SpringerLink
Log in

Lessons from Cryptococcal Laccase: From Environmental Saprophyte to Pathogen

  • Genomics and Pathogenesis (Shmuel Shoham, Section Editor)
  • Published:
Current Fungal Infection Reports Aims and scope Submit manuscript

Abstract

Cryptococcus is an opportunistic pathogen that lives in the environment as a free-living yeast and inflicts disease in humans, primarily in immunocompromised patients such as organ-transplant recipients and people with HIV/AIDS. A key factor allowing emergence of this fungal pathogen is a copper-containing laccase enzyme that facilitates nutrient foraging as a saprophyte and offers protection against environmental dangers such as free-living amoebae and mammalian macrophages during infection. The promiscuous substrate specificity of laccase facilitates the degradation of hard plant lignin polymers as well as the synthesis of lignin-like pigments from plant flavonoids and melanin pigments from dopamine. The enzyme also possesses an iron oxidase activity that prevents Fenton product formation in macrophages and another activity that allows synthesis of immune-modulatory prostaglandins that fool the host, shutting off an effective immune response. This review provides a brief overview of key points in laccase function and its role in virulence, as well as regulation and trafficking of the enzyme during the interconversion between saprophyte and pathogen, yielding insights into pathogenesis from this adaptable pathogen.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Heitman J, and American Society for Microbiology. Cryptococcus: from human pathogen to model yeast. 2011. Washington, DC: ASM Press. xvii, 620.

  2. National Center for Zoonotic, V-B, and Enteric Diseases. Cryptococcus (Cryptococcosis). 2010; CDC website detailing general information for Cryptococcosis]. Available from: http://www.cdc.gov/nczved/divisions/dfbmd/diseases/cryptococcus/index.html#top.

  3. Li SS, Mody CH. Cryptococcus. Proc Am Thorac Soc. 2010;7(3):186–96.

    PubMed  Google Scholar 

  4. Park BJ et al. Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS. 2009;23(4):525–30.

    PubMed  Google Scholar 

  5. Diamond RD, Bennett JE. Prognostic factors in cryptococcal meningitis. A study in 111 cases. Ann Intern Med. 1974;80(2):176–81.

    PubMed  CAS  Google Scholar 

  6. Olszewski MA, Zhang Y, Huffnagle GB. Mechanisms of cryptococcal virulence and persistence. Future Microbiol. 2010;5(8):1269–88.

    PubMed  CAS  Google Scholar 

  7. Sanfelice F. Contributo alla morfolgia e biologia dei blastomiceti che si sviluppano nei succhi de alcuni frutti. Ann Igien. 1894;4:463–95.

    Google Scholar 

  8. Ruiz A, Fromtling RA, Bulmer GS. Distribution of Cryptococcus neoformans in a natural site. Infect Immun. 1981;31(2):560–3.

    PubMed  CAS  Google Scholar 

  9. Garcia-Hermoso D, Janbon G, Dromer F. Epidemiological evidence for dormant Cryptococcus neoformans infection. J Clin Microbiol. 1999;37(10):3204–9.

    PubMed  CAS  Google Scholar 

  10. Lundell TK, Makela MR, Hilden K. Lignin-modifying enzymes in filamentous basidiomycetes–ecological, functional and phylogenetic review. J Basic Microbiol. 2010;50(1):5–20.

    PubMed  CAS  Google Scholar 

  11. Zhu X, Williamson PR. Role of laccase in the biology and virulence of Cryptococcus neoformans. FEMS Yeast Res. 2004;5(1):1–10.

    PubMed  CAS  Google Scholar 

  12. Chang YC et al. Cryptococcal yeast cells invade the central nervous system via transcellular penetration of the blood-brain barrier. Infect Immun. 2004;72(9):4985–95.

    PubMed  CAS  Google Scholar 

  13. Eisenman HC, Casadevall A, McClelland EE. New insights on the pathogenesis of invasive Cryptococcus neoformans infection. Curr Infect Dis Rep. 2007;9(6):457–64.

    PubMed  Google Scholar 

  14. Waterman SR et al. Cell wall targeting of laccase of Cryptococcus neoformans during infection of mice. Infect Immun. 2007;75(2):714–22.

