Degradation, foraging, and depletion of mucus sialoglycans by the vagina-adapted actinobacterium Gardnerella vaginalis

Journal of Biological Chemistry

Volumn 288, Issue 17, 2013, Pages 12067-12079

  Lewis, Warren G ^a   Robinson, Lloyd S ^a   Gilbert, Nicole M ^a   Perry, Justin C ^a   Lewis, Amanda L ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL SPECIES; CLINICAL SETTINGS; EXTRACELLULAR; HEALTH OUTCOMES; MUCUS BARRIER; N-ACETYLNEURAMINIC ACID; N-GLYCOLYLNEURAMINIC ACID; SIALIDASE ACTIVITIES;

BACILLI; CARBOXYLIC ACIDS; ENZYME ACTIVITY;

BODY FLUIDS;

FRUCTOSE BISPHOSPHATE ALDOLASE; LYASE; N ACETYLNEURAMINIC ACID; N GLYCOLOYLNEURAMINIC ACID; SIALIC ACID; SIALIDASE; SIALOGLYCOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; FEMALE; FORAGING; GARDNERELLA INFECTION; GARDNERELLA VAGINALIS; HUMAN; HUMAN TISSUE; HYDROLYSIS; IN VITRO STUDY; IN VIVO STUDY; LACTOBACILLUS; MOUSE; MUCUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; VAGINA FLORA;

ANIMALS; BACTERIAL PROTEINS; DISEASE MODELS, ANIMAL; FEMALE; GARDNERELLA VAGINALIS; HUMANS; MICE; MUCOUS MEMBRANE; N-ACETYLNEURAMINIC ACID; NEURAMINIDASE; PROTEOGLYCANS; VAGINOSIS, BACTERIAL;

BACTERIA (MICROORGANISMS); GARDNERELLA VAGINALIS; MURINAE;

EID: 84876916642     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.453654     Document Type: Article

References (95)

