The Cryptococcus neoformans transcriptome at the site of human meningitis

mBio

Volumn 5, Issue 1, 2014, Pages

  Chen, Yuan ^a   Toffaletti, Dena L ^a   Tenor, Jennifer L ^a   Litvintseva, Anastasia P ^a   Fang, Charles ^a   Mitchell, Thomas G ^a   McDonald, Tami R ^b   Nielsen, Kirsten ^b   Boulware, David R ^b   Bicanic, Tihana ^c   Perfect, John R ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c ST GEORGE S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL RNA; TRANSCRIPTOME;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ARTICLE; CASE REPORT; CEREBROSPINAL FLUID; CFO1 GENE; CONTROLLED STUDY; CRYPTOCOCCAL MENINGITIS; CRYPTOCOCCUS NEOFORMANS; ENA1 GENE; EX VIVO STUDY; FUNGAL GENE; FUNGAL VIRULENCE; FUNGUS GROWTH; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC VARIABILITY; HUMAN; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RIM101 GENE; RNA SEQUENCE; STRAIN DIFFERENCE; UPREGULATION; YEAST CELL;

CEREBROSPINAL FLUID; CRYPTOCOCCUS NEOFORMANS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HIV INFECTIONS; HUMANS; MENINGITIS, CRYPTOCOCCAL; RNA, FUNGAL; TRANSCRIPTOME;

EID: 84903362731     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01087-13     Document Type: Article

References (67)

1. Park BJ, Wannemuehler KA, Marston BJ, Govender N, Pappas PG, Chiller TM. 2009. Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 23:525-530. http://dx.doi.org/10.1097/QAD.0b013e328322ffac.
2. Heitman J. 2011. Cryptococcus: from human pathogen to model yeast. American Society for Microbiology, Washington, DC.
3. Chun CD, Brown JC, Madhani HD. 2011. A major role for capsuleindependent phagocytosis-inhibitory mechanisms in mammalian infection by Cryptococcus neoformans. Cell Host Microbe 9:243-251. http:// dx.doi.org/10.1016/j.chom.2011.02.003.
4. Ngamskulrungroj P, Price J, Sorrell T, Perfect JR, Meyer W. 2011. Cryptococcus gattii virulence composite: candidate genes revealed by microarray analysis of high and less virulent Vancouver Island outbreak strains. PLoS One 6:e16076. http://dx.doi.org/10.1371/ journal.pone.0016076.
5. Kmetzsch L, Staats CC, Simon E, Fonseca FL, Oliveira DL, Joffe LS, Rodrigues J, Lourenço RF, Gomes SL, Nimrichter L, Rodrigues ML, Schrank A, Vainstein MH. 2011. The GATA-type transcriptional activator Gat1 regulates nitrogen uptake and metabolism in the human pathogen Cryptococcus neoformans. Fungal Genet. Biol. 48:192-199. http:// dx.doi.org/10.1016/j.fgb.2010.07.011.
6. Kronstad J, Saikia S, Nielson ED, Kretschmer M, Jung W, Hu G, Geddes JM, Griffiths EJ, Choi J, Cadieux B, Caza M, Attarian R. 2012. Adaptation of Cryptococcus neoformans to mammalian hosts: integrated regulation of metabolism and virulence. Eukaryot. Cell 11:109-118. http://dx.doi.org/10.1128/EC.05273-11.
7. Chaturvedi V, Nierman WC. 2012. Cryptococcus gattii comparative genomics and transcriptomics: a NIH/NIAID white paper. Mycopathologia 173:367-373. http://dx.doi.org/10.1007/s11046-011-9512-9.
8. Kraus PR, Boily MJ, Giles SS, Stajich JE, Allen A, Cox GM, Dietrich FS, Perfect JR, Heitman J. 2004. Identification of Cryptococcus neoformans temperature-regulated genes with a genomic-DNA microarray. Eukaryot. Cell 3:1249-1260. http://dx.doi.org/10.1128/EC.3.5.1249-1260.2004.
9. Chow ED, Liu OW, O'Brien S, Madhani HD. 2007. Exploration of whole-genome responses of the human AIDS-associated yeast pathogen Cryptococcus neoformans var. grubii: nitric oxide stress and body temperature. Curr. Genet. 52:137-148. http://dx.doi.org/10.1007/s00294-007-0147-9.
