NEMO is a key component of NF-κB- and IRF-3-dependent TLR3-mediated immunity to herpes simplex virus

Journal of Allergy and Clinical Immunology

Volumn 128, Issue 3, 2011, Pages

  Audry, Magali ^a   Ciancanelli, Michael ^a   Yang, Kun ^b,c   Cobat, Aurelie ^b   Chang, Huey Hsuan ^b   Sancho Shimizu, Vanessa ^b   Lorenzo, Lazaro ^b   Niehues, Tim ^d   Reichenbach, Janine ^e   Li, Xiao Xia ^f   Israel, Alain ^g   Abel, Laurent ^a,b   Casanova, Jean Laurent ^a,b,c,h   Zhang, Shen Ying ^a,b,c   Jouanguy, Emmanuelle ^a,b,c   Puel, Anne ^b  

^a ROCKEFELLER UNIVERSITY   (United States)

^b IMAGINE INSTITUTE   (France)

^c SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^d HEINRICH HEINE UNIVERSITY   (Germany)

^e UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^f LERNER RESEARCH INSTITUTE   (United States)

^g INSTITUT PASTEUR   (France)

^h HÔPITAL NECKER ENFANTS MALADES   (France)

Author keywords

herpes simplex encephalitis; immunodeficiency; NEMO; Toll like receptor 3

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 1; ALPHA INTERFERON; BETA INTERFERON; CYTOKINE; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 6; MESSENGER RNA; PROTEIN; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR AGONIST;

ARTICLE; CASE REPORT; CELL LEVEL; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DIMERIZATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FETUS; FIBROBLAST; GEL; GEL MOBILITY SHIFT ASSAY; GENE MUTATION; HERPES SIMPLEX ENCEPHALITIS; HERPES SIMPLEX VIRUS; HUMAN; HUMAN CELL; MOLECULAR BIOLOGY; PATHOGENESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; VESICULAR STOMATITIS VIRUS;

EID: 80052273575     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2011.04.059     Document Type: Article

References (67)

