A live attenuated vaccine to prevent severe neonatal Escherichia coli K1 infections.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
08 Apr 2024
08 Apr 2024
Historique:
received:
25
08
2023
accepted:
11
03
2024
medline:
9
4
2024
pubmed:
9
4
2024
entrez:
8
4
2024
Statut:
epublish
Résumé
Preterm birth is currently the leading cause of neonatal morbidity and mortality. Genetic, immunological and infectious causes are suspected. Preterm infants have a higher risk of severe bacterial neonatal infections, most of which are caused by Escherichia coli an in particular E. coli K1strains. Women with history of preterm delivery have a high risk of recurrence and therefore constitute a target population for the development of vaccine against E. coli neonatal infections. Here, we characterize the immunological, microbiological and protective properties of a live attenuated vaccine candidate in adult female mice and their pups against after a challenge by K1 and non-K1 strains of E. coli. Our results show that the E. coli K1 E11 ∆aroA vaccine induces strong immunity, driven by polyclonal bactericidal antibodies. In our model of meningitis, mothers immunized prior to mating transfer maternal antibodies to pups, which protect newborn mice against various K1 and non-K1 strains of E. coli. Given the very high mortality rate and the neurological sequalae associated with neonatal E. coli K1 meningitis, our results constitute preclinical proof of concept for the development of a live attenuated vaccine against severe E. coli infections in women at risk of preterm delivery.
Identifiants
pubmed: 38589401
doi: 10.1038/s41467-024-46775-x
pii: 10.1038/s41467-024-46775-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3021Subventions
Organisme : Agence Nationale de la Recherche (French National Research Agency)
ID : AAPG2020
Informations de copyright
© 2024. The Author(s).
Références
Vogel, J. P. et al. The global epidemiology of preterm birth. Best. Pract. Res. Clin. Obstet. Gynaecol. 52, 3–12 (2018).
pubmed: 29779863
doi: 10.1016/j.bpobgyn.2018.04.003
Blencowe, H. et al. National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet 379, 2162–2172 (2012).
pubmed: 22682464
doi: 10.1016/S0140-6736(12)60820-4
Walani, S. R. Global burden of preterm birth. Int. J. Gynecol. Obstet. 150, 31–33 (2020).
doi: 10.1002/ijgo.13195
Goldenberg, R. L., Culhane, J. F., Iams, J. D. & Romero, R. Epidemiology and causes of preterm birth. Lancet 371, 75–84 (2008).
pubmed: 18177778
pmcid: 7134569
doi: 10.1016/S0140-6736(08)60074-4
Romero, R. et al. The preterm parturition syndrome. BJOG 113, 17–42 (2006).
pubmed: 17206962
pmcid: 7062298
doi: 10.1111/j.1471-0528.2006.01120.x
Sikias, P. et al. Early-onset neonatal sepsis in the Paris area: a population-based surveillance study from 2019 to 2021. Arch. Dis. Child Fetal Neonatal Ed. 108, 114–120 (2023).
pubmed: 35902218
doi: 10.1136/archdischild-2022-324080
Collins, A., Weitkamp, J.-H. & Wynn, J. L. Why are preterm newborns at increased risk of infection? Arch. Dis. Child Fetal Neonatal Ed. 103, F391–F394 (2018).
pubmed: 29382648
doi: 10.1136/archdischild-2017-313595
Pammi, M. & Brocklehurst, P. Granulocyte transfusions for neonates with confirmed or suspected sepsis and neutropenia. Cochrane Database Syst. Rev. 2011, CD003956 (2011).
pubmed: 21975741
pmcid: 7104253
Bae, Y. M. et al. Effect of exogenous surfactant therapy on levels of pulmonary surfactant proteins A and D in preterm infants with respiratory distress syndrome. J. Perinat. Med 37, 561–564 (2009).
