Neuronal survival activity of S100ββ is enhanced by calcineurin inhibitors and requires activation of NF-κB

FASEB Journal

Volumn 13, Issue 12, 1999, Pages 1611-1620

  Alexanian, Arshak R ^a   Hamburg, James R ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Cyclosporin A; Cypermethrin; FK506; Immunophilins; Immunosuppressants; Rapamycin

Indexed keywords

CALCINEURIN; CALCIUM BINDING PROTEIN; CIPERMETHRIN; CYCLOSPORIN A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NEUROTROPHIC FACTOR; RAPAMYCIN; TACROLIMUS;

ANIMAL CELL; ARTICLE; CELL SURVIVAL; FOREBRAIN; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; NERVE CELL; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0032851616     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.13.12.1611     Document Type: Article

References (61)

1. Korsching, S. (1993) The neurotrophic factor concept: a reexamination. J. Neurosci. 13, 2739-2748
2. Friedman, B., Kleinfeld, D., Ip, N. Y., Verge, V. M. K., Moulton, R., Boland, P., Zlotchenko, E., Lindsay, R. M., and Miu, L. (1995) BDNF and NT-4/5 exert neurotrophic influences on injured adult spinal motor neurons. J. Neurosci. 15, 1044-1056
3. Grothe, C., and Wewetzer, K. (1996) Fibroblast growth factor and its implications for developing and regenerating neurons. Int. J. Dev. Biol. 40, 403-410
4. Zhao, B., and Schwartz, J. P. (1998) Involvement of cytokines in normal CNS development and neurological disease: recent progress and perspectives. J. Neurosci. Res. 52, 7-16
5. Morganti-Kossmann, M. C., Kossmann, T., and Wahl, S. M. (1992) Cytokines and neuropathology. Trends Pharmacol. Sci. 13, 286-291
6. Steiner, J. P., Dawson, T. M., Fotuhi, M., Glatt, C. E., Snowman, A. M., Cohen, N., and Snyder, S. H. (1992) High brain densities of the immunophilin FKBP colocalized with calcineurin. Nature (London) 358, 584-587
7. Rothwell, N. J., and Strijbos, P. J., (1995) Cytokines in neurodegeneration and repair. Int. J. Dev. Neurosci. 13, 179-185
8. Steiner, J. P., Hamilton, G. S., Ross, D. T., Valentine, H. L., Guo, H., Connolly, M. A., Liang, S., Ramsey, C., Li, J. H., Huang, W., Howorth, P., Soni, R., Fuller, M., Sauer, H., Nowotink, A. C., and Suzdak, P. D. (1997) Neurotrophic immunophilin ligands stimulate structural and functional recovery in neurodegenerative animal models. Proc. Natl. Acad. Sci. USA 94, 2019-2024
9. Donato, R. (1986) S-100 proteins. Cell Calcium 7, 123-145
10. Van Eldik, L. J., and Zimmer, D. B. (1988) Mechanism of action of the S100 family of calcium modulated proteins. In Calcium and Calcium Binding Proteins (Gerday, C. H., Gilles, R., and Bolis, L., eds) pp. 114-127, Springer-Verlag, Berlin, Germany
11. Hu, J., Ferreira, A., and Van Eldik, L. J. (1997) S-100 beta induces neuronal cell death through nitric oxide release from astrocytes. J Neurochem. 69, 2294-2301
12. Winningham-Major, F., Staecker, J. L., Barger, S. W., Coats, S., and Van Eldik, L. J. (1989) Neurite extension and neuronal survival activities of recombinant S100 beta proteins that differ in the content and position of cysteine residues. J. Cell Biol. 109, 3063-3071
13. Bhattacharyya, A., Oppenheim, R. W., Prevette, D., Moore, B. W., Brackenbury, R., and Ratner, N. (1992) S-100 is present in developing chicken neurons and Schwann cells and promotes neuron survival in vivo. J. Neurobiol. 23, 451-466
14. Barger, S. W., Van Eldik, L. J., and Mattson, M. P. (1995) S100 beta protects hippocampal neurons from damage induced by glucose deprivation. Brain Res. 677, 167-170
15. Bierer, B. E., Mattila, P. S., Standaert, R. F., Herzenberg, L. A., Burakoff, S. J., Crabtree, G., and Schreiber, S. L. (1990) Two distinct signal transmission pathways in T lymphocytes are inhibited by complexes formed between an immunophilin and either FK506 or rapamycin. Proc. Natl. Acad. Sci. USA 87, 9231-9235
16. Liu, J., Farmer, J. D. Jr., Lane, W. S., Friedman, J., Weissman, I., and Schreiber, S. L. (1991) Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66, 807-815
17. Liu, Y. C., and Storm, D. R. (1989) Dephosphorylation of neuromodulin by calcineurin. J. Biol. Chem. 264, 12800-12804
