Phosphorylation of RNA helicase a by DNA-dependent protein kinase is indispensable for expression of the MDR1 gene product P-glycoprotein in multidrag-resistant human leukemia cells

Biochemistry

Volumn 46, Issue 19, 2007, Pages 5766-5775

  Zhong, Xiaoling ^a   Safa, Ahmad R ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DRUG TRANSPORT; LEUKEMIA CELLS; MULTIDRUG RESISTANCE (MDR);

CATALYSIS; CELLS; DNA; GENE EXPRESSION; PHOSPHORYLATION; RNA;

ENZYME KINETICS;

DNA DEPENDENT PROTEIN KINASE; GENE PRODUCT; GLYCOPROTEIN P; MULTIDRUG RESISTANCE PROTEIN 1; MULTIPROTEIN COMPLEX; RNA HELICASE; RNA HELICASE A; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVE SITE; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; KNOCKOUT GENE; LEUKEMIA CELL; MIGRATION INHIBITION; MULTIDRUG RESISTANCE; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN INDUCTION;

ANIMALS; DEAD-BOX RNA HELICASES; DNA-ACTIVATED PROTEIN KINASE; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; ESCHERICHIA COLI; GENES, MDR; HL-60 CELLS; HUMANS; NEOPLASM PROTEINS; P-GLYCOPROTEIN; PHOSPHOPROTEINS; PHOSPHORYLATION; PROMOTER REGIONS (GENETICS); RECOMBINANT PROTEINS; SPODOPTERA;

EID: 34248584499     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700063b     Document Type: Article

References (49)

