Membrane Vesicles of Group B Streptococcus Disrupt Feto-Maternal Barrier Leading to Preterm Birth

PLoS Pathogens

Volumn 12, Issue 9, 2016, Pages

  Surve, Manalee Vishnu ^a   Anil, Anjali ^a   Kamath, Kshama Ganesh ^a   Bhutda, Smita ^a   Sthanam, Lakshmi Kavitha ^a   Pradhan, Arpan ^a   Srivastava, Rohit ^a   Basu, Bhakti ^b   Dutta, Suryendu ^a   Sen, Shamik ^a   Modi, Deepak ^c   Banerjee, Anirban ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY BOMBAY   (India)

^b BHABHA ATOMIC RESEARCH CENTRE   (India)

^c NATIONAL INSTITUTE FOR RESEARCH IN REPRODUCTIVE HEALTH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; CYCLIC AMP; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; METALLOPROTEINASE; PROTEINASE INHIBITOR; TUMOR NECROSIS FACTOR; VIRULENCE FACTOR; CYTOKINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; CYTOTOXICITY; FATTY ACID ANALYSIS; FEMALE; GROUP B STREPTOCOCCAL INFECTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LEUKOCYTE COUNT; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MEMBRANE VESICLE; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PREMATURE FETUS MEMBRANE RUPTURE; PREMATURE LABOR; PROTEIN ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; STREPTOCOCCUS AGALACTIAE; TRANSMISSION ELECTRON MICROSCOPY; TUNEL ASSAY; UPREGULATION; AMNION; AMNION FLUID; ANIMAL; CHORIOAMNIONITIS; COMPLICATION; DECIDUA; DISEASE MODEL; IMMUNOLOGY; INFLAMMATION; METABOLISM; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY; PREGNANCY; PREMATURITY; SEROTYPE; STREPTOCOCCUS INFECTION; TUMOR CELL LINE;

AMNION; AMNIOTIC FLUID; ANIMALS; CELL LINE, TUMOR; CHORIOAMNIONITIS; CYTOKINES; DECIDUA; DISEASE MODELS, ANIMAL; FEMALE; FETAL MEMBRANES, PREMATURE RUPTURE; HUMANS; INFLAMMATION; MICE; PREGNANCY; PREMATURE BIRTH; SEROGROUP; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS AGALACTIAE;

EID: 84989854734     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005816     Document Type: Article

References (62)

