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PMID: 10823949 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Inflammation in the developing human intestine: A possible pathophysiologic contribution to necrotizing enterocolitis.

Nanthakumar NN, Fusunyan RD, Sanderson I, Walker WA

Abstract

Necrotizing enterocolitis (NEC), a major cause of morbidity and mortality in premature infants, occurs after the introduction of oral feedings in conjunction with initial bacterial colonization of the gut and is hypothesized to be due to an immature (inappropriate) enterocyte response to bacterial stimuli. To test this hypothesis, we compared the enterocyte IL-8 response to inflammatory stimuli [lipopolysaccharide (LPS) and IL-1beta] in immature vs. mature human small intestine. Initial in vitro studies comparing confluent Caco-2 cells, a model for mature human enterocytes, with a primary human fetal intestinal cell line (H4 cells) demonstrated that after inflammatory stimulation fetal cells secreted more IL-8 (LPS, 8-fold; IL-1beta, 20-fold) than Caco-2 cells. IL-8 mRNA activity in fetal compared to Caco-2 cells was proportionately increased by the same magnitude with both stimuli. To validate the in vitro observations, small intestinal organ cultures from fetuses vs. older children were exposed to LPS and IL-1beta. Again in human organ cultures from fetuses compared to older children, IL-8 secretion was greater (LPS, 2.5-fold; IL-1beta, 200-fold) and mRNA activity after stimulation was comparably higher, suggesting that increased transcription of the IL-8 gene may account for the excessive response. Using immunohistochemical staining to identify the cellular source of IL-8, activity was noted predominantly in villous and crypt epithelium but also in a few immunoresponsive lymphoid cells. The observation that immature human enterocytes react with excessive pro-inflammatory cytokine production after inflammatory stimulation may help in part explain why prematures exposed to initial colonizing bacteria develop necrotizing enterocolitis.

MeSH Terms
Adenocarcinoma/pathology Age Factors Cell Line Child Colonic Neoplasms/pathology Duodenum/drug effects,embryology,growth & development,immunology,metabolism,pathology Enterocolitis, Necrotizing/etiology Gestational Age Gram-Negative Bacteria/immunology Humans Inflammation Interleukin-1/pharmacology Interleukin-8/biosynthesis,genetics,metabolism Intestinal Mucosa/cytology,drug effects,metabolism Lipopolysaccharides/pharmacology Organ Culture Techniques RNA, Messenger/biosynthesis Tumor Cells, Cultured/drug effects,metabolism
Chemicals
Interleukin-1 Interleukin-8 Lipopolysaccharides RNA, Messenger
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Nanthakumar N N
Developmental Gastroenterology Laboratory, Combined Program in Pediatric Gastroenterology and Nutrition, Massachusetts General Hospital, Department of Pediatrics, Harvard Medical School, 149 13th Street, Charlestown, MA 02129, USA.
Fusunyan R D
Sanderson I
Walker W A
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Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2000-05-23
Pages
6043-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC18555
Subset
IM
Grants
NIDDK NIH HHS · P01 DK-33506 · United States
NIDDK NIH HHS · P30 DK040561 · United States
NICHD NIH HHS · R37 HD012437 · United States
NIDDK NIH HHS · P01 DK033506 · United States
NICHD NIH HHS · R37 HD-12437 · United States
NICHD NIH HHS · R01 HD-31852 · United States
NICHD NIH HHS · R01 HD031852 · United States
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