Localization of heat shock protein HSPA6 (HSP70B') to sites of transcription in cultured differentiated human neuronal cells following thermal stress

Journal of Neurochemistry

Volumn 131, Issue 6, 2014, Pages 743-754

  Khalouei, Sam ^a   Chow, Ari M ^a   Brown, Ian R ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Heat shock proteins; HSP70B'; HSPA1A; HSPA6; nucleus; SH SY5Y

Indexed keywords

HEAT SHOCK PROTEIN 70; PROTEIN HSP70B; PROTEIN HSPA1A; UNCLASSIFIED DRUG; YELLOW FLUORESCENT PROTEIN; HSP70B' PROTEIN, HUMAN; HSPA1A PROTEIN, HUMAN; SMALL INTERFERING RNA;

ARTICLE; CONTROLLED STUDY; GENE; HSPA6 GENE; HUMAN; HUMAN CELL; NERVE CELL; NERVE CELL CULTURE; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RNA SPLICING; RNA TRANSCRIPTION; TEMPERATURE STRESS; CELL DIFFERENTIATION; CELL LINE; CELL SURVIVAL; CYTOLOGY; GENETIC TRANSCRIPTION; GENETICS; HEAT; HEAT SHOCK RESPONSE; METABOLISM; PHYSIOLOGY;

ANIMALIA; RATTUS;

CELL DIFFERENTIATION; CELL LINE; CELL SURVIVAL; HEAT-SHOCK RESPONSE; HOT TEMPERATURE; HSP70 HEAT-SHOCK PROTEINS; HUMANS; NEURONS; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC;

EID: 84918813132     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12970     Document Type: Article

References (120)

