The impact of protein glycosylation on Flo11-dependent adherence in Saccharomyces cerevisiae

FEMS Yeast Research

Volumn 12, Issue 7, 2012, Pages 809-818

  Meem, Mahbuba H ^a   Cullen, Paul J ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

Biofilm; Flocculation; Glycosylation; Invasive growth; Mat; Pseudohyphal growth

Indexed keywords

CELL ADHESION MOLECULE; MUCIN 1; PROTEIN FLO11; UNCLASSIFIED DRUG;

ARTICLE; BIOFILM; CELL ADHESION; CELL STRESS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HALF LIFE TIME; NONHUMAN; PROTEIN BINDING; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; WILD TYPE;

CELL ADHESION; GLYCOSYLATION; MEMBRANE GLYCOPROTEINS; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 84867646877     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/j.1567-1364.2012.00832.x     Document Type: Article

References (62)

1. Bai C, Xu XL, Chan FY, Lee RT & Wang Y (2006) MNN5 encodes an iron-regulated alpha-1, 2-mannosyltransferase important for protein glycosylation, cell wall integrity, morphogenesis, and virulence in Candida albicans. Eukaryot Cell 5: 238-247.
2. Ballou L, Alvarado E, Tsai PK, Dell A & Ballou CE (1989) Protein glycosylation defects in the Saccharomyces cerevisiae mnn7 mutant class. Support for the stop signal proposed for regulation of outer chain elongation. J Biol Chem 264: 11857-11864.
3. Belle A, Tanay A, Bitincka L, Shamir R & O'Shea EK (2006) Quantification of protein half-lives in the budding yeast proteome. P Natl Acad Sci USA 103: 13004-13009.
4. Bruckner S & Mosch HU (2011) Choosing the right lifestyle: adhesion and development in Saccharomyces cerevisiae. FEMS Microbiol Rev 36: 25-58.
5. Bumgarner SL, Dowell RD, Grisafi P, Gifford DK & Fink GR (2009) Toggle involving cis-interfering noncoding RNAs controls variegated gene expression in yeast. P Natl Acad Sci USA 106: 18321-18326.
6. Buurman ET, Westwater C, Hube B, Brown AJ, Odds FC & Gow NA (1998) Molecular analysis of CaMnt1p, a mannosyl transferase important for adhesion and virulence of Candida albicans. P Natl Acad Sci USA 95: 7670-7675.
7. Chavel CA, Dionne HM, Birkaya B, Joshi J & Cullen PJ (2010) Multiple signals converge on a differentiation MAPK pathway. PLoS Genet 6: e1000883.
8. Cullen PJ, Schultz J, Horecka J, Stevenson BJ, Jigami Y & Sprague GF Jr (2000) Defects in protein glycosylation cause SHO1-dependent activation of a STE12 signaling pathway in yeast. Genetics 155: 1005-1018.
9. Cullen PJ, Sabbagh W Jr, Graham E, Irick MM, van Olden EK, Neal C, Delrow J, Olden J, Bardwell L & Sprague GF Jr (2004) A signaling mucin at the head of the Cdc42- and MAPK-dependent filamentous growth pathway in yeast. Genes Dev 18: 1695-1708.
10. Douglas LJ (2003) Candida biofilms and their role in infection. Trends Microbiol 11: 30-36.
11. Douglas LM, Li L, Yang Y & Dranginis AM (2007) Expression and characterization of the flocculin Flo11/Muc1, a Saccharomyces cerevisiae mannoprotein with homotypic properties of adhesion. Eukaryot Cell 6: 2214-2221.
12. Fidalgo M, Barrales RR, Ibeas JI & Jimenez J (2006) Adaptive evolution by mutations in the FLO11 gene. P Natl Acad Sci USA 103: 11228-11233.
13. Finkel JS & Mitchell AP (2011) Genetic control of Candida albicans biofilm development. Nat Rev Microbiol 9: 109-118.
14. Fu Y, Ibrahim AS, Sheppard DC, Chen YC, French SW, Cutler JE, Filler SG & Edwards JE Jr. (2002) Candida albicans Als1p: an adhesin that is a downstream effector of the EFG1 filamentation pathway. Mol Microbiol 44: 61-72.
15. Gaur NK & Klotz SA (1997) Expression, cloning, and characterization of a Candida albicans gene, ALA1, that confers adherence properties upon Saccharomyces cerevisiae for extracellular matrix proteins. Infect Immun 65: 5289-5294.
16. Goldstein AL & McCusker JH (1999) Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541-1553.
17. Gow NA, Netea MG, Munro CA et al. (2007) Immune recognition of Candida albicans beta-glucan by dectin-1. J Infect Dis 196: 1565-1571.
