An interspecies regulatory network inferred from simultaneous RNA-seq of Candida albicans invading innate immune cells

Frontiers in Microbiology

Volumn 3, Issue MAR, 2012, Pages

  Tierney, Lanay ^a   Linde, Jörg ^b   Müller, Sebastian ^b   Brunke, Sascha ^b,c   Molina, Juan Camilo ^b   Hube, Bernhard ^b,d   Schöck, Ulrike ^e   Guthke, Reinhard ^b   Kuchler, Karl ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b HANS KNÖLL INSTITUTE   (Germany)

^c JENA UNIVERSITY HOSPITAL   (Germany)

^d FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^e GATC Biotech AG   (Germany)

Author keywords

Candida; Dendritic cells; Host pathogen; Modeling; Network inference; Reverse engineering; RNA seq

Indexed keywords

EID: 84865175959     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00085     Document Type: Article

References (81)

1. Almeida, R. S., Brunke, S., Albrecht, A., Thewes, S., Laue, M., Edwards, J. E., Filler, S. G., and Hube, B. (2008). The hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin. PLoS Pathog. 4, e1000217. doi:10.1371/journal.ppat.1000217
2. Altwasser, R., Linde, J., Buyko, E., Hahn, U., and Guthke, R. (2012). Genome-wide scale-free network inference for Candida albicans. Front. Microbiol. 3:51. doi:10.3389/fmicb.2012.00051
3. Aranda, B., Achuthan, P., Alam-Faruque, Y., Armean, I., Bridge, A., Derow, C., Feuermann, M., Ghanbarian, A. T., Kerrien, S., Khadake, J., Leroy, C., Menden, M., Michaut, M., Montecchi-Palazzi, L., Neuhauser, S. N., Orchard, S., Perreau, V., Roechert, B., van Eijk, K., and Hermjakob, H. (2010). The IntAct molecular interaction database in 2010. Nucleic Acids Res. 38,D525-D531.
4. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E., Ringwald, M., Rubin, G. M., and Sherlock, G. (2000). Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat. Genet. 25,25-29.
5. Baek, Y. U., Li, M., and Davis, D. A. (2008). Candida albicans ferric reductases are differentially regulated in response to distinct forms of iron limitation by the Rim101 and CBF transcription factors. Eukaryot. Cell 7,1168-1179.
6. Baker, L. G., Specht, C. A., Donlin, M. J., and Lodge, J. K. (2007). Chitosan, the deacetylated form of chitin, is necessary for cell wall integrity in Cryptococcus neoformans. Eukaryot. Cell 6, 855-867.
7. Barabasi, A. L., and Oltvai,Z. N. (2004). Network biology: understanding the cell's functional organization. Nat. Rev. Genet.5, 101-113.
8. Bezdek, J. (1992). Fuzzy Models for Pattern Recognition: Methods that Search for Structures in Data. New York: Institute of Electrical and Electronics Engineers (IEEE) Press.
9. Blake, J. A., Bult, C. J., Kadin, J. A., Richardson, J. E., and Eppig, J. T. (2011). The mouse genome database (MGD): premier model organism resource for mammalian genomics and genetics. Nucleic Acids Res. 39, D842-D848.
10. Bourgeois, C., Majer, O., Frohner, I., and Kuchler, K. (2009). In vitro systems for studying the interaction of fungal pathogens with primary cells from the mammalian innate immune system. Methods Mol. Biol. 470,125-139.
11. Bourgeois, C., Majer, O., Frohner, I. E., Tierney, L., and Kuchler, K. (2010). Fungal attacks on mammalian hosts: pathogen elimination requires sensing and tasting. Curr. Opin. Microbiol. 13,401-408.
12. Braun, B. R., and Johnson, A. D. (1997). Control of filament formation in Candida albicans by the transcriptional repressor TUP1. Science 277, 105-109.
