Nuclear speckle localisation of the small heat shock protein αB-crystallin and its inhibition by the R120G cardiomyopathy-linked mutation

Experimental Cell Research

Volumn 287, Issue 2, 2003, Pages 249-261

  Van Den IJssel, Paul ^a,d   Wheelock, Robert ^b   Prescott, Alan ^a   Russell, Paul ^b   Quinlan, Roy A ^c  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b NATIONAL EYE INSTITUTE   (United States)

^c DURHAM UNIVERSITY   (United Kingdom)

^d VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Cardiomyopathy; Chaperone; Interchromatin granules; Nuclear speckles; B crystallin

Indexed keywords

ALPHAB CRYSTALLIN; CELL MARKER; CHAPERONE; HEAT SHOCK PROTEIN 27; ISOPROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG; ALPHA CRYSTALLIN; ANTINEOPLASTIC ANTIBIOTIC; DACTINOMYCIN; HEAT SHOCK PROTEIN; HSPB1 PROTEIN, HUMAN; NUCLEAR PROTEIN; TUMOR MARKER; TUMOR PROTEIN;

ARTICLE; CARDIOMYOPATHY; CELL CULTURE; CELL GRANULE; CELL IMMORTALIZATION; CELL TRANSFORMATION; CHEMICAL ANALYSIS; CONTROLLED STUDY; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HELA CELL; HUMAN; HUMAN CELL; IMMUNOLOCALIZATION; MUTATION; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN VARIANT; RNA SPLICING; TISSUE CULTURE; TWO DIMENSIONAL GEL ELECTROPHORESIS; CELL INCLUSION; CELL LINE; CELL NUCLEUS; CHEMISTRY; COMPARATIVE STUDY; DRUG EFFECT; GENETICS; METABOLISM; PATHOLOGY;

ALPHA-CRYSTALLIN B CHAIN; ANTIBIOTICS, ANTINEOPLASTIC; CARDIOMYOPATHIES; CELL LINE; CELL NUCLEOLUS; CELL NUCLEUS; DACTINOMYCIN; HEAT-SHOCK PROTEINS; HELA CELLS; HUMANS; INCLUSION BODIES; MOLECULAR CHAPERONES; MUTATION; NEOPLASM PROTEINS; NUCLEAR PROTEINS; PROTEIN ISOFORMS; TUMOR MARKERS, BIOLOGICAL;

EID: 0043205911     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4827(03)00092-2     Document Type: Article

References (104)

