Sialic acids are structurally diverse nine-carbon ketosugars found mostly in humans and other animals as the terminal units on carbohydrate chains linked to proteins or lipids. The sialic acids function in cell-cell and cell-molecule interactions necessary for organismic development and homeostasis. They not only pose a barrier to microorganisms inhabiting or invading an animal mucosal surface, but also present a source of potential carbon, nitrogen, and cell wall metabolites necessary for bacterial colonization, persistence, growth, and, occasionally, disease. The explosion of microbial genomic sequencing projects reveals remarkable diversity in bacterial sialic acid metabolic potential. How bacteria exploit host sialic acids includes a surprisingly complex array of metabolic and regulatory capabilities that is just now entering a mature research stage. This paper attempts to describe the variety of bacterial sialometabolic systems by focusing on recent advances at the molecular and host-microbe-interaction levels. The hope is that this focus will provide a framework for further research that holds promise for better understanding of the metabolic interplay between bacterial growth and the host environment. An ability to modify or block this interplay has already yielded important new insights into potentially new therapeutic approaches for modifying or blocking bacterial colonization or infection. 1. Introduction At least at some level common experience indicates to almost everyone that life is constrained by competition for limited resources. Formally trained biologists understand this competition as central to evolution, the only fundamental theory in biology. For some microorganisms competitive success in colonizing a mammalian or avian host depends upon specialized metabolism that may support growth in only certain niches. For example, Freter [1] has summarized his own and the work of others by describing the mechanisms of association of bacteria with mucosal surfaces. These mechanisms include “(a) chemotactic attraction of motile bacteria to the surface of the mucus [layer], (b) penetration and trapping within the mucus [layer], (c) adhesion to receptors…, (d) adhesion to epithelial cell surfaces, and (e) multiplication of the mucosa-associated bacteria.” The combined set of traits or phenotypes expressed by a given bacterium defines its potential “virulence factors” or relative colonization success [1, 2]. In the current paper the final stage of the host-microbial interaction is exclusively focused upon multiplication of bacteria at mucosal
References
[1]
R. Freter, “Mechanisms of association of bacteria with mucosal surfaces,” Ciba Foundation Symposium, vol. 80, pp. 36–55, 1981.
[2]
R. Freter, “Control mechanisms of the large-intestinal microflora and its influence on the host,” Acta Gastroenterologica Latinoamericana, vol. 19, no. 4, pp. 197–217, 1989.
[3]
E. R. Vimr, K. A. Kalivoda, E. L. Deszo, and S. M. Steenbergen, “Diversity of microbial sialic acid metabolism,” Microbiology and Molecular Biology Reviews, vol. 68, no. 1, pp. 132–153, 2004.
[4]
J. V. Li and J. R. Marchesi, “Gut microbe-host metabolic interactions in health and disease: exploring host and gut microbiota connections could uncover the mechanisms of various diseases along with targets for drugs with which to treat them,” Microbe, vol. 7, no. 7, pp. 310–318, 2012.
[5]
E. R. Vimr and S. M. Steenbergen, “Targeting microbial sialic acid metabolism for new drug development,” in Protein-Carbohydrate Interactions in Infectious Diseases, C. A. Bewley, Ed., RCS, London, UK, 2006.
[6]
B. S. Drasar and P. A. Barrow, “Intestinal microbiology,” Aspects of Microbiology, vol. 10, 1985.
[7]
P. Lepage, M. C. Leclerc, M. Joossens et al., “A metagenomic insight into our gut’s microbiome,” Gut, 2013. In press.
[8]
F. O. Gl？ckner, M. Kube, M. Bauer et al., “Complete genome sequence of the marine planctomycete Pirellula sp. strain 1,” Proceedings of the National Academy of Science, vol. 100, pp. 8298–8303, 2003.
[9]
A. L. Koch, “How bacteria face depression, recession, and depression,” Perspectives in Biology and Medicine, vol. 20, no. 1, pp. 44–63, 1976.
[10]
S. Almagro-Moreno and E. F. Boyd, “Insights into the evolution of sialic acid catabolism among bacteria,” BMC Evolutionary Biology, vol. 9, no. 1, article 118, 2009.
[11]
H. Faillard, “The early history of sialic acids,” Trends in Biochemical Sciences, vol. 14, no. 6, pp. 237–241, 1989.
[12]
S. Nees and R. Schauer, “Induction of neuraminidase from Clostridium perfringens and the cooperation of this enzyme with acylneuraminate pyruvate lyase,” Behring Institute Mitteilungen, vol. 55, pp. 68–78, 1974.