    PubMed  CAS  Google Scholar 

  15. Cox GM et al. Urease as a virulence factor in experimental cryptococcosis. Infect Immun. 2000;68(2):443–8.

    PubMed  CAS  Google Scholar 

  16. •• Panepinto J, et al. Sec6-dependent sorting of fungal extracellular exosomes and laccase of Cryptococcus neoformans. Mol Microbiol. 2009;71(5):1165–76. The presence of extracellular vesicles and their dependence on Sec6-dependent secretion provided the first molecular proof of exosome formation in fungi.

    PubMed  CAS  Google Scholar 

  17. •• Chayakulkeeree M, et al. SEC14 is a specific requirement for secretion of phospholipase B1 and pathogenicity of Cryptococcus neoformans. Mol Microbiol. 2011;80(4):1088–101. This paper shows differential sorting of the virulence factor, laccase, and another virulence factor, phospholipase B1, demonstrating that different virulence factors can be transported by distinct pathways.

    PubMed  CAS  Google Scholar 

  18. Hu G et al. PI3K signaling of autophagy is required for starvation tolerance and virulenceof Cryptococcus neoformans. J Clin Invest. 2008;118(3):1186–97.

    PubMed  CAS  Google Scholar 

  19. Liu L, Tewari RP, Williamson PR. Laccase protects Cryptococcus neoformans from antifungal activity of alveolar macrophages. Infect Immun. 1999;67(11):6034–9.

    PubMed  CAS  Google Scholar 

  20. Shea JM, Del Poeta M. Lipid signaling in pathogenic fungi. Curr Opin Microbiol. 2006;9(4):352–8.

    PubMed  CAS  Google Scholar 

  21. Thurston CF. The structure and function of fungal laccases. Microbiology. 1994;140(1):19–26.

    CAS  Google Scholar 

  22. Mayer AM, Staples RC. Laccase: new functions for an old enzyme. Phytochemistry. 2002;60(6):551–65.

    PubMed  CAS  Google Scholar 

  23. Brijwani K, Rigdon A, Vadlani PV. Fungal laccases: production, function, and applications in food processing. Enzyme Res. 2010;2010:149748.

    PubMed  Google Scholar 

  24. Giardina P et al. Laccases: a never-ending story. Cell Mol Life Sci. 2010;67(3):369–85.

    PubMed  CAS  Google Scholar 

  25. Fowler ZL et al. Melanization of flavonoids by fungal and bacterial laccases. Yeast. 2011;28(3):181–8.

    PubMed  CAS  Google Scholar 

  26. Williamson PR. Biochemical and molecular characterization of the diphenol oxidase of Cryptococcus neoformans: identification as a laccase. J Bacteriol. 1994;176(3):656–64.

    PubMed  CAS  Google Scholar 

  27. Zhao Q, Dixon RA. Transcriptional networks for lignin biosynthesis: more complex than we thought? Trends Plant Sci. 2011;16(4):227–33.

    PubMed  CAS  Google Scholar 

  28. Leonowicz A et al. Fungal laccase: properties and activity on lignin. J Basic Microbiol. 2001;41(3–4):185–227.

    PubMed  CAS  Google Scholar 

  29. Eggert C. Laccase-catalyzed formation of cinnabarinic acid is responsible for antibacterial activity of Pycnoporus cinnabarinus. Microbiol Res. 1997;152(3):315–8.

    PubMed  CAS  Google Scholar 

  30. Perry CR et al. The structure of laccase protein and its synthesis by the commercial mushroom Agaricus bisporus. J Gen Microbiol. 1993;139(1):171–8.

    PubMed  CAS  Google Scholar 

  31. Bertrand T et al. Crystal structure of a four-copper laccase complexed with an arylamine: insights into substrate recognition and correlation with kinetics. Biochemistry. 2002;41(23):7325–33.

    PubMed  CAS  Google Scholar 

  32. Hakulinen N et al. Crystal structure of a laccase from Melanocarpus albomyces with an intact trinuclear copper site. Nat Struct Biol. 2002;9(8):601–5.

    PubMed  CAS  Google Scholar 

  33. Mylonakis E et al. Killing of Caenorhabditis elegans by Cryptococcus neoformans as a model of yeast pathogenesis. Proc Natl Acad Sci USA. 2002;99(24):15675–80.

    PubMed  CAS  Google Scholar 

  34. Walton FJ, Idnurm A, Heitman J. Novel gene functions required for melanization of the human pathogen Cryptococcus neoformans. Mol Microbiol. 2005;57(5):1381–96.

