Фосфорилирование αВ-кристаллина: успехи и проблемы

Сноски

* Адресат для корреспонденции.

Финансирование

Работа выполнена при финансовой поддержке РНФ (грант 14-35-00026) и частично при поддержке РФФИ (грант 16-04-00016).

Список литературы

1. Maaroufi, H., and Tanguay, R.M. (2013) Analysis and phylogeny of small heat shock proteins from marine viruses and their cyanobacteria host, PLoS One, 8, e81207.

2. Basha, E., O’Neill, H., and Vierling, E. (2012) Small heat shock proteins and alpha-crystallins: dynamic proteins with flexible functions, Trends Biochem. Sci., 37, 106–117.

3. Haslbeck, M., and Vierling, E. (2015) A first line of stress defense: small heat shock proteins and their function in protein homeostasis, J. Mol. Biol., 427, 1537–1548.

4. Kriehuber, T., Rattei, T., Weinmaier, T., Bepperling, A., Haslbeck, M., and Buchner, J. (2010) Independent evolution of the core domain and its flanking sequences in small heat shock proteins, FASEB J., 24, 3633–3642.

5. Fontaine, J.M., Rest, J.S., Welsh, M.J., and Benndorf, R. (2003) The sperm outer dense fiber protein is the 10th member of the superfamily of mammalian small stress proteins, Cell Stress Chaperones, 8, 62–69.

6. Kappe, G., Franck, E., Verschuure, P., Boelens, W.C., Leunissen, J.A., and de Jong, W.W. (2003) The human genome encodes 10 alpha-crystallin-related small heat shock proteins: HspB1-10, Cell Stress Chaperones, 8, 53–61.

7. Mymrikov, E.V., Seit-Nebi, A.S., and Gusev, N.B. (2011) Large potentials of small heat shock proteins, Physiol. Rev., 91, 1123–1159.

8. Bakthisaran, R., Tangirala, R., and Rao, C.M. (2015) Small heat shock proteins: role in cellular functions and pathology, Biochim. Biophys. Acta, 1854, 291–319.

9. Hochberg, G.K.A., Shepherd, D.A., Marklund, E.G., Santhanagoplan, I., Degiacomi, M.T., Laganowsky, A., Allison, T.M., Basha, E., Marty, M.T., Galpin, M.R., Struwe, W.B., Baldwin, A.J., Vierling, E., and Benesch, J.L.P. (2018) Structural principles that enable oligomeric small heat-shock protein paralogs to evolve distinct functions, Science, 359, 930–935.

10. Peschek, J., Braun, N., Rohrberg, J., Back, K.C., Kriehuber, T., Kastenmuller, A., Weinkauf, S., and Buchner, J. (2013) Regulated structural transitions unleash the chaperone activity of alphaB-crystallin, Proc. Natl. Acad. Sci. USA, 110, 3780–3789.

11. Weeks, S.D., Baranova, E.V., Heirbaut, M., Beelen, S., Shkumatov, A.V., Gusev, N.B., and Strelkov, S.V. (2014) Molecular structure and dynamics of the dimeric human small heat shock protein HSPB6, J. Struct. Biol., 185, 342–354.

12. Mymrikov, E.V., Seit-Nebi, A.S., and Gusev, N.B. (2012) Heterooligomeric complexes of human small heat shock proteins, Cell Stress Chaperones, 17, 157–169.

13. Arrigo, A.P. (2013) Human small heat shock proteins: pro- tein interactomes of homo- and hetero-oligomeric complexes: an update, FEBS Lett., 587, 1959–1969.

14. Bukach, O.V., Glukhova, A.E., Seit-Nebi, A.S., and Gusev, N.B. (2009) Heterooligomeric complexes formed by human small heat shock proteins HspB1 (Hsp27) and HspB6 (Hsp20), Biochim. Biophys. Acta, 1794, 486–495.

15. Heirbaut, M., Lermyte, F., Martin, E.M., Beelen, S., Verschueren, T., Sobott, F., Strelkov, S.V., and Weeks, S.D. (2016) The preferential heterodimerization of human small heat shock proteins HSPB1 and HSPB6 is dictated by the N-terminal domai, Arch. Biochem. Biophys., 610, 41–50.

16. Vos, M.J., Kanon, B., and Kampinga, H.H. (2009) HSPB7 is a SC35 speckle resident small heat shock protein, Biochim. Biophys. Acta, 1793, 1343–1353.

17. Horwitz, J. (2003) Alpha-crystallin, Exp. Eye Res., 76, 145–153.

18. Srinivas, P.N., Reddy, P.Y., and Reddy, G.B. (2008) Significance of alpha-crystallin heteropolymer with a 3 : 1 alphaA/alphaB ratio: chaperone-like activity, structure and hydrophobicity, Biochem. J., 414, 453–460.

