The N-terminal extension of βb1-crystallin chaperones β-crystallin folding and cooperates with αa-crystallin

Biochemistry

Volumn 53, Issue 15, 2014, Pages 2464-2473

  Leng, Xiao Yao ^a   Wang, Sha ^a   Cao, Ni Qian ^a   Qi, Liang Bo ^a   Yan, Yong Bin ^a  

^a Peking University   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALS;

DILUTED SOLUTIONS; INTRAMOLECULAR CHAPERONE; MOLECULAR CHAPERONES; N-TERMINAL EXTENSION; N-TERMINAL TRUNCATION; PROTEIN STRUCTURES; SECONDARY AND TERTIARY STRUCTURES; STRUCTURAL PROTEINS;

PROTEINS;

ALPHA CRYSTALLIN; BETA CRYSTALLIN; CHAPERONE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN REFOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; BASE SEQUENCE; CRYSTALLINS; DNA PRIMERS; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PROTEIN FOLDING; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84899425563     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi500146d     Document Type: Article

References (61)

1. Bassnett, S. (2009) On the mechanism of organelle degradation in the vertebrate lens Exp. Eye Res. 88, 133-139
2. Andley, U. P. (2007) Crystallins in the eye: function and pathology Prog. Retinal Eye Res. 26, 78-98
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. Sharma, K. K. and Santhoshkumar, P. (2009) Lens aging: Effects of crystallins Biochim. Biophys. Acta 1790, 1095-1108
5. Delaye, M. and Tardieu, A. (1983) Short-range order of crystallin proteins accounts for eye lens transparency Nature 302, 415-417
6. Benedek, G. B. (1971) Theory of transparency of the eye Appl. Opt. 10, 459-473
7. Benedek, G. B. (1997) Cataract as a protein condensation disease: the Proctor Lecture Invest. Ophthalmol. Vis. Sci. 38, 1911-1921
8. Moreau, K. L. and King, J. A. (2012) Protein misfolding and aggregation in cataract disease and prospects for prevention Trends Mol. Med. 18, 273-282
9. Shiels, A., Bennett, T. M., and Hejtmancik, J. F. (2010) Cat-Map: putting cataract on the map Mol. Vis. 16, 2007-2015
10. Chan, M. P., Dolinska, M., Sergeev, Y. V., Wingfield, P. T., and Hejtmancik, J. F. (2008) Association properties of βB1- and βA3-crystallins: ability to form heterotetramers Biochemistry 47, 11062-11069
11. Slingsby, C. and Bateman, O. A. (1990) Quaternary interactions in eye lens beta-crystallins: basic and acidic subunits of β-crystallins favor heterologous association Biochemistry 29, 6592-6599
12. 1 chains FEBS Lett. 161, 225-229
13. Lapatto, R., Nalini, V., Bax, B., Driessen, H., Lindley, P. F., Blundell, T. L., and Slingsby, C. (1991) High resolution structure of an oligomeric eye lens beta-crystallin. Loops, arches, linkers and interfaces in beta B2 dimer compared to a monomeric gamma-crystallin J. Mol. Biol. 222, 1067-1083
14. Nalini, V., Bax, B., Driessen, H., Moss, D. S., Lindley, P. F., and Slingsby, C. (1994) Close packing of an oligomeric eye lens β-crystallin induces loss of symmetry and ordering of sequence extensions J. Mol. Biol. 236, 1250-1258
15. Bax, B., Lapatto, R., Nalini, V., Driessen, H., Lindley, P. F., Mahadevan, D., Blundell, T. L., and Slingsby, C. (1990) X-ray analysis of βB2-crystallin and evolution of oligomeric lens proteins Nature 347, 776-780
16. Ajaz, M. S., Ma, Z., Smith, D. L., and Smith, J. B. (1997) Size of human lens β-crystallin aggregates are distinguished by N-terminal truncation of βB1 J. Biol. Chem. 272, 11250-11255
17. Sergeev, Y. V., David, L. L., Chen, H. C., Hope, J. N., and Hejtmancik, J. F. (1998) Local microdomain structure in the terminal extensions of betaA3- and betaB2-crystallins Mol. Vis. 4, 9
18. Montfort, R. L. M. v., Bateman, O. A., Lubsen, N. H., and Slingsby, C. (2003) Crystal structure of truncated human βB1-crystallin Protein Sci. 12, 2606-2612
19. Bateman, O. A., Sarra, R., van Genesen, S. T., Kapp, G., Lubsen, N. H., and Slingsby, C. (2003) The stability of human acidic β-crystallin oligomers and hetero-oligomers Exp. Eye Res. 77, 409-422
20. Hejtmancik, J. F., Wingfield, P. T., and Sergeev, Y. V. (2004) Beta-crystallin association Exp. Eye Res. 79, 377-383
