Chapter 15 : Host Sialic Acids: A Delicacy for the Pathogen with Discerning Taste

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Sialic acids (neuraminic acids) are a diverse family of nine carbon (nonulosonic) α-keto acidic carbohydrates. The canonical sialic acid, 2-keto-3-deoxy-5-acetamido-D--D--nonulosonic acid, also known as -acetylneuraminic acid (Neu5Ac) is the backbone on which a large number of known modifications are made ( ). The Neu5Ac structure is typified by a 6-carbon carboxylic acid ring structure with a glycerol tail, an acetamido at the C-5 position and hydroxyl groups present on C-4, C-7, C-8, and C-9. Modifications occur primarily on the hydroxyl groups, with -acetylation being the most common alteration, and substitutions have been shown to occur after the completion of the core structure ( ). Other modifications such as -methylation, -lactylation, and -sulfation add to the diversity of this molecule . Two structurally similar sialic acids, -glycolylneuraminic acid (Neu5c), which differs from Neu5c by the presence of a hydroxyl group on the N-5 acetyl moiety, and 2-keto-3-deoxyl-D--D--nonulosonic acid (KDN), a deaminated form of Neu5c, also occur in nature and similar modifications are made to their core structure ( ). These three main structures (Neu5c, Neu5c, and KDN) encompass the family of sialic acids due to their retention of the same stereochemical configuration of the 9-carbon backbone.

Citation: Haines-menges B, Whitaker W, Lubin J, Boyd E. 2015. Host Sialic Acids: A Delicacy for the Pathogen with Discerning Taste, p 321-342. In Conway T, Cohen P (ed), Metabolism and Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MBP-0005-2014
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Figure 1

Bacterial sialylation of surface components. This diagram depicts the different surface structures in bacteria that are known to be decorated with nonulosonic acids (neuraminic, pseudaminic, or legionaminic). Also indicated are bacterial species demonstrated to have different surfaces sialylated.

Citation: Haines-menges B, Whitaker W, Lubin J, Boyd E. 2015. Host Sialic Acids: A Delicacy for the Pathogen with Discerning Taste, p 321-342. In Conway T, Cohen P (ed), Metabolism and Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MBP-0005-2014
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Image of Figure 2
Figure 2

Schematic representation of the catabolism of sialic acid in Bacteria. The first step in catabolism is the uptake into the bacterial cell of free sialic acid molecules across the cell wall and cell membrane. Four type of transport systems have been described for transport across the cell membrane, MFS, SSS, TRAP, and ABC systems. NanH, Neuraminidase; Neu5Ac, -acetylneuraminic acid. The sialic acid catabolic pathway involves several steps beginning with NanA. NanA, -acetylneuraminic acid lyase; ManNAc, -acetylmannosamine; NanK, -acetylmannosamine kinase; ManNAc-6-P, -acetylmannosamine-6-phosphate; NanE, -acetylmannosamine-6-P epimerase; GlcNAc-6-P, -acetylglucosamine-6-phosphate; NagA, -acetylglucosamine-6-phosphate deacteylase; GlcN-6-P, Glucosamine-6-phosphate; NagB, Glucosamine-6-phosphate deaminase; Fru-6-P, Fructose-6-phosphate; LPS, lipopolysaccharide.

Citation: Haines-menges B, Whitaker W, Lubin J, Boyd E. 2015. Host Sialic Acids: A Delicacy for the Pathogen with Discerning Taste, p 321-342. In Conway T, Cohen P (ed), Metabolism and Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MBP-0005-2014
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Figure 3

sialic acid metabolism. is an extracellular intestinal pathogen that colonizes the mucus layer of the small intestine and elaborates cholera toxin and sialidase. Sialidase cleaves sialic acid from high order gangliosides to release sialic acid and expose the GM1 ganglioside, the receptor for cholera toxin. Free sialic acid can be transported into the cell via the TRAP transporter SiaPQM contained on the pathogenicity island VPI-2, which also contains the genes for sialic acid catabolism.

Citation: Haines-menges B, Whitaker W, Lubin J, Boyd E. 2015. Host Sialic Acids: A Delicacy for the Pathogen with Discerning Taste, p 321-342. In Conway T, Cohen P (ed), Metabolism and Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MBP-0005-2014
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Figure 4

Schematic diagram of the pathogenicity island VPI-2 in choleragenic isolates. ORFs of interest are depicted as arrows indicting the direction of transcription. The entire sialic acid catabolism cluster encompasses 12 kb on the 57 kb VPI-2 region.

