Characterization of mutants of human small heat shock protein HspB1 carrying replacements in the N-terminal domain and associated with hereditary motor neuron diseases

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Muranova, Lydia K ^a   Weeks, Stephen D ^b   Strelkov, Sergei V ^b   Gusev, Nikolai B ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b DEPARTMENT OF PHARMACEUTICAL AND PHARMACOLOGICAL SCIENCES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN B6; INSULIN; LYSOZYME; MALATE DEHYDROGENASE; OLIGOMER; UNCLASSIFIED DRUG; HEAT SHOCK PROTEIN 20; HSPB1 PROTEIN, HUMAN; HSPB6 PROTEIN, HUMAN; PROTEIN BINDING;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; DISSOCIATION; FLUORESCENCE; IN VITRO STUDY; LOW TEMPERATURE; MOLECULAR INTERACTION; MOLECULAR WEIGHT; MOTOR NEURON DISEASE; MUTATIONAL ANALYSIS; PHYSICAL CHEMISTRY; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STABILITY; THERMOSTABILITY; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOTONEURON; MUSCULAR ATROPHY, SPINAL; MUTATION; PATHOLOGY; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; PROTEINOSIS;

HSP20 HEAT-SHOCK PROTEINS; HSP27 HEAT-SHOCK PROTEINS; HUMANS; MOLECULAR CHAPERONES; MOTOR NEURONS; MUSCULAR ATROPHY, SPINAL; MUTATION; PHOSPHORYLATION; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEOLYSIS;

EID: 84930647179     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126248     Document Type: Article

References (59)

1. Maaroufi H, Tanguay RM. Analysis and phylogeny of small heat shock proteins from marine viruses and their cyanobacteria host. PLoS ONE. 2013; 8(11):e81207. doi: 10.1371/journal.pone.0081207 PMID: 24265841; PubMed Central PMCID: PMC3827213.
2. Basha E, O 'Neill H, Vierling E. Small heat shock proteins and alpha-crystallins: dynamic proteins with flexible functions. Trends Biochem Sci. 2012; 37(3):106-17. S0968-0004(11)00190-3. PMID: 22177323. doi: 10.1016/j.tibs.2011.11.005
3. Mymrikov EV, Seit-Nebi AS, Gusev NB. Large potentials of small heat shock proteins. Physiol Rev. 2011; 91(4):1123-59. 91/4/1123. PMID: 22013208. doi: 10.1152/physrev.00023.2010
4. Treweek TM, Meehan S, Ecroyd H, Carver JA. Small heat-shock proteins: important players in regulating cellular proteostasis. Cell Mol Life Sci. 2015; 72(3):429-451. doi: 10.1007/s00018-014-1754-5 PMID: 25352169.
5. Kappe G, Boelens WC, de Jong WW. Why proteins without an alpha-crystallin domain should not be included in the human small heat shock protein family HSPB. Cell Stress Chaperones. 2010; 15(4):457-61. doi: 10.1007/s12192-009-0155-4 PMID: 19921466.
6. Bagneris C, Bateman OA, Naylor CE, Cronin N, Boelens WC, Keep NH, et al. Crystal structures of alpha-crystallin domain dimers of alphaB-crystallin and Hsp20. J Mol Biol. 2009; 392(5):1242-52. S0022-2836(09)00936-X. PMID: 19646995. doi: 10.1016/j.jmb.2009.07.069
7. Laganowsky A, Benesch JL, Landau M, Ding L, Sawaya MR, Cascio D, et al. Crystal structures of truncated alphaA and alphaB crystallins reveal structural mechanisms of polydispersity important for eye lens function. Protein Sci. 2010; 19(5):1031-43. doi: 10.1002/pro.380 PMID: 20440841; PubMed Central PMCID: PMC2868245.
8. Baranova EV, Weeks SD, Beelen S, Bukach OV, Gusev NB, Strelkov SV. Three-dimensional structure of alpha-crystallin domain dimers of human small heat shock proteins HSPB1 and HSPB6. J Mol Biol. 2011; 411(1):110-22. S0022-2836(11)00574-2. PMID: 21641913. doi: 10.1016/j.jmb.2011.05.024
9. Delbecq SP, Jehle S, Klevit R. Binding determinants of the small heat shock protein, alphaB-crystallin: recognition of the 'IxI' motif. EMBO J. 2012; 31(24):4587-94. emboj2012318. PMID: 23188086; PubMed Central PMCID: PMC3545294. doi: 10.1038/emboj.2012.318
10. Hilton GR, Lioe H, Stengel F, Baldwin AJ, Benesch JL. Small Heat-Shock Proteins: Paramedics of the Cell. Top Curr Chem. 2013; 328:69-98. doi: 10.1007/128-2012-324 PMID: 22576357.
11. Hochberg GK, Benesch JL. Dynamical structure of alphaB-crystallin. Prog Biophys Mol Biol. 2014; 115(1):11-20. doi: 10.1016/j.pbiomolbio.2014.03.003 PMID: 24674783.
12. Jehle S, Vollmar BS, Bardiaux B, Dove KK, Rajagopal P, Gonen T, et al. N-terminal domain of alphaB-crystallin provides a conformational switch for multimerization and structural heterogeneity. Proc Natl Acad Sci U S A. 2011; 108(16):6409-14. doi: 1014656108 PMID: 21464278; PubMed Central PMCID: PMC3081008.
13. Kappe G, Franck E, Verschuure P, Boelens WC, Leunissen JA, de Jong WW. The human genome encodes 10 alpha-crystallin-related small heat shock proteins: HspB1-10. Cell Stress Chaperones. 2003; 8(1):53-61. PMID: 12820654; PubMed Central PMCID: PMC514853.
14. th member of the superfamily of mammalian small stress proteins. Cell Stress Chaperones. 2003; 8(1):62-9. PMID: 12820655; PubMed Central PMCID: PMC514854.
15. Taylor RP, Benjamin IJ. Small heat shock proteins: a new classification scheme in mammals. J Mol Cell Cardiol. 2005; 38(3):433-44. S0022-2828(05)00003-9. PMID: 15733903.
16. McHaourab HS, Godar JA, Stewart PL. Structure and mechanism of protein stability sensors: chaperone activity of small heat shock proteins. Biochemistry. 2009; 48(18):3828-37. doi: 10.1021/bi900212j PMID: 19323523; PubMed Central PMCID: PMC2785012.
17. Cox D, Carver JA, Ecroyd H. Preventing alpha-synuclein aggregation: the role of the small heat-shock molecular chaperone proteins. Biochim Biophys Acta. 2014; 1842(9):1830-43. doi: 10.1016/j.bbadis.2014.06.024 PMID: 24973551.
18. Carra S, Crippa V, Rusmini P, Boncoraglio A, Minoia M, Giorgetti E, et al. Alteration of protein folding and degradation in motor neuron diseases: Implications and protective functions of small heat shock proteins. Prog Neurobiol. 2012; 97(2):83-100. S0301-0082(11)00176-6. PMID: 21971574. doi: 10.1016/j.pneurobio.2011.09.009
19. Arrigo AP. Human small heat shock proteins: protein interactomes of homo- and hetero-oligomeric complexes: an update. FEBS Lett. 2013; 587(13):1959-69. S0014-5793(13)00353-0. PMID: 23684648. doi: 10.1016/j.febslet.2013.05.011
20. Acunzo J, Katsogiannou M, Rocchi P. Small heat shock proteins HSP27 (HspB1), alphaB-crystallin (HspB5) and HSP22 (HspB8) as regulators of cell death. Int J Biochem Cell Biol. 2012; 44(10):1622-31. S1357-2725(12)00126-4. PMID: 22521623. doi: 10.1016/j.biocel.2012.04.002
21. Paul C, Simon S, Gibert B, Virot S, Manero F, Arrigo AP. Dynamic processes that reflect anti-apoptotic strategies set up by HspB1 (Hsp27). Exp Cell Res. 2010; 316(9):1535-52. S0014-4827(10)00113-8. PMID: 20233592. doi: 10.1016/j.yexcr.2010.03.006
22. Yang C, Trent S, Ionescu-Tiba V, Lan L, Shioda T, Sgroi D, et al. Identification of cyclin D1- and estrogen-regulated genes contributing to breast carcinogenesis and progression. Cancer Res. 2006; 66(24):11649-58. 66/24/11649. PMID: 17178859.