[13]
L. R. L. Davies, O. M. T. Pearce, M. B. Tessier et al., “Metabolism of vertebrate amino sugars with N-glycolyl groups: resistance of α2-8-linked N-glycolylneuraminic acid to enzymatic cleavage,” The Journal of Biological Chemistry, vol. 287, no. 34, pp. 28917–28931, 2012.
[14]
C. Robbe, C. Capon, E. Maes et al., “Evidence of regio-specific glycosylation in human intestinal mucins: presence of an acidic gradient along the intestinal tract,” The Journal of Biological Chemistry, vol. 278, no. 47, pp. 46337–46348, 2003.
[15]
A. Rinninger, C. Richet, A. Pons et al., “Localisation and distribution of O-acetylated N-acetylneuraminic acids, the endogenous substrates of the hemagglutinin-esterases of murine coronaviruses, in mouse tissue,” Glycoconjugate Journal, vol. 23, no. 1-2, pp. 73–84, 2006.
[16]
A. P. Moran, A. Gupta, and L. Joshi, “Sweet-talk: role of host glycosylation in bacterial pathogenesis of the gastrointestinal tract,” Gut, vol. 60, pp. 1412–1425, 2011.
[17]
M. E. V. Johansson, D. Ambort, T. Pelaseyed et al., “Composition and functional role of the mucus layers in the intestine,” Cellular and Molecular Life Sciences, vol. 68, no. 22, pp. 3635–3641, 2011.
[18]
M. A. McGuckin, S. K. Lindén, P. Sutton, and T. H. Florin, “Mucin dynamics and enteric pathogens,” Nature Reviews Microbiology, vol. 9, no. 4, pp. 265–278, 2011.
[19]
E. R. Vimr, “Microbial sialidases: does bigger always mean better?” Trends in Microbiology, vol. 2, no. 8, pp. 271–277, 1994.
[20]
E. R. Vimr, L. Lawrisuk, J. Galen, and J. B. Kaper, “Cloning and expression of the Vibrio cholerae neuraminidase gene nanH in Escherichia coli,” Journal of Bacteriology, vol. 170, no. 4, pp. 1495–1504, 1988.
[21]
L. L. Hoyer, A. C. Hamilton, S. M. Steenbergen, and E. R. Vimr, “Cloning, sequencing and distribution of the Salmonella typhimurium LT2 sialidase gene, nanH, provides evidence for interspecies gene transfer,” Molecular Microbiology, vol. 6, no. 7, pp. 873–884, 1992.
[22]
L. L. Hoyer, P. Roggentin, R. Schauer, and E. R. Vimr, “Purification and properties of cloned Salmonella typhimurium LT2 sialidase with virus-typical kinetic preference for sialyl α2 → 3 linkages,” Journal of Biochemistry, vol. 110, no. 3, pp. 462–467, 1991.
[23]
S. J. Crennell, E. F. Garman, W. G. Laver, E. R. Vimr, and G. L. Taylor, “Crystal structure of a bacterial sialidase (from Salmonella typhimurium LT2) shows the same fold as an influenza virus neuraminidase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 21, pp. 9852–9856, 1993.
[24]
P. Roggentin, R. Schauer, L. L. Hoyer, and E. R. Vimr, “The sialidase superfamily and its spread by horizontal gene transfer,” Molecular Microbiology, vol. 9, no. 5, pp. 915–921, 1993.
[25]
A. L. Lewis and W. G. Lewis, “Host sialoglycans and bacterial sialidases: a mucosal perspective,” Cellular Microbiology, vol. 14, no. 8, pp. 1174–1182, 2012.
[26]
E. R. Vimr and F. A. Troy, “Identification of an inducible catabolic system for sialic acids (nan) in Escherichia coli,” Journal of Bacteriology, vol. 164, no. 2, pp. 845–853, 1985.
[27]
E. R. Vimr and F. A. Troy, “Regulation of sialic acid metabolism in Escherichia coli: role of N-acylneuraminate pyruvate-lyase,” Journal of Bacteriology, vol. 164, no. 2, pp. 854–860, 1985.
[28]
J. Plumbridge and E. Vimr, “Convergent pathways for utilization of the amino sugars N-acetylglucosamine, N-acetylmannosamine, and N-acetylneuraminic acid by Escherichia coli,” Journal of Bacteriology, vol. 181, no. 1, pp. 47–54, 1999.
