Heat Stress in Avian Cells

  • Milton J. Schlesinger


Among the many diverse biological materials that have been utilized to study the stress response, avian cells grown in tissue culture have proved to be particularly advantageous. Monolayers of homogeneous populations of 106 to 108 fibroblasts can be prepared readily from 11-day chicken embryos and cultured for several days in relatively simple media. A stress agent, either chemical or physical, can be applied under controlled conditions for varying lengths of time and the effects on cellular morphology or metabolism easily monitored. In the specific case of a heat shock, a primary culture of chicken embryo fibroblasts “senses” the stress within minutes of a shift up in temperature that corresponds to as little as a 10% increase above the physiological temperature of the bird, which is usually around 41°C. For cells from human tissue, a temperature of 41°C is sufficient to trigger the cellular stress response (Ron and Birkenfeld, 1987). In the avian fibroblast tissue culture system, response to hyperthermic stress—as measured by enhanced transcription of heat shock genes (i.e., detection of higher levels of mRNAs) and appearance of newly synthesized heat shock proteins—is detected at 42 to 43°C with the full complement of heat shock proteins induced after 30 min at 45°C (Kelley and Schlesinger, 1978). The latter temperature is considered physiological in that the internal temperature of the adult bird reaches 45°C when the bird goes into flight.


Heat Shock Heat Stress Heat Shock Protein Heat Shock Transcription Factor Chicken Embryo Fibroblast 


