A multifunctional, synthetic Gaussia princeps luciferase reporter for live imaging of Candida albicans infections

Infection and Immunity

Volumn 77, Issue 11, 2009, Pages 4847-4858

  Enjalbert, Brice ^a,e   Rachini, Anna ^b   Vediyappan, Govindsamy ^c,d,f   Pietrella, Donatella ^b   Spaccapelo, Roberta ^b   Vecchiarelli, Anna ^b   Brown, Alistair J P ^a   D'Enfert, Christophe ^c,d  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b UNIVERSITY OF PERUGIA   (Italy)

^c INSTITUT PASTEUR   (France)

^d INRA F 75015   (France)

^e UMR792 INGÉNIERIE DES SYSTÈMES BIOLOGIQUES ET DES PROCÉDÉS   (France)

^f TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHOTERICIN B; CELL MEMBRANE PROTEIN; CYCLOPHOSPHAMIDE; ECONAZOLE; GLYCOSYLPHOSPHATIDYLINOSITOL; LUCIFERASE;

ACT1 GENE; ACT1 GLUC59 GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; CANDIDA ALBICANS; CANDIDIASIS; CELL VIABILITY; CONTROLLED STUDY; EFT3 GENE; FEMALE; FUSION GENE; GENE CONTROL; GENE EXPRESSION; GENOTYPE; GLUC59 GENE; HOST PATHOGEN INTERACTION; HWP1 GENE; IMMUNOSUPPRESSIVE TREATMENT; IPF9996 GENE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REPORTER GENE; TRR1 GENE; TRX1 GENE;

ANIMALS; ARTIFICIAL GENE FUSION; BASE SEQUENCE; CANDIDA ALBICANS; CANDIDIASIS; COPEPODA; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; GENES, REPORTER; HUMANS; LUCIFERASES; MICE; MOLECULAR SEQUENCE DATA; NEUTROPHILS;

EID: 70350463600     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00223-09     Document Type: Article

References (50)