[29]
M. A. Ringenberg, S. M. Steenbergen, and E. R. Vimr, “The first committed step in the biosynthesis of sialic acid by Escherichia coliK1 does not involve a phosphorylated N-acetylmannosamine intermediate,” Molecular Microbiology, vol. 50, no. 3, pp. 961–975, 2003.
[30]
C. Brigham, R. Caughlan, R. Gallegos, M. B. Dallas, V. G. Godoy, and M. H. Malamy, “Sialic acid (N-acetyl neuraminic acid) utilization by Bacteroides fragilis requires a novel N-acetyl mannosamine epimerase,” Journal of Bacteriology, vol. 191, no. 11, pp. 3629–3638, 2009.
[31]
K. A. Kalivoda, S. M. Steenbergen, E. R. Vimr, and J. Plumbridge, “Regulation of sialic acid catabolism by the DNA binding protein NanR in Escherichia coli,” Journal of Bacteriology, vol. 185, no. 16, pp. 4806–4815, 2003.
[32]
E. Vimr, S. Steenbergen, and M. Cieslewicz, “Biosynthesis of the polysialic acid capsule in Escherichia coli K1,” Journal of Industrial Microbiology, vol. 15, no. 4, pp. 352–360, 1995.
[33]
E. Vimr and C. Lichtensteiger, “To sialylate, or not to sialylate: that is the question,” Trends in Microbiology, vol. 10, no. 6, pp. 254–257, 2002.
[34]
S. M. Steenbergen, C. A. Lichtensteiger, R. Caughlan, J. Garfinkle, T. E. Fuller, and E. R. Vimr, “Sialic acid metabolism and systemic pasteurellosis,” Infection and Immunity, vol. 73, no. 3, pp. 1284–1294, 2005.
[35]
F. M. Tatum, L. B. Tabatabai, and R. E. Briggs, “Sialic acid uptake is necessary for virulence of Pasteurella multocida in turkeys,” Microbial Pathogenesis, vol. 46, no. 6, pp. 337–344, 2009.
[36]
E. Vimr, C. Lichtensteiger, and S. Steenbergen, “Sialic acid metabolism's dual function in Haemophilus influenzae,” Molecular Microbiology, vol. 36, no. 5, pp. 1113–1123, 2000.
[37]
S. Almagro-Moreno and E. F. Boyd, “Sialic acid catabolism confers a competitive advantage to pathogenic Vibrio cholerae in the mouse intestine,” Infection and Immunity, vol. 77, no. 9, pp. 3807–3816, 2009.
[38]
H. G. Jeong, M. H. Oh, B. S. Kim, M. Y. Lee, H. J. Han, and S. H. Choi, “The capability of catabolic utilization of N-acetylneuraminic acid, a sialic acid, is essential for Vibrio vulnificus pathogenesis,” Infection and Immunity, vol. 77, no. 8, pp. 3209–3217, 2009.
[39]
B. S. Kim, J. Hwang, M. H. Kim, and S. H. Choi, “Cooperative regulation of the Vibrio vulnificus nan gene cluster by NanR protein, cAMP receptor protein, and N-acetylmannosamine 6-phosphate,” The Journal of Biological Chemistry, vol. 286, no. 47, pp. 40889–40899, 2011.
[40]
C. J. Alteri, S. N. Smith, and H. L. T. Mobley, “Fitness of Escherichia coli during urinary tract infection requires gluconeogenesis and the TCA cycle,” PLoS Pathogens, vol. 5, no. 5, Article ID e1000448, 2009.
[41]
S. N. Smith, E. C. Hagan, M. C. Lane, and H. L. T. Mobley, “Dissemination and systemic colonization of uropathogenic Escherichia coli in a murine model of bacteremia,” mBio, vol. 1, no. 5, Article ID e00262-10, 2010.
[42]
D. E. Chang, D. J. Smalley, D. L. Tucker et al., “Carbon nutrition of Escherichia coli in the mouse intestine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 19, pp. 7427–7432, 2004.
[43]
A. J. Fabich, S. A. Jones, F. Z. Chowdhury et al., “Comparison of carbon nutrition for pathogenic and commensal Escherichia coli strains in the mouse intestine,” Infection and Immunity, vol. 76, no. 3, pp. 1143–1152, 2008.