18. Guo B, Styles CA, Feng Q & Fink GR (2000) A Saccharomyces gene family involved in invasive growth, cell-cell adhesion, and mating. P Natl Acad Sci USA 97: 12158-12163.
19. Halme A, Bumgarner S, Styles C & Fink GR (2004) Genetic and epigenetic regulation of the FLO gene family generates cell-surface variation in yeast. Cell 116: 405-415.
20. Hernandez LM, Ballou L, Alvarado E, Tsai PK & Ballou CE (1989) Structure of the phosphorylated N-linked oligosaccharides from the mnn9 and mnn10 mutants of Saccharomyces cerevisiae. J Biol Chem 264: 13648-13659.
21. Immervoll T, Gentzsch M & Tanner W (1995) PMT3 and PMT4, two new members of the protein-O-mannosyltransferase gene family of Saccharomyces cerevisiae. Yeast 11: 1345-1351.
22. Jungmann J & Munro S (1998) Multi-protein complexes in the cis Golgi of Saccharomyces cerevisiae with alpha-1, 6-mannosyltransferase activity. EMBO J 17: 423-434.
23. Karunanithi S, Vadaie N, Chavel CA, Birkaya B, Joshi J, Grell L & Cullen PJ (2010) Shedding of the mucin-like flocculin Flo11p reveals a new aspect of fungal adhesion regulation. Curr Biol 20: 1389-1395.
24. Krysan DJ, Ting EL, Abeijon C, Kroos L & Fuller RS (2005) Yapsins are a family of aspartyl proteases required for cell wall integrity in Saccharomyces cerevisiae. Eukaryot Cell 4: 1364-1374.
25. Lambrechts MG, Bauer FF, Marmur J & Pretorius IS (1996) Muc1, a mucin-like protein that is regulated by Mss10, is critical for pseudohyphal differentiation in yeast. P Natl Acad Sci USA 93: 8419-8424.
26. Leach MD & Brown AJ (2011) Post-translational modifications of proteins in the pathobiology of medically relevant fungi. Eukaryot Cell 11: 98-108.
27. Lehle L, Strahl S & Tanner W (2006) Protein glycosylation, conserved from yeast to man: a model organism helps elucidate congenital human diseases. Angew Chem Int Ed Engl 45: 6802-6818.
28. Li F, Svarovsky MJ, Karlsson AJ, Wagner JP, Marchillo K, Oshel P, Andes D & Palecek SP (2007) Eap1p, an adhesin that mediates Candida albicans biofilm formation in vitro and in vivo. Eukaryot Cell 6: 931-939.
29. Lo WS & Dranginis AM (1996) FLO11, a yeast gene related to the STA genes, encodes a novel cell surface flocculin. J Bacteriol 178: 7144-7151.
30. Lo WS & Dranginis AM (1998) The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae. Mol Biol Cell 9: 161-171.
31. Lo HJ, Kohler JR, DiDomenico B, Loebenberg D, Cacciapuoti A & Fink GR (1997) Nonfilamentous C. albicans mutants are avirulent. Cell 90: 939-949.
32. Lommel M & Strahl S (2009) Protein O-mannosylation: conserved from bacteria to humans. Glycobiology 19: 816-828.
33. Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P & Pringle JR (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
34. McKenzie CG, Koser U, Lewis LE, Bain JM, Mora-Montes HM, Barker RN, Gow NA & Erwig LP (2010) Contribution of Candida albicans cell wall components to recognition by and escape from murine macrophages. Infect Immun 78: 1650-1658.
35. Mukherjee PK, Zhou G, Munyon R & Ghannoum MA (2005) Candida biofilm: a well-designed protected environment. Med Mycol 43: 191-208.
36. Munro CA, Bates S, Buurman ET et al. (2005) Mnt1p and Mnt2p of Candida albicans are partially redundant alpha-1, 2-mannosyltransferases that participate in O-linked mannosylation and are required for adhesion and virulence. J Biol Chem 280: 1051-1060.
37. Netea MG, Gow NA, Munro CA et al. (2006) Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J Clin Invest 116: 1642-1650.
38. Ng DT, Spear ED & Walter P (2000) The unfolded protein response regulates multiple aspects of secretory and membrane protein biogenesis and endoplasmic reticulum quality control. J Cell Biol 150: 77-88.
39. Nobile CJ & Mitchell AP (2006) Genetics and genomics of Candida albicans biofilm formation. Cell Microbiol 8: 1382-1391.
40. Octavio LM, Gedeon K & Maheshri N (2009) Epigenetic and conventional regulation is distributed among activators of FLO11 allowing tuning of population-level heterogeneity in its expression. PLoS Genet 5: e1000673.
41. Oriol R, Martinez-Duncker I, Chantret I, Mollicone R & Codogno P (2002) Common origin and evolution of glycosyltransferases using Dol-P-monosaccharides as donor substrate. Mol Biol Evol 19: 1451-1463.
