Heterozygous NPR2 mutations cause disproportionate short stature, similar to Léri-Weill dyschondrosteosis

Journal of Clinical Endocrinology and Metabolism

Volumn 100, Issue 8, 2015, Pages E1133-E1142

  Hisado Oliva, Alfonso ^a,b   Garre Vázquez, Ana I ^a   Santaolalla Caballero, Fabiola ^a   Belinchón, Alberta ^a,b   Barreda Bonis, Ana C ^a   Vasques, Gabriela A ^c   Ramirez, Joaquin ^d   Luzuriaga, Cristina ^e   Carlone, Gianni ^f   González Casado, Isabel ^a   Benito Sanz, Sara ^a,b   Jorge, Alexander A ^c   Campos Barros, Angel ^a,b   Heath, Karen E ^a,b  

^a HOSPITAL UNIVERSITARIO LA PAZ   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d HOSPITAL UNIVERSITARIO PRÍNCIPE DE ASTURIAS   (Spain)

^e HOSPITAL UNIVERSITARIO MARQUÉS DE VALDECILLA   (Spain)

^f HOSPITAL VIRGEN DEL PUERTO   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN NATRIURETIC PEPTIDE; CYCLIC GMP; GUANYLATE CYCLASE; NATRIURETIC PEPTIDE RECEPTOR C; ATRIAL NATRIURETIC FACTOR RECEPTOR; NATRIURETIC PEPTIDE RECEPTOR B;

ADOLESCENT; ADULT; ARTICLE; CELL MIGRATION; CHILD; DYSCHONDROSTEOSIS; ENZYME ACTIVITY; EXON; FEMALE; GENE FREQUENCY; GENE MUTATION; GENETIC CODE; GENETIC SCREENING; GENETIC VARIABILITY; HETEROZYGOTE; HUMAN; HUMAN CELL; INTRON; MAJOR CLINICAL STUDY; MALE; MUTATIONAL ANALYSIS; MUTATOR GENE; NPR2 GENE; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SCHOOL CHILD; SHORT STATURE; AMINO ACID SUBSTITUTION; ANIMAL; CHLOROCEBUS AETHIOPS; COHORT ANALYSIS; COS 1 CELL LINE; DWARFISM; GENETICS; GROWTH DISORDERS; MISSENSE MUTATION; OSTEOCHONDRODYSPLASIAS; TUMOR CELL CULTURE;

AMINO ACID SUBSTITUTION; ANIMALS; CERCOPITHECUS AETHIOPS; COHORT STUDIES; COS CELLS; DWARFISM; FEMALE; GENE FREQUENCY; GROWTH DISORDERS; HETEROZYGOTE; HUMANS; MALE; MUTATION, MISSENSE; OSTEOCHONDRODYSPLASIAS; RECEPTORS, ATRIAL NATRIURETIC FACTOR; TUMOR CELLS, CULTURED;

EID: 84939204401     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2015-1612     Document Type: Article

References (42)