13. Bulawa, C. E., Miller, D. W., Henry, L. K., and Becker, J. M. (1995). Attenuated virulence of chitindeficient mutants of Candida albicans. Proc. Natl. Acad. Sci. U.S.A. 92, 10570-10574.
14. Butte, A. J., and Kohane, I. S. (2000). Mutual information relevance networks: functional genomic clustering using pairwise entropy measurements. Pac. Symp. Biocomput. 5, 418-429.
15. Chaffin, W. L. (2008). Candida albicans cell wall proteins. Microbiol. Mol. Biol. Rev. 72, 495-544.
16. Chen, C., Pande, K., French, S. D., Tuch, B. B., and Noble, S. M. (2011). An iron homeostasis regulatory circuit with reciprocal roles in Candida albicans commensalism and pathogenesis. Cell Host Microbe 10,118-135.
17. D'Haeseleer, P., Wen, X., Fuhrman, S., and Somogyi, R. (1999). Linear modelling of mRNA expression levels during CNS development and injury. Pac. Symp. Biocomput. 4, 41-52.
18. Diniz, S. N., Nomizo, R., Cisalpino, P. S., Teixeira, M. M., Brown, G. D., Mantovani, A., Gordon, S., Reis, L. F., and Dias, A. A. (2004). PTX3 function as an opsonin for the dectin-1-dependent internaliza-tion of zymosan by macrophages. J. Leukoc. Biol. 75, 649-656.
19. Doedt, T., Krishnamurthy, S., Bock-muhl, D. P., Tebarth, B., Stempel, C., Russell, C. L., Brown, A. J., and Ernst, J. F. (2004). APSES proteins regulate morphogenesis and metabolism in Candida albicans. Mol. Biol. Cell 15, 3167-3180.
20. Faith, J. J., Hayete, B., Thaden, J. T., Mogno, I., Wierzbowski, J., Cottarel, G., Kasif, S., Collins, J. J., and Gardner, T. S. (2007). Large-scale mapping and validation of Escherichia coli transcriptional regulation from a compendium of expression profiles. PLoS Biol. 5, e8. doi:10.1371/journal.pbio.0050008
21. Feng, Q., and Zhang, Y. (2003). The NuRD complex: linking histone modification to nucleosome remodeling. Curr. Top. Microbiol. Immunol. 274, 269-290.
22. Flicek, P., Amode, M. R., Barrell, D., Beal, K., Brent, S., Chen, Y., Clapham, P., Coates, G., Fairley, S., Fitzgerald, S., Gil, L., Gordon, L., Hendrix, M., Hourlier, T., Johnson, N., Kähäri, A. K., Keefe, D., Keenan, S., Kinsella, R., Komorowska, M., Koscielny, G., Kulesha, E., Larsson, P., Longden, I., McLaren, W., Muffato, M., Over-duin, B., Pignatelli, M., Pritchard, B., Riat, H. S., Ritchie, G. R., Ruffier, M., Schuster, M., Sobral, D., Tang, Y. A., Taylor, K., Trevanion, S., Van-drovcova, J., White, S., Wilson, M., Wilder, S. P., Aken, B. L., Birney, E., Cunningham, F., Dunham, I., Durbin, R., Fernández-Suarez, X. M., Harrow, J., Herrero, J., Hubbard, T. J., Parker, A., Proctor, G., Spudich, G.,Vogel, J.,Yates,A.,Zadissa,A., and Searle, S. M. (2011). Ensembl 2011. Nucleic Acids Res. 39,D800-D806.
23. Fradin, C., De Groot, P., MacCallum, D., Schaller, M., Klis, F., Odds, E C., and Hube, B. (2005). Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol. Microbiol. 56, 397-415.
24. Friedman, S. R., Kottiri, B. J., Neaigus, A., Curtis, R., Vermund, S. H., and Des Jarlais, D. C. (2000). Network-related mechanisms may help explain long-term HIV-1 sero-prevalence levels that remain high but do not approach population-group saturation. Am. J. Epidemiol. 152,913-922.
25. Frohner, I. E., Bourgeois, C., Yatsyk, K., Majer, O., and Kuchler, K. (2009). Candida albicans cell surface superoxide dismutases degrade host-derived reactive oxygen species to escape innate immune surveillance. Mol. Microbiol. 71, 240-252.