Citation: Haines-menges B, Whitaker W, Lubin J, Boyd E. 2015. Host Sialic Acids: A Delicacy for the Pathogen with Discerning Taste, p 321-342. In Conway T, Cohen P (ed), Metabolism and Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MBP-0005-2014
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1. Angata T,, Varki A . 2002. Chemical diversity in the sialic acids and related alpha-keto acids: an evolutionary perspective. Chem Rev 102 : 439 469.[PubMed] [CrossRef]
2. Butor C,, Diaz S,, Varki A . 1993. High level O-acetylation of sialic acids on N-linked oligosaccharides of rat liver membranes. Differential subcellular distribution of 7- and 9-O-acetyl groups and of enzymes involved in their regulation. J Biol Chem 268 : 10197 10206.[PubMed]
3. Varki A . 2001. Loss of N-glycolylneuraminic acid in humans: Mechanisms, consequences, and implications for hominid evolution. Am J Phys Anthropol Suppl 33 : 54 69.[PubMed] [CrossRef]
4. Inoue S,, Kitajima K . 2006. KDN (deaminated neuraminic acid): dreamful past and exciting future of the newest member of the sialic acid family. Glycoconj J 23 : 277 290.[PubMed] [CrossRef]
5. Kazatchkine MD,, Fearon DT,, Austen KF . 1979. Human alternative complement pathway: membrane-associated sialic acid regulates the competition between B and beta1 H for cell-bound C3b. J Immunol 122 : 75 81.[PubMed]
6. Bennett M,, Schmid K . 1980. Immunosuppression by human plasma alpha 1-acid glycoprotein: importance of the carbohydrate moiety. Proc Natl Acad Sci USA 77 : 6109. [PubMed] [CrossRef]
7. Ozkan AN,, Ninnemann JL . 1985. Suppression of in vitro lymphocyte and neutrophil responses by a low molecular weight suppressor active peptide from burn-patient sera. J Clin Immunol 5 : 172 179.[CrossRef]
8. Cameron DJ,, Churchill WH . 1982. Specificity of macrophage mediated cytotoxicity: role of target cell sialic acid. Jpn J Exp Med 52 : 9 16.[PubMed]
9. Lanoue A,, Batista FD,, Stewart M,, Neuberger MS . 2002. Interaction of CD22 with alpha2,6-linked sialoglycoconjugates: innate recognition of self to dampen B cell autoreactivity? Eur J Immunol 32 : 348 355.[CrossRef]
10. Rutishauser U . 2008. Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat Rev Neurosci 9 : 26 35.[PubMed] [CrossRef]
11. Wang B . 2012. Molecular mechanism underlying sialic acid as an essential nutrient for brain development and cognition. Adv Nutr 3 : 465S 472S.[PubMed] [CrossRef]
12. Blix G . 1936. Concerning the carbohydrate groups of submaxillary mucin. Hoppe-Seylers Zeitschrift Fur Physiologische Chemie 240 : 43 54.[CrossRef]
13. Culling CFA,, Reid PE,, Clay MG,, Dunn WL . 1974. The histochemical demonstration of O-acylated sialic acid in gastrointestinal mucins. Their association with the potassium hydroxide-periodic acid-schiff effect. J Histochem Cytochem 22 : 826 831.[PubMed] [CrossRef]
14. Thornton DJ,, Carlstedt I,, Howard M,, Devine PL,, Price MR,, Sheehan JK . 1996. Respiratory mucins: identification of core proteins and glycoforms. Biochem J 316( Pt 3) : 967 975.[PubMed]
15. Scudder PR,, Chantler EN . 1982. Control of human cervical mucin glycosylation by endogenous fucosyl and sialyltransferases. Adv Exp Med Biol 144 : 265 267.[CrossRef]
16. Robbe C,, Capon C,, Coddeville B,, Michalski JC . 2004. Structural diversity and specific distribution of O-glycans in normal human mucins along the intestinal tract. Biochem J 384 : 307 316.[PubMed] [CrossRef]
17. Slomiany BL,, Murty VLN,, Piotrowski J,, Slomiany A . 1996. Salivary mucins in oral mucosal defense. Gen Pharmacol—Vascular Syst 27 : 761 771.[CrossRef]
18. Ho JJ,, Cheng S,, Kim YS . 1995. Access to peptide regions of a surface mucin (MUC1) is reduced by sialic acids. Biochem Biophys Res Commun 210 : 866 873.[PubMed] [CrossRef]
19. Ogasawara Y,, Namai T,, Yoshino F,, Lee MC,, Ishii K . 2007. Sialic acid is an essential moiety of mucin as a hydroxyl radical scavenger. FEBS Letters 581 : 2473 2477.[PubMed] [CrossRef]
