Molecular mechanism by which palmitate inhibits PKR autophosphorylation

Biochemistry

Volumn 50, Issue 6, 2011, Pages 1110-1119

  Cho, Hyunju ^a   Mukherjee, Shayantani ^b   Palasuberniam, Pratheeba ^b   Pillow, Lisa ^a   Bilgin, Betul ^a   Nezich, Catherine ^b   Walton, S Patrick ^a   Feig, Michael ^b   Chan, Christina ^a,b  

^a Michigan State University   (United States)

^b Michigan State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATED PROTEINS; APOPTOSIS; APOPTOTIC PATHWAYS; ATP-BINDING SITE; AUTOPHOSPHORYLATION; COMPUTATIONAL STUDIES; DOUBLE-STRANDED RNA; INNATE IMMUNITY; MOLECULAR MECHANISM; SIGNALING PATHWAYS;

BINDING SITES; CELL DEATH; DRUG INTERACTIONS; DRUG THERAPY; PHOSPHORYLATION; RNA; SATURATED FATTY ACIDS;

ENZYMES;

ADENOSINE TRIPHOSPHATE; ASPARTIC ACID; LYSINE; PALMITIC ACID; PROTEIN KINASE R; THREONINE;

ARTICLE; AUTOPHOSPHORYLATION; BINDING SITE; BIOCHEMISTRY; CELL FUNCTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FLUORESCENCE; HUMAN; HUMAN CELL; MOLECULAR DOCKING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; BINDING SITES; EIF-2 KINASE; KINETICS; MODELS, MOLECULAR; MUTATION; PALMITATES; PHOSPHORYLATION;

EID: 79851495873     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101923r     Document Type: Article

References (55)

