ENU-induced missense mutation in the C-propeptide coding region of Col2a1 creates a mouse model of platyspondylic lethal skeletal dysplasia, Torrance type

Mammalian Genome

Volumn 22, Issue 5-6, 2011, Pages 318-328

  Furuichi, Tatsuya ^a,b   Masuya, Hiroshi ^c   Murakami, Tomohiko ^d   Nishida, Keiichiro ^e   Nishimura, Gen ^f   Suzuki, Tomohiro ^c   Imaizumi, Kazunori ^g   Kudo, Takashi ^h   Ohkawa, Kiyoshi ^a   Wakana, Shigeharu ^c   Ikegawa, Shiro ^b  

^a JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b RIKEN   (Japan)

^c RIKEN BIORESOURCE CENTER   (Japan)

^d UNIVERSITY OF MIYAZAKI   (Japan)

^e OKAYAMA UNIVERSITY   (Japan)

^f TOKYO METROPOLITAN CHILDREN'S MEDICAL CENTER   (Japan)

^g HIROSHIMA UNIVERSITY   (Japan)

^h OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

C PEPTIDE; C PROPEPTIDE; COLLAGEN TYPE 2; ETHYLNITROSOUREA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DYSPLASIA; BRACHYDACTYLY; COL2A1 GENE; ENDOPLASMIC RETICULUM STRESS; ENZYME REGULATION; FEMALE; GENE; HETEROZYGOTE; HOMOZYGOTE; HYPOPLASIA; MALE; MISSENSE MUTATION; MOUSE; MUTAGENESIS; NONHUMAN; PELVIC DISEASE; PHENOTYPE; PLATYSPONDYLIC LETHAL SKELETAL DYSPLASIA; PROTEIN EXPRESSION; PROTEIN SECRETION; SPONDYLOSIS;

ALCIAN BLUE; ANIMALS; ANTHRAQUINONES; BONE AND BONES; CHROMOSOME MAPPING; COLLAGEN TYPE II; DISEASE MODELS, ANIMAL; DNA PRIMERS; ETHYLNITROSOUREA; GENOTYPE; IMMUNOHISTOCHEMISTRY; MICE; MICE, MUTANT STRAINS; MICROSCOPY, ELECTRON, TRANSMISSION; MUTAGENESIS; MUTATION, MISSENSE; OSTEOCHONDRODYSPLASIAS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

ANIMALIA; MUS;

EID: 80051549271     PISSN: 09388990     EISSN: 14321777     Source Type: Journal    
DOI: 10.1007/s00335-011-9329-3     Document Type: Article

References (45)