1. Ambudkar, S. V., Kimchi-Sarfaty, C., Sauna, Z. E., and Gottesman, M. M. (2003) P-glycoprotein: from genomics to mechanism, Oncogene 22, 7468-7485.
2. Safa, A. R. (1998) Photoaffinity labels for characterizing drug interaction sites of P-glycoprotein, Methods Enzymol. 292, 289-307.
3. Fairchild, C. R., Moscow, J. A., O'Brien, E. E., and Cowan, K. H. (1990) Multidrug resistance in cells transfected with human genes encoding a variant P-glycoprotein and glutathione S-transferase-pi, Mol. Pharmacol. 37, 801-809.
4. Guild, B. C., Mulligan, R. C., Gros, P., and Housman, D. E. (1988) Retroviral transfer of a murine cDNA for multidrug resistance confers pleiotropic drug resistance to cells without prior drug selection, Proc. Natl. Acad. Sci. U.S.A. 85, 1595-1599.
5. Scotto, K. W. (2003) Transcriptional regulation of ABC drug transporters, Oncogene 22, 7496-7511.
6. Leonard, G. D., Fojo, T., and Bates, S. E. (2003) The role of ABC transporters in clinical practice, Oncologist 8, 411-424.
7. Leith, C. P., Kopecky, K. J., Chen, I. M., Eijdems, L., Slovak, M. L., McConnell, T. S., Head, D. R., Weick, J., Grever, M. R., Appelbaum, F. R., and Willman, C. L. (1999) Frequency and clinical significance of the expression of the multidrug resistance proteins MDR1/P-glycoprotein, MRP1, and LRP in acute myeloid leukemia: a Southwest Oncology Group Study, Blood 94, 1086-1099.
8. Ogretmen, B., and Safa, A. R. (2000) Identification and characterization of the MDR1 promoter-enhancing factor 1 (MEF1) in the multidrug resistant HL60/VCR human acute myeloid leukemia cell line, Biochemistry 39, 194-204.
9. Zhong, X., and Safa, A. R. (2004) RNA helicase A in the MEF1 transcription factor complex up-regulates the MDR1 gene in multidrug-resistant cancer cells, J. Biol. Chem. 279, 17134-17141.
10. Nakajima, T., Uchida, C., Anderson, S. F., Lee, C. G., Hurwitz, J., Parvin, J. D., and Montminy, M. (1997) RNA helicase A mediates association of CBP with RNA polymerase II, Cell 90, 1107-1112.
11. Anderson, S. F., Schlegel, B. P., Nakajima, T., Wolpin, E. S., and Parvin, J. D. (1998) BRCA1 protein is linked to the RNA polymerase II holoenzyme complex via RNA helicase A, Nat. Genet. 19, 254-256.
12. Aratani, S., Fujii, R., Oishi, T., Fujita, H., Amano, T., Ohshima, T., Hagiwara, M., Fukamizu, A., and Nakajima, T. (2001) Dual roles of RNA helicase A in CREB-dependent transcription, Mol. Cell. Biol. 21, 4460-4469.
13. Fujii, R., Okamoto, M., Aratani, S., Oishi, T., Ohshima, T., Taira, K., Baba, M., Fukamizu, A., and Nakajima, T. (2001) A role of RNA helicase A in cis-acting transactivation response element-mediated transcriptional regulation of human immunodeficiency virus type 1, J. Biol. Chem. 276, 5445-5451.
14. Toretsky, J. A., Erkizan, V., Levenson, A., Abaan, O. D., Parvin, J. D., Cripe, T. P., Rice, A. M., Lee, S. B., and Uren, A. (2006) Oncoprotein EWS-FLI1 activity is enhanced by RNA helicase A, Cancer Res. 66, 5574-5581.
15. Colla, E., Lee, S. D., Sheen, M. R., Woo, S. K., and Kwon, H. M. (2006) TonEBP is inhibited by RNA helicase A via interaction involving the E′F loop, Biochem. J. 393, 411-419.
16. Hartman, T. R., Qian, S., Bolinger, C., Fernandez, S., Schoenberg, D. R., and Boris-Lawrie, K. (2006) RNA helicase A is necessary for translation of selected messenger RNAs, Nat. Struct. Mol. Biol. 13, 509-516.
17. Zhang, S., Schlott, B., Gorlach, M., and Grosse, F. (2004) DNA-dependent protein kinase (DNA-PK) phosphorylates nuclear DNA helicase II/RNA helicase A and hnRNP proteins in an RNA-dependent manner, Nucleic Acids Res. 32, 1-10.
18. Smith, G. C., and Jackson, S. P. (1999) The DNA-dependent protein kinase, Genes Dev. 13, 916-934.
19. Collis, S. J., DeWeese, T. L., Jeggo, P. A., and Parker, A. R. (2005) The life and death of DNA-PK, Oncogene 24, 949-961.
20. Dip, R., and Naegeli, H. (2005) More than just strand breaks: the recognition of structural DNA discontinuities by DNA-dependent protein kinase catalytic subunit, FASEB J. 19, 704-715.
21. Chu, G. (1997) Double strand break repair, J. Biol. Chem. 272, 24097-24100.
22. Gell, D., and Jackson, S. P. (1999) Mapping of protein-protein interactions within the DNA-dependent protein kinase complex, Nucleic Acids Res. 27, 3494-3502.
23. Ma, Y., Pannicke, U., Schwarz, K., and Lieber, M. R. (2002) Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination, Cell 108, 781-794.
24. Hsu, H. L., Yannone, S. M., and Chen, D. J. (2002) Defining interactions between DNA-PK and ligase IV/XRCC4, DNA Repair (Amsterdam) 1, 225-235.
25. Ariumi, Y., Masutani, M., Copeland, T. D., Mimori, T., Sugimura, T., Shimotohno, K., Ueda, K., Hatanaka, M., and Noda, M. (1999) Suppression of the poly(ADP-ribose) polymerase activity by DNA-dependent protein kinase in vitro, Oncogene 18, 4616-4625.
26. Stiff, T., O'Driscoll, M., Rief, N., Iwabuchi, K., Lobrich, M., and Jeggo, P. A. (2004) ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation, Cancer Res. 64, 2390-2396.
27. Park, E. J., Chan, D. W., Park, J. H., Oettinger, M. A., and Kwon, J. (2003) DNA-PK is activated by nucleosomes and phosphorylates H2AX within the nucleosomes in an acetylation-dependent manner, Nucleic Acids Res. 31, 6819-6827.
28. Shieh, S. Y., Ikeda, M., Taya, Y., and Prives, C. (1997) DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2, Cell 91, 325-334.
29. Dignam, J. D., Lebovitz, R. M., and Roeder, R. G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei, Nucleic Acids Res. 11, 1475-1489.
30. Zhang, S., Maacke, H., and Grosse, F. (1995) Molecular cloning of the gene encoding nuclear DNA helicase II. A bovine homologue of human RNA helicase A and Drosophila Mle protein, J. Biol. Chem. 270, 16422-16427.
31. Iakoucheva, L. M., Radivojac, P., Brown, C. J., O'Connor, T. R., Sikes, J. G., Obradovic, Z., and Dunker, A. K. (2004) The importance of intrinsic disorder for protein phosphorylation, Nucleic Acids Res. 32, 1037-1049.
32. Kharrat, A., Macias, M. J., Gibson, T. J., Nilges, M., and Pastore, A. (1995) Structure of the dsRNA binding domain of E. coli RNase III, EMBO J. 14, 3572-3584.
33. Nicholson, A. W. (1999) Function, mechanism and regulation of bacterial ribonucleases, FEMS Microbiol. Rev. 23, 371-390.
34. Kennelly, P. J. (2002) Protein kinases and protein phosphatases in prokaryotes: a genomic perspective, FEMS Microbiol. Lett. 206, 1-8.
35. Douglas, P., Moorhead, G. B., Ye, R., and Lees-Miller, S. P. (2001) Protein phosphatases regulate DNA-dependent protein kinase activity, J. Biol. Chem. 276, 18992-18998.
36. Wechsler, T., Chen, B. P., Harper, R., Morotomi-Yano, K., Huang, B. C., Meek, K., Cleaver, J. E., Chen, D. J., and Wabl, M. (2004) DNA-PKcs function regulated specifically by protein phosphatase 5, Proc. Natl. Acad. Sci. U.S.A. 101, 1247-1252.
37. Durant, S., and Karran, P. (2003) Vanillins - a novel family of DNA-PK inhibitors, Nucleic Acids Res. 31, 5501-5512.
38. Mischo, H. E., Hemmerich, P., Grosse, F., and Zhang, S. (2005) Actinomycin D induces histone gamma-H2AX foci and complex formation of gamma-H2AX with Ku70 and nuclear DNA helicase II, J. Biol. Chem. 280, 9586-9594.
39. Cohen, P. (2000) The regulation of protein function by multisite phosphorylation - a 25 year update, Trends Biochem. Sci. 25, 596-601.
40. Friedemann, J., Grosse, F., and Zhang, S. (2005) Nuclear DNA helicase II (RNA helicase A) interacts with Werner syndrome helicase and stimulates its exonuclease activity, J. Biol. Chem. 280, 31303-31313.
41. Dyson, H. J., and Wright, P. E. (2005) Intrinsically unstructured proteins and their functions, Nat. Rev. Mol. Cell Biol. 6, 197-208.
42. Liu, J., Perumal, N. B., Oldfield, C. J., Su, E. W., Uversky, V. N., and Dunker, A. K. (2006) Intrinsic disorder in transcription factors, Biochemistry 45, 6873-6888.
43. Zhao, Y., Thomas, H. D., Batey, M. A., Cowell, I. G., Richardson, C. J., Griffin, R. J., Calvert, A. H., Newell, D. R., Smith, G. C., and Curtin, N. J. (2006) Preclinical evaluation of a potent novel DNA-dependent protein kinase inhibitor NU7441, Cancer Res. 66, 5354-5362.
44. Shinohara, E. T., Geng, L., Tan, J., Chen, H., Shir, Y., Edwards, E., Halbrook, J., Kesicki, E. A., Kashishian, A., and Hallahan, D. E. (2005) DNA-dependent protein kinase is a molecular target for the development of noncytotoxic radiation-sensitizing drugs, Cancer Res. 65, 4987-4992.
45. Cohen, P., Holmes, C. F., and Tsukitani, Y. (1990) Okadaic acid: a new probe for the study of cellular regulation, Trends Biochem. Sci. 15, 98-102.
46. Honkanen, R. E., and Golden, T. (2002) Regulators of serine/ threonine protein phosphatases at the dawn of a clinical era?, Curr. Med. Chem. 9, 2055-2075.
47. Douglas, P., Sapkota, G. P., Morrice, N., Yu, Y., Goodarzi, A. A., Merkle, D., Meek, K., Alessi, D. R., and Lees-Miller, S. P. (2002) Identification of in vitro and in vivo phosphorylation sites in the catalytic subunit of the DNA-dependent protein kinase, Biochem. J. 368, 243-251.
48. Bollen, M., and Beullens, M. (2002) Signaling by protein phosphatases in the nucleus, Trends Cell Biol. 12, 138-145.
49. Moorhead, G. B., Trinkle-Mulcahy, L., and Ulke-Lemee, A. (2007) Emerging roles of nuclear protein phosphatases, Nat. Rev. Mol. Cell Biol. 8, 234-244.