Missense mutations in dystrophin that trigger muscular dystrophy decrease protein stability and lead to cross-β aggregates

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 34, 2010, Pages 15069-15074

  Singh, Surinder M ^a   Kongari, Narsimulu ^a   Cabello Villegas, Javier ^a   Mallela, Krishna M G ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Actin binding domain; Becker muscular dystrophy; Calponin homology domain; Duchenne muscular dystrophy; Protein aggregation

Indexed keywords

ACTIN BINDING PROTEIN; CONGO RED; DYSTROPHIN; THIOFLAVINE; MULTIPROTEIN COMPLEX; MUTANT PROTEIN; RECOMBINANT PROTEIN;

ARTICLE; BIREFRINGENCE; CIRCULAR DICHROISM; CLINICAL ASSESSMENT; DISEASE ASSOCIATION; FLUORESCENCE; MISSENSE MUTATION; MUSCULAR DYSTROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN STABILITY; THERMOSTABILITY; BIOPHYSICS; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; IN VITRO STUDY; METABOLISM; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; THERMODYNAMICS; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

BIOPHYSICAL PHENOMENA; DYSTROPHIN; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; MUSCULAR DYSTROPHIES; MUTANT PROTEINS; MUTATION, MISSENSE; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; THERMODYNAMICS;

EID: 77956994292     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1008818107     Document Type: Article

References (49)

