N-acetylglucosamine (GlcNAc) Triggers a Rapid, Temperature-Responsive Morphogenetic Program in Thermally Dimorphic Fungi

PLoS Genetics

Volumn 9, Issue 9, 2013, Pages

  Gilmore, Sarah A ^a   Naseem, Shamoon ^b   Konopka, James B ^b   Sil, Anita ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; N ACETYLGLUCOSAMINE;

ARTICLE; BLASTOMYCES DERMATITIDIS; CATB GENE; CBP1 GENE; CONTROLLED STUDY; CYTOSKELETON; DDR48 GENE; DISEASE TRANSMISSION; DOWN REGULATION; EFG1 GENE; FBC1 GENE; FILAMENTATION; FILAMENTOUS GROWTH; FUNGAL CELL; FUNGAL FILAMENT; FUNGAL GENE; FUNGUS; FUNGUS GROWTH; GENE EXPRESSION PROFILING; GENETIC CONSERVATION; HETEROLOGOUS EXPRESSION; HISTOPLASMA CAPSULATUM; LIPOLYSIS; MFS2 GENE; MICROCLIMATE; MORPHOGENESIS; MS95 GENE; NGT1 GENE; NGT2 GENE; NIR1 GENE; NONHUMAN; PHASE TRANSITION; RNA INTERFERENCE; SID1 GENE; SSU1 GENE; TEMPERATURE; THERMALLY DIMORPHIC FUNGI; TRANSCRIPTION REGULATION; TYR1 GENE; UPREGULATION; YPS21 GENE;

ACETYLGLUCOSAMINE; BLASTOMYCES; CANDIDA ALBICANS; CELL WALL; FUNGI; GENE EXPRESSION REGULATION, FUNGAL; GENOME, FUNGAL; HISTOPLASMA; HUMANS; MORPHOGENESIS; SIGNAL TRANSDUCTION; SOIL MICROBIOLOGY; TEMPERATURE;

EID: 84884678224     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003799     Document Type: Article

References (71)

