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TIP Revista Especializada en Ciencias Químico-Biológicas

2020, Number 1

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TIP Rev Esp Cienc Quim Biol 2020; 23 (1)

Common characteristics of small dimeric chaperones

Nava RT, Hansberg W

Language: Spanish
References: 90
Page: 1-13
PDF size: 489.36 Kb.


ABSTRACT

Molecular chaperones constitute an important mechanism to prevent cell death caused by protein aggregation. ATPindependent chaperones are a group of low molecular weight proteins that can protect or restore the native structure of unfolded or mis-folded proteins without expenditure of energy. Because we recently found that the C-terminal domain of large-size subunit catalases has a chaperone activity, we are reviewing common characteristics of the most studied low molecular size chaperones, such as αB-crystalline, Hsp20, Spy, Hsp33 and Hsp31. We particularly examine the participation of hydrophobic and charged amino acid residues in protein substrate recognition and the role of dimer formation and its oligomerization in the molecular chaperone activity. We review for each of these molecular chaperones its protein structure, its cellular function and localization, and its importance for the cell.


REFERENCES

  1. Akhtar, M. W., Srinivas, V., Raman, B., Ramakrishna, T., Inobe, T., Maki, K., Arai, M., Kuwajima, K. & Rao, C. M. (2004). Oligomeric Hsp33 with enhanced chaperone activity: gel filtration, cross-linking, and small angle x-ray scattering (SAXS) analysis. Journal of Biological Chemistry, 279(53), 55760–55769. DOI: 10.1074/jbc.M406333200

  2. Alvarez-Castelao, B., Muñoz, C., Sánchez, I., Goethals, M., Vandekerckhove, J. & Castaño, J. G. (2012). Reduced protein stability of human DJ-1/PARK7 L166P, linked to autosomal recessive Parkinson disease, is due to direct endoproteolytic cleavage by the proteasome. Biochimica et Biophysica Acta, 1823(2), 524–533. DOI: 10.1016/j. bbamcr.2011.11.010

  3. Aslam, K. & Hazbun, T. R. (2016). Hsp31, a member of the DJ-1 superfamily, is a multitasking stress responder with chaperone activity. Prion, 10(2), 103–111. DOI: 10.1080/19336896.2016.1141858

  4. Bagnéris, C., Bateman, O., Naylor, C., Cronin, N., Boelens, W., Keep, N. & Slingsby, C. (2009). Crystal structures of a-crystallin domain dimers of aB-crystallin and Hsp20. Journal of Molecular Biology, 394(3), 1242-1252. DOI: 10.1016/j.jmb.2009.09.060

  5. Bankapalli, K., Saladi, S., Awadia, S. S., Goswami, A. V., Samaddar, M. & D’Silva, P. (2015). Robust glyoxalase activity of Hsp31, a ThiJ/DJ-1/PfpI family member protein, is critical for oxidative stress resistance in Saccharomyces cerevisiae. Journal of Biological Chemistry, 290(44), 26491–26507. DOI: 10.1074/jbc.M115.673624

  6. Blackinton, J., Ahmad, R., Miller, D. W., van der Brug, M. P., Canet-Avilés, R. M., Hague, S. M., Kaleem, M. & Cookson, M. R. (2005). Effects of DJ-1 mutations and polymorphisms on protein stability and subcellular localization. Molecular Brain Research, 134(1), 76–83. DOI: 10.1016/j.molbrainres.2004.09.004

  7. Boelens, W. (2014). Cell biological roles of aB-crystallin. Progress in Biophysics and Molecular Biology, 115(1), 3–10. DOI: 10.1016/j.pbiomolbio.2014.02.005

  8. Braun, N., Zacharias, M., Peschek, J., Kastenmueller, A., Zou, J., Hanzlik, M., Haslbeck, M., Rappsilber, J., Buchner, J. & Weinkauf, S. (2011). Multiple molecular architectures of the eye lens chaperone alpha beta-crystallin elucidated by a triple hybrid approach. Proceedings of the National Academia of Sciences of the United Estates of America, 108(51), 20491–20496. DOI: 10.1073/pnas.1111014108

