Clinical and molecular findings in 39 patients with KBG syndrome caused by deletion or mutation of ANKRD11

American Journal of Medical Genetics, Part A

Volumn 170, Issue 11, 2016, Pages 2847-2859

  Goldenberg, Alice ^a   Riccardi, Florence ^b   Tessier, Aude ^a   Pfundt, Rolph ^c   Busa, Tiffany ^b   Cacciagli, Pierre ^d   Capri, Yline ^e   Coutton, Charles ^f   Delahaye Duriez, Andree ^g   Frebourg, Thierry ^a   Gatinois, Vincent ^h   Guerrot, Anne Marie ^a   Genevieve, David ^h   Lecoquierre, Francois ^a   Jacquette, Aurélia ⁱ   Khau Van Kien, Philippe ^j   Leheup, Bruno ^k   Marlin, Sandrine ^l   Verloes, Alain ^e   Michaud, Vincent ^m   Nadeau, Gwenael ⁿ   Mignot, Cyril ⁱ   Parent, Philippe ^o   Rossi, Massimiliano ^p   Toutain, Annick ^q   Schaefer, Elise ^r   Thauvin Robinet, Christel ^s   Van Maldergem, Lionel ^t   Thevenon, Julien ^s   Satre, Véronique ^f   Perrin, Laurence ^e   Vincent Delorme, Catherine ^u   Sorlin, Arthur ^k   Missirian, Chantal ^b   Villard, Laurent ^d   Mancini, Julien ^b,v   Saugier Veber, Pascale ^a   Philip, Nicole ^b,d   more..

^a UNIVERSITÉ DE ROUEN   (France)

^b TIMONE HOSPITAL   (France)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d AIX MARSEILLE UNIVERSITY   (France)

^e HÔPITAL ROBERT DEBRÉ   (France)

^f UNIV GRENOBLE ALPES   (France)

^g UNIVERSITÉ PARIS 13   (France)

^h HÔPITAL ARNAUD DE VILLENEUVE   (France)

ⁱ ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^j DEPARTMENT OF NEUROLOGY   (France)

^k CHU NANCY BRABOIS   (France)

^l HÔPITAL NECKER ENFANTS MALADES   (France)

^m BORDEAUX UNIVERSITY HOSPITAL   (France)

ⁿ CENTRE HOSPITALIER DE VALENCE   (France)

^o CHU MORVAN   (France)

^p HOSPICES CIVILS DE LYON   (France)

^q CHU BRETONNEAU   (France)

^r HÔPITAL DE HAUTEPIERRE   (France)

^s HÔPITAL DU BOCAGE   (France)

^t HÔPITAL SAINT JACQUES   (France)

^u LILLE UNIVERSITY HOSPITAL   (France)

^v AIX MARSEILLE UNIV   (France)

more..

Author keywords

16q24.3 deletion; ANKRD11; haploinsufficiency; KBG syndrome; long term prognosis

Indexed keywords

ANKRD11 GENE; ARTICLE; BODY DYSMORPHIC DISORDER; CLINICAL ARTICLE; CLINICAL EVALUATION; COMPARATIVE GENOMIC HYBRIDIZATION; CRANIOFACIAL MALFORMATION; DEVELOPMENTAL DISORDER; EXON; FEMALE; FOLLOW UP; FRAMESHIFT MUTATION; GENE; GENE DELETION; GENE MUTATION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC IDENTIFICATION; GENETIC PREDISPOSITION; GENETIC VARIABILITY; HAPLOINSUFFICIENCY; HEARING IMPAIRMENT; HUMAN; INHERITANCE; INTELLECTUAL IMPAIRMENT; KBG SYNDROME; MALE; MOLECULAR DIAGNOSIS; NONSENSE MUTATION; PALATOPHARYNGEAL INCOMPETENCE; PHENOTYPE; PRECOCIOUS PUBERTY; PRIORITY JOURNAL; SHORT STATURE; SLEEP DISORDER; TELOMERE SHORTENING; ABNORMALITIES, MULTIPLE; ADOLESCENT; ADULT; AGED; ALLELE; AMINO ACID SUBSTITUTION; BONE DISEASES, DEVELOPMENTAL; CHILD; CHROMOSOME 16; CHROMOSOME DELETION; FACIES; GENETIC ASSOCIATION STUDY; GENETICS; INFANT; INTELLECTUAL DISABILITY; MIDDLE AGED; MUTATION; PRESCHOOL CHILD; RETROSPECTIVE STUDY; TOOTH ABNORMALITIES; YOUNG ADULT;

ANKRD11 PROTEIN, HUMAN; REPRESSOR PROTEIN;

ABNORMALITIES, MULTIPLE; ADOLESCENT; ADULT; AGED; ALLELES; AMINO ACID SUBSTITUTION; BONE DISEASES, DEVELOPMENTAL; CHILD; CHILD, PRESCHOOL; CHROMOSOME DELETION; CHROMOSOMES, HUMAN, PAIR 16; COMPARATIVE GENOMIC HYBRIDIZATION; FACIES; FEMALE; GENETIC ASSOCIATION STUDIES; HUMANS; INFANT; INTELLECTUAL DISABILITY; MALE; MIDDLE AGED; MUTATION; PHENOTYPE; REPRESSOR PROTEINS; RETROSPECTIVE STUDIES; TOOTH ABNORMALITIES; YOUNG ADULT;

EID: 84987625560     PISSN: 15524825     EISSN: 15524833     Source Type: Journal    
DOI: 10.1002/ajmg.a.37878     Document Type: Article

References (40)

1. Ansari M, Poke G, Ferry Q, Williamson K, Aldridge R, Meynert AM, Bengani H, Chan CY, Kayserili H, Avci S, Hennekam RC, Lampe AK, Redeker E, Homfray T, Ross A, Falkenberg Smeland M, Mansour S, Parker MJ, Cook JA, Splitt M, Fisher RB, Fryer A, Magee AC, Wilkie A, Barnicoat A, Brady AF, Cooper NS, Mercer C, Deshpande C, Bennett CP, Pilz DT, Ruddy D, Cilliers D, Johnson DS, Josifova D, Rosser E, Thompson EM, Wakeling E, Kinning E, Stewart F, Flinter F, Girisha KM, Cox H, Firth HV, Kingston H, Wee JS, Hurst JA, Clayton-Smith J, Tolmie J, Vogt J, Tatton-Brown K, Chandler K, Prescott K, Wilson L, Behnam M, McEntagart M, Davidson R, Lynch SA, Sisodiya S, Mehta SG, McKee SA, Mohammed S, Holden S, Park SM, Holder SE, Harrison V, McConnell V, Lam WK, Green AJ, Donnai D, Bitner-Glindzicz M, Donnely DE, Nellaker C, Taylor MS, FitzPatrick DR. 2014. Genetic heterogeneity in Cornelia de Lange syndrome (CdLS) and CdLS-like phenotypes with observed and predicted levels of mosaicism. J Med Genet 51:659–668.
2. Brancati F, D'Avanzo MG, Digilio MC, Sarkozy A, Biondi M, De Brasi D, Mingarelli R, Dallapiccola B. 2004. KBG syndrome in a cohort of Italian patients. Am J Med Genet Part A 131A:144–149.
3. Casilli F, Di Rocco ZC, Gad S, Tournier I, Stoppa-Lyonnet D, Frebourg T, Tosi M. 2002. Rapid detection of novel BRCA1 rearrangements in high-risk breast-ovarian cancer families using multiplex PCR of short fluorescent fragments. Hum Mutat 20:218–226.
4. Coutton C, Monnier N, Rendu J, Lunardi J. 2010. Development of a multiplex ligation-dependent probe amplification (MLPA) assay for quantification of the OCRL1 gene. Clin Biochem 43:609–614.
5. Crippa M, Rusconi D, Castronovo C, Bestetti I, Russo S, Cereda A, Selicorni A, Larizza L, Finelli P. 2015. Familial intragenic duplication of ANKRD11 underlying three patients of KBG syndrome. Mol Cytogenet 8:20.
6. Deardorff MA, Kaur M, Yaeger D, Rampuria A, Korolev S, Pie J, Gil-Rodríguez C, Arnedo M, Loeys B, Kline AD, Wilson M, Lillquist K, Siu V, Ramos FJ, Musio A, Jackson LS, Dorsett D, Krantz ID. 2007. Mutations in cohesin complex members SMC3 and SMC1A cause a mild variant of Cornelia de Lange syndrome with predominant mental retardation. Am J Hum Genet 80:485–494.
