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High-Throughput Screen for Novel Antimicrobials using a Whole Animal Infection Model

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Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115
Department of Molecular Biology
§ Center for Computational and Integrative Biology
Center for Systems Biology, Massachusetts General Hospital, Boston, Massachusetts 02114
Department of Biology, Northeastern University, Boston, Massachusetts 02115
Imaging Platform, Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142
* Corresponding author, [email protected]
Cite this: ACS Chem. Biol. 2009, 4, 7, 527–533
Publication Date (Web):June 29, 2009
https://doi.org/10.1021/cb900084v
Copyright © 2009 American Chemical Society
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Abstract

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The nematode Caenorhabditis elegans is a unique whole animal model system for identifying small molecules with in vivo anti-infective properties. C. elegans can be infected with a broad range of human pathogens, including Enterococcus faecalis, an important human nosocomial pathogen. Here, we describe an automated, high-throughput screen of 37,200 compounds and natural product extracts for those that enhance survival of C. elegans infected with E. faecalis. Using a robot to dispense live, infected animals into 384-well plates and automated microscopy and image analysis, we identified 28 compounds and extracts not previously reported to have antimicrobial properties, including six structural classes that cure infected C. elegans animals but do not affect the growth of the pathogen in vitro, thus acting by a mechanism of action distinct from antibiotics currently in clinical use.

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  1. Daiheon Lee, Honggu Hwang, Jun-Sung Kim, Jongmin Park, Donghwan Youn, Duhwan Kim, Jungseok Hahn, Myungeun Seo, Haeshin Lee. VATA: A Poly(vinyl alcohol)- and Tannic Acid-Based Nontoxic Underwater Adhesive. ACS Applied Materials & Interfaces 2020, 12 (18) , 20933-20941. https://doi.org/10.1021/acsami.0c02037
  2. Tatu Rimpiläinen, Joana Andrade, Alexandra Nunes, Epole Ntungwe, Ana S. Fernandes, João R. Vale, João Rodrigues, João Paulo Gomes, Patricia Rijo, Nuno R. Candeias. Aminobenzylated 4-Nitrophenols as Antibacterial Agents Obtained from 5-Nitrosalicylaldehyde through a Petasis Borono–Mannich Reaction. ACS Omega 2018, 3 (11) , 16191-16202. https://doi.org/10.1021/acsomega.8b02381
  3. Rui Wang, Daniel E. Mason, Keith P. Choe, Alfred S. Lewin, Eric C. Peters, and Hendrik Luesch . In Vitro and in Vivo Characterization of a Tunable Dual-Reactivity Probe of the Nrf2-ARE Pathway. ACS Chemical Biology 2013, 8 (8) , 1764-1774. https://doi.org/10.1021/cb4000103
  4. Soo Min Kim, Iliana Escorbar, Kiho Lee, Beth Burgwyn Fuchs, Eleftherios Mylonakis, Wooseong Kim. Anti-MRSA agent discovery using Caenorhabditis elegans-based high-throughput screening. Journal of Microbiology 2020, 58 (6) , 431-444. https://doi.org/10.1007/s12275-020-0163-8
  5. Carla Palacios-Gorba, Raquel Pina, Miguel Tortajada-Girbés, Ana Jiménez-Belenguer, Érica Siguemoto, Maria Antonia Ferrús, Dolores Rodrigo, Maria Consuelo Pina-Pérez. Caenorhabditis elegans as an in vivo model to assess fucoidan bioactivity preventing Helicobacter pylori infection. Food & Function 2020, 11 (5) , 4525-4534. https://doi.org/10.1039/D0FO00768D
  6. Arun Kumar, Aiswarya Baruah, Masahiro Tomioka, Yuichi Iino, Mohan C. Kalita, Mojibur Khan. Caenorhabditis elegans: a model to understand host–microbe interactions. Cellular and Molecular Life Sciences 2020, 77 (7) , 1229-1249. https://doi.org/10.1007/s00018-019-03319-7
  7. Long Chen, Martin Strauch, Matthias Daub, Xiaochen Jiang, Marcus Jansen, Hans-Georg Luigs, Susanne Schultz-Kuhlmann, Stefan Krussel, Dorit Merhof. A CNN Framework Based on Line Annotations for Detecting Nematodes in Microscopic Images. 2020,,, 508-512. https://doi.org/10.1109/ISBI45749.2020.9098465
  8. Nicholas A. Hummell, Natalia V. Kirienko. Repurposing bioactive compounds for treating multidrug-resistant pathogens. Journal of Medical Microbiology 2020, 14 https://doi.org/10.1099/jmm.0.001172
  9. Saida Benomar, Patrick Lansdon, Aaron M. Bender, Blake R. Peterson, Josephine R. Chandler, Brian D. Ackley, . The C. elegans CHP1 homolog, pbo-1, functions in innate immunity by regulating the pH of the intestinal lumen. PLOS Pathogens 2020, 16 (1) , e1008134. https://doi.org/10.1371/journal.ppat.1008134