1. Argimon, S., J. A. Wishart, R. Leng, S. Macaskill, A. Mavor, T. Alexandris, S. Nicholls, A. W. Knight, B. Enjalbert, R. Walmsley, F. C. Odds, N. A. R. Gow, and A. J. P. Brown. 2007. Developmental regulation of an adhesin gene during cellular morphogenesis in the fungal pathogen Candida albicans. Eukaryot. Cell 6:682-692. (Pubitemid 46697549)
2. Barelle, C. J., C. L. Manson, D. M. MacCallum, F. C. Odds, N. A. Gow, and A. J. Brown. 2004. GFP as a quantitative reporter of gene regulation in Candida albicans. Yeast 21:333-340.
3. Barelle, C. J., C. L. Priest, D. M. Maccallum, N. A. Gow, F. C. Odds, and A. J. Brown. 2006. Niche-specific regulation of central metabolic pathways in a fungal pathogen. Cell. Microbiol. 8:961-971.
4. Brown, A. J., G. Bertram, P. J. Feldmann, M. W. Peggie, and R. K. Swoboda. 1991. Codon utilisation in the pathogenic yeast, Candida albicans. Nucleic Acids Res. 19:4298.
5. Calderone, R. 2002. Candida and candidiasis. ASM Press, Washington, DC.
6. Contag, C. H., P. R. Contag, J. I. Mullins, S. D. Spilman, D. K. Stevenson, and D. A. Benaron. 1995. Photonic detection of bacterial pathogens in living hosts. Mol. Microbiol. 18:593-603.
7. Cormack, B. P., G. Bertram, M. Egerton, N. A. Gow, S. Falkow, and A. J. Brown. 1997. Yeast-enhanced green fluorescent protein (yEGFP): a reporter of gene expression in Candida albicans. Microbiology 143:303-311. (Pubitemid 27092165)
8. Doyle, T. C., K. A. Nawotka, C. B. Kawahara, K. P. Francis, and P. R. Contag. 2006. Visualizing fungal infections in living mice using bioluminescent pathogenic Candida albicans strains transformed with the firefly luciferase gene. Microb. Pathog. 40:82-90.
9. Doyle, T. C., K. A. Nawotka, A. F. Purchio, A. R. Akin, K. P. Francis, and P. R. Contag. 2006. Expression of firefly luciferase in Candida albicans and its use in the selection of stable transformants. Microb. Pathog. 40:69-81.
10. Enjalbert, B., D. M. MacCallum, F. C. Odds, and A. J. Brown. 2007. Nichespecific activation of the oxidative stress response by the pathogenic fungus Candida albicans. Infect. Immun. 75:2143-2151. (Pubitemid 46744300)
11. Fonzi, W. A., and M. Y. Irwin. 1993. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134:717-728.
12. Fradin, C., M. Kretschmar, T. Nichterlein, C. Gaillardin, C. d'Enfert, and B. Hube. 2003. Stage-specific gene expression of Candida albicans in human blood. Mol. Microbiol. 47:1523-1543.
13. Gaspari, A. A., R. Burns, A. Nasir, D. Ramirez, R. K. Barth, and C. G. Haidaris. 1998. CD86 (B7-2), but not CD80 (B7-1), expression in the epidermis of transgenic mice enhances the immunogenicity of primary cutaneous Candida albicans infections. Infect. Immun. 66:4440-4449.
14. Gow, N. A., Y. Knox, C. A. Munro, and W. D. Thompson. 2003. Infection of chick chorioallantoic membrane (CAM) as a model for invasive hyphal growth and pathogenesis of Candida albicans. Med. Mycol. 41:331-338.
15. Goyard, S., P. Knechtle, M. Chauvel, A. Mallet, M. C. Prevost, C. Proux, J. Y. Coppee, P. Schwartz, F. Dromer, H. Park, S. G. Filler, G. Janbon, and C. d'Enfert. 2008. The Yak1 kinase is involved in the initiation and maintenance of hyphal growth in Candida albicans. Mol. Biol. Cell 19:2251-2266.
16. Green, C. B., X. Zhao, and L. L. Hoyer. 2005. Use of green fluorescent protein and reverse transcription-PCR to monitor Candida albicans agglutinin- like sequence gene expression in a murine model of disseminated candidiasis. Infect. Immun. 73:1852-1855.
17. Harry, J. B., B. G. Oliver, J. L. Song, P. M. Silver, J. T. Little, J. Choiniere, and T. C. White. 2005. Drug-induced regulation of the MDR1 promoter in Candida albicans. Antimicrob. Agents Chemother. 49:2785-2792.
18. Hay, R. 1999. The management of superficial candidiasis. J. Am. Acad. Dermatol. 40:S35-S42.
19. Hutchens, M., and G. D. Luker. 2007. Applications of bioluminescence imaging to the study of infectious diseases. Cell. Microbiol. 9:2315-2322.
20. Koh, A. Y., J. R. Kohler, K. T. Coggshall, N. Van Rooijen, and G. B. Pier. 2008. Mucosal damage and neutropenia are required for Candida albicans dissemination. PLoS Pathog. 4:e35.
21. Lachke, S. A., T. Srikantha, and D. R. Soll. 2003. The regulation of EFG1 in white-opaque switching in Candida albicans involves overlapping promoters. Mol. Microbiol. 48:523-536.
22. Lloyd, A. T., and P. M. Sharp. 1992. Evolution of codon usage patterns: the extent and nature of divergence between Candida albicans and Saccharomyces cerevisiae. Nucleic Acids Res. 20:5289-5295.
23. Lorenz, M. C., J. A. Bender, and G. R. Fink. 2004. Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot. Cell 3:1076-1087.
24. MacCallum, D. M., and F. C. Odds. 2005. Temporal events in the intravenous challenge model for experimental Candida albicans infections in female mice. Mycoses 48:151-161.
25. Magliani, W., S. Conti, A. Salati, S. Arseni, R. Frazzi, L. Ravanetti, and L. Polonelli. 2002. New strategies for treatment of Candida vaginal infections. Rev. Iberoam. Micol. 19:144-148.