23. Wettstein G, Bellaye PS, Micheau O, Bonniaud P. Small heat shock proteins and the cytoskeleton: An essential interplay for cell integrity? Int J Biochem Cell Biol. 2012; 44(10):1680-6. S1357-2725(12)00190-2. PMID: 22683760. doi: 10.1016/j.biocel.2012.05.024
24. Elliott JL, Der Perng M, Prescott AR, Jansen KA, Koenderink GH, Quinlan RA. The specificity of the interaction between alphaB-crystallin and desmin filaments and its impact on filament aggregation and cell viability. Philos Trans R Soc Lond B Biol Sci. 2013; 368(1617):20120375. rstb.2012.0375. PMID: 23530264. doi: 10.1098/rstb.2012.0375
25. Datskevich PN, Nefedova VV, Sudnitsyna MV, Gusev NB. Mutations of small heat shock proteins and human congenital diseases. Biochemistry. 2012; 77(13):1500-14. BCM77130203. PMID: 23379525. doi: 10.1134/S0006297912130081
26. Benndorf R, Martin JL, Kosakovsky Pond SL, Wertheim JO. Neuropathy- and myopathy-associated mutations in human small heat shock proteins: Characteristics and evolutionary history of the mutation sites. Mutat Res. 2014. doi: 10.1016/j.mrrev.2014.02.004 PMID: 24607769.
27. Evgrafov OV, Mersiyanova I, Irobi J, Van Den Bosch L, Dierick I, Leung CL, et al. Mutant small heat-shock protein 27 causes axonal Charcot-Marie-Tooth disease and distal hereditary motor neuropathy. Nat Genet. 2004; 36(6):602-6. doi: 10.1038/ng1354 PMID: 15122254.
28. Almeida-Souza L, Goethals S, de Winter V, Dierick I, Gallardo R, Van Durme J, et al. Increased monomerization of mutant HSPB1 leads to protein hyperactivity in Charcot-Marie-Tooth neuropathy. J Biol Chem. 2010; 285(17):12778-86. M109.082644. PMID: 20178975; PubMed Central PMCID: PMC2857091. doi: 10.1074/jbc.M109.082644
29. Nefedova VV, Datskevich PN, Sudnitsyna MV, Strelkov SV, Gusev NB. Physico-chemical properties of R140G and K141Q mutants of human small heat shock protein HspB1 associated with hereditary peripheral neuropathies. Biochimie. 2013; 95(8):1582-92. doi: 10.1016/j.biochi.2013.04.014 PMID: 23643870.
30. Nefedova VV, Sudnitsyna MV, Strelkov SV, Gusev NB. Structure and properties of G84R and L99M mutants of human small heat shock protein HspB1 correlating with motor neuropathy. Arch Biochem Biophys. 2013; 538(1):16-24. doi: 10.1016/j.abb.2013.07.028 PMID: 23948568.
31. Chalova AS, Sudnitsyna MV, Strelkov SV, Gusev NB. Characterization of human small heat shock protein HspB1 that carries C-terminal domain mutations associated with hereditary motor neuron diseases. Biochim Biophys Acta. 2014; 1844(12):2116-26. doi: 10.1016/j.bbapap.2014.09.005 PMID: 25220807.
