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The chemical structures and biological activities of indole diterpenoids |
| Jingwen Niu1, Jianzhao Qi1,2, Pengchao Wang1, Chengwei Liu1, and Jin2 |
1 Key Laboratory for Enzyme and Enzyme-Like Material Engineering of Heilongjiang, College of Life Science, Northeast Forestry University, Harbin 150040, Heilongjiang, China;
2 Shaanxi Key Laboratory of Natural Products and Chemical Biology, College of Chemistry and Pharmacy, Northwest A&F University, Yangling 712100, Shaanxi, China |
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Abstract Indole diterpenoids (IDTs) are an essential class of structurally diverse fungal secondary metabolites, that generally appear to be restricted to a limited number of fungi, such as Penicillium, Aspergillus, Claviceps, and Epichloe species, etc. These compounds share a typical core structure consisting of a cyclic diterpene skeleton of geranylgeranyl diphosphate (GGPP) and an indole ring moiety derived from indole-3-glycerol phosphate (IGP). 3-geranylgeranylindole (3-GGI) is the common precursor of all IDTs. On this basis, it is modified by cyclization, oxidation, and prenylation to generate a large class of compounds with complex structures. These compounds exhibit antibacterial, anti-insect, and ion channel inhibitory activities. We summarized 204 compounds of IDTs discovered from various fungi over the past 50 years, these compounds were reclassified, and their biological activities were summarized. This review will help to understand the structural diversity of IDTs and provide help for their physiological activities.
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| Keywords
Indole diterpenoids
Structural classification
Physiological activity
Fungus
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| Fund:This work was funded by the National Natural Science Foundation of China (Project No. 22077102 and 21877089), and the Shaanxi Key Laboratory of Natural Product & Chemical Biology Open Foundation (Project No. SXNPCB 2021001). |
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Corresponding Authors:
Chengwei Liu,E-mail:liuchw@nefu.edu.cn;Jin-ming Gao,E-mail:jinminggao@nwsuaf.edu.cn
E-mail: liuchw@nefu.edu.cn;jinminggao@nwsuaf.edu.cn
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Issue Date: 08 March 2023
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1. Saikia S, Nicholson MJ, Young C, Parker EJ, Scott B. The genetic basis for indole-diterpene chemical diversity in filamentous fungi. Mycol Res. 2008;112:184-99.
2. Andersen B, Frisvad JC. Natural occurrence of fungi and fungal metabolites in moldy tomatoes. J Agric Food Chem. 2004;52:7507-13.
3. Evans TJ, Gupta RC. Tremorgenic mycotoxins. In:Gupta RC, editor. Veterinary toxicology. Academic; 2018. p. 1033-41.
4. Roll DM, Barbieri LR, Bigelis R, McDonald LA, Arias DA, Li PC, et al. The lecanindoles, nonsteroidal progestins from the terrestrial fungus Verticillium lecanii 6144. J Nat Prod. 2009;72:1944-8.
5. Reddy P, Guthridge K, Vassiliadis S, Hemsworth J, Hettiarachchige I, Spangenberg G, et al. Tremorgenic mycotoxins:structure diversity and biological activity. Toxins (Basel). 2019;11:302.
6. Garcia ML, Goetz MA, Kaczorowski GJ, Mcmanus OB, Monaghan RL, Strohl WR, et al. U.S. Patent WO-03105724-A2, 13 Jun 2003.
7. Fan Y, Wang Y, Liu P, Fu P, Zhu T, Wang W, et al. Indole-diterpenoids with anti-H1N1 activity from the aciduric fungus Penicillium camemberti OUCMDZ-1492. J Nat Prod. 2013;76:1328-36.
8. Gloer JB, TePaske MR, Sima JS, Wicklow DT, Dowd PF. Antiinsectan aflavinine derivatives from the sclerotia of Aspergillus flavus. J Org Chem. 1988;53:5457-60.
