Copper metabolism domain-containing 1 represses genes that promote inflammation and protects mice from colitis and colitis-associated cancer

Gastroenterology

Volumn 147, Issue 1, 2014, Pages

  Li, Haiying ^a   Chan, Lillienne ^a   Bartuzi, Paulina ^c   Melton, Shelby D ^d   Weber, Axel ^e   Ben Shlomo, Shani ^f   Varol, Chen ^f   Raetz, Megan ^b   Mao, Xicheng ^a   Starokadomskyy, Petro ^a   Van Sommeren, Suzanne ^c   Mokadem, Mohamad ^a   Schneider, Heike ⁱ   Weisberg, Reid ^a   Westra, Harm Jan ^c   Esko, Tõnu ^g   Metspalu, Andres ^g   Kumar, Vinod ^c   Faubion, William A ^h   Yarovinsky, Felix ^b   Hofker, Marten ^c   Wijmenga, Cisca ^c   Kracht, Michael ^e   Franke, Lude ^c   Aguirre, Vincent ^a   Weersma, Rinse K ^c   Gluck, Nathan ^f   Van De Sluis, Bart ^c   Burstein, Ezra ^a,b   more..

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d VA NORTH TEXAS HEALTH CARE SYSTEM   (United States)

^e JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

^f TEL AVIV SOURASKY MEDICAL CENTER   (Israel)

^g UNIVERSITY OF TARTU   (Estonia)

^h MAYO CLINIC   (United States)

ⁱ HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

CD; Gene Regulation; Mouse Model; UC

Indexed keywords

AZOXYMETHANE; COPPER METABOLISM MURR1 DOMAIN CONTAINING 1; DEXTRAN SULFATE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; MESSENGER RNA; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CELL FUNCTION; CELL POPULATION; CLINICAL ARTICLE; COHORT ANALYSIS; COLON BIOPSY; COLON DISEASE; COLON DYSPLASIA; CONTROLLED STUDY; COPPER METABOLISM; CROHN DISEASE; DYSPLASIA; GENE REPRESSION; GENETIC VARIABILITY; HUMAN; HUMAN TISSUE; IMMUNOCOMPETENT CELL; INFLAMMATORY BOWEL DISEASE; KNOCKOUT MOUSE; MOUSE; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; SEPSIS; SINGLE NUCLEOTIDE POLYMORPHISM; ULCERATIVE COLITIS; VALIDATION STUDY; WILD TYPE;

CD; GENE REGULATION; MOUSE MODEL; UC;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AZOXYMETHANE; BIOPSY; CASE-CONTROL STUDIES; COLITIS; COLON; COLONIC NEOPLASMS; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; HUMANS; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; MICE; MICE, KNOCKOUT; NF-KAPPA B; POLYMORPHISM, SINGLE NUCLEOTIDE; RNA, MESSENGER;

EID: 84902980023     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2014.04.007     Document Type: Article

References (57)