1. Liu L, Johnson HL, Cousens S, Perin J, Scott S, et al. (2012) Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet379: 2151–2161. doi: 10.1016/S0140-6736(12)60560-122579125
2. Beck S, Wojdyla D, Say L, Betran AP, Merialdi M, et al. (2010) The worldwide incidence of preterm birth: a systematic review of maternal mortality and morbidity. Bull World Health Organ88: 31–38. doi: 10.2471/BLT.08.06255420428351
3. Seo K, McGregor JA, French JI, (1992) Preterm birth is associated with increased risk of maternal and neonatal infection. Obstet Gynecol79: 75–80. 1727591
4. Mwaniki MK, Atieno M, Lawn JE, Newton CR, (2012) Long-term neurodevelopmental outcomes after intrauterine and neonatal insults: a systematic review. Lancet379: 445–452. doi: 10.1016/S0140-6736(11)61577-822244654
5. Goldenberg RL, Hauth JC, Andrews WW, (2000) Intrauterine infection and preterm delivery. N Engl J Med342: 1500–1507. 10816189
6. Regan JA, Klebanoff MA, Nugent RP, (1991) The epidemiology of group B streptococcal colonization in pregnancy. Vaginal Infections and Prematurity Study Group. Obstet Gynecol77: 604–610. 2002986
7. Yancey MK, Schuchat A, Brown LK, Ventura VL, Markenson GR, (1996) The accuracy of late antenatal screening cultures in predicting genital group B streptococcal colonization at delivery. Obstet Gynecol88: 811–815. 8885919
8. Campbell JR, Hillier SL, Krohn MA, Ferrieri P, Zaleznik DF, et al. (2000) Group B streptococcal colonization and serotype-specific immunity in pregnant women at delivery. Obstet Gynecol96: 498–503. 11004347
9. Thomsen AC, Morup L, Hansen KB, (1987) Antibiotic elimination of group-B streptococci in urine in prevention of preterm labour. Lancet1: 591–593. 2881132
10. Newton ER, Clark M, (1988) Group B streptococcus and preterm rupture of membranes. Obstet Gynecol71: 198–202. 3275914
11. Anderson BL, Simhan HN, Simons KM, Wiesenfeld HC, (2007) Untreated asymptomatic group B streptococcal bacteriuria early in pregnancy and chorioamnionitis at delivery. Am J Obstet Gynecol196: 524 e521–525.
12. Regan JA, Chao S, James LS, (1981) Premature rupture of membranes, preterm delivery, and group B streptococcal colonization of mothers. Am J Obstet Gynecol141: 184–186. 7025636
13. McDonald H, Vigneswaran R, O'Loughlin JA, (1989) Group B streptococcal colonization and preterm labour. Aust N Z J Obstet Gynaecol29: 291–293. 2695054
14. Allen U, Nimrod C, Macdonald N, Toye B, Stephens D, et al. (1999) Relationship between antenatal group B streptococcal vaginal colonization and premature labour. Paediatr Child Health4: 465–469. 20212961
15. Seyyed EZ, Toossi E, Jalalvand A, Sajadi M, (2013) Group B Streptococci investigation in pre-term labors. Med Arch67: 124–125. 24341060
16. Vanderhoeven JP, Bierle CJ, Kapur RP, McAdams RM, Beyer RP, et al. (2014) Group B streptococcal infection of the choriodecidua induces dysfunction of the cytokeratin network in amniotic epithelium: a pathway to membrane weakening. PLoS Pathog10: e1003920. doi: 10.1371/journal.ppat.100392024603861
17. Whidbey C, Vornhagen J, Gendrin C, Boldenow E, Samson JM, et al. (2015) A streptococcal lipid toxin induces membrane permeabilization and pyroptosis leading to fetal injury. EMBO Mol Med7: 488–505. doi: 10.15252/emmm.20140488325750210
18. Gervasi MT, Romero R, Bracalente G, Erez O, Dong Z, et al. (2012) Midtrimester amniotic fluid concentrations of interleukin-6 and interferon-gamma-inducible protein-10: evidence for heterogeneity of intra-amniotic inflammation and associations with spontaneous early (<32 weeks) and late (>32 weeks) preterm delivery. J Perinat Med40: 329–343. doi: 10.1515/jpm-2012-003422752762
19. Adams Waldorf KM, Gravett MG, McAdams RM, Paolella LJ, Gough GM, et al. (2011) Choriodecidual group B streptococcal inoculation induces fetal lung injury without intra-amniotic infection and preterm labor in Macaca nemestrina. PLoS One6: e28972. doi: 10.1371/journal.pone.002897222216148
20. Mashburn LM, Whiteley M, (2005) Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature437: 422–425. 16163359
21. Baumgarten T, Sperling S, Seifert J, von Bergen M, Steiniger F, et al. (2012) Membrane vesicle formation as a multiple-stress response mechanism enhances Pseudomonas putida DOT-T1E cell surface hydrophobicity and biofilm formation. Appl Environ Microbiol78: 6217–6224. doi: 10.1128/AEM.01525-1222752175
