The molecular response to reductive stress in LLC-PK1 renal epithelial cells: Coordinate transcriptional regulation of gadd153 and grp78 genes by thiols

Cell Stress and Chaperones

Volumn 2, Issue 1, 1997, Pages 31-40

  Halleck, Margaretann M ^a,c   Holbrook, Nikki J ^b   Skinner, Jeffrey ^a   Liu, Hong ^a   Stevens, James L ^a  

^a Adirondack Biomedical Research Institute Inc   (United States)

^b NATIONAL INSTITUTE ON AGING   (United States)

^c MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; CELL PROTEIN; CYTOCHALASIN B; DITHIOTHREITOL; HYDROGEN PEROXIDE; MESSENGER RNA; SUPEROXIDE; SUPEROXIDE DISMUTASE; THIOL;

ANIMAL CELL; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; EUKARYOTIC CELL; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE INDUCTION; GENOME; KIDNEY CELL; KIDNEY EPITHELIUM; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; STRESS; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ANIMALS; CARRIER PROTEINS; CCAAT-ENHANCER-BINDING PROTEINS; CYTOCHALASIN B; CYTOTOXINS; DITHIOTHREITOL; DNA-BINDING PROTEINS; GENE EXPRESSION; HEAT-SHOCK PROTEINS; LLC-PK1 CELLS; MOLECULAR CHAPERONES; NUCLEAR PROTEINS; OXIDATION-REDUCTION; PROMOTER REGIONS (GENETICS); RNA, MESSENGER; STRESS; SULFHYDRYL REAGENTS; SWINE; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 0030971176     PISSN: 13558145     EISSN: None     Source Type: Journal    
DOI: 10.1379/1466-1268(1997)002<0031:TMRTRS>2.3.CO;2     Document Type: Article

References (74)

