Preterm infant gut microbiota affects intestinal epithelial development in a humanized microbiome gnotobiotic mouse model

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 311, Issue 3, 2016, Pages G521-G532

  Yu, Yueyue ^a   Lu, Lei ^a   Sun, Jun ^b   Petrof, Elaine O ^c   Claud, Erika C ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c QUEEN S UNIVERSITY   (Canada)

Author keywords

Development; Gnotobiotic; Gut; Microbiota; Preterm

Indexed keywords

MESSENGER RNA; MUCIN 2; MUCIN 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CASE REPORT; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CELL PROLIFERATION; FEMALE; GENE EXPRESSION; GNOTOBIOTICS; GOBLET CELL; HUMAN; INFANT; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; INTESTINE FUNCTION; LASER CAPTURE MICRODISSECTION; MICROBIAL COLONIZATION; MOUSE; MOUSE MODEL; NONHUMAN; PANETH CELL; PREMATURITY; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; GENETICS; GERMFREE ANIMAL; INTESTINE MUCOSA; MICROBIOLOGY; MICROFLORA;

ANIMALS; GERM-FREE LIFE; HUMANS; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MICROBIOTA;

EID: 84986568278     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00022.2016     Document Type: Article

References (53)

1. Abrams GD, Bauer H, Sprinz H. Influence of the normal flora on mucosal morphology and cellular renewal in the ileum. A comparison of germ-free and conventional mice. Lab Invest 12: 355-364, 1963
2. Banasaz M, Norin E, Holma R, Midtvedt T. Increased enterocyte production in gnotobiotic rats mono-associated with Lactobacillus rhamnosus GG. Appl Environ Microbiol 68: 3031-3034, 2002
3. Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A, Rottier O, Geurts L, Naslain D, Neyrinck A, Lambert DM, Muccioli GG, Delzenne NM. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58: 1091-1103, 2009
4. Cario E, Gerken G, Podolsky DK. Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function. Gastroenterology 132: 1359-1374, 2007
5. Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat Rev Genet 13: 260-270, 2012
6. Claud EC, Keegan KP, Brulc JM, Lu L, Bartels D, Glass E, Chang EB, Meyer F, Antonopoulos DA. Bacterial community structure and functional contributions to emergence of health or necrotizing enterocolitis in preterm infants. Microbiome 1: 20, 2013
7. Clevers HC, Bevins CL. Paneth cells: maestros of the small intestinal crypts. Annu Rev Physiol 75: 289-311, 2013
8. Coutinho HB, da Mota HC, Coutinho VB, Robalinho TI, Furtado AF, Walker E, King G, Mahida YR, Sewell HF, Wakelin D. Absence of lysozyme (muramidase) in the intestinal Paneth cells of newborn infants with necrotising enterocolitis. J Clin Pathol 51: 512-514, 1998
9. Deplancke B, Gaskins HR. Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. Am J Clin Nutr 73: 1131S-1141S, 2001
10. DiGiulio DB, Romero R, Amogan HP, Kusanovic JP, Bik EM, Gotsch F, Kim CJ, Erez O, Edwin S, Relman DA. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PloS one 3: e3056, 2008
11. Ellison RT 3rd, Giehl TJ. Killing of gram-negative bacteria by lactoferrin and lysozyme. J Clin Invest 88: 1080-1091, 1991
12. Falk PG, Hooper LV, Midtvedt T, Gordon JI. Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology. Microbiol Mol Biol Rev 62: 1157-1170, 1998
13. Fanaro S, Chierici R, Guerrini P, Vigi V. Intestinal microflora in early infancy: composition and development. Acta Paediatr 91: 48-55, 2003
14. Flint HJ, Scott KP, Louis P, Duncan SH. The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol 9: 577-589, 2012
15. Glaister JR. Factors affecting the lymphoid cells in the small intestinal epithelium of the mouse. Int Arch Allergy Appl Immunol 45: 719-730, 1973
16. Gordon HA, Bruckner-Kardoss E. Effect of normal microbial flora on intestinal surface area. Am J Physiol 201: 175-178, 1961
17. Groer MW, Luciano AA, Dishaw LJ, Ashmeade TL, Miller E, Gilbert JA. Development of the preterm infant gut microbiome: a research priority. Microbiome 2: 38, 2014
18. Ho SB, Dvorak LA, Moor RE, Jacobson AC, Frey MR, Corredor J, Polk DB, Shekels LL. Cysteine-rich domains of muc3 intestinal mucin promote cell migration, inhibit apoptosis, and accelerate wound healing. Gastroenterology 131: 1501-1517, 2006
19. Hooper LV. Bacterial contributions to mammalian gut development. Trends Microbiol 12: 129-134, 2004
20. Hunter CJ, Upperman JS, Ford HR, Camerini V. Understanding the susceptibility of the premature infant to necrotizing enterocolitis (NEC). Pediatr Res 63: 117-123, 2008
21. Jimenez E, Marin ML, Martin R, Odriozola JM, Olivares M, Xaus J, Fernandez L, Rodriguez JM. Is meconium from healthy newborns actually sterile? Res Microbiol 159: 187-193, 2008
22. Khoury KA, Floch MH, Hersh T. Small intestinal mucosal cell proliferation and bacterial flora in the conventionalization of the germfree mouse. J Exp Med 130: 659-670, 1969
23. Lendrum AC. The phloxin-tartrazine method as a general histological stain and for the demonstration of inclusion bodies. J Pathol Bacteriol 59: 399-404, 1947
24. Leser TD, Molbak L. Better living through microbial action: the benefits of the mammalian gastrointestinal microbiota on the host. Environ Microbiol 11: 2194-2206, 2009
25. Liu Z, Li N, Neu J. Tight junctions, leaky intestines, and pediatric diseases. Acta Paediatr 94: 386-393, 2005
26. Lu L, Yu Y, Guo Y, Wang Y, Chang EB, Claud EC. Transcriptional modulation of intestinal innate defense/inflammation genes by preterm infant microbiota in a humanized gnotobiotic mouse model. PLos One 10: e0124504, 2015
27. Mack DR, Michail S, Wei S, McDougall L, Hollingsworth MA. Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. Am J Physiol Gastrointest Liver Physiol 276: G941-G950, 1999
28. Mackie RI, Sghir A, Gaskins HR. Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 69: 1035S-1045S, 1999
29. Magne F, Suau A, Pochart P, Desjeux JF. Fecal microbial community in preterm infants. J Pediatr Gastroenterol Nutr 41: 386-392, 2005
30. Mallow EB, Harris A, Salzman N, Russell JP, DeBerardinis RJ, Ruchelli E, Bevins CL. Human enteric defensins. Gene structure and developmental expression. J Biol Chem 271: 4038-4045, 1996
31. Matamoros S, Gras-Leguen C, Le Vacon F, Potel G, de La Cochetiere MF. Development of intestinal microbiota in infants and its impact on health. Trends Microbiol 21: 167-173, 2013
32. Mattar AF, Teitelbaum DH, Drongowski RA, Yongyi F, Harmon CM, Coran AG. Probiotics up-regulate MUC-2 mucin gene expression in a Caco-2 cell-culture model. Pediatr Surg Int 18: 586-590, 2002
33. Miele L, Valenza V, La Torre G, Montalto M, Cammarota G, Ricci R, Masciana R, Forgione A, Gabrieli ML, Perotti G, Vecchio FM, Rapaccini G, Gasbarrini G, Day CP, Grieco A. Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease. Hepatology 49: 1877-1887, 2009
34. Moles L, Gomez M, Heilig H, Bustos G, Fuentes S, de Vos W, Fernandez L, Rodriguez JM, Jimenez E. Bacterial diversity in meconium of preterm neonates and evolution of their fecal microbiota during the first month of life. PLos One 8: e66986, 2013
