Hemoglobin is an effective inducer of hyphal differentiation in Candida albicans

Medical Mycology

Volumn 45, Issue 1, 2007, Pages 61-71

  Pendrak, Michael L ^a   Roberts, David D ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; BUFFER; FUNGAL PROTEIN; GLOBIN; GLUCOSE; GLUTAMINE; HEME; HEMOGLOBIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATE; PROTEIN ECE1; PROTEIN HWP1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; CPH1 PROTEIN, CANDIDA ALBICANS; DNA BINDING PROTEIN; ECE1 PROTEIN, CANDIDA ALBICANS; EFG1 PROTEIN, CANDIDA ALBICANS; HWP1 PROTEIN, CANDIDA ALBICANS; MEMBRANE PROTEIN; NITROGEN;

ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; CULTURE MEDIUM; FUNGAL CELL CULTURE; FUNGUS HYPHAE; MORPHOGENESIS; NONHUMAN; PH; PROCESS OPTIMIZATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TEMPERATURE DEPENDENCE; BIOSYNTHESIS; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

CANDIDA ALBICANS;

CANDIDA ALBICANS; DNA-BINDING PROTEINS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GLUCOSE; HEMOGLOBINS; HYPHAE; MEMBRANE GLYCOPROTEINS; MORPHOGENESIS; NITROGEN; TRANSCRIPTION FACTORS;

EID: 34249662827     PISSN: 13693786     EISSN: 14602709     Source Type: Journal    
DOI: 10.1080/13693780601028691     Document Type: Article

References (56)

