Genetic, Cellular and Clinical Features of ICF Syndrome: a French National Survey

Journal of Clinical Immunology

Volumn 36, Issue 2, 2016, Pages 149-159

  Sterlin, Delphine ^a   Velasco, Guillaume ^b   Moshous, Despina ^c,d   Touzot, Fabien ^a,c,d   Mahlaoui, Nizar ^a,c   Fischer, Alain ^a,c,d,e   Suarez, Felipe ^a,c,f   Francastel, Claire ^b   Picard, Capucine ^a,c,d  

^a HÔPITAL NECKER ENFANTS MALADES   (France)

^b Université Sorbonne Paris Cité   (France)

^c ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^d IMAGINE INSTITUTE   (France)

^e Centre de Recherche Interdisciplinaire en Biologie   (France)

^f CNRS   (France)

Author keywords

autoimmune disease; centromeric instability; ICF syndrome; memory B cells; primary immunodeficiency

Indexed keywords

ALEMTUZUMAB; ALKALINE PHOSPHATASE; CEPHALOSPORIN; CORTICOSTEROID; COTRIMOXAZOLE; CYCLOSPORIN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; DNA METHYLTRANSFERASE 3B; FLUDARABINE; GAMMA GLUTAMYLTRANSFERASE; GANCICLOVIR; GENOMIC DNA; GROWTH HORMONE; IMMUNOGLOBULIN G; IMMUNOSUPPRESSIVE AGENT; IRON; MACROLIDE; PENICILLIN DERIVATIVE; TACROLIMUS; TUMOR NECROSIS FACTOR ANTIBODY;

ADOLESCENT; ADULT; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ANTIBIOTIC PROPHYLAXIS; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNE HEPATITIS; AUTOIMMUNE NEPHRITIS; AUTOIMMUNE THYROIDITIS; B LYMPHOCYTE; BACTERIAL INFECTION; BRONCHIECTASIS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHILD; CLINICAL ARTICLE; CLINICAL FEATURE; COHORT ANALYSIS; CYTOMEGALOVIRUS INFECTION; DNMT3B GENE; EAR NOSE THROAT DISEASE; EPIDEMIOLOGICAL DATA; FACE DYSMORPHIA; FAILURE TO THRIVE; FEMALE; GASTROINTESTINAL DISEASE; GENE MUTATION; GRAFT VERSUS HOST REACTION; GROWTH DISORDER; HEALTH SURVEY; HEREDITY; HETEROZYGOTE; HOMOZYGOTE; HUMAN; HUMORAL IMMUNITY; IMMUNE DEFICIENCY; IMMUNODEFICIENCY CENTROMERIC INSTABILITY AND FACIAL DYSMORPHISM SYNDROME; IMMUNOGLOBULIN DEFICIENCY; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOTHERAPY; INFANT; INFECTION; INFLAMMATORY CELL; IRON DEFICIENCY ANEMIA; MACROPHAGE; MALE; MEMORY CELL; MENTAL DEFICIENCY; MISSENSE MUTATION; MYCOSIS; NEPHRITIS; NONSENSE MUTATION; PANCYTOPENIA; PHENOTYPE; PHYSIOTHERAPY; PRIORITY JOURNAL; PSORIASIS; RECURRENT INFECTION; RESPIRATORY TRACT DISEASE; SPLICING DEFECT; VIRUS INFECTION; ZBTB24 GENE; AUTOIMMUNITY; DISEASE MANAGEMENT; FRANCE; GENETIC PREDISPOSITION; GENETIC SCREENING; IMMUNOLOGIC DEFICIENCY SYNDROMES; IMMUNOLOGICAL PROCEDURES; MUTATION; NEWBORN; OUTCOME ASSESSMENT; PRESCHOOL CHILD;

AUTOIMMUNITY; CHILD; CHILD, PRESCHOOL; DISEASE MANAGEMENT; FEMALE; FRANCE; GENETIC PREDISPOSITION TO DISEASE; GENETIC TESTING; HUMANS; IMMUNOLOGIC DEFICIENCY SYNDROMES; IMMUNOLOGIC TESTS; INFANT; INFANT, NEWBORN; INFECTION; MALE; MUTATION; OUTCOME ASSESSMENT (HEALTH CARE); PHENOTYPE; POPULATION SURVEILLANCE;

