The transmembrane protein Opy2 mediates activation of the Cek1 MAP kinase in Candida albicans

Fungal Genetics and Biology

Volumn 50, Issue 1, 2013, Pages 21-32

  Herrero de Dios, Carmen ^a   Román, Elvira ^a   Diez, Carla ^a   Alonso Monge, Rebeca ^a   Pla, Jesús ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Candida albicans; Cell wall integrity; MAPK phosphorylation; Osmotic stress; Pathogenic fungus; SVG

Indexed keywords

CEK1 PROTEIN; CONGO RED; FUNGAL PROTEIN; HOG1 PROTEIN; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MUTANT PROTEIN; PROTEIN OPY2; TUNICAMYCIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FUNGAL CELL WALL; FUNGAL GENE; FUNGAL VIRULENCE; FUNGUS GROWTH; GENE DELETION; GENE EXPRESSION REGULATION; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; NONHUMAN; OPY2 GENE; OSMOLARITY; OSMOTIC STRESS; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

ANIMALS; ANTIFUNGAL AGENTS; CANDIDA ALBICANS; CONGO RED; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENE KNOCKOUT TECHNIQUES; GENETIC COMPLEMENTATION TEST; LEPIDOPTERA; MEMBRANE PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE 3; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; VIRULENCE; VIRULENCE FACTORS;

CANDIDA ALBICANS; EUKARYOTA; FUNGI; GALLERIA MELLONELLA; SACCHAROMYCES CEREVISIAE;

EID: 84871363778     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2012.11.001     Document Type: Article

References (50)