20. Vann WF,, Daines DA,, Murkin AS,, Tanner ME,, Chaffin DO,, Rubens CE,, Vionnet J,, Silver RP . 2004. The NeuC protein of Escherichia coli K1 is a UDP N-acetylglucosamine 2-epimerase. J Bacteriol 186 : 706 712.[PubMed] [CrossRef]
21. Vann WF,, Silver RP,, Abeijon C,, Chang K,, Aaronson W,, Sutton A,, Finn CW,, Lindner W,, Kotsatos M . 1987. Purification, properties, and genetic location of Escherichia coli cytidine 5′-monophosphate N-acetylneuraminic acid synthetase. J Biol Chem 262 : 17556 17562.[PubMed]
22. Vann WF,, Tavarez JJ,, Crowley J,, Vimr E,, Silver RP . 1997. Purification and characterization of the Escherichia coli K1 neuB gene product N-acetylneuraminic acid synthetase. Glycobiology 7 : 697 701.[PubMed] [CrossRef]
23. Knirel YA,, Rietschel ET,, Marre R,, ZÄHringer U . 1994. The structure of the O-specific chain of Legionella pneumophila serogroup 1 lipopolysaccharide. Eur J Biochem 221 : 239 245.[PubMed] [CrossRef]
24. Knirel YA,, Vinogradov EV,, L’Vov VL,, Kocharova NA,, Shashkov AS,, Dmitriev BA,, Kochetkov NK . 1984. Sialic acids of a new type from the lipopolysaccharides of Pseudomonas aeruginosa and Shigella boydii . Carbohydr Res 133 : C5 C8.[CrossRef]
25. Parsons NJ,, Patel PV,, Tan EL,, Andrade JR,, Nairn CA,, Goldner M,, Cole JA,, Smith H . 1988. Cytidine 5′-monophospho-N-acetyl neuraminic acid and a low molecular weight factor from human blood cells induce lipopolysaccharide alteration in gonococci when conferring resistance to killing by human serum. Microb Pathog 5 : 303 309.[CrossRef]
26. Mushtaq N,, Redpath MB,, Luzio JP,, Taylor PW . 2004. Prevention and Cure of Systemic Escherichia coli K1 Infection by Modification of the Bacterial Phenotype. Antimicrob Agents Chemother 48 : 1503 1508.[PubMed] [CrossRef]
27. Kline KA,, Schwartz DJ,, Lewis WG,, Hultgren SJ,, Lewis AL . 2011. Immune activation and suppression by group B streptococcus in a murine model of urinary tract infection. Infect Immun 79 : 3588 3595.[PubMed] [CrossRef]
28. Bouchet V,, Hood DW,, Li J,, Brisson JR,, Randle GA,, Martin A,, Li Z,, Goldstein R,, Schweda EKH,, Pelton SI,, Richards JC,, Moxon ER . 2003. Host-derived sialic acid is incorporated into Haemophilus influenzae lipopolysaccharide and is a major virulence factor in experimental otitis media. Proc Natl Acad Sci USA 100 : 8898 8903.[PubMed] [CrossRef]
29. Soong G,, Muir A,, Gomez MI,, Waks J,, Reddy B,, Planet P,, Singh PK,, Kaneko Y,, Wolfgang MC,, Hsiao YS,, Tong L,, Prince A . 2006. Bacterial neuraminidase facilitates mucosal infection by participating in biofilm production. J Clin Invest 116 : 2297 2305.[PubMed] [CrossRef]
30. Jurcisek J,, Greiner L,, Watanabe H,, Zaleski A,, Apicella MA,, Bakaletz LO . 2005. Role of sialic acid and complex carbohydrate biosynthesis in biofilm formation by nontypeable Haemophilus influenzae in the chinchilla middle ear. Infect Immun 73 : 3210 3218.[PubMed] [CrossRef]
31. Trappetti C,, Kadioglu A,, Carter M,, Hayre J,, Iannelli F,, Pozzi G,, Andrew PW,, Oggioni MR . 2009. Sialic acid: a preventable signal for pneumococcal biofilm formation, colonization, and invasion of the host. J Infect Dis 199 : 1497 1505.[PubMed] [CrossRef]
32. Parker D,, Soong G,, Planet P,, Brower J,, Ratner AJ,, Prince A . 2009. The NanA neuraminidase of Streptococcus pneumoniae is involved in biofilm formation. Infect Immun 77 : 3722 3730.[PubMed] [CrossRef]
33. Lewis AL,, Desa N,, Hansen EE,, Knirel YA,, Gordon JI,, Gagneux P,, Nizet V,, Varki A . 2009. Innovations in host and microbial sialic acid biosynthesis revealed by phylogenomic prediction of nonulosonic acid structure. Proc Natl Acad Sci USA 106 : 13552 13557.[PubMed] [CrossRef]
34. Almagro-Moreno S,, Boyd EF . 2009. Sialic acid catabolism confers a competitive advantage to pathogenic Vibrio cholerae in the mouse intestine. Infect Immun 77 : 3807 3816.[PubMed] [CrossRef]
35. Almagro-Moreno S,, Boyd EF . 2010. Bacterial catabolism of nonulosonic (sialic) acid and fitness in the gut. Gut Microbes 1 : 45 50.[PubMed] [CrossRef]
36. Vimr ER,, Troy FA . 1985. Regulation of sialic acid metabolism in Escherichia coli: role of N-acylneuraminate pyruvate-lyase. J Bacteriol 164 : 854 860.[PubMed]
