Genome-wide expression profiling identifies an impairment of negative feedback signals in the Crohn's disease-associated NOD2 variant L1007fsinsC

Journal of Immunology

Volumn 186, Issue 7, 2011, Pages 4027-4038

  Billmann Born, Susanne ^a   Till, Andreas ^a   Arlt, Alexander ^b   Lipinski, Simone ^a   Sina, Christian ^a,b   Latiano, Anna ^c   Annese, Vito ^c   Häsler, Robert ^a   Kerick, Martin ^a   Manke, Thomas ^d   Seegert, Dirk ^e   Hanidu, Adedayo ^f   Schäfer, Heiner ^b   Van Heel, David ^g   Li, Jun ^f   Schreiber, Stefan ^a,b   Rosenstiel, Philip ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^c CASA SOLLIEVO DELLA SOFFERENZA HOSPITAL   (Italy)

^d MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^e Boehringer Ingelheim Pharmaceuticals ^*  (Germany)

^f BOEHRINGER INGELHEIM PHARMACEUTICALS INC   (United States)

^g QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; CHEMOKINE; CYSTEINE; GROWTH FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LEUCINE; MURAMYL DIPEPTIDE;

ANIMAL CELL; ARTICLE; CELL INVASION; CELL STRAIN HEK293; CONTROLLED STUDY; CROHN DISEASE; ENZYME ACTIVATION; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GENOTYPE; HUMAN; HUMAN CELL; MONOCYTE; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN VARIANT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS; UNINDEXED SEQUENCE; UPREGULATION; WILD TYPE;

ANIMALS; CELL LINE, TUMOR; CELLS, CULTURED; CROHN DISEASE; DOWN-REGULATION; FRAMESHIFT MUTATION; GENE EXPRESSION PROFILING; GENOME, HUMAN; HEK293 CELLS; HELA CELLS; HUMANS; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOCYTES; NOD2 SIGNALING ADAPTOR PROTEIN;

EID: 79955018886     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000085     Document Type: Article

References (53)