1. Allsworth, J. E., and Peipert, J. F. (2007) Prevalence of bacterial vaginosis. 2001-2004 National Health and Nutrition Examination Survey data. Obstet. Gynecol. 109, 114-120
2. Gelber, S. E., Aguilar, J. L., Lewis, K. L., and Ratner, A. J. (2008) Functional and phylogenetic characterization of Vaginolysin, the human-specific cytolysin from Gardnerella vaginalis. J. Bacteriol. 190, 3896-3903
3. Donders, G. G., Bosmans, E., Dekeersmaecker, A., Vereecken, A., Van Bulck, B., and Spitz, B. (2000) Pathogenesis of abnormal vaginal bacterial flora. Am. J. Obstet. Gynecol. 182, 872-878
4. Hay, P. E., Lamont, R. F., Taylor-Robinson, D., Morgan, D. J., Ison, C., and Pearson, J. (1994) Abnormal bacterial colonisation of the genital tract and subsequent preterm delivery and late miscarriage. BMJ 308, 295-298
5. Svare, J. A., Schmidt, H., Hansen, B. B., and Lose, G. (2006) Bacterial vaginosis in a cohort of Danish pregnant women. Prevalence and relationship with preterm delivery, low birth weight and perinatal infections. BJOG 113, 1419-1425
6. McGregor, J. A., French, J. I., Jones, W., Milligan, K., McKinney, P. J., Patterson, E., and Parker, R. (1994) Bacterial vaginosis is associated with prematurity and vaginal fluid mucinase and sialidase. Results of a controlled trial of topical clindamycin cream. Am. J. Obstet. Gynecol. 170, 1048-1059; discussion 1059-1060
7. Holst, E., Goffeng, A. R., and Andersch, B. (1994) Bacterial vaginosis and vaginal microorganisms in idiopathic premature labor and association with pregnancy outcome. J. Clin. Microbiol. 32, 176-186
8. Hillier, S. L., Nugent, R. P., Eschenbach, D. A., Krohn, M. A., Gibbs, R. S., Martin, D. H., Cotch, M. F., Edelman, R., Pastorek, J. G., 2nd, and Rao, A. V. (1995) Association between bacterial vaginosis and preterm delivery of a low-birth weight infant. The Vaginal Infections and Prematurity Study Group. N. Engl. J. Med. 333, 1737-1742
9. Hillier, S. L., Martius, J., Krohn, M., Kiviat, N., Holmes, K. K., and Eschenbach, D. A. (1988) A case-control study of chorioamnionic infection and histologic chorioamnionitis in prematurity. N. Engl. J. Med. 319, 972-978
10. Hendler, I., Andrews, W. W., Carey, C. J., Klebanoff, M. A., Noble, W. D., Sibai, B. M., Hillier, S. L., Dudley, D., Ernest, J. M., Leveno, K. J., Wapner, R., Iams, J. D., Varner, M., Moawad, A., Miodovnik, M., O'Sullivan, M. J., and Van Dorsten, P. J. (2007) The relationship between resolution of asymptomatic bacterial vaginosis and spontaneous preterm birth in fetal fibronectin-positive women. Am. J. Obstet. Gynecol. 197, 488.e1-5
11. Hitti, J., Hillier, S. L., Agnew, K. J., Krohn, M. A., Reisner, D. P., and Eschenbach, D. A. (2001) Vaginal indicators of amniotic fluid infection in preterm labor. Obstet. Gynecol. 97, 211-219
12. Rezeberga, D., Lazdane, G., Kroica, J., Sokolova, L., and Donders, G. G. (2008) Placental histological inflammation and reproductive tract infections in a low risk pregnant population in Latvia. Acta Obstet. Gynecol. Scand. 87, 360-365
13. Silver, H. M., Sperling, R. S., St Clair, P. J., and Gibbs, R. S. (1989) Evidence relating bacterial vaginosis to intraamniotic infection. Am. J. Obstet. Gynecol. 161, 808-812
14. Zhang, X., Xu, X., Li, J., Li, N., Yan, T., and Ju, X. (2002) Relationship between vaginal sialidase bacteria vaginosis and chorioammionitis. Zhonghua fu chan ke za zhi 37, 588-590
15. Brotman, R. M., Klebanoff, M. A., Nansel, T. R., Yu, K. F., Andrews, W. W., Zhang, J., and Schwebke, J. R. (2010) Bacterial vaginosis assessed by gram stain and diminished colonization resistance to incident gonococcal, chlamydial, and trichomonal genital infection. J. Infect. Dis. 202, 1907-1915
16. Cohen, C. R., Lingappa, J. R., Baeten, J. M., Ngayo, M. O., Spiegel, C. A., Hong, T., Donnell, D., Celum, C., Kapiga, S., Delany, S., and Bukusi, E. A. (2012) Bacterial vaginosis associated with increased risk of female-to-male HIV-1 transmission. A prospective cohort analysis among African couples. PLoS Med. 9, e1001251
