Schafhauser, T.; Microbiology and Biotechnology, Interfaculty Institute of Microbiology and Infection Medicine, Eberhard Karls University Tübingen, Tübingen, 72076, Germany, Institute of Botany, Technische Universität Dresden, Dresden, 01217, Germany, General Biochemistry, Technische Universität Dresden, Dresden, 01062, Germany
Jahn, L.; Institute of Botany, Technische Universität Dresden, Dresden, 01217, Germany
Kirchner, N.; Pharmaceutical Institute, Department of Pharmaceutical Biology, Eberhard Karls University Tübingen, Tübingen, 72076, Germany
Kulik, A.; Microbiology and Biotechnology, Interfaculty Institute of Microbiology and Infection Medicine, Eberhard Karls University Tübingen, Tübingen, 72076, Germany
Flor, L.; General Biochemistry, Technische Universität Dresden, Dresden, 01062, Germany
Lang, A.; General Biochemistry, Technische Universität Dresden, Dresden, 01062, Germany
Caradec, T.; Institut Charles Viollette, Equipe d'Accueil 7394, University of Lille, Lille, 59000, France
Fewer, D. P.; Department of Microbiology, University of Helsinki, Helsinki, 00014, Finland
Sivonen, K.; Department of Microbiology, University of Helsinki, Helsinki, 00014, Finland
Van Berkel, W. J. H.; Laboratory of Biochemistry, Wageningen University and Research, Wageningen, 6708 WE, Netherlands
Jacques, Philippe ; Université de Liège - ULiège > Département GxABT > Microbial, food and biobased technologies
Weber, T.; Microbiology and Biotechnology, Interfaculty Institute of Microbiology and Infection Medicine, Eberhard Karls University Tübingen, Tübingen, 72076, Germany, Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Kgs. Lyngby, 2800, Denmark
Gross, H.; Pharmaceutical Institute, Department of Pharmaceutical Biology, Eberhard Karls University Tübingen, Tübingen, 72076, Germany
Van Pée, K.-H.; General Biochemistry, Technische Universität Dresden, Dresden, 01062, Germany
Wohlleben, W.; Microbiology and Biotechnology, Interfaculty Institute of Microbiology and Infection Medicine, Eberhard Karls University Tübingen, Tübingen, 72076, Germany
Ludwig-Müller, J.; Institute of Botany, Technische Universität Dresden, Dresden, 01217, Germany
Antitumor astins originate from the fungal endophyte Cyanodermella asteris living within the medicinal plant Aster tataricus
Publication date :
2019
Journal title :
Proceedings of the National Academy of Sciences of the United States of America
ISSN :
0027-8424
eISSN :
1091-6490
Publisher :
National Academy of Sciences
Volume :
116
Issue :
52
Pages :
26909-26917
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
Project Astinprod; Project ACTS 053.80.713
Funders :
EU - European Union Free State of Saxony Sächsische Staatsministerium für Wissenschaft und Kunst SAB - Sächsische Aufbaubank University of Tübingen BMBF - Bundesministerium für Bildung und Forschung ULille - Université de Lille JAES - Jane and Aatos Erkko Foundation NWO - Nederlandse Organisatie voor Wetenschappelijk Onderzoek NNF - Novo Nordisk Foundation
B. David, J. L. Wolfender, D. A. Dias, The pharmaceutical industry and natural products: Historical status and new trends. Phytochem. Rev. 14, 299-315 (2015).
G. A. Cordell, Sustainable medicines and global health care. Planta Med. 77, 1129-1138 (2011).
M. Ekor, The growing use of herbal medicines: Issues relating to adverse reactions and challenges in monitoring safety. Front. Pharmacol. 4, 177 (2014).
D. J. Newman, G. M. Cragg, Natural products as sources of new drugs over the 30 years from 1981 to 2010. J. Nat. Prod. 75, 311-335 (2012).
A. D. Kinghorn, L. Pan, J. N. Fletcher, H. Chai, The relevance of higher plants in lead compound discovery programs. J. Nat. Prod. 74, 1539-1555 (2011).
D. L. Klayman et al., Isolation of artemisinin (qinghaosu) from Artemisia annua growing in the United States. J. Nat. Prod. 47, 715-717 (1984).
G. M. Cragg, D. J. Newman, Natural products: A continuing source of novel drug leads. Biochim. Biophys. Acta 1830, 3670-3695 (2013).
A. G. Atanasov et al., Discovery and resupply of pharmacologically active plantderived natural products: A review. Biotechnol. Adv. 33, 1582-1614 (2015).
B. Miralpeix et al., Metabolic engineering of plant secondary products: Which way forward? Curr. Pharm. Des. 19, 5622-5639 (2013).