9. Jesus AE, Gorst-Allman CP, Steyn PS, Heerden FR, Vleggaar R, Wessels PL, et al. Tremorgenic mycotoxins from Penicillium crustosum. Biosynthesis of penitrem A. J Chem Soc, Perkin Trans. 1983;1(1):1863-8.
10. Tagami K, Liu C, Minami A, Noike M, Isaka T, Fueki S, et al. Reconstitution of biosynthetic machinery for indole-diterpene paxilline in Aspergillus oryzae. J Am Chem Soc. 2013;135:1260-3.
11. Kozak L, Szilagyi Z, Tóth L, Pócsi I, Molnar I. Tremorgenic and neurotoxic paspaline-derived indole-diterpenes:biosynthetic diversity, threats and applications. Appl Microbiol Biot. 2019;103:1599-616.
12. Schatz DJ, Kuenstner EJ, George DT, Pronin SV. Synthesis of rearranged indole diterpenes of the paxilline type. Nat Prod Rep. 2022;39:946-68.
13. Liu CW, Minami A, Ozaki T, Oikawa H. Biosynthesis of indole diterpenes. Comprehensive natural products III:chemistry and biology. Elsevier 2022:446-66.
14. Minami A, Liu C, Oikawa H. Total biosynthesis of fungal indole diterpenes using cell factories. HETEROCYCLES. 2016;92:397-421.
15. Ozaki T, Minami A, Oikawa H. Biosynthesis of indole diterpenes:a reconstitution approach in a heterologous host. Nat Prod Rep. 2022. https://doi.org/10.1002/chin.201617243.
16. Ondeyka JG, Helms GL, Hensens OD, Singh SB, Etal EA. Nodulisporic acid A, a novel and potent insecticide from a Nodulisporium sp. isolation, structure determination, and chemical transformations. J Am Chem Soc. 1997;119:8809-16.
17. Meinke PT, Smith MM, Shoop WL. Nodulisporic acid:its chemistry and biology. Curr Top Med Chem. 2002;2:655-74.
18. Singh SB, Ondeyka JG, Jayasuriya H, Zink DL, Ha SN, Dahl-Roshak A, et al. Nodulisporic acids D-F:structure, biological activities, and biogenetic relationships. J Nat Prod. 2004;67:1496-506.
19. Hensens OD, Ondeyka JG, Dombrowski AW, Ostlind DA, Zink DL. Isolation and structure of nodulisporic acid A1 and A2, novel insecticides from a Nodulisporium sp. Tetrahedron Lett. 1999;40:5455-8.
20. Ondeyka JG, Dahl-Roshak AM, Tkacz JS, Zink DL, Zakson-Aiken M, Shoop WL, et al. Nodulisporic acid B, B1, and B2:a series of 1'-deoxynodulisporic acids from Nodulisporium sp. Bioorg Med Chem Lett. 2002;12:2941-4.
21. Ondeyka JG, Byrne K, Vesey D, Zink DL, Shoop WL, Goetz MA, et al. Nodulisporic acids C, C1, and C2:a series of D-ring-opened nodulisporic acids from the fungus Nodulisporium sp. J Nat Prod. 2003;66:121-4.
22. Zhang YH, Li L, Li YQ, Luo JH, Li W, Li LF, et al. Oxalierpenes A and B, unusual indole-diterpenoid derivatives with antiviral activity from a marine-derived strain of the fungus Penicillium oxalicum. J Nat Prod. 2022;85:1880-5.
23. Fehr T, Acklin W. Die isolierung zweier neuartiger indol-derivate aus dem mycel von Claviceps paspali STEVENSet HALL. Helv Chim Acta. 1966;49:1907-10.
24. Sallam AA, Ayoub NM, Foudah AI, Gissendanner CR, Meyer SA, El-Sayed KA. Indole diterpene alkaloids as novel inhibitors of the Wnt/β-catenin pathway in breast cancer cells. Eur J Med Chem. 2013;70:594-606.