17. Watts, D. H., Krohn, M. A., Hillier, S. L., and Eschenbach, D. A. (1990) Bacterial vaginosis as a risk factor for post-cesarean endometritis. Obstet. Gynecol. 75, 52-58
18. Gajer, P., Brotman, R. M., Bai, G., Sakamoto, J., Schutte, U. M., Zhong, X., Koenig, S. S., Fu, L., Ma, Z. S., Zhou, X., Abdo, Z., Forney, L. J., and Ravel, J. (2012) Temporal dynamics of the human vaginal microbiota. Sci. Transl. Med. 4, 132ra152
19. Fredricks, D. N. (2011) Molecular methods to describe the spectrum and dynamics of the vaginal microbiota. Anaerobe 17, 191-195
20. Ravel, J., Gajer, P., Abdo, Z., Schneider, G. M., Koenig, S. S., McCulle, S. L., Karlebach, S., Gorle, R., Russell, J., Tacket, C. O., Brotman, R. M., Davis, C. C., Ault, K., Peralta, L., and Forney, L. J. (2011) Vaginal microbiome of reproductive-age women. Proc. Natl. Acad. Sci. U. S. A. 108, 4680-4687
21. Srinivasan, S., Liu, C., Mitchell, C. M., Fiedler, T. L., Thomas, K. K., Agnew, K. J., Marrazzo, J. M., and Fredricks, D. N. (2010) Temporal variability of human vaginal bacteria and relationship with bacterial vaginosis. PLoS One 5, e10197
22. Hillier, S. L., Krohn, M. A., Rabe, L. K., Klebanoff, S. J., and Eschenbach, D. A. (1993) The normal vaginal flora, H2O2-producing lactobacilli, and bacterial vaginosis in pregnant women. Clin. Infect. Dis. 16, S273-281
23. Krohn, M. A., Hillier, S. L., and Eschenbach, D. A. (1989) Comparison of methods for diagnosing bacterial vaginosis among pregnant women. J. Clin. Microbiol. 27, 1266-1271
24. Amsel, R., Totten, P. A., Spiegel, C. A., Chen, K. C., Eschenbach, D., and Holmes, K. K. (1983) Nonspecific vaginitis. Diagnostic criteria and microbial and epidemiologic associations. Am. J. Med. 74, 14-22
25. Eschenbach, D. A., Hillier, S., Critchlow, C., Stevens, C., DeRouen, T., and Holmes, K. K. (1988) Diagnosis and clinical manifestations of bacterial vaginosis. Am. J. Obstet. Gynecol. 158, 819-828
26. Srinivasan, S., Hoffman, N. G., Morgan, M. T., Matsen, F. A., Fiedler, T. L., Hall, R. W., Ross, F. J., McCoy, C. O., Bumgarner, R., Marrazzo, J. M., and Fredricks, D. N. (2012) Bacterial communities in women with bacterial vaginosis. High resolution phylogenetic analyses reveal relationships of microbiota to clinical criteria. PloS One 7, e37818
27. Lewis, A. L., and Lewis, W. G. (2012) Host sialoglycans and bacterial sialidases. A mucosal perspective. Cell. Microbiol. 14, 1174-1182
28. Slomiany, B. L., Murty, V. L., Piotrowski, J., and Slomiany, A. (1996) Salivary mucins in oral mucosal defense. Gen. Pharmacol. 27, 761-771
29. Moran, A. P., Gupta, A., and Joshi, L. (2011) Sweet-talk. Role of host glycosylation in bacterial pathogenesis of the gastrointestinal tract. Gut 60, 1412-1425
30. Anthony, R. M., and Ravetch, J. V. (2010) A novel role for the IgG Fc glycan. The anti-inflammatory activity of sialylated IgG Fcs. J. Clin. Immunol. 30, S9-14
31. Yoo, E. M., and Morrison, S. L. (2005) IgA. An immune glycoprotein. Clin. Immunol. 116, 3-10
32. Briselden, A. M., Moncla, B. J., Stevens, C. E., and Hillier, S. L. (1992) Sialidases (neuraminidases) in bacterial vaginosis and bacterial vaginosis-associated microflora. J. Clin. Microbiol. 30, 663-666
33. Howe, L., Wiggins, R., Soothill, P. W., Millar, M. R., Horner, P. J., and Corfield, A. P. (1999) Mucinase and sialidase activity of the vaginal microflora. Implications for the pathogenesis of preterm labour. Int. J. STD AIDS 10, 442-447
34. Olmsted, S. S., Meyn, L. A., Rohan, L. C., and Hillier, S. L. (2003) Glycosidase and proteinase activity of anaerobic Gram-negative bacteria isolated from women with bacterial vaginosis. Sex. Transm. Dis. 30, 257-261
35. Smayevsky, J., Canigia, L. F., Lanza, A., and Bianchini, H. (2001) Vaginal microflora associated with bacterial vaginosis in nonpregnant women. Reliability of sialidase detection. Infect. Dis. Obstet. Gynecol. 9, 17-22
36. +-D-N-acetylneuraminic acid in a novel spot test. To identify sialidase activity in vaginal swabs from women with bacterial vaginosis. J. Clin. Microbiol. 38, 3096-3097
