UKbyJq44PAH2ZAEnSXyulHdyP3Wm4DVStOlORoxb404JOdorn1d1Mz2P1R3P_IWOXmsLPBXF6UuMokouCqYsTAmMRvHVhozJG_Q2HmTgLr3_PwMAMU4izk81ntfA30fjG1Um8IAL4UqWr2ap72a4LOmV3yCgOreZZPDqApEG6ichDs7kN1f_HZfjI1iiFxpqx3UAcRH6BbQ-osGk_v-6BA-JKKH1l6H9UvA97zYeOtrL__7zlfkGEimbOL2Tslge7ezr4HIbfUI3Hcu4JpNoxF5cH5xffN15D-KwHWWZCPv2H8ABi9Olw |
| link.rule.ids | 230,315,733,786,790,870,891,2115,2236,12083,12250,21416,24346,27957,27958,31754,31755,33301,33302,33779,33780,43345,43614,43840,53827,53829,74102,74371,74659 |
| linkProvider | National Library of Medicine |
| linkToHtml | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV3fb9MwELagSIwXBAO2wmBGQuKFsCSO45oXNCqmDtq9sEl7ixz_oJXWpCwtEn8H_zB3jhsWNPFaO27i-3y-s---I-SNzmPrsAagzco4ymSiYM3xJMrBG-FCciEY5jvPzvLJRfblkl-GA7cmhFVudaJX1KbWeEZ-BLgDUwQ2O_lx9SPCqlF4uxpKaNwl9zIGGw1mio-7EA8uuS9SCjYK5l2lIqTOMZEcBUm9X1VrgxyGIsXjjxtbk2fw7_T0YHVVN7cZof_GUt7YnE4ekYfBqqTHLQwekzu22iU7420xt11yfxbu0J-Q36dVgyEcdFFRmNa5vVouKh_1TgPzz_wDnSrzi5bWApIiAyD9aQ1Fkms8vLVUtUEgtNmAogGovqPIjempY0HMMKqhyA9N8VaArrAukLMt0mjt6DftSY6beqnoUmHy2eIpuTj5fD6eRKE0Q6TzNFtHjLncwaSl0oH_kysuY-nKkS2FkrpMlLGiZFzEI81ASehcghmmylxyMAhMogR7RgZVXdl9QoXgTpQyHrnUgjWnSmdNqROrU8PhD0ZDEm2lUqxaBo7CX8MJ8Fza6S1QikWQ4pB8QtF1fZE_2_9QX38vwnIsUmXBlnVJ7hKdCcOVYdqCfmI2Ta3UekgOUfBFm4zaaYHiGBDFOEs5vNZb3wP1AAheq5DOAB-FjFq9nge9niB53WveR3Btv6Up_iIdntwC7vbm110zDorhcpWtN9AHIJ-AKxjD6HstPrv5QApIdJSHRPSQ25uwfku1mHvicbBecdDn_3-tQ7IzOZ9Ni-np2dcX5AFYmLIN2jsgg_X1xr4EK25dvvJL9Q9tIEcF |
| linkToPdf | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV3db9MwELegSIMXBONjhcGMhMQLoUlcxzUvaAyqDbYJCSbtLfInrbQmZWmR-Dv4h7lz3LCgidfacRPfz-c7--53hLw0Reo81gB0Y50mY5kpWHM8SwrwRriQXAiG-c4np8Xh2fjTOT-P8U9NDKvc6MSgqG1t8Ix8BLgDUwQ2OznyMSziy4fpu-WPBCtI4U1rLKdxk9yCXTLFagbivHO-uOShYCnYK5iDlYuYRsdENopSe7OsVhb5DEWORyFXtqnA5t_p7MHyom6uM0j_jau8slFN75G70cKk-y0k7pMbrtomtw82hd22ydZJvE9_QH4fVQ2Gc9B5RWGKZ-5iMa9CBDyNLECzt_RY2V9UOweoSiwA9qezFAmv8SDXUdUGhNBmDUoHYPuaIk9moJEFkcOoliJXNMUbArrEGkHetaijtadfTSA8buqFoguFiWjzh-Rs-vHbwWESyzQkpsjHq4QxX3iYtFx68IUKxWUqvZ44LZQ0OlPWCc24SCeGgcIwhQSTTOlCcjAObKYEe0QGVV25HUKF4F5omU587sCyU9o7q03mTG45_MFkSJKNVMply8ZRhis5AV5MO70lSrGMUhyS9yi6ri9yaYcf6svvZVyaZa4c2LU-K3xmxsJyZZlxoKuYy3MnjRmSPRR82Samdhqh3AdEMc5yDq_1KvRAnQCCNyqmNsBHIbtWr-durydI3vSadxBcm29pyr-ohyc3gLu--UXXjINi6Fzl6jX0Achn4BamMPrjFp_dfCAdJDrNQyJ6yO1NWL-lms8CCTlYsjjok_-_1h7ZglVaHh-dfn5K7oCxKdv4vV0yWF2u3TMw6Fb6eVipfwATektm |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Insects+in+anthelminthics+research%3A+Lady+beetle-derived+harmonine+affects+survival%2C+reproduction+and+stem+cell+proliferation+of+Schistosoma+mansoni&rft.jtitle=PLoS+neglected+tropical+diseases&rft.au=Kellershohn%2C+Josina&rft.au=Thomas%2C+Laura&rft.au=Hahnel%2C+Steffen+R.&rft.au=Gr%C3%BCnweller%2C+Arnold&rft.date=2019-03-01&rft.issn=1935-2735&rft.eissn=1935-2735&rft.volume=13&rft.issue=3&rft.spage=e0007240&rft_id=info:doi/10.1371%2Fjournal.pntd.0007240&rft.externalDBID=n%2Fa&rft.externalDocID=10_1371_journal_pntd_0007240 |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1935-2735&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1935-2735&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1935-2735&client=summon |