25. Qiao MF, Ji NY, Liu XH, Li K, Zhu QM, Xue QZ. Indoloditerpenes from an algicolous isolate of Aspergillus oryzae. Bioorg Med Chem Lett. 2010;20:5677-80.
26. Chen MY, Xie QY, Kong FD, Ma QY, Zhou LM, Yuan JZ, et al. Two new indole-diterpenoids from the marine-derived fungus Penicillium sp. KFD28. J Asian Nat Prod Res. 2021;23:1030-6.
27. Chaiyosang B, Kanokmedhakul K, Yodsing N, Boonlue S, Yang JX, Wang YA, et al. Three new indole diterpenoids from Aspergillus aculeatus KKUCT2. Nat Prod Res. 2022;36:4973-81.
28. Nozawa K, Nakajima S, Kawai K, Udagawa S. Studies on fungal products. Part 17. Isolation and structures of novel indoloditerpenes, emindoles DA and DB, from Emericella desertorum:X-ray molecular structure of emindole DA acetate. J Chem Soc. 1988;7:1689-94.
29. Nozawa K, Horie Y, Udagawa S, Kawai K, Yamazaki M. Isolation of a new tremorgenic indoloditerpene, 1'-O-acetylpaxilline, from Emericella striata and distribution of paxilline in Emericella spp. Chem Pharm Bull (Tokyo). 1989;37:1387-9.
30. Gloer JB, Rinderknecht BL, Wicklow DT, Dowd PF. Nominine:a new insecticidal indole diterpene from the sclerotia of Aspergillus nomius. J Org Chem. 1989;54:2530-2.
31. Laakso JA, Gloer JB, Wicklow DT, Dowd PF. Radarins A-D:new antiinsectan and cytotoxic indole diterpenoids from the sclerotia of Aspergillus sulphureus. J Org Chem. 1992;57:138-41.
32. Kimura Y, Nishibe M, Nakajima H, Hamasaki T, Shigemitsu N, Sugawara F, et al. Emeniveol:a new pollen growth inhibitor from the fungus, Emericella nivea. Tetrahedron Lett. 1992;33:6987-90.
33. Hosoe T, Itabashi T, Kobayashi N, Udagawa S, Kawai K. Three new types of indoloditerpenes, emindole PA-PC, from Emericella purpurea. Revision of the structure of emindole PA. Chem Pharm Bull (Tokyo). 2006;54:185-7.
34. Liu L, Xu W, Li S, Chen MY, Cheng YJ, Yuan WJ, et al. Penicindopene A, a new indole diterpene from the deep-sea fungus Penicillium sp. YPCMAC1. Nat Prod Res. 2019;33:2988-94.
35. Dai LT, Yang L, Kong FD, Ma QY, Xie QY, Dai HF, et al. Cytotoxic indolediterpenoids from the marine-derived fungus Penicillium sp. KFD28. Mar Drugs. 2021;19:613.
36. Tepaske MR, Gloer JB, Wicklow DT, Dowd PF. Three new aflavinines from the sclerotia of Aspergillus tubingensis. Tetrahedron. 1989;45:4961-8.
37. Han X, Bao XF, Wang CX, Xie J, Song XJ, Dai P, et al. Cladosporine A, a new indole diterpenoid alkaloid with antimicrobial activities from Cladosporium sp. Nat Prod Res. 2021;35:1115-21.
38. TePaske MR, Gloer JB, Wicklow DT, Dowd PF. Tubingensin A:an antiviral carbazole alkaloid from the sclerotia of Aspergillus tubingensis. J Org Chem. 1989;54:4743-6.
39. Tepaske MR, Gloer JB, Wicklow DT, Dowd PF. The structure of tubingensin B:a cytotoxic carbazole alkaloid from the sclerotia of Aspergillus tubingensis. Tetrahedron Lett. 1989;30:5965-8.
40. Tepaske MR, Gloer JB, Wicklow DT, Dowd PF. Aflavazole:a new antiinsectan carbazole metabolite from the sclerotia of Aspergillus flavus. J Org Chem. 1990;55:5299-301.
