Effect of early postnatal supplementation of newborns with probiotic strain E. coli O83:K24:H31 on allergy incidence, dendritic cells, and microbiota

IntroductionProbiotic administration seems to be a rational approach to promote maturation of the neonatal immune system. Mutual interaction of the microbiota with the host immune system is critical for the setting of appropriate immune responses including a tolerogenic one and thevmaintenance of ho...

Full description

Bibliographic Details
Main Authors: Lenka Súkeníková, Viktor Černý, Tomáš Thon, Radka Roubalová, Zuzana Jirásková Zákostelská, Olga Novotná, Petra Petrásková, Kristýna Boráková, Ingrid Kocourková, Rája Lodinová-Žádníková, Zdeněk Musil, Libuše Kolářová, Ludmila Prokešová, Zdeněk Valenta, Jiří Hrdý
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-01-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2022.1038328/full
_version_ 1797956411619016704
author Lenka Súkeníková
Viktor Černý
Tomáš Thon
Radka Roubalová
Zuzana Jirásková Zákostelská
Olga Novotná
Petra Petrásková
Kristýna Boráková
Ingrid Kocourková
Rája Lodinová-Žádníková
Zdeněk Musil
Libuše Kolářová
Ludmila Prokešová
Zdeněk Valenta
Jiří Hrdý
author_facet Lenka Súkeníková
Viktor Černý
Tomáš Thon
Radka Roubalová
Zuzana Jirásková Zákostelská
Olga Novotná
Petra Petrásková
Kristýna Boráková
Ingrid Kocourková
Rája Lodinová-Žádníková
Zdeněk Musil
Libuše Kolářová
Ludmila Prokešová
Zdeněk Valenta
Jiří Hrdý
author_sort Lenka Súkeníková
collection DOAJ
description IntroductionProbiotic administration seems to be a rational approach to promote maturation of the neonatal immune system. Mutual interaction of the microbiota with the host immune system is critical for the setting of appropriate immune responses including a tolerogenic one and thevmaintenance of homeostasis. On the other hand, our knowledge on the modes of actions of probiotics is still scarce.MethodsIn our study, probiotic strain Escherichia coli O83:K24:H31 (EcO83) was administered to neonates of allergic mothers (AMs; neonates with increased risk for allergy development) within 48 h after the delivery, and the impact of this early postnatal supplementation on allergy incidence and selected immune markers has been analyzed 10 years after the primary EcO83 administration.ResultsWe have observed decreased allergy incidence in 10-year-old children supplemented with EcO83 (13 of 52 children were allergic) in comparison with non-supplemented children of AMs (16 of 42 children were allergic). The early postnatal EcO83 supplementation appeared to limit the allergy in the high-risk group (children of AMs) compared to that in the low-risk group (children of healthy mothers). Dendritic cells (DCs) in the peripheral blood of EcO83-supplemented children do not differ significantly in cell surface presence of CD83. The immunomodulatory capacity of EcO83 on DCs was tested in vitro as well. Both directly isolated myeloid and in vitro monocyte-derived DCs from cord blood increased CD83 expression together with interleukin (IL)-10 secretion after EcO83 stimulation. The effect of early postnatal EcO83 supplementation on the microbiota composition of 10-year-old children was characterized by next-generation sequencing, and we have not observed significant changes in the microbiota composition of EcO83-supplemented and non-supplemented children at the age of 10 years.ConclusionsEarly postnatal EcO83 supplementation appears to lower allergy incidence in children of AMs. It seems that the beneficial effect of EcO83 is mediated via modulation of DC functional capacities without impacting the microbiota composition. Larger-scale studies will be necessary to confirm these preliminary findings.