  9. Brodehl, A., Gaertner-Rommel, A., Klauke, B., Grewe, S. A., Schirmer, I., Peterschröder, A., Faber, L., Vorgerd, M., Gummert, J., Anselmetti, D., Schulz, U., Paluszkiewicz, L. & Milting, H. (2017). The novel aB-crystallin (CRYAB) mutation p.D109G causes restrictive cardiomyopathy. Human Mutation, 38(8), 947–952. DOI: 10.1002/ humu.23248

  10. Bukach, O. V., Seit-Nebi, A. S., Marston, S. B. & Gusev, N. B. (2004). Some properties of human small heat shock protein Hsp20 (HspB6). European Journal of Biochemistry, 271(2), 291–302. DOI: 10.1046/j.1432-1033.2003.03928.x

  11. Chelikani, P., Donald, L. J., Duckworth, H. W. & Loewen, P. C. (2003). Hydroperoxidase II of Escherichia coli exhibits enhanced resistance to proteolytic cleavage compared to other catalases. Biochemistry, 42(19), 5729–5735. DOI: 10.1021/bi034208j

  12. Chi, S. W., Jeong, D. G., Woo, J. R., Lee, H. S., Park, B. C., Kim., B. Y., Erikson, R. L., Ryu, S. E. & Kim, S. J. (2011). Crystal structure of constitutively monomeric E. coli Hsp33 mutant with chaperone activity. FEBS Letters, 585(4), 664- 670. DOI: 10.1016/j.febslet.2011.01.029

  13. Cremers, C. M., Reichmann, D., Hausmann, J., Ilbert, M. & Jacob, U. (2010). Unfolding of metastable linker region is at the core of Hsp33 activation as a redox-regulated chaperone. Journal of Biological Chemistry, 285(15), 11243–11251. DOI: 10.1074/jbc.M109.084350

  14. den Engelsman, J., Bennink, E., Doerwald, L., Onnekink, C., Wunderink, L., Andley, U. P., Kato, K., de Jong, W. W. & Boeleens, W. C. (2004). Mimicking phosphorylation of the small heat-shock protein aB-crystallin recruits the F-box protein FBX4 to nuclear SC35 speckles. European Journal of Biochemistry, 271(21), 4195–4203. DOI: 10.1111/j.1432- 1033.2004.04359.x

  15. Díaz, A., Valdés, V. J., Rudiño-Piñera, E., Horjales, E. & Hansberg, W. (2009). Structure-function relationships in fungal large-subunit catalases. Journal of Molecular Biology, 386(1), 218–232. DOI: 10.1016/j. jmb.2008.12.019

  16. Dimauro, I., Antonioni, A., Mercatelli, N. & Caporossi, D. (2017). The role of aB-crystallin in skeletal and cardiac muscle tissues. Cell Stress and Chaperones, 23(4), 491–505. DOI: 10.1007/s12192-017-0866-x

  17. Dolgacheva, L. P., Berezhnov, A. V., Fedotova, E. I., Zinchenko, V. P. & Abramov, A. Y. (2019). Role of DJ-1 in the mechanism of pathogenesis of Parkinson’s disease. Journal of Bioenergetics and Biomembranes, 51(3), 175–188. DOI: 10.1007/s10863-019-09798-4

  18. Dreiza, C. M., Komalavilas, P., Furnish, E. J., Flynn, C. R., Sheller, M., Smoke, C. C., Lopes, L. B. & Brophy, C. M. (2010). The small heat shock protein, HSPB6, in muscle function and disease. Cell Stress and Chaperones, 15(1), 1–11. DOI: 10.1007/s12192-009-0127-8

  19. Edwards, H. V., Cameron, R. T. & Baillie, G. S. (2011). The emerging role of HSP20 as a multifunctional protective agent. Cell Signalling, 23(9), 1447–1454. DOI: 10.1016/j. cellsig.2011.05.009

  20. Fan, G. C. & Kranias, E. (2010). Small heat shock protein 20 (HspB6) in cardiac hypertrophy and failure. Journal of Molecular and Cellular Cardiology, 51(4), 574–577. DOI: 10.1016/j.yjmcc.2010.09.013

  21. Fuchs, M., Poirier, D. J., Seguin, S. J., Lambert, H., Carra, S., Charette, S. J. & Landry, J. (2009). Identification of the key structural motifs involved in HspB8/HspB6-Bag3 interaction. Biochemical Journal, 425(1), 245–255. DOI: 10.1042/BJ20090907

