Expression of Paracoccidioides brasiliensis AMY1 in a Histoplasma capsulatum amy1 Mutant, Relates an α-(1,4)-Amylase to Cell Wall α-(1,3)-Glucan Synthesis

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Camacho, Emma ^a   Sepulveda, Victoria E ^b,c   Goldman, William E ^b   San Blas, Gioconda ^a   Niño Vega, Gustavo A ^a  

^a Instituto Venezolano de Investigaciones Cientificas Centro de Microbiologia y Biologia Celular   (Venezuela)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA (1,3) GLUCAN; ALPHA (1,4) AMYLASE; AMYLASE; AMYLOPEPTIN; OLIGOSACCHARIDE; STARCH; UNCLASSIFIED DRUG;

AMY1 GENE; ARTICLE; CARBOHYDRATE SYNTHESIS; CELL WALL; CONTROLLED STUDY; ENZYME ACTIVITY; FUNGAL GENE; FUNGAL VIRULENCE; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENETIC COMPLEMENTATION; GENETIC TRANSCRIPTION; HISTOPLASMA CAPSULATUM; HYDROLYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PARACOCCIDIOIDES BRASILIENSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION;

ALPHA-AMYLASES; AMINO ACID SEQUENCE; AMYLOPECTIN; CELL WALL; FUNGAL PROTEINS; GENE EXPRESSION; GENETIC COMPLEMENTATION TEST; GLUCANS; HISTOPLASMA; MOLECULAR SEQUENCE DATA; MUTATION; PARACOCCIDIOIDES; PHYLOGENY; SEQUENCE ALIGNMENT; STARCH; SUBSTRATE SPECIFICITY; VIRULENCE;

AJELLOMYCES CAPSULATUS; AJELLOMYCES DERMATITIDIS; PARACOCCIDIOIDES BRASILIENSIS;

EID: 84869837385     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050201     Document Type: Article

References (55)

1. San-Blas G, Nino-Vega G, Iturriaga T, (2002) Paracoccidioides brasiliensis and paracoccidioidomycosis: molecular approaches to morphogenesis, diagnosis, epidemiology, taxonomy and genetics. Med Mycol 40: 225-242.
2. Matute DR, McEwen JG, Puccia R, Montes BA, San-Blas G, et al. (2006) Cryptic speciation and recombination in the fungus Paracoccidioides brasiliensis as revealed by gene genealogies. Mol Biol Evol 23: 65-73.
3. Theodoro RC, Teixeira Mde M, Felipe MS, Paduan Kdos S, Ribolla PM, et al. (2012) Genus Paracoccidioides: species recognition and biogeographic aspects. PLOS ONE 7: e37694.
4. Brummer E, Castaneda E, Restrepo A, (1993) Paracoccidioidomycosis: an update. Clin Microbiol Rev 6: 89-117.
5. Kanetsuna F, Carbonell LM, Gil F, Azuma I, (1974) Chemical and ultrastructural studies on the cell walls of the yeastlike and mycelial forms of Histoplasma capsulatum. Mycopathol Mycol Appl 54: 1-13.
6. Hogan LH, Klein BS, (1994) Altered expression of surface alpha-1,3-glucan in genetically related strains of Blastomyces dermatitidis that differ in virulence. Infect Immun 62: 3543-3546.
7. Reese AJ, Doering TL, (2003) Cell wall alpha-1,3-glucan is required to anchor the Cryptococcus neoformans capsule. Mol Microbiol 50: 1401-1409.
8. Fontaine T, Simenel C, Dubreucq G, Adam O, Delepierre M, et al. (2000) Molecular organization of the alkali-insoluble fraction of Aspergillus fumigatus cell wall. J Biol Chem 275: 27594-27607.
9. Carbonell LM, Kanetsuna F, Gil F, (1970) Chemical morphology of glucan and chitin in the cell wall of the yeast phase of Paracoccidioides brasiliensis. J Bacteriol 101: 636-642.
10. Sorais F, Barreto L, Leal JA, Bernabe M, San-Blas G, et al. (2010) Cell wall glucan synthases and GTPases in Paracoccidioides brasiliensis. Med Mycol 48: 35-47.
11. Rappleye CA, Engle JT, Goldman WE, (2004) RNA interference in Histoplasma capsulatum demonstrates a role for alpha-(1,3)-glucan in virulence. Mol Microbiol 53: 153-165.
12. San-Blas G, San-Blas F, Serrano LE, (1977) Host-parasite relationships in the yeastlike form of Paracoccidioides brasiliensis strain IVIC Pb9. Infect Immun 15: 343-346.
13. Katayama S, Hirata D, Arellano M, Perez P, Toda T, (1999) Fission yeast alpha-glucan synthase Mok1 requires the actin cytoskeleton to localize the sites of growth and plays an essential role in cell morphogenesis downstream of protein kinase C function. J Cell Biol 144: 1173-1186.
14. Hochstenbach F, Klis FM, van den Ende H, van Donselaar E, Peters PJ, et al. (1998) Identification of a putative alpha-glucan synthase essential for cell wall construction and morphogenesis in fission yeast. PNAS 95: 9161-9166.
15. Garcia I, Tajadura V, Martin V, Toda T, Sanchez Y, (2006) Synthesis of alpha-glucans in fission yeast spores is carried out by three alpha-glucan synthase paralogues, Mok12p, Mok13p and Mok14p. Mol Microbiol 59: 836-853.
16. Grun CH, Hochstenbach F, Humbel BM, Verkleij AJ, Sietsma JH, et al. (2005) The structure of cell wall alpha-glucan from fission yeast. Glycobiology 15: 245-257.
17. Kuriki T, Imanaka T, (1999) The concept of the alpha-amylase family: structural similarity and common catalytic mechanism. J Biosci Bioeng 87: 557-565.
18. MacGregor EA, Janecek S, Svensson B, (2001) Relationship of sequence and structure to specificity in the alpha-amylase family of enzymes. Biochim Biophys Acta 1546: 1-20.
19. Davies GJ, Wilson KS, (1999) Trapped in the act of catalysis. Nat Struct Biol 6: 406-408.
20. Morita T, Tanaka N, Hosomi A, Giga-Hama Y, Takegawa K, (2006) An alpha-amylase homologue, aah3, encodes a GPI-anchored membrane protein required for cell wall integrity and morphogenesis in Schizosaccharomyces pombe. Biosci Biotech Biochem 70: 1454-1463.
21. Yuan XL, van der Kaaij RM, van den Hondel CA, Punt PJ, van der Maarel MJ, et al. (2008) Aspergillus niger genome-wide analysis reveals a large number of novel alpha-glucan acting enzymes with unexpected expression profiles. Mol Genet Genom 279: 545-561.
22. van der Kaaij RM, Yuan XL, Franken A, Ram AF, Punt PJ, et al. (2007) Two novel, putatively cell wall-associated and glycosylphosphatidylinositol-anchored alpha-glucanotransferase enzymes of Aspergillus niger. Eukaryot Cell 6: 1178-1188.
23. Marion CL, Rappleye CA, Engle JT, Goldman WE, (2006) An alpha-(1,4)-amylase is essential for alpha-(1,3)-glucan production and virulence in Histoplasma capsulatum. Mol Microbiol 62: 970-983.
24. van der Kaaij RM, Janecek S, van der Maarel MJ, Dijkhuizen L, (2007) Phylogenetic and biochemical characterization of a novel cluster of intracellular fungal alpha-amylase enzymes. Microbiology 153: 4003-4015.
25. Keller NP, Hohn TM, (1997) Metabolic pathway gene clusters in filamentous fungi. Fungal Genet Biol 21: 17-29.
26. Worsham PL, Goldman WE, (1988) Quantitative plating of Histoplasma capsulatum without addition of conditioned medium or siderophores. Med Mycol 26: 137-143.
27. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL, (2006) GenBank. Nucleic Acids Res 34: D16-20.
28. Wu CH, Apweiler R, Bairoch A, Natale DA, Barker WC, et al. (2006) The Universal Protein Resource (UniProt): an expanding universe of protein information. Nucleic Acids Res 34: D187-191.
29. Da Lage JL, Feller G, Janecek S, (2004) Horizontal gene transfer from Eukarya to bacteria and domain shuffling: the alpha-amylase model. Cel Mol Life Sciences 61: 97-109.
30. Saitou N, Nei M, (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
31. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
32. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
33. Woods JP, Heinecke EL, Goldman WE, (1998) Electrotransformation and expression of bacterial genes encoding hygromycin phosphotransferase and beta-galactosidase in the pathogenic fungus Histoplasma capsulatum. Infect Immun 66: 1697-1707.
34. Kanetsuna F, Carbonell LM, Azuma I, Yamamura Y, (1972) Biochemical studies on the thermal dimorphism of Paracoccidioides brasiliensis. J Bacteriol 110: 208-218.
35. Ashwell G, (1957) Colorimetric analysis of sugars. Methods Enzymol 3: 73-103.
36. Eissenberg LG, Schlesinger PH, Goldman WE, (1988) Phagosome-lysosome fusion in P388D1 macrophages infected with Histoplasma capsulatum. J Leukocyte Biol 43: 483-491.
37. Sebghati TS, Engle JT, Goldman WE, (2000) Intracellular parasitism by Histoplasma capsulatum: fungal virulence and calcium dependence. Science 290: 1368-1372.
38. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
39. Randez-Gil F, Sanz P, (1993) Expression of Aspergillus oryzae alpha-amylase gene in Saccharomyces cerevisiae. FEMS Microbiol Letters 112: 119-123.
40. Bendtsen JD, Nielsen H, von Heijne G, Brunak S, (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795.
41. Janecek S, (1997) alpha-Amylase family: molecular biology and evolution. Progr Biophys Mol Biol 67: 67-97.
42. de Lourdes Corradi da Silva M, Fukuda EK, Vasconcelos AF, Dekker RF, Matias AC, et al. (2008) Structural characterization of the cell wall D-glucans isolated from the mycelium of Botryosphaeria rhodina MAMB-05. Carbohydr Res 343: 793-798.
43. Liu Y, Himmelsbach DS, Barton FE 2nd (2004) Two-dimensional Fourier transform Raman correlation spectroscopy determination of the glycosidic linkages in amylose and amylopectin. App Spectros 58: 745-749.
44. Adt I, Toubas D, Pinon JM, Manfait M, Sockalingum GD, (2006) FTIR spectroscopy as a potential tool to analyse structural modifications during morphogenesis of Candida albicans. Arch Microbiol 185: 277-285.
45. Stam MR, Danchin EG, Rancurel C, Coutinho PM, Henrissat B, (2006) Dividing the large glycoside hydrolase family 13 into subfamilies: towards improved functional annotations of alpha-amylase-related proteins. Prot Eng Design Select 19: 555-562.
46. Vallejo MC, Nakayasu ES, Matsuo AL, Sobreira TJ, Longo LV, et al. (2012) Vesicle and vesicle-free extracellular proteome of Paracoccidioides brasiliensis: comparative analysis with other pathogenic fungi. J Proteom Res 11: 1676-1685.
47. Holbrook ED, Edwards JA, Youseff BH, Rappleye CA, (2011) Definition of the extracellular proteome of pathogenic-phase Histoplasma capsulatum. J Proteom Res 10: 1929-1943.
48. Benoliel B, Arraes FB, Reis VC, Siqueira SJ, Parachin NS, et al. (2005) Hydrolytic enzymes in Paracoccidioides brasiliensis-ecological aspects. Gen Mol Res 4: 450-461.
49. Teixeira MM, Theodoro RC, de Carvalho MJ, Fernandes L, Paes HC, et al. (2009) Phylogenetic analysis reveals a high level of speciation in the Paracoccidioides genus. Mol Phylogenet Res 52: 273-283.
50. Kanetsuna F, Carbonell LM, Moreno RE, Rodriguez J, (1969) Cell wall composition of the yeast and mycelial forms of Paracoccidioides brasiliensis. J Bacteriol 97: 1036-1041.
51. Rappleye CA, Eissenberg LG, Goldman WE, (2007) Histoplasma capsulatum alpha-(1,3)-glucan blocks innate immune recognition by the beta-glucan receptor. PNAS 104: 1366-1370.
52. Nino-Vega GA, Munro CA, San-Blas G, Gooday GW, Gow NA, (2000) Differential expression of chitin synthase genes during temperature-induced dimorphic transitions in Paracoccidioides brasiliensis. Med Mycol 38: 31-39.
53. Zekovic DB, Kwiatkowski S, Vrvic MM, Jakovljevic D, Moran CA, (2005) Natural and modified (1->3)-beta-D-glucans in health promotion and disease alleviation. Critical Rev Biotech 25: 205-230.
54. Ram AF, Kapteyn JC, Montijn RC, Caro LH, Douwes JE, et al. (1998) Loss of the plasma membrane-bound protein Gas1p in Saccharomyces cerevisiae results in the release of beta1,3-glucan into the medium and induces a compensation mechanism to ensure cell wall integrity. J Bacteriol 180: 1418-1424.
55. Walker LA, Gow NA, Munro CA, (2010) Fungal echinocandin resistance. Fungal Genet Biol 47: 117-126.