1. Rosenstiel, P., G. Jacobs, A. Till, and S. Schreiber. 2008. NOD-like receptors: Ancient sentinels of the innate immune system. Cell. Mol. Life Sci. 65: 1361-1377.
2. Inohara, N., Y. Ogura, A. Fontalba, O. Gutierrez, F. Pons, J. Crespo, K. Fukase, S. Inamura, S. Kusumoto, M. Hashimoto, et al. 2003. Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn's disease. J. Biol. Chem. 278: 5509-5512. (Pubitemid 36800790)
3. Girardin, S. E., I. G. Boneca, J. Viala, M. Chamaillard, A. Labigne, G. Thomas, D. J. Philpott, and P. J. Sansonetti. 2003. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol. Chem. 278: 8869-8872. (Pubitemid 36800360)
4. 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)
5. 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)
6. Hampe, J., A. Cuthbert, P. J. Croucher, M. M. Mirza, S. Mascheretti, S. Fisher, H. Frenzel, K. King, A. Hasselmeyer, A. J. MacPherson, et al. 2001. Association between insertion mutation in NOD2 gene and Crohn's disease in German and British populations. Lancet 357: 1925-1928. (Pubitemid 32568333)
7. Inohara, N., T. Koseki, J. Lin, L. del Peso, P. C. Lucas, F. F. Chen, Y. Ogura, and G. Núñez. 2000. An induced proximity model for NF-kappa B activation in the Nod1/RICK and RIP signaling pathways. J. Biol. Chem. 275: 27823-27831.
8. Chamaillard, M., S. E. Girardin, J. Viala, and D. J. Philpott. 2003. Nods, Nalps and Naip: Intracellular regulators of bacterial-induced inflammation. Cell. Microbiol. 5: 581-592. (Pubitemid 37080669)
9. Rosenstiel, P., M. Fantini, K. Bräutigam, T. Kühbacher, G. H. Waetzig, D. Seegert, and S. Schreiber. 2003. TNF-alpha and IFN-gamma regulate the expression of the NOD2 (CARD15) gene in human intestinal epithelial cells. Gastroenterology 124: 1001-1009. (Pubitemid 36389803)
10. Voss, E., J. Wehkamp, K. Wehkamp, E. F. Stange, J. M. Schroder, and J. Harder. 2005. NOD2/CARD15 mediates induction of the antimicrobial peptide human beta-defensin-2. J. Biol. Chem. 30: 30.
11. Li, J., T. Moran, E. Swanson, C. Julian, J. Harris, D. K. Bonen, M. Hedl, D. L. Nicolae, C. Abraham, and J. H. Cho. 2004. Regulation of IL-8 and IL- 1beta expression in Crohn's disease associated NOD2/CARD15 mutations. Hum. Mol. Genet. 13: 1715-1725. (Pubitemid 39173441)
12. Rosenstiel, P., C. Sina, C. End, M. Renner, S. Lyer, A. Till, S. Hellmig, S. Nikolaus, U. R. Fölsch, B. Helmke, et al. 2007. Regulation of DMBT1 via NOD2 and TLR4 in intestinal epithelial cells modulates bacterial recognition and invasion. J. Immunol. 178: 8203-8211. (Pubitemid 46898093)
13. Kobayashi, K. S., M. Chamaillard, Y. Ogura, O. Henegariu, N. Inohara, G. Nuñez, and R. A. Flavell. 2005. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 307: 731-734. (Pubitemid 40194644)
14. Weichart, D., J. Gobom, S. Klopfleisch, R. Häsler, N. Gustavsson, S. Billmann, H. Lehrach, D. Seegert, S. Schreiber, and P. Rosenstiel. 2006. Analysis of NOD2-mediated proteome response to muramyl dipeptide in HEK293 cells. J. Biol. Chem. 281: 2380-2389. (Pubitemid 43845829)
15. Waetzig, G. H., P. Rosenstiel, A. Arlt, A. Till, K. Bräutigam, H. Schäfer, S. Rose- John, D. Seegert, and S. Schreiber. 2005. Soluble tumor necrosis factor (TNF) receptor-1 induces apoptosis via reverse TNF signaling and autocrine transforming growth factor-beta1. FASEB J. 19: 91-93. (Pubitemid 40069928)
16. Sebens Müerköster, S., A. V. Rausch, A. Isberner, J. Minkenberg, E. Blaszczuk, M. Witt, U. R. Fölsch, F. Schmitz, H. Schäfer, and A. Arlt. 2008. The apoptosisinducing effect of gastrin on colorectal cancer cells relates to an increased IEX-1 expression mediating NF-kappa B inhibition. Oncogene 27: 1122-1134. (Pubitemid 351253191)
17. Arlt, A., J. Minkenberg, B. Kocs, M. Grossmann, M. L. Kruse, U. R. Fölsch, and H. Schäfer. 2004. The expression of immediate early gene X-1 (IEX-1) is differentially induced by retinoic acids in NB4 and KG1 cells: Possible implication in the distinct phenotype of retinoic acid-responsive and -resistant leukemic cells. Leukemia 18: 1646-1655. (Pubitemid 39386343)
