THE OCCURRENCE OF ECDYSTEROIDS AND ECDYSTEROID-RELATED COMPOUNDS IN SPECIES

Laurie Dinan1, Nilufar Mamadalieva2 and René Lafont1,3

1Institut Biophytis, Sorbonne Université, 4 place Jussieu, Paris 7505, France

2S. Yu. Yusonov Institute for the Chemistry of Plant Substances, Academy of Sciences of the Republic of Uzbekistan, Tashkent, Republic of Uzbekistan

3Sorbonne Université, Paris-Seine Biology Institute (BIOSIPE), CNRS, 75005 Paris, France

Version 1: 24th October, 2019

The list of edible fungi is based on information from Wikipedia (Edible mushroom) with additional species added. The presence of ecdysteroids or ecdysteroid-related compounds in the fruiting bodies of these species was identified from the review of Kovganko (1999) and additional literature searches.

Important notice:

This database has been designed as a tool to help the scientific community in research on ecdysteroids. The authors wish it to be an evolving system and would encourage other researchers to submit new data, additional publications, proposals for modifications or comments to the authors for inclusion. All new material will be referenced to its contributor.

Reproduction of the material in this database in its entirety is not permitted. Reproduction of parts of the database is only permitted under the following conditions:

• reproduction is for personal use, for teaching and research, but not for distribution to others • reproduction is not for commercial use • the origin of the material is indicated in the reproduction • we should be notified in advance to allow us to document that the reproduction is being made Where data are reproduced in published texts, they should be acknowledged by the reference:

Lafont R., Harmatha J., Marion-Poll F., Dinan L., Wilson I.D.: The Ecdysone Handbook, 3rd edition, on-line, http://ecdybase.org

Illustrations may not under any circumstances be used in published texts, commercial or otherwise, without previous written permission of the author(s).

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Please notify Laurie Dinan ([email protected]) of any errors or additional literature sources.

© 2019: Laurence Dinan, Nilufar Mamadalieva and René Lafont

Latin Name Family Common Category Ecdysteroids and Reference Name Ecdysteroid- & Method related Compounds Agaricus Agariaceae Horse Edible wild nt arvensis mushroom species Agaricus Agariaceae Almond Commercially cerevisterol Kawagishi blazei (A. mushroom, cultivated (2.3mg from 5kg et al. subrufescens) himematsuta fw), 3β,5α- (1988); ke dihydroxy-6β- isolation methoxyergosta- and 7,22-diene spectroscop (3.4mg), ic 3β,5α,,6β,9α- identificatio tetrahydroxyergos n ta-7,22-diene (6.3mg), 3β,5α,9α- trihydroxyergosta- 7,22-diene-6-one (5.7mg) Agaricus Agariaceae Common Commercially Chestnut: 0.32μg Findeisen bisporus mushroom cultivated 20E eq./g dw (2004); EIA White 1: 20.1 20E of eq. μg/g dw ecdysteroid White 2: 95.2 20E s (DBL-2 eq. μg/g dw antiserum) - Biophytis (unpublishe d); HPLC- MS/MS for 20E Agaricus Agariaceae Pinewood Edible wild nt silvaticus mushroom species Amanita Amanitaceae Caesar’s Edible wild nt caesarea mushroom species Amanita Amanitaceae Tawny Edible only nt fulva grisette after cooking Amanita Amanitaceae Fly agaric Edible only - Dinan muscaria after cooking (unpublishe d); RIA for ecdysteroid s (DBL1 antiserum) Amanita Amanitaceae Blusher Edible only - Dinan

2 rubescens after cooking (unpublishe d); RIA for ecdysteroid s (DBL1 antiserum) Armillaria Physalacriacea Honey Edible wild nt mellea species Auricularia Auriculariaceae Jew’s ear, Commerically nt auricular- jelly ear cultivated judae mushroom Auricularia Auriculariaceae Cloud-ear Commercially nt polytricha fungus harvested from the wild Boletus Boletaceae Dark cep, Commercially nt aereus bronze harvested bolete from the wild Boletus Boletaceae Bay bolete Edible wild nt badius species Boletus edulis Boletaceae Edible Commercially - Dinan boletus harvested (unpublishe from the wild d); RIA for ecdysteroid s (DBL1 antiserum) Calocybe Lyophyllaceae St. George’s Edible wild nt gambosa mushroom species Lycoperdaceae Purple- Edible wild calvasterone Kawahara cyathiformis spored species ([6,6’R]-biergosta- et al. 4,4’,7,7’,22,22’- (1993); hexaene-3,3’- isolation dione and spectroscop ic identificatio n cyathisterone Kawahara (ergosta-7,22- et al. diene-3,6-dione; (1994); 30mg from 4kg isolation fw)), cyathisterol and (8β- spectroscop hydroxyergost- ic 4,6,22-trien-3-one; identificatio 80mg), ergosta- n 4,7,22-triene-3,6- dione (300mg), ergosta- 4,6,8(14),22- tetraen-3-one (200mg) calvasterol A (14α- Kawahara