    PubMed  CAS  Google Scholar 

  35. Pukkila-Worley R et al. Transcriptional network of multiple capsule and melanin genes governed by the Cryptococcus neoformans cyclic AMP cascade. Eukaryot Cell. 2005;4(1):190–201.

    PubMed  CAS  Google Scholar 

  36. Salas SD et al. Effect of the laccase gene CNLAC1, on virulence of Cryptococcus neoformans. J Exp Med. 1996;184(2):377–86.

    PubMed  CAS  Google Scholar 

  37. Eisenman HC et al. Cryptococcus neoformans laccase catalyses melanin synthesis from both D- and L-DOPA. Microbiology. 2007;153(Pt 12):3954–62.

    PubMed  CAS  Google Scholar 

  38. Williamson PR. Laccase and melanin in the pathogenesis of Cryptococcus neoformans. Front Biosci. 1997;2:e99–107.

    PubMed  CAS  Google Scholar 

  39. Lerch K, Germann UA. Evolutionary relationships among copper proteins containing coupled binuclear copper sites. Prog Clin Biol Res. 1988;274:331–48.

    PubMed  CAS  Google Scholar 

  40. Ito S, Kato T, Fujita K. Covalent binding of catechols to proteins through the sulphydryl group. Biochem Pharmacol. 1988;37(9):1707–10.

    PubMed  CAS  Google Scholar 

  41. Riley PA. Melanin. Int J Biochem Cell Biol. 1997;29(11):1235–9.

    PubMed  CAS  Google Scholar 

  42. Sharma S, Wagh S, Govindarajan R. Melanosomal proteins–role in melanin polymerization. Pigment Cell Res. 2002;15(2):127–33.

    PubMed  CAS  Google Scholar 

  43. Wagh S et al. Melanosomal proteins promote melanin polymerization. Pigment Cell Res. 2000;13(6):442–8.

    PubMed  CAS  Google Scholar 

  44. Sidjanski S, Mathews GV, Vanderberg JP. Electrophoretic separation and identification of phenoloxidases in hemolymph and midgut of adult Anopheles stephensi mosquitoes. J Parasitol. 1997;83(4):686–91.

    PubMed  CAS  Google Scholar 

  45. Staib F, Senska M. Brown pigmentation (brown colour effect, BCE) of Cryptococcus neoformans on Guizotia abyssinica-creatinine-agar as dependent on the initial pH value (author’s transl). Zentralbl Bakteriol Orig A. 1973;225(1):113–24.

    PubMed  CAS  Google Scholar 

  46. Kwon-Chung KJ, Bennett JE. Medical mycology. Philadelphia: Lea & Febiger. ix; 1992. p. 866.

  47. Fleet GH. Yeast interactions and wine flavour. Int J Food Microbiol. 2003;86(1–2):11–22.

    PubMed  CAS  Google Scholar 

  48. Kwon-Chung KJ, Polacheck I, Popkin TJ. Melanin-lacking mutants of Cryptococcus neoformans and their virulence for mice. J Bacteriol. 1982;150(3):1414–21.

    PubMed  CAS  Google Scholar 

  49. Loftus BJ et al. The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science. 2005;307(5713):1321–4.

    PubMed  Google Scholar 

  50. Nosanchuk JD et al. Melanization of Cryptococcus neoformans in murine infection. Mol Cell Biol. 1999;19(1):745–50.

    PubMed  CAS  Google Scholar 

  51. Nosanchuk JD et al. Evidence that Cryptococcus neoformans is melanized in pigeon excreta: implications for pathogenesis. Infect Immun. 1999;67(10):5477–9.

    PubMed  CAS  Google Scholar 

  52. Eisenman HC et al. Vesicle-associated melanization in Cryptococcus neoformans. Microbiology. 2009;155(Pt 12):3860–7.

    PubMed  CAS  Google Scholar 

  53. Perfect JR et al. Clinical practice guidelines for the management of cryptococcal disease: 2010 update by the Infectious Diseases Society of America. Clin Infect Dis. 2010;50(3):291–322.

    PubMed  Google Scholar 

  54. Te Dorsthorst DT et al. In vitro interaction of flucytosine combined with amphotericin B or fluconazole against thirty-five yeast isolates determined by both the fractional inhibitory concentration index and the response surface approach. Antimicrob Agents Chemother. 2002;46(9):2982–9.

    Google Scholar 

  55. Hastings TG. The role of dopamine oxidation in mitochondrial dysfunction: implications for Parkinson’s disease. J Bioenerg Biomembr. 2009;41(6):469–72.

