Persistence of intracellular and extracellular changes after incompletely suppressing expression of the R789C (p.R989C) and R992C (p.R1192C) collagen II mutants

Human Mutation

Volumn 32, Issue 7, 2011, Pages 794-805

  Jensen, Deborah A ^a   Steplewski, Andrzej ^a   Gawron, Katarzyna ^a,b   Fertala, Andrzej ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

Cartilage; Collagen II; Collagen mutations; Endoplasmic reticulum stress; Spondyloepiphyseal dysplasia

Indexed keywords

COLLAGEN TYPE 2; DOXYCYCLINE FOSFATEX; GREEN FLUORESCENT PROTEIN; PROTEIN DISULFIDE ISOMERASE; TETRACYCLINE;

APOPTOSIS; ARTICLE; CELL MIGRATION; CELL MOTILITY; CELL MUTANT; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENE MUTATION; HUMAN; HUMAN CELL; NICK END LABELING; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ALLELES; CELL LINE, TUMOR; CELL MIGRATION ASSAYS; COLLAGEN TYPE II; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC VARIATION; HUMANS; MUTATION; PHOTOBLEACHING; TETRACYCLINE;

EID: 79959700903     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.21506     Document Type: Article

References (50)

1. Adachi E, Katsumata O, Yamashina S, Prockop DJ, Fertala A. 1999. Collagen II containing a Cys substitution for Arg-alpha1-519. Analysis by atomic force microscopy demonstrates that mutated monomers alter the topography of the surface of collagen II fibrils. Matrix Biol 18:189-196.
2. Bienkowski RS, Curran SF, Berg RA. 1986. Kinetics of intracellular degradation of newly synthesized collagen. Biochemistry 25:2455-2459.
3. Bleasel JF, Bisagni-Faure A, Holderbaum 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.
4. Bleasel JF, Holderbaum D, Brancolini V, Moskowitz RW, Considine EL, Prockop DJ, Devoto M, Williams CJ. 1998. Five families with arginine 519-cysteine mutation in COL2A1: evidence for three distinct founders. Hum Mutat 12:172-176.
5. 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 N Y Acad Sci 785:215-218.
6. 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.
7. Burton-Wurster N, Lust G, Macleod JN. 1997. Cartilage fibronectin isoforms: in search of functions for a special population of matrix glycoproteins. Matrix Biol 15:441-454.
8. Cabral WA, Fertala A, Green LK, Korkko J, Forlino A, Marini JC. 2002. Procollagen with skipping of alpha 1(I) exon 41 has lower binding affinity for alpha 1(I) C-telopeptide, impaired in vitro fibrillogenesis, and altered fibril morphology. J Biol Chem 277:4215-4222.
9. 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.
10. Chon JH, Wang HS, Chaikof EL. 1997. Role of fibronectin and sulfated proteoglycans in endothelial cell migration on a cultured smooth muscle layer. J Surg Res 72:53-59.
11. Chung HJ, Jensen DA, Gawron K, Steplewski A, Fertala A. 2009. R992C (p.R1192C) Substitution in collagen II alters the structure of mutant molecules and induces the unfolded protein response. J Mol Biol 390:306-318.
12. Dawson PA, Marini JC. 2000. Hammerhead ribozymes selectively suppress mutant type I collagen mRNA in osteogenesis imperfecta fibroblasts. Nucleic Acids Res 28:4013-4020.
13. 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.
14. Durr J, Goodman S, Potocnik A, von der Mark H, von der Mark K. 1993. Localization of beta 1-integrins in human cartilage and their role in chondrocyte adhesion to collagen and fibronectin. Exp Cell Res 207:235-244.
15. Dzamba BJ, Wu H, Jaenisch R, Peters DM. 1993. Fibronectin binding site in type I collagen regulates fibronectin fibril formation. J Cell Biol 121:1165-1172.
16. Eyre DR, Weis MA, Moskowitz RW. 1991. Cartilage expression of a type II collagen mutation in an inherited form of osteoarthritis associated with a mild chondrodysplasia. J Clin Invest 87:357-361.
17. 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.
18. 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.
19. Forlino A, Marini JC. 2000. Osteogenesis imperfecta: prospects for molecular therapeutics. Mol Genet Metab 71:225-232.
20. Fritsch A, Spassov S, Elfert S, Schlosser A, Gache Y, Meneguzzi G, Bruckner-Tuderman L. 2009. Dominant-negative effects of COL7A1 mutations can be rescued by controlled overexpression of normal collagen VII. J Biol Chem 284:30248-30256.
21. 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 their gene expression profile and reactivity to IL-1beta. Osteoarthritis Cartilage 13:697-708.
22. Gossen M, Freundlieb S, Bender G, Muller G, Hillen W, Bujard H. 1995. Transcriptional activation by tetracyclines in mammalian cells. Science 268:1766-1769.
23. 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.
