Protective effects of bifidobacterium on intestinal barrier function in LPS-induced enterocyte barrier injury of Caco-2 monolayers and in a rat NEC model

PLoS ONE

Volumn 11, Issue 8, 2016, Pages

  Ling, Xiang ^a,c   Linglong, Peng ^b   Weixia, Du ^b   Hong, Wei ^a  

^a BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^b CHONGQING MEDICAL UNIVERSITY   (China)

^c Second People's Hospital of Chengdu   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 3; INTERLEUKIN 6; PROBIOTIC AGENT; PROTEIN ZO1; TUMOR NECROSIS FACTOR; BIOLOGICAL MARKER; CHOLERA TOXIN; CYTOKINE; ZONULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIFIDOBACTERIUM; CACO 2 CELL LINE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; DRUG MECHANISM; HUMAN; HUMAN CELL; ILEUM; IN VITRO STUDY; IN VIVO STUDY; INTESTINAL BARRIER FUNCTION; INTESTINE; INTESTINE CELL; INTESTINE MUCOSA PERMEABILITY; NECROTIZING ENTEROCOLITIS; NEWBORN; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SECRETION; RAT; SURVIVAL RATE; TIGHT JUNCTION; UPREGULATION; ANIMAL; CACO-2 CELL LINE; DISEASE MODEL; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; PATHOLOGY; PERMEABILITY; PHYSIOLOGY; SEVERITY OF ILLNESS INDEX;

ANIMALS; BIFIDOBACTERIUM; BIOMARKERS; CACO-2 CELLS; CHOLERA TOXIN; CYTOKINES; DISEASE MODELS, ANIMAL; ENTEROCOLITIS, NECROTIZING; ENTEROCYTES; HUMANS; ILEUM; INTESTINAL MUCOSA; PERMEABILITY; RATS; SEVERITY OF ILLNESS INDEX; TIGHT JUNCTIONS;

EID: 84984797655     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0161635     Document Type: Article

References (43)