  10. Kitlangki Suchiang, Ramatchandirane Mahesh. Caenorhabditis elegans: A Tool for Antimicrobial Drug Discovery. 2020,,, 559-596. https://doi.org/10.1007/978-981-15-1695-5_29
  11. Jobina Rajkumari, Madhu Dyavaiah, Asad Syed, Busi Siddhardha. Model Organisms and Antimicrobial Drug Discovery. 2020,,, 527-543. https://doi.org/10.1007/978-981-15-1695-5_27
  12. Stephan J. Ihle, Andreas M. Reichmuth, Sophie Girardin, Hana Han, Flurin Stauffer, Anne Bonnin, Marco Stampanoni, Karthik Pattisapu, János Vörös, Csaba Forró. Unsupervised data to content transformation with histogram-matching cycle-consistent generative adversarial networks. Nature Machine Intelligence 2019, 1 (10) , 461-470. https://doi.org/10.1038/s42256-019-0096-2
  13. Guanghui Liu, Fenfen Dong, Chuanhai Fu, Zachary J. Smith. Automated morphometry toolbox for analysis of microscopic model organisms using simple bright-field imaging. Biology Open 2019, 8 (3) , bio037788. https://doi.org/10.1242/bio.037788
  14. Nicholas D. Peterson, Hilary K. Cheesman, Pengpeng Liu, Sarah M. Anderson, Kyle J. Foster, Richa Chhaya, Paola Perrat, Jose Thekkiniath, Qiyuan Yang, Cole M. Haynes, Read Pukkila-Worley, . The nuclear hormone receptor NHR-86 controls anti-pathogen responses in C. elegans. PLOS Genetics 2019, 15 (1) , e1007935. https://doi.org/10.1371/journal.pgen.1007935
  15. Timothy G. Hammond, Holly H. Birdsall. Vaccines in Space. 2019,,, 1-17. https://doi.org/10.1007/978-3-319-50909-9_7-1
  16. William C. Wimley. Application of Synthetic Molecular Evolution to the Discovery of Antimicrobial Peptides. 2019,,, 241-255. https://doi.org/10.1007/978-981-13-3588-4_13
  17. Shanmugaraj Gowrishankar, Shunmugiah Karutha Pandian, Boopathi Balasubramaniam, Krishnaswamy Balamurugan. Quorum quelling efficacy of marine cyclic dipeptide -cyclo(L-leucyl-L-prolyl) against the uropathogen Serratia marcescens. Food and Chemical Toxicology 2019, 123 , 326-336. https://doi.org/10.1016/j.fct.2018.11.013
  18. Jianping Yang, Meiqiong Zheng, Fan Yang, Xiulian Zhang, Wei Yin, Xiaojun Liu, Guo-Jun Zhang, Zuanguang Chen. Pseudomonas aeruginosa infected nematode-on-a-chip model array for antibacterials screening. Sensors and Actuators B: Chemical 2018, 275 , 373-381. https://doi.org/10.1016/j.snb.2018.08.062
  19. Tatiana Johnston, Daria Van Tyne, Roy F. Chen, Nicolas L. Fawzi, Bumsup Kwon, Michael J. Kelso, Michael S. Gilmore, Eleftherios Mylonakis. Propyl-5-hydroxy-3-methyl-1-phenyl-1H-pyrazole-4-carbodithioate (HMPC): a new bacteriostatic agent against methicillin—resistant Staphylococcus aureus. Scientific Reports 2018, 8 (1) https://doi.org/10.1038/s41598-018-25571-w
  20. Blanca Hernando-Rodríguez, Annmary Paul Erinjeri, María Jesús Rodríguez-Palero, Val Millar, Sara González-Hernández, María Olmedo, Bettina Schulze, Ralf Baumeister, Manuel J. Muñoz, Peter Askjaer, Marta Artal-Sanz. Combined flow cytometry and high-throughput image analysis for the study of essential genes in Caenorhabditis elegans. BMC Biology 2018, 16 (1) https://doi.org/10.1186/s12915-018-0496-5
  21. Hui Xie, Yonghua Zhan, Xueli Chen, Qi Zeng, Dan Chen, Jimin Liang. Brevinin-2 Drug Family—New Applied Peptide Candidates Against Methicillin-Resistant Staphylococcus aureus and Their Effects on Lys-7 Expression of Innate Immune Pathway DAF-2/DAF-16 in Caenorhabditis elegans. Applied Sciences 2018, 8 (12) , 2627. https://doi.org/10.3390/app8122627
  22. Wei Ding, Daniel P. Higgins, Dilip K. Yadav, Adwait A. Godbole, Read Pukkila-Worley, Amy K. Walker, . Stress-responsive and metabolic gene regulation are altered in low S-adenosylmethionine. PLOS Genetics 2018, 14 (11) , e1007812. https://doi.org/10.1371/journal.pgen.1007812
  23. Frederick M. Ausubel. Tracing My Roots: How I Became a Plant Biologist. Annual Review of Genetics 2018, 52 (1) , 1-20. https://doi.org/10.1146/annurev-genet-120417-031722
  24. Sakthimala Jagadeesan, Abdul Hakkim. RNAi Screening: Automated High-Throughput Liquid RNAi Screening in Caenorhabditis elegans. Current Protocols in Molecular Biology 2018, 124 (1) , e65. https://doi.org/10.1002/cpmb.65
  25. Nicholas D Peterson, Read Pukkila-Worley. Caenorhabditis elegans in high-throughput screens for anti-infective compounds. Current Opinion in Immunology 2018, 54 , 59-65. https://doi.org/10.1016/j.coi.2018.06.003
