pH response pathways in fungi: Adapting to host-derived and environmental signals

Mycobiology

Volumn 39, Issue 4, 2011, Pages 249-256

  Selvig, Kyla ^a   Alspaugh, J Andrew ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aspergillus nidulans; Candida albicans; Cryptococcus neoformans; PacC; Rim101; Saccharomyces cerevisiae; Signal transduction; Yeast

Indexed keywords

CANDIDA ALBICANS; EMERICELLA NIDULANS; FILOBASIDIELLA NEOFORMANS; FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 84856337339     PISSN: 12298093     EISSN: 20929323     Source Type: Journal    
DOI: 10.5941/MYCO.2011.39.4.249     Document Type: Review

References (53)

1. Peñalva MA, Tilburn J, Bignell E, Arst HN Jr. Ambient pH gene regulation in fungi: making connections. Trends Microbiol 2008;16:291-300.
2. Peñalva MA, Arst HN Jr. Recent advances in the characterization of ambient pH regulation of gene expression in filamentous fungi and yeasts. Annu Rev Microbiol 2004;58:425-51.
3. Arst HN, Peñalva MA. pH regulation in Aspergillus and parallels with higher eukaryotic regulatory systems. Trends Genet 2003;19:224-31.
4. Shenoy SK, Lefkowitz RJ. beta-Arrestin-mediated receptor trafficking and signal transduction. Trends Pharmacol Sci 2011;32:521-33.
5. Herrador A, Herranz S, Lara D, Vincent O. Recruitment of the ESCRT machinery to a putative seven-transmembranedomain receptor is mediated by an arrestin-related protein. Mol Cell Biol 2010;30:897-907.
6. Herranz S, Rodríguez JM, Bussink HJ, Sánchez-Ferrero JC, Arst HN Jr, Peñalva MA, Vincent O. Arrestin-related proteins mediate pH signaling in fungi. Proc Natl Acad Sci U S A 2005;102:12141-6.
7. Hervás-Aguilar A, Galindo A, Peñalva MA. Receptorindependent ambient pH signaling by ubiquitin attachment to fungal arrestin-like PalF. J Biol Chem 2010;285:18095-102.
8. Calcagno-Pizarelli AM, Negrete-Urtasun S, Denison SH, Rudnicka JD, Bussink HJ, Múnera-Huertas T, Stanton L, Hervás-Aguilar A, Espeso EA, Tilburn J, et al. Establishment of the ambient pH signaling complex in Aspergillus nidulans: PalI assists plasma membrane localization of PalH. Eukaryot Cell 2007;6:2365-75.
9. Rothfels K, Tanny JC, Molnar E, Friesen H, Commisso C, Segall J. Components of the ESCRT pathway, DFG16, and YGR122w are required for Rim101 to act as a corepressor with Nrg1 at the negative regulatory element of the DIT1 gene of Saccharomyces cerevisiae. Mol Cell Biol 2005;25:6772-88.
10. Barwell KJ, Boysen JH, Xu W, Mitchell AP. Relationship of DFG16 to the Rim101p pH response pathway in Saccharomyces cerevisiae and Candida albicans. Eukaryot Cell 2005;4:890-9.
11. Henne WM, Buchkovich NJ, Emr SD. The ESCRT pathway. Dev Cell 2011;21:77-91.
12. Xu W, Smith FJ Jr, Subaran R, Mitchell AP. Multivesicular body-ESCRT components function in pH response regulation in Saccharomyces cerevisiae and Candida albicans. Mol Biol Cell 2004;15:5528-37.
13. Galindo A, Hervás-Aguilar A, Rodríguez-Galán O, Vincent O, Arst HN Jr, Tilburn J, Peñalva MA. PalC, one of two Bro1 domain proteins in the fungal pH signalling pathway, localizes to cortical structures and binds Vps32. Traffic 2007;8:1346-64.
14. Vincent O, Rainbow L, Tilburn J, Arst HN Jr, Peñalva MA. YPXL/I is a protein interaction motif recognized by aspergillus PalA and its human homologue, AIP1/Alix. Mol Cell Biol 2003;23:1647-55.
