Download PDF
Planta Medica International Open 2017; 4(01): e1-e7
DOI: 10.1055/s-0042-121608
Letter
Georg Thieme Verlag KG Stuttgart · New York

Inhibition of Degranulation of RBL-2H3 Cells by Extracts and Compounds from Armillaria ostoyae

Simon Merdivan
1   Institute of Pharmacy, Ernst-Moritz-Arndt University Greifswald, Greifswald, Germany
,
Kristina Jenett-Siems
2   Institute of Pharmacy, Freie Universität Berlin, Berlin, Germany
,
Karsten Siems
3   AnalytiCon Discovery GmbH, Potsdam, Germany
,
Timo Niedermeyer
4   Interfaculty Institute of Microbiology and Infection Medicine, Eberhard Karls University Tübingen, Tübingen, Germany
,
Michael J. Solis
5   Institute of Botany and Landscape Ecology, Ernst-Moritz-Arndt University Greifswald, Greifswald, Germany
6   Department of Natural Sciences, College of Science and Information Technology, Ateneo de Zamboanga University, Zamboanga City, Philippines
,
Martin Unterseher
5   Institute of Botany and Landscape Ecology, Ernst-Moritz-Arndt University Greifswald, Greifswald, Germany
,
Ulrike Lindequist
1   Institute of Pharmacy, Ernst-Moritz-Arndt University Greifswald, Greifswald, Germany
› Author Affiliations
Further Information

Publication History

received 22 July 2016
revised 04 November 2016

accepted 09 November 2016

Publication Date:
16 February 2017 (online)

   Permissions and Reprints

Abstract

Armillaria ostoyae (Romagn.) Herink is an edible honey mushroom from the family Physalacriaceae (Agaricales, Basidiomycota). Dichloromethane extracts of mushroom mycelium and fruiting bodies exhibited a significant degranulation inhibiting effect on RBL-2H3 cells using noncytotoxic concentrations. Bioactivity-guided fractionation of the mycelial dichloromethane extract led to the isolation of sesquiterpen aryl esters. Methyl linoleate could also be isolated. These substances were obtained from A. ostoyae for the first time, with one compound representing an undescribed natural product. Purified compounds melleolide H and J inhibited degranulation significantly. A. ostoyae could be a candidate for support of allergy treatments.

Key words

Armillaria ostoyae - Physalacriaceae - RBL-2H3 - sesquiterpene aryl esters - β-hexosaminidase assay - melleolide - cytotoxicity

Supporting Information

Graphics from RAxML and MrBayes for species determination of the mycelium of A. ostoyae (Fig. S1–S2), CD, ATIR, and UV spectra and 1H- as well as 1H,1H-COSY NMR spectra of 1 (Fig. S3–S8), and LC chromatograms of crude extracts and active fractions (Fig. S9–S11) are available as Supporting Information.

 