18. Robison, E. H., T. S. Mondala, A. R. Williams, S. R. Head, D. R. Salomon, and S. M. Kurian. 2009. Whole genome transcript profiling from fingerstick blood samples: A comparison and feasibility study. BMC Genomics 10: 617.
19. Eisen, M. B., P. T. Spellman, P. O. Brown, and D. Botstein. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 95: 14863-14868. (Pubitemid 29003722)
20. Gentleman, R. C., V. J. Carey, D. M. Bates, B. Bolstad, M. Dettling, S. Dudoit, B. Ellis, L. Gautier, Y. Ge, J. Gentry, et al. 2004. Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol. 5: R80.
21. Smyth, G. K. 2004. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3: Article3.
22. Kerr, M. K., M. Martin, and G. A. Churchill. 2000. Analysis of variance for gene expression microarray data. J. Comput. Biol. 7: 819-837.
23. Benjamini, Y., and Y. Hochberg. 1995. A practical and powerful approach to multiple testing. J. R. Stat. Soc. 57: 289-300.
24. Tavazoie, S., J. D. Hughes, M. J. Campbell, R. J. Cho, and G. M. Church. 1999. Systematic determination of genetic network architecture. Nat. Genet. 22: 281-285. (Pubitemid 29297256)
25. Manke, T., H. G. Roider, and M. Vingron. 2008. Statistical modeling of transcription factor binding affinities predicts regulatory interactions. PLOS Comput. Biol. 4: E1000039.
26. Olsen, C. H. 2003. Review of the use of statistics in infection and immunity. Infect. Immun. 71: 6689-6692. (Pubitemid 37475294)
27. Waetzig, G. H., D. Seegert, P. Rosenstiel, S. Nikolaus, and S. Schreiber. 2002. p38 mitogen-activated protein kinase is activated and linked to TNF-alpha signaling in inflammatory bowel disease. J. Immunol. 168: 5342-5351. (Pubitemid 34496003)
28. Till, A., P. Rosenstiel, A. Krippner-Heidenreich, S. Mascheretti- Croucher, P. J. Croucher, H. Schäfer, P. Scheurich, D. Seegert, and S. Schreiber. 2005. The Met-196 -. Arg variation of human tumor necrosis factor receptor 2 (TNFR2) affects TNF-alpha-induced apoptosis by impaired NF-kappaB signaling and target gene expression. J. Biol. Chem. 280: 5994-6004. (Pubitemid 40280083)
29. Ogura, Y., N. Inohara, A. Benito, F. F. Chen, S. Yamaoka, and G. Nunez. 2001. Nod2, a Nod1/Apaf-1 family member that is restricted to monocytes and activates NF-kappaB. J. Biol. Chem. 276: 4812-4818.
30. Hisamatsu, T., M. Suzuki, H. C. Reinecker, W. J. Nadeau, B. A. McCormick, and D. K. Podolsky. 2003. CARD15/NOD2 functions as an antibacterial factor in human intestinal epithelial cells. Gastroenterology 124: 993-1000. (Pubitemid 36389802)
31. Hitotsumatsu, O., R. C. Ahmad, R. Tavares, M. Wang, D. Philpott, E. E. Turer, B. L. Lee, N. Shiffin, R. Advincula, B. A. Malynn, et al. 2008. The ubiquitinediting enzyme A20 restricts nucleotide-binding oligomerization domain containing 2-triggered signals. Immunity 28: 381-390. (Pubitemid 351343859)
32. Kim, Y. G., J. H. Park, S. Daignault, K. Fukase, and G. Núñez. 2008. Crosstolerization between Nod1 and Nod2 signaling results in reduced refractoriness to bacterial infection in Nod2-deficient macrophages. J. Immunol. 181: 4340-4346.
33. Herskovits, A. A., V. Auerbuch, and D. A. Portnoy. 2007. Bacterial ligands generated in a phagosome are targets of the cytosolic innate immune system. PLoS Pathog. 3: E51.
34. Arlt, A., P. Rosenstiel, M. L. Kruse, F. Grohmann, J. Minkenberg, N. D. Perkins, U. R. Fölsch, S. Schreiber, and H. Schäfer. 2008. IEX-1 directly interferes with RelA/p65 dependent transactivation and regulation of apoptosis. Biochim. Biophys. Acta 1783: 941-952.
35. Till, A., P. Rosenstiel, K. Bräutigam, C. Sina, G. Jacobs, H. H. Oberg, D. Seegert, T. Chakraborty, and S. Schreiber. 2008. A role for membrane-bound CD147 in NOD2-mediated recognition of bacterial cytoinvasion. J. Cell Sci. 121: 487-495. (Pubitemid 351405057)
36. Maeda, S., L. C. Hsu, H. Liu, L. A. Bankston, M. Iimura, M. F. Kagnoff, L. Eckmann, and M. Karin. 2005. Nod2 mutation in Crohn's disease potentiates NF-kappaB activity and IL-1beta processing. Science 307: 734-738. (Pubitemid 40194645)
37. Rogler, G., K. Brand, D. Vogl, S. Page, R. Hofmeister, T. Andus, R. Knuechel, P. A. Baeuerle, J. Schölmerich, and V. Gross. 1998. Nuclear factor kappaB is activated in macrophages and epithelial cells of inflamed intestinal mucosa. Gastroenterology 115: 357-369. (Pubitemid 28363428)
38. Schreiber, S., S. Nikolaus, and J. Hampe. 1998. Activation of nuclear factor kappa B inflammatory bowel disease. Gut 42: 477-484. (Pubitemid 28186562)
39. Viatour, P., S. Legrand-Poels, C. van Lint, M. Warnier, M. P. Merville, J. Gielen, J. Piette, V. Bours, and A. Chariot. 2003. Cytoplasmic IkappaBalpha increases NF-kappaB-independent transcription through binding to histone deacetylase (HDAC) 1 and HDAC3. J. Biol. Chem. 278: 46541-46548. (Pubitemid 37452227)
40. Eliopoulos, A. G., C. D. Dumitru, C. C. Wang, J. Cho, and P. N. Tsichlis. 2002. Induction of COX-2 by LPS in macrophages is regulated by Tpl2-dependent CREB activation signals. EMBO J. 21: 4831-4840.
41. Banerjee, A., R. Gugasyan, M. McMahon, and S. Gerondakis. 2006. Diverse Toll-like receptors utilize Tpl2 to activate extracellular signal-regulated kinase (ERK) in hemopoietic cells. Proc. Natl. Acad. Sci. USA 103: 3274-3279. (Pubitemid 43346460)
42. Cho, J., M. Melnick, G. P. Solidakis, and P. N. Tsichlis. 2005. Tpl2 (tumor progression locus 2) phosphorylation at Thr290 is induced by lipopolysaccharide via an Ikappa-B Kinase-beta-dependent pathway and is required for Tpl2 activation by external signals. J. Biol. Chem. 280: 20442-20448. (Pubitemid 40776743)
43. Arlt, A., J. Minkenberg, M. L. Kruse, F. Grohmann, U. R. Fölsch, and H. Schäfer. 2007. Immediate early gene-X1 interferes with 26 S proteasome activity by attenuating expression of the 19 S proteasomal components S5a/ Rpn10 and S1/Rpn2. Biochem. J. 402: 367-375. (Pubitemid 46383434)
44. Onose, A., S. Hashimoto, S. Hayashi, S. Maruoka, F. Kumasawa, K. Mizumura, I. Jibiki, K. Matsumoto, Y. Gon, T. Kobayashi, et al. 2006. An inhibitory effect of A20 on NF-kappaB activation in airway epithelium upon influenza virus infection. Eur. J. Pharmacol. 541: 198-204. (Pubitemid 43903479)
45. Lee, E. G., D. L. Boone, S. Chai, S. L. Libby, M. Chien, J. P. Lodolce, and A. Ma. 2000. Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science 289: 2350-2354.
46. Vereecke, L., R. Beyaert, and G. van Loo. 2009. The ubiquitin-editing enzyme A20 (TNFAIP3) is a central regulator of immunopathology. Trends Immunol. 30: 383-391.
47. Wang, J., Y. Ouyang, Y. Guner, H. R. Ford, and A. V. Grishin. 2009. Ubiquitinediting enzyme A20 promotes tolerance to lipopolysaccharide in enterocytes. J. Immunol. 183: 1384-1392.
48. Lodes, M. J., Y. Cong, C. O. Elson, R. Mohamath, C. J. Landers, S. R. Targan, M. Fort, and R. M. Hershberg. 2004. Bacterial flagellin is a dominant antigen in Crohn disease. J. Clin. Invest. 113: 1296-1306. (Pubitemid 39069929)
49. Vinay, D. S., K. Cha, and B. S. Kwon. 2006. Dual immunoregulatory pathways of 4-1BB signaling. J. Mol. Med. 84: 726-736. (Pubitemid 44328064)
50. Maerten, P., K. Geboes, G. De Hertogh, C. Shen, P. Cadot, D. M. Bullens, G. Van Assche, F. Penninckx, P. Rutgeerts, and J. L. Ceuppens. 2004. Functional expression of 4-1BB (CD137) in the inflammatory tissue in Crohn's disease. Clin. Immunol. 112: 239-246. (Pubitemid 39078699)
51. Shaw, M. H., T. Reimer, C. Sánchez-Valdepeñas, N. Warner, Y. G. Kim, M. Fresno, and G. Nuñez. 2009. T cell-intrinsic role of Nod2 in promoting type 1 immunity to Toxoplasma gondii. Nat. Immunol. 10: 1267-1274.
52. Sabbah, A., T. H. Chang, R. Harnack, V. Frohlich, K. Tominaga, P. H. Dube, Y. Xiang, and S. Bose. 2009. Activation of innate immune antiviral responses by Nod2. Nat. Immunol. 10: 1073-1080.
53. Castellaneta, A., T. L. Sumpter, L. Chen, D. Tokita, and A. W. Thomson. 2009. NOD2 ligation subverts IFN-alpha production by liver plasmacytoid dendritic cells and inhibits their T cell allostimulatory activity via B7-H1 up-regulation. J. Immunol. 183: 6922-6932.