1. Adachi H., Katsuno M., Waza M., Minamiyama M., Tanaka F., and, Sobue G., (2009) Heat shock proteins in neurodegenerative diseases: pathogenic roles and therapeutic implications. Int J. Hyperthermia. 25, 647-654.
2. Agorogiannis E. I., Agorogiannis G. I., Papadimitriou A., and, Hadjigeorgiou G. M., (2004) Protein misfolding in neurodegenerative diseases. Neuropathol. Appl. Neurobiol. 30, 215-224.
3. Allen T. A., Von Kaenel S., Goodrich J. A., and, Kugel J. F., (2004) The SINE-encoded mouse B2 RNA represses mRNA transcription in response to heat shock. Nat. Struct. Mol. Biol. 11, 816-821.
4. Asea A. A., and, Brown I. R., (2008) Heat shock proteins and the brain: implications for neurodegenerative diseases and neuroprotection. Springer Science, New York.
5. Beck S. C., and, De Maio A., (1994) Stabilization of protein synthesis in thermotolerant cells during heat shock. Association of heat shock protein-72 with ribosomal subunits of polysomes. J. Biol. Chem. 269, 21803-21811.
6. Benarroch E. E., (2011) Heat shock proteins: multiple neuroprotective functions and implications for neurologic disease. Neurology 76, 660-667.
7. Biamonti G., (2004) Nuclear stress bodies: a heterochromatin affair? Nat. Rev. Mol. Cell Biol. 5, 493-498.
8. Biamonti G., and, Caceres J. F., (2009) Cellular stress and RNA splicing. Trends Biochem. Sci. 34, 146-153.
9. Biamonti G., and, Vourc'h C., (2010) Nuclear stress bodies. Cold Spring Harb. Perspect. Biol. 2, a000695.
10. Bithell A., Johnson R., and, Buckley N. J., (2009) Transcriptional dysregulation of coding and non-coding genes in cellular models of Huntington's disease. Biochem. Soc. Trans. 37, 1270-1275.
11. Boisvert F. M., van Koningsbruggen S., Navascues J., and, Lamond A. I., (2007) The multifunctional nucleolus. Nat. Rev. Mol. Cell Biol. 8, 574-585.
12. Bond U., (1988) Heat shock but not other stress inducers leads to the disruption of a sub-set of snRNPs and inhibition of in vitro splicing in HeLa cells. EMBO J. 7, 3509-3518.
13. Boulon S., Westman B. J., Hutten S., Boisvert F. M., and, Lamond A. I., (2010) The nucleolus under stress. Mol. Cell 40, 216-227.
14. Bregman D. B., Du L., van der Zee S., and, Warren S. L., (1995) Transcription-dependent redistribution of the large subunit of RNA polymerase II to discrete nuclear domains. J. Cell Biol. 129, 287-298.
15. Brown I. R., (2007a) Heat shock proteins and neurodegenerative diseases, in Cell Stress Proteins, (, Calderwood S. T., ed.). Springer, New York.
16. Brown I. R., (2007b) Heat shock proteins and protection of the nervous system. Ann. N. Y. Acad. Sci. 1113, 147-158.
17. Brown I. R., (2008) Heat shock proteins at the synapse: implications for functional protection of the nervous system, in Heat shock proteins and the brain: implications for neurodegenerative diseases and neuroprotection (, Asea A. A., and, Brown I. R., eds), pp. 239-254. Springer, Dordrecht, Netherlands.
18. Brown J. M., Green J., das Neves R. P., et al. (2008) Association between active genes occurs at nuclear speckles and is modulated by chromatin environment. J. Cell Biol. 182, 1083-1097.
19. Bukau B., Weissman J., and, Horwich A., (2006) Molecular chaperones and protein quality control. Cell 125, 443-451.
20. Caldeira G. L., Ferreira I. L., and, Rego A. C., (2013) Impaired transcription in Alzheimer's disease: key role in mitochondrial dysfunction and oxidative stress. J. Alzheimers Dis. 34, 115-131.
21. Cha J. H., (2000) Transcriptional dysregulation in Huntington's disease. Trends Neurosci. 23, 387-392.
22. Chow A. M., and, Brown I. R., (2007) Induction of heat shock proteins in differentiated human and rodent neurons by celastrol. Cell Stress Chaperones. 12, 237-244.
23. Corell R. A., and, Gross R. H., (1992) Splicing thermotolerance maintains Pre-mRNA transcripts in the splicing pathway during severe heat shock. Exp. Cell Res. 202, 233-242.
24. Daguenet E., Baguet A., Degot S., et al. (2012) Perispeckles are major assembly sites for the exon junction core complex. Mol. Biol. Cell 23, 1765-1782.
25. Daugaard M., Rohde M., and, Jaattela M., (2007) The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Lett. 581, 3702-3710.
