Rhb1 regulates the expression of secreted aspartic protease 2 through the TOR signaling pathway in Candida albicans

Eukaryotic Cell

Volumn 11, Issue 2, 2012, Pages 168-182

  Chen, Yu Ting ^a   Lin, Chia Ying ^a   Tsai, Pei Wen ^a   Yang, Cheng Yao ^b   Hsieh, Wen Ping ^c   Lan, Chung Yu ^a,d  

^a Institute of Molecular and Cellular Biology   (Taiwan)

^b Institute of Statistics   (Taiwan)

^c Department of Life Science ^*  (Taiwan)

^d NATIONAL TSING HUA UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC PROTEINASE; FUNGAL PROTEIN; GUANOSINE TRIPHOSPHATASE; PROTEIN KINASE; SAP2 PROTEIN, CANDIDA;

ARTICLE; CANDIDA ALBICANS; DNA MICROARRAY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; SIGNAL TRANSDUCTION; VIRULENCE;

ASPARTIC ACID ENDOPEPTIDASES; CANDIDA ALBICANS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GTP PHOSPHOHYDROLASES; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN KINASES; SIGNAL TRANSDUCTION; VIRULENCE;

CANDIDA ALBICANS;

EID: 84863057823     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.05200-11     Document Type: Article

References (84)

