Mds3 regulates morphogenesis in Candida albicans through the TOR pathway

Molecular and Cellular Biology

Volumn 30, Issue 14, 2010, Pages 3695-3710

  Zacchi, Lucia F ^a   Gomez Raja, Jonatan ^a   Davis, Dana A ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MDS3 PROTEIN; NITROGEN; PROTEIN; RAPAMYCIN; RAS PROTEIN; RIBOSOME PROTEIN; TARGET OF RAPAMYCIN KINASE; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; FUNGAL GENE; FUNGAL STRAIN; GENE DELETION; GENE EXPRESSION; GENOTYPE; IMMUNOPRECIPITATION; MICROARRAY ANALYSIS; MORPHOGENESIS; NONHUMAN; NORTHERN BLOTTING; PH; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN PURIFICATION; WESTERN BLOTTING;

BASE SEQUENCE; CANDIDA ALBICANS; DNA PRIMERS; DNA, FUNGAL; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; HUMANS; MORPHOGENESIS; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SIROLIMUS;

CANDIDA ALBICANS;

EID: 77954364299     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01540-09     Document Type: Article

References (81)

1. Adams, A., D. E. Gotschling, C. A. Kaiser, and T. Stearns. 1997. Methods in yeast genetics, 1997 ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. Adams, J., R. Kelso, and L. Cooley. 2000. The kelch repeat superfamily of proteins: propellers of cell function. Trends Cell Biol. 10:17-24. (Pubitemid 30017862)
3. Alonso-Monge, R., E. Roman, D. M. Arana, J. Pla, and C. Nombela. 2009. Fungi sensing environmental stress. Clin. Microbiol. Infect. 15(Suppl. 1):17-19.
4. Bastidas, R. J., J. Heitman, and M. E. Cardenas. 2009. The protein kinase Tor1 regulates adhesin gene expression in Candida albicans. PLoS Pathog. 5:e1000294.
5. Benni, M. L., and L. Neigeborn. 1997. Identification of a new class of negative regulators affecting sporulation-specific gene expression in yeast. Genetics 147:1351-1366.
6. Bensen, E. S., S. J. Martin, M. Li, J. Berman, and D. A. Davis. 2004. Transcriptional profiling in C. albicans reveals new adaptive responses to extracellular pH and functions for Rim101p. Mol. Microbiol. 54:1335-1351.
7. Cafferkey, R., P. R. Young, M. M. McLaughlin, D. J. Bergsma, Y. Koltin, G. M. Sathe, L. Faucette, W. K. Eng, R. K. Johnson, and G. P. Livi. 1993. Dominant missense mutations in a novel yeast protein related to mammalian phosphatidylinositol 3-kinase and VPS34 abrogate rapamycin cytotoxicity. Mol. Cell. Biol. 13:6012-6023.
8. Cardenas, M. E., N. S. Cutler, M. C. Lorenz, C. J. Di Como, and J. Heitman. 1999. The TOR signaling cascade regulates gene expression in response to nutrients. Genes Dev. 13:3271-3279.
9. Chen, E. J., and C. A. Kaiser. 2003. LST8 negatively regulates amino acid biosynthesis as a component of the TOR pathway. J. Cell Biol. 161:333-347.
10. Cottier, F., and F. A. Muhlschlegel. 2009. Sensing the environment: response of Candida albicans to the X factor. FEMS Microbiol. Lett. 295:1-9.
11. Cox, K. H., A. Kulkarni, J. J. Tate, and T. G. Cooper. 2004. Gln3 phosphorylation and intracellular localization in nutrient limitation and starvation differ from those generated by rapamycin inhibition of Tor1/2 in Saccharomyces cerevisiae. J. Biol. Chem. 279:10270-10278.
12. Crespo, J. L., T. Powers, B. Fowler, and M. N. Hall. 2002. The TOR-controlled transcription activators GLN3, RTG1, and RTG3 are regulated in response to intracellular levels of glutamine. Proc. Natl. Acad. Sci. U. S. A. 99:6784-6789.
13. Cruz, M. C., A. L. Goldstein, J. Blankenship, M. Del Poeta, J. R. Perfect, J. H. McCusker, Y. L. Bennani, M. E. Cardenas, and J. Heitman. 2001. Rapamycin and less immunosuppressive analogs are toxic to Candida albicans and Cryptococcus neoformans via FKBP12-dependent inhibition of TOR. Antimicrob. Agents Chemother. 45:3162-3170.
