The NF-κB signaling pathway in human genetic diseases

Cellular and Molecular Life Sciences

Volumn 62, Issue 15, 2005, Pages 1682-1691

  Courtois, Gilles ^a  

^a SAINT LOUIS HOSPITAL   (France)

Author keywords

Anhidrotic ectodermal dysplasia with immunodeficiency; CYLD; Cylindromatosis; Incontinentia pigmenti; NEMO; NF B

Indexed keywords

I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; CHUK PROTEIN, HUMAN; CHUK PROTEIN, MOUSE; I KAPPA B; I KAPPA B KINASE; IKBKB PROTEIN, HUMAN; IKBKB PROTEIN, MOUSE; IKBKE PROTEIN, HUMAN; IKBKE PROTEIN, MOUSE; NF KAPPAB INHIBITOR ALPHA; NF-KAPPAB INHIBITOR ALPHA; PROTEIN SERINE THREONINE KINASE;

ALBERS SCHOENBERG DISEASE; ANHIDROTIC ECTODERMAL DYSPLASIA; APOPTOSIS; AUTOSOMAL DOMINANT DISORDER; CELL GROWTH; CORRELATION ANALYSIS; CYLINDROMA; EMBRYO DEVELOPMENT; ENZYME ACTIVATION; GENETIC DISORDER; GENOTYPE; HUMAN; IMMUNE DEFICIENCY; IMMUNE RESPONSE; INFLAMMATION; LYMPHEDEMA; MUTATION; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; SKIN APPENDAGE; SKIN INFLAMMATION; TRICHOEPITHELIOMA; ANIMAL; ECTODERMAL DYSPLASIA; FEMALE; GENETICS; INCONTINENTIA PIGMENTI; MALE; METABOLISM; MOUSE;

ANIMALS; ECTODERMAL DYSPLASIA; FEMALE; GENETIC DISEASES, INBORN; HUMANS; I-KAPPA B KINASE; I-KAPPA B PROTEINS; IMMUNOLOGIC DEFICIENCY SYNDROMES; INCONTINENTIA PIGMENTI; MALE; MICE; MUTATION; NF-KAPPA B; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

EID: 23844485308     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00018-005-5031-5     Document Type: Review

References (76)