P. R. Hardoim et al., The hidden world within plants: Ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol. Mol. Biol. Rev. 79, 293-320 (2015).
S. Kusari, C. Hertweck, M. Spiteller, Chemical ecology of endophytic fungi: Origins of secondary metabolites. Chem. Biol. 19, 792-798 (2012).
S. Chandra, Endophytic fungi: Novel sources of anticancer lead molecules. Appl. Microbiol. Biotechnol. 95, 47-59 (2012).
A. Venugopalan, S. Srivastava, Endophytes as in vitro production platforms of high value plant secondary metabolites. Biotechnol. Adv. 33, 873-887 (2015).
M. Crüsemann et al., Heterologous expression, biosynthetic studies, and ecological function of the selective Gq-signaling inhibitor FR900359. Angew. Chem. Int. Ed. Engl. 57, 836-840 (2018).
S. C. Puri, V. Verma, T. Amna, G. N. Qazi, M. Spiteller, An endophytic fungus from Nothapodytes foetida that produces camptothecin. J. Nat. Prod. 68, 1717-1719 (2005).
A. Stierle, G. Strobel, D. Stierle, Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of Pacific yew. Science 260, 214-216 (1993).
S. Kusari, S. Singh, C. Jayabaskaran, Biotechnological potential of plant-associated endophytic fungi: Hope versus hype. Trends Biotechnol. 32, 297-303 (2014).
P. Yu et al., Expectorant, antitussive, anti-inflammatory activities and compositional analysis of Aster tataricus. J. Ethnopharmacol. 164, 328-333 (2015).
T. B. Ng, F. Liu, Y. Lu, C. H. Cheng, Z. Wang, Antioxidant activity of compounds from the medicinal herb Aster tataricus. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 136, 109-115 (2003).
H. Morita, S. Nagashima, K. Takeya, H. Itokawa, Astins A and B, antitumor cyclic pentapeptides from Aster tataricus. Chem. Pharm. Bull. (Tokyo) 41, 992-993 (1993).
D. Cheng, Y. Shao, Terpenoid glycosides from the roots of Aster tataricus. Phytochemistry 35, 173-176 (1994).
R. Cozzolino et al., Antineoplastic cyclic astin analogues kill tumour cells via caspasemediated induction of apoptosis. Carcinogenesis 26, 733-739 (2005).
H. Morita et al., Cyclic peptides from higher plants. XXVIII. Antitumor activity and hepatic microsomal biotransformation of cyclic pentapeptides, astins, from Aster tataricus. Chem. Pharm. Bull. (Tokyo) 44, 1026-1032 (1996).
F. Rossi et al., New antitumour cyclic astin analogues: Synthesis, conformation and bioactivity. J. Pept. Sci. 10, 92-102 (2004).
Y. Shen et al., Mitochondria-dependent apoptosis of activated T lymphocytes induced by astin C, a plant cyclopeptide, for preventing murine experimental colitis. Biochem. Pharmacol. 82, 260-268 (2011).
S. Li et al., The cyclopeptide astin c specifically inhibits the innate immune CDN sensor STING. Cell Rep. 25, 3405-3421.e7 (2018).
S. Kosemura, T. Ogawa, K. Totsuka, Isolation and structure of asterin, a new halogenated cyclic pentapeptide from Aster tataricus. Tetrahedron Lett. 34, 1291-1294 (1993).
H. Morita, S. Nagashima, O. Shirota, K. Takeya, H. Itokawa, Two novel monochlorinated cyclic pentapeptides, astin D and astin E from Aster tataricus. Chem. Lett. 11, 1877-1880 (1993).
H. Morita, S. Nagashima, K. Takeya, H. Itokawa, Cyclic peptides from higher plants 8: 3 novel cyclic pentapeptides, astin F, astin G and astin H from Aster tataricus. Heterocycles 38, 2247-2252 (1994).
H. Morita, S. Nagashima, K. Takeya, H. Itokawa, A novel cyclic pentapeptide with a beta-hydroxy-gamma-chloroproline from Aster tataricus. Chem. Lett. 11, 2009-2010 (1994).
H.M. Xu et al., Six new chlorinated cyclopentapeptides from Aster tataricus. Tetrahedron 69, 7964-7969 (2013).
H. Morita, S. Nagashima, K. Takeya, H. Itokawa, Structure of a new peptide, astin J, from Aster tataricus. Chem. Pharm. Bull. (Tokyo) 43, 271-273 (1995).
H. M. Xu et al., Tataricins A and B, two novel cyclotetrapeptides from Aster tataricus, and their absolute configuration assignment. Tetrahedron Lett. 54, 1380-1383 (2013).