  22. Golenhofen, N., Perng, M. D., Quinlan, R. A. & Drenckhahn, D. (2004). Comparison of small heat shock proteins alphaBcrystallin, MKBP, HSP25, HSP20, cvHSP in heart and skeletal muscle. Histochemistry and Cell Biology, 122(5), 415–425. DOI: 10.1007/s00418-004-0711-z

  23. Graumann, J., Lilie, H., Tang, X., Tucker, K. A., Hoffmann, J. H., Vijayalakshmi, J., Saper, M., Bardwell, J. C. & Jakob, U. (2001). Activation of the redox-regulated molecular chaperone Hsp33 — A two-step mechanism. Structure, 9(5), 377–387. DOI: 10.1016/s0969-2126(01)00599-8

  24. Groitl, B., Horowitz, S., Makepeace, K. A. T., Petrotchenko, E. V., Borchers, C. H., Reichmann, D., Bardwell, J. C. A. & Jacob, U. (2016). Protein unfolding as a switch from self-recognition to high-affinity client binding. Nature Communications, 7(1), 1-12. DOI: 10.1038/ ncomms10357

  25. Gruvberger-Saal, S. & Parsons, R. (2006). Is the small heat shock protein aB-crystallin an oncogene? The Journal of Clinical Investigation, 116(1), 30–32. DOI: 10.1172/JCI27462

  26. Hall, D. (2019). On the nature of the optimal form of the holdase‐type chaperone stress response. FEBS Letters, 594(1), 43–66. DOI: 10.1002/1873-3468.13580

  27. Hansberg, W., Salas-Lizana, R. & Domínguez, L. (2012). Fungal catalases: function, phylogenetic origin and structure. Archives of Biochemistry and Biophysics, 525(2), 170–180. DOI: 10.1016/j.abb.2012.05.014

  28. Hartl, F. U., Bracher, A. & Hayer-Hartl, M. (2011). Molecular chaperones in protein folding and proteostasis. Nature, 575(7356), 324–332. DOI: 10.1038/nature10317

  29. Hartl, F. U. & Hayer-Hartl, M. (2009). Converging concepts of protein folding in vitro and in vivo. Nature Structural and Molecular Biology, 16(6), 574–581. DOI: 10.1038/ nsmb.1591

  30. He, L., Sharpe, T., Mazur, A. & Hiller, S. (2016). A molecular mechanism of chaperone-client recognition. Science Advances, 2(11), e1601625-e1601629. DOI: 10.1126/ sciadv.1601625

  31. Heirbaut, M., Beelen, S., Strelkov, S. V. & Weeks, S. D. (2014). Dissecting the functional role of the N-terminal domain of the human small heat shock protein HSPB6. PLoS One, 9(8), e105892- e105892. DOI: 10.1371/journal.pone.0105892

  32. Hiller, S. & Burmann, B. M. (2018). Chaperone–client complexes: a dynamic liaison. Journal of Magnetic Resonance, 289(1), 142–155. DOI: 10.1016/j.jmr.2017.12.008

  33. Honbou, K., Suzuki, N. N., Horiuchi, M., Niki, T., Taira, T., Ariga, H. & Inagaki, F. (2003). The Crystal structure of DJ-1, a protein related to male fertility and Parkinson’s disease. Journal of Biological Chemistry, 278(33), 31380–31384. DOI: 10.1074/jbc.M305878200

  34. Janda, I., Devedjiev, Y., Derewenda, U., Dauter, Z., Bielnicki, J., Cooper, D. R., Graf, P. C., Joachimiak, A., Jakob, U. & Derewenda, Z. S. (2004). The crystal structure of the reduced, Zn2+-bound form of the B. subtilis Hsp33 chaperone and its implications for the activation mechanism. Structure, 12(10), 1901–1907. DOI: 10.1016/j.str.2004.08.003

  35. Jaspard, E. & Hunault, G. (2016). sHSPdb: A database for the analysis of small Heat Shock Proteins. BCM Plant Biology, 16(1), 135-146. DOI: 10.1186/s12870-016-0820-6

  36. Jin, J., Whittaker, R., Glassy, M., Barlow, S., Gottlieb, R. & Glembotski, C. (2008). Localization of phosphorylated aB-crystallin to heart mitochondria during ischemiareperfusion. American Journal of Physiology-Heart and Circulatory Physiology, 294(1), H337–H344. DOI: 10.1152/ajpheart.00881.200

