Generic placeholder image

Current Pediatric Reviews

Editor-in-Chief

ISSN (Print): 1573-3963
ISSN (Online): 1875-6336

Review Article

The Impact of MicroRNAs in Neonatal Necrotizing Enterocolitis and other Inflammatory Conditions of Intestine: A Review

Author(s): Keyur Donda, Tanima Bose, Christof Dame and Akhil Maheshwari*

Volume 19, Issue 1, 2023

Published on: 15 June, 2022

Page: [5 - 14] Pages: 10

DOI: 10.2174/1573396318666220117102119

Price: $65

Abstract

The understanding of necrotizing enterocolitis (NEC) etiopathogenesis is incomplete, contributing to the lack of early biomarkers and therapeutic options. Micro RNAs (miRNAs) are a class of RNAs that can alter gene expression and modulate various physiological and pathological processes. Several studies have been performed to evaluate the role of miRNA in the pathogenesis of NEC. In this article, we review the information on miRNAs that have been specifically identified in NEC or have been noted in other inflammatory bowel disorders that share some of the histopathological abnormalities seen frequently in NEC. This review highlights miRNAs that could be useful as early biomarkers of NEC and suggests possible approaches for future translational studies focused on these analytes. It is a novel field with potential for immense translational and clinical relevance in preventing, detecting, or treating NEC in very premature infants.

Impact

• Current information categorizes necrotizing enterocolitis (NEC) as a multifactorial disease, but microRNAs (miRNAs) may influence the risk of occurrence of NEC.

• MiRNAs may alter the severity of the intestinal injury and the clinical outcome of NEC.

• The literature on intestinal diseases of adults suggests additional miRNAs that have not been studied in NEC yet but share some features and deserve further exploration in human NEC, especially if affecting gut dysbiosis, intestinal perfusion, and coagulation disorders.

Keywords: Micro RNA, necrotizing enterocolitis, neonates, genetic predisposition, spontaneous intestinal perforation, intestinal inflammation.

