Laccases involved in 1,8-dihydroxynaphthalene melanin biosynthesis in Aspergillus fumigatus are regulated by developmental factors and copper homeostasis

Eukaryotic Cell

Volumn 12, Issue 12, 2013, Pages 1641-1652

  Upadhyay, Srijana ^a   Torres, Guadalupe ^a   Lin, Xiaorong ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,8 DIHYDROXYNAPHTHALENE MELANIN; 1,8-DIHYDROXYNAPHTHALENE MELANIN; COPPER; FUNGAL PROTEIN; LACCASE; MELANIN; NAPHTHOL DERIVATIVE;

ARTICLE; ASPERGILLUS FUMIGATUS; BIOSYNTHESIS; ENZYMOLOGY; FUNGUS HYPHAE; FUNGUS SPORE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

ASPERGILLUS FUMIGATUS; COPPER; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, FUNGAL; HYPHAE; LACCASE; MELANINS; NAPHTHOLS; SPORES, FUNGAL;

EID: 84888264582     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00217-13     Document Type: Article

References (68)

1. Denning DW, Tucker RM, Hanson LH, Hamilton JR, Stevens DA. 1989. Itraconazole therapy for cryptococcal meningitis and cryptococcosis. Arch. Intern. Med. 149:2301-2308.
2. Adams TH, Wieser JK, Yu JH. 1998. Asexual sporulation in Aspergillus nidulans. Microbiol. Mol. Biol. Rev. 62:35-54.
3. Samson RA, Varga J, Dter PS. 2008. Morphology and reproductive mode of Aspergillus fumigatus, p 7-14. In Latge J-P, Steinbach WJ (ed), Aspergillus fumigatus and aspergillosis. ASM Press, Washington, DC.
4. Adams TH, Boylan MT, Timberlake WE. 1988. brlA is necessary and sufficient to direct conidiophore development in Aspergillus nidulans. Cell 54:353-362.
5. Mah J, Yu J. 2006. Upstream and downstream regulation of asexual development in Aspergillus fumigatus. Eukaryot. Cell 5:1585-1595.
6. Tao L, Yu J-H. 2011 AbaA and WetA govern distinct stages of Aspergillus fumigatus development. Microbiology 57:313-326.
7. Kwon-Chung KJ, Bennett JE, Rhodes JC. 1982. Taxonomic studies on Filobasidiella species and their anamorphs. Antonie Van Leeuwenhoek 48:25-38.
8. Casadevall A, Rosas AL, Nosanchuk JD. 2000. Melanin and virulence in Cryptococcus neoformans. Curr. Opin. Microbiol. 3:354-358.
9. Jahn B, Koch A, Schmidt A, Wanner G, Gehringer H, Bhakdi S, Brakhage AA. 1997. Isolation and characterization of a pigmentlessconidium mutant of Aspergillus fumigatus with altered conidial surface and reduced virulence. Infect. Immun. 65:5110-5117.
10. Tsai HF, Chang YC, Washburn RG, Wheeler MH, Kwon-Chung KJ. 1998. The developmentally regulated alb1 gene of Aspergillus fumigatus: its role in modulation of conidial morphology and virulence. J. Bacteriol. 180:3031-3038.
11. Dixon DM, Polak A, Szaniszlo PJ. 1987. Pathogenicity and virulence of wild-type and melanin-deficient Wangiella dermatitidis. J. Med. Vet. Mycol. 25:97-106.
12. Mednick AJ, Nosanchuk JD, Casadevall A. 2005. Melanization of Cryptococcus neoformans affects lung inflammatory responses during cryptococcal infection. Infect. Immun. 73:2012-2019.
13. Howard RJ, Valent B. 1996. Breaking and entering: host penetration by the fungal rice blast pathogen Magnaporthe grisea. Annu. Rev. Microbiol. 50:491-512.
14. Pukkila-Worley R, Gerrald QD, Kraus PR, Boily MJ, Davis MJ, Giles SS, Cox GM, Heitman J, Alspaugh JA. 2005. Transcriptional network of multiple capsule and melanin genes governed by the Cryptococcus neoformans cyclic AMP cascade. Eukaryot. Cell 4:190-201.
15. Williamson PR. 1997. Laccase and melanin in the pathogenesis of Cryptococcus neoformans. Front. Biosci. 2:e99-e107.
16. Williamson PR, Wakamatsu K, Ito S. 1998. Melanin biosynthesis in Cryptococcus neoformans. J. Bacteriol. 180:1570-1572.
