Chemoproteomic analysis of intertissue and interspecies isoform diversity of AMP-activated protein kinase (AMPK)

Journal of Biological Chemistry

Volumn 288, Issue 50, 2013, Pages 35904-35912

  Wu, Jiang ^a,b   Puppala, Dinesh ^a   Feng, Xidong ^a   Monetti, Mara ^a   Lapworth, Amanda Lee ^a   Geoghegan, Kieran F ^a  

^a PFIZER INC   (United States)

^b SHIRE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMP-ACTIVATED PROTEIN KINASE; ATP-BINDING SITE; BIOLOGICAL FUNCTIONS; HUMAN LIVER TISSUES; METABOLIC FUNCTION; RELATIVE QUANTITATIONS; SEQUENCE SIMILARITY; TISSUE SPECIFICITY;

BINDING SITES; ENZYMES; PROBES; PROTEINS;

TISSUE;

ADENOSINE TRIPHOSPHATE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; ISOPROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; BIODIVERSITY; CHEMICAL LABELING; CHEMOPROTEOMICS ANALYSIS; CONTROLLED STUDY; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNODETECTION; MOLECULAR PROBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEOMICS; QUANTITATIVE ANALYSIS; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE;

AMP-ACTIVATED KINASE (AMPK); CHEMICAL BIOLOGY; CHEMICAL MODIFICATION; DRUG DISCOVERY; MASS SPECTROMETRY (MS);

AMINO ACID SEQUENCE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CELL LINE; DOGS; HEK293 CELLS; HEPATOCYTES; HUMANS; ISOENZYMES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; MYOCARDIUM; ORGAN SPECIFICITY; PROTEIN STRUCTURE, QUATERNARY; PROTEOMICS; RATS; RNA, MESSENGER; SPECIES SPECIFICITY;

EID: 84890382052     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.508747     Document Type: Article

References (60)