1. de Jong W.W., Caspers G.J., Leunissen J.A. Genealogy of the alpha-crystallin - small heat-shock protein superfamily. Int. J. Biol. Macromol. 22:1998;151-162.
2. Krief S., Faivre J.F., Robert P., Le Douarin B., Brument-Larignon N., Lefrere I., Bouzyk M.M., Anderson K.M., Greller L.D., Tobin F.L., Souchet M., Bril A. Identification and characterization of cvHsp. A novel human small stress protein selectively expressed in cardiovascular and insulin-sensitive tissues. J. Biol. Chem. 274:1999;36592-36600.
3. Kappe G., Verschuure P., Philipsen R.L., Staalduinen A.A., Van de Boogaart P., Boelens W.C., De Jong W.W. Characterization of two novel human small heat shock proteins protein kinase-related HspB8 and testis-specific HspB9. Biochim. Biophys. Acta. 1520:2001;1-6.
4. Kato K., Shinohara H., Kurobe N., Goto S., Inaguma Y., Ohshima K. Immunoreactive alpha A crystallin in rat non-lenticular tissues detected with a sensitive immunoassay method. Biochim. Biophys. Acta. 1080:1991;173-180.
5. Kato K., Goto S., Inaguma Y., Hasegawa K., Morishita R., Asano T. Purification and characterization of a 20-kDa protein that is highly homologous to alpha B crystallin. J. Biol. Chem. 269:1994;15302-15309.
6. Sugiyama Y., Suzuki A., Kishikawa M., Akutsu R., Hirose T., Waye M.M., Tsui S.K., Yoshida S., Ohno S. 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.
7. Klemenz R., Andres A.C., Frohli E., Schafer R., Aoyama A. Expression of the murine small heat shock proteins hsp 25 and alpha B crystallin in the absence of stress. J. Cell Biol. 120:1993;639-645.
8. Kato K., Shinohara H., Kurobe N., Inaguma Y., Shimizu K., Ohshima K. Tissue distribution and developmental profiles of immunoreactive αB crystallin in the rat non-lenticular tissues determined with a sensitive immunoassay system. Biochim. Biophys. Acta. 1074:1991;201-208.
9. Litt M., Kramer P., LaMorticella D.M., Murphey W., Lovrien E.W., Weleber R.G. Autosomal dominant congenital cataract associated with a missense mutation in the human alpha crystallin gene CRYAA. Hum. Mol. Genet. 7:1998;471-474.
10. Vicart P., Caron A., Guicheney P., Li Z., Prevost M.C., Faure A., Chateau D., Chapon F., Tome F., Dupret J.M., Paulin D., Fardeau M. A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nat. Genet. 20:1998;92-95.
11. V. Berry, P. Francis, M.A. Reddy, D. Collyer, E. Vithana, I. MacKay, G. Dawson, A.H. Carey, A. Moore, S.S. Bhattacharya, R.A. Quinlan, Alpha-B crystallin gene (CRYAB) mutation causes dominant congenital posterior polar cataract in humans. Am. J. Hum. Genet. 69 (2001).
12. Nicholl I.D., Quinlan R.A. Chaperone activity of α-crystallins modulates intermediate filament assembly. EMBO J. 13:1994;945-953.
13. Quinlan R., van den IJssel P. Fatal attraction when chaperone turns harlot. Nat. Med. 5:1999;25-26.
14. Perng M.D., Muchowski P.J., van den IJssel P., Wu G.J.S., Clark J.I., Quinlan R.A. The cardiomyopathy and lens cataract mutation in αB-crystallin compromises secondary, tertiary and quaternary protein structure and reduces in vitro chaperone activity. J. Biol. Chem. 274:1999;33235-33243.
15. Goldfarb L.G., Park K.Y., Cervenakova L., Gorokhova S., Lee H.S., Vasconcelos O., Nagle J.W., Semino-Mora C., Sivakumar K., Dalakas M.C. Missense mutations in desmin associated with familial cardiac and skeletal myopathy. Nat. Genet. 19:1998;402-403.
16. Li D., Tapscoft T., Gonzalez O., Burch P.E., Quinones M.A., Zoghbi W.A., Hill R., Bachinski L.L., Mann D.L., Roberts R. Desmin mutation responsible for idiopathic dilated cardiomyopathy. Circulation. 100:1999;461-464.
17. Dalakas M.C., Park K.Y., Semino-Mora C., Lee H.S., Sivakumar K., Goldfarb L.G. Desmin myopathy, a skeletal myopathy with cardiomyopathy caused by mutations in the desmin gene. N. Engl. J. Med. 342:2000;770-780.
18. Munoz-Marmol A.M., Strasser G., Isamat M., Coulombe P.A., Yang Y., Roca X., Vela E., Mate J.L., Coll J., Fernandez-Figueras M.T., Navas-Palacios J.J., Ariza A., Fuchs E. A dysfunctional desmin mutation in a patient with severe generalized myopathy. Proc. Natl. Acad. Sci. USA. 95:1998;11312-11317.
