Abstract
Melanin synthesis is associated with virulence for the pathogenic fungus Cryptococcus neoformans. Exposure of nonmelanized C. neoformans 4067 cells to 4 M guanidinium isothiocyanate followed by 6 M HCl at 100 degrees C resulted in complete solubilization of cellular structures. However, exposure of melanized C. neoformans 24067 to the same conditions produced a suspension of black particles. Analysis of black particles with transmission and scanning electron microscopy revealed cell "ghosts" with electron-dense walls. Electron spin resonance (ESR) spectroscopy of suspensions of black particles revealed a signal indicative of a stable free radical population. The magnitude of the ESR signal was increased by illumination, Zn2+ ions, and basic pH. Boiling the black particles produced only a small reduction in the magnitude of the ESR signal. These ESR changes are characteristic of melanin. Exposure of melanized black cells to 0.1 or 0.5% NaOCl bleached the cells white and abolished the ESR signal, consistent with melanin disruption. ESR spectroscopy was used to study the rate of stable free radical formation, taken as an index of melanization, of C. neoformans 24067 cells growing in medium with 1.0 mM L-dopa at 30 and 37 degrees C over the course of 14 days. Melanization was slower at 37 degrees C. but by day 14, cells grown at 30 and 37 degrees C. had comparable levels or melanin. ESR spectroscopy of seven melanized C. neoformans strains revealed that some strains differed by up to eightfold in melanin content. The ESR spectra of C. neoformans 24067 grown in minimal medium containing either 1.0 mM catechol, dopamine, or L-dopa revealed large differences in signal amplitude. The relative melanin contents were 0.05, 0.45, and 1.0 for C. neoformans grown in media with catechol, dopamine. and L-dopa, respectively. Quantitative analysis revealed that melanin comprised 15.4% of the dry mass of the cell after 10 days of growth in medium containing 1.0 mM L-dopa. The results suggest (i) a useful protocol for isolating C. neoformans melanin, (ii) a role for melanin in maintaining cell wall integrity, (iii) disruption of melanin by NaOCl, (iv) strain differences in melanin content after growth in L-dopa, and (v) quantitative and/or qualitative differences in the melanin produced after growth in various substrates.
MeSH Terms
AIDS-Related Opportunistic Infections/microbiology
Catechols/metabolism
Cell Wall/metabolism
Cryptococcosis/complications,microbiology
Cryptococcus neoformans/metabolism,pathogenicity,ultrastructure
Dopamine/metabolism
Electron Spin Resonance Spectroscopy
Free Radicals/metabolism
Guanidines/pharmacology
Humans
Hydrochloric Acid/pharmacology
Isothiocyanates/pharmacology
Levodopa/metabolism
Melanins/chemistry,metabolism
Microscopy, Electron
Microscopy, Electron, Scanning
Species Specificity
Virulence
Chemicals
Catechols
Free Radicals
Guanidines
Isothiocyanates
Melanins
guanidine isothiocyanate
Levodopa
catechol
Hydrochloric Acid
Dopamine
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Wang Y
Department of Microbiology and Immunology, Albert Einstein College of Medicine, Bronx, New York 10461, USA.
Aisen P
Casadevall A
References (20)
20 references, click to expand
-
Biochemical studies of phenoloxidase and utilization of catecholamines in Cryptococcus neoformans.
J Bacteriol. 1982 Jun;150(3):1212-20
PMID: 6804439
-
Reactive oxygen species in normal physiology, cell injury and phagocytosis.
Adv Exp Med Biol. 1994;366:17-27
PMID: 7771251
-
Phenoloxidase activity and virulence in isogenic strains of Cryptococcus neoformans.
Infect Immun. 1982 Jun;36(3):1175-84
PMID: 6807845
-
Encapsulation and melanin formation as indicators of virulence in Cryptococcus neoformans.
Infect Immun. 1986 Jan;51(1):218-23
PMID: 3079732
-
Melanins and their importance in pathogenic fungi.
Curr Top Med Mycol. 1988;2:338-87
PMID: 3288360
-
Catecholamines and virulence of Cryptococcus neoformans.
Infect Immun. 1990 Sep;58(9):2919-22
PMID: 2117574
-
Temperature regulation of the cryptococcal phenoloxidase.
J Med Vet Mycol. 1991;29(2):121-4
PMID: 1908897
-
Melanin standard method: empirical formula 2.
Pigment Cell Res. 1992 Nov;5(5 Pt 1):240-6
PMID: 1287627
-
A standardized test for the identification and characterization of melanins using electron paramagnetic resonance (EPR) spectroscopy.
Pigment Cell Res. 1993 Mar;6(2):91-9
PMID: 8391699
-
Antioxidant function of fungal melanin.
J Bacteriol. 1993 Nov;175(21):7102-4
PMID: 8226653
-
Biochemical and molecular characterization of the diphenol oxidase of Cryptococcus neoformans: identification as a laccase.
J Bacteriol. 1994 Feb;176(3):656-64
PMID: 8300520
-
Susceptibility of melanized and nonmelanized Cryptococcus neoformans to nitrogen- and oxygen-derived oxidants.
Infect Immun. 1994 Jul;62(7):3004-7
PMID: 8005689
-
Cryptococcus neoformans melanin and virulence: mechanism of action.
Infect Immun. 1995 Aug;63(8):3131-6
PMID: 7622240
-
Monoclonal antibody mediated capsular reactions (Quellung) in Cryptococcus neoformans.
J Immunol Methods. 1995 Jul 17;184(1):139-43
PMID: 7622865
-
Relationship between superoxide dismutase and melanin in a pathogenic fungus.
Infect Immun. 1994 Sep;62(9):4085-6
PMID: 8063430
-
Decreased susceptibility of melanized Cryptococcus neoformans to UV light.
Appl Environ Microbiol. 1994 Oct;60(10):3864-6
PMID: 7986054
-
Growth of Cryptococcus neoformans in presence of L-dopa decreases its susceptibility to amphotericin B.
Antimicrob Agents Chemother. 1994 Nov;38(11):2648-50
PMID: 7872761
-
Estimation of the prevalence of cryptococcal infection among patients infected with the human immunodeficiency virus in New York City.
Clin Infect Dis. 1994 Dec;19(6):1029-33
PMID: 7888529
-
Role of nitric oxide and melanogenesis in the accomplishment of anticryptococcal activity by the BV-2 microglial cell line.
J Neuroimmunol. 1995 Apr;58(1):111-6
PMID: 7730446
-
Melanin-lacking mutants of Cryptococcus neoformans and their virulence for mice.
J Bacteriol. 1982 Jun;150(3):1414-21
PMID: 6804444