N-myristoylation is essential for protein phosphatases PPM1A and PPM1B to dephosphorylate their physiological substrates in cells

Biochemical Journal

Volumn 449, Issue 3, 2013, Pages 741-749

  Chida, Toko ^a   Ando, Masakatsu ^a   Matsuki, Tasuku ^a   Masu, Yutaro ^a   Nagaura, Yuko ^a   Takano Yamamoto, Teruko ^a   Tamura, Shinri ^a   Kobayashi, Takayasu ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

AMP activated protein kinase (AMPK); Metal dependent protein phosphatase 1A (PPM1A); Metal dependent protein phosphatase 1B (PPM1B); N myristoylation; Protein phosphatase 2C (PP2C)

Indexed keywords

4 NITROPHENYL PHOSPHATE; ADENYLATE KINASE; ADENYLATE KINASE ALPHA; PHOSPHOPROTEIN PHOSPHATASE; PPM1A PROTEIN; PPM1B PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; EMBRYO; GENE MUTATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MUTANT; MYRISTYLATION; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BASE SEQUENCE; CATALYTIC DOMAIN; HEK293 CELLS; HELA CELLS; HUMANS; MICE; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MYRISTIC ACID; NITROPHENOLS; ORGANOPHOSPHORUS COMPOUNDS; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT PROTEINS; RNA, SMALL INTERFERING; SUBSTRATE SPECIFICITY;

EID: 84872440362     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121201     Document Type: Article

References (42)

1. Resh, M. D. (2006) Trafficking and signaling by fatty-acylated and prenylated proteins. Nat. Chem. Biol. 2, 584-590
2. Wright, M. H., Heal, W. P., Mann, D. J. and Tate, E. W. (2010) Protein myristoylation in health and disease. J. Chem. Biol. 3, 19-35
3. Martin, D. D., Beauchamp, E. and Berthiaume, L. G. (2011) Post-translational myristoylation: fat matters in cellular life and death. Biochimie 93, 18-31
4. Zheng, J., Knighton, D. R., Xuong, N. H., Taylor, S. S., Sowadski, J. M. and Ten Eyck, L. F. (1993) Crystal structures of the myristylated catalytic subunit of cAMP-dependent protein kinase reveal open and closed conformations. Protein Sci. 2, 1559-1573 (Pubitemid 23294335)
5. Hantschel, O., Nagar, B., Guettler, S., Kretzschmar, J., Dorey, K., Kuriyan, J. and Superti-Furga, G. (2003) A myristoyl/phosphotyrosine switch regulates c-Abl. Cell 112, 845-857 (Pubitemid 36378886)
6. Nagar, B., Hantschel, O., Young, M. A., Scheffzek, K., Veach, D., Bornmann, W., Clarkson, B., Superti-Furga, G. and Kuriyan, J. (2003) Structural basis for the autoinhibition of c-Abl tyrosine kinase. Cell 112, 859-871 (Pubitemid 36378887)
7. Oakhill, J. S., Chen, Z. P., Scott, J. W., Steel, R., Castelli, L. A., Ling, N., Macaulay, S. L. and Kemp, B. E. (2010) β-Subunit myristoylation is the gatekeeper for initiating metabolic stress sensing by AMP-activated protein kinase (AMPK). Proc. Natl. Acad. Sci. U.S.A. 107, 19237-19241
8. McLaughlin, S. and Aderem, A. (1995) The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. Trends Biochem. Sci. 20, 272-276
9. Shi, Y. (2009) Serine/threonine phosphatases: mechanism through structure. Cell 139, 468-484
10. Lammers, T. and Lavi, S. (2007) Role of type 2C protein phosphatases in growth regulation and in cellular stress signaling. Crit. Rev. Biochem. Mol. Biol. 42, 437-461 (Pubitemid 350232897)
11. Tamura, S., Hanada, M., Ohnishi, M., Katsura, K., Sasaki, M. and Kobayashi, T. (2002) Regulation of stress-activated protein kinase signaling pathways by protein phosphatases. Eur. J. Biochem. 269, 1060-1066 (Pubitemid 34175363)
12. Tamura, S., Toriumi, S., Saito, J., Awano, K., Kudo, T. A. and Kobayashi, T. (2006) PP2C family members play key roles in regulation of cell survival and apoptosis. Cancer Sci. 97, 563-567 (Pubitemid 44056602)
13. Saito, S., Matsui, H., Kawano, M., Kumagai, K., Tomishige, N., Hanada, K., Echigo, S., Tamura, S. and Kobayashi, T. (2008) Protein phosphatase 2Cε is an endoplasmic reticulum integral membrane protein that dephosphorylates the ceramide transport protein CERT to enhance its association with organelle membranes. J. Biol. Chem. 283, 6584-6593
14. Tamura, S., Lynch, K. R., Larner, J., Fox, J., Yasui, A., Kikuchi, K., Suzuki, Y. and Tsuiki, S. (1989) Molecular cloning of rat type 2C (IA) protein phosphatase mRNA. Proc. Natl. Acad. Sci. U.S.A. 86, 1796-1800 (Pubitemid 19087021)
15. Sasaki, M., Ohnishi, M., Tashiro, F., Niwa, H., Suzuki, A., Miyazaki, J., Kobayashi, T. and Tamura, S. (2007) Disruption of the mouse protein Ser/Thr phosphatase 2Cβ gene leads to early pre-implantation lethality. Mech. Dev. 124, 489-499 (Pubitemid 46771136)
16. Yang, X., Teng, Y., Hou, N., Fan, X., Cheng, X., Li, J., Wang, L., Wang, Y. and Wu, X. (2011) Delayed re-epithelialization in Ppm1a gene-deficient mice is mediated by enhanced activation of Smad2. J. Biol. Chem. 286, 42267-42273
17. Takekawa, M., Maeda, T. and Saito, H. (1998) Protein phosphatase 2Cα inhibits the human stress-responsive p38 and JNK MAPK pathways. EMBO J. 17, 4744-4752 (Pubitemid 28377174)
18. Duan, X., Liang, Y. Y., Feng, X. H. and Lin, X. (2006) Protein serine/threonine phosphatase PPM1A dephosphorylates Smad1 in the bone morphogenetic protein signaling pathway. J. Biol. Chem. 281, 36526-36532 (Pubitemid 46042119)
19. Lin, X., Duan, X., Liang, Y. Y., Su, Y., Wrighton, K. H., Long, J., Hu, M., Davis, C. M., Wang, J., Brunicardi, F. C. et al. (2006) PPM1A functions as a Smad phosphatase to terminate TGFβ signaling. Cell 125, 915-928 (Pubitemid 43795197)
20. Dai, F., Shen, T., Li, Z., Lin, X. and Feng, X. H. (2011) PPM1A dephosphorylates RanBP3 to enable efficient nuclear export of Smad2 and Smad3. EMBO Rep. 12, 1175-1181
21. Hanada, M., Kobayashi, T., Ohnishi, M., Ikeda, S., Wang, H., Katsura, K., Yanagawa, Y., Hiraga, A., Kanamaru, R. and Tamura, S. (1998) Selective suppression of stress-activated protein kinase pathway by protein phosphatase 2C in mammalian cells. FEBS Lett. 437, 172-176 (Pubitemid 28511151)
22. Hanada, M., Ninomiya-Tsuji, J., Komaki, K., Ohnishi, M., Katsura, K., Kanamaru, R., Matsumoto, K. and Tamura, S. (2001) Regulation of the TAK1 signaling pathway by protein phosphatase 2C. J. Biol. Chem. 276, 5753-5759 (Pubitemid 37385728)
23. Prajapati, S., Verma, U., Yamamoto, Y., Kwak, Y. T. and Gaynor, R. B. (2004) Protein phosphatase 2Cβ association with the IκB kinase complex is involved in regulating NF-κB activity. J. Biol. Chem. 279, 1739-1746 (Pubitemid 38084441)
24. Sun, W., Yu, Y., Dotti, G., Shen, T., Tan, X., Savoldo, B., Pass, A. K., Chu, M., Zhang, D., Lu, X. et al. (2009) PPM1A and PPM1B act as IKKκ phosphatases to terminate TNFα-induced IKKβ-NF-κB activation. Cell. Signalling 21, 95-102
25. Marley, A. E., Sullivan, J. E., Carling, D., Abbott, W. M., Smith, G. J., Taylor, I. W., Carey, F. and Beri, R. K. (1996) Biochemical characterization and deletion analysis of recombinant human protein phosphatase 2Cα. Biochem. J. 320, 801-806 (Pubitemid 27013794)
26. Takai, A. and Mieskes, G. (1991) Inhibitory effect of okadaic acid on the p-nitrophenyl phosphate phosphatase activity of protein phosphatases. Biochem. J. 275, 233-239
27. Hardie, D. G. (2011) AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev. 25, 1895-1908
28. Carling, D., Mayer, F. V., Sanders, M. J. and Gamblin, S. J. (2011) AMP-activated protein kinase: nature's energy sensor. Nat. Chem. Biol. 7, 512-518
29. Mitchelhill, K. I., Michell, B. J., House, C. M., Stapleton, D., Dyck, J., Gamble, J., Ullrich, C., Witters, L. A. and Kemp, B. E. (1997) Posttranslational modifications of the 5′-AMP-activated protein kinase β1 subunit. J. Biol. Chem. 272, 24475-24479 (Pubitemid 27418657)
30. Moore, F., Weekes, J. and Hardie, D. G. (1991) Evidence that AMP triggers phosphorylation as well as direct allosteric activation of rat liver AMP-activated protein kinase. A sensitive mechanism to protect the cell against ATP depletion. Eur. J. Biochem. 199, 691-697
31. Davies, S. P., Helps, N. R., Cohen, P. T. and Hardie, D. G. (1995) 5′-AMP inhibits dephosphorylation, as well as promoting phosphorylation, of the AMP-activated protein kinase. Studies using bacterially expressed human protein phosphatase-2Cα and native bovine protein phosphatase-2AC. FEBS Lett. 377, 421-425 (Pubitemid 26027159)
32. Steinberg, G. R., Michell, B. J., van Denderen, B. J., Watt, M. J., Carey, A. L., Fam, B. C., Andrikopoulos, S., Proietto, J., Gorgun, C. Z., Carling, D. et al. (2006) Tumor necrosis factor α-induced skeletal muscle insulin resistance involves suppression of AMP-kinase signaling. Cell Metab. 4, 465-474 (Pubitemid 44834113)
33. Voss, M., Paterson, J., Kelsall, I. R., Martin-Granados, C., Hastie, C. J., Peggie, M. W. and Cohen, P. T. (2011) Ppm1E is an in cellulo AMP-activated protein kinase phosphatase. Cell. Signalling 23, 114-124
34. Henmi, T., Amano, K., Nagaura, Y., Matsumoto, K., Echigo, S., Tamura, S. and Kobayashi, T. (2009) A mechanism for the suppression of interleukin-1- induced nuclear factor κB activation by protein phosphatase 2Cη-2. Biochem. J. 423, 71-78
35. 2+-dependent protein phosphatase α. Gene 145, 311-312
36. Hawley, S. A., Boudeau, J., Reid, J. L., Mustard, K. J., Udd, L., Makela, T. P., Alessi, D. R. and Hardie, D. G. (2003) Complexes between the LKB1 tumor suppressor, STRAD α/β and MO25 α/β are upstream kinases in the AMP-activated protein kinase cascade. J. Biol. 2, 28
37. Chen, C. and Okayama, H. (1987) High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7, 2745-2752
38. Buss, J. E., Kamps, M. P. and Sefton, B. M. (1984) Myristic acid is attached to the transforming protein of Rous sarcoma virus during or immediately after synthesis and is present in both soluble and membrane-bound forms of the protein. Mol. Cell. Biol. 4, 2697-2704 (Pubitemid 15113608)
39. Ofek, P., Ben-Meir, D., Kariv-Inbal, Z., Oren, M. and Lavi, S. (2003) Cell cycle regulation and p53 activation by protein phosphatase 2Cα. J. Biol. Chem. 278, 14299-14305 (Pubitemid 36799979)
40. Das, A. K., Helps, N. R., Cohen, P. T. and Barford, D. (1996) Crystal structure of the protein serine/threonine phosphatase 2C at 2.0 Å resolution. EMBO J. 15, 6798-6809
41. Lifschitz-Mercer, B., Sheinin, Y., Ben-Meir, D., Bramante-Schreiber, L., Leider-Trejo, L., Karby, S., Smorodinsky, N. I. and Lavi, S. (2001) Protein phosphatase 2Cα expression in normal human tissues: an immunohistochemical study. Histochem. Cell Biol. 116, 31-39 (Pubitemid 32695815)
42. Tsugama, D., Liu, S. and Takano, T. (2012) A putative myristoylated 2C-type protein phosphatase, PP2C74, interacts with SnRK1 in Arabidopsis. FEBS Lett. 586, 693-698