19. Sjoberg G., Saavedra-Matiz C.A., Rosen D.R., Wijsman E.M., Borg K., Horowitz S.H., Sejersen T. A missense mutation in the desmin rod domain is associated with autosomal dominant distal myopathy, and exerts a dominant negative effect on filament formation. Hum. Mol. Genet. 8:1999;2191-2198.
20. Perng M.D., Cairns L., van den IJssel P., Prescott A., Hutcheson A.M., Quinlan R.A. Intermediate filament interactions can be altered by HSP27 and αB-crystallin. J. Cell Sci. 112:1999;2099-2112.
21. Horwitz J. Alpha-crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. USA. 89:1992;10449-10453.
22. Merck K.B., Groenen P.J., Voorter C.E., de Haard Hoekman W.A., Horwitz J., Bloemendal H., de Jong W.W. Structural and functional similarities of bovine alpha-crystallin and mouse small heat-shock protein. A family of chaperones. J. Biol. Chem. 268:1993;1046-1052.
23. Suzuki A., Sugiyama Y., Hayashi Y., Nyu-i N., Yoshida M., Nonaka I., Ishiura S., Arahata K., Ohno S. MKBP, a novel member of the small heat shock protein family, binds and activates the myotonic dystrophy protein kinase. J. Cell Biol. 140:1998;1113-1124.
24. Velazquez J.M., Lindquist S. hsp70 nuclear concentration during environmental stress and cytoplasmic storage during recovery. Cell. 36:1984;655-662.
25. Kampinga H.H., Brunsting J.F., Stege G.J., Konings A.W., Landry J. Cells overexpressing Hsp27 show accelerated recovery from heat-induced nuclear protein aggregation. Biochem. Biophys. Res. Commun. 204:1994;1170-1177.
26. van de Klundert F.A.J.M., Gijsen M.L.J., van den IJssel P.R.L.A., Snoeckx L.H.E.H., de Jong W.W. alpha B-crystallin and hsp25 in neonatal cardiac cells - differences in cellular localization under stress conditions. Eur. J. Cell Biol. 75:1998;38-45.
27. Velazquez J.M., DiDomenico B.J., Lindquist S. Intracellular localization of heat shock proteins in Drosophila. Cell. 20:1980;679-689.
28. Arrigo A.P., Suhan J.P., Welch W.J. Dynamic changes in the structure and intracellular locale of the mammalian low-molecular-weight heat shock protein. Mol. Cell. Biol. 8:1988;5059-5071.
29. Rossi J.M., Lindquist S. The intracellular location of yeast heat-shock protein 26 varies with metabolism. J. Cell Biol. 108:1989;425-439.
30. Preville X., Schultz H., Knauf U., Gaestel M., Arrigo A.P. Analysis of the role of Hsp25 phosphorylation reveals the importance of the oligomerization state of this small heat shock protein in its protective function against TNFalpha- and hydrogen peroxide-induced cell death. J. Cell Biochem. 69:1998;436-452.
31. Loktionova S.A., Ilyinskaya O.P., Gabai V.L., Kabakov A.E. Distinct effects of heat shock and ATP depletion on distribution and isoform patterns of human Hsp27 in endothelial cells. FEBS Lett. 392:1996;100-104.
32. McClaren M., Isseroff R.R. Dynamic changes in intracellular localization and isoforms of the 27-kD stress protein in human keratinocytes. J. Invest. Dermatol. 102:1994;375-381.
33. van Breukelen F., Maier R., Hand S.C. Depression of nuclear transcription and extension of mRNA half-life under anoxia in Artemia franciscana embryos. J. Exp. Biol. 203:(Pt 7):2000;1123-1130.
34. Willsie J.K., Clegg J.S. Nuclear p26, a small heat shock/ alpha-crystallin protein, and its relationship to stress resistance in Artemia franciscana embryos. J. Exp. Biol. 204:2001;2339-2350.
35. MacRae T.H. Structure and function of small heat shock/alpha-crystallin proteins established concepts and emerging ideas. Cell. Mol. Life Sci. 57:2000;899-913.
36. Andley U.P., Song Z., Wawrousek E.F., Brady J.P., Bassnett S., Fleming T.P. Lens epithelial cells derived from alphaB-crystallin knockout mice demonstrate hyperproliferation and genomic instability. FASEB J. 15:2001;221-229.
37. Sleeman J.E., Lamond A.I. Newly assembled snRNPs associate with coiled bodies before speckles, suggesting a nuclear snRNP maturation pathway [In Process Citation]. Curr. Biol. 9:1999;1065-1074.
38. Bellini M., Gall J.G. Coilin shuttles between the nucleus and cytoplasm in Xenopus oocytes. Mol. Biol. Cell. 10:1999;3425-3434.
39. Boudonck K., Dolan L., Shaw P.J. The movement of coiled bodies visualized in living plant cells by the green fluorescent protein. Mol. Biol. Cell. 10:1999;2297-2307.
