Functional validation of hydrophobic adaptation to physiological temperature in the small heat shock protein αA-crystallin

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Posner, Mason ^a   Kiss, Andor J ^b   Skiba, Jackie ^a   Drossman, Amy ^a   Dolinska, Monika B ^c   Hejtmancik, J Fielding ^c   Sergeev, Yuri V ^c  

^a ASHLAND UNIVERSITY   (United States)

^b MIAMI UNIVERSITY   (United States)

^c NATIONAL EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CRYSTALLIN; SMALL HEAT SHOCK PROTEIN; RECOMBINANT PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CIRCULAR DICHROISM; COLD ACCLIMATIZATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYPRINODON; DANIO; DISSOSTICHUS; ENZYME ACTIVITY; GENETIC VARIABILITY; HEAT ACCLIMATIZATION; HOMEOSTASIS; HYDROPHOBICITY; NONHUMAN; NOTOTHENIA; NUCLEOTIDE SEQUENCE; ONCORHYNCHUS; PHYSICAL CHEMISTRY; PIMEPHALES; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN MODIFICATION; PROTEIN STABILITY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; TELEOST; TEMPERATURE ACCLIMATIZATION; THERMOSTABILITY; VALIDATION PROCESS; ACCLIMATIZATION; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; FISH; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN CONFORMATION;

DANIO RERIO; TELEOSTEI;

ACCLIMATIZATION; ALPHA-CRYSTALLIN A CHAIN; AMINO ACID SEQUENCE; ANIMALS; FISHES; HEAT-SHOCK PROTEINS, SMALL; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; PROTEIN STABILITY; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT;

EID: 84859095792     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034438     Document Type: Article

References (74)

