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The role of laccase in prostaglandin production by Cryptococcus neoformans

dc.contributor.authorErb-Downward, John R.en_US
dc.contributor.authorNoggle, Rachael M.en_US
dc.contributor.authorWilliamson, Peter R.en_US
dc.contributor.authorHuffnagle, Gary B.en_US
dc.date.accessioned2010-06-01T19:54:42Z
dc.date.available2010-06-01T19:54:42Z
dc.date.issued2008-06en_US
dc.identifier.citationErb-Downward, John R.; Noggle, Rachael M.; Williamson, Peter R.; Huffnagle, Gary B. (2008). "The role of laccase in prostaglandin production by Cryptococcus neoformans ." Molecular Microbiology 68(6): 1428-1437. <http://hdl.handle.net/2027.42/73041>en_US
dc.identifier.issn0950-382Xen_US
dc.identifier.issn1365-2958en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/73041
dc.identifier.urihttp://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=18410494&dopt=citationen_US
dc.description.abstractRecently, it has been demonstrated that the opportunistic fungal pathogen Cryptococcus neoformans can synthesize authentic immunomodulatory prostaglandins. The mechanism by which this takes place is unclear as there is no cyclooxygenase homologue in the cryptococcal genome. In this study, we show that cryptococcal production of both PGE 2 and PGF 2α can be chemically inhibited by caffeic acid, resveratrol and nordihydroguaiaretic acid. These polyphenolic molecules are frequently used as inhibitors of lipoxygenase enzymes; however, blast searches of the cryptococcal genome were unable to identify any homologues of mammalian, plant or fungal lipoxygenases. Next we investigated cryptococcal laccase, an enzyme known to bind polyphenols, and found that either antibody depletion or genetic deletion of the primary cryptococcal laccase ( lac1 δ) resulted in a loss of cryptococcal prostaglandin production. To determine how laccase is involved, we tested recombinant laccase activity on the prostaglandin precursors, arachidonic acid (AA), PGG 2 and PGH 2 . Using mass spectroscopy we determined that recombinant Lac1 does not modify AA or PGH 2 , but does have a marked activity toward PGG 2 converting it to PGE 2 and 15-keto-PGE 2 . These data demonstrate a critical role for laccase in cryptococcal prostaglandin production, and provides insight into a new and unique fungal prostaglandin pathway.en_US
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dc.publisherBlackwell Publishing Ltden_US
dc.rightsJournal compilation © 2008 Blackwell Publishingen_US
dc.titleThe role of laccase in prostaglandin production by Cryptococcus neoformansen_US
dc.typeArticleen_US
dc.subject.hlbsecondlevelMicrobiology and Immunologyen_US
dc.subject.hlbtoplevelScienceen_US
dc.description.peerreviewedPeer Revieweden_US
dc.contributor.affiliationumDivision of Pulmonary and Critical Care Medicine, Department of Internal Medicine, University of Michigan Medical School, Ann Arbor, MI 48109-0642, USA.en_US
dc.contributor.affiliationumDepartment of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI 48109-0642, USA.en_US
dc.contributor.affiliationotherSection of Infectious Diseases, Department of Medicine, University of Illinois at Chicago, Chicago, IL, USA.en_US
