Bacterial Imprinting of the Neonatal Immune System: Lessons From Maternal Cells?

Autores
Perez, Pablo Fernando; Doré, Joel; Leclerc, Marion; Levenez, Florence; Benyacoub, Jalil; Serrant, Patrick; Segura Roggero, Iris; Schiffrin, Eduardo J.; Donnet Hughes, Anne
Año de publicación
2007
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
OBJECTIVE. We examined the presence of a natural bacterial inoculum in breast milk and its intracellular transport from the maternal intestine to the breast through the circulation. METHODS. Breast milk and peripheral blood were collected aseptically from healthy donors at various times after delivery, and the presence of viable bacteria was determined through plating. Temporal temperature gradient gel electrophoresis was used to examine the bacterial ribosomal DNA content in milk cells, maternal peripheral blood mononuclear cells, and feces and in corresponding infant feces. Blood from nongravid nonlactating women served as control samples. Bacterial translocation to extraintestinal tissues was also evaluated in virgin, pregnant, and lactating mice. RESULTS. Breast milk contained a low total concentration of microbes of <103 colony-forming units per mL. Temporal temperature gradient gel electrophoresis revealed that maternal blood and milk cells contained the genetic material of a greater biodiversity of enteric bacteria. Some bacterial signatures were common to infant feces and to samples of maternal origin. Bacterial translocation from the gut to mesenteric lymph nodes and mammary gland occurred during late pregnancy and lactation in mice. CONCLUSIONS. Bacterial translocation is a unique physiologic event, which is increased during pregnancy and lactation in rodents. Human breast milk cells contain a limited number of viable bacteria but a range of bacterial DNA signatures, as also found in maternal peripheral blood mononuclear cells. Those peripheral blood mononuclear cells showed greater biodiversity than did peripheral blood mononuclear cells from control women. Taken together, our results suggest that intestinally derived bacterial components are transported to the lactating breast within mononuclear cells. We speculate that this programs the neonatal immune system to recognize specific bacterial molecular patterns and to respond appropriately to pathogens and commensal organisms.
Fil: Perez, Pablo Fernando. Provincia de Buenos Aires. Gobernación. Comisión de Investigaciones Científicas. Centro de Investigación y Desarrollo en Criotecnología de Alimentos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Centro de Investigación y Desarrollo en Criotecnología de Alimentos. Universidad Nacional de La Plata. Facultad de Ciencias Exactas. Centro de Investigación y Desarrollo en Criotecnología de Alimentos; Argentina
Fil: Doré, Joel. Nestlé Research Centre. Nestec; Francia
Fil: Leclerc, Marion. National Institute for Agronomic Research. Unit for Ecology and Physiology of the Digestive Tract; Francia
Fil: Levenez, Florence. National Institute for Agronomic Research. Unit for Ecology and Physiology of the Digestive Tract; Francia
Fil: Benyacoub, Jalil. Nestlé Research Centre. Nestec; Francia
Fil: Serrant, Patrick. Nestlé Research Centre. Nestec; Francia
Fil: Segura Roggero, Iris. Nestlé Research Centre. Nestec; Francia
Fil: Schiffrin, Eduardo J.. Nestlé Research Centre. Nestec; Francia
Fil: Donnet Hughes, Anne. Nestlé Research Centre. Nestec; Francia
Materia
Bacterial translocation
Breast milk
Immunity
Maternal and child health
Lactation
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/110456

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network_name_str CONICET Digital (CONICET)
spelling Bacterial Imprinting of the Neonatal Immune System: Lessons From Maternal Cells?Perez, Pablo FernandoDoré, JoelLeclerc, MarionLevenez, FlorenceBenyacoub, JalilSerrant, PatrickSegura Roggero, IrisSchiffrin, Eduardo J.Donnet Hughes, AnneBacterial translocationBreast milkImmunityMaternal and child healthLactationhttps://purl.org/becyt/ford/2.11https://purl.org/becyt/ford/2OBJECTIVE. We examined the presence of a natural bacterial inoculum in breast milk and its intracellular transport from the maternal intestine to the breast through the circulation. METHODS. Breast milk and peripheral blood were collected aseptically from healthy donors at various times after delivery, and the presence of viable bacteria was determined through plating. Temporal temperature gradient gel electrophoresis was used to examine the bacterial ribosomal DNA content in milk cells, maternal peripheral blood mononuclear cells, and feces and in corresponding infant feces. Blood