1. Karin M. and Ben-Neriah Y. (2000) Phosphorylation meets ubiquitination: the control of NF-κB activity. Ann. Rev. Immunol. 18: 621-663
2. Hayden M. S. and Ghosh S. (2004) Signaling to NF-κB. Genes Dev. 18: 2195-2224
3. Chen G., Cao P. and Goeddel D. V. (2002) TNF-induced recruitment and activation of the IKK complex require Cdc37 and Hsp90. Mol. Cell 9: 401-410
4. Ducut Sigala J. L., Bottero V., Young D. B., Shevchenko A., Mercurio F. and Verma I. M. (2004) Activation of transcription factor NF-κB requires ELKS, an IκB kinase regulatory subunit. Science 304: 1963-1967
5. Jin D. and Jeang K. T. (1999) Isolation of full-length cDNA and chromosomal localization of human NF-κB modulator NEMO to Xq28. J. Biochem. Sci. 6: 115-120
6. Yamaoka S., Courtois G., Bessia C., Whiteside S. T., Weil R., Agou F. et al. (1998) Complementation cloning of NEMO, a component of the IκB kinase complex essential for NF-κB activation. Cell 93: 1231-1240
7. Pomerantz J. L. and Baltimore D. (2002) Two pathways to NF-κB. Mol. Cell 10: 693-695
8. Wilkinson K. D. (2003) Signal transduction: aspirin, ubiquitin and cancer. Nature 424: 738-739
9. Beg A. A., Sha W. C., Bronson R. T., Ghosh S. and Baltimore D. (1995) Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-κB. Nature 376: 167-170
10. Li Q. T., Van Antwerp D., Mercurio F., Lee K. F. and Verma I. M. (1999) Severe liver degeneration in mice lacking the IκB kinase 2 gene. Science 284: 321-325
11. Li Z. W., Chu W. M., Hu Y. L., Delhase M., Deerinck T., Ellisman M. et al. (1999) The IKK-β subunit of IκB kinase (IKK) is essential for nuclear factor κB activation and prevention of apoptosis. J. Exp. Med. 189: 1839-1845
12. Tanaka M., Fuentes M. E., Yamaguchi K., Durnin M. H., Dalrymple S. A. and Hardy K. L. (1999) Embryonic lethality, liver degeneration and impaired NF-κB activation in IKK-β-deficient mice. Immunity. 10: 421-429
13. Rudolph D., Yeh W. C., Wakeham A., Rudolph B., Nallainathan D., Elia A. et al. (2000) Severe liver degeneration and lack of NF-κB activation in NEMO/IKKγ-deficient mice. Genes Dev. 14: 854-862
14. Makris C., Godfrey V. L., Krahn-Senftleben G., Takahashi T., Roberts J. L., Schwarz T. et al. (2000) Female mice heterozygous for IKKγ/NEMO deficiencies develop a dermatopathy similar to the human X-linked disorder incontinentia pigmenti. Mol. Cell 5: 969-979
15. Schmidt-Supprian M., Bloch W., Courtois G., Addicks K., Israël A. and Rajewsky K. (2000) NEMO/IKKγ deficient mice model incontinentia pigmenti. Mol. Cell 5: 981-992
16. Gerondakis S., Grossmann M., Nakamura Y., Pohl T. and Grumont R. (1999) Genetic approaches in mice to understand Rel/NF-κB and IκB function: transgenics and knockouts. Oncogene 18: 6888-6895
17. Landi S. J. and Donnai D. (1993) Incontinentia pigmenti (Bloch-Sulzberger syndrome). J. Med. Genet. 30: 53-59
18. van Leeuwen R. L., Wintzen M. and van Praag M. C. (2000) Incontinentia pigmenti: an extensive second episode of a "first-stage" vesicobullous eruption. Pediatr. Dermatol. 17: 70-74
19. Bodak N., Hadj-Rabia S., Hamel-Teillac D., de Prost Y. and Bodemer C. (2003) Late recurrence of inflammatory first-stage lesions in incontinentia pigmenti: an unusual phenomenon and a fascinating pathologic mechanism. Arch. Dermatol. 139: 201-204
20. Coleman R., Genet S. A., Harper J. I. and Wilkie A. O. (1993) Interaction of incontinentia pigmenti and factor VIII mutations in a female with biased X inactivation, resulting in haemophilia. J. Med. Genet. 30: 497-500
21. Smahi A., Courtois G., Vabres P., Yamaoka S., Heuertz S., Munnich A. et al. (2000) Genomic rearrangement in NEMO impairs NF-κB activation and is a cause of incontinentia pigmenti. Nature 405: 466-472
22. Aradhya S., Bardaro T., Galgoczy P., Yamagata T., Esposito T., Patlan H. et al. (2001) Multiple pathogenic and benign genomic rearrangements occur at a 35 kb duplication involving the NEMO and LAGE2 genes. Hum. Mol. Genet. 10: 2557-2567
