The effects of hormones and vaginal microflora on the glycome of the female genital Tract: Cervical-vaginal fluid

PLoS ONE

Volumn 11, Issue 7, 2016, Pages

  Moncla, Bernard J ^a,b   Chappell, Catherine A ^a,b   Debo, Brian M ^c   Meyn, Leslie A ^b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; ALPHA GALACTOSIDASE; ALPHA GLUCOSIDASE; BETA GALACTOSIDASE; GLYCAN; GLYCOSIDASE; HORMONE; MANNOSE; MUCIN 1; MUCIN 4; MUCIN 5AC; MUCIN 7; SIALIC ACID; LECTIN; MUC1 PROTEIN, HUMAN; MUC4 PROTEIN, HUMAN; MUC5B PROTEIN, HUMAN; MUC7 PROTEIN, HUMAN; MUCIN; MUCIN 5B; N ACETYLNEURAMINIC ACID; SALIVA PROTEIN; SIALIDASE;

ARTICLE; BINDING SITE; CERVICAL VAGINAL FLUID; CLINICAL ARTICLE; ENZYME ACTIVITY; FABACEAE; FEMALE; FEMALE GENITAL TRACT PARAMETERS; GLYCOBIOLOGY; HOST PATHOGEN INTERACTION; HUMAN; MAACKIA AMURENSIS; MENSTRUAL CYCLE; NONHUMAN; POSTMENOPAUSE; PROTEIN SECRETION; SAMBUCUS NIGRA; VAGINA FLORA; VAGINITIS; BODY FLUID; ENZYMOLOGY; FEMALE GENITAL SYSTEM; METABOLISM; MICROBIOLOGY; PATHOLOGY; UTERINE CERVIX MUCUS; VAGINA;

ALPHA-GALACTOSIDASE; BETA-GALACTOSIDASE; BODY FLUIDS; CERVIX MUCUS; FEMALE; GENITALIA, FEMALE; GLYCOSIDE HYDROLASES; HORMONES; HUMANS; LECTINS; MENSTRUAL CYCLE; MUCIN-1; MUCIN-4; MUCIN-5B; MUCINS; N-ACETYLNEURAMINIC ACID; NEURAMINIDASE; SALIVARY PROTEINS AND PEPTIDES; VAGINA; VAGINOSIS, BACTERIAL;

EID: 84979284360     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0158687     Document Type: Article

References (97)

1. Carson D, DeSouza M, Kardon R, Zhou X, Lagow E, Julian J. Mucin expression and function in the female reproductive tract. Human Reproduction Update. 1998; 4(5):459-64. doi: 10.1093/humupd/4.5. 459 PMID: 10027596
2. Cone RA. Barrier properties of mucus. Adv Drug Deliv Rev. 2009; 61(2):75-85. Epub 2009/01/13. doi: 10.1016/j.addr.2008.09.008 PMID: 19135107.
3. Dekker J, Rossen JW, Buller HA, Einerhand AW. The MUC family: an obituary. Trends Biochem Sci. 2002; 27(3):126-31. Epub 2002/03/15. PMID: 11893509.
4. Forstner G. Signal transduction, packaging and secretion of mucins. Annu Rev Physiol. 1995; 57:585-605. Epub 1995/01/01. doi: 10.1146/annurev.ph.57.030195.003101 PMID: 7778879.
5. Gipson I, Spurr-Michaud S, Moccia R, Zhan Q, Toribara N, Ho S, et al. MUC4 and MUC5B transcripts are the prevalent mucin messenger ribonucleic acids of the human endocervix. Biol Reprod. 1999; 60:58-64. PMID: 9858486
6. Gipson IK, Moccia R, Spurr-Michaud S, Argueso P, Gargiulo AR, Hill JA 3rd, et al. The Amount of MUC5B mucin in cervical mucus peaks at midcycle. J Clin Endocrinol Metab. 2001; 86(2):594-600. Epub 2001/02/07. PMID: 11158014.