21. Sergeev, Y. V., Hejtmancik, J. F., and Wingfield, P. T. (2004) Energetics of domain-domain interactions and entropy driven association of β-crystallins Biochemistry 43, 415-424
22. Pande, A., Pande, J., Ogun, O., Lubsen, N. H., and Benedek, G. B. (2005) Oligomerization and phase transitions in aqueous solutions of native and truncated human βB1-crystallin Biochemistry 44, 1316-1328
23. Wang, S., Leng, X.-Y., and Yan, Y.-B. (2011) The benefits of being β-crystallin heteromers: βB1-crystallin protects βA3-crystallin against aggregation during co-refolding Biochemistry 50, 10451-10461
24. 1H-NMR spectroscopy of bovine lens βB2-crystallin Eur. J. Biochem. 213, 321-328
25. Kroone, R. C., Elliott, G. S., Ferszt, A., Slingsby, C., Lubsen, N. H., and Schoenmakers, J. G. (1994) The role of the sequence extensions in β-crystallin assembly Protein Eng. 7, 1395-1399
26. Dolinska, M. B., Sergeev, Y. V., Chan, M. P., Palmer, I., and Wingfield, P. T. (2009) N-terminal extension of βB1-crystallin: identification of a critical region that modulates protein interaction with βA3-crystallin Biochemistry 48, 9684-9695
27. Srivastava, K., Gupta, R., Chaves, J. M., and Srivastava, O. P. (2009) Truncated human βB1-crystallin shows altered structural properties and interaction with human βA3-crystallin Biochemistry 48, 7179-7189
28. Bateman, O. A., Lubsen, N. H., and Slingsby, C. (2001) Association behaviour of human βB1-crystallin and its truncated forms Exp. Eye Res. 73, 321-331
29. Lampi, K. J., Kim, Y. H., Bachinger, H. P., Boswell, B. A., Lindner, R. A., Carver, J. A., Shearer, T. R., David, L. L., and Kapfer, D. M. (2002) Decreased heat stability and increased chaperone requirement of modified human βB1-crystallins Mol. Vis. 8, 359-366
30. Lampi, K. J., Ma, Z., Hanson, S. R. A., Azuma, M., Shih, M., Shearer, T. R., Smith, D. L., Smith, J. B., and David, L. L. (1998) Age-related changes in human lens crystallins identified by two-dimensional electrophoresis and mass spectrometry Exp. Eye Res. 67, 31-43
31. Ma, Z., Hanson, S. R. A., Lampi, K. J., David, L. L., Smith, D. L., and Smith, J. B. (1998) Age-related changes in human lens crystallins identified by HPLC and mass spectrometry Exp. Eye Res. 67, 21-30
32. Santhoshkumar, P., Udupa, P., Murugesan, R., and Sharma, K. K. (2008) Significance of interactions of low molecular weight crystallin fragments in lens aging and cataract formation J. Biol. Chem. 283, 8477-8485
33. Su, S. P., McArthur, J. D., and Andrew Aquilina, J. (2010) Localization of low molecular weight crystallin peptides in the aging human lens using a MALDI mass spectrometry imaging approach Exp. Eye Res. 91, 97-103
34. Wang, S., Zhao, W.-J., Liu, H., Gong, H., and Yan, Y.-B. (2013) Increasing βB1-crystallin sensitivity to proteolysis caused by the congenital cataract-microcornea syndrome mutation S129R Biochim. Biophys. Acta, Mol. Basis Dis. 1832, 302-311
35. David, L. L., Lampi, K. J., Lund, A. L., and Smith, J. B. (1996) The sequence of human βB1-crystallin cDNA allows mass spectrometric detection of βB1 protein missing portions of its N-terminal extension J. Biol. Chem. 271, 4273-4279
36. Kim, Y. H., Kapfer, D. M., Boekhorst, J., Lubsen, N. H., Bachinger, H. P., Shearer, T. R., David, L. L., Feix, J. B., and Lampi, K. J. (2002) Deamidation, but not truncation, decreases the urea stability of a lens structural protein, βB1-crystallin Biochemistry 41, 14076-14084
37. Pang, M., Su, J.-T., Feng, S., Tang, Z.-W., Gu, F., Zhang, M., Ma, X., and Yan, Y.-B. (2010) Effects of congenital cataract mutation R116H on αA-crystallin structure, function and stability Biochim. Biophys. Acta, Proteins Proteomics 1804, 948-956
38. Wang, K. J., Wang, S., Cao, N.-Q., Yan, Y.-B., and Zhu, S. Q. (2011) A novel mutation in CRYBB1 associated with congenital cataract-microcornea syndrome: the p.Ser129Arg mutation destabilizes the βB1/βA3-crystallin heteromer but not the βB1-crystallin homomer Hum. Mutat. 32, E2050-E2060
39. Sun, T.-X., Das, B. K., and Liang, J. J. N. (1997) Conformational and functional differences between recombinant human lens αA- and αB-crystallin J. Biol. Chem. 272, 6220-6225
40. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72, 248-254
