Cells expressing partially unfolded R789C/p.R989c type II procollagen mutant associated with spondyloepiphyseal dysplasia undergo apoptosis

Human Mutation

Volumn 29, Issue 6, 2008, Pages 841-851

  Hintze, Vera ^a   Steplewski, Andrzej ^a   Ito, Hidetoshi ^a   Jensen, Deborah A ^a   Rodeck, Ulrich ^a   Fertala, Andrzej ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Apoptosis; Cartilage; COL2A1; ER stress; Mutant collagen; Spondyloepiphyseal dysplasia (SED); Unfolded protein response (UPR)

Indexed keywords

CASPASE 3; CHAPERONE; COLLAGEN TYPE 2; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MUTANT PROTEIN; PROCOLLAGEN; TETRACYCLINE;

APOPTOSIS; ARTICLE; CARTILAGE CELL; CELL SURVIVAL; COL2A1 GENE; COMPLEX FORMATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ASSAY; ENZYME DEGRADATION; GENE; GENE EXPRESSION; GENETIC ASSOCIATION; GROWTH PLATE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; NICK END LABELING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SPONDYLOEPIPHYSEAL DYSPLASIA; THERMOSTABILITY; UNFOLDED PROTEIN RESPONSE;

AMINO ACID SUBSTITUTION; ANIMALS; APOPTOSIS; CHONDROCYTES; COLLAGEN TYPE II; COLLAGEN TYPE XI; GREEN FLUORESCENT PROTEINS; MICE; MUTATION, MISSENSE; OSTEOCHONDRODYSPLASIAS;

MUS;

EID: 44849121163     PISSN: 10597794     EISSN: None     Source Type: Journal    
DOI: 10.1002/humu.20736     Document Type: Article

References (40)

