Effects of heat shock on the distribution and expression levels of nuclear proteins in HeLa S3 cells

Journal of Cellular Biochemistry

Volumn 105, Issue 6, 2008, Pages 1485-1500

  Haddad, Nisrine ^a   Paulin Levasseur, Micheline ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Heat shock; HeLa S3 cells; Nuclear envelope; Nuclear function structure relationships; Nuclear interior; Nuclear matrix

Indexed keywords

EMERIN; FIBRILLARIN; HEAT SHOCK PROTEIN 70; LAMIN A; LAMIN ASSOCIATED PROTEIN 2BETA; LAMIN C; NUCLEAR PROTEIN; NUCLEOCYTOPLASMIC TRANSPORT PROTEIN; NUCLEOCYTOPLASMIC TRANSPORT PROTEIN 2A7; NUCLEOLAR PROTEIN 2H12; UNCLASSIFIED DRUG;

ARTICLE; BIOLOGICAL MONITORING; CELL CYCLE; CELL CYCLE PROGRESSION; CELL GROWTH; CELL STRESS; CELL VIABILITY; CELLULAR DISTRIBUTION; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; HEAT SHOCK; HEAT STRESS; HUMAN; HUMAN CELL; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

CELL CYCLE; CELL PROLIFERATION; CELL SURVIVAL; CHROMOSOMAL PROTEINS, NON-HISTONE; FEVER; FLUORESCENT ANTIBODY TECHNIQUE; HEAT-SHOCK RESPONSE; HELA CELLS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; NUCLEAR ENVELOPE; NUCLEAR PROTEINS;

EID: 57349153151     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21968     Document Type: Article

References (62)