  26. Anne E. Clatworthy, Keith P. Romano, Deborah T. Hung. Whole-organism phenotypic screening for anti-infectives promoting host health. Nature Chemical Biology 2018, 14 (4) , 331-341. https://doi.org/10.1038/s41589-018-0018-3
  27. Wooseong Kim, Gabriel L Hendricks, Katerina Tori, Beth B Fuchs, Eleftherios Mylonakis. Strategies against methicillin-resistant Staphylococcus aureus persisters. Future Medicinal Chemistry 2018, 10 (7) , 779-794. https://doi.org/10.4155/fmc-2017-0199
  28. Lara Rajeev. Antibiotic Discovery. Materials and Methods 2018, 8 https://doi.org/10.13070/mm.en.8.2671
  29. Irina Sánchez-Diener, Laura Zamorano, Carla López-Causapé, Gabriel Cabot, Xavier Mulet, Carmen Peña, Rosa del Campo, Rafael Cantón, Antonio Doménech-Sánchez, Luis Martínez-Martínez, Susana C. Arcos, Alfonso Navas, Antonio Oliver. Interplay among Resistance Profiles, High-Risk Clones, and Virulence in the Caenorhabditis elegansPseudomonas aeruginosa Infection Model. Antimicrobial Agents and Chemotherapy 2017, 61 (12) https://doi.org/10.1128/AAC.01586-17
  30. Xianting Ding, Zach Njus, Taejoon Kong, Wenqiong Su, Chih-Ming Ho, Santosh Pandey. Effective drug combination for Caenorhabditis elegans nematodes discovered by output-driven feedback system control technique. Science Advances 2017, 3 (10) , eaao1254. https://doi.org/10.1126/sciadv.aao1254
  31. Elamparithi Jayamani, Nagendran Tharmalingam, Rajmohan Rajamuthiah, Jeffrey J. Coleman, Wooseong Kim, Ikechukwu Okoli, Ana M. Hernandez, Kiho Lee, Gerard J. Nau, Frederick M. Ausubel, Eleftherios Mylonakis. Characterization of a Francisella tularensis-Caenorhabditis elegans Pathosystem for the Evaluation of Therapeutic Compounds. Antimicrobial Agents and Chemotherapy 2017, 61 (9) https://doi.org/10.1128/AAC.00310-17
  32. Nagendran Tharmalingam, Elamparithi Jayamani, Rajmohan Rajamuthiah, Dawilmer Castillo, Beth Burgwyn Fuchs, Michael J Kelso, Eleftherios Mylonakis. Activity of a novel protonophore against methicillin-resistant Staphylococcus aureus. Future Medicinal Chemistry 2017, 9 (12) , 1401-1411. https://doi.org/10.4155/fmc-2017-0047
  33. Wooseong Kim, Gabriel Lambert Hendricks, Kiho Lee, Eleftherios Mylonakis. An update on the use of C. elegans for preclinical drug discovery: screening and identifying anti-infective drugs. Expert Opinion on Drug Discovery 2017, 12 (6) , 625-633. https://doi.org/10.1080/17460441.2017.1319358
  34. Holly E. Kinser, Zachary Pincus. High-throughput screening in the C. elegans nervous system. Molecular and Cellular Neuroscience 2017, 80 , 192-197. https://doi.org/10.1016/j.mcn.2016.06.001
  35. Nicole M. Vega, Jeff Gore, . Stochastic assembly produces heterogeneous communities in the Caenorhabditis elegans intestine. PLOS Biology 2017, 15 (3) , e2000633. https://doi.org/10.1371/journal.pbio.2000633
  36. Piper Reid Hunt. The C. elegans model in toxicity testing. Journal of Applied Toxicology 2017, 37 (1) , 50-59. https://doi.org/10.1002/jat.3357
  37. Chiara Borsetto, Elizabeth M. H. Wellington. Bioprospecting Soil Metagenomes for Antibiotics. 2017,,, 113-136. https://doi.org/10.1007/978-3-319-47935-4_6
  38. Cin Kong, Su-Anne Eng, Mei-Perng Lim, Sheila Nathan. Beyond Traditional Antimicrobials: A Caenorhabditis elegans Model for Discovery of Novel Anti-infectives. Frontiers in Microbiology 2016, 7 https://doi.org/10.3389/fmicb.2016.01956
  39. Kevin Strange. Drug Discovery in Fish, Flies, and Worms. ILAR Journal 2016, 57 (2) , 133-143. https://doi.org/10.1093/ilar/ilw034
  40. Mohammed M. Abdelsamea. A semi-automated system based on level sets and invariant spatial interrelation shape features for Caenorhabditis elegans phenotypes. Journal of Visual Communication and Image Representation 2016, 41 , 314-323. https://doi.org/10.1016/j.jvcir.2016.10.011
  41. Mark D. Mathew, Neal D. Mathew, Angela Miller, Mike Simpson, Vinci Au, Stephanie Garland, Marie Gestin, Mark L. Edgley, Stephane Flibotte, Aruna Balgi, Jennifer Chiang, Guri Giaever, Pamela Dean, Audrey Tung, Michel Roberge, Calvin Roskelley, Tom Forge, Corey Nislow, Donald Moerman, . Using C. elegans Forward and Reverse Genetics to Identify New Compounds with Anthelmintic Activity. PLOS Neglected Tropical Diseases 2016, 10 (10) , e0005058. https://doi.org/10.1371/journal.pntd.0005058
  42. Andrew R. Schwendeman, Shai Shaham, . A High-Throughput Small Molecule Screen for C. elegans Linker Cell Death Inhibitors. PLOS ONE 2016, 11 (10) , e0164595. https://doi.org/10.1371/journal.pone.0164595
