Signal Transducer and Activator of Transcription 3 (STAT3) degradation by proteasome controls a developmental switch in neurotrophin dependence

Journal of Biological Chemistry

Volumn 288, Issue 28, 2013, Pages 20151-20161

  Murase, Sachiko ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEVELOPMENTAL SWITCH; HIPPOCAMPAL NEURONS; NATURALLY OCCURRING; NEUROTROPHINS; PROTEASOMES; SIGNAL TRANSDUCERS; TUMOR SUPPRESSORS; UBIQUITINATION;

BRAIN; NEURONS; PROTEINS; TRANSCRIPTION; TRANSDUCERS;

ENZYME INHIBITION;

ANDROGEN RECEPTOR CO-ACTIVATOR 160; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCINEURIN; CELL PROTEIN; NEUROTROPHIN; PROTEIN BAX; PROTEIN P53; STAT3 PROTEIN; TACROLIMUS; TATA ELEMENT MODULATORY FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN DEVELOPMENT; BRAIN REGION; CONTROLLED STUDY; DEVELOPMENTAL SWITCH; DEVELOPMENTAL, AGE AND GROWTH PARAMETERS; DOWN REGULATION; EMBRYO; FEMALE; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION; UBIQUITINATION; UPREGULATION;

BAX; CALCINEURIN; DEVELOPMENTAL DEATH; NEUROTROPHINS; P53; STAT3; UBIQUITIN-PROTEASOME PATHWAY;

ANIMALS; ANIMALS, NEWBORN; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CALCINEURIN; CELLS, CULTURED; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; NERVE GROWTH FACTORS; NEURONS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TACROLIMUS; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN-PROTEIN LIGASES; VESICULAR TRANSPORT PROTEINS;

EID: 84880050712     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.470583     Document Type: Article

References (57)