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hydroxyergosta- et al. 4,7,9,22-teraen- (1995); 3,6-dione; 10mg isolation from 4kg fw), and calvasterol B spectroscop (9α,14α- ic dihydroxyergosta- identificatio 4,7,22-trien-3,6- n dione; 15mg from 4kg fw), Calvatia Lycoperdaceae Giant Edible wild nt gigantea puffball species Calvatia Lycoperdaceae Edible wild nt utriformis species (Lycoperdon utriforme, ) Cantharellus Cantherellacea Golden Commercially nt cibarius e chanterelle harvested from the wild Cantharellus Cantherellacea Funnel Commercially nt tubaeformis e chanterelle, harvested (Craterellus yellow-foot from the wild tubaeformis) Chroogomph Gomphidiaceae Pine-spikes, Edible wild nt us rutilus spike-caps, species brown slimecap, copper spike Clavariaceae Clavariaceae Coral fungi Edible wild nt spp. species Clavulinaceae Clavulinaceae Coral fungi Edible wild nt spp. species Clitocybe Tricholomatace Wood blewit Commercially nt nuda (Lepista ae harvested nuda) from the wild/ Commerically cultivated/ Edible only after cooking Coprinopsis Psathyrellaceae Common ink Must not be nt atramentaria cap consumed with alcohol Coprinus Shaggy Edible wild nt comatus inkcap species/Only young fruiting bodies are edible Cortinarius Cortinariaceae Gypsy Commercially nt caperatus mushroom harvested

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from the wild Cortinarius Cortinariaceae Schleierling Edible wild nt variicolor species Craterellus Cantherellacea Horn of Commercially nt cornucopioid e plenty, harvested es trompette de from the wild la morte Cyclocybe undefined Pioppino, Commercially nt aegerita poplar cultivated mushroom Cyttaria Cyttariaceae Digüeñe Edible wild nt espinosae species Flammulina Physalacriaceae Enoki Commercially 5α,8α-epidioxy- Yaoita et al. velutipes mushroom, cultivated (24S)-ergost-6-en- (1998); velvet shank, 3β-ol (0.9mg from isolation winter 4.1kg fw), and fungus (22E,24R)-ergosta- spectroscop 7,22-diene- ic 3β,5α,6α,9α-tetrol identificatio (0.2mg), n (22E,24R)-ergosta- 7,22-diene- 3β,5α,6β-triol (0.5mg), (24S)- ergost-7-ene- 3β,5α,6β-triol (0.2mg) Fistulina Fistulinaceae Beefsteak Edible wild nt hepatica polypore, ox species tongue Ganoderma Ganodermatac Lingzhi Commercially ergosta-4,7,22- Hirotani et lucidum eae exploited for triene-3,6-dione al. (1987); nutritional (314mg from isolation and dietary 5.32kg fw) and products spectroscop ic identificatio n 6α- Nishitoba et hydroxyergosta- al. (1988); 4,7,22-trien-3-one, isolation 6β- and hydroxyergosta- spectroscop 4,7,22-trien-3-one ic identificatio n Grifola Meripilaceae Maitake, Commercially (22E,24R)-ergosta- Ishizuka et frondosa hen-of-the- harvested 7,9(11),22-triene- al. (1997); woods from the wild 3β,5α,6β-triol isolation (2.7mg from 20kg and fw), (22E,24R)- spectroscop