[1]
Neu J. Necrotizing enterocolitis: A multi-omic approach and the role of the microbiome. Dig Dis Sci 2020; 65(3): 789-96.
[http://dx.doi.org/10.1007/s10620-020-06104-w] [PMID: 32008132]
[2]
MohanKumar K, Namachivayam K, Cheng F, et al. Trinitrobenzene sulfonic acid-induced intestinal injury in neonatal mice activates transcriptional networks similar to those seen in human necrotizing enterocolitis. Pediatr Res 2017; 81(1-1): 99-112.
[http://dx.doi.org/10.1038/pr.2016.189] [PMID: 27656771]
[3]
Denning PW, Maheshwari A. Necrotizing enterocolitis: hope on the horizon. Clin Perinatol 2013; 40(1): xvii-ix.
[http://dx.doi.org/10.1016/j.clp.2013.01.001] [PMID: 23415273]
[4]
Jonas S, Izaurralde E. Towards a molecular understanding of microRNA-mediated gene silencing. Nat Rev Genet 2015; 16(7): 421-33.
[http://dx.doi.org/10.1038/nrg3965] [PMID: 26077373]
[5]
Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993; 75(5): 843-54.
[http://dx.doi.org/10.1016/0092-8674(93)90529-Y] [PMID: 8252621]
[6]
Moran Y, Agron M, Praher D, Technau U. The evolutionary origin of plant and animal microRNAs. Nat Ecol Evol 2017; 1(3): 27.
[http://dx.doi.org/10.1038/s41559-016-0027] [PMID: 28529980]
[7]
Ozsolak F, Poling LL, Wang Z, et al. Chromatin structure analyses identify miRNA promoters. Genes Dev 2008; 22(22): 3172-83.
[http://dx.doi.org/10.1101/gad.1706508] [PMID: 19056895]
[8]
Yi R, Qin Y, Macara IG, Cullen BR. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev 2003; 17(24): 3011-6.
[http://dx.doi.org/10.1101/gad.1158803] [PMID: 14681208]
[9]
Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 2005; 123(4): 631-40.
[http://dx.doi.org/10.1016/j.cell.2005.10.022] [PMID: 16271387]
[10]
Denli AM, Tops BB, Plasterk RH, Ketting RF, Hannon GJ. Processing of primary microRNAs by the Microprocessor complex. Nature 2004; 432(7014): 231-5.
[http://dx.doi.org/10.1038/nature03049] [PMID: 15531879]
[11]
Steinkraus BR, Toegel M, Fulga TA. Tiny giants of gene regulation: experimental strategies for microRNA functional studies. Wiley Interdiscip Rev Dev Biol 2016; 5(3): 311-62.
[http://dx.doi.org/10.1002/wdev.223] [PMID: 26950183]
[12]
Peterson SM, Thompson JA, Ufkin ML, Sathyanarayana P, Liaw L, Congdon CB. Common features of microRNA target prediction tools. Front Genet 2014; 5: 23.
[http://dx.doi.org/10.3389/fgene.2014.00023] [PMID: 24600468]
[13]
Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. Prediction of mammalian microRNA targets. Cell 2003; 115(7): 787-98.
[http://dx.doi.org/10.1016/S0092-8674(03)01018-3] [PMID: 14697198]
[14]
Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009; 19(1): 92-105.
[http://dx.doi.org/10.1101/gr.082701.108] [PMID: 18955434]
[15]
Kondkar AA, Abu-Amero KK. Utility of circulating microRNAs as clinical biomarkers for cardiovascular diseases. BioMed Res Int 2015; 2015: 821823.
[http://dx.doi.org/10.1155/2015/821823] [PMID: 25710029]
[16]
Sanders AP, Gennings C, Svensson K, et al. Bacterial and cytokine mixtures predict the length of gestation and are associated with miRNA expression in the cervix. Epigenomics 2017; 9(1): 33-45.
[http://dx.doi.org/10.2217/epi-2016-0095] [PMID: 27936911]
[17]
Elovitz MA, Anton L, Bastek J, Brown AG. Can microRNA profiling in maternal blood identify women at risk for preterm birth? Am J Obstet Gynecol 2015; 212(6): 782.e1-5.
[http://dx.doi.org/10.1016/j.ajog.2015.01.023] [PMID: 25617732]
[18]
