First mouse model for combined osteogenesis imperfecta and ehlers-danlos syndrome

Journal of Bone and Mineral Research

Volumn 29, Issue 6, 2014, Pages 1412-1423

  Chen, Frieda ^a   Guo, Ruolin ^a   Itoh, Shousaku ^a   Moreno, Luisa ^b   Rosenthal, Esther ^a   Zappitelli, Tanya ^a   Zirngibl, Ralph A ^a   Flenniken, Ann ^c   Cole, William ^d   Grynpas, Marc ^a,b   Osborne, Lucy R ^a,c   Vogel, Wolfgang ^a   Adamson, Lee ^a,c,e   Rossant, Janet ^a,c,d   Aubin, Jane E ^a,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c Toronto Centre for Phenogenomics   (Canada)

^d HOSPITAL FOR SICK CHILDREN   (Canada)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

BONE MINERAL DENSITY; COLLAGEN; MINERALIZATION; OSTEOBLAST; OSTEOCLAST

Indexed keywords

AMINO ACID; AMINO TERMINAL TELOPEPTIDE; COLLAGEN; COLLAGEN ALPHA1; COLLAGEN TYPE 1; ETHYLNITROSOUREA; UNCLASSIFIED DRUG; COLLAGEN TYPE I, ALPHA 1 CHAIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DENSITY; BONE MARROW; BONE MASS; BONE MINERALIZATION; CELL DIFFERENTIATION; COLLAGEN SYNTHESIS; CONTROLLED STUDY; DISEASE ASSOCIATION; EHLERS DANLOS SYNDROME; EXON; EXTRACELLULAR MATRIX; FEMALE; FIBROBLAST CULTURE; FRACTURE; GENE DELETION; GENE MAPPING; GENETIC ASSOCIATION; IN VITRO STUDY; IN VIVO STUDY; MALE; MORPHOMETRICS; MOUSE; MUTANT; NONHUMAN; OSTEOBLAST; OSTEOGENESIS IMPERFECTA; PATHOPHYSIOLOGY; SKIN; SKIN FIBROBLAST; SPINE; STROMA CELL; TAIL; TENDON; TENSILE STRENGTH; TRABECULAR BONE; YOUNG ADULT; ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL; BONE; BONE MATRIX; BONE REMODELING; CHEMISTRY; COMPLICATION; DISEASE MODEL; FEMUR; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PATHOLOGY; PHOTON ABSORPTIOMETRY; PROTEIN TERTIARY STRUCTURE; RADIOGRAPHY; ULTRASTRUCTURE;

ABSORPTIOMETRY, PHOTON; ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BONE AND BONES; BONE MATRIX; BONE REMODELING; CALCIFICATION, PHYSIOLOGIC; COLLAGEN TYPE I; DISEASE MODELS, ANIMAL; EHLERS-DANLOS SYNDROME; FEMUR; MALE; MICE; MOLECULAR SEQUENCE DATA; MUTATION; OSTEOGENESIS IMPERFECTA; PROTEIN STRUCTURE, TERTIARY; STROMAL CELLS;

EID: 84901255508     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2177     Document Type: Article

References (67)