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ergosta- ic 7,9(11),22-triene- identificatio 3β,5α,6α-triol n (1.5mg), 3β,5α- dihydroxy- (22E,24R)-ergosta- 7,22-dien-6-one (1.1mg), 3β,5α,9α- trihydroxy- (22E,24R)-ergosta- 7,22-dien-6-one (4.3mg), (22E,24R)-ergosta- 7,22-diene- 3β,5α,6α-triol (1.0mg), (22E,24R)-ergosta- 7,22-diene- 3β,5α,6β-triol (8.2mg), (22E,24R)-ergosta- 7,22-diene- 3β,5α,6β,9α-tetrol (4.7mg) Gyromitra Discinaceae False morel Commercially nt esculenta harvested from the wild/ Edible only after cooking Hericium Hericiaceae Lion’s mane, Commercially cerevisterol (73mg Takaishi et erinaceus monkey cultivated/ from 3.8kg dw), al. (1991); head Commercially cerevisterol-3- isolation harvested glucoside (29mg), and from the 3β,5α,9α- spectroscop wild/Used as trihydroxyergosta- ic food additive 7,22-dien-6-one identificatio (32mg) n Hydnum Hydnaceae Hedgehog Commercially nt repandum mushroom harvested from the wild Hygrophorus Hygrophoracea Gold-flecked Edible wild nt chrysodon e woodwax species Hypsizygus Tricholomatace Beech Commercially 5α,9α-epidioxy- Yaoita et al. tesselatus (H. ae mushroom cultivated/Edi 3β-hydroxy- (1998); marmoreus) ble only after (22E,24R)-ergosta- isolation cooking 7,22-dien-6-one and (8.4mg from 4.3kg spectroscop fw), 5α,9α- ic epidioxy-3β- identificatio hydroxy-(24S)- n ergost-7-en-6-one

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(4.2mg), 3β,5α,9α- trihydroxy-(24S)- ergost-7-en-6-one (1.0mg), 3β,5α,9α,14α- tetrahydroxy- (22E,24R)-ergosta- 7,22-dien-6-one (1.4mg), 3β,5α,9α- trihydroxy- (22E,24R)-ergosta- 7,22-dien-6-one (3.6mg), (24S)- ergost-7-ene- 3β,5α,6β-triol (12.8mg), (22E,24R)-ergosta- 7,22-diene- 3β,5α,6β-triol (38mg), (22E,24R)- ergosta-7,22- diene- 3β,5α,6α,9α-tetrol (1.4mg), ergosta- 7,24(28)-diene- 3β,5α,6β-triol (0.3mg) Kalaharituber Pezizaceae Kalahari Edible wild nt pfeilii truffle species Lactarius Russulaceae Saffron milk- Commercially nt deliciosus cap harvested from the wild Lactarius Russulaceae Orange milk- Edible wild nt determinus cap species Lactarius Russulaceae Edible wild nt salmonicolor species/Edible after cooking or pickling Lactarius Russulaceae Mild milk- Edible wild nt subdulcis cap species/Edible after cooking or pickling Lactarius Russulaceae Weeping Edible wild nt volemus milk-cap species/Edible (Lactefluus after cooking volemus) or pickling Laetiporus Polyporaceae Sulphur Edible wild nt sulphureus shelf, species chicken mushroom Leccinum Boletaceae Red-capped Edible wild nt

7 aurantiacum scaber stalk species Leccinum Boletaceae Birch bolete Edible wild nt scabrum species Leccinum Boletaceae Orange birch Edible wild nt versipelle bolete species Lentinula Marasmiaceae Shiitake Commercially 3β,5α,9α- Yaoita et al. edodes mushroom cultivated trihydroxy- (1998); (Lentinus (22E,24R)-23- isolation edodes) methylergosta- and 7,22-dien-6-one spectroscop (0.5mg from 4.7kg ic fw), 3β,5α,9α- identificatio trihydroxy-(24S)- n ergost-7-en-6-one (0.9mg), 3β,5α,9α,14α- tetrahydroxy- 22E,24R)-ergosta- 7,22-dien-6-one (1.0mg), 3β,5α,9α- trihydroxy- (22E,24R)-ergosta- 7,22,-dien-6-one (17.1mg), (22E,24R)-ergosta- 7,22-diene- 3β,5α,6α,9α-tetrol (1.3mg), (22E,24R)-ergosta- 7,22-diene- 3β,5α,6a-triol (0.6mg), (22E,24R)-ergosta- 7,9(11),22-triene- 3β,5α,6α-triol (0.6mg),(22E,24R)- ergosta-7,22- diene-3β,5α,6β- triol (3.3mg), (22E,24R)-ergosta- 7,22-diene- 3β,5α,6β,9α-tetrol (6.2mg) Lepista saeva Tricholomatace Field blewit, Edible only nt (L. personata, ae blue-leg after cooking Tricholoma personatum) Macrolepiota Agaricaceae Parasol Edible wild nt procera mushroom species Marasmius Marasmiaceae Fairy ring Edible wild nt oreades mushroom, species