1. Benavente R, Krohne G. 1986. Involvement of nuclear lamins in postmitotic reorganization of chromatin as demonstrated by microinjection of lamin antibodies. J Cell Biol 103:1847-1854.
2. Berezney R. 1991. The nuclear matrix: A heuristic model for investigating genomic organization and function in the cell nucleus. J Cell Biochem 47:109-123.
3. Biamonti G. 2004. Nuclear stress bodies: A heterochromatin affair? Nat Rev Mol Cell Biol 5:493-498.
4. Bosman FT. 1999. The nuclear matrix in pathology. Virchows Arch 435:391-399.
5. Bond U. 1988. Heat shock but no 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.
6. Cai M, Huang Y, Ghirlando R, Wilson KL, Craigie R, Clore GM. 2001. Solution structure of the constant region of nuclear envelope protein LAP2 reveals two LEM-domain structures: One binds BAF and the other binds DNA. EMBO J 20:4399-4407.
7. Caizergues-Ferrer M, Dousseau F, Gas N, Bouche G, Stevens B, Almaric F. 1984. Induction of new proteins in the nuclear matrix of CHO cells by a heat shock: Detection of a specific set in the nucleolar matrix. Biochem Biophys Res Commun 118:444-450.
8. Celis JE. 1994. Cell biology. A Laboratory Handbook. London, UK: Academic Press Limited. pp 387-393.
9. Chaly N, Bladon T, Setterfield G, Little JE, Kaplan JG, Brown DL. 1984. Changes in distribution of nuclear matrix antigens during the mitotic cycle. J Cell Biol 99:661-671.
10. Chaly N, Little J, Brown DL. 1985. Localization of nuclear antigens during preparation of nuclear matrices in situ. Can J Biochem Cell Biol 63:644-653.
11. Clements L, Manilal S, Love DR, Morris GE. 2000. Direct interaction between emerin and lamin A. Biochem Biophys Res Commun 267(3): 709-714.
12. Dechat T, Gotzmann J, Stockinger A, Harris CA, Talle MA, Siekierka JJ, Foisner R. 1998. Detergent-salt resistance of LAP2 alpha in interphase nuclei and phosphorylation-dependent association with chromosomes early in nuclear assembly implies functions in nuclear structure dynamics. EMBO J 17:4887-4902.
13. De Maio A. 1999. Heat shock proteins: Facts, thoughts and dreams. Shock 11:1-12.
14. Dynlacht JR, Story MD, Zhu W-G, Danner J. 1999. Lamin B is a prompt heat shock protein. J Cell Physiol 178:28-34.
15. Fairley EA, Kendrick-Jones J, Ellis JA. 1999. The Emery-Dreifuss muscular dystrophy phenotype arises from aberrant targeting and binding of emerin at the inner nuclear membrane. J Cell Sci 112:2571-2582.
16. Fisher DZ, Chaudary N, Blobel G. 1986. cDNA sequencing of nuclear lamins A and C reveals primary and secondary structural homology to intermediate filament proteins. Proc Natl Acad Sci USA 83:6450-6454.
17. Foisner R, Gerace L. 1993. Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes, and binding is modulated by mitotic phosphorylation. Cell 73:1267-1279.
18. Furukawa K. 1999. LAP2 binding protein I (L2BP1/BAF) is a candidate mediator of LAP2-chromatin interaction. J Cell Sci 112:2485-2492.
19. Furukawa K, Fritze CE, Gerace L. 1998. The major nuclear envelope targeting domain of LAP2 coincides with its lamin binding region but is distinct from its chromatin interaction domain. J Biol Chem 273:4213-4219.
20. Furukawa K, Glass C, Kondo T. 1997. Characterization of the chromatin binding activity of lamina-associated polypeptide (LAP) 2. Biochem Biophys Res Commun 238(1): 240-246.
21. Furukawa K, Pante N, Aebi U, Gerace L. 1995. Cloning of a cDNA for lamina-associated polypeptide 2 (LAP2) and identification of regions that specify targeting to the nuclear envelope. EMBO J 14:1626-1636.
22. Fuse T, Yamada K, Asai K, Kato T, Nakanishi M. 1996. Heat shock-mediated cell cycle arrest is accompanied by induction of p21 CKI. Biochem Biophys Res Comm 225:759-763.
23. Gerace L, Burke B. 1988. Functional organization of the nuclear envelope. Annu Rev Cell Biol 4:335-374.
24. Gruenbaum Y, Wilson KL, Harel A, Goldberg M, Cohen M. 2000. Review: Nuclear lamins - Structural proteins with fundamental functions. J Struct Biol 129(2-3): 313-323.
25. Haraguchi T, Koujin T, Hayakawa T, Kaneda T, Tsutsumi C, Imamoto N, Akazawa C, Sukegawa J, Yoneda Y, Hiraoka Y. 2000. Live fluorescence imaging reveals early recruitment of emerin, LBR, RanBP2, and Nup153 to reforming functional nuclear envelopes. J Cell Sci 113:779-794.
26. Holaska JM, Lee KK, Kowalski AK, Wilson KL. 2003. Transcriptional repressor germ cell-less (GCL) and barrier to integration factor (BAF) compete for binding to emerin in vitro. J Biol Chem 278(9): 6969-6975.
27. Hut HMJ, Kampinga HH, Sibon OCM. 2005. Hsp70 protects mitotic cells against heat-induced centrosome damage and division abnormalities. Mol Biol Cell 16:3776-3785.
28. Kühl NM, Rensing L. 2000. Heat shock effects on cell cycle progression. Cell Mol Life Sci 57:450-461.
29. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
30. Lamarre D, Talbot B, de Murcia G, Laplante C, Leduc Y, Mazen A, Poirier GG. 1988. Structural and functional analysis of poly(ADP ribose) polymerase: An immunological study. Biochim Biophys Acta 950(2): 147-160.
31. Lee KK, Haraguchi T, Lee RS, Koujin T, Hiroaka Y, Wilson KL. 2001. Distinct functional domains in emerin bind lamin A and DNA-bridging protein BAF. J Cell Sci 114:4567-4573.
32. Li GC, Werb Z. 1982. Correlation between synthesis of heat shock proteins and development of thermotolerance in Chinese hamster fibroblasts. Proc Natl Acad Sci USA 79:3218-3222.
