Clinical and molecular analysis in families with autosomal recessive osteogenesis imperfecta identifies mutations in five genes and suggests genotype-phenotype correlations

American Journal of Medical Genetics, Part A

Volumn 161, Issue 6, 2013, Pages 1354-1369

  Caparrós Martin, José A ^a,b   Valencia, María ^a   Pulido, Veronica ^a   Martínez Glez, Victor ^b,c   Rueda Arenas, Inmaculada ^c   Amr, Khalda ^d   Farra, Chantal ^e   Lapunzina, Pablo ^b,c   Ruiz Perez, Victor L ^a,b   Temtamy, Samia ^d   Aglan, Mona ^d  

^a CSIC   (Spain)

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

^c HOSPITAL UNIVERSITARIO LA PAZ IDIPAZ   (Spain)

^d NATIONAL RESEARCH CENTRE   (Egypt)

^e AMERICAN UNIVERSITY OF BEIRUT   (Lebanon)

Author keywords

AluYb8; Bruck syndrome; Collagen type I; Osteogenesis imperfecta

Indexed keywords

CALCIUM; ZOLEDRONIC ACID; BISPHOSPHONIC ACID DERIVATIVE; COLLAGEN TYPE 1; CRTAP PROTEIN, HUMAN; CYCLOPHILIN; CYCLOPHILIN B; EYE PROTEIN; FK 506 BINDING PROTEIN; FKBP10 PROTEIN, HUMAN; LEPRE1 PROTEIN, HUMAN; MEMBRANE PROTEIN; NERVE GROWTH FACTOR; PIGMENT EPITHELIUM-DERIVED FACTOR; PROTEOGLYCAN; SCLEROPROTEIN; SERINE PROTEINASE INHIBITOR;

ARTICLE; AUTOSOMAL RECESSIVE DISORDER; BONE DENSITY; CLINICAL ASSESSMENT; CONTROLLED STUDY; CRANIOFACIAL MALFORMATION; CRTAP GENE; DISEASE SEVERITY; FEMALE; FKBP10 GENE; GENE; GENE EXPRESSION; GENE INSERTION; GENE MUTATION; GENETIC ASSOCIATION; GENOTYPE PHENOTYPE CORRELATION; HUMAN; LEPRE1 GENE; MALE; MICROSATELLITE MARKER; NUCLEOTIDE SEQUENCE; OSTEOGENESIS IMPERFECTA; PPIB GENE; PRIORITY JOURNAL; SERPINF1 GENE; ADOLESCENT; ALU SEQUENCE; CHILD; DNA SEQUENCE; GENETIC ASSOCIATION STUDY; GENETICS; INFANT; MOLECULAR GENETICS; MUTATION; PATHOLOGY; PEDIGREE; PRESCHOOL CHILD; RADIOGRAPHY; RECESSIVE GENE; YOUNG ADULT;

ADOLESCENT; ALU ELEMENTS; CHILD; CHILD, PRESCHOOL; COLLAGEN TYPE I; CYCLOPHILINS; DIPHOSPHONATES; EXTRACELLULAR MATRIX PROTEINS; EYE PROTEINS; FEMALE; GENES, RECESSIVE; GENETIC ASSOCIATION STUDIES; HUMANS; INFANT; MALE; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; NERVE GROWTH FACTORS; OSTEOGENESIS IMPERFECTA; PEDIGREE; PROTEOGLYCANS; SEQUENCE ANALYSIS, DNA; SERPINS; TACROLIMUS BINDING PROTEINS; YOUNG ADULT;

EID: 84878245621     PISSN: 15524825     EISSN: 15524833     Source Type: Journal    
DOI: 10.1002/ajmg.a.35938     Document Type: Article

References (42)

