Unfolding a folding disease: Folding, misfolding and aggregation of the marble brain syndrome-associated mutant H107Y of human carbonic anhydrase II

Journal of Molecular Biology

Volumn 342, Issue 2, 2004, Pages 619-633

  Almstedt, Karin ^a   Lundqvist, Martin ^a   Carlsson, Jonas ^a   Karlsson, Martin ^a   Persson, Bengt ^a   Jonsson, Bengt Harald ^a   Carlsson, Uno ^a   Hammarström, Per ^a  

^a LINKÖPING UNIVERSITY   (Sweden)

Author keywords

aggregation; loss of function; misfolding; misfolding inhibitor; molten globule

Indexed keywords

8 ANILINO 1 NAPHTHALENESULFONIC ACID; ACETAZOLAMIDE; CARBONATE DEHYDRATASE II; CARBONATE DEHYDRATASE INHIBITOR; GUANIDINE; HISTIDINE; MUTANT PROTEIN; SERINE; TYROSINE;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CARBONIC ANHYDRASE II DEFICIENCY SYNDROME; CIRCULAR DICHROISM; DISEASE ASSOCIATION; ENZYME ACTIVITY; EQUILIBRIUM CONSTANT; FLUORESCENCE; HIGH TEMPERATURE; HYDRATION; HYDROPHOBICITY; LOW TEMPERATURE; MARBLE BRAIN SYNDROME; MOLECULAR BIOLOGY; MOLECULAR INTERACTION; MOLECULAR MODEL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PATHOPHYSIOLOGY; PH; POINT MUTATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN DEFECT; PROTEIN DENATURATION; PROTEIN DETERMINATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; TEMPERATURE DEPENDENCE; THERMODYNAMICS; THERMOSTABILITY; WILD TYPE;

EID: 4344710278     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.07.024     Document Type: Article

References (41)