19. Sharma, K.K. and Santhoshkumar, P. (2009) Lens aging: effects of crystallins, Biochim. Biophys. Acta, 1790, 1095–1108.

20. Jovcevski, B., Andrew Aquilina, J., Benesch, J.L.P., and Ecroyd, H. (2018) The influence of the N-terminal region proximal to the core domain on the assembly and chaperone activity of alphaB-crystallin, Cell Stress Chaperones, doi: 10.1007/s12192-018-0889-y.

21. Aquilina, J.A., Benesch, J.L., Bateman, O.A., Slingsby, C., and Robinson, C.V. (2003) Polydispersity of a mammalian chaperone: mass spectrometry reveals the population of oligomers in alphaB-crystallin, Proc. Natl. Acad. Sci. USA, 100, 10611–10616.

22. Braun, N., Zacharias, M., Peschek, J., Kastenmuller, A., Zou, J., Hanzlik, M., Haslbeck, M., Rappsilber, J., Buchner, J., and Weinkauf, S. (2011) Multiple molecular architectures of the eye lens chaperone alphaB-crystallin elucidated by a triple hybrid approach, Proc. Natl. Acad. Sci. USA, 108, 20491–20496.

23. Jehle, S., van Rossum, B., Stout, J.R., Noguchi, S.M., Falber, K., Rehbein, K., Oschkinat, H., Klevit, R.E., and Rajagopal, P. (2009) АlphaB-crystallin: a hybrid solid-state/solution-state NMR investigation reveals structural aspects of the heterogeneous oligomer, J. Mol. Biol., 385, 1481–1497.

24. Delbecq, S.P. and Klevit, R.E. (2013) One size does not fit all: the oligomeric states of alphaB crystallin, FEBS Lett., 587, 1073–1080.

25. Jehle, S., Vollmar, B.S., Bardiaux, B., Dove, K.K., Rajagopal, P., Gonen, T., Oschkinat, H., and Klevit, R.E. (2011) N-terminal domain of alphaB-crystallin provides a conformational switch for multimerization and structural heterogeneity, Proc. Natl. Acad. Sci. USA, 108, 6409–6414.

26. Jehle, S., Rajagopal, P., Bardiaux, B., Markovic, S., Kuhne, R., Stout, J.R., Higman, V.A., Klevit, R.E., van Rossum, B.J., and Oschkinat, H. (2010) Solid-state NMR and SAXS studies provide a structural basis for the activation of alphaB-crystallin oligomers, Nat. Struct. Mol. Biol., 17, 1037–1042.

27. Benesch, J.L., Ayoub, M., Robinson, C.V., and Aquilina, J.A. (2008) Small heat shock protein activity is regulated by variable oligomeric substructure, J. Biol. Chem., 283, 28513–28517.

28. Cheng, C., Xia, C.H., Huang, Q., Ding, L., Horwitz, J., and Gong, X. (2010) Altered chaperone-like activity of alpha-crystallins promotes cataractogenesis, J. Biol. Chem., 285, 41187–41193.

29. Lee, J.S., Liao, J.H., Wu, S.H., and Chiou, S.H. (1997) Аlpha-сrystallin acting as a molecular chaperonin against photodamage by UV irradiatio, J. Protein Chem., 16, 283–289.

30. Ecroyd, H., Meehan, S., Horwitz, J., Aquilina, J.A., Benesch, J.L., Robinson, C.V., Macphee, C.E., and Carver, J.A. (2007) Mimicking phosphorylation of alphaB-crystallin affects its chaperone activity, Biochem. J., 401, 129–141.

31. Ahmad, M.F., Raman, B., Ramakrishna, T., and Rao Ch, M. (2008) Effect of phosphorylation on alpha B-crystallin: differences in stability, subunit exchange and chaperone activity of homo and mixed oligomers of alpha B-crystallin and its phosphorylation-mimicking mutant, J. Mol. Biol., 375, 1040–1051.

32. Ito, H., Kamei, K., Iwamoto, I., Inaguma, Y., Nohara, D., and Kato, K. (2001) Phosphorylation-induced change of the oligomerization state of alphaB-crystallin, J. Biol. Chem., 276, 5346–5352.

33. Koteiche, H.A., and McHaourab, H.S. (2003) Mechanism of chaperone function in small heat-shock proteins. Phosphorylation-induced activation of two-mode binding in alphaB-crystalli, J. Biol. Chem., 278, 10361–10367.