22. Manning AJ, Kuehn MJ, (2011) Contribution of bacterial outer membrane vesicles to innate bacterial defense. BMC Microbiol11: 258. doi: 10.1186/1471-2180-11-25822133164
23. McBroom AJ, Kuehn MJ, (2007) Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol Microbiol63: 545–558. 17163978
24. Gurung M, Moon DC, Choi CW, Lee JH, Bae YC, et al. (2011) Staphylococcus aureus produces membrane-derived vesicles that induce host cell death. PLoS One6: e27958. doi: 10.1371/journal.pone.002795822114730
25. Rivera J, Cordero RJ, Nakouzi AS, Frases S, Nicola A, et al. (2010) Bacillus anthracis produces membrane-derived vesicles containing biologically active toxins. Proc Natl Acad Sci U S A107: 19002–19007. doi: 10.1073/pnas.100884310720956325
26. Jiang Y, Kong Q, Roland KL, Curtiss R, 3rd (2014) Membrane vesicles of Clostridium perfringens type A strains induce innate and adaptive immunity. Int J Med Microbiol304: 431–443. doi: 10.1016/j.ijmm.2014.02.00624631214
27. Brown L, Kessler A, Cabezas-Sanchez P, Luque-Garcia JL, Casadevall A, (2014) Extracellular vesicles produced by the Gram-positive bacterium Bacillus subtilis are disrupted by the lipopeptide surfactin. Mol Microbiol93: 183–198. doi: 10.1111/mmi.1265024826903
28. Olaya-Abril A, Prados-Rosales R, McConnell MJ, Martin-Pena R, Gonzalez-Reyes JA, et al. (2014) Characterization of protective extracellular membrane-derived vesicles produced by Streptococcus pneumoniae. J Proteomics106: 46–60. doi: 10.1016/j.jprot.2014.04.02324769240
29. Haas B, Grenier D, (2015) Isolation, Characterization and Biological Properties of Membrane Vesicles Produced by the Swine Pathogen Streptococcus suis. PLoS One10: e0130528. doi: 10.1371/journal.pone.013052826110524
30. Prados-Rosales R, Baena A, Martinez LR, Luque-Garcia J, Kalscheuer R, et al. (2011) Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice. J Clin Invest121: 1471–1483. doi: 10.1172/JCI4426121364279
31. Keenan J, Day T, Neal S, Cook B, Perez-Perez G, et al. (2000) A role for the bacterial outer membrane in the pathogenesis of Helicobacter pylori infection. FEMS Microbiol Lett182: 259–264. 10620676
32. Bielaszewska M, Ruter C, Kunsmann L, Greune L, Bauwens A, et al. (2013) Enterohemorrhagic Escherichia coli hemolysin employs outer membrane vesicles to target mitochondria and cause endothelial and epithelial apoptosis. PLoS Pathog9: e1003797. doi: 10.1371/journal.ppat.100379724348251
33. Chatterjee D, Chaudhuri K, (2013) Vibrio cholerae O395 outer membrane vesicles modulate intestinal epithelial cells in a NOD1 protein-dependent manner and induce dendritic cell-mediated Th2/Th17 cell responses. J Biol Chem288: 4299–4309. doi: 10.1074/jbc.M112.40830223275338
34. Lee JH, Choi CW, Lee T, Kim SI, Lee JC, et al. (2013) Transcription factor sigmaB plays an important role in the production of extracellular membrane-derived vesicles in Listeria monocytogenes. PLoS One8: e73196. doi: 10.1371/journal.pone.007319623977379
35. Carey AJ, Tan CK, Mirza S, Irving-Rodgers H, Webb RI, et al. (2014) Infection and cellular defense dynamics in a novel 17beta-estradiol murine model of chronic human group B streptococcus genital tract colonization reveal a role for hemolysin in persistence and neutrophil accumulation. J Immunol192: 1718–1731. doi: 10.4049/jimmunol.120281124453257
36. Renelli M, Matias V, Lo RY, Beveridge TJ, (2004) DNA-containing membrane vesicles of Pseudomonas aeruginosa PAO1 and their genetic transformation potential. Microbiology150: 2161–2169. 15256559
37. Perez-Cruz C, Carrion O, Delgado L, Martinez G, Lopez-Iglesias C, et al. (2013) New type of outer membrane vesicle produced by the Gram-negative bacterium Shewanella vesiculosa M7T: implications for DNA content. Appl Environ Microbiol79: 1874–1881. doi: 10.1128/AEM.03657-1223315742
38. Yaron S, Kolling GL, Simon L, Matthews KR, (2000) Vesicle-mediated transfer of virulence genes from Escherichia coli O157:H7 to other enteric bacteria. Appl Environ Microbiol66: 4414–4420. 11010892
39. Haurat MF, Aduse-Opoku J, Rangarajan M, Dorobantu L, Gray MR, et al. (2011) Selective sorting of cargo proteins into bacterial membrane vesicles. J Biol Chem286: 1269–1276. doi: 10.1074/jbc.M110.18574421056982
40. Elhenawy W, Debelyy MO, Feldman MF, (2014) Preferential packing of acidic glycosidases and proteases into Bacteroides outer membrane vesicles. MBio5: e00909–00914. doi: 10.1128/mBio.00909-1424618254