7. Venkataraman N, Cole AL, Svoboda P, Pohl J, Cole AM. Cationic Polypeptides Are Required for Anti-HIV-1 Activity of Human Vaginal Fluid. The Journal of Immunology. 2005; 175(11):7560-7. PMID: 16301665
8. Vogel I, Gronbaek H, Flyvbjerg A, Thorsen P. Albumin in vaginal secretion is a marker of infection. Int J Gynaecol Obstet. 2003; 83:307-8. PMID: 14643045
9. Corfield AP, Wagner SA, Clamp JR, Kriaris MS, Hoskins LC. Mucin degradation in the human colon: production of sialidase, sialate O-acetylesterase, N-acetylneuraminate lyase, arylesterase, and glycosulfatase activities by strains of fecal bacteria. Infection and Immunity. 1992; 60(10):3971-8. Epub 1992/10/01. PMID: 1398908; PubMed Central PMCID: PMC257425.
10. Roberton A, Corfield A. Mucin degradation and its significance in inflammatory conditions of the gastrointestinal tract. In: Tannock G, editor. Medical Importance of the Normal Microflora: Springer US; 1999. p. 222-61.
11. Andrianifahanana M, Moniaux N, Batra SK. Regulation of mucin expression: mechanistic aspects and implications for cancer and inflammatory diseases. Biochimica et Biophysica Acta (BBA)-Reviews on Cancer. 2006; 1765(2):189-222.
12. Cohen M, Varki A. The sialome-far more than the sum of its parts. Omics: a journal of integrative biology. 2010; 14(4):455-64. doi: 10.1089/omi.2009.0148 PMID: 20726801
13. Corfield AP. Mucins: A biologically relevant glycan barrier in mucosal protection. Biochimica et Biophysica Acta (BBA)-General Subjects. 2015; 1850(1):236-52. http://dx.doi.org/10.1016/j.bbagen.2014. 05.003.
14. McGuckin MA, Lindén SK, Sutton P, Florin TH. Mucin dynamics and enteric pathogens. Nature Reviews Microbiology. 2011; 9(4):265-78. doi: 10.1038/nrmicro2538 PMID: 21407243
15. Schauer R. Sialic acids as regulators of molecular and cellular interactions. Curr Opin Struct Biol. 2009; 19(5):507-14. Epub 2009/08/25. doi: 10.1016/j.sbi.2009.06.003 PMID: 19699080.
16. Varki A, Schauer R. Sialic Acids. In: Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, et al., editors. Essentials of Glycobiology. 2nd ed. Cold Spring Harbor (NY)2009.
17. Moncla LH, Zhong G, Nelson CW, Dinis JM, Mutschler J, Hughes AL, et al. Selective Bottlenecks Shape Evolutionary Pathways Taken during Mammalian Adaptation of a 1918-like Avian Influenza Virus. Cell Host & Microbe. 2016; 19(2):169-80.
18. Strober W, Hanson LÅ, Sell KW. Recent advances in mucosal immunity: Raven Press New York; 1982.
19. Keller MJ, Madan RP, Shust G, Carpenter CA, Torres NM, Cho S, et al. Changes in the soluble mucosal immune environment during genital herpes outbreaks. J Acquir Immune Defic Syndr. 2012; 61(2):194-202. Epub 2012/07/24. doi: 10.1097/QAI.0b013e31826867ae PMID: 22820806.
20. Olmsted SS, Padgett JL, Yudin AI, Whaley KJ, Moench TR, Cone RA. Diffusion of Macromolecules and Virus-Like Particles in Human Cervical Mucus. Biophysical Journal. 2001; 81(4):1930-7. http://dx. doi.org/10.1016/S0006-3495(01)75844-4. PMID: 11566767
21. Valore EV, Park CH, Igreti SL, Ganz T. Antimicrobial components of vaginal fluid. Am J Obstet Gynecol. 2002; 187(3):561-8. PMID: 12237628
22. Chappell CA, Rohan LC, Moncla BJ, Wang L, Meyn LA, Bunge K, et al. The effects of reproductive hormones on the physical properties of cervicovaginal fluid. Am J Obstet Gynecol. 2014. Epub 2014/03/ 26. doi: 10.1016/j.ajog.2014.03.041 PMID: 24662718.