from nongravid nonlactating women served as control samples. Bacterial translocation to extraintestinal tissues was also evaluated in virgin, pregnant, and lactating mice. RESULTS. Breast milk contained a low total concentration of microbes of <103 colony-forming units per mL. Temporal temperature gradient gel electrophoresis revealed that maternal blood and milk cells contained the genetic material of a greater biodiversity of enteric bacteria. Some bacterial signatures were common to infant feces and to samples of maternal origin. Bacterial translocation from the gut to mesenteric lymph nodes and mammary gland occurred during late pregnancy and lactation in mice. CONCLUSIONS. Bacterial translocation is a unique physiologic event, which is increased during pregnancy and lactation in rodents. Human breast milk cells contain a limited number of viable bacteria but a range of bacterial DNA signatures, as also found in maternal peripheral blood mononuclear cells. Those peripheral blood mononuclear cells showed greater biodiversity than did peripheral blood mononuclear cells from control women. Taken together, our results suggest that intestinally derived bacterial components are transported to the lactating breast within mononuclear cells. We speculate that this programs the neonatal immune system to recognize specific bacterial molecular patterns and to respond appropriately to pathogens and commensal organisms.Fil: Perez, Pablo Fernando. Provincia de Buenos Aires. Gobernación. Comisión de Investigaciones Científicas. Centro de Investigación y Desarrollo en Criotecnología de Alimentos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Centro de Investigación y Desarrollo en Criotecnología de Alimentos. Universidad Nacional de La Plata. Facultad de Ciencias Exactas. Centro de Investigación y Desarrollo en Criotecnología de Alimentos; ArgentinaFil: Doré, Joel. Nestlé Research Centre. Nestec; FranciaFil: Leclerc, Marion. National Institute for Agronomic Research. Unit for Ecology and Physiology of the Digestive Tract; FranciaFil: Levenez, Florence. National Institute for Agronomic Research. Unit for Ecology and Physiology of the Digestive Tract; FranciaFil: Benyacoub, Jalil. Nestlé Research Centre. Nestec; FranciaFil: Serrant, Patrick. Nestlé Research Centre. Nestec; FranciaFil: Segura Roggero, Iris. Nestlé Research Centre. Nestec; FranciaFil: Schiffrin, Eduardo J.. Nestlé Research Centre. Nestec; FranciaFil: Donnet Hughes, Anne. Nestlé Research Centre. Nestec; FranciaAmerican Academy of Pediatrics2007-06info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/110456Perez, Pablo Fernando; Doré, Joel; Leclerc, Marion; Levenez, Florence; Benyacoub, Jalil; et al.; Bacterial Imprinting of the Neonatal Immune System: Lessons From Maternal Cells?; American Academy of Pediatrics; Pediatrics; 119; 3; 6-2007; e724-e7320031-40051098-4275CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://pediatrics.aappublications.org/content/119/3/e724info:eu-repo/semantics/altIdentifier/doi/10.1542/peds.2006-1649info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:37:51Zoai:ri.conicet.gov.ar:11336/110456instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 09:37:51.719CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Bacterial Imprinting of the Neonatal Immune System: Lessons From Maternal Cells?
title Bacterial Imprinting of the Neonatal Immune System: Lessons From Maternal Cells?
spellingShingle Bacterial Imprinting of the Neonatal Immune System: Lessons From Maternal Cells?
Perez, Pablo Fernando
Bacterial translocation
Breast milk
Immunity
Maternal and child health
Lactation
title_short Bacterial Imprinting of the Neonatal Immune System: Lessons From Maternal Cells?
title_full Bacterial Imprinting of the Neonatal Immune System: Lessons From Maternal Cells?
title_fullStr Bacterial Imprinting of the Neonatal Immune System: Lessons From Maternal Cells?
title_full_unstemmed Bacterial Imprinting of the Neonatal Immune System: Lessons From Maternal Cells?
title_sort Bacterial Imprinting of the Neonatal Immune System: Lessons From Maternal Cells?
dc.creator.none.fl_str_mv Perez, Pablo Fernando
Doré, Joel
Leclerc, Marion
Levenez, Florence
Benyacoub, Jalil
Serrant, Patrick
Segura Roggero, Iris
Schiffrin, Eduardo J.
Donnet Hughes, Anne
author Perez, Pablo Fernando
author_facet Perez, Pablo Fernando
Doré, Joel
Leclerc, Marion
Levenez, Florence
Benyacoub, Jalil
Serrant, Patrick
Segura Roggero, Iris
Schiffrin, Eduardo J.
Donnet Hughes, Anne
author_role author
author2 Doré, Joel
Leclerc, Marion
Levenez, Florence
Benyacoub, Jalil
Serrant, Patrick
Segura Roggero, Iris
Schiffrin, Eduardo J.