1. Aglan MS, Hosny L, El-Houssini R, Abdelhadi S, Salem F, ElBanna RAS, Awad SA, Zaki ME, Temtamy SA. 2012. A scoring system for the assessment of clinical severity in osteogenesis imperfecta. J Child Orthop 6:29-35.
2. Alanay Y, Avaygan H, Camacho N, Utine GE, Boduroglu K, Aktas D, Alikasifoglu M, Tuncbilek E, Orhan D, Bakar FT, Zabel B, Superti-Furga A, Bruckner-Tuderman L, Curry CJ, Pyott S, Byers PH, Eyre DR, Baldridge D, Lee B, Merrill AE, Davis EC, Cohn DH, Akarsu N, Krakow D. 2010. Mutations in the gene encoding the RER protein FKBP65 cause autosomal-recessive osteogenesis imperfecta. Am J Hum Genet 86:551-559.
3. Asharani PV, Keupp K, Semler O, Wang W, Li Y, Thiele H, Yigit G, Pohl E, Becker J, Frommolt P, Sonntag C, Altmuller J, Zimmermann K, Greenspan DS, Akarsu NA, Netzer C, Schonau E, Wirth R, Hammerschmidt M, Nurnberg P, Wollnik B, Carney TJ. 2012. Attenuated BMP1 function compromises osteogenesis, leading to bone fragility in humans and zebrafish. Am J Hum Genet 90:661-674.
4. Barnes AM, Chang W, Morello R, Cabral WA, Weis M, Eyre DR, Leikin S, Makareeva E, Kuznetsova N, Uveges TE, Ashok A, Flor AW, Mulvihill JJ, Wilson PL, Sundaram UT, Lee B, Marini JC. 2006. Deficiency of cartilage-associated protein in recessive lethal osteogenesis imperfecta. N Engl J Med 355:2757-2764.
5. Barnes AM, Carter EM, Cabral WA, Weis M, Chang W, Makareeva E, Leikin S, Rotimi CN, Eyre DR, Raggio CL, Marini JC. 2010. Lack of cyclophilin B in osteogenesis imperfecta with normal collagen folding. N Engl J Med 362:521-528.
6. Barnes AM, Cabral WA, Weis M, Makareeva E, Mertz EL, Leikin S, Eyre D, Trujillo C, Marini JC. 2012. Absence of FKBP10 in recessive type XI OI leads to diminished collagen cross-linking and reduced collagen deposition in extracellular matrix. Hum Mutat 33:1589-1598.
7. Batzer MA, Deininger PL. 2002. Alu repeats and human genomic diversity. Nat Rev Genet 3:370-379.
8. Becker J, Semler O, Gilissen C, Li Y, Bolz HJ, Giunta C, Bergmann C, Rohrbach M, Koerber F, Zimmermann K, de Vries P, Wirth B, Schoenau E, Wollnik B, Veltman JA, Hoischen A, Netzer C. 2011. Exome sequencing identifies truncating mutations in human SERPINF1 in autosomal-recessive osteogenesis imperfecta. Am J Hum Genet 88:362-371.
9. Byers PH, Steiner RD. 1992. Osteogenesis imperfecta. Annu Rev Med 43:269-282.
10. Cabral WA, Chang W, Barnes AM, Weis M, Scott MA, Leikin S, Makareeva E, Kuznetsova NV, Rosenbaum KN, Tifft CJ, Bulas DI, Kozma C, Smith PA, Eyre DR, Marini JC. 2007. Prolyl 3-hydroxylase 1 deficiency causes a recessive metabolic bone disorder resembling lethal/severe osteogenesis imperfecta. Nat Genet 39:359-365.
11. Canty EG, Kadler KE. 2005. Procollagen trafficking, processing and fibrillogenesis. J Cell Sci 118:1341-1353.
12. Chang W, Barnes AM, Cabral WA, Bodurtha JN, Marini JC. 2010. Prolyl 3-hydroxylase 1 and CRTAP are mutually stabilizing in the endoplasmic reticulum collagen prolyl 3-hydroxylation complex. Hum Mol Genet 19:223-234.
13. Chines A, Boniface A, McAlister W, Whyte M. 1995. Hypercalciuria in osteogenesis imperfecta: A follow-up study to assess renal effects. Bone 16:333-339.
14. Cho TJ, Lee KE, Lee SK, Song SJ, Kim KJ, Jeon D, Lee G, Kim HN, Lee HR, Eom HH, Lee ZH, Kim OH, Park WY, Park SS, Ikegawa S, Yoo WJ, Choi IH, Kim JW. 2012. A single recurrent mutation in the 5'-UTR of IFITM5 causes osteogenesis imperfecta Type V. Am J Hum Genet 91:343-348.
15. Christiansen HE, Schwarze U, Pyott SM, AlSwaid A, Al Balwi M, Alrasheed S, Pepin MG, Weis MA, Eyre DR, Byers PH. 2010. Homozygosity for a missense mutation in SERPINH1, which encodes the collagen chaperone protein HSP47, results in severe recessive osteogenesis imperfecta. Am J Hum Genet 86:389-398.