26. Denegri M., Chiodi I., Corioni M., Cobianchi F., Riva S., and, Biamonti G., (2001) Stress-induced nuclear bodies are sites of accumulation of pre-mRNA processing factors. Mol. Biol. Cell 12, 3502-3514.
27. Donmez-Altuntas H., Akalin H., Karaman Y., Demirtas H., Imamoglu N., and, Ozkul Y., (2005) Evaluation of the nucleolar organizer regions in Alzheimer's disease. Gerontology 51, 297-301.
28. Dundr M., and, Misteli T., (2001) Functional architecture in the cell nucleus. Biochem. J. 356, 297-310.
29. Espinoza C. A., Goodrich J. A., and, Kugel J. F., (2007) Characterization of the structure, function, and mechanism of B2 RNA, an ncRNA repressor of RNA polymerase II transcription. RNA 13, 583-596.
30. Evans C. G., Chang L., and, Gestwicki J. E., (2010) Heat shock protein 70 (hsp70) as an emerging drug target. J. Med. Chem. 53, 4585-4602.
31. Fang N. N., Ng A. H., Measday V., and, Mayor T., (2011) Hul5 HECT ubiquitin ligase plays a major role in the ubiquitylation and turnover of cytosolic misfolded proteins. Nat. Cell Biol. 13, 1344-1352.
32. Fedorova E., and, Zink D., (2008) Nuclear architecture and gene regulation. Biochim. Biophys. Acta 1783, 2174-2184.
33. Fraser P., and, Bickmore W., (2007) Nuclear organization of the genome and the potential for gene regulation. Nature 447, 413-417.
34. Georgopoulos C., and, Welch W. J., (1993) Role of the major heat shock proteins as molecular chaperones. Annu. Rev. Cell Biol. 9, 601-634.
35. Giepmans B. N., Adams S. R., Ellisman M. H., and, Tsien R. Y., (2006) The fluorescent toolbox for assessing protein location and function. Science 312, 217-224.
36. Hall L. L., Smith K. P., Byron M., and, Lawrence J. B., (2006) Molecular anatomy of a speckle. Anat. Rec. A Discov. Mol. Cell Evol. Biol. 288, 664-675.
37. Handwerger K. E., and, Gall J. G., (2006) Subnuclear organelles: new insights into form and function. Trends Cell Biol. 16, 19-26.
38. Hernandez-Verdun D., Roussel P., Thiry M., Sirri V., and, Lafontaine D. L., (2010) The nucleolus: structure/function relationship in RNA metabolism. Wiley Interdiscip. Rev. RNA. 1, 415-431.
39. Hetman M., and, Pietrzak M., (2012) Emerging roles of the neuronal nucleolus. Trends Neurosci. 35, 305-314.
40. Hieda M., Winstanley H., Maini P., Iborra F. J., and, Cook P. R., (2005) Different populations of RNA polymerase II in living mammalian cells. Chromosome Res. 13, 135-144.
41. Hut H. M., Kampinga H. H., and, Sibon O. C., (2005) Hsp70 protects mitotic cells against heat-induced centrosome damage and division abnormalities. Mol. Biol. Cell 16, 3776-3785.
42. Jacobs S., Lie D. C., DeCicco K. L., Shi Y., DeLuca L. M., Gage F. H., and, Evans R. M., (2006) Retinoic acid is required early during adult neurogenesis in the dentate gyrus. Proc. Natl Acad. Sci. USA 103, 3902-3907.
43. Kampinga H. H., Hageman J., Vos M. J., Kubota H., Tanguay R. M., Bruford E. A., Cheetham M. E., Chen B., and, Hightower L. E., (2009) Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones. 14, 105-111.
44. Khalouei S., Chow A. M., and, Brown I. R., (2014) Stress-induced localization of HSPA6 (HSP70B') and HSPA1A (HSP70-1) proteins to centrioles in human neuronal cells. Cell Stress Chaperones. 19, 321-327.
45. Kiang J. G., and, Tsokos G. C., (1998) Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology. Pharmacol. Ther. 80, 183-201.
46. Kim Y. E., Hipp M. S., Bracher A., Hayer-Hartl M., and, Ulrich Hartl F., (2013) Molecular chaperone functions in protein folding and proteostasis. Annu. Rev. Biochem. 82, 323-355.
47. Knowlton A. A., and, Salfity M., (1996) Nuclear localization and the heat shock proteins. J. Biosci. 21, 123-132.
48. Korecka J. A., van Kesteren R. E., Blaas E., Spitzer S. O., Kamstra J. H., Smit A. B., Swaab D. F., Verhaagen J., and, Bossers K., (2013) Phenotypic characterization of retinoic acid differentiated SH-SY5Y cells by transcriptional profiling. PLoS ONE 8, e63862.
49. Kotoglou P., Kalaitzakis A., Vezyraki P., Tzavaras T., Michalis L. K., Dantzer F., Jung J. U., and, Angelidis C., (2009) Hsp70 translocates to the nuclei and nucleoli, binds to XRCC1 and PARP-1, and protects HeLa cells from single-strand DNA breaks. Cell Stress Chaperones. 14, 391-406.