7. Deardorff MA, Bando M, Nakato R, Watrin E, Itoh T, Minamino M, Saitoh K, Komata M, Katou Y, Clark D, Cole KE, De Baere E, Decroos C, Di Donato N, Ernst S, Francey LJ, Gyftodimou Y, Hirashima K, Hullings M, Ishikawa Y, Jaulin C, Kaur M, Kiyono T, Lombardi PM, Magnaghi-Jaulin L, Mortier GR, Nozaki N, Petersen MB, Seimiya H, Siu VM, Suzuki Y, Takagaki K, Wilde JJ, Willems PJ, Prigent C, Gillessen-Kaesbach G, Christianson DW, Kaiser FJ, Jackson LG, Hirota T, Krantz ID, Shirahige K. 2012a. HDAC8 mutations in Cornelia de Lange syndrome affect the cohesin acetylation cycle. Nature 489:313–317.
8. Deardorff MA, Wilde JJ, Albrecht M, Dickinson E, Tennstedt S, Braunholz D, Mönnich M, Yan Y, Xu W, Gil-Rodríguez MC, Clark D, Hakonarson H, Halbach S, Michelis LD, Rampuria A, Rossier E, Spranger S, Van Maldergem L, Lynch SA, Gillessen-Kaesbach G, Lüdecke HJ, Ramsay RG, McKay MJ, Krantz ID, Xu H, Horsfield JA, Kaiser FJ. 2012b. RAD21 mutations cause a human cohesinopathy. Am J Hum Genet 90:1014–1027.
9. Gallagher D, Voronova A, Zander MA, Cancino GI, Bramall A, Krause MP, Abad C, Tekin M, Neilsen PM, Callen DF, Scherer SW, Keller GM, Kaplan DR, Walz K, Miller FD. 2015. ANKRD11 is a chromatin regulator involved in autism that is essential for neural development. Dev Cell 32:31–42.
10. Hellani A, Mohamed S, Al-Akoum S, Bosley TM, Abu-Amero KK. 2010. A t(5;16)(p15.32;q23.3) generating 16q23.3->qter duplication and 5p15.32->pter deletion in two siblings with mental retardation, dysmorphic features, and speech delay. Am J Med Genet Part A 152A:1555–1560.
11. Herrmann J, Pallister PD, Tiddy W, Opitz JM. 1975. The KBG syndrome-a syndrome of short stature, characteristic facies, mental retardation, macrodontia and skeletal anomalies. Birth Defects Orig Artic Ser 11:7–18.
12. Isrie M, Hendriks Y, Gielissen N, Sistyermans EA, Willemsen MH, Peeters H, Vermeesch JR, Kleefstra T, Van Esch H. 2012. Haploinsufficiency of ANKRD11 causes mild cognitive impairment, short stature and minor dysmorphisms. Eur J Hum Genet 20:131–133.
13. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA, van Berkum NL, Ebmeier CC, Goossens J, Rahl PB, Levine SS, Taatjes DJ, Dekker J, Young RA. 2010. Mediator and cohesin connect gene expression and chromatin architecture. Nature 467:430–435.
14. Khalifa M, Stein J, Grau L, Nelson V, Meck J, Aradhya S, Duby J. 2013. Partial deletion of ANKRD11 results in the KBG phenotype distinct from the 16q24.3 microdeletion syndrome. Am J Med Genet Part A 161A:835–840.
15. Kim HJ, Cho E, Park JB, Im WY, Kim HJ. 2015. A Korean family with KBG syndrome identified by ANKRD11 mutation, and phenotypic comparison of ANKRD11 mutation and 16q24.3 microdeletion. Eur J Med Genet 58:86–94.
16. Lim SP, Wong NC, Suetani RJ, Ho K, Ng JL, Neilsen PM, Gill PG, Kumar R, Callen DF. 2012. Specific-site methylation of tumour suppressor ANKRD11 in breast cancer. Eur J Cancer 48:3300–3309.
17. Lim J-H, Seo E-J, Kim YM, Cho HY, Lee JO, Cheon CK, Yoo HW. 2014. A de novo microdeletion of ANKRD11 gene in a Korean patient with KBG syndrome. Ann Lab Med 34:390–394.
18. Lo-Castro A, Brancati F, Digilio MC, Garaci FG, Bollero P, Alfieri A, Curatolo P. 2013. Neurobehavioral phenotype observed in KBG syndrome caused by ANKRD11 mutations. Am J Med Genet Part B 162B:17–23.
