Ergochromes: Heretofore Neglected Side of Ergot Toxicity
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
31349616
PubMed Central
PMC6722540
DOI
10.3390/toxins11080439
PII: toxins11080439
Knihovny.cz E-zdroje
- Klíčová slova
- Claviceps, cereals, ergochromes, ergot alkaloids, food safety, mycotoxins, secalonic acid, tetrahydroxanthones,
- MeSH
- apoptóza účinky léků MeSH
- Claviceps chemie MeSH
- HeLa buňky MeSH
- Jurkat buňky MeSH
- lidé MeSH
- mitochondrie účinky léků MeSH
- mykotoxiny analýza farmakologie toxicita MeSH
- námelové alkaloidy analýza toxicita MeSH
- viabilita buněk účinky léků MeSH
- xantheny analýza toxicita MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- ergochromes MeSH Prohlížeč
- mykotoxiny MeSH
- námelové alkaloidy MeSH
- xantheny MeSH
Ergot, fungal genus Claviceps, are worldwide distributed grass pathogens known for their production of toxic ergot alkaloids (EAs) and the great agricultural impact they have on both cereal crop and farm animal production. EAs are traditionally considered as the only factor responsible for ergot toxicity. Using broad sampling covering 13 ergot species infecting wild or agricultural grasses (including cereals) across Europe, USA, New Zealand, and South Africa we showed that the content of ergochrome pigments were comparable to the content of EAs in sclerotia. While secalonic acids A-C (SAs), the main ergot ergochromes (ECs), are well known toxins, our study is the first to address the question about their contribution to overall ergot toxicity. Based on our and published data, the importance of SAs in acute intoxication seems to be negligible, but the effect of chronic exposure needs to be evaluated. Nevertheless, they have biological activities at doses corresponding to quantities found in natural conditions. Our study highlights the need for a re-evaluation of ergot toxicity mechanisms and further studies of SAs' impact on livestock production and food safety.
Zobrazit více v PubMed
Píchová K., Pažoutová S., Kostovčík M., Chudíčková M., Stodůlková E., Novák P., Flieger M., van der Linde E., Kolařík M. Evolutionary history of ergot with a new infrageneric classification (Hypocreales: Clavicipitaceae: Claviceps) Mol. Phylogen. Evol. 2018;123:73–87. doi: 10.1016/j.ympev.2018.02.013. PubMed DOI
Pažoutová S., Pešicová K., Chudíčková M., Šrůtka P., Kolařík M. Delimitation of cryptic species inside Claviceps purpurea. Fungal Biol. 2015;119:7–26. doi: 10.1016/j.funbio.2014.10.003. PubMed DOI
Negård M., Uhlig S., Kauserud H., Andersen T., Høiland K., Vrålstad T. Links between genetic groups, indole alkaloid profiles and ecology within the grass-parasitic Claviceps purpurea species complex. Toxins (Basel) 2015;7:1431–1456. doi: 10.3390/toxins7051431. PubMed DOI PMC
Shoukouhi P., Hicks C., Menzies J.G., Popovic Z., Chen W., Seifert K.A., Assabgui R., Liu M. Phylogeny of Canadian ergot fungi and a detection assay by real-time polymerase chain reaction. Mycologia. 2019;111:493–505. doi: 10.1080/00275514.2019.1581018. PubMed DOI
Arroyo-Manzanares N., Gámiz-Gracia L., García-Campaña A.M., Diana Di Mavungu J., De Saeger S. Ergot alkaloids: Chemistry, biosynthesis, bioactivity, and methods of analysis. In: Mérillon J.-M., Ramawat K.G., editors. Fungal Metabolites. Springer; Berlin, Germany: 2017. pp. 887–929.