  43. Tatiana Johnston, Gabriel Lambert Hendricks, Steven Shen, Roy Fangxing Chen, Bumsup Kwon, Michael John Kelso, Wooseong Kim, Beth Burgwyn Fuchs, Eleftherios Mylonakis. Raf-kinase inhibitor GW5074 shows antibacterial activity against methicillin-resistant Staphylococcus aureus and potentiates the activity of gentamicin. Future Medicinal Chemistry 2016, 8 (16) , 1941-1952. https://doi.org/10.4155/fmc-2016-0104
  44. Daniel R. Kirienko, Alexey V. Revtovich, Natalia V. Kirienko, . A High-Content, Phenotypic Screen Identifies Fluorouridine as an Inhibitor of Pyoverdine Biosynthesis and Pseudomonas aeruginosa Virulence. mSphere 2016, 1 (4) https://doi.org/10.1128/mSphere.00217-16
  45. Mostafa F. N. Abushahba, Haroon Mohammad, Shankar Thangamani, Asmaa A. A. Hussein, Mohamed N. Seleem. Impact of different cell penetrating peptides on the efficacy of antisense therapeutics for targeting intracellular pathogens. Scientific Reports 2016, 6 (1) https://doi.org/10.1038/srep20832
  46. Timothy A. Crombie, Lanlan Tang, Keith P. Choe, David Julian. Inhibition of the oxidative stress response by heat stress in Caenorhabditis elegans. The Journal of Experimental Biology 2016, 219 (14) , 2201-2211. https://doi.org/10.1242/jeb.135327
  47. Shanmugaraj Gowrishankar, Murugesan Sivaranjani, Arumugam Kamaladevi, Arumugam Veera Ravi, Krishnaswamy Balamurugan, Shunmugiah Karutha Pandian, . Cyclic dipeptide cyclo(l-leucyl-l-prolyl) from marine Bacillus amyloliquefaciens mitigates biofilm formation and virulence in Listeria monocytogenes. Pathogens and Disease 2016, 74 (4) , ftw017. https://doi.org/10.1093/femspd/ftw017
  48. Eleftherios Mylonakis, Lars Podsiadlowski, Maged Muhammed, Andreas Vilcinskas. Diversity, evolution and medical applications of insect antimicrobial peptides. Philosophical Transactions of the Royal Society B: Biological Sciences 2016, 371 (1695) , 20150290. https://doi.org/10.1098/rstb.2015.0290
  49. Garima Kulshreshtha, Tudor Borza, Bruce Rathgeber, Glenn S. Stratton, Nikhil A. Thomas, Alan Critchley, Jeff Hafting, Balakrishnan Prithiviraj. Red Seaweeds Sarcodiotheca gaudichaudii and Chondrus crispus down Regulate Virulence Factors of Salmonella Enteritidis and Induce Immune Responses in Caenorhabditis elegans. Frontiers in Microbiology 2016, 7 https://doi.org/10.3389/fmicb.2016.00421
  50. Cin Kong, Hui-min Neoh, Sheila Nathan. Targeting Staphylococcus aureus Toxins: A Potential form of Anti-Virulence Therapy. Toxins 2016, 8 (3) , 72. https://doi.org/10.3390/toxins8030072
  51. Han-Chu Chang, Yu-Ting Huang, Chang-Shi Chen, Yi-Wei Chen, Yu-Tsung Huang, Jung-Chen Su, Lee-Jeng Teng, Chung-Wai Shiau, Hao-Chieh Chiu. In vitro and in vivo activity of a novel sorafenib derivative SC5005 against MRSA. Journal of Antimicrobial Chemotherapy 2016, 71 (2) , 449-459. https://doi.org/10.1093/jac/dkv367
  52. Maged Muhammed, Marios Arvanitis, Eleftherios Mylonakis. Whole animal HTS of small molecules for antifungal compounds. Expert Opinion on Drug Discovery 2016, 11 (2) , 177-184. https://doi.org/10.1517/17460441.2016.1122591
  53. Natalia J Martinez, Steven A Titus, Amanda K Wagner, Anton Simeonov. High-throughput fluorescence imaging approaches for drug discovery using in vitro and in vivo three-dimensional models. Expert Opinion on Drug Discovery 2015, 10 (12) , 1347-1361. https://doi.org/10.1517/17460441.2015.1091814
  54. Rajmohan Rajamuthiah, Elamparithi Jayamani, Hiwa Majed, Annie L. Conery, Wooseong Kim, Bumsup Kwon, Beth Burgwyn Fuchs, Michael J. Kelso, Frederick M. Ausubel, Eleftherios Mylonakis. Antibacterial properties of 3-(phenylsulfonyl)-2-pyrazinecarbonitrile. Bioorganic & Medicinal Chemistry Letters 2015, 25 (22) , 5203-5207. https://doi.org/10.1016/j.bmcl.2015.09.066
  55. Maya A. Farha, Eric D. Brown. Unconventional screening approaches for antibiotic discovery. Annals of the New York Academy of Sciences 2015, 1354 (1) , 54-66. https://doi.org/10.1111/nyas.12803
  56. Rajmohan Rajamuthiah, Beth Burgwyn Fuchs, Annie L. Conery, Wooseong Kim, Elamparithi Jayamani, Bumsup Kwon, Frederick M. Ausubel, Eleftherios Mylonakis, . Repurposing Salicylanilide Anthelmintic Drugs to Combat Drug Resistant Staphylococcus aureus. PLOS ONE 2015, 10 (4) , e0124595. https://doi.org/10.1371/journal.pone.0124595
  57. Dong-Hyun Kim, Darren J Creek. What role can metabolomics play in the discovery and development of new medicines for infectious diseases?. Bioanalysis 2015, 7 (6) , 629-631. https://doi.org/10.4155/bio.15.5