26. Mays, S. R., M. A. Bogle, and G. P. Bodey. 2006. Cutaneous fungal infections in the oncology patient: recognition and management. Am. J. Clin. Dermatol. 7:31-43.
27. Moreno-Ruiz, E., G. Ortu, P. W. de Groot, F. Cottier, C. Loussert, M. C. Prevost, C. de Koster, F. M. Klis, S. Goyard, and C. d'Enfert. 2009. The GPI-modified proteins Pga59 and Pga62 of Candida albicans are required for cell wall integrity. Microbiology 155:2004-2020.
28. Morschhauser, J., S. Michel, and J. Hacker. 1998. Expression of a chromosomally integrated, single-copy GFP gene in Candida albicans, and its use as a reporter of gene regulation. Mol. Gen. Genet. 257:412-420.
29. Murad, A. M., P. R. Lee, I. D. Broadbent, C. J. Barelle, and A. J. Brown. 2000. CIp10, an efficient and convenient integrating vector for Candida albicans. Yeast 16:325-327.
30. Myers, K. K., W. A. Fonzi, and P. S. Sypherd. 1992. Isolation and sequence analysis of the gene for translation elongation factor 3 from Candida albicans. Nucleic Acids Res. 11:1705-1710.
31. Netea, M. G., N. A. Gow, C. A. Munro, S. Bates, C. Collins, G. Ferwerda, R. P. Hobson, G. Bertram, H. B. Hughes, T. Jansen, L. Jacobs, E. T. Buurman, K. Gijzen, D. L. Williams, R. Torensma, A. McKinnon, D. M. MacCallum, F. C. Odds, J. W. Van der Meer, A. J. Brown, and B. J. Kullberg. 2006. Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J. Clin. Investig. 116:1642-1650.
32. Phan, Q. T., C. L. Myers, Y. Fu, D. C. Sheppard, M. R. Yeaman, W. H. Welch, A. S. Ibrahim, J. E. Edwards, Jr., and S. G. Filler. 2007. Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS biology 5:e64.
33. Pietrella, D., R. Mazzolla, P. Lupo, L. Pitzurra, M. J. Gomez, R. Cherniak, and A. Vecchiarelli. 2002. Mannoprotein from Cryptococcus neoformans promotes T-helper type 1 anticandidal responses in mice. Infect. Immun. 70: 6621-6627.
34. Santos, M. A., and M. F. Tuite. 1995. The CUG codon is decoded in vivo as serine and not leucine in Candida albicans. Nucleic Acids Res. 23:1481-1486.
35. Saville, S. P., A. L. Lazzell, C. Monteagudo, and J. L. Lopez-Ribot. 2003. Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot. Cell 2:1053-1060.
36. Schaller, M., M. Bein, H. C. Korting, S. Baur, G. Hamm, M. Monod, S. Beinhauer, and B. Hube. 2003. The secreted aspartyl proteinases Sap1 and Sap2 cause tissue damage in an in vitro model of vaginal candidiasis based on reconstituted human vaginal epithelium. Infect. Immun. 71:3227-3234.
37. Serganova, I., E. Moroz, M. Moroz, N. Pillarsetty, and R. Blasberg. 2006. Non-invasive molecular imaging and reporter genes. Centr. Eur. J. Biol. 1:88-123.
38. Sherman, F. 1991. Getting started with yeast. Methods Enzymol. 194:3-21.
39. Sobel, J. 1992. Pathogenesis and treatment of recurrent vulvovaginal candidiasis. Clin. Infect. Dis. 14:S148-S153.
40. Sobel, J. 2002. Pathogenesis of recurrent vulvovaginal candidiasis. Curr. Infect. Dis. Rep. 4:514-519.
41. Srikantha, T., A. Klapach, W. W. Lorenz, L. K. Tsai, L. A. Laughlin, J. A. Gorman, and D. R. Soll. 1996. The sea pansy Renilla reniformis luciferase serves as a sensitive bioluminescent reporter for differential gene expression in Candida albicans. J. Bacteriol. 178:121-129. (Pubitemid 26006073)
42. Staab, J. F., C. A. Ferrer, and P. Sundstrom. 1996. Developmental expression of a tandemly repeated, proline-and glutamine-rich amino acid motif on hyphal surfaces on Candida albicans. J. Biol. Chem. 271:6298-6305. (Pubitemid 126552325)
43. Stroschein-Stevenson, S. L., E. Foley, P. H. O'Farrell, and A. D. Johnson. 2006. Identification of Drosophila gene products required for phagocytosis of Candida albicans. PLoS Biol. 4:e4.
44. Tannous, B. A., D. E. Kim, J. L. Fernandez, R. Weissleder, and X. O. Breakefield. 2005. Codon-optimized Gaussia luciferase cDNA for mammalian gene expression in culture and in vivo. Mol. Ther. 11:435-443.
45. Thewes, S., M. Kretschmar, H. Park, M. Schaller, S. G. Filler, and B. Hube. 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.
46. Uhl, M. A., and A. D. Johnson. 2001. Development of Streptococcus thermophilus lacZ as a reporter gene for Candida albicans. Microbiology 147: 1189-1195.
47. Verhaegent, M., and T. K. Christopoulos. 2002. Recombinant Gaussia luciferase. Overexpression, purification, and analytical application of a bioluminescent reporter for DNA hybridization. Anal. Chem. 74:4378-4385.
48. Walther, A., and J. Wendland. 2003. An improved transformation protocol for the human fungal pathogen Candida albicans. Curr. Genet. 42:339-343.
49. Wilson, R. B., D. Davis, and A. P. Mitchell. 1999. Rapid hypothesis testing with Candida albicans through gene disruption with short homology regions. J. Bacteriol. 181:1868-1874.
50. Zakikhany, K., J. R. Naglik, A. Schmidt-Westhausen, G. Holland, M. Schaller, and B. Hube. 2007. In vivo transcript profiling of Candida albicans identifies a gene essential for interepithelial dissemination. Cell. Microbiol. 9:2938-2954.