1. S. Lindskog Structure and mechanism of carbonic anhydrase Pharmacol. Ther. 74 1997 1 20
2. K.S. Smith, and J.G. Ferry Prokaryotic carbonic anhydrases FEMS Microbiol. Rev. 24 2000 335 366
3. W.R. Chegwidden Introduction to the carbonic anhydrases W.R. Chegwidden N.D. Carter Y.H. Edwards The Carbonic Anhydrases New Horizons 2000 Birkhäuser Basel 13 28
4. K. Håkansson, M. Carlsson, L.A. Svensson, and A. Liljas Structure of native and apo carbonic anhydrase II and structure of some of its anion-ligand complexes J. Mol. Biol. 227 1992 1192 1204
5. U. Carlsson, and B.-H. Jonsson Folding and stability of human carbonic anhydrase W.R. Chegwidden N.D. Carter Y.H. Edwards The Carbonic Anhydrases New Horizons 2000 Birkhäuser Basel 241 259
6. N. Bergenhem, and U. Carlsson The role of the metal ion in the refolding of denatured bovine Co(II)-carbonic anhydrase II Biochim. Biophys. Acta 998 1989 277 285
7. D. Andersson, P. Hammarström, and U. Carlsson Cofactor-induced refolding: refolding of molten globule carbonic anhydrase induced by Zn(II) and Co(II) Biochemistry 40 2001 2653 2661
8. P. Hammarström, M. Persson, P.-O. Freskgård, L.-G. Mårtensson, D. Andersson, B.-H. Jonsson, and U. Carlsson Structural mapping of an aggregation nucleation site in a molten globule intermediate J. Biol. Chem. 274 1999 32897 32903
9. P. Hammarström, M. Persson, and U. Carlsson Protein compactness measured by fluorescence resonance energy transfer. Human carbonic anhydrase ii is considerably expanded by the interaction of GroEL J. Biol. Chem. 276 2001 21765 21775
10. P. Hammarström, R. Owenius, L.-G. Mårtensson, U. Carlsson, and M. Lindgren High-resolution probing of local conformational changes in proteins by the use of multiple labeling: unfolding and self-assembly of human carbonic anhydrase II monitored by spin, fluorescent, and chemical reactivity probes Biophys. J. 80 2001 2867 2885
11. W.S. Sly, D. Hewett-Emmett, M.P. Whyte, Y.S. Yu, and R.E. Tashian Carbonic anhydrase II deficiency identified as the primary defect in the autosomal recessive syndrome of osteopetrosis with renal tubular acidosis and cerebral calcification Proc. Natl Acad. Sci. USA 80 1983 2752 2756
12. W.S. Sly Carbonic anhydrase II deficiency syndrome: clinical delineation, interpretation and implications S.J. Dodgson R.E. Tashian G. Gros N.D. Carter The Carbonic Anhydrases 1991 Plenum Press New York 183 193
13. S. Aramaki, I. Yoshida, M. Yoshino, M. Kondo, Y. Sato, K. Noda, R. Jo, A. Okue, N. Sai, and F. Yamashita Carbonic anhydrase deficiency in three unrelated patients J. Inher. Metab. Dis. 16 1993 982 990
14. W.S. Sly, and P.Y. Hu Human carbonic anhydrases and carbonic anhydrase deficiencies Annu. Rev. Biochem. 64 1995 375 401
15. P.Y. Hu, E.J. Lim, J. Ciccolella, P. Strisciuglio, and W.S. Sly Seven novel mutations in carbonic anhydrase II deficiency syndrome identified by SSCP and direct sequencing analysis Hum. Mutat. 9 1997 383 387
16. H. Soda, S. Yukizane, I. Yoshida, Y. Koga, S. Aramak, and H. Kato A point mutation in exon 3 (His107→Tyr) in two unrelated Japanese patients with carbonic anhydrase II deficiency with central nervous system involvement Hum. Genet. 97 1996 435 437
17. C. Tu, J.M. Couton, G. Van Heeke, N.G. Richards, and D.N. Silverman Kinetic analysis of a mutant (His107-→Tyr) responsible for human carbonic anhydrase II deficiency syndrome J. Biol. Chem. 268 1993 4775 4779
18. R.F. Chen, and J.C. Kernohan Combination of bovine carbonic anhydrase with a fluorescent sulfonamide J. Biol. Chem. 242 1967 5813 5823
19. L.-G. Mårtensson, B.-H. Jonsson, P.-O. Freskgård, A. Kihlgren, M. Svensson, and U. Carlsson Characterization of folding intermediates of human carbonic anhydrase II: probing substructure by chemical labeling of SH groups introduced by site-directed mutagenesis Biochemistry 32 1993 224 231
20. M. Persson, P. Hammarström, M. Lindgren, B.-H. Jonsson, M. Svensson, and U. Carlsson EPR mapping of interactions between spin-labeled variants of human carbonic anhydrase II and GroEL: evidence for increased flexibility of the hydrophobic core by the interaction Biochemistry. 38 1999 432 441