15. Lamb TM, Mitchell AP. The transcription factor Rim101p governs ion tolerance and cell differentiation by direct repression of the regulatory genes NRG1 and SMP1 in Saccharomyces cerevisiae. Mol Cell Biol 2003;23:677-86.
16. Li W, Mitchell AP. Proteolytic activation of Rim1p, a positive regulator of yeast sporulation and invasive growth. Genetics 1997;145:63-73.
17. Díez E, Alvaro J, Espeso EA, Rainbow L, Suárez T, Tilburn J, Arst HN Jr, Peñalva MA. Activation of the Aspergillus PacC zinc finger transcription factor requires two proteolytic steps. EMBO J 2002;21:1350-9.
18. Hervás-Aguilar A, Rodríguez JM, Tilburn J, Arst HN Jr, Peñalva MA. Evidence for the direct involvement of the proteasome in the proteolytic processing of the Aspergillus nidulans zinc finger transcription factor PacC. J Biol Chem 2007;282:34735-47.
19. Peñalva MA, Arst HN Jr. Regulation of gene expression by ambient pH in filamentous fungi and yeasts. Microbiol Mol Biol Rev 2002;66:426-46.
20. Caddick MX, Brownlee AG, Arst HN Jr. Regulation of gene expression by pH of the growth medium in Aspergillus nidulans. Mol Gen Genet 1986;203:346-53.
21. Lamb TM, Xu W, Diamond A, Mitchell AP. Alkaline response genes of Saccharomyces cerevisiae and their relationship to the RIM101 pathway. J Biol Chem 2001;276:1850-6.
22. Davis DA. How human pathogenic fungi sense and adapt to pH: the link to virulence. Curr Opin Microbiol 2009;12:365-70.
23. Davis D. Adaptation to environmental pH in Candida albicans and its relation to pathogenesis. Curr Genet 2003;44:1-7.
24. Davis D, Edwards JE Jr, Mitchell AP, Ibrahim AS. Candida albicans RIM101 pH response pathway is required for hostpathogen interactions. Infect Immun 2000;68:5953-9.
25. Davis D, Wilson RB, Mitchell AP. RIM101-dependent andindependent pathways govern pH responses in Candida albicans. Mol Cell Biol 2000;20:971-8.
26. Mitchell AP. Dimorphism and virulence in Candida albicans. Curr Opin Microbiol 1998;1:687-92.
27. De Bernardis F, Mühlschlegel FA, Cassone A, Fonzi WA. The pH of the host niche controls gene expression in and virulence of Candida albicans. Infect Immun 1998;66:3317-25.
28. Cornet M, Richard ML, Gaillardin C. The homologue of the Saccharomyces cerevisiae RIM9 gene is required for ambient pH signalling in Candida albicans. Res Microbiol 2009;160:219-23.
29. Li M, Martin SJ, Bruno VM, Mitchell AP, Davis DA. Candida albicans Rim13p, a protease required for Rim101p processing at acidic and alkaline pHs. Eukaryot Cell 2004;3:741-51.
30. Baek YU, Li M, Davis DA. Candida albicans ferric reductases are differentially regulated in response to distinct forms of iron limitation by the Rim101 and CBF transcription factors. Eukaryot Cell 2008;7:1168-79.
31. Bensen ES, Martin SJ, Li M, Berman J, Davis DA. Transcriptional profiling in Candida albicans reveals new adaptive responses to extracellular pH and functions for Rim101p. Mol Microbiol 2004;54:1335-51.
32. Nobile CJ, Solis N, Myers CL, Fay AJ, Deneault JS, Nantel A, Mitchell AP, Filler SG. Candida albicans transcription factor Rim101 mediates pathogenic interactions through cell wall functions. Cell Microbiol 2008;10:2180-96.
33. Thewes S, Kretschmar M, Park H, Schaller M, Filler SG, Hube B. In vivo and ex vivo comparative transcriptional profiling of invasive and non-invasive Candida albicans isolates identifies genes associated with tissue invasion. Mol Microbiol 2007;63:1606-28.
