In vivo heat-shock response in the brain: Signalling pathway and transcription factor activation

Molecular Brain Research

Volumn 119, Issue 1, 2003, Pages 90-99

  Maroni, Paola ^a   Bendinelli, Paola ^a   Tiberio, Laura ^b   Rovetta, Francesca ^b   Piccoletti, Roberta ^a   Schiaffonati, Luisa ^b  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF BRESCIA   (Italy)

Author keywords

Akt; Cerebellum; Heat shock; Hippocampus; Mitogen activated protein kinases; Transcription factors

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; HEAT SHOCK PROTEIN 70; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR AP 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BODY TEMPERATURE; BRAIN INJURY; BRAIN REGION; CELL SURVIVAL; CEREBELLUM; CONTROLLED STUDY; DNA BINDING; GENE EXPRESSION REGULATION; HEAT STRESS; HIPPOCAMPUS; HYPERTHERMIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; RAT; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

EID: 0142246636     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbrainres.2003.08.018     Document Type: Article

References (70)

1. Ananthan J., Goldberg A.L., Voellmy R. Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heath shock genes. Science. 232:1986;522-524.
2. Angel P., Imagawa M., Kiu R., Stein B., Imbra R.J., Rahmsdorf H.J., Jonat C., Herrlich P., Karin M. Phorbol ester-inducible genes contain a common cis element recognized by a TPA-modulated transactivating factor. Cell. 49:1987;729-739.
3. Bendinelli P., Maroni P., Pecori Giraldi F., Piccoletti R. Leptin activates Stat3, Stat1 and AP-1 in mouse adipose tissue. Mol. Cell. Endocrinol. 168:2000;11-20.
4. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254.
5. Brazil D.P., Hemmings B.A. Ten years of protein kinase B signalling: a hard Akt to follow. Trends Biochem. Sci. 26:2001;657-664.
6. Brunet A., Bonni A., Zigmond M.J., Lin M.Z., Juo P., Hu L.S., Anderson M.J., Arden K.C., Blenis J., Greenberg M.E. Akt promotes cell survival by phosphorylating and inhibiting a forkhead transcription factor. Cell. 96:1999;857-868.
7. Camps M., Nichols A., Gillieron C., Antonsson B., Muda M., Chabert C., Boschert U., Arkinstall S. Catalytic activation of the phosphatase MKP-3 by ERK2 mitogen-activated protein kinase. Science. 280:1998;1262-1265.
8. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
9. Coffer P.J., Jin J., Woodgett J.R. Protein kinase B (c-Akt): a multifunctional mediator of phosphatidylinositol 3-kinase activation. Biochem. J. 335:1998;1-13.
10. 2-terminal kinase targeting and phosphorylation of heat shock factor-1 suppress its transcriptional activity. J. Biol. Chem. 275:2000;18210-18218.
11. DiDomenico B.J., Bugaisky G.E., Lindquist S. The heat shock response is self-regulated at both the transcriptional and posttranscriptional levels. Cell. 31:1982;593-603.
12. Dorion S., Landry J. Activation of the mitogen-activated protein kinase pathways by heat shock. Cell Stress Chaperones. 7:2002;200-206.
13. Dorion S., Berube J., Huot J., Landry J. A short lived protein involved in the heat shock sensing mechanisms responsible for stress-activated protein kinase 2 (SAPK2/p38) activation. J. Biol. Chem. 274:1999;37591-37597.
14. Dubois M.F., Bensaude O. MAP kinase activation during heat shock in quiescent and exponentially growing mammalian cells. FEBS Lett. 324:1993;191-195.
