Fecal microbiota transplantation (FMT) could reverse the severity of experimental necrotizing enterocolitis (NEC) via oxidative stress modulation

Free Radical Biology and Medicine

Volumn 108, Issue , 2017, Pages 32-43

  Li, Xiaomei ^a   Li, Xiaowen ^a   Shang, Qingjuan ^a,b   Gao, Zongwei ^a,b   Hao, Fabao ^a   Guo, Hongjie ^a   Guo, Chunbao ^a  

^a CHILDREN S HOSPITAL OF CHONGQING MEDICAL UNIVERSITY   (China)

^b LINYI PEOPLE'S HOSPITAL   (China)

Author keywords

eNOS; FMT; NO; S glutathionylation; TLR4

Indexed keywords

CYTOKINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FREE RADICAL; NITRIC OXIDE; PREBIOTIC AGENT; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; GLRX PROTEIN, MOUSE; GLUTAREDOXIN; REACTIVE OXYGEN METABOLITE; TLR4 PROTEIN, MOUSE; TLR9 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL FLORA; BACTERIAL TRANSLOCATION; CONTROLLED STUDY; DISEASE SEVERITY; EXPERIMENTAL MODEL; EXPERIMENTAL NECROTIZING ENTEROCOLITIS; FECAL MICROBIOTA TRANSPLANTATION; HISTOPATHOLOGY; INTESTINE MUCOSA; LYMPHOCYTE; MOUSE; NECROTIZING ENTEROCOLITIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; DISEASE EXACERBATION; GENETICS; HUMAN; IMMUNOLOGY; INFLAMMATION; INTESTINE FLORA; KNOCKOUT MOUSE; METABOLISM; SIGNAL TRANSDUCTION; TRANSCYTOSIS;

ANIMALS; DISEASE PROGRESSION; ENTEROCOLITIS, NECROTIZING; FECAL MICROBIOTA TRANSPLANTATION; GASTROINTESTINAL MICROBIOME; GLUTAREDOXINS; HUMANS; INFLAMMATION; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, ANIMAL; NITRIC OXIDE SYNTHASE TYPE III; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTOR 9; TRANSCYTOSIS;

EID: 85015735207     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2017.03.011     Document Type: Article

References (37)

