Lactobacillus reuteri DSM 17938 changes the frequency of Foxp3+ regulatory T cells in the intestine and mesenteric lymph node in experimental necrotizing enterocolitis
Necrotizing enterocolitis (NEC) is an inflammatory disease of the intestine in premature infants. Lactobacillus reuteri DSM 17938 improves survival and reduces the incidence and severity of NEC in a rodent model. Foxp3(+) regulatory T cells (Tregs) maintain intestinal homeostasis by controlling infl...
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| description | Necrotizing enterocolitis (NEC) is an inflammatory disease of the intestine in premature infants. Lactobacillus reuteri DSM 17938 improves survival and reduces the incidence and severity of NEC in a rodent model. Foxp3(+) regulatory T cells (Tregs) maintain intestinal homeostasis by controlling inflammation and inducing tolerance. To determine whether there are insufficient numbers of Tregs to control inflammation in NEC and to determine if LR17938 increases the frequency of Tregs, we studied selected groups of newborn Sprague-Dawley rats according to feeding plan: dam±LR17938, formula±LR17938, and NEC±LR17938. NEC was induced by gavage feeding with special formula and exposure to hypoxic conditions. Lymphocytes isolated from ileum, mesenteric lymph nodes (MLN), spleen and thymus were labeled for T cell surface markers (CD3, CD4, CD8) and intracellular Foxp3; and labeled cells were analyzed by flow cytometry. The percentage of CD3(+) T cells and Foxp3(+) Tregs in the ileum significantly decreased in pups with NEC, compared to normal controls. Feeding LR17938 to neonatal rats with NEC increased the % of Foxp3(+) T cells in the ileum while decreasing the percentage of cells in the MLN. Administration of LR17938 to dam-fed rats significantly increased Foxp3(+)Tregs in the ileum as early as day of life (DOL)1 but did not produce an increase in Tregs in formula-fed rats on DOL1. These results suggest that factors in breast milk may enhance the early immunomodulatory effects of LR17938. An anti-inflammatory effect of LR17938 in NEC was associated with the modulation of immune responses and induction and what appears to be migration of Foxp3(+) Tregs to the diseased gut. Probiotic-facilitated development of Tregs might play an important role in the prevention of NEC. |
| doi_str_mv | 10.1371/journal.pone.0056547 |
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Lactobacillus reuteri DSM 17938 improves survival and reduces the incidence and severity of NEC in a rodent model. Foxp3(+) regulatory T cells (Tregs) maintain intestinal homeostasis by controlling inflammation and inducing tolerance. To determine whether there are insufficient numbers of Tregs to control inflammation in NEC and to determine if LR17938 increases the frequency of Tregs, we studied selected groups of newborn Sprague-Dawley rats according to feeding plan: dam±LR17938, formula±LR17938, and NEC±LR17938. NEC was induced by gavage feeding with special formula and exposure to hypoxic conditions. Lymphocytes isolated from ileum, mesenteric lymph nodes (MLN), spleen and thymus were labeled for T cell surface markers (CD3, CD4, CD8) and intracellular Foxp3; and labeled cells were analyzed by flow cytometry. The percentage of CD3(+) T cells and Foxp3(+) Tregs in the ileum significantly decreased in pups with NEC, compared to normal controls. Feeding LR17938 to neonatal rats with NEC increased the % of Foxp3(+) T cells in the ileum while decreasing the percentage of cells in the MLN. Administration of LR17938 to dam-fed rats significantly increased Foxp3(+)Tregs in the ileum as early as day of life (DOL)1 but did not produce an increase in Tregs in formula-fed rats on DOL1. These results suggest that factors in breast milk may enhance the early immunomodulatory effects of LR17938. An anti-inflammatory effect of LR17938 in NEC was associated with the modulation of immune responses and induction and what appears to be migration of Foxp3(+) Tregs to the diseased gut. Probiotic-facilitated development of Tregs might play an important role in the prevention of NEC.