RNAi screen in mouse astrocytes identifies phosphatases that regulate NF-κB signaling

Molecular Cell

Volumn 24, Issue 4, 2006, Pages 497-509

  Li, Shitao ^a   Wang, Lingyan ^a   Berman, Michael A ^a   Zhang, Ye ^a,b   Dorf, Martin E ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b PEKING UNION MEDICAL COLLEGE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE; HOLOENZYME; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 2A; RNA; THREONINE; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN PHOSPHATASE 2A REGULATORY SUBUNIT 65 KDA; TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; ARTICLE; ASTROCYTE; GENE IDENTIFICATION; IMMUNOPRECIPITATION; MODULATION; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; RNA INTERFERENCE; SCREENING; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CELL STRAIN 3T3; CLASSIFICATION; GENE LIBRARY; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ASTROCYTES; CELLS, CULTURED; GENE LIBRARY; I-KAPPA B KINASE; MICE; MICE, INBRED BALB C; NF-KAPPA B; NIH 3T3 CELLS; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED FACTOR 2; TRANSCRIPTION FACTOR RELA;

EID: 37349111560     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2006.10.015     Document Type: Article

References (46)

1. Bouwmeester, T., Bauch, A., Ruffner, H., Angrand, P.O., Bergamini, G., Croughton, K., Cruciat, C., Eberhard, D., Gagneur, J., Ghidelli, S., et al. (2004). A physical and functional map of the human TNF-alpha/NF-kappa B signal transduction pathway. Nat. Cell Biol. 6, 97-105.
2. Bureau, F., Vanderplasschen, A., Jaspar, F., Minner, F., Pastoret, P.P., Merville, M.P., Bours, V., and Lekeux, P. (2002). Constitutive nuclear factor-kappaB activity preserves homeostasis of quiescent mature lymphocytes and granulocytes by controlling the expression of distinct Bcl-2 family proteins. Blood 99, 3683-3691.
3. Bush, T.G., Puvanachandra, N., Horner, C.H., Polito, A., Ostenfeld, T., Svendsen, C.N., Mucke, L., Johnson, M.H., and Sofroniew, M.V. (1999). Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron 23, 297-308.
4. Chaudhuri, A., Orme, S., Vo, T., Wang, W., and Cherayil, B.J. (1999). Phosphorylation of TRAF2 inhibits binding to the CD40 cytoplasmic domain. Biochem. Biophys. Res. Commun. 256, 620-625.
5. DasGupta, R., Kaykas, A., Moon, R.T., and Perrimon, N. (2005). Functional genomic analysis of the Wnt-wingless signaling pathway. Science 308, 826-833.
6. Delhase, M., Hayakawa, M., Chen, Y., and Karin, M. (1999). Positive and negative regulation of IkappaB kinase activity through IKKbeta subunit phosphorylation. Science 284, 309-313.
7. DiDonato, J.A., Hayakawa, M., Rothwarf, D.M., Zandi, E., and Karin, M. (1997). A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB. Nature 388, 548-554.
8. Franke, T.F., Kaplan, D.R., Cantley, L.C., and Toker, A. (1997). Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4- bisphosphate. Science 275, 665-668.
9. Fu, D.X., Kuo, Y.L., Liu, B.Y., Jeang, K.T., and Giam, C.Z. (2003). Human T-lymphotropic virus type I tax activates I-kappa B kinase by inhibiting I-kappa B kinase-associated serine/threonine protein phosphatase 2A. J. Biol. Chem. 278, 1487-1493.
10. Garcia-Segura, L.M., Naftolin, F., Hutchison, J.B., Azcoitia, I., and Chowen, J.A. (1999). Role of astroglia in estrogen regulation of synaptic plasticity and brain repair. J. Neurobiol. 40, 574-584.
11. Gotz, J., Probst, A., Ehler, E., Hemmings, B., and Kues, W. (1998). Delayed embryonic lethality in mice lacking protein phosphatase 2A catalytic subunit Calpha. Proc. Natl. Acad. Sci. USA 95, 12370-12375.