1. A. Smahi, G. Courtois, P. Vabres, S. Yamaoka, S. Heuertz, and A. Munnich Genomic rearrangement in NEMO impairs NF-kappaB activation and is a cause of incontinentia pigmenti. The International Incontinentia Pigmenti (IP) Consortium Nature 405 2000 466 472 (Pubitemid 30367424)
2. S. Aradhya, G. Courtois, A. Rajkovic, R.A. Lewis, M. Levy, and A. Israel Atypical forms of incontinentia pigmenti in male individuals result from mutations of a cytosine tract in exon 10 of NEMO (IKK-gamma) Am J Hum Genet 68 2001 765 771 (Pubitemid 32202769)
3. F. Fusco, T. Bardaro, G. Fimiani, V. Mercadante, M.G. Miano, and G. Falco Molecular analysis of the genetic defect in a large cohort of IP patients and identification of novel NEMO mutations interfering with NF-kappaB activation Hum Mol Genet 13 2004 1763 1773 (Pubitemid 39173445)
4. M. Abinun, G. Spickett, A.L. Appleton, T. Flood, and A.J. Cant Anhidrotic ectodermal dysplasia associated with specific antibody deficiency Eur J Pediatr 155 1996 146 147 (Pubitemid 26043007)
5. R. Doffinger, A. Smahi, C. Bessia, F. Geissmann, J. Feinberg, and A. Durandy X-linked anhidrotic ectodermal dysplasia with immunodeficiency is caused by impaired NF-kappaB signaling Nat Genet 27 2001 277 285 (Pubitemid 32201848)
6. J.S. Orange, S.R. Brodeur, A. Jain, F.A. Bonilla, L.C. Schneider, and R. Kretschmer Deficient natural killer cell cytotoxicity in patients with IKK-gamma/NEMO mutations J Clin Invest 109 2002 1501 1509 (Pubitemid 34596176)
7. S. Dupuis-Girod, N. Corradini, S. Hadj-Rabia, J.C. Fournet, L. Faivre, and F. Le Deist Osteopetrosis, lymphedema, anhidrotic ectodermal dysplasia, and immunodeficiency in a boy and incontinentia pigmenti in his mother Pediatrics 109 2002 e97
8. A. Jain, C.A. Ma, S. Liu, M. Brown, J. Cohen, and W. Strober Specific missense mutations in NEMO result in hyper-IgM syndrome with hypohydrotic ectodermal dysplasia Nat Immunol 2 2001 223 228 (Pubitemid 33705998)
9. K. Kosaki, N. Shimasaki, H. Fukushima, M. Hara, T. Ogata, and N. Matsuo Female patient showing hypohidrotic ectodermal dysplasia and immunodeficiency (HED-ID) Am J Hum Genet 69 2001 664 666
10. J.S. Orange, O. Levy, S.R. Brodeur, K. Krzewski, R.M. Roy, and J.E. Niemela Human nuclear factor kappa B essential modulator mutation can result in immunodeficiency without ectodermal dysplasia J Allergy Clin Immunol 114 2004 650 656 (Pubitemid 39194943)
11. S. Mansour, H. Woffendin, S. Mitton, I. Jeffery, T. Jakins, and S. Kenwrick Incontinentia pigmenti in a surviving male is accompanied by hypohidrotic ectodermal dysplasia and recurrent infection Am J Med Genet 99 2001 172 177
12. C.L. Ku, S. Dupuis-Girod, A.M. Dittrich, J. Bustamante, O.F. Santos, and I. Schulze NEMO mutations in 2 unrelated boys with severe infections and conical teeth Pediatrics 115 2005 e615 e619
13. A. Puel, C. Picard, C.L. Ku, A. Smahi, and J.L. Casanova Inherited disorders of NF-kappaB-mediated immunity in man Curr Opin Immunol 16 2004 34 41 (Pubitemid 38198115)
14. T. Niehues, J. Reichenbach, J. Neubert, S. Gudowius, A. Puel, and G. Horneff Nuclear factor kappaB essential modulator-deficient child with immunodeficiency yet without anhidrotic ectodermal dysplasia J Allergy Clin Immunol 114 2004 1456 1462 (Pubitemid 39575905)
15. A. Puel, J. Reichenbach, J. Bustamante, C.L. Ku, J. Feinberg, and R. Doffinger The NEMO mutation creating the most-upstream premature stop codon is hypomorphic because of a reinitiation of translation Am J Hum Genet 78 2006 691 701
16. J.L. Mooster, C. Cancrini, A. Simonetti, P. Rossi, G. Di Matteo, and M.L. Romiti Immune deficiency caused by impaired expression of nuclear factor-kappaB essential modifier (NEMO) because of a mutation in the 5' untranslated region of the NEMO gene J Allergy Clin Immunol 126 2010 127 132.e7