1. [1] B.J. Stoll, N.I. Hansen, E.F. Bell, M.C. Walsh, W.A. Carlo, S. Shankaran, A.R. Laptook, P.J. Sánchez, K.P. Van Meurs, M. Wyckoff, A. Das, E.C. Hale, M.B. Ball, N.S. Newman, K. Schibler, B.B. Poindexter, K.A. Kennedy, C.M. Cotten, K.L. Watterberg, C.T. D′Angio, S.B. DeMauro, W.E. Truog, U. Devaskar, R.D. Higgins, Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network, Trends in care practices, morbidity, and mortality of extremely preterm neonates 1993–2012, JAMA, 201, 31, pp. 1039–51.
2. [2] R.M. Patel, S. Kandefer, M.C. Walsh, E.F. Bell, W.A. Carlo, A.R. Laptook, P.J. Sánchez, S. Shankaran, K.P. Van Meurs, M.B. Ball, E.C. Hale, N.S. Newman, A. Das, R.D. Higgins, B.J. Stoll, Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network, Causes and timing of death in extremely premature infants from 2000 through 2011, N. Engl. J. Med., 372, 2015, pp. 331–40.
3. [3] Mannoia, K., Boskovic, D.S., Slater, L., Plank, M.S., Angeles, D.M., Gollin, G., Necrotizing enterocolitis is associated with neonatal intestinal injury. J. Pediatr. Surg. 46 (2011), 81–85.
4. [4] Yazji, I., Sodhi, C.P., Lee, E.K., Good, M., Egan, C.E., Afrazi, A., Neal, M.D., Jia, H., Lin, J., Ma, C., Branca, M.F., Prindle, T., Richardson, W.M., Ozolek, J., Billiar, T.R., Binion, D.G., Gladwin, M.T., Hackam, D.J., Endothelial TLR4 activation impairs intestinal microcirculatory perfusion in necrotizing enterocolitis via eNOS-NO-nitrite signaling. Proc. Natl. Acad. Sci. USA 110 (2013), 9451–9456.
5. [5] Jilling, T., Simon, D., Lu, J., Meng, F.J., Li, D., Schy, R., Thomson, R.B., Soliman, A., Arditi, M., Caplan, M.S., The roles of bacteria and TLR4 in rat and murine models of necrotizing enterocolitis. J. Immunol. 177 (2006), 3273–3282.
6. [6] Lu, Peng, Sodhi, Chhinder P., Jia, Hongpeng, Shaffiey, Shahab, Good, Misty, Branca, Maria F., Hackam, David J., Animal models of gastrointestinal and liver diseases. Animal models of necrotizing enterocolitis: pathophysiology, translational relevance, and challenges. Am. J. Physiol. Gastrointest. Liver Physiol. 306 (2014), G917–G928.
7. [7] Morrow, A.L., Lagomarcino, A.J., Schibler, K.R., Taft, D.H., Yu, Z., Wang, B., Altaye, M., Wagner, M., Gevers, D., Ward, D.V., Kennedy, M.A., Huttenhower, C., Newburg, D.S., Early microbial and metabolomic signatures predict later onset of necrotizing enterocolitis in preterm infants. Microbiome, 1, 2013, 13.
8. [8] Hansen, C.H., Yurkovetskiy, L.A., Chervonsky, A.V., Cutting edge: commensal microbiota has disparate effects on manifestations of polyglandular autoimmune inflammation. J. Immunol. 197 (2016), 701–705.
9. [9] Frank, D.N., St Amand, A.L., Feldman, R.A., Boedeker, E.C., Harpaz, N., Pace, N.R., Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. USA 104 (2007), 13780–13785.
10. [10] Yurkovetskiy, L.A., Pickard, J.M., Chervonsky, A.V., Microbiota and autoimmunity: exploring new avenues. Cell Host Microbe 17 (2015), 548–552.
11. [11] Dzutsev, A., Goldszmid, R.S., Viaud, S., Zitvogel, L., Trinchieri, G., The role of the microbiota in inflammation, carcinogenesis, and cancer therapy. Eur. J. Immunol. 45 (2015), 17–31.
12. [12] Sampson, T.R., Mazmanian, S.K., Control of brain development, function, and behavior by the microbiome. Cell Host Microbe 17 (2015), 565–576.
13. [13] Khan, M.T., Nieuwdorp, M., Backhed, F., Microbial modulation of insulin sensitivity. Cell Metab. 20 (2014), 753–760.
14. [14] Tang, W.H., Hazen, S.L., The contributory role of gut microbiota in cardiovascular disease. J. Clin. Investig. 124 (2014), 4204–4211.
15. [15] Torrazza, R.M., Ukhanova, M., Wang, X., Sharma, R., Hudak, M.L., Neu, J., Mai, V., Intestinal microbial ecology and environmental factors affecting necrotizing enterocolitis. PLoS One, 8, 2013, e83304.
16. [16] Hunter, C.J., Bean, J.F., Cronobacter: an emerging opportunistic pathogen associated with neonatal meningitis, sepsis and necrotizing enterocolitis. J. Perinatol. 33 (2013), 581–585.
17. [17] Wójkowska-Mach, J., Różańska, A., Borszewska-Kornacka, M., Domańska, J., Gadzinowski, J., Gulczyńska, E., Helwich, E., Kordek, A., Pawlik, D., Szczapa, J., Heczko, P.B., Necrotising enterocolitis in preterm infants: epidemiology and antibiotic consumption in the polish neonatology network neonatal intensive care units in 2009. PLoS One, 9, 2014, e92865.
18. [18] Chen, A.C., Chung, M.Y., Chang, J.H., Lin, H.C., Pathogenesis implication for necrotizing enterocolitis prevention in preterm very-low-birth-weight infants. J. Pediatr. Gastroenterol. Nutr. 58 (2014), 7–11.
19. [19] Ganguli, K., Meng, D., Rautava, S., Lu, L., Walker, W.A., Nanthakumar, N., Probiotics prevent necrotizing enterocolitis by modulating enterocyte genes that regulate innate immune-mediated inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 304 (2013), G132–G141.
20. [20] Liu, Y., Fatheree, N.Y., Mangalat, N., Rhoads, J.M., Lactobacillus reuteri strains reduce incidence and severity of experimental necrotizing enterocolitis via modulation of TLR4 and NF-κB signaling in the intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 302 (2012), G608–G617.