1. Alonso-Monge R, et al. 2010. The Sko1 protein represses the yeast-to-hypha transition and regulates the oxidative stress response in Candida albicans. Fungal Genet. Biol. 47:587-601.
2. Aronova S, Wedaman K, Anderson S, Yates J, Powers T. 2007. Probing the membrane environment of the TOR kinases reveals functional interactions between TORC1, actin, and membrane trafficking in Saccharomyces cerevisiae. Mol. Biol. Cell 18:2779-2794.
3. Aspuria PJ, Tamanoi F. 2004. The Rheb family of GTP-binding proteins. Cell Signal. 16:1105-1112.
4. Bain JM, Stubberfield C, Gow NA. 2001. Ura-status-dependent adhesion of Candida albicans mutants. FEMS Microbiol. Lett. 204:323-328.
5. Barbet NC, et al. 1996. TOR controls translation initiation and early G1 progression in yeast. Mol. Biol. Cell 7:25-42.
6. Bastidas RJ, Heitman J, Cardenas ME. 2009. The protein kinase Tor1 regulates adhesin gene expression in Candida albicans. PLoS Pathog. 5:e1000294.
7. Beck T, Hall MN. 1999. The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature 402:689- 692.
8. Bernardo SM, Khalique Z, Kot J, Jones JK, Lee SA. 2008. Candida albicans VPS1 contributes to protease secretion, filamentation, and bio-film formation. Fungal Genet. Biol. 45:861-877.
9. Bertram PG, et al. 2000. Tripartite regulation of Gln3p by TOR, Ure2p, and phosphatases. J. Biol. Chem. 275:35727-35733.
10. Biswas K, Morschhauser J. 2005. The Mep2p ammonium permease controls nitrogen starvation-induced filamentous growth in Candida albi-cans. Mol. Microbiol. 56:649-669.
11. Brand A, MacCallum DM, Brown AJ, Gow NA, Odds FC. 2004. Ectopic expression of URA3 can influence the virulence phenotypes and proteome of Candida albicans but can be overcome by targeted reintegration of URA3 at the RPS10 locus. Eukaryot. Cell 3:900-909.
12. Calderone RA. 2002. Candida and candidiasis. ASM Press, Washington, DC.
13. Calderone RA, Fonzi WA. 2001. Virulence factors of Candida albicans. Trends Microbiol. 9:327-335.
14. Cardenas ME, Cutler NS, Lorenz MC, Di Como CJ, Heitman J. 1999. The TOR signaling cascade regulates gene expression in response to nutrients. Genes Dev. 13:3271-3279.
15. Chen EJ, Kaiser CA. 2003. LST8 negatively regulates amino acid biosynthesis as a component of the TOR pathway. J. Cell Biol. 161:333-347.
16. Cheng S, et al. 2003. Evaluationof the roles of four Candida albicans genes in virulence by using gene disruption strains that express URA3 from the native locus. Infect. Immun. 71:6101-6103.
17. Correia A, et al. 2010. Limited role of secreted aspartyl proteinases Sap1 to Sap6 in Candida albicans virulence and host immune response in mu-rine hematogenously disseminated candidiasis. Infect. Immun. 78:4839- 4849.
18. Cox KH, et al. 2000. Saccharomyces cerevisiae GATA sequences function as TATA elements during nitrogen catabolite repression and when Gln3p is excluded from the nucleus by overproduction of Ure2p. J. Biol. Chem. 275:17611-17618.
19. Crandall M, and Edwards JE Jr. 1987. Segregation of proteinase-negative mutants from heterozygous Candida albicans. J. Gen. Microbiol. 133: 2817-2824.
20. Cruz MC, et al. 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.
21. Dabas N, Morschhauser J. 2007. Control of ammonium permease expression andfilamentous growthbythe GATA transcription factorsGLN3 and GAT1 in Candida albicans. Eukaryot. Cell 6:875-888.
22. Dabas N, Morschhauser J. 2008. A transcription factor regulatory cascade controls secreted aspartic protease expression in Candida albicans. Mol. Microbiol. 69:586-602.
23. deHart AK, Schnell JD, Allen DA, Tsai JY, Hicke L. 2003. Receptor internalization in yeast requires the Tor2-Rho1 signaling pathway. Mol. Biol. Cell 14:4676-4684.
24. Fadri M, Daquinag A, Wang S, Xue T, Kunz J. 2005. The pleckstrin homology domain proteins Slm1 and Slm2 are required for actin cytoskel-eton organization in yeast and bind phosphatidylinositol-4,5-bisphosphate and TORC2. Mol. Biol. Cell 16:1883-1900.
25. Garami A, et al. 2003. Insulin activation of Rheb, a mediator of mTOR/ S6K/4E-BP signaling, is inhibited by TSC1 and 2. Mol. Cell 11:1457-1466.
26. Gillum AM, Tsay EY, Kirsch DR. 1984. Isolation of the Candida 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. Hardwick JS, Kuruvilla FG, Tong JK, Shamji AF, Schreiber SL. 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.
28. Heitman J, Movva NR, Hall MN. 1991. Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253:905-909.
29. Hinnebusch AG.1997. Translational regulation ofyeastGCN4. A window on factors that control initiator-trna binding to the ribosome. J. Biol. Chem. 272:21661-21664.
