Utilization of fluorescent chimeras for investigation of heterooligomeric complexes formed by human small heat shock proteins

Biochimie

Volumn 94, Issue 8, 2012, Pages 1794-1804

  Datskevich, Petr N ^a   Mymrikov, Evgeny V ^a   Gusev, Nikolai B ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Fluorescent proteins; Heterooligomeric complexes; Small heat shock proteins

Indexed keywords

ENHANCED CYAN FLUORESCENT PROTEIN; ENHANCED YELLOW FLUORESCENT PROTEIN; FLUORESCENT DYE; HEAT SHOCK PROTEIN B1; HEAT SHOCK PROTEIN B5; HEAT SHOCK PROTEIN B6; HEAT SHOCK PROTEIN B8; OLIGOMER; SMALL HEAT SHOCK PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; MOLECULAR WEIGHT; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; TEMPERATURE; WILD TYPE;

ALPHA-CRYSTALLIN B CHAIN; BACTERIAL PROTEINS; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEAT-SHOCK PROTEINS; HEAT-SHOCK PROTEINS, SMALL; HSP20 HEAT-SHOCK PROTEINS; HSP27 HEAT-SHOCK PROTEINS; HUMANS; LUMINESCENT PROTEINS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT FUSION PROTEINS;

EID: 84862855789     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2012.04.012     Document Type: Article

References (45)

