Intrauterine growth restriction alters mouse intestinal architecture during development

PLoS ONE

Volumn 11, Issue 1, 2016, Pages

  Fung, Camille M ^a   White, Jessica R ^b   Brown, Ashley S ^a   Gong, Huiyu ^b   Weitkamp, Jörn Hendrik ^c   Frey, Mark R ^d   McElroy, Steven J ^b  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c VANDERBILT UNIVERSITY   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BODY WEIGHT; CELL LINEAGE; CELL MATURATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; FETUS; GOBLET CELL; HOMEOSTASIS; ILEAL LENGTH; ILEAL WEIGHT; INNATE IMMUNITY; INTESTINAL DEVELOPMENT; INTESTINAL STRUCTURE; INTESTINE; INTRAUTERINE GROWTH RETARDATION; MATERNAL HYPERTENSION; MOUSE; NONHUMAN; ORGANOGENESIS; PANETH CELL; STOMACH EPITHELIUM; WEIGHT, MASS AND SIZE; ANIMAL; BIRTH WEIGHT; C57BL MOUSE; GENE EXPRESSION; GROWTH, DEVELOPMENT AND AGING; HUMAN; ILEUM; NEWBORN; ORGAN SIZE; PATHOLOGY; PHYSIOLOGY; PREGNANCY;

ANIMALS; APOPTOSIS; BIRTH WEIGHT; CELL PROLIFERATION; FEMALE; FETAL GROWTH RETARDATION; GENE EXPRESSION; GOBLET CELLS; HUMANS; ILEUM; INFANT, NEWBORN; MICE, INBRED C57BL; ORGAN SIZE; PANETH CELLS; PREGNANCY;

EID: 84954341960     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0146542     Document Type: Article

References (37)