34. Baek YU, Martin SJ, Davis DA. Evidence for novel pHdependent regulation of Candida albicans Rim101, a direct transcriptional repressor of the cell wall beta-glycosidase Phr2. Eukaryot Cell 2006;5:1550-9.
35. Heitman J, Kozel TR, Kwon-Chung KJ, Perfect JR, Casadevall A. Cryptococcus: from human pathogen to model yeast. Washington, D.C.: ASM Press; 2010.
36. Cox GM, Harrison TS, McDade HC, Taborda CP, Heinrich G, Casadevall A, Perfect JR. Superoxide dismutase influences the virulence of Cryptococcus neoformans by affecting growth within macrophages. Infect Immun 2003;71:173-80.
37. Nyberg K, Johansson U, Johansson A, Camner P. Phagolysosomal pH in alveolar macrophages. Environ Health Perspect 1992;97:149-52.
38. Liu OW, Chun CD, Chow ED, Chen C, Madhani HD, Noble SM. Systematic genetic analysis of virulence in the human fungal pathogen Cryptococcus neoformans. Cell 2008;135:174-88.
39. O'Meara TR, Norton D, Price MS, Hay C, Clements MF, Nichols CB, Alspaugh JA. Interaction of Cryptococcus neoformans Rim101 and protein kinase A regulates capsule. PLoS Pathog 2010;6:e1000776.
40. Okagaki LH, Wang Y, Ballou ER, O'Meara TR, Bahn YS, Alspaugh JA, Xue C, Nielsen K. Cryptococcal titan cell formation is regulated by G-protein signaling in response to multiple stimuli. Eukaryot Cell 2011;10:1306-16.
41. Okagaki LH, Strain AK, Nielsen JN, Charlier C, Baltes NJ, Chrétien F, Heitman J, Dromer F, Nielsen K. Cryptococcal cell morphology affects host cell interactions and pathogenicity. PLoS Pathog 2010;6:e1000953.
42. Zaragoza O, García-Rodas R, Nosanchuk JD, Cuenca-Estrella M, Rodriguez-Tudela JL, Casadevall A. Fungal cell gigantism during mammalian infection. PLoS Pathog 2010;6:e1000945.
43. Chun CD, Madhani HD. Ctr2 links copper homeostasis to polysaccharide capsule formation and phagocytosis inhibition in the human fungal pathogen Cryptococcus neoformans. PLoS One 2010;5;e12503.
44. Cervantes-Chávez JA, Ortiz-Castellanos L, Tejeda-Sartorius M, Gold S, Ruiz-Herrera J. Functional analysis of the pH responsive pathway Pal/Rim in the phytopathogenic basidiomycete Ustilago maydis. Fungal Genet Biol 2010;47:446-57.
45. Aréchiga-Carvajal ET, Ruiz-Herrera J. The RIM101/pacC homologue from the basidiomycete Ustilago maydis is functional in multiple pH-sensitive phenomena. Eukaryot Cell 2005;4:999-1008.
46. Kullas AL, Martin SJ, Davis D. Adaptation to environmental pH: integrating the Rim101 and calcineurin signal transduction pathways. Mol Microbiol 2007;66:858-71.
47. Ariño J. Integrative responses to high pH stress in S. cerevisiae. OMICS 2010;14:517-23.
48. Wang H, Liang Y, Zhang B, Zheng W, Xing L, Li M. Alkaline stress triggers an immediate calcium fluctuation in Candida albicans mediated by Rim101p and Crz1p transcription factors. FEMS Yeast Res 2011;11:430-9.
49. Casado C, González A, Platara M, Ruiz A, Ariño J. The role of the protein kinase A pathway in the response to alkaline pH stress in yeast. Biochem J 2011;438:523-33.
50. 2 sensing in fungi and beyond. Curr Opin Microbiol 2006;9:572-8.
51. 2 through the carbonic anhydrase Can2 and the adenylyl cyclase Cac1. Eukaryot Cell 2006;5:103-11.
52. Zacchi LF, Gomez-Raja J, Davis DA. Mds3 regulates morphogenesis in Candida albicans through the TOR pathway. Mol Cell Biol 2010;30:3695-710.
53. Vylkova S, Carman AJ, Danhof HA, Collette JR, Zhou H, Lorenz MC. The fungal pathogen Candida albicans autoinduces hyphal morphogenesis by raising extracellular pH. MBio 2011;2:e00055-11.