23. Aradhya S., Woffendin H., Jakins T., Bardaro T., Esposito T., Smahi A. et al. (2001) A recurrent deletion in the ubiquitously expressed NEMO (IKK-γ) gene accounts for the vast majority of incontinentia pigmenti mutations. Hum. Mol. Genet. 10: 2171-2719
24. Fusco F., Bardaro T., Fimiani G., Mercadante V., Miano M.., Falco G. et al. (2004) Molecular analysis of the genetic defect in a large cohort of IP patients and identification of novel NEMO mutations interfering with NF-κB activation. Hum. Mol. Genet. 13: 1763-1673
25. Pasparakis M., Courtois G., Hafner M., Schmidt-Supprian M., Nenci A., Toksoy A. et al. (2002) TNF-mediated inflammatory skin disease in mice with epidermis-specific deletion of IKK2. Nature 417: 861-866
26. Frix C. D. and Bronson D. M. (1986) Acute miliary tuberculosis in a child with anhidrotic ectodermal dysplasia. Pediat. Dermatol. 3: 464-467
27. Sitton J. E. and Reimund E. L. (1992) Extramedullary hematopoieisis of the cranial dura and anhidrotic ectodermal dysplasia. Neuropediatrics 23: 108-110
28. Abinun M., Spickett G., Appleton A. L., Flood T. and Cant A. J. (1996) Anhidrotic ectodermal dysplasia associated with specific antibody deficiency. Eur. J. Pediatr. 155: 146-147
29. Schweizer P., Kalhoff H., Horneff G., Wahn V. and Diekmann L. (1999) Polysaccharide specific humoral immunodeficiency in ectodermal dysplasia. Case report of a boy with two affected brothers. Klin. Padiatr. 211: 459-461
30. Zonana J., Elder M. E., Schneider L. C., Orlow S. J., Moss C. and Golabi M. (2000). A novel X-linked disorder of immune deficiency and hypohidrotic ectodermal dysplasia is allelic to incontinentia pigmenti and due to mutations in IKKγ(NEMO). Am. J. Hum. Genet. 67: 1555-1562
31. Döffinger R., Smahi A., Bessia C., Geissmann F., Feinberg J., Durandy A. et al. (2001) X-linked anhidrotic ectodermal dysplasia with immunodeficiency is caused by impaired NF-κB signaling. Nat. Genet. 27: 277-285
32. Aradhya S., Courtois G., Rajkovic A., Lewis A. L., Levy M., Israël A. et al. (2001) Atypical forms of Incontinentia pigmenti in male individuals result from mutations of a cytosine tract in exon 10 of NEMO (IKK-γ). Am. J. Hum. Genet. 68: 765-771
33. Jain A., Ma C. A., Liu S., Brown M., Cohen J. and Strober W. (2001) Specific missense mutations in NEMO result in hyper-IgM syndrome with hypohydrotic ectodermal dysplasia. Nat. Immunol. 2: 223-228
34. Orange J. S., Brodeur S. R., Jain A., Bonilla F. A., Schneider L. C., Kretschmer R. et al. (2002) Deficient natural killer cell cytotoxicity in patients with IKK-γ/NEMO mutations. J. Clin. Invest. 109: 1501-1509
35. Kaisho T. and Akira S. (2004) Pleiotropic function of Toll-like receptors. Microbes Infect. 6: 1388-1394
36. Pinheiro M. and Freire-Maia N. (1994) Ectodermal dysplasia: a clinical classification and a causal review. Am. J. Med. Genet. 53: 153-162
37. Kere J., Srivastava A. K., Montonen O., Zonana J., Thomas N., Ferguson B. et al. (1996) X-linked anhidrotic (hypohidrotic) ectodermal dysplasia is caused by mutation in a novel transmembrane protein. Nat. Genet. 13: 409-416
38. Montonen O., Ezer S., Saarialho-Kere U. K., Herva R., Karjalainen-Lindsberg M. L. and Kaitila I. (1998) The gene defective in anhidrotic ectodermal dysplasia is expressed in the developing epithelium, neuroectoderm, thymus and bone. J. Histochem. Cytochem. 46: 281-289
39. Ezer S., Bayes M., Elomaa O., Schlessinger D. and Kere J. (1999) Ectodysplasin is a collagenous trimeric type II membrane protein with a tumour necrosis factor-like domain and co-localizes with cytoskeletal structures at lateral and apical surfaces of cells. Hum. Mol. Genet. 8: 2079-2086
40. Mikkola M. L., Pispa J., Pekkanen M., Paulin L., Nieminen P., Kere J. et al. (1999) Ectodysplasin, a protein required for epithelial morphogenesis, is a novel TNF homologue and promotes cell-matrix adhesion. Mech. Dev. 88: 133-146
