Hydrolysis of secreted sialoglycoprotein immunoglobulin a (IgA) in ex vivo and biochemical models of bacterial vaginosis

Journal of Biological Chemistry

Volumn 287, Issue 3, 2012, Pages 2079-2089

  Lewis, Warren G ^a   Robinson, Lloyd S ^a   Perry, Justin ^a   Bick, Jennifer L ^a   Peipert, Jeffrey F ^a   Allsworth, Jenifer E ^a   Lewis, Amanda L ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL MODEL; COLLECTIVE ACTION; DATA SUPPORT; DEGLYCOSYLATION; EX-VIVO; GALACTOSIDASES; GLYCOSIDASES; HEALTH OUTCOMES; HEAVY CHAIN; HEXOSAMINIDASE; HYDROLYTIC ACTIVITIES; IMMUNE FUNCTION; PRETERM BIRTH; SIALIC ACIDS; SIALIDASE INHIBITORS; SIALIDASES;

CARBOHYDRATES; CARBOXYLIC ACIDS; HYDROLYSIS;

PROTEOLYSIS;

BETA GALACTOSIDASE; BETA N ACETYLHEXOSAMINIDASE; GALACTOSIDASE; GLYCOSIDASE; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAIN; MANNOSE; PROTEINASE; SIALIC ACID; SIALOGLYCOPROTEIN;

ARTICLE; BIOCHEMISTRY; CONTROLLED STUDY; DEGLYCOSYLATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SUBSTRATE; EX VIVO STUDY; FEMALE; GEL ELECTROPHORESIS; HUMAN; HYDROLYSIS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN GLYCOSYLATION; PROTEIN SECRETION; SIALYLATION; VAGINITIS;

CLINICAL TRIALS AS TOPIC; COHORT STUDIES; FEMALE; HUMANS; MODELS, BIOLOGICAL; MUCOUS MEMBRANE; N-ACETYLNEURAMINIC ACID; NEURAMINIDASE; PROTEOLYSIS; SECRETORY COMPONENT; VAGINOSIS, BACTERIAL;

BACTERIA (MICROORGANISMS);

EID: 84855832123     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.278135     Document Type: Article

References (53)