14. Cutler, N. S., X. Pan, J. Heitman, and M. E. Cardenas. 2001. The TOR signal transduction cascade controls cellular differentiation in response to nutrients. Mol. Biol. Cell 12:4103-4113.
15. Davis, D., J. E. Edwards, Jr., A. P. Mitchell, and A. S. Ibrahim. 2000. Candida albicans RIM101 pH response pathway is required for host-pathogen interactions. Infect. Immun. 68:5953-5959.
16. Davis, D., R. B. Wilson, and A. P. Mitchell. 2000. RIM101-dependent and-independent pathways govern pH responses in Candida albicans. Mol. Cell. Biol. 20:971-978.
17. Davis, D. A. 2009. How human pathogenic fungi sense and adapt to pH: the link to virulence. Curr. Opin. Microbiol. 12:365-370.
18. Davis, D. A., V. M. Bruno, L. Loza, S. G. Filler, and A. P. Mitchell. 2002. Candida albicans Mds3p, a conserved regulator of pH responses and virulence identified through insertional mutagenesis. Genetics 162:1573-1581.
19. Delgoffe, G. M., T. P. Kole, Y. Zheng, P. E. Zarek, K. L. Matthews, B. Xiao, P. F. Worley, S. C. Kozma, and J. D. Powell. 2009. The mTOR kinase differentially regulates effector and regulatory T cell lineage commitment. Immunity 30:832-844.
20. Di Como, C. J., and K. T. Arndt. 1996. Nutrients, via the Tor proteins, stimulate the association of Tap42 with type 2A phosphatases. Genes Dev. 10:1904-1916.
21. Di Como, C. J., and Y. Jiang. 2006. The association of Tap42 phosphatase complexes with TORC1: another level of regulation in Tor signaling. Cell Cycle 5:2729-2732.
22. Düvel, K., and J. R. Broach. 2004. The role of phosphatases in TOR signaling in yeast. Curr. Top. Microbiol. Immunol. 279:19-38.
23. Düvel, K., A. Santhanam, S. Garrett, L. Schneper, and J. R. Broach. 2003. Multiple roles of Tap42 in mediating rapamycin-induced transcriptional changes in yeast. Mol. Cell 11:1467-1478. (Pubitemid 36776534)
24. Esposito, R. E., and S. Klapholz. 1981. Meiosis and ascospore development, p. 211-288. In J. N. Strathern, E. W. Jones, and J. R. Broach (ed.), The molecular biology of the yeast Saccharomyces: life cycle and inheritance, 11A ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
25. Feierbach, B., F. Verde, and F. Chang. 2004. Regulation of a formin complex by the microtubule plus end protein tea1p. J. Cell Biol. 165:697-707. (Pubitemid 38765771)
26. Feng, Q., E. Summers, B. Guo, and G. Fink. 1999. Ras signaling is required for serum-induced hyphal differentiation in Candida albicans. J. Bacteriol. 181:6339-6346. (Pubitemid 29512943)
27. Gavin, A. C., P. Aloy, P. Grandi, R. Krause, M. Boesche, M. Marzioch, C. Rau, L. J. Jensen, S. Bastuck, B. Dumpelfeld, A. Edelmann, M. A. Heurtier, V. Hoffman, C. Hoefert, K. Klein, M. Hudak, A. M. Michon, M. Schelder, M. Schirle, M. Remor, T. Rudi, S. Hooper, A. Bauer, T. Bouwmeester, G. Casari, G. Drewes, G. Neubauer, J. M. Rick, B. Kuster, P. Bork, R. B. Russell, and G. Superti-Furga. 2006. Proteome survey reveals modularity of the yeast cell machinery. Nature 440:631-636.
28. Gavin, A. C., M. Bosche, R. Krause, P. Grandi, M. Marzioch, A. Bauer, J. Schultz, J. M. Rick, A. M. Michon, C. M. Cruciat, M. Remor, C. Hofert, M. Schelder, M. Brajenovic, H. Ruffner, A. Merino, K. Klein, M. Hudak, D. Dickson, T. Rudi, V. Gnau, A. Bauch, S. Bastuck, B. Huhse, C. Leutwein, M. A. Heurtier, R. R. Copley, A. Edelmann, E. Querfurth, V. Rybin, G. Drewes, M. Raida, T. Bouwmeester, P. Bork, B. Seraphin, B. Kuster, G. Neubauer, and G. Superti-Furga. 2002. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415:141-147.