23. Chappell CA, Isaacs CE, Xu W, Meyn LA, Uranker K, Dezzutti CS, et al. The effect of menopause on the innate antiviral activity of cervicovaginal lavage. Am J Obstet Gynecol. 2015.
24. Hagen KT. O-Glycosylation and Development. In: Endo T, Seeberger PH, Hart GW, Wong C-H, Taniguchi N, editors. Glycoscience: Biology and Medicine: Springer Japan; 2014. p. 1-8.
25. Wilson IBH, Breton C, Imberty A, Tvaroška I. Molecular Basis for the Biosynthesis of Oligo- and Polysaccharides. In: Fraser-Reid B, Tatsuta K, Thiem J, editors. Glycoscience: Springer Berlin Heidelberg; 2008. p. 2265-323.
26. Gipson I, Ho S, Spurr-Michaud S, Tisdale A, Zhan Q, Torlakovic E, et al. Mucin genes expressed by human female reproductive tract epithelia. Biol Reprod. 1997; 56:999-1011. PMID: 9096884
27. Moncla BJ, Chappell CA, Mahal LK, Debo BM, Meyn LA, Hillier SL. Impact of Bacterial Vaginosis, as Assessed by Nugent Criteria and Hormonal Status on Glycosidases and Lectin Binding in Cervicovaginal Lavage Samples. PLoS One. 2015; 10(5):e0127091. doi: 10.1371/journal.pone.0127091 PMID: 26011704
28. Wang L, Koppolu S, Chappell C, Moncla BJ, Hillier SL, Mahal LK. Studying the Effects of Reproductive Hormones and Bacterial Vaginosis on the Glycome of Lavage Samples from the Cervicovaginal Cavity. PLoS One. 2015; 10(5):e0127021. doi: 10.1371/journal.pone.0127021 PMID: 25993513
29. Roberton AM, Wiggins R, Horner PJ, Greenwood R, Crowley T, Fernandes A, et al. A Novel Bacterial Mucinase, Glycosulfatase, Is Associated with Bacterial Vaginosis. Journal of Clinical Microbiology. 2005; 43(11):5504-8. doi: 10.1128/jcm.43.11.5504-5508.2005 PMID: 16272477
30. Varki A. Nothing in glycobiology makes sense, except in the light of evolution. Cell. 2006; 126(5):841-5. PMID: 16959563
31. Varki NM, Varki A. Diversity in cell surface sialic acid presentations: implications for biology and disease. Lab Invest. 2007; 87(9):851-7. PMID: 17632542
32. Hillier SL, Nugent RP, Eschenbach DA, Krohn MA, Gibbs RS, Martin DH, et al. Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. The Vaginal Infections and Prematurity Study Group. N Engl J Med. 1995; 333(26):1737-42. Epub 1995/12/28. doi: 10.1056/ NEJM199512283332604 PMID: 7491137.
33. Klebanoff MA, Hillier SL, Nugent RP, MacPherson CA, Hauth JC, Carey JC, et al. Is bacterial vaginosis a stronger risk factor for preterm birth when it is diagnosed earlier in gestation? Am J Obstet Gynecol. 2005; 192(2):470-7. Epub 2005/02/08. doi: 10.1016/j.ajog.2004.07.017 PMID: 15695989.
34. Nugent RP, Krohn MA, Hillier SL. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. Journal of Clinical Microbiology. 1991; 29(2):297-301. Epub 1991/02/01. PMID: 1706728; PubMed Central PMCID: PMC269757.
