The growth response to GH treatment is greater in patients with SHOX enhancer deletions compared to SHOX defects

European Journal of Endocrinology

Volumn 173, Issue 5, 2015, Pages 611-621

  Donze, S H ^a   Meijer, C R ^a   Kant, S G ^a   Zandwijken, G R J ^b   Van Der Hout, A H ^c   Van Spaendonk, R M L ^d   Van Den Ouweland, A M W ^e   Wit, J M ^a   Losekoot, M ^a   Oostdijk, W ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b Dutch Growth Research Foundation ('Stichting Kind en Groei')   (Netherlands)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^e ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

RECOMBINANT GROWTH HORMONE; SOMATOMEDIN C; HOMEODOMAIN PROTEIN; HUMAN GROWTH HORMONE; SHOX PROTEIN, HUMAN;

ARM CIRCUMFERENCE; ARTICLE; BODY GROWTH; BODY HEIGHT; BONE MATURATION; CHILD; CONTROLLED STUDY; DRUG RESPONSE; ENHANCER REGION; FEMALE; GENE; GENE DELETION; GENE DUPLICATION; GROWTH RATE; HUMAN; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; RETROSPECTIVE STUDY; SHORT STATURE; SHOX GENE; ADOLESCENT; CLINICAL TRIAL; COMPARATIVE STUDY; DRUG EFFECTS; GENETICS; GROWTH DISORDERS; INFANT; MULTICENTER STUDY; MUTATION; PRESCHOOL CHILD; TREATMENT OUTCOME;

ADOLESCENT; BODY HEIGHT; CHILD; CHILD, PRESCHOOL; FEMALE; GENE DELETION; GROWTH DISORDERS; HOMEODOMAIN PROTEINS; HUMAN GROWTH HORMONE; HUMANS; INFANT; MALE; MUTATION; TREATMENT OUTCOME;

EID: 84946018858     PISSN: 08044643     EISSN: 1479683X     Source Type: Journal    
DOI: 10.1530/EJE-15-0451     Document Type: Article

References (40)