1. Rappleye CA, Goldman WE, (2006) Defining virulence genes in the dimorphic fungi. Annu Rev Microbiol 60: 281-303.
2. Klotz SA, Drutz DJ, Huppert M, Sun SH, DeMarsh PL, (1984) The critical role of CO2 in the morphogenesis of Coccidioides immitis in cell-free subcutaneous chambers. J Infect Dis 150: 127-134.
3. Restrepo A, Salazar ME, Cano LE, Stover EP, Feldman D, et al. (1984) Estrogens inhibit mycelium-to-yeast transformation in the fungus Paracoccidioides brasiliensis: implications for resistance of females to paracoccidioidomycosis. Infect Immun 46: 346-353.
4. Sugar AM, Picard M, (1991) Macrophage- and oxidant-mediated inhibition of the ability of live Blastomyces dermatitidis conidia to transform to the pathogenic yeast phase: implications for the pathogenesis of dimorphic fungal infections. J Infect Dis 163: 371-375.
5. Maresca B, Kobayashi GS, (1989) Dimorphism in Histoplasma capsulatum: a model for the study of cell differentiation in pathogenic fungi. Microbiol Rev 53: 186-209.
6. Klein BS, Tebbets B, (2007) Dimorphism and virulence in fungi. Curr Opin Microbiol 10: 314-319.
7. Conant NF, (1941) Cultural Study of the Life-Cycle of Histoplasma capsulatum Darling 1906. J Bacteriol 41: 563-579.
8. DeMonbreun WA, (1934) The cultivation and cultural characteristics of Darling's Histoplasma capsulatum. Am J Trop Med Hyg 14: 93-125.
9. Egeberg RO, Ely AF, (1956) Coccidioides immitis in the soil of the southern San Joaquin Valley. Am J Med Sci 231: 151-154.
10. Gerald L. Mandell JEB, Raphael Dolin (2005) Mandell, Douglas, and Bennett's Principles and Practice of Infectious Diseases: Elsevier/Churchill Livingstone.
11. Hwang L, Hocking-Murray D, Bahrami AK, Andersson M, Rine J, et al. (2003) Identifying phase-specific genes in the fungal pathogen Histoplasma capsulatum using a genomic shotgun microarray. Mol Biol Cell 14: 2314-2326.
12. Nguyen VQ, Sil A, (2008) Temperature-induced switch to the pathogenic yeast form of Histoplasma capsulatum requires Ryp1, a conserved transcriptional regulator. Proc Natl Acad Sci U S A 105: 4880-4885.
13. Beyhan S, Gutierrez M, Voorhies M, Sil A, (2013) (In press) A temperature-responsive network links cell shape and virulence traits in a primary fungal pathogen. PLoS Biol.
14. Webster RH, Sil A, (2008) Conserved factors Ryp2 and Ryp3 control cell morphology and infectious spore formation in the fungal pathogen Histoplasma capsulatum. Proc Natl Acad Sci U S A 105: 14573-14578.
15. Nemecek JC, Wuthrich M, Klein BS, (2006) Global control of dimorphism and virulence in fungi. Science 312: 583-588.
16. Gauthier GM, Sullivan TD, Gallardo SS, Brandhorst TT, Vanden Wymelenberg AJ, et al. (2010) SREB, a GATA transcription factor that directs disparate fates in Blastomyces dermatitidis including morphogenesis and siderophore biosynthesis. PLoS Pathog 6: e1000846.
17. Hwang LH, Seth E, Gilmore SA, Sil A, (2012) SRE1 regulates iron-dependent and-independent pathways in the fungal pathogen Histoplasma capsulatum. Eukaryot Cell 11: 16-25.
18. Boyce KJ, Schreider L, Kirszenblat L, Andrianopoulos A, (2011) The two-component histidine kinases DrkA and SlnA are required for in vivo growth in the human pathogen Penicillium marneffei. Mol Microbiol 82: 1164-1184.
19. Maresca B, Medoff G, Schlessinger D, Kobayashi GS, (1977) Regulation of dimorphism in the pathogenic fungus Histoplasma capsulatum. Nature 266: 447-448.
20. Whiteway M, Bachewich C, (2007) Morphogenesis in Candida albicans. Annu Rev Microbiol 61: 529-553.
21. Simonetti N, Strippoli V, Cassone A, (1974) Yeast-mycelial conversion induced by N-acetyl-D-glucosamine in Candida albicans. Nature 250: 344-346.
22. Rigali S, Nothaft H, Noens EE, Schlicht M, Colson S, et al. (2006) The sugar phosphotransferase system of Streptomyces coelicolor is regulated by the GntR-family regulator DasR and links N-acetylglucosamine metabolism to the control of development. Mol Microbiol 61: 1237-1251.
23. Hart GW, Housley MP, Slawson C, (2007) Cycling of O-linked beta-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 446: 1017-1022.