17. Liu L, Wakamatus K, Ito S, Williamson PR. 1999. Catecholamine oxidative products, but not melanin, are produced by Cryptococcus neoformans during neuropathogenesis in mice. Infect. Immun. 67:108-112.
18. Kubo Y, Takano Y, Furusawa I. 1996. Molecular genetic analysis of melanin biosynthetic genes essential for appressorium function in Colletotrichum lagenarium, p 73-82. In Mills D, Kunoh H, Keen N, Mayama S (ed), Molecular aspects of pathogenicity: requirements for signal transduction. APS Press, St. Paul, MN.
19. Howard RJ, Ferrari MA. 1989. Role of melanin in appressorium formation. Exp. Mycol. 13:403-418.
20. Kawamura C, Moriwaki J, Kimura N, Fujita Y, Fuji S, Hirano T, Koizumi S, Tsuge T. 1997. The melanin biosynthesis genes of Alternaria alternata can restore pathogenicity of the melanin-deficient mutants of Magnaporthe grisea. Mol. Plant Microbe Interact. 10:446-453.
21. Langfelder K, Streibel M, Jahn B, Haase G, Brakhage AA. 2003. Biosynthesis of fungal melanins and their importance for human pathogenic fungi. Fungal Genet. Biol. 38:143-158.
22. Tsai HF, Wheeler MH, Chang YC, Kwon-Chung KJ. 1999. A developmentally regulated gene cluster involved in conidial pigment biosynthesis in Aspergillus fumigatus. J. Bacteriol. 181:6469-6477.
23. Saitoh Y, Izumitsu K, Morita A, Tanaka C. 2010. A copper-transporting ATPase BcCCC2 is necessary for pathogenicity of Botrytis cinerea. Mol. Genet. Genomics 284:33-43.
24. Heinekamp T, Thywissen A, Macheleidt J, Keller S, Valiante V, Brakhage AA. 2012. Aspergillus fumigatus melanins: interference with the host endocytosis pathway and impact on virulence. Front. Microbiol. 3:440. doi:10.3389/fmicb.2012.00440.
25. Law DJ, Timberlake WE. 1980. Developmental regulation of laccase levels in Aspergillus nidulans. J. Bacteriol. 144:509-517.
26. Aramayo R, Timberlake WE. 1990. Sequence and molecular structure of the Aspergillus nidulans yA (laccase I) gene. Nucleic Acids Res. 18:3415.
27. Tsai HF, Washburn RG, Chang YC, Kwon-Chung KJ. 1997. Aspergillus fumigatus arp1 modulates conidial pigmentation and complement deposition. Mol. Microbiol. 26:175-183.
28. Twumasi-Boateng K, Yu Y, Chen D, Gravelat FN, Nierman WC, Sheppard DC. 2009. Transcriptional profiling identifies a role for BrlA in the response to nitrogen depletion and for StuA in the regulation of secondary metabolite clusters in Aspergillus fumigatus. Eukaryot. Cell 8:104-115.
29. Sugareva V, Hartl A, Brock M, Hubner K, Rohde M, Heinekamp T, Brakhage AA. 2006. Characterisation of the laccase-encoding gene abr2 of the dihydroxynaphthalene-like melanin gene cluster of Aspergillus fumigatus. Arch. Microbiol. 186:345-355.
30. Griffith GW, Easton GL, Detheridge A, Roderick K, Edwards A, Worgan HJ, Nicholson J, Perkins WT. 2007. Copper deficiency in potato dextrose agar causes reduced pigmentation in cultures of various fungi. FEMS Microbiol. Lett. 276:165-171.
31. Williamson PR. 1994. Biochemical and molecular characterization of the diphenol oxidase of Cryptococcus neoformans: identification as a laccase. J. Bacteriol. 176:656-664.
32. Clutterbuck AJ. 1972. Absence of laccase from yellow-spored mutants of Aspergillus nidulans. J. Gen. Microbiol. 70:423-435.
33. Clutterbuck AJ. 1990. The genetics of conidiophore pigmentation in Aspergillus nidulans. J. Gen. Microbiol. 136:1731-1738.
34. Parisot D, Dufresne M, Veneault C, Laugé R, Langin T. 2002. clap1, a gene encoding a copper-transporting ATPase involved in the process of infection by the phytopathogenic fungus Colletotrichum lindemuthianum. Mol. Genet. Genomics 268:139-151.
