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. 1984 Oct 1;99(4):1316–1323. doi: 10.1083/jcb.99.4.1316

Cell-specific expression of heat shock proteins in chicken reticulocytes and lymphocytes

PMCID: PMC2113331  PMID: 6480695

Abstract

We have found that chicken reticulocytes respond to elevated temperatures by the induction of only one heat shock protein, HSP70, whereas lymphocytes induce the synthesis of all four heat shock proteins (89,000 mol wt, HSP89; 70,000 mol wt, HSP70; 23,000 mol wt, HSP23; and 22,000 mol wt, HSP22). The synthesis of HSP70 in lymphocytes was rapidly induced by small increases in temperature (2 degrees-3 degrees C) and blocked by preincubation with actinomycin D. Proteins normally translated at control temperatures in reticulocytes or lymphocytes were not efficiently translated after incubation at elevated temperatures. The preferential translation of mRNAs that encode the heat shock proteins paralleled a block in the translation of other cellular proteins. This effect was most prominently observed in reticulocytes where heat shock almost completely repressed alpha- and beta-globin synthesis. HSP70 is one of the major nonglobin proteins in chicken reticulocytes, present in the non-heat-shocked cell at approximately 3 X 10(6) molecules per cell. We compared HSP70 from normal and heat-shocked reticulocytes by two-dimensional gel electrophoresis and by digestion with Staphylococcus aureus V8 protease and found no detectable differences to suggest that the P70 in the normal cell is different from the heat shock-induced protein, HSP70. P70 separated by isoelectric focusing gel electrophoresis into two major protein spots, an acidic P70A (apparent pl = 5.95) and a basic P70B (apparent pl = 6.2). We observed a tissue-specific expression of P70A and P70B in lymphocytes and reticulocytes. In lymphocytes, P70A is the major 70,000-mol-wt protein synthesized at normal temperatures whereas only P70B is synthesized at normal temperatures in reticulocytes. Following incubation at elevated temperatures, the synthesis of both HSP70A and HSP70B was rapidly induced in lymphocytes, but synthesis of only HSP70B was induced in reticulocytes.

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Selected References

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  1. Arrigo A. P., Fakan S., Tissières A. Localization of the heat shock-induced proteins in Drosophila melanogaster tissue culture cells. Dev Biol. 1980 Jul;78(1):86–103. doi: 10.1016/0012-1606(80)90320-6. [DOI] [PubMed] [Google Scholar]
  2. Ashburner M., Bonner J. J. The induction of gene activity in drosophilia by heat shock. Cell. 1979 Jun;17(2):241–254. doi: 10.1016/0092-8674(79)90150-8. [DOI] [PubMed] [Google Scholar]
  3. Bensaude O., Babinet C., Morange M., Jacob F. Heat shock proteins, first major products of zygotic gene activity in mouse embryo. Nature. 1983 Sep 22;305(5932):331–333. doi: 10.1038/305331a0. [DOI] [PubMed] [Google Scholar]
  4. Bensaude O., Morange M. Spontaneous high expression of heat-shock proteins in mouse embryonal carcinoma cells and ectoderm from day 8 mouse embryo. EMBO J. 1983;2(2):173–177. doi: 10.1002/j.1460-2075.1983.tb01401.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bienz M., Gurdon J. B. The heat-shock response in Xenopus oocytes is controlled at the translational level. Cell. 1982 Jul;29(3):811–819. doi: 10.1016/0092-8674(82)90443-3. [DOI] [PubMed] [Google Scholar]
  6. Bonanou-Tzedaki S. A., Sohi M. K., Arnstein H. R. Regulation of protein synthesis in reticulocyte lysates. Characterization of the inhibitor generated in the postribosomal supernatant by heating at 44 degrees C. Eur J Biochem. 1981;114(1):69–77. [PubMed] [Google Scholar]
  7. Cleveland D. W., Fischer S. G., Kirschner M. W., Laemmli U. K. Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J Biol Chem. 1977 Feb 10;252(3):1102–1106. [PubMed] [Google Scholar]
  8. Eden F. C., Hendrick J. P. Unusual organization of DNA sequences in the chicken. Biochemistry. 1978 Dec 26;17(26):5838–5844. doi: 10.1021/bi00619a035. [DOI] [PubMed] [Google Scholar]
  9. Findly R. C., Pederson T. Regulated transcription of the genes for actin and heat-shock proteins in cultured Drosophila cells. J Cell Biol. 1981 Feb;88(2):323–328. doi: 10.1083/jcb.88.2.323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fleischman R. A., Custer R. P., Mintz B. Totipotent hematopoietic stem cells: normal self-renewal and differentiation after transplantation between mouse fetuses. Cell. 1982 Sep;30(2):351–359. doi: 10.1016/0092-8674(82)90233-1. [DOI] [PubMed] [Google Scholar]
  11. Gerner E. W., Russell D. H. The relationship between polyamine accumulation and DNA replication in synchronized Chinese hamster ovary cells after heat shock. Cancer Res. 1977 Feb;37(2):482–489. [PubMed] [Google Scholar]
  12. Ingolia T. D., Slater M. R., Craig E. A. Saccharomyces cerevisiae contains a complex multigene family related to the major heat shock-inducible gene of Drosophila. Mol Cell Biol. 1982 Nov;2(11):1388–1398. doi: 10.1128/mcb.2.11.1388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Joffe J., Keene M., Weintraub H. Histones H2a, H2b, H3, and H4 are present in equimolar amounts in chick erythroblasts. Biochemistry. 1977 Mar 22;16(6):1236–1238. doi: 10.1021/bi00625a032. [DOI] [PubMed] [Google Scholar]
  14. Johnston D., Oppermann H., Jackson J., Levinson W. Induction of four proteins in chick embryo cells by sodium arsenite. J Biol Chem. 1980 Jul 25;255(14):6975–6980. [PubMed] [Google Scholar]
  15. Kelley P. M., Schlesinger M. J. Antibodies to two major chicken heat shock proteins cross-react with similar proteins in widely divergent species. Mol Cell Biol. 1982 Mar;2(3):267–274. doi: 10.1128/mcb.2.3.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kelley P. M., Schlesinger M. J. The effect of amino acid analogues and heat shock on gene expression in chicken embryo fibroblasts. Cell. 1978 Dec;15(4):1277–1286. doi: 10.1016/0092-8674(78)90053-3. [DOI] [PubMed] [Google Scholar]
  17. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  18. Laskey R. A., Mills A. D. Quantitative film detection of 3H and 14C in polyacrylamide gels by fluorography. Eur J Biochem. 1975 Aug 15;56(2):335–341. doi: 10.1111/j.1432-1033.1975.tb02238.x. [DOI] [PubMed] [Google Scholar]
  19. Levinson W., Oppermann H., Jackson J. Transition series metals and sulfhydryl reagents induce the synthesis of four proteins in eukaryotic cells. Biochim Biophys Acta. 1980;606(1):170–180. doi: 10.1016/0005-2787(80)90108-2. [DOI] [PubMed] [Google Scholar]