Young C.A., Schardl C.L., Panaccione D.G., Florea S., Takach J.E., Charlton N.D., Moore N., Webb J.S., Jaromczyk J. Genetics, genomics and evolution of ergot alkaloid diversity. Toxins (Basel) 2015;7:1273–1302. doi: 10.3390/toxins7041273. PubMed DOI PMC
EFSA Scientific opinion on ergot alkaloids in food and feed. EFSA J. 2012;10:158. doi: 10.2903/j.efsa.2012.2798. DOI
Belser-Ehrlich S., Harper A., Hussey J., Hallock R. Human and cattle ergotism since 1900: Symptoms, outbreaks, and regulations. Toxicol. Ind. Health. 2013;29:307–316. doi: 10.1177/0748233711432570. PubMed DOI
Klotz J. Activities and effects of ergot alkaloids on livestock physiology and production. Toxins (Basel) 2015;7:2801–2821. doi: 10.3390/toxins7082801. PubMed DOI PMC
Bauer J.I., Gross M., Cramer B., Wegner S., Hausmann H., Hamscher G., Usleber E. Detection of the tremorgenic mycotoxin paxilline and its desoxy analog in ergot of rye and barley: A new class of mycotoxins added to an old problem. Anal. Bioanal. Chem. 2017;409:5101–5112. doi: 10.1007/s00216-017-0455-y. PubMed DOI
Miedaner T., Dänicke S., Schmiedchen B., Wilde P., Wortmann H., Dhillon B., Geiger H., Mirdita V. Genetic variation for ergot (Claviceps purpurea) resistance and alkaloid concentrations in cytoplasmic-male sterile winter rye under pollen isolation. Euphytica. 2010;173:299–306. doi: 10.1007/s10681-009-0083-5. DOI
Mulder P., Van Raamsdonk L., Van Egmond H., Van Der Horst T., De Jong J. Report/RIKILT 2012. Institute of Food Safety; Wageningen, The Netherlands: 2012. [(accessed on 24 July 2019)]. Dutch survey ergot alkaloids and sclerotia in animal feeds. Available online: http://edepot.wur.nl/234699.
Franzmann C., Wächter J., Dittmer N., Humpf H.-U. Ricinoleic acid as a marker for ergot impurities in rye and rye products. J. Agric. Food Chem. 2010;58:4223–4229. doi: 10.1021/jf1006903. PubMed DOI
Appelt M., Ellner F.M. Investigations into the occurrence of alkaloids in ergot and single sclerotia from the 2007 and 2008 harvests. Mycotoxin Res. 2009;25:95–101. doi: 10.1007/s12550-009-0014-2. PubMed DOI
Fajardo J., Dexter J., Roscoe M., Nowicki T. Retention of ergot alkaloids in wheat during processing1, 2. Cereal Chem. 1995;72:291–298.
Pažoutová S., Olšovská J., Linka M., Kolínská R., Flieger M. Chemoraces and habitat specialization of Claviceps purpurea populations. Appl. Environ. Microbiol. 2000;66:5419–5425. doi: 10.1128/AEM.66.12.5419-5425.2000. PubMed DOI PMC
Aboling S., Drotleff A., Cappai M., Kamphues J. Contamination with ergot bodies (Claviceps purpurea sens ulato) of two horse pastures in Northern Germany. Mycotoxin Res. 2016;32:207–219. doi: 10.1007/s12550-016-0253-y. PubMed DOI
Uhlig S., Vikøren T., Ivanova L., Handeland K. Ergot alkaloids in Norwegian wild grasses: A mass spectrometric approach. Rapid Commun. Mass Spectrom. 2007;21:1651–1660. doi: 10.1002/rcm.3005. PubMed DOI
Stoll A., Renz J., Brack A. Über gelbe Farbstoffe im Mutterkorn. 11. Mitteilung über antibakterielle Stoffe. Helv. Chim. Acta. 1952;35:2022–2034. doi: 10.1002/hlca.19520350632. DOI
Franck B. Structure and biosynthesis of the ergot pigments. Angew. Chem. Int. Ed. Engl. 1969;8:251–260. doi: 10.1002/anie.196902511. PubMed DOI
Buchta M., Cvak L. Ergot alkaloids and other metabolites of the genus Claviceps. In: Křen V., Cvak L., editors. Ergot: The Genus Claviceps. Harwood Academic Publishers; Amsterdam, The Netherlands: 1999. pp. 173–200.
