The structure of the cataract-causing P23T mutant of human γD-crystallin exhibits distinctive local conformational and dynamic changes

Biochemistry

Volumn 48, Issue 12, 2009, Pages 2597-2609

  Jung, Jinwon ^a   Byeon, In Ja L ^a   Wang, Yongting ^b   King, Jonathan ^b   Gronenborn, Angela M ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOPHYSICAL ANALYSIS; CONGENITAL CATARACTS; CRYSTALLIN; DATA SUPPORTS; DYNAMIC BEHAVIORS; DYNAMIC CHANGES; EYE LENS; GLOBAL STRUCTURES; LENS TRANSPARENCIES; MUTANT PROTEINS; MUTATION SITES; SELF ASSOCIATIONS; SOLUTION STRUCTURES; STRUCTURAL CHANGES; STRUCTURAL INFORMATIONS; WILD TYPES; WILD-TYPE PROTEINS; X-RAY STRUCTURES;

ANIMAL CELL CULTURE; ASSOCIATION REACTIONS; BIOCHEMISTRY; LENSES; MONOMERS; OPTICAL INSTRUMENTS; PLANTS (BOTANY); POLYMERS;

CONFORMATIONS;

CRYSTALLIN; GAMMA D CRYSTALLIN; HISTIDINE; IMIDAZOLE; MUTANT PROTEIN; P 23T PROTEIN; THREONINE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CONGENITAL CATARACT; MOLECULAR DYNAMICS; MUTATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN STRUCTURE; WILD TYPE; X RAY;

CATARACT; CRYSTALLINS; HISTIDINE; HUMANS; KINETICS; MODELS, MOLECULAR; MUTATION; PROTEIN CONFORMATION;

EID: 65249160170     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi802292q     Document Type: Article

References (63)