35. Gipson IK. Mucins of the human endocervix. Front Biosci. 2001; 6:D1245-55. Epub 2001/10/02. PMID: 11578960.
36. Braham PH, Moncla BJ. Rapid presumptive identification and further characterization of Bacteroides forsythus. Journal of Clinical Microbiology. 1992; 30(3):649-54. Epub 1992/03/01. PMID: 1551981; PubMed Central PMCID: PMC265126.
37. Cauci S, Culhane JF, Di Santolo M, McCollum K. Among pregnant women with bacterial vaginosis, the hydrolytic enzymes sialidase and prolidase are positively associated with interleukin-1beta. Am J Obstet Gynecol. 2008; 198(1):132 e1-7. Epub 2007/08/24. doi: 10.1016/j.ajog.2007.05.035 PMID: 17714681.
38. Cauci S, McGregor J, Thorsen P, Grove J, Guaschino S. Combination of vaginal pH with vaginal sialidase and prolidase activities for prediction of low birth weight and preterm birth. Am J Obstet Gynecol. 2005; 192(2):489-96. Epub 2005/02/08. doi: 10.1016/j.ajog.2004.07.023 PMID: 15695992.
39. McGregor JA, French JI, Jones W, Milligan K, McKinney PJ, Patterson E, et al. 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. 1994; 170(4):1048-59; discussion 59-60. Epub 1994/ 04/01. PMID: 8166188.
40. Moncla BJ, Braham P, Hillier SL. Sialidase (neuraminidase) activity among gram-negative anaerobic and capnophilic bacteria. Journal of Clinical Microbiology. 1990; 28(3):422-5. Epub 1990/03/01. PMID: 2108991; PubMed Central PMCID: PMC269635.
41. Moncla BJ, Braham P, Rabe LK, Hillier SL. Rapid presumptive identification of black-pigmented gramnegative anaerobic bacteria by using 4-methylumbelliferone derivatives. Journal of Clinical Microbiology. 1991; 29(9):1955-8. Epub 1991/09/01. PMID: 1774320; PubMed Central PMCID: PMC270241.
42. Moncla BJ, Pryke KM. Oleate lipase activity in Gardnerella vaginalis and reconsideration of existing biotype schemes. BMC Microbiol. 2009; 9:78. Epub 2009/04/24. doi: 10.1186/1471-2180-9-78 PMID: 19386125; PubMed Central PMCID: PMC2680412.
43. Roberts G, Tarelli E, Homer KA, Philpott-Howard J, Beighton D. Production of an Endo-β-N-Acetylglucosaminidase Activity Mediates Growth of Enterococcus faecalis on a High-Mannose-Type Glycoprotein. Journal of Bacteriology. 2000; 182(4):882-90. PMC94360. PMID: 10648510
44. Birse KM, Burgener A, Westmacott GR, McCorrister S, Novak RM, Ball TB. Unbiased Proteomics Analysis Demonstrates Significant Variability in Mucosal Immune Factor Expression Depending on the Site and Method of Collection. PLoS One. 2013; 8(11):e79505. doi: 10.1371/journal.pone.0079505 PMID: 24244515
45. Fields S, Song B, Rasoul B, Fong J, Works MG, Shew K, et al. New Candidate Biomarkers in the Female Genital Tract to Evaluate Microbicide Toxicity. PLoS One. 2014; 9(10):e110980. doi: 10.1371/ journal.pone.0110980 PMID: 25333937
46. Mitchell C, Paul K, Agnew K, Gaussman R, Coombs RW, Hitti J. Estimating volume of cervicovaginal secretions in cervicovaginal lavage fluid collected for measurement of genital HIV-1 RNA levels in women. Journal of clinical microbiology. 2011; 49(2):735-6. doi: 10.1128/JCM.00991-10 PMID: 21106793
47. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951; 193(1):265-75. PMID: 14907713