1. Sillence DO, Senn A, Danks DM., Genetic heterogeneity in osteogenesis imperfecta. J Med Genet. 1979; 16 (2): 101-16.
2. Morello R, Bertin TK, Chen Y, et al. CRTAP is required for prolyl 3- hydroxylation and mutations cause recessive osteogenesis imperfecta. Cell. 2006; 127 (2): 291-304.
3. Cabral WA, Chang W, Barnes AM., et al. Prolyl 3-hydroxylase 1 deficiency causes a recessive metabolic bone disorder resembling lethal/severe osteogenesis imperfecta. Nat Genet. 2007; 39 (3): 359-65.
4. van Dijk FS, Nesbitt IM, Zwikstra EH, et al. PPIB mutations cause severe osteogenesis imperfecta. Am J Hum Genet. 2009; 85 (4): 521-7.
5. Alanay Y, Avaygan H, Camacho N, et al. Mutations in the gene encoding the RER protein FKBP65 cause autosomal-recessive osteogenesis imperfecta. Am J Hum Genet. 2010; 86 (4): 551-9.
6. Kelley BP, Malfait F, Bonafe L, et al. Mutations in FKBP10 cause recessive osteogenesis imperfecta and bruck syndrome. J Bone Miner Res. 2011; 26 (3): 666-72.
7. Christiansen HE, Schwarze U, Pyott SM, et al. Homozygosity for a missense mutation in SERPINH1, which encodes the collagen chaperone protein HSP47, results in severe recessive osteogenesis imperfecta. Am J Hum Genet. 2010; 86 (3): 389-98.
8. Pyeritz RE., Ehlers-Danlos Syndrome. N Engl J Med. 2000; 342 (10): 730-2.
9. Plancke A, Holder-Espinasse M, Rigau V, Manouvrier S, Claustres M, Van Kien PK., Homozygosity for a null allele of COL3A1 results in recessive Ehlers-Danlos syndrome. Eur J Hum Genet. 2009; 17 (11): 1411-6.
10. Dalgleish R., The Human Collagen Mutation Database 1998. Nucleic Acids Res. 1998; 26 (1): 253-5.
11. Wenstrup RJ, Witte DP, Florer JB., Abnormal differentiation in MC3T3-E1 preosteoblasts expressing a dominant-negative type I collagen mutation. Connect Tissue Res. 1996; 35 (1-4): 249-57.
12. Wenstrup RJ, Langland GT, Willing MC, D'Souza VN, Cole WG., A splice-junction mutation in the region of COL5A1 that codes for the carboxyl propeptide of pro alpha 1(V) chains results in the gravis form of the Ehlers-Danlos syndrome (type I). Hum Mol Genet. 1996; 5 (11): 1733-6.
13. Toriello HV, Glover TW, Takahara K, et al. A translocation interrupts the COL5A1 gene in a patient with Ehlers-Danlos syndrome and hypomelanosis of Ito. Nat Genet. 1996; 13 (3): 361-5.
14. Nicholls AC, Oliver JE, McCarron S, Harrison JB, Greenspan DS, Pope FM., An exon skipping mutation of a type V collagen gene (COL5A1) in Ehlers-Danlos syndrome. J Med Genet. 1996; 33 (11): 940-6.
15. De Paepe A, Nuytinck L, Hausser I, Anton-Lamprecht I, Naeyaert JM., Mutations in the COL5A1 gene are causal in the Ehlers-Danlos syndromes I and II. Am J Hum Genet. 1997; 60 (3): 547-54.
16. Burrows NP, Nicholls AC, Yates JR, Richards AJ, Pope FM., Genetic linkage to the collagen alpha 1 (V) gene (COL5A1) in two British Ehlers-Danlos syndrome families with variable type I and II phenotypes. Clin Exp Dermatol. 1997; 22 (4): 174-6.
17. Bouma P, Cabral WA, Cole WG, Marini JC., COL5A1 exon 14 splice acceptor mutation causes a functional null allele, haploinsufficiency of α1(V) and abnormal heterotypic interstitial fibrils in Ehlers-Danlos syndrome II. J Biol Chem. 2001; 276 (16): 13356-64.
18. Schwarze U, Atkinson M, Hoffman GG, Greenspan DS, Byers PH., Null alleles of the COL5A1 gene of type V collagen are a cause of the classical forms of Ehlers-Danlos syndrome (types I and II). Am J Hum Genet. 2000; 66 (6): 1757-65.
19. Malfait F, Coucke P, Symoens S, Loeys B, Nuytinck L, De Paepe A., The molecular basis of classic Ehlers-Danlos syndrome: a comprehensive study of biochemical and molecular findings in 48 unrelated patients. Hum Mut. 2005; 25 (1): 28-37.
20. Richards AJ, Martin S, Nicholls AC, Harrison JB, Pope FM, Burrows NP., A single base mutation in COL5A2 causes Ehlers-Danlos syndrome type II. J Med Genet. 1998; 35 (10): 846-8.
21. Michalickova K, Susic M, Willing MC, Wenstrup RJ, Cole WG., Mutations of the α2(V) chain of type V collagen impair matrix assembly and produce Ehlers-Danlos syndrome type I. Hum Mol Genet. 1998; 7 (2): 249-55.
22. Beighton P, De Paepe A, Steinmann B, Tsipouras P, Wenstrup RJ., Ehlers-Danlos syndromes: revised nosology, Villefranche, 1997. Am J Hum Genet. 1998; 77 (1): 31-7.