1. Wistow, G. J., and Piatigorsky, J. (1988) Lens crystallins: The evolution and expression of proteins for a highly specialized tissue. Annu. Rev. Biochem. 57, 479-504.
2. Horwitz, J. (2003) a-Crystallin. Exp. Eye Res. 76, 145-153.
3. Bloemendal, H., de Jong, W., Jaenicke, R., Lubsen, N. H., Slingsby, C, and Tardieu, A. (2004) Ageing and vision: Structure, stability and function of lens crystallins. Prog. Biophys. Mol. Biol. 86, 407-485.
4. Jaenicke, R., and Slingsby, C. (2001) Lens crystallins and their microbial homologs: Structure, stability, and function. Crit. Rev. Biochem. Mol. Biol. 36, 435-499.
5. Foster, A. (2001) Cataract and "Vision 2020-the right to sight" initiative. Br. J. Ophthalmol. 85, 635-637.
6. Toh, T., Morton, J., Coxon, J., and Elder, M. J. (2007) Medical treatment of cataract. Clin. Exp. Ophthalmol. 35, 664-671.
7. Chirgadze, Y. N, Driessen, H. P., Wright, G., Slingsby, C., Hay, R. E., and Lindley, P. F. (1996) Structure of bovine eye lens γD (γIIIb)-crystallin at 1.95 Å. Acta Crystallogr. D52, 712-721.
8. Basak, A. K., Bateman, O., Slingsby, C., Pande, A., Asherie, N, Ogun, O., Benedek, G. B., and Pande, J. (2003) High-resolution X-ray crystal structures of human γD crystallin (1.25 Å) and the R58H mutant (1.15 Å) associated with aculeiform cataract. J. Mol. Biol. 328, 1137-1147.
9. Wu, Z., Delaglio, F., Wyatt, K., Wistow, G, and Bax, A. (2005) Solution structure of γS-crystallin by molecular fragment replacement NMR. Protein Sci. 14, 3101-3114.
10. Rudolph, R., Siebendritt, R., Nesslauer, G., Sharma, A. K., and Jaenicke, R. (1990) Folding of an all-β protein: Independent domain folding in γII-crystallin from calf eye lens. Proc. Natl. Acad. Sci. U.S.A. 87, 4625-4629.
11. Stephan, D. A., Gillanders, E., Vanderveen, D., Freas-Lutz, D., Wistow, G., Baxevanis, A. D., Robbins, C. M., VanAuken, A., Quesenberry, M. I., Bailey-Wilson, J., Juo, S. H., Trent, J. M., Smith, L., and Brownstein, M. J. (1999) Progressive juvenile-onset punctate cataracts caused by mutation of the γD-crystallin gene. Proc. Natl. Acad. Sci. U.S.A. 96, 1008-1012.
12. Pande, A., Pande, J., Asherie, N, Lomakin, A., Ogun, O., King, J. A., Lubsen, N. H, Walton, D., and Benedek, G. B. (2000) Molecular basis of a progressive juvenile-onset hereditary cataract. Proc. Natl. Acad. Sci. U.S.A. 97, 1993-1998.
13. Kmoch, S., Brynda, J., Asfaw, B., Bezouska, K., Novák, P., Rezácová, P., Ondrová, L., Filipec, M., Sedlácek, J., and Elleder, M. (2000) Link between a novel human γD-crystallin allele and a unique cataract phenotype explained by protein crystallography. Hum. Mol. Genet. 9, 1779-1786.
14. Pande, A., Pande, J., Asherie, N, Lomakin, A., Ogun, O. O., King, J. A., Lubsen, N. H, Walton, D., and Benedek, G. B. (2000) Molecular basis of a progressive juvenile-onset hereditary cataract. Proc. Natl. Acad. Sci. U.S.A. 97, 1993-1998.
15. Santhiya, S. T., Shyam Manohar, M., Rawlley, D., Vijayalakshmi, P., Namperumalsamy, P., Gopinath, P. M., Löster, J., and Graw, J. (2002) Novel mutations in the γ-crystallin genes cause autosomal dominant congenital cataracts. J. Med. Genet. 39, 352-358.
16. Nandrot, E., Slingsby, C., Basak, A. K, Cherif-Chefchaouni, M., Benazzouz, B., Hajaji, Y., Boutayeb, S., Gribouval, O., Arbogast, L., Berraho, A., Abitbol, M., and Hilal, L. (2003) γ-D crystallin gene (CRYGD) mutation causes autosomal dominant congenital cerulean cataracts. J. Med. Genet. 40, 262-267.
17. Burdon, K. P., Wirth, M. G., Mackey, D. A., Russell-Eggitt, I. M., Craig, J. E., Elder, J. E., Dickinson, J. L., and Sale, M. M. (2004) Investigation of crystallin genes in familial cataract, and report of two disease associated mutations. Br. J. Ophthalmol. 88, 79-83.
