Copy number variants in short children born small for gestational age

Hormone Research in Paediatrics

Volumn 82, Issue 5, 2014, Pages 310-318

  Wit, Jan M ^a   Van Duyvenvoorde, Hermine A ^a   Van Klinken, Jan B ^a   Caliebe, Janina ^b   Bosch, Cathy A J ^a   Lui, Julian C ^c   Gijsbers, Antoinet C J ^a   Bakker, Egbert ^a   Breuning, Martijn H ^a   Oostdijk, Wilma ^a   Losekoot, Monique ^a   Baron, Jeffrey ^c   Binder, Gerhard ^b   Ranke, Michael B ^b   Ruivenkamp, Claudia A L ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Copy number variations; Genetics; Growth; Short stature; Single nucleotide polymorphism array; Small for gestational age

Indexed keywords

AGPS GENE; ARTICLE; CHILD; CHROMOSOME 14; CHROMOSOME 15; CHROMOSOME 7; CLINICAL ARTICLE; CLUBFOOT; COPY NUMBER VARIATION; DGKB GENE; DIGEORGE SYNDROME; ENHANCER REGION; FEMALE; GENE; GENE DELETION; GENE DUPLICATION; GENE EXPRESSION; GENETIC ASSOCIATION; HETEROZYGOSITY LOSS; HOXD4 GENE; HUMAN; INTRAUTERINE GROWTH RETARDATION; KYPHOSIS; MALE; MICROCEPHALY; MULTIPLEX LIGATION DEPENDENT PROBE AMPLIFICATION; OSBPL6 GENE; PDE11A GENE; PLEKHA3 GENE; PRECOCIOUS PUBERTY; PRKRA GENE; SHORT STATURE; SILVER RUSSELL SYNDROME; SINGLE NUCLEOTIDE POLYMORPHISM; SMALL FOR DATE INFANT; TNFRSF11B GENE; UNIPARENTAL DISOMY; ANIMAL; CLINICAL TRIAL; GENOME-WIDE ASSOCIATION STUDY; MOUSE;

ANIMALS; DNA COPY NUMBER VARIATIONS; FEMALE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; INFANT, SMALL FOR GESTATIONAL AGE; MALE; MICE; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84912133237     PISSN: 16632818     EISSN: 16632826     Source Type: Journal    
DOI: 10.1159/000367712     Document Type: Article

References (60)

1. Lango Allen H, Estrada K, Lettre G, et al: Hundreds of variants clustered in genomic loci and biological pathways affect human height. Nature 2010; 467: 832-838.
2. Oostdijk W, Grote FK, de Muinck Keizer- Schrama S, Wit JM: Diagnostic approach in children with short stature. Horm Res 2009; 72: 206-217.
3. Seaver LH, Irons M: ACMG practice guideline: genetic evaluation of short stature. Genet Med 2009; 11: 465-470.
4. Wit JM, Kiess W, Mullis P: Genetic evaluation of short stature. Best Pract Res Clin Endocrinol Metab 2011; 25: 1-17.
5. Wit JM, van Duyvenvoorde HA, Scheltinga SA, de Bruin S, Hafkenscheid L, Kant SG, Ruivenkamp CA, Gijsbers AC, van Doorn J, Feigerlova E, Noordam C, Walenkamp MJ, Claahsen-van de Grinten H, Stouthart P, Bonapart IE, Pereira AM, Gosen J, Delemarrevan de Waal H, Hwa V, Breuning MH, Domene HM, Oostdijk W, Losekoot M: Genetic analysis of short children with apparent growth hormone insensitivity. Horm Res Paediatr 2012; 77: 320-333.
6. Clayton PE, Cianfarani S, Czernichow P, Johannsson G, Rapaport R, Rogol A: Management of the child born small for gestational age through to adulthood: A consensus statement of the International Societies of Pediatric Endocrinology and the Growth Hormone Research Society. J Clin Endocrinol Metab 2007; 92: 804-810.
