Skip to main content
NCBI home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1989 May;9(5):2153–2162. doi: 10.1128/mcb.9.5.2153

Glucose-regulated protein (GRP94 and GRP78) genes share common regulatory domains and are coordinately regulated by common trans-acting factors.

S C Chang 1, A E Erwin 1, A S Lee 1
PMCID: PMC363009  PMID: 2546060

Abstract

We isolated the promoter of the human gene encoding the 94,000-dalton glucose-regulated protein (GRP94). The 5'-flanking region important for its expression was identified by deletion analysis. Comparison of the promoters of the genes for GRP78 and GRP94 derived from human, rat, and chicken cells revealed a common domain of 28 base pairs within the putative regulatory regions of both genes. This domain has been shown to interact with protein factors in the promoter of the gene for GRP78. Since the genes for GRP94 and GRP78 are transcriptionally regulated with similar kinetics under a variety of stress conditions, we are interested in examining the possible mechanisms for their coordinated expression. Through in vitro and in vivo competition assays, we found that the protein factors which interact with the promoter of the gene for GRP94 also have affinity for the conserved domain of the promoter of the gene for GRP78. These findings suggest that the genes for GRP94 and GRP78 are coordinately regulated through common trans-acting factors which recognize a common regulatory domain of glucose-regulated protein gene promoters.

Full text

PDF
2153

Images in this article

2157Image
on p.2157
2157Image
on p.2157
2158Image
on p.2158
2159Image
on p.2159
2160Image
on p.2160