32. Houlden H, Laura M, Wavrant-De Vrieze F, Blake J, Wood N, Reilly MM. Mutations in the HSP27 (HSPB1) gene cause dominant, recessive, and sporadic distal HMN/CMT type 2. Neurology. 2008; 71(21):1660-8. 01.wnl.0000319696.14225.67. PMID: 18832141. doi: 10.1212/01.wnl.0000319696.14225.67
33. Capponi S, Geroldi A, Fossa P, Grandis M, Ciotti P, Gulli R, et al. HSPB1 and HSPB8 in inherited neuropathies: study of an Italian cohort of dHMN and CMT2 patients. J Peripher Nerv Syst. 2011; 16(4):287-94. doi: 10.1111/j.1529-8027.2011.00361.x PMID: 22176143.
34. Bukach OV, Seit-Nebi AS, Marston SB, Gusev NB. Some properties of human small heat shock protein Hsp20 (HspB6). Eur J Biochem. 2004; 271(2):291-302. 3928. PMID: 14717697.
35. Datskevich PN, Mymrikov EV, Sluchanko NN, Shemetov AA, Sudnitsyna MV, Gusev NB. Expression, purification and some properties of fluorescent chimeras of human small heat shock proteins. Protein Expr Purif. 2012; 82(1):45-54. S1046-5928(11)00313-5. PMID: 22100527. doi: 10.1016/j.pep.2011.11.004
36. Mymrikov EV, Bukach OV, Seit-Nebi AS, Gusev NB. The pivotal role of the beta 7 strand in the intersubunit contacts of different human small heat shock proteins. Cell Stress Chaperones. 2010; 15(4):365-77. doi: 10.1007/s12192-009-0151-8 PMID: 19856132.
37. Medvedeva MV, Bushueva TL, Shirinsky VP, Lukas TJ, Watterson DM, Gusev NB. Interaction of smooth muscle caldesmon with calmodulin mutants. FEBS Lett. 1995; 360(1):89-92. 0014-5793(95)00058-H. PMID: 7875308.
38. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259):680-5. PMID: 5432063.
39. Perrie WT, Perry SV. An electrophoretic study of the low-molecular-weight components of myosin. Biochem J. 1970; 119(1):31-8. PMID: 5485752; PubMed Central PMCID: PMC1179315.
40. Hayes D, Napoli V, Mazurkie A, Stafford WF, Graceffa P. Phosphorylation dependence of hsp27 multimeric size and molecular chaperone function. J Biol Chem. 2009; 284(28):18801-7. doi: M109.011353 PMID: 19411251; PubMed Central PMCID: PMC2707219.
41. Ehrnsperger M, Lilie H, Gaestel M, Buchner J. The dynamics of Hsp25 quaternary structure. Structure and function of different oligomeric species. J Biol Chem. 1999; 274(21):14867-74. PMID: 10329686.
42. Chalova AS, Sudnitsyna MV, Semenyuk PI, Orlov VN, Gusev NB. Effect of disulfide crosslinking on thermal transitions and chaperone-like activity of human small heat shock protein HspB1. Cell Stress Chaperones. 2014; 19(6):963-72. doi: 10.1007/s12192-014-0520-9 PMID: 24898092.
43. Stokoe D, Engel K, Campbell DG, Cohen P, Gaestel M. Identification of MAPKAP kinase 2 as a major enzyme responsible for the phosphorylation of the small mammalian heat shock proteins. FEBS Lett. 1992; 313(3):307-13. 0014-5793(92)81216-9. PMID: 1332886.
44. Rogalla T, Ehrnsperger M, Preville X, Kotlyarov A, Lutsch G, Ducasse C, et al. Regulation of Hsp27 oligomerization, chaperone function, and protective activity against oxidative stress/tumor necrosis factor alpha by phosphorylation. J Biol Chem. 1999; 274(27):18947-56. PMID: 10383393.
