Respective roles of hematopoietic and nonhematopoietic Nod2 on the gut microbiota and mucosal homeostasis

Inflammatory Bowel Diseases

Volumn 22, Issue 4, 2016, Pages 763-773

  Alnabhani, Ziad ^a,b,c,d   Hugot, Jean Pierre ^a,b,e   Montcuquet, Nicolas ^f,g   Le Roux, Karine ^c,d   Dussaillant, Monique ^a,b   Roy, Maryline ^a,b   Leclerc, Marion ^c,d   Cerf Bensussan, Nadine ^f,g   Lepage, Patricia ^c,d   Barreau, Frédérick ^a,b,h  

^a CENTRE DE RECHERCHE SUR L INFLAMMATION   (France)

^b Labex Inflamex   (France)

^c UMR1319 MICALIS   (France)

^d AGROPARISTECH   (France)

^e HÔPITAL ROBERT DEBRÉ   (France)

^f INSERM   (France)

^g UNIVERSITÉ PARIS DESCARTES   (France)

^h UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

antimicrobial peptides; Crohn's disease; gut permeability; microbiota; Nod2; Peyer's patches

Indexed keywords

ADENOSINE PHOSPHATE; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CD3 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; MUCIN; POLYPEPTIDE ANTIBIOTIC AGENT; TUMOR NECROSIS FACTOR ALPHA; CARD15 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; BACTERIAL TRANSLOCATION; BACTEROIDETES; CD3+ T LYMPHOCYTE; CLOSTRIDIUM; CONTROLLED STUDY; CROHN DISEASE; DENDRITIC CELL; DYSBIOSIS; FECES ANALYSIS; FIRMICUTES; GENE DELETION; GENE EXPRESSION; GENETIC BACKGROUND; HEMATOPOIETIC STEM CELL; HOMEOSTASIS; INTESTINE FLORA; INTESTINE LYMPHATIC TISSUE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PERMEABILITY; PEYER PATCH; PORPHYROMONADACEAE; PRIORITY JOURNAL; REGULATORY MECHANISM; ANIMAL; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY;

ANIMALS; DYSBIOSIS; GASTROINTESTINAL MICROBIOME; HEMATOPOIETIC STEM CELLS; HOMEOSTASIS; INTESTINAL MUCOSA; MICE; MICE, KNOCKOUT; NOD2 SIGNALING ADAPTOR PROTEIN;

EID: 84962218773     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0000000000000749     Document Type: Article

References (43)

