Regulation of copper toxicity by Candida albicans GPA2

Eukaryotic Cell

Volumn 12, Issue 7, 2013, Pages 954-961

  Schwartz, Jennifer A ^a,b,d   Olarte, Karen T ^a   Michalek, Jamie L ^c   Jandu, Gurjinder S ^a   Michel, Sarah L J ^c   Brunoa, Vincent M ^a,b  

^a Institute for Genome Sciencesa and Department of Microbiology and Immunology   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

^d Profectus BioSciences Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CADMIUM; CISPLATIN; COPPER; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; FUNGAL PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; IRON; SILVER;

ARTICLE; CANDIDA ALBICANS; CYTOLOGY; DRUG EFFECT; FUNGAL GENE; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; METABOLISM; SIGNAL TRANSDUCTION;

CADMIUM; CANDIDA ALBICANS; CISPLATIN; COPPER; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FUNGAL PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; GTP-BINDING PROTEIN ALPHA SUBUNITS; HOMEOSTASIS; IRON; SIGNAL TRANSDUCTION; SILVER;

CANDIDA ALBICANS; FILOBASIDIELLA NEOFORMANS; SACCHAROMYCES CEREVISIAE;

EID: 84879383041     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00344-12     Document Type: Article

References (41)

1. Boal AK, Rosenzweig AC. 2009. Structural biology of copper trafficking. Chem. Rev. 109:4760-4779.
2. Nevitt T, Höhrvik Thiele DJ. 2012. Charting the travels of copper in eukaryotes from yeast to mammals. Biochim. Biophys. Acta 1823:1580-1593.
3. Borkow G. 2009. Copper, an ancient remedy returning to fight microbial, fungal and viral infections. Curr. Chem. Biol. 3:272-278.
4. Osman D, Waldron KJ, Denton H, Taylor CM, Grant AJ, Mastroeni P, Robinson NJ, Cavet JS. 2010. Copper homeostasis in Salmonella is atypical and copper-CueP is a major periplasmic metal complex. J. Biol. Chem. 285:25259-25268.
5. White C, Lee J, Kambe T, Fritsche K. 2009. A role for the ATP7A copper-transporting ATPase in macrophage bactericidal activity. J. Biol. Chem. 284:33949-33956.
6. Wolschendorf F, Ackart D, Shrestha TB, Hascall-Dove L, Nolan S, Lamichhane G, Wang Y, Bossmann SH, Basaraba RJ, Niederweis M. 2011. Copper resistance is essential for virulence of Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U. S. A. 108:1621-1626.
7. Georgatsou E, Mavrogiannis LA, Fragiadakis GS, Alexandraki D. 1997. The yeast Fre1p/Fre2p cupric reductases facilitate copper uptake and are regulated by the copper-modulated Mac1p activator. J. Biol. Chem. 272: 13786-13792.
8. Labbé S, Zhu Z, Thiele DJ. 1997. Copper-specific transcriptional repression of yeast genes encoding critical components in the copper transport pathway. J. Biol. Chem. 272:15951-15958.
9. Liu XD, Thiele DJ. 1997. Yeast metallothionein gene expression in response to metals and oxidative stress. Methods 11:289-299.
10. Odermatt A, Suter H, Krapf R, Solioz M. 1992. An ATPase operon involved in copper resistance by Enterococcus hirae. Ann. N. Y. Acad. Sci. 671:484-486.
11. Ooi CE, Rabinovich E, Dancis A, Bonifacino JS, Klausner RD. 1996. Copper-dependent degradation of the Saccharomyces cerevisiae plasma membrane copper transporter Ctr1p in the apparent absence of endocytosis. EMBO J. 15:3515-3523.