26. Gillum, A. M., Tsay, E. Y., and Kirsch, D. R. (1984). Isolation of the Can dida albicans gene for orotidine-5'-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol. Gen. Genet. 198, 179-182.
27. Gola, S., Martin, R., Walther, A., Dunkler, A., and Wendland, J. (2003). New modules for PCR-based gene targeting in Candida albicans: rapid and efficient gene targeting using 100bp of flanking homology region. Yeast 20, 1339-1347.
28. Griffin, T. A., Barnes, M. G., Ilowite, N. T., Olson, J. C., Sherry, D. D., Gottlieb, B. S., Aronow, B. J., Pavlidis, P., Hinze, C. H., Thornton, S., Thompson, S. D., Grom, A. A., Colbert, R. A., and Glass, D. N. (2009). Gene expression signatures in polyarticular juvenile idio-pathic arthritis demonstrate disease heterogeneity and offer a molecular classification of disease subsets. Arthritis Rheum. 60,2113-2123.
29. Gudlaugsson, O., Gillespie, S., Lee, K., Vande Berg, J., Hu, J., Messer, S., Her-waldt, L., Pfaller, M., and Diekema, D. (2003). Attributable mortality of nosocomial candidemia, revisited. Clin. Infect. Dis. 37, 1172-1177.
30. Gustafsson, M., Björkengren, J., and Tegne, J. (2008). "Soft integration of data for reverse engineering," in International Conference on Systems Biology, Göteborg, 127-127.
31. Guthke, R., Albrecht, D., Brackhage, A. A., and Möller, U. (2007). Discovery of gene regulatory networks in Aspergillus fumigatus. Lect. Notes Bioinform. 4366,22-41.
32. Guthke, R., Moller, U., Hoffmann, M., Thies, F., and Topfer, S. (2005). Dynamic network reconstruction from gene expression data applied to immune response during bacterial infection. Bioinformatics 21, 1626-1634.
33. Hamon, M. A., and Cossart, P. (2008). Histone modifications and chromatin remodelling during bacterial infections. Cell Host Microbe 4, 100-109.
34. Han, Y., Kozel, T. R., Zhang, M. X., MacGill, R. S., Carroll, M. C., and Cutler, J. E. (2001). Complement is essential for protection by an IgM and an IgG3 monoclonal antibody against experimental, hematogenously disseminated candidiasis. J. Immunol. 167, 1550-1557.
35. Hardcastle, T. J., and Kelly, K. A. (2010). Bayseq: empirical Bayesian methods for identifying differential expression in sequence count data. BMC Bioinformatics 11, 422. doi:10.1186/1471-2105-11-422
36. Hecker, M., Goertsches, R. H., Engel-mann, R., Thiesen, H. J., and Guthke, R. (2009a). Integrative modelling of transcriptional regulation in response to antirheumatic therapy. BMC Bioinformatics 10, 262. doi:10.1186/1471-2105-10-262
37. Hecker, M., Lambeck, S., Toepfer, S., van Someren, E., and Guthke, R. (2009b). Gene regulatory network inference: data integration in dynamic models-a review. BioSystems 96, 86-103.
38. Hinze, C. H., Fall, N., Thornton, S., Mo, J. Q., Aronow, B. J., Layh-Schmitt, G., Griffin, T. A., Thompson, S. D., Colbert, R. A., Glass, D. N., Barnes, M. G., and Grom, A. A. (2010). Immature cell populations and an erythropoiesis gene-expression signature in systemic juvenile idio-pathic arthritis: implications for pathogenesis. Arthritis Res. Ther. 12,R123.
39. Holter, N. S., Maritan, A., Cieplak, M., Fedoroff, N. V., and Banavar, J. R. (2001). Dynamic modelling of gene expression data. Proc. Natl. Acad. Sci. U.S.A. 98, 1693-1698.