  58. Elamparithi Jayamani, Rajmohan Rajamuthiah, Jonah Larkins-Ford, Beth Burgwyn Fuchs, Annie L. Conery, Andreas Vilcinskas, Frederick M. Ausubel, Eleftherios Mylonakis. Insect-Derived Cecropins Display Activity against Acinetobacter baumannii in a Whole-Animal High-Throughput Caenorhabditis elegans Model. Antimicrobial Agents and Chemotherapy 2015, 59 (3) , 1728-1737. https://doi.org/10.1128/AAC.04198-14
  59. Alan L. Harvey, RuAngelie Edrada-Ebel, Ronald J. Quinn. The re-emergence of natural products for drug discovery in the genomics era. Nature Reviews Drug Discovery 2015, 14 (2) , 111-129. https://doi.org/10.1038/nrd4510
  60. Sajal Sarabhai, Neena Capalash, Prince Sharma. Caenorhabditis elegans as an In Vivo Non-Mammalian Model System to Study Quorum Sensing in Pathogens. 2015,,, 185-195. https://doi.org/10.1007/978-81-322-1982-8_17
  61. Shanmugaraj Gowrishankar, Arumugam Kamaladevi, Krishnasamy Sorimuthu Ayyanar, Krishnaswamy Balamurugan, Shunmugiah Karutha Pandian. Bacillus amyloliquefaciens-secreted cyclic dipeptide – cyclo( l -leucyl- l -prolyl) inhibits biofilm and virulence production in methicillin-resistant Staphylococcus aureus. RSC Advances 2015, 5 (116) , 95788-95804. https://doi.org/10.1039/C5RA11641D
  62. Cin Kong, Wageeh A Yehye, Noorsaadah Abd Rahman, Man-Wah Tan, Sheila Nathan. Discovery of potential anti-infectives against Staphylococcus aureus using a Caenorhabditis elegans infection model. BMC Complementary and Alternative Medicine 2014, 14 (1) https://doi.org/10.1186/1472-6882-14-4
  63. Alexander Curt, Jiuli Zhang, Justin Minnerly, Kailiang Jia. Intestinal autophagy activity is essential for host defense against Salmonella typhimurium infection in Caenorhabditis elegans. Developmental & Comparative Immunology 2014, 45 (2) , 214-218. https://doi.org/10.1016/j.dci.2014.03.009
  64. Francis Raj Gandhi Amrit, Ramesh Ratnappan, Scott Alexander Keith, Arjumand Ghazi. The C. elegans lifespan assay toolkit. Methods 2014, 68 (3) , 465-475. https://doi.org/10.1016/j.ymeth.2014.04.002
  65. Read Pukkila-Worley, Rhonda L. Feinbaum, Deborah L. McEwan, Annie L. Conery, Frederick M. Ausubel, . The Evolutionarily Conserved Mediator Subunit MDT-15/MED15 Links Protective Innate Immune Responses and Xenobiotic Detoxification. PLoS Pathogens 2014, 10 (5) , e1004143. https://doi.org/10.1371/journal.ppat.1004143
  66. Nathan S. Blow. Finding the Middle Ground: Drug Discovery Technology in the Era of Academic Screening Centers. 2014,,, 487-498. https://doi.org/10.1002/9781118778166.ch28
  67. Christopher J. Schulze, Roger G. Linington. Image-Based Screening Approaches to Natural Products Discovery. 2014,,, 371-395. https://doi.org/10.1002/9781118794623.ch20
  68. Annie L. Conery, Jonah Larkins‐Ford, Frederick M. Ausubel, Natalia V. Kirienko. High‐Throughput Screening for Novel Anti‐Infectives Using a C. elegans Pathogenesis Model. Current Protocols in Chemical Biology 2014, 6 (1) , 25-37. https://doi.org/10.1002/9780470559277.ch130160
  69. Grace J. Yuen, Frederick M. Ausubel. Enterococcus infection biology: Lessons from invertebrate host models. Journal of Microbiology 2014, 52 (3) , 200-210. https://doi.org/10.1007/s12275-014-4011-6
  70. Rajmohan Rajamuthiah, Beth Burgwyn Fuchs, Elamparithi Jayamani, Younghoon Kim, Jonah Larkins-Ford, Annie Conery, Frederick M. Ausubel, Eleftherios Mylonakis, . Whole Animal Automated Platform for Drug Discovery against Multi-Drug Resistant Staphylococcus aureus. PLoS ONE 2014, 9 (2) , e89189. https://doi.org/10.1371/journal.pone.0089189
  71. Mengzhou Zhou, Hai Yu, Xianhua Yin, Parviz M. Sabour, Wei Chen, Joshua Gong, . Lactobacillus zeae Protects Caenorhabditis elegans from Enterotoxigenic Escherichia coli-Caused Death by Inhibiting Enterotoxin Gene Expression of the Pathogen. PLoS ONE 2014, 9 (2) , e89004. https://doi.org/10.1371/journal.pone.0089004
  72. Naveen K. Dolla, Chao Chen, Jonah Larkins-Ford, Rajmohan Rajamuthiah, Sakthimala Jagadeesan, Annie L. Conery, Frederick M. Ausubel, Eleftherios Mylonakis, John B. Bremner, Kim Lewis, Michael J. Kelso. On the Mechanism of Berberine–INF55 (5-Nitro-2-phenylindole) Hybrid Antibacterials. Australian Journal of Chemistry 2014, 67 (10) , 1471. https://doi.org/10.1071/CH14426
  73. Jinhee Choi, Olga V. Tsyusko, Jason M. Unrine, Nivedita Chatterjee, Jeong-Min Ahn, Xinyu Yang, B. Lila Thornton, Ian T. Ryde, Daniel Starnes, Joel N. Meyer. A micro-sized model for the in vivo study of nanoparticle toxicity: what has Caenorhabditis elegans taught us?. Environmental Chemistry 2014, 11 (3) , 227. https://doi.org/10.1071/EN13187