    PubMed  CAS  Google Scholar 

  56. Nyhus KJ, Wilborn AT, Jacobson ES. Ferric iron reduction by Cryptococcus neoformans. Infect Immun. 1997;65(2):434–8.

    PubMed  CAS  Google Scholar 

  57. Howard DH. Acquisition, transport, and storage of iron by pathogenic fungi. Clin Microbiol Rev. 1999;12(3):394–404.

    PubMed  CAS  Google Scholar 

  58. Zhu X et al. Laccase of Cryptococcus neoformans is a cell wall-associated virulence factor. Infect Immun. 2001;69(9):5589–96.

    PubMed  CAS  Google Scholar 

  59. Sargent PJ, Farnaud S, Evans RW. Structure/function overview of proteins involved in iron storage and transport. Curr Med Chem. 2005;12(23):2683–93.

    PubMed  CAS  Google Scholar 

  60. Erb-Downward JR et al. The role of laccase in prostaglandin production by Cryptococcus neoformans. Mol Microbiol. 2008;68(6):1428–37.

    PubMed  CAS  Google Scholar 

  61. Naito Y. Molecular mechanism of cytokine gene expression in Th1 and Th2. Rinsho Byori. 1998;46(9):900–7.

    PubMed  CAS  Google Scholar 

  62. Stashenko P, Teles R, D’Souza R. Periapical inflammatory responses and their modulation. Crit Rev Oral Biol Med. 1998;9(4):498–521.

    PubMed  CAS  Google Scholar 

  63. Noverr MC et al. Pathogenic yeasts Cryptococcus neoformans and Candida albicans produce immunomodulatory prostaglandins. Infect Immun. 2001;69(5):2957–63.

    PubMed  CAS  Google Scholar 

  64. Erb-Downward JR, Huffnagle GB. Cryptococcus neoformans produces authentic prostaglandin E2 without a cyclooxygenase. Eukaryot Cell. 2007;6(2):346–50.

    PubMed  CAS  Google Scholar 

  65. Jiang N et al. Negative roles of a novel nitrogen metabolite repression-related gene, TAR1, in laccase production and nitrate utilization by the basidiomycete Cryptococcus neoformans. Appl Environ Microbiol. 2009;75(21):6777–82.

    PubMed  CAS  Google Scholar 

  66. Bahn YS et al. Adenylyl cyclase-associated protein Aca1 regulates virulence and differentiation of Cryptococcus neoformans via the cyclic AMP-protein kinase A cascade. Eukaryot Cell. 2004;3(6):1476–91.

    PubMed  CAS  Google Scholar 

  67. Heung LJ et al. The role and mechanism of diacylglycerol-protein kinase C1 signaling in melanogenesis by Cryptococcus neoformans. J Biol Chem. 2005;280(31):28547–55.

    PubMed  CAS  Google Scholar 

  68. Heung LJ et al. The sphingolipid pathway regulates Pkc1 through the formation of diacylglycerol in Cryptococcus neoformans. J Biol Chem. 2004;279(20):21144–53.

    PubMed  CAS  Google Scholar 

  69. Jiang N et al. A copper-responsive factor gene CUF1 is required for copper induction of laccase in Cryptococcus neoformans. FEMS Microbiol Lett. 2009;296(1):84–90.

    PubMed  CAS  Google Scholar 

  70. Jung WH et al. Iron regulation of the major virulence factors in the AIDS-associated pathogen Cryptococcus neoformans. PLoS Biol. 2006;4(12):e410.

    PubMed  Google Scholar 

  71. Nyhus K, Jacobson ES. Oxy2 as a transcriptional activator gene for copper uptake in Cryptococcus neoformans. Med Mycol. 2004;42(4):325–31.

    PubMed  CAS  Google Scholar 

  72. Rhome R, Del Poeta M. Lipid signaling in pathogenic fungi. Annu Rev Microbiol. 2009;63:119–31.

    PubMed  CAS  Google Scholar 

  73. D’Souza CA, Heitman J. Conserved cAMP signaling cascades regulate fungal development and virulence. FEMS Microbiol Rev. 2001;25(3):349–64.

    PubMed  Google Scholar 

  74. Idnurm A et al. Deciphering the model pathogenic fungus Cryptococcus neoformans. Nat Rev Microbiol. 2005;3(10):753–64.