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  1. Arrigo, A.-P., and Landry, J., 1994, Expression and function of the low-molecularweight heat shock proteins, in: The Biology of Heat Shock Proteins and Molecular Chaperones ( R. I. Morimoto, A. Tissieres, and C. Georgopoulos, eds.), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 335–373.Google Scholar
  2. Atkinson, B. G., 1981, Synthesis of heat-shock proteins by cells undergoing myogenesis, J. Cell Biol. 89: 666–671.PubMedCrossRefGoogle Scholar
  3. Atkinson, B. G., and Dean, R. L., 1985, Effects of stress on the gene expression of amphibian, avian, and mammalian blood cells, in: Changes in Eukaryotic Gene Expression in Response to Environmental Stress ( B. G. Atkinson and D. B. Whelan, eds.), Academic Press, San Diego, pp. 159–179.CrossRefGoogle Scholar
  4. Benndorf, R., Hayess, K., Ryazantsev, S., Wieske, M., Behlke, J., and Lutsch, G., 1994, Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity, J. Biol. Chem. 269: 20780–20784.PubMedGoogle Scholar
  5. Bohen, S. P., and Yamamoto, K., 1994, Modulation of steroid receptor signal transduction by heat shock proteins, in: The Biology of Heat Shock Proteins and Molecular Chaperones ( R I. Morimoto, A. Tissieres, and C. Georgopoulos, eds.), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 313–334.Google Scholar
  6. Bond, U., and Schlesinger, M. J., 1986, The chicken ubiquitin gene contains a heat shock promoter and expresses an unstable mRNA in heat-shocked cells, Mol. Cell. Biol. 6: 4602–4610.Google Scholar
  7. Bond, U., Agell, N., Haas, A. L., Redman, K., and Schlesinger, M. J., 1988, Ubiqui-tin in stressed chicken embryo fibroblasts, J. Biol. Chem. 263: 2384–2388.Google Scholar
  8. Brugge, J., 1986, Interaction of the Rous sarcoma virus protein pp60src with the cellular proteins pp50 and pp90, Curt Top. Microbial. Immunol. 123: 1–22.CrossRefGoogle Scholar
  9. Chappell, T. G., Welch, W. J., Schlossman, D. M., Palter, K. B., Schlesinger, M.J., and Rothman, J. E., 1986, UncoatingATPase is a member of the 70 kilodalton family of stress proteins, Cell 45: 3–13.PubMedCrossRefGoogle Scholar
  10. Collier, N. C., and Schlesinger, M. J., 1986a, Induction of heat-shock proteins in the embryonic chicken lens, Exp. Eye Res. 42: 103–117.CrossRefGoogle Scholar
  11. Collier, N. C., and Schlesinger, M. J., 1986b, The dynamic state of heat shock proteins in chicken embryo fibroblasts, J. Cell Biol. 103: 1495–1507.PubMedCrossRefGoogle Scholar
  12. Collier, N. C., Heuser, J., Levy, M. A., and Schlesinger, M. J., 1988, Ultrastructural and biochemical analysis of the stress granule in chicken embryo fibroblasts, J. Cell Biol. 106: 1131–1139.PubMedCrossRefGoogle Scholar
  13. Collier, N. C., Sheetz, M. P., and Schlesinger, M. J., 1993, Concomitant changes in mitochondria and intermediate filaments during heat shock and recovery of chicken embryo fibroblasts, J. Cell. Biochem. 52: 297–307.PubMedCrossRefGoogle Scholar
  14. DiDomenico, B. J., Bugalsky, G. E., and Lindquist, S., 1982, The heat shock response is self regulated at both the transcriptional and post-transcriptional level, Cell 31: 593–603.PubMedCrossRefGoogle Scholar
  15. Doyle, H., and Bishop, J., 1993, Torso, a receptor tyrosine kinase required for embryonic pattern formation, shares substrates with the sevenless and EGF-R pathways in Drosophila, Genes Dey. 7: 633–646.CrossRefGoogle Scholar
  16. Flaherty, K. M., DeLuca-Flaherty, C., and McKay, D. B., 1990, Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein, Nature 346: 623–628.PubMedCrossRefGoogle Scholar
  17. Goldberg, N. D., Passonneau, J. V., and Lowly, O. H., 1966, Effects of changes in brain metabolism on the levels of citric acid cycle intermediates, J. Biol. Chem. 241: 3997–4003.PubMedGoogle Scholar
  18. Hu, J., and Seeger, C., 1996, Hsp90 is required for the activity of a hepatitis B virus reverse transcriptase, Proc. Natl. Acad. Sci. USA 93: 1060–1064.PubMedCrossRefGoogle Scholar
  19. Ingolia, T. D., and Craig, E. A., 1982, Four small Drosophila heat shock proteins are related to each other and to mammalian a crystallin, Proc. Natl. Acad. Sci. USA 79:2360–2364.Google Scholar
  20. Kelley, P. M., and Schlesinger, M. J., 1978, The effect of amino acid analogues and heat shock on gene expression in chicken embryo fibroblasts, Cell 15: 1277 1286.Google Scholar
  21. Kelley, P. M., and Schlesinger, M. J., 1982, Antibodies to two major heat shock proteins cross react with similar proteins in widely divergent species, Mol. Cell. Biol. 2: 267–274.PubMedGoogle Scholar