1. Hardie, D. G., Ross, F. A., and Hawley, S. A. (2012) AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell Biol. 13, 251-262
2. Gowans, G. J., Hawley, S. A., Ross, F. A., and Hardie, D. G. (2013) AMP is a true physiological regulator of AMP-activated protein kinase by both allosteric activation and enhancing net phosphorylation. Cell Metab. 18, 556-566
3. Hardie, D. G., Carling, D., and Gamblin, S. J. (2011) AMP-activated protein kinase: also regulated by ADP? Trends Biochem. Sci. 36, 470-477
4. Steinberg, G. R., and Kemp, B. E. (2009) AMPK in health and disease. Physiol. Rev. 89, 1025-1078
5. Fogarty, S., and Hardie, D. G. (2010) Development of protein kinase activators: AMPK as a target in metabolic disorders and cancer. Biochim. Biophys. Acta 1804, 581-591
6. Hardie, D. G., and Sakamoto, K. (2006) AMPK: a key sensor of fuel and energy status in skeletal muscle. Physiology 21, 48-60
7. Viollet, B., Guigas, B., Leclerc, J., Hébrard, S., Lantier, L., Mounier, R., Andreelli, F., and Foretz, M. (2009) AMP-activated protein kinase in the regulation of hepatic energy metabolism: from physiology to therapeutic perspectives. Acta Physiol. 196, 81-98
8. Viollet, B., Mounier, R., Leclerc, J., Yazigi, A., Foretz, M., and Andreelli, F. (2007) Targeting AMP-activated protein kinase as a novel therapeutic approach for the treatment of metabolic disorders. Diabetes Metab. 33, 395-402
9. Boyle, J. G., Salt, I. P., and McKay, G. A. (2010) Metformin action on AMP-activated protein kinase: a translational research approach to understanding a potential new therapeutic target. Diabet. Med. 27, 1097-1106
10. Hardie, D. G. (2007) AMP-activated protein kinase as a drug target. Annu. Rev. Pharmacol. Toxicol. 47, 185-210
11. Hardie, D. G. (2011) AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev. 25, 1895-1908
12. Stephenne, X., Foretz, M., Taleux, N., van der Zon, G. C., Sokal, E., Hue, L., Viollet, B., and Guigas, B. (2011) Metformin activates AMP-activated protein kinase in primary human hepatocytes by decreasing cellular energy status. Diabetologia 54, 3101-3110
13. Viollet, B., Guigas, B., Sanz Garcia, N., Leclerc, J., Foretz, M., and Andreelli, F. (2012) Cellular and molecular mechanisms of metformin: an overview. Clin. Sci. 122, 253-270
14. Zhang, B. B., Zhou, G., and Li, C. (2009) AMPK: an emerging drug target for diabetes and the metabolic syndrome. Cell Metab. 9, 407-416
15. Zhou, G., Myers, R., Li, Y., Chen, Y., Shen, X., Fenyk-Melody, J., Wu, M., Ventre, J., Doebber, T., Fujii, N., Musi, N., Hirshman, M. F., Goodyear, L. J., and Moller, D. E. (2001) Role of AMP-activated protein kinase in mechanism of metformin action. J. Clin. Investig. 108, 1167-1174
16. Xiao, B., Sanders, M. J., Underwood, E., Heath, R., Mayer, F. V., Carmena, D., Jing, C., Walker, P. A., Eccleston, J. F., Haire, L. F., Saiu, P., Howell, S. A., Aasland, R., Martin, S. R., Carling, D., and Gamblin, S. J. (2011) Structure of mammalian AMPK and its regulation by ADP. Nature 472, 230-233
17. Arad, M., Seidman, C. E., and Seidman, J. G. (2007) AMP-activated protein kinase in the heart: role during health and disease. Circ. Res. 100, 474-488
18. Birk, J. B., and Wojtaszewski, J. F. (2006) Predominant α2/β2/γ3 AMPK activation during exercise in human skeletal muscle. J. Physiol. 577, 1021-1032
19. Cheung, P. C., Salt, I. P., Davies, S. P., Hardie, D. G., and Carling, D. (2000) Characterization of AMP-activated protein kinase γ-subunit isoforms and their role in AMP binding. Biochem. J. 346, 659-669
20. Mahlapuu, M., Johansson, C., Lindgren, K., Hjälm, G., Barnes, B. R., Krook, A., Zierath, J. R., Andersson, L., and Marklund, S. (2004) Expression profiling of the γ-subunit isoforms of AMP-activated protein kinase suggests a major role for γ3 in white skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 286, E194-E200
21. Wojtaszewski, J. F., Birk, J. B., Frøsig, C., Holten, M., Pilegaard, H., and Dela, F. (2005) 5′AMP activated protein kinase expression in human skeletal muscle: effects of strength training and type 2 diabetes. J. Physiol. 564, 563-573
22. Zanders, E. D. (2012) Overview of chemical genomics and proteomics. Methods Mol. Biol. 800, 3-10
23. Wierzba, K., Muroi, M., and Osada, H. (2011) Proteomics accelerating the identification of the target molecule of bioactive small molecules. Curr. Opin. Chem. Biol. 15, 57-65
24. Van Summeren, A., Renes, J., van Delft, J. H., Kleinjans, J. C., and Mariman, E. C. (2012) Proteomics in the search for mechanisms and biomarkers of drug-induced hepatotoxicity. Toxicol. in Vitro 26, 373-385
25. Miao, Q., Zhang, C. C., and Kast, J. (2012) Chemical proteomics and its impact on the drug discovery process. Expert Rev. Proteomics 9, 281-291
26. Drewes, G. (2012) Chemical proteomics in drug discovery. Methods Mol. Biol. 803, 15-21
27. Cravatt, B. F., Wright, A. T., and Kozarich, J. W. (2008) Activity-based protein profiling: from enzyme chemistry to proteomic chemistry. Annu. Rev. Biochem. 77, 383-414
28. Patricelli, M. P., Nomanbhoy, T. K., Wu, J., Brown, H., Zhou, D., Zhang, J., Jagannathan, S., Aban, A., Okerberg, E., Herring, C., Nordin, B., Weissig, H., Yang, Q., Lee, J. D., Gray, N. S., and Kozarich, J. W. (2011) In situ kinase profiling reveals functionally relevant properties of native kinases. Chem. Biol. 18, 699-710
29. Rajamohan, F., Harris, M. S., Frisbie, R. K., Hoth, L. R., Geoghegan, K. F., Valentine, J. J., Reyes, A. R., Landro, J. A., Qiu, X., and Kurumbail, R. G. (2010) Escherichia coli expression, purification and characterization of functional full-length recombinant α2β2γ3 heterotrimeric complex of human AMP-activated protein kinase. Protein Expr. Purif. 73, 189-197
30. Berry, M. N., and Friend, D. S. (1969) High-yield preparation of isolated rat liver parenchymal cells: a biochemical and fine structural study. J. Cell Biol. 43, 506-520
31. Hubbell, E., Liu, W. M., and Mei, R. (2002) Robust estimators for expression analysis. Bioinformatics 18, 1585-1592
32. Perkins, D. N., Pappin, D. J., Creasy, D. M., and Cottrell, J. S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567
33. Hwang, G. W., Tobita, M., Takahashi, T., Kuge, S., Kita, K., and Naganuma, A. (2010) siRNA-mediated AMPKα1 subunit gene PRKAA1 silencing enhances methylmercury toxicity in HEK293 cells. J. Toxicol. Sci. 35, 601-604
34. Hawley, S. A., Fullerton, M. D., Ross, F. A., Schertzer, J. D., Chevtzoff, C., Walker, K. J., Peggie, M. W., Zibrova, D., Green, K. A., Mustard, K. J., Kemp, B. E., Sakamoto, K., Steinberg, G. R., and Hardie, D. G. (2012) The ancient drug salicylate directly activates AMP-activated protein kinase. Science 336, 918-922
35. Patricelli, M. P., Szardenings, A. K., Liyanage, M., Nomanbhoy, T. K., Wu, M., Weissig, H., Aban, A., Chun, D., Tanner, S., and Kozarich, J. W. (2007) Functional interrogation of the kinome using nucleotide acyl phosphates. Biochemistry 46, 350-358
36. McAllister, F. E., Niepel, M., Haas, W., Huttlin, E., Sorger, P. K., and Gygi, S. P. (2013) Mass spectrometry based method to increase throughput for kinome analyses using ATP probes. Anal. Chem. 85, 4666-4674
37. Old, W. M., Meyer-Arendt, K., Aveline-Wolf, L., Pierce, K. G., Mendoza, A., Sevinsky, J. R., Resing, K. A., and Ahn, N. G. (2005) Comparison of label-free methods for quantifying human proteins by shotgun proteomics. Mol. Cell. Proteomics 4, 1487-1502
38. Balgley, B. M., Wang, W., Song, T., Fang, X., Yang, L., and Lee, C. S. (2008) Evaluation of confidence and reproducibility in quantitative proteomics performed by a capillary isoelectric focusing-based proteomic platform coupled with a spectral counting approach. Electrophoresis 29, 3047-3054
39. Braisted, J. C., Kuntumalla, S., Vogel, C., Marcotte, E. M., Rodrigues, A. R., Wang, R., Huang, S. T., Ferlanti, E. S., Saeed, A. I., Fleischmann, R. D., Peterson, S. N., and Pieper, R. (2008) The APEX quantitative proteomics tool: generating protein quantitation estimates from LC-MS/MS proteomics results. BMC Bioinformatics 9, 529
40. Cooper, B., Feng, J., and Garrett, W. M. (2010) Relative, label-free protein quantitation: spectral counting error statistics from nine replicate Mud- PIT samples. J. Am. Soc. Mass Spectrom. 21, 1534-1546
41. Piersma, S. R., Fiedler, U., Span, S., Lingnau, A., Pham, T. V., Hoffmann, S., Kubbutat, M. H., and Jiménez, C. R. (2010) Workflow comparison for label-free, quantitative secretome proteomics for cancer biomarker discovery: method evaluation, differential analysis, and verification in serum. J. Proteome Res. 9, 1913-1922
42. Borg, J., Campos, A., Diema, C.,Omeñaca, N., de Oliveira, E., Guinovart, J., and Vilaseca, M. (2011) Spectral counting assessment of protein dynamic range in cerebrospinal fluid following depletion with plasma-designed immunoaffinity columns. Clin. Proteomics 8, 6
43. Houston, N. L., Lee, D. G., Stevenson, S. E., Ladics, G. S., Bannon, G. A., McClain, S., Privalle, L., Stagg, N., Herouet-Guicheney, C., MacIntosh, S. C., and Thelen, J. J. (2011) Quantitation of soybean allergens using tandem mass spectrometry. J. Proteome Res. 10, 763-773
44. Mosley, A. L., Sardiu, M. E., Pattenden, S. G., Workman, J. L., Florens, L., and Washburn, M. P. (2011) Highly reproducible label free quantitative proteomic analysis of RNA polymerase complexes. Mol. Cell. Proteomics. 10, M110.000687
45. Neilson, K. A., Ali, N. A., Muralidharan, S., Mirzaei, M., Mariani, M., Assadourian, G., Lee, A., van Sluyter, S. C., and Haynes, P. A. (2011) Less label, more free: approaches in label-free quantitative mass spectrometry. Proteomics 11, 535-553
46. Vogel, C., and Marcotte, E. M. (2012) Label-free protein quantitation using weighted spectral counting. Methods Mol. Biol. 893, 321-341
47. Frøsig, C., Jørgensen, S. B., Hardie, D. G., Richter, E. A., and Wojtaszewski, J. F. (2004) 5′-AMP-activated protein kinase activity and protein expression are regulated by endurance training in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 286, E411-E417
48. Gruzman, A., Babai, G., and Sasson, S. (2009) Adenosine monophosphate-activated protein kinase (AMPK) as a new target for antidiabetic drugs: a review on metabolic, pharmacological and chemical considerations. Rev. Diabet. Stud. 6, 13-36
49. Cool, B., Zinker, B., Chiou, W., Kifle, L., Cao, N., Perham, M., Dickinson, R., Adler, A., Gagne, G., Iyengar, R., Zhao, G., Marsh, K., Kym, P., Jung, P., Camp, H. S., and Frevert, E. (2006) Identification and characterization of a small molecule AMPK activator that treats key components of type 2 diabetes and the metabolic syndrome. Cell Metab. 3, 403-416
50. Pang, T., Zhang, Z. S., Gu, M., Qiu, B. Y., Yu, L. F., Cao, P. R., Shao, W., Su, M. B., Li, J. Y., Nan, F. J., and Li, J. (2008) Small molecule antagonizes autoinhibition and activates AMP-activated protein kinase in cells. J. Biol. Chem. 283, 16051-16060
51. Scott, J. W., van Denderen, B. J., Jorgensen, S. B., Honeyman, J. E., Steinberg, G. R., Oakhill, J. S., Iseli, T. J., Koay, A., Gooley, P. R., Stapleton, D., and Kemp, B. E. (2008) Thienopyridone drugs are selective activators of AMP-activated protein kinase β1-containing complexes. Chem. Biol. 15, 1220-1230
52. McConell, G. K., Lee-Young, R. S., Chen, Z. P., Stepto, N. K., Huynh, N. N., Stephens, T. J., Canny, B. J., and Kemp, B. E. (2005) Short-term exercise training in humans reduces AMPK signalling during prolonged exercise independent of muscle glycogen. J. Physiol. 568, 665-676
53. Nielsen, J. N., Mustard, K. J., Graham, D. A., Yu, H., MacDonald, C. S., Pilegaard, H., Goodyear, L. J., Hardie, D. G., Richter, E. A., and Wojtaszewski, J. F. (2003) 5′-AMP-activated protein kinase activity and subunit expression in exercise-trained human skeletal muscle. J. Appl. Physiol. 94, 631-641
54. Wadley, G. D., Lee-Young, R. S., Canny, B. J., Wasuntarawat, C., Chen, Z. P., Hargreaves, M., Kemp, B. E., and McConell, G. K. (2006) Effect of exercise intensity and hypoxia on skeletal muscle AMPK signaling and substrate metabolism in humans. Am. J. Physiol. Endocrinol. Metab. 290, E694-E702
55. Yu, M., Stepto, N. K., Chibalin, A. V., Fryer, L. G., Carling, D., Krook, A., Hawley, J. A., and Zierath, J. R. (2003) Metabolic and mitogenic signal transduction in human skeletal muscle after intense cycling exercise. J. Physiol. 546, 327-335
56. Cooney, J. M., Barnett, M. P., Brewster, D., Knoch, B., McNabb, W. C., Laing, W. A., and Roy, N. C. (2012) Proteomic analysis of colon tissue from interleukin-10 gene-deficient mice fed polyunsaturated fatty acids with comparison to transcriptomic analysis. J. Proteome Res. 11, 1065-1077
57. Pinter, K., Jefferson, A., Czibik, G., Watkins, H., and Redwood, C. (2012) Subunit composition of AMPK trimers present in the cytokinetic apparatus: implications for drug target identification. Cell Cycle 11, 917-921
58. 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
59. Polekhina, G., Gupta, A., Michell, B. J., van Denderen, B., Murthy, S., Feil, S. C., Jennings, I. G., Campbell, D. J., Witters, L. A., Parker, M. W., Kemp, B. E., and Stapleton, D. (2003) AMPK β subunit targets metabolic stress sensing to glycogen. Curr. Biol. 13, 867-871
60. Viollet, B., Foretz, M., Guigas, B., Horman, S., Dentin, R., Bertrand, L., Hue, L., and Andreelli, F. (2006) Activation of AMP-activated protein kinase in the liver: a new strategy for the management of metabolic hepatic disorders. J. Physiol. 574, 41-53