37. Lewis WG,, Robinson LS,, Gilbert NM,, Perry JC,, Lewis AL . 2013. Degradation, foraging, and depletion of mucus sialoglycans by the vagina-adapted Actinobacterium Gardnerella vaginalis . J Biol Chem 288 : 12067 12079.[PubMed] [CrossRef]
38. Condemine G,, Berrier C,, Plumbridge J,, Ghazi A . 2005. Function and Expression of an N-Acetylneuraminic Acid-Inducible Outer Membrane Channel in Escherichia coli . J Bacteriol 187 : 1959 1965.[PubMed] [CrossRef]
39. Vimr ER,, Troy FA . 1985. Identification of an inducible catabolic system for sialic acids (nan) in Escherichia coli . J Bacteriol 164 : 845 853.[PubMed]
40. Martinez J,, Steenbergen S,, Vimr E . 1995. Derived structure of the putative sialic acid transporter from Escherichia coli predicts a novel sugar permease domain. J Bacteriol 177 : 6005 6010.[PubMed]
41. Allen S,, Zaleski A,, Johnston JW,, Gibson BW,, Apicella MA . 2005. Novel sialic acid transporter of Haemophilus influenzae . Infect Immun 73 : 5291 5300.[PubMed] [CrossRef]
42. Post DM,, Mungur R,, Gibson BW,, Munson RS Jr . 2005. Identification of a novel sialic acid transporter in Haemophilus ducreyi . Infect Immun 73 : 6727 6735.[PubMed] [CrossRef]
43. Severi E,, Randle G,, Kivlin P,, Whitfield K,, Young R,, Moxon R,, Kelly D,, Hood D,, Thomas GH . 2005. Sialic acid transport in Haemophilus influenzae is essential for lipopolysaccharide sialylation and serum resistance and is dependent on a novel tripartite ATP-independent periplasmic transporter. Mol Microbiol 58 : 1173 1185.[PubMed] [CrossRef]
44. Severi E,, Hood DW,, Thomas GH . 2007. Sialic acid utilization by bacterial pathogens. Microbiology 153 : 2817 2822.[PubMed] [CrossRef]
45. Mulligan C,, Geertsma ER,, Severi E,, Kelly DJ,, Poolman B,, Thomas GH . 2009. The substrate-binding protein imposes directionality on an electrochemical sodium gradient-driven TRAP transporter. Proc Natl Acad Sci USA 106 : 1778 1783.[PubMed] [CrossRef]
46. Severi E,, Hosie AH,, Hawkhead JA,, Thomas GH . 2010. 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 Microbiol Lett 304 : 47 54.[PubMed] [CrossRef]
47. Almagro-Moreno S,, Boyd EF . 2009. Insights into the evolution of sialic acid catabolism among bacteria. BMC Evol Biol 9 : 118. [PubMed] [CrossRef]
48. Wade WG . 2013. The oral microbiome in health and disease. Pharmacol Res 69 : 137 143.[PubMed] [CrossRef]
49. Freter R, . 1983. Mechanisms that control the microflora in the large intestine, p 33 54. In Hentges DJ (ed), Human intestinal microflora in health and disease. Academic Press, Inc., New York. [CrossRef]
50. Freter R . 1988. Mechanisms of bacterial colonization of the mucosal surfaces of the gut, p 45 60. Virulence mechanisms of bacterial pathogens. American Society for Microbiology, Washington, DC.
51. Roy S,, Douglas CW,, Stafford GP . 2010. A novel sialic acid utilization and uptake system in the periodontal pathogen Tannerella forsythia . J Bacteriol 192 : 2285 2293.[PubMed] [CrossRef]
52. Stafford G,, Roy S,, Honma K,, Sharma A . 2012. Sialic acid, periodontal pathogens and Tannerella forsythia: stick around and enjoy the feast! Mol Oral Microbiol 27 : 11 22.[PubMed] [CrossRef]
53. Brigham C,, Caughlan R,, Gallegos R,, Dallas MB,, Godoy VG,, Malamy MH . 2009. Sialic acid (N-acetyl neuraminic acid) utilization by Bacteroides fragilis requires a novel N-acetyl mannosamine epimerase. J Bacteriol 191 : 3629 3638.[PubMed] [CrossRef]
54. Brigham CJ,, Malamy MH . 2005. Characterization of the RokA and HexA broad-substrate-specificity hexokinases from Bacteroides fragilis and their role in hexose and N-acetylglucosamine utilization. J Bacteriol 187 : 890 901.[PubMed] [CrossRef]
55. Honma K,, Mishima E,, Sharma A . 2011. Role of Tannerella forsythia NanH sialidase in epithelial cell attachment. Infect Immun 79 : 393 401.[PubMed] [CrossRef]
56. Thompson H,, Homer KA,, Rao S,, Booth V,, Hosie AH . 2009. An orthologue of Bacteroides fragilis NanH is the principal sialidase in Tannerella forsythia . J Bacteriol 191 : 3623 3628.[PubMed] [CrossRef]