1. Arrigo, A. P., Tanaka, K., Goldberg, A. L., and Welch, W. J. (1988) Identity of the 19S "prosome" particle with the large multifunctional protease complex of mammalian cells (the proteasome). Nature 331, 192-194 (Pubitemid 18042153)
2. Hershko, A., Heller, H., Elias, S., and Ciechanover, A. (1983) Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown. J. Biol. Chem. 258, 8206-8214
3. McClellan, A. J., Tam, S., Kaganovich, D., and Frydman, J. (2005) Protein quality control. Chaperones culling corrupt conformations. Nat. Cell Biol. 7, 736-741 (Pubitemid 41079041)
4. Chung, K. K., Dawson, V. L., and Dawson, T. M. (2001) The role of the ubiquitin-proteasomal pathway in Parkinson's disease and other neurodegenerative disorders. Trends Neurosci. 24, S7-S14
5. Hershko, A. (1997) Roles of ubiquitin-mediated proteolysis in cell cycle control. Curr. Opin. Cell Biol. 9, 788-799
6. Hirsch, C., Gauss, R., and Sommer, T. (2006) Coping with stress. Cellular relaxation techniques. Trends Cell Biol. 16, 657-663 (Pubitemid 44809888)
7. Chen, Z., Hagler, J., Palombella, V. J., Melandri, F., Scherer, D., Ballard, D., and Maniatis, T. (1995) Signal-induced site-specific phosphorylation targets I kappa B α to the ubiquitin-proteasome pathway. Genes Dev. 9, 1586-1597
8. Aberle, H., Bauer, A., Stappert, J., Kispert, A., and Kemler, R. (1997) β-Catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 16, 3797-3804
9. Salceda, S., and Caro, J. (1997) Hypoxia-inducible factor 1α (HIF-1α) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J. Biol. Chem. 272, 22642-22647 (Pubitemid 27386079)
10. DiAntonio, A., Haghighi, A. P., Portman, S. L., Lee, J. D., Amaranto, A. M., and Goodman, C. S. (2001) Ubiquitination-dependent mechanisms regulate synaptic growth and function. Nature 412, 449-452 (Pubitemid 32702710)
11. Oppenheim, R. W. (1991) Cell death during development of the nervous system. Annu. Rev. Neurosci. 14, 453-501
12. Gould, E., Woolley, C. S., and McEwen, B. S. (1991) Naturally occurring cell death in the developing dentate gyrus of the rat. J. Comp. Neurol. 304, 408-418
13. Ferrer, I., Tortosa, A., Blanco, R., Martín, F., Serrano, T., Planas, A., and Macaya, A. (1994) Naturally occurring cell death in the developing cerebral cortex of the rat. Evidence of apoptosis-associated internucleosomal DNA fragmentation. Neurosci. Lett. 182, 77-79 (Pubitemid 24362026)
14. Murase, S., Owens, D. F., and McKay, R. D. (2011) In the newborn hippocampus, neurotrophin-dependent survival requires spontaneous activity and integrin signaling. J. Neurosci. 31, 7791-7800
15. Murase, S., Kim, E., Lin, L., Hoffman, D. A., and McKay, R. D. (2012) Loss of signal transducer and activator of transcription 3 (STAT3) signaling during elevated activity causes vulnerability in hippocampal neurons. J. Neurosci. 32, 15511-15520
16. Levy, D. E., and Darnell, J. E., Jr. (2002) Stats. Transcriptional control and biological impact. Nat. Rev. Mol. Cell Biol. 3, 651-662 (Pubitemid 34987786)
17. Deverman, B. E., and Patterson, P. H. (2009) Cytokines and CNS development. Neuron 64, 61-78
18. Pallen, C. J., and Wang, J. H. (1985) A multifunctional calmodulin-stimulated phosphatase. Arch. Biochem. Biophys. 237, 281-291 (Pubitemid 15144883)
19. Schreiber, S. L. (1992) Immunophilin-sensitive protein phosphatase action in cell signaling pathways. Cell 70, 365-368
20. Klee, C. B., Crouch, T. H., and Krinks, M. H. (1979) Calcineurin. A calcium- and calmodulin-binding protein of the nervous system. Proc. Natl. Acad. Sci. U.S.A. 76, 6270-6273 (Pubitemid 10163382)
21. Ferreira, A., Kincaid, R., and Kosik, K. S. (1993) Calcineurin is associated with the cytoskeleton of cultured neurons and has a role in the acquisition of polarity. Mol. Biol. Cell 4, 1225-1238 (Pubitemid 24045754)
22. Michod, D., Bartesaghi, S., Khelifi, A., Bellodi, C., Berliocchi, L., Nicotera, P., and Salomoni, P. (2012) Calcium-dependent dephosphorylation of the histone chaperone DAXX regulates H3.3 loading and transcription upon neuronal activation. Neuron 74, 122-135
