A hemolytic pigment of Group B Streptococcus allows bacterial penetration of human placenta

Journal of Experimental Medicine

Volumn 210, Issue 6, 2013, Pages 1265-1281

  Whidbey, Christopher ^a,b,c   Harrell, Maria Isabel ^b   Burnside, Kellie ^a   Ngo, Lisa ^b   Becraft, Alexis K ^b   Iyer, Lakshminarayan M ^d   Aravind, L ^d   Hitti, Jane ^a   Adams Waldorf, Kristina M ^a   Rajagopal, Lakshmi ^a,b,c  

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

^b SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOLYSIN; ORNITHINE; RHAMNOLIPID;

AMNION CELL; AMNION FLUID; ARTICLE; CELL ACTIVITY; CELL INVASION; CELL ISOLATION; CONTROLLED STUDY; FEMALE; FETUS MEMBRANE; GENE EXPRESSION; GENE MUTATION; HEMOLYSIS; HUMAN; NEWBORN MORTALITY; PLACENTA; PREMATURE LABOR; PRIORITY JOURNAL; REPRESSOR GENE; STREPTOCOCCUS AGALACTIAE;

AMNIOTIC FLUID; ENDOPEPTIDASE K; EPITHELIAL CELLS; FEMALE; FETUS; GLYCOLIPIDS; HEMOLYSIN PROTEINS; HUMANS; NF-KAPPA B; OBSTETRIC LABOR, PREMATURE; ORNITHINE; PIGMENTS, BIOLOGICAL; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS AGALACTIAE;

EID: 84880689891     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20122753     Document Type: Article

References (78)

1. Ala-Kokko, T.I., P. Myllynen, and K. Vahakangas. 2000. Ex vivo perfusion of the human placental cotyledon: implications for anesthetic pharmacology. Int. J. Obstet. Anesth. 9:26-38. http://dx.doi.org/10.1054/ijoa.1999.0312
2. Bebien, M., M.E. Hensler, S. Davanture, L.C. Hsu, M. Karin, J.M. Park, L. Alexopoulou, G.Y. Liu, V. Nizet, and T. Lawrence. 2012. The poreforming toxin β hemolysin/cytolysin triggers p38 MAPK-dependent IL-10 production in macrophages and inhibits innate immunity. PLoS Pathog. 8:e1002812. http://dx.doi.org/10.1371/journal.ppat.1002812
3. Behrman, R.E., and A.S. Butler, editors. 2007. Preterm Birth: Causes, Consequences and Prevention. The National Academies Press, Washington, D.C. 792 pp.
4. Bobitt, J.R., and W.J. Ledger. 1977. Unrecognized amnionitis and prematurity: a preliminary report. J. Reprod. Med. 19:8-12.
5. Bourne, G.L. 1960. The microscopic anatomy of the human amnion and chorion. Am. J. Obstet. Gynecol. 79:1070-1073.
6. Chaffin, D.O., and C.E. Rubens. 1998. Blue/white screening of recombinant plasmids in Gram-positive bacteria by interruption of alkaline phosphatase gene (phoZ) expression. Gene. 219:91-99. http://dx.doi.org/10.1016/S0378-1119(98)00396-5
7. Chaffin, D.O., S.B. Beres, H.H. Yim, and C.E. Rubens. 2000. The serotype of type Ia and III group B streptococci is determined by the polymerase gene within the polycistronic capsule operon. J. Bacteriol. 182:4466-4477. http://dx.doi.org/10.1128/JB.182.16.4466-4477.2000
8. Dal, M.-C., and H. Monteil. 1983. Hemolysin produced by group B Streptococcus agalactiae. FEMS Microbiol. Lett. 16:89-94. http://dx.doi.org/10.1111/j.1574-6968.1983.tb00265.x
9. de la Rosa, M., M. Perez, C. Carazo, L. Pareja, J.I. Peis, and F. Hernandez. 1992. New Granada Medium for detection and identification of group B streptococci. J. Clin. Microbiol. 30:1019-1021.