41. Li H, Chen Q, Lu Z, Li A. Total syntheses of aflavazole and 14-hydroxyaflavinine. J Am Chem Soc. 2016;138:15555-8.
42. Ariantari NP, Ancheeva E, Wang C, Mandi A, Knedel TO, Kurtan T. Indole diterpenoids from an endophytic Penicillium sp. J Nat Prod. 2019;82:1412-23.
43. Miles CO, Wilkins AL, Gallagher RT, Hawkes AD, Munday SC, Towers NR. Synthesis and tremorgenicity of paxitriols and lolitriol:possible biosynthetic precursors of lolitrem B. J Agric Food Chem. 1992;40:234-8.
44. Laakso JA, Gloer JB, Wicklow DT, Dowd PF. Sulpinines A-C and secopenitrem B:new antiinsectan metabolites from the sclerotia of Aspergillus sulphureus. J Org Chem. 1992;57:2066-71.
45. Staub GM, Gloer J, Wicklow DT, Dowd PF. Aspernomine:a cytotoxic antiinsectan metabolite with a novel ring system from the sclerotia of Aspergillus nomius. J Am Chem Soc. 1992;114:1015-7.
46. Ooike M, Nozawa K, Udagawa S, Kawai K. Structures of a new type of indoloditerpene, petromindole, and a new asterriquinone derivative, PM-53, from the ascostromata of Petromyces muricatus. Chem Pharm Bull (Tokyo). 1997;45:1694-6.
47. Chen L, Gloer JB, Wicklow DT, Dowd PF. Thiersinines A and B:novel antiinsectan indole diterpenoids from a new fungicolous Penicillium species (NRRL 28147). Org Lett. 2002;4:3095-8.
48. Ogata M, Ueda JY, Hoshi M, Hashimoto J, Nakashima T, Anzai K, et al. A novel indole-diterpenoid, JBIR-03 with anti-MRSA activity from Dichotomomyces cejpii var. cejpii NBRC 103559. J Antibiot (Tokyo). 2007;60:645-8.
49. Gao SS, Li XM, Williams K, Proksch P, Ji NY, Wang BG. Rhizovarins A-F, indole-diterpenes from the mangrove-derived endophytic fungus Mucor irregularis QEN-189. J Nat Prod. 2016;79:2066-74.
50. Zhao JC, Luan ZL, Liang JH, Cheng ZB, Sun CP, Wang YL, et al. Drechmerin H, a novel 1(2), 2(18)-diseco indole diterpenoid from the fungus Drechmeria sp. as a natural agonist of human pregnane X receptor. Bioorg Chem. 2018;79:250-6.
51. Xu LL, Hai P, Zhang SB, Xiao JF, Gao Y, Ma BJ, et al. Prenylated indole diterpene alkaloids from a mine-soil-derived Tolypocladium sp. J Nat Prod. 2019;82:221-31.
52. Nur EAA, Kobayashi K, Amagai A, Ohshiro T, Tomoda H. New terpendole congeners, inhibitors of sterol O-acyltransferase, produced by Volutella citrinella BF-0440. Molecules. 2020;25:3079.
53. Zhou G, Sun C, Hou X, Che Q, Zhang G, Gu Q, et al. Ascandinines A-D, indole diterpenoids, from the sponge-derived fungus Aspergillus candidus HDN15-152. J Org Chem. 2021;86:2431-6.
54. Springer JP, Clardy J. Paspaline and paspalicine, two indole-mevalonate metabolites from Claviceps paspali. Tetrahedron Lett. 1980;21:231-4.
55. Munday-Finch SC, Wilkins AL, Miles CO. Isolation of paspaline B, an indole-diterpenoid from Penicilium paxilli. Phytochemistry. 1996;41:327-32.
56. Cole RJ, Kirksey JW, Wells JM. A new tremorgenic metabolite from Penicillium paxilli. Can J Microbiol. 1974;20:1159-62.