18. Mittal, C. K., and Jadhav, A. L. (1994) Calcium-dependent inhibition of constitutive nitric oxide synthase. Biochem. Biophys. Res. Commun. 201, 8-15
19. 2+-dependent signal transduction pathways. J. Immunol. 155, 4685-4691
20. Beg, A. A., Ruben, S. M., Scheinman, R. I., Haskill, S., Rosen, C. A., and Baldwin, A. J. (1992) IκB interacts with the nuclear localization sequences of the subunits of NF-κB: a mechanism for cytosolic retention. Genes Dev. 61, 1899-1913
21. Suzuki, T., Mitake, S., Okumura-Noji, K., Yang, J. P., Fujii, T., and Okamoto, T. (1997) Presence of NF-κB-like and IκB-like immunoreactivities in postsynaptic densities. NeuroReport 8, 2931-2935
22. Kaltschmidt, C., Kaltschmidt, B., and Baeuerle, P. A. (1995) Stimulation of ionotrophic glutamate receptors activates transcription factor NF-κB in primary neurons. Proc. Natl. Acad. Sci. USA 92, 9618-9622
23. Carter, B. D., Kaltschmidt, C., Kaltschmidt, B., Offenhauser, N., Bohm-Matthaei, R., Baeuerle, P. A., and Barde, Y. A. (1996) Selective activation of NF-kappaB by nerve growth factor through the neurotrophin receptor p75. Science 272, 542-545
24. Mercurio, F., Zhu, H., Murray, B. W., Shevchenko, A., Bennett B. L., Li, J., Young, D. B., Barbosa M., Mann, M., Manning, A., and Rao, A. (1997) IKK-1 and IKK-2: cytokine-activated Ikappa B kinases essential for NF-kappaB activation. Science 278, 860-866
25. Woronicz, J. D., Gao, X., Cao, Z, Rothe, M., and Goeddel, D. V. (1997) IkappaB kinase-beta: NF-kappaB activation and complex formation with IkappaB kinase-alpha and NIK. Science 278, 866-869
26. Schreck, R., Rieber, P., and Baeuerle, P. A. (1991) Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J. 10, 2247-2258
27. Staal, F. J., Anderson, M. T., and Herzenberg, L. A. (1995) Redox regulation of activation of NF-kappa B transcription factor complex: effects of N-acetylcysteine. Methods Enzymol. 252, 168-174
28. Anderson, M. T., Staal, F. J., Gilter, C., Herzenberg, L. A., and Herzenberg, L. A. (1994) Separation of oxidant-initiated and redox-regulated steps in the NF-kappaB signal transduction pathway. Proc. Natl. Acad. Sci. USA 91, 11527-11531
29. Ghosh, S., May, M. J., and Kopp, E. B. (1998) NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16, 225-260
30. Perez-Otano, I., McMillian, M. K., Chen, J., Bing, G., Hong, J. S., and Pennypacker, K. R. (1996) Induction of NF-κB-like transcription factors in brain areas susceptible to kainate toxicity. Glia 16, 306-315
31. O'Neill, L. A., and Kaltschmidt, C. (1998) NF-kappa B: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci. 20, 252-258
32. Hunot, S., Brugg, B., Ricard, D., Michel, P. P., Muriel, M. P., Ruberg, M., Faucheux, B. A., Agid, Y., and Hirsch, E. C. (1997) Nuclear translocation of NF-kappaB is increased in dopaminergic neurons of patients with Parkinson disease. Proc. Natl. Acad. Sci. USA 94, 7531-7536
33. Boissiere, F., Hunot S., Faucheux, B., Duyckaerts, C., Hauw, J. J. Agid, Y., and Hirsch, E. C. (1997) Nuclear translocation of NF-κB in cholinergic neurons of patients with Alzheimer's disease. NeuroReport 8, 2849-2852
34. Geo, Q., Robinson, N., Mattson, M. P. (1998) Secreted beta-amyloid precursor protein counteracts the proapoptotic action of mutant presenilin-1 by activation of NF-kappaB and stabilization of calcium homeostasis. J. Biol. Chem. 273, 12341-12351
35. Isobe, T., Nakajima, T., and Okuyama, T. (1977) Reinvestigation of extremely acidic proteins in bovine brain. Biochim. Biophys. Acta 494, 222-232
36. Baudier, J., Holtzscherer, C., and Gerard, D. (1982) Zinc-dependent affinity chromatography of the S-100β protein on phenyl-Sepharose. FEBS Lett. 148, 231-234
37. Barger, S. W., Wolchok, S. R., and Van Eldik, L. J. (1992) Disulfide-linked S100 beta dimers and signal transduction. Biochim. Biophys. Acta 1160, 105-112
38. Wessel, D., and Flügge, U. I. (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem 138, 141-143
39. Laemmli, U. K., (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227, 680-685