1. Sartor RB. Microbial influences in inflammatory bowel diseases. Gastroenterology. 2008;134:577-594.
2. Jung C, Hugot JP, Barreau F. Peyers patches: the immune Sensors of the intestine. Int J Inflam. 2010;2010:823710.
3. Hollander D, Vadheim CM, Brettholz E, et al. Increased intestinal permeability in patients with Crohns disease and their relatives. A possible etiologic factor. Ann Intern Med. 1986;105:883-885.
4. Hugot JP, Chamaillard M, Zouali H, et al. Association of NOD2 leucinerich repeat variants with susceptibility to Crohns disease. Nature. 2001; 411:599-603.
5. Ogura Y, Bonen DK, Inohara N, et al. A frameshift mutation in NOD2 associated with susceptibility to Crohns disease. Nature. 2001;411: 603-606.
6. Girardin SE, Boneca IG, Viala J, et al. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem. 2003;278:8869-8872.
7. Traub S, von Aulock S, Hartung T, et al. MDP and other muropeptides-Direct and synergistic effects on the immune system. J Endotoxin Res. 2006;12:69-85.
8. Barreau F, Meinzer U, Chareyre F, et al. CARD15/NOD2 is required for Peyers patches homeostasis in mice. PLoS One. 2007;2:e523.
9. Hedl M, Abraham C. Distinct roles for Nod2 protein and autocrine interleukin-1beta in muramyl dipeptide-induced mitogen-Activated protein kinase activation and cytokine secretion in human macrophages. J Biol Chem. 2011;286:26440-26449.
10. 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;39:521-536.
11. Yamamoto-Furusho JK, Barnich N, Hisamatsu T, et al. MDP-NOD2 stimulation induces HNP-1 secretion, which contributes to NOD2 antibacterial function. Inflamm Bowel Dis. 2010;16:736-742.
12. Barreau F, Madre C, Meinzer U, et al. Nod2 regulates the host response towards microflora by modulating T cell function and epithelial permeability in mouse Peyers patches. Gut. 2010;59:207-217.
13. Cruickshank SM, Wakenshaw L, Cardone J, et al. Evidence for the involvement of NOD2 in regulating colonic epithelial cell growth and survival. World J Gastroenterol. 2008;14:5834-5841.
14. Li E, Hamm CM, Gulati AS, et al. Inflammatory bowel diseases phenotype, C. difficile and NOD2 genotype are associated with shifts in human ileum associated microbial composition. PLoS One. 2012;7:e26284.
15. Rehman A, Sina C, Gavrilova O, et al. Nod2 is essential for temporal development of intestinal microbial communities. Gut. 2011;60: 1354-1362.
16. Mondot S, Barreau F, Al Nabhani Z, et al. Altered gut microbiota composition in immune-impaired Nod2(-/-) mice. Gut. 2012;61:634-635.
17. Couturier-Maillard A, Secher T, Rehman A, et al. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J Clin Invest. 2013;123:700-711.
18. Barreau F, Hugot J. Intestinal barrier dysfunction triggered by invasive bacteria. Curr Opin Microbiol. 2014;17C:91-98.
19. Alnabhani Z, Montcuquet N, Biaggini K, et al. Pseudomonas fluorescens alters the intestinal barrier function by modulating IL-1beta expression through hematopoietic NOD2 signaling. Inflamm Bowel Dis. 2015;21: 543-555.
20. Biswas A, Liu YJ, Hao L, et al. Induction and rescue of Nod2-Dependent Th1-Driven granulomatous inflammation of the ileum. Proc Natl Acad Sci U S A. 2010;107:14739-14744.
21. Meinzer U, Esmiol-Welterlin S, Barreau F, et al. Nod2 mediates susceptibility to Yersinia pseudotuberculosis in mice. PLoS One. 2008;3:e2769.
22. Meinzer U, Barreau F, Esmiol-Welterlin S, et al. Yersinia pseudotuberculosis effector YopJ subverts the Nod2/RICK/TAK1 pathway and activates caspase-1 to induce intestinal barrier dysfunction. Cell Host Microbe. 2012;11:337-351.
23. Kobayashi KS, Chamaillard M, Ogura Y, et al. Nod2-Dependent regulation of innate and adaptive immunity in the intestinal tract. Science. 2005; 307:731-734.
24. Berrebi D, Maudinas R, Hugot JP, et al. Card15 gene overexpression in mononuclear and epithelial cells of the inflamed Crohns disease colon. Gut. 2003;52:840-846.
25. Jung C, Meinzer U, Montcuquet N, et al. Yersinia pseudotuberculosis disrupts intestinal barrier integrity through hematopoietic TLR-2 signaling. J Clin Invest. 2012;122:2239-2251.
26. Lepage P, Seksik P, Sutren M, et al. Biodiversity of the mucosa-Associated microbiota is stable along the distal digestive tract in healthy individuals and patients with IBD. Inflamm Bowel Dis. 2005;11:473-480.
27. Seksik P, Rigottier-Gois L, Gramet G, et al. Alterations of the dominant faecal bacterial groups in patients with Crohns disease of the colon. Gut. 2003;52:237-242.
28. Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-Throughput community sequencing data. Nat Methods. 2010;7: 335-336.
29. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22: 1658-1659.
30. Cole JR, Wang Q, Cardenas E, et al. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 2009;37:D141-D145.
31. Hugot JP, Zouali H, Lesage S. Lessons to be learned from the NOD2 gene in Crohns disease. Eur J Gastroenterol Hepatol. 2003;15:593-597.
32. Lesage S, Zouali H, Cezard JP, et al. CARD15/NOD2 mutational analysis and genotype-phenotype correlation in 612 patients with inflammatory bowel disease. Am J Hum Genet. 2002;70:845-857.
33. Smith RJ, Jeffries TC, Roudnew B, et al. Metagenomic comparison of microbial communities inhabiting confined and unconfined aquifer ecosystems. Environ Microbiol. 2012;14:240-253.
34. Petnicki-Ocwieja T, Hrncir T, Liu YJ, et al. Nod2 is required for the regulation of commensal microbiota in the intestine. Proc Natl Acad Sci U S A. 2009;106:15813-15818.
35. Hildebrand F, Nguyen TL, Brinkman B, et al. Inflammation-Associated enterotypes, host genotype, cage and inter-individual effects drive gut microbiota variation in common laboratory mice. Genome Biol. 2013;14:R4.
36. Wehkamp J, Harder J, Weichenthal M, et al. NOD2 (CARD15) mutations in Crohns disease are associated with diminished mucosal alpha-Defensin expression. Gut. 2004;53:1658-1664.
37. Robertson SJ, Zhou JY, Geddes K, et al. Nod1 and Nod2 signaling does not alter the composition of intestinal bacterial communities at homeostasis. Gut Microbes. 2013;4:222-231.
38. Shanahan MT, Carroll IM, Grossniklaus E, et al. Mouse Paneth cell antimicrobial function is independent of Nod2. Gut. 2014;63:903-910.
39. Su L, Shen L, Clayburgh DR, et al. Targeted epithelial tight junction dysfunction causes immune activation and contributes to development of experimental colitis. Gastroenterology. 2009;136:551-563.
40. Liu X, Xu J, Mei Q, et al. Myosin light chain kinase inhibitor inhibits dextran sulfate sodium-induced colitis in mice. Dig Dis Sci. 2013;58: 107-114.
41. Buhner S, Buning C, Genschel J, et al. Genetic basis for increased intestinal permeability in families with Crohns disease: role of CARD15 3020insC mutation? Gut. 2006;55:342-347.
42. Verdam FJ, Fuentes S, de Jonge C, et al. Human Intestinal Microbiota Composition Is Associated with Local and Systemic Inflammation in Obesity. Obesity (Silver Spring). 2013;21:E607-E615.
43. Penack O, Smith OM, Cunningham-Bussel A, et al. NOD2 regulates hematopoietic cell function during graft-versus-host disease. J Exp Med. 2009;206:2101-2110.