  37. Jung, H. J., Kim, S., Kim, Y. J., Kim, M-K., Kang, S. G., Lee, J-H., Kim, W. & Cha, S-S. (2012). Dissection of the dimerization modes in the DJ-1 superfamily. Molecules and Cells, 33(2), 163–171. DOI: 10.1007/s10059-012-2220-6

  38. Kim, J., Choi, D., Cha, S. Y., Oh, Y. M., Hwang, E., Park, C. & Ryu, K. S. (2018). Zinc-mediated reversible multimerization of Hsp31 enhances the activity of holding chaperone. Journal of Molecular Biology, 430(12), 1760–1772. DOI: 10.1016/j.jmb.2018.04.029

  39. Kim, K. S., Kim, J. S., Park, J-Y., Suh, Y. H., Jou, I., Joe, E. H. & Park, S. M. (2013). DJ-1 associates with lipid rafts by palmitoylation and regulates lipid rafts-dependent endocytosis in astrocytes. Human Molecular Genetics, 22(23), 4805–4817. DOI: 10.1093/hmg/ddt332

  40. Kim, S-J., Park, Y-J., Hwang, I-Y., Youdim, M. B. H., Park, K. S. & Oh, Y. J. (2012). Nuclear translocation of DJ-1 during oxidative stress-induced neuronal cell death. Free Radical Biology & Medicine, 53(4), 936–950. DOI: 10.1016/j. freeradbiomed.2012.05.035

  41. Klemenz, R., Andres, A., Fröhli, E., Schäfer, R. & Aoyama, A. (1993). Expression of the murine small heat shock proteins HSP25 and alpha B crystallin in the absence of stress. Journal of Cell Biology, 120(3), 639–645. DOI: 10.1083/jcb.120.3.639

  42. Koldewey, P., Horowitz, S. & Bardwell, J. (2017). Chaperone-client interactions: Non-specificity engenders multifunctionality. Journal of Biological Chemistry, 292(29), 12010–12017. DOI: 10.1074/jbc.R117.796862

  43. Koldewey, P., Stull, F., Horowitz, S., Martin, R. & Bardwell, J. (2016). Forces driving chaperone action. Cell, 166(2), 369–379. DOI: 10.1016/j.cell.2016.05.054

  44. Kriegenburg, F., Jakopec, V., Poulsen, E. G., Nielsen, S. V., Roguev, A., Krogan, N., Gordon, C., Fleig, U. & Hartmann- Petersen, R. (2014). A chaperone-assisted degradation pathway targets kinetochore proteins to ensure genome stability. PLoS Genetics, 10(1), e1004140- e1004140. DOI: 10.1371/journal.pgen.1004140

  45. Kumsta, C. & Jakob, U. (2009). Redox-regulated chaperones. Biochemistry, 48(22), 4666–4676.DOI: 10.1021/bi9003556

  46. Kwon, E., Kim, D. Y., Gross, C. A., Gross, J. D. & Kim, K. K. (2010). The crystal structure Escherichia coli Spy. Protein Sciencies, 19(11), 2252–2259. DOI: 10.1002/pro.489

  47. Lee, S-J., Kim, S. J., Kim, I-K., Ko, J., Jeong, C-S., Kim, G-H., Park, C., Kang, S-O., Suh, P-G., Lee, H-L. & Cha, S-S. (2003). Crystal structures of human DJ‐1 and Escherichia coli Hsp31 that share an evolutionarily conserved domain. Journal of Biological Chemistry, 278(45), 44552–44559. DOI: 10.1074/jbc.M304517200

  48. Li, F., Xiao, H., Zhou, F., Hu, Z. & Yang, B. (2017). Study of HspB6: insights into the properties of multifunctional protective agent. Cell Physiology and Biochemistry, 44(1), 314–332. DOI: 10.1159/000484889

  49. Liu, Z., Wang, C., Li, Y., Zhao, C., Li, T., Li, D., Zhang, S. & Liu, C. (2018). Mechanistic insights into the switch of aB-crystallin chaperone activity and self-multimerization. Journal of Biological Chemistry, 293(38), 14880–14890. DOI: 10.1074/jbc.ra118.004034