    PubMed  CAS  Google Scholar 

  75. Maeng S et al. Comparative transcriptome analysis reveals novel roles of the Ras and cyclic AMP signaling pathways in environmental stress response and antifungal drug sensitivity in Cryptococcus neoformans. Eukaryot Cell. 2010;9(3):360–78.

    PubMed  CAS  Google Scholar 

  76. Fan W et al. Cryptococcus neoformans gene expression during murine macrophage infection. Eukaryot Cell. 2005;4(8):1420–33.

    PubMed  CAS  Google Scholar 

  77. Griffioen G, Thevelein JM. Molecular mechanisms controlling the localisation of protein kinase A. Curr Genet. 2002;41(4):199–207.

    PubMed  CAS  Google Scholar 

  78. Scott JD. Dissection of protein kinase and phosphatase targeting interactions. Soc Gen Physiol Ser. 1997;52:227–39.

    PubMed  CAS  Google Scholar 

  79. Thevelein JM. The RAS-adenylate cyclase pathway and cell cycle control in Saccharomyces cerevisiae. Antonie Van Leeuwenhoek. 1992;62(1–2):109–30.

    PubMed  CAS  Google Scholar 

  80. Yvert G et al. Trans-acting regulatory variation in Saccharomyces cerevisiae and the role of transcription factors. Nat Genet. 2003;35(1):57–64.

    PubMed  CAS  Google Scholar 

  81. Chang YC, Kwon-Chung KJ. Complementation of a capsule-deficient mutation of Cryptococcus neoformans restores its virulence. Mol Cell Biol. 1994;14(7):4912–9.

    PubMed  CAS  Google Scholar 

  82. Alspaugh JA et al. Adenylyl cyclase functions downstream of the Galpha protein Gpa1 and controls mating and pathogenicity of Cryptococcus neoformans. Eukaryot Cell. 2002;1(1):75–84.

    PubMed  CAS  Google Scholar 

  83. D’Souza CA et al. Cyclic AMP-dependent protein kinase controls virulence of the fungal pathogen Cryptococcus neoformans. Mol Cell Biol. 2001;21(9):3179–91.

    PubMed  Google Scholar 

  84. Hu G et al. Transcriptional regulation by protein kinase A in Cryptococcus neoformans. PLoS Pathog. 2007;3(3):e42.

    PubMed  Google Scholar 

  85. Kwon-Chung KJ, Edman JC, Wickes BL. Genetic association of mating types and virulence in Cryptococcus neoformans. Infect Immun. 1992;60(2):602–5.

    PubMed  CAS  Google Scholar 

  86. Chang YC, Penoyer LA, Kwon-Chung KJ. The second STE12 homologue of Cryptococcus neoformans is MATa-specific and plays an important role in virulence. Proc Natl Acad Sci USA. 2001;98(6):3258–63.

    PubMed  CAS  Google Scholar 

  87. Chang YC et al. Cryptococcus neoformans STE12alpha regulates virulence but is not essential for mating. J Exp Med. 2000;191(5):871–82.

    PubMed  CAS  Google Scholar 

  88. Wickes BL, Edman U, Edman JC. The Cryptococcus neoformans STE12alpha gene: a putative Saccharomyces cerevisiae STE12 homologue that is mating type specific. Mol Microbiol. 1997;26(5):951–60.

    PubMed  CAS  Google Scholar 

  89. Dromer F et al. Molecular ty** of Cryptococcus neoformans serotype D clinical isolates. J Clin Microbiol. 1994;32(10):2364–71.

    PubMed  CAS  Google Scholar 

  90. Lin X et al. Impact of mating type, serotype, and ploidy on the virulence of Cryptococcus neoformans. Infect Immun. 2008;76(7):2923–38.

    PubMed  CAS  Google Scholar 

  91. Huffnagle GB, Casadevall A, Perfect JR. Cryptococcus neoformans [book review]. Mycopathologia. 1999;147(1):59–60.

    Google Scholar 

  92. Bahn YS et al. Specialization of the HOG pathway and its impact on differentiation and virulence of Cryptococcus neoformans. Mol Biol Cell. 2005;16(5):2285–300.

    PubMed  CAS  Google Scholar 

  93. Park YD et al. Mating pheromone in Cryptococcus neoformans is regulated by a transcriptional/degradative “futile” cycle. J Biol Chem. 2010;285(45):34746–56.

    PubMed  CAS  Google Scholar 

  94. Panepinto J et al. The DEAD-box RNA helicase Vad1 regulates multiple virulence-associated genes in Cryptococcus neoformans. J Clin Invest. 2005;115(3):632–41.