first_indexed 2024-04-10T23:48:37Z
format Article
id doaj.art-e3a8bc19c20143c3a5c0fbf735c7eebe
institution Directory Open Access Journal
issn 1664-3224
language English
last_indexed 2024-04-10T23:48:37Z
publishDate 2023-01-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Immunology
spelling doaj.art-e3a8bc19c20143c3a5c0fbf735c7eebe2023-01-10T22:15:45ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-01-011310.3389/fimmu.2022.10383281038328Effect of early postnatal supplementation of newborns with probiotic strain E. coli O83:K24:H31 on allergy incidence, dendritic cells, and microbiotaLenka Súkeníková0Viktor Černý1Tomáš Thon2Radka Roubalová3Zuzana Jirásková Zákostelská4Olga Novotná5Petra Petrásková6Kristýna Boráková7Ingrid Kocourková8Rája Lodinová-Žádníková9Zdeněk Musil10Libuše Kolářová11Ludmila Prokešová12Zdeněk Valenta13Jiří Hrdý14Institute of Immunology and Microbiology, First Faculty of Medicine, Charles University, Prague, CzechiaInstitute of Immunology and Microbiology, First Faculty of Medicine, Charles University, Prague, CzechiaInstitute of Microbiology, Academy of Sciences, Prague, CzechiaInstitute of Microbiology, Academy of Sciences, Prague, CzechiaInstitute of Microbiology, Academy of Sciences, Prague, CzechiaInstitute of Immunology and Microbiology, First Faculty of Medicine, Charles University, Prague, CzechiaInstitute of Immunology and Microbiology, First Faculty of Medicine, Charles University, Prague, CzechiaDepartment of Neonatology, Institute for the Care of Mother and Child, Prague, CzechiaDepartment of Neonatology, Institute for the Care of Mother and Child, Prague, CzechiaDepartment of Neonatology, Institute for the Care of Mother and Child, Prague, CzechiaInstitute of Biology and Medical Genetics, First Faculty of Medicine, Charles University, Prague, CzechiaInstitute of Immunology and Microbiology, First Faculty of Medicine, Charles University, Prague, CzechiaInstitute of Immunology and Microbiology, First Faculty of Medicine, Charles University, Prague, CzechiaDepartment of Statistical Modelling, Institute of Computer Science of the Czech Academy of Sciences, Prague, CzechiaInstitute of Immunology and Microbiology, First Faculty of Medicine, Charles University, Prague, CzechiaIntroductionProbiotic administration seems to be a rational approach to promote maturation of the neonatal immune system. Mutual interaction of the microbiota with the host immune system is critical for the setting of appropriate immune responses including a tolerogenic one and thevmaintenance of homeostasis. On the other hand, our knowledge on the modes of actions of probiotics is still scarce.MethodsIn our study, probiotic strain Escherichia coli O83:K24:H31 (EcO83) was administered to neonates of allergic mothers (AMs; neonates with increased risk for allergy development) within 48 h after the delivery, and the impact of this early postnatal supplementation on allergy incidence and selected immune markers has been analyzed 10 years after the primary EcO83 administration.ResultsWe have observed decreased allergy incidence in 10-year-old children supplemented with EcO83 (13 of 52 children were allergic) in comparison with non-supplemented children of AMs (16 of 42 children were allergic). The early postnatal EcO83 supplementation appeared to limit the allergy in the high-risk group (children of AMs) compared to that in the low-risk group (children of healthy mothers). Dendritic cells (DCs) in the peripheral blood of EcO83-supplemented children do not differ significantly in cell surface presence of CD83. The immunomodulatory capacity of EcO83 on DCs was tested in vitro as well. Both directly isolated myeloid and in vitro monocyte-derived DCs from cord blood increased CD83 expression together with interleukin (IL)-10 secretion after EcO83 stimulation. The effect of early postnatal EcO83 supplementation on the microbiota composition of 10-year-old children was characterized by next-generation sequencing, and we have not observed significant changes in the microbiota composition of EcO83-supplemented and non-supplemented children at the age of 10 years.ConclusionsEarly postnatal EcO83 supplementation appears to lower allergy incidence in children of AMs. It seems that the beneficial effect of EcO83 is mediated via modulation of DC functional capacities without impacting the microbiota composition. Larger-scale studies will be necessary to confirm these preliminary findings.https://www.frontiersin.org/articles/10.3389/fimmu.2022.1038328/fullprobioticdendritic cellIL-10CD83Escherichia coli O83:K24:H31flow cytometry