15. Dudek H., Datta S.R., Franke T.F., Birnbaum M.J., Yao R., Cooper G.M., Segal R.A., Kaplan D.R., Greenberg M.E. Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science. 275:1997;661-665.
16. Fiorenza N.T., Farkas T., Dissing M., Kolding D., Zimarino V. Complex expression of murine heat shock transcription factors. Nucleic Acid. Res. 23:1995;467-474.
17. Foster J., Brown I.R. Differential induction of heat shock mRNA in oligodendrocytes, microglia, and astrocytes following hyperthermia. Mol. Brain Res. 45:1997;207-218.
18. Frame S., Cohen P. GSK3 takes centre stage more than 20 years after its discovery. Biochem. J. 359:2001;1-16.
19. Glazner G.W., Camandola S., Mattson M.P. Nuclear factor-kB mediates the cell survival-promoting action of activity dependent neutrophic factor peptide-9. J. Neurochem. 75:2000;101-108.
20. Grilli M.G., Memo M. Possible role of NF-κB and p53 in the glutamate-induced pro-apoptotic neuronal pathway. Cell Death Differ. 6:1999;22-27.
21. Hattori M., Tugores A., Westwick J.K., Veloz L., Leffert H.L., Karin M., Brenner D.A. Activation of activating protein 1 during hepatic acute phase response. Am. J. Physiol. 264:1993;G95-G103.
22. He B., Meng Y.H., Mivechi N.F. Glycogen synthase kinase 3beta and extracellular signal-regulated kinase inactivate heat shock transcription factor 1 by facilitating the disappearance of transcriptionally active granules after heat shock. Mol. Cell. Biol. 18:1998;6624-6633.
23. Herdegen T., Waetzig V. AP-1 proteins in the adult brain: facts and fiction about effectors of neuroprotection and neurodegeneration. Oncogene. 20:2001;2424-2437.
24. Hetman M., Hsuan S.-L., Habas A., Higgins M.J., Xia Z. ERK1/2 antagonizes glycogen synthase kinase-3β-induced apoptosis in cortical neurons. J. Biol. Chem. 277:2002;49577-49584.
25. Higashi T., Nakai A., Uemura Y., Kikuchi H., Nagata K. Activation of heat shock factor 1 in rat brain during cerebral ischemia or after heat shock. Mol. Brain Res. 34:1995;262-270.
26. Kao H.T., Nevins J.R. Transcriptional activation and subsequent control of the human heat shock gene during adenovirus infection. Mol. Cell. Biol. 3:1983;2058-2065.
27. Kato Y., Kravchenko V.V., Tapping R.I., Han J., Ulevitch R.J., Lee J.D. BMK1/ERK5 regulates serum-induced early gene expression through transcription factor MEF2C. EMBO J. 16:1997;7054-7066.
28. Kaytor M.D., Orr H.T. The GSK3β signaling cascade and neurodegenerative disease. Curr. Opin. Neurobiol. 12:2002;275-278.
29. Khan V.R., Brown I.R. The effect of hyperthermia on the induction of cell death in brain, testis, and thymus of the adult and developing rat. Cell Stress Chaperones. 7:2002;73-90.
30. Kulik G., Klippel A., Weber M.J. Antiapoptotic signalling by the insulin-like growth factor I receptor, phosphatidylinositol 3-kinase, and Akt. Mol. Cell. Biol. 17:1997;1595-1606.
31. Kyriakis J.M., Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81:2001;807-869.
32. Leifer D., Krainc D., Yu Y.-T., McDermott J., Breitbart R.E., Heng J., Neve R.L., Kosofsky B., Nadal-Ginard B., Lipton S.A. MEF2C, a MADS/MEF2-family transcription factor expressed in a laminar distribution in cerebral cortex. Proc. Natl. Acad. Sci. U. S. A. 90:1993;1546-1550.
33. Le-Niculescu H., Bonfoco E., Kasuya Y., Claret F.X., Green D.R., Karin M. Withdrawal of survival factors results in activation of the JNK pathway in neuronal cells leading to Fas ligand induction and cell death. Mol. Cell. Biol. 19:1999;751-763.