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0056547</identifier><identifier>PMID: 23437165</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Antigens ; Bacteria ; Biology ; Breast milk ; Breastfeeding & lactation ; CD3 antigen ; CD4 antigen ; CD8 antigen ; Cell surface ; Cytometry ; Enterocolitis ; Enterocolitis - chemically induced ; Enterocolitis - metabolism ; Enterocolitis - pathology ; Feeding ; Flow cytometry ; Forkhead Transcription Factors - metabolism ; Foxp3 protein ; Gastroenterology ; Gastrointestinal diseases ; Homeostasis ; Hypoxia ; Ileum ; Immune response ; Immune system ; Immunological tolerance ; Immunology ; Immunomodulation ; Immunoregulation ; Infants ; Inflammation - drug therapy ; Inflammation - immunology ; Inflammation - metabolism ; Intestinal Mucosa - metabolism ; Intestine ; Intestines - drug effects ; Intestines - immunology ; Lactobacillus reuteri ; Lactobacillus reuteri - chemistry ; Leukocyte migration ; Lupus ; Lymph ; Lymph nodes ; Lymph Nodes - drug effects ; Lymph Nodes - immunology ; Lymph Nodes - metabolism ; Lymph Nodes - pathology ; Lymphatic system ; Lymphocytes ; Lymphocytes T ; Medical schools ; Medicine ; Mesentery - drug effects ; Mesentery - immunology ; Mesentery - metabolism ; Mesentery - pathology ; Milk ; Necrosis ; Necrotizing enterocolitis ; Neonates ; Newborn babies ; Pediatrics ; Probiotics ; Probiotics - administration & dosage ; Probiotics - chemistry ; Rats ; Rats, Sprague-Dawley ; Rodents ; Science ; Small intestine ; Spleen ; Surface markers ; T-Lymphocytes, Regulatory - immunology ; T-Lymphocytes, Regulatory - metabolism ; T-Lymphocytes, Regulatory - pathology ; Thymus</subject><ispartof>PloS one, 2013-02, Vol.8 (2), p.e56547</ispartof><rights>2013 Liu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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Lactobacillus reuteri DSM 17938 improves survival and reduces the incidence and severity of NEC in a rodent model. Foxp3(+) regulatory T cells (Tregs) maintain intestinal homeostasis by controlling inflammation and inducing tolerance. To determine whether there are insufficient numbers of Tregs to control inflammation in NEC and to determine if LR17938 increases the frequency of Tregs, we studied selected groups of newborn Sprague-Dawley rats according to feeding plan: dam±LR17938, formula±LR17938, and NEC±LR17938. NEC was induced by gavage feeding with special formula and exposure to hypoxic conditions. Lymphocytes isolated from ileum, mesenteric lymph nodes (MLN), spleen and thymus were labeled for T cell surface markers (CD3, CD4, CD8) and intracellular Foxp3; and labeled cells were analyzed by flow cytometry. The percentage of CD3(+) T cells and Foxp3(+) Tregs in the ileum significantly decreased in pups with NEC, compared to normal controls. Feeding LR17938 to neonatal rats with NEC increased the % of Foxp3(+) T cells in the ileum while decreasing the percentage of cells in the MLN. Administration of LR17938 to dam-fed rats significantly increased Foxp3(+)Tregs in the ileum as early as day of life (DOL)1 but did not produce an increase in Tregs in formula-fed rats on DOL1. These results suggest that factors in breast milk may enhance the early immunomodulatory effects of LR17938. An anti-inflammatory effect of LR17938 in NEC was associated with the modulation of immune responses and induction and what appears to be migration of Foxp3(+) Tregs to the diseased gut. Probiotic-facilitated development of Tregs might play an important role in the prevention of NEC.