21. [21] Good, M., Siggers, R.H., Sodhi, C.P., Afrazi, A., Alkhudari, F., Egan, C.E., Neal, M.D., Yazji, I., Jia, H., Lin, J., Branca, M.F., Ma, C., Prindle, T., Grant, Z., Shah, S., Slagle, D. 2nd, Paredes, J., Ozolek, J., Gittes, G.K., Hackam, D.J., Amniotic fluid inhibits toll-like receptor 4 signaling in the fetal and neonatal intestinal epithelium. Proc. Natl. Acad. Sci. USA 109 (2012), 11330–11335.
22. [22] Yu, X., Radulescu, A., Zorko, N., Besner, G.E., Heparin-binding EGF-like growth factor increases intestinal microvascular blood flow in necrotizing enterocolitis. Gastroenterology 137 (2009), 221–230.
23. [23] Good, M., Siggers, R.H., Sodhi, C.P., Afrazi, A., Alkhudari, F., Egan, C.E., Neal, M.D., Yazji, I., Jia, H., Lin, J., Branca, M.F., Ma, C., Prindle, T., Grant, Z., Shah, S., Slagle, D. 2nd, Paredes, J., Ozolek, J., Gittes, G.K., Hackam, D.J., Amniotic fluid inhibits Toll-like receptor 4 signaling in the fetal and neonatal intestinal epithelium. Proc. Natl. Acad. Sci. USA 109 (2012), 11330–11335.
24. [24] Chen, Chun-An, Wang, Tse-Yao, Varadharaj, Saradhadevi, Reyes, Levy A., Hemann, Craig, Talukder, M.A. Hassan, Chen, Yeong-Renn, Druhan, Lawrence J., Zweier, Jay L., S-glutathionylation uncouples eNOS and regulates its cellular and vascular function. Nature 468 (2010), 1115–1118.
25. [25] Zhang, T., Cui, B., Li, P., He, Z., Long, C., Wei, L., Peng, Z., Ji, G., Zhang, F., Short-term surveillance of cytokines and C-reactive protein cannot predict efficacy of fecal microbiota transplantation for ulcerative colitis. PLoS One, 11, 2016, e0158227.
26. [26] Li, M., Liang, P., Li, Z., Wang, Y., Zhang, G., Gao, H., Wen, S., Tang, L., Fecal microbiota transplantation and bacterial consortium transplantation have comparable effects on the re-establishment of mucosal barrier function in mice with intestinal dysbiosis. Front Microbiol., 6, 2015, 692.
27. [27] Brower-Sinning, R., Zhong, D., Good, M., Firek, B., Baker, R., Sodhi, C.P., Hackam, D.J., Morowitz, M.J., Mucosa-associated bacterial diversity in necrotizing enterocolitis. PLoS One, 9, 2014, e105046.
28. [28] Konturek, P.C., Haziri, D., Brzozowski, T., Hess, T., Heyman, S., Kwiecien, S., Konturek, S.J., Koziel, J., Emerging role of fecal microbiota therapy in the treatment of gastrointestinal and extra-gastrointestinal diseases. J. Physiol. Pharmacol. 66 (2015), 483–491.
29. [29] Ganguli, K., Collado, M.C., Rautava, J., Lu, L., Satokari, R., von Ossowski, I., Reunanen, J., de Vos, W.M., Palva, A., Isolauri, E., Salminen, S., Walker, W.A., Rautava, S., Lactobacillus rhamnosus GG and its SpaC pilus adhesin modulate inflammatory responsiveness and TLR-related gene expression in the fetal human gut. Pediatr. Res. 77 (2015), 528–535.
30. [30] Repa, A., Thanhaeuser, M., Endress, D., Weber, M., Kreissl, A., Binder, C., Berger, A., Haiden, N., Probiotics (Lactobacillus acidophilus and Bifidobacterium infantis) prevent NEC in VLBW infants fed breast milk but not formula [corrected]. Pediatr. Res. 77 (2015), 381–388.
31. [31] Zweier, J.L., Chen, C.A., Druhan, L.J., S-glutathionylation reshapes our understanding of endothelial nitric oxide synthase uncoupling and nitric oxide/reactive oxygen species-mediated signaling. Antioxid. Redox Signal. 14 (2011), 1769–1775.
32. [32] Chen, C.A., Lin, C.H., Druhan, L.J., Wang, T.Y., Chen, Y.R., Zweier, J.L., Superoxide induces endothelial nitric-oxide synthase protein thiyl radical formation, a novel mechanism regulating eNOS function and coupling. J. Biol. Chem. 286 (2011), 29098–29107.
33. [33] Tanner, S.M., Berryhill, T.F., Ellenburg, J.L., Jilling, T., Cleveland, D.S., Lorenz, R.G., Martin, C.A., Pathogenesis of necrotizing enterocolitis: modeling the innate immune response. Am. J. Pathol. 185 (2015), 4–16.
34. [34] Yazji, Ibrahim, Sodhi, Chhinder P., Lee, Elizabeth K., Good, Misty, Egan, Charlotte E., Afrazi, Amin, Neal, Matthew D., Jia, Hongpeng, Lin, Joyce, Ma, Congrong, Branca, Maria F., Prindle, Thomas, Richardson, Ward M., Ozolek, John, Billiar, Timothy R., Binion, David G., Gladwin, Mark T., Hackam, David J., Endothelial TLR4 activation impairs intestinal microcirculatory perfusion in necrotizing enterocolitis via eNOS–NO–nitrite signaling. Proc. Natl. Acad. Sci. USA 110:23 (2013), 9451–9456.
35. [35] Patel, R.M., Denning, P.W., Intestinal microbiota and its relationship with necrotizing enterocolitis. Pediatr. Res. 78:3 (2015), 232–238.
36. [36] Leaphart, C.L., Cavallo, J., Gribar, S.C., Cetin, S., Li, J., Branca, M.F., Dubowski, T.D., Sodhi, C.P., Hackam, D.J., A critical role for TLR4 in the pathogenesis of necrotizing enterocolitis by modulating intestinal injury and repair. J. Immunol. 179:7 (2007), 4808–4820.
37. [37] Ajamieh, H., Farrell, G., Wong, H.J., Yu, J., Chu, E., Chen, J., Teoh, N., Atorvastatin protects obese mice against hepatic ischemia-reperfusion injury by toll-like receptor-4 suppression and endothelial nitric oxide synthase activation. J. Gastroenterol. Hepatol. 27:8 (2012), 1353–1361.