37. Sumeksri, P., Koprasert, C., and Panichkul, S. (2005) BVBLUE test for diagnosis of bacterial vaginosis in pregnant women attending antenatal care at Phramongkutklao Hospital. J. Med. Assoc. Thai. 88, S7-13
38. Myziuk, L., Romanowski, B., and Johnson, S. C. (2003) BVBlue test for diagnosis of bacterial vaginosis. J. Clin. Microbiol. 41, 1925-1928
39. Cauci, S., and Culhane, J. F. (2011) High sialidase levels increase preterm birth risk among women who are bacterial vaginosis-positive in early gestation. Am. J. Obstet. Gynecol. 204, 142.e1-9
40. Cauci, S., McGregor, J., Thorsen, P., Grove, J., and Guaschino, S. (2005) Combination of vaginal pH with vaginal sialidase and prolidase activities for prediction of low birth weight and preterm birth. Am. J. Obstet. Gynecol. 192, 489-496
41. Bradshaw, C. S., Morton, A. N., Garland, S. M., Horvath, L. B., Kuzevska, I., and Fairley, C. K. (2005) Evaluation of a point-of-care test, BVBlue, and clinical and laboratory criteria for diagnosis of bacterial vaginosis. J. Clin. Microbiol. 43, 1304-1308
42. Moncla, B. J., Braham, P., and Hillier, S. L. (1990) Sialidase (neuraminidase) activity among Gram-negative anaerobic and capnophilic bacteria. J. Clin. Microbiol. 28, 422-425
43. von Nicolai, H., Hammann, R., Salehnia, S., and Zilliken, F. (1984) A newly discovered sialidase from Gardnerella vaginalis. Zentralbl. Bakteriol. Mikrobiol. Hyg. A 258, 20-26
44. Oakley, B. B., Fiedler, T. L., Marrazzo, J. M., and Fredricks, D. N. (2008) Diversity of human vaginal bacterial communities and associations with clinically defined bacterial vaginosis. Appl. Environ. Microbiol. 74, 4898-4909
45. Srinivasan, S., Liu, C., Mitchell, C. M., Fiedler, T. L., Thomas, K. K., Agnew, K. J., Marrazzo, J. M., and Fredricks, D. N. (2010) Temporal variability of human vaginal bacteria and relationship with bacterial vaginosis. PLoS One 5, e10197
46. Gardner, H. L., and Dukes, C. D. (1954) New eitologic agent in bacterial vaginitis. Science 120, 853
47. Briselden, A. M., and Hillier, S. L. (1990) Longitudinal study of the biotypes of Gardnerella vaginalis. J. Clin. Microbiol. 28, 2761-2764
48. Harwich, M. D., Jr., Alves, J. M., Buck, G. A., Strauss, J. F., 3rd, Patterson, J. L., Oki, A. T., Girerd, P. H., and Jefferson, K. K. (2010) Drawing the line between commensal and pathogenic Gardnerella vaginalis through genome analysis and virulence studies. BMC Genomics 11, 375
49. Patterson, J. L., Stull-Lane, A., Girerd, P. H., and Jefferson, K. K. (2010) Analysis of adherence, biofilm formation and cytotoxicity suggests a greater virulence potential of Gardnerella vaginalis relative to other bacterialvaginosis-associated anaerobes. Microbiology 156, 392-399
50. Fredricks, D. N., Fiedler, T. L., Thomas, K. K., Oakley, B. B., and Marrazzo, J. M. (2007) Targeted PCR for detection of vaginal bacteria associated with bacterial vaginosis. J. Clin. Microbiol. 45, 3270-3276
51. Marrs, C. N., Knobel, S. M., Zhu, W. Q., Sweet, S. D., Chaudhry, A. R., and Alcendor, D. J. (2012) Evidence for Gardnerella vaginalis uptake and internalization by squamous vaginal epithelial cells. Implications for the pathogenesis of bacterial vaginosis. Microbes Infect. 14, 500-508
52. Lewis, W. G., Robinson, L. S., Perry, J., Bick, J. L., Peipert, J. F., Allsworth, J. E., and Lewis, A. L. (2012) Hydrolysis of secreted sialoglycoprotein immunoglobulin A (IgA) in ex vivo and biochemical models of bacterial vaginosis. J. Biol. Chem. 287, 2079-2089
53. Lewis, A. L., Cao, H., Patel, S. K., Diaz, S., Ryan, W., Carlin, A. F., Thon, V., Lewis, W. G., Varki, A., Chen, X., and Nizet, V. (2007) NeuA sialic acid O-acetylesterase activity modulates O-acetylation of capsular polysaccharide in group B Streptococcus. J. Biol. Chem. 282, 27562-27571
54. Lewis, A. L., Desa, N., Hansen, E. E., Knirel, Y. A., Gordon, J. I., Gagneux, P., Nizet, V., and Varki, A. (2009) Innovations in host and microbial sialic acid biosynthesis revealed by phylogenomic prediction of nonulosonic acid structure. Proc. Natl. Acad. Sci. U. S. A. 106, 13552-13557
