Infarct volume after transient middle cerebral artery occlusion (MCAo) can be reduced by attenuation but not by inactivation of c-Jun action

Brain Research

Volumn 1151, Issue 1, 2007, Pages 12-19

  Vogel, Johannes ^a,f   Weigand, Markus A ^b   Behrens, Axel ^c,d   Wagner, Erwin F ^c   Schorpp Kistner, Marina ^e   Zimmermann, Manfred ^a   Schenkel, Johannes ^a,e  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b Heidelberg Medical School   (Germany)

^c RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^d THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^f UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Activating transcription factor 2 (ATF 2); Activator protein 1 (AP 1); Apoptosis; c Jun; Cell death; Ischemia

Indexed keywords

CASPASE 3; PROTEIN C JUN; SERINE;

ANIMAL TISSUE; ARTICLE; ATTENUATION; BRAIN INFARCTION; BRAIN INFARCTION SIZE; CONTROLLED STUDY; DNA MODIFICATION; GENE INACTIVATION; GENE OVEREXPRESSION; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; REPERFUSION; STAINING; TRANSGENIC MOUSE;

ACTIVATING TRANSCRIPTION FACTOR 2; ANALYSIS OF VARIANCE; ANIMALS; CASPASE 3; IN SITU NICK-END LABELING; INDOLES; INFARCTION, MIDDLE CEREBRAL ARTERY; INTERMEDIATE FILAMENT PROTEINS; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURONS; PROTO-ONCOGENE PROTEINS C-JUN; SERINE; TIME FACTORS;

MUS; MUS MUSCULUS;

EID: 34248185059     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2007.03.023     Document Type: Article

References (64)