1. 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. Osteoarthritis Cartilage 10:808-815.
2. Arnold WV, Fertala A, Sieron AL, Hattori H, Mechling D, Bachinger HP, Prockop DJ. 1998. Recombinant procollagen II: deletion of D period segments identifies sequences that are required for helix stabilization and generates a temperature-sensitive N-proteinase cleavage site. J Biol Chem 273:31822-31828.
3. Ballock RT, O'Keefe RJ. 2003. The biology of the growth plate. J Bone Joint Surg Am 85A:715-726.
4. Barbieri O, Astigiano S, Morini M, Tavella S, Schito A, Corsi A, Di Martino D, Bianco P, Cancedda R, Garofalo S. 2003. Depletion of cartilage collagen fibrils in mice carrying a dominant negative Col2a1 transgene affects chondrocyte differentiation. Am J Physiol Cell Physiol 285:C1504-C1512.
5. Bleasel JF, Bisagni-Faure A, Holderhaum D, Vacher-Lavenu MC, Haqqi TM, Moskowitz RW, Menkes CJ. 1995. Type II procollagen gene (COL2A1) mutation in exon 11 associated with spondyloepiphyseal dysplasia, tall stature and precocious osteoarthritis. J Rheumatol 22:255-261.
6. Bleasel JF, Holderbaum D, Brancolini V, Moskowitz RW, Haqqi TM, Considine E, Prockop DJ, Devoto M, Williams CJ. 1996a. Arg519-Cys mutation in COL2A1: evidence for multiple founders. Ann NY Acad Sci 785:215-218.
7. Bleasel JF, Holderbaum D, Mallock V, Haqqi TM, Williams HJ, Moskowitz RW. 1996b. Hereditary osteoarthritis with mild spondyloepiphyseal dysplasia - are there "hot spots" on COL2A1? J Rheumatol 23:1594-1598.
8. Bogaert R, Tiller GE, Weis MA, Gruber HE, Rimoin DL, Cohn DH, Eyre DR. 1992. An amino acid substitution (Gly853- > Glu) in the collagen alpha 1(II) chain produces hypochondrogenesis. J Biol Chem 267:22522-22526.
9. Bottomley MJ, Batten MR, Lumb RA, Bulleid NJ. 2001. Quality control in the endoplasmic reticulum: PDI mediates the ER retention of unassembled procollagen C-propeptides. Curr Biol 11:1114-1118.
10. Chan D, Taylor TK, Cole WG. 1993. Characterization of an arginine 789 to cysteine substitution in alpha 1 (II) collagen chains of a patient with spondyloepiphyseal dysplasia. J Biol Chem 268:15238-15245.
11. Chessler SD, Byers PH. 1992. Defective folding and stable association with protein disulfide isomerase/prolyl hydroxylase of type I procollagen with a deletion in the pro alpha 2(I) chain that preserves the Gly-X-Y repeat pattern. J Biol Chem 267:7751-7757.
12. Chessler SD, Byers PH. 1993. BiP hinds 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.
13. Cruickshank J, Grossman DI, Peng RK, Famula TR, Oberbauer AM. 2005. Spatial distribution of growth hormone receptor, insulin-like growth factor-I receptor and apoptotic chondrocytes during growth plate development. J Endocrinol 184:543-553.
14. 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.
15. Fertala A, Ala-Kokko L, Wiaderkiewicz R, Prockop DJ. 1997. Collagen II containing a Cys substitution for arg-alpha1-519. Homotrimeric monomers containing the mutation do not assemble into fibrils but alter the self-assembly of the normal protein. J Biol Chem 272:6457-6464.
16. Fertala A, Sieron AL, Adachi E, Jimenez SA. 2001. Collagen II containing a Cys substitution for Arg-alpha1-519: abnormal interactions of the mutated molecules with collagen IX. Biochemistry 40:14422-14428.
17. Flynn GC, Pohl J, Flocco MT, Rothman JE. 1991. Peptide-binding specificity of the molecular chaperone BiP. Nature 353:726-730.
18. Fromme JC, Schekman R. 2005. COPII-coated vesicles: flexible enough for large cargo? Curr Opin Cell Biol 17:345-352.
19. Gaiser KG, Maddox BK, Bann JG, Boswell BA, Keene DR, Garofalo S, Horton WA. 2002. Y-position collagen II mutation disrupts cartilage fotmation and skeletal development in a transgenic mouse model of spondyloepiphyseal dysplasia. J Bone Miner Res 17:39-47.
20. Gebauer M, Saas J, Sohler F, Haag J, Soder S, Pieper M, Bartnik E, Beninga J, Zimmer R, Aigner T. 2005. Comparison of the chondrosarcoma cell line SW1353 with primary human adult articular chondrocytes with regard to theit gene expression profile and reactivity to IL-1beta. Osteoarthritis Cartilage 13:697-708.
21. Gossen M, Freundlieb S, Bender G, Muller G, Hillen W, Bujard H. 1995. Transcriptional activation by tetracyclines in mammalian cells. Science 268:1766-1769.
22. Hecht JT, Makitie O, Hayes E, Haynes R, Susic M, Montufar-Solis D, Duke PJ, Cole WG. 2004. Chondrocyte cell death and intracellular distribution of COMP and type IX collagen in the pseudoachondroplasia growth plate. J Orthop Res 22:759-767.
23. Ito H, Rucker E, Steplewski A, McAdams E, Brittingham RJ, Alahyeva T, Fertala A. 2005. Guilty by association: some collagen II mutants alter the formation of ECM as a result of atypical interaction with fibronectin. J Mol Biol 352:382-395.
24. Kaufman RJ. 1999. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 13:1211-1233.
25. Knowlton RG, Katzenstein PL, Moskowitz RW, Weaver EJ, Malemud CJ, Pathria MN, Jimenez SA, Prockop DJ. 1990. Genetic linkage of a polymorphism in the type II procollagen gene (COL2A1) to primary osteoarthritis associated with mild chondrodysplasia. N Engl J Med 322:526-530.
26. Kuivaniemi H, Tromp G, Prockop DJ. 1991. Mutations in collagen genes: causes of rare and some common diseases in humans. FASEB J 5:2052-2060.
27. McLaughlin SH, Bulleid NJ. 1998. Molecular recognition in procollagen chain assembly. Matrix Biol 16:369-377.
28. Olsen BR. 1995. Mutations in collagen genes resulting in metaphyseal and epiphyseal dysplasias. Bone 17(2 Suppl):45S-49S.
29. Pirog-Garcia KA, Meadows RS, Knowles L, Heinegard D, Thornton DJ, Kadler KE, Boot-Handford RP, Briggs MD. 2007. Reduced cell proliferation and increased apoptosis are significant pathological mechanisms in a murine model of mild pseudoachondroplasia resulting from a mutation in the C-terminal domain of COMP. Hum Mol Genet 16:2072-2088.
30. Prockop DJ, Kivirikko KI. 1995. Collagens: molecular biology, diseases, and potentials for therapy. Annu Rev Biochem 64:403-434.
31. Prockop DJ, Fertala A. 1998. Inhibition of the self-assembly of collagen I into fibrils with synthetic peptides. Demonstration that assembly is driven hy specific binding sites on the monomers. J Biol Chem 273:15598-15604.
32. Royce PM, Steinmann B. 2002. Connective tissue and its heritable disorders: molecular, genetic, and medical aspects. New York: John Wiley & Sons.
33. Rutishauser J, Spiess M. 2002. Endoplasmic reticulum storage diseases. Swiss Med Wkly 132:211-222.
34. Schroder M, Kaufman RJ. 2005. ER stress and the unfolded protein response. Mutat Res 569:29-63.
35. Steplewski A, Ito H, Rucker E, Brittingham RJ, Alahyeva T, Gandhi M, Ko FK, Birk DE, Jimenez SA, Fertala A. 2004a. Position of single amino acid substitutions in the collagen triple helix determines their effect on structure of collagen fibrils. J Struct Biol 148:326-337.
36. Steplewski A, Majsterek I, McAdams E, Rucker E, Brittingham RJ, Ito H, Hirai K, Adachi E, Jimenez SA, Fertala A. 2004b. Thermostability gradient in the collagen triple helix reveals its multi-domain structure. J Mol Biol 338:989-998.
37. Tasab M, Batten MR, Bulleid NJ. 2000. Hsp47: a molecular chaperone that interacts with and stabilizes correctly-folded procollagen. EMBO J 19:2204-2211.
38. Walmsley AR, Batten MR, Lad U, Bulleid NJ. 1999. Intracellular retention of procollagen within the endoplasmic reticulum is mediated by prolyl 4-hydroxylase. J Biol Chem 274:14884-14892.
39. Williams CJ, Considine EL, Knowlton RG, Reginato A, Neumann G, Harrison D, Buxton P, Jimenez S, Prockop DJ. 1993. Spondyloepiphyseal dysplasia and precocious osteoarthritis in a family with an Arg75-Cys mutation in the procollagen type II gene (COL2A1). Hum Genet 92:499-505.
40. Yang C, Li SW, Helminen HJ, Khillan JS, Bao Y, Prockop DJ. 1997. Apoptosis of chondrocytes in transgenic mice lacking collagen II. Exp Cell Res 235:370-373.