10. Jung WH, Saikia S, Hu G, Wang J, Fung CK, D'Souza C, White R, Kronstad JW. 2010. HapX positively and negatively regulates the transcriptional response to iron deprivation in Cryptococcus neoformans. PLoS Pathog. 6:e1001209. http://dx.doi.org/10.1371/journal.ppat.1001209.
11. Haynes BC, Skowyra ML, Spencer SJ, Gish SR, Williams M, Held EP, Brent MR, Doering TL. 2011. Toward an integrated model of capsule regulation in Cryptococcus neoformans. PLoS Pathog. 7:e1002411. http:// dx.doi.org/10.1371/journal.ppat.1002411.
12. 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. http://dx.doi.org/ 10.1128/EC.4.1.190-201.2005.
13. Song MH, Lee JW, Kim MS, Yoon JK, White TC, Floyd A, Heitman J, Strain AK, Nielsen JN, Nielsen K, Bahn YS. 2012. A flucytosineresponsive Mbp1/Swi4-like protein, Mbs1, plays pleiotropic roles in antifungal drug resistance, stress response, and virulence of Cryptococcus neoformans. Eukaryot. Cell 11:53-67.
14. Fan W, Kraus PR, Boily MJ, Heitman J. 2005. Cryptococcus neoformans gene expression during murine macrophage infection. Eukaryot. Cell 4:1420-1433. http://dx.doi.org/10.1128/EC.4.8.1420-1433.2005.
15. Hu G, Cheng PY, Sham A, Perfect JR, Kronstad JW. 2008. Metabolic adaptation in Cryptococcus neoformans during early murine pulmonary infection. Mol. Microbiol. 69:1456-1475. http://dx.doi.org/10.1111/ j.1365-2958.2008.06374.x.
16. Litvintseva AP, Mitchell TG. 2012. Population genetic analyses reveal the African origin and strain variation of Cryptococcus neoformans var. grubii. PLoS Pathog. 8:e1002495. http://dx.doi.org/10.1371/ journal.ppat.1002495.
17. Rude TH, Toffaletti DL, Cox GM, Perfect JR. 2002. Relationship of the glyoxylate pathway to the pathogenesis of Cryptococcus neoformans. Infect. Immun. 70:5684-5694. http://dx.doi.org/10.1128/IAI.70.10.5684-5694.2002.
18. Steen BR, Zuyderduyn S, Toffaletti DL, Marra M, Jones SJ, Perfect JR, Kronstad J. 2003. Cryptococcus neoformans gene expression during experimental cryptococcal meningitis. Eukaryot. Cell 2:1336-1349. http:// dx.doi.org/10.1128/EC.2.6.1336-1349.2003.
19. Ngamskulrungroj P, Gilgado F, Faganello J, Litvintseva AP, Leal AL, Tsui KM, Mitchell TG, Vainstein MH, Meyer W. 2009. Genetic diversity of the Cryptococcus species complex suggests that Cryptococcus gattii deserves to have varieties. PLoS One 4:e5862. http://dx.doi.org/10.1371/ journal.pone.0005862.
20. Petzold EW, Himmelreich U, Mylonakis E, Rude T, Toffaletti D, Cox GM, Miller JL, Perfect JR. 2006. Characterization and regulation of the trehalose synthesis pathway and its importance in the pathogenicity of Cryptococcus neoformans. Infect. Immun. 74:5877-5887. http:// dx.doi.org/10.1128/IAI.00624-06.
21. Litvintseva AP, Carbone I, Rossouw J, Thakur R, Govender NP, Mitchell TG. 2011. Evidence that the human pathogenic fungus Cryptococcus neoformans var. grubii may have evolved in Africa. PLoS One 6:e19688. http://dx.doi.org/10.1371/journal.pone.0019688.
22. Litvintseva AP, Thakur R, Vilgalys R, Mitchell TG. 2006. Multilocus sequence typing reveals three genetic subpopulations of Cryptococcus neoformans var. grubii (serotype A), including a unique population in Botswana. Genetics 172:2223-2238.
23. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25. http://dx.doi.org/10.1186/gb-2009-10-3-r25.
24. Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105-1111. http:// dx.doi.org/10.1093/bioinformatics/btp120.
25. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28:511-515. http:// dx.doi.org/10.1038/nbt.1621.
26. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol. 11:R106. http://dx.doi.org/10.1186/gb-2010-11-10-r106.
27. Team RDC. 2008. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
28. Bovers M, Hagen F, Kuramae EE, Boekhout T. 2008. Six monophyletic lineages identified within Cryptococcus neoformans and Cryptococcus gattii by multi-locus sequence typing. Fungal Genet. Biol. 45:400-421. http:// dx.doi.org/10.1016/j.fgb.2007.12.004.
29. Meyer W, Castañeda A, Jackson S, Huynh M, Castañeda E, IberoAmerican Cryptococcal Study Group. 2003. Molecular typing of IberoAmerican Cryptococcus neoformans isolates. Emerg. Infect. Dis. 9:189-195.
30. Jung WH, Hu G, Kuo W, Kronstad JW. 2009. Role of ferroxidases in iron uptake and virulence of Cryptococcus neoformans. Eukaryot. Cell 8:1511-1520. http://dx.doi.org/10.1128/EC.00166-09.
31. Idnurm A, Walton FJ, Floyd A, Reedy JL, Heitman J. 2009. Identification of ENA1 as a virulence gene of the human pathogenic fungus Cryptococcus neoformans through signature-tagged insertional mutagenesis. Eukaryot. Cell 8:315-326. http://dx.doi.org/10.1128/EC.00375-08.
32. Jang HH, Lee KO, Chi YH, Jung BG, Park SK, Park JH, Lee JR, Lee SS, Moon JC, Yun JW, Choi YO, Kim WY, Kang JS, Cheong GW, Yun DJ, Rhee SG, Cho MJ, Lee SY. 2004. Two enzymes in one; two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell 117:625-635. http://dx.doi.org/ 10.1016/j.cell.2004.05.002.
33. O'Meara TR, Norton D, Price MS, Hay C, Clements MF, Nichols CB, Alspaugh JA. 2010. Interaction of Cryptococcus neoformans Rim101 and protein kinase A regulates capsule. PLoS Pathog. 6:e1000776. http:// dx.doi.org/10.1371/journal.ppat.1000776.
34. Liu OW, Chun CD, Chow ED, Chen C, Madhani HD, Noble SM. 2008. Systematic genetic analysis of virulence in the human fungal pathogen Cryptococcus neoformans. Cell 135:174-188. http://dx.doi.org/10.1016/ j.cell.2008.07.046.
35. Soriano FX, Baxter P, Murray LM, Sporn MB, Gillingwater TH, Hardingham GE. 2009. Transcriptional regulation of the AP-1 and Nrf2 target gene sulfiredoxin. Mol. Cells 27:279-282. http://dx.doi.org/10.1007/ s10059-009-0050-y.
36. Biteau B, Labarre J, Toledano MB. 2003. ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425: 980-984. http://dx.doi.org/10.1038/nature02075.
37. Tangen KL, Jung WH, Sham AP, Lian T, Kronstad JW. 2007. The ironand cAMP-regulated gene SIT1 influences ferrioxamine B utilization, melanization and cell wall structure in Cryptococcus neoformans. Microbiology 153:29-41.
38. Heymann P, Gerads M, Schaller M, Dromer F, Winkelmann G, Ernst JF. 2002. The siderophore iron transporter of Candida albicans (Sit1p/ Arn1p) mediates uptake of ferrichrome-type siderophores and is required for epithelial invasion. Infect. Immun. 70:5246-5255. http://dx.doi.org/ 10.1128/IAI.70.9.5246-5255.2002.
39. Yang P, Yang C, Wirschell M, Davis S. 2009. Novel LC8 mutations have disparate effects on the assembly and stability of flagellar complexes. J. Biol. Chem. 284:31412-31421. http://dx.doi.org/10.1074/ jbc.M109.050666.
40. Florent M, Noël T, Ruprich-Robert G, Da Silva B, Fitton-Ouhabi V, Chastin C, Papon N, Chapeland-Leclerc F. 2009. Nonsense and missense mutations in FCY2 and FCY1 genes are responsible for flucytosine resistance and flucytosine-fluconazole cross-resistance in clinical isolates of Candida lusitaniae. Antimicrob. Agents Chemother. 53:2982-2990. http://dx.doi.org/10.1128/AAC.00880-08.