57. Ishikura H,, Arakawa S,, Nakajima T,, Tsuchida N,, Ishikawa I . 2003. Cloning of the Tannerella forsythensis ( Bacteroides forsythus) siaHI gene and purification of the sialidase enzyme. J Med Microbiol 52 : 1101 1107.[PubMed] [CrossRef]
58. Wyss C,, Moter A,, Choi BK,, Dewhirst FE,, Xue Y,, Schupbach P,, Gobel UB,, Paster BJ,, Guggenheim B . 2004. Treponema putidum sp. nov., a medium-sized proteolytic spirochaete isolated from lesions of human periodontitis and acute necrotizing ulcerative gingivitis. Int J Syst Evol Microbiol 54 : 1117 1122.[PubMed] [CrossRef]
59. Kurniyati K,, Zhang W,, Zhang K,, Li C . 2013. A surface-exposed neuraminidase affects complement resistance and virulence of the oral spirochaete Treponema denticola . Mol Microbiol 89 : 842 856.[PubMed] [CrossRef]
60. Byers HL,, Homer KA,, Beighton D . 1996. Utilization of sialic acid by viridans streptococci. J Dent Res 75 : 1564 1571.[PubMed] [CrossRef]
61. Byers HL,, Tarelli E,, Homer KA,, Hambley H,, Beighton D . 1999. Growth of Viridans streptococci on human serum alpha1-acid glycoprotein. J Dent Res 78 : 1370 1380.[PubMed] [CrossRef]
62. Beck JM,, Young VB,, Huffnagle GB . 2012. The microbiome of the lung. Transl Res 160 : 258 266.[PubMed] [CrossRef]
63. Cui L,, Morris A,, Ghedin E . 2013. The human mycobiome in health and disease. Genome Med 5 : 63. [PubMed] [CrossRef]
64. Huang YJ,, Lynch SV . 2011. The emerging relationship between the airway microbiota and chronic respiratory disease: clinical implications. Expert Rev Respir Med 5 : 809 821.[PubMed] [CrossRef]
65. Lilley GG,, Barbosa JA,, Pearce LA . 1998. Expression in Escherichia coli of the putative N-acetylneuraminate lyase gene (nanA) from Haemophilus influenzae: overproduction, purification, and crystallization. Protein Expr Purif 12 : 295 304.[PubMed] [CrossRef]
66. Hood DW,, Makepeace K,, Deadman ME,, Rest RF,, Thibault P,, Martin A,, Richards JC,, Moxon ER . 1999. Sialic acid in the lipopolysaccharide of Haemophilus influenzae: strain distribution, influence on serum resistance and structural characterization. Mol Microbiol 33 : 679 692.[PubMed] [CrossRef]
67. Vimr E,, Lichtensteiger C,, Steenbergen S . 2000. Sialic acid metabolism’s dual function in Haemophilus influenzae . Mol Microbiol 36 : 1113 1123.[PubMed] [CrossRef]
68. Johnston JW,, Zaleski A,, Allen S,, Mootz JM,, Armbruster D,, Gibson BW,, Apicella MA,, Munson RS Jr . 2007. Regulation of sialic acid transport and catabolism in Haemophilus influenzae . Mol Microbiol 66 : 26 39.[PubMed] [CrossRef]
69. Pettigrew MM,, Fennie KP,, York MP,, Daniels J,, Ghaffar F . 2006. Variation in the presence of neuraminidase genes among Streptococcus pneumoniae isolates with identical sequence types. Infect Immun 74 : 3360 3365.[PubMed] [CrossRef]
70. King SJ . 2010. Pneumococcal modification of host sugars: a major contributor to colonization of the human airway? Mol Oral Microbiol 25 : 15 24.[PubMed] [CrossRef]
71. Marion C,, Aten AE,, Woodiga SA,, King SJ . 2011. Identification of an ATPase, MsmK, which energizes multiple carbohydrate ABC transporters in Streptococcus pneumoniae . Infect Immun 79 : 4193 4200.[PubMed] [CrossRef]
72. Xu G,, Kiefel MJ,, Wilson JC,, Andrew PW,, Oggioni MR,, Taylor GL . 2011. Three Streptococcus pneumoniae sialidases: three different products. J Am Chem Soc 133 : 1718 1721.[PubMed] [CrossRef]
73. Brittan JL,, Buckeridge TJ,, Finn A,, Kadioglu A,, Jenkinson HF . 2012. Pneumococcal neuraminidase A: an essential upper airway colonization factor for Streptococcus pneumoniae . Mol Oral Microbiol 27 : 270 283.[PubMed] [CrossRef]
74. Manco S,, Hernon F,, Yesilkaya H,, Paton JC,, Andrew PW,, Kadioglu A . 2006. Pneumococcal neuraminidases A and B both have essential roles during infection of the respiratory tract and sepsis. Infect Immun 74 : 4014 4020.[PubMed] [CrossRef]
75. Orihuela CJ,, Gao G,, Francis KP,, Yu J,, Tuomanen EI . 2004. Tissue-specific contributions of pneumococcal virulence factors to pathogenesis. J Infect Dis 190 : 1661 1669.[PubMed] [CrossRef]