40. Kruhlak M.J., Lever M.A., Fischle W., Verdin E., Bazett-Jones D.P., Hendzel M.J. Reduced mobility of the alternate splicing factor (ASF) through the nucleoplasm and steady state speckle compartments. J. Cell Biol. 150:2000;41-51.
41. Phair R.D., Misteli T. High mobility of proteins in the mammalian cell nucleus. Nature. 404:2000;604-609.
42. Yin X., Landay M.F., Han W., Levitan E.S., Watkins S.C., Levenson R.M., Farkas D.L., Prochownik E.V. Dynamic in vivo interactions among Myc network members. Oncogene. 20:2001;4650-4664.
43. Sleeman J.E., Ajuh P., Lamond A.I. snRNP protein expression enhances the formation of Cajal bodies containing p80-coilin and SMN. J. Cell Sci. 114:2001;4407-4419.
44. Raska I., Ochs R.L., Andrade L.E., Chan E.K., Burlingame R., Peebles C., Gruol D., Tan E.M. Association between the nucleolus and the coiled body. J. Struct. Biol. 104:1990;120-127.
45. Antomou M., Carmofonseca M., Ferreira J., Lamond A.I. Nuclear-organization of splicing snrnps during differentiation of murine erythroleukemia-cells in-vitro. J. Cell Biol. 123:1993;1055-1068.
46. Santama N., Dotti C.G., Lamond A.I. Neuronal differentiation in the rat hippocampus involves a stage-specific reorganization of subnuclear structure both in-vivo and in-vitro. Eur. J. Neurosci. 8:1996;892-905.
47. Lain S., Xirodimas D., Lane D.P. Accumulating active p53 in the nucleus by inhibition of nuclear export a novel strategy to promote the p53 tumor suppressor function. Exp. Cell Res. 253:1999;315-324.
48. Dahm R., van Marle J., Prescott A.R., Quinlan R.A. Gap junctions containing alpha8-connexin (MP70) in the adult mammalian lens epithelium suggests a re-evaluation of its role in the lens. Exp. Eye Res. 69:1999;45-56.
49. Muchowski P.J., Hays L.G., Yates J.R. 3rd, Clark J.I. ATP and the core "alpha-crystallin" domain of the small heat-shock protein alphaB-crystallin. J. Biol. Chem. 274:1999;30190-30195.
50. Westendorf J.M., Konstantinov K.N., Wormsley S., Shu M.D., Matsumoto-Taniura N., Pirollet F., Klier F.G., Gerace L., Baserga S.J. M phase phosphoprotein 10 is a human U3 small nucleolar ribonucleoprotein component. Mol. Biol. Cell. 9:1998;437-449.
51. Sandilands A. Characterisation of the intermediate filament proteins filensin and CP49 within the eye lens. Ph.D. thesis. 1995;University of Dundee, Dundee, UK.
52. Roobol A., Grantham J., Whitaker H.C., Carden M.J. Disassembly of the cytosolic chaperonin in mammalian cell extracts at intracellular levels of K+ and ATP. J. Biol. Chem. 274:1999;19220-19227.
53. Hopwood D., Moitra S., Vojtesek B., Johnston D.A., Dillon J.F., Hupp T.R. Biochemical analysis of the stress protein response in human oesophageal epithelium. Gut. 41:1997;156-163.
54. Inaguma Y., Goto S., Shinohara K., Hasegawa K., Ohshima K., Kato K. Physiological and pathological changes in levels of the two small stress proteins, HSP27 and αB-crystallin, in rat hindlimb muscles. J. Biochem. 114:1993;378-384.
55. King R.J., Finley J.R., Coffer A.I., Millis R.R., Rubens R.D. Characterization and biological relevance of a 29-kDa, oestrogen receptor-related protein. J. Steroid Biochem. 27:1987;471-475.
56. Debus E., Weber K., Osborn M. Monoclonal antibodies specific for glial fibrillary acidic (GFA) protein and for each of the neurofilament triplet polypeptides. Differentiation. 25:1983;193-203.
57. Dahm R., Gribbon C., Quinlan R.A., Prescott A.R. Changes in the nucleolar and coiled body compartments precede lamina and chromatin reorganization during fibre cell denucleation in the bovine lens. Eur. J. Cell Biol. 75:1998;237-246.
58. Gribbon C., Dahm R., Prescott A.R., Quinlan R.A. Association of the nuclear matrix component NuMA with the Cajal body and nuclear speckle compartments during transitions in transcriptional activity in lens cell differentiation. Eur. J. Cell Biol. 81:2002;1-10.
59. Merdes A., Ramyar K., Vechio J.D., Cleveland D.W. A complex of NuMA and cytoplasmic dynein is essential for mitotic spindle assembly. Cell. 87:1996;447-458.
60. Kambach C., Mattaj I.W. Intracellular distribution of the U1A protein depends on active transport and nuclear binding to U1 snRNA. J. Cell Biol. 118:1992;11-21.
