Spleen development is modulated by neonatal gut microbiota

M Manuela Rosado, Alaitz Aranburu, Marco Scarsella, Simona Cascioli, Ezio Giorda, Federica Del Chierico, Stefano Levi Mortera, Eva Piano Mortari, Stefania Petrini, Lorenza Putignani, Rita Carsetti

Research output: Contribution to journalArticle

Abstract

The full development of the mammalian immune system occurs after birth upon exposure to non self-antigens. The gut is the first site of bacterial colonization where it is crucial to create the appropriate microenvironment able to balance effector or tolerogenic responses to external stimuli. It is a well-established fact that at mucosal sites bacteria play a key role in developing the immune system but we ignore how colonising bacteria impact the maturation of the spleen. Here we addressed this issue. Taking advantage of the fact that milk SIgA regulates bacterial colonization of the newborn intestine, we generated immunocompetent mice born either from IgA pro-efficient or IgA deficient females. Having demonstrated that SIgA in maternal milk modulates neonatal gut microbiota by promoting an increased diversity of the colonizing species we also found that immunocompetent pups, not exposed to milk SIgA, fail to properly develop the FDC network and primary follicles in the spleen compromising the response to T-dependent antigens. The presence of a less diverse microbiota with a higher representation of pathogenic species leads to a fast replenishment of the marginal zone and the IgM plasma cell compartment of the spleen as well as IgA plasma cells in the gut.

Original languageEnglish
Pages (from-to)1-15
Number of pages15
JournalImmunology Letters
Volume199
DOIs
Publication statusPublished - Jul 2018

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Secretory Immunoglobulin A
Immunoglobulin A
Milk
Spleen
Plasma Cells
Immune System
Bacteria
Microbiota
Viral Tumor Antigens
Autoantigens
Intestines
Immunoglobulin M
Mothers
Parturition
Gastrointestinal Microbiome

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Spleen development is modulated by neonatal gut microbiota. / Rosado, M Manuela; Aranburu, Alaitz; Scarsella, Marco; Cascioli, Simona; Giorda, Ezio; Del Chierico, Federica; Mortera, Stefano Levi; Mortari, Eva Piano; Petrini, Stefania; Putignani, Lorenza; Carsetti, Rita.

In: Immunology Letters, Vol. 199, 07.2018, p. 1-15.

Research output: Contribution to journalArticle

Rosado, M Manuela ; Aranburu, Alaitz ; Scarsella, Marco ; Cascioli, Simona ; Giorda, Ezio ; Del Chierico, Federica ; Mortera, Stefano Levi ; Mortari, Eva Piano ; Petrini, Stefania ; Putignani, Lorenza ; Carsetti, Rita. / Spleen development is modulated by neonatal gut microbiota. In: Immunology Letters. 2018 ; Vol. 199. pp. 1-15.
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abstract = "The full development of the mammalian immune system occurs after birth upon exposure to non self-antigens. The gut is the first site of bacterial colonization where it is crucial to create the appropriate microenvironment able to balance effector or tolerogenic responses to external stimuli. It is a well-established fact that at mucosal sites bacteria play a key role in developing the immune system but we ignore how colonising bacteria impact the maturation of the spleen. Here we addressed this issue. Taking advantage of the fact that milk SIgA regulates bacterial colonization of the newborn intestine, we generated immunocompetent mice born either from IgA pro-efficient or IgA deficient females. Having demonstrated that SIgA in maternal milk modulates neonatal gut microbiota by promoting an increased diversity of the colonizing species we also found that immunocompetent pups, not exposed to milk SIgA, fail to properly develop the FDC network and primary follicles in the spleen compromising the response to T-dependent antigens. The presence of a less diverse microbiota with a higher representation of pathogenic species leads to a fast replenishment of the marginal zone and the IgM plasma cell compartment of the spleen as well as IgA plasma cells in the gut.",
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AU - Del Chierico, Federica

AU - Mortera, Stefano Levi

AU - Mortari, Eva Piano

AU - Petrini, Stefania

AU - Putignani, Lorenza

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AB - The full development of the mammalian immune system occurs after birth upon exposure to non self-antigens. The gut is the first site of bacterial colonization where it is crucial to create the appropriate microenvironment able to balance effector or tolerogenic responses to external stimuli. It is a well-established fact that at mucosal sites bacteria play a key role in developing the immune system but we ignore how colonising bacteria impact the maturation of the spleen. Here we addressed this issue. Taking advantage of the fact that milk SIgA regulates bacterial colonization of the newborn intestine, we generated immunocompetent mice born either from IgA pro-efficient or IgA deficient females. Having demonstrated that SIgA in maternal milk modulates neonatal gut microbiota by promoting an increased diversity of the colonizing species we also found that immunocompetent pups, not exposed to milk SIgA, fail to properly develop the FDC network and primary follicles in the spleen compromising the response to T-dependent antigens. The presence of a less diverse microbiota with a higher representation of pathogenic species leads to a fast replenishment of the marginal zone and the IgM plasma cell compartment of the spleen as well as IgA plasma cells in the gut.

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