  50. Lucas, J. I. & Marín, I. (2007). A new evolutionary paradigm for the Parkinson disease gene DJ-1. Molecular Biology and Evolution, 24(2), 551–556. DOI: 10.1093/molbev/ msl186

  51. Macario, A., Conway de Macario, E. & Cappello, F. (2013). Chaperones: general characteristics and classifications. In The Chaperonopathies pp. 15–33. SpringerBriefs in Biochemistry and Molecular Biology, Springer, Dordrecht. DOI: 10.1007/978-94-007-4667-1_2%0A

  52. Malki, A., Kern, R., Abdallah, J. & Richarme, G. (2003). Characterization of the Escherichia coli YedU protein as a molecular chaperone. Biochemical and Biophysical Research Communications, 301(2), 430–436.DOI: 10.1016/ s0006-291x(02)03053-x

  53. Merdanovic, M., Clausen, T., Kaiser, M., Huber, R. & Ehrmann, M. (2004). Protein quality control in the bacterial periplasm. Annual Review of Microbiology, 65(1), 149–168. DOI: 10.1146/annurev-micro-090110-102925

  54. Miller-Fleming, L., Antas, P., Pais, T. F., Smalley, J. L., Giorgini, F. & Outeiro, T. F. (2014). Yeast DJ-1 superfamily members are required for diauxic-shift reprogramming and cell survival in stationary phase. Proceedings of the National Academia of Sciences of the United Estates of America, 111(19), 7012–7017. DOI: 10.1073/ pnas.1319221111

  55. Morimoto, R. (2002). Dynamic remodeling of transcription complexes by molecular chaperones. Cell, 110(3), P281- 284. DOI: 10.1016/S0092-8674(02)00860-7

  56. Moutaoufik, M. T., Malty, R, Amin S., Zhang Q., Phanse S., Gagarinova A., Zilocchi M., Hoell L., Minic Z., Gagarinova M., Aoki H., Stockwell J., Jessulat M., Goebels F., Broderick K., Scott N. E., Vlasblom J., Musso G., Prasad B, Lamantea E., Garavaglia B., Rajput A., Murayama K., Okazaki Y., Foster L. J., Bader G. D., Cayabyab F. S. & Babu M. (2019). Rewiring of the human mitochondrial interactome during neuronal reprogramming reveals regulators of the respirasome and neurogenesis. ISciences, 19(27), 1114–1132. DOI: 10.1016/j.isci.2019.08.057

  57. Mujacic, M., Bader, M. W. & Baneyx, F. (2004). Escherichia coli Hsp31 functions as a holding chaperone that cooperates with the DnaK‐DnaJ‐GrpE system in the management of protein misfolding under severe stress conditions. Molecular Microbiology, 51(3), 849– 859. DOI: 10.1046/j.1365- 2958.2003.03871.x

  58. Mujacic, M. & Baneyx, F. (2006). Regulation of Escherichia coli hchA, a stress‐inducible gene encoding molecular chaperone Hsp31. Molecular Microbiology, 60(6), 1576–1589. DOI: 10.1111/j.1365-2958.2006.05207.x

  59. Muranova, L. & Gusev, N. S. (2018). aB-crystallin phosphorylation: advances and problems. Biochemistry (Moscow), 83(10), 1196–1206. DOI: 10.1146/annurevmicro- 090110-102925.

  60. Mymrikov, E. V., Riedl, M., Peters, C., Weinkauf, S., Haslbeck, M. & Buchner, J. (2019). Regulation of small heat shock proteins by hetero-oligomer formation. Journal of Biological Chemistry, 295(1), 158-169. DOI: 10.1074/jbc. RA119.011143

  61. Nava Ramírez, T. (2017). Las catalasas de subunidad grande también son chaperonas. Tesis de Maestría, UNAM. 1-84

  62. Nava Ramírez, T. & Hansberg, W. (2020).Chaperone activity of large-size subunit catalases. Free Radical Biology & Medicine, 156, 99–106. DOI: 10.1016/j. freeradbiomed.2020.05.020

  63. Niwa, M., Kozawa, O., Matsuno, H., Kato, K. & Uematsu, T. (2000). Small molecular weight heat shock-related protein, HSP20, exhibits an anti-platelet activity by inhibiting receptor-mediated calcium influx. Life Sciences, 66(1), PL7-12. DOI: 10.1016/s0024-3205(99)00566-4

