publication . Other literature type . Article . 2014

The microbiota regulates neutrophil homeostasis and host resistance to Escherichia coli K1 sepsis in neonatal mice

Hitesh S Deshmukh; Yuhong Liu; Ogechukwu R Menkiti; Junjie Mei; Ning Dai; Claire E O'Leary; Paula M Oliver; Jay K Kolls; Jeffrey N Weiser; G Scott Worthen;
  • Published: 20 Apr 2014
  • Publisher: Springer Science and Business Media LLC
Abstract
Acquisition of microbes by the neonate, which begins immediately during birth, is influenced by gestational age and mother’s microbiota and modified by exposure to antibiotics1. In neonates, prolonged duration of antibiotic therapy is associated with increased risk of sepsis after 4 days of life, known as late-onset sepsis (LOS)2, a disorder critically controlled by neutrophils3, but a role for the microbiota in regulating neutrophil behavior in the neonate has not been described. We exposed pregnant mouse dams to antibiotics in drinking water to limit transfer of maternal microbes to the neonates. Antibiotic exposure of dams decreased the total number of microb...
Subjects
free text keywords: General Biochemistry, Genetics and Molecular Biology, General Medicine, Immunology, Granulocyte, medicine.anatomical_structure, medicine, Granulocyte colony-stimulating factor, Innate lymphoid cell, Escherichia coli, medicine.disease_cause, Neutrophil homeostasis, Granulocytosis, medicine.disease, Microbiology, Biology, Interleukin 17, Sepsis, Article
Funded by
NIH| Nedd4-family adaptors and their regulation of T cell function.
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01AI093566-05
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
,
NIH| Mechanisms of pneumococcal persistence during carriage
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01AI038446-13
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
,
NIH| Training Program in Genome-Environment Interactions in Neonatal Disease
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5T32HD060556-03
  • Funding stream: EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH & HUMAN DEVELOPMENT
,
NIH| T cells and P carinii Pneumonia
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01HL062052-18
  • Funding stream: NATIONAL HEART, LUNG, AND BLOOD INSTITUTE
,
NIH| CXC Chemokines and Regulation of Granulopoiesis
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01AI099479-03
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
45 references, page 1 of 3

Penders, J. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006; 118: 511-521 [OpenAIRE] [PubMed]

Kuppala, VS, Meinzen-Derr, J, Morrow, AL, Schibler, KR. Prolonged initial empirical antibiotic treatment is associated with adverse outcomes in premature infants. The Journal of pediatrics. 2011; 159: 720-725 [OpenAIRE] [PubMed]

Sarkar, S, Bhagat, I, Hieber, S, Donn, SM. Can neutrophil responses in very low birth weight infants predict the organisms responsible for late-onset bacterial or fungal sepsis?. Journal of perinatology: official journal of the California Perinatal Association. 2006; 26: 501-505 [OpenAIRE] [PubMed]

Schwiertz, A. Development of the intestinal bacterial composition in hospitalized preterm infants in comparison with breast-fed, full-term infants. Pediatric research. 2003; 54: 393-399 [OpenAIRE] [PubMed]

Pflughoeft, KJ, Versalovic, J. Human microbiome in health and disease. Annual review of pathology. 2012; 7: 99-122 [OpenAIRE]

Mai, V. Distortions in development of intestinal microbiota associated with late onset sepsis in preterm infants. PloS one. 2013; 8: e52876 [OpenAIRE] [PubMed]

Palmer, C, Bik, EM, DiGiulio, DB, Relman, DA, Brown, PO. Development of the human infant intestinal microbiota. PLoS biology. 2007; 5: e177 [OpenAIRE] [PubMed]

Vael, C, Desager, K. The importance of the development of the intestinal microbiota in infancy. Current opinion in pediatrics. 2009; 21: 794-800 [OpenAIRE] [PubMed]

Koenig, JE. Succession of microbial consortia in the developing infant gut microbiome. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108 (Suppl 1): 4578-4585 [OpenAIRE] [PubMed]

Alm, B. Neonatal antibiotic treatment is a risk factor for early wheezing. Pediatrics. 2008; 121: 697-702 [PubMed]

Clark, RH, Bloom, BT, Spitzer, AR, Gerstmann, DR. Empiric use of ampicillin and cefotaxime, compared with ampicillin and gentamicin, for neonates at risk for sepsis is associated with an increased risk of neonatal death. Pediatrics. 2006; 117: 67-74 [PubMed]

Manroe, BL, Weinberg, AG, Rosenfeld, CR, Browne, R. The neonatal blood count in health and disease. I. Reference values for neutrophilic cells. The Journal of pediatrics. 1979; 95: 89-98 [OpenAIRE] [PubMed]

Gessler, P. Neonatal neutropenia in low birthweight premature infants. American journal of perinatology. 1995; 12: 34-38 [PubMed]

Martin, C. Chemokines acting via CXCR2 and CXCR4 control the release of neutrophils from the bone marrow and their return following senescence. Immunity. 2003; 19: 583-593 [PubMed]

