Defects of B-cell terminal differentiation in patients with type-1 Kabuki syndrome

Journal of Allergy and Clinical Immunology

Volumn 137, Issue 1, 2016, Pages 179-187.e10

  Lindsley, Andrew W ^a,b   Saal, Howard M ^a,b   Burrow, Thomas A ^a,b   Hopkin, Robert J ^a,b   Shchelochkov, Oleg ^d   Khandelwal, Pooja ^a,b   Xie, Changchun ^c   Bleesing, Jack ^a,b   Filipovich, Lisa ^a,b   Risma, Kimberly ^a,b   Assa'Ad, Amal H ^a,b   Roehrs, Phillip A ^e   Bernstein, Jonathan A ^c  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

^e UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

AICDA; AID; CD21lo B cells; class switch recombination; hypogammaglobulinemia; Kabuki syndrome; KDM6A; KMT2D; memory B cells; polymerase eta; PTIP; somatic hypermutation

Indexed keywords

IMMUNOGLOBULIN G; IMMUNOGLOBULIN MU CHAIN; DNA BINDING PROTEIN; MLL2 PROTEIN, HUMAN; TUMOR PROTEIN;

ADOLESCENT; ADULT; ARTICLE; AUTOIMMUNE DISEASE; CELL DIFFERENTIATION; CHILD; CLINICAL ARTICLE; GENE MUTATION; HETEROZYGOTE; HUMAN; HUMORAL IMMUNE DEFICIENCY; IMMUNOGLOBULIN A DEFICIENCY; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOGLOBULIN DEFICIENCY; INFANT; KABUKI MAKEUP SYNDROME; KMT2D GENE; LYMPHOCYTE FUNCTION; MEMORY CELL; MISSENSE MUTATION; NONSENSE MUTATION; PRESCHOOL CHILD; PRIORITY JOURNAL; RNA SPLICING; SCHOOL CHILD; SOMATIC HYPERMUTATION; YOUNG ADULT; ABNORMALITIES; AGAMMAGLOBULINEMIA; B LYMPHOCYTE; CYTOLOGY; FACE; GENETICS; HEMATOLOGIC DISEASE; IMMUNOLOGY; MULTIPLE MALFORMATION SYNDROME; MUTATION; VESTIBULAR DISORDER;

ABNORMALITIES, MULTIPLE; ADOLESCENT; ADULT; AGAMMAGLOBULINEMIA; B-LYMPHOCYTES; CELL DIFFERENTIATION; CHILD; CHILD, PRESCHOOL; DNA-BINDING PROTEINS; FACE; HEMATOLOGIC DISEASES; HUMANS; INFANT; MUTATION; NEOPLASM PROTEINS; VESTIBULAR DISEASES; YOUNG ADULT;

EID: 84953635139     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2015.06.002     Document Type: Article

References (52)

1. N. Niikawa, N. Matsuura, Y. Fukushima, T. Ohsawa, and T. Kajii Kabuki make-up syndrome: a syndrome of mental retardation, unusual facies, large and protruding ears, and postnatal growth deficiency J Pediatr 99 1981 565 569
2. Y. Kuroki, Y. Suzuki, H. Chyo, A. Hata, and I. Matsui A new malformation syndrome of long palpebral fissures, large ears, depressed nasal tip, and skeletal anomalies associated with postnatal dwarfism and mental retardation J Pediatr 99 1981 570 573
3. N. Matsumoto, and N. Niikawa Kabuki make-up syndrome: a review Am J Med Genet C Semin Med Genet 117C 2003 57 65
4. L. Armstrong, A. Abd El Moneim, K. Aleck, D.J. Aughton, C. Baumann, S.R. Braddock, and et al. Further delineation of Kabuki syndrome in 48 well-defined new individuals Am J Med Genet A 132A 2005 265 272
5. C.T. Schrander-Stumpel, L. Spruyt, L.M. Curfs, T. Defloor, and J.J. Schrander Kabuki syndrome: Clinical data in 20 patients, literature review, and further guidelines for preventive management Am J Med Genet A 132A 2005 234 243
6. H. Kawame, M.C. Hannibal, L. Hudgins, and R.A. Pagon Phenotypic spectrum and management issues in Kabuki syndrome J Pediatr 134 1999 480 485
7. J.D. Hoffman, K.L. Ciprero, K.E. Sullivan, P.B. Kaplan, D.M. McDonald-McGinn, E.H. Zackai, and et al. Immune abnormalities are a frequent manifestation of Kabuki syndrome Am J Med Genet A 135 2005 278 281
8. J.E. Ming, K.L. Russell, D.M. McDonald-McGinn, and E.H. Zackai Autoimmune disorders in Kabuki syndrome Am J Med Genet A 132A 2005 260 262
9. N. Bogershausen, and B. Wollnik Unmasking Kabuki syndrome Clin Genet 83 2013 201 211
10. S.B. Ng, A.W. Bigham, K.J. Buckingham, M.C. Hannibal, M.J. McMillin, H.I. Gildersleeve, and et al. Exome sequencing identifies MLL2 mutations as a cause of Kabuki syndrome Nat Genet 42 2010 790 793
11. D. Lederer, B. Grisart, M.C. Digilio, V. Benoit, M. Crespin, S.C. Ghariani, and et al. Deletion of KDM6A, a histone demethylase interacting with MLL2, in three patients with Kabuki syndrome Am J Hum Genet 90 2012 119 124
12. I. Issaeva, Y. Zonis, T. Rozovskaia, K. Orlovsky, C.M. Croce, T. Nakamura, and et al. Knockdown of ALR (MLL2) reveals ALR target genes and leads to alterations in cell adhesion and growth Mol Cell Biol 27 2007 1889 1903
13. K.I. Ansari, and S.S. Mandal Mixed lineage leukemia: roles in gene expression, hormone signaling and mRNA processing FEBS J 277 2010 1790 1804
14. E. Smith, C. Lin, and A. Shilatifard The super elongation complex (SEC) and MLL in development and disease Genes Dev 25 2011 661 672
15. M.G. Lee, R. Villa, P. Trojer, J. Norman, K.P. Yan, D. Reinberg, and et al. Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination Science 318 2007 447 450
16. C. Guo, C.C. Chang, M. Wortham, L.H. Chen, D.N. Kernagis, X. Qin, and et al. Global identification of MLL2-targeted loci reveals MLL2's role in diverse signaling pathways Proc Natil Acad Sci U S A 109 2012 17603 17608
17. D. Hu, X. Gao, M.A. Morgan, H.M. Herz, E.R. Smith, and A. Shilatifard The MLL3/MLL4 branches of the COMPASS family function as major histone H3K4 monomethylases at enhancers Mol Cell Biol 33 2013 4745 4754
18. Y.W. Cho, T. Hong, S. Hong, H. Guo, H. Yu, D. Kim, and et al. PTIP associates with MLL3- and MLL4-containing histone H3 lysine 4 methyltransferase complex J Biol Chem 282 2007 20395 20406
19. K.R. Schwab, S.R. Patel, and G.R. Dressler Role of PTIP in class switch recombination and long-range chromatin interactions at the immunoglobulin heavy chain locus Mol Cell Biol 31 2011 1503 1511
20. J.A. Daniel, M.A. Santos, Z. Wang, C. Zang, K.R. Schwab, M. Jankovic, and et al. PTIP promotes chromatin changes critical for immunoglobulin class switch recombination Science 329 2010 917 923
21. Y. Li, N. Bogershausen, Y. Alanay, P.O. Simsek Kiper, N. Plume, K. Keupp, and et al. A mutation screen in patients with Kabuki syndrome Hum Genet 130 2011 715 724
22. L. Micale, B. Augello, C. Fusco, A. Selicorni, M.N. Loviglio, M.C. Silengo, and et al. Mutation spectrum of MLL2 in a cohort of Kabuki syndrome patients Orphanet J Rare Dis 6 2011 38
23. S. Banka, R. Veeramachaneni, W. Reardon, E. Howard, S. Bunstone, N. Ragge, and et al. How genetically heterogeneous is Kabuki syndrome?: MLL2 testing in 116 patients, review and analyses of mutation and phenotypic spectrum Eur J Hum Genet 20 2012 381 388
24. J.L. Lin, W.I. Lee, J.L. Huang, P.K. Chen, K.C. Chan, L.J. Lo, and et al. Immunologic assessment and KMT2D mutation detection in Kabuki syndrome Clin Genet 2014 [Epub ahead of print]
25. F. Brackmann, M. Krumbholz, T. Langer, W. Rascher, W. Holter, and M. Metzler Novel MLL2 mutation in Kabuki syndrome with hypogammaglobulinemia and severe chronic thrombopenia J Pediatr Hematol Oncol 35 2013 e314 e316
26. P. Giordano, G. Lassandro, M. Sangerardi, M.F. Faienza, F. Valente, and B. Martire Autoimmune haematological disorders in two Italian children with Kabuki syndrome Ital J Pediatr 40 2014 10
27. N.A. Begum, A. Stanlie, M. Nakata, H. Akiyama, and T. Honjo The histone chaperone Spt6 is required for activation-induced cytidine deaminase target determination through H3K4me3 regulation J Biol Chem 287 2012 32415 32429
28. S.P. Bradley, D.A. Kaminski, A.H. Peters, T. Jenuwein, and J. Stavnezer The histone methyltransferase Suv39h1 increases class switch recombination specifically to IgA J Immunol 177 2006 1179 1188
29. W. Beguelin, R. Popovic, M. Teater, Y. Jiang, K.L. Bunting, M. Rosen, and et al. EZH2 is required for germinal center formation and somatic EZH2 mutations promote lymphoid transformation Cancer cell 23 2013 677 692
30. M.G. Reese, F.H. Eeckman, D. Kulp, and D. Haussler Improved splice site detection in Genie J Comput Biol 4 1997 311 323
31. J.J. van Dongen, A.W. Langerak, M. Bruggemann, P.A. Evans, M. Hummel, F.L. Lavender, and et al. Design and standardization of PCR primers and protocols for detection of clonal immunoglobulin and T-cell receptor gene recombinations in suspect lymphoproliferations: report of the BIOMED-2 Concerted Action BMH4-CT98-3936 Leukemia 17 2003 2257 2317
32. M.A. Berkowska, G.J. Driessen, V. Bikos, C. Grosserichter-Wagener, K. Stamatopoulos, A. Cerutti, and et al. Human memory B cells originate from three distinct germinal center-dependent and -independent maturation pathways Blood 118 2011 2150 2158
33. P. Ruminy, P. Etancelin, L. Couronne, F. Parmentier, V. Rainville, S. Mareschal, and et al. The isotype of the BCR as a surrogate for the GCB and ABC molecular subtypes in diffuse large B-cell lymphoma Leukemia 25 2011 681 688
34. J. Ye, N. Ma, T.L. Madden, and J.M. Ostell IgBLAST: an immunoglobulin variable domain sequence analysis tool Nucleic Acids Res 41 Web Server issue 2013 W34 W40
35. T. Maccarthy, S. Roa, M.D. Scharff, and A. Bergman SHMTool: a webserver for comparative analysis of somatic hypermutation datasets DNA Repair 8 2009 137 141
36. R. Ettinger, G.P. Sims, A.M. Fairhurst, R. Robbins, Y.S. da Silva, R. Spolski, and et al. IL-21 induces differentiation of human naive and memory B cells into antibody-secreting plasma cells J Immunol 175 2005 7867 7879
37. N. Niikawa, Y. Kuroki, T. Kajii, N. Matsuura, S. Ishikiriyama, H. Tonoki, and et al. Kabuki make-up (Niikawa-Kuroki) syndrome: a study of 62 patients Am J Med Genet 31 1988 565 589
38. L. Micale, B. Augello, C. Maffeo, A. Selicorni, F. Zucchetti, C. Fusco, and et al. Molecular analysis, pathogenic mechanisms, and readthrough therapy on a large cohort of Kabuki syndrome patients Hum Mutat 35 2014 841 850
39. S.A. Shinsky, M. Hu, V.E. Vought, S.B. Ng, M.J. Bamshad, J. Shendure, and et al. A non-active-site SET domain surface crucial for the interaction of MLL1 and the RbBP5/Ash2L heterodimer within MLL family core complexes J Mol Biol 426 2014 2283 2299
40. C. Cunningham-Rundles Autoimmune manifestations in common variable immunodeficiency J Clin Immunol 28 suppl 1 2008 S42 S45
41. W.M. Comans-Bitter, R. de Groot, R. van den Beemd, H.J. Neijens, W.C. Hop, K. Groeneveld, and et al. Immunophenotyping of blood lymphocytes in childhood. Reference values for lymphocyte subpopulations J Pediatr 130 1997 388 393
42. J.S. Orange, M. Ballow, E.R. Stiehm, Z.K. Ballas, J. Chinen, M. De La Morena, and et al. Use and interpretation of diagnostic vaccination in primary immunodeficiency: a working group report of the Basic and Clinical Immunology Interest Section of the American Academy of Allergy, Asthma & Immunology J Allergy Clin Immunol 130 suppl 2012 S1 S24
43. C. Wehr, T. Kivioja, C. Schmitt, B. Ferry, T. Witte, E. Eren, and et al. The EUROclass trial: defining subgroups in common variable immunodeficiency Blood 111 2008 77 85
44. J.C. Weill, S. Weller, and C.A. Reynaud Human marginal zone B cells Annu Rev Immunol 27 2009 267 285
45. J.F. Fecteau, G. Cote, and S. Neron A new memory CD27-IgG+ B cell population in peripheral blood expressing VH genes with low frequency of somatic mutation J Immunol 177 2006 3728 3736
46. Y. Chong, H. Ikematsu, K. Yamaji, M. Nishimura, S. Kashiwagi, and J. Hayashi Age-related accumulation of Ig V(H) gene somatic mutations in peripheral B cells from aged humans Clin Exp Immunol 133 2003 59 66
47. U. Klein, R. Kuppers, and K. Rajewsky Evidence for a large compartment of IgM-expressing memory B cells in humans Blood 89 1997 1288 1298
48. M. Bemark, P. Boysen, and N.Y. Lycke Induction of gut IgA production through T cell-dependent and T cell-independent pathways Ann N Y Acad Sci 1247 2012 97 116
49. G.M. Borchert, N.W. Holton, K.A. Edwards, L.A. Vogel, and E.D. Larson Histone H2A and H2B are monoubiquitinated at AID-targeted loci PLoS One 5 2010 e11641
50. A. Stanlie, M. Aida, M. Muramatsu, T. Honjo, and N.A. Begum Histone3 lysine4 trimethylation regulated by the facilitates chromatin transcription complex is critical for DNA cleavage in class switch recombination Proc Natl Acad Sci U S A 107 2010 22190 22195
51. G. Li, H. Zan, Z. Xu, and P. Casali Epigenetics of the antibody response Trends Immunol 34 2013 460 470
52. K. Helin, and D. Dhanak Chromatin proteins and modifications as drug targets Nature 502 2013 480 488