Probiotics prevent necrotizing enterocolitis by modulating enterocyte genes that regulate innate immune-mediated inflammation

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 304, Issue 2, 2013, Pages

  Ganguli, Kriston ^a,b   Meng, Di ^a,b   Rautava, Samuli ^a,b   Lu, Lei ^a,b   Walker, W Allan ^a,b   Nanthakumar, Nanda ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Bifidobacterium infantis; Development of intestinal defense; Innate immune response; Probiotic secretions; Toll like receptors

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; DEOXYRIBONUCLEASE; INTERLEUKIN 6; INTERLEUKIN 8; PLACEBO; PROBIOTIC AGENT; PROTEINASE; RIBONUCLEASE; SIGIRR PROTEIN; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 2; TOLLIP PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIUM CULTURE; BIFIDOBACTERIUM LONGUM INFANTIS; CELL MATURATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSFECTION; HEAT STRESS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOASSAY; IMMUNOGENETICS; IMMUNOMODULATION; INFANT; INNATE IMMUNITY; INTESTINE CELL; LACTOBACILLUS ACIDOPHILUS; MAJOR CLINICAL STUDY; NECROTIZING ENTEROCOLITIS; NEWBORN; PREMATURITY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; VERY LOW BIRTH WEIGHT;

ANIMALS; BIFIDOBACTERIUM; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; ENTEROCOLITIS, NECROTIZING; ENTEROCYTES; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; INTERLEUKIN-6; INTERLEUKIN-8; INTESTINE, SMALL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LACTOBACILLUS ACIDOPHILUS; MICE; MICE, SCID; ORGAN CULTURE TECHNIQUES; PRIMARY CELL CULTURE; PROBIOTICS; RECEPTORS, INTERLEUKIN-1; RNA INTERFERENCE; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

EID: 84872389063     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00142.2012     Document Type: Article

References (32)