41. Chen Y., Molloy S. S., Thomas L., Gambee J., Bachinger H. P., Ferguson B. et al. (2001) Mutations within a furin consensus sequence block proteolytic release of ectodysplasin and cause X-linked hypohidrotic ectodermal dysplasia. Proc. Natl. Acad. Sci. USA 98: 7218-7223
42. Elomaa O., Pulkkinen K., Hannelius U., Mikkola M., Saarialho-Kere U. and Kere J. (2001) Ectodysplasin is released by proteolytic shedding and binds to the EDAR protein. Hum. Mol. Genet. 10: 953-962
43. Schneider P., Street S. L., Gaide O., Hertig S., Tardivel A. and Tschopp J. (2001) Mutations leading to X-linked hypohidrotic ectodermal dysplasia affect three major functional domains in the TNF family member EDA. J. Biol. Chem. 276: 18819-18827
44. Headon D. J. and Overbeek P. A. (1999) Involvement of a novel Tnf receptor homologue in hair follicle induction. Nat. Genet. 22: 370-374
45. Monreal A. W., Ferguson B. M., Headon D. J., Street S. L., Overbeek P. A. and Zonana J. (1999) Mutations in the human homologue of mouse dl cause autosomal recessive and dominant hypohidrotic ectodermal dysplasia. Nat. Genet. 22: 366-369
46. Kumar A., Eby M. T., Sinha S., Jasmin A. and Chaudhary P. M. (2000) Ectodermal dysplasia receptor activates the nuclear factor κB, c-Jun N-terminal kinase and cell death pathways and binds to ectodysplasin A. J. Biol. Chem. 276: 2668-2677
47. Tucker A. S., Headon D. J., Schneider P., Ferguson B. M., Overbeek P., Tschopp J. et al. (2000) Edar/Eda interactions regulate enamel knot formation in tooth morphogenesis. Development 127: 4691-4700
48. Yan M. H., Wang L. C., Hymowitz S. G., Schilbach S., Lee J., Goddard A. et al. (2000) Two-amino acid molecular switch in an epithelial morphogen that regulates binding to two distincts receptors. Science 290: 523-527
49. Laurikkala J., Mikkola M., Mustonen T., Aberg T., Koppinen P., Pispa J. et al. (2001) TNF signaling via the ligand-receptor pair ectodysplasin and edar controls the function of epithelia signaling centers and is regulated by Wnt and activin during tooth organogenesis. Dev. Biol. 229: 443-455
50. Headon D. J., Emmal S. A., Ferguson B. M., Tucker A. S., Justice M. J., Sharpe P. T. et al. (2001) Gene defect in ectodermal dysplasia implicates a death domain adapter in development. Nature 414: 913-916
51. Yan M., Zhang Z., Brady J. R., Schilbach S., Fairbrother W. J. and Dixit V. M. (2002) Identification of a novel death domain-containing adaptor molecule for ectodysplasin-A receptor that is mutated in crinkled mice. Curr Biol. 12: 409-413
52. Mansour S., Woffendin H., Mitton S., Jeffery I., Jakins T., Kenwrick S. et al. (2001) Incontinentia pigmenti in a surviving male is accompanied by hypohidrotic ectodermal dysplasia and recurrent infection. Am. J. Med. Genet. 99: 172-177
53. Franzoso G., Carlson L., Xing L., Poljak L., Shores E. W., Brown K. D. et al. (1997) Requirement for NF-κB in osteoclast and B-cell development. Genes Dev. 11: 3482-3496
54. Iotsova V., Caamano J., Loy J., Yang Y., Lewin A. and Bravo R. (1997) Osteopetrosis in mice lacking nf-kappa-b1 and nf-kappa-b2. Nat. Med. 3: 1285-1289
55. Hsu H., Lacey D. L., Dunstan C. R., Solovyev I., Colombero A., Timms E. et al. (1999) Tumor necrosis factor receptor family member RANK mediates osteoclast differentiation and activation induced by osteoprotegerin ligand. Proc. Natl. Acad. Sci. USA 96: 3540-3545
56. Karkkainen M. J., Ferrell R. E., Lawrence E. C., Kimak M. A., Levinson K. L., McTigue M. A. et al. (2000) Missense mutations interfere with VEGFR-3 signaling in primary lymphoedema. Nat. Genet. 25: 153-159
57. Orange J. S., Levy O., Brodeur S. R., Krzewski K., Roy R. M., Niemela J. E. et al. (2004) Human nuclear factor kappa B essential modulator mutation can result in immunodeficiency without ectodermal dysplasia. J. Allergy Clin. Immunol. 114: 650-656
