Disordered macrophage cytokine secretion underlies impaired acute inflammation and bacterial clearance in Crohn's disease

Journal of Experimental Medicine

Volumn 206, Issue 9, 2009, Pages 1883-1897

  Smith, Andrew M ^a   Rahman, Farooq Z ^a   Hayee, Bu'Hussain ^a   Graham, Simon J ^b   Marks, Daniel J B ^a   Sewell, Gavin W ^a   Palmer, Christine D ^a   Wilde, Jonathan ^b   Foxwell, Brian M J ^c   Gloger, Israel S ^b   Sweeting, Trevor ^a   Marsh, Mark ^a   Walker, Ann P ^a   Bloom, Stuart L ^d   Segal, Anthony W ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b GLAXOSMITHKLINE   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON HOSPITALS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INDIUM 111; MESSENGER RNA; PHOSPHORUS 32; TOLL LIKE RECEPTOR AGONIST; TUMOR NECROSIS FACTOR;

ARTICLE; BLOOD FLOW; CELL LABELING; CHRONICITY; CLINICAL ARTICLE; CONTROLLED STUDY; CROHN DISEASE; CYTOKINE RELEASE; ESCHERICHIA COLI; FOREARM; GENE EXPRESSION; GENETIC TRANSCRIPTION; GRANULOMA; HUMAN; INFECTION RESISTANCE; INFLAMMATION; INTESTINE; ISOTOPE LABELING; LYSOSOME; MACROPHAGE; NEUTROPHIL; PRIORITY JOURNAL; PROTEIN DEGRADATION;

ADULT; AGED; CROHN DISEASE; CYTOKINES; ESCHERICHIA COLI; FEMALE; GENE EXPRESSION PROFILING; HUMANS; INDIUM RADIOISOTOPES; LINEAR MODELS; MACROPHAGES; MALE; MIDDLE AGED; NEUTROPHILS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORUS RADIOISOTOPES; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA;

EID: 69449105914     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20091233     Document Type: Article

References (63)

1. Aggarwal, B.B., W.J. Kohr, P.E. Hass, B. Moffat, S.A. Spencer, W.J. Henzel, T.S. Bringman, G.E. Nedwin, D.V. Goeddel, and R.N. Harkins. 1985. Human tumor necrosis factor. Production, purification, and characterization. J. Biol. Chem. 260:2345-2354. (Pubitemid 15104839)
2. Ambrose, N.S., J. Alexander-Williams, and M.R. Keighley. 1984a. Audit of sepsis in operations for inflammatory bowel disease. Dis. Colon Rectum. 27:602-604. (Pubitemid 14028633)
3. Ambrose, N.S., M. Johnson, D.W. Burdon, and M.R. Keighley. 1984b. Incidence of pathogenic bacteria from mesenteric lymph nodes and ileal serosa during Crohn's disease surgery. Br. J. Surg. 71:623-625.
4. Barrett, J.C., S. Hansoul, D.L. Nicolae, J.H. Cho, R.H. Duerr, J.D. Rioux, S.R. Brant, M.S. Silverberg, K.D. Taylor, M.M. Barmada, et al; NIDDK IBD Genetics Consortium; Belgian-French IBD Consortium; Wellcome Trust Case Control Consortium. 2008. Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease. Nat. Genet. 40:955-962.
5. Bazzoni, F., and B. Beutler. 1996. The tumor necrosis factor ligand and receptor families. N. Engl. J. Med. 334:1717-1725. (Pubitemid 26193625)
6. Benjamini, Y., and Y. Hochberg. 1995. Controlling the false discovery rate - a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B. 57:289-300.
7. Burczynski, M.E., R.L. Peterson, N.C. Twine, K.A. Zuberek, B.J. Brodeur, L. Casciotti, V. Maganti, P.S. Reddy, A. Strahs, F. Immermann, et al. 2006. Molecular classification of Crohn's disease and ulcerative colitis patients using transcriptional profiles in peripheral blood mononuclear cells. J. Mol. Diagn. 8:51-61.
8. Cadwell, K., J.Y. Liu, S.L. Brown, H. Miyoshi, J. Loh, J.K. Lennerz, C. Kishi, W. Kc, J.A. Carrero, S. Hunt, et al. 2008. A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature. 456:259-263.
9. Cameron, J.L., S.R. Hamilton, J. Coleman, J.V. Sitzmann, and T.M. Bayless. 1992. Patterns of ileal recurrence in Crohn's disease. A prospective randomized study. Ann. Surg. 215:546-551, discussion :551-552.
10. Cartwright, G.E., J.W. Athens, and M.M. Wintrobe. 1964. The kinetics of granulopoiesis in normal man. Blood. 24:780-803.
11. Castronovo, F.P. Jr., K.A. McKusick, and H.W. Strauss. 1988. The infiltrated radiopharmaceutical injection: dosimetric considerations. Eur. J. Nucl. Med. 14:93-97.
12. Charach, G., I. Grosskopf, and M. Weintraub. 2008. Development of Crohn's disease in a patient with multiple sclerosis treated with copaxone. Digestion. 77:198-200.
13. Costello, C.M., N. Mah, R. Häsler, P. Rosenstiel, G.H. Waetzig, A. Hahn, T. Lu, Y. Gurbuz, S. Nikolaus, M. Albrecht, et al. 2005. Dissection of the inflammatory bowel disease transcriptome using genomewide cDNA microarrays. PLoS Med. 2:e199.
14. Cuthbert, A.P., S.A. Fisher, M.M. Mirza, K. King, J. Hampe, P.J. Croucher, S. Mascheretti, J. Sanderson, A. Forbes, J. Mansfield, et al. 2002. The contribution of NOD2 gene mutations to the risk and site of disease in inflammatory bowel disease. Gastroenterology. 122:867-874.
15. Donnelly, P. 2008. Progress and challenges in genome-wide association studies in humans. Nature. 456:728-731.
16. Ephgrave, K. 2007. Extra-intestinal manifestations of Crohn's disease. Surg. Clin. North Am. 87:673-680.
17. Farthing, M.J. 2004. Bugs and the gut: an unstable marriage. Best Pract. Res. Clin. Gastroenterol. 18:233-239.
18. Finegold, S.M. 1969. Intestinal bacteria. The role they play in normal physiology, pathologic physiology, and infection. Calif. Med. 110:455-459.
19. Fujishima, S., A.R. Hoffman, T. Vu, K.J. Kim, H. Zheng, D. Daniel, Y. Kim, E.F. Wallace, J.W. Larrick, and T.A. Raffin. 1993. Regulation of neutrophil interleukin 8 gene expression and protein secretion by LPS, TNF-alpha, and IL-1 beta. J. Cell. Physiol. 154:478-485. (Pubitemid 23076315)
20. Greten, F.R., M.C. Arkan, J. Bollrath, L.C. Hsu, J. Goode, C. Miething, S.I. Göktuna, M. Neuenhahn, J. Fierer, S. Paxian, et al. 2007. NF-kappaB is a negative regulator of IL-1beta secretion as revealed by genetic and pharmacological inhibition of IKKbeta. Cell. 130:918-931.