1. Bin-Nun A, Bromiker R, Wilschanski M, Kaplan M, Rudensky B, Caplan M, Hammerman C. Oral probiotics prevent necrotizing enterocolitis in very low birth weight neonates. J Pediatr 147: 192-196, 2005.
2. Broekaert IJ, Nanthakumar NN, Walker WA. Secreted probiotic factors ameliorate enteropathogenic infection in zinc-deficient human Caco-2 and T84 cell lines. Pediatr Res 62: 139-144, 2007.
3. Caplan MS, Simon D, Jilling T. The role of PAF, TLR, and the inflammatory response in neonatal necrotizing enterocolitis. Semin Pediatr Surg 14: 145-151, 2005.
4. Claud EC, Lu L, Anton PM, Savidge T, Walker WA, Cherayil B. Developmentally regulated IkB expression in intestinal epithelium and susceptibility to flagellin-induced inflammation. Proc Natl Acad Sci USA 101: 7404-7408, 2004.
5. Claud EC, Walker WA. Bacterial colonization, probiotics, and necrotizing enterocolitis. J Clin Gastroenterol 42 Suppl: S46-S52, 2008.
6. Deshpande G, Rao S, Patole S, Bulsara M. Updated meta-analysis of probiotics for preventing necrotizing enterocolitis in preterm neonates. Pediatrics 125: 921-930, 2010.
7. Eibl MM, Wolf HM, Fürnkranz H, Rosenkranz A. Prevention of necrotizing enterocolitis in low-birth-weight infants by IgA-IgG feeding. N Engl J Med 319: 1-7, 1988.
8. Food and Agriculture Organization (FAO) of the United Nations and World Health Organization (WHO). Guidelines for the Evaluation of Probiotics in Food. Report of a Joint FAO/WHO Working Group on Drafting Guidelines for the Evaluation of Probiotics in Food (Online). http://ftp.fao.org/es/esn/food/wgreport2.pdf [7 Dec. 2006].
9. Fusunyan RD, Nanthakumar NN, Baldeon ME, Walker WA. Evidence for an innate immune response in the immature human intestine: Toll-like receptors on fetal enterocytes. Pediatr Res 49: 589-593, 2001.
10. Ganguli K, Walker WA. Probiotics in the prevention of necrotizing enterocolitis. J Clin Gastroenterol 45 Suppl: S133-S138, 2011.
11. Grave GD, Nelson SA, Walker WA, Moss RL, Dvorak B, Hamilton FA, Higgins R, Raju TNK. New therapies and preventive approaches for necrotizing enterocolitis: report of a research planning workshop. Pediatr Res 62: 510-514, 2007.
12. Halac E, Halac J, Bégué EF, Casañas JM, Indiveri DR, Petit JF, Figueroa MJ, Olmas JM, Rodríguez LA, Obregón RJ, Martinez MV, Grinblat DA, Vilarrodona HO. Prenatal and postnatal corticosteroid therapy to prevent neonatal necrotizing enterocolitis: a controlled trial. J Pediatr 117: 132-138, 1990.
13. Henry MC, Moss RL. Necrotizing enterocolitis. Annu Rev Med 60: 111-124, 2009.
14. Jilling T, Simon D, Lu J, Meng FJ, Li D, Schy R, Thomson RB, Soliman A, Arditi M, Caplan MS. The roles of bacteria and TLR4 in rat and murine models of necrotizing enterocolitis. J Immunol 177: 3273-3282, 2006.
15. Lee JS, Polin RA. Treatment and prevention of necrotizing enterocolitis. Semin Neonatol 8: 449-459, 2003.
16. Lin HC, Su BH, Chen AC, Lin TW, Tsai CH, Yeh TF, Oh W. Oral probiotics reduce the incidence and severity of necrotizing enterocolitis in very low birth weight infants. Pediatrics 115: 1-4, 2005.
17. Lin HC, Hsu CH, Chen HL, Chung MY, Hsu JF, Lien RI, Tsao LY, Chen CH, Su BH. Oral probiotics prevent necrotizing enterocolitis in very low birth weight preterm infants: a multicenter, randomized, controlled trial. Pediatrics 122: 693-700, 2008.
18. Lin PW, Stoll BJ. Necrotising enterocolitis. Lancet 368: 1271-1283, 2006.
19. Lu L, Li T, Williams G, Petit E, Borowsky M, Walker WA. Hydrocortisone induces changes in gene expression and differentiation in immature human enterocytes. Am J Physiol Gastrointest Liver Physiol 300: G425-G432, 2011.
20. Nanthakumar NN, Fusunyan RD, Sanderson I, Walker WA. Inflammation in the developing human intestine: a possible pathophysiological contribution to necrotizing enterocolitis. Proc Natl Acad Sci USA 97: 6043-6048, 2000.
21. Nanthakumar NN, Klopcic CE, Fernandez I, Walker WA. Normal and glucocorticoid-induced development of the human small intestinal xenograft. Am J Physiol Regul Integr Comp Physiol 285: R162-R170, 2003.
22. Nanthakumar NN, Young C, Ko JS, Meng D, Buie T, Walker WA. Glucocorticoid responsiveness in developing human intestine: possible role in prevention of necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 288: G85-G92, 2005.
23. Nanthakumar N, Meng D, Goldstein AM, Zhu W, Lu L, Uauy R, Llanos A, Claud EC, Walker WA. The mechanism of excessive intestinal inflammation in necrotizing enterocolitis: an immature innate immune response. PLoS ONE 6: e17776, 2011.
24. Neu J, Walker WA. Necrotizing enterocolitis. N Engl J Med 364: 255-264, 2011.
25. Ohnuma K, Yamochi T, Uchiyama M, Nishibashi K, Iwata S, Hosono O, Kawasaki H, Tanaka H, Dang NH, Morimoto C. CD26 mediates dissociation of Tollip and IRAK-1 from caveolin-1 and induces upregulation of CD86 on antigen-presenting cells. Mol Cell Biol 25: 7743-7757, 2005.
26. Otte JM, Cario E, Podolsky DK. Mechanisms of cross hyporesponsiveness to Toll-like receptor bacterial ligands in intestinal epithelial cells. Gastroenterology 126: 1054-1070, 2004.
27. Rautava S. Potential uses of probiotics in the neonate. Semin Fetal Neonatal Med 12: 45-53, 2007.
28. Slattery MM, Morrison JJ. Preterm delivery. Lancet 360: 1489-1497, 2002.
29. Soliman A, Michelsen KS, Karahashi H, Lu J, Meng FJ, Qu X, Crother TR, Rabizadeh S, Chen S, Caplan MS, Arditi M, Jilling T. Platelet-activating factor induces TLR4 expression in intestinal epithelial cells: implication for the pathogenesis of necrotizing enterocolitis. PLoS One 5: e15044, 2010.
30. Stark AR, Carlo WA, Tyson JE, Papile LA, Wright LL, Shankaran S, Donovan EF, Oh W, Bauer CR, Saha S, Poole WK, Stoll BJ, Fanaroff AA, Ehrenkranz RA, Korones SB, Stevenson DK. Adverse effects of early dexamethasone treatment in extremely-low-birth-weight infants. N Engl J Med 344: 95-101, 2001.
31. Weng M, Walker WA, Sanderson IR. Butyrate regulates the expression of pathogen-triggered IL-8 in intestinal epithelia. Pediatr Res 62: 542-546, 2007.
32. Xiao H, Gulen MF, Qin J, Yao J, Bulek K, Kish D, Altuntas CZ, Wald D, Ma C, Zhou H, Tuohy VK, Fairchild RL, de la Motte C, Cua D, Vallance BA, Li X. The Toll-interleukin-1 receptor member SIGIRR regulates colonic epithelial homeostasis, inflammation, and tumorigenesis. Immunity 26: 461-475, 2007.