1. Regev RH, Reichman B. Prematurity and intrauterine growth retardation-double jeopardy? Clinics in perinatology. 2004; 31(3):453-73. doi: 10.1016/j.clp.2004.04.017 PMID: 15325532.
2. Bozzetti V, Tagliabue PE, Visser GH, van Bel F, Gazzolo D. Feeding issues in IUGR preterm infants. Early human development. 2013; 89 Suppl 2:S21-3. doi: 10.1016/j.earlhumdev.2013.07.006 PMID: 23886560.
3. Baserga M, Bertolotto C, Maclennan NK, Hsu JL, Pham T, Laksana GS, et al. Uteroplacental insufficiency decreases small intestine growth and alters apoptotic homeostasis in term intrauterine growth retarded rats. Early human development. 2004; 79(2):93-105. doi: 10.1016/j.earlhumdev.2004.04.015 PMID: 15324990.
4. Garite TJ, Clark R, Thorp JA. Intrauterine growth restriction increases morbidity and mortality among premature neonates. American journal of obstetrics and gynecology. 2004; 191(2):481-7. doi: 10.1016/j.ajog.2004.01.036 PMID: 15343225.
5. Bernstein IM, Horbar JD, Badger GJ, Ohlsson A, Golan A. Morbidity and mortality among very-lowbirth-weight neonates with intrauterine growth restriction. The Vermont Oxford Network. American journal of obstetrics and gynecology. 2000; 182(1 Pt 1):198-206. PMID: 10649179.
6. March MI, Gupta M, Modest AM, Wu L, Hacker MR, Martin CR, et al. Maternal risk factors for neonatal necrotizing enterocolitis. The journal of maternal-fetal & neonatal medicine. 2014:1-6. doi: 10.3109/14767058.2014.951624 PMID: 25162307.
7. Gordon PV, Clark R, Swanson JR, Spitzer A. Can a national dataset generate a nomogram for necrotizing enterocolitis onset? Journal of perinatology. 2014; 34(10):732-5. doi: 10.1038/jp.2014.137 PMID: 25078862.
8. Gilbert WM, Danielsen B. Pregnancy outcomes associated with intrauterine growth restriction. American journal of obstetrics and gynecology. 2003; 188(6):1596-9; discussion 9-601. PMID: 12824998.
9. Fung C, Brown A, Cox J, Callaway C, McKnight R, Lane R. Novel thromboxane A(2) analog-induced IUGR mouse model. J Dev Orig Hlth Dis. 2011; 2(5):291-301. doi: 10.1017/S2040174411000535 PMID: WOS:000296534800005.
10. Liu HS, Chu TY, Yu MH, Chang YK, Ko CS, Chao CF. Thromboxane and prostacyclin in maternal and fetal circulation in pre-eclampsia. International journal of gynaecology and obstetrics. 1998; 63(1):1-6. PMID: 9849704.
11. Moore HM, Kelly A, McShane LM, Vaught J. Biospecimen reporting for improved study quality (BRISQ). Clin Chim Acta. 2012; 413(15-16):1305. doi: 10.1016/j.cca.2012.04.013 PMID: 22543057.
12. 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):G656-66. doi: 10.1152/ajpgi. 00550.2010 PMID: 21737776; PubMed Central PMCID: PMCPMC3191555.
13. Weitkamp JH, Rosen MJ, Zhao Z, Koyama T, Geem D, Denning TL, et al. Small intestinal intraepithelial TCRgammadelta+ T lymphocytes are present in the premature intestine but selectively reduced in surgical necrotizing enterocolitis. PLoS One. 2014; 9(6):e99042. doi: 10.1371/journal.pone.0099042 PMID: 24905458; PubMed Central PMCID: PMC4048281.
14. Brown KS, Gong H, Frey MR, Pope B, Golden M, Martin K, et al. Tumor necrosis factor induces developmental stage-dependent structural changes in the immature small intestine. Mediators Inflamm. 2014; 2014:852378. doi: 10.1155/2014/852378 PMID: 25242872; PubMed Central PMCID: PMCPMC4163315.
15. McElroy SJ, Castle SL, Bernard JK, Almohazey D, Hunter CJ, Bell BA, et al. The ErbB4 ligand neuregulin- 4 protects against experimental necrotizing enterocolitis. Am J Pathol. 2014; 184(10):2768-78. doi: 10.1016/j.ajpath.2014.06.015 PMID: 25216938.
16. Bernard JK, McCann SP, Bhardwaj V, Washington MK, Frey MR. Neuregulin-4 is a survival factor for colon epithelial cells both in culture and in vivo. J Biol Chem. 2012; 287(47):39850-8. doi: 10.1074/jbc. M112.400846 PMID: 23033483; PubMed Central PMCID: PMC3501086.
17. Zhang C, Sherman MP, Prince LS, Bader D, Weitkamp JH, Slaughter JC, et al. Paneth cell ablation in the presence of Klebsiella pneumoniae induces necrotizing enterocolitis (NEC)-like injury in the small intestine of immature mice. Dis Model Mech. 2012; 5(4):522-32. doi: 10.1242/dmm.009001 PMID: 22328592; PubMed Central PMCID: PMCPMC3380715.