34. Leoni S., Brambilla D., Risuleo G., de Feo G., Scarsella G. Effect of different whole body hyperthermic sessions on the heat shock response in mice liver and brain. Mol. Cell. Biochem. 204:2000;41-47.
35. Liebregts M.T., McLachlan R.S., Leung L.S. Hyperthermia induces age-dependent changes in rat hippocampal excitability. Ann. Neurol. 52:2002;318-326.
36. Lyons G.E., Micales B.K., Schwarz J., Martin J.F., Olson E.N. Expression of mef2 genes in the mouse central nervous system suggests a role in neuronal maturation. J. Neurosci. 15:1995;5727-5738.
37. Malago J.J., Koninkx J.F., van Dijk J.E. The heat shock response and cytoprotection of the intestinal epithelium. Cell Stress Chaperones. 7:2002;191-199.
38. Manzerra P., Rush S.J., Brown I.R. Temporal and spatial distribution of heat shock mRNA and protein (hsp70) in the rabbit cerebellum in response to hyperthermia. J. Neurosci. Res. 36:1993;480-490.
39. Marcuccilli C.J., Mathur S.K., Morimoto R.I., Miller R.J. Regulatory differences in the stress response of hippocampal neurons and glial cells after heat shock. J. Neurosci. 16:1996;478-485.
40. Markowitz R.B., Hermann A.S., Taylor D.F., He L., Anthony-Cahill S., Ahn N.G., Dynan W.S. Phosphorylation of the C-terminal domain of RNA polymerase II by the extracellular-signal-regulated protein kinase ERK2. Biochem. Biophys. Res. Commun. 207:1995;1051-1057.
41. Maroni P., Bendinelli P., Zuccorononno C., Schiaffonati L., Piccoletti R. Cellular signalling after in vivo heat shock in the liver. Cell Biol. Int. 24:2000;145-152.
42. McKinsey T.A., Zhang C.L., Olson E.N. MEF2: a calcium-dependent regulator of cell division, differentiation and death. Trends Biochem. Sci. 27:2002;40-47.
43. Mearow K.M., Dodge M.E., Rahimtula M., Yegappan C. Stress-mediated signaling in PC12 cells - the role of the small heat shock protein, Hsp27, and Akt in protecting cells from heat stress and nerve growth factor withdrawal. J. Neurochem. 83:2002;452-462.
44. Mezger V., Bensaude O., Morange M. Unusual levels of heat shock element-binding activity in embryonal carcinoma cells. Mol. Cell. Biol. 9:1989;3888-3896.
45. Mivechi N.F., Giaccia A.J. Mitogen-activated protein kinase acts as a negative regulator of the heat shock response in NIH3T3 cells. Cancer Res. 55:1995;5512-5519.
46. Mockridge J.W., Marber M.S., Heads R.J. Activation of Akt during simulated ischemia/reperfusion in cardiac myocytes. Biochem. Biophys. Res. Commun. 270:2000;947-952.
47. Morrison A.J., Rush S.J., Brown I.R. Heat shock transcription factors and hsp70 induction response in brain and kidney of the hyperthermic rat during postnatal development. J. Neurochem. 75:2000;363-372.
48. Nunneley S.A., Martin C.C., Slauson J.W., Hearon C.M., Nickerson L.D.H., Mason P.A. Changes in regional cerebral metabolism during systemic hyperthermia in humans. J. Appl. Physiol. 92:2002;846-851.
49. Okamoto S.-I., Krainc D., Sherman K., Lipton S.A. Antiapoptotic role of the p38 mitogen-activated protein kinase-myocyte enhancer factor 2 transcription factor pathway during neuronal differentiation. Proc. Natl. Acad. Sci. U. S. A. 97:2000;7561-7566.
50. Pearson G., Robinson F., Beers Gibson T., Xu B.E., Karandikar M., Berman K., Cobb M.H. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22:2001;153-183.