48. Moncla B, Charnetzky W. Free form lipoproteins in Yersinia pestis. Microbios letters. 1986; 32(126):81-6.
49. Patton DL, Cosgrove Sweeney YT, Balkus JE, Rohan LC, Moncla BJ, Parniak AA, et al. Preclinical safety assessments of UC781 anti-human immunodeficiency virus topical microbicide formulations. Antimicrobial Agents and Chemotherapy. 2007; 51(5):1608-15. doi: 10.1128/aac.00984-06 WOS:000246541500003. PMID: 17353240
50. Lewis WG, Robinson LS, Gilbert NM, Perry JC, Lewis AL. Degradation, foraging, and depletion of mucus sialoglycans by the vagina-adapted Actinobacterium Gardnerella vaginalis. J Biol Chem. 2013; 288(17):12067-79. Epub 2013/03/13. doi: 10.1074/jbc.M113.453654 PMID: 23479734; PubMed Central PMCID: PMC3636892.
51. Lewis WG, Robinson LS, Perry J, Bick JL, Peipert JF, Allsworth JE, et al. Hydrolysis of secreted sialoglycoprotein immunoglobulin A (IgA) in ex vivo and biochemical models of bacterial vaginosis. J Biol Chem. 2012; 287(3):2079-89. Epub 2011/12/03. doi: 10.1074/jbc.M111.278135 PMID: 22134918; PubMed Central PMCID: PMC3265887.
52. Briselden AM, Moncla BJ, Stevens CE, Hillier SL. Sialidases (neuraminidases) in bacterial vaginosis and bacterial vaginosis-associated microflora. Journal of Clinical Microbiology. 1992; 30(3):663-6. PMID: 1551983
53. Howe L, Wiggins R, Soothill PW, Millar MR, Horner PJ, Corfield AP. Mucinase and sialidase activity of the vaginal microflora: implications for the pathogenesis of preterm labour. Int J STD AIDS. 1999; 10 (7):442-7. Epub 1999/08/24. PMID: 10454178.
54. Lopes dos Santos Santiago G, Deschaght P, El Aila N, Kiama TN, Verstraelen H, Jefferson KK, et al. Gardnerella vaginalis comprises three distinct genotypes of which only two produce sialidase. Am J Obstet Gynecol. 2011; 204(5):450.e1-.e7. http://dx.doi.org/10.1016/j.ajog.2010.12.061.
55. Homer KA, Whiley RA, Beighton D. Production of specific glycosidase activities by Streptococcus intermedius strain UNS35 grown in the presence of mucin. Journal of Medical Microbiology. 1994; 41 (3):184-90. doi: 10.1099/00222615-41-3-184 PMID: 8064838
56. King SJ, Hippe KR, Weiser JN. Deglycosylation of human glycoconjugates by the sequential activities of exoglycosidases expressed by Streptococcus pneumoniae. Mol Microbiol. 2006; 59(3):961-74. PMID: 16420364
57. Wiggins R, Hicks SJ, Soothill PW, Millar MR, Corfield AP. Mucinases and sialidases: their role in the pathogenesis of sexually transmitted infections in the female genital tract. Sex Transm Infect. 2001; 77(6):402-8. doi: 10.1136/sti.77.6.402 PMID: 11714935
58. Homer KA, Roberts G, Byers HL, Tarelli E, Whiley RA, Philpott-Howard J, et al. Mannosidase production by viridans group streptococci. Journal of clinical microbiology. 2001; 39(3):995-1001. Epub 2001/ 03/07. doi: 10.1128/JCM.39.3.995-1001.2001 PMID: 11230417; PubMed Central PMCID: PMC87863.
