1,217
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Antenatal Ureaplasma infection induces ovine small intestinal goblet cell defects: a strong link with NEC pathology

, , , , , , , , , , , & ORCID Icon show all
Article: 2158016 | Received 31 May 2022, Accepted 05 Dec 2022, Published online: 28 Dec 2022

References

  • Sweeney EL, Dando SJ, Kallapur SG, Knox CL. The human ureaplasma species as causative agents of chorioamnionitis. Clin Microbiol Rev. 2017;30(1):388–403. doi:10.1128/CMR.00091-16.
  • Thomas W, Speer CP. Chorioamnionitis: important risk factor or innocent bystander for neonatal outcome? Neonatology. 2011;99(3):177–187. doi:10.1159/000320170.
  • Gantert M, Been JV, Gavilanes AW, Garnier Y, Zimmermann LJI, Kramer BW. Chorioamnionitis: a multiorgan disease of the fetus? J Perinatology: Offl J California Perinatal Ass. 2010;30Suppl(S1):S21–30. doi:10.1038/jp.2010.96.
  • Heymans C, de Lange IH, Hütten MC, Lenaerts K, de Ruijter NJE, Kessels LCGA, Rademakers G, Melotte V, Boesmans W, Saito M, et al. Chronic intra-uterine ureaplasma parvum infection induces injury of the enteric nervous system in ovine fetuses. Front Immunol. 2020;11:189. doi:10.3389/fimmu.2020.00189.
  • Wolfs TG, Kallapur SG, Knox CL, Thuijls G, Nitsos I, Polglase GR, Collins JJP, Kroon E, Spierings J, Shroyer NF, et al. Antenatal ureaplasma infection impairs development of the fetal ovine gut in an IL-1-dependent manner. Mucosal Immunol. 2013;6(3):547–556. doi:10.1038/mi.2012.97.
  • Gotsch F, Romero R, Kusanovic JP, MAZAKI-TOVI S, Pineles BL, Erez O, Espinoza J, Hassan SS. The fetal inflammatory response syndrome. Clin Obstet Gynecol. 2007;50(3):652–683. doi:10.1097/GRF.0b013e31811ebef6.
  • Sprong KE, Mabenge M, Wright CA, Govender S. Ureaplasma species and preterm birth: current perspectives. Crit Rev Microbiol. 2020;46(2):169–181. doi:10.1080/1040841X.2020.1736986.
  • Been JV, Lievense S, Zimmermann LJ, Kramer BW, Wolfs TGAM. Chorioamnionitis as a risk factor for necrotizing enterocolitis: a systematic review and meta-analysis. J Pediatr. 2013;162(2):236–242.e232. doi:10.1016/j.jpeds.2012.07.012.
  • Neu J, Walker WA. Necrotizing enterocolitis. N Engl J Med. 2011;364(3):255–264. doi:10.1056/NEJMra1005408.
  • 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.
  • McElroy SJ, Prince LS, Weitkamp JH, Reese J, Slaughter JC, Polk DB. Tumor necrosis factor receptor 1-dependent depletion of mucus in immature small intestine: a potential role in neonatal necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol. 2011;301(4):G656–666. doi:10.1152/ajpgi.00550.2010.
  • Schaart MW, de Bruijn AC, Bouwman DM, de Krijger RR, van Goudoever JB, Tibboel D, Renes IB. Epithelial functions of the residual bowel after surgery for necrotising enterocolitis in human infants. J Pediatr Gastroenterol Nutr. 2009;49(1):31–41. doi:10.1097/MPG.0b013e318186d341.
  • Elgin TG, Fricke EM, Gong H, Reese J, Mills DA, Kalantera KM, Underwood MA, McElroy SJ. Fetal exposure to maternal inflammation interrupts murine intestinal development and increases susceptibility to neonatal intestinal injury. Dis Model Mech. 2019, 21 October;12(10). doi:10.1242/dmm.040808.
  • van Gorp C, de Lange IH, Massy KRI, Kessels L, Jobe AH, Cleutjens JPM, Kemp MW, Saito M, Usada H, Newnham J, et al. Intestinal goblet cell loss during chorioamnionitis in fetal lambs: mechanistic insights and postnatal implications. Int J Mol Sci. 2021;22(4):1946. doi:10.3390/ijms22041946.
  • Coleman OI, Haller D. ER stress and the UPR in shaping intestinal tissue homeostasis and immunity. Front Immunol. 2019;10:2825. doi:10.3389/fimmu.2019.02825.
  • Afrazi A, Branca MF, Sodhi CP, Good M, Yamaguchi Y, Egan CE, Lu P, Jia H, Shaffiey S, Lin J, et al. Toll-like receptor 4-mediated endoplasmic reticulum stress in intestinal crypts induces necrotizing enterocolitis. J Biol Chem. 2014;289(14):9584–9599. doi:10.1074/jbc.M113.526517.
  • Lu P, Struijs MC, Mei J, Witte-Bouma J, Korteland-van Male AM, de Bruijn ACJM, van Goudoever JB, Renes IB. Endoplasmic reticulum stress, unfolded protein response and altered T cell differentiation in necrotizing enterocolitis. PloS one. 2013;8(10):e78491. doi:10.1371/journal.pone.0078491.
  • Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol. 2012;13(2):89–102. doi:10.1038/nrm3270.
  • Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol. 2007;8(7):519–529. doi:10.1038/nrm2199.
  • McGuckin MA, Eri RD, Das I, Lourie R, Florin TH. ER stress and the unfolded protein response in intestinal inflammation. Am J Physiol Gastrointest Liver Physiol. 2010;298(6):G820–832. doi:10.1152/ajpgi.00063.2010.
  • van Gorp C, de Lange IH, Spiller OB, Dewez F, Cillero Pastor B, Heeren RMA, Kessels L, Kloosterboer N, van Gemert WG, Beeton ML, et al. Protection of the ovine fetal gut against ureaplasma-induced chorioamnionitis: a potential role for plant sterols. Nutrients. 2019;11(5):968. doi:10.3390/nu11050968.
  • Hurd EA, Holmén JM, Hansson GC, Domino SE. Gastrointestinal mucins of Fut2-null mice lack terminal fucosylation without affecting colonization by Candida albicans. Glycobiology. 2005;15(10):1002–1007. doi:10.1093/glycob/cwi089.
  • Yamabayashi S. Periodic acid-Schiff-alcian blue: a method for the differential staining of glycoproteins. Histochem J. 1987;19(10–11):565–571. doi:10.1007/BF01687364.
  • Bankhead P, Loughrey MB, Fernández JA, Dombrowski Y, McArt DG, Dunne PD, McQuaid S, Gray RT, Murray LJ, Coleman HG, et al. QuPath: open source software for digital pathology image analysis. Sci Rep. 2017;7(1):16878. doi:10.1038/s41598-017-17204-5.
  • Gustafsson JK, Ermund A, Johansson MEV, Schütte A, Hansson GC, Sjövall H. An ex vivo method for studying mucus formation, properties, and thickness in human colonic biopsies and mouse small and large intestinal explants. Am J Physiol Gastrointest Liver Physiol. 2012;302(4):G430–G438. doi:10.1152/ajpgi.00405.2011.
  • Gussenhoven R, Westerlaken RJJ, Ophelders DRMG, Jobe AH, Kemp MW, Kallapur SG, Zimmermann LJ, Sangild PT, Pankratova S, Gressens P, et al. Chorioamnionitis, neuroinflammation, and injury: timing is key in the preterm ovine fetus. J Neuroinflammation. 2018;15(1):113. doi:10.1186/s12974-018-1149-x.
  • Hasnain SZ, Evans CM, Roy M, Gallagher AL, Kindrachuk KN, Barron L, Dickey BF, Wilson MS, Wynn TA, Grencis RK, et al. Muc5ac: a critical component mediating the rejection of enteric nematodes. J Exp Med. 2011;208(5):893–900. doi:10.1084/jem.20102057.