76. Tong HH,, Blue LE,, James MA,, DeMaria TF . 2000. Evaluation of the virulence of a Streptococcus pneumoniae neuraminidase-deficient mutant in nasopharyngeal colonization and development of otitis media in the chinchilla model. Infect Immun 68 : 921 924.[PubMed] [CrossRef]
77. Srinivasan S,, Hoffman NG,, Morgan MT,, Matsen FA,, Fiedler TL,, Hall RW,, Ross FJ,, McCoy CO,, Bumgarner R,, Marrazzo JM,, Fredricks DN . 2012. Bacterial communities in women with bacterial vaginosis: high resolution phylogenetic analyses reveal relationships of microbiota to clinical criteria. PLoS One 7 : e37818. [PubMed] [CrossRef]
78. Lewis AL,, Lewis WG . 2012. Host sialoglycans and bacterial sialidases: a mucosal perspective. Cell Microbiol 14 : 1174 1182.[PubMed] [CrossRef]
79. von Nicolai H,, Hammann R,, Salehnia S,, Zilliken F . 1984. A newly discovered sialidase from Gardnerella vaginalis . Zentralbl Bakteriol Mikrobiol Hyg A 258 : 20 26.[CrossRef]
80. Hopkins AP,, Hawkhead JA,, Thomas GH . 2013. Transport and catabolism of the sialic acids N-glycolylneuraminic acid and 3-keto-3-deoxy-D-glycero-D-galactonononic acid by Escherichia coli K-12. FEMS Microbiol Lett 347 : 14 22.[PubMed] [CrossRef]
81. Gilbert NM,, Lewis WG,, Lewis AL . 2013. Clinical features of bacterial vaginosis in a murine model of vaginal infection with Gardnerella vaginalis . PLoS One 8 : e59539. [PubMed] [CrossRef]
82. Pezzicoli A,, Ruggiero P,, Amerighi F,, Telford JL,, Soriani M . 2012. Exogenous sialic acid transport contributes to group B streptococcus infection of mucosal surfaces. J Infect Dis 206 : 924 931.[PubMed] [CrossRef]
83. McGuckin MA,, Linden SK,, Sutton P,, Florin TH . 2011. Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9 : 265 278.[PubMed] [CrossRef]
84. LaMont JT,, Ventola AS . 1980. Purification and composition of colonic epithelial mucin. Biochim Biophys Acta 626 : 234 243.[CrossRef]
85. Peekhaus N,, Conway T . 1998. What’s for dinner?: Entner-Doudoroff metabolism in Escherichia coli . J Bacteriol 180 : 3495 3502.[PubMed]
86. Chang DE,, Smalley DJ,, Tucker DL,, Leatham MP,, Norris WE,, Stevenson SJ,, Anderson AB,, Grissom JE,, Laux DC,, Cohen PS,, Conway T . 2004. Carbon nutrition of Escherichia coli in the mouse intestine. Proc Natl Acad Sci USA 101 : 7427 7432.[PubMed] [CrossRef]
87. Vimr ER,, Kalivoda KA,, Deszo EL,, Steenbergen SM . 2004. Diversity of microbial sialic acid metabolism. Microbiol Mol Biol Rev 68 : 132 153.[PubMed] [CrossRef]
88. Fabich AJ,, Jones SA,, Chowdhury FZ,, Cernosek A,, Anderson A,, Smalley D,, McHargue JW,, Hightower GA,, Smith JT,, Autieri SM,, Leatham MP,, Lins JJ,, Allen RL,, Laux DC,, Cohen PS,, Conway T . 2008. Comparison of carbon nutrition for pathogenic and commensal Escherichia coli strains in the mouse intestine. Infect Immun 76 : 1143 1152.[PubMed] [CrossRef]
89. Bertin Y,, Chaucheyras-Durand F,, Robbe-Masselot C,, Durand A,, de la Foye A,, Harel J,, Cohen PS,, Conway T,, Forano E,, Martin C . 2013. Carbohydrate utilization by enterohaemorrhagic Escherichia coli O157:H7 in bovine intestinal content. Environ Microbiol 15 : 610 622.[PubMed] [CrossRef]
90. Polzin S,, Huber C,, Eylert E,, Elsenhans I,, Eisenreich W,, Schmidt H . 2013. Growth media simulating ileal and colonic environments affect the intracellular proteome and carbon fluxes of enterohemorrhagic Escherichia coli O157:H7 strain EDL933. Appl Environ Microbiol 79 : 3703 3715.[PubMed] [CrossRef]
91. Steenbergen SM,, Jirik JL,, Vimr ER . 2009. YjhS (NanS) is required for Escherichia coli to grow on 9-O-acetylated N-acetylneuraminic acid. J Bacteriol 191 : 7134 7139.[PubMed] [CrossRef]
92. 2013. Incidence and trends of infection with pathogens transmitted commonly through food — foodborne diseases active surveillance network, 10 U.S. sites, 1996–2012. Morb Mortal Wkly Rep 62: 283287.[PubMed]
93. Coburn B,, Grassl GA,, Finlay BB . 2007. Salmonella, the host and disease: a brief review. Immunol Cell Biol 85 : 112 118.[PubMed] [CrossRef]