12. Yamaguchi-Iwai Y, Serpe M, Haile D, Yang W, Kosman DJ, Klausner RD, Dancis A. 1997. Homeostatic regulation of copper uptake in yeast via direct binding of MAC1 protein to upstream regulatory sequences of FRE1 and CTR1. J. Biol. Chem. 272:17711-17718.
13. Jeeves RE, Mason RP, Woodacre A, Cashmore AM. 2011. Ferric reductase genes involved in high-affinity iron uptake are differentially regulated in yeast and hyphae of Candida albicans. Yeast 28:629-644.
14. Marvin ME, Mason RP, Cashmore AM. 2004. The CaCTR1 gene is required for high-affinity iron uptake and is transcriptionally controlled by a copper-sensing transactivator encoded by CaMAC1. Microbiology 150:2197-2208.
15. Woodacre A, Mason RP, Jeeves RE, Cashmore AM. 2008. Copperdependent transcriptional regulation by Candida albicans Mac1p. Microbiology 154:1502-1512.
16. Graden JA, Winge DR. 1997. Copper-mediated repression of the activation domain in the yeast Mac1p transcription factor. Proc. Natl. Acad. Sci. U. S. A. 94:5550-5555.
17. Hassett R, Kosman DJ. 1995. Evidence for Cu(II) reduction as a component of copper uptake by Saccharomyces cerevisiae. J. Biol. Chem. 270: 128-134.
18. Yonkovich J. 2002. Copper ion-sensing transcription factor Mac1p posttranslationally controls the degradation of its target gene product Ctr1p. J. Biol. Chem. 277:23981-23984.
19. Riggle PJ, Kumamoto CA. 2000. Role of a Candida albicans P1-type ATPase in resistance to copper and silver ion toxicity. J. Bacteriol. 182: 4899-4905.
20. Weissman Z, Berdicevsky I, Cavari BZ, Kornitzer D. 2000. The high copper tolerance of Candida albicans is mediated by a P-type ATPase. Proc. Natl. Acad. Sci. U. S. A. 97:3520-3525.
21. Buchman C, Skroch P, Welch J, Fogel S, Karin M. 1989. The CUP2 gene product, regulator of yeast metallothionein expression, is a copperactivated DNA-binding protein. Mol. Cell. Biol. 9:4091-4095.
22. Szczypka MS, Thiele DJ. 1989. A cysteine-rich nuclear protein activates yeast metallothionein gene transcription. Mol. Cell. Biol. 9:421-429.
23. Thiele DJ. 1988. ACE1 regulates expression of the Saccharomyces cerevisiae metallothionein gene. Mol. Cell. Biol. 8:2745-2752.
24. Homann OR, Dea J, Noble SM, Johnson AD. 2009. A phenotypic profile of the Candida albicans regulatory network. PLoS Genet. 5:e1000783.
25. Bruno VM, Wang Z, Marjani SL, Euskirchen GM, Martin J, Sherlock G, Snyder M. 2010. Comprehensive annotation of the transcriptome of the human fungal pathogen Candida albicans using RNA-seq. Genome Res. 20:1451-1458.
26. Bennett RJ, Johnson AD. 2006. The role of nutrient regulation and the Gpa2 protein in the mating pheromone response of C. albicans. Mol. Microbiol. 62:100-119.
27. Ishida S, Lee J, Thiele DJ, Herskowitz I. 2002. Uptake of the anticancer drug cisplatin mediated by the copper transporter Ctr1 in yeast and mammals. Proc. Natl. Acad. Sci. U. S. A. 99:14298-14302.
28. Marvin ME, Williams PH, Cashmore AM. 2003. The Candida albicans CTR1 gene encodes a functional copper transporter. Microbiology 149: 1461-1474.
29. Karin M, Najarian R, Haslinger A, Valenzuela P, Welch J, Fogel S. 1984. Primary structure and transcription of an amplified genetic locus: the CUP1 locus of yeast. Proc. Natl. Acad. Sci. U. S. A. 81:337-341.