33. Lin F, Blake DL, Callebaut I, Skerjanc IS, Holmer L, McBurney MW, Paulin-Levasseur M, Worman HJ. 2000. MAN1, an inner nuclear membrane protein that shares the LEM domain with lamina-associated polypeptide 2 and emerin. J Biol Chem 275:4840-4847.
34. Luus L, Paulin-Levasseur M. 1997. Characterization of the 1B4 antigen. Mol Biol Cell 8:217a.
35. Manilal S, Nguyen TM, Sewry CA, Morris GE. 1996. The Emery-Dreifuss muscular dystrophy protein, emerin, is a nuclear membrane protein. Hum Mol Genet 5:801-808.
36. Marshall WF, Fung JC, Sedat JW. 1997. Deconstructing the nucleus: Global architecture from local interactions. Curr Opin Genet Dev 7:259-263.
37. McKeon FD, Kirshner MW, Caput D. 1986. Homologies in both primary and secondary structure between nuclear envelope and intermediate filaments proteins. Nature 319:463-468.
38. Miyamoto Y, Saiwaki T, Yamashita J, Yasuda Y, Kotera I, Shibata S, Shigeta M, Hiraoka Y, Haraguchi T, Yoneda Y. 2004. Cellular stresses induce the nuclear accumulation of importin α and cause a conventional nuclear import block. J Cell Biol 165:617-623.
39. Morimoto RI, Tissieres A, Georgopoulos C, editors. 1990. The stress response, function of the proteins, and perspectives. In: Stress proteins in biology and medicine. New York: Cold Spring Harbor Laboratory Press. pp 1-36.
40. Nagano A, Koga R, Ogawa M, Kurano Y, Kawada J, Okada R, Hayashi YK, Tsukahara T, Arahata K. 1996. Emerin deficiency at the nuclear membrane in patients with Emery-Dreifuss muscular dystrophy. Nat Genet 12:254-259.
41. Nickerson JA. 1998. Nuclear dreams: The malignant alteration of nuclear architecture. J Cell Biochem 70:172-180.
42. Nili E, Cojocaru GS, Kalma Y, Ginsberg D, Copeland NG, Gilbert DJ, Jenkins NA, Berger R, Shaklai S, Amariglio N, Brok-Simoni F, Simon AJ, Rechavi G. 2001. Nuclear membrane protein LAP2beta mediates transcriptional repression alone and together with its binding partner GCL (germ-cell-less). J Cell Sci 114:3297-3307.
43. Ochs RL, Smetana K. 1991. Detection of fibrillarin in nucleolar remnants and the nucleolar matrix. Exp Cell Res 197:183-190.
44. Ornelles DA, Penman S. 1990. Prompt heat-shock and heat-shifted proteins associated with the nuclear matrix-intermediate filament scaffold in Drosophila melanogaster cells. J Cell Sci 95:393-404.
45. Park HG, Han SI, Oh SY, Kang HS. 2005. Cellular responses to mild heat stress. Cell Mol Life Sci 62:10-23.
46. Paulin-Levasseur M, Julien M. 1999. Characterization of the 2A7 antigen as a 85-kDa human nucleocytoplasmic shuttling protein. Exp Cell Res 250:439-451.
47. Paulin-Levasseur M, Julien M, Horner M, Chen G. 1995. Characterization of the 2H12 antigen as a nonshuttling human isoelectric variant of the nucleolar protein B23. Exp Cell Res 219:514-526.
48. Pederson T. 1998. Thinking about a nuclear matrix. J Mol Biol 277:147-159.
49. Pederson T. 2000. Half a century of "the nuclear matrix". Mol Biol Cell 11(3):799-805.
50. Read RA, Fox MH, Bedford JS. 1984. The cell cycle dependence of thermotolerance. 2. CHO cells heated at 45°C. Radiat Res 98:491-505.
51. Reiter T, Penman S. 1983. "Prompt" heat shock proteins: Translationally regulated synthesis of new proteins associated with the nuclear matrix-intermediate filaments as an early response to heat shock. Proc Natl Acad Sci USA 80:4737-4741.
52. Stierle V, Couprie J, Ostlund C, Krimm I, Zinn-Justin S, Hossenlop P, Worman HJ, Courvalin J. 2003. The carboxyl-terminal region common to lamins A and C contains a DNA binding domain. Biochem 42(17): 4819-4828.
53. Sugano T, Nitta M, Ohmori H, Yamaizumi M. 1995. Nuclear accumulation of p53 in normal human fibroblasts is induced by various cellular stresses which evoke the heat shock response, independently of the cell cycle. Jpn Cancer Res 86:415-418.
54. Sullivan T, Escalante-Alcade D, Bhatt H, Anver M, Bhat N, Nagashima K, Stewart CL, Burke B. 1999. Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J Cell Biol 147:913-920.
55. Tran EJ, Wente SR. 2006. Dynamic nuclear pore complexes: Life on the edge. Cell 125(6): 1041-1053.
56. Ulitzur N, Harel A, Feinstein N, Gruenbaum Y. 1992. Lamin activity is essential for nuclear envelope assembly in a Drosophila embryo cell-free extract. J Cell Biol 119:17-25.
57. Valgardsdottir R, Chiodi I, Giordano M, Cobianchi F, Riva S, Biamonti G. 2005. Structural and functional characterization of noncoding repetitive RNAs transcribed in stressed human cells. Mol Biol Cell 16:2597-2604.
58. Valgardsdottir R, Chiodi I, Giordano M, Rossi A, Bazzani S, Ghigna C, Riva S, Biamonti G. 2008. Transcription of Satellite III non-coding RNAs is a general stress response in human cells. Nucleic Acids Res 36(2): 423-434.
59. Wang Y, Guan J, Wang H, Wang Y, Leeper D, Iliakis G. 2001. Regulation of DNA replication after heat shock by replication protein A-nucleolin interactions. J Biol Chem 276:20579-20588.
60. Wilson KL. 2000. The nuclear envelope, muscular dystrophy and gene expression. Trends Cell Biol 10:125-129.
61. Worman HJ, Courvalin J-C. 2000. The inner nuclear membrane. J Membr Biol 177:1-11.
62. Zhu W-G, Roberts ZV, Dynlacht JR. 1999. Heat-induced modulation of lamin B content in two different cell lines. J Cell Biochem 75:620-628.