35. Petris MJ, Strausak D, Mercer JFB. 2000. The Menkes copper transporter is required for the activation of tyrosinase. Hum. Mol. Genet. 9:2845-2851.
36. Momany M, Westfall PJ, Abramowsky G. 1999. Aspergillus nidulans swo mutants show defects in polarity establishment, polarity maintenance and hyphal morphogenesis. Genetics 151:557-567.
37. Yang L, Ukil LA, Osmani A, Nahm F, Davies J, De Souza CP, Dou X, Perez-Balaguer A, Osmani SA. 2004. Rapid production of gene replacement constructs and generation of a green fluorescent protein-tagged centromeric marker in Aspergillus nidulans. Eukaryot. Cell 3:1359-1362.
38. Yelton MM, Hamer JE, Timberlake WE. 1984. Transformation of Aspergillus nidulans by using a trpC plasmid. Proc. Natl. Acad. Sci. U. S. A. 81:1470-1474.
39. Chung D-W, Greenwald C, Upadhyay S, Ding S, Wilkinson HH, Ebbole DJ, Shaw BD. 2011. Acon-3, the Neurospora crassa ortholog of the developmental modifier, medA, complements the conidiation defect of the Aspergillus nidulans mutant. Fungal Genet. Biol. 48:370-376.
40. Zhang Y. 2008. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9:40. doi:10.1186/1471-2105-9-40.
41. Mullins E, Chen X, Romaine R, Raina R, Geiser D, Kang S. 2001. Agrobacterium-mediated transformation of Fusarium oxysporum: an efficient tool for insertional mutagenesis and gene transformation. Phytopathology 91:173-180.
42. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
43. Mylonakis E. 2008. Galleria mellonella and the study of fungal pathogenesis: making the case for another genetically tractable model host. Mycopathologia 165:1-3.
44. Bogú MI, Kedra E, Bania J, Szczepanik M, Czygier M, Jablonski P, Pasztaleniec A, Samborski J, Mazgajska J, Polanowski A. 2007. Different defense strategies of Dendrolimus pini, Galleria mellonella, and Calliphora vicina against fungal infection. J. Insect Physiol. 53:909-922.
45. Youngchim S, Morris-Jones R, Hay RJ, Hamilton AJ. 2004. Production of melanin by Aspergillus fumigatus. J. Med. Microbiol. 53:175-181.
46. Youngchim S, Pornsuwan S, Nosanchuk JD, Dankai W, Vanittanakom N. 2011. Melanogenesis in dermatophyte species in vitro and during infection. Microbiology 157:2348-2356.
47. Zhu X, Williamson PR. 2003. A CLC-type chloride channel gene is required for laccase activity and virulence in Cryptococcus neoformans. Mol. Microbiol. 50:1271-1281.
48. Jiang N, Liu X, Pan J, Wang Y, Zhu X. 2009. Effect of the copperresponsive factor Cuf1 on the capsule biosynthesis in Cryptococcus neoformans. Wei Sheng Wu Xue Bao 49:1459-1464.
49. Yuan DS, Stearman R, Dancis A, Dunn T, Beeler T, Klausner RD. 1995. The Menkes/Wilson disease gene homologue in yeast provides copper to a ceruloplasmin-like oxidase required for iron uptake. Proc. Natl. Acad. Sci. U. S. A. 92:2632-2636.
50. Dancis A, Yuan DS, Haile D, Askwith C, Eide D, Moehle C, Kaplan J, Klausner RD. 1994. Molecular characterization of a copper transport protein in S. cerevisiae: an unexpected role for copper in iron transport. Cell 76:393-402.
51. Dwyer FPJ, Mellor DP. 1964. Chelating agents and metal chelates. Academic Press, New York, NY.
52. Ding C, Festa RA, Chen YL, Espart A, Palacios O, Espin J, Capdevila M, Atrian S, Heitman J, Thiele DJ. 2013. Cryptococcus neoformans copper detoxification machinery is critical for fungal virulence. Cell Host Microbe 13:265-276.
53. Jackson JC, Higgins LA, Lin X. 2009. Conidiation color mutants of Aspergillus fumigatus are highly pathogenic to the heterologous insect host Galleria mellonella. PLoS One 4:e4224. doi:10.1371/journal.pone.0004224.