23. Yeowell HN, Walker LC., Mutations in the lysyl hydroxylase 1 gene that result in enzyme deficiency and the clinical phenotype of Ehlers-Danlos syndrome type VI. Mol Genet Metab. 2000; 71 (1-2): 212-24.
24. Heikkinen J, Hautala T, Kivirikko KI, Myllyla R., Structure and expression of the human lysyl hydroxylase gene (PLOD): introns 9 and 16 contain Alu sequences at the sites of recombination in Ehlers-Danlos syndrome type VI patients. Genomics. 1994; 24 (3): 464-71.
25. Schalkwijk J, Zweers MC, Steijlen PM, et al. A recessive form of the Ehlers-Danlos syndrome caused by tenascin-X deficiency. N Engl J Med. 2001; 345 (16): 1167-75.
26. Mao JR, Taylor G, Dean WB, et al. Tenascin-X deficiency mimics Ehlers-Danlos syndrome in mice through alteration of collagen deposition. Nat Genet. 2002; 30 (4): 421-5.
27. Colige A, Sieron AL, Li SW, et al. Human Ehlers-Danlos syndrome type VIIC and bovine dermatosparaxis are caused by mutations in the procollagen IN-proteinase gene. Am J Hum Genet. 1999; 5 (2): 308-17.
28. Li SW, Arita M, Fertala A, et al. Transgenic mice with inactive alleles for procollagen N-proteinase (ADAMTS-2) develop fragile skin and male sterility. Biochem J. 2001; 355: 271-8.
29. Cabral WA, Makareeva E, Colige A, et al. Mutations near amino end of alpha1(I) collagen cause combined osteogenesis imperfecta/Ehlers-Danlos syndrome by interference with N-propeptide processing. J Biol Chem. 2005; 280 (19): 19259-69.
30. Dalgleish R., The human type I collagen mutation database. Nucleic Acids Res. 1997; 25 (1): 181-7.
31. Marini JC, Forlino A, Cabral WA, et al. Consortium for osteogenesis imperfecta mutations in the helical domain of type I collagen: regions rich in lethal mutations align with collagen binding sites for integrins and proteoglycans. Hum Mutat. 2007; 28 (3): 209-21.
32. Forlino A, Cabral WA, Barnes AM, Marini JC., New perspectives on osteogenesis imperfecta. Nat Rev Endocrinol. 2011; 7 (9): 540-57.
33. Chen F, Aubin JE., Mouse models of osteogenesis imperfecta. In:, Rauch F, Smith P, Harris G, editors. Transitional care in osteogenesis imperfecta: advances in biology, technology and clinical practice. Marquette University/OREC, 2010. [In press.].
34. Andrikopoulos K, Liu X, Keene DR, Jaenisch R, Ramirez F., Targeted mutation in the col5a2 gene reveals a regulatory role for type V collagen during matrix assembly. Nat Genet. 1995; 9 (1): 31-6.
35. Liu X, Wu H, Byrne M, Krane S, Jaenisch R., Type III collagen is crucial for collagen I fibrillogenesis and for normal cardiovascular development. Proc Natl Acad Sci USA. 1997; 94 (5): 1852-6.
36. Wenstrup RJ, Florer JB, Davidson JM, et al. Murine model of the Ehlers-Danlos syndrome. col5a1 haploinsufficiency disrupts collagen fibril assembly at multiple stages. J Biol Chem. 2006; 281 (18): 12888-95.
37. Smith LB, Hadoke PW, Dyer E, et al. Haploinsufficiency of the murine Col3a1 locus causes aortic dissection: a novel model of the vascular type of Ehlers-Danlos syndrome. Cardiovasc Res. 2011; 90 (1): 182-90.
38. Mao J-R, Bristow J., The Ehlers-Danlos syndrome: on beyond collagens. J Clin Invest. 2001; 107 (9): 1063-9.
39. Justice MJ, Carpenter DA, Favor J, et al. Effects of ENU dosage on mouse strains. Mamm Genome. 2000; 11 (7): 484-8.
40. Flenniken AM, Osborne LR, Anderson N, et al. A Gja1 missense mutation in a mouse model of oculodentodigital dysplasia. Development. 2005; 132 (19): 4375-86.
41. Valverde-Franco G, Liu H, Davidson D, et al. Defective bone mineralization and osteopenia in young adult FGFR3-/- mice. Hum Mol Genet. 2004; 13 (3): 271-84.
42. Dobson KR, Reading L, Haberey M, Marine X, Scutt A., Centrifugal isolation of bone marrow from bone: an improved method for the recovery and quantitation of bone marrow osteoprogenitor cells from rat tibiae and femurae. Calcif Tissue Int. 1999; 65 (5): 411-3.
43. Bellows CG, Aubin JE., Determination of numbers of osteoprogenitors present in isolated fetal-rat calvaria cells in vitro. Dev Biol. 1989; 133 (1): 8-13.
44. Bellows CG, Aubin JE, Heersche JNM, Antosz ME., Mineralized bone nodules formed in vitro from enzymatically released rat calvaria cell populations. Calcif Tissue Int. 1986; 38 (3): 143-54.
45. Zhao S, Fernald RD., Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol. 2005; 12 (8): 1047-64.