1. H.S. McHaourab, J.A. Godar, P.L. Stewart, Structure and mechanism of protein stability sensors: chaperone activity of small heat shock proteins, Biochemistry 48 (2009) 3828-3837.
2. M.J. Vos, J. Hageman, S. Carra, H.H. Kampinga, Structural and functional diversities between members of the human HSPB, HSPH, HSPA, and DNAJ chaperone families, Biochemistry 47 (2008) 7001-7011.
3. G. Kappe, W.C. Boelens, W.W. de Jong, Why proteins without an alpha-crystallin domain should not be included in the human small heat shock protein family HSPB, Cell Stress Chaperones 15 (2010) 457-461.
4. E.V. Mymrikov, A.S. Seit-Nebi, N.B. Gusev, Large potentials of small heat shock proteins, Physiol. Rev. 91 (2011) 1123-1159.
5. E. Basha, H. O'Neill, E. Vierling, Small heat shock proteins and alpha-crystallins: dynamic proteins with flexible functions, Trends Biochem. Sci. 37 (2011) 106-117.
6. A.J. Baldwin, H. Lioe, C.V. Robinson, L.E. Kay, J.L. Benesch, AlphaB-crystallin polydispersity is a consequence of unbiased quaternary dynamics, J. Mol. Biol. 413 (2011) 297-309.
7. S. Jehle, B.S. Vollmar, B. Bardiaux, K.K. Dove, P. Rajagopal, T. Gonen, H. Oschkinat, R.E. Klevit, N-terminal domain of alphaB-crystallin provides a conformational switch for multimerization and structural heterogeneity, Proc. Natl. Acad. Sci. U.S.A. 108 (2011) 6409-6414.
8. J.M. Fontaine, J.S. Rest, M.J. Welsh, R. Benndorf, The sperm outer dense fiber protein is the 10th member of the superfamily of mammalian small stress proteins, Cell Stress Chaperones 8 (2003) 62-69.
9. G. Kappe, E. Franck, P. Verschuure, W.C. Boelens, J.A. Leunissen, W.W. de Jong, The human genome encodes 10 alpha-crystallin-related small heat shock proteins: HspB1-10, Cell Stress Chaperones 8 (2003) 53-61.
10. R.P. Taylor, I.J. Benjamin, Small heat shock proteins: a new classification scheme in mammals, J. Mol. Cell. Cardiol. 38 (2005) 433-444.
11. Y. Sugiyama, A. Suzuki, M. Kishikawa, R. Akutsu, T. Hirose, M.M. Waye, S.K. Tsui, S. Yoshida, S. Ohno, Muscle develops a specific form of small heat shock protein complex composed of MKBP/HSPB2 and HSPB3 during myogenic differentiation, J. Biol. Chem. 275 (2000) 1095-1104.
12. J. den Engelsman, S. Boros, P.Y. Dankers, B. Kamps, W.T. Vree Egberts, C.S. Bode, L.A. Lane, J.A. Aquilina, J.L. Benesch, C.V. Robinson, W.W. de Jong, W.C. Boelens, The small heat-shock proteins HSPB2 and HSPB3 form well-defined heterooligomers in a unique 3 to 1 subunit ratio, J. Mol. Biol. 393 (2009) 1022-1032.
13. J. Horwitz, Alpha-crystallin, Exp. Eye Res. 76 (2003) 145-153.
14. M.P. Bova, H.S. McHaourab, Y. Han, B.K. Fung, Subunit exchange of small heat shock proteins. Analysis of oligomer formation of alphaA-crystallin and Hsp27 by fluorescence resonance energy transfer and site-directed truncations, J. Biol. Chem. 275 (2000) 1035-1042.
15. A. Zantema, M. Verlaan-De Vries, D. Maasdam, S. Bol, A. van der Eb, Heat shock protein 27 and alpha B-crystallin can form a complex, which dissociates by heat shock, J. Biol. Chem. 267 (1992) 12936-12941.
16. F. Skouri-Panet, M. Michiel, C. Ferard, E. Duprat, S. Finet, Structural and functional specificity of small heat shock protein HspB1 and HspB4, two cellular partners of HspB5: role of the in vitro hetero-complex formation in chaperone activity, Biochimie 94 (2012) 975-984.
17. K. Kato, H. Shinohara, S. Goto, Y. Inaguma, R. Morishita, T. Asano, Copurification of small heat shock protein with alpha B crystallin from human skeletal muscle, J. Biol. Chem. 267 (1992) 7718-7725.
18. O.V. Bukach, A.S. Seit-Nebi, S.B. Marston, N.B. Gusev, Some properties of human small heat shock protein Hsp20 (HspB6), Eur. J. Biochem. 271 (2004) 291-302.
19. O.V. Bukach, A.E. Glukhova, A.S. Seit-Nebi, N.B. Gusev, Heterooligomeric complexes formed by human small heat shock proteins HspB1 (Hsp27) and HspB6 (Hsp20), Biochim. Biophys. Acta 1794 (2009) 486-495.
20. E.V. Mymrikov, A.S. Seit-Nebi, N.B. Gusev, Heterooligomeric complexes of human small heat shock proteins, Cell Stress Chaperones 17 (2012) 157-169.
21. X. Sun, J.M. Fontaine, J.S. Rest, E.A. Shelden, M.J. Welsh, R. Benndorf, Interaction of human HSP22 (HSPB8) with other small heat shock proteins, J. Biol. Chem. 279 (2004) 2394-2402.
22. J.M. Fontaine, X. Sun, R. Benndorf, M.J. Welsh, Interactions of HSP22 (HSPB8) with HSP20, alphaB-crystallin, and HSPB3, Biochem. Biophys. Res. Commun. 337 (2005) 1006-1011.
23. J.M. Fontaine, X. Sun, A.D. Hoppe, S. Simon, P. Vicart, M.J. Welsh, R. Benndorf, Abnormal small heat shock protein interactions involving neuropathy-associated HSP22 (HSPB8) mutants, FASEB J. 20 (2006) 2168-2170.