19. Marshall CR, Noor A, Vincent JB, Lionel AC, Feuk L, Skaug J, Shago M, Moessner R, Pinto D, Ren Y, Thiruvahindrapduram B, Fiebig A, Schreiber S, Friedman J, Ketelaars CE, Vos YJ, Ficicioglu C, Kirkpatrick S, Nicolson R, Sloman L, Summers A, Gibbons CA, Teebi A, Chitayat D, Weksberg R, Thompson A, Vardy C, Crosbie V, Luscombe S, Baatjes R, Zwaigenbaum L, Roberts W, Fernandes B, Szatmari P, Scherer SW. 2008. Structural variation of chromosomes in autism spectrum disorder. Am J Hum Genet 82:477–488.
20. Miyatake S, Murakami A, Okamoto N, Sakamoto M, Miyake N, Saitsu H, Matsumoto Nl. 2013. A de novo deletion at 16q24.3 involving ANKRD11 in a Japanese patient with KBG syndrome. Am J Med Genet Part A 161A:1073–1077.
21. Musio A, Selicorni A, Focarelli ML, Gervasini C, Milani D, Russo S, Vezzoni P, Larizza L. 2006. X-linked Cornelia de Lange syndrome owing to SMC1L1 mutations. Nat Genet 38:528–530.
22. Neilsen PM, Cheney KM, Li CW, Chen JD, Cawrse JE, Schulz RB, Powell JA, Kumar R, Callen DF. 2008. Identification of ANKRD11 as a p53 coactivator. J Cell Sci 121:3541–3552.
23. Ockeloen CW, Willemsen MH, de Munnik S, van Bon BW, de Leeuw N, Verrips A, Kant SG, Jones EA, Brunner HG, van Loon RL, Smeets EE, van Haelst MM, van Haaften G, Nordgren A, Malmgren H, Grigelioniene G, Vermeer S, Louro P, Ramos L, Maal TJ, van Heumen CC, Yntema HG, Carels CE, Kleefstra T. 2015. Further delineation of the KBG syndrome phenotype caused by ANKRD11 aberrations. Eur J Hum Genet 23:1176–1185.
24. Parenti I, Gervasini C, Pozojevic J, Graul-Neumann L, Azzollini J, Braunholz D, Watrin E, Wendt KS, Cereda A, Cittaro D, Gillessen-Kaesbach G, Lazarevic D, Mariani M, Russo S, Werner R, Krawitz P, Larizza L, Selicorni A, Kaiser FJ. 2016. Broadening of cohesinopathies: Exome sequencing identifies mutations in ANKRD11 in two patients with Cornelia de Lange-overlapping phenotype. Clin Genet 89:74–81.
25. Reynaert N, Ockeloen CW, Sävendahl L, Beckers D, Devriendt K, Kleefstra T, Carels CE, Grigelioniene G, Nordgren A, Francois I, de Zegher F, Casteels K. 2015. Short stature in KBG syndrome: First responses to growth hormone treatment. Horm Res Pædiatrics 83:361–364.
26. Sacharow S, Li D, Fan YS, Tekin M. 2012. Familial 16q24.3 microdeletion involving ANKRD11 causes a KBG-like syndrome. Am J Med Genet Part A 158A:547–552.
27. Samanta D, Willis E. 2015. Electroencephalographic findings in KBG syndrome: A child with novel mutation in ANKRD11 gene. Acta Neurol Belg 115:779–782.
28. Schneider M, Debbané M, Bassett AS, Chow EW, Fung WL, van den Bree M, Owen M, Murphy KC, Niarchou M, Kates WR, Antshel KM, Fremont W, McDonald-McGinn DM, Gur RE, Zackai EH, Vorstman J, Duijff SN, Klaassen PW, Swillen A, Gothelf D, Green T, Weizman A, Van Amelsvoort T, Evers L, Boot E, Shashi V, Hooper SR, Bearden CE, Jalbrzikowski M, Armando M, Vicari S, Murphy DG, Ousley O, Campbell LE, Simon TJ, Eliez S. 2014. Psychiatric disorders from childhood to adulthood in 22q11.2 deletion syndrome: Results from the international consortium on brain and behavior in 22q11.2 deletion syndrome. Am J Psychiatry 171:627–639.
