Critical design aspects involved in the study of Paneth cells and the intestinal microbiota

Gut Microbes

Volumn 5, Issue 2, 2013, Pages

  Shanahan, Michael T ^a   Carroll, Ian M ^a   Gulati, Ajay S ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Background strain; Defensin; Inflammatory bowel diseases; Microbiota; Nod2; Paneth cell

Indexed keywords

ALPHA DEFENSIN; CASPASE RECRUITMENT DOMAIN PROTEIN 15; MATRILYSIN; POLYPEPTIDE ANTIBIOTIC AGENT; T CELL FACTOR PROTEIN; T CELL FACTOR PROTEIN 4; UNCLASSIFIED DRUG; DEFENSIN; ANGIOGENIN; CHOLINERGIC RECEPTOR STIMULATING AGENT; LECTIN; LYSOZYME; PEPTIDE; POTASSIUM CHANNEL; PRIMER DNA; RNA 16S; SECRETORY PHOSPHOLIPASE A2;

ACID UREA POLYACRYLAMIDE GEL ELECTROPHORESIS; ALLELE; ANTIMICROBIAL ACTIVITY; ARTICLE; CELL FUNCTION; CELLULAR SECRETION; CROHN DISEASE; FLOW CYTOMETRY; GENETIC TRANSCRIPTION; INTESTINE FLORA; MASS SPECTROMETRY; NONHUMAN; PANETH CELL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; PROTEIN PROCESSING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RISK; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; GENETICS; HUMAN; INTESTINE; METABOLISM; MICROBIOLOGY; MICROFLORA; MOUSE; PHYSIOLOGY; BACTERIAL TRANSLOCATION; BACTERICIDAL ACTIVITY; EXOCYTOSIS; GENE DELETION; IMMUNOGOLD STAINING; LASER CAPTURE MICRODISSECTION; MRNA EXPRESSION ASSAY; RISK FACTOR; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SECRETORY GRANULE;

ANIMALS; DEFENSINS; HUMANS; INTESTINES; MICE; MICROBIOTA; NOD2 SIGNALING ADAPTOR PROTEIN; PANETH CELLS;

EID: 84899424851     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/gmic.27466     Document Type: Article

References (48)