34. Wang, K., and Spector, A. (1996) Аlpha-crystallin stabilizes actin filaments and prevents cytochalasin-induced depolymerization in a phosphorylation-dependent manner, Eur. J. Biochem., 242, 56–66.

35. Elliott, J.L., Der Perng, M., Prescott, A.R., Jansen, K.A., Koenderink, G.H., and Quinlan, R.A. (2013) 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., 368, 20120375.

36. Houck, S.A., and Clark, J.I. (2010) Dynamic subunit exchange and the regulation of microtubule assembly by the stress response protein human alphaB crystallin, PLoS One, 5, e11795.

37. Haslbeck, M., Peschek, J., Buchner, J., and Weinkauf, S. (2016) Structure and function of alpha-crystallins: traversing from in vitro to in vivo, Biochim. Biophys. Acta, 1860, 149–166.

38. Bakthisaran, R., Akula, K.K., Tangirala, R., and Rao Ch, M. (2016) Phosphorylation of alphaB-crystallin: role in stress, aging and patho-physiological conditions, Biochim. Biophys. Acta, 1860, 167–182.

39. Datskevich, P.N., Nefedova, V.V., Sudnitsyna, M.V., and Gusev, N.B. (2012) Mutations of small heat shock proteins and human congenital diseases, Biochemistry, 77, 1500–1514.

40. Thornell, E., and Aquilina, A. (2015) Regulation of alphaA- and alphaB-crystallins via phosphorylation in cellular homeostasis, Cell. Mol. Life Sci., 72, 4127–4137.

41. Benndorf, R., Martin, J.L., Kosakovsky Pond, S.L., and Wertheim, J.O. (2014) Neuropathy- and myopathy-associated mutations in human small heat shock proteins: characteristics and evolutionary history of the mutation sites, Mut. Res. Rev., 761, 15–30.

42. Boncoraglio, A., Minoia, M., and Carra, S. (2012) The family of mammalian small heat shock proteins (HSPBs): implications in protein deposit diseases and motor neuropathie, Int. J. Biochem. Cell Biol., 44, 1657–1669.

43. Fujii, N., Takata, T., Fujii, N., and Aki, K. (2016) Isomerization of aspartyl residues in crystallins and its influence upon cataract, Biochim. Biophys. Acta, 1860, 183–191.

44. MacCoss, M.J., McDonald, W.H., Saraf, A., Sadygov, R., Clark, J.M., Tasto, J.J., Gould, K.L., Wolters, D., Washburn, M., Weiss, A., Clark, J.I., and Yates, J.R., 3rd. (2002) Shotgun identification of protein modifications from protein complexes and lens tissue, Proc. Natl. Acad. Sci. USA, 99, 7900–7905.

45. Miesbauer, L.R., Zhou, X., Yang, Z., Yang, Z., Sun, Y., Smith, D.L., and Smith, J.B. (1994) Post-translational modifications of water-soluble human lens crystallins from young adults, J. Biol. Chem., 269, 12494–12502.

46. Wilmarth, P.A., Tanner, S., Dasari, S., Nagalla, S.R., Riviere, M.A., Bafna, V., Pevzner, P.A., and David, L.L. (2006) Age-related changes in human crystallins determined from comparative analysis of post-translational modifications in young and aged lens: does deamidation contribute to crystallin insolubility? J. Proteome Res., 5, 2554–2566.

47. Kato, K., Ito, H., Kamei, K., Inaguma, Y., Iwamoto, I., and Saga, S. (1998) Phosphorylation of alphaB-crystallin in mitotic cells and identification of enzymatic activities responsible for phosphorylation, J. Biol. Chem., 273, 28346–28354.

48. Kantorow, M., Horwitz, J., van Boekel, M.A., de Jong, W.W., and Piatigorsky, J. (1995) Conversion from oligomers to tetramers enhances autophosphorylation by lens alphaA-crystallin. Specificity between alpha A- and alpha B-crystallin subunits, J. Biol. Chem., 270, 17215–17220.

49. Spector, A., Chiesa, R., Sredy, J., and Garner, W. (1985) cAMP-dependent phosphorylation of bovine lens alpha-crystallin, Proc. Natl. Acad. Sci. USA, 82, 4712–4716.

50. Samanta, B., Nagdas, S.K., Das, K., and Sen, P.C. (2007) Protein kinase catalytic subunit (PKAcat) from bovine lens: purification, characterization and phosphorylation of lens crystallins, Mol. Cell. Biochem., 304, 155–165.

51. Lee, S.W., Rho, J.H., Lee, S.Y., Yoo, S.H., Kim, H.Y., Chung, W.T., and Yoo, Y.H. (2016) AlphaB-crystallin protects rat articular chondrocytes against casein kinase II inhibition-induced apoptosis, PLoS One, 11, e0166450.