pubmed: 19492923
doi: 10.1515/JPM.2009.100
McGreal, E. P., Hearne, K. & Spiller, O. B. Off to a slow start: under-development of the complement system in term newborns is more substantial following premature birth. Immunobiology 217, 176–186 (2012).
pubmed: 21868122
doi: 10.1016/j.imbio.2011.07.027
Stoll, B. J. et al. Early-Onset Neonatal Sepsis 2015 to 2017, the Rise of Escherichia coli, and the Need for Novel Prevention Strategies. JAMA Pediatr. 174, e200593 (2020).
pubmed: 32364598
pmcid: 7199167
doi: 10.1001/jamapediatrics.2020.0593
Dawson, K. G., Emerson, J. C. & Burns, J. L. Fifteen years of experience with bacterial meningitis. Pediatr. Infect. Dis. J. 18, 816–822 (1999).
pubmed: 10493344
doi: 10.1097/00006454-199909000-00014
Gaschignard, J., Levy, C., Bingen, E. & Cohen, R. Épidémiologie des méningites néonatales à Escherichia coli. Arch. de. Pédiatrie 19, S129–S134 (2012).
doi: 10.1016/S0929-693X(12)71286-1
Krohn, M. A., Thwin, S. S., Rabe, L. K., Brown, Z. & Hillier, S. L. Vaginal colonization by Escherichia coli as a risk factor for very low birth weight delivery and other perinatal complications. J. Infect. Dis. 175, 606–610 (1997).
pubmed: 9041332
doi: 10.1093/infdis/175.3.606
Gu, H. et al. Rational design and evaluation of an artificial Escherichia coli K1 protein vaccine candidate based on the structure of ompA. Front. Cell Infect. Microbiol. 8, 172 (2018).
pubmed: 29876324
pmcid: 5974202
doi: 10.3389/fcimb.2018.00172
Zhang, J. et al. Development of a chitosan‐modified PLGA nanoparticle vaccine for protection against Escherichia coli K1 caused meningitis in mice. J. Nanobiotechnol. 19, 69 (2021).
doi: 10.1186/s12951-021-00812-9
Patel, C. D. et al. Maternal immunization confers protection against neonatal herpes simplex mortality and behavioral morbidity. Sci. Transl. Med. 11, eaau6039 (2019).
pubmed: 30971454
pmcid: 6681804
doi: 10.1126/scitranslmed.aau6039
Shan, C. et al. Maternal vaccination and protective immunity against Zika virus vertical transmission. Nat. Commun. 10, 5677 (2019).
pubmed: 31831806
pmcid: 6908683
doi: 10.1038/s41467-019-13589-1
Locht, C. & Mielcarek, N. Live attenuated vaccines against pertussis. Expert Rev. Vaccines 13, 1147–1158 (2014).
pubmed: 25085735
doi: 10.1586/14760584.2014.942222
Gruslin, A. et al. Immunization in pregnancy. J. Obstet. Gynaecol. Can. 31, 1085–1101 (2009).
pubmed: 20175349
doi: 10.1016/S1701-2163(16)34354-7
MPH, I. T. G. Vaccines For Women: Before Conception, During Pregnancy, And After a Birth. https://www.health.harvard.edu/blog/vaccines-for-women-before-conception-during-pregnancy-and-after-a-birth-2020011018649 (2020).
Ministry of Health, State of Israel. Vaccines for Women Before Pregnancy, During Pregnancy and After Childbirth. https://www.health.gov.il/English/Topics/Pregnancy/during/Pages/vaccine_pregnant.aspx (2024).