10. Doran, K.S., J.C. Chang, V.M. Benoit, L. Eckmann, and V. Nizet. 2002. Group B streptococcal beta-hemolysin/cytolysin promotes invasion of human lung epithelial cells and the release of interleukin-8. J. Infect. Dis. 185:196-203. http://dx.doi.org/10.1086/338475
11. Doran, K.S., E.J. Engelson, A. Khosravi, H.C. Maisey, I. Fedtke, O. Equils, K.S. Michelsen, M. Arditi, A. Peschel, and V. Nizet. 2005. Blood-brain barrier invasion by group B Streptococcus. proper cell-surface anchoring of lipoteichoic acid. J. Clin. Invest. 115:2499-2507. http://dx.doi.org/10.1172/JCI23829
12. Firon, A., A. Tazi, V. Da Cunha, S. Brinster, E. Sauvage, S. Dramsi, D.T. Golenbock, P. Glaser, C. Poyart, and P. Trieu-Cuot. 2013. The Abidomain protein Abx1 interacts with the CovS histidine kinase to control virulence gene expression in group B Streptococcus. PLoS Pathog. 9:e1003179. http://dx.doi.org/10.1371/journal.ppat.1003179
13. Forquin, M.P., A. Tazi, M. Rosa-Fraile, C. Poyart, P. Trieu-Cuot, and S. Dramsi. 2007. The putative glycosyltransferase-encoding gene cylJ and the group B Streptococcus (GBS)-specific gene cylK modulate hemolysin production and virulence of GBS. Infect. Immun. 75:2063-2066. http://dx.doi.org/10.1128/IAI.01565-06
14. Geiger, O., N. González-Silva, I.M. López-Lara, and C. Sohlenkamp. 2010. Amino acid-containing membrane lipids in bacteria. Prog. Lipid Res. 49:46-60. http://dx.doi.org/10.1016/j.plipres.2009.08.002
15. Giaever, I., and C.R. Keese. 1991. Micromotion of mammalian cells measured electrically. Proc. Natl. Acad. Sci. USA. 88:7896-7900. http://dx.doi.org/10.1073/pnas.88.17.7896
16. Giaever, I., and C.R. Keese. 1993. A morphological biosensor for mammalian cells. Nature. 366:591-592. http://dx.doi.org/10.1038/366591a0
17. Glaser, P., C. Rusniok, C. Buchrieser, F. Chevalier, L. Frangeul, T. Msadek, M. Zouine, E. Couvé, L. Lalioui, C. Poyart, et al. 2002. Genome sequence of Streptococcus agalactiae, a pathogen causing invasive neonatal disease. Mol. Microbiol. 45:1499-1513. http://dx.doi.org/10.1046/j.1365-2958.2002.03126.x
18. Goldenberg, R.L., J.C. Hauth, and W.W. Andrews. 2000. Intrauterine infection and preterm delivery. N. Engl. J. Med. 342:1500-1507. http://dx.doi.org/10.1056/NEJM200005183422007
19. Gonzalez, M.R., M. Bischofberger, L. Pernot, F.G. van der Goot, and B. Frêche. 2008. Bacterial pore-forming toxins: the (w)hole story? Cell. Mol. Life Sci. 65:493-507. http://dx.doi.org/10.1007/s00018-007-7434-y
20. Gotsch, F., R. Romero, J.P. Kusanovic, S. Mazaki-Tovi, B.L. Pineles, O. Erez, J. Espinoza, and S.S. Hassan. 2007. The fetal inflammatory response syndrome. Clin. Obstet. Gynecol. 50:652-683. http://dx.doi.org/10.1097/GRF.0b013e31811ebef6
21. Gottschalk, B., G. Bröker, M. Kuhn, S. Aymanns, U. Gleich-Theurer, and B. Spellerberg. 2006. Transport of multidrug resistance substrates by the Streptococcus agalactiae hemolysin transporter. J. Bacteriol. 188:5984-5992. http://dx.doi.org/10.1128/JB.00768-05
22. Gravett, M.G., C.E. Rubens, and T.M. Nunes; GAPPS Review Group. 2010. Global report on preterm birth and stillbirth (2 of 7): discovery science. BMC Pregnancy Childbirth. 10:S2. http://dx.doi.org/10.1186/1471-2393-10-S1-S2
23. Häussler, S., M. Nimtz, T. Domke, V. Wray, and I. Steinmetz. 1998. Purification and characterization of a cytotoxic exolipid of Burkholderia pseudomallei. Infect. Immun. 66:1588-1593.
24. Henneke, P., O. Takeuchi, R. Malley, E. Lien, R.R. Ingalls, M.W. Freeman, T. Mayadas, V. Nizet, S. Akira, D.L. Kasper, and D.T. Golenbock. 2002. Cellular activation, phagocytosis, and bactericidal activity against group B streptococcus involve parallel myeloid differentiation factor 88-dependent and independent signaling pathways. J. Immunol. 169:3970-3977.