61. Laemmli U. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 277:1970;680-685.
62. Bradford M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254.
63. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets. Proc. Natl. Acad. Sci. USA. 76:1979;4350-4354.
64. Sandilands A., Prescott A.R., Carter J.M., Hutcheson A.M., Quinlan R.A., Richards J., FitzGerald P.G. Vimentin and CP49/Filensin form distinct networks in the lens which are independantly modulated during lens fibre cell differentiation. J. Cell Sci. 108:1995;1397-1406.
65. Iwaki T., Iwaki A., Tateishi J., Goldman J.E. Sense and antisense modification of glial alpha B-crystallin production results in alterations of stress fiber formation and thermoresistance. J. Cell Biol. 125:1994;1385-1393.
66. Tumminia S.J., Russell P. Alpha B-crystallin accumulation in human astroglioma cell line U373MG is stress-dependent and phosphorylation- independent. J. Biochem. Tokyo. 116:1994;973-979.
67. Ito H., Okamoto K., Nakayama H., Isobe T., Kato K. Phosphorylation of alpha B-crystallin in response to various types of stress. J. Biol. Chem. 272:1997;29934-29941.
68. Wisniewski T., Goldman J.E. alpha B-crystallin is associated with intermediate filaments in astrocytoma cells. Neurochem. Res. 23:1998;385-392.
69. Koyama Y., Goldman J.E. Formation of GFAP cytoplasmic inclusions in astrocytes and their disaggregation by alphaB-crystallin [In Process Citation]. Am. J. Pathol. 154:1999;1563-1572.
70. Andrade L.E., Chan E.K., Raska I., Peebles C.L., Roos G., Tan E.M. Human autoantibody to a novel protein of the nuclear coiled body immunological characterization and cDNA cloning of p80-coilin. J. Exp. Med. 173:1991;1407-1419.
71. Ramon-y-Cajal S. Un sencillo metodo de coloracion selectiva del reticulo protoplamico y sus efectos en los diversos organos nerviosos de vertebrados e invertebrdos. Trab. Lab. Invest. Biol. 2:1903;129-221.
72. Andersen J.S., Lyon C.E., Fox A.H., Leung A.K., Lam Y.W., Steen H., Mann M., Lamond A.I. Directed proteomic analysis of the human nucleolus. Curr. Biol. 12:2002;1-11.
73. Bhat S.P., Hale I.L., Matsumoto B., Elghanayan D. Ectopic expression of alpha B-crystallin in Chinese hamster ovary cells suggests a nuclear role for this protein. Eur. J. Cell Biol. 78:1999;143-150.
74. Ito H., Kamei K., Iwamoto I., Inaguma Y., Nohara D., Kato K. Phosphorylation-induced change of the oligomerization state of alpha B-crystallin. J. Biol. Chem. 276:2001;5346-5352.
75. Benndorf R., Hayess K., Ryazantsev S., Wieske M., Behlke J., Lutsch G. Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. J. Biol. Chem. 269:1994;20780-20784.
76. Rogalla T., Ehrnsperger M., Preville X., Kotlyarov A., Lutsch G., Ducasse C., Paul C., Wieske M., Arrigo A.P., Buchner J., Gaestel M. Regulation of Hsp27 oligomerization, chaperone function, and protective activity against oxidative stress/tumor necrosis factor alpha by phosphorylation. J. Biol. Chem. 274:1999;18947-18956.
77. Wieske M., Benndorf R., Behlke J., Dolling R., Grelle G., Bielka H., Lutsch G. Defined sequence segments of the small heat shock proteins HSP25 and alphaB-crystallin inhibit actin polymerization. Eur. J. Biochem. 268:2001;2083-2090.
78. Lyon C.E., Bohmann K., Sleeman J., Lamond A.I. Inhibition of protein dephosphorylation results in the accumulation of splicing snRNPs and coiled bodies within the nucleolus. Exp. Cell Res. 230:1997;84-93.
79. Wei X., Somanathan S., Samarabandu J., Berezney R. Three-dimensional visualization of transcription sites and their association with splicing factor-rich nuclear speckles. J. Cell Biol. 146:1999;543-558.
80. Lamond A.I., Earnshaw W.C. Structure and function in the nucleus. Science. 280:1998;547-553.
81. Dundr M., Misteli T. Functional architecture in the cell nucleus. Biochem. J. 356:2001;297-310.
82. Pederson T. Protein mobility within the nucleus - what are the right moves. Cell. 104:2001;635-638.
83. Bova M.P., Yaron O., Huang Q., Ding L., Haley D.A., Stewart P.L., Horwitz J. Mutation R120G in alphaB-crystallin, which is linked to a desmin-related myopathy, results in an irregular structure and defective chaperone-like function [In Process Citation]. Proc. Natl. Acad. Sci. USA. 96:1999;6137-6142.
