Top

Published in:

01-04-2013 | Original Paper

Marine-derived fungal sesterterpenes, ophiobolins, inhibit biofilm formation of Mycobacterium species

Authors: Masayoshi Arai, Hiroki Niikawa, Motomasa Kobayashi

Published in: Journal of Natural Medicines | Issue 2/2013

Abstract

Biofilm formation in pathogenic bacteria defends them from antibiotics and the host’s immune system. In the course of our search for new inhibitors of biofilm formation in Mycobacterium species, we isolated the sesterterpenes ophiobolin K (1), 6-epi-ophiobolin K (2), and 6-epi-ophiobolin G (3) from a culture of marine-derived fungus of Emericella variecolor. Ophiobolins 1–3 inhibited biofilm formation of Mycobacterium smegmatis with MICs of 4.1–65 μM, whereas these compounds did not show antimicrobial activity at the concentrations that showed anti-biofilm formation activity. Ophiobolin K (1) was also effective against the biofilm formation of M. bovis BCG and was able to restore the antimicrobial activity of isoniazid against M. smegmatis by inhibiting biofilm formation.

Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322PubMedCrossRef

Donlan RM (2000) Role of biofilms in antimicrobial resistance. ASAIO J 46:S47–S52PubMedCrossRef

Stewart PS, Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358:135–138PubMedCrossRef

Leid JG, Willson CJ, Shirtliff ME, Hassett DJ, Parsek MR, Jeffers AK (2005) The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-γ-mediated macrophage killing. J Immunol 175:7512–7518PubMed

Leid JG, Shirtliff ME, Costerton JW, Stoodley P (2002) Human leukocytes adhere to, penetrate, and respond to Staphylococcus aureus biofilms. Infect Immun 70:6339–6345PubMedCrossRef

Idemyor V (2007) HIV and tuberculosis coinfection: inextricably linked liaison. J Natl Med Assoc 99:1414–1419PubMed

Marsollier L, Aubry J, Coutanceau E, André JS, Small PL, Milon G, Legras P, Guadagnini S, Carbonnelle B, Cole ST (2005) Colonization of the salivary glands of Naucoris cimicoides by Mycobacterium ulcerans requires host plasmatocytes and a macrolide toxin, mycolactone. Cell Microbiol 7:935–943PubMedCrossRef

Wu CW, Schmoller SK, Bannantine JP, Eckstein TM, Inamine JM, Livesey M, Albrecht R, Talaat AM (2009) A novel cell wall lipopeptide is important for biofilm formation and pathogenicity of Mycobacterium avium subspecies paratuberculosis. Microb Pathog 46:222–230PubMedCrossRef

Ojha A, Anand M, Bhatt A, Kremer L, Jacobs WR Jr, Hatfull GF (2005) GroEL1: a dedicated chaperone involved in mycolic acid biosynthesis during biofilm formation in mycobacteria. Cell 123:861–873PubMedCrossRef

10.

Ojha AK, Baughn AD, Sambandan D, Hsu T, Trivelli X, Guerardel Y, Alahari A, Kremer L, Jacobs WR Jr, Hatfull GF (2008) Growth of Mycobacterium tuberculosis biofilms containing free mycolic acids and harbouring drug-tolerant bacteria. Mol Microbiol 69:164–174PubMedCrossRef

11.

Ojha AK, Trivelli X, Guerardel Y, Kremer L, Hatfull GF (2010) Enzymatic hydrolysis of trehalose dimycolate releases free mycolic acids during mycobacterial growth in biofilms. J Biol Chem 285:17380–17389PubMedCrossRef

12.

Ishida S, Arai M, Niikawa H, Kobayashi M (2011) Inhibitory effect of cyclic trihydroxamate siderophore, desferrioxamine E, on the biofilm formation of Mycobacterium species. Biol Pharm Bull 34:917–920PubMedCrossRef

13.

Recht J, Kolter R (2001) Glycopeptidolipid acetylation affects sliding motility and biofilm formation in Mycobacterium smegmatis. J Bacteriol 183:5718–5724PubMedCrossRef

14.

Toutain-Kidd CM, Kadivar SC, Bramante CT, Bobin SA, Zegans ME (2009) Polysorbate 80 inhibition of Pseudomonas aeruginosa biofilm formation and its cleavage by the secreted lipase LipA. Antimicrob Agents Chemother 53:136–145PubMedCrossRef

15.

Arai M, Sobou M, Vilchéze C, Baughn A, Hashizume H, Pruksakorn P, Ishida S, Matsumoto M, Jacobs WR Jr, Kobayashi M (2008) Halicyclamine A, a marine spongean alkaloid as a lead for anti-tuberculosis agent. Bioorg Med Chem 16:6732–6736PubMedCrossRef

16.

Singh SB, Smith JL, Sabnis GS, Dombrowski AW, Schaeffer JM, Goetz MA, Bills GF (1991) Structure and conformation of ophiobolin K and 6-epiophiobolin K from Aspergillus ustus as a nematocidal agent. Tetrahedron 47:6931–6938CrossRef

17.

Wei H, Itoh T, Kinoshita M, Nakai Y, Kurotaki M, Kobayashi M (2004) Cytotoxic sesterterpenes, 6-epi-ophiobolin G and 6-epi-ophiobolin N, from marine derived fungus Emericella variecolor GF10. Tetrahedron 60:6015–6019CrossRef

18.

Evidente A, Andolfi A, Cimmino A, Vurro M, Fracchiolla M, Charudattan R (2006) Herbicidal potential of ophiobolins produced by Drechslera gigantea. J Agric Food Chem 54:1779–1783PubMedCrossRef

19.

Au TK, Chick WS, Leung PC (2000) The biology of ophiobolins. Life Sci 67:733–742PubMedCrossRef

20.

Leung PC, Taylor WA, Wang JH, Tipton CL (1984) Ophiobolin A. A natural product inhibitor of calmodulin. J Biol Chem 259:2742–2747PubMed

Title: Marine-derived fungal sesterterpenes, ophiobolins, inhibit biofilm formation of Mycobacterium species
Authors: Masayoshi Arai
Hiroki Niikawa
Motomasa Kobayashi
Publication date: 01-04-2013
Publisher: Springer Japan
Published in: Journal of Natural Medicines / Issue 2/2013
Print ISSN: 1340-3443
Electronic ISSN: 1861-0293
DOI: https://doi.org/10.1007/s11418-012-0676-5

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Marine-derived fungal sesterterpenes, ophiobolins, inhibit biofilm formation of Mycobacterium species

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2013

Two new cembranoids from the leaves of Croton longissimus Airy Shaw

Sanjecumins A and B: new limonoids from Sandoricum koetjape

Four new myrsinol diterpenes from Euphorbia prolifera

New cycloartane glycosides from the aerial part of Thalictrum fortunei

Hirtionosides A–C, gallates of megastigmane glucosides, 3-hydroxyoctanoic acid glucosides and a phenylpropanoid glucoside from the whole plants of Euphorbia hirta

Regular ingestion of cinnamomi cortex pulveratus offers gastroprotective activity in mice