1. A. Kaser, S. Zeissig, and R.S. Blumberg Inflammatory bowel disease Annu Rev Immunol 28 2010 573 621
2. M.S. Hayden, and S. Ghosh NF-κB, the first quarter-century: remarkable progress and outstanding questions Genes Dev 26 2012 203 234
3. L. Jostins, S. Ripke, and R.K. Weersma et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease Nature 491 2012 119 124
4. C.W. Lees, J.C. Barrett, and M. Parkes et al. New IBD genetics: common pathways with other diseases Gut 60 2011 1739 1753
5. A. Hoffmann, A. Levchenko, and M.L. Scott et al. The IκB-NF- κB signaling module: temporal control and selective gene activation Science 298 2002 1241 1245
6. A. Kovalenko, C. Chable-Bessia, and G. Cantarella et al. The tumour suppressor CYLD negatively regulates NF-κB signalling by deubiquitination Nature 424 2003 801 805
7. I.E. Wertz, K.M. O'Rourke, and H. Zhou et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-κB signalling Nature 430 2004 694 699
8. G. Natoli, and S. Chiocca Nuclear ubiquitin ligases, NF-κB degradation, and the control of inflammation Sci Signal 1 2008 pe1
9. S. Saccani, I. Marazzi, and A.A. Beg et al. Degradation of promoter-bound p65/RelA is essential for the prompt termination of the nuclear factor κB response J Exp Med 200 2004 107 113
10. X. Mao, N. Gluck, and D. Li et al. GCN5 is a required cofactor for a ubiquitin ligase that targets NF-κB/RelA Genes Dev 23 2009 849 861
11. A. Ryo, F. Suizu, and Y. Yoshida et al. Regulation of NF-κB signaling by Pin1-dependent prolyl isomerization and ubiquitin-mediated proteolysis of p65/RelA Mol Cell 12 2003 1413 1426
12. G.N. Maine, X. Mao, and C.M. Komarck et al. COMMD1 promotes the ubiquitination of NF-κB subunits through a Cullin-containing ubiquitin ligase EMBO J 26 2007 436 447
13. H. Geng, T. Wittwer, and O. Dittrich-Breiholz et al. Phosphorylation of NF-κB p65 at Ser468 controls its COMMD1-dependent ubiquitination and target gene-specific proteasomal elimination EMBO Rep 10 2009 381 386
14. E. Burstein, J.E. Hoberg, and A.S. Wilkinson et al. COMMD proteins: a novel family of structural and functional homologs of MURR1 J Biol Chem 280 2005 22222 22232
15. + lymphocytes Nature 426 2003 853 857
16. B. van de Sluis, J. Rothuizen, and P.L. Pearson et al. Identification of a new copper metabolism gene by positional cloning in a purebred dog population Hum Mol Genet 11 2002 165 173
17. W. Biasio, T. Chang, and C.J. McIntosh et al. Identification of Murr1 as a regulator of the human δ epithelial sodium channel J Biol Chem 279 2004 5429 5434
18. L. Drevillon, G. Tanguy, and A. Hinzpeter et al. COMMD1-mediated ubiquitination regulates CFTR trafficking PLoS One 6 2011 e18334
19. L. Smith, P. Litman, and C.M. Liedtke COMMD1 interacts with the COOH terminus of NKCC1 in Calu-3 airway epithelial cells to modulate NKCC1 ubiquitination Am J Physiol Cell Physiol 305 2013 C133 C146
20. B. van de Sluis, X. Mao, and Y. Zhai et al. COMMD1 disrupts HIF-1α/β dimerization and inhibits human tumor cell invasion J Clin Invest 120 2010 2119 2130
21. J. Fu, M.G. Wolfs, and P. Deelen et al. Unraveling the regulatory mechanisms underlying tissue-dependent genetic variation of gene expression PLoS Genet 8 2012 e1002431
22. R.S. Fehrmann, R.C. Jansen, and J.H. Veldink et al. Trans-eQTLs reveal that independent genetic variants associated with a complex phenotype converge on intermediate genes, with a major role for the HLA PLoS Genet 7 2011 e1002197
23. B. van de Sluis, P. Muller, and K. Duran et al. Increased activity of hypoxia-inducible factor 1 is associated with early embryonic lethality in Commd1 null mice Mol Cell Biol 27 2007 4142 4156
24. W.I. Vonk, P. Bartuzi, and P. de Bie et al. Liver-specific Commd1 knockout mice are susceptible to hepatic copper accumulation PLoS One 6 2011 e29183
25. X. Mao, N. Gluck, and B. Chen et al. Copper metabolism MURR1 domain containing 1 (COMMD1) regulates Cullin-RING ligases by preventing Cullin-associated NEDD8-dissociated (CAND1) binding J Biol Chem 286 2011 32355 32365
26. P. Starokadomskyy, N. Gluck, and H. Li et al. CCDC22 deficiency in humans blunts activation of proinflammatory NF-κB signaling J Clin Invest 123 2013 2244 2256
27. G.D. Barish, R.T. Yu, and M. Karunasiri et al. Bcl-6 and NF-κB cistromes mediate opposing regulation of the innate immune response Genes Dev 24 2010 2760 2765
28. J.D. Reveille, A.M. Sims, and P. Danoy et al. Genome-wide association study of ankylosing spondylitis identifies non-MHC susceptibility loci Nat Genet 42 2010 123 127
29. Y. Okada, C. Terao, K. Ikari, and Y. Kochi et al. Meta-analysis identifies nine new loci associated with rheumatoid arthritis in the Japanese population Nat Genet 44 2012 511 516
30. E.E. Kenny, I. Pe'er, and A. Karban et al. A genome-wide scan of Ashkenazi Jewish Crohn's disease suggests novel susceptibility loci PLoS Genet 8 2012 e1002559
31. C.A. Anderson, G. Boucher, and C.W. Lees et al. Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47 Nat Genet 43 2011 246 252
32. A. Franke, D.P. McGovern, and J.C. Barrett et al. Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci Nat Genet 42 2010 1118 1125
33. Consortium TEP A user's guide to the encyclopedia of DNA elements (ENCODE) PLoS Biol 9 2011 e1001046
34. M.U. Kaikkonen, N.J. Spann, and S. Heinz et al. Remodeling of the enhancer landscape during macrophage activation is coupled to enhancer transcription Mol Cell 51 2013 310 325
35. D.L. Nicolae, E. Gamazon, and W. Zhang et al. Trait-associated SNPs are more likely to be eQTLs: annotation to enhance discovery from GWAS PLoS Genet 6 2010 e1000888
36. F.R. Greten, L. Eckmann, and T.F. Greten et al. IKKβ links inflammation and tumorigenesis in a mouse model of colitis-associated cancer Cell 118 2004 285 296
37. J. Bollrath, T.J. Phesse, and V.A. von Burstin et al. gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis Cancer Cell 15 2009 91 102
38. J. Bollrath, and F.R. Greten IKK/NF-κB and STAT3 pathways: central signalling hubs in inflammation-mediated tumour promotion and metastasis EMBO Rep 10 2009 1314 1319
39. K.H. Weiss, J.C. Lozoya, and S. Tuma et al. Copper-induced translocation of the Wilson disease protein ATP7B independent of Murr1/COMMD1 and Rab7 Am J Pathol 173 2008 1783 1794
40. T. Miyayama, D. Hiraoka, and F. Kawaji et al. Roles of COMM-domain-containing 1 in stability and recruitment of the copper-transporting ATPase in a mouse hepatoma cell line Biochem J 429 2010 53 61
41. T. Chang, Y. Ke, and K. Ly et al. COMMD1 regulates the delta epithelial sodium channel (δENaC) through trafficking and ubiquitination Biochem Biophys Res Commun 411 2011 506 511
42. A. Nenci, C. Becker, and A. Wullaert et al. Epithelial NEMO links innate immunity to chronic intestinal inflammation Nature 446 2007 557 561
43. S.I. Grivennikov, F.R. Greten, and M. Karin Immunity, inflammation, and cancer Cell 140 2010 883 899
44. B.K. Popivanova, K. Kitamura, and Y. Wu et al. Blocking TNF-α in mice reduces colorectal carcinogenesis associated with chronic colitis J Clin Invest 118 2008 560 570
45. B. Kabakchiev, and M.S. Silverberg Expression quantitative trait loci analysis identifies associations between genotype and gene expression in human intestine Gastroenterology 144 2013 1488 1496 1496 e1-3
46. M.A. Rivas, M. Beaudoin, and A. Gardet et al. Deep resequencing of GWAS loci identifies independent rare variants associated with inflammatory bowel disease Nat Genet 43 2011 1066 1073
47. W.I. Vonk, P. Bartuzi, and P. de Bie et al. Liver-specific Commd1 knockout mice are susceptible to hepatic copper accumulation PLoS One 6 2011 e29183
48. M.G. Toscano, D. Ganea, and A.M. Gamero Cecal ligation puncture procedure J Vis Exp 2011 pii:2860
49. D. Kirkland, A. Benson, and J. Mirpuri et al. B cell-intrinsic MyD88 signaling prevents the lethal dissemination of commensal bacteria during colonic damage Immunity 36 2012 228 238
50. H.S. Cooper, S.N. Murthy, and R.S. Shah et al. Clinicopathologic study of dextran sulfate sodium experimental murine colitis Lab Invest 69 1993 238 249
51. E. Burstein, J.E. Hoberg, and A.S. Wilkinson et al. COMMD proteins: a novel family of structural and functional homologs of MURR1 J Biol Chem 280 2005 22222 22232
52. W.I. Vonk, P. de Bie, and C.G. Wichers et al. The copper-transporting capacity of ATP7A mutants associated with Menkes disease is ameliorated by COMMD1 as a result of improved protein expression Cell Mol Life Sci 69 2012 149 163
53. D.J. Ahnen, T.A. Reed, and J.M. Bozdech Isolation and characterization of populations of mature and immature rat colonocytes Am J Physiol 254 1988 G610 G621
54. E. Burstein, L. Ganesh, and R.D. Dick et al. A novel role for XIAP in copper homeostasis through regulation of MURR1 EMBO J 23 2004 244 254
55. X. Mao, N. Gluck, and D. Li et al. GCN5 is a required cofactor for a ubiquitin ligase that targets NF-κB/RelA Genes Dev 23 2009 849 861
56. P. Starokadomskyy, N. Gluck, and H. Li et al. CCDC22 deficiency in humans blunts activation of proinflammatory NF-κB signaling J Clin Invest 123 2013 2244 2256
57. G.D. Barish, R.T. Yu, and M. Karunasiri et al. Bcl-6 and NF-κB cistromes mediate opposing regulation of the innate immune response Genes Dev 24 2010 2760 2765