Iterative Catalysis in the Biosynthesis of Mitochondrial Complex II Inhibitors Harzianopyridone and Atpenin B

Journal of the American Chemical Society

Volumn 142, Issue 19, 2020, Pages 8550-8554

  Bat Erdene, Undramaa ^a   Kanayama, Daiki ^b   Tan, Dan ^a   Turner, William C ^a   Houk, K N ^a,b   Ohashi, Masao ^a   Tang, Yi ^a,b  

^a University of California   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; MITOCHONDRIA;

ALPHA-EFFECT; DIRECTING GROUPS; FLAVIN-DEPENDENT MONOOXYGENASE; METHOXY GROUP; METHYLTRANSFERASES; MITOCHONDRIAL COMPLEX; NATURAL PRODUCTS; POTENT INHIBITOR;

BIOSYNTHESIS;

ATPENIN B; HARZIANOPYRIDONE; OXIDOREDUCTASE INHIBITOR; UNCLASSIFIED DRUG; BIOLOGICAL PRODUCT; METHYLTRANSFERASE; MIXED FUNCTION OXIDASE; PYRIDONE DERIVATIVE;

ARTICLE; ASPERGILLUS NIDULANS; BIOSYNTHESIS; BIOTRANSFORMATION; CATALYSIS; CHEMICAL REACTION; ELECTROPHILIC AROMATIC SUBSTITUTION; HYDROXYLATION; METHOXYLATION; METHYLATION; NONHUMAN; NUCLEOPHILICITY; OXIDATION; SACCHAROMYCES CEREVISIAE; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; HYPOCREALES; METABOLISM;

BIOCATALYSIS; BIOLOGICAL PRODUCTS; HYPOCREALES; METHYLTRANSFERASES; MIXED FUNCTION OXYGENASES; MOLECULAR STRUCTURE; PYRIDONES;

EID: 85094629663     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/jacs.0c03438     Document Type: Article

References (24)