58. Niehues T., Reichenbach J., Neubert J., Gudowius S., Puel A., Horneff G. et al. (2004) Nuclear factor kappaB essential modulator-deficient child with immunodeficiency yet without anhidrotic ectodermal dysplasia. J. Allergy Clin. Immunol. 114: 1456-1462
59. Tobin E., Rohwedder A., Holland S. M., Philips B. and Carlson J. A. (2003). Recurrent 'sterile' verrucous cyst abscesses and epidermodysplasia verruciformis-like eruption associated with idiopathic CD4 lymphopenia. Br. J. Dermatol. 149: 627-633
60. Agou F., Traincard F., Vinolo E., Courtois G., Yamaoka S., Israël A. et al. (2004) The trimerization domain of NEMO is composed of the interacting C-terminal CC2 and LZ coiled-coil subdomains. J. Biol. Chem. 279: 27861-27869
61. Makris C., Roberts J. L. and Karin M. (2002) The carboxyl-terminal region of IκB kinase g (IKKγ) is required for full IKK activation. Mol. Cell. Biol. 22: 6573-6581
62. Courtois G., Smahi A., Reichenbach J., Doffinger R., Cancrini C., Bonnet M. et al. (2003) A hypermorphic IκBα mutation is associated with autosomal dominant anhidrotic ectodermal dysplasia and T cell immunodeficiency. J. Clin. Invest. 112: 1108-1115
63. Janssen R., van Wengen A., Hoeve M. A., ten Dam M., van der Burg M., van Dongen J. et al. (2004) The same IκBα mutation in two related individuals leads to completely different clinical syndromes. J. Exp. Med. 200: 559-568
64. Bignell G. R., Warren W., Seal S., Takahashi M., Rapley E., Barfoot R. et al. (2000) Identification of the familial cylindromatosis tumour-suppressor gene. Nat. Genet. 25: 160-165
65. Poblete Gutierrez P., Eggermann T., Holler D., Jugert F. K., Beermann T., Grussendorf-Conen E. I. et al. (2002) Phenotype diversity in familial cylindromatosis: a frameshift mutation in the tumor suppressor gene CYLD underlies different tumors of skin appendages. J. Invest. Dermatol. 119: 527-531
66. Zheng G., Hu L., Huang W., Chen K., Zhang X., Yang S. et al. (2004) CYLD mutation causes multiple familial trichoepithelioma in three Chinese families. Hum. Mutat. 23: 400
67. Zhang X. J., Liang Y. H., He P. P., Yang S., Wang H. Y., Chen J. J. et al. (2004) Identification of the cylindromatosis tumor-suppressor gene responsible for multiple familial trichoepithelioma. J. Invest. Dermatol. 122: 658-664
68. Salhi A., Bornholdt D., Oeffner F., Malik S., Heid E., Happle R. et al. (2004) Multiple familial trichoepithelioma caused by mutations in the cylindromatosis tumor suppressor gene. Cancer Res. 64: 5113-5117
69. Kovalenko A., Chable-Bessia C., Cantarella G., Israel A., Wallach D. and Courtois G. (2003) The tumour suppressor CYLD negatively regulates NF-κB signalling by deubiquitination. Nature 424: 801-805
70. Trompouki E., Hatzivassiliou E., Tsichritzis T., Farmer H., Ashworth A. and Mosialos G. (2003) CYLD is a deubiquitinating enzyme that negatively regulates NF-κB activation by TNFR family members. Nature 424: 793-796
71. Regamey A., Hohl D., Liu J. W., Roger T., Kogerman P., Toftgard R. et al. (2003) The tumor suppressor CYLD interacts with TRIP and regulates negatively nuclear factor kappaB activation by tumor necrosis factor. J. Exp. Med. 198: 1959-1964
72. Brummelkamp T. R., Nijman S. M., Dirac A. M. and Bernards R. (2003) Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-κB. Nature 424: 797-801
73. Deng L., Wang C., Spencer E., Braun A., You J., Slaughter C. et al. (2000) Activation of the IκB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103: 351-361
74. Wang C., Deng L., Hong M., Akkaraju G. R., Inoue J. and Chen Z. J. (2001) TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412: 346-351
75. Kanayama A., Seth R. B., Sun L., Ea C. K., Hong M., Shaito A. et al. (2004) TAB2 and TAB3 activate the NF-κB pathway through binding to polyubiquitin chains. Mol. Cell 15: 535-548
76. Reiley W., Zhang M. and Sun S. C. (2004) Negative regulation of JNK signaling by the tumor suppressor CYLD. J. Biol. Chem. 279: 55161-55167