7. Van Duyvenvoorde HA, Lui JC, Kant SG, Oostdijk W, Gijsbers AC, Hoffer MJ, Karperien M, Walenkamp MJ, Noordam C, Voorhoeve PG, Mericq V, Pereira AM, Claahsen-van de Grinten HL, van Gool SA, Breuning MH, Losekoot M, Baron J, Ruivenkamp CA, Wit JM: Copy number variants in patients with short stature. Eur J Hum Genet 2014; 22: 602-609.
8. Zahnleiter D, Uebe S, Ekici AB, Hoyer J, Wiesener A, Wieczorek D, Kunstmann E, Reis A, Doerr HG, Rauch A, Thiel CT: Rare copy number variants are a common cause of short stature. PLoS Genet 2013; 9:e1003365.
9. Canton AP, Costa SS, Rodrigues TC, Bertola DR, Malaquias AC, Correa FA, Arnhold IJ, Rosenberg C, Jorge AA: Genome-wide screening of copy number variants in children born small for gestational age reveal several candidate genes involved in growth pathways. Eur J Endocrinol 2014; 171: 253-262.
10. Cirulli ET, Goldstein DB: Uncovering the roles of rare variants in common disease through whole-genome sequencing. Nat Rev Genet 2010; 11: 415-425.
11. Dauber A, Lafranchi SH, Maliga Z, Lui JC, Moon JE, McDeed C, Henke K, Zonana J, Kingman GA, Pers TH, Baron J, Rosenfeld RG, Hirschhorn JN, Harris MP, Hwa V: Novel microcephalic primordial dwarfism disorder associated with variants in the centrosomal protein ninein. J Clin Endocrinol Metab 2012; 97:E2140-E2151.
12. Dauber A, Stoler J, Hechter E, Safer J, Hirschhorn JN: Whole-exome sequencing reveals a novel mutation in CUL7 in a patient with an undiagnosed growth disorder. J Pediatr 2013; 162: 202-204.
13. Caliebe J, Broekman S, Boogaard M, Bosch CA, Ruivenkamp CA, Oostdijk W, Kant SG, Binder G, Ranke MB, Wit JM, Losekoot M: IGF1, IGF1R and SHOX mutation analysis in short children born small for gestational age and short children with normal birth size (idiopathic short stature). Horm Res Paediatr 2012; 77: 250-260.
14. Wit JM, Clayton PE, Rogol AD, Savage MO, Saenger PH, Cohen P: Idiopathic short stature: definition, epidemiology, and diagnostic evaluation. Growth Horm IGF Res 2008; 18: 89-110.
15. Dauber A, Yu Y, Turchin MC, Chiang CW, Meng YA, Demerath EW, Patel SR, Rich SS, Rotter JI, Schreiner PJ, Wilson JG, Shen Y, Wu BL, Hirschhorn JN: Genome-wide association of copy-number variation reveals an association between short stature and the presence of low-frequency genomic deletions. Am J Hum Genet 2011; 89: 751-759.
16. Prader A, Largo RH, Molinari L, Issler C: Physical growth of Swiss children from birth to 20 years of age. First Zurich longitudinal study of growth and development. Helv Paediatr Acta Suppl 1989; 52: 1-125.
17. Niklasson A, Ericson A, Fryer JG, Karlberg J, Lawrence C, Karlberg P: An update of the Swedish reference standards for weight, length and head circumference at birth for given gestational age (1977-1981). Acta Paediatr Scand 1991; 80: 756-762.
18. Cole TJ, Freeman JV, Preece MA: Body mass index reference curves for the UK, 1990. Arch Dis Child 1995; 73: 25-29.
19. Blum WF, Ranke MB, Kietzmann K, Gauggel E, Zeisel HJ, Bierich JR: A specific radioimmunoassay for the growth hormone (GH)- dependent somatomedin-binding protein: its use for diagnosis of GH deficiency. J Clin Endocrinol Metab 1990; 70: 1292-1298.
20. Blum WF, Breier BH: Radioimmunoassays for IGFs and IGFBPs. Growth Regul 1994; 4(suppl 1):11-19.
21. Caliebe J, Martin DD, Ranke MB, Wit JM: The Auxological and Biochemical Continuum of Short Children Born Small for Gestational Age (SGA) or with Normal Birth Size (Idiopathic Short Stature). Int J Pediatr Endocrinol 2010; 2010: 852967.