59. King SJ. Pneumococcal modification of host sugars: a major contributor to colonization of the human airway? Molecular Oral Microbiology. 2010; 25(1):15-24. doi: 10.1111/j.2041-1014.2009.00564.x PMID: 20331791
60. Roberts G, Homer KA, Tarreti E, Philpott-Howard J, Devriese LA, Beighton D. Distribution of endo-β-Nacetylglucosaminidase amongst enterococci. Journal of Medical Microbiology. 2001; 50(7):620-6. PMID: 11444772
61. Hart ML, Saifuddin M, Uemura K, Bremer EG, Hooker B, Kawasaki T, et al. High mannose glycans and sialic acid on gp120 regulate binding of mannose-binding lectin (MBL) to HIV type 1. AIDS Res Hum Retroviruses. 2002; 18(17):1311-7. PMID: 12487819
62. Ji X, Gewurz H, Spear GT. Mannose binding lectin (MBL) and HIV. Molecular immunology. 2005; 42 (2):145-52. PMID: 15488604
63. Dohrman A, Miyata S, Gallup M, Li JD, Chapelin C, Coste A, et al. Mucin gene (MUC 2 and MUC 5AC) upregulation by Gram-positive and Gram-negative bacteria. Biochim Biophys Acta. 1998; 1406 (3):251-9. Epub 1998/06/19. PMID: 9630659.
64. Radtke AL, Quayle AJ, Herbst-Kralovetz MM. Microbial products alter the expression of membraneassociated mucin and antimicrobial peptides in a three-dimensional human endocervical epithelial cell model. Biology of Reproduction. 2012; 87(6):132. Epub 2012/10/12. doi: 10.1095/biolreprod.112. 103366 PMID: 23053434.
65. Lemjabbar H, Basbaum C. Platelet-activating factor receptor and ADAM10 mediate responses to Staphylococcus aureus in epithelial cells. Nat Med. 2002; 8(1):41-6. PMID: 11786905
66. Linden SK, Sutton P, Karlsson NG, Korolik V, McGuckin MA. Mucins in the mucosal barrier to infection. Mucosal Immunol. 2008; 1(3):183-97. doi: 10.1038/mi.2008.5 PMID: 19079178
67. Smirnova MG, Guo L, Birchall JP, Pearson JP. LPS up-regulates mucin and cytokine mRNA expression and stimulates mucin and cytokine secretion in goblet cells. Cellular Immunology. 2003; 221 (1):42-9. http://dx.doi.org/10.1016/S0008-8749(03)00059-5. PMID: 12742381
68. Yanagihara K, Seki M, Cheng P-W. Lipopolysaccharide induces mucus cell metaplasia in mouse lung. American journal of respiratory cell and molecular biology. 2001; 24(1):66-73. PMID: 11152652
69. Appelmelk BJ, Monteiro MA, Martin SL, Moran AP, Vandenbroucke-Grauls CM. Why Helicobacter pylori has Lewis antigens. Trends in microbiology. 2000; 8(12):565-70. PMID: 11115753
70. Gallego MP, Hulen C. Influence of sialic acid and bacterial sialidase on differential adhesion of Pseudomonas aeruginosa to epithelial cells. Colloids and Surfaces B: Biointerfaces. 2006; 52(2):154-6. PMID: 16781124
71. Pang SS, Nguyen STS, Perry AJ, Day CJ, Panjikar S, Tiralongo J, et al. The Three-dimensional Structure of the Extracellular Adhesion Domain of the Sialic Acid-binding Adhesin SabA from Helicobacter pylori. Journal of Biological Chemistry. 2014; 289(10):6332-40. doi: 10.1074/jbc.M113.513135 PMID: 24375407
72. Biswas N, Rodriguez-Garcia M, Shen Z, Crist SG, Bodwell JE, Fahey JV, et al. Effects of Tenofovir on Cytokines and Nucleotidases in HIV-1 Target Cells and the Mucosal Tissue Environment in the Female Reproductive Tract. Antimicrobial Agents and Chemotherapy. 2014; 58(11):6444-53. doi: 10.1128/ aac.03270-14 PMID: 25136003
73. Lehman DA, Ronen K, Blish CA, Baeten JM, Jalalian-Lechak Z, Jaoko W, et al. Systemic Cytokine Levels Show Limited Correlation With Risk of HIV-1 Acquisition. JAIDS Journal of Acquired Immune Deficiency Syndromes. 2014; 66(2):135-9 doi: 10.1097/QAI.0000000000000104 PMID: 24413043
74. Mueller Y, Fraietta J, Ratner D, Boesteanu A, Gupta P, Katsikis P. Anti-HIV, anti-inflammatory and safety profile of the PDB microbicide candidate (HUM8P.342). The Journal of Immunology. 2014; 192 (1 Supplement):185.17.