40. Hou, J., Aerts, J., den Hamer, B., van Ijcken, W., den Bakker, M., Riegman, P., van der Leest, C., van der Spek, P., Foekens, J. A., Hoogsteden, H. C., Grosveld, F., and Philipsen, S. (2010). Gene expression-based classification of non-small cell lung carcinomas and survival prediction. PLoS ONE 5, e10312. doi:10.1371/jour-nal.pone.0010312
41. Jaillon, S., Peri, G., Delneste, Y., Fre-maux, I., Doni, A., Moalli, F., Gar-landa, C., Romani, L., Gascan, H., Bellocchio, S., Bozza, S., Cassatella, M. A., Jeannin, P., and Mantovani, A. (2007). The humoral pattern recognition receptor PTX3 is stored in neutrophil granules and localizes in extracellular traps. J. Exp. Med. 204, 793-804.
42. Knight, S. A., Vilaire, G., Lesuisse, E., and Dancis, A. (2005). Iron acquisition from transferrin by Candida albicans depends on the reductive pathway. Infect. Immun. 73, 5482-5492.
43. Lane, S., Birse, C., Zhou, S., Matson, R., and Liu, H. (2001). DNA array studies demonstrate convergent regulation of virulence factors by Cph1, Cph2, and Efg1 in Candida albicans. J. Biol. Chem. 276,48988-48996.
44. Le Novere, N., Hucka, M., Mi, H., Moodie, S., Schreiber, F., Sorokin, A., Demir, E., Wegner, K., Aladjem, M. I., Wimalaratne, S. M., Bergman, E T., Gauges, R., Ghazal, P., Kawaji, H., Li, L., Matsuoka, Y., Villéger, A., Boyd, S. E., Calzone, L., Courtot, M., Dogrusoz, U., Freeman, T. C., Funahashi, A., Ghosh, S., Jouraku, A., Kim, S., Kolpakov, F., Luna, A., Sahle, S., Schmidt, E., Watterson, S., Wu, G., Goryanin, I., Kell, D. B., Sander, C., Sauro, H., Snoep, J. L., Kohn,K.,andKitano,H. (2009).The systems biology graphical notation. Nat. Biotechnol. 27, 735-741.
45. Linde, J., Wilson, D., Hube, B., and Guthke, R. (2010). Regulatory network modelling of iron acquisition by a fungal pathogen in contact with epithelial cells. BMC Syst. Biol. 4, 148. doi:10.1186/1752-0509-4-148
46. Lu, X., Kovalev, G. I., Chang, H., Kallin, E., Knudsen, G., Xia, L., Mishra, N., Ruiz, P., Li, E., Su, L., and Zhang, Y. (2008). Inactivation of NuRD component Mta2 causes abnormal T cell activation and lupus-like autoimmune disease in mice. J. Biol. Chem. 283,13825-13833.
47. Ma, Y. J., Doni, A., Skjoedt, M. O., Honore, C., Arendrup, M., Mantovani, A., and Garred, P. (2011). Het-erocomplexes of mannose-binding lectin and the pentraxins PTX3 or serum amyloid P component trigger cross-activation of the complement system. J. Biol. Chem. 286, 3405-3417.
48. Manavathi, B., Singh, K., and Kumar, R. (2007). MTA family of coregu-lators in nuclear receptor biology and pathology. Nucl. Recept. Signal 5,e010.
49. Marbach, D., Prill, R. J., Schaffter, T., Mattiussi, C., Floreano, D., and Stolovitzky, G. (2010). Revealing strengths and weaknesses of methods for gene network inference. Proc. Natl. Acad. Sci. U.S.A. 107, 6286-6291.
50. Martchenko, M., Alarco, A. M., Harcus, D.,andWhiteway, M. (2004). Super-oxide dismutases in Candida albicans: transcriptional regulation and functional characterization of the hyphal-induced SOD5 gene. Mol. Biol. Cell 15,456-467.
51. Martinou, A., Koutsioulis, D., and Bouriotis, V. (2002). Expression, purification, and characterization of a cobalt-activated chitin deacety-lase (Cda2p) from Saccharomyces cerevisiae. Protein Expr. Purif. 24, 111-116.
52. Moalli, F., Doni, A., Deban, L., Zelante, T.,Zagarella,S.,Bottazzi,B., Romani, L., Mantovani, A., and Garlanda, C. (2010). Role of complement and Fcγ receptors in the protective activity of the long pentraxin PTX3 against Aspergillus fumigatus. Blood 116,5170-5180.