1. Ouellette AJ. Paneth cell α-defensins in enteric innate immunity. Cell Mol Life Sci 2011; 68: 2215-29; PMID: 21560070; http://dx. doi. org/10. 1007/s00018-011-0714-6.
2. Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, Ouellette AJ. Secretion of microbicidal alpha-defensins by intestinal Paneth cells in response to bacteria. Nat Immunol 2000; 1: 113-8; PMID: 11248802; http://dx. doi. org/10. 1038/77783.
3. Wang G, Li X, Wang Z. APD2: the updated antimicrobial peptide database and its application in peptide design. Nucleic Acids Res 2009; 37: D933-7; PMID: 18957441; http://dx. doi. org/10. 1093/nar/gkn823.
4. Bevins CL, Salzman NH. Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat Rev Microbiol 2011; 9: 356-68; PMID: 21423246; http://dx. doi. org/10. 1038/nrmicro2546.
5. Wilson CL, Ouellette AJ, Satchell DP, Ayabe T, López-Boado YS, Stratman JL, Hultgren SJ, Matrisian LM, Parks WC. Regulation of intestinal alpha-defensin activation by the metalloproteinase matrilysin in innate host defense. Science 1999; 286: 113-7; PMID: 10506557; http://dx. doi. org/10. 1126/science. 286. 5437. 113.
6. Salzman NH, Hung K, Haribhai D, Chu H, Karlsson-Sjöberg J, Amir E, Teggatz P, Barman M, Hayward M, Eastwood D, et al. Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 2010; 11: 76-83; PMID: 19855381; http://dx. doi. org/10. 1038/ni. 1825.
7. Shanahan MT, Carroll IM, Grossniklaus E, White A, von Furstenberg RJ, Barner R, Fodor AA, Henning SJ, Sartor RB, Gulati AS. Mouse Paneth cell antimicrobial function is independent of Nod2. Gut 2013; PMID: 23512834; http://dx. doi. org/10. 1136/gutjnl-2012-304190.
8. Vaishnava S, Behrendt CL, Ismail AS, Eckmann L, Hooper LV. Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc Natl Acad Sci U S A 2008; 105: 20858-63; PMID: 19075245; http://dx. doi. org/10. 1073/pnas. 0808723105.
9. Cadwell K, Liu JY, Brown SL, Miyoshi H, Loh J, Lennerz JK, Kishi C, Kc W, Carrero JA, Hunt S, et al. A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 2008; 456: 259-63; PMID: 18849966; http://dx. doi. org/10. 1038/nature07416.
10. Gulati AS, Shanahan MT, Arthur JC, Grossniklaus E, von Furstenberg RJ, Kreuk L, Henning SJ, Jobin C, Sartor RB. Mouse background strain profoundly influences Paneth cell function and intestinal microbial composition. PLoS One 2012; 7: e32403; PMID: 22384242; http://dx. doi. org/10. 1371/journal. pone. 0032403.
11. Ouellette AJ. Paneth cells and innate mucosal immunity. Curr Opin Gastroenterol 2010; 26: 547-53; PMID: 20693892; http://dx. doi. org/10. 1097/MOG. 0b013e32833dccde.
12. Darmoul D, Ouellette AJ. Positional specificity of defensin gene expression reveals Paneth cell heterogeneity in mouse small intestine. Am J Physiol 1996; 271: G68-74; PMID: 8760109.
13. Karlsson J, Pütsep K, Chu H, Kays RJ, Bevins CL, Andersson M. Regional variations in Paneth cell antimicrobial peptide expression along the mouse intestinal tract. BMC Immunol 2008; 9: 37; PMID: 18637162; http://dx. doi. org/10. 1186/1471-2172-9-37.
14. Shirafuji Y, Tanabe H, Satchell DP, Henschen-Edman A, Wilson CL, Ouellette AJ. Structural determinants of procryptdin recognition and cleavage by matrix metalloproteinase-7. J Biol Chem 2003; 278: 7910-9; PMID: 12482850; http://dx. doi. org/10. 1074/jbc. M210600200.
15. Lehrer RI, Rosenman M, Harwig SS, Jackson R, Eisenhauer P. Ultrasensitive assays for endogenous antimicrobial polypeptides. J Immunol Methods 1991; 137: 167-73; PMID: 1901580; http://dx. doi. org/10. 1016/0022-1759(91)90021-7.
16. Satoh Y, Habara Y, Ono K, Kanno T. Carbamylcholine-and catecholamine-induced intracellular calcium dynamics of epithelial cells in mouse ileal crypts. Gastroenterology 1995; 108: 1345-56; PMID: 7729625; http://dx. doi. org/10. 1016/0016-5085(95)90681-9.
17. Ayabe T, Wulff H, Darmoul D, Cahalan MD, Chandy KG, Ouellette AJ. Modulation of mouse Paneth cell alpha-defensin secretion by mIKCa1, a Ca2+-activated, intermediate conductance potassium channel. J Biol Chem 2002; 277: 3793-800; PMID: 11724775; http://dx. doi. org/10. 1074/jbc. M107507200.
