Functional interaction of protein kinase CK2 and activating transcription factor 4 (ATF4), a key player in the cellular stress response

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 3, 2013, Pages 439-451

  Ampofo, Emmanuel ^a   Sokolowsky, Tasja ^a   Götz, Claudia ^a   Montenarh, Mathias ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

Phosphorylation; Protein kinase; Protein stability; Transcription; Transcription factor

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; CASEIN KINASE II; SERINE;

ARTICLE; CELLULAR STRESS RESPONSE; ENDOPLASMIC RETICULUM STRESS; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; NUCLEUS ACCUMBENS; PRIORITY JOURNAL;

ACTIVATING TRANSCRIPTION FACTOR 4; BLOTTING, WESTERN; CASEIN KINASE II; CELL NUCLEUS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; MUTATION; PHOSPHORYLATION; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTION, GENETIC;

EID: 84871856283     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.10.025     Document Type: Article

References (69)

1. Pinna L.A. Casein kinase 2: an 'eminence grise' in cellular regulation. Biochim. Biophys. Acta Mol. Cell Res. 1990, 1054:267-284.
2. Guerra B., Issinger O.G. Protein kinase CK2 and its role in cellular proliferation, development and pathology. Electrophoresis 1999, 20:391-408.
3. Niefind K., Guerra B., Ermakowa I., Issinger O.G. Crystal structure of human protein kinase CK2: insights into basic properties of the CK2 holoenzyme. EMBO J. 2001, 20:5320-5331.
4. Guerra B., Siemer S., Boldyreff B., Issinger O.G. Protein kinase CK2: evidence for a protein kinase CK2b subunit fraction, devoid of the catalytic CK2a subunit, in mouse brain and testicles. FEBS Lett. 1999, 462:353-357.
5. Lüscher B., Litchfield D.W. Biosynthesis of casein kinase II in lymphoid cell lines. Eur. J. Biochem. 1994, 220:521-526.
6. Mannowetz N., Kartarius S., Wennemuth G., Montenarh M. Protein kinase CK2 and binding partners during spermatogenesis. Cell. Mol. Life Sci. 2010, 67:3905-3913.
7. Lehnert S., Götz C., Montenarh M. Protein kinase CK2 interacts with the splicing factor hPrp3p. Oncogene 2008, 27:2390-2400.
8. Meng R., Al-Quobaili F., Müller I., Götz C., Thiel G., Montenarh M. CK2 phosphorylation of Pdx-1 regulates its transcription factor activity. Cell. Mol. Life Sci. 2010, 67:2481-2489.
9. Meng R., Götz C., Montenarh M. The role of protein kinase CK2 in the regulation of the insulin production of pancreatic islets. Biochem. Biophys. Res. Commun. 2010, 401:203-206.
10. Schäfer B., Götz C., Dudek J., Hessenauer A., Matti U., Montenarh M. KIF5C, a new binding partner for protein kinase CK2 with a preference for CK2a'. Cell. Mol. Life Sci. 2009, 66:339-349.
11. Schäfer B., Götz C., Montenarh M. The kinesin I family member KIF5C is a novel substrate for protein kinase CK2. Biochem. Biophys. Res. Commun. 2008, 375:179-183.
12. Olsen B.B., Guerra B. Ability of CK2beta to selectively regulate cellular protein kinases. Mol. Cell. Biochem. 2008, 316:115-126.
13. Karpinski B.A., Morle G.D., Huggenvik J., Uhler M.D., Leiden J.M. Molecular cloning of human CREB-2: an ATF/CREB transcription factor that can negatively regulate transcription from the cAMP response element. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:4820-4824.
14. Harding H.P., Zhang Y., Zeng H., Novoa I., Lu P.D., Calfon M., Sadri N., Yun C., Popko B., Paules R., Stojdl D.F., Bell J.C., Hettmann T., Leiden J.M., Ron D. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 2003, 11:619-633.
15. Harding H.P., Novoa I., Zhang Y., Zeng H., Wek R., Schapira M., Ron D. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 2000, 6:1099-1108.