D. Cheng, Y. Shao, R. Hartman, E. Roder, K. Zhao, Oligopeptides from Aster tataricus. Phytochemistry 36, 945-948 (1994).
D. L. Cheng, Y. Shao, K. Zhao, R. Hartmann, E. Roeder, Pentapeptides from the roots of Aster tataricus. Pharmazie 51, 185-186 (1996).
D. X. Zhao, B. Q. Hu, M. Zhang, C. F. Zhang, X. H. Xu, Simultaneous separation and determination of phenolic acids, pentapeptides, and triterpenoid saponins in the root of Aster tataricus by high-performance liquid chromatography coupled with electrospray ionization quadrupole time-of-flight mass spectrometry. J. Sep. Sci. 38, 571-575 (2015).
X. Liu, P. Cao, C. Zhang, X. Xu, M. Zhang, Screening and analyzing potential hepatotoxic compounds in the ethanol extract of Asteris Radix by HPLC/DAD/ESI-MS(n) technique. J. Pharm. Biomed. Anal. 67-68, 51-62 (2012).
F. Li et al., Design and synthesis of plant cyclopeptide Astin C analogues and investigation of their immunosuppressive activity. Bioorg. Med. Chem. Lett. 28, 2523-2527 (2018).
K. K. Schumacher et al., First total synthesis of astin G. Tetrahedron Lett. 40, 455-458 (1999).
N. H. Tan, J. Zhou, Plant cyclopeptides. Chem. Rev. 106, 840-895 (2006).
C. T. Walsh, R. V. O'Brien, C. Khosla, Nonproteinogenic amino acid building blocks for nonribosomal peptide and hybrid polyketide scaffolds. Angew. Chem. Int. Ed. Engl. 52, 7098-7124 (2013).
K. Mizutani, Y. Hirasawa, Y. Sugita-Konishi, N. Mochizuki, H. Morita, Structural and conformational analysis of hydroxycyclochlorotine and cyclochlorotine, chlorinated cyclic peptides from Penicillium islandicum. J. Nat. Prod. 71, 1297-1300 (2008).
L. Jahn et al., Cyanodermella asteris sp. nov. (Ostropales) from the inflorescence axis of Aster tataricus. Mycotaxon 132, 107-123 (2017).
L. Jahn et al., Linking secondary metabolites to biosynthesis genes in the fungal endophyte Cyanodermella asteris: The anti-cancer bisanthraquinone skyrin. J. Biotechnol. 257, 233-239 (2017).
S. Kusari, S. Zühlke, M. Spiteller, An endophytic fungus from Camptotheca acuminata that produces camptothecin and analogues. J. Nat. Prod. 72, 2-7 (2009).
J. Y. Li et al., The induction of taxol production in the endophytic fungus-Periconia sp. from Torreya grandifolia. J. Ind. Microbiol. Biotechnol. 20, 259-264 (1998).
X. Pu et al., Camptothecin-producing endophytic fungus Trichoderma atroviride LY357: Isolation, identification, and fermentation conditions optimization for camptothecin production. Appl. Microbiol. Biotechnol. 97, 9365-9375 (2013).
A. Staniek, H. J. Woerdenbag, O. Kayser, Taxomyces andreanae: A presumed paclitaxel producer demystified? Planta Med. 75, 1561-1566 (2009).
E. J. van Nieuwenhuijzen et al., Wood staining fungi revealed taxonomic novelties in Pezizomycotina: New order Superstratomycetales and new species Cyanodermella oleoligni. Stud. Mycol. 85, 107-124 (2016).
H. Itokawa, K. Takeya, Y. Hitotsuyanagi, H. Morita, "Antitumor compounds isolated from higher plants" in Studies in Natural Products Chemistry (Part E), Atta-ur-Rahman, Ed. (Elsevier, 2000), vol. 24, pp. 269-350.
T. Schafhauser et al., The cyclochlorotine mycotoxin is produced by the nonribosomal peptide synthetase CctN in Talaromyces islandicus ('Penicillium islandicum'). Environ. Microbiol. 18, 3728-3741 (2016).
X. Gao et al., Cyclization of fungal nonribosomal peptides by a terminal condensationlike domain. Nat. Chem. Biol. 8, 823-830 (2012).
T. Kittilä et al., Halogenation of glycopeptide antibiotics occurs at the amino acid level during non-ribosomal peptide synthesis. Chem. Sci. (Camb.) 8, 5992-6004 (2017).
P. C. Dorrestein, E. Yeh, S. Garneau-Tsodikova, N. L. Kelleher, C. T. Walsh, Dichlorination of a pyrrolyl-S-carrier protein by FADH2-dependent halogenase PltA during pyoluteorin biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 102, 13843-13848 (2005).
S. Lin, S. G. Van Lanen, B. Shen, Regiospecific chlorination of (S)-beta-tyrosyl-S-carrier protein catalyzed by SgcC3 in the biosynthesis of the enediyne antitumor antibiotic C-1027. J. Am. Chem. Soc. 129, 12432-12438 (2007).