52. Maddala, R., and Rao, V.P. (2005) alpha-Crystallin localizes to the leading edges of migrating lens epithelial cells, Exp. Cell Res., 306, 203–215.

53. Launay, N., Goudeau, B., Kato, K., Vicart, P., and Lilienbaum, A. (2006) Cell signaling pathways to alphaB-crystallin following stresses of the cytoskeleton, Exp. Cell. Res., 312, 3570–3584.

54. Kato, K., Ito, H., Kamei, K., Iwamoto, I., and Inaguma, Y. (2002) Innervation-dependent phosphorylation and accumulation of alphaB-crystallin and Hsp27 as insoluble complexes in disused muscle, FASEB J., 16, 1432–1434.

55. Hoover, H.E., Thuerauf, D.J., Martindale, J.J., and Glembotski, C.C. (2000) Аlpha B-crystallin gene induction and phosphorylation by MKK6-activated p38. A potential role for alphaB-crystallin as a target of the p38 branch of the cardiac stress response, J. Biol. Chem., 275, 23825–23833.

56. Eaton, P., Fuller, W., Bell, J.R., and Shattock, M.J. (2001) AlphaB crystallin translocation and phosphorylation: signal transduction pathways and preconditioning in the isolated rat heart, J. Mol. Cell. Cardiol., 33, 1659–1671.

57. Moroni, M., and Garland, D. (2001) In vitro dephosphorylation of alpha-crystallin is dependent on the state of oligomerization, Biochim. Biophys. Acta, 1546, 282–290.

58. Ifeanyi, F., and Takemoto, L. (1991) Interaction of lens crystallins with lipid vesicles, Exp. Eye Res., 52, 535–538.

59. Tang, D., Borchman, D., Yappert, M.C., and Cenedella, R.J. (1998) Influence of cholesterol on the interaction of alpha-crystallin with phospholipids, Exp. Eye Res., 66, 559–567.

60. Su, S.P., McArthur, J.D., Friedrich, M.G., Truscott, R.J., and Aquilina, J.A. (2011) Understanding the alpha-crystallin cell membrane conjunction, Mol. Vis., 17, 2798–2807.

61. Wang, K., Ma, W., and Spector, A. (1995) Phosphorylation of alpha-crystallin in rat lenses is stimulated by H2O2 but phosphorylation has no effect on chaperone activity, Exp. Eye Res., 61, 115–124.

62. Carver, J.A., Nicholls, K.A., Aquilina, J.A., and Truscott, R.J. (1996) Age-related changes in bovine alpha-crystallin and high-molecular-weight protein, Exp. Eye Res., 63, 639–647.

63. Golenhofen, N., Htun, P., Ness, W., Koob, R., Schaper, W., and Drenckhahn, D. (1999) Binding of the stress protein alphaB-crystallin to cardiac myofibrils correlates with the degree of myocardial damage during ischemia/reperfusion in vivo, J. Mol. Cell. Cardiol., 31, 569–580.

64. Morrison, L.E., Hoover, H.E., Thuerauf, D.J., and Glembotski, C.C. (2003) Mimicking phosphorylation of alphaB-crystallin on serine-59 is necessary and sufficient to provide maximal protection of cardiac myocytes from apoptosis, Circ. Res., 92, 203–211.

65. Li, R., and Reiser, G. (2011) Phosphorylation of Ser45 and Ser59 of alphaB-crystallin and p38/extracellular regulated kinase activity determine alphaB-crystallin-mediated protection of rat brain astrocytes from C2-ceramide- and staurosporine-induced cell death, J. Neurochem., 118, 354–364.

66. Aquilina, J.A., Benesch, J.L., Ding, L.L., Yaron, O., Horwitz, J., and Robinson, C.V. (2004) Phosphorylation of alphaB-crystallin alters chaperone function through loss of dimeric substructure, J. Biol. Chem., 279, 28675–28680.

67. Ito, H., Okamoto, K., Nakayama, H., Isobe, T., and Kato, K. (1997) Phosphorylation of alphaB-crystallin in response to various types of stress, J. Biol. Chem., 272, 29934–29941.

68. Rogalla, T., Ehrnsperger, M., Preville, X., Kotlyarov, A., Lutsch, G., Ducasse, C., Paul, C., Wieske, M., Arrigo, A.P., Buchner, J., and Gaestel, M. (1999) Regulation of Hsp27 oligomerization, chaperone function, and protective activity against oxidative stress/tumor necrosis factor alpha by phosphorylation, J. Biol. Chem., 274, 18947–18956.

