ACS Publications. Most Trusted. Most Cited. Most Read
Thiol-Based Probe for Electrophilic Natural Products Reveals That Most of the Ammosamides Are Artifacts

OR SEARCH CITATIONS

My Activity
Publications

Figure 1Loading Img
Download Hi-Res ImageDownload to MS-PowerPointCite This:J. Nat. Prod. 2017, 80, 1, 126-133
    Article

    Thiol-Based Probe for Electrophilic Natural Products Reveals That Most of the Ammosamides Are Artifacts
    Click to copy article linkArticle link copied!

    View Author Information
    Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, California 92093-0204, United States
    *Tel: (858) 534-7121. E-mail: [email protected]
    Other Access OptionsSupporting Information (1)

    Journal of Natural Products

    Cite this: J. Nat. Prod. 2017, 80, 1, 126–133
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.jnatprod.6b00773
    Published January 5, 2017
    Copyright © 2017 The American Chemical Society and American Society of Pharmacognosy
    Request reuse permissions

    Abstract

    Click to copy section linkSection link copied!
    Abstract Image

    To date, 16 members of the ammosamide family of natural products have been discovered, and except for ammosamide D each of these metabolites is characterized by an unusual chlorinated pyrrolo[4,3,2-de]quinoline skeleton. Several ammosamides have been shown to inhibit quinone reductase 2, a flavoenzyme responsible for quelling toxic oxidative species in cells or for killing cancer cells outright. Treatment of the extract from an ammosamide-producing culture (Streptomyces strain CNR-698) with a thiol-based reagent designed to label electrophilic natural products produced an ammosamide C-thiol adduct. This observation led us to hypothesize, and then demonstrate through experimentation, that all of the other ammosamides are derived from ammosamide C via nonenzymatic processes involving exposure to nucleophiles, air, and light. Like many established electrophilic natural products, reaction with the thiol probe suggests that ammosamide C is itself an electrophilic natural product. Although ammosamide C did not show substantial cytotoxicity against cancer cells, its activity against a marine Bacillus bacterial strain may reflect its ecological role.

    Copyright © 2017 The American Chemical Society and American Society of Pharmacognosy

    Subjects

    what are subjects

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. Add or change your institution or let them know you’d like them to include access.

    Supporting Information

    Click to copy section linkSection link copied!

    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jnatprod.6b00773.

    • One-dimensional (1H) and two-dimensional (COSY, HSQC, HMBC) NMR spectra of 17, 20, 23, 24, 26, and 27 as well as UV/vis and HRMS data of all characterized compounds (PDF)

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    Click to copy section linkSection link copied!

    This article is cited by 32 publications.

    1. Jiaxu Shang, Shupeng Yin, Jingjing Shen, Chao Gao, Weihong Wang, Ke Sun, Weiming Zhu, Peng Fu. Amino-Based Probe for Natural Products with Covalent Binding Ability to Lysine and Mechanism of Action of Medermycin. Organic Letters 2024, 26 (47) , 10129-10134. https://doi.org/10.1021/acs.orglett.4c03803
    2. Samuele Sala, Masashi Shimomura, Louisa Tham, Juri Sakata, Alexandre N. Sobolev, Stephen A. Moggach, Jane Fromont, Oliver Gomez, Matthew J. Piggott, Hidetoshi Tokuyama, Scott G. Stewart, Gavin R. Flematti. Semisynthetic Studies Establish a Role for Conjugate Halide Exchange in the Formation of Chlorinated Pyrroloiminoquinones and Related Alkaloids. Journal of Natural Products 2024, 87 (10) , 2507-2514. https://doi.org/10.1021/acs.jnatprod.4c00549
    3. Josseline Ramos Figueroa, Lingyang Zhu, Wilfred A. van der Donk. Unexpected Transformations during Pyrroloiminoquinone Biosynthesis. Journal of the American Chemical Society 2024, 146 (20) , 14235-14245. https://doi.org/10.1021/jacs.4c03677
    4. Chayanid Ongpipattanakul, Emily K. Desormeaux, Adam DiCaprio, Wilfred A. van der Donk, Douglas A. Mitchell, Satish K. Nair. Mechanism of Action of Ribosomally Synthesized and Post-Translationally Modified Peptides. Chemical Reviews 2022, 122 (18) , 14722-14814. https://doi.org/10.1021/acs.chemrev.2c00210
    5. Yinyi Gao, Kaili Li, Lijun Zhang, Chu Chen, Chuan Bai. A Nucleophilic Chemical Probe Targeting Electrophilic Functional Groups in an Untargeted Way to Explore Cysteine Modulators in Natural Products. ACS Chemical Biology 2022, 17 (7) , 1685-1690. https://doi.org/10.1021/acschembio.2c00385
    6. Martin I. McLaughlin, Yue Yu, Wilfred A. van der Donk. Substrate Recognition by the Peptidyl-(S)-2-mercaptoglycine Synthase TglHI during 3-Thiaglutamate Biosynthesis. ACS Chemical Biology 2022, 17 (4) , 930-940. https://doi.org/10.1021/acschembio.2c00087
    7. Hai-bo Wu, Hai-bin Wu, Ming-shan Kuang, Hui-peng Lan, Yu-xin Wen, Ting-ting Liu. Novel Bithiophene Dimers from Echinops latifolius as Potential Antifungal and Nematicidal Agents. Journal of Agricultural and Food Chemistry 2020, 68 (43) , 11939-11945. https://doi.org/10.1021/acs.jafc.0c00169
    8. Takefumi Kuranaga, Mayuri Minote, Ryota Morimoto, Chengqian Pan, Haruka Ogawa, Hideaki Kakeya. Highly Sensitive Labeling Reagents for Scarce Natural Products. ACS Chemical Biology 2020, 15 (9) , 2499-2506. https://doi.org/10.1021/acschembio.0c00517
    9. Du Gao, Ting Zhou, Lin-Tai Da, Torsten Bruhn, Li-Li Guo, Yu-Hang Chen, Jun Xu, Min-Juan Xu. Characterization and Nonenzymatic Transformation of Three Types of Alkaloids from Streptomyces albogriseolus MGR072 and Discovery of Inhibitors of Indoleamine 2,3-Dioxygenase. Organic Letters 2019, 21 (21) , 8577-8581. https://doi.org/10.1021/acs.orglett.9b03149
    10. Gabriel Castro-Falcón, Natalie Millán-Aguiñaga, Catherine Roullier, Paul R. Jensen, Chambers C. Hughes. Nitrosopyridine Probe To Detect Polyketide Natural Products with Conjugated Alkenes: Discovery of Novodaryamide and Nocarditriene. ACS Chemical Biology 2018, 13 (11) , 3097-3106. https://doi.org/10.1021/acschembio.8b00598
    11. Hong-Liang Li, Motomu Kanai, and Yoichiro Kuninobu . Iridium/Bipyridine-Catalyzed ortho-Selective C–H Borylation of Phenol and Aniline Derivatives. Organic Letters 2017, 19 (21) , 5944-5947. https://doi.org/10.1021/acs.orglett.7b02936
    12. Caroline Kie Ishimoto, Bruno Nicolau Paulino, Iramaia Angelica Neri-Numa, Juliano Lemos Bicas. The blue palette of life: A comprehensive review of natural bluish colorants with potential commercial applications. Food Research International 2024, 196 , 115082. https://doi.org/10.1016/j.foodres.2024.115082
    13. Isabel P.-M. Pfeiffer, Maria-Paula Schröder, Silja Mordhorst. Opportunities and challenges of RiPP-based therapeutics. Natural Product Reports 2024, 41 (7) , 990-1019. https://doi.org/10.1039/D3NP00057E
    14. Petra Králová, Miroslav Soural. Biological properties of pyrroloquinoline and pyrroloisoquinoline derivatives. European Journal of Medicinal Chemistry 2024, 57 , 116287. https://doi.org/10.1016/j.ejmech.2024.116287
    15. Victor Flon, Coralie Pavesi, Samuel Oger, Stéphane Leleu, Pascal Retailleau, Laurence K. Jennings, Soizic Prado, Xavier Franck. Mass-tagged aminated probes for rapid discovery of azaphilic natural products in fungal crude extracts. Chemical Communications 2024, https://doi.org/10.1039/D4CC05122J
    16. Zeng-hong Gao, Xiu-yin Guo, Yi-zhi Liu, Qiu-mei Zhang, Xin-jie Tong, Li-hong Qiu. Trinickia violacea sp. nov. and Trinickia terrae sp. nov., isolated from forest soil. International Journal of Systematic and Evolutionary Microbiology 2023, 73 (11) https://doi.org/10.1099/ijsem.0.006147
    17. Gordon W. Gribble. Naturally Occurring Organohalogen Compounds—A Comprehensive Review. 2023, 1-546. https://doi.org/10.1007/978-3-031-26629-4_1
    18. Michelle Jessy Müller, Andrea Dorst, Constanze Paulus, Imran Khan, Simon Sieber. Catch-enrich-release approach for amine-containing natural products. Chemical Communications 2022, 15 https://doi.org/10.1039/D2CC04905H
    19. Lonnie A. Harris, Douglas A. Mitchell. Reactivity-based screening for natural product discovery. 2022, 177-208. https://doi.org/10.1016/bs.mie.2021.11.018