1. Adler V., Schaffner A., Kim J., Dolan L., and Ronai Z. UV irradiation and heat shock mediate JNK activation via alternate pathways. J. Biol. Chem. 27 (1996) 26071-26077
2. Angel P., and Karin M. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim. Biophys. Acta 1072 (1991) 129-157
3. Barone F.C., Knudsen D.J., Nelson A.H., Feuerstein G.Z., and Willette R.N. Mouse strain differences in susceptibility to cerebral ischemia are related to cerebral vascular anatomy. J. Cereb. Blood Flow Metab. 13 (1993) 683-692
4. Beer J., Mielke K., Zipp M., Zimmermann M., and Herdegen T. Expression of c-jun, junB, c-fos, fra-1 and fra-2 mRNA in the rat brain following seizure activity and axotomy. Brain Res. 794 (1988) 255-266
5. Behrens A., Sibilia M., and Wagner E.F. Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat. Genet. 21 (1999) 326-329
6. Behrens A., Sabapathy K., Graef I., Cleary M., Crabtree G.R., and Wagner E.F. Jun N-terminal kinase 2 modulates thymocyte apoptosis and T cell activation through c-Jun and nuclear factor of activated T cell (NF-AT). Proc. Natl. Acad. Sci. U. S. A. 98 4 (2001) 1769-1774
7. Berger A.J., Kluger H.M., Li N., Kielhorn E., Halaban R., Ronai Z., and Rimm D.L. Subcellular localization of activating transcription factor 2 in melanoma specimens predicts patient survival. Cancer Res. 63 23 (2003) 8103-8107
8. Bossy-Wetzel E., Bakiri L., and Yaniv M. Induction of apoptosis by the transcription factor c-Jun. EMBO J. 16 7 (1997) 1695-1709
9. Brecht S., Kirchhof R., Chromik A., Willesen M., Nicolaus T., Raivich G., Wessig J., Waetzig V., Goetz M., Claussen M., Pearse D., Kuan C.Y., Vaudano E., Behrens A., Wagner E., Flavell R.A., Davis R.J., and Herdegen T. Specific pathophysiological functions of JNK isoforms in the brain. Eur. J. Neurosci. 21 2 (2005) 363-377
10. Chiu R., Angel P., and Karin M. Jun-B differs in its biological properties from, and is a negative regulator of, c-Jun. Cell 59 6 (1989) 979-986
11. Connolly E.S., Winfree C.J., Stern D.M., Solomon R.A., and Pinsky D.J. Procedural and strain related variables significantly affect outcome in a murine model of focal cerebral ischemia. Neurosurgery 38 (1996) 523-531
12. Deng T., and Karin M. JunB differs from c-Jun in its DNA-binding and dimerization domains, and represses c-Jun by formation of inactive heterodimers. Genes Dev. 7 (1993) 479-490
13. Dubal D.B., Shughrue P.J., Wilson M.E., Merchenthaler I., and Wise P.M. Estradiol modulates bcl-2 in cerebral ischemia: a potential role for estrogen receptors. J. Neurosci. 19 (1999) 6385-6393
14. Eferl R., Ricci R., Kenner L., Zenz R., David J.P., Rath M., and Wagner E.F. Liver tumor development. c-Jun antagonizes the proapoptotic activity of p53. Cell 112 2 (2003) 181-192
15. Grimm C., Wenzel A., Behrens A., Hafezi F., Wagner E.F., and Reme C.E. AP-1 mediated retinal photoreceptor apoptosis is independent of N-terminal phosphorylation of c-Jun. Cell Death Differ. 8 8 (2001) 859-867
16. Ham J., Babij C., Whitfield J., Pfarr C.M., Lallemand D., Yaniv M., and Rubin L.L. A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron 14 (1995) 927-939
17. Herdegen T., Kovary K., Buhl A., Bravo R., Zimmermann M., and Gass P. Basal expression of the inducible transcription factors c-Jun, JunB, JunD, c-Fos, FosB, and Krox-24 in the adult rat brain. J. Comp. Neurol. 354 1 (1995) 39-56
18. Herdegen T., Skene P., and Bähr M. The c-Jun protein-transcriptional mediator of neuronal survival, regeneration and death. Trends Neurosci. 20 (1997) 227-231
19. Herdegen T., Claret F.X., Kallunki T., Martin-Villalba A., Winter C., Hunter T., and Karin M. Lasting N-terminal phosphorylation of c-Jun and activation of c-Jun N-terminal kinases after neuronal injury. J. Neurosci. 18 14 (1998) 5124-5135
20. Hibi M., Lin A., Smeal T., Minden A., and Karin M. Identification of an oncoprotein- and Uv-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev. 7 11 (1993) 2135-2148
21. Hockenbery D., Nunez G., Milliman C., Schreiber R.D., and Korsmeyer S.J. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 348 (1990) 334-336
22. Johnson R.S., van Lingen B., Papaioannou V.E., and Spiegelman B.M. A null mutation at the cjun locus causes embryonic lethality and retarded cell growth in culture. Genes Dev. 7 (1993) 1309-1317
23. Kang C.D., Jang J.H., Kim K.W., Lee H.J., Jeong C.S., Kim C.M., Kim S.H., and Chung B.S. Activation of c-jun N-terminal kinase/stress-activated protein kinase and the decreased ratio of Bcl-2 to Bax are associated with the auto-oxidized dopamine-induced apoptosis in PC12 cells. Neurosci. Lett. 256 (1998) 37-40
24. Kapinya K., Penzel R., Sommer C., and Kiessling M. Temporary changes of the AP-1 transcription factor binding activity in the gerbil hippocampus after transient global ischemia, and ischemic tolerance induction. Brain Res. 872 1-2 (2000) 282-293
25. Karin M. The regulation of AP-1 activity by mitogen-activated protein kinases. J. Biol. Chem. 270 (1995) 16483-16486
26. Katchanov J., Waeber C., Gertz K., Gietz A., Winter B., Bruck W., Dirnagl U., Veh R.W., and Endres M. Selective neuronal vulnerability following mild focal brain ischemia in the mouse. Brain Pathol. 13 (2003) 452-464
27. Kim Y.H., and Kim S.S. Increase of MnSOD expression and decrease of JNK activity determine the TNF sensitivity in bcl2-transfected L929 cells. Cytokine 11 (1999) 274-281
28. Korematsu K., Goto S., Nagahiro S., and Ushio Y. Changes of immunoreactivity for synaptophysin ('protein p38') following a transient cerebral ischemia in the rat striatum. IBrain. Res. 616 (1993) 320-324
29. Kwon D., Cheong J.H., Lee J.C., Kwon J.H., and Kim W.K. Lipopolysaccharides-activated human astroglioma cells induce apoptotic death of T-lymphocytes via c-Jun N-terminal kinases-dependent up-regulation of TRAIL. Neurosci. Res. 54 4 (2006) 338-343
30. LeBlanc A.C. Natural cellular inhibitors of caspases. Prog. Neuro-psychopharmacol. Biol. Psychiatry 27 2 (2003) 215-229
31. Lee L., Irani K., and Finkel T. Bcl-2 regulates nonapoptotic signal transduction: inhibition of c-Jun N-terminal kinase (JNK) activation by IL-1 beta and hydrogen peroxide. Mol. Genet. Metab. 64 (1998) 19-24
32. Li Y., Chopp M., Jiang N., Yao F., and Zaloga C. Temporal profile of in situ DNA fragmentation after transient middle cerebral artery occlusion in the rat. J. Cereb. Blood Flow Metab. 15 (1995) 389-397
33. Lin T.N., He Y.Y., Wu G., Khan M., and Hsu C.Y. Effect of brain edema on infarct volume in a focal cerebral ischemia model in rats. Stroke 24 (1993) 117-121
34. Martinou J.C., Dubois-Dauphin M., Staple J.K., Rodriguez I., Frankowski H., Missotten M., Albertini P., Talabot D., Catsicas S., Pietra C., et al. Overexpression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron 13 4 (1994) 1017-1030
35. Martin-Villalba A., Herr I., Jeremias I., Hahne M., Brandt R., Vogel J., Schenkel J., Herdegen T., and Debatin K.M. CD95 ligand (Fas-L/APO-1L) and tumor necrosis factor-related apoptosis-inducing ligand mediate ischemia-induced apoptosis in neurons. J. Neurosci. 19 (1999) 3809-3817
36. Martin-Villalba A., Hahne M., Kleber S., Vogel J., Falk W., Schenkel J., and Krammer P.H. Therapeutic neutralization of CD95-ligand and TNF attenuates brain damage in stroke. Cell Death Differ. 8 7 (2001) 679-686
37. Mueller T.H., Kienle K., Beham A., Geissler E.K., Jauch K.W., and Rentsch M. Caspase 3 inhibition improves survival and reduces early graft injury after ischemia and reperfusion in rat liver transplantation. Transplantation 78 9 (2004) 1267-1273
38. Paganini-Hill A. Estrogen replacement therapy and stroke. Prog. Cardiovasc. Dis. 38 (1995) 223-242
39. Passegue E., Jochum W., Behrens A., Ricci R., and Wagner E.F. JunB can substitute for Jun in mouse development and cell proliferation. Nat. Genet. 30 2 (2001) 116-158
40. Passegue E., Jochum W., Behrens A., Ricci R., and Wagner E.F. JunB can substitute for Jun in mouse development and cell proliferation. Nat. Genet. 30 2 (2002) 158-166
41. Pearson A.G., Curtis M.A., Waldvogel H.J., Faull R.L., and Dragunow M. Activating transcription factor 2 expression in the adult human brain: association with both neurodegeneration and neurogenesis. Neuroscience 133 2 (2005) 437-451
42. Raivich G., Bohatschek M., Da Costa C., Iwata O., Galiano M., Hristova M., Nateri A.S., Makwana M., Riera-Sans L., Wolfer D.P., Lipp H.P., Aguzzi A., Wagner E.F., and Behrens A. The AP-1 transcription factor c-Jun is required for efficient axonal regeneration. Neuron 43 1 (2004) 57-67