46. Bateman JF, Mascara T, Chan D, Cole WG., Abnormal type I collagen metabolism by cultured fibroblasts in lethal perinatal osteogenesis imperfecta. Biochem J. 1984; 217 (1): 103-15.
47. Bateman JF, Chan D, Mascara T, Rogers JG, Cole WG., Collagen defects in lethal perinatal osteogenesis imperfecta. Biochem J. 1986; 240 (3): 699-708.
48. Franceschi RT, Iyer BS., Relationship between collagen synthesis and expression of the osteoblast phenotype in MC3T3-E1 cells. J Bone Miner Res. 1992; 7 (2): 235-46.
49. Xiao G, Wang D, Benson MD, Karsenty G, Franceschi RT., Role of the alpha2-integrin in osteoblast-specific gene expression and activation of the Osf2 transcription factor. J Biol Chem. 1998; 273 (49): 32988-94.
50. Forlino A, Porter FD, Lee EJ, Westphal H, Marini JC., Use of the Cre/lox recombination system to develop a non-lethal knock-in murine model for osteogenesis imperfecta with an alpha1(I) G349C substitution. Variability in phenotype in BrtlIV mice. J Biol Chem. 1999; 274 (53): 37923-31.
51. Daley E, Streeten EA, Sorkin JD, et al. Variable bone fragility associated with an Amish COL1A2 variant and a knock-in mouse model. J Bone Miner Res. 2010; 25 (2): 247-61.
52. Uveges TE, Collin-Osdoby P, Cabral WA, et al. Cellular mechanism of decreased bone in Brtl mouse model of OI: imbalance of decreased osteoblast function and increased osteoclasts and their precursors. J Bone Miner Res. 2008; 23 (12): 1983-94.
53. Zhang H, Doty SB, Hughes C, Dempster D, Camacho NP., Increased resorptive activity and accompanying morphological alterations in osteoclasts derived from the Oim/Oim mouse model of osteogenesis imperfecta. J Cell Biochem. 2007; 102 (4): 1011-20.
54. Paterson CR, McAllion S, Stellman JL., Osteogenesis imperfecta after the menopause. N Engl J Med. 1984; 310 (26): 1694-6.
55. Kozloff KM, Carden A, Bergwitz C, et al. Brittle IV mouse model for osteogenesis imperfecta IV demonstrates postpubertal adaptations to improve whole bone strength. J Bone Miner Res. 2004; 19 (4): 614-22.
56. Bonadio J, Jepsen KJ, Mansoura MK, Jaenisch R, Kuhn JL, Goldstein SA., A murine skeletal adaptation that significantly increases cortical bone mechanical properties-implications for human skeletal fragility. J Clin Invest. 1993; 92 (4): 1697-705.
57. Pereira RF, Hume EL, Halford KW, Prockop DJ., Bone fragility in transgenic mice expressing a mutated gene for type I procollagen (COL1A1) parallels the age-dependent phenotype of human osteogenesis imperfecta. J Bone Miner Res. 1995; 10 (12): 1837-43.
58. McBride DJ Jr, Shapiro JR, Dunn MG., Bone geometry and strength measurements in aging mice with the oim mutation. Calcif Tissue Int. 1998; 62 (2): 172-6.
59. Fedde KN, Blair L, Silverstein J, et al. Alkaline phosphatase knock-out mice recapitulate the metabolic and skeletal defects of infantile hypophosphatasia. J Bone Miner Res. 1999; 14 (12): 2015-26.
60. Sodek J, Ganss B, McKee MD., Osteopontin. Crit Rev Oral Biol Med. 2000; 11 (3): 279-303.
61. Sanders JE, Goldstein BS, Leotta DF., Skin response to mechanical stress: adaptation rather than breakdown-a review of the literature. J Rehab Res Dev. 1995; 32 (3): 214-26.
62. Makareeva E, Cabral WA, Marini JC, Leikin S., Molecular mechanism of alpha 1(I)-osteogenesis imperfecta/Ehlers-Danlos syndrome: unfolding of an N-anchor domain at the N-terminal end of the type I collagen triple helix. J Biol Chem. 2006; 281 (10): 6463-70.
63. Prockop DJ., Osteogenesis imperfecta: phenotypic heterogeneity, protein suicide, short and long collagen. Am J Hum Genet. 1984; 36 (3): 499-505.
64. Khillan JS, Olsen AS, Kontusaari S, Sokolov B, Prockop DJ., Transgenic mice that express a mini-gene version of the human gene for type I procollagen (COL1A1) develop a phenotype resembling a lethal form of osteogenesis imperfecta. J Biol Chem. 1991; 266 (34): 23373-9.
65. Lin JH, Walter P, Yen TSB., Endoplasmic reticulum stress in disease pathogenesis. Ann Rev Pathol Mech Dis. 2008; 3: 399-425.
66. Lisse TS, Thiele F, Fuchs H, et al. ER stress-mediated apoptosis in a new mouse model of osteogenesis imperfecta. PLoS Genet. 2008; 4 (2): e7.
67. Wang X, Seed B., A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res. 2003; 31 (24): e154.