24. Alvarez FJ, Konopka JB, (2007) Identification of an N-acetylglucosamine transporter that mediates hyphal induction in Candida albicans. Mol Biol Cell 18: 965-975.
25. Carratu L, Franceschelli S, Pardini CL, Kobayashi GS, Horvath I, et al. (1996) Membrane lipid perturbation modifies the set point of the temperature of heat shock response in yeast. Proc Natl Acad Sci U S A 93: 3870-3875.
26. Cook JG, Bardwell L, Thorner J, (1997) Inhibitory and activating functions for MAPK Kss1 in the S. cerevisiae filamentous-growth signalling pathway. Nature 390: 85-88.
27. Dib L, Hayek P, Sadek H, Beyrouthy B, Khalaf RA, (2008) The Candida albicans Ddr48 protein is essential for filamentation, stress response, and confers partial antifungal drug resistance. Med Sci Monit 14: BR113-121.
28. Keath EJ, Painter AA, Kobayashi GS, Medoff G, (1989) Variable expression of a yeast-phase-specific gene in Histoplasma capsulatum strains differing in thermotolerance and virulence. Infect Immun 57: 1384-1390.
29. Patel JB, Batanghari JW, Goldman WE, (1998) Probing the yeast phase-specific expression of the CBP1 gene in Histoplasma capsulatum. J Bacteriol 180: 1786-1792.
30. Abidi FE, Roh H, Keath EJ, (1998) Identification and characterization of a phase-specific, nuclear DNA binding protein from the dimorphic pathogenic fungus Histoplasma capsulatum. Infect Immun 66: 3867-3873.
31. Hwang LH, Mayfield JA, Rine J, Sil A, (2008) Histoplasma requires SID1, a member of an iron-regulated siderophore gene cluster, for host colonization. PLoS Pathog 4: e1000044.
32. Sebghati TS, Engle JT, Goldman WE, (2000) Intracellular parasitism by Histoplasma capsulatum: fungal virulence and calcium dependence. Science 290: 1368-1372.
33. Hilty J, George Smulian A, Newman SL, (2011) Histoplasma capsulatum utilizes siderophores for intracellular iron acquisition in macrophages. Med Mycol 49: 633-642.
34. Hart GW, Slawson C, Ramirez-Correa G, Lagerlof O, (2011) Cross talk between O-GlcNAcylation and phosphorylation: roles in signaling, transcription, and chronic disease. Annu Rev Biochem 80: 825-858.
35. Gunasekera A, Alvarez FJ, Douglas LM, Wang HX, Rosebrock AP, et al. (2010) Identification of GIG1, a GlcNAc-induced gene in Candida albicans needed for normal sensitivity to the chitin synthase inhibitor nikkomycin Z. Eukaryot Cell 9: 1476-1483.
36. Natarajan K, Datta A, (1993) Molecular cloning and analysis of the NAG1 cDNA coding for glucosamine-6-phosphate deaminase from Candida albicans. J Biol Chem 268: 9206-9214.
37. Yamada-Okabe T, Sakamori Y, Mio T, Yamada-Okabe H, (2001) Identification and characterization of the genes for N-acetylglucosamine kinase and N-acetylglucosamine-phosphate deacetylase in the pathogenic fungus Candida albicans. Eur J Biochem 268: 2498-2505.
38. Kumar MJ, Jamaluddin MS, Natarajan K, Kaur D, Datta A, (2000) The inducible N-acetylglucosamine catabolic pathway gene cluster in Candida albicans: discrete N-acetylglucosamine-inducible factors interact at the promoter of NAG1. Proc Natl Acad Sci U S A 97: 14218-14223.
39. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, et al. (2006) Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443: 818-822.
40. Naseem S, Gunasekera A, Araya E, Konopka JB, (2011) N-acetylglucosamine (GlcNAc) induction of hyphal morphogenesis and transcriptional responses in Candida albicans are not dependent on its metabolism. J Biol Chem 286: 28671-28680.
41. Liu H, Kohler J, Fink GR, (1994) Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266: 1723-1726.
42. Liu H, Styles CA, Fink GR, (1993) Elements of the yeast pheromone response pathway required for filamentous growth of diploids. Science 262: 1741-1744.
43. Csank C, Schroppel K, Leberer E, Harcus D, Mohamed O, et al. (1998) Roles of the Candida albicans mitogen-activated protein kinase homolog, Cek1p, in hyphal development and systemic candidiasis. Infect Immun 66: 2713-2721.
44. Banerjee S, Robbins PW, Samuelson J, (2009) Molecular characterization of nucleocytosolic O-GlcNAc transferases of Giardia lamblia and Cryptosporidium parvum. Glycobiology 19: 331-336.
45. Dennis JW, Nabi IR, Demetriou M, (2009) Metabolism, cell surface organization, and disease. Cell 139: 1229-1241.