  • References

  • 1 Romagnesi H. Observations on Armillaria. Bull Trimest Soc Mycol Fr 1970; 86: 257-265
    PubMedGoogle Scholar
  • 2 Dobbertin M, Baltensweiler A, Rigling D. Tree mortality in an unmanaged mountain pine (Pinus mugo var. uncinata) stand in the Swiss National Park impacted by root rot fungi. For Ecol Manage 2001; 145: 79-89
    CrossrefPubMedGoogle Scholar
  • 3 Cleary MR, van der Kamp BJ, Morrison DJ. Effects of wounding and fungal infection with Armillaria ostoyae in three conifer species. II. Host response to the pathogen. Forest Pathol 2011; 42: 109-123
    PubMedGoogle Scholar
  • 4 Cleary MR, van der Kamp BJ, Morrison DJ. Effects of wounding and fungal infection with Armillaria ostoyae in three conifer species. I. Host response to abiotic wounding in non-infected roots. Forest Pathol 2012; 42: 100-108
    CrossrefPubMedGoogle Scholar
  • 5 Cruickshank M, Morrison DJ, Lalumière A. The interaction between competition in interior Douglas-fir plantations and disease caused by Armillaria ostoyae in British Columbia. For Ecol Manage 2009; 257: 443-452
    CrossrefPubMedGoogle Scholar
  • 6 Entry JA, Cromack jr. K, Hansen E, Waring R. Response of western coniferous seedlings to infection by Armillaria ostoyae under limited light and nitrogen. Phytophathology 1991; 81: 89-94
    CrossrefPubMedGoogle Scholar
  • 7 Pearce RB. Tansley Review No. 87. Antimicrobial defences in the wood of living trees. New Phytol 1996; 132: 203-233
    CrossrefPubMedGoogle Scholar
  • 8 Schmitt CL, Tatum ML. The Malheur national forest: Location of the worldʼs largest living organism [The humongous fungus]. Portland, Oregon: United States Department of Agriculture (USDA), Forest Service, Pacific Northwest Region; 2008
    Google Scholar
  • 9 Mihail JD. Bioluminescence patterns among North American Armillaria species. Fungal Biol 2015; 119: 528-537
    CrossrefPubMedGoogle Scholar
  • 10 Arnone A, Cardillo R, Nasini G. Structures of melleolides B–D, three antibacterial sesquiterpenoids from Armillaria mellea . Phytochemistry 1986; 25: 471-474
    CrossrefPubMedGoogle Scholar
  • 11 Arnone A, Cardillo R, Di Modugno V, Nasini G. Secondary mold metabolites. XXII. Isolation and structure elucidation of melledonals D and E and melleolides E–H, novel sesquiterpenoid aryl esters from Clitocybe elegans and Armillaria mellea . Gazz Chim Ital 1988; 118: 517-521
    PubMedGoogle Scholar
  • 12 Arnone A, Cardillo R, Nasini G. Secondary mould metabolites. Part 19. Structure elucidation and absolute configuration of melledonals B and C, novel antibacterial sesquiterpenoids from Armillaria mellea. X-ray molecular structure of melledonal C. J Chem Soc Perkin Trans I 1988; 503-510
    PubMedGoogle Scholar
  • 13 Chen CC, Kuo YH, Cheng JJ, Sung PJ, Ni CL, Chen CC, Shen CC. Three new sesquiterpene aryl esters from the mycelium of Armillaria mellea . Molecules 2015; 20: 9994-10003
    CrossrefPubMedGoogle Scholar
  • 14 Donnelly DMX, Sanada S, OʼReilly J, Polonsky J, Prangé T, Pascard C. Isolation and structure (X-ray analysis) of the orsellinate of armillol, a new antibacterial metabolite from Armillaria mellea . J Chem Soc Chem Commun 1982; 135-137
    PubMedGoogle Scholar
  • 15 Donnelly DMX, Hutchinson RM, Coveney D, Yonemitsu M. Sesquiterpene aryl esters from Armillaria mellea . Phytochemistry 1990; 29: 2569-2572
    CrossrefPubMedGoogle Scholar
  • 16 Donnelly DMX, Abe F, Coveney D, Fukuda N, OʼReilly J. Antibacterial sesquiterpene aryl esters from Armillaria mellea . J Nat Prod 1985; 48: 10-16
    CrossrefPubMedGoogle Scholar
  • 17 Liu TP, Chen CC, Shiao PY, Shieh HR, Chen YY, Chen YJ. Armillaridin, a honey medicinal mushroom, Armillaria mellea (higher basidiomycetes) component, inhibits differentiation and activation of human macrophages. Int J Med Mushrooms 2015; 17: 161-168
    CrossrefPubMedGoogle Scholar
  • 18 Midland SL, Izac RR, Wing RM, Zaki A, Munnecke D, Sims JJ. Melleolide, a new antibiotic from Armillaria mellea . Tetrahedron Lett 1982; 23: 2515-2518
    CrossrefPubMedGoogle Scholar
  • 19 Momose I, Sekizawa R, Hosokawa N, Iinuma H, Matsui S, Nakamura H, Naganawa H, Hamada M, Takeuchi T. Melleolides K, L and M, new melleolides from Armillaria mellea . J Antibiot 2000; 53: 137-143
    CrossrefPubMedGoogle Scholar