24. Hoornaert KP, Dewinter C, Vereecke I, Beemer FA, Courtens W, Fryer A, Fryssira H, Lees M, Mullner-Eidenbock A, Rimoin DL, Siderius L, Superti-Furga A, Temple K, Willems PJ, Zankl A, Zweier C, De Paepe A, Coucke P, Mortier GR. 2006. The phenotypic spectrum in patients with arginine to cysteine mutations in the COL2A1 gene. J Med Genet 43:406-413.
25. Horwitz EM, Gordon PL, Koo WK, Marx JC, Neel MD, McNall RY, Muul L, Hofmann T. 2002. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone. Proc Natl Acad Sci USA 99:8932-8937.
26. Horwitz EM, Prockop DJ, Fitzpatrick LA, Koo WW, Gordon PL, Neel M, Sussman M, Orchard P, Marx JC, Pyeritz RE and others. 1999. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 5:309-313.
27. Horwitz EM, Prockop DJ, Gordon PL, Koo WW, Fitzpatrick LA, Neel MD, McCarville ME, Orchard PJ, Pyeritz RE, Brenner MK. 2001. Clinical responses to bone marrow transplantation in children with severe osteogenesis imperfecta. Blood 97:1227-1231.
28. Ito H, Rucker E, Steplewski A, McAdams E, Brittingham RJ, Alabyeva 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.
29. Ito H, Steplewski A, Alabyeva T, Fertala A. 2006. Testing the utility of rationally engineered recombinant collagen-like proteins for applications in tissue engineering. J Biomed Mater Res A 76:551-560.
30. Katzenstein PL, Malemud CJ, Pathria MN, Carter JR, Sheon RP, Moskowitz RW. 1990. Early-onset primary osteoarthritis and mild chondrodysplasia. Radiographic and pathologic studies with an analysis of cartilage proteoglycans. Arthritis Rheum 33:674-684.
31. 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.
32. Little CD, Chen WT. 1982. Masking of extracellular collagen and the co-distribution of collagen and fibronectin during matrix formation by cultured embryonic fibroblasts. J Cell Sci 55:35-50.
33. Martin JA, Buckwalter JA. 1998. Effects of fibronectin on articular cartilage chondrocyte proteoglycan synthesis and response to insulin-like growth factor-I. J Orthop Res 16:752-757.
34. Olsen BR. 1995. Mutations in collagen genes resulting in metaphyseal and epiphyseal dysplasias. Bone 17:45S-49S.
35. Peace BE, Florer JB, Witte D, Smicun Y, Toudjarska I, Wu G, Kilpatrick MW, Tsipouras P, Wenstrup RJ. 2005. Endogenously expressed multimeric self-cleaving hammerhead ribozymes ablate mutant collagen in cellulo. Mol Ther 12:128-136.
36. Pereira RF, Halford KW, O'Hara MD, Leeper DB, Sokolov BP, Pollard MD, Bagasra O, Prockop DJ. 1995. Cultured adherent cells from marrow can serve as long-lasting precursor cells for bone, cartilage, and lung in irradiated mice. Proc Natl Acad Sci USA 92:4857-4861.
37. Pereira RF, O'Hara MD, Laptev AV, Halford KW, Pollard MD, Class R, Simon D, Livezey K, Prockop DJ. 1998. Marrow stromal cells as a source of progenitor cells for nonhematopoietic tissues in transgenic mice with a phenotype of osteogenesis imperfecta. Proc Natl Acad Sci USA 95:1142-1147.
38. Prockop DJ. 1984. Osteogenesis imperfecta: phenotypic heterogeneity, protein suicide, short and long collagen. Am J Hum Genet 36:499-505.
39. Prockop DJ. 1997. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71-74.
40. Reits EA, Neefjes JJ. 2001. From fixed to FRAP: measuring protein mobility and activity in living cells. Nat Cell Biol 3:E145-E147.
41. Royce PM, Steinmann B. 2002. Connective tissue and its heritable disorders: molecular, genetic, and medical aspects. New York: John Wiley.
42. Steplewski A, Brittingham R, Jimenez SA, Fertala A. 2005. Single amino acid substitutions in the C-terminus of collagen II alter its affinity for collagen IX. Biochem Biophys Res Commun 335:749-755.
43. Steplewski A, Ito H, Rucker E, Brittingham RJ, Alabyeva 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.
44. 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.
45. Velling T, Risteli J, Wennerberg K, Mosher DF, Johansson S. 2002. Polymerization of type I and III collagens is dependent on fibronectin and enhanced by integrins alpha 11beta 1 and alpha 2beta 1. J Biol Chem 277:37377-37381.
46. Vernon RB, Gooden MD. 2002. An improved method for the collagen gel contraction assay. In Vitro Cell Dev Biol Anim 38:97-101.
47. Vernon RB, Sage EH. 1999. A novel, quantitative model for study of endothelial cell migration and sprout formation within three-dimensional collagen matrices. Microvasc Res 57:118-133.
48. Wang Q, Marini JC. 1996. Antisense oligodeoxynucleotides selectively suppress expression of the mutant alpha 2(I) collagen allele in type IV osteogenesis imperfecta fibroblasts. A molecular approach to therapeutics of dominant negative disorders. J Clin Invest 97:448-454.
49. 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.
50. 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.