23. Schwartz, N., Schohl, A., and Ruthazer, E. S. (2009) Neural activity regulates synaptic properties and dendritic structure in vivo through calcineurin/NFAT signaling. Neuron 62, 655-669
24. Mansuy, I. M., Mayford, M., Jacob, B., Kandel, E. R., and Bach, M. E. (1998) Restricted and regulated overexpression reveals calcineurin as a key component in the transition from short-term to long-term memory. Cell 92, 39-49 (Pubitemid 28053296)
25. Murase, S., and McKay, R. D. (2006) A specific survival response in dopamine neurons at most risk in Parkinson's disease. J. Neurosci. 26, 9750-9760 (Pubitemid 44427714)
26. Horton, A. C., Rácz, B., Monson, E. E., Lin, A. L., Weinberg, R. J., and Ehlers, M. D. (2005) Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 48, 757-771 (Pubitemid 41759427)
27. Ballas, N., Battaglioli, E., Atouf, F., Andres, M. E., Chenoweth, J., Anderson, M. E., Burger, C., Moniwa, M., Davie, J. R., Bowers, W. J., Federoff, H. J., Rose, D. W., Rosenfeld, M. G., Brehm, P., and Mandel, G. (2001) Regulation of neuronal traits by a novel transcriptional complex. Neuron 31, 353-365 (Pubitemid 32778556)
28. Cunningham, M. G., and McKay, R. D. (1993) A hypothermic miniaturized stereotaxic instrument for surgery in newborn rats. J. Neurosci. Methods 47, 105-114 (Pubitemid 23130541)
29. Darnell, J. E., Jr., Kerr, I. M., and Stark, G. R. (1994) Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264, 1415-1421 (Pubitemid 24217131)
30. Niu, G., Wright, K. L., Ma, Y., Wright, G. M., Huang, M., Irby, R., Briggs, J., Karras, J., Cress, W. D., Pardoll, D., Jove, R., Chen, J., and Yu, H. (2005) Role of Stat3 in regulating p53 expression and function. Mol. Cell Biol. 25, 7432-7440 (Pubitemid 41170107)
31. Deckwerth, T. L., Elliott, J. L., Knudson, C. M., Johnson, E. M., Jr., Snider, W. D., and Korsmeyer, S. J. (1996)BAXis required for neuronal death after trophic factor deprivation and during development. Neuron 17, 401-411 (Pubitemid 26322212)
32. O'Keefe, S. J., Tamura, J., Kincaid, R. L., Tocci, M. J., and O'Neill, E. A. (1992) FK-506- and CsA-sensitive activation of the interleukin-2 promoter by calcineurin. Nature 357, 692-694
33. Daino, H., Matsumura, I., Takada, K., Odajima, J., Tanaka, H., Ueda, S., Shibayama, H., Ikeda, H., Hibi, M., Machii, T., Hirano, T., and Kanakura, Y. (2000) Induction of apoptosis by extracellular ubiquitin in human hematopoietic cells. Possible involvement of STAT3 degradation by proteasome pathway in interleukin 6-dependent hematopoietic cells. Blood 95, 2577-2585 (Pubitemid 30210536)
34. Conaway, J. W., Kamura, T., and Conaway, R. C. (1998) The Elongin BC complex and the von Hippel-Lindau tumor suppressor protein. Biochim. Biophys. Acta 1377, M49-M54 (Pubitemid 28207047)
35. Kaelin, W. G., Jr. (2002) Molecular basis of the VHL hereditary cancer syndrome. Nat. Rev. Cancer 2, 673-682
36. Garcia, J. A., Ou, S. H., Wu, F., Lusis, A. J., Sparkes, R. S., and Gaynor, R. B. (1992) Cloning and chromosomal mapping of a human immunodeficiency virus 1 "TATA" element modulatory factor. Proc. Natl. Acad. Sci. U.S.A. 89, 9372-9376
37. Hsiao, P. W., and Chang, C. (1999) Isolation and characterization of ARA160 as the first androgen receptor N-terminal-associated coactivator in human prostate cells. J. Biol. Chem. 274, 22373-22379
38. Perry, E., Tsruya, R., Levitsky, P., Pomp, O., Taller, M., Weisberg, S., Parris, W., Kulkarni, S., Malovani, H., Pawson, T., Shpungin, S., and Nir, U. (2004) TMF/ARA160 is a BC-box-containing protein that mediates the degradation of Stat3. Oncogene 23, 8908-8919 (Pubitemid 39657781)
39. Schwartz, Y., Ben-Dor, I., Navon, A., Motro, B., and Nir, U. (1998) Tyrosine phosphorylation of the TATA element modulatory factor by the FER nuclear tyrosine kinases. FEBS Lett. 434, 339-345 (Pubitemid 29052253)