1. Eyles SJ, Gierasch LM, (2010) Nature's molecular sponges: small heat shock proteins grow into their chaperone roles. Proc Natl Acad Sci USA 107: 2727-2728.
2. Horwitz J, (1992) α-crystallin can function as a molecular chaperone. Proc Natl Acad Sci USA 89: 10449-10453.
3. Sun Y, Macrae TH, (2005) Small heat shock proteins: molecular structure and chaperone function. Cell Mol Life Sci 62: 2460-2476.
4. Bhat SP, Hale IL, Matsumoto B, Elghanayan D, (1999) Ectopic expression of alpha B-crystallin in Chinese hamster ovary cells suggests a nuclear role for this protein. Eur J Cell Biol 78: 143-150.
5. Gangalum RK, Bhat SP, (2009) AlphaB-crystallin: a Golgi-associated membrane protein in the developing ocular lens. Invest Ophthalmol Vis Sci 50: 3283-3290.
6. Iwaki T, Kume-Iwaki A, Liem RKH, Goldman JE, (1989) αB-crystallin is expressed in non-lenticular tissues and accumulates in Alexander's disease brain. Cell 57: 71-78.
7. Ousman SS, Tomooka BH, van Noort JM, Wawrousek EF, O'Connor KC, et al. (2007) Protective and therapeutic role for alphaB-crystallin in autoimmune demyelination. Nature 448: 474-479.
8. Stegh AH, Kesari S, Mahoney JE, Jenq HT, Forloney KL, et al. (2008) Bcl2L12-mediated inhibition of effector caspase-3 and caspase-7 via distinct mechanisms in glioblastoma. Proc Natl Acad Sci USA 105: 10703-10708.
9. Vicart P, Caron A, Guicheney P, Li Z, Prevost MC, et al. (1998) A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nat Genet 20: 92-95.
10. Bhat SP, Nagineni CN, (1989) αB subunit of lens-specific protein alpha-crystallin is present in other ocular and non-ocular tissues. Biochem Biophys Res Commun 158: 319-325.
11. Dubin RA, Wawrousek EF, Piatigorsky J, (1989) Expression of the murine αB-crystallin is not restricted to the lens. Mol Cell Bio 9: 1083-1091.
12. Klemenz R, Frohli E, Steiger RH, Schafer R, Aoyamo A, (1991) αB-crystallin is a small heat shock protein. Proc Natl Acad Sci USA 88: 3652-3656.
13. Horwitz J, (2009) Alpha crystallin: the quest for a homogeneous quaternary structure. Exp Eye Res 88: 190-194.
14. Jaya N, Garcia V, Vierling E, (2009) Substrate binding site flexibility of the small heat shock protein molecular chaperones. Proc Natl Acad Sci USA 106: 15604-15609.
15. Mchaourab HS, Dodson EK, Koteiche HA, (2002) Mechanism of chaperone function in small heat shock proteins. Two-mode binding of the excited states of T4 lysozyme mutants by alphaA-crystallin. J Biol Chem 277: 40557-40566.
16. McHaourab HS, Godar JA, Stewart PL, (2009) Structure and mechanism of protein stability sensors: chaperone activity of small heat shock proteins. Biochemistry 48: 3828-3837.
17. Stengel F, Baldwin AJ, Painter AJ, Jaya N, Basha E, et al. (2010) Quaternary dynamics and plasticity underlie small heat shock protein chaperone function. Proc Natl Acad Sci USA 107: 2007-2012.
18. Derham BK, van Boekel MA, Muchowski PJ, Clark JI, Horwitz J, et al. (2001) Chaperone function of mutant versions of alpha A- and alpha B-crystallin prepared to pinpoint chaperone binding sites. Eur J Biochem 268: 713-721.
19. Treweek TM, Ecroyd H, Williams DM, Meehan S, Carver JA, et al. (2007) Site-directed mutations in the C-terminal extension of human alphaB-crystallin affect chaperone function and block amyloid fibril formation. PLoS ONE 2: e1046.
20. Ghosh JG, Houck SA, Clark JI, (2007) Interactive sequences in the stress protein and molecular chaperone human alphaB crystallin recognize and modulate the assembly of filaments. Int J Biochem Cell Biol 39: 1804-1815.
21. Bova MP, Ding L-L, Horwitz J, Fung BK-K, (1997) Subunit exchange of αA-crystallin. J Biol Chem 272: 29511-29517.
22. Aquilina JA, Benesch JL, Ding LL, Yaron O, Horwitz J, et al. (2005) Subunit exchange of polydisperse proteins: mass spectrometry reveals consequences of alphaA-crystallin truncation. J Biol Chem 280: 14485-14491.
23. Benesch JLP, Ayoub M, Robinson CV, Aquilina JA, (2008) Small heat shock protein activity is regulated by variable oligomeric substructure. J Biol Chem 283: 28513-28517.
24. Reddy GB, Kumar PA, Kumar MS, (2006) Chaperone-like activity and hydrophobicity of alpha-crystallin. IUBMB Life 58: 632-641.
25. Kumar MS, Kapoor M, Sinha S, Reddy GB, (2005) Insights into Hydrophobicity and the Chaperone-like Function of {alpha}A- and {alpha}B-crystallins: an isothermal titration calorimetric study. J Biol Chem 280: 21726-21730.
26. Liang JJ-N, Sun T-X, Akhtar NJ, (2000) Heat induced conformational change of human lens recombinant αA- and αB-crystallins. Mol Vis 6: 10-14.
27. Reddy GB, Das KP, Petrash JM, Surewicz WK, (2000) Temperature-dependent chaperone activity and structural properties of human alphaA- and alphaB-crystallins. J Biol Chem 275: 4565-4570.
28. McFall-Ngai M, Horwitz J, (1990) A comparative study of the thermal stability of the vertebrate eye lens: antarctic ice fish to the desert iguana. Exp Eye Res 50: 703-709.
29. Posner M, Kantorow M, Horwitz J, (1999) Cloning, sequencing and differential expression of αB-crystallin in the zebrafish, Danio rerio. Biochimica et Biophysica Acta 1447: 271-277.
30. Smith AA, Wyatt K, Vacha J, Vihtelic TS, Zigler JS Jr, et al. (2006) Gene duplication and separation of functions in alphaB-crystallin from zebrafish (Danio rerio). Febs J 273: 481-490.
31. Dahlman JM, Margot KL, Ding L, Horwitz J, Posner M, (2005) Zebrafish alpha-crystallins: protein structure and chaperone-like activity compared to their mammalian orthologs. Mol Vis 11: 88-96.
32. Runkle S, Hill J, Kantorow M, Horwitz J, Posner M, (2002) Sequence and spatial expression of zebrafish (Danio rerio) alphaA-crystallin. Mol Vis 8: 45-50.
33. Posner M, Hawke M, Lacava C, Prince CJ, Bellanco NR, et al. (2008) A proteome map of the zebrafish (Danio rerio) lens reveals similarities between zebrafish and mammalian crystallin expression. Mol Vis 14: 806-814.
34. Kiss AJ, Mirarefi AY, Ramakrishnan S, Zukoski CF, Devries AL, et al. (2004) Cold-stable eye lens crystallins of the Antarctic nototheniid toothfish Dissostichus mawsoni Norman. J Exp Biol 207: 4633-4649.
35. Reddy GB, Das KP, Petrash JM, Surewicz WK, (2000) Temperature-dependent chaperone activity and structural properties of human αA- and αB-crystallins. J Biol Chem 275: 4565-4570.
36. Bagnéris C, Bateman OA, Naylor CE, Cronin N, Boelens WC, et al. (2009) Crystal structures of alpha-crystallin domain dimers of alphaB-crystallin and Hsp20. J Mol Biol 392: 1242-1252.
37. Laganowsky A, Benesch JLP, Landau M, Ding L, Sawaya MR, et al. (2010) Crystal structures of truncated alphaA and alphaB crystallins reveal structural mechanisms of polydispersity important for eye lens function. Protein Sci 19: 1031-1043.
38. Laganowsky A, Eisenberg D, (2010) Non-3D domain swapped crystal structure of truncated zebrafish alphaA crystallin. Protein Sci 19: 1978-1984.
39. Jaenicke R, (2000) Do ultrastable proteins from hyperthermophiles have high or low conformational rigidity? Proc Natl Acad Sci USA 97: 2962-2964.
40. Schrank TP, Bolen DW, Hilser VJ, (2009) Rational modulation of conformational fluctuations in adenylate kinase reveals a local unfolding mechanism for allostery and functional adaptation in proteins. Proc Natl Acad Sci USA 106: 16984-16989.
41. Hayes VH, Devlin G, Quinlan RA, (2008) Truncation of alphaB-crystallin by the myopathy-causing Q151X mutation significantly destabilizes the protein leading to aggregate formation in transfected cells. J Biol Chem 283: 10500-10512.
42. Campbell KL, Roberts JEE, Watson LN, Stetefeld J, Sloan AM, et al. (2010) Substitutions in woolly mammoth hemoglobin confer biochemical properties adaptive for cold tolerance. Nat Genet 42: 536-540.
43. Pauling L, Itano Ha, (1949) Sickle cell anemia a molecular disease. 110: 543-548 Science (New York, NY).
44. Geffeney SL, Fujimoto E, Brodie ED, Ruben PC, (2005) Evolutionary diversification of TTX-resistant sodium channels in a predator-prey interaction. Nature 434: 759-763.
45. Graves JE, Somero GN, (1982) Electrophoretic and functional enzymic evolution in four species of eastern Pacific barracudas from different thermal environments. Evolution 36: 97-106.
46. Holland LZ, McFall-Ngai MJ, Somero GN, (1997) Evolution of lactate dehydrogenase-A homologs of barracuda fishes (genus Sphyraena) from different thermal environments: differences in kinetic properties and thermal stability are due to amino acid substitutions outside the active site. Biochemistry 36: 3207-3215.