dc.identifier.pmid18410494en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/73041/1/j.1365-2958.2008.06245.x.pdf
dc.identifier.doi10.1111/j.1365-2958.2008.06245.xen_US
dc.identifier.sourceMolecular Microbiologyen_US
dc.identifier.citedreferenceAngeli, V., Faveeuw, C., Roye, O., Fontaine, J., Teissier, E., Capron, A., et al. ( 2001 ) Role of the parasite-derived prostaglandin D2 in the inhibition of epidermal Langerhans cell migration during schistosomiasis infection. J Exp Med 193: 1135 – 1147.en_US
dc.identifier.citedreferenceCasa, R., D'Annibale, A., Pieruccetti, F., Stazi, S.R., Giovannozzi Sermanni, G., and Lo Cascio, B. ( 2003 ) Reduction of the phenolic components in olive-mill wastewater by an enzymatic treatment and its impact on durum wheat ( Triticum durum Desf.) germinability. Chemosphere 50: 959 – 966.en_US
dc.identifier.citedreferenceChou, W.L., Chuang, L.M., Chou, C.C., Wang, A.H., Lawson, J.A., FitzGerald, G.A., and Chang, Z.F. ( 2007 ) Identification of a novel prostaglandin reductase reveals the involvement of prostaglandin E2 catabolism in regulation of peroxisome proliferator-activated receptor gamma activation. J Biol Chem 282: 18162 – 18172.en_US
dc.identifier.citedreferenceCox, G.M., McDade, H.C., Chen, S.C., Tucker, S.C., Gottfredsson, M., Wright, L.C., et al. ( 2001 ) Extracellular phospholipase activity is a virulence factor for Cryptococcus neoformans. Mol Microbiol 39: 166 – 175.en_US
dc.identifier.citedreferenceErb-Downward, J.R., and Huffnagle, G.B. ( 2006 ) Role of oxylipins and other lipid mediators in fungal pathogenesis. Future Microbiol 1: 219 – 227.en_US
dc.identifier.citedreferenceErb-Downward, J.R., and Huffnagle, G.B. ( 2007 ) Cryptococcus neoformans produces authentic prostaglandin E2 without a cyclooxygenase. Eukaryot Cell 6: 346 – 350.en_US
dc.identifier.citedreferenceErb-Downward, J.R., and Noverr, M.C. ( 2007 ) Characterization of prostaglandin E2 production by Candida albicans. Infect Immun 75: 3498 – 3505.en_US
dc.identifier.citedreferenceGomez, B.L., and Nosanchuk, J.D. ( 2003 ) Melanin and fungi. Curr Opin Infect Dis 16: 91 – 96.en_US
dc.identifier.citedreferenceHarris, S.G., Padilla, J., Koumas, L., Ray, D., and Phipps, R.P. ( 2002 ) Prostaglandins as modulators of immunity. Trends Immunol 23: 144 – 150.en_US
dc.identifier.citedreferenceHerve, M., Angeli, V., Pinzar, E., Wintjens, R., Faveeuw, C., Narumiya, S., et al. ( 2003 ) Pivotal roles of the parasite PGD2 synthase and of the host D prostanoid receptor 1 in schistosome immune evasion. Eur J Immunol 33: 2764 – 2772.en_US
dc.identifier.citedreferenceKarlsson, S., Holmbom, B., Spetz, P., Mustranta, A., and Buchert, J. ( 2001 ) Reactivity of Trametes laccases with fatty and resin acids. Appl Microbiol Biotechnol 55: 317 – 320.en_US
dc.identifier.citedreferenceKilunga Kubata, B., Eguchi, N., Urade, Y., Yamashita, K., Mitamura, T., Tai, K., et al. ( 1998 ) Plasmodium falciparum produces prostaglandins that are pyrogenic, somnogenic, and immunosuppressive substances in humans. J Exp Med 188: 1197 – 1202.en_US
dc.identifier.citedreferenceKimura, Y., Okuda, H., and Arichi, S. ( 1985 ) Effects of stilbenes on arachidonate metabolism in leukocytes. Biochim Biophys Acta 834: 275 – 278.en_US