EID: 84959246098     PISSN: 02719142     EISSN: 15732592     Source Type: Journal    
DOI: 10.1007/s10875-016-0240-2     Document Type: Article

References (73)

1. Tiepolo L, Maraschio P, Gimelli G, Cuoco C, Gargani GF, Romano C Multibranched chromosomes 1, 9, and 16 in a patient with combined IgA and IgE deficiency. Hum Genet. 1979;51:127–37.
2. Blanco-Betancourt CE, Moncla A, Milili M, Jiang YL, Viegas-Pequignot EM, Roquelaure B, Thuret I, Schiff C Defective B-cell-negative selection and terminal differentiation in the ICF syndrome. Blood. 2004;103:2683–90.
3. Franceschini P, Martino S, Ciocchini M, Ciuti E, Vardeu MP, Guala A, Signorile F, Camerano P, Franceschini D, Tovo PA Variability of clinical and immunological phenotype in immunodeficiency-centromeric instability-facial anomalies syndrome. Report of two new patients and review of the literature. Eur J Pediatr. 1995;154:840–6.
4. Ueda Y, Okano M, Williams C, Chen T, Georgopoulos K, Li E Roles for Dnmt3b in mammalian development: a mouse model for the ICF syndrome. Development. 2006;133:1183–92.
5. Kondo T, Bobek MP, Kuick R, Lamb B, Zhu X, Narayan A, Bourc'his D, Viegas-Pequignot E, Ehrlich M, Hanash SM Whole-genome methylation scan in ICF syndrome: hypomethylation of non-satellite DNA repeats D4Z4 and NBL2. Hum Mol Genet. 2000;9:597–604.
6. Miniou P, Bourc'his D, Molina Gomes D, Jeanpierre M, Viegas-Pequignot E Undermethylation of Alu sequences in ICF syndrome: molecular and in situ analysis. Cytogenet Cell Genet. 1997;77:308–13.
7. Miniou P, Jeanpierre M, Bourc'his D, Coutinho Barbosa AC, Blanquet V, Viegas-Pequignot E alpha-satellite DNA methylation in normal individuals and in ICF patients: heterogeneous methylation of constitutive heterochromatin in adult and fetal tissues. Hum Genet. 1997;99:738–45.
8. Jeanpierre M, Turleau C, Aurias A, Prieur M, Ledeist F, Fischer A, Viegas-Pequignot E An embryonic-like methylation pattern of classical satellite DNA is observed in ICF syndrome. Hum Mol Genet. 1993;2:731–5.
9. Xu GL, Bestor TH, Bourc'his D, Hsieh CL, Tommerup N, Bugge M, Hulten M, Qu X, Russo JJ, Viegas-Pequignot E Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature. 1999;402:187–91.
10. Jiang YL, Rigolet M, Bourc'his D, Nigon F, Bokesoy I, Fryns JP, Hulten M, Jonveaux P, Maraschio P, Megarbane A, et al. DNMT3B mutations and DNA methylation defect define two types of ICF syndrome. Hum Mutat. 2005;25:56–63.
11. Jin B, Tao Q, Peng J, Soo HM, Wu W, Ying J, Fields CR, Delmas AL, Liu X, Qiu J, et al. DNA methyltransferase 3B (DNMT3B) mutations in ICF syndrome lead to altered epigenetic modifications and aberrant expression of genes regulating development, neurogenesis and immune function. Hum Mol Genet. 2008;17:690–709.
12. de Greef JC, Wang J, Balog J, den Dunnen JT, Frants RR, Straasheijm KR, Aytekin C, van der Burg M, Duprez L, Ferster A, et al. Mutations in ZBTB24 are associated with immunodeficiency, centromeric instability, and facial anomalies syndrome type 2. Am J Hum Genet. 2011;88:796–804.
13. Yoon HS, Scharer CD, Majumder P, Davis CW, Butler R, Zinzow-Kramer W, Skountzou I, Koutsonanos DG, Ahmed R, Boss JM ZBTB32 is an early repressor of the CIITA and MHC class II gene expression during B cell differentiation to plasma cells. J Immunol. 2012;189:2393–403.
14. Dent AL, Shaffer AL, Yu X, Allman D, Staudt LM Control of inflammation, cytokine expression, and germinal center formation by BCL-6. Science. 1997;276:589–92.
15. Nitta H, Unoki M, Ichiyanagi K, Kosho T, Shigemura T, Takahashi H, Velasco G, Francastel C, Picard C, Kubota T, et al. Three novel ZBTB24 mutations identified in Japanese and Cape Verdean type 2 ICF syndrome patients. J Hum Genet. 2013;58:455–60.
16. Weemaes CM, van Tol MJ, Wang J, van Ostaijen-ten Dam MM, van Eggermond MC, Thijssen PE, Aytekin C, Brunetti-Pierri N, van der Burg M, Graham Davies E, et al. Heterogeneous clinical presentation in ICF syndrome: correlation with underlying gene defects. Eur J Hum Genet. 2013;21:1219–25.
17. Thijssen PE, Ito Y, Grillo G, Wang J, Velasco G, Nitta H, Unoki M, Yoshihara M, Suyama M, Sun Y, et al. Mutations in CDCA7 and HELLS cause immunodeficiency-centromeric instability-facial anomalies syndrome. Nat Commun. 2015;6:7870.
18. Brown DC, Grace E, Sumner AT, Edmunds AT, Ellis PM ICF syndrome (immunodeficiency, centromeric instability and facial anomalies): investigation of heterochromatin abnormalities and review of clinical outcome. Hum Genet. 1995;96:411–6.
19. Hagleitner MM, Lankester A, Maraschio P, Hulten M, Fryns JP, Schuetz C, Gimelli G, Davies EG, Gennery A, Belohradsky BH, et al. Clinical spectrum of immunodeficiency, centromeric instability and facial dysmorphism (ICF syndrome). J Med Genet. 2008;45:93–9.
20. Colucci M, Cocito L, Capello E, Mancardi GL, Serrati C, Cinque P, Schenone A Progressive multifocal leukoencephalopathy in an adult patient with ICF syndrome. J Neurol Sci. 2004;217:107–10.
21. Shirohzu H, Kubota T, Kumazawa A, Sado T, Chijiwa T, Inagaki K, Suetake I, Tajima S, Wakui K, Miki Y, et al. Three novel DNMT3B mutations in Japanese patients with ICF syndrome. Am J Med Genet. 2002;112:31–7.
22. Schuetz C, Barbi G, Barth TF, Hoenig M, Schulz A, Moeller P, Smeets D, de Greef JC, van der Maarel SM, Vogel W, et al. ICF syndrome: high variability of the chromosomal phenotype and association with classical Hodgkin lymphoma. Am J Med Genet A. 2007;143A:2052–7.
23. Kaya N, Al-Muhsen S, Al-Saud B, Al-Bakheet A, Colak D, Al-Ghonaium A, Al-Dhekri H, Al-Mousa H, Arnaout R, Al-Owain M, et al. ICF syndrome in Saudi Arabia: immunological, cytogenetic and molecular analysis. J Clin Immunol. 2011;31:245–52.
24. Kloeckener-Gruissem B, Betts DR, Zankl A, Berger W, Gungor T A new and a reclassified ICF patient without mutations in DNMT3B and its interacting proteins SUMO-1 and UBC9. Am J Med Genet A. 2005;136:31–7.
25. Pezzolo A, Prigione I, Chiesa S, Castellano E, Gimelli G, Pistoia V A novel case of immunodeficiency, centromeric instability, and facial anomalies (the ICF syndrome): immunologic and cytogenetic studies. Haematologica. 2002;87:329–31.
26. Bjorck EJ, Bui TH, Wijmenga C, Grandell U, Nordenskjold M Early prenatal diagnosis of the ICF syndrome. Prenat Diagn. 2000;20:828–31.
27. Cerbone M, Wang J, Van der Maarel SM, D'Amico A, D'Agostino A, Romano A, Brunetti-Pierri N Immunodeficiency, centromeric instability, facial anomalies (ICF) syndrome, due to ZBTB24 mutations, presenting with large cerebral cyst. Am J Med Genet A. 2012;158A:2043–6.
28. Chouery E, Abou-Ghoch J, Corbani S, El Ali N, Korban R, Salem N, Castro C, Klayme S, Azoury-Abou Rjeily M, Khoury-Matar R, et al. A novel deletion in ZBTB24 in a Lebanese family with immunodeficiency, centromeric instability, and facial anomalies syndrome type 2. Clin Genet. 2012;82:489–93.
29. De Ravel TJ, Deckers E, Alliet PL, Petit P, Fryns JP The ICF syndrome: new case and update. Genet Couns. 2001;12:379–85.
30. Gimelli G, Varone P, Pezzolo A, Lerone M, Pistoia V ICF syndrome with variable expression in sibs. J Med Genet. 1993;30:429–32.
31. Makay B, Anal O, Kose G, Bozkaya O, Ozer E, Bora E, Ulgenalp A, Ercal D Lymphoid tissue histology in a patient with ICF syndrome. J Investig Allergol Clin Immunol. 2012;22:220–1.
32. Maraschio P, Zuffardi O, Dalla Fior T, Tiepolo L Immunodeficiency, centromeric heterochromatin instability of chromosomes 1, 9, and 16, and facial anomalies: the ICF syndrome. J Med Genet. 1988;25:173–80.
33. Rigolet M, Gregoire A, Lefort G, Blanchet P, Courbes C, Rodiere M, Sarda P, Viegas-Pequignot E Early prenatal diagnosis of ICF syndrome by mutation detection. Prenat Diagn. 2007;27:1075–8.
34. Sawyer JR, Swanson CM, Wheeler G, Cunniff C Chromosome instability in ICF syndrome: formation of micronuclei from multibranched chromosomes 1 demonstrated by fluorescence in situ hybridization. Am J Med Genet. 1995;56:203–9.
35. Schuffenhauer S, Bartsch O, Stumm M, Buchholz T, Petropoulou T, Kraft S, Belohradsky B, Hinkel GK, Meitinger T, Wegner RD DNA, FISH and complementation studies in ICF syndrome: DNA hypomethylation of repetitive and single copy loci and evidence for a trans acting factor. Hum Genet. 1995;96:562–71.
36. Reisli I, Yildirim MS, Koksal Y, Avunduk MC, Acar A A case with ICF syndrome lost to rubella pneumonitis. Turk J Pediatr. 2005;47:85–8.
37. van den Brand M, Flucke UE, Bult P, Weemaes CM, van Deuren M Angiosarcoma in a patient with immunodeficiency, centromeric region instability, facial anomalies (ICF) syndrome. Am J Med Genet A. 2011;155A:622–5.
38. Kieback P, Wendisch H, Lorenz P, Hinkel K ICF syndrome. Immunodeficiency, chromosomal centromere instability, facial anomalies. Case report and literature review. Monatsschr Kinderheilkd. 1992;140:91–4.
39. Kubota T, Furuumi H, Kamoda T, Iwasaki N, Tobita N, Fujiwara N, Goto Y, Matsui A, Sasaki H, Kajii T ICF syndrome in a girl with DNA hypomethylation but without detectable DNMT3B mutation. Am J Med Genet A. 2004;129A:290–3.
40. Smeets DF, Moog U, Weemaes CM, Vaes-Peeters G, Merkx GF, Niehof JP, Hamers G ICF syndrome: a new case and review of the literature. Hum Genet. 1994;94:240–6.
41. Turleau C, Cabanis MO, Girault D, Ledeist F, Mettey R, Puissant H, Prieur M, de Grouchy J Multibranched chromosomes in the ICF syndrome: immunodeficiency, centromeric instability, and facial anomalies. Am J Med Genet. 1989;32:420–4.
42. Valkova G, Ghenev E, Tzancheva M Centromeric instability of chromosomes 1, 9 and 16 with variable immune deficiency. Support of a new syndrome. Clin Genet. 1987;31:119–24.
43. Fasth A, Forestier E, Holmberg E, Holmgren G, Nordenson I, Soderstrom T, Wahlstrom J Fragility of the centromeric region of chromosome 1 associated with combined immunodeficiency in siblings. A recessively inherited entity? Acta Paediatr Scand. 1990;79:605–12.
44. Tauris P, Hansen PW Functional studies on lymphocytes from two siblings with congenital hypogammaglobulinaemia. Scand J Haematol. 1983;30:117–24.
45. Ostergaard PA A girl with recurrent infections, low IgM and an abnormal chromosome number 1. Acta Paediatr Scand. 1973;62:211–5.
46. Carpenter NJ, Filipovich A, Blaese RM, Carey TL, Berkel AI Variable immunodeficiency with abnormal condensation of the heterochromatin of chromosomes 1, 9, and 16. J Pediatr. 1988;112:757–60.
47. Fryns JP, Azou M, Jaeken J, Eggermont E, Pedersen JC, Van den Berghe H Centromeric instability of chromosomes 1, 9, and 16 associated with combined immunodeficiency. Hum Genet. 1981;57:108–10.
48. Howard PJ, Lewis IJ, Harris F, Walker S Centromeric instability of chromosomes 1 and 16 with variable immune deficiency: a new syndrome. Clin Genet. 1985;27:501–5.
49. Wijmenga C, van den Heuvel LP, Strengman E, Luyten JA, van der Burgt IJ, de Groot R, Smeets DF, Draaisma JM, van Dongen JJ, De Abreu RA, et al. Localization of the ICF syndrome to chromosome 20 by homozygosity mapping. Am J Hum Genet. 1998;63:803–9.
50. Andre N, Roquelaure B, Caillez M, Chrestian M, Moncla A, Blanco-Betancourt C, Schiff C Macrophage activation syndrome mimicking life-threatening infection in a patient with variable immunodeficiency, centromeric instability, and facial anomalies. Pediatrics. 2004;114:1127.
51. von Bernuth H, Ravindran E, Du H, Frohler S, Strehl K, Kramer N, Issa-Jahns L, Amulic B, Ninnemann O, Xiao MS, et al. Combined immunodeficiency develops with age in Immunodeficiency-centromeric instability-facial anomalies syndrome 2 (ICF2). Orphanet J Rare Dis. 2014;9:116.
52. Chandesris MO, Melki I, Natividad A, Puel A, Fieschi C, Yun L, Thumerelle C, Oksenhendler E, Boutboul D, Thomas C, et al. Autosomal dominant STAT3 deficiency and hyper-IgE syndrome: molecular, cellular, and clinical features from a French national survey. Medicine (Baltimore). 2012;91:e1–19.
53. Gardes P, Forveille M, Alyanakian MA, Aucouturier P, Ilencikova D, Leroux D, Rahner N, Mazerolles F, Fischer A, Kracker S, et al. Human MSH6 deficiency is associated with impaired antibody maturation. J Immunol. 2012;188:2023–9.
54. Velasco G, Walton EL, Sterlin D, Hedouin S, Nitta H, Ito Y, Fouyssac F, Megarbane A, Sasaki H, Picard C, et al. Germline genes hypomethylation and expression define a molecular signature in peripheral blood of ICF patients: implications for diagnosis and etiology. Orphanet J Rare Dis. 2014;9:56.
55. Duchamp M, Sterlin D, Diabate A, Uring-Lambert B, Guerin-El Khourouj V, Le Mauff B, Monnier D, Malcus C, Labalette M, Picard C B-cell subpopulations in children: National reference values. Immun Inflammation Dis. 2014;2:131–40.
56. Okano M, Bell DW, Haber DA, Li E DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell. 1999;99:247–57.
57. Velasco G, Hube F, Rollin J, Neuillet D, Philippe C, Bouzinba-Segard H, Galvani A, Viegas-Pequignot E, Francastel C Dnmt3b recruitment through E2F6 transcriptional repressor mediates germ-line gene silencing in murine somatic tissues. Proc Natl Acad Sci U S A. 2010;107:9281–6.
58. Nielsen JV, Thomassen M, Mollgard K, Noraberg J, Jensen NA Zbtb20 defines a hippocampal neuronal identity through direct repression of genes that control projection neuron development in the isocortex. Cereb Cortex. 2014;24:1216–29.
59. Mitchelmore C, Kjaerulff KM, Pedersen HC, Nielsen JV, Rasmussen TE, Fisker MF, Finsen B, Pedersen KM, Jensen NA Characterization of two novel nuclear BTB/POZ domain zinc finger isoforms. Association with differentiation of hippocampal neurons, cerebellar granule cells, and macroglia. J Biol Chem. 2002;277:7598–609.
60. Gennery AR, Slatter MA, Bredius RG, Hagleitner MM, Weemaes C, Cant AJ, Lankester AC Hematopoietic stem cell transplantation corrects the immunologic abnormalities associated with immunodeficiency-centromeric instability-facial dysmorphism syndrome. Pediatrics. 2007;120:e1341–4.
61. Crouzier R, Martin T, Pasquali JL Heavy chain variable region, light chain variable region, and heavy chain CDR3 influences on the mono- and polyreactivity and on the affinity of human monoclonal rheumatoid factors. J Immunol. 1995;154:4526–35.
62. Bas S, Djavad N, Schwager J, Vischer T, Roosnek E Relation between the heavy chain complementarity region 3 characteristics and rheumatoid factor binding properties. Autoimmunity. 1998;27:191–9.
63. Henry-Bonami RA, Williams JM, Rachakonda AB, Karamali M, Kendall PL, Thomas JW B lymphocyte “original sin” in the bone marrow enhances islet autoreactivity in type 1 diabetes-prone nonobese diabetic mice. J Immunol. 2013;190:5992–6003.
64. Cho MJ, Lo AS, Mao X, Nagler AR, Ellebrecht CT, Mukherjee EM, Hammers CM, Choi EJ, Sharma PM, Uduman M, et al. Shared VH1-46 gene usage by pemphigus vulgaris autoantibodies indicates common humoral immune responses among patients. Nat Commun. 2014;5:4167.
65. Carneiro-Sampaio M, Coutinho A Early-onset autoimmune disease as a manifestation of primary immunodeficiency. Front Immunol. 2015;6:185.
66. Baroudjian B, Viguier M, Battistella M, Beneton N, Pages C, Gener G, Begon E, Bachelez H Psoriasis associated with idiopathic CD4+ T-cell lymphopenia: a regulatory T-cell defect? Br J Dermatol. 2014;171:186–9.
67. Tangye SG, Liu YJ, Aversa G, Phillips JH, de Vries JE Identification of functional human splenic memory B cells by expression of CD148 and CD27. J Exp Med. 1998;188:1691–703.
68. Klein U, Rajewsky K, Kuppers R Human immunoglobulin (Ig)M + IgD+ peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J Exp Med. 1998;188:1679–89.
69. Ehrlich M, Sanchez C, Shao C, Nishiyama R, Kehrl J, Kuick R, Kubota T, Hanash SM ICF, an immunodeficiency syndrome: DNA methyltransferase 3B involvement, chromosome anomalies, and gene dysregulation. Autoimmunity. 2008;41:253–71.
70. Fecteau JF, Cote G, Neron S A new memory CD27-IgG+ B cell population in peripheral blood expressing VH genes with low frequency of somatic mutation. J Immunol. 2006;177:3728–36.
71. Wirths S, Lanzavecchia A ABCB1 transporter discriminates human resting naive B cells from cycling transitional and memory B cells. Eur J Immunol. 2005;35:3433–41.
72. Cunningham-Rundles C Key aspects for successful immunoglobulin therapy of primary immunodeficiencies. Clin Exp Immunol. 2011;164(Suppl 2):16–9.
73. Oksenhendler E, Gerard L, Fieschi C, Malphettes M, Mouillot G, Jaussaud R, Viallard JF, Gardembas M, Galicier L, Schleinitz N, et al. Infections in 252 patients with common variable immunodeficiency. Clin Infect Dis. 2008;46:1547–54.