CCDC22 deficiency in humans blunts activation of proinfammatory NF-κB signaling

Journal of Clinical Investigation

Volumn 123, Issue 5, 2013, Pages 2244-2256

  Starokadomskyy, Petro ^a,b   Gluck, Nathan ^c,d   Li, Haiying ^a   Chen, Baozhi ^a   Wallis, Mathew ^e   Maine, Gabriel N ^f   Mao, Xicheng ^a   Zaidi, Iram W ^a   Hein, Marco Y ^g   McDonald, Fiona J ^h   Lenzner, Steffen ⁱ   Zecha, Agnes ⁱ   Ropers, Hans Hilger ⁱ   Kuss, Andreas W ^i,j,k   McGaughran, Julie ^e,l   Gecz, Jozef ^m,n   Burstein, Ezra ^a,b  

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

^b UNIVERSITY OF TEXAS AT DALLAS   (United States)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^d TEL AVIV SOURASKY MEDICAL CENTER   (Israel)

^e ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

^f WILLIAM BEAUMONT HOSPITAL   (United States)

^g MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^h UNIVERSITY OF OTAGO   (New Zealand)

ⁱ MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^j UNIVERSITY MEDICINE GREIFSWALD   (Germany)

^k UNIVERSITY OF GREIFSWALD   (Germany)

^l UNIVERSITY OF QUEENSLAND   (Australia)

^m WOMEN S AND CHILDREN S HOSPITAL   (Australia)

ⁿ UNIVERSITY OF ADELAIDE   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

COILED COIL DOMAIN CONTAINING PROTEIN 22; COPPER METABOLISM MURR1 DOMAIN CONTAINING 8; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ECTODERMAL DYSPLASIA; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; INTELLECTUAL IMPAIRMENT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UBIQUITINATION; X CHROMOSOME LINKED DISORDER;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CARRIER PROTEINS; CHROMOSOMES, HUMAN, X; ECTODERMAL DYSPLASIA; GENE EXPRESSION REGULATION; GENETIC LINKAGE; HEK293 CELLS; HELA CELLS; HUMANS; I-KAPPA B PROTEINS; INFLAMMATION; MICROSCOPY, FLUORESCENCE; MUTATION; NEOPLASMS; NF-KAPPA B; PROTEIN STRUCTURE, TERTIARY; PROTEINS; SIGNAL TRANSDUCTION; UBIQUITIN;

EID: 84877146813     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI66466     Document Type: Article

References (53)

1. Burstein E, et al. COMMD proteins: A novel family of structural and functional homologs of MURR1. J Biol Chem. 2005;280(23):22222-22232.
2. van de Sluis B, Rothuizen J, Pearson PL, van Oost BA, Wijmenga C. Identification of a new copper metabolism gene by positional cloning in a purebred dog population. Hum Mol Genet. 2002; 11(2):165-173.
3. Burstein E, et al. A novel role for XIAP in copper homeostasis through regulation of MURR1. EMBO J. 2004;23(1):244-254.
4. Klomp AE, van de Sluis B, Klomp LW, Wijmenga C. The ubiquitously expressed MURR1 protein is absent in canine copper toxicosis. J Hepatol. 2003; 39(5):703-709.
5. Biasio W, Chang T, McIntosh CJ, McDonald FJ. Identification of Murr1 as a regulator of the human δ epithelial sodium channel. J Biol Chem. 2004; 279(7):5429-5434.
6. Ke Y, Butt AG, Swart M, Liu YF, McDonald FJ. COMMD1 downregulates the epithelial sodium channel through Nedd4-2. Am J Physiol Renal Physiol. 2010;298(6):F1445-F1456.
7. Chang T, Ke Y, Ly K, McDonald FJ. COMMD1 regulates the delta epithelial sodium channel (δENaC) through trafficking and ubiquitination. Biochem Biophys Res Commun. 2011;411(3):506-511.
8. Drevillon L, et al. COMMD1-mediated ubiquitination regulates CFTR trafficking. PLoS One. 2011; 6(3):e18334.
9. van de Sluis B, et al. Increased activity of hypoxiainducible factor 1 is associated with early embryonic lethality in Commd1 null mice. Mol Cell Biol. 2007; 27(11):4142-4156.
10. van de Sluis B, et al. COMMD1 disrupts HIF-1α/β dimerization and inhibits human tumor cell invasion. J Clin Invest. 2010;120(6):2119-2130.
11. + lymphocytes. Nature. 2003;426(6968):853-857.
12. Maine GN, Mao X, Komarck CM, Burstein E. COMMD1 promotes the ubiquitination of NF-KB subunits through a Cullin-containing ubiquitin ligase. EMBO J. 2007;26(2):436-447.
13. Burkly L, et al. Expression of relB is required for the development of thymic medulla and dendritic cells. Nature. 1995;373(6514):531-536.
14. Kontgen F, et al. Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity, and interleukin-2 expression. Genes Dev. 1995;9(16):1965-1977.
15. Sha WC, Liou HC, Tuomanen EI, Baltimore D. Targeted disruption of the p50 subunit of NF-KB leads to multifocal defects in immune responses. Cell. 1995;80(2):321-330.
16. Mao X, et al. Copper metabolism MURR1 domain containing 1 (COMMD1) regulates Cullin-RING ligases by preventing Cullin-associated NEDD8dissociated (CAND1) binding. J Biol Chem. 2011; 286(37):32355-32365.
17. Petroski MD, Deshaies RJ. Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol. 2005;6(1):9-20.
18. Hay den MS, Ghosh S. Shared principles in NF-KB signaling. Cell. 2008;132(3):344-362.
19. Chen Z, et al. Signal-induced site-specific phosphorylation targets IKBCC to the ubiquitin-pro teasome pathway. Genes Dev. 1995;9:1586-1597
20. Henkel T, Machleidt T, Alkalay I, Krönke M, BenNeriah Y, Baeuerle PA. Rapid proteolysis of IKB-CX is necessary for activation of transcription factor NF-KB. Nature. 1993;365(6442):182-185.
21. Yaron A, et al. Identification of the receptor component of the IKBCC-ubiquitin ligase. Nature. 1998; 396(6711):590-594.
22. Baeuerle PA, Baltimore D. IKB: a specific inhibitor of the NF-KB transcription factor. Science. 1988; 242(4878):540-546.
23. Frescas D, Pagano M. Deregulated proteolysis by the F-box proteins SKP2 and β-TrCP: tipping the scales of cancer. Nat Rev Cancer. 2008;8(6):438-449.
24. Geng H, Wittwer T, Dittrich-Breiholz O, Kracht M, Schmitz ML. Phosphorylation of NF-KB p65 at Ser468 controls its COMMD1-dependent ubiquitination and target gene-specific proteasomal elimination. EMBO Rep. 2009;10(4):381-386.
25. Mao X, et al. GCN5 is a required cofactor for a ubiquitin ligase that targets NF-KB/RelA. Genes Dev. 2009; 23(7):849-861.
26. Voineagu I, et al. CCDC22: a novel candidate gene for syndromic X-linked intellectual disability. Mol Psychiatry. 2012;17(1):4-7.
27. Wu C, et al. BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol. 2009;10(11):R130.
28. de Bie P, et al. Characterization of COMMD protein-protein interactions in NF-κB signalling. Biochem J. 2006;398(1):63-71.
29. Hubner NC, et al. Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J Cell Biol. 2010;189(4):739-754.
30. Poser I, et al. BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals. Nat Methods. 2008;5(5):409-415.
31. Barbe L, et al. Toward a confocal subcellular atlas of the human proteome. Mol Cell Proteomics. 2008; 7(3):499-508.
32. Marchler-Bauer A, et al. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 2011;39(Database issue):D225-D229.
33. Schleiffer A, Kaitna S, Maurer-Stroh S, Glotzer M, Nasmyth K, Eisenhaber F. Kleisins: a superfamily of bacterial and eukaryotic SMC protein partners. Mol Cell. 2003;11(3):571-575.
34. Doffinger R, et al. X-linked anhidrotic ectodermal dysplasia with immunodeficiency is caused by impaired NF-κB signaling. Nat Genet. 2001; 27(3):277-285.
35. Jain A, Ma CA, Liu S, Brown M, Cohen J, Strober W. Specific missense mutations in NEMO result in hyper-IgM syndrome with hypohydrotic ectodermal dysplasia. Nat Immunol. 2001;2(3):223-228.
36. Picard C, Casanova JL, Puel A. Infectious diseases in patients with IRAK-4, MyD88, NEMO, or IκBα deficiency. Clin Microbiol Rev. 2011;24(3):490-497.
37. Mikkola ML. Molecular aspects of hypohidrotic ectodermal dysplasia. Am J Med Genet A. 2009; 149A(9):2031-2036.
38. Schmidt-Ullrich R, Aebischer T, Hulsken J, Birchmeier W, Klemm U, Scheidereit C. Requirement of NF-κB/Rel for the development of hair follicles and other epidermal appendices. Development. 2001; 128(19):3843-3853.
39. Narindrasorasak S, Kulkarni P, Deschamps P, She YM, Sarkar B. Characterization and copper binding properties of human COMMD1 (MURR1). Biochemistry. 2007;46(11):3116-3128.
40. Nakagawa T, Xiong Y. X-linked mental retardation gene CUL4B targets ubiquitylation of H3K4 methyltransferase component WDR5 and regulates neuronal gene expression. Mol Cell. 2011;43(3):381-391.
41. Boersma MC, Dresselhaus EC, De Biase LM, Mihalas AB, Bergles DE, Meffert MK. A requirement for nuclear factor-κB in developmental and plasticity-associated synaptogenesis. J Neurosci. 2011; 31(14):5414-5425.
42. Meffert MK, Chang JM, Wiltgen BJ, Fanselow MS, Baltimore D. NF-κB functions in synaptic signaling and behavior. Nat Neurosci. 2003;6(10):1072- 1078.
43. Chen Y, et al. HDAC-mediated deacetylation of NF-κB is critical for Schwann cell myelination. Nat Neurosci. 2011;14(4):437-441.
44. Sancho-Shimizu V, et al. Herpes simplex encephalitis in children with autosomal recessive and dominant TRIF deficiency. J Clin Invest. 2011; 121(12):4889-4902.
45. Suttner K, et al. Genetic variants harbored in the forkhead box protein 3 locus increase hay fever risk. J Allergy Clin Immunol. 2010;125(6):1395-1399.
46. Duckett CS, Li F, Wang Y, Tomaselli KJ, Thompson CB, Armstrong RC. Human IAP-like protein regulates programmed cell death downstream of Bcl-xL and cytochrome c. Mol Cell Biol. 1998;18(1):608-615.
47. Richter BW, et al. Molecular cloning of ILP-2, a novel member of the inhibitor of apoptosis protein family. Mol Cell Biol. 2001;21(13):4292-4301.
48. Duckett CS, Gedrich RW, Gilfillan MC, Thompson CB. Induction of nuclear factor κB by the CD30 receptor is mediated by TRAF1 and TRAF2. Mol Cell Biol. 1997;17(3):1535-1542.
49. Neitzel H. A routine method for the establishment of permanent growing lymphoblastoid cell lines. Hum Genet. 1986;73(4):320-326.
50. Li H, et al. Regulation of NF-κB activity by competition between RelA acetylation and ubiquitination. Oncogene. 2012;31(5):611-623.
51. Maine GN, Gluck N, Zaidi IW, Burstein E. Bimolecular Affinity Purification (BAP): Tandem affinity purification using two protein baits. Cold Spring Harb Protoc. 2009;2009(11):pdb.prot5318.
52. Vaira S, Alhawagri M, Anwisye I, Kitaura H, Faccio R, Novack DV. RelA/p65 promotes osteoclast differentiation by blocking a RANKL-induced apoptotic JNK pathway in mice. J Clin Invest. 2008; 118(6):2088-2097.
53. Warner N, et al. A genome-wide siRNA screen reveals positive and negative regulators of the NOD2 and NF-κB signaling pathways. Sci Signal. 2013;6(258):rs3.