1. Abate C, Patel L, Rauscher FJ and Curran T (1990) Redox regulation of fos and jun DNA-binding activity in vitro. Science 249, 1157-1161.
2. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA and Struhl K (1991) Nuclear runoff transcription in mammalian cells. In: Current Protocols in Molecular Biology, John Wiley and Sons, New York, 4.10.1-4.10.4.
3. Badley JE, Bishop GA, St John T and Frelinger JA (1988) A simple, rapid method for the purification of poly A+ RNA. Biotechniques 6, 114-116.
4. Bardwell JCA and Beckwith J (1993) The bonds that tie: catalyzed disulfide bond formation. Cell 74, 769-771.
5. Bartlett JD, Luethy JD, Carlson SG, Sollot SJ and Holbrook NJ (1992) Calcium ionophore A23187 induces expression of the growth arrest and DNA damage inducible CCAAT/enhancer-binding protein (C/EBP)-related gene, gadd153. J. Biol. Chem. 267, 20465-20470.
6. Batchvarova N, Wang X-Z and Ron D (1995) Inhibition of adipogenesis by the stress-induced protein CHOP (Gadd 153). EMBO J. 14, 4654-4661.
7. Beckman RP, Lovett M and Welch WJ (1992) Examining the function and regulation of hsp 70 in cells subjected to metabolic stress. J. Cell Biol. 117, 1137-1150.
8. Braakman I, Helenius J and Helenius A (1992) Role of ATP and disulphide bonds during protein folding in the endoplamsic reticulum. Nature 356, 260-262.
9. Brostrom MA, Prostko CR, Gmitter D and Brostrom CO (1995) Independent signaling of grp78 gene transcription and phosphorylation of eukaryotic inititation factor 2-alpha by the stressed endoplasmic reticulum. J. Biol. Chem. 270, 4127-4132.
10. Cao X, Zhou Y and Lee AS (1995) Requirement for tyrosine- and serine/threonine kinases in the transcriptional activation of the mammalian grp78/BiP promoter by thapsigargin. J. Biol. Chem. 270, 494-502.
11. Carlson SG, Fawcett TW, Bartlett JD, Bernier M and Holbrook NJ (1993) Regulation of the CEBP-related gene gadd153 by glucose deprivation. Mol. Cell. Biol. 13, 4736-4744.
12. Celano P, Berchtold C and Casero RAJr (1989) A simplification of the nuclear run-off transcription assay. Biotechniques 7, 942-943.
13. Cerutti PA and Trump BF (1991) Inflammation and oxidative stress in carcinogenesis. Cancer Cells 3, 1-7.
14. Chen Q and Stevens JL (1991) Inhibition of iodoacetamide and t-butylhydroperoxide toxicity in LLC-PK1 cells by antioxidants: A role for lipid peroxidation in alkylation induced cytotoxicity. Arch. Biochem. Biophys. 284, 422-430.
15. Chen Q, Jones TW, Brown PC and Stevens JL (1990) The mechanism of cysteine conjugate cytotoxicity in renal epithelial cells. Covalent binding leads to thiol depletion and lipid peroxidation. J. Biol. Chem. 265, 21603-21611.
16. Chen Q, Yu K, Holbrook NJ and Stevens JL (1992a) Activation of the growth arrest and DNA damage-inducible gene gadd153 by nephrotoxic cysteine conjugates and dithiothreitol. J. Biol. Chem. 267, 8207-8212.
17. Chen Q, Yu K and Stevens JL (1992b) Regulation of the cellular stress response by reactive electrophiles: The role of covalent binding and cellular thiols in transcriptional activation of the 7OkD heat shock protein gene by nephrotoxic cysteine conjugates. J. Biol. Chem. 267, 24322-24327.
18. Cox JS, Shamu CE and Walter P (1993) Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73, 1197-1206.
19. Crawford D, Zbinden I, Amstad P and Cerutti P (1988) Oxidant stress induces the proto-oncogenes c-fos and c-myc in mouse epidermal cells. Oncogene 3, 27-32.
20. Devary Y, Gottlieb RA, Lau LF and Karin M (1991) Rapid and preferential activation of the c-jun gene during the mammalian UV response. Mol. Cell Biol. 11, 2804-2811.
21. Donati YRA, Slosman DO and Polla BS (1990) Oxidative injury and the heat shock response. Biochem. Pharmacol. 40, 2571-2577.
22. Feinberg AP and Vogelstein B (1984) A technique for labelling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 137, 266-267.
23. Fornace AJ (1992) mammalian genes induced by radiation-activation of genes associated with growth control. Annu. Rev. Genet. 26, 507-526.
24. Fornace AJ Jr, Nebert DW, Hollander MC, Luethy JD, Papathanasiou M, Fargnoli J and Holbrook NJ (1989) Mammalian genes coordinately regulated by growth arrest signals and DNA-damaging agents. Mol. Cell Biol. 9, 4196-4203.
25. Freeman ML, Borrelli MJ, Syed K, Senisterra G, Stafford DM and Lepcock JR (1995) Characterization of a signal generated by oxidation of protein thiols that activates the heat shock transcription factor. J. Cell. Physiol. 16, 356-366.
26. Gething M-J and Sambrook J (1992) Protein folding in the cell. Nature 355, 33-45.