42. Otoo HN, Lee KG, Qiu W & Lipke PN (2008) Candida albicans Als adhesins have conserved amyloid-forming sequences. Eukaryot Cell 7: 776-782.
43. Pitoniak A, Birkaya B, Dionne HM, Vadaie N & Cullen PJ (2009) The signaling mucins Msb2 and Hkr1 differentially regulate the filamentation mitogen-activated protein kinase pathway and contribute to a multimodal response. Mol Biol Cell 20: 3101-3114.
44. Prill SK, Klinkert B, Timpel C, Gale CA, Schroppel K & Ernst JF (2005) PMT family of Candida albicans: five protein mannosyltransferase isoforms affect growth, morphogenesis and antifungal resistance. Mol Microbiol 55: 546-560.
45. Ramsook CB, Tan C, Garcia MC et al. (2010) Yeast cell adhesion molecules have functional amyloid-forming sequences. Eukaryot Cell 9: 393-404.
46. Reynolds TB & Fink GR (2001) Bakers' yeast, a model for fungal biofilm formation. Science 291: 878-881.
47. Roberts RL & Fink GR (1994) Elements of a single MAP kinase cascade in Saccharomyces cerevisiae mediate two developmental programs in the same cell type: mating and invasive growth. Genes Dev 8: 2974-2985.
48. Rouabhia M, Schaller M, Corbucci C, Vecchiarelli A, Prill SK, Giasson L & Ernst JF (2005) Virulence of the fungal pathogen Candida albicans requires the five isoforms of protein mannosyltransferases. Infect Immun 73: 4571-4580.
49. Runge KW & Robbins PW (1986) A new yeast mutation in the glucosylation steps of the asparagine-linked glycosylation pathway. Formation of a novel asparagine-linked oligosaccharide containing two glucose residues. J Biol Chem 261: 15582-15590.
50. Rupp S, Summers E, Lo HJ, Madhani H & Fink G (1999) MAP kinase and cAMP filamentation signaling pathways converge on the unusually large promoter of the yeast FLO11 gene. EMBO J 18: 1257-1269.
51. Sarode N, Miracle B, Peng X, Ryan O & Reynolds TB (2011) Vacuolar protein sorting genes regulate mat formation in Saccharomyces cerevisiae by Flo11p-dependent and -independent mechanisms. Eukaryot Cell 10: 1516-1526.
52. Smith DJ, Proudfoot A, Friedli L, Klig LS, Paravicini G & Payton MA (1992) PMI40, an intron-containing gene required for early steps in yeast mannosylation. Mol Cell Biol 12: 2924-2930.
53. Sprague GF Jr & Herskowitz I (1981) Control of yeast cell type by the mating type locus. I. Identification and control of expression of the a-specific gene BAR1. J Mol Biol 153: 305-321.
54. Staab JF, Bradway SD, Fidel PL & Sundstrom P (1999) Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 283: 1535-1538.
55. Tatebayashi K, Tanaka K, Yang HY, Yamamoto K, Matsushita Y, Tomida T, Imai M & Saito H (2007) Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. EMBO J 26: 3521-3533.
56. Timpel C, Strahl-Bolsinger S, Ziegelbauer K & Ernst JF (1998) Multiple functions of Pmt1p-mediated protein O-mannosylation in the fungal pathogen Candida albicans. J Biol Chem 273: 20837-20846.
57. Timpel C, Zink S, Strahl-Bolsinger S, Schroppel K & Ernst J (2000) Morphogenesis, adhesive properties, and antifungal resistance depend on the Pmt6 protein mannosyltransferase in the fungal pathogen Candida albicans. J Bacteriol 182: 3063-3071.
58. Vadaie N, Dionne H, Akajagbor DS, Nickerson SR, Krysan DJ & Cullen PJ (2008) Cleavage of the signaling mucin Msb2 by the aspartyl protease Yps1 is required for MAPK activation in yeast. J Cell Biol 181: 1073-1081.
59. Verstrepen KJ, Jansen A, Lewitter F & Fink GR (2005) Intragenic tandem repeats generate functional variability. Nat Genet 37: 986-990.
60. Yang HY, Tatebayashi K, Yamamoto K & Saito H (2009) Glycosylation defects activate filamentous growth Kss1 MAPK and inhibit osmoregulatory Hog1 MAPK. EMBO J 28: 1380-1391.
61. Yen HC, Xu Q, Chou DM, Zhao Z & Elledge SJ (2008) Global protein stability profiling in mammalian cells. Science 322: 918-923.
62. Zhao X, Oh SH, Yeater KM & Hoyer LL (2005) Analysis of the Candida albicans Als2p and Als4p adhesins suggests the potential for compensatory function within the Als family. Microbiology 151: 1619-1630.