53. Moalli, F., Paroni, M., Veliz Rodriguez, T., Riva, F., Polentarutti, N., Bot-tazzi, B., Valentino, S., Mantero, S., Nebuloni, M., Mantovani, A., Bragonzi, A., and Garlanda, C. (2011). The therapeutic potential of the humoral pattern recognition molecule PTX3 in chronic lung infection caused by Pseudomonas aeruginosa J. Immunol..J.186, 5425-5434.
54. Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L., and Wold, B. (2008). Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621-628.
55. Murad, A. M., Lee, P. R., Broadbent, I. D., Barelle,C.J.,andBrown,A.J. (2000). CIp10, an efficient and convenient integrating vector for Candida albicans. Yeast 16, 325-327.
56. Netea, M. G., Brown, G. D., Kullberg, B. J., and Gow, N. A. (2008). An integrated model of the recognition of Candida albicans by the innate immune system. Nat. Rev. Microbiol. 6, 67-78.
57. Nobile, C. J., Solis, N., Myers, C. L., Fay, A. J., Deneault, J. S., Nantel, A., Mitchell, A. P., and Filler, S. G. (2008). Candida albicans transcription factor Rim101 mediates pathogenic interactions through cell wall functions. Cell. Microbiol. 10, 2180-2196.
58. Oberholzer, U., Nantel, A., Berman, J., and Whiteway, M. (2006). Transcript profiles of Candida albicans cortical actin patch mutants reflect their cellular defects: contribution of the Hog1p and Mkc1p signaling pathways. Eukaryot. Cell 5, 1252-1265.
59. Park, Y. N., and Morschhäuser, J. (2005). Candida albicans MTLα tup 1Δ mutants can reversibly switch to mating-competent, filamentous growth forms. Mol. Microbiol. 58, 1288-1302.
60. Priebe, S., Linde, J., Albrecht, D., Guthke, R., and Brakhage, A. A. (2011). FungiFun: a web-based application for functional categorization of fungal genes and proteins. Fungal Genet. Biol. 48, 353-358.
61. Raman, T., O'Connor, T. P., Hackett, N. R., Wang, W., Harvey, B. G., Attiyeh, M. A., Dang, D. T., Teater, M., and Crystal, R. G. (2009). Quality control in microarray assessment of gene expression in human airway epithelium. BMC Genomics 10, 493. doi:10.1186/1471-2164-10-493
62. Rizzetto, L., and Cavalieri, D. (2011). Friend or foe: using systems biology to elucidate interactions between fungi and their hosts. Trends Microbiol. 19,509-515.
63. Rohde, J. R. (2011). Microbiology. Liste-ria unwinds host DNA. Science 331, 1271-1272.
64. Ruepp, A., Zollner, A., Maier, D., Albermann, K., Hani, J., Mokrejs, M., Tetko, I., Guldener, U., Mannhaupt, G., Munsterkotter, M., and Mewes, H. W. (2004). The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res. 32, 5539-5545.
65. Sellam, A., Al-Niemi, T., McInnerney, K., Brumfield, S., Nantel, A., and Suci,P.A. (2009). A Candida albicans early stage biofilm detachment event in rich medium. BMC Microbiol. 9, 25. doi:10.1186/1471-2180-9-25
66. Skrzypek, M. S., Arnaud, M. B., Costanzo, M. C., Inglis, D. O., Shah, P., Binkley, G., Miyasato, S. R., and Sherlock, G. (2010). New tools at the Candida genome database: biochemical pathways and full-text literature search. Nucleic Acids Res. 38, D428-D432.
67. Smith, J. J., Deane, N. G., Wu, F., Merchant, N. B., Zhang, B., Jiang, A., Lu, P., Johnson, J. C., Schmidt, C., Bailey, C. E., Eschrich, S., Kis, C., Levy, S., Washington, M. K., Hes-lin, M. J., Coffey, R. J., Yeatman, T. J., Shyr, Y., and Beauchamp, R. D. (2010). Experimentally derived metastasis gene expression profile predicts recurrence and death in patients with colon cancer. Gas-troenterology 138,958-968.