51. Piccoletti R., Bendinelli P., Maroni P. Signal transduction pathway of prolactin in rat liver. Mol. Cell. Endocrinol. 135:1997;169-177.
52. Rouse J., Cohen P., Trigon S., Morange M., Alonso-Llamazares A., Zamanillo D., Hunt T., Nebreda A.R. A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell. 78:1994;1027-1037.
53. Schiaffonati L., Tacchini L., Pappalardo C. Heat shock response in the liver: expression and regulation of the HSP70 gene family and early response genes after in-vivo hyperthermia. Hepatology. 20:1994;975-983.
54. Schiaffonati L., Maroni P., Bendinelli P., Tiberio L., Piccoletti R. Hyperthermia induces gene expression of heat shock protein 70 and phosphorylation of mitogen activated protein kinases in the rat cerebellum. Neurosci. Lett. 312:2001;75-78.
55. Schneider A., Martin-Villalba A., Weih F., Vogel J., Wirth T., Schwaninger M. NF-κB is activated and promotes cell death in focal cerebral ischemia. Nat. Med. 5:1999;554-559.
56. Sharma H.S., Hoopes P.J. Hyperthermia induced pathophysiology of the central nervous system. Int. J. Hypertherm. 19:2003;325-354.
57. Shaulian E., Karin M. AP-1 as a regulator of cell life and death. Nat. Cell Biol. 4:2002;E131-E136.
58. 2 or heat shock is mediated by phosphoinositide 3-kinase and not by mitogen-activated protein kinase-activated protein kinase-2. Biochem. J. 336:1998;241-246.
59. Simon R.P., Cho H., Gwinn R., Lowestein D.H. The temporal profile of 72-kDa heat shock protein expression following global ischemia. J. Neurosci. 11:1991;881-889.
60. Smeyne R. Continuous c-Fos expression precedes programmed cell death in vivo. Nature. 363:1993;166-169.
61. Sorger P.K. Heat shock factor and the heat shock response. Cell. 65:1991;363-366.
62. Takahashi S., Tanaka R., Watanabe M., Takahashi H., Kakinuma K., Suda T., Yamada M., Takahashi H. Effects of whole-body hyperthermia on the canine central nervous system. Int. J. Hypertherm. 15:1999;203-216.
63. Tso J.Y., Sun X., Kao T., Reece K.S., Wu R. Isolation and characterization of rat and human glyceraldehyde-3-phosphate dehydrogenase cDNAs: genomic complexity and molecular evolution of the gene. Nucleic Acids Res. 13:1985;2485-2502.
64. Tunici P., Schiaffonati L., Rabellotti E., Tiberio L., Perin A., Sessa A. In vivo modulation of 73 kDa heat shock cognate and 78 kDa glucose-regulating protein gene expression in rat liver and brain by ethanol. Alcohol. Clin. Exp. Res. 23:1999;1861-1867.
65. Vogel P., Dukes E., Wiessner E. Evidence of apoptosis in primary neuronal cultures after heat shock. Brain Res. 764:1997;205-213.
66. Wang T., Zhang X., Li J.J. The role of NF-κB in the regulation of cell stress response. Int. Immunopharmacol. 2:2002;1509-1520.
67. Yang D.D., Kuan C.Y., Whitmarsh A.J., Rincon M., Zheng T.S., Davies R.J., Rakic P., Flavell R.A. Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the JNK3 gene. Nature. 389:1997;865-870.
68. Yenari M.A., Giffard R.G., Sapolsky R.M., Steinberg G.K. The neuroprotective potential of heat shock protein70 (HSP 70). Mol. Med. Today. 5:1999;525-531.
69. Zhao M., New L., Kravchenko V.V., Kato Y., Gram H., Di Padova F., Olson E.N., Ulevitch R.J., Han J. Regulation of the MEF2 family of transcription factors by p38. Mol. Cell. Biol. 19:1999;21-30.
70. Zhou G., Bao Z.Q., Dixon J.E. Component of a new human protein kinase signal transduction pathway. J. Biol. Chem. 270:1995;12665-12669.