1. Odds, FC. (1988) Candida and candidosis, Bailliere Tindall, Philadelphia
2. Slutsky, B., Staebell, M. and Anderson, J. (1987) "White-opaque transition": A second high-frequency switching system in Candida albicans. J Bacteriol, 169, pp. 189-197.
3. Brown, AJ and Gow, NA. (1999) Regulatory networks controlling Candida albicans morphogenesis. Trends Microbiol, 7, pp. 333-338.
4. Ernst, JF. (2000) Transcription factors in Candida albicans - environmental control of morphogenesis. Microbiology, 146, pp. 1763-1774.
5. Sudbery, P., Gow, N. and Berman, J. (2004) The distinct morphogenic states of Candida albicans. Trends Microbiol, 12, pp. 317-324.
6. Kumamoto, CA and Vinces, MD. (2005) Contributions of hyphae and hypha-co-regulated genes to Candida albicans virulence. Cell Microbiol, 7, pp. 1546-1554.
7. Garcia-Sanchez, S., Mavor, AL and Russell, CL (2005) Global roles of Ssn6 in Tup1- and Nrg1-dependent gene regulation in the fungal pathogen, Candida albicans. Mol Biol Cell, 16, pp. 2913-2925.
8. Bignell, E., Rogers, T. and Haynes, K. (2004) Host Recognition by Fungal Pathogens. Pathogenic Fungi: Host Interactions and Emerging Strategies for Control, pp. 3-48. Caister, Norfolk
9. Brown, AJP. (2002) Expression of Growth Form-Specific Factors during Morphogenesis in Candida albicans, ASM Press, Washington, DC
10. Lo, HJ, Kohler, JR and DiDomenico, B. (1997) Nonfilamentous C. albicans mutants are avirulent. Cell, 90, pp. 939-949.
11. Stoldt, VR, Sonneborn, A., Leuker, CE and Ernst, JF. (1997) Efg1p, an essential regulator of morphogenesis of the human pathogen Candida albicans, is a member of a conserved class of bHLH proteins regulating morphogenetic processes in fungi. EMBO J, 16, pp. 1982-1991.
12. Lane, S., Zhou, S., Pan, T., Dai, Q. and Liu, H. (2001) The basic helix-loop-helix transcription factor Cph2 regulates hyphal development in Candida albicans partly via TEC1. Mol Cell Biol, 21, pp. 6418-6428.
13. Vinces, MD, Haas, C. and Kumamoto, CA. (2006) Expression of the Candida albicans morphogenesis regulator gene CZF1 and its regulation by Efg1p and Czf1p. Eukaryot Cell, 5, pp. 825-835.
14. Barkani, A El, Kurzai, O. and Fonzi, WA (2000) Dominant active alleles of RIM101 (PRR2) bypass the pH restriction on filamentation of Candida albicans. Mol Cell Biol, 20, pp. 4635-4647.
15. Lee, KL, Buckley, HR and Campbell, CC. (1975) An amino acid liquid synthetic medium for the development of mycelial and yeast forms of Candida albicans. Sabouraudia, 13, pp. 148-153.
16. Sherman, F. (1991) Getting started with yeast. Method Enzymol., 191, pp. 3-21.
17. Daniels, R. (2002)
18. Feng, Q., Summers, E., Guo, B. and Fink, G. (1999) Ras signaling is required for serum-induced hyphal differentiation in Candida albicans. J Bacteriol, 181, pp. 6339-6346.
19. Hudson, DA, Sciascia, QL and Sanders, RJ (2004) Identification of the dialysable serum inducer of germ-tube formation in Candida albicans. Microbiology, 150, pp. 3041-3049.
20. Noverr, MC and Huffnagle, GB. (2004) Regulation of Candida albicans morphogenesis by fatty acid metabolites. Infect Immun, 72, pp. 6206-6210.
21. Genco, CA and Dixon, DW. (2001) Emerging strategies in microbial haem capture. Mol Microbiol, 39, pp. 1-11.
22. Seery, VL and Muller-Eberhard, U. (1973) Binding of porphyrins to rabbit hemopexin and albumin. J Biol Chem, 248, pp. 3796-3800.
23. Casanova, M., Cervera, AM, Gozalbo, D. and Martinez, JP. (1997) Hemin induces germ tube formation in Candida albicans. Infect Immun, 65, pp. 4360-4364.
24. Fradin, C., Kretschmar, M. and Nichterlein, T. (2003) Stage-specific gene expression of Candida albicans in human blood. Mol Microbiol, 47, pp. 1523-1543.
25. Barelle, CJ, Priest, CL and Maccallum, DM (2006) Niche-specific regulation of central metabolic pathways in a fungal pathogen. Cell Microbiol, 8, pp. 961-971.
26. Pendrak, ML, Yan, SS and Roberts, DD. (2004) Sensing the host environment: Recognition of hemoglobin by the pathogenic yeast Candida albicans. Arch Biochem Biophys, 426, pp. 148-156.
27. Yan, S., Rodrigues, RG, Cahn-Hidalgo, D., Walsh, TJ and Roberts, DD. (1998) Hemoglobin induces binding of several extracellular matrix proteins to Candida albicans. Identification of a common receptor for fibronectin, fibrinogen, and laminin. J Biol Chem, 273, pp. 5638-5644.
28. Pendrak, ML, Krutzsch, HC and Roberts, DD. (2000) Structural requirements for hemoglobin to induce fibronectin receptor expression in Candida albicans. Biochemistry, 39, pp. 16110-16118.
29. Yan, S., Rodrigues, RG and Roberts, DD. (1998) Hemoglobin-induced binding of Candida albicans to the cell-binding domain of fibronectin is independent of the Arg-Gly-Asp sequence. Infect Immun, 66, pp. 1904-1909.