dc.identifier.citedreferenceKimura, Y., Okuda, H., and Kubo, M. ( 1995 ) Effects of stilbenes isolated from medicinal plants on arachidonate metabolism and degranulation in human polymorphonuclear leukocytes. J Ethnopharmacol 45: 131 – 139.en_US
dc.identifier.citedreferenceKoshihara, Y., Neichi, T., Murota, S., Lao, A., Fujimoto, Y., and Tatsuno, T. ( 1984 ) Caffeic acid is a selective inhibitor for leukotriene biosynthesis. Biochim Biophys Acta 792: 92 – 97.en_US
dc.identifier.citedreferenceKubata, B.K., Duszenko, M., Kabututu, Z., Rawer, M., Szallies, A., Fujimori, K., et al. ( 2000 ) Identification of a novel prostaglandin f(2alpha) synthase in Trypanosoma brucei. J Exp Med 192: 1327 – 1338.en_US
dc.identifier.citedreferenceKubata, B.K., Kabututu, Z., Nozaki, T., Munday, C.J., Fukuzumi, S., Ohkubo, K., et al. ( 2002 ) A key role for old yellow enzyme in the metabolism of drugs by Trypanosoma cruzi. J Exp Med 196: 1241 – 1251.en_US
dc.identifier.citedreferenceLamacka, M., and Sajbidor, J. ( 1995 ) The occurrence of prostaglandins and related compounds in lower organisms. Prostaglandins Leukot Essent Fatty Acids 52: 357 – 364.en_US
dc.identifier.citedreferenceLeonowicz, A., Cho, N.S., Luterek, J., Wilkolazka, A., Wojtas-Wasilewska, M., Matuszewska, A., et al. ( 2001 ) Fungal laccase: properties and activity on lignin. J Basic Microbiol 41: 185 – 227.en_US
dc.identifier.citedreferenceLi, B.H., Ma, X.F., Wang, Y., and Tian, W.X. ( 2005 ) Structure-activity relationship of polyphenols that inhibit fatty acid synthase. J Biochem (Tokyo) 138: 679 – 685.en_US
dc.identifier.citedreferenceLiu, L., Tewari, R.P., and Williamson, P.R. ( 1999 ) Laccase protects Cryptococcus neoformans from antifungal activity of alveolar macrophages. Infect Immun 67: 6034 – 6039.en_US
dc.identifier.citedreferenceNoverr, M.C., Erb-Downward, J.R., and Huffnagle, G.B. ( 2003a ) Production of eicosanoids and other oxylipins by pathogenic eukaryotic microbes. Clin Microbiol Rev 16: 517 – 533.en_US
dc.identifier.citedreferenceNoverr, M.C., Cox, G.M., Perfect, J.R., and Huffnagle, G.B. ( 2003b ) Role of PLB1 in pulmonary inflammation and cryptococcal eicosanoid production. Infect Immun 71: 1538 – 1547.en_US
dc.identifier.citedreferenceNoverr, M.C., and Huffnagle, G.B. ( 2004 ) Regulation of Candida albicans morphogenesis by fatty acid metabolites. Infect Immun 72: 6206 – 6210.en_US
dc.identifier.citedreferenceNoverr, M.C., Phare, S.M., Toews, G.B., Coffey, M.J., and Huffnagle, G.B. ( 2001 ) Pathogenic yeasts Cryptococcus neoformans and Candida albicans produce immunomodulatory prostaglandins. Infect Immun 69: 2957 – 2963.en_US
dc.identifier.citedreferenceNoverr, M.C., Toews, G.B., and Huffnagle, G.B. ( 2002 ) Production of prostaglandins and leukotrienes by pathogenic fungi. Infect Immun 70: 400 – 402.en_US
dc.identifier.citedreferencePinto, M.C., Garcia-Barrado, J.A., and Macias, P. ( 1999 ) Resveratrol is a potent inhibitor of the dioxygenase activity of lipoxygenase. J Agric Food Chem 47: 4842 – 4846.en_US
dc.identifier.citedreferenceSalari, H., Braquet, P., and Borgeat, P. ( 1984 ) Comparative effects of indomethacin, acetylenic acids, 15-HETE, nordihydroguaiaretic acid and BW755C on the metabolism of arachidonic acid in human leukocytes and platelets. Prostaglandins Leukot Med 13: 53 – 60.en_US