57. Springer JP, Clardy J, Wells JM, Cole RJ, Kirksey JW. The structure of paxilline, a tremorgenic metabolite of bainier. Tetrahedron Lett. 1975;16:2531-4.
58. Nozawa K, Horie Y, Udagawa S, Kawai K, Yamazaki M. Isolation of a new tremorgenic indologiterpene, 1'-O-acetylpaxilline, from Emericella striata and distribution of paxilline in Emericella spp. Chem Pharm Bull (Tokyo). 1989;37:1387-9.
59. Yamaguchi T, Nozawa K, Hosoe T, Nakajima S, Kawai K. Indoloditerpenes related to tremorgenic mycotoxins, penitrems, from Penicillium crustosum. Phytochemistry. 1993;32:1177-81.
60. Zhao LL. Search for new antineoplastic substances from marinederived fungi. Dissertation, Fudan University, 2008.
61. Mantle PG, Weedon CM. Biosynthesis and transformation of tremorgenic indolediterpenoids by Penicillium paxilli and Acremonium lolii. Phytochemistry. 1994;36:1209-17.
62. Tomoda H, Tabata N, Yang DJ, Takayanagi H, Omura S. Terpendoles, novel ACAT inhibitors produced by Albophoma yamanashiensis. III. Production, isolation and structure elucidation of new components. J Antibiot. 1995;48:1-4.
63. Tarui Y, Chinen T, Nagumo Y, Motoyama T, Hayashi T, Hirota H, et al. Terpendole E and its derivative inhibit STLC- and GSK-1-resistant Eg5. ChemBioChem. 2014;15:934-8.
64. Xu LL, Pang XJ, Shi Q, Xian PJ, Tao YD, Yang XL. Two new prenylated indole diterpenoids from Tolypocladium sp. and their antimicrobial activities. Chem Biodivers. 2019;16:e1900116.
65. Belofsky GN, Gloer JB, Wicklow DT, Dowd PF. Antiinsectan alkaloids:shearinines A-C and a new paxilline derivative from the ascostromata of Eupenicillium shearii. Tetrahedron. 1995;51:3959-68.
66. Itabashi T, Hosoe T, Wakana D, Fukushima K, Takizawa K, Yaguchi T, et al. A new indoloditerpene derivative, penijanthine A, isolated from Penicillium janthinellum. J Nat Med. 2009;63:96-9.
67. Zhang YH, Huang SD, Pan HQ, Bian XQ, Wang ZY, Han AH, et al. Structure determination of two new indole-diterpenoids from Penicillium sp. CM-7 by NMR spectroscopy. Magn Reson Chem. 2014;52:306-9.
68. Gallagher RT, Finer J, Clardy J, Leutwiler A, Weibel FR, Acklin W, et al. Paspalinine, a tremorgenic metabolite from Claviceps paspali Stevens et Hall. Tetrahedron Lett. 1980;21:235-8.
69. Staub GM, Gloer KB, Gloer JB, Wicklow DT, Dowd PF. New paspalinine derivatives with antiinsectan activity from the sclerotia of Aspergillus nomius. Tetrahedron Lett. 1993;34:2569-72.
70. Huang XH, Nishida H, Tomoda H, Tabata N, Shiomi K, Yang DJ. Terpendoles, novel ACAT inhibitors produced by Albophoma yamanashiensis. II. Structure elucidation of terpendoles A, B, C and D. J Antibiot (Tokyo). 1995;48:5-11.
71. Gatenby WA, Munday-Finch SC, Wilkins AL, Miles CO. Terpendole M, a novel indole-diterpenoid isolated from Lolium perenne infected with the endophytic fungus Neotyphodium lolii. J Agric Food Chem. 1999;47:1092-7.
72. Junker B, Walker A, Connors N, Seeley A, Masurekar P, Hesse M. Production of indole diterpenes by Aspergillus alliaceus. Biotechnol Bioeng. 2006;95:919-37.