Haneklaus M, Gerlic M, O’Neill LA, Masters SL. miR-223: infection, inflammation and cancer. J Intern Med 2013; 274(3): 215-26.
[http://dx.doi.org/10.1111/joim.12099] [PMID: 23772809]
[19]
Garg M, Potter JA, Abrahams VM. Identification of microRNAs that regulate tlr2-mediated trophoblast apoptosis and inhibition of IL-6 mRNA. 2013; 8(10): e77249.
[http://dx.doi.org/10.1371/journal.pone.0077249]
[20]
Mayor-Lynn K, Toloubeydokhti T, Cruz AC, Chegini N. Expression profile of microRNAs and mRNAs in human placentas from pregnancies complicated by preeclampsia and preterm labor. Reprod Sci 2011; 18(1): 46-56.
[http://dx.doi.org/10.1177/1933719110374115] [PMID: 21079238]
[21]
Renthal NE, Chen CC, Williams KC, Gerard RD, Prange-Kiel J, Mendelson CR. miR-200 family and targets, ZEB1 and ZEB2, modulate uterine quiescence and contractility during pregnancy and labor. Proc Natl Acad Sci USA 2010; 107(48): 20828-33.
[http://dx.doi.org/10.1073/pnas.1008301107] [PMID: 21079000]
[22]
MohanKumar K, Namachivayam K, Song T, et al. A murine neonatal model of necrotizing enterocolitis caused by anemia and red blood cell transfusions. Nat Commun 2019; 10(1): 3494.
[http://dx.doi.org/10.1038/s41467-019-11199-5] [PMID: 31375667]
[23]
De Plaen IG, Liu SX, Tian R, et al. Inhibition of nuclear factor-kappaB ameliorates bowel injury and prolongs survival in a neonatal rat model of necrotizing enterocolitis. Pediatr Res 2007; 61(6): 716-21.
[http://dx.doi.org/10.1203/pdr.0b013e3180534219] [PMID: 17426653]
[24]
Jilling T, Lu J, Jackson M, Caplan MS. Intestinal epithelial apoptosis initiates gross bowel necrosis in an experimental rat model of neonatal necrotizing enterocolitis. Pediatr Res 2004; 55(4): 622-9.
[http://dx.doi.org/10.1203/01.PDR.0000113463.70435.74] [PMID: 14764921]
[25]
Jilling T, Simon D, Lu J, et al. The roles of bacteria and TLR4 in rat and murine models of necrotizing enterocolitis. J Immunol 2006; 177(5): 3273-82.
[http://dx.doi.org/10.4049/jimmunol.177.5.3273] [PMID: 16920968]
[26]
MohanKumar K, Namachivayam K, Chapalamadugu KC, et al. Smad7 interrupts TGF-β signaling in intestinal macrophages and promotes inflammatory activation of these cells during necrotizing enterocolitis. Pediatr Res 2016; 79(6): 951-61.
[http://dx.doi.org/10.1038/pr.2016.18] [PMID: 26859364]
[27]
Namachivayam K, Blanco CL, MohanKumar K, et al. Smad7 inhibits autocrine expression of TGF-β2 in intestinal epithelial cells in baboon necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 2013; 304(2): G167-80.
[http://dx.doi.org/10.1152/ajpgi.00141.2012] [PMID: 23154975]
[28]
Frank D, Vince JE. Pyroptosis versus necroptosis: similarities, differences, and crosstalk. Cell Death Differ 2019; 26(1): 99-114.
[http://dx.doi.org/10.1038/s41418-018-0212-6] [PMID: 30341423]
[29]
Dhuriya YK, Sharma D. Necroptosis: a regulated inflammatory mode of cell death. J Neuroinflammation 2018; 15(1): 199.
[http://dx.doi.org/10.1186/s12974-018-1235-0] [PMID: 29980212]
[30]
Werts AD, Fulton WB, Ladd MR, et al. A novel role for necroptosis in the pathogenesis of necrotizing enterocolitis. Cell Mol Gastroenterol Hepatol 2020; 9(3): 403-23.
[http://dx.doi.org/10.1016/j.jcmgh.2019.11.002] [PMID: 31756560]
[31]
Li X, Wang Y, Wang Y, He X. MiR-141-3p ameliorates RIPK1-mediated necroptosis of intestinal epithelial cells in necrotizing enterocolitis. Aging (Albany NY) 2020; 12(18): 18073-83.
[http://dx.doi.org/10.18632/aging.103608] [PMID: 32702669]
[32]
Baek D, Villén J, Shin C, Camargo FD, Gygi SP, Bartel DP. The impact of microRNAs on protein output. Nature 2008; 455(7209): 64-71.
[http://dx.doi.org/10.1038/nature07242] [PMID: 18668037]
[33]
Chen H, Zeng L, Zheng W, Li X, Lin B. Increased expression of microRNA-141-3p improves necrotizing enterocolitis of neonates through targeting MNX1. Front Pediatr 2020; 8: 385.
[http://dx.doi.org/10.3389/fped.2020.00385] [PMID: 32850524]
[34]
Wu YZ, Chan KYY, Leung KT, et al. Dysregulation of miR-431 and target gene FOXA1 in intestinal tissues of infants with necrotizing enterocolitis. FASEB J 2019; 33(4): 5143-52.
[http://dx.doi.org/10.1096/fj.201801470R] [PMID: 30624964]
[35]
Ng PC, Chan KYY, Yuen TP, et al. Plasma miR-1290 Is a novel and specific biomarker for early diagnosis of necrotizing enterocolitis-biomarker discovery with prospective cohort evaluation. J Pediatr 2019; 205: 83-90.e10.
[http://dx.doi.org/10.1016/j.jpeds.2018.09.031] [PMID: 30529132]
[36]
Imaoka H, Toiyama Y, Fujikawa H, et al. Circulating microRNA-1290 as a novel diagnostic and prognostic biomarker in human colorectal cancer. Ann Oncol 2016; 27(10): 1879-86.
[http://dx.doi.org/10.1093/annonc/mdw279] [PMID: 27502702]
[37]
van der Sluis M, Vincent A, Bouma J, et al. Forkhead box transcription factors Foxa1 and Foxa2 are important regulators of Muc2 mucin expression in intestinal epithelial cells. Biochem Biophys Res Commun 2008; 369(4): 1108-13.
[http://dx.doi.org/10.1016/j.bbrc.2008.02.158] [PMID: 18336786]
[38]
Maheshwari A, Kelly DR, Nicola T, et al. TGF-β2 suppresses macrophage cytokine production and mucosal inflammatory responses in the developing intestine. Gastroenterology 2011; 140(1): 242-53.
[http://dx.doi.org/10.1053/j.gastro.2010.09.043] [PMID: 20875417]
[39]
Mara MA, Good M, Weitkamp JH. Innate and adaptive immunity in necrotizing enterocolitis. Semin Fetal Neonatal Med 2018; 23(6): 394-9.
[http://dx.doi.org/10.1016/j.siny.2018.08.002] [PMID: 30146477]
[40]
Yin Y, Qin Z, Xu X, et al. Inhibition of miR-124 improves neonatal necrotizing enterocolitis via an MYPT1 and TLR9 signal regulation mechanism. J Cell Physiol 2019; 234(7): 10218-24.
[http://dx.doi.org/10.1002/jcp.27691] [PMID: 30480807]
[41]
Xu Y, Liu Y, Xie H, et al. Profile analysis reveals endogenous RNAs regulate necrotizing enterocolitis progression. Biomed Pharmacother 2020; 125: 109975.
[http://dx.doi.org/10.1016/j.biopha.2020.109975] [PMID: 32036223]
[42]
Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell 2010; 140(6): 805-20.
[http://dx.doi.org/10.1016/j.cell.2010.01.022] [PMID: 20303872]
[43]
Chuang AY, Chuang JC, Zhai Z, Wu F, Kwon JH. NOD2 expression is regulated by microRNAs in colonic epithelial HCT116 cells. Inflamm Bowel Dis 2014; 20(1): 126-35.
[http://dx.doi.org/10.1097/01.MIB.0000436954.70596.9b] [PMID: 24297055]
[44]
Wu W, He C, Liu C, et al. miR-10a inhibits dendritic cell activation and Th1/Th17 cell immune responses in IBD. Gut 2015; 64(11): 1755-64.
[http://dx.doi.org/10.1136/gutjnl-2014-307980] [PMID: 25281418]
[45]
Xu X, Ma C, Liu C, Duan Z, Zhang L. Knockdown of long noncoding RNA XIST alleviates oxidative low-density lipoprotein-mediated endothelial cells injury through modulation of miR-320/NOD2 axis. Biochem Biophys Res Commun 2018; 503(2): 586-92.
[http://dx.doi.org/10.1016/j.bbrc.2018.06.042] [PMID: 29902461]
[46]