T. Caradec et al., Prediction of monomer isomery in florine: A workflow dedicated to nonribosomal peptide discovery. PLoS One 9, e85667 (2014).
C. S. Neumann, D. G. Fujimori, C. T. Walsh, Halogenation strategies in natural product biosynthesis. Chem. Biol. 15, 99-109 (2008).
K. H. van Pée, Enzymatic chlorination and bromination. Methods Enzymol. 516, 237-257 (2012).
V. Weichold, D. Milbredt, K. H. van Pée, Specific enzymatic halogenation-From the discovery of halogenated enzymes to their applications in vitro and in vivo. Angew. Chem. Int. Ed. Engl. 55, 6374-6389 (2016).
H. B. Bode, B. Bethe, R. Höfs, A. Zeeck, Big effects from small changes: Possible ways to explore nature's chemical diversity. ChemBioChem 3, 619-627 (2002).
D. J. Newman, G. M. Cragg, Endophytic and epiphytic microbes as "sources" of bioactive agents. Front Chem. 3, 34 (2015).
J. Piel, Metabolites from symbiotic bacteria. Nat. Prod. Rep. 26, 338-362 (2009).
J. F. Martín, P. Liras, Evolutionary formation of gene clusters by reorganization: The meleagrin/roquefortine paradigm in different fungi. Appl. Microbiol. Biotechnol. 100, 1579-1587 (2016).
H. Bártíková et al., Xenobiotic-metabolizing enzymes in plants and their role in uptake and biotransformation of veterinary drugs in the environment. Drug Metab. Rev. 47, 374-387 (2015).
F. Berthiller et al., Masked mycotoxins: A review. Mol. Nutr. Food Res. 57, 165-186 (2013).
D. E. Riechers, K. Kreuz, Q. Zhang, Detoxification without intoxication: Herbicide safeners activate plant defense gene expression. Plant Physiol. 153, 3-13 (2010).
K. Scherlach, B. Busch, G. Lackner, U. Paszkowski, C. Hertweck, Symbiotic cooperation in the biosynthesis of a phytotoxin. Angew. Chem. Int. Ed. Engl. 51, 9615-9618 (2012).
S. Kusari, S. Zühlke, M. Spiteller, Effect of artificial reconstitution of the interaction between the plant Camptotheca acuminata and the fungal endophyte Fusarium solani on camptothecin biosynthesis. J. Nat. Prod. 74, 764-775 (2011).
P. Kusari et al., Cross-species biosynthesis of maytansine in Maytenus serrata. RSC Adv. 6, 10011-10016 (2016).
G. Saviano et al., Influence of conformational flexibility on biological activity in cyclic astin analogues. Biopolymers 76, 477-484 (2004).
S. Kusari, S. Singh, C. Jayabaskaran, Rethinking production of Taxol (paclitaxel) using endophyte biotechnology. Trends Biotechnol. 32, 304-311 (2014).
T. J. White, T. Bruns, S. Lee, J. W. Taylor, "Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics" in PCR Protocols: A Guide to Methods and Applications, M. A. Innis, D. H. Gelfand, J. J. Sninsky, T. J. White, Eds. (Academic, New York, 1990), pp. 315-322.
M. Gardes, T. D. Bruns, ITS primers with enhanced specificity for basidiomycetes- Application to the identification of mycorrhizae and rusts. Mol. Ecol. 2, 113-118 (1993).
E. M. Möller, G. Bahnweg, H. Sandermann, H. H. Geiger, A simple and efficient protocol for isolation of high molecular weight DNA from filamentous fungi, fruit bodies, and infected plant tissues. Nucleic Acids Res. 20, 6115-6116 (1992).
D. Fitze, A. Wiepning, M. Kaldorf, J. Ludwig-Müller, Auxins in the development of an arbuscular mycorrhizal symbiosis in maize. J. Plant Physiol. 162, 1210-1219 (2005).
M. M. Heberling et al., Ironing out their differences: Dissecting the structural determinants of a phenylalanine aminomutase and ammonia lyase. ACS Chem. Biol. 10, 989-997 (2015).
I. G. Fotheringham, N. Grinter, D. P. Pantaleone, R. F. Senkpeil, P. P. Taylor, Engineering of a novel biochemical pathway for the biosynthesis of L-2-aminobutyric acid in Escherichia coli K12. Bioorg. Med. Chem. 7, 2209-2213 (1999).
Y. Ye et al., Unveiling the biosynthetic pathway of the ribosomally synthesized and post-translationally modified peptide ustiloxin B in filamentous fungi. Angew. Chem. Int. Ed. Engl. 55, 8072-8075 (2016).
