1887

Journal of General Virology header logo

Volume 77, Issue 9

The Highly Inducible Member of the 70 kDa Family of Heat Shock Proteins Increases Canine Distemper Virus Polymerase Activity Free

Abstract

The cellular stress response is characterized by the production of heat shock proteins (HSP) which serve important cytoprotective functions. Paradoxically, induction of the stress response promotes cytopathic effect mediated by infection with canine distemper virus (CDV). The stress-mediated increase in cytopathic effect is correlated to the formation of complexes between the viral nucleocapsid (NC) and the major inducible member of the ≈ 70 kDa family of HSP (hsp72). The objective of the present study was to document the functional significance of CDV NC-HSP interaction. Cytoplasmic NC was purified from Vero cells lytically infected with the Onderstepoort strain of CDV. Both ultrastructural variants of CDV NC interacted with both hsp72 and the constitutively expressed member of the ≈ 70 kDa family of HSP (hsp73) in a reversible and ATP-dependent manner. An effect of hsp72/73 on NC polymerase activity was demonstrated using cell-free assays derived from either Vero or HeLa cell lines. Antibody specific to hsp72 suppressed both basal and stress-enhanced polymerase activity whereas hsp73-specific antibody had no affect. Supplementation of purified hsp72/73, but not hsp73 alone, enhanced basal polymerase activity in a dosage-dependent manner. Using purified NC variants, polymerase activity was demonstrated in pre-formed hsp72/73-NC complexes but not in NC devoid of HSP. These results suggest that the stimulatory effect of the stress response upon CDV gene expression may, in part, be mediated by a reversible and direct interaction between hsp72 and the viral core particle.

  • Received:
  • Accepted:
  • Published Online:
© Journal of General Virology 1996
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-77-9-2125
1996-09-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/77/9/JV0770092125.html?itemId=/content/journal/jgv/10.1099/0022-1317-77-9-2125&mimeType=html&fmt=ahah