41. Malak TM, Ockleford CD, Bell SC, Dalgleish R, Bright N, et al. (1993) Confocal immunofluorescence localization of collagen types I, III, IV, V and VI and their ultrastructural organization in term human fetal membranes. Placenta14: 385–406. 8248033
42. Malak TM, Bell SC, (1994) Structural characteristics of term human fetal membranes: a novel zone of extreme morphological alteration within the rupture site. Br J Obstet Gynaecol101: 375–386. 8018607
43. Skinner SJ, Campos GA, Liggins GC, (1981) Collagen content of human amniotic membranes: effect of gestation length and premature rupture. Obstet Gynecol57: 487–489. 7243099
44. Vornhagen J, Quach P, Boldenow E, Merillat S, Whidbey C, et al. (2016) Bacterial Hyaluronidase Promotes Ascending GBS Infection and Preterm Birth. MBio7.
45. Kacerovsky M, Pliskova L, Bolehovska R, Musilova I, Hornychova H, et al. (2011) The microbial load with genital mycoplasmas correlates with the degree of histologic chorioamnionitis in preterm PROM. Am J Obstet Gynecol205: 213 e211–217.
46. Shobokshi A, Shaarawy M, (2002) Maternal serum and amniotic fluid cytokines in patients with preterm premature rupture of membranes with and without intrauterine infection. Int J Gynaecol Obstet79: 209–215. 12445984
47. Romero R, Miranda J, Chaiworapongsa T, Korzeniewski SJ, Chaemsaithong P, et al. (2014) Prevalence and clinical significance of sterile intra-amniotic inflammation in patients with preterm labor and intact membranes. Am J Reprod Immunol72: 458–474. doi: 10.1111/aji.1229625078709
48. Jacobsson B, Mattsby-Baltzer I, Andersch B, Bokstrom H, Holst RM, et al. (2003) Microbial invasion and cytokine response in amniotic fluid in a Swedish population of women with preterm prelabor rupture of membranes. Acta Obstet Gynecol Scand82: 423–431. 12752072
49. DiGiulio DB, Romero R, Kusanovic JP, Gomez R, Kim CJ, et al. (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 Immunol64: 38–57. doi: 10.1111/j.1600-0897.2010.00830.x20331587
50. Kacerovsky M, Musilova I, Khatibi A, Skogstrand K, Hougaard DM, et al. (2012) Intraamniotic inflammatory response to bacteria: analysis of multiple amniotic fluid proteins in women with preterm prelabor rupture of membranes. J Matern Fetal Neonatal Med25: 2014–2019. doi: 10.3109/14767058.2012.67187322519389
51. Choi GB, Yim YS, Wong H, Kim S, Kim H, et al. (2016) The maternal interleukin-17a pathway in mice promotes autism-like phenotypes in offspring. Science351: 933–939. doi: 10.1126/science.aad031426822608
52. Bomberger JM, Maceachran DP, Coutermarsh BA, Ye S, O'Toole GA, et al. (2009) Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog5: e1000382. doi: 10.1371/journal.ppat.100038219360133
53. Thay B, Wai SN, Oscarsson J, (2013) Staphylococcus aureus alpha-toxin-dependent induction of host cell death by membrane-derived vesicles. PLoS One8: e54661. doi: 10.1371/journal.pone.005466123382935
54. Jung AL, Stoiber C, Herkt CE, Schulz C, Bertrams W, et al. (2016) Legionella pneumophila-Derived Outer Membrane Vesicles Promote Bacterial Replication in Macrophages. PLoS Pathog12: e1005592. doi: 10.1371/journal.ppat.100559227105429
55. Eisenman HC, Frases S, Nicola AM, Rodrigues ML, Casadevall A, (2009) Vesicle-associated melanization in Cryptococcus neoformans. Microbiology155: 3860–3867. doi: 10.1099/mic.0.032854-019729402
56. Basu B, Apte SK, (2012) Gamma radiation-induced proteome of Deinococcus radiodurans primarily targets DNA repair and oxidative stress alleviation. Mol Cell Proteomics11: M111 011734. doi: 10.1074/mcp.M111.01173421989019
57. Chatterjee D, Chaudhuri K, (2011) Association of cholera toxin with Vibrio cholerae outer membrane vesicles which are internalized by human intestinal epithelial cells. FEBS Lett585: 1357–1362. doi: 10.1016/j.febslet.2011.04.01721510946
58. Bangham AD, Standish MM, Watkins JC, (1965) Diffusion of univalent ions across the lamellae of swollen phospholipids. J Mol Biol13: 238–252. 5859039
59. Godbole G, Modi D, (2010) Regulation of decidualization, interleukin-11 and interleukin-15 by homeobox A 10 in endometrial stromal cells. J Reprod Immunol85: 130–139. doi: 10.1016/j.jri.2010.03.00320478621
60. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods25: 402–408. 11846609
61. Godbole GB, Modi DN, Puri CP, (2007) Regulation of homeobox A10 expression in the primate endometrium by progesterone and embryonic stimuli. Reproduction134: 513–523. 17709569
62. Junqueira LC, Bignolas G, Brentani RR, (1979) Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J11: 447–455. 91593