Ghorpade DS, et al. NOD2-nitric oxide-responsive microRNA-146a activates sonic hedgehog signaling to orchestrate inflammatory responses in murine model of inflammatory bowel disease. Immunology 2013; 288(46): 33037-48.
[http://dx.doi.org/10.1074/jbc.M113.492496]
[47]
Chen Y, Wang C, Liu Y, et al. miR-122 targets NOD2 to decrease intestinal epithelial cell injury in Crohn’s disease. Biochem Biophys Res Commun 2013; 438(1): 133-9.
[http://dx.doi.org/10.1016/j.bbrc.2013.07.040] [PMID: 23872065]
[48]
Brain O, Owens BM, Pichulik T, et al. The intracellular sensor NOD2 induces microRNA-29 expression in human dendritic cells to limit IL-23 release. Immunity 2013; 39(3): 521-36.
[http://dx.doi.org/10.1016/j.immuni.2013.08.035] [PMID: 24054330]
[49]
Frakking FN, Brouwer N, Zweers D, et al. High prevalence of mannose-binding lectin (MBL) deficiency in premature neonates. Clin Exp Immunol 2006; 145(1): 5-12.
[http://dx.doi.org/10.1111/j.1365-2249.2006.03093.x] [PMID: 16792667]
[50]
de Benedetti F, Auriti C, D’Urbano LE, et al. Low serum levels of mannose binding lectin are a risk factor for neonatal sepsis. Pediatr Res 2007; 61(3): 325-8.
[http://dx.doi.org/10.1203/pdr.0b013e318030d12f] [PMID: 17314691]
[51]
Schlapbach LJ, Latzin P, Regamey N, et al. Mannose-binding lectin cord blood levels and respiratory symptoms during infancy: A prospective birth cohort study. Pediatr Allergy Immunol 2009; 20(3): 219-26.
[http://dx.doi.org/10.1111/j.1399-3038.2008.00782.x] [PMID: 18700861]
[52]
Takahashi K. Mannose-binding lectin and the balance between immune protection and complication. Expert Rev Anti Infect Ther 2011; 9(12): 1179-90.
[http://dx.doi.org/10.1586/eri.11.136] [PMID: 22114968]
[53]
Prencipe G, Azzari C, Moriondo M, et al. Association between mannose-binding lectin gene polymorphisms and necrotizing enterocolitis in preterm infants. J Pediatr Gastroenterol Nutr 2012; 55(2): 160-5.
[http://dx.doi.org/10.1097/MPG.0b013e31824e5f7a] [PMID: 22331020]
[54]
Xu C-Y, Dong JF, Chen ZQ, Ding GS, Fu ZR. MiR-942-3p promotes the proliferation and invasion of hepatocellular carcinoma cells by targeting MBL2. Cancer Contr 2019; 26(1): 1073274819846593.
[http://dx.doi.org/10.1177/1073274819846593] [PMID: 31046434]
[55]
Bowker RM, Yan X, De Plaen IG. Intestinal microcirculation and necrotizing enterocolitis: The vascular endothelial growth factor system. Semin Fetal Neonatal Med 2018; 23(6): 411-5.
[http://dx.doi.org/10.1016/j.siny.2018.08.008] [PMID: 30213591]
[56]
Crafts TD, Jensen AR, Blocher-Smith EC, Markel TA. Vascular endothelial growth factor: therapeutic possibilities and challenges for the treatment of ischemia. Cytokine 2015; 71(2): 385-93.
[http://dx.doi.org/10.1016/j.cyto.2014.08.005] [PMID: 25240960]
[57]
Sabnis A, Carrasco R, Liu SX, et al. Intestinal vascular endothelial growth factor is decreased in necrotizing enterocolitis. Neonatology 2015; 107(3): 191-8.
[http://dx.doi.org/10.1159/000368879] [PMID: 25659996]
[58]
Liu H, Wang YB. Systematic large-scale meta-analysis identifies miRNA-429/200a/b and miRNA-141/200c clusters as biomarkers for necrotizing enterocolitis in newborn. Biosci Rep 2019; 39(9): BSR20191503.
[http://dx.doi.org/10.1042/BSR20191503] [PMID: 31383782]
[59]
Zhao J, Yin L, He L. The MicroRNA landscapes profiling reveals potential signatures of necrotizing enterocolitis in infants. J Comput Biol 2020; 27(1): 30-9.