  • 20 Yang JS, Su YL, Wang YL, Feng XZ, Yu DQ, Liang XT. Two novel protoilludane norsesquiterpenoid esters, armillasin and armillatin, from Armillaria mellea . Planta Med 1991; 57: 478-480
    Article in Thieme ConnectPubMedGoogle Scholar
  • 21 Arnone A, Cardillo R, Nasini G. Secondary mould metabolites. XXIII. Isolation and structure elucidation of melleolides I and J and armellides A and B, novel sesquiterpenoid aryl esters from Armillaria novae-zelandiae . Gazz Chim Ital 1988; 118: 523-527
    PubMedGoogle Scholar
  • 22 Donnelly DMX, Konishi T, Dunne O, Cremin P. Sesquiterpene aryl esters from Armillaria tabescens . Phytochemistry 1997; 44: 1473-1478
    CrossrefPubMedGoogle Scholar
  • 23 Cell Degranulation – MeSH – NCBI. Available at. https://www.ncbi.nlm.nih.gov/mesh/?term=cell+degranulation Accessed October 5, 2016
    PubMedGoogle Scholar
  • 24 Mastuda H, Morikawa T, Ueda K, Yoshikawa M. Structural requirements of flavonoids for inhibition of antigen-induced degranulation, TNF-α and IL-4 production from RBL-2H3 cells. Bioorg Med Chem 2002; 10: 3123-3128
    CrossrefPubMedGoogle Scholar
  • 25 Kobori H, Sekiya A, Suzuki T, Choi JH, Hirai H, Kawagishi H. Bioactive sesquiterpene aryl esters from the culture broth of Armillaria sp. J Nat Prod 2015; 78: 163-167
    CrossrefPubMedGoogle Scholar
  • 26 Appendino G, Gariboldi P, Menichini F. Oxygenated nerolidol derivatives from Artemisia alba . Phytochemistry 1985; 24: 1729-1733
    CrossrefPubMedGoogle Scholar
  • 27 Yang JS, Su YL, Wang YL, Feng XZ, Yu DQ, Liang XT. Chemical constituents of Armillaria mellea mycelium. V. Isolation and characterization of armillarilin and armillarinin. Yao Xue Xue Bao 1990; 25: 24-28
    PubMedGoogle Scholar
  • 28 Bohnert M, Nützmann HW, Schroeckh V, Horn F, Dahse HM, Brakhage AA, Hoffmeister D. Cytotoxic and antifungal activities of melleolide antibiotics follow dissimilar structure – activity relationships. Phytochemistry 2014; 105: 101-108
    CrossrefPubMedGoogle Scholar
  • 29 Bohnert M, Miethbauer S, Dahse HM, Ziemen J, Nett M, Hoffmeister D. In vitro cytotoxicity of melleolide antibiotics: structural and mechanistic aspects. Bioorg Med Chem Lett 2011; 21: 2003-2006
    CrossrefPubMedGoogle Scholar
  • 30 Misiek M, Williams J, Schmich K, Hüttel W, Merfort I, Salomon CE, Aldrich CC, Hoffmeister D. Structure and cytotoxicity of arnamial and related fungal sesquiterpene aryl esters. J Nat Prod 2009; 72: 1888-1891
    CrossrefPubMedGoogle Scholar
  • 31 Abramson J, Pecht I. Clustering the mast cell function-associated antigen (MAFA) leads to tyrosine phosphorylation of p62Dok and SHIP and affects RBL-2H3 cell cycle. Immunol Lett 2002; 82: 23-28
    CrossrefPubMedGoogle Scholar
  • 32 Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc Natl Acad Sci U S A 2012; 109: 6241-6246
    CrossrefPubMedGoogle Scholar
  • 33 Solis MJL, Yurkov A, dela Cruz TE, Unterseher M. Leaf-inhabiting endophytic yeasts are abundant but unevenly distributed in three Ficus species from botanical garden greenhouses in Germany. Mycol Prog 2015; 14: 1019
    CrossrefPubMedGoogle Scholar
  • 34 Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. GenBank. Nucleic Acids Res 2012; 41: D36-D42
    CrossrefPubMedGoogle Scholar
  • 35 Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid mulitple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002; 30: 3059-3066
    CrossrefPubMedGoogle Scholar
  • 36 Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30: 772-780
    CrossrefPubMedGoogle Scholar
  • 37 Maddison WP, Madisson DR. Mesquite: a modular system for evolutionary analysis, Version 2.75. Available at. http://mesquiteproject.org
    PubMedGoogle Scholar
  • 38 Gouy M, Guindon S, Gascuel O. SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010; 27: 221-224
    CrossrefPubMedGoogle Scholar
  • 39 Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30: 2725-2729
    CrossrefPubMedGoogle Scholar
  • 40 Page RD. TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 1996; 12: 357-358
    PubMedGoogle Scholar
  • 41 Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001; 17: 754-755
    CrossrefPubMedGoogle Scholar
  • 42 Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30: 1312-1313
    CrossrefPubMedGoogle Scholar
  • 43 Silvestro D, Michalak I. raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 2012; 12: 335-337
    CrossrefPubMedGoogle Scholar