25. Hensler, M.E., G.Y. Liu, S. Sobczak, K. Benirschke, V. Nizet, and G.P. Heldt. 2005. Virulence role of group B Streptococcus beta-hemolysin/cytolysin in a neonatal rabbit model of early-onset pulmonary infection. J. Infect. Dis. 191:1287-1291. http://dx.doi.org/10.1086/428946
26. Hillier, S.L., J. Martius, M. Krohn, N. Kiviat, K.K. Holmes, and D.A. Eschenbach. 1988. A case-control study of chorioamnionic infection and histologic chorioamnionitis in prematurity. N. Engl. J. Med. 319:972-978. http://dx.doi.org/10.1056/NEJM198810133191503
27. Hillier, S.L., M.A. Krohn, N.B. Kiviat, D.H. Watts, and D.A. Eschenbach. 1991. Microbiologic causes and neonatal outcomes associated with chorioamnion infection. Am. J. Obstet. Gynecol. 165:955-961. http://dx.doi.org/10.1016/0002-9378(91)90447-Y
28. Hitti, J., M.A. Krohn, D.L. Patton, P. Tarczy-Hornoch, S.L. Hillier, E.M. Cassen, and D.A. Eschenbach. 1997. Amniotic fluid tumor necrosis factor-alpha and the risk of respiratory distress syndrome among preterm infants. Am. J. Obstet. Gynecol. 177:50-56. http://dx.doi.org/10.1016/S0002-9378(97)70437-X
29. Horton, R.M. 1995. PCR-mediated recombination and mutagenesis. SOEing together tailor-made genes. Mol. Biotechnol. 3:93-99. http://dx.doi.org/10.1007/BF02789105
30. Hutson, J.R., F. Garcia-Bournissen, A. Davis, and G. Koren. 2011. The human placental perfusion model: a systematic review and development of a model to predict in vivo transfer of therapeutic drugs. Clin. Pharmacol. Ther. 19:67-76. http://dx.doi.org/10.1038/clpt.2011.66
31. Jiang, S.M., M.J. Cieslewicz, D.L. Kasper, and M.R. Wessels. 2005. Regulation of virulence by a two-component system in group B streptococcus. J. Bacteriol. 187:1105-1113. http://dx.doi.org/10.1128/JB.187.3.1105-1113.2005
32. Jiang, S.M., N. Ishmael, J. Dunning Hotopp, M. Puliti, L. Tissi, N. Kumar, M.J. Cieslewicz, H. Tettelin, and M.R. Wessels. 2008. Variation in the group B Streptococcus CsrRS regulon and effects on pathogenicity. J. Bacteriol. 190:1956-1965. http://dx.doi.org/10.1128/JB.01677-07
33. Kawai, Y., A. Moribayashi, and I. Yano. 1982. Ornithine-containing lipid of Bordetella pertussis that carries hemagglutinating activity. J. Bacteriol. 152:907-910.
34. Knopik-Skrocka, A., and J. Bielawski. 2002. The mechanism of the hemolytic activity of polyene antibiotics. Cell. Mol. Biol. Lett. 7:31-48.