dc.identifier.citedreferenceShea, J.M., and Del Poeta, M. ( 2006 ) Lipid signaling in pathogenic fungi. Curr Opin Microbiol 9: 352 – 358.en_US
dc.identifier.citedreferenceSmith, W.L., DeWitt, D.L., and Garavito, R.M. ( 2000 ) Cyclooxygenases: structural, cellular, and molecular biology. Annu Rev Biochem 69: 145 – 182.en_US
dc.identifier.citedreferenceSmith, C.A., Want, E.J., O'Maille, G., Abagyan, R., and Siuzdak, G. ( 2006 ) XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal Chem 78: 779 – 787.en_US
dc.identifier.citedreferenceTanaka, E., Niiyama, S., Sato, S., Yamada, A., and Higashi, H. ( 2003 ) Arachidonic acid metabolites contribute to the irreversible depolarization induced by in vitro ischemia. J Neurophysiol 90: 3213 – 3223.en_US
dc.identifier.citedreferenceTsitsigiannis, D.I., and Keller, N.P. ( 2006 ) Oxylipins act as determinants of natural product biosynthesis and seed colonization in Aspergillus nidulans. Mol Microbiol 59: 882 – 892.en_US
dc.identifier.citedreferenceTsitsigiannis, D.I., and Keller, N.P. ( 2007 ) Oxylipins as developmental and host-fungal communication signals. Trends Microbiol 15: 109 – 118.en_US
dc.identifier.citedreferenceTsitsigiannis, D.I., Bok, J.W., Andes, D., Nielsen, K.F., Frisvad, J.C., and Keller, N.P. ( 2005a ) Aspergillus cyclooxygenase-like enzymes are associated with prostaglandin production and virulence. Infect Immun 73: 4548 – 4559.en_US
dc.identifier.citedreferenceTsitsigiannis, D.I., Kowieski, T.M., Zarnowski, R., and Keller, N.P. ( 2005b ) Three putative oxylipin biosynthetic genes integrate sexual and asexual development in Aspergillus nidulans. Microbiology 151: 1809 – 1821.en_US
dc.identifier.citedreferenceValderrama, B., Oliver, P., Medrano-Soto, A., and Vazquez-Duhalt, R. ( 2003 ) Evolutionary and structural diversity of fungal laccases. Antonie Van Leeuwenhoek 84: 289 – 299.en_US
dc.identifier.citedreferenceWhitman, S., Gezginci, M., Timmermann, B.N., and Holman, T.R. ( 2002 ) Structure-activity relationship studies of nordihydroguaiaretic acid inhibitors toward soybean, 12-human, and 15-human lipoxygenase. J Med Chem 45: 2659 – 2661.en_US
dc.identifier.citedreferenceWilliamson, P.R. ( 1994 ) Biochemical and molecular characterization of the diphenol oxidase of Cryptococcus neoformans: identification as a laccase. J Bacteriol 176: 656 – 664.en_US
dc.identifier.citedreferenceXue, C., Tada, Y., Dong, X., and Heitman, J. ( 2007 ) The human fungal pathogen Cryptococcus can complete its sexual cycle during a pathogenic association with plants. Cell Host Microbe 1: 263 – 273.en_US
dc.identifier.citedreferenceZhang, X., Eigendorf, G., Stebbing, D.W., Mansfield, S.D., and Saddler, J.N. ( 2002 ) Degradation of trilinolein by laccase enzymes. Arch Biochem Biophys 405: 44 – 54.en_US
dc.identifier.citedreferenceZhu, X., and Williamson, P.R. ( 2004 ) Role of laccase in the biology and virulence of Cryptococcus neoformans. FEMS Yeast Res 5: 1 – 10.en_US
dc.identifier.citedreferenceZhu, X., Gibbons, J., Garcia-Rivera, J., Casadevall, A., and Williamson, P.R. ( 2001 ) Laccase of Cryptococcus neoformans is a cell wall-associated virulence factor. Infect Immun 69: 5589 – 5596.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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