</description><subject>Animals</subject><subject>Antigens</subject><subject>Bacteria</subject><subject>Biology</subject><subject>Breast milk</subject><subject>Breastfeeding & lactation</subject><subject>CD3 antigen</subject><subject>CD4 antigen</subject><subject>CD8 antigen</subject><subject>Cell surface</subject><subject>Cytometry</subject><subject>Enterocolitis</subject><subject>Enterocolitis - chemically induced</subject><subject>Enterocolitis - metabolism</subject><subject>Enterocolitis - pathology</subject><subject>Feeding</subject><subject>Flow cytometry</subject><subject>Forkhead Transcription Factors - metabolism</subject><subject>Foxp3 protein</subject><subject>Gastroenterology</subject><subject>Gastrointestinal diseases</subject><subject>Homeostasis</subject><subject>Hypoxia</subject><subject>Ileum</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immunological tolerance</subject><subject>Immunology</subject><subject>Immunomodulation</subject><subject>Immunoregulation</subject><subject>Infants</subject><subject>Inflammation - drug therapy</subject><subject>Inflammation - immunology</subject><subject>Inflammation - metabolism</subject><subject>Intestinal Mucosa - metabolism</subject><subject>Intestine</subject><subject>Intestines - drug effects</subject><subject>Intestines - immunology</subject><subject>Lactobacillus reuteri</subject><subject>Lactobacillus reuteri - chemistry</subject><subject>Leukocyte migration</subject><subject>Lupus</subject><subject>Lymph</subject><subject>Lymph nodes</subject><subject>Lymph Nodes - drug effects</subject><subject>Lymph Nodes - immunology</subject><subject>Lymph Nodes - metabolism</subject><subject>Lymph Nodes - pathology</subject><subject>Lymphatic system</subject><subject>Lymphocytes</subject><subject>Lymphocytes T</subject><subject>Medical schools</subject><subject>Medicine</subject><subject>Mesentery - drug effects</subject><subject>Mesentery - immunology</subject><subject>Mesentery - metabolism</subject><subject>Mesentery - pathology</subject><subject>Milk</subject><subject>Necrosis</subject><subject>Necrotizing enterocolitis</subject><subject>Neonates</subject><subject>Newborn babies</subject><subject>Pediatrics</subject><subject>Probiotics</subject><subject>Probiotics - administration & dosage</subject><subject>Probiotics - chemistry</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Rodents</subject><subject>Science</subject><subject>Small intestine</subject><subject>Spleen</subject><subject>Surface markers</subject><subject>T-Lymphocytes, Regulatory - immunology</subject><subject>T-Lymphocytes, Regulatory - metabolism</subject><subject>T-Lymphocytes, Regulatory - pathology</subject><subject>Thymus</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNp1kstuEzEUhkcIREvhDRBYYokS7PE1G6SqUKhUxIKytjyeM4kjxx5sD2p4IV4T59KqXbCy5fOf71z8N81rgueESvJhHacUjJ-PMcAcYy44k0-aU7Kg7Uy0mD59cD9pXuS8riKqhHjenLSUVYTgp83fa2NL7Ix13k8ZJZgKJIc-_fiGiFxQhezKhCVkVFaAhgS_Jgh2i-KALuPtSN_XjOXkTYlpi26QBe8zcmGvdqFALi4AMqFHG8gQdmyL_HYzrlCI_U6D4Hasr5saNB4FsCkW98eFJdrLo43eFZdfNs8G4zO8Op5nzc_LzzcXX2fX379cXZxfzyyXssxaBj3jw8AYHSQnigtiFnwBhAjKlDAMuq61Q8-V4IKaDgZJhewVbpVsiRH0rHl74I4-Zn3ccdaEUqxUizmuiquDoo9mrcfauklbHY3T-4eYltqk4qwH3cqKXyjAEjBrhTCyU7hvMcaDxRbTyvp4rDZ1G-htHTkZ_wj6OBLcSi_jb03rtIqzCnh3BKRYvyaX_7TMDqq63JwTDPcVCNY7M91l6Z2Z9NFMNe3Nw-7uk-7cQ_8BPHbKTA</recordid><startdate>20130220</startdate><enddate>20130220</enddate><creator>Liu, Yuying</creator><creator>Fatheree, Nicole Y</creator><creator>Dingle, Bridgette M</creator><creator>Tran, Dat Q</creator><creator>Rhoads, Jon Marc</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20130220</creationdate><title>Lactobacillus reuteri DSM 17938 changes the frequency of Foxp3+ regulatory T cells in the intestine and mesenteric lymph node in experimental necrotizing enterocolitis</title><author>Liu, Yuying ; Fatheree, Nicole Y ; Dingle, Bridgette M ; Tran, Dat Q ; Rhoads, Jon Marc</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c577t-24ed45ff443f7518561a959e1163486a4ebb2cfd586563abef7367d8028721a63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animals</topic><topic>Antigens</topic><topic>Bacteria</topic><topic>Biology</topic><topic>Breast