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The developmentally regulated fetal enterocyte gene, ZP4, mediates anti-inflammation by the symbiotic bacterial surface factor polysaccharide A on Bacteroides fragilis

Journal article
Authors Frida Gorreja
S. T. A. Rush
D. L. Kasper
D. Meng
W. A. Walker
Published in American Journal of Physiology-Gastrointestinal and Liver Physiology
Volume 317
Issue 4
Pages G398-G407
ISSN 0193-1857
Publication year 2019
Published at Institute of Biomedicine, Department of Microbiology and Immunology
Pages G398-G407
Language en
Links dx.doi.org/10.1152/ajpgi.00046.2019
Keywords immature enterocytes, initial intestinal colonization, necrotizing, enterocolitis, polysaccharide A, zona pellucida protein 4, zona-pellucida glycoproteins, necrotizing enterocolitis, domain, proteins, epithelium, probiotics, infantis, colonization, expression, secretions, microbiota, Gastroenterology & Hepatology, Physiology
Subject categories Physiology, Gastroenterology and Hepatology

Abstract

Initial colonizing bacteria play a critical role in completing the development of the immune system in the gastrointestinal tract of infants. Yet, the interaction of colonizing bacterial organisms with the developing human intestine favors inflammation over immune homeostasis. This characteristic of bacterial-intestinal interaction partially contributes to the pathogenesis of necrotizing enterocolitis (NEC), a devastating premature infant intestinal inflammatory disease. However, paradoxically some unique pioneer bacteria (initial colonizing species) have been shown to have a beneficial effect on the homeostasis of the immature intestine and the prevention of inflammation. We have reported that one such pioneer bacterium, Bacteroides fragilis (B. fragilis), and its surface component polysaccharide A (PSA) inhibit IL-1β-induced inflammation in a human primary fetal small intestinal cell line (H4 cells). In this study, using transcription profiling of H4 cellular RNA after pretreatment with or without PSA before an inflammatory stimulation of IL-1β, we have begun to further determine the cellular mechanism for anti-inflammation. We show that a developmentally regulated gene, zona pellucida protein 4 (ZP4), is uniquely elevated after IL-1β stimulation and reduced with PSA exposure. ZP4 was known as a sperm receptor-mediating species-specific binding protein in the initial life of mammals. However, its intestinal epithelial function is unclear. We found that ZP4 is a developmentally regulated gene involved with immune function and regulated by both Toll-like receptor 2 and 4. Knockdown of ZP4-affected PSA inhibited IL-8 mRNA expression in response to IL-1β. This represents an initial study of ZP4 innate immune function in immature enterocytes. This study may lead to new opportunity for efficient treatment of NEC. NEW & NOTEWORTHY This study extends previous observations to define the cellular mechanisms of polysaccharide A-induced anti-inflammation in immature enterocytes using transcription profiling of enterocyte genes after preexposure to polysaccharide A before an inflammatory stimulus with IL-1β.

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