75. Stute P, Kollmann Z, Bersinger N, von Wolff M, Thurman AR, Archer DF. Vaginal cytokines do not differ between postmenopausal women with and without symptoms of vulvovaginal irritation. Menopause. 2014; 21(8):1.
76. Li X, Wang L, Nunes DP, Troxler RF, Offner GD. Pro-inflammatory Cytokines Up-regulate MUC1 Gene Expression in Oral Epithelial Cells. Journal of Dental Research. 2003; 82(11):883-7. doi: 10.1177/ 154405910308201107 PMID: 14578499
77. Albertsmeyer A-C, Kakkassery V, Spurr-Michaud S, Beeks O, Gipson IK. Effect of pro-inflammatory mediators on membrane-associated mucins expressed by human ocular surface epithelial cells. Exp Eye Res. 2010; 90(3):444-51. http://dx.doi.org/10.1016/j.exer.2009.12.009. doi: 10.1016/j.exer.2009. 12.009 PMID: 20036239
78. Corti S, Nizzardo M, Nardini M, Donadoni C, Salani S, Ronchi D, et al. Embryonic stem cell-derived neural stem cells improve spinal muscular atrophy phenotype in mice. Brain. 2010; 133(Pt 2):465-81. Epub 2009/12/25. doi: 10.1093/brain/awp318 PMID: 20032086.
79. Aplin J, Hey N, Li T. MUC1 as a cell surface and secretory component of endometrial epithelium: reduced levels in recurrent miscarriage. Am J Reprod Immunol. 1996; 35:261-6. PMID: 8962658
80. Brayman M, Thathiah A, Carson Daniel D. MUC1: A multifunctional cell surface component of reproductive tissue epithelia. Reproductive Biology and Endocrinology. 2004; 2(1):4.
81. Gipson IK, Blalock T, Tisdale A, Spurr-Michaud S, Allcorn S, Stavreus-Evers A, et al. MUC16 is lost from the uterodome (pinopode) surface of the receptive human endometrium: in vitro evidence that MUC16 is a barrier to trophoblast adherence. Biology of Reproduction. 2008; 78(1):134-42. Epub 2007/10/19. doi: 10.1095/biolreprod.106.058347 PMID: 17942799.
82. Cauci S, Driussi S, Monte R, Lanzafame P, Pitzus E, Quadrifoglio F. Immunoglobulin A response against Gardnerella vaginalis hemolysin and sialidase activity in bacterial vaginosis. Am J Obstet Gynecol. 1998; 178(3):511-5. Epub 1998/04/16. PMID: 9539518.
83. Carraway K, Idris N. Regulation of sialomucin complex/Muc4 in the female rat reproductive tract. Biochem Soc Trans. 2001; 29(2):162-6.