1. Stark, G. R., Kerr, I. M., Williams, B. R., Silverman, R. H., and Schreiber, R. D. (1998) How cells respond to interferons Annu. Rev. Biochem. 67, 227-264
2. Dey, M., Cao, C., Dar, A. C., Tamura, T., Ozato, K., Sicheri, F., and Dever, T. E. (2005) Mechanistic link between PKR dimerization, autophosphorylation, and eIF2alpha substrate recognition Cell 122, 901-913
3. Gale, M., Jr. and Katze, M. G. (1998) Molecular mechanisms of interferon resistance mediated by viral-directed inhibition of PKR, the interferon-induced protein kinase Pharmacol. Ther. 78, 29-46
4. Xu, Z. and Williams, B. R. (2000) The B56alpha regulatory subunit of protein phosphatase 2A is a target for regulation by double-stranded RNA-dependent protein kinase PKR Mol. Cell. Biol. 20, 5285-5299
5. Williams, B. R. (1999) PKR; a sentinel kinase for cellular stress Oncogene 18, 6112-6120
6. Nanduri, S., Carpick, B. W., Yang, Y., Williams, B. R., and Qin, J. (1998) Structure of the double-stranded RNA-binding domain of the protein kinase PKR reveals the molecular basis of its dsRNA-mediated activation EMBO J. 17, 5458-5465
7. Nanduri, S., Rahman, F., Williams, B. R., and Qin, J. (2000) A dynamically tuned double-stranded RNA binding mechanism for the activation of antiviral kinase PKR EMBO J. 19, 5567-5574
8. Dar, A. C., Dever, T. E., and Sicheri, F. (2005) Higher-order substrate recognition of eIF2alpha by the RNA-dependent protein kinase PKR Cell 122, 887-900
9. Johnson, L. N., Noble, M. E., and Owen, D. J. (1996) Active and inactive protein kinases: structural basis for regulation Cell 85, 149-158
10. Nolen, B., Taylor, S., and Ghosh, G. (2004) Regulation of protein kinases; controlling activity through activation segment conformation Mol. Cell 15, 661-675
11. McKenna, S. A., Lindhout, D. A., Kim, I., Liu, C. W., Gelev, V. M., Wagner, G., and Puglisi, J. D. (2007) Molecular framework for the activation of RNA-dependent protein kinase J. Biol. Chem. 282, 11474-11486
12. Lee, S. B. and Esteban, M. (1994) The interferon-induced double-stranded RNA-activated protein kinase induces apoptosis Virology 199, 491-496
13. Takizawa, T., Ohashi, K., and Nakanishi, Y. (1996) Possible involvement of double-stranded RNA-activated protein kinase in cell death by influenza virus infection J. Virol. 70, 8128-8132
14. Kibler, K. V., Shors, T., Perkins, K. B., Zeman, C. C., Banaszak, M. P., Biesterfeldt, J., Langland, J. O., and Jacobs, B. L. (1997) Double-stranded RNA is a trigger for apoptosis in vaccinia virus-infected cells J. Virol. 71, 1992-2003
15. Yeung, M. C., Chang, D. L., Camantigue, R. E., and Lau, A. S. (1999) Inhibitory role of the host apoptogenic gene PKR in the establishment of persistent infection by encephalomyocarditis virus in U937 cells Proc. Natl. Acad. Sci. U.S.A. 96, 11860-11865
16. Garcia, M. A., Gil, J., Ventoso, I., Guerra, S., Domingo, E., Rivas, C., and Esteban, M. (2006) Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action Microbiol. Mol. Biol. Rev. 70, 1032-1060
17. Kim, S. H., Forman, A. P., Mathews, M. B., and Gunnery, S. (2000) Human breast cancer cells contain elevated levels and activity of the protein kinase, PKR Oncogene 19, 3086-3094
18. Kim, S. H., Gunnery, S., Choe, J. K., and Mathews, M. B. (2002) Neoplastic progression in melanoma and colon cancer is associated with increased expression and activity of the interferon-inducible protein kinase, PKR Oncogene 21, 8741-8748
19. Hiasa, Y., Kamegaya, Y., Nuriya, H., Onji, M., Kohara, M., Schmidt, E. V., and Chung, R. T. (2003) Protein kinase R is increased and is functional in hepatitis C virus-related hepatocellular carcinoma Am. J. Gastroenterol. 98, 2528-2534
20. Delgado Andre, N. and De Lucca, F. L. (2007) Knockdown of PKR expression by RNAi reduces pulmonary metastatic potential of B16-F10 melanoma cells in mice: possible role of NF-kappaB Cancer Lett. 258, 118-125
21. Li, Z., Srivastava, S., Mittal, S., Yang, X., Sheng, L., and Chan, C. (2007) A three stage integrative pathway search (TIPS) framework to identify toxicity relevant genes and pathways BMC Bioinf. 8, 202
22. Yang, X. and Chan, C. (2009) Repression of PKR mediates palmitate-induced apoptosis in HepG2 cells through regulation of Bcl-2 Cell Res. 19, 469-486
23. Bhattacharya, A. A., Grune, T., and Curry, S. (2000) Crystallographic analysis reveals common modes of binding of medium and long-chain fatty acids to human serum albumin J. Mol. Biol. 303, 721-732
24. Chmurzynska, A. (2006) The multigene family of fatty acid-binding proteins (FABPs): function, structure and polymorphism J. Appl. Genet. 47, 39-48 (Pubitemid 43232158)
25. Furuhashi, M. and Hotamisligil, G. S. (2008) Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets Nat. Rev. 7, 489-503
26. Richieri, G. V., Anel, A., and Kleinfeld, A. M. (1993) Interactions of long-chain fatty acids and albumin: determination of free fatty acid levels using the fluorescent probe ADIFAB Biochemistry 32, 7574-7580
27. Veerkamp, J. H., van Moerkerk, H. T., Prinsen, C. F., and van Kuppevelt, T. H. (1999) Structural and functional studies on different human FABP types Mol. Cell. Biochem. 192, 137-142
28. Richieri, G. V., Ogata, R. T., Zimmerman, A. W., Veerkamp, J. H., and Kleinfeld, A. M. (2000) Fatty acid binding proteins from different tissues show distinct patterns of fatty acid interactions Biochemistry 39, 7197-7204
29. Wisely, G. B., Miller, A. B., Davis, R. G., Thornquest, A. D., Jr., Johnson, R., Spitzer, T., Sefler, A., Shearer, B., Moore, J. T., Miller, A. B., Willson, T. M., and Williams, S. P. (2002) Hepatocyte nuclear factor 4 is a transcription factor that constitutively binds fatty acids Structure 10, 1225-1234
30. Bevilacqua, P. C. and Cech, T. R. (1996) Minor-groove recognition of double-stranded RNA by the double-stranded RNA-binding domain from the RNA-activated protein kinase PKR Biochemistry 35, 9983-9994
31. Lemaire, P. A., Lary, J., and Cole, J. L. (2005) Mechanism of PKR activation: dimerization and kinase activation in the absence of double-stranded RNA J. Mol. Biol. 345, 81-90
32. Jammi, N. V. and Beal, P. A. (2001) Phosphorylation of the RNA-dependent protein kinase regulates its RNA-binding activity Nucleic Acids Res. 29, 3020-3029
33. Matsui, T., Tanihara, K., and Date, T. (2001) Expression of unphosphorylated form of human double-stranded RNA-activated protein kinase in Escherichia coli Biochem. Biophys. Res. Commun. 284, 798-807
34. Lippa, B., Pan, G., Corbett, M., Li, C., Kauffman, G. S., Pandit, J., Robinson, S., Wei, L., Kozina, E., Marr, E. S., Borzillo, G., Knauth, E., Barbacci-Tobin, E. G., Vincent, P., Troutman, M., Baker, D., Rajamohan, F., Kakar, S., Clark, T., and Morris, J. (2008) Synthesis and structure based optimization of novel Akt inhibitors Bioorg. Med. Chem. Lett. 18, 3359-3363
35. Day, P. J., Cleasby, A., Tickle, I. J., O’Reilly, M., Coyle, J. E., Holding, F. P., McMenamin, R. L., Yon, J., Chopra, R., Lengauer, C., and Jhoti, H. (2009) Crystal structure of human CDK4 in complex with a D-type cyclin Proc. Natl. Acad. Sci. U.S.A. 106, 4166-4170
36. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., and Bourne, P. E. (2000) The Protein Data Bank Nucleic Acids Res. 28, 235-242
37. Kiefer, F., Arnold, K., Kunzli, M., Bordoli, L., and Schwede, T. (2009) The SWISS-MODEL Repository and associated resources Nucleic Acids Res. 37, D387-392
38. White, A., Pargellis, C. A., Studts, J. M., Werneburg, B. G., and Farmer, B. T., II (2007) Molecular basis of MAPK-activated protein kinase 2:p38 assembly Proc. Natl. Acad. Sci. U.S.A. 104, 6353-6358
39. Brooks, B. R., Brooks, C. L., III, Mackerell, A. D., Jr., Nilsson, L., Petrella, R. J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., Caflisch, A., Caves, L., Cui, Q., Dinner, A. R., Feig, M., Fischer, S., Gao, J., Hodoscek, M., Im, W., Kuczera, K., Lazaridis, T., Ma, J., Ovchinnikov, V., Paci, E., Pastor, R. W., Post, C. B., Pu, J. Z., Schaefer, M., Tidor, B., Venable, R. M., Woodcock, H. L., Wu, X., Yang, W., York, D. M., and Karplus, M. (2009) CHARMM: the biomolecular simulation program J. Comput. Chem. 30, 1545-1614
40. Mackerell, A. D., Jr., Feig, M., and Brooks, C. L., III (2004) Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations J. Comput. Chem. 25, 1400-1415
41. Wu, G., Robertson, D. H., Brooks, C. L., III, and Vieth, M. (2003) Detailed analysis of grid-based molecular docking: a case study of CDOCKER-A CHARMm-based MD docking algorithm J. Comput. Chem. 24, 1549-1562
42. Erickson, J. A., Jalaie, M., Robertson, D. H., Lewis, R. A., and Vieth, M. (2004) Lessons in molecular recognition: the effects of ligand and protein flexibility on molecular docking accuracy J. Medi. Chem. 47, 45-55
43. Richieri, G. V. and Kleinfeld, A. M. (1995) Unbound free fatty acid levels in human serum J. Lipid Res. 36, 229-240
44. 3H]palmitate to BSA Am. J. Physiol. 275, G638-644
45. Kornev, A. P., Haste, N. M., Taylor, S. S., and Eyck, L. F. (2006) Surface comparison of active and inactive protein kinases identifies a conserved activation mechanism Proc. Natl. Acad. Sci. U.S.A. 103, 17783-17788
46. Wittayanarakul, K., Hannongbua, S., and Feig, M. (2008) Accurate prediction of protonation state as a prerequisite for reliable MM-PB(GB)SA binding free energy calculations of HIV-1 protease inhibitors J. Comput. Chem. 29, 673-685
47. Lemaire, P. A., Tessmer, I., Craig, R., Erie, D. A., and Cole, J. L. (2006) Unactivated PKR exists in an open conformation capable of binding nucleotides Biochemistry 45, 9074-9084
48. Thumser, A. E. and Storch, J. (2007) Characterization of a BODIPY-labeled fluorescent fatty acid analogue. Binding to fatty acid-binding proteins, intracellular localization, and metabolism Mol. Cell. Biochem. 299, 67-73
49. Rioux, V., Lemarchal, P., and Legrand, P. (2000) Myristic acid, unlike palmitic acid, is rapidly metabolized in cultured rat hepatocytes J. Nutr. Biochem. 11, 198-207
50. Takai, Y., Kishimoto, A., Iwasa, Y., Kawahara, Y., Mori, T., and Nishizuka, Y. (1979) Calcium-dependent activation of a multifunctional protein kinase by membrane phospholipids J. Biol. Chem. 254, 3692-3695
51. Newton, A. C. (2003) Regulation of the ABC kinases by phosphorylation: protein kinase C as a paradigm Biochem. J. 370, 361-371 (Pubitemid 36315124)
52. Calleja, V., Alcor, D., Laguerre, M., Park, J., Vojnovic, B., Hemmings, B. A., Downward, J., Parker, P. J., and Larijani, B. (2007) Intramolecular and intermolecular interactions of protein kinase B define its activation in vivo PLoS Biol. 5, e95
53. Diskin, R., Engelberg, D., and Livnah, O. (2008) A novel lipid binding site formed by the MAP kinase insert in p38 alpha J. Mol. Biol. 375, 70-79
54. Barber, G. N. (2005) The dsRNA-dependent protein kinase, PKR and cell death Cell Death Differ. 12, 563-570 (Pubitemid 40767160)
55. Knight, J. D., Qian, B., Baker, D., and Kothary, R. (2007) Conservation, variability and the modeling of active protein kinases PloS One 2, e982