16. Dawson DW, Volpert OV, Gillis P, Crawford SE, Xu H, Benedict W, Bouck NP. 1999. Pigment epithelium-derived factor: A potent inhibitor of angiogenesis. Science 285:245-248.
17. den Dunnen JT, Antonarakis SE. 2000. Mutation nomenclature extensions and suggestions to describe complex mutations: A discussion. Hum Mutat 15:7-12.
18. den Dunnen JT, Paalman MH. 2003. Standardizing mutation nomenclature: Why bother? Hum Mutat 22:181-182.
19. Ha-Vinh R, Alanay Y, Bank RA, Campos-Xavier AB, Zankl A, Superti-Furga A, Bonafe L. 2004. Phenotypic and molecular characterization of Bruck syndrome (osteogenesis imperfecta with contractures of the large joints) caused by a recessive mutation in PLOD2. Am J Med Genet Part A 131A:115-120.
20. Homan EP, Rauch F, Grafe I, Lietman C, Doll JA, Dawson B, Bertin T, Napierala D, Morello R, Gibbs R, White L, Miki R, Cohn DH, Crawford S, Travers R, Glorieux FH, Lee B. 2011. Mutations in SERPINF1 cause osteogenesis imperfecta type VI. J Bone Miner Res 26:2798-2803.
21. Kelley BP, Malfait F, Bonafe L, Baldridge D, Homan E, Symoens S, Willaert A, Elcioglu N, Van Maldergem L, Verellen-Dumoulin C, Gillerot Y, Napierala D, Krakow D, Beighton P, Superti-Furga A, De Paepe A, Lee B. 2011. Mutations in FKBP10 cause recessive osteogenesis imperfecta and Bruck syndrome. J Bone Miner Res 26:666-672.
22. Koerber F, Schulze Uphoff U, Koerber S, Schonau E, Maintz D, Semler O. 2012. Introduction of a new standardized assessment score of spine morphology in osteogenesis imperfecta. Rofo 184:719-725.
23. Lapunzina P, Aglan M, Temtamy S, Caparros-Martin JA, Valencia M, Leton R, Martinez-Glez V, Elhossini R, Amr K, Vilaboa N, Ruiz-Perez VL. 2010. Identification of a frameshift mutation in Osterix in a patient with recessive osteogenesis imperfecta. Am J Hum Genet 87:110-114.
24. Marini JC, Cabral WA, Barnes AM. 2010. Null mutations in LEPRE1 and CRTAP cause severe recessive osteogenesis imperfecta. Cell Tissue Res 339:59-70.
25. Martinez-Glez V, Valencia M, Caparros-Martin JA, Aglan M, Temtamy S, Tenorio J, Pulido V, Lindert U, Rohrbach M, Eyre D, Giunta C, Lapunzina P, Ruiz-Perez VL. 2012. Identification of a mutation causing deficient BMP1/mTLD proteolytic activity in autosomal recessive osteogenesis imperfecta. Hum Mutat 33:343-350.
26. Morello R, Bertin TK, Chen Y, Hicks J, Tonachini L, Monticone M, Castagnola P, Rauch F, Glorieux FH, Vranka J, Bachinger HP, Pace JM, Schwarze U, Byers PH, Weis M, Fernandes RJ, Eyre DR, Yao Z, Boyce BF, Lee B. 2006. CRTAP is required for prolyl 3-hydroxylation and mutations cause recessive osteogenesis imperfecta. Cell 127:291-304.
27. Puig-Hervas MT, Temtamy S, Aglan M, Valencia M, Martinez-Glez V, Ballesta-Martinez MJ, Lopez-Gonzalez V, Ashour AM, Amr K, Pulido V, Guillen-Navarro E, Lapunzina P, Caparros-Martin JA, Ruiz-Perez VL. 2012. Mutations in PLOD2 cause autosomal-recessive connective tissue disorders within the Bruck syndrome-Osteogenesis imperfecta phenotypic spectrum. Hum Mutat 33:1444-1449.
28. Pyott SM, Schwarze U, Christiansen HE, Pepin MG, Leistritz DF, Dineen R, Harris C, Burton BK, Angle B, Kim K, Sussman MD, Weis M, Eyre DR, Russell DW, McCarthy KJ, Steiner RD, Byers PH. 2011. Mutations in PPIB (cyclophilin B) delay type I procollagen chain association and result in perinatal lethal to moderate osteogenesis imperfecta phenotypes. Hum Mol Genet 20:1595-1609.
29. Rohrbach M, Giunta C. 2012. Recessive osteogenesis imperfecta: Clinical, radiological, and molecular findings. Am J Med Genet Part C 160C:175-189.