18. Meyer-Hoffert U, Hornef MW, Henriques-Normark B, Axelsson LG, Midtvedt T, Pütsep K, Andersson M. Secreted enteric antimicrobial activity localises to the mucus surface layer. Gut 2008; 57: 764-71; PMID: 18250125; http://dx. doi. org/10. 1136/gut. 2007. 141481.
19. Masuda K, Sakai N, Nakamura K, Yoshioka S, Ayabe T. Bactericidal activity of mouse α-defensin cryptdin-4 predominantly affects noncommensal bacteria. J Innate Immun 2011; 3: 315-26; PMID: 21099205; http://dx. doi. org/10. 1159/000322037.
20. Lehrer RI, Ganz T, Szklarek D, Selsted ME. Modulation of the in vitro candidacidal activity of human neutrophil defensins by target cell metabolism and divalent cations. J Clin Invest 1988; 81: 1829-35; PMID: 3290255; http://dx. doi. org/10. 1172/JCI113527.
21. De Lisle RC. Altered transit and bacterial overgrowth in the cystic fibrosis mouse small intestine. Am J Physiol Gastrointest Liver Physiol 2007; 293: G104-11; PMID: 17363465; http://dx. doi. org/10. 1152/ajpgi. 00548. 2006.
22. Sartor RB. Microbial influences in inflammatory bowel diseases. Gastroenterology 2008; 134: 577-94; PMID: 18242222; http://dx. doi. org/10. 1053/j. gastro. 2007. 11. 059.
23. Keshav S. Paneth cells: leukocyte-like mediators of innate immunity in the intestine. J Leukoc Biol 2006; 80: 500-8; PMID: 16793911; http://dx. doi. org/10. 1189/jlb. 1005556.
24. van Es JH, Jay P, Gregorieff A, van Gijn ME, Jonkheer S, Hatzis P, Thiele A, van den Born M, Begthel H, Brabletz T, et al. Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat Cell Biol 2005; 7: 381-6; PMID: 15778706; http://dx. doi. org/10. 1038/ncb1240.
25. Koslowski MJ, Kübler I, Chamaillard M, Schaeffeler E, Reinisch W, Wang G, Beisner J, Teml A, Peyrin-Biroulet L, Winter S, et al. Genetic variants of Wnt transcription factor TCF-4 (TCF7L2) putative promoter region are associated with small intestinal Crohn's disease. PLoS One 2009; 4: e4496; PMID: 19221600; http://dx. doi. org/10. 1371/journal. pone. 0004496.
26. Wehkamp J, Wang G, Kübler I, Nuding S, Gregorieff A, Schnabel A, Kays RJ, Fellermann K, Burk O, Schwab M, et al. The Paneth cell alpha-defensin deficiency of ileal Crohn's disease is linked to Wnt/Tcf-4. J Immunol 2007; 179: 3109-18; PMID: 17709525.
27. Wehkamp J, Harder J, Weichenthal M, Schwab M, Schäffeler E, Schlee M, Herrlinger KR, Stallmach A, Noack F, Fritz P, et al. NOD2 (CARD15) mutations in Crohn's disease are associated with diminished mucosal alpha-defensin expression. Gut 2004; 53: 1658-64; PMID: 15479689; http://dx. doi. org/10. 1136/gut. 2003. 032805.
28. Kaser A, Lee AH, Franke A, Glickman JN, Zeissig S, Tilg H, Nieuwenhuis EE, Higgins DE, Schreiber S, Glimcher LH, et al. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 2008; 134: 743-56; PMID: 18775308; http://dx. doi. org/10. 1016/j. cell. 2008. 07. 021.
29. Simms LA, Doecke JD, Roberts RL, Fowler EV, Zhao ZZ, McGuckin MA, Huang N, Hayward NK, Webb PM, Whiteman DC, et al. KCNN4 gene variant is associated with ileal Crohn's Disease in the Australian and New Zealand population. Am J Gastroenterol 2010; 105: 2209-17; PMID: 20407432; http://dx. doi. org/10. 1038/ajg. 2010. 161.
30. Zheng W, Rosenstiel P, Huse K, Sina C, Valentonyte R, Mah N, Zeitlmann L, Grosse J, Ruf N, Nürnberg P, et al. Evaluation of AGR2 and AGR3 as candidate genes for inflammatory bowel disease. Genes Immun 2006; 7: 11-8; PMID: 16222343; http://dx. doi. org/10. 1038/sj. gene. 6364263.
31. Liu B, Gulati AS, Cantillana V, Henry SC, Schmidt EA, Daniell X, Grossniklaus E, Schoenborn AA, Sartor RB, Taylor GA. Irgm1-deficient mice exhibit Paneth cell abnormalities and increased susceptibility to acute intestinal inflammation. Am J Physiol Gastrointest Liver Physiol 2013; 305: G573-84; PMID: 23989005; http://dx. doi. org/10. 1152/ajpgi. 00071. 2013.
32. Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY, Lee JC, Schumm LP, Sharma Y, Anderson CA, et al.; International IBD Genetics Consortium (IIBDGC). Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 2012; 491: 119-24; PMID: 23128233; http://dx. doi. org/10. 1038/nature11582.