41. Arai K, Morishita K, Shinmura K, Kohno T, Kim SR, Nohmi T, Taniwaki M, Ohwada S, Yokota J. 1997. Cloning of a human homolog of the yeast OGG1 gene that is involved in the repair of oxidative DNA damage. Oncogene 14:2857-2861. http://dx.doi.org/10.1038/ sj.onc.1201139.
42. Dujon B, Sherman D, Fischer G, Durrens P, Casaregola S, Lafontaine I, de Montigny J, Marck C, Neuvéglise C, Talla E, Goffard N, Frangeul L, Aigle M, Anthouard V, Babour A, Barbe V, Barnay S, Blanchin S, Beckerich JM, Beyne E, Bleykasten C, Boisramé A, Boyer J, Cattolico L, Confanioleri F, de Daruvar A, Despons L, Fabre E, Fairhead C, Ferry-Dumazet H, Groppi A, Hantraye F, Hennequin C, Jauniaux N, Joyet P, Kachouri R, Kerrest A, Koszul R, Lemaire M, Lesur I, Ma L, Muller H, Nicaud J-M, Nikolski M, Oztas S, Ozier-Kalogeropoulos O, Pellenz S, Potier S, Richard G-F, Straub M-L, Suleau A, Swennen D, Tekaia F, Wésolowski-Louvel M, Westhof E, Wirth B, Zeniou-Meyer M, Zivanovic I, Bolotin-Fukuhara M, Thierry A, Bouchier C, Caudron B, Scarpelli C, Gaillardin C, Weissenbach J, Wincker P, Souciet J-L. 2004. Genome evolution in yeasts. Nature 430:35-44. http://dx.doi.org/ 10.1038/nature02579.
43. Kemen E, Gardiner A, Schultz-Larsen T, Kemen AC, Balmuth AL, Robert-Seilaniantz A, Bailey K, Holub E, Studholme DJ, MacLean D, Jones JD. 2011. Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. PLOS Biol. 9:e1001094. http://dx.doi.org/10.1371/journal.pbio.1001094.
44. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29:644-652. http://dx.doi.org/10.1038/nbt.1883.
45. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674-3676. http:// dx.doi.org/10.1093/bioinformatics/bti610.
46. Nookaew I, Papini M, Pornputtapong N, Scalcinati G, Fagerberg L, Uhlén M, Nielsen J. 2012. A comprehensive comparison of RNA-Seqbased transcriptome analysis from reads to differential gene expression and cross-comparison with microarrays: a case study in Saccharomyces cerevisiae. Nucleic Acids Res. 40:10084-10097. http://dx.doi.org/10.1093/ nar/gks804.
47. Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y. 2008. RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res. 18:1509-1517. http://dx.doi.org/10.1101/ gr.079558.108.
48. Lee A, Toffaletti DL, Tenor J, Soderblom EJ, Thompson JW, Moseley MA, Price M, Perfect JR. 2010. Survival defects of Cryptococcus neoformans mutants exposed to human cerebrospinal fluid result in attenuated virulence in an experimental model of meningitis. Infect. Immun. 78: 4213-4225. http://dx.doi.org/10.1128/IAI.00551-10.
49. Bicanic T, Muzoora C, Brouwer AE, Meintjes G, Longley N, Taseera K, Rebe K, Loyse A, Jarvis J, Bekker LG, Wood R, Limmathurotsakul D, Chierakul W, Stepniewska K, White NJ, Jaffar S, Harrison TS. 2009. Independent association between rate of clearance of infection and clinical outcome of HIV-associated cryptococcal meningitis: analysis of a combined cohort of 262 patients. Clin. Infect. Dis. 49:702-709. http:// dx.doi.org/10.1086/604716.
50. Perfect JR, Lang SD, Durack DT. 1980. Chronic cryptococcal meningitis: a new experimental model in rabbits. Am. J. Pathol. 101:177-194.
51. Stajich JE, Harris T, Brunk BP, Brestelli J, Fischer S, Harb OS, Kissinger JC, Li W, Nayak V, Pinney DF, Stoeckert CJ, Roos DS. 2012. FungiDB: an integrated functional genomics database for fungi. Nucleic Acids Res. 40:D675-D681. http://dx.doi.org/10.1093/nar/gkr918.