[http://dx.doi.org/10.1089/cmb.2019.0183] [PMID: 31390270]
[60]
Giuliani S, Tan YW, Zheng D, et al. Coagulation gene expression profiling in infants with necrotizing enterocolitis. J Pediatr Gastroenterol Nutr 2016; 63(6): e169-75.
[http://dx.doi.org/10.1097/MPG.0000000000001215] [PMID: 27050058]
[61]
Namachivayam K, MohanKumar K, Shores DR, et al. Targeted inhibition of thrombin attenuates murine neonatal necrotizing enterocolitis. Proc Natl Acad Sci USA 2020; 117(20): 10958-69.
[http://dx.doi.org/10.1073/pnas.1912357117] [PMID: 32366656]
[62]
Cui Y-L, Wang B, Gao HM, et al. Interleukin-18 and miR-130a in severe sepsis patients with thrombocytopenia. Patient Prefer Adherence 2016; 10(10): 313-9.
[http://dx.doi.org/10.2147/PPA.S95588] [PMID: 27042022]
[63]
Schuijers J, Clevers H. Adult mammalian stem cells: the role of Wnt, Lgr5 and R-spondins. EMBO J 2012; 31(12): 2685-96.
[http://dx.doi.org/10.1038/emboj.2012.149] [PMID: 22617424]
[64]
Yu RQ, Wang M, Jiang SY, Zhang YH, Zhou XY, Zhou Q. Small RNA sequencing reveals differentially expressed miRNAs in necrotizing enterocolitis in rats. BioMed Res Int 2020; 2020: 5150869.
[http://dx.doi.org/10.1155/2020/5150869] [PMID: 32934961]
[65]
Goodrich JK, Davenport ER, Beaumont M, et al. Genetic determinants of the gut microbiome in UK twins. Cell Host Microbe 2016; 19(5): 731-43.
[http://dx.doi.org/10.1016/j.chom.2016.04.017] [PMID: 27173935]
[66]
Goodrich JK, Waters JL, Poole AC, et al. Human genetics shape the gut microbiome. Cell 2014; 159(4): 789-99.
[http://dx.doi.org/10.1016/j.cell.2014.09.053] [PMID: 25417156]
[67]
Turpin W, Espin-Garcia O, Xu W, et al. GEM project research consortium. Association of host genome with intestinal microbial composition in a large healthy cohort. Nat Genet 2016; 48(11): 1413-7.
[http://dx.doi.org/10.1038/ng.3693] [PMID: 27694960]
[68]
Liu S, Weiner HL. Control of the gut microbiome by fecal microRNA. Microb Cell 2016; 3(4): 176-7.
[http://dx.doi.org/10.15698/mic2016.04.492] [PMID: 28357349]
[69]
Link A, Becker V, Goel A, Wex T, Malfertheiner P. Feasibility of fecal microRNAs as novel biomarkers for pancreatic cancer. PLoS One 2012; 7(8): e42933.
[http://dx.doi.org/10.1371/journal.pone.0042933] [PMID: 22905187]
[70]
Ahmed FE, Jeffries CD, Vos PW, et al. Diagnostic microRNA markers for screening sporadic human colon cancer and active ulcerative colitis in stool and tissue. Cancer Genomics Proteomics 2009; 6(5): 281-95.
[PMID: 19996134]
[71]
Liu S, da Cunha AP, Rezende RM, et al. The host shapes the gut microbiota via fecal microRNA. Cell Host Microbe 2016; 19(1): 32-43.
[http://dx.doi.org/10.1016/j.chom.2015.12.005] [PMID: 26764595]
[72]
Mohan M, Chow CT, Ryan CN, et al. Dietary gluten-induced gut dysbiosis is accompanied by selective upregulation of micrornas with intestinal tight junction and bacteria-binding motifs in rhesus macaque model of celiac disease. Nutrients 2016; 8(11): 684.
[http://dx.doi.org/10.3390/nu8110684] [PMID: 27801835]
[73]
Rojas-Feria M, Romero-García T, Fernández Caballero-Rico JÁ, et al. Modulation of faecal metagenome in Crohn’s disease: Role of microRNAs as biomarkers. World J Gastroenterol 2018; 24(46): 5223-33.
[http://dx.doi.org/10.3748/wjg.v24.i46.5223] [PMID: 30581271]
[74]
Ambrozkiewicz F, Karczmarski J, Kulecka M, et al. In search for interplay between stool microRNAs, microbiota and short chain fatty acids in Crohn’s disease - a preliminary study. BMC Gastroenterol 2020; 20(1): 307.