1. Alonso-Monge R., Navarro-García F., Molero G., Diez-Orejas R., Gustin M., Pla J., Sánchez M., Nombela C. Role of the mitogen-activated protein kinase Hog1p in morphogenesis and virulence of Candida albicans. J. Bacteriol. 1999, 181(10):3058-3068.
2. Alonso-Monge R., Real E., Wojda I., Bebelman J.P., Mager W.H., Siderius M. Hyperosmotic stress response and regulation of cell wall integrity in Saccharomyces cerevisiae share common functional aspects. Mol. Microbiol. 2001, 41(3):717-730.
3. Alonso-Monge R., Navarro-García F., Román E., Negredo A.I., Eisman B., Nombela C., Pla J. The Hog1 mitogen-activated protein kinase is essential in the oxidative stress response and chlamydospore formation in Candida albicans. Eukaryot. Cell 2003, 2(2):351-361.
4. Alonso-Monge R., Carvaihlo S., Nombela C., Rial E., Pla J. The Hog1 MAP kinase controls respiratory metabolism in the fungal pathogen Candida albicans. Microbiology 2009, 155(Pt 2):413-423.
5. Arana D.M., Nombela C., Alonso-Monge R., Pla J. The Pbs2 MAP kinase kinase is essential for the oxidative-stress response in the fungal pathogen Candida albicans. Microbiology 2005, 151(Pt 4):1033-1049.
6. Arana D.M., Alonso-Monge R., Du C., Calderone R., Pla J. Differential susceptibility of mitogen-activated protein kinase pathway mutants to oxidative-mediated killing by phagocytes in the fungal pathogen Candida albicans. Cell Microbiol. 2007, 9(7):1647-1659.
7. Bermejo C., et al. The sequential activation of the yeast HOG and SLT2 pathways is required for cell survival to cell wall stress. Mol. Biol. Cell 2008, 19(3):1113-1124.
8. Brennan M., Thomas D., Whiteway M., Kavanagh K. Correlation between virulence of Candida albicans mutants in mice and Galleria mellonella larvae. FEMS Immunol. Med. Microbiol. 2002, 34(2):153.
9. Calera J.A., Zhao X.J., Calderone R. Defective hyphal development and avirulence caused by a deletion of the SSK1 response regulator gene in Candida albicans. Infect. Immun. 2000, 68(2):518-525.
10. Cantero P.D., Lengsfeld C., Prill S.K., Subanovic M., Roman E., Pla J., Ernst J.F. Transcriptional and physiological adaptation to defective protein-O-mannosylation in Candida albicans. Mol. Microbiol. 2007, 64(4):1115-1128.
11. Chauhan N., Inglis D., Roman E., Pla J., Li D., Calera J.A., Calderone R. Candida albicans response regulator gene SSK1 regulates a subset of genes whose functions are associated with cell wall biosynthesis and adaptation to oxidative stress. Eukaryot. Cell 2003, 2(5):1018-1024.
12. Cheetham J., Smith D.A., da Silva D.A., Doris K.S., Patterson M.J., Bruce C.R., Quinn J. A single MAPKKK regulates the Hog1 MAPK pathway in the pathogenic fungus Candida albicans. Mol. Biol. Cell 2007, 18(11):4603-4614.
13. Chen D.C., Yang B.C., Kuo T.T. One-step transformation of yeast in stationary phase. Curr. Genet. 1992, 21(1):83-84.
14. Chen J., Chen J., Lane S., Liu H. A conserved mitogen-activated protein kinase pathway is required for mating in Candida albicans. Mol. Microbiol. 2002, 46(5):1335-1344.
15. Csank C., Schröppel K., Leberer E., Harcus D., Mohamed O., Meloche S., Thomas D.Y., Whiteway M. Roles of the Candida albicans mitogen-activated protein kinase homolog, Cek1p, in hyphal development and systemic candidiasis. Infect. Immun. 1998, 66(6):2713-2721.
16. Desalermos, A., Fuchs, B.B., Mylonakis, E., 2012. Selecting an invertebrate model host for the study of fungal pathogenesis. Plos Pathog. 8(2).
17. Diez-Orejas R., Molero G., Navarro-García F., Pla J., Nombela C., Sánchez-Pérez M. Reduced virulence of Candida albicans MKC1 mutants: a role for a mitogen-activated protein kinase in pathogenesis. Infect. Immun. 1997, 65(2):833-837.
18. Eisman B., Alonso-Monge R., Román E., Arana D., Nombela C., Pla J. The Cek1 and Hog1 mitogen-activated protein kinases play complementary roles in cell wall biogenesis and chlamydospore formation in the fungal pathogen Candida albicans. Eukaryot. Cell 2006, 5(2):347-358.
19. Ekiel I., et al. Binding the atypical RA domain of Ste50p to the unfolded Opy2p cytoplasmic tail is essential for the high-osmolarity glycerol pathway. Mol. Biol. Cell 2009, 20(24):5117-5126.
20. Enjalbert B., Smith D.A., Cornell M.J., Alam I., Nicholls S., Brown A.J., Quinn J. Role of the Hog1 stress-activated protein kinase in the global transcriptional response to stress in the fungal pathogen Candida albicans. Mol. Biol. Cell. 2006, 17(2):1018-1032.
21. Fonzi W.A., Irwin M.Y. Isogenic strain construction and gene mapping in Candida albicans. Genetics 1993, 134(3):717-728.
22. Garcia R., Bermejo C., Grau C., Perez R., Rodriguez-Pena J.M., Francois J., Nombela C., Arroyo J. The global transcriptional response to transient cell wall damage in Saccharomyces cerevisiae and its regulation by the cell integrity signaling pathway. J. Biol. Chem. 2004, 279(15):15183-15195.
23. Garcia R., Rodriguez-Pena J.M., Bermejo C., Nombela C., Arroyo J. The high osmotic response and cell wall integrity pathways cooperate to regulate transcriptional responses to zymolyase-induced cell wall stress in Saccharomyces cerevisiae. J. Biol. Chem. 2009, 284(16):10901-10911.
24. Gari E., Piedrafita L., Aldea M., Herrero E. A set of vectors with a tetracycline-regulatable promoter system for modulated gene expression in Saccharomyces cerevisiae. Yeast 1997, 13(9):837-848.
25. Kultz D. Phylogenetic and functional classification of mitogen- and stress-activated protein kinases. J. Mol. Evol. 1998, 46(5):571-588.
26. Kumamoto C.A. A contact-activated kinase signals Candida albicans invasive growth and biofilm development. Proc. Natl. Acad. Sci. U.S.A. 2005, 102(15):5576-5581.
27. Lee B.N., Elion E.A. The MAPKKK Ste11 regulates vegetative growth through a kinase cascade of shared signaling components. Proc. Natl. Acad. Sci. U.S.A. 1999, 96(22):12679-12684.
28. Martin H., Rodriguez-Pachon J.M., Ruiz C., Nombela C., Molina M. Regulatory mechanisms for modulation of signaling through the cell integrity Slt2-mediated pathway in Saccharomyces cerevisiae. J. Biol. Chem. 2000, 275(2):1511-1519.
29. Mullick A., et al. Gene expression in HL60 granulocytoids and human polymorphonuclear leukocytes exposed to Candida albicans. Infect. Immun. 2004, 72(1):414-429.
30. Mylonakis E. Galleria mellonella and the study of fungal pathogenesis: making the case for another genetically tractable model host. Mycopathologia 2008, 165(1):1-3.
31. Navarro-García F., Sanchez M., Pla J., Nombela C. Functional characterization of the MKC1 gene of Candida albicans, which encodes a mitogen-activated protein kinase homolog related to cell integrity. Mol. Cell. Biol. 1995, 15(4):2197-2206.
32. Navarro-García F., Alonso-Monge R., Rico H., Pla J., Sentandreu R., Nombela C. A role for the MAP kinase gene MKC1 in cell wall construction and morphological transitions in Candida albicans. Microbiology 1998, 144(Pt 2):411-424.
33. Navarro-Garcia F., Eisman B., Fiuza S.M., Nombela C., Pla J. The MAP kinase Mkc1p is activated under different stress conditions in Candida albicans. Microbiology 2005, 151(Pt 8):2737-2749.
34. Negredo, A., Monteoliva, L., Gil, C., Pla, J., Nombela, C., 1997. Cloning, analysis and one-step disruption of the ARG5,6 gene of Candida albicans.
35. Odds F.C. Candida and Candidosis London 1988, Baillière Tindall.
36. O'Rourke S.M., Herskowitz I. A third osmosensing branch in Saccharomyces cerevisiae requires the Msb2 protein and functions in parallel with the Sho1 branch. Mol. Cell Biol. 2002, 22(13):4739-4749.
37. Park Y.N., Morschhauser J. Tetracycline-inducible gene expression and gene deletion in Candida albicans. Eukaryot. Cell 2005, 4(8):1328-1342.
38. Posas F., Wurgler-Murphy S.M., Maeda T., Witten E.A., Thai T.C., Saito H. Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 " two-component" osmosensor. Cell 1996, 86(6):865-875.
39. Reuss O., Vik A., Kolter R., Morschhauser J. The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 2004, 341:119-127.
40. Román E., Nombela C., Pla J. The Sho1 adaptor protein links oxidative stress to morphogenesis and cell wall biosynthesis in the fungal pathogen Candida albicans. Mol. Cell Biol. 2005, 25(23):10611-10627.
41. Román E., Alonso-Monge R., Gong Q.H., Li D.M., Calderone R., Pla J. The Cek1 MAPK is a short-lived protein regulated by quorum sensing in the fungal pathogen Candida albicans. FEMS Yeast Res. 2009, 9(6):942-955.
42. Román E., Cottier F., Ernst J.F., Pla J. Msb2 signaling mucin controls activation of Cek1 mitogen-activated protein kinase in Candida albicans. Eukaryot. Cell 2009, 8(8):1235-1249.
43. San José C., Alonso-Monge R., Pérez-Díaz R.M., Pla J., Nombela C. The mitogen-activated protein kinase homolog HOG1 gene controls glycerol accumulation in the pathogenic fungus Candida albicans. J. Bacteriol. 1996, 178(19):5850-5852.
44. Smith D.A., Nicholls S., Morgan B.A., Brown A.J., Quinn J. A conserved stress-activated protein kinase regulates a core stress response in the human pathogen Candida albicans. Mol. Biol. Cell. 2004, 15:4179-4190.
45. Soll D.R. Evolution of a new signal transduction pathway in Candida albicans. Trends Microbiol. 2011, 19(1):8-13.
46. Tatebayashi K., Tanaka K., Yang H.Y., Yamamoto K., Matsushita Y., Tomida T., Imai M., Saito H. Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. EMBO J. 2007, 26(15):3521-3533.
47. Wu C.L., Jansen G., Zhang L.C., Thomas D.Y., Whiteway M. Adaptor protein Ste50p links the Ste11p MEKK to the HOG pathway through plasma membrane association. Genes Dev. 2006, 20(6):734-746.
48. Yamamoto K., Tatebayashi K., Tanaka K., Saito H. Dynamic control of yeast MAP kinase network by induced association and dissociation between the Ste50 scaffold and the Opy2 membrane anchor. Mol. Cell 2010, 40(1):87-98.
49. Yang H.Y., Tatebayashi K., Yamamoto K., Saito H. Glycosylation defects activate filamentous growth Kss1 MAPK and inhibit osmoregulatory Hog1 MAPK. EMBO J. 2009, 28(10):1380-1391.
50. Yi, S., Sahni, N., Daniels, K.J., Lu, K.L., Srikantha, T., Huang, G.H., Garnaas, A.M., Soll, D.R., 2011. Alternative mating type configurations (a/alpha versus a/a or a/alpha) of Candida albicans result in alternative biofilms regulated by different pathways. Plos Biol. 9(8).