The ADP-glucose pyrophosphorylase from Streptococcus mutans provides evidence for the regulation of polysaccharide biosynthesis in Firmicutes

Molecular Microbiology

Volumn 90, Issue 5, 2013, Pages 1011-1027

  Asención Diez, Matías D ^a,b   Demonte, Ana M ^a   Guerrero, Sergio A ^a   Ballicora, Miguel A ^b   Iglesias, Alberto A ^a  

^a Universidad Nacional del Litoral   (Argentina)

^b LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FRUCTOSE 1,6 BISPHOSPHATE; GLUCOSE 1 PHOSPHATE ADENYLYLTRANSFERASE; INORGANIC SALT; PHOSPHOENOLPYRUVATE; POLYSACCHARIDE;

ALLOSTERISM; ARTICLE; BACTERIAL GENE; CARBOHYDRATE METABOLISM; CARBOHYDRATE SYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME KINETICS; ENZYME REGULATION; FIRMICUTES; GENE EXPRESSION; GLGC GENE; GLGD GENE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; STREPTOCOCCUS MUTANS;

BACTERIA (MICROORGANISMS); FIRMICUTES; STREPTOCOCCUS MUTANS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CLONING, MOLECULAR; CONSERVED SEQUENCE; FRUCTOSEPHOSPHATES; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GLUCOSE-1-PHOSPHATE ADENYLYLTRANSFERASE; MODELS, MOLECULAR; PHOSPHOENOLPYRUVATE; PHYLOGENY; POLYSACCHARIDES, BACTERIAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; SALTS; STREPTOCOCCUS MUTANS;

EID: 84888346250     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12413     Document Type: Article

References (78)

1. Abbe, K., and Yamada, T. (1982) Purification and properties of pyruvate kinase from Streptococcus mutans. J Bacteriol 149: 299-305.
2. Abranches, J., Chen, Y.Y., and Burne, R.A. (2004) Galactose metabolism by Streptococcus mutans. Appl Environ Microbiol 70: 6047-6052.
3. Ajdic, D., McShan, W.M., McLaughlin, R.E., Savic, G., Chang, J., Carson, M.B., etal. (2002) Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc Natl Acad Sci USA 99: 14434-14439.
4. Asencion Diez, M.D., Demonte, A., Giacomelli, J., Garay, S., Rodrigues, D., Hofmann, B., etal. (2010) Functional characterization of GDP-mannose pyrophosphorylase from Leptospira interrogans serovar Copenhageni. Arch Microbiol 192: 103-114.
5. Asencion Diez, M.D., Peiru, S., Demonte, A.M., Gramajo, H., and Iglesias, A.A. (2012) Characterization of recombinant UDP- and ADP-glucose pyrophosphorylases and glycogen synthase to elucidate glucose-1-phosphate partitioning into oligo- and polysaccharides in Streptomyces coelicolor. J Bacteriol 194: 1485-1493.
6. Ballicora, M.A., Iglesias, A.A., and Preiss, J. (2003) ADP-glucose pyrophosphorylase, a regulatory enzyme for bacterial glycogen synthesis. Microbiol Mol Biol Rev 67: 213-225.
7. Ballicora, M.A., Iglesias, A.A., and Preiss, J. (2004) ADP-glucose pyrophosphorylase: a regulatory enzyme for plant starch synthesis. Photosynth Res 79: 1-24.
8. Ballicora, M.A., Erben, E.D., Yazaki, T., Bertolo, A.L., Demonte, A.M., Schmidt, J.R., etal. (2007) Identification of regions critically affecting kinetics and allosteric regulation of the Escherichia coli ADP-glucose pyrophosphorylase by modeling and pentapeptide-scanning mutagenesis. J Bacteriol 189: 5325-5333.
9. Bejar, C.M., Ballicora, M.A., Gomez-Casati, D.F., Iglesias, A.A., and Preiss, J. (2004) The ADP-glucose pyrophosphorylase from Escherichia coli comprises two tightly bound distinct domains. FEBS Lett 573: 99-104.
10. Bejar, C.M., Jin, X., Ballicora, M.A., and Preiss, J. (2006) Molecular architecture of the glucose 1-phosphate site in ADP-glucose pyrophosphorylases. J Biol Chem 281: 40473-40484.
11. Birkhed, D., and Tanzer, J.M. (1979) Glycogen synthesis pathway in Streptococcus mutans strain NCTC 10449S and its glycogen synthesis-defective mutant 805. Arch Oral Biol 24: 67-73.
12. Bosco, M.B., Machtey, M., Iglesias, A.A., and Aleanzi, M. (2009) UDPglucose pyrophosphorylase from Xanthomonas spp. Characterization of the enzyme kinetics, structure and inactivation related to oligomeric dissociation. Biochimie 91: 204-213.
13. Boyd, D.A., Cvitkovitch, D.G., and Hamilton, I.R. (1995) Sequence, expression, and function of the gene for the nonphosphorylating, NADP-dependent glyceraldehyde-3-phosphate dehydrogenase of Streptococcus mutans. J Bacteriol 177: 2622-2627.
14. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
15. Brown, A.T., and Wittenberger, C.L. (1971) The occurrence of multiple glyceraldehyde-3-phosphate dehydrogenases in cariogenic streptococci. Biochem Biophys Res Commun 43: 217-224.
16. Brown, A.T., and Wittenberger, C.L. (1972) Fructose-1, 6-diphosphate-dependent lactate dehydrogenase from a cariogenic streptococcus: purification and regulatory properties. J Bacteriol 110: 604-615.
17. Busuioc, M., Mackiewicz, K., Buttaro, B.A., and Piggot, P.J. (2009) Role of intracellular polysaccharide in persistence of Streptococcus mutans. J Bacteriol 191: 7315-7322.
18. Crevillen, P., Ballicora, M.A., Merida, A., Preiss, J., and Romero, J.M. (2003) The different large subunit isoforms of Arabidopsis thaliana ADP-glucose pyrophosphorylase confer distinct kinetic and regulatory properties to the heterotetrameric enzyme. J Biol Chem 278: 28508-28515.
19. Cupp-Vickery, J.R., Igarashi, R.Y., Perez, M., Poland, M., and Meyer, C.R. (2008) Structural analysis of ADP-glucose pyrophosphorylase from the bacterium Agrobacterium tumefaciens. Biochemistry 47: 4439-4451.
20. Cvitkovitch, D.G., Gutierrez, J.A., and Bleiweis, A.S. (1997) Role of the citrate pathway in glutamate biosynthesis by Streptococcus mutans. J Bacteriol 179: 650-655.
21. Figueroa, C.M., Esper, M.C., Bertolo, A., Demonte, A.M., Aleanzi, M., Iglesias, A.A., and Ballicora, M.A. (2011) Understanding the allosteric trigger for the fructose-1, 6-bisphosphate regulation of the ADP-glucose pyrophosphorylase from Escherichia coli. Biochimie 93: 1816-1823.
22. Freedman, M.L., and Coykendall, A.L. (1975) Variation in internal polysaccharide synthesis among Streptococcus mutans strains. Infect Immun 12: 475-479.
23. Frueauf, J.B., Ballicora, M.A., and Preiss, J. (2001) Aspartate residue 142 is important for catalysis by ADP-glucose pyrophosphorylase from Escherichia coli. J Biol Chem 276: 46319-46325.
24. Frueauf, J.B., Ballicora, M.A., and Preiss, J. (2003) ADP-glucose pyrophosphorylase from potato tuber: site-directed mutagenesis of homologous aspartic acid residues in the small and large subunits. Plant J 33: 503-511.
25. Fu, Y., Ballicora, M.A., and Preiss, J. (1998) Mutagenesis of the glucose-1-phosphate-binding site of potato tuber ADP-glucose pyrophosphorylase. Plant Physiol 117: 989-996.
26. Fusari, C., Demonte, A.M., Figueroa, C.M., Aleanzi, M., and Iglesias, A.A. (2006) A colorimetric method for the assay of ADP-glucose pyrophosphorylase. Anal Biochem 352: 145-147.
27. Gibbons, R.J. (1964) Metabolism of intracellular polysaccharide by Streptococcus mitis and its relation to inducible enzyme formation. J Bacteriol 87: 1512-1520.
28. Gibbons, R.J., and Kapsimalis, B. (1963) Synthesis of intracellular iodophilic polysaccharide by Streptococcus mitis. Arch Oral Biol 8: 319-329.
29. Gouy, M., Guindon, S., and Gascuel, O. (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27: 221-224.
30. Guindon, S., and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
31. Hamilton, I.R. (1977) Effects of fluoride on enzymatic regulation of bacterial carbohydrate metabolism. Caries Res 11 (Suppl. 1): 262-291.
32. Harris, G.S., Michalek, S.M., and Curtiss, R., 3rd. (1992) Cloning of a locus involved in Streptococcus mutans intracellular polysaccharide accumulation and virulence testing of an intracellular polysaccharide-deficient mutant. Infect Immun 60: 3175-3185.
33. Hill, M.A., Kaufmann, K., Otero, J., and Preiss, J. (1991) Biosynthesis of bacterial glycogen. Mutagenesis of a catalytic site residue of ADP-glucose pyrophosphorylase from Escherichia coli. J Biol Chem 266: 12455-12460.
34. Hillman, J.D. (1978) Lactate dehydrogenase mutants of Streptococcus mutans: isolation and preliminary characterization. Infect Immun 21: 206-212.
35. Hillman, J.D., Chen, A., Duncan, M., and Lee, S.W. (1994) Evidence that L-(+)-lactate dehydrogenase deficiency is lethal in Streptococcus mutans. Infect Immun 62: 60-64.
36. van Houte, J., and Saxton, C.A. (1971) Cell wall thickening and intracellular polysaccharide in microorganisms of the dental plaque. Caries Res 5: 30-43.
37. van Houte, J., Winkler, K.C., and Jansen, H.M. (1969) Iodophilic polysaccharide synthesis, acid production and growth in oral streptococci. Arch Oral Biol 14: 45-61.
38. van Houte, J., de Moor, C.E., and Jansen, H.M. (1970) Synthesis of iodophilic polysaccharide by human oral streptococci. Arch Oral Biol 15: 263-266.
39. Huis in 't Veld, J.H., and Backer Dirks, O. (1978) Intracellular polysaccharide metabolism in Streptococcus mutans. Caries Res 12: 243-249.
40. Iglesias, A.A., Barry, G.F., Meyer, C., Bloksberg, L., Nakata, P.A., Greene, T., etal. (1993) Expression of the potato tuber ADP-glucose pyrophosphorylase in Escherichia coli. J Biol Chem 268: 1081-1086.
41. Jeanmougin, F., Thompson, J.D., Gouy, M., Higgins, D.G., and Gibson, T.J. (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23: 403-405.
42. Jin, X., Ballicora, M.A., Preiss, J., and Geiger, J.H. (2005) Crystal structure of potato tuber ADP-glucose pyrophosphorylase. EMBO J 24: 694-704.
43. Kanapka, J.A., Khandelwal, R.L., and Hamilton, I.R. (1971) Fluoride inhibition of glucose-6-P formation in Streptococcus salivarius: relation to glycogen synthesis and degradation. Arch Biochem Biophys 144: 596-602.
44. Keevil, C.W., Marsh, P.D., and Ellwood, D.C. (1984) Regulation of glucose metabolism in oral streptococci through independent pathways of glucose 6-phosphate and glucose 1-phosphate formation. J Bacteriol 157: 560-567.
45. Kiel, J.A., Boels, J.M., Beldman, G., and Venema, G. (1994) Glycogen in Bacillus subtilis: molecular characterization of an operon encoding enzymes involved in glycogen biosynthesis and degradation. Mol Microbiol 11: 203-218.
46. Kim, E.-J., Ryu, S.-I., Bae, H.-A., Huong, N.T., and Lee, S.-B. (2008) Biochemical characterization of a glycogen branching enzyme from Streptococcus mutans: enzymatic modification of starch. Food Chem 110: 979-984.
47. Kuhn, M.L., Figueroa, C.M., Aleanzi, M., Olsen, K.W., Iglesias, A.A., and Ballicora, M.A. (2010) Bi-national and interdisciplinary course in enzyme engineering. Biochem Mol Biol Educ 38: 370-379.
48. Kumar, A., Tanaka, T., Lee, Y.M., and Preiss, J. (1988) Biosynthesis of bacterial glycogen. Use of site-directed mutagenesis to probe the role of tyrosine 114 in the catalytic mechanism of ADP-glucose synthetase from Escherichia coli. J Biol Chem 263: 14634-14639.
49. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
50. Lee, Y.M., and Preiss, J. (1986) Covalent modification of substrate-binding sites of Escherichia coli ADP-glucose synthetase. Isolation and structural characterization of 8-azido-ADP-glucose-incorporated peptides. J Biol Chem 261: 1058-1064.
51. Lemos, J.A., and Burne, R.A. (2008) A model of efficiency: stress tolerance by Streptococcus mutans. Microbiology 154: 3247-3255.
52. Lemos, J.A., Abranches, J., and Burne, R.A. (2005) Responses of cariogenic streptococci to environmental stresses. Curr Issues Mol Biol 7: 95-107.
53. Leung, P., Lee, Y.M., Greenberg, E., Esch, K., Boylan, S., and Preiss, J. (1986) Cloning and expression of the Escherichia coli glgC gene from a mutant containing an ADPglucose pyrophosphorylase with altered allosteric properties. J Bacteriol 167: 82-88.
54. Luthy, R., Bowie, J.U., and Eisenberg, D. (1992) Assessment of protein models with three-dimensional profiles. Nature 356: 83-85.
55. Machtey, M., Kuhn, M.L., Flasch, D.A., Aleanzi, M., Ballicora, M.A., and Iglesias, A.A. (2012) Insights into glycogen metabolism in chemolithoautotrophic bacteria from distinctive kinetic and regulatory properties of ADP-glucose pyrophosphorylase from Nitrosomonas europaea. J Bacteriol 194: 6056-6065.
56. Ning, B., and Elbein, A.D. (1999) Purification and properties of mycobacterial GDP-mannose pyrophosphorylase. Arch Biochem Biophys 362: 339-345.
57. Notredame, C., Higgins, D.G., and Heringa, J. (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302: 205-217.
58. Preiss, J. (1984) Bacterial glycogen synthesis and its regulation. Annu Rev Microbiol 38: 419-458.
59. Preiss, J. (2009) Glycogen biosynthesis. In Encyclopaedia of Microbiology. Schaechter, M. (ed.). San Diego, CA, USA: Elsevier Inc, pp. 145-158.
60. Sali, A., and Blundell, T.L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234: 779-815.
61. Sambrook, J., and Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, New York, USA: Cold Spring Harbor Laboratory Press.
62. Skinner, A., and Naylor, M.N. (1972) Influence of sugar type on the pattern of acid production by Streptococcus mutans. J Dent Res 51: 1022-1024.
63. de Soet, J.J., Nyvad, B., and Kilian, M. (2000) Strain-related acid production by oral streptococci. Caries Res 34: 486-490.
64. Spatafora, G., Rohrer, K., Barnard, D., and Michalek, S. (1995) A Streptococcus mutans mutant that synthesizes elevated levels of intracellular polysaccharide is hypercariogenic in vivo. Infect Immun 63: 2556-2563.
65. Spatafora, G.A., Sheets, M., June, R., Luyimbazi, D., Howard, K., Hulbert, R., etal. (1999) Regulated expression of the Streptococcus mutans dlt genes correlates with intracellular polysaccharide accumulation. J Bacteriol 181: 2363-2372.
66. Takahashi, N., and Nyvad, B. (2011) The role of bacteria in the caries process: ecological perspectives. J Dent Res 90: 294-303.
67. Takahashi, N., Abbe, K., Takahashi-Abbe, S., and Yamada, T. (1987) Oxygen sensitivity of sugar metabolism and interconversion of pyruvate formate-lyase in intact cells of Streptococcus mutans and Streptococcus sanguis. Infect Immun 55: 652-656.
68. Takahashi, N., Iwami, Y., and Yamada, T. (1991) Metabolism of intracellular polysaccharide in the cells of Streptococcus mutans under strictly anaerobic conditions. Oral Microbiol Immunol 6: 299-304.
69. Takahashi, N., Washio, J., and Mayanagi, G. (2010) Metabolomics of supragingival plaque and oral bacteria. J Dent Res 89: 1383-1388.
70. Takahashi-Abbe, S., Abe, K., and Takahashi, N. (2003) Biochemical and functional properties of a pyruvate formate-lyase (PFL)-activating system in Streptococcus mutans. Oral Microbiol Immunol 18: 293-297.
71. Takata, H., Takaha, T., Okada, S., Takagi, M., and Imanaka, T. (1997) Characterization of a gene cluster for glycogen biosynthesis and a heterotetrameric ADP-glucose pyrophosphorylase from Bacillus stearothermophilus. J Bacteriol 179: 4689-4698.
72. Tanzer, J.M., Freedman, M.L., Fitzgerald, R.J., and Larson, R.H. (1974) Diminished virulence of glucan synthesis-defective mutants of Streptococcus mutans. Infect Immun 10: 197-203.
73. Thompson, J., and Thomas, T.D. (1977) Phosphoenolpyruvate and 2-phosphoglycerate: endogenous energy source(s) for sugar accumulation by starved cells of Streptococcus lactis. J Bacteriol 130: 583-595.
74. Vadeboncoeur, C., and Pelletier, M. (1997) The phosphoenolpyruvate:sugar phosphotransferase system of oral streptococci and its role in the control of sugar metabolism. FEMS Microbiol Rev 19: 187-207.
75. Vaitukaitis, J.L. (1981) Production of antisera with small doses of immunogen: multiple intradermal injections. Methods Enzymol 73: 46-52.
76. Weissborn, A.C., Liu, Q., Rumley, M.K., and Kennedy, E.P. (1994) UTP: alpha-D-glucose-1-phosphate uridylyltransferase of Escherichia coli: isolation and DNA sequence of the galU gene and purification of the enzyme. J Bacteriol 176: 2611-2618.
77. Yamada, T., and Carlsson, J. (1975) Glucose-6-phosphate-dependent pyruvate kinase in Streptococcus mutans. J Bacteriol 124: 562-563.
78. Yep, A., Bejar, C.M., Ballicora, M.A., Dubay, J.R., Iglesias, A.A., and Preiss, J. (2004) An assay for adenosine 5'-diphosphate (ADP)-glucose pyrophosphorylase that measures the synthesis of radioactive ADP-glucose with glycogen synthase. Anal Biochem 324: 52-59.