12. Hasegawa, S., Morioka, M., Goto, S., Korematsu, K., Okamura, A., Yano, S., Kai, Y., Hamada, J.I., and Ushio, Y. (2000). Expression of neuron specific phosphatase, striatal enriched phosphatase (STEP) in reactive astrocytes after transient forebrain ischemia. Glia 29, 316-329.
13. Hayden, M.S., and Ghosh, S. (2004). Signaling to NF-kappaB. Genes Dev. 18, 2195-2224.
14. Hu, M.C., Tang-Oxley, Q., Qiu, W.R., Wang, Y.P., Mihindukulasuriya, K.A., Afshar, R., and Tan, T.H. (1998). Protein phosphatase X interacts with c-Rel and stimulates c-Rel/nuclear factor kappaB activity. J. Biol. Chem. 273, 33561-33565.
15. Ibarra-Sanchez, M.J., Wagner, J., Ong, M.T., Lampron, C., and Tremblay, M.L. (2001). Murine embryonic fibroblasts lacking TC-PTP display delayed G1 phase through defective NF-kappaB activation. Oncogene 20, 4728-4739.
16. Kang, J., Jiang, L., Goldman, S.A., and Nedergaard, M. (1998). Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat. Neurosci. 1, 683-692.
17. Kaykas, A., and Moon, R.T. (2004). A plasmid-based system for expressing small interfering RNA libraries in mammalian cells. BMC Cell Biol. 5, 16.
18. Kim, J.M., Oh, Y.K., Lee, J.H., Im, D.Y., Kim, Y.J., Youn, J., Lee, C.H., Son, H., Lee, Y.S., Park, J.Y., and Choi, I.H. (2005). Induction of proinflammatory mediators requires activation of the TRAF, NIK, IKK and NF-kappaB signal transduction pathway in astrocytes infected with Escherichia coli. Clin. Exp. Immunol. 140, 450-460.
19. Li, Q.Q., Bever, C.T., Burt, D.R., Judge, S.I., and Trisler, G.D. (2001). Induction of RANTES chemokine expression in human astrocytic cells is dependent upon activation of NF-kappaB transcription factor. Int. J. Mol. Med. 7, 527-533.
20. Li, M.G., Katsura, K., Nomiyama, H., Komaki, K., Ninomiya-Tsuji, J., Matsumoto, K., Kobayashi, T., and Tamura, S. (2003). Regulation of the interleukin-1-induced signaling pathways by a novel member of the protein phosphatase 2C family (PP2Cepsilon). J. Biol. Chem. 278, 12013-12021.
21. Luo, Y., Berman, M.A., Zhai, Q., Fischer, F.R., Abromson-Leeman, S.R., Zhang, Y., Kuziel, W.A., Gerard, C., and Dorf, M.E. (2002). RANTES stimulates inflammatory cascades and receptor modulation in murine astrocytes. Glia 39, 19-30.
22. MacEwan, D.J. (2002). TNF receptor subtype signalling: differences and cellular consequences. Cell. Signal. 14, 477-492.
23. MacKeigan, J.P., Murphy, L.O., and Blenis, J. (2005). Sensitized RNAi screen of human kinases and phosphatases identifies new regulators of apoptosis and chemoresistance. Nat. Cell Biol. 7, 591-600.
24. Mauch, D.H., Nagler, K., Schumacher, S., Goritz, C., Muller, E.C., Otto, A., and Pfrieger, F.W. (2001). CNS synaptogenesis promoted by glia-derived cholesterol. Science 294, 1354-1357.
25. Mayo, M.W., Madrid, L.V., Westerheide, S.D., Jones, D.R., Yuan, X.J., Baldwin, A.S., Jr., and Whang, Y.E. (2002). PTEN blocks tumor necrosis factor-induced NF-kappa B-dependent transcription by inhibiting the transactivation potential of the p65 subunit. J. Biol. Chem. 277, 11116-11125.
26. 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 IkappaB kinases essential for NF-kappaB activation. Science 278, 860-866.
27. Miller, G. (2005). Neuroscience. The dark side of glia. Science 308, 778-781.
28. Moreno, C.S., Ramachandran, S., Ashby, D.G., Laycock, N., Plattner, C.A., Chen, W., Hahn, W.C., and Pallas, D.C. (2004). Signaling and transcriptional changes critical for transformation of human cells by simian virus 40 small tumor antigen or protein phosphatase 2A B56gamma knockdown. Cancer Res. 64, 6978-6988.