35. O’Connor DT, Burton D, Deftos LJ. Chromogranin A: immunohistology reveals its universal occurrence in normal polypeptide hormone producing endocrine glands. Life Sci 33: 1657-1663, 1983
36. 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 (re-)introduce enteral nutrition? J Pediatr Surg 36: 587-592, 2001
37. Potten CS, Merritt A, Hickman J, Hall P, Faranda A. Characterization of radiation-induced apoptosis in the small intestine and its biological implications. Int J Radiat Biol 65: 71-78, 1994
38. Reinhardt C, Bergentall M, Greiner TU, Schaffner F, Ostergren-Lunden G, Petersen LC, Ruf W, Backhed F. Tissue factor and PAR1 promote microbiota-induced intestinal vascular remodelling. Nature 483: 627-631, 2012
39. Salzman NH, Hung K, Haribhai D, Chu H, Karlsson-Sjoberg J, Amir E, Teggatz P, Barman M, Hayward M, Eastwood D, Stoel M, Zhou Y, Sodergren E, Weinstock GM, Bevins CL, Williams CB, Bos NA. Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 11: 76-83, 2010
40. Salzman NH, Underwood MA, Bevins CL. Paneth cells, defensins, and the commensal microbiota: a hypothesis on intimate interplay at the intestinal mucosa. Semin Immunol 19: 70-83, 2007
41. Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, van den Born M, Barker N, Shroyer NF, van de Wetering M, Clevers H. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469: 415-418, 2011
42. Stappenbeck TS, Hooper LV, Gordon JI. Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci USA 99: 15451-15455, 2002
43. Stappenbeck TS, Hooper LV, Manchester JK, Wong MH, Gordon JI. Laser capture microdissection of mouse intestine: characterizing mRNA and protein expression, and profiling intermediary metabolism in specified cell populations. Methods Enzymol 356: 167-196, 2002
44. Sternini C, Anselmi L, Rozengurt E. Enteroendocrine cells: a site of ‘taste’ in gastrointestinal chemosensing. Curr Opin Endocrinol Diabet Obes 15: 73-78, 2008
45. Suzuki T. Regulation of intestinal epithelial permeability by tight junctions. Cell Mol Life Sci 70: 631-659, 2013
46. Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9: 799-809, 2009
47. Verburg M, Renes IB, Meijer HP, Taminiau JA, Buller HA, Einerhand AW, Dekker J. Selective sparing of goblet cells and Paneth cells in the intestine of methotrexate-treated rats. Am J Physiol Gastrointest Liver Physiol 279: G1037-G1047, 2000
48. Watson AJ, Pritchard DM. Lessons from genetically engineered animal models. VII. Apoptosis in intestinal epithelium: lessons from transgenic and knockout mice. Am J Physiol Gastrointest Liver Physiol 278: G1-G5, 2000
49. Wehkamp J, Salzman NH, Porter E, Nuding S, Weichenthal M, Petras RE, Shen B, Schaeffeler E, Schwab M, Linzmeier R, Feathers RW, Chu H, Lima H Jr., Fellermann K, Ganz T, Stange EF, Bevins CL. Reduced Paneth cell alpha-defensins in ileal Crohn’s disease. Proc Natl Acad Sci USA 102: 18129-18134, 2005
50. Westerbeek EA, van den Berg A, Lafeber HN, Knol J, Fetter WP, van Elburg RM. The intestinal bacterial colonisation in preterm infants: a review of the literature. Clin Nutr 25: 361-368, 2006
51. Wimley WC, Selsted ME, White SH. Interactions between human defensins and lipid bilayers: evidence for formation of multimeric pores. Prot Sci 3: 1362-1373, 1994
52. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 415: 389-395, 2002
53. Zhang C, Sherman MP, Prince LS, Bader D, Weitkamp JH, Slaughter JC, McElroy SJ. Paneth cell ablation in the presence of Klebsiella pneumoniae induces necrotizing enterocolitis (NEC)-like injury in the small intestine of immature mice. Dis Models Mech 5: 522-532, 2012