22. Miller SA, Dykes DD, Polesky HF: A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 1988; 16: 1215.
23. Nannya Y, Sanada M, Nakazaki K, Hosoya N, Wang L, Hangaishi A, Kurokawa M, Chiba S, Bailey DK, Kennedy GC, Ogawa S: A robust algorithm for copy number detection using high-density oligonucleotide single nucleotide polymorphism genotyping arrays. Cancer Res 2005; 65: 6071-6079.
24. Hehir-Kwa JY, Egmont-Petersen M, Janssen IM, Smeets D, van Kessel AG, Veltman JA: Genome-wide copy number profiling on high-density bacterial artificial chromosomes, single-nucleotide polymorphisms, and oligonucleotide microarrays: A platform comparison based on statistical power analysis. DNA Res 2007; 14: 1-11.
25. Kozomara A, Griffiths-Jones S: miRBase: Annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 2014; 42:D68-D73.
26. Hsu SD, Tseng YT, Shrestha S, Lin YL, Khaleel A, Chou CH, Chu CF, Huang HY, Lin CM, Ho SY, Jian TY, Lin FM, Chang TH, Weng SL, Liao KW, Liao IE, Liu CC, Huang HD: miRTarBase update 2014: An information resource for experimentally validated miRNAtarget interactions. Nucleic Acids Res 2014; 42:D78-D85.
27. Lalic T, Vossen RH, Coffa J, Schouten JP, Guc-Scekic M, Radivojevic D, Djurisic M, Breuning MH, White SJ, den Dunnen JT: Deletion and duplication screening in the DMD gene using MLPA. Eur J Hum Genet 2005; 13: 1231-1234.
28. McKusick VA: Mendelian Inheritance in Man. A Catalog of Human Genes and Genetic Disorders. Baltimore, Johns Hopkins University Press, 1998.
29. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel- Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G: Gene ontology: Tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 2000; 25: 25-29.
30. Kamburov A, Pentchev K, Galicka H, Wierling C, Lehrach H, Herwig R: ConsensusPathDB: Toward a more complete picture of cell biology. Nucleic Acids Res 2011; 39:D712-D717.
31. Lui JC, Andrade AC, Forcinito P, Hegde A, Chen W, Baron J, Nilsson O: Spatial and temporal regulation of gene expression in the mammalian growth plate. Bone 2010; 46: 1380-1390.
32. Lui JC, Nilsson O, Chan Y, Palmer CD, Andrade AC, Hirschhorn JN, Baron J: Synthesizing genome-wide association studies and expression microarray reveals novel genes that act in the human growth plate to modulate height. Hum Mol Genet 2012; 21: 5193-5201.
33. Yun TJ, Tallquist MD, Aicher A, Rafferty KL, Marshall AJ, Moon JJ, Ewings ME, Mohaupt M, Herring SW, Clark EA: Osteoprotegerin, a crucial regulator of bone metabolism, also regulates B-cell development and function. J Immunol 2001; 166: 1482-1491.
34. Mizuno A, Amizuka N, Irie K, Murakami A, Fujise N, Kanno T, Sato Y, Nakagawa N, Yasuda H, Mochizuki S, Gomibuchi T, Yano K, Shima N, Washida N, Tsuda E, Morinaga T, Higashio K, Ozawa H: Severe osteoporosis in mice lacking osteoclastogenesis inhibitory factor/osteoprotegerin. Biochem Biophys Res Commun 1998; 247: 610-615.
35. Ryan AK, Goodship JA, Wilson DI, Philip N, Levy A, Seidel H, Schuffenhauer S, Oechsler H, Belohradsky B, Prieur M, Aurias A, Raymond FL, Clayton-Smith J, Hatchwell E, McKeown C, Beemer FA, Dallapiccola B, Novelli G, Hurst JA, Ignatius J, Green AJ, Winter RM, Brueton L, Brondum-Nielsen K, Scambler PJ: Spectrum of clinical features associated with interstitial chromosome 22q11 deletions: A European collaborative study. J Med Genet 1997; 34: 798-804.