55. Lewis, A. L., Lubin, J. B., Argade, S., Naidu, N., Choudhury, B., and Boyd, E. F. (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
56. Lewis, A. L., Nizet, V., and Varki, A. (2004) Discovery and characterization of sialic acid O-acetylation in group B Streptococcus. Proc. Natl. Acad. Sci. U. S. A. 101, 11123-11128
57. Weiman, S., Dahesh, S., Carlin, A. F., Varki, A., Nizet, V., and Lewis, A. L. (2009) Genetic and biochemical modulation of sialic acid O-acetylation on group B Streptococcus. Phenotypic and functional impact. Glycobiology 19, 1204-1213
58. Secura, G. M., Allsworth, J. E., Madden, T., Mullersman, J. L., and Peipert, J. F. (2010) The Contraceptive CHOICE Project. Reducing barriers to long-acting reversible contraception. Am. J. Obstet. Gynecol. 203, 115.e1-7
59. Nugent, R. P., Krohn, M. A., and Hillier, S. L. (1991) Reliability of diagnosing bacterial vaginosis is improved by a standardized method of Gram stain interpretation. J. Clin. Microbiol. 29, 297-301
60. Singh, P. K., and Hollingsworth, M. A. (2006) Cell surface-associated mucins in signal transduction. Trends Cell Biol. 16, 467-476
61. Hattrup, C. L., and Gendler, S. J. (2008) Structure and function of the cell surface (tethered) mucins. Annu. Rev. Physiol. 70, 431-457
62. McGuckin, M. A., Lindén, S. K., Sutton, P., and Florin, T. H. (2011) Mucin dynamics and enteric pathogens. Nat. Rev. Microbiol. 9, 265-278
63. Chou, H. H., Hayakawa, T., Diaz, S., Krings, M., Indriati, E., Leakey, M., Paabo, S., Satta, Y., Takahata, N., and Varki, A. (2002) Inactivation of CMP-N-acetylneuraminic acid hydroxylase occurred prior to brain expansion during human evolution. Proc. Natl. Acad. Sci. U. S. A. 99, 11736-11741
64. Varki, A. (2001) Loss of N-glycolylneuraminic acid in humans. Mechanisms, consequences, and implications for hominid evolution. Am. J. Phys. Anthrop. 33, 54-69
65. Chou, H. H., Takematsu, H., Diaz, S., Iber, J., Nickerson, E., Wright, K. L., Muchmore, E. A., Nelson, D. L., Warren, S. T., and Varki, A. (1998) A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence. Proc. Natl. Acad. Sci. U. S. A. 95, 11751-11756
66. Vimr, E. R., Kalivoda, K. A., Deszo, E. L., and Steenbergen, S. M. (2004) Diversity of microbial sialic acid metabolism. Microbiol. Mol. Biol. Rev. 68, 132-153
67. Trinh, H. T., Lee, I. A., Hyun, Y. J., and Kim, D. H. (2011) Artemisia princeps Pamp. Essential oil and its constituents eucalyptol and α-terpineol ameliorate bacterial vaginosis and vulvovaginal candidiasis in mice by inhibiting bacterial growth and NF-κB activation. Planta Med. 77, 1996-2002
68. Joo, H. M., Hyun, Y. J., Myoung, K. S., Ahn, Y. T., Lee, J. H., Huh, C. S., Han, M. J., and Kim, D. H. (2011) Lactobacillus johnsonii HY7042 ameliorates Gardnerella vaginalis-induced vaginosis by killing Gardnerella vaginalis and inhibiting NF-κB activation. Int. Immunopharmacol. 11, 1758-1765
69. Swidsinski, A., Loening-Baucke, V., Verstraelen, H., Osowska, S., and Doerffel, Y. (2008) Biostructure of fecal microbiota in healthy subjects and patients with chronic idiopathic diarrhea. Gastroenterology 135, 568-579
70. Xavier, R. J., and Podolsky, D. K. (2007) Unravelling the pathogenesis of inflammatory bowel disease. Nature 448, 427-434
71. Tamboli, C. P., Neut, C., Desreumaux, P., and Colombel, J. F. (2004) Dysbiosis in inflammatory bowel disease. Gut 53, 1-4
72. Lubin, J. B., Kingston, J. J., Chowdhury, N., and Boyd, E. F. (2012) Sialic acid catabolism and transport gene clusters are lineage specific in Vibrio vulnificus. Appl. Environ. Microbiol. 78, 3407-3415
73. Mulligan, C., Leech, A. P., Kelly, D. J., and Thomas, G. H. (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
74. Thomas, G. H., and Boyd, E. F. (2011) On sialic acid transport and utilization by Vibrio cholerae. Microbiology 157, 3253-3254; discussion 3254-3255
75. Mulligan, C., Fischer, M., and Thomas, G. H. (2011) Tripartite ATP-independent periplasmic (TRAP) transporters in bacteria and archaea. FEMS Microbiol. Rev. 35, 68-86