69. Weeks, S.D., Muranova, L.K., Heirbaut, M., Beelen, S., Strelkov, S.V., and Gusev, N.B. (2018) Characterization of human small heat shock protein HSPB1 alpha-crystallin domain localized mutants associated with hereditary motor neuron diseases, Sci. Rep., 8, 688.

70. Schmidt, T., Bartelt-Kirbach, B., and Golenhofen, N. (2012) Phosphorylation-dependent subcellular localization of the small heat shock proteins HspB1/Hsp25 and HspB5/alphaB-crystallin in cultured hippocampal neurons, Histochem. Cell Biol., 138, 407–418.

71. Bartelt-Kirbach, B., Moron, M., Glomb, M., Beck, C.M., Weller, M.P., and Golenhofen, N. (2016) HspB5/alphaB-crystallin increases dendritic complexity and protects the dendritic arbor during heat shock in cultured rat hippocampal neurons, Cell. Mol. Life Sci., 73, 3761–3775.

72. Whittaker, R., Glassy, M.S., Gude, N., Sussman, M.A., Gottlieb, R.A., and Glembotski, C.C. (2009) Kinetics of the translocation and phosphorylation of alphaB-crystallin in mouse heart mitochondria during ex vivo ischemia, Am. J. Physiol. Heart Circ. Physiol., 296, 1633–1642.

73. Golenhofen, N., Ness, W., Koob, R., Htun, P., Schaper, W., and Drenckhahn, D. (1998) Ischemia-induced phosphorylation and translocation of stress protein alphaB-crystallin to Z lines of myocardium, Am. J. Physiol., 274, 1457–1464.

74. Fung, G., Wong, J., Berhe, F., Mohamud, Y., Xue, Y.C., and Luo, H. (2017) Phosphorylation and degradation of alphaB-crystallin during enterovirus infection facilitates viral replication and induces viral pathogenesis, Oncotarget, 8, 74767–74780.

75. Singh, B.N., Rao, K.S., Ramakrishna, T., Rangaraj, N., and Rao, Ch.M. (2007) Association of alphaB-crystallin, a small heat shock protein, with actin: role in modulating actin filament dynamics in vivo, J. Mol. Biol., 366, 756–767.

76. Clements, R.T., Sodha, N.R., Feng, J., Mieno, S., Boodhwani, M., Ramlawi, B., Bianchi, C., and Sellke, F.W. (2007) Phosphorylation and translocation of heat shock protein 27 and alphaB-crystallin in human myocardium after cardioplegia and cardiopulmonary bypass, J. Thorac. Cardiovasc. Surg., 134, 1461–1470.

77. Nicholl, I.D., and Quinlan, R.A. (1994) Chaperone activity of alpha-crystallins modulates intermediate filament assembly, EMBO J., 13, 945–953.

78. Inaguma, Y., Ito, H., Iwamoto, I., Saga, S., and Kato, K. (2001) AlphaB-crystallin phosphorylated at Ser-59 is localized in centrosomes and midbodies during mitosis, Eur. J. Cell Biol., 80, 741–748.

79. Aggeli, I.K., Beis, I., and Gaitanaki, C. (2008) Oxidative stress and calpain inhibition induce alphaB-crystallin phosphorylation via p38-MAPK and calcium signalling pathways in H9c2 cells, Cell. Signal., 20, 1292–1302.

80. Ciano, M., Allocca, S., Ciardulli, M.C., Della Volpe, L., Bonatti, S., and D’Agostino, M. (2016) Differential phosphorylation-based regulation of alphaB-crystallin chaperone activity for multipass transmembrane proteins, Biochem. Biophys. Res. Commun., 479, 325–330.

81. Adhikari, A.S., Singh, B.N., Rao, K.S., and Rao, Ch.M. (2011) АlphaB-crystallin, a small heat shock protein, modulates NF-kappaB activity in a phosphorylation-dependent manner and protects muscle myoblasts from TNF-alpha induced cytotoxicity, Biochim. Biophys. Acta, 1813, 1532–1542.

82. Launay, N., Tarze, A., Vicart, P., and Lilienbaum, A. (2010) Serine 59 phosphorylation of alphaB-crystallin down-regulates its anti-apoptotic function by binding and sequestering Bcl-2 in breast cancer cells, J. Biol. Chem., 285, 37324–37332.

83. Kamradt, M.C., Chen, F., Sam, S., and Cryns, V.L. (2002) The small heat shock protein alphaB-crystallin negatively regulates apoptosis during myogenic differentiation by inhibiting caspase-3 activation, J. Biol. Chem., 277, 38731–38736.