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 (Pubitemid 46035517)
2. 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
3. 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
4. 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
5. 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
6. 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 (Pubitemid 351317482)
7. 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 (Pubitemid 32126335)
8. Wiesenfeld, H. C., Hillier, S. L., Krohn, M. A., Amortegui, A. J., Heine, R. P., Landers, D. V., and Sweet, R. L. (2002) Lower genital tract infection and endometritis: insight into subclinical pelvic inflammatory disease. Obstet. Gynecol. 100, 456-463 (Pubitemid 35246131)
9. Wiesenfeld, H. C., Hillier, S. L., Krohn, M. A., Landers, D. V., and Sweet, R. L. (2003) Bacterial vaginosis is a strong predictor of Neisseria gonorrhoeae and Chlamydia trachomatis infection. Clin. Infect Dis. 36, 663-668 (Pubitemid 36259574)
10. 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 (Pubitemid 20047932)
11. Donders, G. G., Van Calsteren, K., Bellen, G., Reybrouck, R., Van den Bosch, T., Riphagen, I., and Van Lierde, S. (2009) Predictive value for Preterm birth of abnormal vaginal flora, bacterial vaginosis, and aerobic vaginitis during the first trimester of pregnancy. Br. J. Obstet. Gynaecol. 116, 1315-1324
12. 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 birthweight and perinatal infections. Br. J. Obstet. Gynaecol. 113, 1419-1425 (Pubitemid 44736687)
13. DiGiulio, D. B., Romero, R., Kusanovic, J. P., Gómez, R., Kim, C. J., Seok, K. S., Gotsch, F., Mazaki-Tovi, S., Vaisbuch, E., Sanders, K., Bik, E. M., Chaiworapongsa, T., Oyarzún, E., and Relman, D. A. (2010) Prevalence and diversity of microbes in the amniotic fluid, the fetal inflammatory response, and pregnancy outcome in women with preterm pre-labor rupture of membranes. Am. J. Reprod Immunol. 64, 38-57
14. Larsson, P. G. (1992) Treatment of bacterial vaginosis. Int. J. STD AIDS 3, 239-247
15. Bradshaw, C. S., Morton, A. N., Hocking, J., Garland, S. M., Morris, M. B., Moss, L. M., Horvath, L. B., Kuzevska, I., and Fairley, C. K. (2006) High recurrence rates of bacterial vaginosis over the course of 12 months after oral metronidazole therapy and factors associated with recurrence. J. Infect. Dis. 193, 1478-1486 (Pubitemid 43794575)
16. Carey, J. C., Klebanoff, M. A., Hauth, J. C., Hillier, S. L., Thom, E. A., Ernest, J. M., Heine, R. P., Nugent, R. P., Fischer, M. L., Leveno, K. J., Wapner, R., and Varner, M. (2000) Metronidazole to prevent preterm delivery in pregnant women with asymptomatic bacterial vaginosis. National Institute of Child Health and Human Development Network of Maternal-Fetal Medicine Units. N. Engl. J. Med. 342, 534-540
17. Simcox, R., Sin, W. T., Seed, P. T., Briley, A., and Shennan, A. H. (2007) Prophylactic antibiotics for the prevention of preterm birth in women at risk: a meta-analysis. Aust. N. Z. J. Obstet. Gynaecol. 47, 368-377 (Pubitemid 47433839)
18. McDonald, H. M., Brocklehurst, P., and Gordon, A. (2007) Antibiotics for treating bacterial vaginosis in pregnancy. Cochrane Database Syst. Rev. Jan 24; (1): CD000262
19. 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 (Pubitemid 13221599)
20. 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
21. 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
22. Varki, A., and Schauer, R. (2009) Sialic Acids in Essentials of Glycobiology, 2nd Ed., Ch. 14, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
23. Angata, T., and Varki, A. (2002) Chemical diversity in the sialic acids and related α-keto acids: an evolutionary perspective. Chem. Rev. 102, 439-469 (Pubitemid 35381636)
24. 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
25. Briselden, A. M., Moncla, B. J., Stevens, C. E., and Hillier, S. L. (1992) Sialidases (neuraminidases) in bacterial vaginosis and bacterial vaginosisassociated microflora. J. Clin. Microbiol. 30, 663-666
26. Olmsted, S. S., Meyn, L. A., Rohan, L. C., and Hillier, S. L. (2003) Sex. Trans. Dis. 30, 257-261
27. Linden, S. K., Sutton, P., Karlsson, N. G., Korolik, V., and McGuckin, M. A. (2008) Mucins in the mucosal barrier to infection. Mucosal Immunol. 1, 183-197 (Pubitemid 351541304)
28. McGuckin, M. A., Lindén, S. K., Sutton, P., and Florin, T. H. (2011) Mucin dynamics and enteric pathogens. Nat. Rev. Microbiol. 9, 265-278
29. 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 mass and preterm birth. Am. J. Obstet. Gynecol. 192, 489-496 (Pubitemid 40214985)
30. 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 (Pubitemid 20078107)
31. Kerr, M. A. (1990) The structure and function of human IgA. Biochem. J. 271, 285-296