References

  1. Abravaya K., Myers M. P., Murphy S. P., Morimoto R. 1992; The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock-gene expression. Genes and Development 6:1153–1164
     [Google Scholar]
  2. Alfano C., McMacken R. 1989; Heat shock protein-mediated disassembly of nucleoprotein structures is required for the initiation of bacteriophage λ DNA replication. Journal of Biological Chemistry 264:10709–10718
     [Google Scholar]
  3. Allen R. L., O’Brien D. A., Eddy E. M. 1988; A novel hsp70-like protein (P70) is present in mouse spermatogenic cells. Molecular and Cellular Biology 8:828–832
     [Google Scholar]
  4. Andrews J. M., Ogiesbee M. J., Trevino A. V., Guyot D. J., Newbound G. C., Lairmore M. D. 1995; Enhanced human T-cell lymphotrophic virus type I expression following induction of the cellular stress response. Virology 208:816–820
     [Google Scholar]
  5. Brown R. C., Martin R. L., Hansen W. J., Beckmann R. P., Welch W. J. 1993; The constitutive and stress inducible forms of hsp70 exhibit functional similarities and interact with one another in an ATP-dependent fashion. Journal of Cell Biology 120:1101–1112
     [Google Scholar]
  6. Bruner R., Vinograd J. 1965; The evaluation of standard sedimentation coefficients of sodium RNA and sodium DNA from sedimentation velocity data in concentrated NaCl and CsCl solutions. Biochimica et Biophysica Acta 108:18–29
     [Google Scholar]
  7. Bussell R. H., Karzon D. T. 1965; Canine distemper vims in primary and continuous cell lines of human and monkey origin. Archiv fiir die Gesamte Virusforschung 17:183–202
     [Google Scholar]
  8. Collins P. C., Hightower L. E. 1982; Newcastle disease vims stimulates the cellular accumulation of stress (heat shock) protein mRNA and proteins. Journal of Virology 44:703–707
     [Google Scholar]
  9. De B. P., Burdsall A. L., Banerjee A. K. 1993; The role of cellular actin in human parainfluenza vims type 3 genomic transcription. Journal of Biological Chemistry 268:5703–5710
     [Google Scholar]
  10. DeLuce-Flaherty C., McKay D. B. 1991; Nucleotide sequence of the cDNA of a bovine heat shock cognate protein. Nucleic Acids Research 18:5569
     [Google Scholar]
  11. Earl P. L., Moss B., Dorns R. W. 1991; Folding, interaction with GRP78-BiP, assembly, and transport of the human immunodeficiency type 1 envelope protein. Journal of Virology 65:2047–2055
     [Google Scholar]
  12. Ferris D. K., Harel-Bellan A., Morimoto R. I., Welch W. J., Farrar W. L. 1988; Mitogen and Lymphokine stimulation of heat shock proteins in T lymphocytes. Proceedings of the National Academy of Sciences, USA 85:3850–3854
     [Google Scholar]
  13. Garry R. F., Ulug E. T., Bose H. R. 1983; Induction of stress proteins in Sindbis vims-and vesicular stomatitis vims-infected cells. Virology 129:319–332
     [Google Scholar]
  14. Gething M.-J., Sambrook J. 1988; Protein folding and intracellular transport: studies on influenza vims hemagglutinin. Biochemical Society Symposia 55:155–166
     [Google Scholar]
  15. Grosz M. D., Womack J. E., Skow L. 1992; Syntenic conservation of HSP70 genes in cattle and humans. Genomics 14:863–868
     [Google Scholar]
  16. Gutierrez J. A., Guerriero V. 1995; Chemical modifications of a recombinant bovine stress-inducible 70 kDa heat-shock protein (Hsp70) mimics Hsp70 isoforms from tissues. Biochemical Journal 305:197–203
     [Google Scholar]
  17. Hunt C. R., Gasser D. L., Chaplin D. D., Pierce J. C., Kozak C. A. 1993; Chromosomal localization of five murine HSP70 gene family members: Hsp70-1, Hsp70-2, Hsp70-3, Hsc70, and Grp78. Genomics 16:193–198
     [Google Scholar]
  18. Jeoung D. I., Chen S., Windsor J., Pollack R. E. 1991; Human major hsp70 protein complements the localization and functional defects of cytoplasmic mutant SV40 T-antigen in Swiss 3T3 mouse fibroblast cells. Genes & Development 5:2235–2244
     [Google Scholar]
  19. Kenney H., Ogiesbee M. 1994; Sensitive detection of morbillivims cell-free transcription in a direct RNase protection assay. Journal of Virological Methods 48:197–210
     [Google Scholar]
  20. Kobayashi K., Ohgitani E., Tanaka Y., Kita M., Imanishi J. 1994; Herpes simplex vims-induced expression of 70 kDa heat shock protein (hsp70) requires early protein synthesis but not viral DNA replication. Microbiology and Immunology 38:321–325
     [Google Scholar]
  21. Kretz-Remey C., Arrigo A.-P. 1994; The kinetics of HIV-1 long terminal repeat transcriptional activation resemble those of hsp70 promoter in heat-shock treated HeLa cells. FEBS Letters 351:191–196
     [Google Scholar]
  22. Leno G. H., Ledford B. E. 1990; Reversible ADP-ribosylation of the 78 kDa glucose-regulated protein. FEBS Letters 276:29–33
     [Google Scholar]
  23. Leustek T., Amir-Shapira D., Toledo H., Brot N., Weissbach H. 1992; Autophosphorylation of 70 kDa heat shock proteins. Cellular and Molecular Biology 38:1–15
     [Google Scholar]
  24. Lowe D. G., Moran L. A. 1984; Proteins related to the mouse L-cell major heat shock protein are synthesized in the absence of heat shock gene expression. Proceedings of the National Academy of Sciences, USA 81:2317–2321
     [Google Scholar]
  25. Macejak D. G., Sarnow P. 1992; Association of heat shock protein 70 with enterovirus capsid precursor Pi in infected human cells. Journal of Virology 66:1520–1527
     [Google Scholar]
  26. Machammer C. E., Dorns R. W., Bole D. G., Helenius A., Rose J. K. 1990; Heavy chain binding protein recognizes incompletely disulfide-bonded forms of vesicular stomatitis virus G protein. Journal of Biological Chemistry 265:6879–6883
     [Google Scholar]