  64. Quan, S., Koldewey, P., Tapley, T., Kirsch, N., Ruane, K. M., Pfizenmaier, J., Shi, R., Hofmann, S., Foit, L., Ren, G., Jakob, U., Xu, Z., C., Ygler, M. & Bardwell, J. C. (2011). Genetic selection designed to stabilize proteins uncovers a chaperone called Spy. Nature Structural and Molecular Biology, 18(1), 262–269. DOI: 10.1038/nsmb.2016

  65. Quigley, P. M., Korotkov, K., Baneyx, F. & Hol, W. G. (2004). A new native EcHsp31 structure suggests a key role of structural flexibility for chaperone function. Protein Sciencies, 13(1), 269– 277. DOI: 10.1110/ps.03399604

  66. Quigley, P. M., Korotkov, K., Baneyx, F. & Hol, W. G. J. (2003). The 1.6‐Å crystal structure of the class of chaperones represented by Escherichia coli Hsp31 reveals a putative catalytic triad. Proceedings of the National Academia of Sciences of the United Estates of America, 100(6), 3137–3142. DOI: 10.1073/pnas.0530312100

  67. Reichmann, D., Xu, Y., Cremers, C. M., Ilbert, M., Mittelman, R., Fitzgerald, M. C. & Jakob, U. (2012). Order out of disorder: working cycle of an intrinsically unfolded chaperone. Cell, 148(5), 947–957. DOI: 10.1016/j.cell.2012.01.045

  68. Rembold, C. M. & Zhang, E. (2001). Localization of heat shock protein 20 in swine carotid artery. BCM Physiology, 1(20), 1-5. DOI: 10.1186/1472-6793-1-10

  69. Saio, T., Kawagoe, S., Ishimori, K. & Kalodimos, C. (2018). Oligomerization of a molecular chaperone modulates its activity. ELife, 7(e35731). 1-18. DOI: 10.7554/ eLife.35731

  70. Santhanagopalan, I., Degiacomi, M., Shepherd, D., Hochberg, G., Benesch, J. & Vierling, E. (2018). It takes a dimer to tango: oligomeric small heat shock proteins dissociate to capture substrate. Journal of Biological Chemistry, 293(51), 19511–19521. DOI: 10.1074/jbc.RA118.005421

  71. Sastry, M. S., Korotkov, K., Brodsky, Y. & Baneyx, F. (2002). Hsp31, the Escherichia coli yedU gene product, is a molecular chaperone whose activity is inhibited by ATP at high temperatures. Journal of Biological Chemistry, 277(48), 46026-46034. DOI: 10.1074/jbc.M205800200

  72. Sastry, M. S., Quigley, P. M., Hol, W. G. & Baneyx, F. (2004). The linker-loop region of Escherichia coli chaperone Hsp31 functions as a gate that modulates high-affinity substrate binding at elevated temperatures. Proceedings of the National Academia of Sciences of the United Estates of America, 101(23), 8587–8592. DOI: 10.1073/ pnas.0403033101

  73. Segal, N. & Shapira, M. (2015). HSP33 in eukaryotes - an evolutionary tale of a chaperone adapted to photosynthetic organisms. The Plant Journal, 82(5), 850–860. DOI: 10.1111/tpj.12855

  74. Seit-Nebi, A. S. & Gusev, N. B. (2009). Versatility of the small heat shock protein HSPB6 (Hsp20). Cell Stress and Chaperones, 15(3), 233–236. DOI: 10.1007/s12192-009- 0141-x

  75. Skoneczna, A., Kaniak, A. & Skoneczny, M. (2015). Genetic instability in budding and fission yeast-sources and mechanisms. FEMS Microbiology Review, 39(6), 917–967. DOI: 10.1093/femsre/fuv028

  76. Sluchanko, N. N., Beelen, S., Kulikova, A. A., Weeks, S. D., Antson, A. A., Gusev, N. B. & Strelkov, S. V. (2017). Structural basis for the interaction of a human small heat shock protein with the 14-3-3 universal signaling regulator. Structure, 25(2), 305–316. DOI: 10.1016/j.str.2016.12.005