  74. S. Durai, L. Vigneshwari, K. Balamurugan. Caenorhabditis elegans -based in vivo screening of bioactives from marine sponge-associated bacteria against Vibrio alginolyticus. Journal of Applied Microbiology 2013, 115 (6) , 1329-1342. https://doi.org/10.1111/jam.12335
  75. George A. Lemieux, Michael J. Keiser, Maria F. Sassano, Christian Laggner, Fahima Mayer, Roland J. Bainton, Zena Werb, Bryan L. Roth, Brian K. Shoichet, Kaveh Ashrafi, . In Silico Molecular Comparisons of C. elegans and Mammalian Pharmacology Identify Distinct Targets That Regulate Feeding. PLoS Biology 2013, 11 (11) , e1001712. https://doi.org/10.1371/journal.pbio.1001712
  76. Marios Arvanitis, Justin Glavis-Bloom, Eleftherios Mylonakis. C. elegans for anti-infective discovery. Current Opinion in Pharmacology 2013, 13 (5) , 769-774. https://doi.org/10.1016/j.coph.2013.08.002
  77. Ruba A. Alajlouni, Mohamed N. Seleem. Targeting Listeria Monocytogenes rpoA and rpoD Genes Using Peptide Nucleic Acids. Nucleic Acid Therapeutics 2013, 23 (5) , 363-367. https://doi.org/10.1089/nat.2013.0426
  78. R. A. Paveley, Q. D. Bickle. Automated Imaging and other developments in whole-organism anthelmintic screening. Parasite Immunology 2013, 35 (9-10) , 302-313. https://doi.org/10.1111/pim.12037
  79. Natalia V. Kirienko, Daniel R. Kirienko, Jonah Larkins-Ford, Carolina Wählby, Gary Ruvkun, Frederick M. Ausubel. Pseudomonas aeruginosa Disrupts Caenorhabditis elegans Iron Homeostasis, Causing a Hypoxic Response and Death. Cell Host & Microbe 2013, 13 (4) , 406-416. https://doi.org/10.1016/j.chom.2013.03.003
  80. Adriana Monroy, Gordon J. Lithgow, Silvestre Alavez. Curcumin and neurodegenerative diseases. BioFactors 2013, 39 (1) , 122-132. https://doi.org/10.1002/biof.1063
  81. Eirini Lionaki, Nektarios Tavernarakis. High-Throughput and Longitudinal Analysis of Aging and Senescent Decline in Caenorhabditis elegans. 2013,,, 485-500. https://doi.org/10.1007/978-1-62703-239-1_32
  82. Andrew Fraser, Ben Lehner. Systems Biology of Caenorhabditis elegans. 2013,,, 367-390. https://doi.org/10.1016/B978-0-12-385944-0.00019-8
  83. Jianping Yang, Zuanguang Chen, Poying Ching, Qiujia Shi, Xinchun Li. An integrated microfluidic platform for evaluating in vivo antimicrobial activity of natural compounds using a whole-animal infection model. Lab on a Chip 2013, 13 (17) , 3373. https://doi.org/10.1039/c3lc50264c
  84. Lun K. Tsou, Paul D. Dossa, Howard C. Hang. Small molecules aimed at type III secretion systems to inhibit bacterial virulence. Med. Chem. Commun. 2013, 4 (1) , 68-79. https://doi.org/10.1039/C2MD20213A
  85. Shannan J. Ho Sui, Raymond Lo, Aalton R. Fernandes, Mackenzie D.G. Caulfield, Joshua A. Lerman, Lei Xie, Philip E. Bourne, David L. Baillie, Fiona S.L. Brinkman. Raloxifene attenuates Pseudomonas aeruginosa pyocyanin production and virulence. International Journal of Antimicrobial Agents 2012, 40 (3) , 246-251. https://doi.org/10.1016/j.ijantimicag.2012.05.009
  86. Carolina Wählby, Lee Kamentsky, Zihan H Liu, Tammy Riklin-Raviv, Annie L Conery, Eyleen J O'Rourke, Katherine L Sokolnicki, Orane Visvikis, Vebjorn Ljosa, Javier E Irazoqui, Polina Golland, Gary Ruvkun, Frederick M Ausubel, Anne E Carpenter. An image analysis toolbox for high-throughput C. elegans assays. Nature Methods 2012, 9 (7) , 714-716. https://doi.org/10.1038/nmeth.1984
  87. Maged Muhammed, Beth Burgwyn Fuchs, Michael P. Wu, Julia Breger, Jeffrey J. Coleman, Eleftherios Mylonakis. The role of mycelium production and a MAPK-mediated immune response in the C. elegans-Fusarium model system. Medical Mycology 2012, 50 (5) , 488-496. https://doi.org/10.3109/13693786.2011.648217
  88. Read Pukkila-Worley, Rhonda Feinbaum, Natalia V. Kirienko, Jonah Larkins-Ford, Annie L. Conery, Frederick M. Ausubel, . Stimulation of Host Immune Defenses by a Small Molecule Protects C. elegans from Bacterial Infection. PLoS Genetics 2012, 8 (6) , e1002733. https://doi.org/10.1371/journal.pgen.1002733
  89. Liang Ouyang, Yuhui Huang, Yuwei Zhao, Gu He, Yongmei Xie, Jie Liu, Jun He, Bo Liu, Yuquan Wei. Preparation, antibacterial evaluation and preliminary structure–activity relationship (SAR) study of benzothiazol- and benzoxazol-2-amine derivatives. Bioorganic & Medicinal Chemistry Letters 2012, 22 (9) , 3044-3049. https://doi.org/10.1016/j.bmcl.2012.03.079
  90. Alan L. Harvey. Screening Methods for Drug Discovery from Plants. 2012,,, 489-498. https://doi.org/10.1002/9781118260005.ch14
  91. Silvestre Alavez, Gordon J. Lithgow. Pharmacological maintenance of protein homeostasis could postpone age-related disease. Aging Cell 2012, 11 (2) , 187-191. https://doi.org/10.1111/j.1474-9726.2012.00789.x
  92. Read Pukkila-Worley, Frederick M Ausubel. Immune defense mechanisms in the Caenorhabditis elegans intestinal epithelium. Current Opinion in Immunology 2012, 24 (1) , 3-9. https://doi.org/10.1016/j.coi.2011.10.004
  93. Justin Glavis-Bloom, Maged Muhammed, Eleftherios Mylonakis. Of Model Hosts and Man: Using Caenorhabditis elegans, Drosophila melanogaster and Galleria mellonella as Model Hosts for Infectious Disease Research. 2012,,, 11-17. https://doi.org/10.1007/978-1-4419-5638-5_2
  94. Komalavali Dharmalingam, Boon-Khai Tan, Muhd Zulkarnain Mahmud, Saiedatul Akmal Mohamed Sedek, Mohamed Isa Abdul Majid, Meng-Kiat Kuah, Shaida Fariza Sulaiman, Kheng Leong Ooi, Nurzalina Abdul Karim Khan, Tengku Sifzizul Tengku Muhammad, Man-Wah Tan, Alexander Chong Shu-Chien. Swietenia macrophylla extract promotes the ability of Caenorhabditis elegans to survive Pseudomonas aeruginosa infection. Journal of Ethnopharmacology 2012, 139 (2) , 657-663. https://doi.org/10.1016/j.jep.2011.12.016
  95. Xiao Xu, Stuart K. Kim. The early bird catches the worm: new technologies for the Caenorhabditis elegans toolkit. Nature Reviews Genetics 2011, 12 (11) , 793-801. https://doi.org/10.1038/nrg3050
  96. B.P.G.V. Galvão, R.L. Meggersee, V.R. Abratt. Antibiotic resistance and adhesion potential of Bacteroides fragilis clinical isolates from Cape Town, South Africa. Anaerobe 2011, 17 (4) , 142-146. https://doi.org/10.1016/j.anaerobe.2011.02.009
  97. Lucy J Holcombe, Fergal O’Gara, John P Morrissey. Implications of interspecies signaling for virulence of bacterial and fungal pathogens. Future Microbiology 2011, 6 (7) , 799-817. https://doi.org/10.2217/fmb.11.60
  98. Xin Wang, Gregory R. Sliwoski, Edgar A. Buttner. The Relevance of Caenorhabditis elegans Genetics for Understanding Human Psychiatric Disease. Harvard Review of Psychiatry 2011, 19 (4) , 210-218. https://doi.org/10.3109/10673229.2011.599185
  99. Gilles Brackman, Paul Cos, Louis Maes, Hans J. Nelis, Tom Coenye. Quorum Sensing Inhibitors Increase the Susceptibility of Bacterial Biofilms to Antibiotics In Vitro and In Vivo. Antimicrobial Agents and Chemotherapy 2011, 55 (6) , 2655-2661. https://doi.org/10.1128/AAC.00045-11
  100. Athanasios Desalermos, Maged Muhammed, Justin Glavis-Bloom, Eleftherios Mylonakis. Using Caenorhabditis elegans for antimicrobial drug discovery. Expert Opinion on Drug Discovery 2011, 6 (6) , 645-652. https://doi.org/10.1517/17460441.2011.573781
  101. George A Lemieux, Jason Liu, Nasima Mayer, Roland J Bainton, Kaveh Ashrafi, Zena Werb. A whole-organism screen identifies new regulators of fat storage. Nature Chemical Biology 2011, 7 (4) , 206-213. https://doi.org/10.1038/nchembio.534
  102. Anne E. Carpenter. Extracting biomedically important information from large, automated imaging experiments. 2011,,, 1723-1726. https://doi.org/10.1109/ISBI.2011.5872737
  103. Alessandro Stella, Kenneth Segers, Steven De Jonghe, Bart Vanderhoydonck, Jef Rozenski, Jozef Anné, Piet Herdewijn. Synthesis and Antibacterial Evaluation of a Novel Series of 2-(1,2-Dihydro-3-oxo-3H-pyrazol-2-yl)benzothiazoles. Chemistry & Biodiversity 2011, 8 (2) , 253-265. https://doi.org/10.1002/cbdv.201000241
  104. Julian Davies. How to discover new antibiotics: harvesting the parvome. Current Opinion in Chemical Biology 2011, 15 (1) , 5-10. https://doi.org/10.1016/j.cbpa.2010.11.001
  105. Wanessa C. Lima, Emmanuelle Lelong, Pierre Cosson. What can Dictyostelium bring to the study of Pseudomonas infections?. Seminars in Cell & Developmental Biology 2011, 22 (1) , 77-81. https://doi.org/10.1016/j.semcdb.2010.11.006
  106. Terry K Means, Alejandro Aballay. Models to study ancient host–pathogen interactions: lessons from Crete. EMBO reports 2011, 12 (1) , 5-7. https://doi.org/10.1038/embor.2010.205
  107. Sager J. Gosai, Joon Hyeok Kwak, Cliff J. Luke, Olivia S. Long, Dale E. King, Kevin J. Kovatch, Paul A. Johnston, Tong Ying Shun, John S. Lazo, David H. Perlmutter, Gary A. Silverman, Stephen C. Pak, . Automated High-Content Live Animal Drug Screening Using C. elegans Expressing the Aggregation Prone Serpin α1-antitrypsin Z. PLoS ONE 2010, 5 (11) , e15460. https://doi.org/10.1371/journal.pone.0015460