84. Rossi EA, McNeer RR, Price-Schiavi SA, Van den Brande JMH, Komatsu M, Thompson JF, et al. Sialomucin Complex, a Heterodimeric Glycoprotein Complex: EXPRESSION AS A SOLUBLE, SECRETA-BLE FORM IN LACTATING MAMMARY GLAND AND COLON. Journal of Biological Chemistry. 1996; 271(52):33476-85. doi: 10.1074/jbc.271.52.33476 PMID: 8969211
85. Zen Y, Harada K, Sasaki M, Tsuneyama K, Katayanagi K, Yamamoto Y, et al. Lipopolysaccharide Induces Overexpression of MUC2 and MUC5AC in Cultured Biliary Epithelial Cells: Possible Key Phenomenon of Hepatolithiasis. The American Journal of Pathology. 2002; 161(4):1475-84. http://dx.doi. org/10.1016/S0002-9440(10)64423-9. PMID: 12368220
86. Valore EV, Wiley DJ, Ganz T. Reversible deficiency of antimicrobial polypeptides in bacterial vaginosis. Infection and Immunity. 2006; 74(10):5693-702. PMID: 16988245
87. Yudin MH, Landers DV, Meyn L, Hillier SL. Clinical and Cervical Cytokine Response to Treatment With Oral or Vaginal Metronidazole for Bacterial Vaginosis During Pregnancy: A Randomized Trial. Obstetrics & Gynecology. 2003; 102(3):527-34.
88. Aplin JD. MUC-1 glycosylation in endometrium: possible roles of the apical glycocalyx at implantation. Human Reproduction. 1999; 14(suppl 2):17-25. doi: 10.1093/humrep/14.suppl-2.17 PMID: 10690797
89. Escande F, Aubert JP, Porchet N, Buisine MP. Human mucin gene MUC5AC: organization of its 5'-region and central repetitive region. Biochem J. 2001; 358(Pt 3):763-72. Epub 2001/09/06. PMID: 11535137; PubMed Central PMCID: PMC1222110.
90. Yurewicz E, Matsuura F, Moghissi K. Structural characterization of neutral oligosaccharides of human midcycle cervical mucin. Journal of Biological Chemistry. 1982; 257(5):2314-22. PMID: 6277894
91. Rousseau K, Vinall LE, Butterworth SL, Hardy RJ, Holloway J, Wadsworth MEJ, et al. MUC7 Haplotype Analysis: Results from a Longitudinal Birth Cohort Support Protective Effect of the MUC7&z.ast;5 Allele on Respiratory Function. Annals of Human Genetics. 2006; 70(4):417-27. doi: 10.1111/j.1469-1809.2006. 00250.x
92. Imseis HM, Greig PC, Livengood CH, Shunior E, Durda P, Erikson M. Characterization of the Inflammatory Cytokines in the Vagina During Pregnancy and Labor and With Bacterial Vaginosis. Journal of the Society for Gynecologic Investigation. 1997; 4(2):90-4. doi: 10.1177/107155769700400208 PMID: 9101468
93. Cauci S, Driussi S, De Santo D, Penacchioni P, Iannicelli T, Lanzafame P, et al. Prevalence of bacterial vaginosis and vaginal flora changes in peri-and postmenopausal women. Journal of clinical microbiology. 2002; 40(6):2147-52. PMID: 12037079
94. Jacobson JC, Turok DK, Dermish AI, Nygaard IE, Settles ML. Vaginal microbiome changes with levonorgestrel intrauterine system placement. Contraception. 2014; 90(2):130-5. doi: 10.1016/j. contraception.2014.04.006 WOS:000339367700005. PMID: 24835828
95. Petricevic L, Domig KJ, Nierscher FJ, Sandhofer MJ, Krondorfer I, Kneifel W, et al. Differences in the vaginal lactobacilli of postmenopausal women and influence of rectal lactobacilli. Climacteric. 2013; 16 (3):356-61. doi: 10.3109/13697137.2012.725788 WOS:000318937600007. PMID: 23113473
96. Jones AH, Lee CC, Moncla BJ, Robinovitch MR, Birdsell DC. Surface localization of sialic acid on Actinomyces viscosus. Journal of General Microbiology. 1986; 132(12):3381-91. Epub 1986/12/01. PMID: 3655719.
97. Leite B, Hillier S, Moncla BJ. Detection and Localisation of Sialic Acid in Gardnerella vaginalis, Mobiluncus spp., and Other Vaginal Microorganisms. Microbial Ecology in Health and Disease. 1989; 2 (4):255-60. doi: 10.3109/08910608909140228