  22. Löscher, B., and Eisenman, R. N., 1988, c-myc and c-myb protein degradation: Effect of metabolite inhibitors and heat shock, Mol. Cell. Biol. 8: 2504–2512.Google Scholar
  23. Matts, R. L., Xu, A., Pal, J. K., and Chen, J. J., 1992, Interactions of the hemeregulated eIF-2 alpha kinase with heat shock proteins in rabbit reticulocyte lysates, J. Biol. Chem., 267: 18160–18167.PubMedGoogle Scholar
  24. Meng, X., Jerome, V., Devin, J., Baulieu, E. E., and Catelli, M. G., 1993, Cloning of chicken hsp 90 beta: The only vertebrate hsp90 insensitive to heat shock, Biochem. Biophys. Res. Commun. 190: 630–636.Google Scholar
  25. Miller, L., and Qureshi, M. A., 1992, Heat-shock protein synthesis in chicken macrophages: Influence of in vivo and in vitro heat shock, lead acetate and lipopolysaccharide, Poult. Sci. 71: 988–998.PubMedCrossRefGoogle Scholar
  26. Miron, T., Vancompernolle, K., Vandekerckhove, J., Wilchek, M., and Geiger, B., 1991, A 25 kD inhibitor of actin polymerization is a low molecular mass heat shock protein, J. Cell Biol. 114: 255–261.PubMedCrossRefGoogle Scholar
  27. Morimoto, R. I., 1993, Cells in stress: Transcriptional activation of heat shock genes, Science 259: 1409–1410.PubMedCrossRefGoogle Scholar
  28. Morimoto, R. I., and Fodor, E., 1984, Cell-specific expression of heat shock proteins in chicken reticulocytes and lymphocytes, J. Cell Biol. 99: 1316–1323.PubMedCrossRefGoogle Scholar
  29. Munro, S., and Pelham, H. R. B., 1986, An hsp70-like protein in the ER: Identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein, Cell 46: 291–300.PubMedCrossRefGoogle Scholar
  30. Nagata, K., Saga, S., and Yamada, K. M., 1986, A major collagen-binding protein of chick embryo fibroblasts is a novel heat shock protein, J. Cell Biol. 103: 223–229.PubMedCrossRefGoogle Scholar
  31. Nakai, A., and Morimoto, R. I., 1993, Characterization of a novel chicken heat shock transcription factor, heat shock factor 3, suggests a new regulatory pathway, Mol. Cell. Biol. 13: 1983–1997.PubMedGoogle Scholar
  32. Nowak, T. S., Jr., Bond, U., and Schlesinger, M. J., 1990, Heat shock RNA levels in brain and other tissues after hyperthermia and transient ischemia, J. Neurochem. 54: 451–458.PubMedCrossRefGoogle Scholar
  33. Parsell, D. A., and Lindquist, S., 1994, Heat shock proteins and stress tolerance, in: The Biology of Heat Shock Proteins and Molecular Chaperones ( R. I. Mori-moto, A. Tissieres, and C. Georgopoulos, eds.), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 457–494.Google Scholar
  34. Perisic, O., Xiao, H., and Lis, J., 1989, Stable binding of Drosophila heat shock factor to head-to-head and tail-to-tail repeats of a conserved 5 bp recognition unit, Cell 59: 797–806.PubMedCrossRefGoogle Scholar
  35. Rechsteiner, M. (ed.), 1988, Ubiquitin, Plenum Press, New York.Google Scholar
  36. Redmond, T., Sanches, E. R., Bresnick, E. H., Schlesinger, M. J., Toft, D. O., Pratt, W. B., and Welsh, M. J., 1989, Immunofluorescence colocalization of the 90-kDa heat-shock protein and microtubules in interphase and mitotic mammalian cells, Eur. J. Cell Biol. 50: 66–75.PubMedGoogle Scholar
  37. Ron, A., and Birkenfeld, A., 1987, Stress proteins in the human endometrium and decidua, Hum. Reprod. 2: 277–280.PubMedGoogle Scholar
  38. Sarge, K. D., Zimarino, V., Holm, K., Wu, C., and Morimoto, R. I., 1991, Cloning and characterization of two mouse heat shock factors with distinct inducible and constitutive DNA-binding ability, Genes Dey. 5: 1902–1911.CrossRefGoogle Scholar
  39. Schlesinger, M. J., and Ryan, C., 1993, An ATP- and hsc70-dependent oligomerization of nascent heat-shock factor (HSF) polypeptide suggests that HSF itself could be a “sensor” for the cellular stress response, Protein Sci. 2: 1356–1360.PubMedCrossRefGoogle Scholar
  40. Schlesinger, M. J., Ashburner, M., and Tissieres, A. (eds.), 1982, Heat Shock: From Bacteria to Man, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.Google Scholar
  41. Schlesinger, M. J., Ryan, C., Chi, M.-Y., Carter, J. G., Pusateri, M. E., and Lowry, O. H., 1997, Metabolite changes associated with heat-shocked avian fibroblast mitochondria, Cell Stress and Chaperones 2: 25–30.PubMedCrossRefGoogle Scholar
  42. Voellmy, R., and Bromley, P. A., 1982, Massive heat-shock polypeptide synthesis in late chicken embryos: Convenient system for study of protein synthesis in highly differentiated organisms, Moi. Cell. Biol. 2: 479–483.Google Scholar

Copyright information

© Springer Science+Business Media New York 1997

Authors and Affiliations

  • Milton J. Schlesinger
    • 1
  1. 1.Department of Molecular MicrobiologyWashington University School of MedicineSt. LouisUSA

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