36. Botto LD, May K, Fernhoff PM, Correa A, Coleman K, Rasmussen SA, Merritt RK, O'Leary LA, Wong LY, Elixson EM, Mahle WT, Campbell RM: A population-based study of the 22q11.2 deletion: phenotype, incidence, and contribution to major birth defects in the population. Pediatrics 2003; 112: 101-107.
37. Bassett AS, Chow EW, Husted J, Weksberg R, Caluseriu O, Webb GD, Gatzoulis MA: Clinical features of 78 adults with 22q11 deletion syndrome. Am J Med Genet A 2005; 138: 307- 313.
38. Benito-Sanz S, Barroso E, Heine-Suner D, Hisado-Oliva A, Romanelli V, Rosell J, Aragones A, Caimari M, Argente J, Ross JL, Zinn AR, Gracia R, Lapunzina P, Campos-Barros A, Heath KE: Clinical and molecular evaluation of SHOX/PAR1 duplications in Leri- Weill dyschondrosteosis and idiopathic short stature. J Clin Endocrinol Metab 2011; 96:E404-E412.
39. Iughetti L, Capone L, Elsedfy H, Bertorelli R, Predieri B, Bruzzi P, Forabosco A, El Kholy M: Unexpected phenotype in a boy with trisomy of the SHOX gene. J Pediatr Endocrinol Metab 2010; 23: 159-169.
40. Benito-Sanz S, Thomas NS, Huber C, Gorbenko del BD, Aza-Carmona M, Crolla JA, Maloney V, Rappold G, Argente J, Campos- Barros A, Cormier-Daire V, Heath KE: A novel class of pseudoautosomal region 1 deletions downstream of SHOX is associated with Leri-Weill dyschondrosteosis. Am J Hum Genet 2005; 77: 533-544.
41. Benito-Sanz S, del Blanco DG, Aza-Carmona M, Magano LF, Lapunzina P, Argente J, Campos- Barros A, Heath KE: PAR1 deletions downstream of SHOX are the most frequent defect in a Spanish cohort of Leri-Weill dyschondrosteosis probands. Hum Mutat 2006; 27: 1062.
42. Albuisson J, Schmitt S, Baron S, Bezieau S, Benito-Sanz S, Heath KE: Clinical utility gene card for: Leri-Weill dyschondrosteosis and Langer mesomelic dysplasia. Eur J Hum Genet 2012; 20.
43. Barroso E, Benito-Sanz S, Belinchon A, Yuste- Checa P, Gracia R, Aragones A, Campos-Barros A, Heath KE: Identification of the first de novo PAR1 deletion downstream of SHOX in an individual diagnosed with Leri-Weill dyschondrosteosis. Eur J Med Genet 2010; 53: 204-207.
44. Benito-Sanz S, Royo JL, Barroso E, Paumard- Hernandez B, Barreda-Bonis AC, Liu P, Gracia R, Lupski JR, Campos-Barros A, Gomez- Skarmeta JL, Heath KE: Identification of the first recurrent PAR1 deletion in Leri-Weill dyschondrosteosis and idiopathic short stature reveals the presence of a novel SHOX enhancer. J Med Genet 2012; 49: 442-450.
45. Benito-Sanz S, Aza-Carmona M, Rodriguez-Estevez A, Rica-Etxebarria I, Gracia R, Campos- Barros A, Heath KE: Identification of the first PAR1 deletion encompassing upstream SHOX enhancers in a family with idiopathic short stature. Eur J Hum Genet 2012; 20: 125-127.
46. Kant SG, Broekman SJ, de Wit CC, Bos M, Scheltinga SA, Bakker E, Oostdijk W, van der Kamp HJ, van Zwet EW, van der Hout AH, Wit JM, Losekoot M: Phenotypic characterization of patients with deletions in the 3 ′ -flanking SHOX region. PeerJ 2013; 1:e35.
47. Walenkamp MJ, de Muinck Keizer-Schrama S, de Mos M, Kalf ME, van Duyvenvoorde HA, Boot AM, Kant SG, White SJ, Losekoot M, den Dunnen JT, Karperien M, Wit JM: Successful long-term growth hormone therapy in a girl with haploinsufficiency of the insulin- like growth factor-I receptor due to a terminal 15q26.2 → qter deletion detected by multiplex ligation probe amplification. J Clin Endocrinol Metab 2008; 93: 2421-2425.