41. Turoverov, K. K., Haitlina, S. Y., and Pinaev, G. P. (1976) Ultra-violet fluorescence of actin. Determination of native actin content in actin preparations FEBS Lett. 62, 4-6
42. He, G.-J., Zhang, A., Liu, W.-F., Cheng, Y., and Yan, Y.-B. (2009) Conformational stability and multistate unfolding of poly(A)-specific ribonuclease FEBS J. 276, 2849-2860
43. Jiang, Y., Yan, Y.-B., and Zhou, H.-M. (2006) Polyvinylpyrrolidone 40 assists the refolding of bovine carbonic anhydrase B by accelerating the refolding of the first molten globule intermediate J. Biol. Chem. 281, 9058-9065
44. Lampi, K. J., Oxford, J. T., Bachinger, H. P., Shearer, T. R., David, L. L., and Kapfer, D. M. (2001) Deamidation of human βB1 alters the elongated structure of the dimer Exp. Eye Res. 72, 279-288
45. Kurganov, B. I. (2002) Kinetics of protein aggregation. Quantitative estimation of the chaperone-like activity in test-systems based on suppression of protein aggregation Biochemistry (Moscow) 67, 409-422
46. He, G.-J., Liu, W.-F., and Yan, Y.-B. (2011) Dissimilar roles of the four conserved acidic residues in the thermal stability of poly(A)-specific ribonuclease Int. J. Mol. Sci. 12, 2901-2916
47. Horwitz, J. (1992) α-Crystallin can function as a molecular chaperone Proc. Natl. Acad. Sci. U. S. A. 89, 10449-10453
48. Slingsby, C. and Clout, N. J. (1999) Structure of the crystallins Eye (London) 13, 395-402
49. Chen, Y. J. and Inouye, M. (2008) The intramolecular chaperone-mediated protein folding Curr. Opin. Struct. Biol. 18, 765-770
50. Schulz, E. C., Dickmanns, A., Urlaub, H., Schmitt, A., Muhlenhoff, M., Stummeyer, K., Schwarzer, D., Gerardy-Schahn, R., and Ficner, R. (2010) Crystal structure of an intramolecular chaperone mediating triple-beta-helix folding Nat. Struct. Mol. Biol. 17, 210-215
51. Markossian, K. A., Golub, N. V., Khanova, H. A., Levitsky, D. I., Poliansky, N. B., Muranov, K. O., and Kurganov, B. I. (2008) Mechanism of thermal aggregation of yeast alcohol dehydrogenase I: role of intramolecular chaperone Biochim. Biophys. Acta, Proteins Proteomics 1784, 1286-1293
52. Liu, W.-F., Zhang, A., He, G.-J., and Yan, Y.-B. (2007) The R3H domain stabilizes poly(A)-specific ribonuclease by stabilizing the RRM domain Biochem. Biophys. Res. Commun. 360, 846-851
53. He, H.-W., Feng, S., Pang, M., Zhou, H.-M., and Yan, Y.-B. (2007) Role of the linker between the N- and C-terminal domains in the stability and folding of rabbit muscle creatine kinase Int. J. Biochem. Cell Biol. 39, 1816-1827
54. Brunger, A. T., Breidenbach, M. A., Jin, R., Fischer, A., Santos, J. S., and Montal, M. (2007) Botulinum neurotoxin heavy chain belt as an intramolecular chaperone for the light chain PLoS Pathog. 3, 1191-1194
55. Bhattacharyya, J., Santhoshkumar, P., and Sharma, K. K. (2003) A peptide sequence-YSGVCHTDLHAWHGDWPLPVK [40-60]-in yeast alcohol dehydrogenase prevents the aggregation of denatured substrate proteins Biochem. Biophys. Res. Commun. 307, 1-7
56. Ma, B., Tsai, C. J., and Nussinov, R. (2000) Binding and folding: in search of intramolecular chaperone-like building block fragments Protein Eng. 13, 617-627
57. Chen, Z., Chen, X.-J., Xia, M., He, H.-W., Wang, S., Liu, H., Gong, H., and Yan, Y.-B. (2012) Chaperone-like effect of the linker on the isolated C-terminal domain of rabbit muscle creatine kinase Biophys. J. 103, 558-566
58. Zhang, W., Cai, H.-C., Li, F.-F., Xi, Y.-B., Ma, X., and Yan, Y.-B. (2011) The congenital cataract-linked G61C mutation destabilizes γD-crystallin and promotes non-native aggregation PLoS One 6, e20564
59. Xu, J., Wang, S., Zhao, W.-J., Xi, Y.-B., Yan, Y.-B., and Yao, K. (2012) The congenital cataract-linked A2V mutation impairs tetramer formation and promotes aggregation of βB2-crystallin PLoS One 7, e51200
60. Li, J., Zoldak, G., Kriehuber, T., Soroka, J., Schmid, F. X., Richter, K., and Buchner, J. (2013) Unique proline-rich domain regulates the chaperone function of AIPL1 Biochemistry 52, 2089-2096
61. Uversky, V. N. (2013) The most important thing is the tail: Multitudinous functionalities of intrinsically disordered protein termini FEBS Lett. 587, 1891-1901