  77. Srivastava, S. K., Lambadi, P. R., Ghosh, T., Pathania, R. & Navani, N. K. (2014). Genetic regulation of spy gene expression in Escherichia coli in the presence of protein unfolding agent ethanol. Gene, 548(1), 142–148. DOI: 10.1016/j.gene.2014.07.003

  78. Suss, O. & Reichmann, D. (2015). Protein plasticity underlines activation and function of ATP-independent chaperones. Frontiers in Molecular Biosciences, 2(43), 1-10. DOI: 10.3389/fmolb.2015.00043

  79. Tsai, C-J., Aslam, K., Drendel, H. M., Asiago, J. M., Goode, K. M., Paul, L. N., Rochet, J-C. & Hazbun, T. R. (2015). Hsp31 is a stress response chaperone that intervenes in the protein misfolding process. Journal of Biological Chemistry, 290(41), 24816–24834. DOI: 10.1074/jbc.M115.678367

  80. Usami, Y., Hatano, T., Imai, S., Kubo, S., Sato, S., Saiki, S., Fujioka, Y., Ohba, Y., Sato, F., Funayama, M., Eguchi, H., Shiba, K., Ariga, H., Shen, J. & Hattori, N. (2011). DJ-1 associates with synaptic membranes. Neurobiology of Disease, 43(3), 651–662. DOI: 10.1016/j.nbd.2011.05.014

  81. van de Klundert, F. A., Smulders, R. H., Gijsen, M. L., Lindner, R. A., Jaenicke, R., Carver, J. A. & de Jong, W. W. (1998). The mammalian small heat-shock protein Hsp20 forms dimers and is a poor chaperone. European Journal of Biochemistry, 258(3), 1014-21. DOI: 10.1046/j.1432- 1327.1998.2581014.x

  82. Verschuure, P., Croes, Y., van den IJssel, P. R., Quinlan, R. A., de Jong, W. W. & Boelens, W. C. (2002). Translocation of small heat shock proteins to the actin cytoskeleton upon proteasomal inhibition. Journal of Molecular and Cellular Cardiology, 34(2), 117–128. DOI: 10.1006/jmcc.2001.1493

  83. Vogt, S. L. & Raivio, T. L. (2012). Just scratching the surface: an expanding view of the Cpx envelope stress response. FEMS Microbiology Letters, 326(1), 2–11. DOI: 10.1111/j.1574- 6968.2011.02406.x

  84. Vos, M., Kanon, B. & Kampinga, H. (2009). HSPB7 is a SC35 speckle resident small heat shock protein. Biochimica et Biophysica Acta, 1793(8), 1343–1353. DOI: 10.1016/j. bbamcr.2009.05.005

  85. Voth, W. & Jakob, U. (2017). Stress-activated chaperones: a first line of defense. Trends in Biochemical Sciences, 42(11), 899–913. DOI: 10.1016/j.tibs.2017.08.006

  86. Webster, J. M., Darling, A. L., Uversky, V. N. & Blair, L. J. (2019). Small heat shock proteins, big impact on protein aggregation in neurodegenerative disease. Frontiers in Pharmacology, 10(1047), 1-18. DOI: 10.3389/fphar.2019.01047

  87. Weeks, S. D., Baranova, E. V., Heirbaut, M., Beelen, S., Shkumatov, A. V., Gusev, N. B. & Strelkov, S. V. (2014). Molecular structure and dynamics of the dimeric human small heat shock protein HSPB6. Journal of Structural Biology, 185(3), 342–354. DOI: 10.1016/j.jsb.2013.12.009

  88. Wei, Y., Ringe, D., Wilson, M. A. & Ondrechen, M. J. (2007). Identification of functional subclasses in the DJ-1 superfamily proteins. PLoS Computational Biology, 3(1), 120-126. DOI: 10.1371/journal.pcbi.0030010

  89. Won, H. S., Low, L. Y., Guzman, R. D., Martinez-Yamout, M., Jakob, U. & Dyson, H. J. (2004). The zinc-dependent redox switch domain of the chaperone Hsp33 has a novel fold. Journal of Molecular Biology, 341(4), 893–899. DOI: 10.1016/j.jmb.2004.06.046

  90. Wu, K., Stull, F., Lee, C. & Bardwell, J. C. (2019). Protein folding while chaperone bound is dependent on weak interactions. Nature Communications, 10(1), 4833. DOI: 10.1038/s41467-019-12774-6




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