48. Ester WA, van Duyvenvoorde HA, de Wit CC, Broekman AJ, Ruivenkamp CA, Govaerts LC, Wit JM, Hokken-Koelega AC, Losekoot M: Two short children born small for gestational age with insulin-like growth factor 1 receptor haploinsufficiency illustrate the heterogeneity of its phenotype. J Clin Endocrinol Metab 2009; 94: 4717-4727.
49. Klammt J, Kiess W, Pfaffle R: IGF1R mutations as cause of SGA. Best Pract Res Clin Endocrinol Metab 2011; 25: 191-206.
50. Horan GS, Kovacs EN, Behringer RR, Featherstone MS: Mutations in paralogous Hox genes result in overlapping homeotic transformations of the axial skeleton: evidence for unique and redundant function. Dev Biol 1995; 169: 359-372.
51. Horvath A, Boikos S, Giatzakis C, Robinson- White A, Groussin L, Griffin KJ, Stein E, Levine E, Delimpasi G, Hsiao HP, Keil M, Heyerdahl S, Matyakhina L, Libe R, Fratticci A, Kirschner LS, Cramer K, Gaillard RC, Bertagna X, Carney JA, Bertherat J, Bossis I, Stratakis CA: A genome-wide scan identifies mutations in the gene encoding phosphodiesterase 11A4 (PDE11A) in individuals with adrenocortical hyperplasia. Nat Genet 2006; 38: 794-800.
52. Itzkovitz B, Jiralerspong S, Nimmo G, Loscalzo M, Horovitz DD, Snowden A, Moser A, Steinberg S, Braverman N: Functional characterization of novel mutations in GNPAT and AGPS, causing rhizomelic chondrodysplasia punctata types 2 and 3. Hum Mutat 2012; 33: 189-197.
53. Seibler P, Djarmati A, Langpap B, Hagenah J, Schmidt A, Bruggemann N, Siebner H, Jabusch HC, Altenmuller E, Munchau A, Lohmann K, Klein C: A heterozygous frameshift mutation in PRKRA (DYT16) associated with generalised dystonia in a German patient. Lancet Neurol 2008; 7: 380-381.
54. Camargos S, Scholz S, Simon-Sanchez J, Paisan- Ruiz C, Lewis P, Hernandez D, Ding J, Gibbs JR, Cookson MR, Bras J, Guerreiro R, Oliveira CR, Lees A, Hardy J, Cardoso F, Singleton AB: DYT16, a novel young-onset dystonia- parkinsonism disorder: identification of a segregating mutation in the stress-response protein PRKRA. Lancet Neurol 2008; 7: 207-215.
55. Brunetti G, Marzano F, Colucci S, Ventura A, Cavallo L, Grano M, Faienza MF: Genotypephenotype correlation in juvenile Paget disease: role of molecular alterations of the TNFRSF11B gene. Endocrine 2012; 42: 266- 271.
56. Alain N, Zipf WB: Short stature and thyroxine- binding globulin excess: improvement with triiodothyronine treatment. Pediatrics 1988; 81: 674-679.
57. Nakai A, Shigematsu Y, Kikawa Y, Sudo M: A case of familial thyroxine-binding globulin excess associated with growth hormone deficiency. Acta Paediatr Jpn 1994; 36: 408-411.
58. Mori Y, Jing P, Kayama M, Fujieda K, Hasegawa T, Nogimori T, Hirooka Y, Mitsuma T: Gene amplification as a common cause of inherited thyroxine-binding globulin excess: Analysis of one familial and two sporadic cases. Endocr J 1999; 46: 613-619.
59. Mori Y, Miura Y, Takeuchi H, Igarashi Y, Sugiura J, Saito H, Oiso Y: Gene amplification as a cause of inherited thyroxine-binding globulin excess in two Japanese families. J Clin Endocrinol Metab 1995; 80: 3758-3762.
60. Onenli-Mungan N, Yuksel B, Ozer G, Denli G, Topaloglu AK, Teker Z: Familial thyroxinbinding globulin excess with ichthyosis: A case report. Turk J Pediatr 2004; 46: 174-176.