73. Liang JH, Huo XK, Cheng ZB, Sun CP, Zhao JC, Kang XH, et al. An indole diterpenoid isolated from the fungus Drechmeria sp. and its antimicrobial activity. Nat Prod Res. 2019;33:2770-6.
74. Valdes JJ, Cameron JE, Cole RJ. Aflatrem:a tremorgenic mycotoxin with acute neurotoxic effects. Environ Health Persp. 1985;62:459-63.
75. Gallagher RT, Wilson BJ. Aflatrem, the tremorgenic mycotoxin from Aspergillus flavus. Mycopathologia. 1979;66:183-5.
76. Cole RJ, Dorner JW, Lansden JA, Cox RH, Pape C, Cunfer B, et al. Paspalum staggers:isolation and identification of tremorgenic metabolites from sclerotia of Claviceps paspali. J Agric Food Chem. 1977;25:1197-201.
77. Uhlig S, Botha CJ, Vrålstad T, Rolén E, Miles CO. Indole-diterpenes and ergot alkaloids in Cynodon dactylon (bermuda grass) infected with Claviceps cynodontis from an outbreak of tremors in cattle. J Agric Food Chem. 2009;57:11112-9.
78. Alley MC, Scudiero DA, Monks A, Hursey ML, Czerwinski MJ, Fine DL, et al. Feasibility of drug screening with panels of human tumor cell lines using a microculture tetrazolium assay. Cancer Res. 1988;48:589-601.
79. DeFarias FP, Carvalho MF, Lee SH, Kaczorowski GJ, Suarez-Kurtz G. Effects of the K+ channel blockers paspalitrem-C and paxilline on mammalian smooth muscle. Eur J Pharmacol. 1996;314:123-8.
80. Xu MJ, Gessner G, Groth I, Lange C, Christner A, Bruhn T, et al. Shearinines D-K, new indole triterpenoids from an endophytic Penicillium sp. (strain HKI0459) with blocking activity on large-conductance calciumactivated potassium channels. Tetrahedron. 2007;63:435-44.
81. Liu C, Noike M, Minami A, Oikawa H, Dairi T. Functional analysis of a prenyltransferase gene (paxD) in the paxilline biosynthetic gene cluster. Appl Microbiol Biot. 2014;98:199-206.
82. Liu C, Noike M, Minami A, Oikawa H, Dairi T. A fungal prenyltransferase catalyzes the regular diprenylation at positions 20 and 21 of paxilline. Biosci Biotech Bioch. 2014;78:448-54.
83. Ohshiro T, Morita H, Nur EAA, Hosoda K, Uchida R, Tomoda H. Voluhemins, new inhibitors of sterol O-acyltransferase, produced by Volutella citrinella BF-0440. J Antibiot (Tokyo). 2020;73:748-55.
84. Junko O, Arihiro T, Yoshiyuki T, Masaichi N, JPN. Patent JP2004168680, 18 Nov 2002.
85. Liu C, Minami A, Dairi T, Gomi K, Scott B, Oikawa H. Biosynthesis of shearinine:diversification of a tandem prenyl moiety of fungal indole diterpenes. Org Lett. 2016;18:5026-9.
86. Kudo K, Liu C, Matsumoto T, Minami A, Ozaki T, Toshima H, et al. Heterologous biosynthesis of fungal indole sesquiterpene sespendole. ChemBioChem. 2018;19:1492-7.
87. Jesus AE, Steyn PS, Heerden FR, Vleggaar R. Structure elucidation of the janthitrems, novel tremorgenic mycotoxins from Penicillium janthinellum. J Chem Soc Perkin Trans. 1984;1(15):697-701.
88. Wilkins AL, Miles CO, Ede RM, Gallagher RT, Munday SC. Structure elucidation of janthitrem B, a tremorgenic metabolite of Penicillium janthinellum, and relative configuration of the A and B rings of janthitrems B, E, and F. J Agric Food Chem. 1992;40:1307-9.