  27. Marchesi V. T., Ngo N. 1993; In vitro assembly of multimeric complexes containing alpha-tubulin, beta-tubulin, heat shock protein hsp70, and elongation factor-1-alpha. Proceedings of the National Academy of Sciences, USA 90:3028–3032
     [Google Scholar]
  28. Metzler A. E., Higgins R. J., Krakowka S., Koestner A. 1980; Persistent in vitro interaction of virulent and attenuated canine distemper virus with bovine cells. Archives of Virology 66:329–339
     [Google Scholar]
  29. Metzler A. E., Higgins R. J., Krakowka S., Koestner A. 1981; Characterization of bovine cells supporting in vitro growth of both virulent and attenuated canine distemper virus. American Journal of Veterinary Research 42:1257–1262
     [Google Scholar]
  30. Mivechi N. F., Trainor L. D., Hahn G. M. 1993; Purified mammalian hsp-70 kDa activates phosphoprotein phosphatases in vitro . Biochemical and Biophysical Research Communications 192:954–963
     [Google Scholar]
  31. Moyer S. A., Baker S. C., Lessard J. L. 1986; Tubulin: a factor necessary for the synthesis of both Sendai and vesicular stomatitis virus RNAs. Proceedings of the National Academy of Sciences, USA 83:5405–5409
     [Google Scholar]
  32. Moyer S. A., Baker S. C., Horikami S. M. 1990; Host cell proteins required for measles virus reproduction. Journal of General Virology 71:775–783
     [Google Scholar]
  33. Nevins J. R. 1982; Induction of the synthesis of a 70, 000 dalton mammalian heat shock protein by the adenovirus ElA gene product. Cell 29:913–919
     [Google Scholar]
  34. Ng D. T. W., Randall R. E., Lamb R. A. 1989; Intracellular maturation and transport of the SV5 type II glycoprotein hemagglutinin-neuraminidase: specific and transient association with GRP78-BiP in the endoplasmic reticulum and extensive internalization from the cell surface. Journal of Cell Biology 109:3273–3289
     [Google Scholar]
  35. Oglesbee M., Krakowka S. 1993; Cellular stress response induces selective intranuclear trafficking and accumulation of morbillivirus major core protein. Laboratory Investigation 68:109–117
     [Google Scholar]
  36. Oglesbee M., Tatalick L., Rice J., Krakowka S. 1989a; Isolation and characterization of canine distemper virus nucleocapsid variants. Journal of General Virology 70:2409–2419
     [Google Scholar]
  37. Oglesbee M., Tatalick L., Ringler S., Rice J., Krakowka S. 1989b; Rapid isolation of morbillivirus nucleocapsid for genomic RNA cDNA cloning and the production of specific core protein antisera. Journal of Virological Methods 24:285–300
     [Google Scholar]
  38. Oglesbee M., Ringler S., Krakowka S. 1990; Interaction of canine distemper virus nucleocapsid variants with 70K heat-shock proteins. Journal of General Virology 71:1585–1590
     [Google Scholar]
  39. Oglesbee M., Kenney H., Kenney T., Krakowka S. 1993; Enhanced production of morbillivirus gene-specific RNAs following induction of the cellular stress response in stable persisent infection. Virology 192:556–567
     [Google Scholar]
  40. Ray J., Fujinami R. S. 1987; Characterization of in vitro transcription and transcriptional products of measles virus. Journal of Virology 61:3381–3387
     [Google Scholar]
  41. Riabowol K. T., Mizzen L. A., Welch W. J. 1988; Heat shock is lethal to fibroblasts microinjected with antibodies against hsp70. Science 242:433–436
     [Google Scholar]
  42. Roux L. 1990; Selective and transient association of Sendai virus HN glycoprotein with BiP. Virology 175:161–166
     [Google Scholar]
  43. Sainis I., Angelidis C., Pagoulatos G., Lazaridis I. 1994; The hsc70 gene which is slightly induced by heat is the main virus inducible member of the hsp70 gene family. FEBS Letters 355:282–286
     [Google Scholar]
  44. Schlesinger M. J., 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 Science 2:1356–1360
     [Google Scholar]
  45. Schumacher R. J., Hurst R., Sullivan W. P., McMahon N. J., Toft D. O., Matts R. L. 1994; ATP-dependent chaperoning activity of reticulocyte lysate. Journal of Biological Chemistry 269:9493–9499
     [Google Scholar]
  46. Turman M. A., Mathews A. 1996; A simple luciferase assay to measure ATP levels in small numbers of cells using a fluorescence plate reader. In Vitro Cellular and Developmental Biology 32:1–4
     [Google Scholar]
  47. Walton P. A., Wendland M., Subramani S., Rachubinski R. A., Welch W. J. 1994; Involvement of 70-kD heat-shock proteins in peroxisomal import. Journal of Cell Biology 125:1037–1046
     [Google Scholar]
  48. Wang C., Lin J., Lazarides E. 1992; Methyiations of 70, 000-Da heat shock proteins in 3T3 cells: alterations by arsenite treatment, by different stages of growth and by virus transformation. Archives of Biochemistry and Biophysics 297:169–175
     [Google Scholar]
  49. Welch W. J., Feramisco J. R. 1985; Rapid purification of 70, 000 dalton stress proteins: affinity of the proteins for nucleotides. Molecular and Cellular Biology 5:1229–1237
     [Google Scholar]
  50. Williams K. J., Landgraf B. E., Whiting N. L., Zurlo J. 1989; Correlation between the induction of heat shock protein 70 and enhanced viral reactivation in mammalian cells treated with ultraviolet light and heat shock. Cancer Research 49:2735–2742
     [Google Scholar]
  51. Wu B., Hunt C., Morimoto R. 1985; Structure and expression of the human gene encoding major heat shock protein HSP70. Molecular and Cellular Biology 5:330–341
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-77-9-2125
Loading
The Highly Inducible Member of the 70 kDa Family of Heat Shock Proteins Increases Canine Distemper Virus Polymerase Activity
J. Gen. Virol. 77, 2125 (1996); https://doi.org/10.1099/0022-1317-77-9-2125
/content/journal/jgv/10.1099/0022-1317-77-9-2125
/content/journal/jgv/10.1099/0022-1317-77-9-2125
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error