40. Minamide, L. S., and Bamburg, J. R. (1990) A filter paper dye-binding assay for quantitative determination of protein without interference from reducing agents or detergents. Anal. Biochem. 190, 66-70
41. Towbin, H., Staehelin, T., and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350-4354
42. Pettman, B., Kouis, S. C., and Sensenbrenner, M. (1979) Morphological and biochemical maturation of neurons cultured in the absence of glial cells. Nature (London) 281, 378-380
43. Enan, E., and Matsumura, F. (1992) Specific inhibition of calcineurin by type II synthetic pyrethroid insecticides. Biochem. Pharmacol. 43, 1777-1784
44. Snyder, S. H., Lai, M. M., and Burneu, P. E. (1998) Immunophilins in the nervous system. Neuron 21, 283-294
45. Dawson, T. M., Steiner, J. P., Lyons, W. E., Fotuhi, M., Blue, M., and Snyder, S. H. (1994) Immunophilins, FK506 binding protein and cyclophilin, are discretely localized in the brain: relationship to calcineurin. Neuroscience 62, 569-580
46. Lai, M. M., Burnett, P. E., Wolosker, H., Blackshaw, S., and Snyder, S. H. (1998) Cain, a novel physiologic protein inhibitor of calcineurin. J. Biol. Chem. 273, 18325-18331
47. Marinovich, M., Viviani B., Corsini, E., Chilardi, F., and Galli, C. L. (1996) NF-κB activation by triphenyltin triggers apoptosis in HL-60 cells. Exp. Cell Res. 226, 98-104
48. Yamaoka, S., Courtois, G., Bessia, C., Whiteside, S. T., Weil, R., Agou, F., Kirk, H. E., Kay, R. J., and Israel, A. (1998) Complementation cloning of NEMO, a component of the IκB kinase complex essential for NF-κB activation. Cell 93, 1231-1240
49. Natarajan, K., Manna, S. K., Chaturvedi, M. M., and Aggarwal, B. B. (1998) Protein tyrosine kinase inhibitors block tumor necrosis factor-induced activation of nuclear factor-kappaB, degradation of IkappaB alpha, nuclear translocation of p65 and subsequent gene expression. Arch. Biochem. Biophys. 352, 59-70
50. Malinin, N. L, Boldin, M. P., Kovalenko, A. V., and Wallach, D. (1997) MAP3K-related kinase involved in NF-kappaB induction by TNF, CD95 and IL-1. Nature (London) 385, 540-544
51. Migheli, A., Piva, R., Atzori, C., Troost, D., and Schiffer, D. (1997) c-Jun, JNK/SAPK kinases and transcription factor NF-kappaB are selectively activated in astrocytes, but not motor neurons, in amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 56, 1314-1322
52. Harhaj, E. W., and Sun, S. C. (1997) The serine/threonine phosphatase inhibitor calyculin A induces rapid degradation of IKappaBbeta. Requirement of both the N- and C-terminal sequences. J. Biol. Chem. 272, 5409-5412
53. 2+ influx. Functional synergy between Raf and calcineurin. J. Immunol. 157, 5277-5283
54. Clemens, J. A., Stephenson, D. T., Smalstig, E. B., Dixon, E. P., Little, S. P. (1997) Global ischemia activates nuclear factor-kappa B in forebrain neurons of rats. Stroke 28, 1073-1080
55. Mrak, R. E., Sheng, J. G., and Griffin, W. S. (1995) Glial cytokines in Alzheimer's disease: review and pathogenic implications. Human Pathol 26, 816-823
56. Beg, A. A., and Baltimore, D. (1996) An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 274, 782-784
57. Van Antwerp, D. J., Martin, S. J., Kafri, T., Green, D. R., and Verma, I. M. (1996) Suppression of TNF-α-induced apoptosis by NF-κB. Science 274, 787-789
58. Mattson, M. P., Goodman, Y., Luo, H., Fu, W., and Furukawa, K. (1997) Activation of NF-kappaB protects hippocampal neurons against oxidative stress-induced apoptosis: evidence for induction of manganese superoxide dismutase and suppression of peroxynitrite production and protein tyrosine nitration. J. Neurosci. Res. 49, 681-697
59. Wang, C. Y., Mayo, M. W., Korneluk, R. G., Goeddel, D. V., Baldwin, A. S. (1998) NF-κB antiapoptosis: Induction of TRAF1 and TRAF2 and c-IAP1 and C-IAP2 to suppress caspase-8 activation. Science 281, 1680-1683
60. 3 integrin-induced endothelial cell survival. J. Cell Biol. 141, 1083-1093
61. Lin, K. I., Didonato, J. A., Hoffmann, A., Hardwick, J. M., and Ratan, R. R. (1998) Suppression of steady-state, but not stimulus-induced NF-κB activity inhibits alphavirus-induced apoptosis. J. Cell Biol. 141, 1479-1487