30. Yan, S., Negre, E. and Cashel, JA (1996) Specific induction of fibronectin binding activity by hemoglobin in Candida albicans grown in defined media. Infect Immun, 64, pp. 2930-2935.
31. Negre, E., Vogel, T. and Levanon, A. (1994) The collagen binding domain of fibronectin contains a high affinity binding site for Candida albicans. J Biol Chem, 269, pp. 22039-22045.
32. Pendrak, ML, Chao, MP, Yan, SS and Roberts, DD. (2004) Heme oxygenase in Candida albicans is regulated by hemoglobin and is necessary for metabolism of exogenous heme and hemoglobin to alpha-biliverdin. J Biol Chem, 279, pp. 3426-3433.
33. Pendrak, ML, Yan, SS and Roberts, DD. (2004) Hemoglobin regulates expression of an activator of mating-type locus alpha genes in Candida albicans. Eukaryot Cell, 3, pp. 764-775.
34. Bennett, RJ and Johnson, AD. (2005) Mating in Candida albicans and the search for a sexual cycle. Annu Rev Microbiol, 59, pp. 233-255.
35. Weissman, Z. and Kornitzer, D. (2004) A family of Candida cell surface haem-binding proteins involved in haemin and haemoglobin-iron utilization. Mol Microbiol, 53, pp. 1209-1220.
36. Bensen, ES, Filler, SG and Berman, J. (2002) A forkhead transcription factor is important for true hyphal as well as yeast morphogenesis in Candida albicans. Eukaryotic Cell, 1, pp. 787-798.
37. Köhrer, K. and Domdey, H. (1991) Preparation of High Molecular Weight RNA. Yeast Genetics and Molecular Biology, pp. 398-405. Academic Press, San Diego
38. Kalendar, R. (2001) The Third International Bioinformatics Meeting in Scandinavia: Bioinformatics, 2001
39. Pfaffl, MW. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res, 29, p. e45.
40. Sharkey, LL, McNemar, MD, Saporito-Irwin, SM, Sypherd, PS and Fonzi, WA. (1999) HWP1 functions in the morphological development of Candida albicans downstream of EFG1, TUP1, and RBF1. J Bacteriol, 181, pp. 5273-5279.
41. Birse, CE, Irwin, MY, Fonzi, WA and Sypherd, PS. (1993) Cloning and characterization of ECE1, a gene expressed in association with cell elongation of the dimorphic pathogen Candida albicans. Infect Immun, 61, pp. 3648-3655.
42. Biswas, K. and Morschhauser, J. (2005) The Mep2p ammonium permease controls nitrogen starvation-induced filamentous growth in Candida albicans. Mol Microbiol, 56, pp. 649-669.
43. Braun, BR and Johnson, AD. (2000) TUP1, CPH1 and EFG1 make independent contributions to filamentation in Candida albicans. Genetics, 155, pp. 57-67.
44. Hasenclever, HF. (1978) The in vitro interactions of Candida albicans with nonspecific serum proteins. Mycopathologia, 65, pp. 169-176.
45. Barlow, AJ, Aldersley, T. and Chattaway, FW. (1974) Factors present in serum and seminal plasma which promote germ-tube formation and mycelial growth of Candida albicans. J Gen Microbiol, 82, pp. 261-272.
46. Ouyang, J., Taes, YE and Delanghe, JR. (2005) Serum free hemoglobin concentrations in healthy individuals are related to haptoglobin type. Clin Chem, 51, pp. 1754-1755.
47. Shuster, A., Osherov, N. and Rosenberg, M. (2004) Alcohol-mediated haemolysis in yeast. Yeast, 21, pp. 1335-1342.
48. Luo, G., Samaranayake, LP and Yau, JY. (2001) Candida species exhibit differential in vitro hemolytic activities. J Clin Microbiol, 39, pp. 2971-2974.
49. Manns, JM, Mosser, DM and Buckley, HR. (1994) Production of a hemolytic factor by Candida albicans. Infect Immun, 62, pp. 5154-5156.
50. Werner-Washburne, M., Braun, E., Johnston, GC and Singer, RA. (1993) Stationary phase in the yeast Saccharomyces cerevisiae. Microbiol Rev, 57, pp. 383-401.
51. Shepherd, MG, Yin, CY, Ram, SP and Sullivan, PA. (1980) Germ tube induction in Candida albicans. Can J Microbiol, 26, pp. 21-26.
52. Gimeno, CJ, Ljungdahl, PO, Styles, CA and Fink, GR. (1992) Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell, 68, pp. 1077-1090.
53. Magasanik, B. (1992) Regulation of Nitrogen Utilization. Molecular and Cellular Biology of the Yeast Saccharomyces: Gene Expression, pp. 283-317. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
54. Protchenko, O., Rodriguez-Suarez, R., Androphy, R., Bussey, H. and Philpott, CC. (2006) A screen for genes of heme uptake identifies the FLC family required for import of FAD into the endoplasmic reticulum. J Biol Chem, 281, pp. 21445-21457.
55. Santos, R., Buisson, N. and Knight, S. (2003) Haemin uptake and use as an iron source by Candida albicans: Role of CaHMX1-encoded haem oxygenase. Microbiology, 149, pp. 579-588.
56. Liu, H., Kohler, J. and Fink, G. (1994) Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science, 266, pp. 1723-1725.