Reducing the effects of intracellular accumulation of thermolabile collagen II mutants by increasing their thermostability in cell culture conditions

Biochemical and Biophysical Research Communications

Volumn 396, Issue 2, 2010, Pages 213-218

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

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Apoptosis; Cartilage; Collagen mutations; Collagen thermostability

Indexed keywords

COLLAGEN TYPE 2; GLYCEROL; GLYCINE; TRIMETHYLAMINE OXIDE;

AMINO ACID SUBSTITUTION; APOPTOSIS; ARTICLE; BONE GROWTH; CELL CULTURE; CELL STRESS; CELL SURVIVAL; CONTROLLED STUDY; GENE MUTATION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SECRETION; PROTEIN STABILITY; PROTEIN STRUCTURE; SPONDYLOEPIPHYSEAL DYSPLASIA; THERMOSTABILITY; TRIPLE HELIX;

APOPTOSIS; CELL CULTURE TECHNIQUES; COLLAGEN TYPE II; GLYCEROL; HOT TEMPERATURE; HUMANS; METHYLAMINES; MUTATION; OSTEOCHONDRODYSPLASIAS; PROTEIN FOLDING; PROTEIN STABILITY;

EID: 77952744917     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2010.04.056     Document Type: Article

References (31)

1. Gustafsson E., Aszodi A., Ortega N., Hunziker E.B., Denker H.W., Werb Z., and Fassler R. Role of collagen type II and perlecan in skeletal development. Ann. NY Acad. Sci. 995 (2003) 140-150
2. Prockop D.J., and Kivirikko K.I. Collagens: molecular biology, diseases, and potentials for therapy. Annu. Rev. Biochem. 64 (1995) 403-434
3. Olsen B.R. Mutations in collagen genes resulting in metaphyseal and epiphyseal dysplasias. Bone 17 (1995) 45S-49S
4. Williams C.J., and Prockop D.J. Synthesis and processing of a type I procollagen containing shortened pro-alpha 1(I) chains by fibroblasts from a patient with osteogenesis imperfecta. J. Biol. Chem. 258 (1983) 5915-5921
5. Rutishauser J., and Spiess M. Endoplasmic reticulum storage diseases. Swiss Med. Wkly 132 (2002) 211-222
6. Chung H.J., Jensen D.A., Gawron K., Steplewski A., and Fertala A. R992C (p.R1192C) Substitution in collagen II alters the structure of mutant molecules and induces the unfolded protein response. J. Mol. Biol. 390 (2009) 306-318
7. Hintze V., Steplewski A., Ito H., Jensen D.A., Rodeck U., and Fertala A. Cells expressing partially unfolded R789C/p.R989C type II procollagen mutant associated with spondyloepiphyseal dysplasia undergo apoptosis. Hum. Mutat. 29 (2008) 841-851
8. Ito H., Rucker E., Steplewski A., McAdams E., Brittingham R.J., Alabyeva T., and Fertala A. Guilty by association: some collagen II mutants alter the formation of ECM as a result of atypical interaction with fibronectin. J. Mol. Biol. 352 (2005) 382-395
9. Beck K., Chan V.C., Shenoy N., Kirkpatrick A., Ramshaw J.A., and Brodsky B. Destabilization of osteogenesis imperfecta collagen-like model peptides correlates with the identity of the residue replacing glycine. Proc. Natl. Acad. Sci. USA 97 (2000) 4273-4278
10. Penkova R., Goshev I., Gorinstein S., and Nedkov P. Stability of collagen during denaturation. J. Protein. Chem. 18 (1999) 397-401
11. Russell A.E. Effect of alcohols and neutral salt on the thermal stability of soluble and precipitated acid-soluble collagen. Biochem. J. 131 (1973) 335-342
12. Chan D., Taylor T.K., and Cole W.G. Characterization of an arginine 789 to cysteine substitution in alpha 1 (II) collagen chains of a patient with spondyloepiphyseal dysplasia. J. Biol. Chem. 268 (1993) 15238-15245
13. Donahue L.R., Chang B., Mohan S., Miyakoshi N., Wergedal J.E., Baylink D.J., Hawes N.L., Rosen C.J., Ward-Bailey P., Zheng Q.Y., Bronson R.T., Johnson K.R., and Davisson M.T. A missense mutation in the mouse Col2a1 gene causes spondyloepiphyseal dysplasia congenita, hearing loss, and retinoschisis. J. Bone Miner. Res. 18 (2003) 1612-1621
14. Fertala A., Sieron A.L., Ganguly A., Li S.W., Ala-Kokko L., Anumula K.R., and Prockop D.J. Synthesis of recombinant human procollagen II in a stably transfected tumour cell line (HT1080). Biochem. J. 298 (1994) 31-37
15. Sieron A.L., Fertala A., Ala-Kokko L., and Prockop D.J. Deletion of a large domain in recombinant human procollagen II does not alter the thermal stability of the triple helix. J. Biol. Chem. 268 (1993) 21232-21237
16. Kao W.W., Prockop D.J., and Berg R.A. Kinetics for the secretion of nonhelical procollagen by freshly isolated tendon cells. J. Biol. Chem. 254 (1979) 2234-2243
17. Kumar R., Serrette J.M., and Thompson E.B. Osmolyte-induced folding enhances tryptic enzyme activity. Arch. Biochem. Biophys. 436 (2005) 78-82
18. Bornstein P. The biosynthesis of collagen. Annu. Rev. Biochem. 43 (1974) 567-603
19. Barsh G.S., and Byers P.H. Reduced secretion of structurally abnormal type I procollagen in a form of osteogenesis imperfecta. Proc. Natl. Acad. Sci. USA 78 (1981) 5142-5146
20. Kim I., Xu W., and Reed J.C. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat. Rev. Drug Discov. 7 (2008) 1013-1030
21. Cohen F.E., and Kelly J.W. Therapeutic approaches to protein-misfolding diseases. Nature 426 (2003) 905-909
22. Perlmutter D.H. Chemical chaperones: a pharmacological strategy for disorders of protein folding and trafficking. Pediatr. Res. 52 (2002) 832-836
23. Baskakov I., and Bolen D.W. Forcing thermodynamically unfolded proteins to fold. J. Biol. Chem. 273 (1998) 4831-4834
24. Arakawa T., Ejima D., Kita Y., and Tsumoto K. Small molecule pharmacological chaperones: from thermodynamic stabilization to pharmaceutical drugs. Biochim. Biophys. Acta 1764 (2006) 1677-1687
25. Lee D., Santos D., Al-Rawi H., McNeill A.M., and Rugg E.L. The chemical chaperone trimethylamine N-oxide ameliorates the effects of mutant keratins in cultured cells. Br. J. Dermatol. 159 (2008) 252-255
26. Song J.L., and Chuang D.T. Natural osmolyte trimethylamine N-oxide corrects assembly defects of mutant branched-chain alpha-ketoacid decarboxylase in maple syrup urine disease. J. Biol. Chem. 276 (2001) 40241-40246
27. Brown C.R., Hong-Brown L.Q., and Welch W.J. Strategies for correcting the delta F508 CFTR protein-folding defect. J. Bioenerg. Biomembr. 29 (1997) 491-502
28. Burrows J.A., Willis L.K., and Perlmutter D.H. Chemical chaperones mediate increased secretion of mutant alpha 1-antitrypsin (alpha 1-AT) Z: a potential pharmacological strategy for prevention of liver injury and emphysema in alpha 1-AT deficiency. Proc. Natl. Acad. Sci. USA 97 (2000) 1796-1801
29. Reijonen S., Putkonen N., Norremolle A., Lindholm D., and Korhonen L. Inhibition of endoplasmic reticulum stress counteracts neuronal cell death and protein aggregation caused by N-terminal mutant huntingtin proteins. Exp. Cell Res. 314 (2008) 950-960
30. Ozcan U., Yilmaz E., Ozcan L., Furuhashi M., Vaillancourt E., Smith R.O., Gorgun C.Z., and Hotamisligil G.S. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313 (2006) 1137-1140
31. Steplewski A., Majsterek I., McAdams E., Rucker E., Brittingham R.J., Ito H., Hirai K., Adachi E., Jimenez S.A., and Fertala A. Thermostability gradient in the collagen triple helix reveals its multi-domain structure. J. Mol. Biol. 338 (2004) 989-998