21. Hampe, J., A. Franke, P. Rosenstiel, A. Till, M. Teuber, K. Huse, M. Albrecht, G. Mayr, F.M. De La Vega, J. Briggs, et al. 2007. A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat. Genet. 39:207-211. (Pubitemid 46184351)
22. Harvey, R.F., and J.M. Bradshaw. 1980. A simple index of Crohn'sdisease activity. Lancet. 315:514.
23. Heber, S., and B. Sick. 2006. Quality assessment of Affymetrix GeneChip data. OMICS. 10:358-368. (Pubitemid 44736320)
24. Horwood, N.J., T. Mahon, J.P. McDaid, J. Campbell, H. Mano, F.M. Brennan, D. Webster, and B.M. Foxwell. 2003. Bruton's tyrosine kinase is required for lipopolysaccharide-induced tumor necrosis factor α production. J. Exp. Med. 197:1603-1611. (Pubitemid 36745336)
25. Hughes, A.L. 2005. Consistent across-tissue signatures of differential gene expression in Crohn's disease. Immunogenetics. 57:709-716. (Pubitemid 41598617)
26. Hugot, J.P., M. Chamaillard, H. Zouali, S. Lesage, J.P. Cézard, J. Belaiche, S. Almer, C. Tysk, C.A. O'Morain, M. Gassull, et al. 2001. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature. 411:599-603. (Pubitemid 32531408)
27. Hugot, J.P., I. Zaccaria, J. Cavanaugh, H. Yang, S. Vermeire, M. Lappalainen, S. Schreiber, V. Annese, D.P. Jewell, E.V. Fowler, et al; for the IBD International Genetics Consortium. 2007. Prevalence of CARD15/NOD2 mutations in Caucasian healthy people. Am. J. Gastroenterol. 102:1259-1267.
28. Issekutz, T.B., A.C. Issekutz, and H.Z. Movat. 1981. The in vivo quantitation and kinetics of monocyte migration into acute inflammatory tissue. Am. J. Pathol. 103:47-55.
29. Jordan, B. 1970. Use of 33P as an indicator for 32P pulse labeling of nucleic acids in bacterial cultures. J. Bacteriol. 101:657-658.
30. Kaplan, G.G., B.V. Pedersen, R.E. Andersson, B.E. Sands, J. Korzenik, and M. Frisch. 2007. The risk of developing Crohn's disease after an appendectomy: a population-based cohort study in Sweden and Denmark. Gut. 56:1387-1392.
31. Kyle, J. 1980. Urinary complications of Crohn's disease. World J. Surg. 4:153-160.
32. Lawrance, I.C., C. Fiocchi, and S. Chakravarti. 2001. Ulcerative colitis and Crohn's disease: distinctive gene expression profiles and novel susceptibility candidate genes. Hum. Mol. Genet. 10:445-456.
33. Levine, B., and V. Deretic. 2007. Unveiling the roles of autophagy in innate and adaptive immunity. Nat. Rev. Immunol. 7:767-777. (Pubitemid 47480305)
34. Li, Y., A. Karlin, J.D. Loike, and S.C. Silverstein. 2004. Determination of the critical concentration of neutrophils required to block bacterial growth in tissues. J. Exp. Med. 200:613-622. (Pubitemid 39258310)
35. Liu, Y., H.J. van Kruiningen, A.B. West, R.W. Cartun, A. Cortot, and J.F. Colombel. 1995. Immunocytochemical evidence of Listeria, Escherichia coli, and Streptococcus antigens in Crohn's disease. Gastroenterology. 108:1396-1404.
36. Maher, B. 2008. Personal genomes: The case of the missing heritability. Nature. 456:18-21.
37. Malbert, C.H. 2005. The ileocolonic sphincter. Neurogastroenterol. Motil. 17:41-49.
38. Mannick, E.E., J.C. Bonomolo, R. Horswell, J.J. Lentz, M.S. Serrano, A. Zapata-Velandia, M. Gastanaduy, J.L. Himel, S.L. Rose, J.N. Udall Jr., et al. 2004. Gene expression in mononuclear cells from patients with inflammatory bowel disease. Clin. Immunol. 112:247-257. (Pubitemid 39078700)
39. Marks, D.J., and A.W. Segal. 2008. Innate immunity in inflammatory bowel disease: a disease hypothesis. J. Pathol. 214:260-266. (Pubitemid 351160162)
40. Marks, D.J., M.W. Harbord, R. MacAllister, F.Z. Rahman, J. Young, B. Al-Lazikani, W. Lees, M. Novelli, S. Bloom, and A.W. Segal. 2006. Defective acute inflammation in Crohn's disease: a clinical investigation. Lancet. 367:668-678.
41. Meconi, S., A. Vercellone, F. Levillain, B. Payré, T. Al Saati, F. Capilla, P. Desreumaux, A. Darfeuille-Michaud, and F. Altare. 2007. Adherent-invasive Escherichia coli isolated from Crohn's disease patients induce granulomas in vitro. Cell. Microbiol. 9:1252-1261. (Pubitemid 46547142)
42. Medzhitov, R. 2008. Origin and physiological roles of inflammation. Nature. 454:428-435.
43. Mitchell, D.N. 1971. The Kveim test in Crohn's disease. Proc. R. Soc. Med. 64:164-166.