29. Sirmaci A, Spiliopoulos M, Brancati F, Powell E, Duman D, Abrams A, Bademci G, Agolini E, Guo S, Konuk B, Kavaz A, Blanton S, Digilio MC, Dallapiccola B, Young J, Zuchner S, Tekin M. 2011. Mutations in ANKRD11 cause KBG syndrome, characterized by intellectual disability, skelmalformations, and macrodontia. Am J Hum Genet 2 89:289–294.
30. Skjei KL, Martin MM, Slavotinek AM. 2007. KBG syndrome: Report of twins, neurological characteristics, and delineation of diagnostic criteria. Am J Med Genet Part A 143A:292–300.
31. Spengler S, Oehl-Jaschkowitz B, Begemann M, Hennes P, Zerres K, Eggermann T. 2013. Haploinsufficiency of ANKRD11 (16q24.3) is not obligatorily associated with cognitive impairment but shows a clinical overlap with Silver-Russell syndrome. Mol Syndromol 4:246–249.
32. Tekin M, Kavaz A, Berberoğlu M, Fitoz S, Ekim M, Ocal G, Akar N. 2004. The KBG syndrome: Confirmation of autosomal dominant inheritance and further delineation of the phenotype. Am J Med Genet Part A 130A:284–287.
33. A. Thapar M. Cooper Attention deficit hyperactivity disorder The Lancet [Internet]. [citedJan 10]; Available from 2016 http://www.sciencedirect.com/science/article/pii/S014067361500238X.
34. Tonkin ET, Wang TJ, Lisgo S, Bamshad MJ, Strachan T. 2004. NIPBL, encoding a homolog of fungal Scc2-type sister chromatid cohesion proteins and fly Nipped-B, is mutated in Cornelia de Lange syndrome. Nat Genet 36:636–641.
35. Walz K, Cohen D, Neilsen PM, Foster J, Brancati F, Demir K, Fisher R, Moffat M, Verbeek NE, Bjorgo K, Lo Castro A, Curatolo P, Novelli G, Abad C, Lei C, Zhang L, Diaz-Horta O, Young JI, Callen DF, Tekin M. 2015. Characterization of ANKRD11 mutations in humans and mice related to KBG syndrome. Hum Genet 134:181–190.
36. Willemsen MH, Fernandez BA, Bacino CA, Gerkes E, de Brouwer AP, Pfundt R, Sikkema-Raddatz B, Scherer SW, Marshall CR, Potocki L, van Bokhoven H, Kleefstra T. 2010. Identification of ANKRD11 and ZNF778 as candidate genes for autism and variable cognitive impairment in the novel 16q24.3 microdeletion syndrome. Eur J Hum Genet 18:429–435.
37. Youngs EL, Hellings JA, Butler MG. 2011. ANKRD11 gene deletion in a 17-year-old male. Clin Dysmorphol 20:170–171.
38. Zhang A, Yeung PL, Li CW, Tsai SC, Dinh GK, Wu X, Li H, Chen JD. 2004. Identification of a novel family of ankyrin repeats containing cofactors for p160 nuclear receptor coactivators. J Biol Chem 279:33799–33805.
39. Zhang A, Li CW, Chen JD. 2007. Characterization of transcriptional regulatory domains of ankyrin repeat cofactor-1. Biochem Biophys Res Commun 358:1034–1040.
40. Zou YS, Van Dyke DL, Ellison JW. 2007. Microarray comparative genomic hybridization and FISH studies of an unbalanced cryptic telomeric 2p deletion/16q duplication in a patient with mental retardation and behavioral problems. Am J Med Genet A 143A:746–751.