50. Kregel K. C., (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J. Appl. Physiol. (1985). 92, 2177-2186.
51. Kumaran R. I., Muralikrishna B., and, Parnaik V. K., (2002) Lamin A/C speckles mediate spatial organization of splicing factor compartments and RNA polymerase II transcription. J. Cell Biol. 159, 783-793.
52. Lam Y. W., Trinkle-Mulcahy L., and, Lamond A. I., (2005) The nucleolus. J. Cell Sci. 118, 1335-1337.
53. Lam Y. W., Lamond A. I., Mann M., and, Andersen J. S., (2007) Analysis of nucleolar protein dynamics reveals the nuclear degradation of ribosomal proteins. Curr. Biol. 17, 749-760.
54. Lamond A. I., and, Spector D. L., (2003) Nuclear speckles: a model for nuclear organelles. Nat. Rev. Mol. Cell Biol. 4, 605-612.
55. Leung T. K., Rajendran M. Y., Monfries C., Hall C., and, Lim L., (1990) The human heat-shock protein family. Expression of a novel heat-inducible HSP70 (HSP70B') and isolation of its cDNA and genomic DNA. Biochem. J. 267, 125-132.
56. Li P., Carter G., Romero J., Gower K. M., Watson J., Patel N. A., and, Cooper D. R., (2013) Clk/STY (cdc2-like kinase 1) and Akt regulate alternative splicing and adipogenesis in 3T3-L1 pre-adipocytes. PLoS ONE 8, e53268.
57. Lindell T. J., Weinberg F., Morris P. W., Roeder R. G., and, Rutter W. J., (1970) Specific inhibition of nuclear RNA polymerase II by alpha-amanitin. Science 170, 447-449.
58. Lindquist S., (1986) The heat-shock response. Annu. Rev. Biochem. 55, 1151-1191.
59. Lindquist S., and, Craig E. A., (1988) The heat-shock proteins. Annu. Rev. Genet. 22, 631-677.
60. Lowry O. H., Rosebrough N. J., Farr A. L., and, Randall R. J., (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
61. Lusic M., Marini B., Ali H., Lucic B., Luzzati R., and, Giacca M., (2013) Proximity to PML Nuclear Bodies Regulates HIV-1 Latency in CD4+ T Cells. Cell Host Microbe 13, 665-677.
62. Mao Y. S., Zhang B., and, Spector D. L., (2011) Biogenesis and function of nuclear bodies. Trends Genet. 27, 295-306.
63. Marin-Vinader L., Shin C., Onnekink C., Manley J. L., and, Lubsen N. H., (2006) Hsp27 enhances recovery of splicing as well as rephosphorylation of SRp38 after heat shock. Mol. Biol. Cell 17, 886-894.
64. Mariner P. D., Walters R. D., Espinoza C. A., Drullinger L. F., Wagner S. D., Kugel J. F., and, Goodrich J. A., (2008) Human Alu RNA is a modular transacting repressor of mRNA transcription during heat shock. Mol. Cell 29, 499-509.
65. Matera A. G., Izaguire-Sierra M., Praveen K., and, Rajendra T. K., (2009) Nuclear bodies: random aggregates of sticky proteins or crucibles of macromolecular assembly? Dev. Cell 17, 639-647.
66. Meguro-Horike M., Yasui D. H., Powell W., Schroeder D. I., Oshimura M., Lasalle J. M., and, Horike S., (2011) Neuron-specific impairment of inter-chromosomal pairing and transcription in a novel model of human 15q-duplication syndrome. Hum. Mol. Genet. 20, 3798-3810.
67. Meldi L., and, Brickner J. H., (2011) Compartmentalization of the nucleus. Trends Cell Biol. 21, 701-708.
68. Milarski K. L., Welch W. J., and, Morimoto R. I., (1989) Cell cycle-dependent association of HSP70 with specific cellular proteins. J. Cell Biol. 108, 413-423.
69. Mita P., Savas J. N., Ha S., Djouder N., Yates J. R., 3rd, and, Logan S. K., (2013) Analysis of URI Nuclear Interaction with RPB5 and Components of the R2TP/Prefoldin-Like Complex. PLoS ONE 8, e63879.
70. Mitchell J. A., and, Fraser P., (2008) Transcription factories are nuclear subcompartments that remain in the absence of transcription. Genes Dev. 22, 20-25.
71. Miyata S., Mizuno T., Koyama Y., Katayama T., and, Tohyama M., (2013) The endoplasmic reticulum-resident chaperone heat shock protein 47 protects the Golgi apparatus from the effects of O-glycosylation inhibition. PLoS ONE 8, e69732.
72. Morimoto R. I., Tissieres A., and, Georgopoulos C., (1994) The Biology of Heat Shock Proteins and Molecular Chaperones. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