1. Emery AEH (2002) The muscular dystrophies. Lancet 359:687-695.
2. Hoffman EP, Brown J, Robert H, Kunkel LM (1987) Dystrophin: The protein product of the Duchenne Muscular Dystrophy locus. Cell 51:919-928.
3. Emery A (1991) Population frequencies of inherited neuromuscular disorders: A world survey. Neuromuscular Disord 1:19-29.
4. Blake DJ,Weir A, Newey SE, Davies KE (2002) Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev 82:291-329.
5. Bakker E, van Ommen GB (1998) Neuromuscular disorders: Clinical and molecular genetics, ed AEH Emery (John Wiley & Sons, New York), pp 59-85.
6. Muntoni F, Torelli S, Ferlini A (2003) Dystrophin and mutations: One gene, several proteins, multiple phenotypes. Lancet Neurol 2:731-740. (Pubitemid 37443515)
7. Batchelor CL, Winder SJ (2006) Sparks, signals and shock absorbers: How dystrophin loss causes muscular dystrophy. Trends Cell Biol 16:198-205.
8. Ervasti JM (2007) Review: Dystrophin, its interactions with other proteins, and implications. Biochim Biophys Acta 1772:108-117.
9. Vainzof M, Zatz M (2007) Protein misfolding, aggregation, and conformational diseases. Part B: Molecular mechanisms of conformational diseases, eds VN Uversky and AL Fink (Springer, New York).
10. Winder SJ (1995) Dystrophin and utrophin: The missing Links! FEBS Lett 369:27-33.
11. Rybakova IN, Patel JR, Ervasti JM (2000) The dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin. J Cell Biol 150:1209-1214.
12. Roberts RG (2001) Protein family review: Dystrophins and dystrobrevins. Genome Biol 2 reviews3006.3001-3006.3007.
13. Rando TA (2001) The dystrophin-glycoprotein complex, cellular signaling, and the regulation of cell survival in the muscular dystrophies. Muscle Nerve 24:1575-1594.
14. Oak SA, Zhou YW, Jarret HW (2003) Skeletal muscle signaling pathway through the dystrophin glycoprotein complex and Rac1. J Biol Chem 278:39287-39295.
15. Glass DJ (2005) A signaling role for dystrophin: Inhibiting skeletal muscle atrophy pathways. Cancer Cell 8:351-352. (Pubitemid 41579829)
16. Roberts RG, Borrow M, Bentley DR (1992) Point mutations in the dystrophin gene. Proc Natl Acad Sci USA 89:2331-2335.
17. Sitnik R, et al. (1997) Novel point mutations in the dystrophin gene. Hum Mutat 10:217-222.
18. Norwood FL, Sutherland-Smith AJ, Keep NH, Kendrick-Jones J (2000) The structure of the N-terminal actin-binding domain of human dystrophin and how mutations in this domain may cause Duchenne or Becker muscular dystrophy. Structure 8:481-491.
19. Prior TW, et al. (1993) A missense mutation in the dystrophin gene in a Duchenne muscular dystrophy patient. Nat Genet 4:357-360.
20. Roberts RG, Gardner RJ, Bobrow M (1994) Searching for the 1 in 2,400,000: A review of dystrophin gene point mutations. Hum Mutat 4:1-11.
21. Kahana E, Flood G, Gratzer WB (1997) Physical properties of dystrophin rod domain. Cell Motil Cytoskel 36:246-252. (Pubitemid 27104917)
22. Rybakova IN, Ervasti JM (1997) Dystrophin-glycoprotein complex is monomeric and stabilizes actin filaments in vitro through a lateral association. J Biol Chem 272:28771-28778.
23. Broderick MJF, Winder SJ (2002) Towards a complete atomic structure of spectrin family proteins. J Struct Biol 137:184-193.
24. Winder SJ, Gibson TJ, Kendrick-Jones J (1996) Low probability of dystrophin and utrophin coiled coil regions forming dimers. Biochem Soc Trans 24:280S.
25. McGough A, Way M, DeRosier D (1994) Determination of the α-actinin-binding site on actin filaments by cryoelectronmicroscopy and image analysis. J Cell Biol 126:433-443. (Pubitemid 24226259)
26. Goldsmith SC, et al. (1997) The structure of an actin-crosslinking domain from human fimbrin. Nat Struct Biol 4:708-712.
27. Franzot G, Sjöblom B, Gautel M, Carugo KD (2005) The crystal structure of the actin binding domain from α-actinin in its closed conformation: Structural insight into phospholipid regulation of α-actinin. J Mol Biol 348:151-165.
28. 15N NMR relaxation. Prog NMR Spectroscopy 31:63-105.
29. Baynes BM, Wang DIC, Trout BL (2005) Role of arginine in the stabilization of proteins against aggregation. Biochemistry 44:4919-4925.
30. Dong A, Huang P, Caughey WS (1990) Protein secondary structures in water from second-derivative amide I infrared spectra. Biochemistry 29:3303-3308. (Pubitemid 20131472)
31. Dong A, Matsuura J, Manning MC, Carpenter JF (1998) Intermolecular β-sheet results from trifluoroethanol-induced nonnative α-helical structure in β-sheet predominant proteins: Infrared and circular dichroism spectroscopic study. Arch Biochem Biophys 355:275-281.
32. Dong A, Randolph TW, Carpenter JF (2000) Entrapping intermediates of thermal aggregation in α-helical proteins with low concentration of guanidine hydrochloride. J Biol Chem 275:27689-27693.
33. Levine-III H (1993) Thioflavine T interaction with synthetic Alzheimer's disease {beta}-amyloid peptides: Detection of amyloid aggregation in solution. Protein Sci 2:404-410.
34. Klunk WE, Pettegrew JW, Abraham DJ (1989) Quantitative evaluation of congo red binding to amyloid-like proteins with a beta-pleated sheet conformation. J Histochem Cytochem 37:1273-1281.
35. Childers WS, Mehta AK, Lu K, Lynn DG (2009) Templating molecular arrays in amyloid's cross-β grooves. J Am Chem Soc 131:10165-10172.
36. Chakrabartty A, Kortemme T, Baldwin RL (1994) Helix propensities of the amino acids measured in alanine-based peptides without helix-stabilizing side-chain interactions. Protein Sci 3:843-852.
37. Ebert G, Ebert C, Paudjojo L (1978) Effect of water and electrostatic interactions on the conformation conversion of polypeptides and proteins. Prog Coll Pol Sci S 65:60-67.
38. Legardinier S, et al. (2009) A two-amino acid mutation encountered in Duchenne muscular dystrophy decreases stability of the rod domain 23 (R23) spectrin-like repeat of dystrophin. J Biol Chem 284:8822-8832.
39. Thibodeau PH, Brautigam CA, Machius M, Thomas PJ (2005) Side chain and backbone contributions of Phe508 to CFTR folding. Nat Struct Mol Biol 12:10-16. (Pubitemid 40082911)
40. Du K, Sharma M, Lukacs GL (2005) The ΔF508 cystic fibrosis mutation impairs domain-domain interactions and arrests post-translational folding of CFTR. Nat Struct Mol Biol 12:17-25.
41. Mayer S, Rüdiger S, Ang HC, Joerger AC, Fersht AR (2007) Correlation of levels of folded recombinant p53 in Escherichia coli with thermodynamic stability in vitro. J Mol Biol 372:268-276. (Pubitemid 47223226)
42. Joerger AC, Fersht AR (2008) Structural biology of the tumor suppressor p53. Annu Rev Biochem 77:557-582.
43. Mehanna AS (2001) Sickle cell anemia and antisickling agents then and now. Curr Med Chem 8:79-88.
44. Bai Y, Sosnick TR, Mayne L, Englander SW (1995) Protein folding intermediates: Native-state hydrogen exchange. Science 269:192-197.
45. Englander SW, Mayne L, Krishna MMG (2007) Protein folding and misfolding: Mechanism and principles. Q Rev Biophys 40:287-326.
46. Delaglio F, et al. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6:277-293.
47. Blankinship MJ, Gregorevic P, Chamberlain JS (2006) Gene therapy strategies for Duchenne muscular dystrophy utilizing recombinant adeno-associated virus vectors. Mol Ther 13:241-249.
48. Pettersen EF, et al. (2004) UCSF Chimera - a visualization system for exploratory research and analysis. J Comput Chem 25:1605-1612.
49. Henderson DM, Lee A, Ervasti JM (2010) Disease-causing missense mutations in actin binding domain 1 of dystrophin induce thermodynamic instability and protein aggregation. Proc Natl Acad Sci USA 107:9632-9637.