94. Crennell SJ,, Garman EF,, Philippon C,, Vasella A,, Laver WG,, Vimr ER,, Taylor GL . 1996. The structures of Salmonella typhimurium LT2 neuraminidase and its complexes with three inhibitors at high resolution. J Mol Biol 259 : 264 280.[PubMed] [CrossRef]
95. Hoyer LL,, Roggentin P,, Schauer R,, Vimr ER . 1991. Purification and properties of cloned Salmonella typhimurium LT2 sialidase with virus-typical kinetic preference for sialyl alpha 2—3 linkages. J Biochem 110 : 462 467.[PubMed]
96. Hoyer LL,, Hamilton AC,, Steenbergen SM,, Vimr ER . 1992. Cloning, sequencing and distribution of the Salmonella typhimurium LT2 sialidase gene, nanH, provides evidence for interspecies gene transfer. Mol Microbiol 6 : 873 884.[PubMed] [CrossRef]
97. Sakarya S,, Gokturk C,, Ozturk T,, Ertugrul MB . 2010. Sialic acid is required for nonspecific adherence of Salmonella enterica ssp. enterica serovar Typhi on Caco-2 cells. FEMS Immunol Med Microbiol 58 : 330 335.[PubMed]
98. Perkins TT,, Davies MR,, Klemm EJ,, Rowley G,, Wileman T,, James K,, Keane T,, Maskell D,, Hinton JC,, Dougan G,, Kingsley RA . 2013. ChIP-seq and transcriptome analysis of the OmpR regulon of Salmonella enterica serovars Typhi and Typhimurium reveals accessory genes implicated in host colonization. Mol Microbiol 87 : 526 538.[PubMed] [CrossRef]
99. Ng KM,, Ferreyra JA,, Higginbottom SK,, Lynch JB,, Kashyap PC,, Gopinath S,, Naidu N,, Choudhury B,, Weimer BC,, Monack DM,, Sonnenburg JL . 2013. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502 : 96 99.[PubMed] [CrossRef]
100. Chowdhury N,, Norris J,, McAlister E,, Lau SY,, Thomas GH,, Boyd EF . 2012. The VC1777–VC1779 proteins are members of a sialic acid-specific subfamily of TRAP transporters (SiaPQM) and constitute the sole route of sialic acid uptake in the human pathogen Vibrio cholerae . Microbiology 158 : 2158 2167.[PubMed] [CrossRef]
101. Mulligan C,, Leech AP,, Kelly DJ,, Thomas GH . 2012. The membrane proteins SiaQ and SiaM form an essential stoichiometric complex in the sialic acid tripartite ATP-independent periplasmic (TRAP) transporter SiaPQM (VC1777–1779) from Vibrio cholerae . J Biol Chem 287 : 3598 3608.[PubMed] [CrossRef]
102. Sharma SK,, Moe TS,, Srivastava R,, Chandra D,, Srivastava BS . 2011. Functional characterization of VC1929 of Vibrio cholerae El Tor: role in mannose-sensitive haemagglutination, virulence and utilization of sialic acid. Microbiology 157 : 3180 3186.[PubMed] [CrossRef]
103. Thomas GH,, Boyd EF . 2011. On sialic acid transport and utilization by Vibrio cholerae . Microbiology 157 : 3253 3254; discussion 3254–3255.[PubMed] [CrossRef]
104. Jermyn WS,, Boyd EF . 2002. Characterization of a novel Vibrio pathogenicity island (VPI-2) encoding neuraminidase (nanH) among toxigenic Vibrio cholerae isolates. Microbiology 148 : 3681 3693.[PubMed]
105. Holmgren J,, Lonnroth I,, Mansson J,, Svennerholm L . 1975. Interaction of cholera toxin and membrane GM1 ganglioside of small intestine. Proc Natl Acad Sci USA 72 : 2520 2524.[PubMed] [CrossRef]
106. Moustafa I,, Connaris H,, Taylor M,, Zaitsev V,, Wilson JC,, Kiefel MJ,, Von Itzstein M,, Taylor G . 2004. Sialic acid recognition by Vibrio cholerae neuraminidase. J Biol Chem 279 : 40819 40826.[PubMed] [CrossRef]
107. Galen JE,, Ketley JM,, Fasano A,, Richardson SH,, Wasserman SS,, Kaper JB . 1992. Role of Vibrio cholerae neuraminidase in the function of cholera toxin. Infect Immun 60 : 406 415.[PubMed]
108. Holmgren J,, Lonnroth I,, Svennerholm L . 1973. Fixation and inactivation of cholera toxin by GM1 ganglioside. Scand J Infect Dis 5 : 77 78.[PubMed] [CrossRef]
109. Murphy RA,, Boyd EF . 2008. Three pathogenicity islands of Vibrio cholerae can excise from the chromosome and form circular intermediates. J Bacteriol 190 : 636 647.[PubMed] [CrossRef]
110. Boyd EF,, Chowdhury N,, McDonald ND,, Lubin JB . 2014. Host sialic acids are an important bacterial nutrient source that increase fitness of intestinal pathogens in vivo , 114th General Meeting of the American Society for Microbiology. ASM Abstracts.