76. Jenkins, G. A., Figueira, M., Kumar, G. A., Sweetman, W. A., Makepeace, K., Pelton, S. I., Moxon, R., and Hood, D. W. (2010) Sialic acid mediated transcriptional modulation of a highly conserved sialometabolism gene cluster in Haemophilus influenzae and its effect on virulence. BMC Microbiol. 10, 48
77. Severi, E., Randle, G., Kivlin, P., Whitfield, K., Young, R., Moxon, R., Kelly, D., Hood, D., and Thomas, G. H. (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
78. Pezzicoli, A., Ruggiero, P., Amerighi, F., Telford, J. L., and Soriani, M. (2012) Exogenous sialic acid transport contributes to group B streptococcus infection of mucosal surfaces. J. Infect. Dis. 206, 924-931
79. Almagro-Moreno, S., and Boyd, E. F. (2009) Sialic acid catabolism confers a competitive advantage to pathogenic Vibrio cholerae in the mouse intestine. Infect. Immun. 77, 3807-3816
80. Marion, C., Burnaugh, A. M., Woodiga, S. A., and King, S. J. (2011) Sialic acid transport contributes to pneumococcal colonization. Infect. Immun. 79, 1262-1269
81. Roy, S., Honma, K., Douglas, C. W., Sharma, A., and Stafford, G. P. (2011) Role of sialidase in glycoprotein utilization by Tannerella forsythia. Microbiology 157, 3195-3202
82. Roy, S., Douglas, C. W., and Stafford, G. P. (2010) A novel sialic acid utilization and uptake system in the periodontal pathogen Tannerella forsythia. J. Bacteriol. 192, 2285-2293
83. +1-acid glycoprotein mediates growth of Streptococcus oralis. Glycobiology 9, 469-479
84. Rafay, A. M., Homer, K. A., and Beighton, D. (1996) Effect of mucin and glucose on proteolytic and glycosidic activities of Streptococcus oralis. J. Med. Microbiol. 44, 409-417
85. Homer, K. A., Kelley, S., Hawkes, J., Beighton, D., and Grootveld, M. C. (1996) Metabolism of glycoprotein-derived sialic acid and N-acetylglucosamine by Streptococcus oralis. Microbiology 142, 1221-1230
86. Marcobal, A., Barboza, M., Sonnenburg, E. D., Pudlo, N., Martens, E. C., Desai, P., Lebrilla, C. B., Weimer, B. C., Mills, D. A., German, J. B., and Sonnenburg, J. L. (2011) Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host Microbe 10, 507-514
87. Sela, D. A., Chapman, J., Adeuya, A., Kim, J. H., Chen, F., Whitehead, T. R., Lapidus, A., Rokhsar, D. S., Lebrilla, C. B., German, J. B., Price, N. P., Richardson, P. M., and Mills, D. A. (2008) The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc. Natl. Acad. Sci. U. S. A. 105, 18964-18969
88. Sela, D. A., Li, Y., Lerno, L., Wu, S., Marcobal, A. M., German, J. B., Chen, X., Lebrilla, C. B., and Mills, D. A. (2011) An infant-associated bacterial commensal utilizes breast milk sialyloligosaccharides. J. Biol. Chem. 286, 11909-11918
89. Santiago, G. L., Deschaght, P., El Aila, N., Kiama, T. N., Verstraelen, H., Jefferson, K. K., Temmerman, M., and Vaneechoutte, M. (2011) Gardnerella vaginalis comprises three distinct genotypes of which only two produce sialidase. Am. J. Obstet. Gynecol. 204, 450
90. Pleckaityte, M., Janulaitiene, M., Lasickiene, R., and Zvirbliene, A. (2012) Genetic and biochemical diversity of Gardnerella vaginalis strains isolated from women with bacterial vaginosis. FEMS Immunol. Med. Microbiol. 65, 69-77
91. Byers, H. L., Homer, K. A., Tarelli, E., and Beighton, D. (1999) N-Acetylneuraminic acid transport by Streptococcus oralis strain AR3. J. Med. Microbiol. 48, 375-381
92. Chowdhury, S., and Mandal, C. (2009) O-Acetylated sialic acids. Multifaceted role in childhood acute lymphoblastic leukemia. Biotechnol. J. 4, 361-374
93. Schauer, R. (2009) Sialic acids as regulators of molecular and cellular interactions. Curr. Opin. Struct. Biol. 19, 507-514
94. Nakayama-Imaohji, H., Ichimura, M., Iwasa, T., Okada, N., Ohnishi, Y., and Kuwahara, T. (2012) Characterization of a gene cluster for sialoglycoconjugate utilization in Bacteroides fragilis. J. Med. Invest. 59, 79-94
95. Hoskins, L. C., and Boulding, E. T. (1981) Mucin degradation in human colon ecosystems. Evidence for the existence and role of bacterial subpopulations producing glycosidases as extracellular enzymes. J. Clin. Investig. 67, 163-172