Structural and biochemical characterization of the N-terminal domain of flocculin Lg-Flo1p from Saccharomyces pastorianus reveals a unique specificity for phosphorylated mannose

FEBS Journal

Volumn 280, Issue 4, 2013, Pages 1073-1083

  Sim, Lyann ^a   Groes, Magnus ^a   Olesen, Kjeld ^a,b   Henriksen, Anette ^a,b  

^a CARLSBERG LABORATORY   (Denmark)

^b NOVO NORDISK A S   (Denmark)

Author keywords

crystal structure; lectin; NewFlo; phospho mannans; yeast flocculation

Indexed keywords

ADHESIN; ALPHA(1,2)MANNOBIOSE; ALPHA(1,3)DIMANNOSE; ALPHA(1,6)DIMANNOSE; CALCIUM ION; DISACCHARIDE; EPITHELIAL ADHESIN 1; FLOCCULIN 1; FLOCCULIN 5; GLUCOSE 1 PHOSPHATE; LECTIN; MANNOSE; MANNOSE 1 PHOSPHATE; MONOSACCHARIDE; POLYSACCHARIDE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; BINDING AFFINITY; BINDING SITE; COMPARATIVE STUDY; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISSOCIATION CONSTANT; ENZYME SPECIFICITY; FLOCCULATION; FLUORESCENCE SPECTROSCOPY; GENE; IONIC STRENGTH; LG FLO1P GENE; MOLECULAR DYNAMICS; NONHUMAN; PH; PHENOTYPIC VARIATION; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN DOMAIN; SACCHAROMYCES CARLSBERGENSIS; SEQUENCE ALIGNMENT; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; BINDING SITES; CALCIUM; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; FLOCCULATION; FUNGAL PROTEINS; GLUCOSEPHOSPHATES; HYDROGEN-ION CONCENTRATION; MANNOSE-BINDING LECTINS; MANNOSEPHOSPHATES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OSMOLAR CONCENTRATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES; STRUCTURAL HOMOLOGY, PROTEIN; SUBSTRATE SPECIFICITY; SURFACE PROPERTIES;

SACCHAROMYCES PASTORIANUS;

EID: 84874115834     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12102     Document Type: Article

References (45)

1. Miki BL, Poon NH, James AP, &, Seligy VL, (1982) Possible mechanism for flocculation interactions governed by gene FLO1 in Saccharomyces cerevisiae. J Bacteriol 150, 878-889.
2. Miki BL, Poon NH, &, Seligy VL, (1982) Repression and induction of flocculation interactions in Saccharomyces cerevisiae. J Bacteriol 150, 890-899.
3. Bony M, Thines-Sempoux D, Barre P, &, Blondin B, (1997) Localization and cell surface anchoring of the Saccharomyces cerevisiae flocculation protein Flo1p. J Bacteriol 179, 4929-4936.
4. Javadekar VS, Sivaraman H, Sainkar SR, &, Khan MI, (2000) A mannose-binding protein from the cell surface of flocculent Saccharomyces cerevisiae (NCIM 3528): its role in flocculation. Yeast 16, 99-110.
5. Verstrepen KJ, Bauer FF, Michiels C, Winderickx G, Derdelinckx G, Pretorius IS, &, Delvaux FR, (2001) Late fermentation expression of FLO1 in Saccharomyces cerevisiae. J Am Soc Brew Chem 59, 69-76.
6. Brückner S, &, Mösch H-U, (2012) Choosing the right lifestyle: adhesion and development in Saccharomyces cerevisiae. FEMS Microbiol Rev 36, 25-58.
7. Stratford M, (1992) Yeast flocculation: a new perspective. Adv Microb Physiol 33, 2-71.
8. Sulak O, Lameignère E, Wimmerova M, &, Imberty A, (2009) Specificity and affinity studies in lectin/carbohydrate interactions. Carbohydr Chem 35, 1-16.
9. Stratford M, &, Assinder S, (1991) Yeast flocculation: Flo1 and NewFlo phenotypes and receptor structure. Yeast 7, 559-574.
10. Van Mulders SE, Ghequire M, Daenen L, Verbelen PJ, Verstrepen KJ, &, Delvaux FR, (2010) Flocculation gene variability in industrial brewer's yeast strains. Appl Microbiol Biotechnol 88, 1321-1331.
11. Kobayashi O, Hayashi N, Kuroki R, &, Sone H, (1998) Region of FLO1 proteins responsible for sugar recognition. J Bacteriol 180, 6503-6510.
12. Bauer FF, Govender P, &, Bester MC, (2010) Yeast flocculation and its biotechnological relevance. Appl Microbiol Biotechnol 88, 31-39.
13. Vidgren V, &, Londesborough J, (2012) 125th anniversary review: yeast flocculation and sedimentation in brewing. J Inst Brew 117, 475-487.
14. Yamashita I, &, Fukui S, (1984) Genetic background of glucoamylase production in the yeast Saccharomyces. Agric Biol Chem 48, 137-141.
15. Teunissen AW, &, Steensma HY, (1995) Review: the dominant flocculation genes of Saccharomyces cerevisiae constitute a new subtelomeric gene family. Yeast 11, 1001-1013.
16. Kobayashi O, Yoshimoto H, &, Sone H, (1999) Analysis of the genes activated by the FLO8 gene in Saccharomyces cerevisiae. Curr Genet 36, 256-261.
17. Kobayashi O, Suda H, Ohtani T, &, Sone H, (1996) Molecular cloning and analysis of the dominant flocculation gene FLO8 from Saccharomyces cerevisiae. Mol Gen Genet 251, 707-715.
18. Amory DE, &, Rouxhet PG, (1988) Surface properties of Saccharomyces cerevisiae and Saccharomyces carlbergensis: chemical composition, electrostatic charge and hydrophobicity. Biochim Biophys Acta 938, 61-70.
19. Stratford M, (1996) Induction of flocculation in brewing yeasts by change in pH value. FEMS Microbiol Lett 136, 13-18.
20. Goossens KVY, Stassen C, Stals I, Donohue DS, Devreese B, De Greve H, &, Willaert RG, (2011) The N-terminal domain of the Flo1 flocculation protein from Saccharomyces cerevisiae binds specifically to mannose carbohydrates. Eukaryot Cell 10, 110-117.
21. Veelders M, Brückner S, Ott D, Unverzagt C, Mösch H-U, &, Essen L-O, (2010) Structural basis of flocculin-mediated social behavior in yeast. Proc Natl Acad Sci USA 107, 22511-22516.
22. Ballou C, (1976) Structure and biosynthesis of the mannan component of yeast cell envelope. Adv Microb Physiol 14, 93-158.
23. Jigami Y, &, Odani T, (1999) Mannosylphosphate transfer to yeast mannan. Biochim Biophys Acta 1426, 335-345.
24. Masy CL, Henquinet A, &, Mestdagh MM, (1992) Flocculation of Saccharomyces cerevisiae: inhibition by sugars. Can J Microbiol 38, 1298-1306.
25. Stratford M, (1992) Yeast flocculation: receptor definition by mnn mutants and concanavalin A. Yeast 8, 635-645.
26. Thieme TR, &, Ballou CE, (1971) Nature of the phosphodiester linkage of the phosphomannan from the yeast Kloeckera brevis. Biochemistry 10, 4121-4129.
27. 2+-binding proteins. Protein engineering and biophysical studies of calbindin D9k. Biochemistry 26, 6723-6735.
28. Ielasi FS, Decanniere K, &, Willaert RG, (2012) The epithelial adhesin 1 (Epa1p) from the human-pathogenic yeast Candida glabrata: structural and functional study of the carbohydrate-binding domain. Acta Crystallogr D Biol Crystallogr 68, 210-217.
29. Maestre-Reyna M, Diderrich R, Veelders MS, Eulenburg G, Kalugin V, Brückner S, Keller P, Rupp S, Mösch H-U, &, Essen L-O, (2012) Structural basis for promiscuity and specificity during Candida glabrata invasion of host epithelia. Proc Natl Acad Sci USA 109, 16864-16869.
30. Steward GG, &, Russell I, (1981) Yeast flocculation. In Brewing Science (, Pollock JRA, ed.), pp. 61-92, 2, Academic Press, London.
31. Hernandez LM, Ballou L, Alvarado E, Tsai P-K, &, 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.
32. Groes M, Teilum K, Olesen K, Poulsen FM, &, Henriksen A, (2002) Purification, crystallization and preliminary X-ray diffraction analysis of the carbohydrate-binding domain of flocculin, a cell-adhesion molecule from Saccharomyces carlsbergensis. Acta Crystallogr D Biol Crystallogr 58, 2135-2137.
33. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, Read RJ, Sacchettini JC, Sauter NK, &, Terwilliger TC, (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58, 1948-1954.
34. Murshudov GN, Vagin AA, &, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53, 240-255.
35. Emsley P, Lohkamp B, Scott WG, &, Cowtan K, (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66, 486-501.
36. Langer G, Cohen SX, Lamzin VS, &, Perrakis A, (2008) Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat Protoc 3, 1171-1179.
37. Dolinsky TJ, Nielsen JE, McCammon JA, &, Baker NA, (2004) PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res 32, W665-W667.
38. Baker NA, Sept D, Joseph S, Holst MJ, &, McCammon JA, (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA 98, 10037-10041.
39. DeLano WL, (2002) The PyMOL molecular graphics system. http:/www.pymol.org.
40. Fabricius J, Engelsen SB, &, Rasmussen K, (1997) The consistent force field. 5. PEF95SAC: optimized potential energy function for alcohols and carbohydrates. J Carbohydr Chem 16, 751-772.
41. Holmberg S, &, Kielland-Brandt M, (1978) A mutant of Saccharomyces cerevisiae temperature sensitive for flocculation. Influence of oxygen and respiratory deficiency on flocculence. Carlsberg Res Commun 43, 37-47.
42. Helm E, Nùhr H, &, Thorne RSW, (1953) Measurement of yeast flocculation and its significance in brewing. Wallerstein Lab Commun 16, 315-325.
43. Lovell SC, Davis IW, Arendall WB, de Bakker PIW, Word JM, Prisant MG, Richardson JS, &, Richardson DC, (2003) Structure validation by C-alpha geometry: phi, psi and C-beta deviation. Proteins 50, 437-450.
44. Gouet P, Courcelle E, Stuart DI, &, Métoz F, (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305-308.
45. Kabsch W, &, Sander C, (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577-2637.