52. Cheng S, Clancy CJ, Xu W, Schneider F, Hao B, Mitchell AP, Nguyen MH. 2013. Profiling of Candida albicans gene expression during intraabdominal candidiasis identifies biologic processes involved in pathogenesis. J. Infect. Dis. 208:1529-1537. http://dx.doi.org/10.1093/infdis/jit335.
53. Zhang YE, Landback P, Vibranovski MD, Long M. 2011. Accelerated recruitment of new brain development genes into the human genome. PLoS Biol. 9:e1001179. http://dx.doi.org/10.1371/journal.pbio.1001179.
54. Liu X, Hu G, Panepinto J, Williamson PR. 2006. Role of a VPS41 homologue in starvation response, intracellular survival and virulence of Cryptococcus neoformans. Mol. Microbiol. 61:1132-1146. http:// dx.doi.org/10.1111/j.1365-2958.2006.05299.x.
55. Sanguinetti M, Posteraro B, La Sorda M, Torelli R, Fiori B, Santangelo R, Delogu G, Fadda G. 2006. Role of AFR1, an ABC transporter-encoding gene, in the in vivo response to fluconazole and virulence of Cryptococcus neoformans. Infect. Immun. 74:1352-1359. http://dx.doi.org/10.1128/ IAI.74.2.1352-1359.2006.
56. Posteraro B, Sanguinetti M, Sanglard D, La Sorda M, Boccia S, Romano L, Morace G, Fadda G. 2003. Identification and characterization of a Cryptococcus neoformans ATP binding cassette (ABC) transporterencoding gene, CnAFR1, involved in the resistance to fluconazole. Mol. Microbiol. 47:357-371. http://dx.doi.org/10.1046/j.1365-2958.2003.03281.x.
57. Bissinger PH, Kuchler K. 1994. Molecular cloning and expression of the Saccharomyces cerevisiae STS1 gene product. A yeast ABC transporter conferring mycotoxin resistance. J. Biol. Chem. 269:4180-4186.
58. Jung KW, Strain AK, Nielsen K, Jung KH, Bahn YS. 2012. Two cation transporters Ena1 and Nha1 cooperatively modulate ion homeostasis, antifungal drug resistance, and virulence of Cryptococcus neoformans via the HOG pathway. Fungal Genet. Biol. 49:332-345. http://dx.doi.org/ 10.1016/j.fgb.2012.02.001.
59. Small JM, Mitchell TG, Wheat RW. 1986. Strain variation in composition and molecular size of the capsular polysaccharide of Cryptococcus neoformans serotype A. Infect. Immun. 54:735-741.
60. Monk BC, Goffeau A. 2008. Outwitting multidrug resistance to antifungals. Science 321:367-369. http://dx.doi.org/10.1126/science.1159746.
61. Lengeler KB, Wang P, Cox GM, Perfect JR, Heitman J. 2000. Identification of the MATa mating-type locus of Cryptococcus neoformans reveals a serotype A MATa strain thought to have been extinct. Proc. Natl. Acad. Sci. U. S. A. 97:14455-14460. http://dx.doi.org/10.1073/ pnas.97.26.14455.
62. Meyer W, Aanensen DM, Boekhout T, Cogliati M, Diaz MR, Esposto MC, Fisher M, Gilgado F, Hagen F, Kaocharoen S, Litvintseva AP, Mitchell TG, Simwami SP, Trilles L, Viviani MA, Kwon-Chung J. 2009. Consensus multi-locus sequence typing scheme for Cryptococcus neoformans and Cryptococcus gattii. Med. Mycol. 47:561-570. http://dx.doi.org/ 10.1080/13693780902953886.
63. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. http://dx.doi.org/10.1093/bioinformatics/ btm404.
64. Berlocher SH, Swofford DL. 1997. Searching for phylogenetic trees under the frequency parsimony criterion: an approximation using generalized parsimony. Syst. Biol. 46:211-215.
65. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B Stat. Methodol. 57:289-300.
66. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, McKenna A, Fennell TJ, Kernytsky AM, Sivachenko AY, Cibulskis K, Gabriel SB, Altshuler D, Daly MJ. 2011. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43:491-498. http://dx.doi.org/10.1038/ng.806.
67. Kent WJ. 2002. BLAT-the BLAST-like alignment tool. Genome Res. 12:656-664. http://dx.doi.org/10.1101/gr.229202.