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Interkingdom signaling by structurally related cyanobacterial and algal secondary metabolites

Abstract

Several groups of structurally-related compounds, comprised of either five or six-membered ring structures with attached lipophilic carbon chains and in some cases possessing halogen atoms, have been isolated from various marine algae and filamentous cyanobacteria. The related compounds considered in the present work include the coibacins, laurenciones, honaucins, malyngamides and the tumonoic acids. Members of all of these compound families were assayed and found to inhibit the production of nitric oxide in lipopolysaccharides-stimulated macrophages, indicating their anti-inflammatory potential. In addition, several of these same marine natural products were found to inhibit quorum sensing mediated phenotypes in Vibrio harveyi BB120 and/or Escherichia coli JB525. The mechanism and evolutionary significance for inhibition of these cellular processes in prokaryotic and eukaryotic systems are speculated on and discussed.

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References

  • Adcock IM, Caramori G, Chung KF (2008) New targets for drug development in asthma. The Lancet 372(9643):1073–1087

    Article  CAS  Google Scholar 

  • Aelterman W, De Kimpe N, Kalinin V (1997) One-step synthesis of Laurencione. J Nat Prod 60:385–386

    Article  CAS  Google Scholar 

  • Anderson JB, Heydorn A, Hentzer M et al (2001) gfp-Based N-acyl-homoserine-lactone sensor systems for detection of bacterial communication. Appl Environ Microbiol 67:575–585

    Article  Google Scholar 

  • Balunas MJ, Grosso MF,Villa FA et al. (2012) Coibacins A–D, new anti-leishmanial polyketides with intriguing biosynthetic origins. Org Lett (in preparation)

  • Bernart MW, Gerwick WH, Corcoran EE et al (1991) Laurencione, A Heterocycle From The Red Alga Laurencia spectabllis. Phytochemistry 31:1273–1276

    Article  Google Scholar 

  • Cardellina JH II, Marner FJ, Moore RE (1979) Malyngamide A, a novel chlorinated metabolite of the marine cyanophyte Lyngbya majuscula. J Am Chem Soc 101:240–242

    Article  CAS  Google Scholar 

  • Choi H, Mascuch S, Villa FA et al. (2012) Honaucins A–C, potent inhibitors of inflammation and bacterial quorum sensing: synthetic derivatives and structure-activity relationships. Chem Biol (in press)

  • Clark BR, Engene N, Teasdale ME et al (2008) Natural Products Chemistry and Taxonomy of the Marine Cyanobacterium Blennothrix cantharidosmum. J Nat Prod 71:1530–1537

    PubMed  Article  CAS  Google Scholar 

  • Drenkard E, Ausubel FM (2002) Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416(6882):740–743

    PubMed  Article  CAS  Google Scholar 

  • Engene N, Choi H, Esquenazi E (2011) Phylogeny-guided isolation of ethyl tumonoate A from the marine cyanobacterium cf. Oscillatoria margaritifera. J Nat Prod 74:1737–1743

    Article  CAS  Google Scholar 

  • Engene N, Rottacker EC, Kaštovsky′ J et al. (2012) Moorea producta gen. nov., sp. nov. and Moorea bouillonii comb. nov., tropical marine cyanobacteria rich in bioactive secondary metabolites Int J Syst Evol Microbiol (in press)

  • Galloway WRDJ, Hodgkinson JT, Bowden SD et al (2011) Quorum Sensing in Gram-Negative Bacteria: Small-Molecule Modulation of AHL and AI-2 Quorum Sensing Pathways. Chem Rev 111:28–67

    PubMed  Article  CAS  Google Scholar 

  • Grivennikov SI, Greten FR, Karin M (2010) Immunity, Inflammation, and Cancer. Cell 140:883–899

    PubMed  Article  CAS  Google Scholar 

  • Gu L, Wang B, Kulkarni A et al (2009a) Metamorphic enzyme assembly in polyketide diversification. Nature 459(7247):731–735

    PubMed  Article  CAS  Google Scholar 

  • Gu L, Wang B, Kulkarni A et al (2009b) Polyketide decarboxylative chain termination preceded by o-sulfonation in curacin a biosynthesis. J Am Chem Soc 131(44):16033–16035

    PubMed  Article  CAS  Google Scholar 

  • Harrigan GG, Luesch H, Yoshida WH et al (1999) Tumonoic Acids, Novel Metabolites from a Cyanobacterial Assemblage of Lyngbya majuscula and Schizothrix calcicola. J Nat Prod 62:464–467

    PubMed  Article  CAS  Google Scholar 

  • Kravchenko VV, Kaufmann GF, Mathison JC et al (2008) Modulation of gene expression via disruption of NF-kappaB signaling by a bacterial small molecule. Science 321(5886):259–263

    PubMed  Article  CAS  Google Scholar 

  • Kwan JC, Teplitski M, Gunasekera SP et al (2010) Isolation and Biological Evaluation of 8-epi-Malyngamide C from the Floridian Marine Cyanobacterium Lyngbya majuscula. J Nat Prod 73:463–466