    20. Page N. Daniels, Hyunji Lee, Rebecca A. Splain, Chi P. Ting, Lingyang Zhu, Xiling Zhao, Bradley S. Moore, Wilfred A. van der Donk. A biosynthetic pathway to aromatic amines that uses glycyl-tRNA as nitrogen donor. Nature Chemistry 2022, 14 (1) , 71-77. https://doi.org/10.1038/s41557-021-00802-2
    21. Nathan P. Coussens, Douglas S. Auld, Jonathan R. Thielman, Bridget K. Wagner, Jayme L. Dahlin. Addressing Compound Reactivity and Aggregation Assay Interferences: Case Studies of Biochemical High-Throughput Screening Campaigns Benefiting from the National Institutes of Health Assay Guidance Manual Guidelines. SLAS Discovery 2021, 26 (10) , 1280-1290. https://doi.org/10.1177/24725552211026239
    22. Yang Hai, Mei-Yan Wei, Chang-Yun Wang, Yu-Cheng Gu, Chang-Lun Shao. The intriguing chemistry and biology of sulfur-containing natural products from marine microorganisms (1987–2020). Marine Life Science & Technology 2021, 3 (4) , 488-518. https://doi.org/10.1007/s42995-021-00101-2
    23. Yu Tang, J. Brent Friesen, Dejan S. Nikolić, David C. Lankin, James B. McAlpine, Shao-Nong Chen, Guido F. Pauli. Silica Gel-mediated Oxidation of Prenyl Motifs Generates Natural Product-Like Artifacts. Planta Medica 2021, 87 (12/13) , 998-1007. https://doi.org/10.1055/a-1472-6164
    24. Chambers C. Hughes. Chemical labeling strategies for small molecule natural product detection and isolation. Natural Product Reports 2021, 38 (9) , 1684-1705. https://doi.org/10.1039/D0NP00034E
    25. Jun Luo, Dong Yang, Hindra, Ajeeth Adhikari, Liao-Bin Dong, Fei Ye, Xiaohui Yan, Christoph Rader, Ben Shen. Discovery of ammosesters by mining the Streptomyces uncialis DCA2648 genome revealing new insight into ammosamide biosynthesis. Journal of Industrial Microbiology and Biotechnology 2021, 48 (3-4) https://doi.org/10.1093/jimb/kuab027
    26. Diego Caprioglio, Alberto Minassi, Cristina Avonto, Orazio Taglialatela-Scafati, Giovanni Appendino. Thiol-trapping natural products under the lens of the cysteamine assay: friends, foes, or simply alternatively reversible ligands?. Phytochemistry Reviews 2020, 19 (6) , 1307-1321. https://doi.org/10.1007/s11101-020-09700-w
    27. Tingjun Xu, Weiming Chen, Junhong Zhou, Jingfang Dai, Yingyong Li, Yingli Zhao. Virtual Screening for Reactive Natural Products and Their Probable Artifacts of Solvolysis and Oxidation. Biomolecules 2020, 10 (11) , 1486. https://doi.org/10.3390/biom10111486
    28. Wei-Yu Shi, Ya-Nan Ding, Ce Liu, Nian Zheng, Xue-Ya Gou, Ming Li, Zhe Zhang, Hong-Chao Liu, Zhi-Jie Niu, Yong-Min Liang. Three-component ruthenium-catalyzed remote C–H functionalization of 8-aminoquinoline amides. Chemical Communications 2020, 56 (84) , 12729-12732. https://doi.org/10.1039/D0CC05491G
    29. Chunxia Wen, Ronglin Zhong, Zengxin Qin, Mengfei Zhao, Jizhen Li. Regioselective remote C5 cyanoalkoxylation and cyanoalkylation of 8-aminoquinolines with azobisisobutyronitrile. Chemical Communications 2020, 56 (66) , 9529-9532. https://doi.org/10.1039/D0CC00014K
    30. QingLi Jiang, ZhiHui Zhu, PanTing Shou, Fei Teng, Ying Zhu, HuaJun Zhao, Bo Yang. Targeting pharmacophore with probe‐reactivity‐guided fractionation to precisely identify electrophilic sesquiterpenes and its activity of anti‐TNBC. Phytochemical Analysis 2020, 31 (3) , 322-332. https://doi.org/10.1002/pca.2898
    31. Robert J. Capon. Extracting value: mechanistic insights into the formation of natural product artifacts – case studies in marine natural products. Natural Product Reports 2020, 37 (1) , 55-79. https://doi.org/10.1039/C9NP00013E
    32. José Rivera-Chávez, Huzefa A. Raja, Tyler N. Graf, Jacklyn M. Gallagher, Prashant Metri, Ding Xue, Cedric J. Pearce, Nicholas H. Oberlies. Prealamethicin F50 and related peptaibols from Trichoderma arundinaceum: validation of their authenticity via in situ chemical analysis. RSC Adv. 2017, 7 (72) , 45733-45741. https://doi.org/10.1039/C7RA09602J
    Download PDF
    Go to Journal of Natural Products
    Get e-Alerts
    Get e-Alerts

    Journal of Natural Products

    Cite this: J. Nat. Prod. 2017, 80, 1, 126–133
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.jnatprod.6b00773
    Published January 5, 2017
    Copyright © 2017 The American Chemical Society and American Society of Pharmacognosy
    Request reuse permissions

    Article Views

    1626

    Altmetric

    -

    Citations

    32
    Learn about these metrics

    Article Views are the COUNTER-compliant sum of full text article downloads since November 2008 (both PDF and HTML) across all institutions and individuals. These metrics are regularly updated to reflect usage leading up to the last few days.

    Citations are the number of other articles citing this article, calculated by Crossref and updated daily. Find more information about Crossref citation counts.

    The Altmetric Attention Score is a quantitative measure of the attention that a research article has received online. Clicking on the donut icon will load a page at altmetric.com with additional details about the score and the social media presence for the given article. Find more information on the Altmetric Attention Score and how the score is calculated.