27. Hayden PJ and Stevens JL (1990) Cysteine conjugate toxicity, metabolism, and binding to macromolecules in isolated rat kidney mitochondria. Mol. Pharmacol. 37, 468-476.
28. Held KD and Biaglow JE (1993) Role of copper in the oxygen radical-mediated toxicity of the thiol-containing radioprotector dithiothreitol in mammalian cells. Radiat. Res. 134, 375-382.
29. Hightower LE (1991) Heat shock, stress proteins, chaperones and proteotoxicity. Cell 66, 191-197
30. Holbrook NJ and Fornace AJ (1991) Response to adversity: Molecular control of gene activation following genotoxic stress. New Biologist 3, 825-833.
31. Hull RN, Cherry WR and Weaver GW (1976) The origin and characteristics of a pig kidney cell strain, LLC-PK1. In Vitro 12, 670-677.
32. Hwang C, Sinskey AJ and Lodish HF (1992) Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257, 1496-1502.
33. Kim YK and Lee AS (1987) Transcriptional activation of the glucose-regulated protein genes and their heterologous fusion genes by β-mercaptoethanol. Mol. Cell. Biol. 7, 2974-2976.
34. Kim YK, Kim KS and Lee AS (1987) Regulation of the glucose-regulated protein genes by β-mercaptoethanol requires de novo protein synthesis and correlates with inhibition of protein glycosylation. J. Cell. Physiol. 133, 553-559.
35. Kohno K, Normington K, Sambrook J, Gething MJ and Mon K (1993) The promoter region of the yeast KAR2 (BiP) gene contains a regulatory domain that responds to the presence of unfolded proteins in the endoplasmic reticulum. Mol. Cell. Biol. 13, 877-890.
36. Laszlo A (1992) The thermoresistant state: Protection from initial damage or better repair? Exp. Cell Res. 104, 11-17.
37. Lee AS, Delegeane AM, Baker V and Chow PC (1983) Transcriptional regulation of two genes specifically induced by glucose starvation in a hamster mutant fibroblast cell line. J. Biol. Chem. 258, 597-603.
38. Lee K-J and Hahn GM (1988) Abnormal proteins as the trigger for the induction of stress responses: Heat, diamide and sodium arsenite. J. Cell. Physiol. 136, 411-420.
39. Lever JE (1985) Inducers of dome formation in epithelial cell cultures including agents that cause differentiation. In: Tissue Culture of Epithelial Cells, M Taub, ed. Plenum Press, New York, 3-22.
40. Li WWF, Alexandre S, Cao XJ and Lee AS (1993) Transactivation of the grp78 promoter by Ca2+ depletion-A comparative analysis with A23187 and the endoplasmic reticulum Ca2+-ATPase inhibitor thapsigargin. J. Biol. Chem. 268, 12003-12009.
41. Li WW, Sistonen L, Morimoto RI and Lee AS (1994) Stress induction of the mammalian GRP78/BiP protein gene: In vivo genomic footprinting and identification of p70CORE from human nuclear extract as a DNA-binding component specific to the stress regulatory element. Mol. Cell. Biol. 14, 5533-5546.
42. Liu ES, Ou JH and Lee AS (1993) Brefeldin A as a regulator of grp78 gene expression in mammalian cells. J. Biol. Chem. 267, 7128-7133.
43. Liu H, Lightfoot DL and Stevens JL (1996) Activation of heat shock factor (HSF) by alkylating agents is triggered by glutathione depletion and oxidation of protein thiols. J. Biol. Chem. 271, 4805-4812.
44. Lodish HF and Kong N (1993) The secretory pathway is normal in dithiothreitol-treated cells, but disulfide-bonded proteins are reduced and reversibly retained in the endoplasmic reticulum. J. Biol. Chem. 268, 20589-20605.
45. Losch A and Koch-Brandt C (1995) Dithiothreitol treatment of Madin-Darby canine kidney cells reversibly blocks export from the endoplasmic reticulum but does not affect vectorial targeting of secretory protein. J. Biol. Chem. 270, 11543-11548.
46. Luethy JD and Holbrook NJ (1992) Activation of the gadd153 promoter by genotoxic agents: A rapid and specific response to DNA damage. Cancer Res. 52, 5-10.
47. Luethy JD and Holbrook NJ (1994) The pathway regulating GADD153 induction in response to DNA damage is independent of protein kinase C and tyrosine kinases. Cancer Res. 54, 1902S-1906S.
48. Luethy JD, Fargnoli J, Park SJ, Fornace AJ Jr and Holbrook NJ (1990) Isolation and characterization of the hamster gadd153 gene. Activation of promoter activity by agents that damage DNA. J. Biol. Chem. 265, 16521-16526.
49. Mori K, Ma W, Gething MJ and Sambrook J (1993) A transmembrane protein with a cdc2+/CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell 74, 743-756.
50. Morimoto RI (1993) Cells in stress: Transcriptional activation of heat shock genes. Science 259, 1409-1410.
51. Price BD and Calderwood SK (1992) gadd45 and gadd153 messenger RNA levels are increased during hypoxia and after exposure of cells to agents which elevate the levels of the glucose-regulated proteins. Cancer Res. 52, 3814-3817.