16. Hettmann T., Barton K., Leiden T.M. Microphthalmia due to p53-mediated apoptosis of anterior lens epithelial cells in mice lacking the CREB-2 transcription factor. Dev. Biol. 2000, 222:110-123.
17. Chen A., Muzzio I.A., Malleret G., Bartsch D., Verbitsky M., Pavlidis P., Yonan A.L., Vronskaya S., Grody M.B., Cepeda I., Gilliam T.C., Kandel E.R. Inducible enhancement of memory storage and synaptic plasticity in transgenic mice expressing an inhibitor of ATF4 (CREB-2) and C/EBP proteins. Neuron 2003, 39:655-669.
18. Siu F., Bain P.J., LeBlanc-Chaffin R., Chen H., Kilberg M.S. ATF4 is a mediator of the nutrient-sensing response pathway that activates the human asparagine synthetase gene. J. Biol. Chem. 2002, 277:24120-24127.
19. Vattem K.M., Wek R.C. Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:11269-11274.
20. Lange P.S., Chavez J.C., Pinto J.T., Coppola G., Sun C.W., Townes T.M., Geschwind D.H., Ratan R.R. ATF4 is an oxidative stress-inducible, prodeath transcription factor in neurons in vitro and in vivo. J. Exp. Med. 2008, 205:1227-1242.
21. Apopa P.L., He X., Ma Q. Phosphorylation of Nrf2 in the transcription activation domain by casein kinase 2 (CK2) is critical for the nuclear translocation and transcription activation function of Nrf2 in IMR-32 neuroblastoma cells. J. Biochem. Mol. Toxicol. 2008, 22:63-76.
22. Ubeda M., Habener J.F. CHOP transcription factor phosphorylation by casein kinase 2 inhibits transcriptional activation. J. Biol. Chem. 2003, 278:40514-40520.
23. Lassot I., Segeral E., Berlioz-Torrent C., Durand H., Groussin L., Hai T., Benarous R., Margottin-Goguet F. ATF4 degradation relies on a phosphorylation-dependent interaction with the SCF(betaTrCP) ubiquitin ligase. Mol. Cell. Biol. 2001, 21:2192-2202.
24. Frank C.L., Ge X., Xie Z., Zhou Y., Tsai L.H. Control of activating transcription factor 4 (ATF4) persistence by multisite phosphorylation impacts cell cycle progression and neurogenesis. J. Biol. Chem. 2010, 285:33324-33337.
25. Sarno S., Reddy H., Meggio F., Ruzzene M., Davies S.P., Donella-Deana A., Shugar D., Pinna L.A. Selectivity of 4,5,6,7-tetrabromobenzotriazole, an ATP site-directed inhibitor of protein kinase CK2 ('casein kinase-2'). FEBS Lett. 2001, 496:44-48.
26. Cozza G., Mazzorana M., Papinutto E., Bain J., Elliott M., Di M.G., Gianoncelli A., Pagano M.A., Sarno S., Ruzzene M., Battistutta R., Meggio F., Moro S., Zagotto G., Pinna L.A. Quinalizarin as a potent, selective and cell-permeable inhibitor of protein kinase CK2. Biochem. J. 2009, 421:387-395.
27. Bruhat A., Jousse C., Carraro V., Reimold A.M., Ferrara M., Fafournoux P. Amino acids control mammalian gene transcription: activating transcription factor 2 is essential for the amino acid responsiveness of the CHOP promoter. Mol. Cell. Biol. 2000, 20:7192-7204.
28. Thiel G., Al S.J., Vinson C., Stefano L., Bach K. Role of basic region leucine zipper transcription factors cyclic AMP response element binding protein (CREB), CREB2, activating transcription factor 2 and CAAT/enhancer binding protein alpha in cyclic AMP response element-mediated transcription. J. Neurochem. 2005, 92:321-336.
29. Mayer S.I., Dexheimer V., Nishida E., Kitajima S., Thiel G. Expression of the transcriptional repressor ATF3 in gonadotrophs is regulated by Egr-1, CREB, and ATF2 after gonadotropin-releasing hormone receptor stimulation. Endocrinology 2008, 149:6311-6325.
30. Laudet B., Moucadel V., Prudent R., Filhol O., Wong Y.S., Royer D., Cochet C. Identification of chemical inhibitors of protein-kinase CK2 subunit interaction. Mol. Cell. Biochem. 2008, 316:63-69.
31. Schneider C.C., Götz C., Hessenauer A., Günther J., Kartarius S., Montenarh M. Down-regulation of CK2 activity results in a decrease in the level of cdc25C phosphatase in different prostate cancer cell lines. Mol. Cell. Biochem. 2011, 356:177-184.