  • Skrzypek T, Szymańczyk S, Ferenc K, Kazimierczak W, Szczepaniak K, Zabielski R. The contribution of vacuolated foetal-type enterocytes in the process of maturation of the small intestine in piglets. Invited review. J Anim Feed Sci. 2018;27(3):187–201. doi:10.22358/jafs/94167/2018.
  • Waites KB, Katz B, Schelonka RL. Mycoplasmas and ureaplasmas as neonatal pathogens. Clin Microbiol Rev. 2005;18(4):757–789. doi:10.1128/CMR.18.4.757-789.2005.
  • Sweeney EL, Dando SJ, Kallapur SG, Knox CL. The human ureaplasma species as causative agents of chorioamnionitis. Clin Microbiol Rev. 2016;30:349–379.
  • Machado JR, Soave DF, da Silva MV, de Menezes LB, Etchebehere RM, Monteiro MLGDR, Dos Reis MA, Corrêa RRM, Celes MRN. Neonatal sepsis and inflammatory mediators. Mediators Inflamm. 2014;2014:269681. doi:10.1155/2014/269681.
  • Bose CL, Laughon MM, Allred EN, Michael O’Shea T, Van Marter LJ, Ehrenkranz RA, Fichorova RN, Leviton A. Systemic inflammation associated with mechanical ventilation among extremely preterm infants. Cytokine. 2013;61(1):315–322. doi:10.1016/j.cyto.2012.10.014.
  • Gustafsson JK, Ermund A, Ambort D, Johansson MEV, Nilsson HE, Thorell K, Hebert H, Sjövall H, Hansson GC. Bicarbonate and functional CFTR channel are required for proper mucin secretion and link cystic fibrosis with its mucus phenotype. J Exp Med. 2012;209(7):1263–1272. doi:10.1084/jem.20120562.
  • Nyström EEL, Birchenough GMH, van der Post S, Arike L, Gruber AD, Hansson GC, Johansson MEV. Calcium-activated chloride channel regulator 1 (CLCA1) Controls mucus expansion in colon by proteolytic activity. EBioMedicine. 2018;33:134–143. doi:10.1016/j.ebiom.2018.05.031.
  • Cornick S, Tawiah A, Chadee K. Roles and regulation of the mucus barrier in the gut. Tissue Barriers. 2015;3(1–2):e982426. doi:10.4161/21688370.2014.982426.
  • Triantafilou M, De Glanville B, Aboklaish AF, Spiller OB, Kotecha S, Triantafilou K. Synergic activation of toll-like receptor (TLR) 2/6 and 9 in response to Ureaplasma parvum & urealyticum in human amniotic epithelial cells. PloS one. 2013;8(4):e61199. doi:10.1371/journal.pone.0061199.
  • Birchenough GM, Nyström EE, Johansson ME, Hansson GC. A sentinel goblet cell guards the colonic crypt by triggering Nlrp6-dependent Muc2 secretion. Sci. 2016;352(6293):1535–1542. doi:10.1126/science.aaf7419.
  • Kallapur SG, Kramer BW, Jobe AH. Ureaplasma and BPD. Semin Perinatol. 2013;37(2):94–101. doi:10.1053/j.semperi.2013.01.005.
  • Cao SS, Kaufman RJ. Endoplasmic reticulum stress and oxidative stress in cell fate decision and human disease. Antioxid Redox Signal. 2014;21(3):396–413. doi:10.1089/ars.2014.5851.
  • Zhang M, Wu C. The relationship between intestinal goblet cells and the immune response. Biosci Rep. 2020;40(10). doi:10.1042/BSR20201471.
  • Yamoto M, Alganabi M, Chusilp S, Lee D, Yazaki Y, Lee C, Li B, Pierro A. Lysosomal overloading and necrotizing enterocolitis. Pediatr Surg Int. 2020;36(10):1157–1165. doi:10.1007/s00383-020-04724-x.
  • de Lange IH, van Gorp C, Eeftinck Schattenkerk LD, van Gemert WG, Derikx JPM, Wolfs TGAM. Enteral feeding interventions in the prevention of necrotizing enterocolitis: a systematic review of experimental and clinical studies. Nutrients. 2021;13(5):1726. doi:10.3390/nu13051726.