Masters K.-S., Bräse S. Xanthones from fungi, lichens, and bacteria: The natural products and their synthesis. Chem. Rev. 2012;112:3717–3776. doi: 10.1021/cr100446h. PubMed DOI
Wezeman T., Bräse S., Masters K.-S. Xanthone dimers: A compound family which is both common and privileged. Nat. Prod. Rep. 2015;32:6–28. doi: 10.1039/C4NP00050A. PubMed DOI
Ciegler A., Hayes A.W., Vesonder R.F. Production and biological activity of secalonic acid D. Appl. Environ. Microbiol. 1980;39:285–287. PubMed PMC
Reddy C., Reddy R., Hayes A., Ciegler A. Teratogenicity of secalonic acid D in mice. J. Toxicol. Environ. Health A. 1981;7:445–455. doi: 10.1080/15287398109529993. PubMed DOI
Zhang J.-Y., Tao L.-Y., Liang Y.-J., Yan Y.-Y., Dai C.-L., Xia X.-K., She Z.-G., Lin Y.-C., Fu L.-W. Secalonic acid D induced leukemia cell apoptosis and cell cycle arrest of G1 with involvement of GSK-3β/β-catenin/c-Myc pathway. Cell Cycle. 2009;8:2444–2450. doi: 10.4161/cc.8.15.9170. PubMed DOI
Yamazaki M., Maebayshi Y., Miyaki K. The isolation of secalonic acid A from Aspergillus ochraceus cultured on rice. Chem. Pharm. Bull. (Tokyo) 1971;19:199–201. doi: 10.1248/cpb.19.199. PubMed DOI
Steffens J.C., Robeson D.J. Secalonic acid A, a vivotoxin in pink root-infected onion. Phytochemistry. 1987;26:1599–1602. doi: 10.1016/S0031-9422(00)82252-9. DOI
Andersen R., Buechi G., Kobbe B., Demain A.L. Secalonic acids D and F are toxic metabolites of Aspergillus aculeatus. J. Org. Chem. 1977;42:352–353. doi: 10.1021/jo00422a042. PubMed DOI
Elsaid A., Sallam A., Ashour A., Ebrahim W., Lahloub M.F., Saad H.-E. Biologically active metabolites from Penicillium sp., An endophyte isolated from Glaucium arabicum. J. Am. Sci. 2016;12:33–41. doi: 10.7537/marsjas12051603. DOI
Naude T.W., Botha C., Vorster J.H., Roux C., van der Linde E., van der Walt S.I., Rottinghaus G., van Jaarsveld L., Lawrence A.N. Claviceps cyperi, a new cause of severe ergotism in dairy cattle consuming maize silage and teff hay contaminated with ergotised Cyperus esculentus (nut sedge) on the Highveld of South Africa. Onderstepoort J. Vet. Res. 2005;72:23–37. doi: 10.4102/ojvr.v72i1.221. PubMed DOI
Cerri M., Reale L., Moretti C., Buonaurio R., Coppi A., Ferri V., Foggi B., Gigante D., Lastrucci L., Quaglia M. Claviceps arundinis identification and its role in the die-back syndrome of Phragmites australis populations in central Italy. Plant Biosyst. 2018;152:818–824. doi: 10.1080/11263504.2017.1347111. DOI
Boestfleisch C., Drotleff A.M., Ternes W., Nehring S., Pažoutová S., Papenbrock J. The invasive ergot Claviceps purpurea var. spartinae recently established in the European Wadden Sea on common cord grass is genetically homogeneous and the sclerotia contain high amounts of ergot alkaloids. Eur. J. Plant Pathol. 2015;141:445–461. doi: 10.1007/s10658-014-0555-x. DOI
van der Linde E.J., Pešicová K., Pažoutová S., Stodůlková E., Flieger M., Kolařík M. Ergot species of the Claviceps purpurea group from South Africa. Fungal Biol. 2016;120:917–930. doi: 10.1016/j.funbio.2016.05.006. PubMed DOI
Brady L. Phylogenetic distribution of parasitism by Claviceps species. Lloydia. 1962;25:1–36.
Franck B., Gottschalk E.M., Ohnsorge U., Hüper F. Mutterkorn-Farbstoffe, XII. Trennung, Struktur und absolute Konfiguration der diastereomeren Secalonsäuren A, B and C. Chem. Ber. 1966;99:3842–3862. doi: 10.1002/cber.19660991218. DOI
McClymont Peace D., Harwig J. Screening for ergot particles in grain products by light microscopy. Food Res. Int. 1982;15:147–149. doi: 10.1016/S0315-5463(82)72381-8. DOI
Maríne Font A., Moreno Martin F., Costes C. Study of the pigments of ergot. New method for studying ergot in flours. Ann. Falsif. Expert. Chim. 1971;64:80.
Neubauer L., Dopstadt J., Humpf H.-U., Tudzynski P. Identification and characterization of the ergochrome gene cluster in the plant pathogenic fungus Claviceps purpurea. Fungal Biol. Biotechnol. 2016;3:2. doi: 10.1186/s40694-016-0020-z. PubMed DOI PMC
Komarova E., Tolkachev O. The chemistry of peptide ergot alkaloids. Part 1. Classification and chemistry of ergot peptides. Pharm. Chem. J. 2001;35:504–513. doi: 10.1023/A:1014050926916. DOI
Wäli P.P., Wäli P.R., Saikkonen K., Tuomi J. Is the pathogenic ergot fungus a conditional defensive mutualist for its host grass? PLoS ONE. 2013;8:e69249. doi: 10.1371/journal.pone.0069249. PubMed DOI PMC
Zhang W., Krohn K., Egold H., Draeger S., Schulz B. Diversity of antimicrobial pyrenophorol derivatives from an endophytic fungus, Phoma sp. Eur. J. Org. Chem. 2008:4320–4328. doi: 10.1002/ejoc.200800404. DOI
Pettit G.R., Meng Y., Herald D.L., Graham K.A., Pettit R.K., Doubek D.L. Isolation and structure of ruprechstyril from Ruprechtia tangarana. J. Nat. Prod. 2003;66:1065–1069. doi: 10.1021/np0300986. PubMed DOI
Menzies J., Turkington T. An overview of the ergot (Claviceps purpurea) issue in western Canada: Challenges and solutions. Can. J. Plant Pathol. 2015;37:40–51. doi: 10.1080/07060661.2014.986527. DOI
Greatorex J., Mantle P. Experimental ergotism in sheep. Res. Vet. Sci. 1973;15:337–346. doi: 10.1016/S0034-5288(18)33806-2. PubMed DOI
Griffith R., Grauwiler J., Hodel C., Leist K., Matter B. Toxicologic considerations. In: Berde B., Schild H.O., editors. Ergot Alkaloids and Related Compounds. Springer; Berlin, Germany: 1978. pp. 805–851.
Tor-Agbidye J., Blythe L., Craig A. Correlation of endophyte toxins (ergovaline and lolitrem B) with clinical disease: Fescue foot and perennial ryegrass staggers. Vet. Hum. Toxicol. 2001;43:140–146. PubMed
Merrill M., Bohnert D., Harmon D., Craig A., Schrick F. The ability of a yeast-derived cell wall preparation to minimize the toxic effects of high-ergot alkaloid tall fescue straw in beef cattle. J. Anim. Sci. 2007;85:2596–2605. doi: 10.2527/jas.2007-0075. PubMed DOI
Harada M., Yano S., Watanabe H., Yamazaki M., Miyaki K. Phlogistic activity of secalonic acid A. Chem. Pharm. Bull. (Tokyo) 1974;22:1600–1606. doi: 10.1248/cpb.22.1600. PubMed DOI
Steyn P.S. The isolation, structure and absolute configuration of secalonic acid D, the toxic metabolite of Penicillium oxalicum. Tetrahedron. 1970;26:51–57. doi: 10.1016/0040-4020(70)85006-2. PubMed DOI
Mayura K., Wallace Hayes A., Berndt W.O. Teratogenicity of secalonic acid d in rats. Toxicology. 1982;25:311–322. doi: 10.1016/0300-483X(82)90109-3. PubMed DOI
Hanumegowda U.M., Dhulipala V.C., Reddy C.S. Mechanism of secalonic acid D-induced inhibition of transcription factor binding to cyclic AMP response element in the developing murine palate. Toxicol. Sci. 2002;70:55–62. doi: 10.1093/toxsci/70.1.55. PubMed DOI
Zhai A., Zhang Y., Zhu X., Liang J., Wang X., Lin Y., Chen R. Secalonic acid A reduced colchicine cytotoxicity through suppression of JNK, p38 MAPKs and calcium influx. Neurochem. Int. 2011;58:85–91. doi: 10.1016/j.neuint.2010.10.016. PubMed DOI
Zhai A., Zhu X., Wang X., Chen R., Wang H. Secalonic acid A protects dopaminergic neurons from 1-methyl-4-phenylpyridinium (MPP+)-induced cell death via the mitochondrial apoptotic pathway. Eur. J. Pharmacol. 2013;713:58–67. doi: 10.1016/j.ejphar.2013.04.029. PubMed DOI
Kurobane I., Iwahashi S., Fukuda A. Cytostatic activity of naturally isolated isomers of secalonic acids and their chemically rearranged dimers. Drugs Exp. Clin. Res. 1987;13:339–344. PubMed
Millot M., Tomasi S., Studzinska E., Rouaud I., Boustie J. Cytotoxic constituents of the lichen Diploicia canescens. J. Nat. Prod. 2009;72:2177–2180. doi: 10.1021/np9003728. PubMed DOI
Hu Y.-P., Tao L.-Y., Wang F., Zhang J.-Y., Liang Y.-J., Fu L.-W. Secalonic acid D reduced the percentage of side populations by down-regulating the expression of ABCG2. Biochem. Pharmacol. 2013;85:1619–1625. doi: 10.1016/j.bcp.2013.04.003. PubMed DOI
Franck B., Flasch H. Die Ergochrome (Physiologie, Isolierung, Struktur und Biosynthese) In: Grisebach H., Kirby G.W., Herz W., editors. Fortschritte der Chemie Organischer Naturstoffe. Springer; Berlin, Germany: 1973. pp. 151–206. PubMed
Reddy C., Hayes A., Williams W., Ciegler A. Toxicity of secalonic acid D. J. Toxicol. Environ. Health A. 1979;5:1159–1169. doi: 10.1080/15287397909529821. PubMed DOI
Chen L., Li Y.-P., Li X.-X., Lu Z.-H., Zheng Q.-H., Liu Q.-Y. Isolation of 4, 4′-bond secalonic acid D from the marine-derived fungus Penicillium oxalicum with inhibitory property against hepatocellular carcinoma. J. Antibiot. 2019;72:34. doi: 10.1038/s41429-018-0104-5. PubMed DOI
Gao X., Sun H., Liu D., Zhang J., Zhang J., Yan M., Pan X. Secalonic acid-F inhibited cell growth more effectively than 5-fluorouracil on hepatocellular carcinoma in vitro and in vivo. Neoplasma. 2017;64:344–350. doi: 10.4149/neo_2017_304. PubMed DOI
Kawai K., Nakamaru T., Maebayashi Y., Nozawa Y., Yamazaki M. Inhibition by secalonic acid D of oxidative phosphorylation and Ca2+-induced swelling in mitochondria isolated from rat livers. Appl. Environ. Microbiol. 1983;46:793–796. PubMed PMC
Pazoutova S., Olsovska J., Sulc M., Chudickova M., Flieger M. Claviceps nigricans and Claviceps grohii: Their alkaloids and phylogenetic placement. J. Nat. Prod. 2008;71:1085–1088. doi: 10.1021/np8001173. PubMed DOI
Osmundson T.W., Eyre C.A., Hayden K.M., Dhillon J., Garbelotto M.M. Back to basics: An evaluation of NaOH and alternative rapid DNA extraction protocols for DNA barcoding, genotyping, and disease diagnostics from fungal and oomycete samples. Mol. Ecol. Resour. 2013;13:66–74. doi: 10.1111/1755-0998.12031. PubMed DOI
Flieger M., Banďouchová H., Černý J., Chudíčková M., Kolařík M., Kováčová V., Martínková N., Novák P., Šebesta O., Stodůlková E. Vitamin B2 as a virulence factor in Pseudogymnoascus destructans skin infection. Sci. Rep. 2016;6:33200. doi: 10.1038/srep33200. PubMed DOI PMC
Stodůlková E., Císařová I., Kolařík M., Chudíčková M., Novák P., Man P., Kuzma M., Pavlů B., Černý J., Flieger M. Biologically active metabolites produced by the basidiomycete Quambalaria cyanescens. PLoS ONE. 2015;10:e0118913. doi: 10.1371/journal.pone.0118913. PubMed DOI PMC
Hammer Ø., Harper D., Ryan P. PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 2001;4:9.
Finney D.J. Probit Analysis. 3rd ed. Cambridge University Press; Cambridge, UK: 1971.