32. Stokes, C. R., Soothill, J. F., and Turner, M. W. (1975) Immune exclusion is a function of IgA. Nature 255, 745-746
33. Perrier, C., Sprenger, N., and Corthésy, B. (2006) Glycans on secretory component participate in innate protection against mucosal pathogens. J. Biol. Chem. 281, 14280-14287 (Pubitemid 43848356)
34. Cerutti, A., Chen, K., and Chorny, A. (2011) Immunoglobulin responses at the mucosal interface. Annu. Rev. Immunol. 29, 273-293
35. van Egmond, M., Damen, C. A., van Spriel, A. B., Vidarsson, G., van Garderen, E., and van de Winkel, J. G. (2001) IgA and the IgA Fc receptor. Trends Immunol. 22, 205-211 (Pubitemid 32673660)
36. Daele, J., and Zicot, A. F. (2000) Humoral immunodeficiency in recurrent upper respiratory tract infections: some basic, clinical and therapeutic features. Acta Otorhinolaryngol. Belg. 54, 373-390
37. Yel, L. (2010) Selective IgA deficiency. J. Clin. Immunol. 30, 10-16
38. Baenziger, J., and Kornfeld, S. (1974) Structure of the carbohydrate units of IgA1 immunoglobulin: I. Composition, glycopeptide isolation, and structure of the asparagine-linked oligosaccharide units. J. Biol. Chem. 249, 7260-7269
39. Royle, L., Mattu, T. S., Hart, E., Langridge, J. I., Merry, A. H., Murphy, N., Harvey, D. J., Dwek, R. A., and Rudd, P. M. (2002) An analytical and structural database provides a strategy for sequencing O-glycans from microgram quantities of glycoproteins. Anal. Biochem. 304, 70-90 (Pubitemid 34492845)
40. Royle, L., Roos, A., Harvey, D. J., Wormald, M. R., van Gijlswijk-Janssen, D., Redwan, el-R. M., Wilson, I. A., Daha, M. R., Dwek, R. A., and Rudd, P. M. (2003) Secretory IgA N- and O-glycans provide a link between the innate and adaptive immune systems. J. Biol. Chem. 278, 20140-20153 (Pubitemid 36799209)
41. Deshpande, N., Jensen, P. H., Packer, N. H., and Kolarich, D. (2010) GlycoSpectrumScan: fishing glycopeptides from MS spectra of protease digests of human colostrum sIgA. J. Proteome Res. 9, 1063-1075
42. Mattu, T. S., Pleass, R. J., Willis, A. C., Kilian, M., Wormald, M. R., Lellouch, A. C., Rudd, P. M., Woof, J. M., and Dwek, R. A. (1998) The glycosylation and structure of human serum IgA1, Fab, and Fc regions and the role of N-glycosylation on Fcα receptor interactions. J. Biol. Chem. 273, 2260-2272 (Pubitemid 28069279)
43. Phalipon, A., Cardona, A., Kraehenbuhl, J. P., Edelman, L., Sansonetti, P. J., and Corthésy, B. (2002) Secretory component: a new role in secretory IgA-mediated immune exclusion in vivo. Immunity 17, 107-115 (Pubitemid 34874623)
44. Tanaka, M., Seki, G., Someya, T., Nagata, M., and Fujita, T. (2011) Aberrantly glycosylated IgA1 as a factor in the pathogenesis of IgA nephropathy. Clin. Dev. Immunol. 470803
45. Cauci, S., Guaschino, S., Driussi, S., De Santo, D., Lanzafame, P., and Quadrifoglio, F. (2002) Correlation of local interleukin-8 with immunoglobulin A against Gardnerella vaginalis hemolysin and with prolidase and sialidase levels in women with bacterial vaginosis. J. Infect. Dis. 185, 1614-1620 (Pubitemid 34587523)
46. Cauci, S., Monte, R., Driussi, S., Lanzafame, P., and Quadrifoglio, F. (1998) Impairment of the mucosal immune system: IgA and IgM cleavage detected in vaginal washings of a subgroup of patients with bacterial vaginosis. J. Infect Dis. 178, 1698-1706 (Pubitemid 28558142)
47. 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, e111-e117
48. 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 (Pubitemid 40364955)
49. Wiggins, R., Millar, M. R., Soothill, P. W., Hicks, S. J., and Corfield, A. P. (2002) Application of a novel human cervical mucin-based assay demonstrates the absence of increased mucinase activity in bacterial vaginosis. Int. J. STD AIDS 13, 755-760 (Pubitemid 35222009)
50. Lindh, E. (1975) Increased risistance of immunoglobulin A dimers to proteolytic degradation after binding of secretory component. J. Immunol. 114, 284-286
51. Bonner, A., Almogren, A., Furtado, P. B., Kerr, M. A., and Perkins, S. J. (2009) The nonplanar secretory IgA2 and near planar secretory IgA1 solution structures rationalize their different mucosal immune responses. J. Biol. Chem. 284, 5077-5087
52. Boullier, S., Tanguy, M., Kadaoui, K. A., Caubet, C., Sansonetti, P., Corthésy, B., and Phalipon, A. (2009) Secretory IgA-mediated neutralization of Shigella flexneri prevents intestinal tissue destruction by down-regulating inflammatory circuits. J. Immunol. 183, 5879-5885
53. Kilian, M., Reinholdt, J., Lomholt, H., Poulsen, K., and Frandsen, E. V. (1996) Biological significance of IgA1 proteases in bacterial colonization and pathogenesis: critical evaluation of experimental evidence. APMIS 104, 321-338 (Pubitemid 26226034)