24. E.V. Mymrikov, O.V. Bukach, A.S. Seit-Nebi, N.B. Gusev, The pivotal role of the beta 7 strand in the intersubunit contacts of different human small heat shock proteins, Cell Stress Chaperones 15 (2010) 365-377.
25. P.N. Datskevich, E.V. Mymrikov, N.N. Sluchanko, A.A. Shemetov, M.V. Sudnitsyna, N.B. Gusev, Expression, purification and some properties of fluorescent chimeras of human small heat shock proteins, Protein Expr. Purif. (2011).
26. U.K. Laemmli, Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227 (1970) 680-685.
27. F.T. Chan, C.F. Kaminski, G.S. Kaminski Schierle, HomoFRET fluorescence anisotropy imaging as a tool to study molecular self-assembly in live cells, ChemPhysChem 12 (2011) 500-509.
28. D.S. Lidke, P. Nagy, B.G. Barisas, R. Heintzmann, J.N. Post, K.A. Lidke, A.H. Clayton, D.J. Arndt-Jovin, T.M. Jovin, Imaging molecular interactions in cells by dynamic and static fluorescence anisotropy (rFLIM and emFRET), Biochem. Soc. Trans. 31 (2003) 1020-1027.
29. T.J. van Ham, A. Esposito, J.R. Kumita, S.T. Hsu, G.S. Kaminski Schierle, C.F. Kaminski, C.M. Dobson, E.A. Nollen, C.W. Bertoncini, Towards multi-parametric fluorescent imaging of amyloid formation: studies of a YFP model of alpha-synuclein aggregation, J. Mol. Biol. 395 (2010) 627-642.
30. E. Galperin, V.V. Verkhusha, A. Sorkin, Three-chromophore FRET microscopy to analyze multiprotein interactions in living cells, Nat. Methods 1 (2004) 209-217.
31. M.P. Bova, L.L. Ding, J. Horwitz, B.K. Fung, Subunit exchange of alphaA-crystallin, J. Biol. Chem. 272 (1997) 29511-29517.
32. M.P. Bova, Q. Huang, L. Ding, J. Horwitz, Subunit exchange, conformational stability, and chaperone-like function of the small heat shock protein 16.5 from Methanococcus jannaschii, J. Biol. Chem. 277 (2002) 38468-38475.
33. N. Pasupuleti, M. Gangadhariah, S. Padmanabha, P. Santhoshkumar, R.H. Nagaraj, The role of the cysteine residue in the chaperone and anti-apoptotic functions of human Hsp27, J. Cell. Biochem. 110 (2010) 408-419.
34. N. Golenhofen, M.D. Perng, R.A. Quinlan, D. Drenckhahn, Comparison of the small heat shock proteins alphaB-crystallin, MKBP, HSP25, HSP20, and cvHSP in heart and skeletal muscle, Histochem. Cell Biol. 122 (2004) 415-425.
35. B.B. Kirbach, N. Golenhofen, Differential expression and induction of small heat shock proteins in rat brain and cultured hippocampal neurons, J. Neurosci. Res. 89 (2011) 162-175.
36. K. Kato, S. Goto, Y. Inaguma, K. Hasegawa, R. Morishita, T. Asano, Purification and characterization of a 20-kDa protein that is highly homologous to alpha B crystallin, J. Biol. Chem. 269 (1994) 15302-15309.
37. K. Sakuma, K. Watanabe, T. Totsuka, K. Kato, Pathological changes in levels of three small stress proteins, alphaB crystallin, HSP 27 and p20, in the hindlimb muscles of dy mouse, Biochim. Biophys. Acta 1406 (1998) 162-168.
38. G. Lutsch, R. Vetter, U. Offhauss, M. Wieske, H.J. Grone, R. Klemenz, I. Schimke, J. Stahl, R. Benndorf, Abundance and location of the small heat shock proteins HSP25 and alphaB-crystallin in rat and human heart, Circulation 96 (1997) 3466-3476.
39. M.V. Sudnitsyna, E.V. Mymrikov, A.S. Seit-Nebi, N.B. Gusev, The role of intrinsically disordered regions in the structure and functioning of small heat shock proteins, Curr. Protein Pept. Sci. 13 (2012) 76-85.
40. A.J. Baldwin, G.R. Hilton, H. Lioe, C. Bagneris, J.L. Benesch, L.E. Kay, Quaternary dynamics of alphaB-crystallin as a direct consequence of localised tertiary fluctuations in the C-terminus, J. Mol. Biol. 413 (2011) 310-320.
41. M.J. Borrelli, L.J. Bernock, J. Landry, D.R. Spitz, L.A. Weber, E. Hickey, M.L. Freeman, P.M. Corry, Stress protection by a fluorescent Hsp27 chimera that is independent of nuclear translocation or multimeric dissociation, Cell Stress Chaperon. 7 (2002) 281-296.
42. B.M. Doshi, L.E. Hightower, J. Lee, The role of Hsp27 and actin in the regulation of movement in human cancer cells responding to heat shock, Cell Stress Chaperon. 14 (2009) 445-457.
43. R. Benndorf, X. Sun, R.R. Gilmont, K.J. Biederman, M.P. Molloy, C.W. Goodmurphy, H. Cheng, P.C. Andrews, M.J. Welsh, HSP22, a new member of the small heat shock protein superfamily, interacts with mimic of phosphorylated HSP27 ((3D)HSP27), J. Biol. Chem. 276 (2001) 26753-26761.
44. M.J. Vos, M.P. Zijlstra, S. Carra, O.C. Sibon, H.H. Kampinga, Small heat shock proteins, protein degradation and protein aggregation diseases, Autophagy 7 (2011) 101-103.
45. F. Sobott, J.L. Benesch, E. Vierling, C.V. Robinson, Subunit exchange of multi-meric protein complexes. Real-time monitoring of subunit exchange between small heat shock proteins by using electrospray mass spectrometry, J. Biol. Chem. 277 (2002) 38921-38929.