Ionizing radiation induces ataxia telangiectasia mutated kinase (ATM)-mediated phosphorylation of LKB1/STK11 at Thr-366

Biochemical Journal

Volumn 368, Issue 2, 2002, Pages 507-516

  Sapkota, Gopal P ^a   Deak, Maria ^a   Kieloch, Agnieszka ^a   Morrice, Nick ^a   Goodarzi, Aaron A ^b   Smythe, Carl ^a,d   Shiloh, Yosef ^c   Lees Miller, Susan P ^b   Alessi, Dario R ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF CALGARY   (Canada)

^c TEL AVIV UNIVERSITY   (Israel)

^d UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Ataxia telangiectasia related kinase (ATR); DNA dependent protein kinase (DNA PK); Peutz Jeghers syndrome; Phosphopeptide mapping

Indexed keywords

AMINO ACIDS; ANTIBODIES; CELLS; DNA; IONIZING RADIATION; TUMORS;

PHOSPHORYLATION;

ENZYMES;

ATM PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN SERINE THREONINE KINASE; THREONINE;

ANIMAL CELL; ANTIBODY SPECIFICITY; ARTICLE; ATAXIA TELANGIECTASIA; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA DAMAGE; DROSOPHILA; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; GENE MUTATION; HUMAN; HUMAN CELL; IONIZING RADIATION; MELANOMA CELL; NONHUMAN; PEUTZ JEGHERS SYNDROME; PRIORITY JOURNAL; XENOPUS;

AMINO ACID SEQUENCE; ANIMALS; CELL CYCLE PROTEINS; CELL NUCLEUS; CELLS, CULTURED; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RADIATION, IONIZING; THREONINE; TUMOR SUPPRESSOR PROTEINS;

ANIMALIA; ATAXIA; ATAXIA TELANGIECTASIA; MAMMALIA;

EID: 0036901639     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20021284     Document Type: Article

References (58)