46. Koch HU, Schwarz RT, Scholtissek C, (1979) Glucosamine itself mediates reversible inhibition of protein glycosylation. A study of glucosamine metabolism at inhibitory concentrations in influenza-virus-infected cells. Eur J Biochem 94: 515-522.
47. Lau KS, Partridge EA, Grigorian A, Silvescu CI, Reinhold VN, et al. (2007) Complex N-glycan number and degree of branching cooperate to regulate cell proliferation and differentiation. Cell 129: 123-134.
48. Veenhoff LM, Heuberger EH, Poolman B, (2002) Quaternary structure and function of transport proteins. Trends Biochem Sci 27: 242-249.
49. Levy S, Kafri M, Carmi M, Barkai N, (2011) The competitive advantage of a dual-transporter system. Science 334: 1408-1412.
50. Naderer T, Heng J, McConville MJ, (2010) Evidence that intracellular stages of Leishmania major utilize amino sugars as a major carbon source. PLoS Pathog 6: e1001245.
51. Chang DE, Smalley DJ, Tucker DL, Leatham MP, Norris WE, et al. (2004) Carbon nutrition of Escherichia coli in the mouse intestine. Proc Natl Acad Sci U S A 101: 7427-7432.
52. Baumler AJ, Kusters JG, Stojiljkovic I, Heffron F, (1994) Salmonella typhimurium loci involved in survival within macrophages. Infect Immun 62: 1623-1630.
53. Hoskins LC, Agustines M, McKee WB, Boulding ET, Kriaris M, et al. (1985) Mucin degradation in human colon ecosystems. Isolation and properties of fecal strains that degrade ABH blood group antigens and oligosaccharides from mucin glycoproteins. J Clin Invest 75: 944-953.
54. Henke JM, Bassler BL, (2004) Bacterial social engagements. Trends Cell Biol 14: 648-656.
55. Hogan DA, (2006) Talking to themselves: autoregulation and quorum sensing in fungi. Eukaryot Cell 5: 613-619.
56. Farkas V, (1979) Biosynthesis of cell walls of fungi. Microbiol Rev 43: 117-144.
57. Molano J, Bowers B, Cabib E, (1980) Distribution of chitin in the yeast cell wall. An ultrastructural and chemical study. J Cell Biol 85: 199-212.
58. Korgaonkar AK, Whiteley M, (2011) Pseudomonas aeruginosa enhances production of an antimicrobial in response to N-acetylglucosamine and peptidoglycan. J Bacteriol 193: 909-917.
59. Korgaonkar A, Trivedi U, Rumbaugh KP, Whiteley M, (2013) Community surveillance enhances Pseudomonas aeruginosa virulence during polymicrobial infection. Proc Natl Acad Sci U S A 110: 1059-1064.
60. Konopka JB, (2012) N-acetylglucosamine (GlcNAc) functions in cell signaling. Scientifica (Cairo) 2012.
61. Taylor JW, Berbee ML, (2006) Dating divergences in the Fungal Tree of Life: review and new analyses. Mycologia 98: 838-849.
62. Worsham PL, Goldman WE, (1988) Quantitative plating of Histoplasma capsulatum without addition of conditioned medium or siderophores. J Med Vet Mycol 26: 137-143.
63. Krajaejun T, Gauthier GM, Rappleye CA, Sullivan TD, Klein BS, (2007) Development and application of a green fluorescent protein sentinel system for identification of RNA interference in Blastomyces dermatitidis illuminates the role of septin in morphogenesis and sporulation. Eukaryot Cell 6: 1299-1309.
64. Sullivan TD, Rooney PJ, Klein BS, (2002) Agrobacterium tumefaciens integrates transfer DNA into single chromosomal sites of dimorphic fungi and yields homokaryotic progeny from multinucleate yeast. Eukaryot Cell 1: 895-905.
65. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
66. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
67. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, et al. (2012) MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space. Syst Biol 61: 539-542.
68. DeRisi JL, Iyer VR, Brown PO, (1997) Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278: 680-686.
69. Eisen MB, Spellman PT, Brown PO, Botstein D, (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95: 14863-14868.
70. White TC, Andrews LE, Maltby D, Agabian N, (1995) The "universal" leucine codon CTG in the secreted aspartyl proteinase 1 (SAP1) gene of Candida albicans encodes a serine in vivo. J Bacteriol 177: 2953-2955.
71. Oldenburg KR, Vo KT, Michaelis S, Paddon C, (1997) Recombination-mediated PCR-directed plasmid construction in vivo in yeast. Nucleic Acids Res 25: 451-452.