[44]
A. J. Fabich, M. P. Leatham, J. E. Grissom et al., “Genotype and phenotypes of an intestine-adapted Escherichia coli K-12 mutant selected by animal passage for superior colonization,” Infection and Immunity, vol. 79, no. 6, pp. 2430–2439, 2011.
[45]
A. Pezzicoli, P. Ruggiero, F. Amerighi, J. L. Telford, and M. Soriani, “Exogenous sialic acid transport contributes to group B Streptococcus infection of mucosal surfaces,” Journal of Infectious Diseases, vol. 206, no. 6, pp. 924–931, 2012.
[46]
C. Marion, A. M. Burnaugh, S. A. Woodiga, and S. J. King, “Sialic acid transport contributes to pneumococcal colonization,” Infection and Immunity, vol. 79, no. 3, pp. 1262–1269, 2011.
[47]
H. Yesilkaya, S. Manco, A. Kadioglu, V. S. Terra, and P. W. Andrew, “The ability to utilize mucin affects the regulation of virulence gene expression in Streptococcus pneumoniae,” FEMS Microbiology Letters, vol. 278, no. 2, pp. 231–235, 2008.
[48]
V. Bouchet, D. W. Hood, J. Li et al., “Host-derived sialic acid is incorporated into Haemophilus influenzae lipopolysaccharide and is a major virulence factor in experimental otitis media,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 15, pp. 8898–8903, 2003.
[49]
G. A. Jenkins, M. Figueira, G. A. Kumar et al., “Sialic acid mediated transcriptional modulation of a highly conserved sialometabolism gene cluster in Haemophilus influenzae and its effect on virulence,” BMC Microbiology, vol. 10, article 48, 2010.
[50]
J. W. Johnston, A. Zaleski, S. Allen et al., “Regulation of sialic acid transport and catabolism in Haemophilus influenzae,” Molecular Microbiology, vol. 66, no. 1, pp. 26–39, 2007.
[51]
J. W. Johnston and M. A. Apicella, “Sialic acid metabolism and regulation by Haemophilus influenzae: potential novel antimicrobial therapies,” Current Infectious Disease Reports, vol. 10, no. 2, pp. 83–84, 2008.
[52]
J. W. Johnston, H. Shamsulddin, A. F. Miller, and M. A. Apicella, “Sialic acid transport and catabolism are cooperatively regulated by SiaR and CRP in nontypeable Haemophilus influenzae,” BMC Microbiology, vol. 10, article 240, 2010.
[53]
L. L. Greiner, H. Watanabe, N. J. Phillips et al., “Nontypeable Haemophilus influenzae strain 2019 produces a biofilm containing N-acetylneuraminic acid that may mimic sialylated O-linked glycans,” Infection and Immunity, vol. 72, no. 7, pp. 4249–4260, 2004.
[54]
W. E. Swords, M. L. Moore, L. Godzicki, G. Bukofzer, M. J. Mitten, and J. VonCannon, “Sialylation of Lipooligosaccharides Promotes Biofilm Formation by Nontypeable Haemophilus influenzae,” Infection and Immunity, vol. 72, no. 1, pp. 106–113, 2004.
[55]
J. Jurcisek, L. Greiner, H. Watanabe, A. Zaleski, M. A. Apicella, and L. O. Bakaletz, “Role of sialic acid and complex carbohydrate biosynthesis in biofilm formation by nontypeable Haemophilus influenzae in the chinchilla middle ear,” Infection and Immunity, vol. 73, no. 6, pp. 3210–3218, 2005.
[56]
I. Sandal, T. J. Inzana, A. Molinaro et al., “Identification, structure, and characterization of an exopolysaccharide produced by Histophilus somni during biofilm formation,” BMC Microbiology, vol. 11, article 186, 2011.
[57]
E. R. Moxon, W. A. Sweetman, M. E. Deadman, D. J. P. Ferguson, and D. W. Hood, “Haemophilus influenzae biofilms: hypothesis or fact?” Trends in Microbiology, vol. 16, no. 3, pp. 95–100, 2008.
[58]
G. Xu, C. Ryan, M. J. Kiefel, J. C. Wilson, and G. L. Taylor, “Structural Studies on the Pseudomonas aeruginosa Sialidase-Like Enzyme PA2794 Suggest Substrate and Mechanistic Variations,” Journal of Molecular Biology, vol. 386, no. 3, pp. 828–840, 2009.