84. Wang X., Osinska H., Klevitsky R., Gerdes A.M., Nieman M., Lorenz J., Hewett T., Robbins J. Expression of R120G-alphaB-crystallin causes aberrant desmin and alphaB-crystallin aggregation and cardiomyopathy in mice. Circ. Res. 89:2001;84-91.
85. Wang X., Osinska H., Dorn G.W. 2nd, Nieman M., Lorenz J.N., Gerdes A.M., Witt S., Kimball T., Gulick J., Robbins J. Mouse model of desmin-related cardiomyopathy. Circulation. 103:2001;2402-2407.
86. Grossi d.S.M., Martins d.S.C., Harper F., Olink C.M., Huesca M., Scherrer K. The association of prosomes with some of the intermediate filament networks of the animal cell [published erratum appears in J. Cell Biol. 1989 Mar;108(3):following 1175]. J. Cell Biol. 107:1988;1517-1530.
87. Preville X., Gaestel M., Arrigo A.P. Phosphorylation is not essential for protection of L929 cells by Hsp25 against H2O2-mediated disruption actin cytoskeleton, a protection which appears related to the redox change mediated by Hsp25. Cell Stress Chaperones. 3:1998;177-187.
88. Misteli T. Protein dynamics implications for nuclear architecture and gene expression. Science. 291:2001;843-847.
89. Bajramovic J.J., Bsibsi M., Geutskens S.B., HAsankhan R., Verhulst K.C., Stege G.J.J., de Groot C.J.A., van Noort J.M. Differential expression of stress proteins in human adult astrocytes in response to cytokines. J. Neuroimmunol. 106:2000;14-22.
90. Biggiogera M., Tanguay R.M., Marin R., Wu Y., Martin T.E., Fakan S. Localization of heat shock proteins in mouse male germ cells an immunoelectron microscopical study. Exp. Cell Res. 229:1996;77-85.
91. Bickmore W.A., Sutherland H.G. Addressing protein localization within the nucleus. EMBO J. 21:2002;1248-1254.
92. Ito H., Kamei K., Iwamoto I., Inaguma Y., Garcia-Mata R., Sztul E., Kato K. Inhibition of proteasomes induces accumulation, phosphorylation, and recruitment of HSP27 and alphaB-crystallin to aggresomes. J. Biochem. (Tokyo). 131:2002;593-603.
93. Jäkel S., Mingot J.M., Schwarzmaier P., Hartmann E., Gorlich D. Importins fulfil a dual function as nuclear import receptors and cytoplasmic chaperones for exposed basic domains. EMBO J. 21:2002;377-386.
94. Mortillaro M.J., Berezney R. Matrin CYP, an SR-rich cyclophilin that associates with the nuclear matrix and splicing factors. J. Biol. Chem. 273:1998;8183-8192.
95. Horowitz D.S., Lee E.J., Mabon S.A., Misteli T. A cyclophilin functions in pre-mRNA splicing. EMBO J. 21:2002;470-480.
96. Zeng C., He D., Berget S.M., Brinkley B.R. Nuclear-mitotic apparatus protein a structural protein interface between the nucleoskeleton and RNA splicing. Proc. Natl. Acad. Sci. USA. 91:1994;1505-1509.
97. Roti Roti J.L., Kampinga H.H., Malyapa R.S., Wright W.D., vanderWaal R.P., Xu M. Nuclear matrix as a target for hyperthermic killing of cancer cells. Cell Stress Chaperones. 3:1998;245-255.
98. Ehrnsperger M., Graber S., Gaestel M., Buchner J. Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. EMBO J. 16:1997;221-229.
99. Lee G.J., Vierling E. A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiol. 122:2000;189-198.
100. Pietrowski D., Durante M.J., Liebstein A., Schmitt-John T., Werner T., Graw J. Alpha-crystallins are involved in specific interactions with the murine gamma D/E/F-crystallin-encoding gene. Gene. 144:1994;171-178.
101. Pietrowski D., Graw J. Autokinase activity of alpha-crystallin inhibits its specific interaction with the DOTIS element in the murine gamma D/E/F-crystallin promoter in vitro. Biol. Chem. 378:1997;1183-1186.
102. Aguilera A. The connection between transcription and genomic instability. EMBO J. 21:2002;195-201.
103. Tini M., Benecke A., Um S.J., Torchia J., Evans R.M., Chambon P. Association of CBP/p300 acetylase and thymine DNA glycosylase links DNA repair and transcription. Mol. Cell. 9:2002;265-277.
104. Inoue A., Takahashi M., Hatta K., Hotta Y., Okamoto H. Developmental regulation of Islet-1 mRNA expression during neuronal differentiation in embryonic zebrafish. Dev. Dyn. 199:1994;1-11.