Intestinal dysbiosis and bacterial enteroinvasion in a murine model of Hirschsprung's disease

Journal of Pediatric Surgery

Volumn 49, Issue 8, 2014, Pages 1242-1251

  Pierre, Joseph F ^a   Barlow Anacker, Amanda J ^a   Erickson, Christopher S ^a   Heneghan, Aaron F ^a   Leverson, Glen E ^a   Dowd, Scot E ^b   Epstein, Miles L ^a   Kudsk, Kenneth A ^a,c   Gosain, Ankush ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b Research and Testing Laboratory   (United States)

^c WILLIAM S MIDDLETON MEMORIAL VETERANS HOSPITAL   (United States)

Author keywords

Dysbiosis; Hirschsprung's disease; Hirschsprung's associated enterocolitis; Microbiome; Mucosal immunity; Secretory phospholipase A2

Indexed keywords

BACTERIAL DNA; ENDOTHELIN B RECEPTOR; PHOSPHOLIPASE A2; SECRETORY PHOSPHOLIPASE A2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTEROIDES; BLAUTIA; CLOSTRIDIUM; CONTROLLED STUDY; DYSBIOSIS; ENTEROCOLITIS; ESCHERICHIA COLI; EUBACTERIUM; EX VIVO STUDY; FECES ANALYSIS; HIRSCHSPRUNG ASSOCIATED ENTEROCOLITIS; HIRSCHSPRUNG DISEASE; ILEUM; IMMUNOHISTOCHEMISTRY; INTESTINE FLORA; LACTOBACILLUS; MICROBIAL DIVERSITY; MOUSE; NONHUMAN; PANETH CELL; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; ROSEBURIA; RUMINOCOCCUS; STAPHYLOCOCCUS; STREPTOCOCCUS; ANIMAL; BACTERIUM; CELLULAR IMMUNITY; COMPLICATION; DISEASE MODEL; GENETICS; IMMUNOLOGY; INTESTINE; INTESTINE MUCOSA; ISOLATION AND PURIFICATION; MICROBIOLOGY; PATHOLOGY; RISK FACTOR; TRANSGENIC MOUSE;

ANIMALS; BACTERIA; DISEASE MODELS, ANIMAL; DNA, BACTERIAL; DYSBIOSIS; ENTEROCOLITIS; HIRSCHSPRUNG DISEASE; IMMUNITY, CELLULAR; INTESTINAL MUCOSA; INTESTINES; MICE; MICE, TRANSGENIC; RISK FACTORS;

EID: 84905443819     PISSN: 00223468     EISSN: 15315037     Source Type: Journal    
DOI: 10.1016/j.jpedsurg.2014.01.060     Document Type: Article

References (60)

1. J. Amiel, E. Sproat-Emison, and M. Garcia-Barcelo et al. Hirschsprung disease, associated syndromes and genetics: a review J Med Genet 45 2008 1 14
2. V. Sasselli, V. Pachnis, and A.J. Burns The enteric nervous system Dev Biol 366 2012 64 73
3. K.M. Austin The pathogenesis of Hirschsprung's disease-associated enterocolitis Semin Pediatr Surg 21 2012 319 327
4. P.K. Frykman, and S.S. Short Hirschsprung-associated enterocolitis: prevention and therapy Semin Pediatr Surg 21 2012 328 335
5. C. De Filippo, A. Pini-Prato, and G. Mattioli et al. Genomics approach to the analysis of bacterial communities dynamics in Hirschsprung's disease-associated enterocolitis: a pilot study Pediatr Surg Int 26 2010 465 471
6. N.L. Ward, A. Pieretti, and S.E. Dowd et al. Intestinal aganglionosis is associated with early and sustained disruption of the colonic microbiome Neurogastroenterol Motil 24 2012 e400 e874
7. D.-H. Shen, C.-R. Shi, and J.-J. Chen et al. Detection of intestinal bifidobacteria and lactobacilli in patients with Hirschsprung's disease associated enterocolitis World J Pediatr 5 2009 201 205
8. S.E. Dowd, Y. Sun, and R.D. Wolcott et al. Bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP) for microbiome studies: bacterial diversity in the ileum of newly weaned Salmonella-infected pigs Foodborne Pathog Dis 5 2008 459 472
9. S.E. Dowd, T.R. Callaway, and R.D. Wolcott et al. Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP) BMC Microbiol 8 2008 125
10. R.E. Ley, P.J. Turnbaugh, and S. Klein et al. Microbial ecology: human gut microbes associated with obesity Nature 444 2006 1022 1023
11. L. Wen, R.E. Ley, and P.Y. Volchkov et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes Nature 455 2008 1109 1113
12. R.B. Sartor Microbial influences in inflammatory bowel diseases Gastroenterology 134 2008 577 594
13. G.C. Parkes, J. Brostoff, and K. Whelan et al. Gastrointestinal microbiota in irritable bowel syndrome: their role in its pathogenesis and treatment Am J Gastroenterol 103 2008 1557 1567
14. M.-A. Schillde von, G. Hörmannsperger, and M. Weiher et al. Lactocepin secreted by Lactobacillus exerts anti-inflammatory effects by selectively degrading proinflammatory chemokines Cell Host Microbe 11 2012 387 396
15. K. Lucke, S. Miehlke, and E. Jacobs et al. Prevalence of Bacteroides and Prevotella spp. in ulcerative colitis J Med Microbiol 55 2006 617 624
16. N.H. Salzman, K. Hung, and D. Haribhai et al. Enteric defensins are essential regulators of intestinal microbial ecology Nat Immunol 11 2010 76 83
17. M.L. Andersson, J.M.T. Karlsson-Sjöberg, and K.L.-A. Pütsep CRS-peptides: unique defense peptides of mouse Paneth cells Mucosal Immunol 5 2012 367 376
18. S.S. Harwig, L. Tan, and X.D. Qu et al. Bactericidal properties of murine intestinal phospholipase A2 J Clin Invest 95 1995 603 610
19. J.F. Pierre, A.F. Heneghan, and F.H.C. Tsao et al. Route and type of nutrition and surgical stress influence secretory phospholipase A2 secretion of the murine small intestine JPEN J Parenter Enteral Nutr 35 2011 748 756
20. A.K. Foreman-Wykert, Y. Weinrauch, and P. Elsbach et al. Cell-wall determinants of the bactericidal action of group IIA phospholipase A2 against Gram-positive bacteria J Clin Invest 103 1999 715 721
21. J. Wehkamp, J. Harder, and M. Weichenthal et al. NOD2 (CARD15) mutations in Crohn's disease are associated with diminished mucosal alpha-defensin expression Gut 53 2004 1658 1664
22. J. Wehkamp, N.H. Salzman, and E. Porter et al. Reduced Paneth cell alpha-defensins in ileal Crohn's disease Proc Natl Acad Sci U S A 102 2005 18129 18134
23. L.A. Simms, J.D. Doecke, and M.D. Walsh et al. Reduced alpha-defensin expression is associated with inflammation and not NOD2 mutation status in ileal Crohn's disease Gut 57 2008 903 910
24. H. Veiga-Fernandes, M.C. Coles, and K.E. Foster et al. Tyrosine kinase receptor RET is a key regulator of Peyer's patch organogenesis Nature 446 2007 547 551
25. A. Schuchardt, V. D'Agati, and L. Larsson-Blomberg et al. Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret Nature 367 1994 380 383
26. N.R. Druckenbrod, P.A. Powers, and C.R. Bartley et al. Targeting of endothelin receptor-B to the neural crest Genesis 46 2008 396 400
27. J.F. Pierre, A.F. Heneghan, and J.M. Meudt et al. Parenteral nutrition increases susceptibility of ileum to invasion by E coli J Surg Res 183 2013 583 591
28. C.S. Erickson, I. Zaitoun, and K.M. Haberman et al. Sacral neural crest-derived cells enter the aganglionic colon of Ednrb(-/-) mice along extrinsic nerve fibers J Comp Neurol 520 3 2012 620 632
29. J.H. Campbell, C.M. Foster, and T. Vishnivetskaya et al. Host genetic and environmental effects on mouse intestinal microbiota ISME J 6 2012 2033 2044
30. S.E. Dowd, R.D. Wolcott, and Y. Sun et al. Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP) PLoS ONE 3 2008 e3326
31. C.D. Sibley, M.E. Grinwis, and T.R. Field et al. Culture enriched molecular profiling of the cystic fibrosis airway microbiome PLoS ONE 6 2011 e22702
32. J. Kuczynski, J. Stombaugh, and W.A. Walters et al. Using QIIME to analyze 16S rRNA gene sequences from microbial communities Curr Protoc Bioinformatics 2011 Chapter 10:Unit10.7