89. Penn J, Swift R, Wigley LJ, Mantle PG, Bilton JN, Sheppard RN. Janthitrems B and C, two principal indole-diterpenoids produced by Penicillium janthinellum. Phytochemistry. 1993;32:1431-4.
90. Smetanina OF, Kalinovsky AI, Khudyakova YV, Pivkin MV, Dmitrenok PS, Fedorov SN, et al. Indole alkaloids produced by a marine fungus isolate of Penicillium janthinellum Biourge. J Nat Prod. 2007;70:906-9.
91. Hennessy LM, Popay AJ, Finch SC, Clearwater MJ, Cave VM. Temperature and plant genotype alter alkaloid concentrations in ryegrass infected with an Epichloë endophyte and this affects an insect herbivore. Front Plant Sci. 2016;7:1097.
92. Ludlow EJ, Vassiliadis S, Ekanayake PN, Hettiarachchige IK, Reddy P, Sawbridge TI, et al. Analysis of the indole diterpene gene cluster for biosynthesis of the epoxy-janthitrems in Epichloë endophytes. Microorganisms. 2019;7:560.
93. Matsui C, Ikeda Y, Iinuma H, Kushida N, Kunisada T, Simizu S, et al. Isolation of a novel paxilline analog pyrapaxilline from fungus that inhibits LPS-induced NO production. J Antibiot (Tokyo). 2014;67:787-90.
94. Babu JV, Popay AJ, Miles CO, Wilkins AL, di Menna ME, Finch SC. Identification and structure elucidation of janthitrems A and D from Penicillium janthinellum and determination of the tremorgenic and anti-insect activity of janthitrems A and B. J Agric Food Chem. 2018;66:13116-25.
95. Gallagher RT, White EP, Mortimer PH. Ryegrass staggers:isolation of potent neurotoxins lolitrem A and lolitrem B from staggers-producing pastures. N Z Vet J. 1981;29:189-90.
96. Reddy P, Deseo MA, Ezernieks V, Guthridge K, Spangenberg G, Rochfort S. Toxic indole diterpenes from endophyte-infected perennial ryegrass Lolium perenne L.:isolation and stability. Toxins (Basel). 2019;11:16.
97. Miles CO, Munday SC, Wilkins AL, Ede RM, Towers NR. Large-scale isolation of lolitrem B and structure determination of lolitrem E. J Agric Food Chem. 1994;42:1488-92.
98. Imlach WL, Finch SC, Dunlop J, Dalziel JE. Structural determinants of lolitrems for inhibition of BK large conductance Ca2+- activated K+ channels. Eur J Pharmacol. 2009;605:36-45.
99. Munday-Finch SC, Wilkins AL, Miles CO, Ede RM, Thomason RA. Structure elucidation of lolitrem F, a naturally occurring stereoisomer of the tremorgenic mycotoxin lolitrem B, isolated from Lolium perenne infected with Acremonium lolii. J Agric Food Chem. 1996;44:2782-8.
100. Munday-Finch SC, Wilkins AL, Miles CO, Tomoda H, Omura S. Isolation and structure elucidation of lolilline, a possible biosynthetic precursor of the lolitrem family of tremorgenic mycotoxins. J Agric Food Chem. 1997;45:199-204.
101. Munday-Finch SC, Wilkins AL, Miles CO. Isolation of lolicine A, lolicine B, lolitriol, and lolitrem N from Lolium perenne infected with Neotyphodium lolii and evidence for the natural occurrence of 31-epilolitrem N and 31-epilolitrem F. J Agric Food Chem. 1998;46:590-8.
102. Laakso JA, Gloer JB, Wicklow DT, Dowd PF. A new penitrem analog with antiinsectan activity from the sclerotia of Aspergillus sulphureus. J Agric Food Chem. 1993;41:973-5.
103. Moldes-Anaya A, Rundberget T, Uhlig S, Rise F, Wilkins AL. Isolation and structure elucidation of secopenitrem D, an indole alkaloid from Penicillium crustosum Thom. Toxicon. 2011;57:259-65. |
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