73. Mortillaro M. J., Blencowe B. J., Wei X., Nakayasu H., Du L., Warren S. L., Sharp P. A., and, Berezney R., (1996) A hyperphosphorylated form of the large subunit of RNA polymerase II is associated with splicing complexes and the nuclear matrix. Proc. Natl Acad. Sci. USA 93, 8253-8257.
74. Muchowski P. J., and, Wacker J. L., (2005) Modulation of neurodegeneration by molecular chaperones. Nat. Rev. Neurosci. 6, 11-22.
75. Nguyen V. T., Giannoni F., Dubois M. F., Seo S. J., Vigneron M., Kedinger C., and, Bensaude O., (1996) In vivo degradation of RNA polymerase II largest subunit triggered by alpha-amanitin. Nucleic Acids Res. 24, 2924-2929.
76. Noonan E. J., Place R. F., Giardina C., and, Hightower L. E., (2007) Hsp70B' regulation and function. Cell Stress Chaperones. 12, 393-402.
77. Noonan E. J., Fournier G., and, Hightower L. E., (2008) Surface expression of Hsp70B' in response to proteasome inhibition in human colon cells. Cell Stress Chaperones. 13, 105-110.
78. Nover L., Munsche D., Neumann D., Ohme K., and, Scharf K. D., (1986) Control of ribosome biosynthesis in plant cell cultures under heat-shock conditions. Ribosomal RNA. Eur. J. Biochem. 160, 297-304.
79. O'Brien T. P., Bult C. J., Cremer C., et al. (2003) Genome function and nuclear architecture: from gene expression to nanoscience. Genome Res. 13, 1029-1041.
80. Parag H. A., Raboy B., and, Kulka R. G., (1987) Effect of heat shock on protein degradation in mammalian cells: involvement of the ubiquitin system. EMBO J. 6, 55-61.
81. Pardue M. L., Ballinger D. G., and, Hogan N. C., (1992) The heat shock response. Cells coping with transient stress. Ann. N. Y. Acad. Sci. 663, 125-138.
82. Parsian A. J., Sheren J. E., Tao T. Y., Goswami P. C., Malyapa R., Van Rheeden R., Watson M. S., and, Hunt C. R., (2000) The human Hsp70B gene at the HSPA7 locus of chromosome 1 is transcribed but non-functional. Biochim. Biophys. Acta 1494, 201-205.
83. Pelham H. R., (1984) Hsp70 accelerates the recovery of nucleolar morphology after heat shock. EMBO J. 3, 3095-3100.
84. Pickard A. J., and, Bierbach U., (2013) The Cell's Nucleolus: an Emerging Target for Chemotherapeutic Intervention. ChemMedChem 8, 1441-1449.
85. Pietrzak M., Rempala G., Nelson P. T., Zheng J. J., and, Hetman M., (2011) Epigenetic silencing of nucleolar rRNA genes in Alzheimer's disease. PLoS ONE 6, e22585.
86. Raska I., Shaw P. J., and, Cmarko D., (2006) New insights into nucleolar architecture and activity. Int. Rev. Cytol. 255, 177-235.
87. Rieder D., Trajanoski Z., and, McNally J. G., (2012) Transcription factories. Front Genet. 3, 221.
88. Rieder D., Ploner C., Krogsdam A. M., et al. (2014) Co-expressed genes prepositioned in spatial neighborhoods stochastically associate with SC35 speckles and RNA polymerase II factories. Cell. Mol. Life Sci. 71, 1741-1759.
89. Riley B. E., and, Orr H. T., (2006) Polyglutamine neurodegenerative diseases and regulation of transcription: assembling the puzzle. Genes Dev. 20, 2183-2192.
90. Ross C. A., and, Poirier M. A., (2004) Protein aggregation and neurodegenerative disease. Nat. Med. 10 (Suppl), S10-S17.
91. Salsman J., Zimmerman N., Chen T., Domagala M., and, Frappier L., (2008) Genome-wide screen of three herpesviruses for protein subcellular localization and alteration of PML nuclear bodies. PLoS Pathog. 4, e1000100.
92. Schmidt U., Richter K., Berger A. B., and, Lichter P., (2006) In vivo BiFC analysis of Y14 and NXF1 mRNA export complexes: preferential localization within and around SC35 domains. J. Cell Biol. 172, 373-381.
93. Schneider R., and, Grosschedl R., (2007) Dynamics and interplay of nuclear architecture, genome organization, and gene expression. Genes Dev. 21, 3027-3043.
94. Selkoe D. J., (2003) Folding proteins in fatal ways. Nature 426, 900-904.
95. Sharma A., Takata H., Shibahara K., Bubulya A., and, Bubulya P. A., (2010) Son is essential for nuclear speckle organization and cell cycle progression. Mol. Biol. Cell 21, 650-663.
96. Shibata Y., and, Morimoto R. I., (2014) How the Nucleus Copes with Proteotoxic Stress. Curr. Biol. 24, R463-R474.
97. Shin C., Feng Y., and, Manley J. L., (2004) Dephosphorylated SRp38 acts as a splicing repressor in response to heat shock. Nature 427, 553-558.