54. Lavine MD, Strand MR. 2002. Insect hemocytes and their role in immunity. Insect Biochem. Mol. Biol. 32:1295-1309.
55. Plonka PM, Grabacka M. 2006. Melanin synthesis in microorganisms-biotechnological and medical aspects. Acta Biochim. Pol. 53:429-443.
56. Lin SY, Okuda S, Ikeda K, Okuno T, Takano Y. 2012. LAC2 encoding a secreted laccase is involved in appressorial melanization and conidial pigmentation in Colletotrichum orbiculare. Mol. Plant Microbe Interact. 25: 1552-1561.
57. Kubo Y, Suzuki K, Furusawa I, Ishida N, Yamamoto M. 1982. Relation of appressorium pigmentation and penetration on nitrocellulose membranes by Colletotrichum lagenarium. Phytopathology 72:498-501.
58. Chumley FG, Valent B. 1990. Genetic analysis of melanin-deficient, nonpathogenic mutants of Magnaporthe grisea. Mol. Plant Microbe Interact. 3:135-143.
59. Kubo Y, Furusawa I. 1991. Melanin biosynthesis: prerequisite for successful invasion of the plant host by appressoria of Colletotrichum and Pyricularia, p 205-218. In Cole GT, Hoch HC (ed), The fungal spore and disease initiation in plants and animals. Plenum Press, New York, NY.
60. Tsuji G, Kenmochi Y, Takano Y, Sweigard J, Farrall L, Furusawa I, Horino O, Kubo Y. 2000. Novel fungal transcriptional activators, Cmr1p of Colletotrichum lagenarium and Pig1p of Magnaporthe grisea, contain Cys2His2 zinc finger and Zn(II)2Cys6 binuclear cluster DNA-binding motifs and regulate transcription of melanin biosynthesis genes in a developmentally specific manner. Mol. Microbiol. 38:940-954.
61. Eliahu N, Igbaria A, Rose MS, Horwitz BA, Lev S. 2007. Melanin biosynthesis in the maize pathogen Cochliobolus heterostrophus depends on two mitogen-activated protein kinases, Chk1 and Mps1, and the transcription factor Cmr1. Eukaryot. Cell 6:421-429.
62. Gravelat FN, Ejzykowicz DE, Chiang LY, Chabot JC, Urb M, Macdonald KD, al-Bader N, Filler SG, Sheppard DC. 2010. Aspergillus fumigates MedA governs adherence, host cell interactions and virulence. Cell. Microbiol. 12:473-488.
63. Pihet M, Vandeputte P, Tronchin G, Renier G, Saulnier P, Georgeault S, Mallet R, Chabasse D, Symoens F, Bouchara JP. 2009. Melanin is an essential component for the integrity of the cell wall of Aspergillus fumigatus conidia. BMC Microbiol. 9:177. doi:10.1186/1471-2180-9-177.
64. Thywißen A, Heinekamp T, Dahse HM, Schmaler-Ripcke J, Nietzsche S, Zipfel PF, Brakhage AA. 2011. Conidial dihydroxynaphthalene melanin of the human pathogenic fungus Aspergillus fumigatus interferes with the host endocytosis pathway. Front. Microbiol. 2:96. doi:10.3389/fmicb.2011.00096.
65. Buskirk AD, Templeton SP, Nayak AP, Hettick JM, Law BF, Green BJ, Beezhold DH. 6 August 2013, Posting date. Pulmonary immune responses to Aspergillus fumigatus in an immunocompetent mouse model of repeated exposures. J. Immunotoxicol. doi:10.3109/1547691X.2013.819054.
66. Mylonakis E, Casadevall A, Ausubel FM. 2007. Exploiting amoeboid and non-vertebrate animal model systems to study the virulence of human pathogenic fungi. PLoS Pathog. 3:e101. doi:10.1371/journal.ppat.0030101.
67. Mylonakis E, Aballay A. 2005. Worms and flies as genetically tractable animal models to study host-pathogen interactions. Infect. Immun. 73: 3833-3841.
68. Navarro-Velasco G, Prados-Rosales R, Ortíz-Urquiza A, Quesada-Moraga E, Pietro A. 2011. Galleria mellonella as model host for the trans-kingdom pathogen Fusarium oxysporum. Fungal Genet. Biol. 48: 1124-1129.