17. C.L. Ku, K. Yang, J. Bustamante, A. Puel, H. von Bernuth, and O.F. Santos Inherited disorders of human Toll-like receptor signaling: immunological implications Immunol Rev 203 2005 10 20 (Pubitemid 40179690)
18. J. Zonana, M.E. Elder, L.C. Schneider, S.J. Orlow, C. Moss, and M. Golabi 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 2000 1555 1562
19. J.S. Orange, A. Jain, Z.K. Ballas, L.C. Schneider, R.S. Geha, and F.A. Bonilla The presentation and natural history of immunodeficiency caused by nuclear factor kappaB essential modulator mutation J Allergy Clin Immunol 113 2004 725 733 (Pubitemid 38530430)
20. E.D. Carrol, A.R. Gennery, T.J. Flood, G.P. Spickett, and M. Abinun Anhidrotic ectodermal dysplasia and immunodeficiency: the role of NEMO Arch Dis Child 88 2003 340 341 (Pubitemid 36398977)
21. R. Nishikomori, H. Akutagawa, K. Maruyama, M. Nakata-Hizume, K. Ohmori, and K. Mizuno X-linked ectodermal dysplasia and immunodeficiency caused by reversion mosaicism of NEMO reveals a critical role for NEMO in human T-cell development and/or survival Blood 103 2004 4565 4572 (Pubitemid 38745984)
22. C.L. Ku, H. von Bernuth, C. Picard, S.Y. Zhang, H.H. Chang, and K. Yang Selective predisposition to bacterial infections in IRAK-4-deficient children: IRAK-4-dependent TLRs are otherwise redundant in protective immunity J Exp Med 204 2007 2407 2422 (Pubitemid 47529326)
23. O. Filipe-Santos, J. Bustamante, A. Chapgier, G. Vogt, L. de Beaucoudrey, and J. Feinberg Inborn errors of IL-12/23- and IFN-gamma-mediated immunity: molecular, cellular, and clinical features Semin Immunol 18 2006 347 361 (Pubitemid 44540199)
24. O. Filipe-Santos, J. Bustamante, M.H. Haverkamp, E. Vinolo, C.L. Ku, and A. Puel X-linked susceptibility to mycobacteria is caused by mutations in NEMO impairing CD40-dependent IL-12 production J Exp Med 203 2006 1745 1759 (Pubitemid 44036280)
25. J. Feinberg, C. Fieschi, R. Doffinger, M. Feinberg, T. Leclerc, and S. Boisson-Dupuis Bacillus Calmette Guerin triggers the IL-12/IFN-gamma axis by an IRAK-4- and NEMO-dependent, non-cognate interaction between monocytes, NK, and T lymphocytes Eur J Immunol 34 2004 3276 3284 (Pubitemid 39549406)
26. A.E. Medvedev, A. Lentschat, D.B. Kuhns, J.C. Blanco, C. Salkowski, and S. Zhang Distinct mutations in IRAK-4 confer hyporesponsiveness to lipopolysaccharide and interleukin-1 in a patient with recurrent bacterial infections J Exp Med 198 2003 521 531 (Pubitemid 37040387)
27. C. Picard, A. Puel, M. Bonnet, C.L. Ku, J. Bustamante, and K. Yang Pyogenic bacterial infections in humans with IRAK-4 deficiency Science 299 2003 2076 2079 (Pubitemid 36383736)
28. H. von Bernuth, C. Picard, Z. Jin, R. Pankla, H. Xiao, and C.L. Ku Pyogenic bacterial infections in humans with MyD88 deficiency Science 321 2008 691 696
29. C. Picard, H. von Bernuth, P. Ghandil, M. Chrabieh, O. Levy, and P.D. Arkwright Clinical features and outcome of patients with IRAK-4 and MyD88 deficiency Medicine 89 2010 403 425
30. D.R. McDonald, D. Brown, F.A. Bonilla, and R.S. Geha Interleukin receptor-associated kinase-4 deficiency impairs Toll-like receptor-dependent innate antiviral immune responses J Allergy Clin Immunol 118 2006 1357 1362 (Pubitemid 44854118)
31. V. Sancho-Shimizu, S.Y. Zhang, L. Abel, M. Tardieu, F. Rozenberg, and E. Jouanguy Genetic susceptibility to herpes simplex virus 1 encephalitis in mice and humans Curr Opin Allergy Clin Immunol 7 2007 495 505 (Pubitemid 350076444)
32. R.J. Whitley Herpes simplex encephalitis: adolescents and adults Antiviral Res 71 2006 141 148 (Pubitemid 44226488)
33. S. Dupuis, E. Jouanguy, S. Al-Hajjar, C. Fieschi, I.Z. Al-Mohsen, and S. Al-Jumaah Impaired response to interferon-alpha/beta and lethal viral disease in human STAT1 deficiency Nat Genet 33 2003 388 391 (Pubitemid 36278855)
34. A. Chapgier, X.F. Kong, S. Boisson-Dupuis, E. Jouanguy, D. Averbuch, and J. Feinberg A partial form of recessive STAT1 deficiency in humans J Clin Invest 119 2009 1502 1514
35. A. Casrouge, S.Y. Zhang, C. Eidenschenk, E. Jouanguy, A. Puel, and K. Yang Herpes simplex virus encephalitis in human UNC-93B deficiency Science 314 2006 308 312 (Pubitemid 44571977)
36. S.Y. Zhang, E. Jouanguy, S. Ugolini, A. Smahi, G. Elain, and P. Romero TLR3 deficiency in patients with herpes simplex encephalitis Science 317 2007 1522 1527 (Pubitemid 47417427)
37. R. Perez de Diego, V. Sancho-Chimizu, L. Lorenzo, A. Puel, S. Plancoulaine, and C. Picard Impaired TLR3 response and herpes simplex encephalitis in human TRAF3 deficiency Immunity 33 2010 400 411
38. K. Yang, A. Puel, S. Zhang, C. Eidenschenk, C.L. Ku, and A. Casrouge Human TLR-7-, -8-, and -9-mediated induction of IFN-alpha/beta and -lambda is IRAK-4 dependent and redundant for protective immunity to viruses Immunity 23 2005 465 478 (Pubitemid 41587887)
39. J.L. Casanova, and L. Abel Primary immunodeficiencies: a field in its infancy Science 317 2007 617 619 (Pubitemid 47229951)
40. A. Alcais, L. Quintana-Murci, D.S. Thaler, E. Schurr, L. Abel, and J.L. Casanova Life-threatening infectious diseases of childhood: single-gene inborn errors of immunity? Ann N Y Acad Sci 1214 2010 18 33
41. A. Smahi, G. Courtois, S.H. Rabia, R. Doffinger, C. Bodemer, and A. Munnich The NF-kappaB signalling pathway in human diseases: from incontinentia pigmenti to ectodermal dysplasias and immune-deficiency syndromes Hum Mol Genet 11 2002 2371 2375 (Pubitemid 35174700)
42. Sweeney SE, Kimbler TB, Firestein GS. Synoviocyte innate immune responses: II. Pivotal role of IFN regulatory factor 3. J Immunol;184:7162-8.
43. T. Zhao, L. Yang, Q. Sun, M. Arguello, D.W. Ballard, and J. Hiscott The NEMO adaptor bridges the nuclear factor-kappaB and interferon regulatory factor signaling pathways Nat Immunol 8 2007 592 600 (Pubitemid 46785123)
44. K. Honda, H. Yanai, H. Negishi, M. Asagiri, M. Sato, and T. Mizutani IRF-7 is the master regulator of type-I interferon-dependent immune responses Nature 434 2005 772 777 (Pubitemid 44739521)
45. S.Y. Zhang, S. Boisson-Dupuis, A. Chapgier, K. Yang, J. Bustamante, and A. Puel Inborn errors of interferon (IFN)-mediated immunity in humans: insights into the respective roles of IFN-alpha/beta, IFN-gamma, and IFN-lambda in host defense Immunol Rev 226 2008 29 40
46. S.Y. Zhang, E. Jouanguy, V. Sancho-Shimizu, H. von Bernuth, K. Yang, and L. Abel Human Toll-like receptor-dependent induction of interferons in protective immunity to viruses Immunol Rev 220 2007 225 236 (Pubitemid 350045567)
47. S. Sharma, B.R. tenOever, N. Grandvaux, G.P. Zhou, R. Lin, and J. Hiscott Triggering the interferon antiviral response through an IKK-related pathway Science 300 2003 1148 1151 (Pubitemid 36583100)
48. K.A. Fitzgerald, S.M. McWhirter, K.L. Faia, D.C. Rowe, E. Latz, and D.T. Golenbock IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway Nat Immunol 4 2003 491 496 (Pubitemid 36592443)
49. A. Chariot, A. Leonardi, J. Muller, M. Bonif, K. Brown, and U. Siebenlist Association of the adaptor TANK with the I kappa B kinase (IKK) regulator NEMO connects IKK complexes with IKK epsilon and TBK1 kinases J Biol Chem 277 2002 37029 37036
50. E.P. Hanson, L. Monaco-Shawver, L.A. Solt, L.A. Madge, P.P. Banerjee, and M.J. May Hypomorphic nuclear factor-kappaB essential modulator mutation database and reconstitution system identifies phenotypic and immunologic diversity J Allergy Clin Immunol 122 2008 1169 1177 e16
51. C.L. Ku, C. Picard, M. Erdos, A. Jeurissen, J. Bustamante, and A. Puel IRAK4 and NEMO mutations in otherwise healthy children with recurrent invasive pneumococcal disease J Med Genet 44 2007 16 23 (Pubitemid 46142834)
52. T.T. Chang, R. Behshad, R.T. Brodell, and A.C. Gilliam A male infant with anhidrotic ectodermal dysplasia/immunodeficiency accompanied by incontinentia pigmenti and a mutation in the NEMO pathway J Am Acad Dermatol 58 2008 316 320
53. A. Jain, C.A. Ma, E. Lopez-Granados, G. Means, W. Brady, and J.S. Orange Specific NEMO mutations impair CD40-mediated c-Rel activation and B cell terminal differentiation J Clin Invest 114 2004 1593 1602 (Pubitemid 40385550)
54. W.I. Lee, T.R. Torgerson, M.J. Schumacher, L. Yel, Q. Zhu, and H.D. Ochs Molecular analysis of a large cohort of patients with the hyper immunoglobulin M (IgM) syndrome Blood 105 2005 1881 1890 (Pubitemid 40731768)
55. A.J. Mancini, L.P. Lawley, and G. Uzel X-linked ectodermal dysplasia with immunodeficiency caused by NEMO mutation: early recognition and diagnosis Arch Dermatol 144 2008 342 346 (Pubitemid 351439117)
56. J.M. Schmid, S.A. Junge, J.P. Hossle, E.M. Schneider, E. Roosnek, and R.A. Seger Transient hemophagocytosis with deficient cellular cytotoxicity, monoclonal immunoglobulin M gammopathy, increased T-cell numbers, and hypomorphic NEMO mutation Pediatrics 117 2006 e1049 e1056
57. Y.S. Dai, M.G. Liang, S.E. Gellis, F.A. Bonilla, L.C. Schneider, and R.S. Geha Characteristics of mycobacterial infection in patients with immunodeficiency and nuclear factor-kappaB essential modulator mutation, with or without ectodermal dysplasia J Am Acad Dermatol 51 2004 718 722 (Pubitemid 39516884)
58. D.M. Frucht, and S.M. Holland Defective monocyte costimulation for IFN-gamma production in familial disseminated Mycobacterium avium complex infection: abnormal IL-12 regulation J Immunol 157 1996 411 416
59. D.M. Frucht, D.I. Sandberg, M.R. Brown, S.M. Gerstberger, and S.M. Holland IL-12-Independent costimulation pathways for interferon-gamma production in familial disseminated Mycobacterium avium complex infection Clin Immunol 91 1999 234 241 (Pubitemid 29203423)
60. M.H. Haverkamp, S.M. Arend, J.A. Lindeboom, N.G. Hartwig, and J.T. van Dissel Nontuberculous mycobacterial infection in children: a 2-year prospective surveillance study in the Netherlands Clin Infect Dis 39 2004 450 456 (Pubitemid 39120915)
61. S.M. Holland, E.M. Eisenstein, D.B. Kuhns, M.L. Turner, T.A. Fleisher, and W. Strober Treatment of refractory disseminated nontuberculous mycobacterial infection with interferon gamma. A preliminary report N Engl J Med 330 1994 1348 1355
62. S.O. Lie, S. Froland, P. Brandtzaeg, B. Vandvik, and J. Steen-Johnsen Transient B cell immaturity with intractable diarrhoea: a possible new immunodeficiency syndrome J Inherit Metab Dis 1 1978 137 143 (Pubitemid 10070609)
63. N. Martinez-Pomar, I. Munoz-Saa, D. Heine-Suner, A. Martin, A. Smahi, and N. Matamoros A new mutation in exon 7 of NEMO gene: late skewed X-chromosome inactivation in an incontinentia pigmenti female patient with immunodeficiency Hum Genet 118 2005 458 465 (Pubitemid 43091216)
64. J.S. Orange, O. Levy, and R.S. Geha Human disease resulting from gene mutations that interfere with appropriate nuclear factor-kappaB activation Immunol Rev 203 2005 21 37 (Pubitemid 40179691)
65. B.H. Salt, J.E. Niemela, R. Pandey, E.P. Hanson, R.P. Deering, and R. Quinones IKBKG (nuclear factor-kappa B essential modulator) mutation can be associated with opportunistic infection without impairing Toll-like receptor function J Allergy Clin Immunol 121 2008 976 982
66. A. Alcais, L. Abel, and J.L. Casanova Human genetics of infectious diseases: between proof of principle and paradigm J Clin Invest 119 2009 2506 2514
67. Abel L, Plancoulaine S, Jouanguy E, Zhang SY, Mahfoufi N, Nicolas N, et al. Age-dependent Mendelian predisposition to herpes simplex virus type 1 encephalitis in childhood. J Pediatr;157:623-9, 9.e1.