    PubMed  Article  CAS  Google Scholar 

  • Li WI, Berman FW, Okino T et al (2001) Antillatoxin is a marine cyanobacterial toxin that potently activates voltage-gated sodium channels. PNAS 98:7599–7604

    PubMed  Article  CAS  Google Scholar 

  • Lowery CA, McKenzie KM, Qi L et al (2005) Quorum sensing in Vibrio harveyi: probing the specificity of the LuxP binding site. Bioorg Med Chem Lett 15:2395–2398

    PubMed  Article  CAS  Google Scholar 

  • Malloy KL, Villa FA, Engene N et al (2011) Malyngamide 2, an Oxidized Lipopeptide with Nitric Oxide Inhibiting Activity from a Papua New Guinea Marine Cyanobacterium. J Nat Prod 74:95–98

    PubMed  Article  CAS  Google Scholar 

  • Mo S, Krunic A, Chlipala G, Orjala J (2009) Antimicrobial Ambiguine Isonitriles from the Cyanobacterium Fischerella ambigua. J Nat Prod 72:894–899

    PubMed  Article  CAS  Google Scholar 

  • Nagarajan M, Maruthanayagam V, Sundararaman M (2012) A review of pharmacological and toxicological potentials of marine cyanobacterial metabolites. J Appl Toxicol 32:153–185

    PubMed  Article  CAS  Google Scholar 

  • Nagle DG, Paul VJ (1999) Production of secondary metabolites by filamentous tropical marine cyanobacteria: ecological functions of the compounds. J Phycol 35:1529–8817

    Google Scholar 

  • Ng WL, Bassler BL (2009) Bacterial Quorum-Sensing Network Architectures. Annu Rev Genet 43:197–222

    PubMed  Article  CAS  Google Scholar 

  • Ni N, Li M, Wang J et al (2009) Inhibitors and antagonists of bacterial quorum sensing. Med Res Rev 29:65–124

    PubMed  Article  CAS  Google Scholar 

  • Pappas KM, Winans SC (2003) A LuxR-type regulator from Agrobacterium tumefaciens elevates Ti plasmid copy number by activating transcription of plasmid replication genes Mol Micro 48:1059–1073

    CAS  Google Scholar 

  • Teasdale M, Liu J, Wallace J et al (2009) Secondary metabolites produced by a marine Halobacillus salinus that inhibit quorum sensing controlled phenotypes in Gram-negative bacteria. Appl Environ Microbiol 75:567–572

    PubMed  Article  CAS  Google Scholar 

  • Telford G, Wheeler D, Williams P et al (1998) The Pseudomonas aeruginosa quorum-sensing signal molecule N-(3-oxododecanoyl)-l-homoserine lactone has immunomodulatory activity. Infect Immun 66:36–42

    PubMed  CAS  Google Scholar 

  • Teng SW, Schaffer JN, Tu KC et al (2011) Active regulation of receptor ratios controls integration of quorum-sensing signals in Vibrio harveyi. Mol Syst Biol 7:491–505

    PubMed  Article  Google Scholar 

  • Thomsen TR, Hall-Stoodley L, Moser C et al. (2011) The role of bacterial biofilms in infections of catheters and shunts. In : Bjarnsholt T, Østrup Jensen P, Moser C, Høiby N (ed) Biofilm infections 91–109

  • Tidgewell K, Clark BR, Gerwick WH (2010) The natural products chemistry of cyanobacteria. In: Mander L, Lui HW (eds) Comprehensive natural products II chemistry and biology, vol 2. Elsevier, Oxford, pp 141–188

    Chapter  Google Scholar 

  • Villa FA, Lieske K, Gerwick L (2010) Selective MyD88-dependent pathway inhibition by the cyanobacterial natural product malyngamide F acetate. Eur J Pharmacol 629:140–146

    PubMed  Article  CAS  Google Scholar 

  • Zhang R, Pappas T, Brace J et al (2002) Structure of a bacterial quorum- sensing transcription factor complexed with pheromone and DNA. Nature 417:971–974

    PubMed  Article  CAS  Google Scholar 

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Acknowledgments

This research was partially funded by the International Cooperative Biodiversity grant (U01 TW006634), the Ledger Benbough Foundation to L.G, NIH/FIC International Research Scientist Development Award (IRSDA) to M.J.B., NIGMS Training grant in marine biotechnology to S.M., NIH/NIGMS Institutional Research and Academic Career Development Award (IRACDA) fellowship to F.V. and an E.W Scripps Fellowship to P.B.

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Correspondence to Lena Gerwick.

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Gerwick, L., Boudreau, P., Choi, H. et al. Interkingdom signaling by structurally related cyanobacterial and algal secondary metabolites. Phytochem Rev 12, 459–465 (2013). https://doi.org/10.1007/s11101-012-9237-5

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  • DOI: https://doi.org/10.1007/s11101-012-9237-5

Keywords

  • Quorum sensing
  • Anti-inflammatory
  • Lactone
  • Acyl chain
  • Marine natural products