1. Rappold G, Blum WF, Shavrikova EP, et al. Genotypes and phenotypes in children with short stature: clinical indicators of SHOX haploinsufficiency. J Med Genet. 2007;44:306-313.
2. Belin V, Cusin V, Viot G, et al. SHOX mutations in dyschondrosteosis (Leri-Weill syndrome). Nat Genet. 1998;19:67-69.
3. Benito-Sanz S, Thomas NS, Huber C, et al. 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.
4. Benito-Sanz S, Barroso E, Heine-Suner D, et al. Clinical and molecular evaluation of SHOX/PAR1 duplications in Leri-Weill dyschondrosteosis (LWD) and idiopathic short stature (ISS). J Clin Endocrinol Metab. 2011;96:E404-E412.
5. Benito-Sanz S, Royo JL, Barroso E, 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. J Med Genet. 2012;49:442-450.
6. Sabherwal N, Bangs F, Roth R, et al. Long-range conserved no-ncoding SHOX sequences regulate expression in developing chicken limb and are associated with short stature phenotypes in human patients. Hum Mol Genet. 2007;16:210-222.
7. Shears DJ, Vassal HJ, Goodman FR, et al. Mutation and deletion of the pseudoautosomal gene SHOX cause Leri-Weill dyschondrosteosis. Nat Genet. 1998;19:70-73.
8. Chen J, Wildhardt G, Zhong Z, et al. Enhancer deletions of the SHOX gene as a frequent cause of short stature: the essential role of a 250 kb downstream regulatory domain. J Med Genet. 2009;46:834-839.
9. Jorge AA, Souza SC, Nishi MY, et al. SHOX mutations in idiopathic short stature and Leri-Weill dyschondrosteosis: frequency and phenotypic variability. Clin Endocrinol (Oxf). 2007;66(1):130-135.
10. Ross JL, Scott C Jr, Marttila P, et al. Phenotypes associated with SHOX deficiency. J Clin Endocrinol Metab. 2001;86:5674-5680.
11. Shears DJ, Guillen-Navarro E, Sempere-Miralles M, Domingo-Jimenez R, Scambler PJ, Winter RM. Pseudodominant inheritance of Langer mesomelic dysplasia caused by a SHOX homeobox missense mutation. Am J Med Genet. 2002;110:153-157.
12. Zinn AR, Wei F, Zhang L, et al. Complete SHOX deficiency causes Langer mesomelic dysplasia. Am J Med Genet. 2002;110:158-163.
13. Campos-Barros A, Benito-Sanz S, Ross JL, Zinn AR, Heath KE. Compound heterozygosity of SHOX-encompassing and downstream PAR1 deletions results in Langer mesomelic dysplasia (LMD). Am J Med Genet A. 2007;143A:933-938.
14. Bertorelli R, Capone L, Ambrosetti F, et al. The homozygous deletion of the 3′ enhancer of the SHOX gene causes Langer mesomelic dysplasia. Clin Genet. 2007;72:490-491.
15. Maroteaux P, Martinelli B, Campailla E. [Acromesomelic dwarfism]. Presse Medicale. 1971;79:1839-1842.
16. Bartels CF, Bukulmez H, Padayatti P, et al. Mutations in the transmembrane natriuretic peptide receptor NPR-B impair skeletal growth and cause acromesomelic dysplasia, type Maroteaux. Am J Hum Genet. 2004;75:27-34.
17. Tamura N, Doolittle LK, Hammer RE, Shelton JM, Richardson JA, Garbers DL. Critical roles of the guanylyl cyclase B receptor in endochondral ossification and development of female reproductive organs. Proc Natl Acad Sci USA. 2004;101:17300-17305.
18. Tsuji T, Kunieda T. A loss-of-function mutation in natriuretic peptide receptor 2 (Npr2) gene is responsible for disproportionate dwarfism in cn/cn mouse. J Biol Chem. 2005;280:14288-14292.
19. Sogawa C, Tsuji T, Shinkai Y, Katayama K, Kunieda T. Short-limbed dwarfism: slw is a new allele of Npr2 causing chondrodysplasia. J Hered. 2007;98:575-580.
20. Hume AN, Buttgereit J, Al-Awadhi AM, et al. Defective cellular trafficking of missense NPR-B mutants is the major mechanism underlying acromesomelic dysplasia-type Maroteaux. Hum Mol Genet. 2009;18:267-277.
21. Borrelli P, Fasanelli S, Marini R. Acromesomelic dwarfism in a child with an interesting family history. Pediatr Radiol. 1983;13:165-168.
22. Olney RC, Bukulmez H, Bartels CF, et al. Heterozygous mutations in natriuretic peptide receptor-B (NPR2) are associated with short stature. J Clin Endocrinol Metab. 2006;91:1229-1232.
23. Vasques GA, Amano N, Docko AJ, et al. Heterozygous mutations in natriuretic peptide receptor-B (NPR2) gene as a cause of short stature in patients initially classified as idiopathic short stature. J Clin Endocrinol Metab. 2013;98:E1636-E1644.
24. Amano N, Mukai T, Ito Y, et al. Identification and functional characterization of two novel NPR2 mutations in Japanese patients with short stature. J Clin Endocrinol Metab. 2014;99:E713-E718.
25. Wang SR, Jacobsen CM, Carmichael H, et al. Heterozygous mutations in natriuretic peptide receptor-B (NPR2) gene as a cause of short stature. Hum Mutat. 2015;36(4):474-481.
26. Potter LR, Abbey-Hosch S, Dickey DM. Natriuretic peptides, their receptors, and cyclic guanosine monophosphate-dependent signaling functions. Endocr Rev. 2006;27:47-72.
27. Koller KJ, Lowe DG, Bennett GL, et al. Selective activation of the B natriuretic peptide receptor by C-type natriuretic peptide (CNP). Science. 1991;252:120-123.
28. Suga S, Nakao K, Hosoda K, et al. Receptor selectivity of natriuretic peptide family, atrial natriuretic peptide, brain natriuretic peptide, and C-type natriuretic peptide. Endocrinology. 1992;130:229-239.
29. Benito-Sanz S, del Blanco DG, Aza-Carmona M, et al. PAR1 deletions downstream of SHOX are the most frequent defect in a Spanish cohort of Leri-Weill dyschondrosteosis (LWD) probands. Hum Mutat. 2006;27:1062.
30. Huber C, Rosilio M, Munnich A, Cormier-Daire V, French SGM. High incidence of SHOX anomalies in individuals with short stature. J Med Genet. 2006;43:735-739.
31. Carrascosa A, Fernandez JM, Fernandez C, et al. Spanish growth studies 2008. New anthropometric standards. Endocrinol Nutr. 2008;55:484-506.
32. Benito-Sanz S, Gorbenko del Blanco D, Huber C, et al. Characterization of SHOX deletions in Leri-Weill dyschondrosteosis (LWD) reveals genetic heterogeneity and no recombination hotspots. Am J Hum Genet. 2006;7 9(2):409-414.
33. Hachiya R, Ohashi Y, Kamei Y, et al. Intact kinase homology domain of natriuretic peptide receptor-B is essential for skeletal development. J Clin Endocrinol Metab. 2007;92:4009-4014.
34. Barca-Tierno V, Aza-Carmona M, Barroso E, et al. Identification of a gypsy SHOX mutation (p.A170P) in Leri-Weill dyschondrosteosis and Langer mesomelic dysplasia. Eur J Hum Genet. 2011;19:1218-1225.
35. Cohen P, Rogol AD, Deal CL, et al. Consensus statement on the diagnosis and treatment of children with idiopathic short stature: a summary of the Growth Hormone Research Society, the Lawson Wilkins Pediatric Endocrine Society, and the European Society for Paediatric Endocrinology Workshop. J Clin Endocrinol Metab 2008;93:4210-4217.
36. Marchini A, Hacker B, Marttila T, et al. BNP is a transcriptional target of the short stature homeobox gene SHOX. Hum Mol Genet. 2007;16:3081-3087.
37. Aza-Carmona M, Shears DJ, Yuste-Checa P, et al. SHOX interacts with the chondrogenic transcription factors SOX5 and SOX6 to activate the aggrecan enhancer. Hum Mol Genet. 2011;20:1547-1559.
38. Decker E, Durand C, Bender S, et al. FGFR3 is a target of the homeobox transcription factor SHOX in limb development. Hum Mol Genet. 2011;20:1524-1535.
39. Tiecke E, Bangs F, Blaschke R, Farrell ER, Rappold G, Tickle C. Expression of the short stature homeobox gene Shox is restricted by proximal and distal signals in chick limb buds and affects the length of skeletal elements. Dev Biol. 2006;298:585-596.
40. Peake NJ, Hobbs AJ, Pingguan-Murphy B, Salter DM, Berenbaum F, Chowdhury TT. Role of C-type natriuretic peptide signalling in maintaining cartilage and bone function. Osteoarthritis Cartilage. 2014;22:1800-1807.
41. Binder G. Short stature due to SHOX deficiency: genotype, phenotype, and therapy. Horm Res Paediatr. 2011;75:81-89.
42. Blum WF, Crowe BJ, Quigley CA, et al. 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. J Clin Endocrinol Metab. 2007;92:219-228.