Pons, S. et al. A high-throughput sequencing approach identifies immunotherapeutic targets for bacterial meningitis in neonates. EBioMedicine 88, 104439 (2023).
pubmed: 36709579
pmcid: 9900374
doi: 10.1016/j.ebiom.2023.104439
Xing, X.-J. et al. Functional characterization of 5-enopyruvylshikimate-3-phosphate synthase from alkaliphilus metalliredigens in transgenic Arabidopsis. J. Microbiol. Biotechnol. 24, 1421–1426 (2014).
pubmed: 24931502
doi: 10.4014/jmb.1404.04023
Lemaître, C. et al. The ssbL gene harbored by the ColV plasmid of an Escherichia coli neonatal meningitis strain is an auxiliary virulence factor boosting the production of siderophores through the shikimate pathway. J. Bacteriol. 196, 1343–1349 (2014).
pubmed: 24443535
pmcid: 3993347
doi: 10.1128/JB.01153-13
Felgner, S. et al. aroA-deficient salmonella enterica serovar typhimurium is more than a metabolically attenuated mutant. mBio 7, e01220–16 (2016).
pubmed: 27601574
pmcid: 5013297
doi: 10.1128/mBio.01220-16
Priebe, G. P. et al. Construction and characterization of a live, attenuated aroA deletion mutant of pseudomonas aeruginosa as a candidate intranasal vaccine. Infect. Immun. 70, 1507–1517 (2002).
pubmed: 11854239
pmcid: 127764
doi: 10.1128/IAI.70.3.1507-1517.2002
Galal, H. M., Abdrabou, M. I., Faraag, A. H. I., Mah, C. K. & Tawfek, A. M. Evaluation of commercially available aroA delated gene E. coli O78 vaccine in commercial broiler chickens under middle east simulating field conditions. Sci. Rep. 11, 1938 (2021).
pubmed: 33479449
pmcid: 7820230
doi: 10.1038/s41598-021-81523-x
Sebkova, A., Karasova, D., Crhanova, M., Budinska, E. & Rychlik, I. aro Mutations in salmonella enterica cause defects in cell wall and outer membrane integrity. J. Bacteriol. 190, 3155–3160 (2008).
pubmed: 18310348
pmcid: 2347392
doi: 10.1128/JB.00053-08
Barbagelata, M. S. et al. Auxotrophic mutant of staphylococcus aureus interferes with nasal colonization by the wild type. Microbes Infect. 13, 1081–1090 (2011).
pubmed: 21784166
doi: 10.1016/j.micinf.2011.06.010
Liu, R. et al. CD48 and α7 nicotinic acetylcholine receptor synergistically regulate FimH-mediated escherichia coli K1 penetration and neutrophil transmigration across human brain microvascular endothelial cells. J. Infect. Dis. 219, 470–479 (2019).
pubmed: 30202861
doi: 10.1093/infdis/jiy531
Khan, N. A., Kim, Y., Shin, S. & Kim, K. S. FimH-mediated escherichia coli K1 invasion of human brain microvascular endothelial cells. Cell. Microbiol. 9, 169–178 (2007).
pubmed: 17222190
doi: 10.1111/j.1462-5822.2006.00779.x
Datsenko, K. A. & Wanner, B. L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA 97, 6640–6645 (2000).
pubmed: 10829079
pmcid: 18686
doi: 10.1073/pnas.120163297
Klemm, P. Two regulatory fim genes, fimB and fimE, control the phase variation of type 1 fimbriae in Escherichia coli. EMBO J. 5, 1389–1393 (1986).
pubmed: 2874022
pmcid: 1166953
doi: 10.1002/j.1460-2075.1986.tb04372.x
Lemaître, C., Bidet, P., Bingen, E. & Bonacorsi, S. Transcriptional analysis of the Escherichia coli ColV-Ia plasmid pS88 during growth in human serum and urine. BMC Microbiol 12, 115 (2012).
pubmed: 22720670
pmcid: 3438092
doi: 10.1186/1471-2180-12-115
Wijetunge, D. S. S. et al. Characterizing the pathotype of neonatal meningitis causing Escherichia coli (NMEC). BMC Microbiol 15, 211 (2015).
pubmed: 26467858
pmcid: 4606507
doi: 10.1186/s12866-015-0547-9
Pluschke, G., Mayden, J., Achtman, M. & Levine, R. P. Role of the capsule and the O antigen in resistance of O18:K1 Escherichia coli to complement-mediated killing. Infect. Immun. 42, 907–913 (1983).
pubmed: 6196296
pmcid: 264385
doi: 10.1128/iai.42.3.907-913.1983
Weiss, J., Victor, M., Cross, A. S. & Elsbach, P. Sensitivity of K1-encapsulated Escherichia coli to killing by the bactericidal/permeability-increasing protein of rabbit and human neutrophils. Infect. Immun. 38, 1149–1153 (1982).
pubmed: 6759406
pmcid: 347869
doi: 10.1128/iai.38.3.1149-1153.1982
Arredondo-Alonso, S. et al. Evolutionary and functional history of the Escherichia coli K1 capsule. Nat. Commun. 14, 3294 (2023).
pubmed: 37322051
pmcid: 10272209
doi: 10.1038/s41467-023-39052-w
Zhu, M. et al. Multi-drug resistant Escherichia coli causing early-onset neonatal sepsis—a single center experience from China. Infect. Drug Resist. 12, 3695–3702 (2019).
pubmed: 31819551
pmcid: 6885540
doi: 10.2147/IDR.S229799
Li, Y. Y., Kong, C. W. & To, W. W. K. Pathogens in preterm prelabour rupture of membranes and erythromycin for antibiotic prophylaxis: a retrospective analysis. Hong. Kong Med J. 25, 287–294 (2019).
pubmed: 31402340
Yamamoto, T. et al. Electron microscopic structures, serum resistance, and plasmid restructuring of New Delhi metallo-β-lactamase-1 (NDM-1)-producing ST42 Klebsiella pneumoniae emerging in Japan. J. Infect. Chemother. 19, 118–127 (2013).
pubmed: 22971935
doi: 10.1007/s10156-012-0470-z
Blanco, J. et al. National survey of Escherichia coli causing extraintestinal infections reveals the spread of drug-resistant clonal groups O25b:H4-B2-ST131, O15:H1-D-ST393 and CGA-D-ST69 with high virulence gene content in Spain. J. Antimicrob. Chemother. 66, 2011–2021 (2011)
Liu, Y. et al. Escherichia coli causing neonatal meningitis during 2001–2020: a study in eastern China. Int J. Gen. Med 14, 3007–3016 (2021).
pubmed: 34234530
pmcid: 8254664
doi: 10.2147/IJGM.S317299
Basmaci, R. et al. Escherichia coli meningitis features in 325 children from 2001 to 2013 in France. Clin. Infect. Dis. 61, 779–786 (2015).
pubmed: 25944342
doi: 10.1093/cid/civ367
Shan, C. et al. A single-dose live-attenuated vaccine prevents Zika virus pregnancy transmission and testis damage. Nat. Commun. 8, 676 (2017).
pubmed: 28939807
pmcid: 5610254
doi: 10.1038/s41467-017-00737-8
Griffin, D. E. Measles vaccine. Viral Immunol. 31, 86–95 (2018).
pubmed: 29256824
pmcid: 5863094
doi: 10.1089/vim.2017.0143
Zinkernagel, R. M. Maternal antibodies, childhood infections, and autoimmune diseases. N. Engl. J. Med. 345, 1331–1335 (2001).
pubmed: 11794153
doi: 10.1056/NEJMra012493
Hurley, W. L. & Theil, P. K. Perspectives on immunoglobulins in colostrum and milk. Nutrients 3, 442–474 (2011).
pubmed: 22254105
pmcid: 3257684
doi: 10.3390/nu3040442
Stentebjerg-Olesen, B., Chakraborty, T. & Klemm, P. Type 1 fimbriation and phase switching in a natural Escherichia coli fimB null strain, nissle 1917. J. Bacteriol. 181, 7470–7478 (1999).
pubmed: 10601203
pmcid: 94203
doi: 10.1128/JB.181.24.7470-7478.1999
Nimmerjahn, F., Bruhns, P., Horiuchi, K. & Ravetch, J. V. FcgammaRIV: a novel FcR with distinct IgG subclass specificity. Immunity 23, 41–51 (2005).
pubmed: 16039578
doi: 10.1016/j.immuni.2005.05.010
Mendoza-Palomar, N. et al. Escherichia coli early-onset sepsis: trends over two decades. Eur. J. Pediatr. 176, 1227–1234 (2017).
pubmed: 28770413
doi: 10.1007/s00431-017-2975-z
Xu, M. et al. Etiology and clinical features of full-term neonatal bacterial meningitis: a multicenter retrospective cohort study. Front. Pediatr. 7, 31 (2019).
pubmed: 30815433
pmcid: 6381005
doi: 10.3389/fped.2019.00031
Xie, Y., Kim, K. J. & Kim, K. S. Current concepts on Escherichia coli K1 translocation of the blood-brain barrier. FEMS Immunol. Med Microbiol. 42, 271–279 (2004).
pubmed: 15477040
doi: 10.1016/j.femsim.2004.09.001
Sereme, Y., Toumi, E., Saifi, E., Faury, H. & Skurnik, D. Maternal immune factors involved in the prevention or facilitation of neonatal bacterial infections. Cell. Immunol. 395-396, 104796 (2024).
Kachikis, A. & Englund, J. A. Maternal immunization: optimizing protection for the mother and infant. J. Infect. 72, S83–S90 (2016).
pubmed: 27233120
doi: 10.1016/j.jinf.2016.04.027
Englund, J. A. et al. Transplacental antibody transfer following maternal immunization with polysaccharide and conjugate haemophilus influenzae Type B vaccines. J. Infect. Dis. 171, 99–105 (1995).
pubmed: 7798688
doi: 10.1093/infdis/171.1.99
Antoine, C. et al. Phage targeting neonatal meningitis E. coli K1 In Vitro in the intestinal microbiota of pregnant donors and impact on bacterial populations. Int J. Mol. Sci. 24, 10580 (2023).
pubmed: 37445758
pmcid: 10341584
doi: 10.3390/ijms241310580
Glode, M. P., Sutton, A., Moxon, E. R. & Robbins, J. B. Pathogenesis of neonatal Escherichia coli meningitis: induction of bacteremia and meningitis in infant rats fed E. coli K1. Infect. Immun. 16, 75–80 (1977).
pubmed: 326679
pmcid: 421490
doi: 10.1128/iai.16.1.75-80.1977
Kim, K. S. Strategy of Escherichia coli for crossing the blood-brain barrier. J. Infect. Dis. 186, S220–S224 (2002).
pubmed: 12424701
doi: 10.1086/344284
Doran, K. S. et al. Host-pathogen interactions in bacterial meningitis. Acta Neuropathol. 131, 185–209 (2016).
pubmed: 26744349
pmcid: 4713723
doi: 10.1007/s00401-015-1531-z
Palmeira, P., Quinello, C., Silveira-Lessa, A. L., Zago, C. A. & Carneiro-Sampaio, M. IgG placental transfer in healthy and pathological pregnancies. Clin. Dev. Immunol. 2012, 985646 (2012).
pubmed: 22235228
doi: 10.1155/2012/985646
Fleiszig, S. Lipopolysaccharide outer core is a ligand for corneal cell binding and ingestion of Pseudomonas aeruginosa. Invest. Ophthalmol. Vis. Sci. 37, 976–986 (1996).
Lu, X. et al. A Poly-N-Acetylglucosamine−shiga toxin broad-spectrum conjugate vaccine for shiga toxin-producing Escherichia coli. mBio 5, e00974–14 (2014).
pubmed: 24667709
pmcid: 3977355
doi: 10.1128/mBio.00974-14
Granoff, D. M. Relative importance of complement-mediated bactericidal and opsonic activity for protection against meningococcal disease. Vaccine 27, B117 (2009).
pubmed: 19477054
pmcid: 2751589
doi: 10.1016/j.vaccine.2009.04.066