1. Ahmad NN, Ala-Kokko L, Knowlton RG, Jimenez SA, Weaver EJ, Maguire JI, Tasman W, Prockop DJ (1991) Stop codon in the procollagen II gene (COL2A1) in a family with the Stickler syndrome (arthro-ophthalmopathy). Proc Natl Acad Sci USA 88:6624-6627 (Pubitemid 21915001)
2. Arita M, Li SW, Kopen G, Adachi E, Jimenez SA, Fertala A (2002) Skeletal abnormalities and ultrastructural changes of cartilage in transgenic mice expressing a collagen II gene (COL2A1) with a Cys for Arg-alpha1-519 substitution. Osteoarthr Cartil 10:808-815 (Pubitemid 35153722)
3. Bateman JF, Boot-Handford RP, Lamande SR (2009) Genetic diseases of connective tissues: cellular and extracellular effects of ECM mutations. Nat Rev Genet 10:173-183
4. Bomsta BD, Bridgewater LC, Seegmiller RE (2006) Premature osteoarthritis in the Disproportionate micromelia (Dmm) mouse. Osteoarthr Cartil 14:477-485
5. Brown KS, Cranley RE, Greene R, Kleinman HK, Pennypacker JP (1981) Disproportionate micromelia (Dmm): an incomplete dominant mouse dwarfism with abnormal cartilage matrix. J Embryol Exp Morphol 62:165-182 (Pubitemid 11155712)
6. Chessler SD, Byers PH (1993) BiP binds type I procollagen pro alpha chains with mutations in the carboxyl-terminal propeptide synthesized by cells from patients with osteogenesis imperfecta. J Biol Chem 268:18226-18233 (Pubitemid 23260347)
7. Doege KJ, Fessler JH (1986) Folding of carboxyl domain and assembly of procollagen I. J Biol Chem 261:8924-8935 (Pubitemid 17205097)
8. Donahue LR, Chang B, Mohan S, Miyakoshi N, Wergedal JE, Baylink DJ, Hawes NL, Rosen CJ, Ward-Bailey P, Zheng QY, Bronson RT, Johnson KR, Davisson MT (2003) A missense mutation in the mouse Col2a1 gene causes spondyloepiphyseal dysplasia congenita, hearing loss, and retinoschisis. J Bone Miner Res 18:1612-1621 (Pubitemid 37022919)
9. Fernandes RJ, Seegmiller RE, Nelson WR, Eyre DR (2003) Protein consequences of the Col2a1 C-propeptide mutation in the chondrodysplastic Dmm mouse. Matrix Biol 22:449-453 (Pubitemid 37393323)
10. Freisinger P, Bonaventure J, Stoess H, Pontz BF, Emmrich P, Nerlich A (1996) Type II collagenopathies: are there additional family members? Am J Med Genet 63:137-143
11. Hintze V, Steplewski A, Ito H, Jensen DA, Rodeck U, Fertala A (2008) Cells expressing partially unfolded R789C/p.R989C type II procollagen mutant associated with spondyloepiphyseal dysplasia undergo apoptosis. Hum Mutat 29:841-851 (Pubitemid 351794135)
12. Hitotsumachi S, Carpenter DA, Russell WL (1985) Dose-repetition increases the mutagenic effectiveness of N-ethyl-N-nitrosourea in mouse spermatogonia. Proc Natl Acad Sci USA 82:6619-6621 (Pubitemid 16228871)
13. Ikeda T, Mabuchi A, Fukuda A, Kawakami A, Ryo Y, Yamamoto S, Miyoshi K, Haga N, Hiraoka H, Takatori Y, Kawaguchi H, Nakamura K, Ikegawa S (2002) Association analysis of single nucleotide polymorphisms in cartilage-specific collagen genes with knee and hip osteoarthritis in the Japanese population. J Bone Miner Res 17:1290-1296 (Pubitemid 34680506)
14. Inoue M, Sakuraba Y, Motegi H, Kubota N, Toki H, Matsui J, Toyoda Y, Miwa I, Terauchi Y, Kadowaki T, Shigeyama Y, Kasuga M, Adachi T, Fujimoto N, Matsumoto R, Tsuchihashi K, Kagami T, Inoue A, Kaneda H, Ishijima J, Masuya H, Suzuki T, Wakana S, Gondo Y, Minowa O, Shiroishi T, Noda T (2004) A series of maturity onset diabetes of the young, type 2 (MODY2) mouse models generated by a large-scale ENU mutagenesis program. Hum Mol Genet 13:1147-1157 (Pubitemid 38786997)
15. Khoshnoodi J, Cartailler JP, Alvares K, Veis A, Hudson BG (2006) Molecular recognition in the assembly of collagens: terminal noncollagenous domains are key recognition modules in the formation of triple helical protomers. J Biol Chem 281: 38117-38121 (Pubitemid 46041935)