52. Price BD, Mannheim-Rodman LA and Calderwood SK (1992) Brefeldin A, thapsigargin and AlF4- stimulate the accumulation of GRP78 mRNA in a cycloheximide dependent manner, whilst induction by hypoxia is independent of protein synthesis. J. Cell. Physiol. 152, 545-552.
53. Prostko CR, Brostrom MA, Galuska-Malara EM and Brostrom CO (1991) Stimulation of GRP78 gene transcription by phorbol ester and cAMP in GH3 pituitary cells. The accommodation of protein synthesis to chronic deprivation of intracellular sequestered calcium. J. Biol. Chem. 266, 19790-19795.
54. Prostko CR, Brostrom MA, Malara EM and Brostrom CO (1992) Phosphorylation of eukaryotic initiation factor (eIF)2 alpha and inhibition of eIF-2B in GH3 pituitary cells by perturbants of early protein processing that induce GRP78. J. Biol. Chem. 267, 16751-16754.
55. Ron D and Habener JF (1992) CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes Dev. 6, 439-453.
56. Roy B and Lee AS (1995) Transduction of calcium stress through interaction of the human transcription factor CBF with the proximal CCAAT regulatory element of the grp78/BiP promoter. Mol. Cell. Biol. 15, 2263-2274.
57. Sawyer JT, Lukarczyk T and Yilla M (1994) Dithiothreitol treatment induces heterotypic aggregation of newly synthesized secretory proteins in HepG2 cells. J. Biol. Chem. 269, 27344-27350.
58. Schreck R, Albermann K and Baeuerle PA (1992) Nuclear factor kappaB-an oxidative stress-responsive transcription factor of eukaryotic cells (A Review). Free Radical. Res. Commun. 17, 221-237.
59. Shibanuma M, Kuroki T and Nose K (1988) Induction of DNA replication and expression of proto-oncogene c-myc and c-fos in quiescent Balb/3T3 cells by xanthine/xanthine oxidase. Oncogene 3, 17-21.
60. Shibanuma M, Kuroki T and Nose K (1990) Stimulation by hydrogen peroxide of DNA synthesis, competence family gene expression and phosphorylation of a specific protein in quiescent Balb/3T3 cells. Oncogene 5, 1025-1032.
61. Sies H (1993) Strategies of antioxidant defense. Eur. J. Biochem. 215, 213-219.
62. Stevens J, Hayden P and Taylor G (1986) The role of glutathione conjugate metabolism and cysteine conjugate beta-lyase in the mechanism of S-cysteine conjugate toxicity in LLC-PK1 cells. J. Biol. Chem. 261, 3325-3332.
63. Store G, Tartaglia LA and Ames BN (1990a) Transcriptional regulator of oxidative stress-inducible genes: direct activation by oxidation. Science 248, 189-194.
64. Storz G, Tartaglia LA, Farr SB and Ames BN (1990b) Bacterial defenses against oxidative stress. Trends. Genet. 6, 363-368.
65. Sundaresan M, Yu Z-X, Ferrans VJ, Irani K and Finkel T (1995) Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 270, 296-299.
66. Sylvester S, Rhys CMJ, Leuthy-Martindale JD and Holbrook NJ (1994) Induction of GADD153, a CCAAT/enhancer-binding protein (C/EBP)-related gene, during the acute phase response in rats. J. Biol. Chem. 269, 20119-20125.
67. Ubeda M, Wang X-Z, Zinszner H, Wu I, Habener JF and Ron D (1996) Stress-induced binding of the transcription factor CHOP to a novel DNA control element. Mol. Cell. Biol. 16, 1479-1489.
68. Virbasius CS, Virbasius JV and Scarpulla RC (1993) NRF-1, an activator involved in nuclear mitochondrial interactions, utilizes a new DNA-binding domain conserved in a family of developmental regulators. Genes Dev. 7, 2431-2445.
69. Wang X-Z, Lawson B, Brewer JW, Zinszner H, Sanjay A, Mi L-J, Boorstein R, Kreibich G, Hendershot L and Ron D (1996) Signals from the stress endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol. Cell. Biol. 16, 4273-4280.
70. Welch WJ (1992) Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol. Rev. 72, 1063-1081.
71. Whelan SA and Hightower LE (1985) Differential induction of glucose-regulated and heat shock proteins: Effects of pH and sulfhydryl-reducing agents on chicken embryo cells. J. Cell. Physiol. 125, 251-258.
72. Wooden SK, Li LJ, Navarro D, Qadri I, Pereira L and Lee AS (1991) Transactivation of the grp78 promoter by malfolded proteins, glycosylation block, and calcium ionophore is mediated through a proximal region containing a CCAAT motif which interacts with CTF/NF-I. Mol. Cell. Biol. 11, 5612-5623.
73. Yu K, Chen Q, Liu H, Zhan Y and Stevens JL (1994) Signalling the molecular stress response to nephrotoxic and mutagenic cysteine conjugates: differential roles for protein synthesis and calcium in the induction of c-fos and c-myc mRNA in LLC-PK1 cells. J. Cell. Physiol. 161, 303-311.
74. Zhan Q, Lord KA, Alamo IJ et al (1994) The gadd and MyD genes define a novel set of mammalian genes encoding acidic proteins that synergistically suppress cell growth. Mol. Cell. Biol. 14, 2361-2371.