47. Dong Y, Somero GN, (2009) Temperature adaptation of cytosolic malate dehydrogenases of limpets (genus Lottia): differences in stability and function due to minor changes in sequence correlate with biogeographic and vertical distributions. J Exp Biol 212: 169-177.
48. Hochachka PW, Somero GN, (2002) Biochemical Adaptation: Mechanism and Process in Physiological Evolution: Oxford University Press.
49. Eifert C, Burgio MR, Bennett PM, Salerno JC, Koretz JF, (2005) N-terminal control of small heat shock protein oligomerization: changes in aggregate size and chaperone-like function. Biochim Biophys Acta 1748: 146-156.
50. Cheng C, Xia C-h, Huang Q, Ding L, Horwitz J, et al. (2010) Altered chaperone-like activity of alpha-crystallins promotes cataractogenesis. J Biol Chem 285: 41187-41193.
51. Kiss AJ, Cheng C, (2008) Molecular diversity and genomic organisation of the α, β and γ eye lens crystallins from the Antarctic toothfish Dissostichus mawsoni. Comp Biochem Physiol Part D 3: 155-171.
52. Horwitz J, Huang QL, Ding L, Bova MP, (1998) Lens alpha-crystallin: chaperone-like properties. Methods in Enzymology 290: 365-383.
53. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673-4680.
54. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.
55. Needleman SB, Wunsch CD, (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Bio 48: 443-453.
56. Lee C, (1994) Predicting protein mutant energetics by self-consistent ensemble optimization. J Mol Bio 236: 918-939.
57. Lee C, Subbiah S, (1991) Prediction of protein side-chain conformation by packing optimization. J Mol Bio 217: 373-388.
58. Letunic I, Doerks T, Bork P, (2009) SMART 6: recent updates and new developments. Nucleic Acids Res 37: D229-D232.
59. Schultz J, Milpetz F, Bork P, Ponting CP, (1998) SMART, a simple modular architecture research tool: identification of signaling domains. ProcNatlAcadSciUSA 95: 5857-5864.
60. Levitt M, (1992) Accurate modeling of protein conformation by automatic segment matching. J Mol Bio 226: 507-533.
61. Laskowski RA, MacArthur MW, Moss DS, Thornton JM, (1993) PROCHECK: a program to check the stereochemical quality of protein structures. JApplCryst 26: 283-291.
62. Schymkowitz J, Borg J, Stricher F, Nys R, Rousseau F, et al. (2005) The FoldX web server: an online force field. Nucleic Acids Res 33: W382-388.
63. Schymkowitz JWH, Rousseau F, Martins IC, Ferkinghoff-Borg J, Stricher F, et al. (2005) Prediction of water and metal binding sites and their affinities by using the Fold-X force field. Proc Natl Acad Sci USA 102: 10147-10152.
64. Hall BarryG, (2004) Phylogenetic trees made easy: a how-to manual.
65. Waddell PJ, Steel MA, (1997) General time-reversible distances with unequal rates across sites: mixing gamma and inverse Gaussian distributions with invariant sites. Mol Phylogenet Evol 8: 398-414.
66. Nylander JAA, (2004) MrModeltest. Program distributed by the author, Evolutionary Biology Centre, Uppsala University.
67. Woolley S, Johnson J, Smith MJ, Crandall KA, McClellan DA, (2003) TreeSAAP: selection on amino acid properties using phylogenetic trees. Bioinformatics 19: 671-672.
68. Yang Z, (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555-556.
69. Yang Z, (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.
70. McClellan DA, Palfreyman EJ, Smith MJ, Moss JL, Christensen RG, et al. (2005) Physicochemical evolution and molecular adaptation of the cetacean and artiodactyl cytochrome b proteins. Mol Biol Evol 22: 437-455.
71. Abgar S, Backmann J, Aerts T, Vanhoudt J, Clauwaert J, (2000) The structural differences between bovine lens alphaA- and alphaB- crystallin. Eur J Biochem 267: 5916-5925.
72. Gangadhariah MH, Wang B, Linetsky M, Henning C, Spanneberg R, et al. (2010) Hydroimidazolone modification of human [alpha]A-crystallin: Effect on the chaperone function and protein refolding ability. Biochimica et Biophysica Acta (BBA)- Molecular Basis of Disease 1802: 432-441.
73. Kumar MS, Kapoor M, Sinha S, Reddy GB, (2005) Insights into hydrophobicity and the chaperone-like function of alphaA- and alphaB-crystallins: an isothermal titration calorimetric study. J Biol Chem 280: 21726-21730.
74. Woolley S, Johnson J, Smith Matthew J, Crandall Keith A, McClellan David A, (2003) TreeSAAP: selection on amino acid properties using phylogenetic trees. Bioinformatics 19: 671-672.