29. Pomerantz, J.L., and Baltimore, D. (1999). NF-kappaB activation by a signaling complex containing TRAF2, TANK and TBK1, a novel IKK-related kinase. EMBO J. 18, 6694-6704.
30. Prajapati, S., Verma, U., Yamamoto, Y., Kwak, Y.T., and Gaynor, R.B. (2004). Protein phosphatase 2Cbeta association with the IkappaB kinase complex is involved in regulating NF-kappaB activity. J. Biol. Chem. 279, 1739-1746.
31. Prat, A., Biernacki, K., Wosik, K., and Antel, J.P. (2001). Glial cell influence on the human blood-brain barrier. Glia 36, 145-155.
32. Romashkova, J.A., and Makarov, S.S. (1999). NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling. Nature 401, 86-90.
33. Sakurai, H., Suzuki, S., Kawasaki, N., Nakano, H., Okazaki, T., Chino, A., Doi, T., and Saiki, I. (2003). Tumor necrosis factor-alpha-induced IKK phosphorylation of NF-kappaB p65 on serine 536 is mediated through the TRAF2, TRAF5, and TAK1 signaling pathway. J. Biol. Chem. 278, 36916-36923.
34. Schwaninger, M., Petersen, N., Prinz, S., Sallmann, S., Neher, M., and Spranger, M. (2000). Adenosine-induced expression of interleukin-6 in astrocytes through protein kinase A and NF-IL-6. Glia 31, 51-58.
35. Song, H., Stevens, C.F., and Gage, F.H. (2002). Astroglia induce neurogenesis from adult neural stem cells. Nature 417, 39-44.
36. Sun, S.C., Maggirwar, S.B., and Harhaj, E. (1995). Activation of NF-kappa B by phosphatase inhibitors involves the phosphorylation of I kappa B alpha at phosphatase 2A-sensitive sites. J. Biol. Chem. 270, 18347-18351.
37. Takaesu, G., Surabhi, R.M., Park, K.J., Ninomiya-Tsuji, J., Matsumoto, K., and Gaynor, R.B. (2003). TAK1 is critical for IkappaB kinase-mediated activation of the NF-kappaB pathway. J. Mol. Biol. 326, 105-115.
38. Takeuchi, M., Rothe, M., and Goeddel, D.V. (1996). Anatomy of TRAF2. Distinct domains for nuclear factor-kappaB activation and association with tumor necrosis factor signaling proteins. J. Biol. Chem. 271, 19935-19942.
39. Van Wagoner, N.J., and Benveniste, E.N. (1999). Interleukin-6 expression and regulation in astrocytes. J. Neuroimmunol. 100, 124-139.
40. Vermeulen, L., De Wilde, G., Van Damme, P., Vanden Berghe, W., and Haegeman, G. (2003). Transcriptional activation of the NF-kappaB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J. 22, 1313-1324.
41. Viatour, P., Merville, M.P., Bours, V., and Chariot, A. (2005). Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation. Trends Biochem. Sci. 30, 43-52.
42. Volterra, A., and Meldolesi, J. (2005). Astrocytes, from brain glue to communication elements: the revolution continues. Nat. Rev. Neurosci. 6, 626-640.
43. Yang, J., Fan, G.H., Wadzinski, B.E., Sakurai, H., and Richmond, A. (2001). Protein phosphatase 2A interacts with and directly dephosphorylates RelA. J. Biol. Chem. 276, 47828-47833.
44. Zhai, Q., Luo, Y., Zhang, Y., Berman, M.A., and Dorf, M.E. (2004). Low nuclear levels of nuclear factor-kappa B are essential for KC self-induction in astrocytes: requirements for shuttling and phosphorylation. Glia 48, 327-336.
45. Zheng, L., Liu, J., Batalov, S., Zhou, D., Orth, A., Ding, S., and Schultz, P.G. (2004). An approach to genomewide screens of expressed small interfering RNAs in mammalian cells. Proc. Natl. Acad. Sci. USA 101, 135-140.
46. Zhong, H., SuYang, H., Erdjument-Bromage, H., Tempst, P., and Ghosh, S. (1997). The transcriptional activity of NF-kappaB is regulated by the IkappaB-associated PKAc subunit through a cyclic AMP-independent mechanism. Cell 89, 413-424.