milk</topic><topic>Breastfeeding & lactation</topic><topic>CD3 antigen</topic><topic>CD4 antigen</topic><topic>CD8 antigen</topic><topic>Cell surface</topic><topic>Cytometry</topic><topic>Enterocolitis</topic><topic>Enterocolitis - 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Lactobacillus reuteri DSM 17938 improves survival and reduces the incidence and severity of NEC in a rodent model. Foxp3(+) regulatory T cells (Tregs) maintain intestinal homeostasis by controlling inflammation and inducing tolerance. To determine whether there are insufficient numbers of Tregs to control inflammation in NEC and to determine if LR17938 increases the frequency of Tregs, we studied selected groups of newborn Sprague-Dawley rats according to feeding plan: dam±LR17938, formula±LR17938, and NEC±LR17938. NEC was induced by gavage feeding with special formula and exposure to hypoxic conditions. Lymphocytes isolated from ileum, mesenteric lymph nodes (MLN), spleen and thymus were labeled for T cell surface markers (CD3, CD4, CD8) and intracellular Foxp3; and labeled cells were analyzed by flow cytometry. The percentage of CD3(+) T cells and Foxp3(+) Tregs in the ileum significantly decreased in pups with NEC, compared to normal controls. Feeding LR17938 to neonatal rats with NEC increased the % of Foxp3(+) T cells in the ileum while decreasing the percentage of cells in the MLN. Administration of LR17938 to dam-fed rats significantly increased Foxp3(+)Tregs in the ileum as early as day of life (DOL)1 but did not produce an increase in Tregs in formula-fed rats on DOL1. These results suggest that factors in breast milk may enhance the early immunomodulatory effects of LR17938. An anti-inflammatory effect of LR17938 in NEC was associated with the modulation of immune responses and induction and what appears to be migration of Foxp3(+) Tregs to the diseased gut. Probiotic-facilitated development of Tregs might play an important role in the prevention of NEC.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23437165</pmid><doi>10.1371/journal.pone.0056547</doi><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2013-02, Vol.8 (2), p.e56547 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1330882050 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Animals Antigens Bacteria Biology Breast milk Breastfeeding & lactation CD3 antigen CD4 antigen CD8 antigen Cell surface Cytometry Enterocolitis Enterocolitis - chemically induced Enterocolitis - metabolism Enterocolitis - pathology Feeding Flow cytometry Forkhead Transcription Factors - metabolism Foxp3 protein Gastroenterology Gastrointestinal diseases Homeostasis Hypoxia Ileum Immune response Immune system Immunological tolerance Immunology Immunomodulation Immunoregulation Infants Inflammation - drug therapy Inflammation - immunology Inflammation - metabolism Intestinal Mucosa - metabolism Intestine Intestines - drug effects Intestines - immunology Lactobacillus reuteri Lactobacillus reuteri - chemistry Leukocyte migration Lupus Lymph Lymph nodes Lymph Nodes - drug effects Lymph Nodes - immunology Lymph Nodes - metabolism Lymph Nodes - pathology Lymphatic system Lymphocytes Lymphocytes T Medical schools Medicine Mesentery - drug effects Mesentery - immunology Mesentery - metabolism Mesentery - pathology Milk Necrosis Necrotizing enterocolitis Neonates Newborn babies Pediatrics Probiotics Probiotics - administration & dosage Probiotics - chemistry Rats Rats, Sprague-Dawley Rodents Science Small intestine Spleen Surface markers T-Lymphocytes, Regulatory - immunology T-Lymphocytes, Regulatory - metabolism T-Lymphocytes, Regulatory - pathology Thymus |
| title | Lactobacillus reuteri DSM 17938 changes the frequency of Foxp3+ regulatory T cells in the intestine and mesenteric lymph node in experimental necrotizing enterocolitis |
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