35. Lamy, M.C., M. Zouine, J. Fert, M. Vergassola, E. Couve, E. Pellegrini, P. Glaser, F. Kunst, T. Msadek, P. Trieu-Cuot, and C. Poyart. 2004. CovS/CovR of group B streptococcus: a two-component global regulatory system involved in virulence. Mol. Microbiol. 54:1250-1268. http://dx.doi.org/10.1111/j.1365-2958.2004.04365.x
36. Lancefield, R.C., M. McCarty, and W.N. Everly. 1975. Multiple mouseprotective antibodies directed against group B streptococci. Special reference to antibodies effective against protein antigens. J. Exp. Med. 142: 165-179. http://dx.doi.org/10.1084/jem.142.1.165
37. Ledger, W.J. 2008. Perinatal infections and fetal/neonatal brain injury. Curr. Opin. Obstet. Gynecol. 20:120-124. http://dx.doi.org/10.1097/GCO.0b013e3282f734db
38. Lembo, A., M.A. Gurney, K. Burnside, A. Banerjee, M. de los Reyes, J.E. Connelly, W.J. Lin, K.A. Jewell, A. Vo, C.W. Renken, et al. 2010. Regulation of CovR expression in Group B Streptococcus impacts blood-brain barrier penetration. Mol. Microbiol. 77:431-443. http://dx.doi.org/10.1111/j.1365-2958.2010.07215.x
39. Lin, W.J., D. Walthers, J.E. Connelly, K. Burnside, K.A. Jewell, L.J. Kenney, and L. Rajagopal. 2009. Threonine phosphorylation prevents promoter DNA binding of the Group B Streptococcus response regulator CovR. Mol. Microbiol. 71:1477-1495. http://dx.doi.org/10.1111/j.1365-2958.2009.06616.x
40. Liu, G.Y., K.S. Doran, T. Lawrence, N. Turkson, M. Puliti, L. Tissi, and V. Nizet. 2004. Sword and shield: linked group B streptococcal betahemolysin/cytolysin and carotenoid pigment function to subvert host phagocyte defense. Proc. Natl. Acad. Sci. USA. 101:14491-14496. http://dx.doi.org/10.1073/pnas.0406143101
41. Lukacs, S.L., K.C. Schoendorf, and A. Schuchat. 2004. Trends in sepsis-related neonatal mortality in the United States, 1985-1998. Pediatr. Infect. Dis. J. 23:599-603. http://dx.doi.org/10.1097/01.inf.0000131633.74921.90
42. Maione, D., I. Margarit, C.D. Rinaudo, V. Masignani, M. Mora, M. Scarselli, H. Tettelin, C. Brettoni, E.T. Iacobini, R. Rosini, et al. 2005. Identification of a universal Group B streptococcus vaccine by multiple genome screen. Science. 309:148-150. http://dx.doi.org/10.1126/science.1109869
43. Marchlewicz, B.A., and J.L. Duncan. 1980. Properties of a hemolysin produced by group B streptococci. Infect. Immun. 30:805-813.
44. Marchlewicz, B.A., and J.L. Duncan. 1981. Lysis of erythrocytes by a hemolysin produced by a group B Streptococcus sp. Infect. Immun. 34:787-794.
45. Martin, T.R., C.E. Rubens, and C.B. Wilson. 1988. Lung antibacterial defense mechanisms in infant and adult rats: implications for the pathogenesis of group B streptococcal infections in the neonatal lung. J. Infect. Dis. 157:91-100. http://dx.doi.org/10.1093/infdis/157.1.91
46. Musser, J.M., S.J. Mattingly, R. Quentin, A. Goudeau, and R.K. Selander. 1989. Identification of a high-virulence clone of type III Streptococcus agalactiae (group B Streptococcus) causing invasive neonatal disease. Proc. Natl. Acad. Sci. USA. 86:4731-4735. http://dx.doi.org/10.1073/pnas.86.12.4731
47. Naeye, R.L., and E.C. Peters. 1978. Amniotic fluid infections with intact membranes leading to perinatal death: a prospective study. Pediatrics. 61:171-177.
48. Nizet, V. 2002. Streptococcal beta-hemolysins: genetics and role in disease pathogenesis. Trends Microbiol. 10:575-580. http://dx.doi.org/10.1016/S0966-842X(02)02473-3
49. Nizet, V., R.L. Gibson, E.Y. Chi, P.E. Framson, M. Hulse, and C.E. Rubens. 1996. Group B streptococcal beta-hemolysin expression is associated with injury of lung epithelial cells. Infect. Immun. 64:3818-3826.
50. Nizet, V., K.S. Kim, M. Stins, M. Jonas, E.Y. Chi, D. Nguyen, and C.E. Rubens. 1997. Invasion of brain microvascular endothelial cells by group B streptococci. Infect. Immun. 65:5074-5081.