68. Spira, A., Beane, J. E., Shah, V., Steil-ing, K., Liu, G., Schembri, F., Gilman, S., Dumas, Y. M., Calner, P., Sebas-tiani, P., Sridhar, S., Beamis, J., Lamb, C., Anderson, T., Gerry, N., Keane, J., Lenburg, M. E., and Brody, J. S. (2007). Airway epithelial gene expression in the diagnostic evaluation of smokers with suspect lung cancer. Nat. Med. 13, 361-366.
69. Stark, C., Breitkreutz, B. J., Chatr-Aryamontri, A., Boucher, L., Oughtred, R., Livstone, M. S., Nixon, J., Van Auken, K., Wang, X., Shi, X., Reguly, T., Rust, J. M., Winter, A., Dolinski, K., and Tyers, M. (2011). The BioGRID interaction database: 2011 update. Nucleic Acids Res. 39, D698-D704.
70. Thewes, S., Kretschmar, M., Park, H., Schaller, M., Filler, S. G., and Hube, B. (2007). In vivo and ex vivo comparative transcriptional profiling of invasive and non-invasive Candida albicans isolates identifies genes associated with tissue invasion. Mol. Microbiol. 63, 1606-1628.
71. Toepfer, S., Guthke, R., Driesch, D., Woetzel, D., and Pfaff, M. (2007). The Net Generator algorithm: reconstruction of gene regulatory networks. Lect. Notes Bioinform. 4366, 119-130.
72. Tokuyasu, K., Ohnishi-Kameyama, M., and Hayashi, K. (1996). Purification and characterization of extracellular chin deacetylase from Colletotrichum lindemuthianum. Biosci. Biotechnol. Biochem. 60, 1598-1603.
73. Trapnell, C., Pachter, L., and Salzberg, S. L. (2009).TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111.
74. Wachtler, B., Wilson, D., Haedicke, K., Dalle, F., and Hube, B. (2011). From attachment to damage: defined genes of Candida albicans mediate adhesion, invasion and damage during interaction with oral epithelial cells. PLoS ONE 6, e 17046. doi:10.1371/journal.pone.0017046
75. Wang, Q., Diskin, S., Rappaport, E., Attiyeh, E., Mosse, Y., Shue, D., Seiser, E., Jagannathan, J., Shusterman, S., Bansal, M., Khazi, D., Winter, C., Okawa, E., Grant, G., Cnaan, A., Zhao, H., Cheung, N. K., Gerald, W., London, W., Matthay, K. K., Brodeur, G. M., and Maris, J. M. (2006). Integrative genomics identifies distinct molecular classes of neuroblastoma and shows that multiple genes are targeted by regional alterations in DNA copy number. Cancer Res. 66, 6050-6062.
76. Wang, Z., Gerstein, M., and Snyder, M. (2009). RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10, 57-63.
77. Werhli, A. V., and Husmeier, D. (2007). Reconstructing gene regulatory networks with Bayesian networks by combining expression data with multiple sources of prior knowledge. Stat. Appl. Genet. Mol. Biol. 6,15.
78. Zakikhany, K., Naglik, J. R., Schmidt-Westhausen, A., Holland, G., Schaller, M., and Hube, B. (2007). In vivo transcript profiling of Candida albicans identifies a gene essential for interepithelial dissemination. Cell. Microbiol. 9, 2938-2954.
79. Zhang, J., Chiodini, R., Badr, A., and Zhang, G. (2011). The impact of next-generation sequencing on genomics. J. Genet Genomics 38, 95-109.
80. Zhao, X., Oh, S. H., Cheng, G., Green, C. B., Nuessen, J. A., Yeater, K., Leng, R. P., Brown, A. J., and Hoyer, L. L. (2004). ALS3 and ALS8 represent a single locus that encodes a Candida albicans adhesin; functional comparisons between Als3p and Als1p. Microbiology 150,2415-2428.
81. Zhao, Y., Park, R. D., and Muzzarelli, R. A. (2010). Chitin deacetylases: properties and applications. Mar. Drugs 8, 24-46.