    PubMed  CAS  Google Scholar 

  95. Luberto C et al. Roles for inositol-phosphoryl ceramide synthase 1 (IPC1) in pathogenesis of C. neoformans. Genes Dev. 2001;15(2):201–12.

    PubMed  CAS  Google Scholar 

  96. Patki V et al. Identification of an early endosomal protein regulated by phosphatidylinositol 3-kinase. Proc Natl Acad Sci USA. 1997;94(14):7326–30.

    PubMed  CAS  Google Scholar 

  97. Rivier AS et al. Exit of GPI-anchored proteins from the ER differs in yeast and mammalian cells. Traffic. 2010;11(8):1017–33.

    PubMed  CAS  Google Scholar 

  98. Segev N. Coordination of intracellular transport steps by GTPases. Semin Cell Dev Biol. 2011;22(1):33–8.

    PubMed  CAS  Google Scholar 

  99. Chen SH et al. Ypt31/32 GTPases and their novel F-box effector protein Rcy1 regulate protein recycling. Mol Biol Cell. 2005;16(1):178–92.

    PubMed  CAS  Google Scholar 

  100. Erickson T et al. Multiple virulence factors of Cryptococcus neoformans are dependent on VPH1. Mol Microbiol. 2001;42(4):1121–31.

    PubMed  CAS  Google Scholar 

  101. Hsu SC et al. Targeting vesicles to specific sites on the plasma membrane: the role of the sec6/8 complex. Trends Cell Biol. 1999;9(4):150–3.

    PubMed  CAS  Google Scholar 

  102. Rodrigues ML et al. Vesicular trans-cell wall transport in fungi: a mechanism for the delivery of virulence-associated macromolecules? Lipid Insights. 2008;2:27–40.

    PubMed  CAS  Google Scholar 

  103. Rodrigues ML et al. Vesicular polysaccharide export in Cryptococcus neoformans is a eukaryotic solution to the problem of fungal trans-cell wall transport. Eukaryot Cell. 2007;6(1):48–59.

    PubMed  CAS  Google Scholar 

  104. Yoneda A, Doering TL. An unusual organelle in Cryptococcus neoformans links luminal pH and capsule biosynthesis. Fungal Genet Biol. 2009;46(9):682–7.

    PubMed  CAS  Google Scholar 

  105. Oliveira DL et al. Characterization of yeast extracellular vesicles: evidence for the participation of different pathways of cellular traffic in vesicle biogenesis. PLoS One. 2010;5(6):e11113.

    PubMed  Google Scholar 

  106. Piper RC, Katzmann DJ. Biogenesis and function of multivesicular bodies. Annu Rev Cell Dev Biol. 2007;23:519–47.

    PubMed  CAS  Google Scholar 

  107. Tommasino N et al. Atf2 transcription factor binds to the APP1 promoter in Cryptococcus neoformans: stimulatory effect of diacylglycerol. Eukaryot Cell. 2008;7(2):294–301.

    PubMed  CAS  Google Scholar 

  108. Adler A et al. A novel specificity protein 1 (SP1)-like gene regulating protein kinase C-1 (Pkc1)-dependent cell wall integrity and virulence factors in Cryptococcus neoformans. J Biol Chem. 2011;286(23):20977–90.

    PubMed  CAS  Google Scholar 

  109. Shen G et al. Pleiotropic function of intersectin homologue Cin1 in Cryptococcus neoformans. Mol Microbiol. 2010;76(3):662–76.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This work was supported by the Intramural Research Program of the National Institutes of Health, National Institute of Allergy and Infectious Diseases.

Disclosure

No potential conflicts of interest relevant to this article were reported.

Author information

Authors and Affiliations

  1. Translational Mycology Unit, Laboratory for Infectious Diseases, National Institutes of Allergy and Infectious Diseases, National Institutes of Health, 10 Center Drive Building 10, Rm 12S236C, MSC 1888, Bethesda, MD, 20892, USA

    Shu Hui Chen & Peter R. Williamson

Authors
  1. Shu Hui Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter R. Williamson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter R. Williamson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chen, S.H., Williamson, P.R. Lessons from Cryptococcal Laccase: From Environmental Saprophyte to Pathogen. Curr Fungal Infect Rep 5, 233–244 (2011). https://doi.org/10.1007/s12281-011-0069-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12281-011-0069-3

Keywords

Search

Navigation