1. Arrieta MC, Bistritz L, Meddings JB. Alterations in intestinal permeability. Gut. 2006;55(10):1512-20. PMID: 16966705.
2. Fanning AS, Mitic LL, Anderson JM. Transmembrane proteins in the tight junction barrier. J Am Soc Nephrol. 2009;10(6):1337-45. PMID: 10361874.
3. Furuse M, Hata M, Furuse K, Yoshida Y, Haratake A, Sugitani Y, et al. Claudin-based tight junctions are crucial forthe mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J Cell Biol. 2002;156(6):1099-111. PMID: 11889141.
4. Fanning AS, Jameson BJ, Jesaitis LA, Anderson JM. The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J Biol Chem. 1998;273(45):29745-53. PMID: 9792688.
5. Clark JA, Doelle SM, Halpern MD, Saunders TA., Holubec H, Dvorak K, et al. Intestinal barrier failure during experimental necrotizing enterocolitis: protective effect of EGF treatment. Am J Physiol Gastrointest Liver Physiol. 2006;291(5):G938-49. Epub 2006/06/22. PMID: 16798726.
6. Anand RJ, Leaphart CL, Mollen KP, Hackam DJ. The role of the intestinal barrier in the pathogenesis of necrotizing enterocolitis. Shock. 2007;27(2):124-33. PMID: 17224785.
7. Halpern MD, Denning PW. The role of intestinal epithelial barrier function in the development of NEC. Tissue Barriers. 2015;3(1-2):e1000707. doi: 10.1080/21688370.2014.1000707 PMID: 25927016
8. Sharma R, Tepas JJ. Microecology, intestinal epithelial barrier and necrotizing enterocolitis. Pediatr Surg Int. 2010;26(1):11-21. Epub 2009/12/05. doi: 10.1007/s00383-009-2536-2 PMID: 19967379.
9. Yoshioka N, Taniguchi Y, Yoshida A, Nakata K, Nishizawa T, Inagawa H, et al. Intestinal macrophages involved in the homeostasis of the intestine have the potential for responding to LPS. Anticancer Res. 2009;29(11):4861-5.
10. Han X, Fink MP, Yang R, Delude RL. Increased iNOS activity is essential for intestinal epithelial tight junction dysfunction in endotoxemic mice. Shock. 2004;21(3):261-70. PMID: 14770040.
11. Noerr B. Current controversies in the understanding of necrotizing enterocolitis. Adv Neonatal Care. 2003;3(3):107-20. PMID: 12891835.
12. Duffy LC, Zielezny MA, Carrion V, Griffiths E, Dryja D, Hilty M, et al. Concordance of bacterial cultures with endotoxin and interleukin-6 in necrotizing enterocolitis. Dig Dis Sci. 1997;42(2):359-65. PMID: 9052520.
13. Fasano A, Uzzau S. Modulation of intestinal tight junctions by Zonula occludens toxin permits enteral administration of insulin and other macro-molecules in an animal model. J Clin Invest. 1997;99(6):1158-64. PMID: 9077522.
14. Fasano A, Fiorentini C, Donelli G, Uzzau S, Kaper JB, Margaretten K, et al. Zonula occludens toxin modulates tight junctions through protein kinase C-dependent actin reorganization, in vitro. J Clin Invest. 1995;96(2):710-720. PMID: 7635964.
15. Watts T, Berti I, Sapone A, Gerarduzzi T, Not T, Zielke R, et al. Role of the intestinal tight junction modulator zonulin in the pathogenesis of type I diabetes in BB diabetic-prone rats. Proc Natl Acad Sci USA. 2005;102(8):2916-21. Epub 2005/02/14. PMID: 15710870.
16. Fasano A, Not T, Wang W, Uzzau S, Berti I, Tommasini A, et al. Zonulin, a newly discovered modulator of intestinal permeability, and its expression in coeliac disease. Lancet. 2000;355(9214):1518-19. PMID: 10801176.
17. El Asmar R, Panigrahi P, Bamford P, Berti I, Not T, Coppa GV, et al. Host-dependent zonulin secretion causes the impairment of the small intestine barrier function after bacterial exposure. Gastroenterology. 2002;123(5):1607-15. PMID: 12404235.
18. Piena-Spoel M, Albers MJ, ten Kate J, Tibboel D. Intestinal permeability in newborns with necrotizing enterocolitis and controls: does the sugar absorption test provide guidelines for the time to (reintroduce enteral nutrition?. J Pediatr Surg. 2001;36(4):587-92. PMID: 11283883.
19. Hammerman C, Bin-Nun A, Kaplan M. Germ warfare: probiotics in defense of the premature gut. Clin Perinatol. 2004;31(3):489-500. PMID: 15325534.
20. Martin CR, Walker WA. Probiotics: role in pathophysiology and prevention in necrotizing enterocolitis. Semin Perinatol. 2008;32(2):127-37. doi: 10.1053/j.semperi.2008.01.006 PMID: 18346537.
21. Ewaschuk JB, Diaz H, Meddings L, Diederichs B, Dmytrash A, Backer J, et al. Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am J Physiol Gastrointest Liver Physiol. 2008;295(5):G1025-34. Epub 2008/09/11. doi: 10.1152/ajpgi.90227.2008 PMID: 18787064.
22. Khailova L, Dvorak K, Arganbright KM, Halpern MD, Kinouchi T, Yajima M, et al. Bifidobacterium bifidum improves intestinal integrity in a rat model of necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol. 2009;297(5):G940-49. PMID: 20501441.
23. Bergmann KR, Liu SX, Tian R, Kushnir A, Turner JR, Li HL, et al. Bifidobacteria stabilize claudins at tight junctions and prevent intestinal barrier dysfunction in mouse necrotizing enterocolitis. Am J Pathol. 2013;182(5):1595-606. Epub 2013/03/05. doi: 10.1016/j.ajpath.2013.01.013 PMID: 23470164.
24. Lin HC, Hsu CH, Chen HL, Chung MY, Hsu JF, Lien RI, et al. Oral probiotics prevent necrotizing enterocolitis in very low birth weight preterm infants: a multicenter, randomized, controlled trial. Pediatrics. 2008;122(4), 693-700. doi: 10.1542/peds.2007-3007 PMID: 18829790.
25. Nadler EP, Dickinson E, Knisely A, Zhang XR, Boyle P, Beer-Stolz D, et al. Expression of inducible nitric oxide synthase and interleukin-12 in experimental necrotizing enterocolitis. Surg Res. 2000;92(1):71-7. PMID: 10864485.
26. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes. 2008;57(6):1470-81. Epub 2008/02/27. doi: 10.2337/db07-1403 PMID: 18305141.
27. Neu J, Walker WA. Necrotizing enterocolitis. N Engl J Med. 2011;364(3):255-64. doi: 10.1056/NEJMra1005408 PMID: 21247316.
28. Berman L, Moss RL. Necrotizing enterocolitis: an update. Semin Fetal Neonatal Med. 2011;16(3):145-50. Epub 2011/04/22. doi: 10.1016/j.siny.2011.02.002 PMID: 21514258.
29. Ivanov AI, Nusrat A, Parkos CA. The epithelium in inflammatory bowel disease: potential role of endocytosis of junctional proteins in barrier disruption. Novartis Found Symp. 2004;263:115-24; discussion 124-32, 211-8. PMID: 15669638.
30. Chen J, Zhang R, Wang J, Yu P, Liu Q, Zeng D, et al. Protective effects of baicalin on LPS-induced injury in intestinal epithelial cells and intercellulartightjunctions. Can J Physiol Pharmacol. 2015;93(4):233-7. Epub 2014/12/16. doi: 10.1139/cjpp-2014-0262 PMID: 25665915.
31. Groschwitz KR, Hogan SP. Intestinal barrier function: molecular regulation and disease pathogenesis. J Allergy Clin Immunol. 2009;124(1):3-20. doi: 10.1016/j.jaci.2009.05.038 PMID: 19560575.
32. Buck C, Bundschu J, Gallati H, Bartmann P, Pohlandt F. Interleukin-6: a sensitive parameter for the early diagnosis of neonatal bacterial infection. Pediatrics. 1994;93(1):54-8. PMID: 8265324.
33. De Bont ES, Martens A, van Raan J, Samson G, Fetter WP, Okken A, et al. Diagnostic value of plasma levels of tumor necrosis factor alpha (TNF alpha) and interleukin-6 (IL-6) in newborns with sepsis. Acta Paediatr. 1994;83(7):696-9. PMID: 7949797.
34. Schneeberger EE, Lynch RD. The tight junction: a multifunctional complex. Am J Physiol Cell Physiol. 2004;286(6):C1213-28. PMID: 15151915.
35. Nusrat A, Turner JR, Madara JL. Molecular physiology and pathophysiology of tight junctions. IV. Regulation of tight junctions by extracellular stimuli: nutrients, cytokines, and immune cells. Am J Physiol Gastrointest Liver Physiol. 2000;279(5):G851-7. PMID: 11052980.
36. Prasad S, Mingrino R, Kaukinen K, Hayes KL, Powell RM, MacDonald TT, et al. Inflammatory processes have differential effects on claudins2, 3 and 4 in colonic epithelial cells. Lab Invest. 2005;85(9):1139-62. PMID: 16007110.
37. Ivanov AI, Nusrat A, Parkos CA. The epithelium in inflammatory bowel disease: potential role of endocytosis of junctional proteins in barrier disruption. Novartis Found Symp. 2004;263:115-24; discussion 124-32, 211-8. PMID: 15669638.
38. Hackam DJ, Upperman JS, Grishin A, Ford HR. Disordered enterocyte signaling and intestinal barrier dysfunction in the pathogenesis of necrotizing enterocolitis. Semin PediatrSurg. 2005;14(1):49-57. PMID: 15770588.
39. Shiou SR, Yu Y, Chen S, Ciancio MJ, Petrof EO, Sun J, et al. Erythropoietin protects intestinal epithelial barrier function and lowers the incidence of experimental neonatal necrotizing enterocolitis. J Biol Chem. 2011;286(14):12123-32. Epub 2011/01/24. doi: 10.1074/jbc. M110.154625 PMID: 21262973.
40. Muto S, Hata M, Taniguchi J, Tsuruoka S, Moriwaki K, Saitou M, et al. Claudin-2-deficient mice are defective in the leaky and cation-selective paracellular permeability properties of renal proximal tubules. Proc Natl Acad Sci USA. 2010;107(17):8011-6. Epub 2010/04/12. doi: 10.1073/pnas. 0912901107 PMID: 20385797.
41. Saitoh R, Sugano K, Takata N, Tachibana T, Higashida A, Nabuchi Y, et al. Correction of permeability with pore radius of tight junctions in Caco-2 monolayers improves the prediction of the dose fraction of hydrophilic drugs absorbed by humans. Pharm Res. 2004;21(5):749-55. PMID: 15180329.
42. Klaus DA, Motal MC, Burger-Klepp U, Marschalek C, Schmidt EM, Lebherz-Eichinger D, et al. Increased plasma zonulin in patients with sepsis. BiochemMed. 2013;23(1):107-11. PMID: 23457771.
43. Hackam DJ, Upperman JS, Grishin A, Ford HR. Disordered enterocyte signaling and intestinal barrier dysfunction in the pathogenesis of necrotizing enterocolitis. Semin PediatrSurg. 2005;14(1):49-57. PMID: 15770588.