43. Schenkel J. Activation of the c-Jun transcription factor following neurodegeneration in vivo. Neurosci. Lett. 361 1-3 (2004) 36-39
44. Schenkel J., Gaissert H., Protopapa E.E., Weiher H., Gissmann L., and Alonso A. The human papillomavirus type 11 upstream regulatory region triggers hair-follicle-specific gene expression in transgenic mice. J. Invest. Dermatol. 112 6 (1999) 893-898
45. Schmidt R., Fazekas F., Reinhart B., Kapeller P., Fazekas G., Offenbacher H., Eber B., Schumacher M., and Freidl W. Estrogen replacement therapy in older women: a neuropsychological and brain MRI study. J. Am. Geriatr. Soc. 44 (1996) 1307-1313
46. Schorpp M., Jager R., Schellander K., Schenkel J., Wagner E.F., Weiher H., and Angel P. The human ubiquitin C promoter directs high ubiquitous expression of transgenes in mice. Nucleic Acids Res. 24 9 (1996) 1787-1788
47. Schorpp-Kistner M., Wang Z.Q., Angel P., and Wagner E.F. JunB is essential for mammalian placentation. EMBO J. 18 4 (1999) 934-948
48. Simi A., Ingelman-Sundberg M., and Tindberg N. Neuroprotective agent chlomethiazole attenuates c-fos, c-jun, and AP-1 activation through inhibition of p38 MAP kinase. J. Cereb. Blood Flow Metab. 20 7 (2000) 1077-1088
49. Sommer C., Gass P., and Kiessling M. Selective c-Jun expression in CA1 neurons of the gerbil hippocampus during and after acquisition of an ischemia-tolerant state. Brain Pathol. 5 (1995) 135-144
50. Swanson R.A., Morton M.T., Tsao-Wu G., Savalos R.A., Davidson C., and Sharp F.R. A semiautomated method for measuring brain infarct volume. J. Cereb. Blood Flow Metab. 10 (1990) 290-293
51. Tronche F., Kellendonk C., Kretz O., Gass P., Anlag K., Orban P.C., Bock R., Klein R., and Schutz G. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat. Genet. 23 1 (1999) 99-103
52. Vexler Z.S., Roberts T.P.L., Bolen A.W., Derugin N., and Arieff A.I. Transient cerebral ischemia. J. Clin. Invest. 99 (1997) 1453-1459
53. Vogel J., Mobius C., and Kuschinsky W. Early delineation of ischemic tissue in rat brain cryosections by high-contrast staining. Stroke 30 (1999) 1134-1141
54. Vyas S., Javoy-Agid F., Herrero M.T., Strada O., Boissiere F., Hibner U., and Agid Y. Expression of Bcl-2 in adult human brain regions with special reference to neurodegenerative disorders. J. Neurochem. 69 1 (1997) 223-231
55. Wang Z.Q., Ovitt C., Grigoriadis A.E., Möhle-Steinlein U., Rüther U., and Wagner E.F. Bone and haematopoietic defects in mice lacking c-fos. Nature 360 (1992) 741-745
56. Watson A., Eilers A., Lallemand D., Kyriakis J., Rubin L.L., and Ham J. Phosphorylation of c-Jun is necessary for apoptosis induced by survival signal withdrawal in cerebellar granule neurons. J. Neurosci. 18 (1998) 751-762
57. Winter C., Schenkel J., Zimmermann M., and Herdegen T. MAP kinase phosphatase 1 is expressed and enhanced by FK506 in surviving mamillary, but not degenerating nigral neurons following axotomy. Brain Res. 801 (1998) 198-205
58. Winter C., Schenkel J., Burger E., Eickmeier C., Zimmermann M., and Herdegen T. The immunophilin ligand FK506, but not GPI-1046, protects against neuronal death and inhibits c-Jun expression in the substantia nigra pars compacta following transection of the rat medial forebrain bundle. Neuroscience 95 (2000) 753-762
59. Winter C., Weiss C., Martin-Villalba A., Zimmermann M., and Schenkel J. JunB and Bcl-2 overexpression results in protection against cell death of nigral neurons following axotomy. Mol. Brain Res. 104 (2002) 194-202
60. Wisdom R. AP-1: one switch for many signals. Exp. Cell Res. 253 1 (1999) 180-185
61. Yamamoto K., Ichijo H., and Korsmeyer S.J. BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G(2)/M. Mol. Cell. Biol. 19 (1999) 8469-8478
62. Zea Longa E., Weinstein P.R., Carlson S., and Cummis R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20 (1989) 84-91
63. Zenz R., Scheuch H., Martin P., Frank C., Eferl R., Kenner L., Sibilia M., and Wagner E.F. c-Jun regulates eyelid closure and skin tumor development through EGFR signaling. Dev. Cell 4 6 (2003) 879-889
64. Zhong L.T., Sarafian T., Kane D.J., Charles A.C., Mah S.P., Edwards R.H., and Bredesen D.E. Bcl-2 inhibits death of central neural cells induced by multiple agents. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 4533-4537