  20. Li G. C., Werb Z. Correlation between synthesis of heat shock proteins and development of thermotolerance in Chinese hamster fibroblasts. Proc Natl Acad Sci U S A. 1982 May;79(10):3218–3222. doi: 10.1073/pnas.79.10.3218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lindquist S. Translational efficiency of heat-induced messages in Drosophila melanogaster cells. J Mol Biol. 1980 Feb 25;137(2):151–158. doi: 10.1016/0022-2836(80)90322-8. [DOI] [PubMed] [Google Scholar]
  22. McAlister L., Finkelstein D. B. Heat shock proteins and thermal resistance in yeast. Biochem Biophys Res Commun. 1980 Apr 14;93(3):819–824. doi: 10.1016/0006-291x(80)91150-x. [DOI] [PubMed] [Google Scholar]
  23. McKenzie S. L., Meselson M. Translation in vitro of Drosophila heat-shock messages. J Mol Biol. 1977 Nov 25;117(1):279–283. doi: 10.1016/0022-2836(77)90035-3. [DOI] [PubMed] [Google Scholar]
  24. Mizuno S. Temperature sensitivity of protein synthesis initiation in the reticulocyte lysate system. Reduced formation of the 40 S ribosomal subunit - Met-tRNAf complex at an elevated temperature. Biochim Biophys Acta. 1975 Dec 19;414(3):273–282. doi: 10.1016/0005-2787(75)90166-5. [DOI] [PubMed] [Google Scholar]
  25. Mogensen C. E. The glomerular permeability determined by dextran clearance using Sephadex gel filtration. Scand J Clin Lab Invest. 1968;21(1):77–82. doi: 10.3109/00365516809076979. [DOI] [PubMed] [Google Scholar]
  26. Morange M., Diu A., Bensaude O., Babinet C. Altered expression of heat shock proteins in embryonal carcinoma and mouse early embryonic cells. Mol Cell Biol. 1984 Apr;4(4):730–735. doi: 10.1128/mcb.4.4.730. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nevins J. R. Induction of the synthesis of a 70,000 dalton mammalian heat shock protein by the adenovirus E1A gene product. Cell. 1982 Jul;29(3):913–919. doi: 10.1016/0092-8674(82)90453-6. [DOI] [PubMed] [Google Scholar]
  28. O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
  29. Palzer R. J., Heidelberger C. Influence of drugs and synchrony on the hyperthermic killing of HeLa cells. Cancer Res. 1973 Feb;33(2):422–427. [PubMed] [Google Scholar]
  30. Roberts N. J., Jr, Steigbigel R. T. Hyperthermia and human leukocyte functions: effects on response of lymphocytes to mitogen and antigen and bactericidal capacity of monocytes and neutrophils. Infect Immun. 1977 Dec;18(3):673–679. doi: 10.1128/iai.18.3.673-679.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Spradling A., Pardue M. L., Penman S. Messenger RNA in heat-shocked Drosophila cells. J Mol Biol. 1977 Feb 5;109(4):559–587. doi: 10.1016/s0022-2836(77)80091-0. [DOI] [PubMed] [Google Scholar]
  32. Storti R. V., Scott M. P., Rich A., Pardue M. L. Translational control of protein synthesis in response to heat shock in D. melanogaster cells. Cell. 1980 Dec;22(3):825–834. doi: 10.1016/0092-8674(80)90559-0. [DOI] [PubMed] [Google Scholar]
  33. Thomas G. P., Welch W. J., Mathews M. B., Feramisco J. R. Molecular and cellular effects of heat-shock and related treatments of mammalian tissue-culture cells. Cold Spring Harb Symp Quant Biol. 1982;46(Pt 2):985–996. doi: 10.1101/sqb.1982.046.01.092. [DOI] [PubMed] [Google Scholar]
  34. Velazquez J. M., DiDomenico B. J., Lindquist S. Intracellular localization of heat shock proteins in Drosophila. Cell. 1980 Jul;20(3):679–689. doi: 10.1016/0092-8674(80)90314-1. [DOI] [PubMed] [Google Scholar]
  35. Vincent M., Tanguay R. M. Heat-shock induced proteins present in the cell nucleus of Chironomus tentans salivary gland. Nature. 1979 Oct 11;281(5731):501–503. doi: 10.1038/281501a0. [DOI] [PubMed] [Google Scholar]
  36. Voellmy R., Bromley P. A. Massive heat-shock polypeptide synthesis in late chicken embryos: convenient system for study of protein synthesis in highly differentiated organisms. Mol Cell Biol. 1982 May;2(5):479–483. doi: 10.1128/mcb.2.5.479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wang C., Gomer R. H., Lazarides E. Heat shock proteins are methylated in avian and mammalian cells. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3531–3535. doi: 10.1073/pnas.78.6.3531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Zimmerman J. L., Petri W., Meselson M. Accumulation of a specific subset of D. melanogaster heat shock mRNAs in normal development without heat shock. Cell. 1983 Apr;32(4):1161–1170. doi: 10.1016/0092-8674(83)90299-4. [DOI] [PubMed] [Google Scholar]

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