51. Okada, N., R.T. Geist, and M.G. Caparon. 1993. Positive transcriptional control of mry regulates virulence in the group A streptococcus. Mol. Microbiol. 7:893-903. http://dx.doi.org/10.1111/j.1365-2958.1993.tb01180.x
52. Pritzlaff, C.A., J.C. Chang, S.P. Kuo, G.S. Tamura, C.E. Rubens, and V. Nizet. 2001. Genetic basis for the beta-haemolytic/cytolytic activity of group B Streptococcus. Mol. Microbiol. 39:236-247. http://dx.doi.org/10.1046/j.1365-2958.2001.02211.x
53. Puopolo, K.M. 2008. Epidemiology of Neonatal Early-onset Sepsis. NeoReviews. 9:e571-e579. http://dx.doi.org/10.1542/neo.9-12-e571
54. Rajagopal, L., A. Clancy, and C.E. Rubens. 2003. A eukaryotic type serine/threonine kinase and phosphatase in Streptococcus agalactiae reversibly phosphorylate an inorganic pyrophosphatase and affect growth, cell segregation, and virulence. J. Biol. Chem. 278:14429-14441. http://dx.doi.org/10.1074/jbc. M212747200
55. Rajagopal, L., A. Vo, A. Silvestroni, and C.E. Rubens. 2006. Regulation of cytotoxin expression by converging eukaryotic-type and twocomponent signalling mechanisms in Streptococcus agalactiae. Mol. Microbiol. 62:941-957. http://dx.doi.org/10.1111/j.1365-2958.2006.05431.x
56. Romero, R., D.T. Brody, E. Oyarzun, M. Mazor, Y.K. Wu, J.C. Hobbins, and S.K. Durum. 1989a. Infection and labor. III. Interleukin-1: a signal for the onset of parturition. Am. J. Obstet. Gynecol. 160:1117-1123. http://dx.doi.org/10.1016/0002-9378(89)90172-5
57. Romero, R., K.R. Manogue, M.D. Mitchell, Y.K. Wu, E. Oyarzun, J.C. Hobbins, and A. Cerami. 1989b. Infection and labor. IV. Cachectintumor necrosis factor in the amniotic fluid of women with intraamniotic infection and preterm labor. Am. J. Obstet. Gynecol. 161:336-341. http://dx.doi.org/10.1016/0002-9378(89)90515-2
58. Romero, R., M. Sirtori, E. Oyarzun, C. Avila, M. Mazor, R. Callahan, V. Sabo, A.P. Athanassiadis, and J.C. Hobbins. 1989c. Infection and labor. V. Prevalence, microbiology, and clinical significance of intraamniotic infection in women with preterm labor and intact membranes. Am. J. Obstet. Gynecol. 161:817-824. http://dx.doi.org/10.1016/0002-9378(89)90409-2
59. Romero, R., C. Avila, U. Santhanam, and P.B. Sehgal. 1990. Amniotic fluid interleukin 6 in preterm labor. Association with infection. J. Clin. Invest. 85:1392-1400. http://dx.doi.org/10.1172/JCI114583
60. Romero, R., M. Ceska, C. Avila, M. Mazor, E. Behnke, and I. Lindley. 1991. Neutrophil attractant/activating peptide-1/interleukin-8 in term and preterm parturition. Am. J. Obstet. Gynecol. 165:813-820. http://dx.doi.org/10.1016/0002-9378(91)90422-N
61. Rosa-Fraile, M., J. Rodríguez-Granger, A. Haidour-Benamin, J.M. Cuerva, and A. Sampedro. 2006. Granadaene: proposed structure of the group B Streptococcus polyenic pigment. Appl. Environ. Microbiol. 72:6367-6370. http://dx.doi.org/10.1128/AEM.00756-06
62. Sánchez, M., F.J. Aranda, J.A. Teruel, M.J. Espuny, A. Marqués, A. Manresa, and A. Ortiz. 2010. Permeabilization of biological and artificial membranes by a bacterial dirhamnolipid produced by Pseudomonas aeruginosa. J. Colloid Interface Sci. 341:240-247. http://dx.doi.org/10.1016/j.jcis.2009.09.042
63. Santi, I., R. Grifantini, S.M. Jiang, C. Brettoni, G. Grandi, M.R. Wessels, and M. Soriani. 2009. CsrRS regulates group B Streptococcus virulence gene expression in response to environmental pH: a new perspective on vaccine development. J. Bacteriol. 191:5387-5397. http://dx.doi.org/10.1128/JB.00370-09
64. Spellerberg, B., B. Pohl, G. Haase, S. Martin, J. Weber-Heynemann, and R. Lütticken. 1999. Identification of genetic determinants for the hemolytic activity of Streptococcus agalactiae by ISS1 transposition. J. Bacteriol. 181:3212-3219.
65. Spellerberg, B., S. Martin, C. Brandt, and R. Lütticken. 2000. The cyl genes of Streptococcus agalactiae are involved in the production of pigment. FEMS Microbiol. Lett. 188:125-128. http://dx.doi.org/10.1111/j.1574-6968.2000.tb09182.x
66. Stevens, A.M., and J.D. Bancroft. 1977. Theory and Practice of Histological Techniques. Churchill Livingstone, Edinburgh. 436 pp.