30. Winge DR, Nielson KB, Gray WR, Hamer DH. 1985. Yeast metallothionein. Sequence and metal-binding properties. J. Biol. Chem. 260:14464- 14470.
31. Maidan MM, De Rop L, Serneels J, Exler S, Rupp S, Tournu H, Thevelein JM, Van Dijck P. 2005. The G protein-coupled receptor Gpr1 and the Galpha protein Gpa2 act through the cAMP-protein kinase A pathway to induce morphogenesis in Candida albicans. Mol. Biol. Cell 16:1971-1986.
32. Miwa T, Takagi Y, Shinozaki M, Yun C-W, Schell WA, Perfect JR, Kumagai H, Tamaki H. 2004. Gpr1, a putative G-protein-coupled receptor, regulates morphogenesis and hypha formation in the pathogenic fungus Candida albicans. Eukaryot. Cell 3:919-931.
33. Sánchez-Martínez C, Pérez-Martín J. 2002. Gpa2, a G-protein alpha subunit required for hyphal development in Candida albicans. Eukaryot. Cell 1:865-874.
34. Alspaugh JA, Perfect JR, Heitman J. 1997. Cryptococcus neoformans mating and virulence are regulated by the G-protein alpha subunit GPA1 and cAMP. Genes Dev. 11:3206-3217.
35. Colombo S, Ma P, Cauwenberg L, Winderickx J, Crauwels M, Teunissen A, Nauwelaers D, de Winde JH, Gorwa MF, Colavizza D, Thevelein JM. 1998. Involvement of distinct G-proteins, Gpa2 and Ras, in glucoseand intracellular acidification-induced cAMP signalling in the yeast Saccharomyces cerevisiae. EMBO J. 17:3326-3341.
36. D'Souza CA, Alspaugh JA, Yue C, Harashima T, Cox GM, Perfect JR, Heitman J. 2001. Cyclic AMP-dependent protein kinase controls virulence of the fungal pathogen Cryptococcus neoformans. Mol. Cell. Biol. 21:3179-3191.
37. Nakafuku M, Obara T, Kaibuchi K, Miyajima I, Miyajima A, Itoh H, Nakamura S, Arai K, Matsumoto K, Kaziro Y. 1988. Isolation of a second yeast Saccharomyces cerevisiae gene (GPA2) coding for guanine nucleotide- binding regulatory protein: studies on its structure and possible functions. Proc. Natl. Acad. Sci. U. S. A. 85:1374-1378.
38. Tolkacheva T, McNamara P, Piekarz E, Courchesne W. 1994. Cloning of a Cryptococcus neoformans gene, GPA1, encoding a G-protein alphasubunit homolog. Infect. Immun. 62:2849-2856.
39. Silva FD, Rossi DCP, Martinez LR, Frases S, Fonseca FL, Campos CBL, Rodrigues ML, Nosanchuk JD, Daffre S. 2011. Effects of microplusin, a copper-chelating antimicrobial peptide, against Cryptococcus neoformans. FEMS Microbiol. Lett. 324:64-72.
40. Park H, Myers CL, Sheppard DC, Phan QT, Sanchez AA, Edwards JE, Filler SG. 2005. Role of the fungal Ras-protein kinase A pathway in governing epithelial cell interactions during oropharyngeal candidiasis. Cell. Microbiol. 7:499-510.
41. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, Andre B, Bangham R, Benito R, Boeke JD, Bussey H, Chu AM, Connelly C, Davis K, Dietrich F, Dow SW, El Bakkoury M, Foury F, Friend SH, Gentalen E, Giaever G, Hegemann JH, Jones T, Laub M, Liao H, Liebundguth N, Lockhart DJ, Lucau-Danila A, Lussier M, M'Rabet N, Menard P, Mittmann M, Pai C, Rebischung C, Revuelta JL, Riles L, Roberts CJ, Ross-MacDonald P, Scherens B, Snyder M, Sookhai-Mahadeo S, Storms RK, Véronneau S, Voet M, Volckaert G, Ward TR, Wysocki R, Yen GS, Yu K, Zimmermann K, Philippsen P, Johnston M, Davis RW. 1999. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285:901-906.