[59]
A. L. Lewis, N. Desa, E. E. Hansen et al., “Innovations in host and microbial sialic acid biosynthesis revealed by phylogenomic prediction of nonulosonic acid structure,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 32, pp. 13552–13557, 2009.
[60]
G. Soong, A. Muir, M. I. Gomez et al., “Bacterial neuraminidase facilitates mucosal infection by participating in biofilm production,” The Journal of Clinical Investigation, vol. 116, no. 8, pp. 2297–2305, 2006.
[61]
D. Parker, G. Soong, P. Planet, J. Brower, A. J. Ratner, and A. Prince, “The NanA neuraminidase of Streptococcus pneumoniae is involved in biofilm formation,” Infection and Immunity, vol. 77, no. 9, pp. 3722–3730, 2009.
[62]
C. Trappetti, A. Kadioglu, M. Carter et al., “Sialic acid: a preventable signal for pneumococcal biofilm formation, colonization, and invasion of the host,” Journal of Infectious Diseases, vol. 199, no. 10, pp. 1497–1505, 2009.
[63]
G. Xu, M. J. Kiefel, J. C. Wilson, P. W. Andrew, M. R. Oggioni, and G. L. Taylor, “Three Streptococcus pneumoniae sialidases: three different products,” Journal of the American Chemical Society, vol. 133, no. 6, pp. 1718–1721, 2011.
[64]
S. J. King, K. R. Hippe, J. M. Gould et al., “Phase variable desialylation of host proteins that bind to Streptococcus pneumoniaein vivo and protect the airway,” Molecular Microbiology, vol. 54, no. 1, pp. 159–171, 2004.
[65]
H. S. Li-Korotky, C. Y. Lo, and J. M. Banks, “Interaction of pneumococcal phase variation, host and pressure/gas composition: virulence expression of NanA, HylA, PspA and CbpA in simulated otitis media,” Microbial Pathogenesis, vol. 49, no. 4, pp. 204–210, 2010.
[66]
Y.-C. Chang, S. Uchiyama, A. Varki, and V. Nizet, “Leukocyte inflammatory responses provoked by pneumococcal sialidase,” mBio, vol. 3, no. 1, Article ID e00220-11, 2012.
[67]
A. Bigi, L. Morosi, C. Pozzi et al., “Human sialidase NEU4 long and short are extrinsic proteins bound to outer mitochondrial membrane and the endoplasmic reticulum, respectively,” Glycobiology, vol. 20, no. 2, pp. 148–157, 2009.
[68]
S. Mizan, A. Henk, A. Stallings, M. Maier, and M. D. Lee, “Cloning and characterization of sialidases with 2-6′ and 2-3′ sialyl lactose specificity from Pasteurella multocida,” Journal of Bacteriology, vol. 182, no. 24, pp. 6874–6883, 2000.
[69]
M. Mally, H. Shin, C. Paroz, R. Landmann, and G. R. Cornelis, “Capnocytophaga canimorsus a human pathogen feeding at the surface of epithelial cells and phagocytes,” PLoS Pathogens, vol. 4, no. 9, Article ID e1000164, 2008.
[70]
E. C. Martens, H. C. Chiang, and J. I. Gordon, “Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont,” Cell Host and Microbe, vol. 4, no. 5, pp. 447–457, 2008.
[71]
B. Deplancke, O. Vidal, D. Ganessunker, S. M. Donovan, R. I. Mackie, and H. R. Gaskins, “Selective growth of mucolytic bacteria including Clostridium perfringens in a neonatal piglet model of total parenteral nutrition,” American Journal of Clinical Nutrition, vol. 76, no. 5, pp. 1117–1125, 2002.
[72]
N. Fontaine, J. C. Meslin, and J. Doré, “Selective in vitro degradation of the sialylated fraction of germ-free rat mucins by the caecal flora of the rat,” Reproduction Nutrition Development, vol. 38, no. 3, pp. 289–296, 1998.
[73]
M. Berry, A. Harris, R. Lumb, and K. Powell, “Commensal ocular bacteria degrade mucins,” British Journal of Ophthalmology, vol. 86, no. 12, pp. 1412–1416, 2002.
[74]
A. M. Burnaugh, L. J. Frantz, and S. J. King, “Growth of Streptococcus pneumoniae on human glycoconjugates is dependent upon the sequential activity of bacterial exoglycosidases,” Journal of Bacteriology, vol. 190, no. 1, pp. 221–230, 2008.