111. Lubin JB,, Kingston JJ,, Chowdhury N,, Boyd EF . 2012. Sialic acid catabolism and transport gene clusters are lineage specific in Vibrio vulnificus . Appl Environ Microbiol 78 : 3407 3415.[PubMed] [CrossRef]
112. Lewis AL,, Lubin JB,, Argade S,, Naidu N,, Choudhury B,, Boyd EF . 2011. Genomic and metabolic profiling of nonulosonic acids in Vibrionaceae reveal biochemical phenotypes of allelic divergence in Vibrio vulnificus . Appl Environ Microbiol 77 : 5782 5793.[PubMed] [CrossRef]
113. Jeong HG,, Oh MH,, Kim BS,, Lee MY,, Han HJ,, Choi SH . 2009. The capability of catabolic utilization of N-acetylneuraminic acid, a sialic acid, is essential for Vibrio vulnificus pathogenesis. Infect Immun 77 : 3209 3217.[PubMed] [CrossRef]
114. Hwang J,, Kim BS,, Jang SY,, Lim JG,, You DJ,, Jung HS,, Oh TK,, Lee JO,, Choi SH,, Kim MH . 2013. Structural insights into the regulation of sialic acid catabolism by the Vibrio vulnificus transcriptional repressor NanR. Proc Natl Acad Sci USA 110 : E2829 E2837.[PubMed] [CrossRef]
115. Kim BS,, Hwang J,, Kim MH,, Choi SH . 2011. Cooperative regulation of the Vibrio vulnificus nan gene cluster by NanR protein, cAMP receptor protein, and N-acetylmannosamine 6-phosphate. J Biol Chem 286 : 40889 40899.[PubMed] [CrossRef]
116. Fraser AG,, Collee JG . 1975. The production of neuraminidase by food poisoning strains of Clostridium welchii ( C. perfringens). J Med Microbiol 8 : 251 263.[CrossRef]
117. Nees S,, Schauer R,, Mayer F . 1976. Purification and characterization of N-acetylneuraminate lyase from Clostridium perfringens . Hoppe Seylers Z Physiol Chem 357 : 839 853.[PubMed] [CrossRef]
118. Walters DM,, Stirewalt VL,, Melville SB . 1999. Cloning, sequence, and transcriptional regulation of the operon encoding a putative N-acetylmannosamine-6-phosphate epimerase (nanE) and sialic acid lyase (nanA) in Clostridium perfringens . J Bacteriol 181 : 4526 4532.[PubMed]
119. Borriello SP . 1995. Clostridial disease of the gut. Clin Infect Dis 20( Suppl 2) : S242 S250.[PubMed] [CrossRef]
120. Li J,, Sayeed S,, Robertson S,, Chen J,, McClane BA . 2011. Sialidases affect the host cell adherence and epsilon toxin-induced cytotoxicity of Clostridium perfringens type D strain CN3718. PLoS Pathog 7 : e1002429. [PubMed] [CrossRef]
121. Hooper LV,, Midtvedt T,, Gordon JI . 2002. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 22 : 283 307.[PubMed] [CrossRef]
122. Ward RE,, Ninonuevo M,, Mills DA,, Lebrilla CB,, German JB . 2007. In vitro fermentability of human milk oligosaccharides by several strains of bifidobacteria. Mol Nutr Food Res 51 : 1398 1405.[PubMed] [CrossRef]
123. Sela DA,, Mills DA . 2010. Nursing our microbiota: molecular linkages between bifidobacteria and milk oligosaccharides. Trends Microbiol 18 : 298 307.[PubMed] [CrossRef]
124. Gruteser N,, Marin K,, Krämer R,, Thomas GH . 2012. Sialic acid utilization by the soil bacterium Corynebacterium glutamicum . FEMS Microbiol Lett 336 : 131 138.[PubMed] [CrossRef]
125. Joseph S,, Desai P,, Ji Y,, Cummings CA,, Shih R,, Degoricija L,, Rico A,, Brzoska P,, Hamby SE,, Masood N,, Hariri S,, Sonbol H,, Chuzhanova N,, McClelland M,, Furtado MR,, Forsythe SJ . 2012. Comparative analysis of genome sequences covering the seven cronobacter species. PLoS One 7 : e49455. [PubMed] [CrossRef]
126. Joseph S,, Hariri S,, Masood N,, Forsythe S . 2013. Sialic acid utilization by Cronobacter sakazakii . Microb Inform Exp 3 : 3. [PubMed] [CrossRef]
127. Sanchez-Carron G,, Garcia-Garcia MI,, Lopez-Rodriguez AB,, Jimenez-Garcia S,, Sola-Carvajal A,, Garcia-Carmona F,, Sanchez-Ferrer A . 2011. Molecular characterization of a novel N-acetylneuraminate lyase from Lactobacillus plantarum WCFS1. Appl Environ Microbiol 77 : 2471 2478.[PubMed] [CrossRef]
128. May M,, Brown DR . 2008. Genetic variation in sialidase and linkage to N-acetylneuraminate catabolism in Mycoplasma synoviae . Microb Pathog 45 : 38 44.[PubMed] [CrossRef]
129. Steenbergen SM,, Lichtensteiger CA,, Caughlan R,, Garfinkle J,, Fuller TE,, Vimr ER . 2005. Sialic Acid metabolism and systemic pasteurellosis. Infect Immun 73 : 1284 1294.[PubMed] [CrossRef]
130. Crost EH,, Tailford LE,, Le Gall G,, Fons M,, Henrissat B,, Juge N . 2013. Utilisation of Mucin Glycans by the Human Gut Symbiont Ruminococcus gnavus Is Strain-Dependent. PLoS One 8 : e76341. [PubMed] [CrossRef]
131. Olson ME,, King JM,, Yahr TL,, Horswill AR . 2013. Sialic acid catabolism in Staphylococcus aureus . J Bacteriol 195 : 1779 1788.[PubMed] [CrossRef]
132. Marion C,, Burnaugh AM,, Woodiga SA,, King SJ . 2011. Sialic acid transport contributes to pneumococcal colonization. Infect Immun 79 : 1262 1269.[PubMed] [CrossRef]
133. Burnaugh AM,, Frantz LJ,, King SJ . 2008. Growth of Streptococcus pneumoniae on human glycoconjugates is dependent upon the sequential activity of bacterial exoglycosidases. J Bacteriol 190 : 221 230.[PubMed] [CrossRef]


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Bacterial species in which sialic acid catabolism was experimentally examined

Citation: Haines-menges B, Whitaker W, Lubin J, Boyd E. 2015. Host Sialic Acids: A Delicacy for the Pathogen with Discerning Taste, p 321-342. In Conway T, Cohen P (ed), Metabolism and Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MBP-0005-2014

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