18. Mackay, D. S., Andley, U. P., and Shiels, A. (2004) A missense mutation in the γD-crystallin gene (CRYGD) associated with autosomal dominant "coral-like" cataract linked to chromosome 2q. Mol. Vision 10, 155-162.
19. Shentu, X., Yao, K., Xu, W., Zheng, S., Hu, S., and Gong, X. (2004) Special fasciculiform cataract caused by a mutation in the γD-crystallin gene. Mol. Vision 10, 233-239.
20. Messina-Baas, O. M., Gonzalez-Huerta, L. M., and Cuevas-Covarrubias, S. A. (2006) Two affected siblings with nuclear cataract associated with a novel missense mutation in the CRYGD gene. Mol. Vision 12, 995-1000.
21. Li, F., Wang, S., Gao, C, Liu, S., Zhao, B., Zhang, M., Huang, S., Zhu, S., and Ma, X. (2008) Mutation G61C in the CRYGD gene causing autosomal dominant congenital coralliform cataracts. Mol. Vision 14, 378-386.
22. Plotnikova, O. V., Kondrashov, F. A., Vlasov, P. K., Grigorenko,A. P., Ginter, E. K., and Rogaev, E. I. (2007) Conversion and compensatory evolution of the γ-crystallin genes and identification of a cataractogenic mutation that reverses the sequence of the human CRYGD gene to an ancestral state. Am. J. Hum. Genet. 81, 32-43.
23. Evans, P., Wyatt, K., Wistow, G J., Bateman, O. A., Wallace,B. A., and Slingsby, C. (2004) The P23T cataract mutation causes loss of solubility of folded γD-crystallin. J. Mol. Biol. 343, 435-444.
24. Pande, A., Annunziata, O., Asherie, N, Ogun, O., Benedek, G. B., and Pande, J. (2005) Decrease in protein solubility and cataract formation caused by the Pro23 to Thr mutation in human γD-crystallin. Biochemistry 44, 2491-2500.
25. McManus, J. J., Lomakin, A., Ogun, O., Pande, A., Basan, M., Pande, J., and Benedek, G. B. (2007) Altered phase diagram due to a single point mutation in human γD-crystallin. Proc. Natl. Acad. Sci. U.S.A. 104, 16856-16861.
26. Kosinski-Collins, M. S., Flaugh, S. L., and King, J. (2004) Probing folding and fluorescence quenching in human γD crystallin Greek key domains using triple tryptophan mutant proteins. Protein Sci. 13, 2223-2235.
27. Clore, G. M., and Gronenborn, A. M. (1998) Determining the structures of large proteins and protein complexes by NMR. Trends Biotechnol. 16, 22-34.
28. Bax, A., and Grzesiek, S. (1993) Methodological advances in protein NMR. Acc. Chem. Res. 26, 131-138.
29. 1H-HSQC with sensitivity enhancement and a heteronuclear gradient-echo. J. Biomol. NMR 5, 97-102.
30. Day, R. M., Thalhauser, C. J., Sudmeier, J. L., Vincent, M. P., Torchilin, E. V., Sanford, D. G, Bachovchin, C. W., and Bachovchin, W. W. (2003) Tautomerism, acid-base equilibria, and H-bonding of the six histidines in subtilisin BPN' by NMR. Protein Sci. 12, 794-810.
31. Ruckert, M., and Otting, G (2000) Alignment of biological macromolecules in novel nonionic liquid crystalline media for NMR experiments. J. Am. Chem. Soc. 122, 7793-7797.
32. Ottiger, M., Delaglio, F., and Bax, A. (1998) Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J. Magn. Reson. 131, 373-378.
33. Delaglio, F., Grzesiek, S., Vuister, G W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293.
34. Goddard, T. D., and Kneller, D. G. (2004) SPARKY 3, version 3.110, University of California, San Francisco.
35. Herrmann, T., Güntert, P., and Wüthrich, K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol. 319, 209-227.
36. Cornilescu, G., Delaglio, F., and Bax, A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13, 289-302.
37. Brunger, A. T, Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T, and Warren, G L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D54 (Part 5), 905-921.
38. Linge, J. P., Williams, M. A., Spronk, C. A., Bonvin, A. M., and Nilges, M. (2003) Refinement of protein structures in explicit solvent. Proteins 50, 496-506.
39. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486.