Donnet Hughes, Anne
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Bacterial translocation
Breast milk
Immunity
Maternal and child health
Lactation
topic Bacterial translocation
Breast milk
Immunity
Maternal and child health
Lactation
purl_subject.fl_str_mv https://purl.org/becyt/ford/2.11
https://purl.org/becyt/ford/2
dc.description.none.fl_txt_mv OBJECTIVE. We examined the presence of a natural bacterial inoculum in breast milk and its intracellular transport from the maternal intestine to the breast through the circulation. METHODS. Breast milk and peripheral blood were collected aseptically from healthy donors at various times after delivery, and the presence of viable bacteria was determined through plating. Temporal temperature gradient gel electrophoresis was used to examine the bacterial ribosomal DNA content in milk cells, maternal peripheral blood mononuclear cells, and feces and in corresponding infant feces. Blood from nongravid nonlactating women served as control samples. Bacterial translocation to extraintestinal tissues was also evaluated in virgin, pregnant, and lactating mice. RESULTS. Breast milk contained a low total concentration of microbes of <103 colony-forming units per mL. Temporal temperature gradient gel electrophoresis revealed that maternal blood and milk cells contained the genetic material of a greater biodiversity of enteric bacteria. Some bacterial signatures were common to infant feces and to samples of maternal origin. Bacterial translocation from the gut to mesenteric lymph nodes and mammary gland occurred during late pregnancy and lactation in mice. CONCLUSIONS. Bacterial translocation is a unique physiologic event, which is increased during pregnancy and lactation in rodents. Human breast milk cells contain a limited number of viable bacteria but a range of bacterial DNA signatures, as also found in maternal peripheral blood mononuclear cells. Those peripheral blood mononuclear cells showed greater biodiversity than did peripheral blood mononuclear cells from control women. Taken together, our results suggest that intestinally derived bacterial components are transported to the lactating breast within mononuclear cells. We speculate that this programs the neonatal immune system to recognize specific bacterial molecular patterns and to respond appropriately to pathogens and commensal organisms.
Fil: Perez, Pablo Fernando. Provincia de Buenos Aires. Gobernación. Comisión de Investigaciones Científicas. Centro de Investigación y Desarrollo en Criotecnología de Alimentos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Centro de Investigación y Desarrollo en Criotecnología de Alimentos. Universidad Nacional de La Plata. Facultad de Ciencias Exactas. Centro de Investigación y Desarrollo en Criotecnología de Alimentos; Argentina
Fil: Doré, Joel. Nestlé Research Centre. Nestec; Francia
Fil: Leclerc, Marion. National Institute for Agronomic Research. Unit for Ecology and Physiology of the Digestive Tract; Francia
Fil: Levenez, Florence. National Institute for Agronomic Research. Unit for Ecology and Physiology of the Digestive Tract; Francia
Fil: Benyacoub, Jalil. Nestlé Research Centre. Nestec; Francia
Fil: Serrant, Patrick. Nestlé Research Centre. Nestec; Francia
Fil: Segura Roggero, Iris. Nestlé Research Centre. Nestec; Francia
Fil: Schiffrin, Eduardo J.. Nestlé Research Centre. Nestec; Francia
Fil: Donnet Hughes, Anne. Nestlé Research Centre. Nestec; Francia
description OBJECTIVE. We examined the presence of a natural bacterial inoculum in breast milk and its intracellular transport from the maternal intestine to the breast through the circulation. METHODS. Breast milk and peripheral blood were collected aseptically from healthy donors at various times after delivery, and the presence of viable bacteria was determined through plating. Temporal temperature gradient gel electrophoresis was used to examine the bacterial ribosomal DNA content in milk cells, maternal peripheral blood mononuclear cells, and feces and in corresponding infant feces. Blood from nongravid nonlactating women served as control samples. Bacterial translocation to extraintestinal tissues was also evaluated in virgin, pregnant, and lactating mice. RESULTS. Breast milk contained a low total concentration of microbes of <103 colony-forming units per mL. Temporal temperature gradient gel electrophoresis revealed that maternal blood and milk cells contained the genetic material of a greater biodiversity of enteric bacteria. Some bacterial signatures were common to infant feces and to samples of maternal origin. Bacterial translocation from the gut to mesenteric lymph nodes and mammary gland occurred during late pregnancy and lactation in mice. CONCLUSIONS. Bacterial translocation is a unique physiologic event, which is increased during pregnancy and lactation in rodents. Human breast milk cells contain a limited number of viable bacteria but a range of bacterial DNA signatures, as also found in maternal peripheral blood mononuclear cells. Those peripheral blood mononuclear cells showed greater biodiversity than did peripheral blood mononuclear cells from control women. Taken together, our results suggest that intestinally derived bacterial components are transported to the lactating breast within mononuclear cells. We speculate that this programs the neonatal immune system to recognize specific bacterial molecular patterns and to respond appropriately to pathogens and commensal organisms.
publishDate 2007
dc.date.none.fl_str_mv 2007-06
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/110456
Perez, Pablo Fernando; Doré, Joel; Leclerc, Marion; Levenez, Florence; Benyacoub, Jalil; et al.; Bacterial Imprinting of the Neonatal Immune System: Lessons From Maternal Cells?; American Academy of Pediatrics; Pediatrics; 119; 3; 6-2007; e724-e732
0031-4005
1098-4275
CONICET Digital
CONICET
url http://hdl.handle.net/11336/110456
identifier_str_mv Perez, Pablo Fernando; Doré, Joel; Leclerc, Marion; Levenez, Florence; Benyacoub, Jalil; et al.; Bacterial Imprinting of the Neonatal Immune System: Lessons From Maternal Cells?; American Academy of Pediatrics; Pediatrics; 119; 3; 6-2007; e724-e732
0031-4005
1098-4275
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://pediatrics.aappublications.org/content/119/3/e724
info:eu-repo/semantics/altIdentifier/doi/10.1542/peds.2006-1649
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv American Academy of Pediatrics
publisher.none.fl_str_mv American Academy of Pediatrics
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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