29. Georis, I., A. Feller, J. J. Tate, T. G. Cooper, and E. Dubois. 2009. Nitrogen catabolite repression-sensitive transcription as a readout of Tor pathway regulation: the genetic background, reporter gene and GATA factor assayed determine the outcomes. Genetics 181:861-874.
30. Gerami-Nejad, M., K. Dulmage, and J. Berman. 2009. Additional cassettes for epitope and fluorescent fusion proteins in Candida albicans. Yeast 26:399-406.
31. Gettemans, J., K. Meerschaert, J. Vandekerckhove, and V. De Corte. 2003. A kelch beta propeller featuring as a G beta structural mimic: reinventing the wheel? Sci. STKE 2003:PE27.
32. Gow, N. A., A. J. Brown, and F. C. Odds. 2002. Fungal morphogenesis and host invasion. Curr. Opin. Microbiol. 5:366-371.
33. Han, J., B. Wang, Z. Xiao, Y. Gao, Y. Zhao, J. Zhang, B. Chen, X. Wang, and J. Dai. 2008. Mammalian target of rapamycin (mTOR) is involved in the neuronal differentiation of neural progenitors induced by insulin. Mol. Cell Neurosci. 39:118-124.
34. Harashima, T., and J. Heitman. 2002. The Galpha protein Gpa2 controls yeast differentiation by interacting with kelch repeat proteins that mimic Gbeta subunits. Mol. Cell 10:163-173.
35. Hardwick, J. S., F. G. Kuruvilla, J. K. Tong, A. F. Shamji, and S. L. Schreiber. 1999. Rapamycin-modulated transcription defines the subset of nutrient-sensitive signaling pathways directly controlled by the Tor proteins. Proc. Natl. Acad. Sci. U. S. A. 96:14866-14870.
36. Heitman, J., N. R. Movva, and M. N. Hall. 1991. Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253:905-909.
37. Hogues, H., H. Lavoie, A. Sellam, M. Mangos, T. Roemer, E. Purisima, A. Nantel, and M. Whiteway. 2008. Transcription factor substitution during the evolution of fungal ribosome regulation. Mol. Cell 29:552-562.
38. Hwang, M., C. A. Perez, L. Moretti, and B. Lu. 2008. The mTOR signaling network: insights from its role during embryonic development. Curr. Med. Chem. 15:1192-1208.
39. Ihmels, J., S. Bergmann, M. Gerami-Nejad, I. Yanai, M. McClellan, J. Berman, and N. Barkai. 2005. Rewiring of the yeast transcriptional network through the evolution of motif usage. Science 309:938-940.
40. Jiang, Y., and J. R. Broach. 1999. Tor proteins and protein phosphatase 2A reciprocally regulate Tap42 in controlling cell growth in yeast. EMBO J. 18:2782-2792. (Pubitemid 29233950)
41. Kim, D.-H., D. D. Sarbassov, S. M. Ali, J. E. King, R. R. Latek, H. Erdjument-Bromage, P. Tempst, and D. M. Sabatini. 2002. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110:163-175.
42. Kim, D. H., D. D. Sarbassov, S. M. Ali, R. R. Latek, K. V. Guntur, H. Erdjument-Bromage, P. Tempst, and D. M. Sabatini. 2003. GbetaL, a positive regulator of the rapamycin-sensitive pathway required for the nutrient-sensitive interaction between raptor and mTOR. Mol. Cell 11:895-904.
43. Kullas, A. L., S. J. Martin, and D. Davis. 2007. Adaptation to environmental pH: integrating the Rim101 and calcineurin signal transduction pathways. Mol. Microbiol. 66:858-871.
44. Kumamoto, C. A., and M. D. Vinces. 2005. Contributions of hyphae and hypha-co-regulated genes to Candida albicans virulence. Cell Microbiol. 7:1546-1554.
45. Leberer, E., D. Harcus, D. Dignard, L. Johnson, S. Ushinsky, D. Y. Thomas, and K. Schroppel. 2001. Ras links cellular morphogenesis to virulence by regulation of the MAP kinase and cAMP signalling pathways in the pathogenic fungus Candida albicans. Mol. Microbiol. 42:673-687.
46. Lee, C. M., A. Nantel, L. Jiang, M. Whiteway, and S. H. Shen. 2004. The serine/threonine protein phosphatase SIT4 modulates yeast-to-hypha morphogenesis and virulence in Candida albicans. Mol. Microbiol. 51:691-709.
47. Liu, H., J. Kohler, and G. R. Fink. 1994. Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266:1723-1726.
48. Lo, H. J., J. R. Kohler, B. DiDomenico, D. Loebenberg, A. Cacciapuoti, and G. R. Fink. 1997. Nonfilamentous C. albicans mutants are avirulent. Cell 90:939-949.
49. Loewith, R., E. Jacinto, S. Wullschleger, A. Lorberg, J. L. Crespo, D. Bonenfant, W. Oppliger, P. Jenoe, and M. N. Hall. 2002. Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol. Cell 10:457-468. (Pubitemid 35284167)
50. Lu, A., and J. P. Hirsch. 2005. Cyclic AMP-independent regulation of protein kinase A substrate phosphorylation by Kelch repeat proteins. Eukaryot. Cell 4:1794-1800. (Pubitemid 41636871)
51. Luke, M. M., F. Della Seta, C. J. Di Como, H. Sugimoto, R. Kobayashi, and K. T. Arndt. 1996. The SAP, a new family of proteins, associate and function positively with the SIT4 phosphatase. Mol. Cell. Biol. 16:2744-2755.
52. Martchenko, M., A. Levitin, H. Hogues, A. Nantel, and M. Whiteway. 2007. Transcriptional rewiring of fungal galactose-metabolism circuitry. Curr. Biol. 17:1007-1013.
53. Martin, K. A., E. M. Rzucidlo, B. L. Merenick, D. C. Fingar, D. J. Brown, R. J. Wagner, and R. J. Powell. 2004. The mTOR/p70 S6K1 pathway regulates vascular smooth muscle cell differentiation. Am. J. Physiol. Cell Physiol. 286:C507-C517.
54. McDonald, C. M., M. Wagner, M. J. Dunham, M. E. Shin, N. T. Ahmed, and E. Winter. 2009. The Ras/cAMP pathway and the CDK-like kinase Ime2 regulate the MAPK Smk1 and spore morphogenesis in Saccharomyces cerevisiae. Genetics 181:511-523.
55. McMahon, L. P., K. M. Choi, T. A. Lin, R. T. Abraham, and J. C. Lawrence, Jr. 2002. The rapamycin-binding domain governs substrate selectivity by the mammalian target of rapamycin. Mol. Cell. Biol. 22:7428-7438.
56. Mitchell, A. P. 1998. Dimorphism and virulence in Candida albicans. Curr. Opin. Microbiol. 1:687-692.
57. Munn, A. L., and H. Riezman. 1994. Endocytosis is required for the growth of vacuolar H(+)-ATPase-defective yeast: identification of six new END genes. J. Cell Biol. 127:373-386.
58. Murad, A. M., P. Leng, M. Straffon, J. Wishart, S. Macaskill, D. MacCallum, N. Schnell, D. Talibi, D. Marechal, F. Tekaia, C. d'Enfert, C. Gaillardin, F. C. Odds, and A. J. Brown. 2001. NRG1 represses yeast-hypha morphogenesis and hypha-specific gene expression in Candida albicans. EMBO J. 20:4742-4752.
59. Nobile, C. J., D. R. Andes, J. E. Nett, F. J. Smith, F. Yue, Q. T. Phan, J. E. Edwards, S. G. Filler, and A. P. Mitchell. 2006. Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog. 2:e63.
60. Nobile, C. J., V. M. Bruno, M. L. Richard, D. A. Davis, and A. P. Mitchell. 2003. Genetic control of chlamydospore formation in Candida albicans. Microbiology 149:3629-3637.
61. Nobile, C. J., N. Solis, C. L. Myers, A. J. Fay, J. S. Deneault, A. Nantel, A. P. Mitchell, and S. G. Filler. 2008. Candida albicans transcription factor Rim101 mediates pathogenic interactions through cell wall functions. Cell Microbiol. 10:2180-2196.
62. Porta, A., A. M. Ramon, and W. A. Fonzi. 1999. PRR1, a homolog of Aspergillus nidulans palF, controls pH-dependent gene expression and filamentation in Candida albicans. J. Bacteriol. 181:7516-7523.
63. Ramon, A. M., A. Porta, and W. A. Fonzi. 1999. Effect of environmental pH on morphological development of Candida albicans is mediated via the PacC-related transcription factor encoded by PRR2. J. Bacteriol. 181:7524-7530.
64. Reiling, J. H., and D. M. Sabatini. 2006. Stress and mTORture signaling. Oncogene 25:6373-6383.
65. Richard, M. L., C. J. Nobile, V. M. Bruno, and A. P. Mitchell. 2005. Candida albicans biofilm-defective mutants. Eukaryot. Cell 4:1493-1502.
66. Rohde, J. R., and M. E. Cardenas. 2004. Nutrient signaling through TOR kinases controls gene expression and cellular differentiation in fungi. Curr. Top. Microbiol. Immunol. 279:53-72.
67. Schmelzle, T., T. Beck, D. E. Martin, and M. N. Hall. 2004. Activation of the RAS/cyclic AMP pathway suppresses a TOR deficiency in yeast. Mol. Cell. Biol. 24:338-351.
68. Shamji, A. F., F. G. Kuruvilla, and S. L. Schreiber. 2000. Partitioning the transcriptional program induced by rapamycin among the effectors of the Tor proteins. Curr. Biol. 10:1574-1581.
69. Tate, J. J., I. Georis, A. Feller, E. Dubois, and T. G. Cooper. 2009. Rapamycin- induced Gln3 dephosphorylation is insufficient for nuclear localization: Sit4 and PP2A phosphatases are regulated and function differently. J. Biol. Chem. 284:2522-2534.
70. Tsong, A. E., B. B. Tuch, H. Li, and A. D. Johnson. 2006. Evolution of alternative transcriptional circuits with identical logic. Nature 443:415-420.
71. van der Rest, M. E., A. H. Kamminga, A. Nakano, Y. Anraku, B. Poolman, and W. N. Konings. 1995. The plasma membrane of Saccharomyces cerevisiae: structure, function, and biogenesis. Microbiol. Rev. 59:304-322.
72. Vezina, C., A. Kudelski, and S. N. Sehgal. 1975. Rapamycin (AY-22,989), a new antifungal antibiotic. I. Taxonomy of the producing streptomycete and isolation of the active principle. J. Antibiot. (Tokyo) 28:721-726.
73. Vilella-Bach, M., P. Nuzzi, Y. Fang, and J. Chen. 1999. The FKBP12- rapamycin-binding domain is required for FKBP12-rapamycin-associated protein kinase activity and G1 progression. J. Biol. Chem. 274:4266-4272.
74. Vojtek, A. B., S. M. Hollenberg, and J. A. Cooper. 1993. Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell 74:205-214.
75. Weisman, R., and M. Choder. 2001. The fission yeast TOR homolog, tor1+, is required for the response to starvation and other stresses via a conserved serine. J. Biol. Chem. 276:7027-7032.
76. Weissman, Z., R. Shemer, E. Conibear, and D. Kornitzer. 2008. An endocytic mechanism for haemoglobin-iron acquisition in Candida albicans. Mol. Microbiol. 69:201-217.
77. Whiteway, M., and U. Oberholzer. 2004. Candida morphogenesis and host-pathogen interactions. Curr. Opin. Microbiol. 7:350-357.
78. 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.
79. Wullschleger, S., R. Loewith, and M. N. Hall. 2006. TOR signaling in growth and metabolism. Cell 124:471-484.
80. Zheng, X. F., and S. L. Schreiber. 1997. Target of rapamycin proteins and their kinase activities are required for meiosis. Proc. Natl. Acad. Sci. U. S. A. 94:3070-3075.
81. Zurita-Martinez, S. A., and M. E. Cardenas. 2005. Tor and cyclic AMP-protein kinase A: two parallel pathways regulating expression of genes required for cell growth. Eukaryot. Cell 4:63-71.