21. P.-O. Freskgård, L.-G. Mårtensson, P. Jonasson, B.-H. Jonsson, and U. Carlsson Assignment of the contribution of the tryptophan residues to the circular dichroism spectrum of human carbonic anhydrase II Biochemistry 33 1994 14281 14288
22. K. Boren, H. Grankvist, P. Hammarström, and U. Carlsson Reshaping the folding energy landscape by chloride salt: impact on molten-globule formation and aggregation behavior of carbonic anhydrase FEBS Letters 566 2004 95 99
23. L.-G. Mårtensson, P. Jonasson, P.-O. Freskgård, M. Svensson, U. Carlsson, and B.-H. Jonsson Contribution of individual tryptophan residues to the fluorescence spectrum of native and denatured forms of human carbonic anhydrase II Biochemistry 34 1995 1011 1021
24. M.M. Santoro, and D.W. Bolen Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants Biochemistry 27 1988 8063 8068
25. C.T. Supuran, A. Scozzafava, and A. Casini Carbonic anhydrase inhibitors Med. Res. Rev. 23 2003 146 189
26. L.-G. Mårtensson, B.-H. Jonsson, M. Andersson, A. Kihlgren, N. Bergenhem, and U. Carlsson Role of an evolutionarily invariant serine for the stability of human carbonic anhydrase II Biochim. Biophys. Acta 1118 1992 179 186
27. D.A. Erlanson, and G.L. Verdine Falling out of the fold: tumorigenic mutations and p53 Chem. Biol. 1 1994 179 184
28. A. Friedler, B.S. DeDecker, S.M. Freund, C. Blair, S. Rudiger, and A.R. Fersht Structural distortion of p53 by the mutation R249S and its rescue by a designed peptide: implications for "mutant conformation" J. Mol. Biol. 336 2004 187 196
29. P.J. Waters, M.A. Parniak, B.R. Akerman, and C.R. Scriver Characterization of phenylketonuria missense substitutions, distant from the phenylalanine hydroxylase active site, illustrates a paradigm for mechanism and potential modulation of phenotype Mol. Genet. Metab. 69 2000 101 110
30. P.J. Thomas, Y.H. Ko, and P.L. Pedersen Altered protein folding may be the molecular basis of most cases of cystic fibrosis FEBS Letters 312 1992 7 9
31. P.J. Thomas, B.H. Qu, and P.L. Pedersen Defective protein folding as a basis of human disease Trends. Biochem. Sci. 20 1995 456 459
32. P. Hammarström, X. Jiang, A.R. Hurshman, E.T. Powers, and J.W. Kelly Sequence-dependent denaturation energetics: a major determinant in amyloid disease diversity Proc. Natl Acad. Sci. USA 99 2002 16427 16432
33. D.R. Booth, M. Sunde, V. Bellotti, C.V. Robinson, W.L. Hutchinson, and P.E. Fraser Instability, unfolding and aggregation of human lysozyme variants underlying amyloid fibrillogenesis Nature 385 1997 773 775
34. F.E. Cohen, and J.W. Kelly Therapeutic approaches to protein-misfolding diseases Nature 426 2003 905 909
35. P. Hammarström, R.L. Wiseman, E.T. Powers, and J.W. Kelly Prevention of transthyretin amyloid disease by changing protein misfolding energetics Science 299 2003 713 716
36. A.R. Sawkar, W.C. Cheng, E. Beutler, C.H. Wong, W.E. Balch, and J.W. Kelly Chemical chaperones increase the cellular activity of N370S beta-glucosidase: a therapeutic strategy for Gaucher disease Proc. Natl Acad. Sci. USA 99 2002 15428 15433
37. G. Rebello, R. Ramesar, A. Vorster, L. Roberts, L. Ehrenreich, and E. Oppon Apoptosis-inducing signal sequence mutation in carbonic anhydrase IV identified in patients with the RP17 form of retinitis pigmentosa Proc. Natl Acad. Sci. USA 101 2004 6617 6622
38. P. Strisciuglio, R. Sartorio, C. Pecoraro, F. Lotito, and W.S. Sly Variable clinical presentation of carbonic anhydrase deficiency: evidence for heterogeneity? Eur. J. Pediatr. 149 1990 337 340
39. Y. Nozaki The preparation of guanidine hydrochloride Methods Enzymol. 26 1972 43 50
40. R.G. Khalifah, D.J. Strader, S.H. Bryant, and S.M. Gibson Carbon-13 nuclear magnetic resonance probe of active-site ionizations in human carbonic anhydrase B Biochemistry 16 1977 2241 2247
41. E.E. Rickli, S.A.S. Ghazanfar, B.H. Gibbons, and J.T. Edsall Carbonic anhydrases from hyman erythrocytes. Preparation and properties of two enzymes J. Biol. Chem. 239 1964 1065 1078