  108. Jay L. Mellies, Emily R. Lawrence-Pine. Interkingdom signaling between pathogenic bacteria and Caenorhabditis elegans. Trends in Microbiology 2010, 18 (10) , 448-454. https://doi.org/10.1016/j.tim.2010.07.002
  109. Debra J. Woods, Christopher S. Knauer. Discovery of veterinary antiparasitic agents in the 21st Century: A view from industry. International Journal for Parasitology 2010, 40 (10) , 1177-1181. https://doi.org/10.1016/j.ijpara.2010.04.005
  110. , , , David J. Logan, Anne E. Carpenter. Screening Cellular Feature Measurements for Image-Based Assay Development. Journal of Biomolecular Screening 2010, 15 (7) , 840-846. https://doi.org/10.1177/1087057110370895
  111. W. Frank An, Nicola Tolliday. Cell-Based Assays for High-Throughput Screening. Molecular Biotechnology 2010, 45 (2) , 180-186. https://doi.org/10.1007/s12033-010-9251-z
  112. Marc Vendrell, Jun-Seok Lee, Young-Tae Chang. Diversity-oriented fluorescence library approaches for probe discovery and development. Current Opinion in Chemical Biology 2010, 14 (3) , 383-389. https://doi.org/10.1016/j.cbpa.2010.02.020
  113. Claire L. Bagwell, Mark G. Moloney, Muhammad Yaqoob. Oxazolomycins: Natural product lead structures for novel antibacterials by click fragment conjugation. Bioorganic & Medicinal Chemistry Letters 2010, 20 (7) , 2090-2094. https://doi.org/10.1016/j.bmcl.2010.02.066
  114. Carolina Wahlby, Tammy Riklin-Raviv, Vebjorn Ljosa, Annie L. Conery, Polina Golland, Frederick M. Ausubel, Anne E. Carpenter. Resolving clustered worms via probabilistic shape models. 2010,,, 552-555. https://doi.org/10.1109/ISBI.2010.5490286
  115. J. E. Irazoqui, F. M. Ausubel. 99th Dahlem Conference on Infection, Inflammation and Chronic Inflammatory Disorders: Caenorhabditis elegans as a model to study tissues involved in host immunity and microbial pathogenesis. Clinical & Experimental Immunology 2010, 160 (1) , 48-57. https://doi.org/10.1111/j.1365-2249.2010.04122.x
  116. Robert P. Shivers, Daniel J. Pagano, Tristan Kooistra, Claire E. Richardson, Kirthi C. Reddy, Janelle K. Whitney, Odile Kamanzi, Kunihiro Matsumoto, Naoki Hisamoto, Dennis H. Kim, . Phosphorylation of the Conserved Transcription Factor ATF-7 by PMK-1 p38 MAPK Regulates Innate Immunity in Caenorhabditis elegans. PLoS Genetics 2010, 6 (4) , e1000892. https://doi.org/10.1371/journal.pgen.1000892
  117. David O’Callaghan, Annette Vergunst. Non-mammalian animal models to study infectious disease: worms or fly fishing?. Current Opinion in Microbiology 2010, 13 (1) , 79-85. https://doi.org/10.1016/j.mib.2009.12.005
  118. J Richard Miller, Grover L Waldrop. Discovery of novel antibacterials. Expert Opinion on Drug Discovery 2010, 5 (2) , 145-154. https://doi.org/10.1517/17460440903493449
  119. Zachary Pincus, Frank J. Slack. Developmental biomarkers of aging in Caenorhabditis elegans. Developmental Dynamics 2010, 3 , NA-NA. https://doi.org/10.1002/dvdy.22224
  120. T. Riklin Raviv, V. Ljosa, A. L. Conery, F. M. Ausubel, A. E. Carpenter, P. Golland, C. Wählby. Morphology-Guided Graph Search for Untangling Objects: C. elegans Analysis. 2010,,, 634-641. https://doi.org/10.1007/978-3-642-15711-0_79
  121. Javier E. Irazoqui, Jonathan M. Urbach, Frederick M. Ausubel. Evolution of host innate defence: insights from Caenorhabditis elegans and primitive invertebrates. Nature Reviews Immunology 2010, 10 (1) , 47-58. https://doi.org/10.1038/nri2689
  122. James J. La Clair. Natural product mode of action (MOA) studies: a link between natural and synthetic worlds. Natural Product Reports 2010, 27 (7) , 969. https://doi.org/10.1039/b909989c
  123. Vebjorn Ljosa, Anne E. Carpenter, . Introduction to the Quantitative Analysis of Two-Dimensional Fluorescence Microscopy Images for Cell-Based Screening. PLoS Computational Biology 2009, 5 (12) , e1000603. https://doi.org/10.1371/journal.pcbi.1000603
  124. Ikechukwu Okoli, Jeffrey J. Coleman, Emmanouil Tempakakis, W. Frank An, Edward Holson, Florence Wagner, Annie L. Conery, Jonah Larkins-Ford, Gang Wu, Andy Stern, Frederick M. Ausubel, Eleftherios Mylonakis, . Identification of Antifungal Compounds Active against Candida albicans Using an Improved High-Throughput Caenorhabditis elegans Assay. PLoS ONE 2009, 4 (9) , e7025. https://doi.org/10.1371/journal.pone.0007025

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