67. Sun, K., R. Ma, X. Cui, B. Campos, R. Webster, D. Brockman, and L. Myatt. 2003. Glucocorticoids induce cytosolic phospholipase A2 and prostaglandin H synthase type 2 but not microsomal prostaglandin E synthase (PGES) and cytosolic PGES expression in cultured primary human amnion cells. J. Clin. Endocrinol. Metab. 88:5564-5571. http://dx.doi.org/10.1210/jc.2003-030875
68. Tapsall, J.W. 1987. Relationship between pigment production and haemolysin formation by Lancefield group B streptococci. J. Med. Microbiol. 24:83-87. http://dx.doi.org/10.1099/00222615-24-1-83
69. Tapsall, J.W., and E.A. Phillips. 1991. The hemolytic and cytolytic activity of group B streptococcal hemolysin and its possible role in early onset group B streptococcal disease. Pathology. 23:139-144. http://dx.doi.org/10.3109/00313029109060813
70. Tettelin, H., V. Masignani, M.J. Cieslewicz, C. Donati, D. Medini, N.L. Ward, S.V. Angiuoli, J. Crabtree, A.L. Jones, A.S. Durkin, et al. 2005. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome". Proc. Natl. Acad. Sci. USA. 102:13950-13955. http://dx.doi.org/10.1073/pnas.0506758102
71. van Sorge, N.M., D. Quach, M.A. Gurney, P.M. Sullam, V. Nizet, and K.S. Doran. 2009. The group B streptococcal serine-rich repeat 1 glycoprotein mediates penetration of the blood-brain barrier. J. Infect. Dis. 199:1479-1487. http://dx.doi.org/10.1086/598217
72. Vanberg, C., B.F. Lutnaes, T. Langsrud, I.F. Nes, and H. Holo. 2007. Propionibacterium jensenii produces the polyene pigment granadaene and has hemolytic properties similar to those of Streptococcus agalactiae. Appl. Environ. Microbiol. 73:5501-5506. http://dx.doi.org/10.1128/AEM.00545-07
73. Verani, J.R., L. McGee, and S.J. Schrag; Division of Bacterial Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention (CDC). 2010. Prevention of perinatal group B streptococcal disease-revised guidelines from CDC, 2010. MMWR Recomm. Rep. 59(RR-10):1-36.
74. Watts, D.H., M.A. Krohn, S.L. Hillier, and D.A. Eschenbach. 1992. The association of occult amniotic fluid infection with gestational age and neonatal outcome among women in preterm labor. Obstet. Gynecol. 79: 351-357. http://dx.doi.org/10.1097/00006250-199203000-00005
75. Weston, E.J., T. Pondo, M.M. Lewis, P. Martell-Cleary, C. Morin, B. Jewell, P. Daily, M. Apostol, S. Petit, M. Farley, et al. 2011. The burden of invasive early-onset neonatal sepsis in the United States, 2005-2008. Pediatr. Infect. Dis. J. 30:937-941. http://dx.doi.org/10.1097/INF.0b013e318223bad2
76. Winram, S.B., M. Jonas, E. Chi, and C.E. Rubens. 1998. Characterization of group B streptococcal invasion of human chorion and amnion epithelial cells In vitro. Infect. Immun. 66:4932-4941.
77. Yoon, B.H., R. Romero, J.S. Park, C.J. Kim, S.H. Kim, J.H. Choi, and T.R. Han. 2000. Fetal exposure to an intra-amniotic inflammation and the development of cerebral palsy at the age of three years. Am. J. Obstet. Gynecol. 182:675-681. http://dx.doi.org/10.1067/mob.2000.104207
78. Zaga-Clavellina, V., G. Garcia-Lopez, H. Flores-Herrera, A. Espejel-Nuñez, A. Flores-Pliego, D. Soriano-Becerril, R. Maida-Claros, H. Merchant-Larios, and F. Vadillo-Ortega. 2007. In vitro secretion profiles of interleukin (IL)-1beta, IL-6, IL-8, IL-10, and TNF alpha after selective infection with Escherichia coli in human fetal membranes. Reprod. Biol. Endocrinol. 5:46. http://dx.doi.org/10.1186/1477-7827-5-46