16. Korkko J, Cohn DH, Ala-Kokko L, Krakow D, Prockop DJ (2000) Widely distributed mutations in the COL2A1 gene produce achondrogenesis type II/hypochondrogenesis. Am J Med Genet 92:95-100 (Pubitemid 30256434)
17. Kuivaniemi H, Tromp G, Prockop DJ (1997) Mutations in fibrillar collagens (types I, II, III, and XI), fibril-associated collagen (type IX), and network-forming collagen (type X) cause a spectrum of diseases of bone, cartilage, and blood vessels. Hum Mutat 9:300-315 (Pubitemid 27157648)
18. Li SW, Prockop DJ, Helminen H, Fassler R, Lapvetelainen T, Kiraly K, Peltarri A, Arokoski J, Lui H, Arita M et al (1995) Transgenic mice with targeted inactivation of the Col2a1 gene for collagen II develop a skeleton with membranous and periosteal bone but no endochondral bone. Genes Dev 9:2821-2830
19. Loughlin J (2001) Genetic epidemiology of primary osteoarthritis. Curr Opin Rheumatol 13:111-116
20. Maddox BK, Garofalo S, Smith C, Keene DR, Horton WA (1997) Skeletal development in transgenic mice expressing a mutation at Gly574Ser of type II collagen. Dev Dyn 208:170-177 (Pubitemid 27068872)
21. Mankin HJ, Dorfman H, Lippiello L, Zarins A (1971) Biochemical and metabolic abnormalities in articular cartilage from osteoarthritic human hips. II. Correlation of morphology with biochemical and metabolic data. J Bone Joint Surg Am 53: 523-537
22. Masuya H, Inoue M, Wada Y, Shimizu A, Nagano J, Kawai A, Inoue A, Kagami T, Hirayama T, Yamaga A, Kaneda H, Kobayashi K, Minowa O, Miura I, Gondo Y, Noda T, Wakana S, Shiroishi T (2005a) Implementation of the modified-SHIRPA protocol for screening of dominant phenotypes in a large-scale ENU mutagenesis program. Mamm Genome 16:829-837 (Pubitemid 41598705)
23. Masuya H, Shimizu K, Sezutsu H, Sakuraba Y, Nagano J, Shimizu A, Fujimoto N, Kawai A, Miura I, Kaneda H, Kobayashi K, Ishijima J, Maeda T, Gondo Y, Noda T, Wakana S, Shiroishi T (2005b) Enamelin (Enam) is essential for amelogenesis: ENUinduced mouse mutants as models for different clinical subtypes of human amelogenesis imperfecta (AI). Hum Mol Genet 14: 575-583 (Pubitemid 40309583)
24. Masuya H, Nishida K, Furuichi T, Toki H, Nishimura G, Kawabata H, Yokoyama H, Yoshida A, Tominaga S, Nagano J, Shimizu A, Wakana S, Gondo Y, Noda T, Shiroishi T, Ikegawa S (2007) A novel dominant-negative mutation in Gdf5 generated by ENU mutagenesis impairs joint formation and causes osteoarthritis in mice. Hum Mol Genet 16:2366-2375 (Pubitemid 47430455)
25. Metsaranta M, Garofalo S, Decker G, Rintala M, de Crombrugghe B, Vuorio E (1992) Chondrodysplasia in transgenic mice harboring a 15-amino-acid deletion in the triple helical domain of pro alpha 1(II) collagen chain. J Cell Biol 118:203-212
26. Mortier GR, Weis M, Nuytinck L, King LM, Wilkin DJ, De Paepe A, Lachman RS, Rimoin DL, Eyre DR, Cohn DH (2000) Report of five novel and one recurrent COL2A1 mutation with analysis of genotype-phenotype correlation in patients with a lethal type II collagen disorder. J Med Genet 37:263-271 (Pubitemid 30245931)
27. Myllyharju J, Kivirikko KI (2004) Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20:33-43 (Pubitemid 38032818)
28. Nishimura G, Nakashima E, Mabuchi A, Shimamoto K, Shimamoto T, Shimao Y, Nagai T, Yamaguchi T, Kosaki R, Ohashi H, Makita Y, Ikegawa S (2004) Identification of COL2A1 mutations in platyspondylic skeletal dysplasia, Torrance type. J Med Genet 41:75-79 (Pubitemid 38125694)