[http://dx.doi.org/10.1186/s12876-020-01444-3] [PMID: 32958038]
[75]
Carrillo-Lozano E, Sebastián-Valles F, Knott-Torcal C. Circulating microRNAs in breast milk and their potential impact on the infant. Nutrients 2020; 12(10): 3066.
[http://dx.doi.org/10.3390/nu12103066] [PMID: 33049923]
[76]
Reif S, Elbaum-Shiff Y, Koroukhov N, Shilo I, Musseri M, Golan-Gerstl R. Cow and human milk-derived exosomes ameliorate colitis in dss murine model. Nutrients 2020; 12(9): 2589.
[http://dx.doi.org/10.3390/nu12092589] [PMID: 32858892]
[77]
Benmoussa A, Diallo I, Salem M, et al. Concentrates of two subsets of extracellular vesicles from cow’s milk modulate symptoms and inflammation in experimental colitis. Sci Rep 2019; 9(1): 14661.
[http://dx.doi.org/10.1038/s41598-019-51092-1] [PMID: 31601878]
[78]
Stremmel W, Weiskirchen R, Melnik BC. Milk exosomes prevent intestinal inflammation in a genetic mouse model of ulcerative colitis: a pilot experiment. Inflamm Intest Dis 2020; 5(3): 117-23.
[http://dx.doi.org/10.1159/000507626] [PMID: 32999884]
[79]
Pisano C, Galley J, Elbahrawy M, et al. Human breast milk-derived extracellular vesicles in the protection against experimental necrotizing enterocolitis. J Pediatr Surg 2020; 55(1): 54-8.
[http://dx.doi.org/10.1016/j.jpedsurg.2019.09.052] [PMID: 31685268]
[80]
Li B, Hock A, Wu RY, et al. Bovine milk-derived exosomes enhance goblet cell activity and prevent the development of experimental necrotizing enterocolitis. PLoS One 2019; 14(1): e0211431.
[http://dx.doi.org/10.1371/journal.pone.0211431] [PMID: 30699187]
[81]
Been JV, Lievense S, Zimmermann LJ, Kramer BW, Wolfs TG. Chorioamnionitis as a risk factor for necrotizing enterocolitis: a systematic review and meta-analysis. J Pediatr 2013; 162(2): 236-42.e2.
[http://dx.doi.org/10.1016/j.jpeds.2012.07.012] [PMID: 22920508]
[82]
Montenegro D, Romero R, Pineles BL, et al. Differential expression of microRNAs with progression of gestation and inflammation in the human chorioamniotic membranes. Am J Obstet Gynecol 2007; 197(3): 289.e1-6.
[http://dx.doi.org/10.1016/j.ajog.2007.06.027] [PMID: 17826424]
[83]
Son G-H, Kim Y, Lee JJ, et al. MicroRNA-548 regulates high mobility group box 1 expression in patients with preterm birth and chorioamnionitis. Sci Rep 2019; 9(1): 19746.
[http://dx.doi.org/10.1038/s41598-019-56327-9] [PMID: 31875024]
[84]
Lee J, Kim CJ, Kim JS, Lee DC, Ahn S, Yoon BH. Increased miR-223 expression in foetal organs is a signature of acute chorioamnionitis with systemic consequences. J Cell Mol Med 2018; 22(2): 1179-89.
[PMID: 29083107]
[85]
Pang Y, Du X, Xu X, Wang M, Li Z. Impairment of regulatory T cells in patients with neonatal necrotizing enterocolitis. Int Immunopharmacol 2018; 63: 19-25.
[http://dx.doi.org/10.1016/j.intimp.2018.07.029] [PMID: 30059947]
[86]
Ma F, Li S, Gao X, et al. Interleukin-6-mediated CCR9+ interleukin-17-producing regulatory T cells polarization increases the severity of necrotizing enterocolitis. EBioMedicine 2019; 44: 71-85.
[http://dx.doi.org/10.1016/j.ebiom.2019.05.042] [PMID: 31129099]
[87]
Kalla R, Adams AT, Ventham NT. Whole blood profiling of T-cell-derived microRNA allows the development of prognostic models in inflammatory bowel disease. J Crohn’s Colitis 2020; 14(12): 1724-33.
[http://dx.doi.org/10.1093/ecco-jcc/jjaa134]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy