Specific NEMO mutations impair CD40-mediated c-Rel activation and B cell terminal differentiation

Journal of Clinical Investigation

Volumn 114, Issue 11, 2004, Pages 1593-1602

  Jain, Ashish ^a   Ma, Chi A ^a   Lopez Granados, Eduardo ^a   Means, Gary ^b   Brady, William ^b   Orange, Jordan S ^c   Liu, Shuying ^a   Holland, Steven ^a   Derry, Jonathan M J ^b  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b AMGEN INC   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 ANTIGEN; CD40 LIGAND; IMMUNOGLOBULIN CLASS; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 4; NEUTRALIZING ANTIBODY; P65 PROTEIN; PROTEIN; UNCLASSIFIED DRUG; AICDA (ACTIVATION INDUCED CYTIDINE DEAMINASE); AICDA (ACTIVATION-INDUCED CYTIDINE DEAMINASE); CARRIER PROTEIN; CYTIDINE DEAMINASE; CYTOSINE DEAMINASE; I KAPPA B KINASE; IKBKG PROTEIN, HUMAN; IMMUNOGLOBULIN; TRANSCRIPTION FACTOR REL;

AID GENE; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; C REL GENE; CELL DIFFERENTIATION; CLASS SWITCH RECOMBINATION; CONTROLLED STUDY; DNA MICROARRAY; ECTODERMAL DYSPLASIA; GENE; GENE ACTIVATION; GENE EXPRESSION; GENE MUTATION; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HYPERIMMUNOGLOBULINEMIA M; NEMO GENE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; SOMATIC HYPERMUTATION; UNINDEXED SEQUENCE; X CHROMOSOME LINKAGE; ZINC FINGER DOMAIN; ADOLESCENT; ADULT; BLOOD; CYTOLOGY; GENE EXPRESSION REGULATION; GENE REARRANGEMENT; GENETICS; HYPERGAMMAGLOBULINEMIA; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; MUTATION; PHYSIOLOGY; PRESCHOOL CHILD; SYNDROME;

ADOLESCENT; ADULT; ANTIGENS, CD40; B-LYMPHOCYTES; CARRIER PROTEINS; CELL DIFFERENTIATION; CHILD, PRESCHOOL; CYTIDINE DEAMINASE; CYTOSINE DEAMINASE; ECTODERMAL DYSPLASIA; GENE EXPRESSION REGULATION; HUMANS; HYPERGAMMAGLOBULINEMIA; I-KAPPA B KINASE; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOGLOBULINS; INTERLEUKIN-4; MOLECULAR SEQUENCE DATA; MUTATION; NF-KAPPA B; PROTO-ONCOGENE PROTEINS C-REL; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN; SYNDROME;

EID: 85047693229     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI21345     Document Type: Article

References (41)

1. Rajewsky, K. 1996. Clonal selection and learning in the antibody system. Nature. 381:751-758.
2. Revy, P., et al. 2000. Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the hyper-IgM syndrome (HIGM2). Cell. 102:565-575.
3. Muramatsu, M., et al. 2000. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell. 102:553-563.
4. Yoshikawa, K., et al. 2002. AID enzyme-induced hypermutation in an actively transcribed gene in fibroblasts. Science. 296:2033-2036.
5. Karin, M., and Ben-Neriah, Y. 2000. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu. Rev. Immunol. 18:621-663.
6. Jain, A., et al. 2001. Specific missense mutations in NEMO result in hyper-IgM syndrome with hypohydrotic ectodermal dysplasia. Nat. Immunol. 2:223-228.
7. Doffinger, R., et al. 2001. X-linked anhidrotic ectodermal dysplasia with immunodeficiency is caused by impaired NF-kappaB signaling. Nat. Genet. 27:277-285.
8. Zonana, J., et al. 2000. A novel X-linked disorder of immune deficiency and hypohidrotic ectodermal dysplasia is allelic to incontinentia pigmenti and due to mutations in IKK-gamma (NEMO). Am. J. Hum. Genet. 67:1555-1562.
9. Orange, J.S., et al. 2002. Deficient natural killer cell cytotoxicity in patients with IKK-/NEMO mutations. J. Clin. Invest. 109:1501-1509. doi:10.1172/ JCI200214858.
10. Stewart, A.K., Huang, C., Stollar, B.D., and Schwartz, R.S. 1993. High-frequency representation of a single VH gene in the expressed human B cell repertoire. J. Exp. Med. 177:409-418.
11. Makris, C., Roberts, J.L., and Karin, M. 2002. The carboxyl-terminal region of IkappaB kinase gamma (IKKgamma) is required for full IKK activation. Mol. Cell. Biol. 22:6573-6581.
12. Digicaylioglu, M., and Lipton, S.A. 2001. Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature. 412:641-647.
13. Sanjabi, S., Hoffmann, A., Liou, H.C., Baltimore, D., and Smale, S.T. 2000. Selective requirement for c-Rel during IL-12 P40 gene induction in macrophages. Proc. Natl. Acad. Sci. U. S. A. 97:12705-12710.
14. Macpherson, A.J., et al. 2000. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science. 288:2222-2226.
15. Chirmule, N., Tazelaar, J., and Wilson, J.M. 2000. Th2-dependent B cell responses in the absence of CD40-CD40 ligand interactions. J. Immunol. 164:248-255.
16. Atkinson, T.P., et al. 1998. Leukocyte transfusion-associated granulocyte responses in a patient with X-linked hyper-IgM syndrome. J. Clin. Immunol. 18:430-439.
17. Tang, E.D., Wang, C.Y., Xiong, Y., and Guan, K.L. 2003. A role for NF-kappaB essential modifier/ IkappaB kinase-gamma (NEMO/IKKgamma) ubiquitination in the activation of the IkappaB kinase complex by tumor necrosis factor-alpha. J. Biol. Chem. 278:37297-37305.
18. Huang, T.T., Wuerzberger-Davis, S.M., Wu, Z.H., and Miyamoto, S. 2003. Sequential modification of NEMO/IKKgamma by SUMO-1 and ubiquitin mediates NF-kappaB activation by genotoxic stress. Cell. 115:565-576.
19. Zhou, H., et al. 2004. Bcl 10 activates the NF-kappaB pathway through ubiquitination of NEMO. Nature. 427:167-171.
20. Pohl, T., et al. 2002. The combined absence of NF-kappa B1 and c-Rel reveals that overlapping roles for these transcription factors in the B cell lineage are restricted to the activation and function of mature cells. Proc. Natl. Acad. Sci. U. S. A. 99:4514-4519.
21. Zelazowski, P., et al. 1997. B cells genetically deficient in the c-Rel transactivation domain have selective defects in germline CH transcription and Ig class switching. J. Immunol. 159:3133-3139.
22. Okazaki, I.M., Kinoshita, K., Muramatsu, M., Yoshikawa, K., and Honjo, T. 2002. The AID enzyme induces class switch recombination in fibroblasts. Nature. 416:340-345.
23. Ma, L., Hu, B., and Kenter, A.L. 1997. Ig S gamma-specific DNA binding protein SNAP is related to the helix-loop-helix transcription factor E47. Int. Immunol. 9:1021-1029.
24. Wuerffel, R., et al. 1992. Switch recombination breakpoints are strictly correlated with DNA recognition motifs for immunoglobulin S gamma 3 DNA-binding proteins. J. Exp. Med. 176:339-349.
25. Kenter, A.L., Wuerffel, R., Sen, R., Jamieson, C.E., and Merkulov, G.V. 1993. Switch recombination breakpoints occur at nonrandom positions in the S gamma tandem repeat. J. Immunol. 151:4718-4731.
26. Miyamoto, A., Cui, X., Naumovski, L., and Cleary, M.L. 1996. Helix-loop-helix proteins LYL1 and E2a form heterodimeric complexes with distinctive DNA-binding properties in hematolymphoid cells. Mol. Cell. Biol. 16:2394-2401.
27. Ferrier, R., et al. 1999. Physical interaction of the bHLH LYL1 protein and NF-kappaB1 p105. Oncogene. 18:995-1005.
28. Petersen, S., et al. 2001. AID is required to initiate Nbs1/gamma-H2AX focus formation and mutations at sites of class switching. Nature. 414:660-665.
29. Tashiro, J., Kinoshita, K., and Honjo, T. 2001. Palindromic but not G-rich sequences are targets of class switch recombination. Int. Immunol. 13:495-505.
30. Roddam, P.L., et al. 2002. Genetic variants of NHEJ DNA ligase IV can affect the risk of developing multiple myeloma, a tumour characterised by aberrant class switch recombination. J. Med. Genet. 39:900-905.
31. Shaffer, A.L., et al. 2001. Signatures of the immune response. Immunity. 15:375-385.
32. Klein, U., et al. 2003. Transcriptional analysis of the B cell germinal center reaction. Proc. Natl. Acad. Sci. U. S. A. 100:2639-2644.
33. Dedeoglu, F., Horwitz, B., Chaudhuri, J., Alt, F.W., and Geha, R.S. 2004. Induction of activation-induced cytidine deaminase gene expression by IL-4 and CD40 ligation is dependent on STAT6 and NFkappaB. Int. Immunol. 16:395-404.
34. Zhou, C., Saxon, A., and Zhang, K. 2003. Human activation-induced cytidine deaminase is induced by IL-4 and negatively regulated by CD45: implication of CD45 as a Janus kinase phosphatase in antibody diversification. J. Immunol. 170:1887-1893.
35. Ta, V.T., et al. 2003. AID mutant analyses indicate requirement for class-switch-specific cofactors. Nat. Immunol. 4:843-848.
36. Doi, T., Kinoshita, K., Ikegawa, M., Muramatsu, M., and Honjo, T. 2003. De novo protein synthesis is required for the activation-induced cytidine deaminase function in class-switch recombination. Proc. Natl. Acad. Sci. U. S. A. 100:2634-2638.
37. Coope, H.J., et al. 2002. CD40 regulates the processing of NF-kappaB2 p100 to p52. EMBO J. 21:5375-5385.
38. Dixit, V., and Mak, T.W. 2002. NF-kappaB signaling. Many roads lead to madrid. Cell. 111:615-619.
39. Mackay, F., Schneider, P., Rennert, P., and Browning, J. 2003. BAFF AND APRIL: a tutorial on B cell survival. Annu. Rev. Immunol. 21:231-264.
40. Early, G.S., Zhao, W., and Burns, C.M. 1996. Anti-CD40 ligand antibody treatment prevents the development of lupus-like nephritis in a subset of New Zealand black x New Zealand white mice. Response correlates with the absence of an anti-antibody response. J. Immunol. 157:3159-3164.
41. Levy, Y., et al. 1998. Defect in IgV gene somatic hypermutation in common variable immunodeficiency syndrome. Proc. Natl. Acad. Sci. U. S. A. 95:13135-13140.