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Scotch bonnet Morchella Morchellaceae Black morel Commercially nt conica var. harvested deliciosa from the wild /Edible only after cooking Morchella Morchellaceae Common Commercially nt esculenta morel, true harvested var. rotunda morel from the wild /Edible only after cooking Pholiota Strophariaceae Nameko, Usually eaten 3β,5α,9α- Yaoita et al. microspora butterscotch cooked trihydroxy-(24S)- (1998); (P. nameko) mushroom ergost-7-en-6-one isolation (1.0mg from 3.0kg and fw), 4 (0.7mg), spectroscop 3β,5α,9α- ic trihydroxy- identificatio (22E,24R)-ergosta- n 7,22-dien-6-one (3.0mg), (22E,24R)-ergosta- 7,22-diene- 3β,5α,6α,9α-tetrol (0.6mg), (24S)- ergost-7-ene- 3β,5α,6β-triol (0.2mg) Pleurotus Pleurotaceae Oyster Commercially 5α,9α-epidioxy- Yaoita et al. ostreatus mushroom cultivated/ 3β-hydroxy- (1998); Commercially (22E,24R)-ergosta- isolation harvested 7,22-dien-6-one and from the wild (1.9mg from 2.7kg spectroscop fw), 3β,5α,9α- ic trihydroxy-(24S)- identificatio ergost-7-en-6-one n (0.6mg), 3β,5α,9α,14α- tetrahydroxy- (22E,24R)-ergosta- 7,22-dien-6-one (0.4mg), 3β,5α,9α- trihydroxy- (22E,24R)-ergosta- 7,22-dien-6-one (3.5mg), (22E,24R)-ergosta- 7,22-diene- 3β,5α,6α,9α-tetrol (0.4mg), 3β,5α-

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dihydroxy- (22E,24R)-ergosta- 7,22-dien-6-one (0.2mg), (22E,24R)-ergosta- 7,22-diene- 3β,5α,6β-triol (13.4mg), (24S)- ergost-7-ene- 3β,5α,6β-triol (0.2mg)

0.07 μg 20E eq./g Findeisen dw (2004); EIA of ecdysteroid s (DBL-2 antiserum) Polyporus Polyporaceae Native Edible wild nt mylittae bread, species (Laccocephal blackfellow’s um mylittae) bread Polyporus Polyporaceae Dryad’s Edible wild nt squamosus saddle, species pheasant’s back mushroom Polyporus Polyporaceae Lumpy Only young polyporusterones Ohsawa et umbellatus bracket, fruiting bodies A (300mg from al. (1992); umbrella are edible 100kg dw), B isolation polypore (300mg), C and (26mg), D (8mg), E spectroscop (22mg), F (10mg) ic and G (10mg) identificatio n (20S,22R,24R)- Zhou et al. 16,22-epoxy- (2007); 3β,14α,23β,25- isolation tetrahydroxyergos and t-7-en-6-one (4mg spectroscop from 39.2kg dw), ic (23R,24R,25R)- identificatio 23,26-epoxy- n 3β,14α,21α,22α- tetrahydroxyergos t-7-en-6-one (8mg) Polyporoids A Sun &

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(2mg from 1kg Yasukawa dw), B (7mg) and C (2008); (3mg), isolation polyporusterones and A (10mg), B spectroscop (14mg), C (18mg) ic and G (3mg), identificatio ergosta-7,22- n diene-3β,5α,6β- triol (3mg) (22E,24R)-ergosta- Zhao et al. 6-en-3β,5α,6β- (2009); triol (0 – HPLC-MS 0.040mg/g dw), (22E,24R)-ergosta- 6,22-dien- 3β,5α,6β-triol (0 – 0.073mg/g dw), polyporusterone F (trace – 0.087mg/g dw) Ramariaceae Ramariaceae Coral fungi Edible wild nt spp. species Rhizopogon Rhizopogonace Edible wild nt luteolus ae species Russula laeta Russulaceae Edible wild nt (R. borealis) species Sparassis Sparassidaceae Cauliflower Edible wild nt crispa mushroom species Stropharia Strophariaceae White cap Commercially nt rugosoannula mushroom, cultivated ta burgundy mushroom Suillus Suillaceae Jersey cow Edible wild nt bovinus mushroom, species bovine bolete Suillus Suillaceae Weeping Edible wild nt granulatus bolete species Suillus luteus Suillaceae Slippery Jack, Edible wild nt sticky bun species Suillus Suillaceae Poorman’s Edible wild nt tomentosus slippery Jack species Tapinella Tapinellaceae Velvet roll- Only young paxillosterone Vokac et al. atrotomentos rim, velvet- fruiting bodies (356mg from (1998); a (Paxillus footed pax are edible 6.65kg fw), isolation atrotomentos paxillosterone and a) 20,22-p- spectroscop hydroxybenzyliden ic e acetal (5.5mg), identificatio atrotosterones A n