40. Maxwell, P. H., Wiesener, M. S., Chang, G. W., Clifford, S. C., Vaux, E. C., Cockman, M. E., Wykoff, C. C., Pugh, C. W., Maher, E. R., and Ratcliffe, P. J. (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399, 271-275 (Pubitemid 29246458)
41. Mori, K., and Kato, H. (2002) A putative nuclear receptor coactivator (TMF/ARA160) associates with hbrm/hSNF2 α and BRG-1/hSNF2 β and localizes in the Golgi apparatus. FEBS Lett. 520, 127-132 (Pubitemid 34607287)
42. 2+- and calmodulin-dependent protein phosphatase. Probable identity with calcineurin (CaM-BP80). FEBS Lett. 137, 80-84
43. Liang, H., Venema, V. J., Wang, X., Ju, H., Venema, R. C., and Marrero, M. B. (1999) Regulation of angiotensin II-induced phosphorylation of STAT3 in vascular smooth muscle cells. J. Biol. Chem. 274, 19846-19851
44. Mulkey, R. M., Herron, C. E., and Malenka, R. C. (1993) An essential role for protein phosphatases in hippocampal long-term depression. Science 261, 1051-1055 (Pubitemid 23300866)
45. Mulkey, R. M., Endo, S., Shenolikar, S., and Malenka, R. C. (1994) Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369, 486-488
46. Blitzer, R. D., Wong, T., Nouranifar, R., Iyengar, R., and Landau, E. M. (1995) Postsynaptic cAMP pathway gates early LTP in hippocampal CA1 region. Neuron 15, 1403-1414 (Pubitemid 26005377)
47. Benedito, A. B., Lehtinen, M., Massol, R., Lopes, U. G., Kirchhausen, T., Rao, A., and Bonni, A. (2005) The transcription factor NFAT3 mediates neuronal survival. J. Biol. Chem. 280, 2818-2825 (Pubitemid 40189389)
48. Luoma, J. I., and Zirpel, L. (2008) Deafferentation-induced activation of NFAT (nuclear factor of activated T-cells) in cochlear nucleus neurons during a developmental critical period. A role for NFATc4-dependent apoptosis in the CNS. J. Neurosci. 28, 3159-3169 (Pubitemid 351442276)
49. Marshall, J., Dolan, B. M., Garcia, E. P., Sathe, S., Tang, X., Mao, Z., and Blair, L. A. (2003) Calcium channel and NMDA receptor activities differentially regulate nuclear C/EBPβ levels to control neuronal survival. Neuron 39, 625-639 (Pubitemid 36993580)
50. Shi, J., Townsend, M., and Constantine-Paton, M. (2000) Activity-dependent induction of tonic calcineurin activity mediates a rapid developmental downregulation of NMDA receptor currents. Neuron 28, 103-114
51. Jurado, S., Biou, V., and Malenka, R. C. (2010) A calcineurin/AKAP complex is required for NMDA receptor-dependent long-term depression. Nat. Neurosci. 13, 1053-1055
52. 2+-calcineurin-NFAT signaling. Nat. Struct. Mol. Biol. 19, 337-345
53. Davies, K. J., Ermak, G., Rothermel, B. A., Pritchard, M., Heitman, J., Ahnn, J., Henrique-Silva, F., Crawford, D., Canaider, S., Strippoli, P., Carinci, P., Min, K. T., Fox, D. S., Cunningham, K. W., Bassel-Duby, R., Olson, E. N., Zhang, Z., Williams, R. S., Gerber, H. P., Pérez-Riba, M., Seo, H., Cao, X., Klee, C. B., Redondo, J. M., Maltais, L. J., Bruford, E. A., Povey, S., Molkentin, J. D., McKeon, F. D., Duh, E. J., Crabtree, G. R., Cyert, M. S., de la Luna, S., and Estivill, X. (2007) Renaming the DSCR1/Adapt78 gene family as RCAN. Regulators of calcineurin. FASEB J. 21, 3023-3028 (Pubitemid 47565558)
54. Porta, S., Martí, E., de la Luna, S., and Arbonés, M. L. (2007) Differential expression of members of the RCAN family of calcineurin regulators suggests selective functions for these proteins in the brain. Eur. J. Neurosci. 26, 1213-1226 (Pubitemid 47351203)
55. Zeng, H., Chattarji, S., Barbarosie, M., Rondi-Reig, L., Philpot, B. D., Miyakawa, T., Bear, M. F., and Tonegawa, S. (2001) Forebrain-specific calcineurin knockout selectively impairs bidirectional synaptic plasticity and working/episodic-like memory. Cell 107, 617-629 (Pubitemid 34014863)
56. 2+ dysregulation with brain aging. J Neurosci. 21, 4066-4073
57. De-Fraja, C., Conti, L., Govoni, S., Battaini, F., and Cattaneo, E. (2000) STAT signalling in the mature and aging brain. Int. J. Dev. Neurosci. 18, 439-446 (Pubitemid 30243074)