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baez M., Sargan D. R., Elbrecht A., Kulomaa M. S., Zarucki-Schulz T., Tsai M. J., O'Malley B. W. Steroid hormone regulation of the gene encoding the chicken heat shock protein hsp 108. J Biol Chem. 1987 May 15;262(14):6582–6588. [PubMed] [Google Scholar]
  2. Bergsma D. J., Chang K. S., Schwartz R. J. Novel chicken actin gene: third cytoplasmic isoform. Mol Cell Biol. 1985 May;5(5):1151–1162. doi: 10.1128/mcb.5.5.1151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bole D. G., Hendershot L. M., Kearney J. F. Posttranslational association of immunoglobulin heavy chain binding protein with nascent heavy chains in nonsecreting and secreting hybridomas. J Cell Biol. 1986 May;102(5):1558–1566. doi: 10.1083/jcb.102.5.1558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Catelli M. G., Binart N., Jung-Testas I., Renoir J. M., Baulieu E. E., Feramisco J. R., Welch W. J. The common 90-kd protein component of non-transformed '8S' steroid receptors is a heat-shock protein. EMBO J. 1985 Dec 1;4(12):3131–3135. doi: 10.1002/j.1460-2075.1985.tb04055.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chang S. C., Wooden S. K., Nakaki T., Kim Y. K., Lin A. Y., Kung L., Attenello J. W., Lee A. S. Rat gene encoding the 78-kDa glucose-regulated protein GRP78: its regulatory sequences and the effect of protein glycosylation on its expression. Proc Natl Acad Sci U S A. 1987 Feb;84(3):680–684. doi: 10.1073/pnas.84.3.680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Day L. E., Hirst A. J., Lai E. C., Mace M., Jr, Woo S. L. 5' Domain and nucleotide sequence of an adult chicken chromosomal beta-globin gene. Biochemistry. 1981 Apr 14;20(8):2091–2098. doi: 10.1021/bi00511a005. [DOI] [PubMed] [Google Scholar]
  7. Dierks P., van Ooyen A., Cochran M. D., Dobkin C., Reiser J., Weissmann C. Three regions upstream from the cap site are required for efficient and accurate transcription of the rabbit beta-globin gene in mouse 3T6 cells. Cell. 1983 Mar;32(3):695–706. doi: 10.1016/0092-8674(83)90055-7. [DOI] [PubMed] [Google Scholar]
  8. Drummond I. A., Lee A. S., Resendez E., Jr, Steinhardt R. A. Depletion of intracellular calcium stores by calcium ionophore A23187 induces the genes for glucose-regulated proteins in hamster fibroblasts. J Biol Chem. 1987 Sep 15;262(26):12801–12805. [PubMed] [Google Scholar]
  9. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  10. Fried M., Crothers D. M. Equilibria and kinetics of lac repressor-operator interactions by polyacrylamide gel electrophoresis. Nucleic Acids Res. 1981 Dec 11;9(23):6505–6525. doi: 10.1093/nar/9.23.6505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hendershot L. M., Ting J., Lee A. S. Identity of the immunoglobulin heavy-chain-binding protein with the 78,000-dalton glucose-regulated protein and the role of posttranslational modifications in its binding function. Mol Cell Biol. 1988 Oct;8(10):4250–4256. doi: 10.1128/mcb.8.10.4250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kim Y. K., Lee A. S. Transcriptional activation of the glucose-regulated protein genes and their heterologous fusion genes by beta-mercaptoethanol. Mol Cell Biol. 1987 Aug;7(8):2974–2976. doi: 10.1128/mcb.7.8.2974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kleinsek D. A., Beattie W. G., Tsai M. J., O'Malley B. W. Molecular cloning of a steroid-regulated 108K heat shock protein gene from hen oviduct. Nucleic Acids Res. 1986 Dec 22;14(24):10053–10069. doi: 10.1093/nar/14.24.10053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Koch G. L., Macer D. R., Wooding F. B. Endoplasmin is a reticuloplasmin. J Cell Sci. 1988 Jul;90(Pt 3):485–491. doi: 10.1242/jcs.90.3.485. [DOI] [PubMed] [Google Scholar]
  16. Koch G. L. Reticuloplasmins: a novel group of proteins in the endoplasmic reticulum. J Cell Sci. 1987 May;87(Pt 4):491–492. doi: 10.1242/jcs.87.4.491. [DOI] [PubMed] [Google Scholar]
  17. Koch G. L., Smith M. J., Mortara R. A. An abundant ubiquitous glycoprotein (GP100) in nucleated mammalian cells. FEBS Lett. 1985 Jan 7;179(2):294–298. doi: 10.1016/0014-5793(85)80537-8. [DOI] [PubMed] [Google Scholar]
  18. Koch G., Smith M., Macer D., Webster P., Mortara R. Endoplasmic reticulum contains a common, abundant calcium-binding glycoprotein, endoplasmin. J Cell Sci. 1986 Dec;86:217–232. doi: 10.1242/jcs.86.1.217. [DOI] [PubMed] [Google Scholar]
  19. Kozutsumi Y., Segal M., Normington K., Gething M. J., Sambrook J. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature. 1988 Mar 31;332(6163):462–464. doi: 10.1038/332462a0. [DOI] [PubMed] [Google Scholar]
  20. Kulomaa M. S., Weigel N. L., Kleinsek D. A., Beattie W. G., Conneely O. M., March C., Zarucki-Schulz T., Schrader W. T., O'Malley B. W. Amino acid sequence of a chicken heat shock protein derived from the complementary DNA nucleotide sequence. Biochemistry. 1986 Oct 7;25(20):6244–6251. doi: 10.1021/bi00368a061. [DOI] [PubMed] [Google Scholar]
  21. Lawn R. M., Fritsch E. F., Parker R. C., Blake G., Maniatis T. The isolation and characterization of linked delta- and beta-globin genes from a cloned library of human DNA. Cell. 1978 Dec;15(4):1157–1174. doi: 10.1016/0092-8674(78)90043-0. [DOI] [PubMed] [Google Scholar]
  22. Lee A. S., Bell J., Ting J. Biochemical characterization of the 94- and 78-kilodalton glucose-regulated proteins in hamster fibroblasts. J Biol Chem. 1984 Apr 10;259(7):4616–4621. [PubMed] [Google Scholar]