Pluschke, G, Pelkonen, S. Host factors in the resistance of newborn mice to K1 Escherichia coli infection. Microbial pathogenesis. 1988; 4: 93-102 [PubMed]

45 references, page 1 of 3
Abstract
Acquisition of microbes by the neonate, which begins immediately during birth, is influenced by gestational age and mother’s microbiota and modified by exposure to antibiotics1. In neonates, prolonged duration of antibiotic therapy is associated with increased risk of sepsis after 4 days of life, known as late-onset sepsis (LOS)2, a disorder critically controlled by neutrophils3, but a role for the microbiota in regulating neutrophil behavior in the neonate has not been described. We exposed pregnant mouse dams to antibiotics in drinking water to limit transfer of maternal microbes to the neonates. Antibiotic exposure of dams decreased the total number of microb...
Subjects
free text keywords: General Biochemistry, Genetics and Molecular Biology, General Medicine, Immunology, Granulocyte, medicine.anatomical_structure, medicine, Granulocyte colony-stimulating factor, Innate lymphoid cell, Escherichia coli, medicine.disease_cause, Neutrophil homeostasis, Granulocytosis, medicine.disease, Microbiology, Biology, Interleukin 17, Sepsis, Article
Funded by
NIH| Nedd4-family adaptors and their regulation of T cell function.
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01AI093566-05
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
,
NIH| Mechanisms of pneumococcal persistence during carriage
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01AI038446-13
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
,
NIH| Training Program in Genome-Environment Interactions in Neonatal Disease
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5T32HD060556-03
  • Funding stream: EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH & HUMAN DEVELOPMENT
,
NIH| T cells and P carinii Pneumonia
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01HL062052-18
  • Funding stream: NATIONAL HEART, LUNG, AND BLOOD INSTITUTE
,
NIH| CXC Chemokines and Regulation of Granulopoiesis
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01AI099479-03
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
45 references, page 1 of 3

Penders, J. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006; 118: 511-521 [OpenAIRE] [PubMed]

Kuppala, VS, Meinzen-Derr, J, Morrow, AL, Schibler, KR. Prolonged initial empirical antibiotic treatment is associated with adverse outcomes in premature infants. The Journal of pediatrics. 2011; 159: 720-725 [OpenAIRE] [PubMed]

Sarkar, S, Bhagat, I, Hieber, S, Donn, SM. Can neutrophil responses in very low birth weight infants predict the organisms responsible for late-onset bacterial or fungal sepsis?. Journal of perinatology: official journal of the California Perinatal Association. 2006; 26: 501-505 [OpenAIRE] [PubMed]

Schwiertz, A. Development of the intestinal bacterial composition in hospitalized preterm infants in comparison with breast-fed, full-term infants. Pediatric research. 2003; 54: 393-399 [OpenAIRE] [PubMed]

Pflughoeft, KJ, Versalovic, J. Human microbiome in health and disease. Annual review of pathology. 2012; 7: 99-122 [OpenAIRE]

Mai, V. Distortions in development of intestinal microbiota associated with late onset sepsis in preterm infants. PloS one. 2013; 8: e52876 [OpenAIRE] [PubMed]

Palmer, C, Bik, EM, DiGiulio, DB, Relman, DA, Brown, PO. Development of the human infant intestinal microbiota. PLoS biology. 2007; 5: e177 [OpenAIRE] [PubMed]

Vael, C, Desager, K. The importance of the development of the intestinal microbiota in infancy. Current opinion in pediatrics. 2009; 21: 794-800 [OpenAIRE] [PubMed]

Koenig, JE. Succession of microbial consortia in the developing infant gut microbiome. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108 (Suppl 1): 4578-4585 [OpenAIRE] [PubMed]

Alm, B. Neonatal antibiotic treatment is a risk factor for early wheezing. Pediatrics. 2008; 121: 697-702 [PubMed]

Clark, RH, Bloom, BT, Spitzer, AR, Gerstmann, DR. Empiric use of ampicillin and cefotaxime, compared with ampicillin and gentamicin, for neonates at risk for sepsis is associated with an increased risk of neonatal death. Pediatrics. 2006; 117: 67-74 [PubMed]

Manroe, BL, Weinberg, AG, Rosenfeld, CR, Browne, R. The neonatal blood count in health and disease. I. Reference values for neutrophilic cells. The Journal of pediatrics. 1979; 95: 89-98 [OpenAIRE] [PubMed]

Gessler, P. Neonatal neutropenia in low birthweight premature infants. American journal of perinatology. 1995; 12: 34-38 [PubMed]

Martin, C. Chemokines acting via CXCR2 and CXCR4 control the release of neutrophils from the bone marrow and their return following senescence. Immunity. 2003; 19: 583-593 [PubMed]

Pluschke, G, Pelkonen, S. Host factors in the resistance of newborn mice to K1 Escherichia coli infection. Microbial pathogenesis. 1988; 4: 93-102 [PubMed]

45 references, page 1 of 3
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