spellingShingle Lenka Súkeníková
Viktor Černý
Tomáš Thon
Radka Roubalová
Zuzana Jirásková Zákostelská
Olga Novotná
Petra Petrásková
Kristýna Boráková
Ingrid Kocourková
Rája Lodinová-Žádníková
Zdeněk Musil
Libuše Kolářová
Ludmila Prokešová
Zdeněk Valenta
Jiří Hrdý
Effect of early postnatal supplementation of newborns with probiotic strain E. coli O83:K24:H31 on allergy incidence, dendritic cells, and microbiota
Frontiers in Immunology
probiotic
dendritic cell
IL-10
CD83
Escherichia coli O83:K24:H31
flow cytometry
title Effect of early postnatal supplementation of newborns with probiotic strain E. coli O83:K24:H31 on allergy incidence, dendritic cells, and microbiota
title_full Effect of early postnatal supplementation of newborns with probiotic strain E. coli O83:K24:H31 on allergy incidence, dendritic cells, and microbiota
title_fullStr Effect of early postnatal supplementation of newborns with probiotic strain E. coli O83:K24:H31 on allergy incidence, dendritic cells, and microbiota
title_full_unstemmed Effect of early postnatal supplementation of newborns with probiotic strain E. coli O83:K24:H31 on allergy incidence, dendritic cells, and microbiota
title_short Effect of early postnatal supplementation of newborns with probiotic strain E. coli O83:K24:H31 on allergy incidence, dendritic cells, and microbiota
title_sort effect of early postnatal supplementation of newborns with probiotic strain e coli o83 k24 h31 on allergy incidence dendritic cells and microbiota
topic probiotic
dendritic cell
IL-10
CD83
Escherichia coli O83:K24:H31
flow cytometry
url https://www.frontiersin.org/articles/10.3389/fimmu.2022.1038328/full
work_keys_str_mv AT lenkasukenikova effectofearlypostnatalsupplementationofnewbornswithprobioticstrainecolio83k24h31onallergyincidencedendriticcellsandmicrobiota
AT viktorcerny effectofearlypostnatalsupplementationofnewbornswithprobioticstrainecolio83k24h31onallergyincidencedendriticcellsandmicrobiota
AT tomasthon effectofearlypostnatalsupplementationofnewbornswithprobioticstrainecolio83k24h31onallergyincidencedendriticcellsandmicrobiota
AT radkaroubalova effectofearlypostnatalsupplementationofnewbornswithprobioticstrainecolio83k24h31onallergyincidencedendriticcellsandmicrobiota
AT zuzanajiraskovazakostelska effectofearlypostnatalsupplementationofnewbornswithprobioticstrainecolio83k24h31onallergyincidencedendriticcellsandmicrobiota
AT olganovotna effectofearlypostnatalsupplementationofnewbornswithprobioticstrainecolio83k24h31onallergyincidencedendriticcellsandmicrobiota
AT petrapetraskova effectofearlypostnatalsupplementationofnewbornswithprobioticstrainecolio83k24h31onallergyincidencedendriticcellsandmicrobiota
AT kristynaborakova effectofearlypostnatalsupplementationofnewbornswithprobioticstrainecolio83k24h31onallergyincidencedendriticcellsandmicrobiota
AT ingridkocourkova effectofearlypostnatalsupplementationofnewbornswithprobioticstrainecolio83k24h31onallergyincidencedendriticcellsandmicrobiota
AT rajalodinovazadnikova effectofearlypostnatalsupplementationofnewbornswithprobioticstrainecolio83k24h31onallergyincidencedendriticcellsandmicrobiota
AT zdenekmusil effectofearlypostnatalsupplementationofnewbornswithprobioticstrainecolio83k24h31onallergyincidencedendriticcellsandmicrobiota
AT libusekolarova effectofearlypostnatalsupplementationofnewbornswithprobioticstrainecolio83k24h31onallergyincidencedendriticcellsandmicrobiota
AT ludmilaprokesova effectofearlypostnatalsupplementationofnewbornswithprobioticstrainecolio83k24h31onallergyincidencedendriticcellsandmicrobiota
AT zdenekvalenta effectofearlypostnatalsupplementationofnewbornswithprobioticstrainecolio83k24h31onallergyincidencedendriticcellsandmicrobiota
AT jirihrdy effectofearlypostnatalsupplementationofnewbornswithprobioticstrainecolio83k24h31onallergyincidencedendriticcellsandmicrobiota