45. Bukach OV, Glukhova AE, Seit-Nebi AS, Gusev NB. Heterooligomeric complexes formed by human small heat shock proteins HspB1 (Hsp27) and HspB6 (Hsp20). Biochim Biophys Acta. 2009; 1794(3):486-95. S1570-9639(08)00372-5. PMID: 19100870. doi: 10.1016/j.bbapap.2008.11.010
46. Haslbeck M, Vierling E. A First Line of Stress Defense: Small Heat Shock Proteins and Their Function in Protein Homeostasis. J Mol Biol. 2015; 427(7):1537-48. doi: 10.1016/j.jmb.2015.02.002 PMID: 25681016.
47. Treweek TM, Meehan S, Ecroyd H, Carver JA. Small heat-shock proteins: important players in regulating cellular proteostasis. Cell Mol Life Sci. 2015; 72(3):429-51. doi: 10.1007/s00018-014-1754-5 PMID: 25352169.
48. Weeks SD, Baranova EV, Heirbaut M, Beelen S, Shkumatov AV, Gusev NB, et al. Molecular structure and dynamics of the dimeric human small heat shock protein HSPB6. J Struct Biol. 2014; 185(3):342-54. doi: 10.1016/j.jsb.2013.12.009 PMID: 24382496.
49. McDonald ET, Bortolus M, Koteiche HA, McHaourab HS. Sequence, structure, and dynamic determinants of Hsp27 (HspB1) equilibrium dissociation are encoded by the N-terminal domain. Biochemistry. 2012; 51(6):1257-68. doi: 10.1021/bi2017624 PMID: 22264079; PubMed Central PMCID: PMC3293247.
50. Ghosh JG, Estrada MR, Clark JI. Interactive domains for chaperone activity in the small heat shock protein, human alphaB crystallin. Biochemistry. 2005; 44(45):14854-69. doi: 10.1021/bi0503910 PMID: 16274233.
51. Heirbaut M, Beelen S, Strelkov SV, Weeks SD. Dissecting the functional role of the N-terminal domain of the human small heat shock protein HSPB6. PLoS ONE. 2014; 9(8):e105892. doi: 10.1371/journal.pone.0105892 PMID: 25157403; PubMed Central PMCID: PMC4144951.
52. Theriault JR, Lambert H, Chavez-Zobel AT, Charest G, Lavigne P, Landry J. Essential role of the NH2-terminal WD/EPF motif in the phosphorylation-activated protective function of mammalian Hsp27. J Biol Chem. 2004; 279(22):23463-71. doi: 10.1074/jbc.M402325200 PMID: 15033973.
53. Kelley PB, Abraham EC. Thermally induced disintegration of the oligomeric structure of alphaB-crystallin mutant F28S is associated with diminished chaperone activity. Mol Cell Biochem. 2003; 252(1-2):273-8. PMID: 14577602.
54. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004; 32(5):1792-7. doi: 10.1093/nar/gkh340 PMID: 15034147; PubMed Central PMCID: PMC390337.
55. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics. 2009; 25(9):1189-91. doi: 10.1093/bioinformatics/btp033 PMID: 19151095; PubMed Central PMCID: PMC2672624.
56. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res. 2004; 14(6):1188-90. doi: 10.1101/gr.849004 PMID: 15173120; PubMed Central PMCID: PMC419797.
57. Ghosh JG, Shenoy AK Jr., Clark JI. N- and C-Terminal motifs in human alphaB crystallin play an important role in the recognition, selection, and solubilization of substrates. Biochemistry. 2006; 45(46):13847-54. doi: 10.1021/bi061471m PMID: 17105203.
58. Shi J, Koteiche HA, McHaourab HS, Stewart PL. Cryoelectron microscopy and EPR analysis of engineered symmetric and polydisperse Hsp16.5 assemblies reveals determinants of polydispersity and substrate binding. J Biol Chem. 2006; 281(52):40420-8. M608322200. PMID: 17079234.
59. Mymrikov EV, Seit-Nebi AS, Gusev NB. Heterooligomeric complexes of human small heat shock proteins. Cell Stress Chaperones. 2012; 17(2):157-69. doi: 10.1007/s12192-011-0296-0 PMID: 22002549.