40. Zweckstetter, M., and Bax, A. (2000) Prediction of sterically induced alignment in a dilute liquid crystalline phase: Aid to protein structure determination by NMR. J. Am. Chem. Soc. 122, 3791-3792.
41. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 51-55, 29-32.
42. 15N NMR relaxation. Biochemistry 33, 5984-6003.
43. Pelton, J. G., Torchia, D. A., Meadow, N. D., and Roseman, S. (1993) Tautomeric states of the active-site histidines of phospho-rylated and unphosphorylated IIIGlc, a signal-transducing protein from Escherichia coli, using two-dimensional heteronuclear NMR techniques. Protein Sci. 2, 543-558.
44. 15N resonance assignments and secondary structure of the human thioredoxin C62A, C69A, C73A mutant. J. Biomol. NMR 2, 431-445.
45. Nozaki, Y., and Tanford, C. (1967) Examination of titration behavior. Methods Enzymol. 11, 715-734.
46. 15N NMR spectroscopy of hydrogen-bonding interactions in the active site of serine proteases: Evidence for a moving histidine mechanism. Biochemistry 25, 7751-7759.
47. Song, J., Laskowski, M., Jr., Qasim, M. A., and Markley, J. L (2003) NMR determination of pKa values for Asp, Glu, His, and Lys mutants at each variable contiguous enzyme-inhibitor contact position of the turkey ovomucoid third domain. Biochemistry 42, 2847-2856.
48. Bachovchin, W. W. (2001) Contributions of NMR spectroscopy to the study of hydrogen bonds in serine protease active sites. Magn. Reson. Chem. 39, S199-S213.
49. Van Dijk, A. A., Scheek, R. M., Dijkstra, K., Wolters, G. K., and Robillard, G T. (1992) Characterization of the protonation and hydrogen bonding state of the histidine residues in IIAmtl, a domain of the phosphoenolpyruvate- dependent mannitol-specific transport protein. Biochemistry 31, 9063-9072.
50. Bhattacharya, S., Sukits, S. F., MacLaughlin, K. L., and Lecomte, J. T. (1997) The tautomeric state of histidines in myoglobin. Biophys. J. 73, 3230-3240.
51. 15N-labeled histidine in aqueous solution. J. Am. Chem. Soc. 99, 8149-8159.
52. Eaton, W. A., and Hofrichter, J. (1987) Hemoglobin S gelation and sickle cell disease. Blood 70, 1245-1266.
53. Eaton, W. A., and Hofrichter, J. (1990) Sickle cell hemoglobin polymerization. AdV. Protein Chem. 40, 63-279.
54. Ferrone, F. A. (1993) The polymerization of sickle hemoglobin in solutions and cells. Experientia 15, 110-117.
55. Hofrichter, J., Ross, P. D., and Eaton, W. A. (1974) Kinetics and mechanism of deoxyhemoglobin S gelation: A new approach to understanding sickle cell disease. Proc. Natl. Acad. Sci. U.S.A. 71, 4864-4868.
56. Ferrone, F. A., Hofrichter, J., and Eaton, W. A. (1985) Kinetics of sickle hemoglobin polymerization. II. A double nucleation mechanism. J. Mol. Biol. 183, 611-631.
57. Byeon, I. J., Louis, J. M., and Gronenborn, A. M. (2003) A protein contortionist: Core mutations of GB1 that induce dimerization and domain swapping. J. Mol. Biol. 333, 141-152.
58. Byeon, I. J., Louis, J. M., and Gronenborn, A. M. (2004) A captured folding intermediate involved in dimerization and domain-swapping of GB1. J. Mol. Biol. 340, 615-625.
59. Louis, J. M., Byeon, I. J., Baxa, U, and Gronenborn, A. M. (2005) The GB1 amyloid fibril: Recruitment of the peripheral β-strands of the domain swapped dimer into the polymeric interface. J. Mol. Biol. 348, 687-698.
60. Schlunegger, M. P., Bennett, M. J., and Eisenberg, D. (1997) Oligomer formation by 3D domain swapping: A model for protein assembly and misassembly. Adv. Protein Chem. 50, 61-122.
61. Gronenborn, A. M. (2009) Curr. Opin. Struct. Biol. (in press).
62. Yamasaki, M., Li, W., Johnson, D. J., and Huntington, J. A. (2008) Crystal structure of a stable dimer reveals the molecular basis of serpin polymerization. Nature 455, 1255-1258.
63. Gouet, P., Courcelle, E., Stuart, D. I., and Metoz, F. (1999) ESPript: Analysis of multiple sequence alignments in PostScript. Bioinfor-matics 15, 305-308.