33. C.A. Lozupone, M. Hamady, and S.T. Kelley et al. Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities Appl Environ Microbiol 73 2007 1576 1585
34. C. Lozupone, M.E. Lladser, and D. Knights et al. UniFrac: an effective distance metric for microbial community comparison ISME J 5 2011 169 172
35. J. Omata, J.F. Pierre, and A.F. Heneghan et al. Parenteral nutrition suppresses the bactericidal response of the small intestine Surgery 153 2013 17 24
36. T. Fujimoto, D.J. Reen, and P. Puri Inflammatory response in enterocolitis in the piebald lethal mouse model of Hirschsprung's disease Pediatr Res 24 1988 152 155
37. Z. Cheng, D. Dhall, and L. Zhao et al. Murine model of Hirschsprung-associated enterocolitis. I: phenotypic characterization with development of a histopathologic grading system J Pediatr Surg 45 2010 475 482
38. N.J. Gotelli, and R.K. Colwell Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness Ecol Lett 4 2001 379 391
39. R.R. Roberts, J.C. Bornstein, and A.J. Bergner et al. Disturbances of colonic motility in mouse models of Hirschsprung's disease Am J Physiol Gastrointest Liver Physiol 294 2008 G996 G1008
40. I. Zaitoun, C.S. Erickson, and A.J. Barlow et al. Altered neuronal density and neurotransmitter expression in the ganglionated region of Ednrb null mice: implications for Hirschsprung's disease Neurogastroenterol Motil 25 3 2013 e233 e244
41. J. Karlsson, K. Pütsep, and H. Chu et al. Regional variations in Paneth cell antimicrobial peptide expression along the mouse intestinal tract BMC Immunol 9 2008 37
42. D. Wilson-Storey, W.G. Scobie, and K.G. McGenity Microbiological studies of the enterocolitis of Hirschsprung's disease Arch Dis Child 65 1990 1338 1339
43. S. Kang, S.E. Denman, and M. Morrison et al. Dysbiosis of fecal microbiota in Crohn's disease patients as revealed by a custom phylogenetic microarray Inflamm Bowel Dis 16 2010 2034 2042
44. A. Darfeuille-Michaud, J. Boudeau, and P. Bulois et al. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease Ygast 127 2004 412 421
45. A. Swidsinski, J. Weber, and V. Loening-Baucke et al. Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease J Clin Microbiol 43 2005 3380 3389
46. S.M. Bloom, V.N. Bijanki, and G.M. Nava et al. Commensal Bacteroides species induce colitis in host-genotype-specific fashion in a mouse model of inflammatory bowel disease Cell Host Microbe 9 2011 390 403
47. A.V. Keita, and J.D. Söderholm The intestinal barrier and its regulation by neuroimmune factors Neurogastroenterol Motil 22 2010 718 733
48. D.H. Teitelbaum, D.A. Caniano, and S.J. Qualman The pathophysiology of Hirschsprung's-associated enterocolitis: importance of histologic correlates J Pediatr Surg 24 1989 1271 1277
49. A. Aslam, R.D. Spicer, and A.P. Corfield Children with Hirschsprung's disease have an abnormal colonic mucus defensive barrier independent of the bowel innervation status J Pediatr Surg 32 1997 1206 1210
50. A.F. Mattar, A.G. Coran, and D.H. Teitelbaum MUC-2 mucin production in Hirschsprung's disease: possible association with enterocolitis development J Pediatr Surg 38 2003 [417-21-discussion417-21]
51. U. Meyer-Hoffert, M.W. Hornef, and B. Henriques-Normark et al. Secreted enteric antimicrobial activity localises to the mucus surface layer Gut 57 2008 764 771
52. S.A. Beers, A.G. Buckland, and R.S. Koduri et al. The antibacterial properties of secreted phospholipases A2: a major physiological role for the group IIA enzyme that depends on the very high pI of the enzyme to allow penetration of the bacterial cell wall J Biol Chem 277 2002 1788 1793
53. Z. Cheng, X. Wang, and D. Dhall et al. Splenic lymphopenia in the endothelin receptor B-null mouse: implications for Hirschsprung associated enterocolitis Pediatr Surg Int 27 2011 145 150
54. S. Schüller, M. Lucas, and J.B. Kaper et al. The ex vivo response of human intestinal mucosa to enteropathogenic Escherichia coli infection Cell Microbiol 11 2009 521 530
55. J.A. Clark, S.M. Doelle, and M.D. Halpern et al. Intestinal barrier failure during experimental necrotizing enterocolitis: protective effect of EGF treatment Am J Physiol Gastrointest Liver Physiol 291 2006 G938 G949
56. M.K. Friswell, H. Gika, and I.J. Stratford et al. Site and strain-specific variation in gut microbiota profiles and metabolism in experimental mice PLoS ONE 5 2010 e8584
57. J. Vaahtovuo, P. Toivanen, and E. Eerola Bacterial composition of murine fecal microflora is indigenous and genetically guided FEMS Microbiol Ecol 44 2003 131 136
58. Q. Wang, J. Dong, and Y. Zhu Probiotic supplement reduces risk of necrotizing enterocolitis and mortality in preterm very low-birth-weight infants: an updated meta-analysis of 20 randomized, controlled trials J Pediatr Surg 47 2012 241 248
59. S. Guandalini Update on the role of probiotics in the therapy of pediatric inflammatory bowel disease Expert Rev Clin Immunol 6 2010 47 54
60. M. El-Sawaf, S. Siddiqui, and M. Mahmoud et al. Probiotic prophylaxis after pullthrough for Hirschsprung disease to reduce incidence of enterocolitis: a prospective, randomized, double-blind, placebo-controlled, multicenter trial J Pediatr Surg 48 2013 111 117