30. Homma M, Chibana H, Tanaka K. 1993. Induction of extracellular proteinase in Candida albicans. J. Gen. Microbiol. 139(Pt. 6):1187-1193.
31. Hsu PC, Yang CY, Lan CY. 2011. Candida albicans Hap43 is a repressor induced under low-iron conditions and is essential for iron-responsive transcriptional regulation and virulence. Eukaryot. Cell 10:207-225.
32. Hube B, Monod M, Schofield DA, Brown AJ, Gow NA. 1994. Expression of seven members of the gene family encoding secretory aspartyl protein-ases in Candida albicans. Mol. Microbiol. 14:87-99.
33. Hube B, Ruchel R, Monod M, Sanglard D, Odds FC. 1998. Functional aspects of secreted Candida proteinases. Adv. Exp. Med. Biol. 436:339- 344.
34. Hube B, et al. 1997. Disruption of each of the secreted aspartyl proteinase genes SAP1, SAP2, and SAP3 of Candida albicans attenuates virulence. Infect. Immun. 65:3529-3538.
35. Kuruvilla FG, Shamji AF, Schreiber SL. 2001. Carbon- and nitrogen-quality signaling to translation are mediated by distinct GATA-type transcription factors. Proc. Natl. Acad. Sci. U. S. A. 98:7283-7288.
36. Lan CY, et al. 2004. Regulatory networks affected by iron availability in Candida albicans. Mol. Microbiol. 53:1451-1469.
37. Lay J, et al. 1998. Altered expression of selectable marker URA3 in gene-disrupted Candida albicans strains complicates interpretation of virulence studies. Infect. Immun. 66:5301-5306.
38. Lee SA, et al. 2009. Candida albicans VPS4 is required for secretion of aspartyl proteases and in vivo virulence. Mycopathologia 167:55-63.
39. Lermann U, Morschhauser J. 2008. Secreted aspartic proteases are not required for invasion of reconstituted human epithelia by Candida albi-cans. Microbiology 154:3281-3295.
40. Liao WL, Ramon AM, Fonzi WA. 2008. GLN3 encodes a global regulator of nitrogen metabolism and virulence of C. albicans. Fungal Genet. Biol. 45:514-526.
41. Loewith R, et al. 2002. Two TOR complexes, only one of which is rapa-mycin sensitive, have distinct roles in cell growth control. Mol. Cell 10: 457-468.
42. Long X, Lin Y, Ortiz-Vega S, Yonezawa K, Avruch J. 2005. Rheb binds and regulates the mTOR kinase. Curr. Biol. 15:702-713.
43. Long X, Ortiz-Vega S, Lin Y, Avruch J. 2005. Rheb binding to mammalian target of rapamycin (mTOR) is regulated by amino acid sufficiency. J. Biol. Chem. 280:23433-23436.
44. Mach KE, Furge KA, Albright CF. 2000. Loss of Rhb1, a Rheb-related GTPase in fission yeast, causes growth arrest with a terminal phenotype similar to that caused by nitrogen starvation. Genetics 155:611-622.
45. Magasanik B. 2005. The transduction of the nitrogen regulation signal in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 102:16537-16538.
46. Magasanik B, Kaiser CA. 2002. Nitrogen regulation in Saccharomyces cerevisiae. Gene 290:1-18.
47. Martínez P, Ljungdahl PO. 2005. Divergence of Stp1 and Stp2 transcription factors in Candida albicans places virulence factors required for proper nutrient acquisition under amino acid control. Mol. Cell. Biol. 25:9435-9446.
48. Matsumoto S, Bandyopadhyay A, Kwiatkowski DJ, Maitra U, Matsu-moto T. 2002. Role of the Tsc1-Tsc2 complex in signaling and transport across the cell membrane in the fission yeast Schizosaccharomyces pombe. Genetics 161:1053-1063.
49. Matsuo T, Otsubo Y, Urano J, Tamanoi F, Yamamoto M. 2007. Loss of the TOR kinase Tor2 mimics nitrogen starvation and activates the sexual development pathway in fission yeast. Mol. Cell. Biol. 27:3154-3164.
50. Naglik JR, Challacombe SJ, Hube B. 2003. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol. Mol. Biol. Rev. 67:400-428.
51. Nakashima A, Sato T, Tamanoi F. 2010. Fission yeast TORC1 regulates phosphorylation of ribosomal S6 proteins in response to nutrients and its activity is inhibited by rapamycin. J. Cell Sci. 123:777-786.
52. Nobile CJ, et al. 2006. Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog. 2:e63.
53. Nobile CJ, Nett JE, Andes DR, Mitchell AP. 2006. Function of Candida albicans adhesin Hwp1 in biofilm formation. Eukaryot. Cell 5:1604-1610.
54. Odds FC. 1988. Candida and candidosis. Baillière Tindall, London, United Kingdom.
55. Otsubo Y, Yamamato M. 2008. TOR signaling in fission yeast. Crit. Rev. Biochem. Mol. Biol. 43:277-283.
56. Park YN, Morschhauser J. 2005. Tetracycline-inducible gene expression and gene deletion in Candida albicans. Eukaryot. Cell 4:1328-1342.
57. Rehmann H, et al. 2008. Biochemical characterisation of TCTP questions its function as a guanine nucleotide exchange factor for Rheb. FEBS Lett. 582:3005-3010.
58. Reinke A, et al. 2004. TOR complex 1 includes a novel component, Tco89p (YPL180w), and cooperates with Ssd1p to maintain cellular integrity in Saccharomyces cerevisiae. J. Biol. Chem. 279:14752-14762.
59. Reuss O, Morschhauser J. 2006. A family of oligopeptide transporters is required for growth of Candida albicans on proteins. Mol. Microbiol. 60:795-812.
60. Reuss O, Vik A, Kolter R, Morschhauser J. 2004. The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341:119- 127.
61. Rohde JR, Bastidas R, Puria R, Cardenas ME. 2008. Nutritional control via Tor signaling in Saccharomyces cerevisiae. Curr. Opin. Microbiol. 11: 153-160.
62. Rohde JR, et al. 2004. TOR controls transcriptional and translational programs via Sap-Sit4 protein phosphatase signaling effectors. Mol. Cell. Biol. 24:8332-8341.
63. Rubio-Texeira M, Kaiser CA. 2006. Amino acids regulate retrieval of the yeast general amino acid permease from the vacuolar targeting pathway. Mol. Biol. Cell 17:3031-3050.
64. Russell CL, Brown AJ. 2005. Expression of one-hybrid fusions with Staphylococcus aureus lexA in Candida albicans confirms that Nrg1 is a transcriptional repressor and that Gcn4 is a transcriptional activator. Fungal Genet. Biol. 42:676-683.
65. Sharkey LL, Liao WL, Ghosh AK, Fonzi WA. 2005. Flanking direct repeats of hisG alter URA3 marker expression at the HWP1 locus of Candida albicans. Microbiology 151:1061-1071.
66. Shin CS, Kim SY, Huh WK. 2009. TORC1 controls degradation of the transcription factor Stp1, a key effector of the SPS amino-acid-sensing pathway in Saccharomyces cerevisiae. J. Cell Sci. 122:2089-2099.
67. Staib P, et al. 2008. Tetracycline-inducible expression of individual secreted aspartic proteases in Candida albicans allows isoenzyme-specific inhibitor screening. Antimicrob. Agents Chemother. 52:146-156.
68. Staschke KA, et al. 2010. Integration of general amino acid control and target of rapamycin (TOR) regulatory pathways in nitrogen assimilation in yeast. J. Biol. Chem. 285:16893-16911.
69. Storey JD, Tibshirani R. 2003. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. U. S. A. 100:9440-9445.
70. Tournu H, et al. 2005. Global role of the protein kinase Gcn2 in the human pathogen Candida albicans. Eukaryot. Cell 4:1687-1696.
71. Tripathi G, et al. 2002. Gcn4 co-ordinates morphogenetic and metabolic responses to amino acid starvation in Candida albicans. EMBO J. 21: 5448-5456.
72. Tsao CC, Chen YT, Lan CY. 2009. A small G protein Rhb1 and a GTPase-activating protein Tsc2 involved in nitrogen starvation-induced morphogenesis and cell wall integrity of Candida albicans. Fungal Genet. Biol. 46:126-136.
73. Urano J, et al. 2005. Identification of novel single amino acid changes that resultin hyperactivationofthe unique GTPase, Rheb, in fission yeast. Mol. Microbiol. 58:1074-1086.
74. Urano J, et al. 2007. Point mutations in TOR confer Rheb-independent growth in fission yeast and nutrient-independent mammalian TOR signaling in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 104:3514-3519.
75. Urano J, Tabancay AP, Yang W, Tamanoi F. 2000. The Saccharomyces cerevisiae Rheb G-protein is involved in regulating canavanine resistance and arginine uptake. J. Biol. Chem. 275:11198-11206.
76. Uritani M, et al. 2006. Fission yeast Tor2 links nitrogen signals to cell proliferation and acts downstream of the Rheb GTPase. Genes Cells 11: 1367-1379.
77. van Slegtenhorst M, Carr E, Stoyanova R, Kruger WD, Henske EP. 2004. Tsc1+ and tsc2+ regulate arginine uptake and metabolism in Schizosaccharomycespombe. J. Biol. Chem. 279:12706-12713.
78. van Slegtenhorst M, Mustafa A, Henske EP. 2005. Pas1, a G1 cyclin, regulates amino acid uptake and rescues a delay in G1 arrest in Tsc1 and Tsc2 mutants in Schizosaccharomyces pombe. Hum. Mol. Genet. 14:2851-2858.
79. Wedaman KP, et al. 2003. Tor kinases are in distinct membrane-associated protein complexes in Saccharomyces cerevisiae. Mol. Biol. Cell 14:1204-1220.
80. Weisman R, Roitburg I, Nahari T, Kupiec M. 2005. Regulation of leucine uptake by tor1 + in Schizosaccharomyces pombe is sensitive to rapa-mycin. Genetics 169:539-550.
81. White TC, Agabian N. 1995. Candida albicans secreted aspartyl protein-ases: isoenzyme pattern is determined by cell type, and levels are determined by environmental factors. J. Bacteriol. 177:5215-5221.
82. Xie MW, et al. 2005. Insights into TOR function and rapamycin response: chemical genomic profiling by using a high-density cell array method. Proc. Natl. Acad. Sci. U. S. A. 102:7215-7220.
83. Zacchi LF, Gomez-Raja J, Davis DA. 2010. Mds3 regulates morphogenesis in Candida albicans through the TOR pathway. Mol. Cell. Biol. 30: 3695-3710.
84. Zhao X, Oh SH, Yeater KM, Hoyer LL. 2005. Analysis of the Candida albicansAls2p and Als4p adhesins suggests the potential for compensatory function within the Als family. Microbiology 151:1619-1630.