1. Kluckova, K.; Bezawork-Geleta, A.; Rohlena, J.; Dong, L.; Neuzil, J. Mitochondrial Complex II, a Novel Target for Anti-Cancer Agents. Biochim. Biophys. Acta, Bioenerg. 2013, 1827, 552-564, 10.1016/j.bbabio.2012.10.015
2. Mori, M.; Nonaka, K.; Masuma, R.; Ō mura, S.; Shiomi, K. Helminth Electron Transport Inhibitors Produced by Fungi. In Physiology and Genetics: Selected Basic and Applied Aspects; Anke, T., Schüffler, A., Eds.; The Mycota; Springer International Publishing: Cham, 2018; pp 297-329.
3. Cutler, H. G.; Jacyno, J. M. Biological Activity of (-)-Harzianopyridone Isolated from Trichoderma Harzianum. Agric. Biol. Chem. 1991, 55, 2629-2631, 10.1271/bbb1961.55.2629
4. Omura, S.; Tomoda, H.; Kimura, K.; Zhent, D.-Z.; Kumagai, H.; Igarashi, K.; Imamura, N.; Takahashi, Y.; Tanaka, Y.; Iwai, Y. Atpenins, newantifungalantibioticsproduced byPenicullium SP. J. Antibiot. 1988, 41, 1769-1773, 10.7164/antibiotics.41.1769
5. Miyadera, H.; Shiomi, K.; Ui, H.; Yamaguchi, Y.; Masuma, R.; Tomoda, H.; Miyoshi, H.; Osanai, A.; Kita, K.; Ō mura, S. Atpenins, Potent and Specific Inhibitors of Mitochondrial Complex II (Succinate-Ubiquinone Oxidoreductase). Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 473-477, 10.1073/pnas.0237315100
6. Horsefield, R.; Yankovskaya, V.; Sexton, G.; Whittingham, W.; Shiomi, K.; Ō mura, S.; Byrne, B.; Cecchini, G.; Iwata, S. Structural and Computational Analysis of the Quinone-Binding Site of Complex II (Succinate-Ubiquinone Oxidoreductase) A mechanismofelectron transferandproton conductionduring ubiquiononereduction. J. Biol. Chem. 2006, 281, 7309-7316, 10.1074/jbc.M508173200
7. Jacob Jessen, H.; Gademann, K. 4-Hydroxy-2-Pyridone Alkaloids: Structures and Synthetic Approaches. Nat. Prod. Rep. 2010, 27, 1168-1185, 10.1039/b911516c
8. Trecourt, F.; Mallet, M.; Mongin, O.; Queguiner, G. Total Synthesis of (.+-.)-Atpenin B. An Original "Clockwise" Functionalization of 2-Chloropyridine. J. Org. Chem. 1994, 59, 6173-6178, 10.1021/jo00100a017
9. Tréecourt, F.; Mallet, M.; Mongin, O.; Quéguiner, G. First Synthesis of (±)-Harzianopyridone by Metalation of Polysubstituted O-Pyridylcarbamates. J. Heterocycl. Chem. 1995, 32, 1117-1124, 10.1002/jhet.5570320403
10. Ohtawa, M.; Ogihara, S.; Sugiyama, K.; Shiomi, K.; Harigaya, Y.; Nagamitsu, T.; Ō mura, S. Enantioselective Total Synthesis of Atpenin A5. J. Antibiot. 2009, 62, 289-294, 10.1038/ja.2009.29
11. Krautwald, S.; Nilewski, C.; Mori, M.; Shiomi, K.; Ō mura, S.; Carreira, E. M. Bioisosteric Exchange of C-Chloro and Methyl Substituents: Synthesis and Initial Biological Studies of Atpenin A5 Analogues. Angew. Chem., Int. Ed. 2016, 55, 4049-4053, 10.1002/anie.201511672
12. Selby, T. P.; Hughes, K. A.; Rauh, J. J.; Hanna, W. S. Synthetic Atpenin Analogs: Potent Mitochondrial Inhibitors of Mammalian and Fungal Succinate-Ubiquinone Oxidoreductase. Bioorg. Med. Chem. Lett. 2010, 20, 1665-1668, 10.1016/j.bmcl.2010.01.066
13. Wang, H.; Huwaimel, B.; Verma, K.; Miller, J.; Germain, T. M.; Kinarivala, N.; Pappas, D.; Brookes, P. S.; Trippier, P. C. Synthesis and Antineoplastic Evaluation of Mitochondrial Complex II (Succinate Dehydrogenase) Inhibitors Derived from Atpenin A5. ChemMedChem 2017, 12, 1033-1044, 10.1002/cmdc.201700196
14. Eley, K. L.; Halo, L. M.; Song, Z.; Powles, H.; Cox, R. J.; Bailey, A. M.; Lazarus, C. M.; Simpson, T. J. Biosynthesis of the 2-Pyridone Tenellin in the Insect Pathogenic Fungus Beauveria Bassiana. ChemBioChem 2007, 8, 289-297, 10.1002/cbic.200600398
15. Dickinson, J. M.; Hanson, J. R.; Hitchcock, P. B.; Claydon, N. Structure and Biosynthesis of Harzianopyridone, an Antifungal Metabolite of Trichoderma Harzianum. J. Chem. Soc., Perkin Trans. 1 1989, 0, 1885-1887, 10.1039/p19890001885
16. Halo, L. M.; Heneghan, M. N.; Yakasai, A. A.; Song, Z.; Williams, K.; Bailey, A. M.; Cox, R. J.; Lazarus, C. M.; Simpson, T. J. Late Stage Oxidations during the Biosynthesis of the 2-Pyridone Tenellin in the Entomopathogenic Fungus Beauveria Bassiana. J. Am. Chem. Soc. 2008, 130, 17988-17996, 10.1021/ja807052c
17. Ohashi, M.; Liu, F.; Hai, Y.; Chen, M.; Tang, M.; Yang, Z.; Sato, M.; Watanabe, K.; Houk, K. N.; Tang, Y. SAM-Dependent Enzyme-Catalysed Pericyclic Reactions in Natural Product Biosynthesis. Nature 2017, 549, 502-506, 10.1038/nature23882
18. Bergmann, S.; Schümann, J.; Scherlach, K.; Lange, C.; Brakhage, A. A.; Hertweck, C. Genomics-Driven Discovery of PKS-NRPS Hybrid Metabolites from Aspergillus Nidulans. Nat. Chem. Biol. 2007, 3, 213-217, 10.1038/nchembio869
19. Liu, N.; Hung, Y.-S.; Gao, S.-S.; Hang, L.; Zou, Y.; Chooi, Y.-H.; Tang, Y. Identification and heterologous production of a benzoyl-primed tricarboxylic acid polyketide intermediate from the zaragozic acid a biosynthetic pathway. Org. Lett. 2017, 19, 3560-3563, 10.1021/acs.orglett.7b01534
20. Wasil, Z.; Pahirulzaman, K. A.; Butts, C.; Simpson, T.; Lazarus, C.; Cox, R. One Pathway, Many Compounds: Heterologous Expression of a Fungal Biosynthetic Pathway Reveals Its Intrinsic Potential for Diversity. Chem. Sci. 2013, 4, 3845-3856, 10.1039/c3sc51785c
21. Penicillium oxalicum as a producer of atpenin A5 can be found in information provided by Prof. Satoshi Ō mura's website: http://www.satoshi-omura.info/molecules/atpenina4.html (accessed Mar 17, 2020).
22. Jencks, W. P. Catalysis in Chemistry and Enzymology; McGraw-Hill Inc: New York, 1969.
23. Bamberger, E. Ueber die Reduction der Nitroverbindungen. Ber. Dtsch. Chem. Ges. 1894, 27, 1347-1350, 10.1002/cber.18940270229
24. Hang, L.; Liu, N.; Tang, Y. Coordinated and Iterative Enzyme Catalysis in Fungal Polyketide Biosynthesis.. ACS Catal. 2016, 6, 5935-5945, 10.1021/acscatal.6b01559