44. Moráin, C.O., A.A. Segal, D. Walker, and A.J. Levi. 1981. Abnormalities of neutrophil function do not cause the migration defect in Crohn's disease. Gut. 22:817-822.
45. Naito, Y., T. Takagi, O. Handa, T. Ishikawa, S. Nakagawa, T. Yamaguchi, N. Yoshida, M. Minami, M. Kita, J. Imanishi, and T. Yoshikawa. 2003. Enhanced intestinal inflammation induced by dextran sulfate sodium in tumor necrosis factor-alpha deficient mice. J. Gastroenterol. Hepatol. 18:560-569. (Pubitemid 36645291)
46. Ogura, Y., D.K. Bonen, N. Inohara, D.L. Nicolae, F.F. Chen, R. Ramos, H. Britton, T. Moran, R. Karaliuskas, R.H. Duerr, et al. 2001. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature. 411:603-606. (Pubitemid 32531409)
47. Palmer, C.D., B.E. Mutch, S. Workman, J.P. McDaid, N.J. Horwood, and B.M. Foxwell. 2008. Bmx tyrosine kinase regulates TLR4-induced IL-6 production in human macrophages independently of p38 MAPK and NFkappB activity. Blood. 111:1781-1788.
48. Parkes, M., J.C. Barrett, N.J. Prescott, M. Tremelling, C.A. Anderson, S.A. Fisher, R.G. Roberts, E.R. Nimmo, F.R. Cummings, D. Soars, et al; Wellcome Trust Case Control Consortium. 2007. Sequence variants in the autophagy gene IRGM and multiple other replicating loci contribute to Crohn's disease susceptibility. Nat. Genet. 39:830-832.
49. Rahman, F.Z., D.J. Marks, B.H. Hayee, A.M. Smith, S.L. Bloom, and A.W. Segal. 2008. Phagocyte dysfunction and inflammatory bowel disease. Inflamm. Bowel Dis. 14:1443-1452.
50. Rhodes, J.M. 2007. The role of Escherichia coli in inflammatory bowel disease. Gut. 56:610-612. (Pubitemid 46662923)
51. Rioux, J.D., R.J. Xavier, K.D. Taylor, M.S. Silverberg, P. Goyette, A. Huett, T. Green, P. Kuballa, M.M. Barmada, L.W. Datta, et al. 2007. Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat. Genet. 39:596-604.
52. Ryan, P., R.G. Kelly, G. Lee, J.K. Collins, G.C. O'Sullivan, J. O'Connell, and F. Shanahan. 2004. Bacterial DNA within granulomas of patients with Crohn's disease - detection by laser capture microdissection and PCR. Am. J. Gastroenterol. 99:1539-1543. (Pubitemid 39180104)
53. Schroeder, K.W., W.J. Tremaine, and D.M. Ilstrup. 1987. Coated oral 5-aminosalicylic acid therapy for mildly to moderately active ulcerative colitis. A randomized study. N. Engl. J. Med. 317:1625-1629.
54. Segal, A.W., and G. Loewi. 1976. Neutrophil dysfunction in Crohn's disease. Lancet. 308:219-221.
55. Segal, A.W., J. Ensell, J.M. Munro, and M. Sarner. 1981. Indium-111 tagged leucocytes in the diagnosis of inflammatory bowel disease. Lancet. 318:230-232. (Pubitemid 11095448)
56. Smythies, L.E., A. Maheshwari, R. Clements, D. Eckhoff, L. Novak, H.L. Vu, L.M. Mosteller-Barnum, M. Sellers, and P.D. Smith. 2006. Mucosal IL-8 and TGF-beta recruit blood monocytes: evidence for cross-talk between the lamina propria stroma and myeloid cells. J. Leukoc. Biol. 80:492-499.
57. Stabin, M.G. 1996. MIRDOSE: personal computer software for internal dose assessment in nuclear medicine. J. Nucl. Med. 37:538-546.
58. van Deventer, S.J. 1999. Review article: targeting TNF alpha as a key cytokine in the inflammatory processes of Crohn's disease - the mechanisms of action of infliximab. Aliment. Pharmacol. Ther. 13:3-8.
59. Wellcome Trust Case Control Consortium. 2007. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature. 447:661-678.
60. Wong, M., D. Ziring, Y. Korin, S. Desai, S. Kim, J. Lin, D. Gjertson, J. Braun, E. Reed, and R.R. Singh. 2008. TNFalpha blockade in human diseases: mechanisms and future directions. Clin. Immunol. 126:121-136.
61. Xavier, R.J., and D.K. Podolsky. 2007. Unravelling the pathogenesis of inflammatory bowel disease. Nature. 448:427-434. (Pubitemid 47123518)
62. Yazisiz, V., A.B. Avci, F. Erbasan, B. Yildirim, and E. Terzioǧlu. 2008. Development of Crohn's disease following anti-tumour necrosis factor therapy (etanercept). Colorectal Dis. 10:953-954.
63. Yourassowsky, E., M.P. Van der Linden, and F. Crokaert. 1989. Correlation between growth curves and killing curves of Escherichia coli in the presence of fleroxacin and ampicillin. Chemotherapy. 35:423-430. (Pubitemid 20019243)