[75]
S. J. King, K. R. Hippe, and J. N. Weiser, “Deglycosylation of human glycoconjugates by the sequential activities of exoglycosidases expressed by Streptococcus pneumoniae,” Molecular Microbiology, vol. 59, no. 3, pp. 961–974, 2006.
[76]
E. R. Vimr and S. M. Steenbergen, “Chromatographic analysis of the Escherichia coli polysialic acid capsule,” in Methods in Molecular Biology-the Bacterial Cell Surface, Methods and Protocols, H. Anne Delcour, Ed., pp. 109–120, 2013.
[77]
C. Robbe, C. Capon, B. Coddeville, and J. C. Michalski, “Structural diversity and specific distribution of O-glycans in normal human mucins along the intestinal tract,” Biochemical Journal, vol. 384, no. 2, pp. 307–316, 2004.
[78]
A. P. Corfield, S. A. Wagner, L. J. D. O'Donnell, P. Durdey, R. A. Mountford, and J. R. Clamp, “The roles of enteric bacterial sialidase, sialate O-acetyl esterase and glycosulfatase in the degradation of human colonic mucin,” Glycoconjugate Journal, vol. 10, no. 1, pp. 72–81, 1993.
[79]
V. G. Godoy, M. M. Dallas, T. A. Russo, and M. H. Malamy, “A role for Bacteroides fragilis neuraminidase in bacterial growth in two model systems,” Infection and Immunity, vol. 61, no. 10, pp. 4415–4426, 1993.
[80]
R. B. Parker, J. E. McCombs, and J. J. Kohler, “Sialidase specificity determined by chemoselective modification of complex sialylated glycans,” ACS Chemical Biology, vol. 9, pp. 1509–1514, 2012.
[81]
G. Condemine, C. Berrier, J. Plumbridge, and A. Ghazi, “Function and expression of an N-acetylneuraminic acid-inducible outer membrane channel in Escherichia coli,” Journal of Bacteriology, vol. 187, no. 6, pp. 1959–1965, 2005.
[82]
C. Wirth, G. Condemine, C. Boiteux, S. Bernèche, T. Schirmer, and C. M. Peneff, “NanC crystal structure, a model for outer-membrane channels of the acidic sugar specific KdgM porin family,” Journal of Molecular Biology, vol. 394, no. 4, pp. 718–731, 2009.
[83]
J. Domka, J. Lee, T. Bansal, and T. K. Wood, “Temporal gene-expression in Escherichia coli K-12 biofilms,” Environmental Microbiology, vol. 9, no. 2, pp. 332–346, 2007.
[84]
C. A. Santiviago, M. M. Reynolds, S. Porwollik et al., “Analysis of pools of targeted Salmonella deletion mutants identifies novel genes affecting fitness during competitive infection in mice,” PLoS Pathogens, vol. 5, no. 7, Article ID e1000477, 2009.
[85]
I. Moustafa, H. Connaris, M. Taylor et al., “Sialic acid recognition by Vibrio cholerae neuraminidase,” The Journal of Biological Chemistry, vol. 279, no. 39, pp. 40819–40826, 2004.
[86]
T. Angata and A. Varki, “Chemical diversity in the sialic acids and related α-keto acids: an evolutionary perspective,” Chemical Reviews, vol. 102, no. 2, pp. 439–469, 2002.
[87]
E. Severi, A. Müller, J. R. Potts et al., “Sialic acid mutarotation is catalyzed by the Escherichia coliβ-propeller protein YjhT,” The Journal of Biological Chemistry, vol. 283, no. 8, pp. 4841–4849, 2008.
[88]
A. R. Joyce, J. L. Reed, A. White et al., “Experimental and computational assessment of conditionally essential genes in Escherichia coli,” Journal of Bacteriology, vol. 188, no. 23, pp. 8259–8271, 2006.
[89]
S. M. Steenbergen, J. L. Jirik, and E. R. Vimr, “YjhS (NanS) is required for Escherichia coli to grow on 9-O-acetylated N-acetylneuraminic acid,” Journal of Bacteriology, vol. 191, no. 22, pp. 7134–7139, 2009.
[90]
S. M. Steenbergen, Y. C. Lee, W. F. Vann, J. Vionnet, L. F. Wright, and E. R. Vimr, “Separate pathways for O acetylation of polymeric and monomeric sialic acids and identification of sialyl O-acetyl esterase in Escherichia coli K1,” Journal of Bacteriology, vol. 188, no. 17, pp. 6195–6206, 2006.