1. Sabherwal N, Bangs F, Roth R, Weiss B, Jantz K, Tiecke E, Hinkel GK, Spaich C, Hauffa BP, van der Kamp H et al. Long-range conserved non-coding SHOX sequences regulate expression in developing chicken limb and are associated with short stature phenotypes in human patients. Human Molecular Genetics 2007 16 210-222. (doi:10.1093/hmg/ddl470)
2. Benito-Sanz S, Thomas NS, Huber C, Gorbenko del Blanco D, Aza-Carmona M, Crolla JA, Maloney V, Rappold G, Argente J, Campos-Barros A et al. A novel class of pseudoautosomal region 1 deletions downstream of SHOX is associated with Leri-Weill dyschondrosteosis. American Journal of Human Genetics 2005 77 533-544. (doi:10.1086/449313)
3. Rao E, Weiss B, Fukami M, Rump A, Niesler B, Mertz A, Muroya K, Binder G, Kirsch S, Winkelmann M et al. Pseudoautosomal deletions encompassing a novel homeobox gene cause growth failure in idiopathic short stature and Turner syndrome. Nature Genetics 1997 16 54-63. (doi:10.1038/ng0597-54)
4. Kant SG, van der Kamp HJ, Kriek M, Bakker E, Bakker B, Hoffer MJ, van Bunderen P, Losekoot M, Maas SM, Wit JM et al. The jumping SHOX gene-crossover in the pseudoautosomal region resulting in unusual inheritance of Leri-Weill dyschondrosteosis. Journal of Clinical Endocrinology and Metabolism 2011 96 E356-E359. (doi:10.1210/jc.2010-1505)
5. Fukami M, Kato F, Tajima T, Yokoya S & Ogata T. Transactivation function of an approximately 800-bp evolutionarily conserved sequence at the SHOX 3 region: implication for the downstream enhancer. American Journal of Human Genetics 2006 78 167-170. (doi:10.1086/499254)
6. Chen J, Wildhardt G, Zhong Z, Roth R, Weiss B, Steinberger D, Decker J, Blum WF & Rappold G. Enhancer deletions of the SHOX gene as a frequent cause of short stature: the essential role of a 250 kb downstream regulatory domain. Journal of Medical Genetics 2009 46 834-839. (doi:10.1136/jmg.2009.067785)
7. Durand C, Bangs F, Signolet J, Decker E, Tickle C & Rappold G. Enhancer elements upstream of the SHOX gene are active in the developing limb. European Journal of Human Genetics 2010 18 527-532. (doi:10.1038/ejhg.2009.216)
8. Kenyon EJ, McEwen GK, Callaway H & Elgar G. Functional analysis of conserved non-coding regions around the short stature hox gene (shox) in whole zebrafish embryos. PLoS ONE 2011 6 e21498. (doi:10.1371/journal.pone.0021498)
9. Evers C, Heidemann PH, Dunstheimer D, Schulze E, Haag C, Janssen JW, Fischer C, Jauch A & Moog U. Pseudoautosomal inheritance of Leri-Weill syndrome: what does it mean? Clinical Genetics 2011 79 489-494. (doi:10.1111/j.1399-0004.2010.01488.x)
10. 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 et al. Phenotypic characterization of patients with deletions in the 3-flanking SHOX region. PeerJ 2013 1 e35. (doi:10.7717/peerj.35)
11. 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 et al. Identification of the first recurrent PAR1 deletion in Leri-Weill dyschondrosteosis and idiopathic short stature reveals the presence of a novel SHOX enhancer. Journal of Medical Genetics 2012 49 442-450. (doi:10.1136/jmedgenet-2011-100678)
12. 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. Journal of Pediatric Endocrinology & Metabolism 2010 23 159-169. (doi:10.1515/JPEM.2010.23.1-2.159)
13. Benito-Sanz S, Barroso E, Heine-Suner D, Hisado-Oliva A, Romanelli V, Rosell J, Aragones A, Caimari M, Argente J, Ross JL et al. Clinical and molecular evaluation of SHOX/PAR1 duplications in Leri-Weill dyschondrosteosis (LWD) and idiopathic short stature (ISS). Journal of Clinical Endocrinology and Metabolism 2011 96 E404-E412. (doi:10.1210/jc.2010-1689)
14. Caliebe J, Broekman S, Boogaard M, Bosch CA, Ruivenkamp CA, Oostdijk W, Kant SG, Binder G, Ranke MB, Wit JM et al. IGF1, IGF1R and SHOX mutation analysis in short children born small for gestational age and short children with normal birth size (idiopathic short stature). Hormone Research in Paediatrics 2012 77 250-260. (doi:10.1159/000338341)
15. Wit JM, van Duyvenvoorde HA, van Klinken JB, Caliebe J, Bosch CA, Lui JC, Gijsbers AC, Bakker E, Breuning MH, Oostdijk W et al. Copy number variants in short children born small for gestational age. Hormone Research in Paediatrics 2014 82 310-318. (doi:10.1159/000367712)
16. Blum WF, Crowe BJ, Quigley CA, Jung H, Cao D, Ross JL, Braun L & Rappold G. Growth hormone is effective in treatment of short stature associated with short stature homeobox-containing gene deficiency: two-year results of a randomized, controlled, multicenter trial. Journal of Clinical Endocrinology and Metabolism 2007 92 219-228. (doi:10.1210/jc.2006-1409)
17. Massart F, Bizzi M, Baggiani A & Miccoli M. Height outcome of the recombinant human growth hormone treatment in patients with SHOX gene haploinsufficiency: a meta-analysis. Pharmacogenomics 2013 14 607-612. (doi:10.2217/pgs.13.44)
18. Bunyan DJ, Baker KR, Harvey JF & Thomas NS. Diagnostic screening identifies a wide range of mutations involving the SHOX gene, including a common 47.5 kb deletion 160 kb downstream with a variable phenotypic effect. American Journal of Medical Genetics. Part A 2013 161A 1329-1338. (doi:10.1002/ajmg.a.35919)
19. 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. Helvetica Paediatrica Acta. Supplementum 1989 52 1-125.
20. Ranke MB, Lindberg A, Brosz M, Kaspers S, Loftus J, Wollmann H, Koltowska-Haggstrom M & Roelants M. Accurate long-term prediction of height during the first four years of growth hormone treatment in prepubertal children with growth hormone deficiency or Turner syndrome. Hormone Research in Paediatrics 2012 78 8-17. (doi:10.1159/000339468)
21. Blum WF, Ross JL, Zimmermann AG, Quigley CA, Child CJ, Kalifa G, Deal C, Drop SL, Rappold G & Cutler GB Jr. GH treatment to final height produces similar height gains in patients with SHOX deficiency and Turner syndrome: results of a multicenter trial. Journal of Clinical Endocrinology and Metabolism 2013 98 E1383-E1392. (doi:10.1210/jc. 2013-1222)
22. Ranke MB & Lindberg A. Observed and predicted growth responses in prepubertal children with growth disorders: guidance of growth hormone treatment by empirical variables. Journal of Clinical Endocrinology and Metabolism 2010 95 1229-1237. (doi:10.1210/jc.2009-1471)
23. Ranke MB, Lindberg A, Chatelain P, Wilton P, Cutfield W, Albertsson-Wikland K & Price DA. Prediction of long-term response to recombi-nant human growth hormone in Turner syndrome: development and validation of mathematical models. KIGS International Board. Kabi International Growth Study. Journal of Clinical Endocrinology and Metabolism 2000 85 4212-4218. (doi:10.1210/jcem.85.11.6976)
24. Ranke MB & Lindberg A. Predicting growth in response to growth hormone treatment. Growth Hormone & IGF Research 2009 19 1-11. (doi:10.1016/j.ghir.2008.08.001)
25. Fredriks AM, van Buuren S, van Heel WJ, Dijkman-Neerincx RH, Verloove-Vanhorick SP & Wit JM. Nationwide age references for sitting height, leg length, and sitting height/height ratio, and their diagnostic value for disproportionate growth disorders. Archives of Disease in Childhood 2005 90 807-812. (doi:10.1136/adc.2004.050799)
26. Schonbeck Y, Talma H, van Dommelen P, Bakker B, Buitendijk SE, HiraSing RA & van Buuren S. The world's tallest nation has stopped growing taller: the height of Dutch children from 1955 to 2009. Pediatric Research 2013 73 371-377. (doi:10.1038/pr.2012.189)
27. van Dommelen P, Schonbeck Y & van Buuren S. A simple calculation of the target height. Archives of Disease in Childhood 2012 97 182. (doi:10.1136/archdischild-2011-301095)
28. Cole TJ & Roede MJ. Centiles of body mass index for Dutch children aged 0-20 years in 1980-a baseline to assess recent trends in obesity. Annals of Human Biology 1999 26 303-308. (doi:10.1080/030144699282633)
29. 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 Paediatrica Scandinavica 1991 80 756-762. (doi:10.1111/j.1651-2227. 1991.tb11945.x)
30. Rikken B, van Doorn J, Ringeling A, Van den Brande JL, Massa G & Wit JM. Plasma levels of insulin-like growth factor (IGF)-I, IGF-II and IGF-binding protein-3 in the evaluation of childhood growth hormone deficiency. Hormone Research 1998 50 166-176. (doi:10.1159/000023268)
31. Binder G, Ranke MB & Martin DD. Auxology is a valuable instrument for the clinical diagnosis of SHOX haploinsufficiency in school-age children with unexplained short stature. Journal of Clinical Endocrinology and Metabolism 2003 88 4891-4896. (doi:10.1210/jc.2003-030136)
32. Freeman JV, Cole TJ, Chinn S, Jones PR, White EM & Preece MA. Cross sectional stature and weight reference curves for the UK, 1990. Archives of Disease in Childhood 1995 73 17-24. (doi:10.1136/adc.73.1.17)
33. Cole TJ. Some questions about how growth standards are used. Hormone Research 1996 45 (Suppl 2) 18-23. (doi:10.1159/000184843)
34. Binder G. Short stature due to SHOX deficiency: genotype, phenotype, and therapy. Hormone Research in Paediatrics 2011 75 81-89. (doi:10.1159/000324105)
35. Rosilio M, Huber-Lequesne C, Sapin H, Carel JC, Blum WF & Cormier-Daire V. Genotypes and phenotypes of children with SHOX deficiency in France. Journal of Clinical Endocrinology and Metabolism 2012 97 E1257-E1265. (doi:10.1210/jc.2011-3460)
36. Rappold G, Blum WF, Shavrikova EP, Crowe BJ, Roeth R, Quigley CA, Ross JL & Niesler B. Genotypes and phenotypes in children with short stature: clinical indicators of SHOX haploinsufficiency. Journal of Medical Genetics 2007 44 306-313. (doi:10.1136/jmg.2006.046581)
37. Ogata T, Matsuo N & Nishimura G. SHOX haploinsufficiency and overdosage: impact of gonadal function status. Journal of Medical Genetics 2001 38 1-6. (doi:10.1136/jmg.38.1.1)
38. Adamson KA, Cross I, Batch JA, Rappold GA, Glass IA & Ball SG. Trisomy of the short stature homeobox-containing gene (SHOX), resulting from a duplication-deletion of the X chromosome. Clinical Endocrinology 2002 56 671-675. (doi:10.1046/j.1365-2265. 2002.01504.x)
39. Thomas NS, Harvey JF, Bunyan DJ, Rankin J, Grigelioniene G, Bruno DL, Tan TY, Tomkins S & Hastings R. Clinical and molecular characterization of duplications encompassing the human SHOX gene reveal a variable effect on stature. American Journal of Medical Genetics. Part A 2009 149A 1407-1414. (doi:10.1002/ajmg.a.32914)
40. Li Q, Barkess G & Qian H. Chromatin looping and the probability of transcription. Trends in Genetics 2006 22 197-202. (doi:10.1016/j.tig. 2006.02.004)