1. Hemminki, A., Markie, D., Tomlinson, I., Avizienyte, E., Roth, S., Loukola, A., Bignell, G., Warren, W., Aminoff, M., Hoglund, P. et al. (1998) A serine/threonine kinase gene defective in Peutz-Jeghers syndrome. Nature (London) 391, 184-187
2. Jenne, D. E., Reimann, H., Nezu, J., Friedel, W., Loff, S., Jeschke, R., Muller, O., Back, W. and Zimmer, M. (1998) Peutz-Jeghers syndrome is caused by mutations in a novel serine threonine kinase. Nat. Genet. 18, 38-43
3. Hemminki, A. (1999) The molecular basis and clinical aspects of Peutz-Jeghers syndrome. Cell. Mol. Life Sci. 55, 735-750
4. Westerman, A. M., Entius, M. M., de Baar, E., Boor, P. P., Koole, R., van Velthuysen, M. L., Offerhaus, G. J., Lindhout, D., de Rooij, F. W. and Wilson, J. H. (1999) Peutz-Jeghers syndrome: 78-Year follow-up of the original family. Lancet 353, 1211-1215
5. Tiainen, M., Ylikorkala, A. and Makela, T. P. (1999) Growth suppression by Lkb1 is mediated by a G(1) cell cycle arrest. Proc. Natl. Acad. Sci. U.S.A. 96, 9248-9251
6. Tiainen, M., Vaahtomeri, K., Ylikorkala, A. and Makela, T. P. (2002) Growth arrest by the LKB1 tumor suppressor: Induction of p21(WAF1/CIP1). Hum. Mol. Genet 11, 1497-1504
7. Yoo, L. I., Chung, D. C. and Yuan, J. (2002) LKB1 A master tumour suppressor of the small intestine and beyond. Nat. Rev. Cancer. 2, 529-535
8. Bardeesy, N., Sinha, M., Hezel, A. F., Signoretti, S., Hathaway, N. A., Sharpless, N. E., Loda, M., Carrasco, D. R. and DePinho, R. A. (2002) Loss of the Lkb1 tumour suppressor provokes intestinal polyposis but resistance to transformation. Nature (London) 419, 162-167
9. Jishage, K. I., Nezu, J. I., Kawase, Y, Iwata, T., Watanabe, M., Miyoshi, A., Ose, A., Habu, K., Kake, T., Kamada, N., Ueda, O. et al. (2002) Role of Lkb1, the causative gene of Peutz-Jegher's syndrome, in embryogenesis and polyposis. Proc. Natl. Acad. Sci. U.S.A. 99, 8903-8908
10. Mihaylova, V. T., Borland, C. Z., Manjarrez, L., Stern, M. J. and Sun, H. (1999) The PTEN tumor suppressor homolog in Caenorhabditis elegans regulates longevity and dauer formation in an insulin receptor-like signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 96, 7427-7432
11. Nakau, M., Miyoshi, H., Seldin, M. F., Imamura, M., Oshima, M. and Taketo, M. M. (2002) Hepatocellular carcinoma caused by loss of heterozygosity in lkb1 gene knockout mice. Cancer Res. 62. 4549-4553
12. Rossi, D. J., Ylikorkala, A., Korsisaari, N., Salovaara, R., Luukko, K., Launonen, V., Henkemeyer, M., Ristimaki, A., Aaltonen, L. A. and Makela, T. P. (2002) Induction of cyclooxygenase-2 in a mouse model of Peutz-Jeghers polyposis. Proc. Natl. Acad. Sci. U.S.A. 99, 12327-12332
13. Karuman, P., Gozani, O., Odze, R. D., Zhou, X. C., Zhu, H., Shaw, R., Brien, T. P., Bozzuto, C. D., Ooi, D., Cantley, L. C. and Yuan, J. (2001) The Peutz-Jegher gene product LKB1 is a mediator of p53-dependent cell death. Mol. Cell 7, 1307-1319
14. Marignani, P. A., Kanai, F. and Carpenter, C. L. (2001) Lkb1 associates with brg1 and is necessary for brg1-induced growth arrest. J. Biol. Chem. 276, 32415-32418
15. Smith, D. P., Rayter, S. I., Niederlander, C., Spicer, J., Jones, C. M. and Ashworth, A. (2001) LIP1, a cytoplasmic protein functionally linked to the Peutz-Jeghers syndrome kinase LKB1. Hum. Mol. Genet. 10, 2869-2877
16. Sapkota, G. P., Boudeau, J., Deak, M., Kieloch, A., Morrice, N. and Alessi, D. R. (2002) Identification and characterization of four novel phosphorylation sites (Ser31, Ser325, Thr336 and Thr366) on LKB1/STK11, the protein kinase mutated in Peutz-Jeghers cancer syndrome. Biochem. J. 362, 481-490
17. Sapkota, G. P., Kieloch, A., Lizcano, J. M., Lain, S., Arthur, J. S., Williams, M. R., Morrice, N., Deak, M. and Alessi, D. R. (2001) Phosphorylation of the protein kinase mutated in Peutz-Jeghers cancer syndrome, LKB1/STK11, at Ser431 by p90RSK and cAMP-dependent protein kinase, but not its farnesylation at Cys433, is essential for LKB1 to suppress cell growth. J. Biol. Chem. 276, 19469-19482
18. Collins, S. P., Reoma, J. L., Gamm, D. M. and Uhler, M. D. (2000) LKB1, a novel serine/threonine protein kinase and potential tumour suppressor, is phosphorylated by cAMP-dependent protein kinase (PKA) and prenylated in vivo. Biochem. J. 345, 673-680
19. Abraham, R. T. (2001) Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15, 2177-2196
20. Durocher, D. and Jackson, S. P. (2001) DNA-PK, ATM and ATR as sensors of DNA damage: Variations on a theme? Curr. Opin. Cell Biol. 13, 225-231
21. Shiloh, Y. and Kastan, M. B. (2001) ATM: Genome stability, neuronal development, and cancer cross paths. Adv. Cancer Res. 83, 209-254
22. Chan, D. W., Mody, C. H., Ting, N. S. and Lees-Miller, S. P. (1996) Purification and characterization of the double-stranded DNA-activated protein kinase, DNA-PK, from human placenta. Biochem. Cell Biol. 74, 67-73
23. Ching, Y. P., Davies, S. P. and Hardie, D. G. (1996) Analysis of the specificity of the AMP-activated protein kinase by site-directed mutagenesis of bacterially expressed 3-hydroxy 3-methylglutaryl-CoA reductase, using a single primer variant of the unique-site-elimination method. Eur. J. Biochem. 237, 800-808
24. Feijoo, C., Hall-Jackson, C., Wu, R., Jenkins, D., Leitch, J., Gilbert, D. M. and Smythe, C. (2001) Activation of mammalian Chk1 during DNA replication arrest: A role for Chk1 in the intra-S phase checkpoint monitoring replication origin firing. J. Cell Biol. 154, 913-923
25. Williams. M. R., Arthur, J. S., Balendran, A., van der Kaay, J., Poli, V., Cohen, P. and Alessi, D. R. (2000) The role of 3-phosphoinositide-dependent protein kinase 1 in activating AGC kinases defined in embryonic stem cells. Curr. Biol. 10, 439-448
26. Banin, S., Moyal, L., Shieh, S., Taya, Y., Anderson, C. W., Chessa, L., Smorodinsky, N. I., Prives, C., Reiss, Y., Shiloh, Y. and Ziv, Y. (1998) Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 281, 1674-1677
27. Achari, Y. and Lees-Miller, S. P. (2000) Detection of DNA-dependent protein kinase in extracts from human and rodent cells. Methods Mol. Biol. 99, 85-97
28. Ziv, Y., Bar-Shira, A., Pecker, I., Russell, P., Jorgensen, T. J., Tsarfati, I. and Shiloh, Y. (1997) Recombinant ATM protein complements the cellular A-T phenotype. Oncogene 15, 159-167
29. Harlow, E. and Lane, D. (1988) Antibodies: A Laboratory Manual, Cold Spring Harbor Press, New York
30. Chan, D. W. and Lees-Miller, S. P. (1996) The DNA-dependent protein kinase is inactivated by autophosphorylation of the catalytic subunit. J. Biol. Chem. 271, 8936-8941
31. Campbell, D. G. and Morrice, N. A. (2002) Identification of protein phosphorylation sites by a combination of mass spectrometry and solid phase Edman sequencing. J. Biomol. Techniq. 13, 121-132
32. Guo, S., Rena, G., Cichy, S., He, X., Cohen, P. and Unterman, T. (1999) Phosphorylation of serine 256 by protein kinase B disrupts transactivation by FKHR and mediates effects of insulin on insulin-like growth factor-binding protein-1 promoter activity through a conserved insulin response sequence. J. Biol. Chem. 274, 17184-17192
33. Liu, Q., Guntuku, S., Cui, X. S., Matsuoka, S., Cortez, D., Tamai, K., Luo, G., Carattini-Rivera, S., DeMayo, F., Bradley, A., Donehower, L. A. and Elledge, S. J. (2000) Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Dev. 14, 1448-1459
34. Zhao, H. and Piwnica-Worms, H. (2001) ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol. Cell. Biol. 21, 4129-4139
35. Vanhaesebroeck, B. and Alessi, D. R. (2000) The PI3K-PDK1 connection: More than just a road to PKB. Biochem. J. 346, 561-576
36. Anderson, C. W. (1993) DNA damage and the DNA-activated protein kinase. Trends Biochem. Sci. 18, 433-437
37. Lees-Miller, S. P., Sakaguchi, K., Ullrich, S. J., Appella, E. and Anderson, C. W. (1992) Human DNA-activated protein kinase phosphorylates serines 15 and 37 in the amino-terminal transactivation domain of human p53. Mol. Cell. Biol. 12, 5041-5049
38. O'Neill, T., Dwyer, A. J., Ziv, Y., Chan, D. W., Lees-Miller, S. P., Abraham, R. H., Lai, J. H., Hill, D., Shiloh, Y., Cantley, L. C. and Rathbun, G. A. (2000) Utilization of oriented peptide libraries to identify substrate motifs selected by ATM. J. Biol. Chem. 275, 22719-22727
39. Kim, S. T., Lim, D. S., Canman, C. E. and Kastan, M. B. (1999) Substrate specificities and identification of putative substrates of ATM kinase family members. J. Biol. Chem. 274, 37538-37543
40. Gasch, A. P., Huang, M., Metzner, S., Botstein, D., Elledge, S. J. and Brown, P. O. (2001) Genomic expression responses to DNA-damaging agents and the regulatory role of the yeast ATR homolog Mec1p. Mol. Biol. Cell 12, 2987-3003
41. Karpova, A. Y., Trost, M., Murray, J. M., Cantley, L. C. and Howley, P. M. (2002) Interferon regulatory factor-3 is an in vivo target of DNA-PK. Proc. Natl. Acad. Sci. U.S.A. 99, 2818-2823
42. Tibbetts, R. S., Cortez, D., Brumbaugh, K. M., Scully, R., Livingston, D., Elledge, S. J. and Abraham, R. T. (2000) Functional interactions between BRCA1 and the checkpoint kinase ATR during genotoxic stress. Genes Dev. 14, 2989-3002
43. Lavin, M. F. and Shiloh, Y. (1997) The genetic defect in ataxia-telangiectasia. Annu. Rev. Immunol. 15, 177-202
44. Shiloh, Y. and Rotman, G. (1996) Ataxia-telangiectasia and the ATM gene: Linking neurodegeneration, immunodeficiency, and cancer to cell cycle checkpoints. J. Clin. Immunol. 16, 254-260
45. Ahn, J. Y., Schwarz, J. K., Piwnica-Worms, H. and Canman, C. E. (2000) Threonine 68 phosphorylation by ataxia telangiectasia mutated is required for efficient activation of Chk2 in response to ionizing radiation. Cancer Res. 60, 5934-5936
46. Smith, G. C., Cary, R. B., Lakin, N. D., Hann, B. C., Teo, S. H., Chen, D. J. and Jackson, S. P. (1999) Purification and DNA binding properties of the ataxia-telangiectasia gene product ATM. Proc. Natl. Acad. Sci. U.S.A. 96, 11134-11139
47. Smith, D. P., Spicer, J., Smith, A., Swift, S. and Ashworth, A. (1999) The mouse Peutz-Jeghers syndrome gene Lkb1 encodes a nuclear protein kinase. Hum. Mol. Genet. 8, 1479-1485
48. Sanchez, Y., Wong, C., Thoma, R. S., Richman, R., Wu, Z., Piwnica-Worms, H. and Elledge, S. J. (1997) Conservation of the Chk1 checkpoint pathway in mammals: Linkage of DNA damage to Cdk regulation through Cdc25. Science 277, 1497-1501
49. Yarden, R. I., Pardo-Reoyo, S., Sgagias, M., Cowan, K. H. and Brody, L. C. (2002) BRCA1 regulares the G2/M checkpoint by activating Chk1 kinase upon DNA damage. Nat. Genet. 30, 285-289
50. Dong, S. M., Kim, K. M., Kim, S. Y., Shin, M. S., Na, E. Y., Lee, S. H., Park, W. S., Yoo, N. J., Jang, J. J., Yoon, C. Y. et al. (1998) Frequent somatic mutations in serine/threonine kinase 11/Peutz-Jeghers syndrome gene in left-sided colon cancer. Cancer Res. 58, 3787-3790
51. Resta, N., Simone, C., Mareni, C., Montera, M., Gentile, M., Susca, F., Gristina, R., Pozzi, S., Bertario, L., Bufo, P. et al. (1998) STK11 mutations in Peutz-Jeghers syndrome and sporadic colon cancer. Cancer Res. 58, 4799-4801
52. Park, W. S., Moon, Y. W., Yang, Y. M., Kim, Y. S., Kim, Y. D., Fuller, B. G., Vortmeyer, A. O., Fogt, F., Lubensky, I. A. and Zhuang, Z. (1998) Mutations of the STK11 gene in sporadic gastric carcinoma. Int. J. Oncol. 13, 601-604
53. Yoon, K. A., Ku, J. L., Choi, H. S., Heo, S. C., Jeong, S. Y., Park, Y. J., Kim, N. K., Kim, J C., Jung, P. M. and Park, J. G. (2000) Germline mutations of the STK11 gene in Korean Peutz-Jeghers syndrome patients. Br. J. Cancer 82, 1403-1406
54. Gruber, S. B., Entius, M. M., Petersen, G. M., Laken, S. J., Longo, P. A., Boyer, R., Levin, A. M., Mujumdar, U. J., Trent, J. M., Kinzler, K. W. et al. (1998) Pathogenesis of adenocarcinoma in Peutz-Jeghers syndrome. Cancer Res. 58, 5267-5270
55. Wang, Z. J., Churchman, M., Avizienyte, E., McKeown, C., Davies, S., Evans, D. G., Ferguson, A., Ellis, I., Xu, W. H., Yan, Z. Y. et al. (1999) Germline mutations of the LKB1 (STK11) gene in Peutz-Jeghers patients. J. Med. Genet. 36, 365-368
56. Olschwang, S., Boisson, C. and Thomas, G. (2001) Peutz-Jeghers families unlinked to STK11/LKB1 gene mutations are highly predisposed to primitive biliary adenocarcinoma. J. Med. Genet. 38, 356-360
57. Su, G. H., Hruban, R. H., Bansal, R. K., Bova, G. S., Tang, D. J., Shekher, M. C., Westerman, A. M., Entius, M. M., Goggins, M., Yeo, C. J. and Kern, S. E. (1999) Germline and somatic mutations of the STK11/LKB1 Peutz-Jeghers gene in pancreatic and biliary cancers. Am. J. Pathol. 154, 1835-1840
58. Ylikorkala, A., Avizienyte, E., Tomlinson, I. P., Tiainen, M., Roth, S., Loukola, A., Hemminki, A., Johansson, M., Sistonen, P., Markie, D. et al. (1999) Mutations and impaired function of LKB1 in familial and non-familial Peutz-Jeghers syndrome and a sporadic testicular cancer. Hum. Mol. Genet. 8, 45-51