33. Ogura Y, Lala S, Xin W, Smith E, Dowds TA, Chen FF, Zimmermann E, Tretiakova M, Cho JH, Hart J, et al. Expression of NOD2 in Paneth cells: a possible link to Crohn's ileitis. Gut 2003; 52: 1591-7; PMID: 14570728; http://dx. doi. org/10. 1136/gut. 52. 11. 1591.
34. Simms LA, Doecke JD, Walsh MD, Huang N, Fowler EV, Radford-Smith GL. Reduced alpha-defensin expression is associated with inflammation and not NOD2 mutation status in ileal Crohn's disease. Gut 2008; 57: 903-10; PMID: 18305068; http://dx. doi. org/10. 1136/gut. 2007. 142588.
35. Kobayashi KS, Chamaillard M, Ogura Y, Henegariu O, Inohara N, Nuñez G, Flavell RA. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 2005; 307: 731-4; PMID: 15692051; http://dx. doi. org/10. 1126/science. 1104911.
36. Petnicki-Ocwieja T, Hrncir T, Liu YJ, Biswas A, Hudcovic T, Tlaskalova-Hogenova H, Kobayashi KS. Nod2 is required for the regulation of commensal microbiota in the intestine. Proc Natl Acad Sci U S A 2009; 106: 15813-8; PMID: 19805227; http://dx. doi. org/10. 1073/pnas. 0907722106.
37. Ouellette AJ, Pravtcheva D, Ruddle FH, James M. Localization of the cryptdin locus on mouse chromosome 8. Genomics 1989; 5: 233-9; PMID: 2571573; http://dx. doi. org/10. 1016/0888-7543(89)90051-7.
38. Shanahan MT, Tanabe H, Ouellette AJ. Strain-specific polymorphisms in Paneth cell α-defensins of C57BL/6 mice and evidence of vestigial myeloid α-defensin pseudogenes. Infect Immun 2011; 79: 459-73; PMID: 21041494; http://dx. doi. org/10. 1128/IAI. 00996-10.
39. Rehman A, Sina C, Gavrilova O, Häsler R, Ott S, Baines JF, Schreiber S, Rosenstiel P. Nod2 is essential for temporal development of intestinal microbial communities. Gut 2011; 60: 1354-62; PMID: 21421666; http://dx. doi. org/10. 1136/gut. 2010. 216259.
40. Mondot S, Barreau F, Al Nabhani Z, Dussaillant M, Le Roux K, Doré J, Leclerc M, Hugot JP, Lepage P. Altered gut microbiota composition in immune-impaired Nod2(-/-) mice. Gut 2012; 61: 634-5; PMID: 21868489; http://dx. doi. org/10. 1136/gutjnl-2011-300478.
41. Couturier-Maillard A, Secher T, Rehman A, Normand S, De Arcangelis A, Haesler R, Huot L, Grandjean T, Bressenot A, Delanoye-Crespin A, et al. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J Clin Invest 2013; 123: 700-11; PMID: 23281400.
42. Robertson SJ, Zhou JY, Geddes K, Rubino SJ, Cho JH, Girardin SE, Philpott DJ. Nod1 and Nod2 signaling does not alter the composition of intestinal bacterial communities at homeostasis. Gut Microbes 2013; 4: 222-31; PMID: 23549220; http://dx. doi. org/10. 4161/gmic. 24373.
43. Ubeda C, Lipuma L, Gobourne A, Viale A, Leiner I, Equinda M, Khanin R, Pamer EG. Familial transmission rather than defective innate immunity shapes the distinct intestinal microbiota of TLR-deficient mice. J Exp Med 2012; 209: 1445-56; PMID: 22826298; http://dx. doi. org/10. 1084/jem. 20120504.
44. Friswell MK, Gika H, Stratford IJ, Theodoridis G, Telfer B, Wilson ID, McBain AJ. Site and strain-specific variation in gut microbiota profiles and metabolism in experimental mice. PLoS One 2010; 5: e8584; PMID: 20052418; http://dx. doi. org/10. 1371/journal. pone. 0008584.
45. rd, Erb-Downward JR, Bassis CM, Shen MC, Toews GB, Young VB, Huffnagle GB. Ecological succession of bacterial communities during conventionalization of germ-free mice. Appl Environ Microbiol 2012; 78: 2359-66; PMID: 22286988; http://dx. doi. org/10. 1128/AEM. 05239-11.
46. McCafferty J, Mühlbauer M, Gharaibeh RZ, Arthur JC, Perez-Chanona E, Sha W, Jobin C, Fodor AA. Stochastic changes over time and not founder effects drive cage effects in microbial community assembly in a mouse model. ISME J 2013; 7: 2116-25; PMID: 23823492; http://dx. doi. org/10. 1038/ismej. 2013. 106.
47. Van Limbergen J, Geddes K, Henderson P, Russell RK, Drummond HE, Satsangi J, Griffiths AM, Philpott DJ, Wilson DC. Paneth cell marker CD24 in NOD2 knockout organoids and in inflammatory bowel disease (IBD). Gut 2013; PMID: 23704317; http://dx. doi. org/10. 1136/gutjnl-2013-305077.
48. Adolph TE, Tomczak MF, Niederreiter L, Ko HJ, Böck J, Martinez-Naves E, Glickman JN, Tschurtschenthaler M, Hartwig J, Hosomi S, et al. Paneth cells as a site of origin for intestinal inflammation. Nature 2013; 503: 272-6; PMID: 24089213.