29. Nishimura G, Haga N, Kitoh H, Tanaka Y, Sonoda T, Kitamura M, Shirahama S, Itoh T, Nakashima E, Ohashi H, Ikegawa S (2005) The phenotypic spectrum of COL2A1 mutations. Hum Mutat 26:36-43 (Pubitemid 40980701)
30. Nolan PM, Kapfhamer D, Bucan M (1997) Random mutagenesis screen for dominant behavioral mutations in mice. Methods 13:379-395
31. Olsen BR (1995) New insights into the function of collagens from genetic analysis. Curr Opin Cell Biol 7:720-727
32. Pace JM, Li Y, Seegmiller RE, Teuscher C, Taylor BA, Olsen BR (1997) Disproportionate micromelia (Dmm) in mice caused by a mutation in the C-propeptide coding region of Col2a1. Dev Dyn 208:25-33 (Pubitemid 27030481)
33. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519-529 (Pubitemid 46985379)
34. Saito A, Hino S, Murakami T, Kanemoto S, Kondo S, Saitoh M, Nishimura R, Yoneda T, Furuichi T, Ikegawa S, Ikawa M, Okabe M, Imaizumi K (2009) Regulation of endoplasmic reticulum stress response by a BBF2H7-mediated Sec23a pathway is essential for chondrogenesis. Nat Cell Biol 11: 1197-1204
35. Schroder M, Kaufman RJ (2005) ER stress and the unfolded protein response. Mutat Res 569:29-63 (Pubitemid 39643256)
36. Seegmiller RE, Bomsta BD, Bridgewater LC, Niederhauser CM, CMontaño C, Sudweeks S, Eyre DR, Fernandes RJ (2008) The heterozygous disproportionate micromelia (Dmm) mouse: morphological changes in fetal cartilage precede postnatal dwarfism and compared with lethal homozygotes can explain the mild phenotype. J Histochem Cytochem 56:1003-1011
37. Tsang KY, Chan D, Cheslett D, Chan WC, So CL, Melhado IG, Chan TW, Kwan KM, Hunziker EB, Yamada Y, Bateman JF, Cheung KM, Cheah KS (2007) Surviving endoplasmic reticulum stress is coupled to altered chondrocyte differentiation and function. PLoS Biol 5:e44
38. Unger S, Korkko J, Krakow D, Lachman RS, Rimoin DL, Cohn DH (2001) Double heterozygosity for pseudoachondroplasia and spondyloepiphyseal dysplasia congenita. Am J Med Genet 104: 140-146 (Pubitemid 33062940)
39. Van der Rest M, Rosenberg LC, Olsen BR, Poole AR (1986) Chondrocalcin is identical with the C-propeptide of type II procollagen. Biochem J 237:923-925 (Pubitemid 16003796)
40. van der Sluijs JA, Geesink RG, van der Linden AJ, Bulstra SK, Kuyer R, Drukker J (1992) The reliability of the Mankin score for osteoarthritis. J Orthop Res 10:58-61
41. Vikkula M, Palotie A, Ritvaniemi P, Ott J, Ala-Kokko L, Sievers U, Aho K, Peltonen L (1993) Early-onset osteoarthritis linked to the type II procollagen gene. Detailed clinical phenotype and further analyses of the gene. Arthritis Rheum 36:401-409 (Pubitemid 23090609)
42. Wilson R, Freddi S, Chan D, Cheah KS, Bateman JF (2005) Misfolding of collagen X chains harboring Schmid metaphyseal chondrodysplasia mutations results in aberrant disulfide bond formation, intracellular retention, and activation of the unfolded protein response. J Biol Chem 280:15544-15552 (Pubitemid 40616670)
43. Winterpacht A, Hilbert M, Schwarze U, Mundlos S, Spranger J, Zabel BU (1993) Kniest and Stickler dysplasia phenotypes caused by collagen type II gene (COL2A1) defect. Nat Genet 3:323-326 (Pubitemid 23112957)
44. Zabel B, Hilbert K, Stoss H, Superti-Furga A, Spranger J, Winterpacht A (1996) A specific collagen type II gene (COL2A1) mutation presenting as spondyloperipheral dysplasia. Am J Med Genet 63:123-128
45. Zankl A, Neumann L, Ignatius J, Nikkels P, Schrander-Stumpel C, Mortier G, Omran H, Wright M, Hilbert K, Bonafe L, Spranger J, Zabel B, Superti-Furga A (2005) Dominant negative mutations in the C-propeptide of COL2A1 cause platyspondylic lethal skeletal dysplasia, torrance type, and define a novel subfamily within the type 2 collagenopathies. Am J Med Genet A 133A:61-66