98. Sirri V., Urcuqui-Inchima S., Roussel P., and, Hernandez-Verdun D., (2008) Nucleolus: the fascinating nuclear body. Histochem. Cell Biol. 129, 13-31.
99. Soto C., and, Estrada L. D., (2008) Protein misfolding and neurodegeneration. Arch. Neurol. 65, 184-189.
100. Spector D. L., and, Lamond A. I., (2011) Nuclear speckles. Cold Spring Harb. Perspect. Biol. 3, pii: a000646.
101. Sutherland H., and, Bickmore W. A., (2009) Transcription factories: gene expression in unions? Nat. Rev. Genet. 10, 457-466.
102. Sytnikova Y. A., Kubarenko A. V., Schafer A., Weber A. N., and, Niehrs C., (2011) Gadd45a is an RNA binding protein and is localized in nuclear speckles. PLoS ONE 6, e14500.
103. Tabellini G., Bortul R., Santi S., et al. (2003) Diacylglycerol kinase-theta is localized in the speckle domains of the nucleus. Exp. Cell Res. 287, 143-154.
104. Tavare J. M., Fletcher L. M., and, Welsh G. I., (2001) Using green fluorescent protein to study intracellular signalling. J. Endocrinol. 170, 297-306.
105. Thiry M., and, Lafontaine D. L., (2005) Birth of a nucleolus: the evolution of nucleolar compartments. Trends Cell Biol. 15, 194-199.
106. Tokunaga K., Shibuya T., Ishihama Y., Tadakuma H., Ide M., Yoshida M., Funatsu T., Ohshima Y., and, Tani T., (2006) Nucleocytoplasmic transport of fluorescent mRNA in living mammalian cells: nuclear mRNA export is coupled to ongoing gene transcription. Genes Cells 11, 305-317.
107. Utans U., Behrens S. E., Luhrmann R., Kole R., and, Kramer A., (1992) A splicing factor that is inactivated during in vivo heat shock is functionally equivalent to the [U4/U6.U5] triple snRNP-specific proteins. Genes Dev. 6, 631-641.
108. Velichko A. K., Markova E. N., Petrova N. V., Razin S. V., and, Kantidze O. L., (2013) Mechanisms of heat shock response in mammals. Cell. Mol. Life Sci. 70, 4229-4241.
109. Vilotti S., Biagioli M., Foti R., Dal Ferro M., Lavina Z. S., Collavin L., Del Sal G., Zucchelli S., and, Gustincich S., (2012) The PML nuclear bodies-associated protein TTRAP regulates ribosome biogenesis in nucleolar cavities upon proteasome inhibition. Cell Death Differ. 19, 488-500.
110. Wei X., Somanathan S., Samarabandu J., and, Berezney R., (1999) Three-dimensional visualization of transcription sites and their association with splicing factor-rich nuclear speckles. J. Cell Biol. 146, 543-558.
111. Welch W. J., and, Feramisco J. R., (1984) Nuclear and nucleolar localization of the 72,000-dalton heat shock protein in heat-shocked mammalian cells. J. Biol. Chem. 259, 4501-4513.
112. Welch W. J., and, Mizzen L. A., (1988) Characterization of the thermotolerant cell. II. Effects on the intracellular distribution of heat-shock protein 70, intermediate filaments, and small nuclear ribonucleoprotein complexes. J. Cell Biol. 106, 1117-1130.
113. Welch W. J., (1992) Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol. Rev. 72, 1063-1081.
114. Woulfe J., (2008) Nuclear bodies in neurodegenerative disease. Biochim. Biophys. Acta 1783, 2195-2206.
115. Xie S. Q., Martin S., Guillot P. V., Bentley D. L., and, Pombo A., (2006) Splicing speckles are not reservoirs of RNA polymerase II, but contain an inactive form, phosphorylated on serine2 residues of the C-terminal domain. Mol. Biol. Cell 17, 1723-1733.
116. Yakovchuk P., Goodrich J. A., and, Kugel J. F., (2009) B2 RNA and Alu RNA repress transcription by disrupting contacts between RNA polymerase II and promoter DNA within assembled complexes. Proc. Natl Acad. Sci. USA 106, 5569-5574.
117. Yost H. J., and, Lindquist S., (1986) RNA splicing is interrupted by heat shock and is rescued by heat shock protein synthesis. Cell 45, 185-193.
118. Yost H. J., and, Lindquist S., (1991) Heat shock proteins affect RNA processing during the heat shock response of Saccharomyces cerevisiae. Mol. Cell. Biol. 11, 1062-1068.
119. Young J. C., (2010) Mechanisms of the Hsp70 chaperone system. Biochem. Cell Biol. 88, 291-300.
120. Zimber A., Nguyen Q. D., and, Gespach C., (2004) Nuclear bodies and compartments: functional roles and cellular signaling in health and disease. Cell. Signal. 16, 1085-1104.