30. Schwarze U, Cundy T, Pyott SM, Christiansen HE, Hegde MR, Bank RA, Pals G, Ankala A, Conneely K, Seaver L, Yandow SM, Raney E, Babovic-Vuksanovic D, Stoler J, Ben-Neriah Z, Segel R, Lieberman S, Siderius L, Al-Aqeel A, Hannibal M, Hudgins L, McPherson E, Clemens M, Sussman MD, Steiner RD, Mahan J, Smith R, Anyane-Yeboa K, Wynn J, Chong K, Uster T, Aftimos S, Sutton VR, Davis EC, Kim LS, Weis MA, Eyre D, Byers PH. 2013. Mutations in FKBP10, which result in Bruck syndrome and recessive forms of osteogenesis imperfecta, inhibit the hydroxylation of telopeptide lysines in bone collagen. Hum Mol Genet 22:1-17.
31. Semler O, Garbes L, Keupp K, Swan D, Zimmermann K, Becker J, Iden S, Wirth B, Eysel P, Koerber F, Schoenau E, Bohlander SK, Wollnik B, Netzer C. 2012a. A mutation in the 5'-UTR of IFITM5 creates an in-frame start codon and causes autosomal-dominant osteogenesis imperfecta Type V with hyperplastic callus. Am J Hum Genet 91:349-357.
32. Semler O, Netzer C, Hoyer-Kuhn H, Becker J, Eysel P, Schoenau E. 2012b. First use of the RANKL antibody denosumab in Osteogenesis Imperfecta Type VI. J Musculoskelet Neuronal Interact 12:183-188.
33. Shaheen R, Al-Owain M, Sakati N, Alzayed ZS, Alkuraya FS. 2010. FKBP10 and Bruck syndrome: Phenotypic heterogeneity or call for reclassification? Am J Hum Genet 87:306-307; author reply 308.
34. Shaheen R, Al-Owain M, Faqeih E, Al-Hashmi N, Awaji A, Al-Zayed Z, Alkuraya FS. 2011. Mutations in FKBP10 cause both Bruck syndrome and isolated osteogenesis imperfecta in humans. Am J Med Genet Part A 155A:1448-1452.
35. Sillence DO, Rimoin DL, Danks DM. 1979. Clinical variability in osteogenesis imperfecta-variable expressivity or genetic heterogeneity. Birth Defects Orig Artic Ser 15:113-129.
36. van der Slot AJ, Zuurmond AM, Bardoel AF, Wijmenga C, Pruijs HE, Sillence DO, Brinckmann J, Abraham DJ, Black CM, Verzijl N, DeGroot J, Hanemaaijer R, TeKoppele JM, Huizinga TW, Bank RA. 2003. Identification of PLOD2 as telopeptide lysyl hydroxylase, an important enzyme in fibrosis. J Biol Chem 278:40967-40972.
37. van Dijk FS, Nesbitt IM, Zwikstra EH, Nikkels PG, Piersma SR, Fratantoni SA, Jimenez CR, Huizer M, Morsman AC, Cobben JM, van Roij MH, Elting MW, Verbeke JI, Wijnaendts LC, Shaw NJ, Hogler W, McKeown C, Sistermans EA, Dalton A, Meijers-Heijboer H, Pals G. 2009. PPIB mutations cause severe osteogenesis imperfecta. Am J Hum Genet 85:521-527.
38. Van Dijk FS, Pals G, Van Rijn RR, Nikkels PG, Cobben JM. 2010. Classification of Osteogenesis Imperfecta revisited. Eur J Med Genet 53:1-5.
39. van Dijk FS, Byers PH, Dalgleish R, Malfait F, Maugeri A, Rohrbach M, Symoens S, Sistermans EA, Pals G. 2012. EMQN best practice guidelines for the laboratory diagnosis of osteogenesis imperfecta. Eur J Hum Genet 20:11-19.
40. Vetter U, Maierhofer B, Muller M, Lang D, Teller WM, Brenner R, Frohneberg D, Worsdorfer O. 1989. Osteogenesis imperfecta in childhood: Cardiac and renal manifestations. Eur J Pediatr 149:184-187.
41. Warman ML, Cormier-Daire V, Hall C, Krakow D, Lachman R, LeMerrer M, Mortier G, Mundlos S, Nishimura G, Rimoin DL, Robertson S, Savarirayan R, Sillence D, Spranger J, Unger S, Zabel B, Superti-Furga A. 2011. Nosology and classification of genetic skeletal disorders: 2010 revision. Am J Med Genet Part A 155A:943-968.
42. Wildeman M, van Ophuizen E, den Dunnen JT, Taschner PE. 2008. Improving sequence variant descriptions in mutation databases and literature using the Mutalyzer sequence variation nomenclature checker. Hum Mutat 29:6-13.