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(41mg), B (3.9mg) &C (5.5mg), 25- hydroxyatotostero nes A (11.9mg) & B (4.2mg), 20- hydroxyecdysone (41mg) Tremella Tremellaceae Snow fungus Commercially nt fuciformis cultivated Tricholoma Tricholomatace Matsutake Commercially nt matsutake ae harvested from the wild Tricholoma Tricholomatace Grey knight Edible wild nt terreum ae species Tuber Tuberaceae Black Commercially nt aestivum summer harvested truffle from the wild Tuber borchii Tuberaceae Whitish Commercially nt truffle harvested from the wild Tuber Tuberaceae Winter Commercially nt brumale truffle, harvested Muscat from the wild truffle Tuber Tuberaceae Chinese Commercially nt indicum black truffle harvested from the wild Tuber Tuberaceae Smooth Commercially nt macrosporu black truffle harvested m from the wild Tuber Tuberaceae Bagnoli Commercially nt mesentericu truffle harvested m from the wild Verpa Morchellaceae Early morel, Sometimes nt bohemica wrinkled toxic thimble-cap Volvariella Pluteaceae Straw Commercially nt volvaceae mushroom cultivated nt: not tested

-: negative

References

Findeisen E (2004) Ecdysteroide in der menschlichen Nahrung. Ph D Thesis, University of Marburg, FRG, pp 69

Hirotani M, Asaka I, Ino C, Furuya T, Shiro M (1987) Ganoderic acid derivatives and ergosta- 4,7,22-triene-3,6-dione from Ganoderma lucidum. Phytochemistry 26: 2797-2803

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Ishizuka T, Yaoita Y, Kikuchi M (1997) constituents from the fruit bodies of Grifola frondosa (Fr.) S.F. Gray. Chemical and Pharmaceutical Bulletin 45: 1756-1760

Kawagishi H, Katsumi R, Sazawa T, Mizuno T, Hagiwara T, Nakamura T (1988) Cytotoxic steroids from the mushroom Agaricus blazei. Phytochemistry 27: 2777-2779

Kawahara N, Sekita S, Satake M (1993) A novel dimeric steroid, calvasterone, from the fungus Calvatia cyathiformis. Chemical and Pharmaceutical Bulletin 41: 1318-1320

Kawahara N, Sekita S, Satake M (1994) Steroids from Calvatia cyathiformis. Phytochemistry 37: 213-215

Kawahara N, Sekita S, Satake M (1995) Two steroids from Calvatia cyathiformis. Phytochemistry 38: 947-950

Kovganko NV (1999) Ecdysteroids and related compounds in fungi. Chemistry of Natural Compounds 35: 597-611

Nishitoba T, Sato H, Oda K, Sakamura S (1988) Novel triterpenoids and a steroid from the fungus Ganoderma lucidum. Agricultural and Biological Chemistry 52: 211-216

Ohsawa T, Yukawa M, Takao C, Murayama M, Bando H (1992) Studies on constituents of fruit body of Polyporus umbellatus and their cytotoxic activity. Chemistry and Pharmaceutical Bulletin 40: 143-147

Sun Y, Yasukawa K (2008) New anti-inflammatory ergostane-type ecdysteroids from the sclerotium of Polyporus umbellatus. Bioorganic & Medicinal Chemistry Letters (doi: 10.1016/j.bmcl.2008.04.008)

Takaishi Y, Uda M, Ohashi T, Nakano K, Murakami K, Tomimatsu T (1991) Glycosides of derivatives from Hericum erinacens [sic]. Phytochemistry 30: 4117-4120

Vokáč K, Budĕšínsky M, Harmatha J, Píš J (1998) New ergostane type ecdysteroids from fungi. Ecdysteroid constituents of mushroom Paxillus atrotomentosus. Tetrahedron 54: 1657-1666

Yaoita Y, Amemiya K, Ohnuma H, Furumura K, Masaki A, Matsuki T, Kikuchi M (1998) Sterol constituents from five edible mushrooms. Chemical and Pharmaceutical Bulletin 46: 944-950

Zhao Y-Y, Cheng X-L, Zhang Y, Zhao Y, Lin R-C, Sun W-J (2009) Simultaneous determination of eight major steroids from Polyporus umbellatus by high-performance liquid chromatography coupled with mass spectrometry detections. Biomedical Chromatography (doi: 10.1002/bmc.1277)

Zhou W-W, Lin W-H, Guo S-X (2007) Two new polyporusterones isolated from the sclerotia of Polyporus umbellatus. Chemical and Pharmaceutical Bulletin 55: 1148-1150

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