32. Faust M., Schuster N., Montenarh M. Specific binding of protein kinase CK2 catalytic subunits to tubulin. FEBS Lett. 1999, 462:51-56.
33. 111/112) enhances recognition of the simian virus 40 large T-antigen nuclear localization sequence by importin. J. Biol. Chem. 1997, 272:17191-17195.
34. Allende-Vega N., McKenzie L., Meek D. Transcription factor TAFII250 phosphorylates the acidic domain of Mdm2 through recruitment of protein kinase CK2. Mol. Cell. Biochem. 2008, 316:99-106.
35. Yamaguchi Y., Wada T., Suzuki F., Takagi T., Hasegawa J., Handa H. Casein kinase II interacts with the bZIP domains of several transcription factors. Nucleic Acids Res. 1998, 26:3854-3861.
36. Johnston I.M., Allison S.J., Morton J.P., Schramm L., Scott P.H., White R.J. CK2 forms a stable complex with TFIIIB and activates RNA polymerase III transcription in human cells. Mol. Cell. Biol. 2002, 22:3757-3768.
37. Michelangeli F., East J.M. A diversity of SERCA Ca2+ pump inhibitors. Biochem. Soc. Trans. 2011, 39:789-797.
38. Jiang H.Y., Wek R.C. Phosphorylation of the alpha-subunit of the eukaryotic initiation factor-2 (eIF2alpha) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition. J. Biol. Chem. 2005, 280:14189-14202.
39. Kuenzel E.A., Mulligan J.A., Sommercorn J., Krebs E.G. Substrate specificity determinants for casein kinase II as deduced from studies with synthetic peptides. J. Biol. Chem. 1987, 262:9136-9140.
40. Pinna L.A. Protein kinase CK2: a challenge to canons. J. Cell Sci. 2002, 115:3873-3878.
41. Manni S., Brancalion A., Quotti T.L., Colpo A., Pavan L., Cabrelle A., Ave E., Zaffino F., Di M.G., Ruzzene M., Adami F., Zambello R., Pitari M.R., Tassone P., Pinna L.A., Gurrieri C., Semenzato G., Piazza F. Protein kinase CK2 protects multiple myeloma cells from ER stress-induced apoptosis and from the cytotoxic effect of HSP90 inhibition through regulation of the unfolded protein response. Clin. Cancer Res. 2012, 18:1888-1900.
42. Hessenauer A., Schneider C.C., Götz C., Montenarh M. CK2 inhibition induces apoptosis via the ER stress response. Cell. Signal. 2011, 23:145-151.
43. Schneider C.C., Ampofo E., Montenarh M. CK2 regulates ATF4 and CHOP transcription within the cellular stress response signalling pathway. Cell. Signal. 2012, 24:1797-1802.
44. Ameri K., Harris A.L. Activating transcription factor 4. Int. J. Biochem. Cell Biol. 2008, 40:14-21.
45. St-Denis N.A., Litchfield D.W. From birth to death: the role of protein kinase CK2 in the regulation of cell proliferation and survival. Cell. Mol. Life Sci. 2009, 66:1817-1829.
46. Burnett G., Kennedy E.P. The enzymatic phosphorylation of proteins. J. Biol. Chem. 1954, 211:969-980.
47. Yue J., Shukla R., Accardi R., Zanella-Cleon I., Siouda M., Cros M.P., Krutovskikh V., Hussain I., Niu Y., Hu S., Becchi M., Jurdic P., Tommasino M., Sylla B.S. Cutaneous human papillomavirus type 38 E7 regulates actin cytoskeleton structure for increasing cell proliferation through CK2 and the eukaryotic elongation factor 1A. J. Virol. 2011, 85:8477-8494.
48. Montenarh M. Cellular regulators of protein kinase CK2. Cell Tissue Res. 2010, 342:139-146.
49. Lee J.H., Kim J.-M., Kim M.-S., Lee Y.-T., Marshak D.R., Bae Y.-S. The highly basic ribosomal protein L41 interacts with the b subunit of protein kinase CKII and stimulates phosphorylation of DNA topoisomerase IIa by CKII. Biochem. Biophys. Res. Commun. 1997, 238:462-467.
50. Kim J.M., Cha J.Y., Marshak D.R., Bae Y.S. Interaction of the b subunit of casein kinase II with the ribosomal protein L5. Biochem. Biophys. Res. Commun. 1996, 226:180-186.
51. Boldyreff B., Issinger O.G. A-Raf kinase is a new interacting partner of protein kinase CK2 b subunit. FEBS Lett. 1997, 403:197-199.
52. Chen M.Z., Li D.X., Krebs E.G., Cooper J.A. The casein kinase II b subunit binds to Mos and inhibits Mos activity. Mol. Cell. Biol. 1997, 17:1904-1912.
53. Kusk M., Ahmed R., Thomsen B., Bendixen C., Issinger O.G., Boldyreff B. Interactions of protein kinase CK2b subunit within the holoenzyme and with other proteins. Mol. Cell. Biochem. 1999, 191:51-58.
54. Llorens F., Roher N., Miró F.A., Sarno S., Ruiz F.X., Meggio F., Plana M., Pinna L.A., Itarte E. Eukaryotic translation-initiation factor elFb binds to protein kinase CK2: effects on CK2a activity. Biochem. J. 2003, 375:623-631.
55. Bosc D.G., Graham K.C., Saulnier R.B., Zhang C.J., Prober D., Gietz R.D., Litchfield D.W. Identification and characterization of CKIP-1, a novel pleckstrin homology domain-containing protein that interacts with protein kinase CK2. J. Biol. Chem. 2000, 275:14295-14306.
56. Zhang K., Kaufman R.J. Signaling the unfolded protein response from the endoplasmic reticulum. J. Biol. Chem. 2004, 279:25935-25938.
57. Tanaka T., Tsujimura T., Takeda K., Sugihara A., Maekawa A., Terada N., Yoshida N., Akira S. Targeted disruption of ATF4 discloses its essential role in the formation of eye lens fibres. Genes Cells 1998, 3:801-810.
58. Masuoka H.C., Townes T.M. Targeted disruption of the activating transcription factor 4 gene results in severe fetal anemia in mice. Blood 2002, 99:736-745.
59. Desagher S., Osen-Sand A., Montessuit S., Magnenat E., Vilbois F., Hochmann A., Journot L., Antonsson B., Martinou J.C. Phosphorylation of Bid by casein kinases I and II regulates its cleavage by caspase 8. Mol. Cell 2001, 8:601-611.
60. Krippner-Heidenreich A., Talanian R.V., Sekul R., Kraft R., Thole H., Ottleben H., Luscher B. Targeting of the transcription factor Max during apoptosis: phosphorylation-regulated cleavage by caspase-5 at an unusual glutamic acid residue in position P1. Biochem. J. 2001, 358:705-715.
61. Channavajhala P., Seldin D.C. Functional interaction of protein kinase CK2 and c-Myc in lymphomagenesis. Oncogene 2002, 21:5280-5288.
62. Vazquez F., Grossman S.R., Takahashi Y., Rokas M.V., Nakamura N., Sellers W.R. Phosphorylation of the PTEN tail acts as an inhibitory switch by preventing its recruitment into a protein complex. J. Biol. Chem. 2001, 276:48627-48630.
63. Scaglioni P.P., Yung T.M., Cai L.F., Erdjument-Bromage H., Kaufman A.J., Singh B., Teruya-Feldstein J., Tempst P., Pandolfi P.P. A CK2-dependent mechanism for degradation of the PML tumor suppressor. Cell 2006, 126:269-283.
64. Ampofo E., Kietzmann T., Zimmer A., Jakupovic M., Montenarh M., Götz C. Phosphorylation of the von Hippel-Lindau protein (VHL) by protein kinase CK2 reduces its protein stability and affects p53 and HIF-1a mediated transcription. Int. J. Biochem. Cell Biol. 2010, 42:1729-1735.
65. Yu V.W., Gauthier C., St-Arnaud R. Inhibition of ATF4 transcriptional activity by FIAT/gamma-taxilin modulates bone mass accrual. Ann. N. Y. Acad. Sci. 2006, 1068:131-142.
66. Yang X., Karsenty G. ATF4, the osteoblast accumulation of which is determined post-translationally, can induce osteoblast-specific gene expression in non-osteoblastic cells. J. Biol. Chem. 2004, 279:47109-47114.
67. Ma Y., Hendershot L.M. Delineation of a negative feedback regulatory loop that controls protein translation during endoplasmic reticulum stress. J. Biol. Chem. 2003, 278:34864-34873.
68. Lee C.Q., Yun Y.D., Hoeffler J.P., Habener J.F. Cyclic-AMP-responsive transcriptional activation of CREB-327 involves interdependent phosphorylated subdomains. EMBO J. 1990, 9:4455-4465.
69. Jiang H.Y., Wek S.A., McGrath B.C., Lu D., Hai T., Harding H.P., Wang X., Ron D., Cavener D.R., Wek R.C. Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response. Mol. Cell. Biol. 2004, 24:1365-1377.