18. Bry L, Falk P, Huttner K, Ouellette A, Midtvedt T, Gordon JI. Paneth cell differentiation in the developing intestine of normal and transgenic mice. Proc Natl Acad Sci U S A. 1994; 91(22):10335-9. Epub 1994/10/25. PMID: 7937951; PubMed Central PMCID: PMC45014.
19. Coutinho HB, da Mota HC, Coutinho VB, Robalinho TI, Furtado AF, Walker E, et al. Absence of lysozyme (muramidase) in the intestinal Paneth cells of newborn infants with necrotising enterocolitis. J Clin Pathol. 1998; 51(7):512-4. Epub 1998/11/03. PMID: 9797727; PubMed Central PMCID: PMC500803.
20. Martin RJ, Fanaroff AA, Walsh MC. Fanaroff and Martin's neonatal-perinatal medicine: diseases of the fetus and infant. 10th edition. ed. Philadelphia, PA: Elsevier/Saunders; 2015. p. p.
21. Noah TK, Donahue B, Shroyer NF. Intestinal development and differentiation. Exp Cell Res. 2011; 317 (19):2702-10. doi: 10.1016/j.yexcr.2011.09.006 PMID: 21978911; PubMed Central PMCID: PMC3210330.
22. Sanderson IR, Walker A, NetLibrary Inc. Development of the gastrointestinal tract. Hamilton, Ont.; London: B C Decker; 1999. Available from: http://www.netLibrary.com/urlapi.asp?action=summary&v=1&bookid=22435.
23. Salzman NH, Underwood MA, Bevins CL. Paneth cells, defensins, and the commensal microbiota: a hypothesis on intimate interplay at the intestinal mucosa. Semin Immunol. 2007; 19(2):70-83. Epub 2007/05/09. S1044-5323(07)00032-2 [pii] doi: 10.1016/j.smim.2007.04.002 PMID: 17485224.
24. Lin PW, Nasr TR, Stoll BJ. Necrotizing enterocolitis: recent scientific advances in pathophysiology and prevention. Semin Perinatol. 2008; 32(2):70-82. Epub 2008/03/19. S0146-0005(08)00005-0 [pii] doi: 10.1053/j.semperi.2008.01.004 PMID: 18346530.
25. Andrianifahanana M, Moniaux N, Batra SK. Regulation of mucin expression: mechanistic aspects and implications for cancer and inflammatory diseases. Biochimica et biophysica acta. 2006; 1765(2):189-222. doi: 10.1016/j.bbcan.2006.01.002 PMID: 16487661.
26. 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 2006/06/27. 00090.2006 [pii] doi: 10.1152/ajpgi. 00090.2006 PMID: 16798726.
27. Porter EM, Bevins CL, Ghosh D, Ganz T. The multifaceted Paneth cell. Cell Mol Life Sci. 2002; 59 (1):156-70. Epub 2002/02/16. PMID: 11846026.
28. Ogura Y, Lala S, Xin W, Smith E, Dowds TA, Chen FF, et al. Expression of NOD2 in Paneth cells: a possible link to Crohn's ileitis. Gut. 2003; 52(11):1591-7. PMID: 14570728; PubMed Central PMCID: PMC1773866.
29. Patel RM, Denning PW. Intestinal microbiota and its relationship with necrotizing enterocolitis. Pediatr Res. 2015; 78(3):232-8. doi: 10.1038/pr.2015.97 PMID: 25992911; PubMed Central PMCID: PMCPMC4655440.
30. McElroy SJ, Underwood MA, Sherman MP. Paneth Cells and Necrotizing Enterocolitis: A Novel Hypothesis for Disease Pathogenesis. Neonatology. 2012; 103(1):10-20. Epub 2012/09/26. doi: 10.1159/000342340 PMID: 23006982.
31. Clevers H. Stem Cells: A unifying theory for the crypt. Nature. 2013; 495(7439):53-4. doi: 10.1038/nature11958 PMID: 23446347.
32. Clevers H, Nusse R. Wnt/beta-catenin signaling and disease. Cell. 2012; 149(6):1192-205. Epub 2012/06/12. doi: 10.1016/j.cell.2012.05.012 PMID: 22682243.
33. Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, van den Born M, et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature. 2011; 469(7330):415-8. Epub 2010/11/30. nature09637 [pii] doi: 10.1038/nature09637 PMID: 21113151.
34. van Es JH, Jay P, Gregorieff A, van Gijn ME, Jonkheer S, Hatzis P, et al. Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat Cell Biol. 2005; 7(4):381-6. doi: 10.1038/ncb1240 PMID: 15778706.
35. Mustata RC, Van Loy T, Lefort A, Libert F, Strollo S, Vassart G, et al. Lgr4 is required for Paneth cell differentiation and maintenance of intestinal stem cells ex vivo. EMBO Rep. 2011; 12(6):558-64. doi: 10.1038/embor.2011.52 PMID: 21508962; PubMed Central PMCID: PMCPMC3128273.
36. Sansom OJ, Reed KR, Hayes AJ, Ireland H, Brinkmann H, Newton IP, et al. Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev. 2004; 18(12):1385-90. doi: 10.1101/gad.287404 PMID: 15198980; PubMed Central PMCID: PMCPMC423189.
37. McElroy SJ, Weitkamp JH. Innate Immunity in the Small Intestine of the Preterm Infant. Neoreviews. 2011; 12(9):e517-e26. doi: 10.1542/neo.12-9-e517 PMID: 22639551; PubMed Central PMCID: PMCPMC3359837.