[91]
P. A. Clarke, N. Mistry, and G. H. Thomas, “Synthesis of the complete series of mono acetates of N-acetyl-d-neuraminic acid,” Organic and Biomolecular Chemistry, vol. 10, no. 3, pp. 529–535, 2012.
[92]
E. S. Rangarajan, K. M. Ruane, A. Proteau et al., “Structural and enzymatic characterization of NanS (YjhS), a 9-O-acetyl N-acetylneuraminic acid esterase from Escherichia coli O157:H7,” Protein Science, vol. 20, no. 7, pp. 1208–1219, 2011.
[93]
A. Teplyakov, G. Obmolova, J. Toedt, M. Y. Galperin, and G. L. Gilliland, “Crystal structure of the bacterial YhcH protein indicates a role in sialic acid catabolism,” Journal of Bacteriology, vol. 187, no. 16, pp. 5520–5527, 2005.
[94]
S. Roy, C. W. Douglas, and G. P. Stafford, “A novel sialic acid utilization and uptake system in the periodontal pathogen Tannerella forsythia,” Journal of Bacteriology, vol. 192, pp. 2285–2293, 2010.
[95]
J. Martinez, S. Steenbergen, and E. Vimr, “Derived structure of the putative sialic acid transporter from Escherichia coli predicts a novel sugar permease domain,” Journal of Bacteriology, vol. 177, no. 20, pp. 6005–6010, 1995.
[96]
P. Allevi, P. Rota, R. Scaringi, R. Colombo, and M. Anastasia, “Chemoselective synthesis of sialic acid 1,7-lactones,” Journal of Organic Chemistry, vol. 75, no. 16, pp. 5542–5548, 2010.
[97]
Y. Ogasawara, T. Namai, F. Yoshino, M. C. I. Lee, and K. Ishii, “Sialic acid is an essential moiety of mucin as a hydroxyl radical scavenger,” FEBS Letters, vol. 581, no. 13, pp. 2473–2477, 2007.
[98]
R. Iijima, H. Takahashi, S. Ikegami, and M. Yamazaki, “Characterization of the reaction between sialic acid (N-acetylneuraminic acid) and hydrogen peroxide,” Biological and Pharmaceutical Bulletin, vol. 30, no. 3, pp. 580–582, 2007.
[99]
E. Severi, A. H. F. Hosie, J. A. Hawkhead, and G. H. Thomas, “Characterization of a novel sialic acid transporter of the sodium solute symporter (SSS) family and in vivo comparison with known bacterial sialic acid transporters,” FEMS Microbiology Letters, vol. 304, no. 1, pp. 47–54, 2010.
[100]
E. R. Vimr and C. G. Miller, “Dipeptidyl carboxypeptidase-deficient mutants of Salmonella typhimurium,” Journal of Bacteriology, vol. 153, no. 3, pp. 1252–1258, 1983.
[101]
E. R. Vimr, L. Green, and C. G. Miller, “Oligopeptidase-deficient mutants of Salmonella typhimurium,” Journal of Bacteriology, vol. 153, no. 3, pp. 1259–1265, 1983.
[102]
T. Bulai, D. Bratosin, V. Artenie, and J. Montreuil, “Characterization of a sialate pyruvate-lyase in the cytosol of human erythrocytes,” Biochimie, vol. 84, no. 7, pp. 655–660, 2002.
[103]
M. T. Pellicer, J. Badía, J. Aguilar, and L. Baldomà, “glc Locus of Escherichia coli: characterization of genes encoding the subunits of glycolate oxidase and the glc regulator protein,” Journal of Bacteriology, vol. 178, no. 7, pp. 2051–2059, 1996.
[104]
A. K. Bergfeld, O. M. T. Pearce, S. L. Diaz et al., “Metabolism of vertebrate amino sugars with N-glycolyl groups: incorporation of N-glycolylhexosamines into mammalian glycans by feeding N- glycolylgalactosamine,” The Journal of Biological Chemistry, vol. 287, no. 34, pp. 28898–28916, 2012.
[105]
C. C. Goller and P. C. Seed, “High-throughput identification of chemical inhibitors of E. coli group 2 capsule biogenesis as anti-virulence agents,” PLoS ONE, vol. 5, no. 7, Article ID e11642, 2010.