  23. Lee A. S., Delegeane A. M., Baker V., Chow P. C. Transcriptional regulation of two genes specifically induced by glucose starvation in a hamster mutant fibroblast cell line. J Biol Chem. 1983 Jan 10;258(1):597–603. [PubMed] [Google Scholar]
  24. Lee A. S. The accumulation of three specific proteins related to glucose-regulated proteins in a temperature-sensitive hamster mutant cell line K12. J Cell Physiol. 1981 Jan;106(1):119–125. doi: 10.1002/jcp.1041060113. [DOI] [PubMed] [Google Scholar]
  25. Lewis M. J., Turco S. J., Green M. Structure and assembly of the endoplasmic reticulum. Biosynthetic sorting of endoplasmic reticulum proteins. J Biol Chem. 1985 Jun 10;260(11):6926–6931. [PubMed] [Google Scholar]
  26. Lin A. Y., Chang S. C., Lee A. S. A calcium ionophore-inducible cellular promoter is highly active and has enhancerlike properties. Mol Cell Biol. 1986 Apr;6(4):1235–1243. doi: 10.1128/mcb.6.4.1235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lin A. Y., Lee A. S. Induction of two genes by glucose starvation in hamster fibroblasts. Proc Natl Acad Sci U S A. 1984 Feb;81(4):988–992. doi: 10.1073/pnas.81.4.988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  29. Mazzarella R. A., Green M. ERp99, an abundant, conserved glycoprotein of the endoplasmic reticulum, is homologous to the 90-kDa heat shock protein (hsp90) and the 94-kDa glucose regulated protein (GRP94). J Biol Chem. 1987 Jun 25;262(18):8875–8883. [PubMed] [Google Scholar]
  30. Munro S., Pelham H. R. An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell. 1986 Jul 18;46(2):291–300. doi: 10.1016/0092-8674(86)90746-4. [DOI] [PubMed] [Google Scholar]
  31. Nakaki T., Deans R. J., Lee A. S. Enhanced transcription of the 78,000-dalton glucose-regulated protein (GRP78) gene and association of GRP78 with immunoglobulin light chains in a nonsecreting B-cell myeloma line (NS-1). Mol Cell Biol. 1989 May;9(5):2233–2238. doi: 10.1128/mcb.9.5.2233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Reinberg D., Roeder R. G. Factors involved in specific transcription by mammalian RNA polymerase II. Purification and functional analysis of initiation factors IIB and IIE. J Biol Chem. 1987 Mar 5;262(7):3310–3321. [PubMed] [Google Scholar]
  33. Resendez E., Jr, Attenello J. W., Grafsky A., Chang C. S., Lee A. S. Calcium ionophore A23187 induces expression of glucose-regulated genes and their heterologous fusion genes. Mol Cell Biol. 1985 Jun;5(6):1212–1219. doi: 10.1128/mcb.5.6.1212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Resendez E., Jr, Wooden S. K., Lee A. S. Identification of highly conserved regulatory domains and protein-binding sites in the promoters of the rat and human genes encoding the stress-inducible 78-kilodalton glucose-regulated protein. Mol Cell Biol. 1988 Oct;8(10):4579–4584. doi: 10.1128/mcb.8.10.4579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sanchez E. R., Toft D. O., Schlesinger M. J., Pratt W. B. Evidence that the 90-kDa phosphoprotein associated with the untransformed L-cell glucocorticoid receptor is a murine heat shock protein. J Biol Chem. 1985 Oct 15;260(23):12398–12401. [PubMed] [Google Scholar]
  36. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Shapiro D. J., Sharp P. A., Wahli W. W., Keller M. J. A high-efficiency HeLa cell nuclear transcription extract. DNA. 1988 Jan-Feb;7(1):47–55. doi: 10.1089/dna.1988.7.47. [DOI] [PubMed] [Google Scholar]
  38. Shiu R. P., Pouyssegur J., Pastan I. Glucose depletion accounts for the induction of two transformation-sensitive membrane proteinsin Rous sarcoma virus-transformed chick embryo fibroblasts. Proc Natl Acad Sci U S A. 1977 Sep;74(9):3840–3844. doi: 10.1073/pnas.74.9.3840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Smith M. J., Koch G. L. Isolation and identification of partial cDNA clones for endoplasmin, the major glycoprotein of mammalian endoplasmic reticulum. J Mol Biol. 1987 Mar 20;194(2):345–347. doi: 10.1016/0022-2836(87)90381-0. [DOI] [PubMed] [Google Scholar]
  40. Sorger P. K., Pelham H. R. The glucose-regulated protein grp94 is related to heat shock protein hsp90. J Mol Biol. 1987 Mar 20;194(2):341–344. doi: 10.1016/0022-2836(87)90380-9. [DOI] [PubMed] [Google Scholar]
  41. Ting J., Lee A. S. Human gene encoding the 78,000-dalton glucose-regulated protein and its pseudogene: structure, conservation, and regulation. DNA. 1988 May;7(4):275–286. doi: 10.1089/dna.1988.7.275. [DOI] [PubMed] [Google Scholar]
  42. Ting J., Wooden S. K., Kriz R., Kelleher K., Kaufman R. J., Lee A. S. The nucleotide sequence encoding the hamster 78-kDa glucose-regulated protein (GRP78) and its conservation between hamster and rat. Gene. 1987;55(1):147–152. doi: 10.1016/0378-1119(87)90258-7. [DOI] [PubMed] [Google Scholar]
  43. Wasylyk B., Chambon P. A T to A base substitution and small deletions in the conalbumin TATA box drastically decrease specific in vitro transcription. Nucleic Acids Res. 1981 Apr 24;9(8):1813–1824. doi: 10.1093/nar/9.8.1813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Yamamoto K. K., Gonzalez G. A., Biggs W. H., 3rd, Montminy M. R. Phosphorylation-induced binding and transcriptional efficacy of nuclear factor CREB. Nature. 1988 Aug 11;334(6182):494–498. doi: 10.1038/334494a0. [DOI] [PubMed] [Google Scholar]
  45. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  46. Zarucki-Schulz T., Tsai S. Y., Itakura K., Soberon X., Wallace R. B., Tsai M. J., Woo S. L., O'Malley B. W. Point mutagenesis of the ovalbumin gene promoter sequence and its effect on in vitro transcription. J Biol Chem. 1982 Sep 25;257(18):11070–11077. [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES