Identification of AMPK Phosphorylation Sites Reveals a Network of Proteins Involved in Cell Invasion and Facilitates Large-Scale Substrate Prediction

Cell Metabolism

Volumn 22, Issue 5, 2015, Pages 907-921

  Schaffer, Bethany E ^a   Levin, Rebecca S ^b   Hertz, Nicholas T ^b   Maures, Travis J ^a   Schoof, Michael L ^a   Hollstein, Pablo E ^c   Benayoun, Bérénice A ^a   Banko, Max R ^a   Shaw, Reuben J ^c   Shokat, Kevan M ^b   Brunet, Anne ^a,d  

^a STANFORD UNIVERSITY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^d Glenn Laboratories for the Biology of Aging   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR NET1A; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; UNCLASSIFIED DRUG; NET1 PROTEIN, HUMAN; ONCOPROTEIN; PEPTIDE;

AGING; ARTICLE; CANCER CELL LINE; CELL ADHESION; CELL INVASION; CELL MOTILITY; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; PREDICTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN MOTIF; ANIMAL; CELL MOTION; CHEMISTRY; ENZYME SPECIFICITY; EXTRACELLULAR MATRIX; GENETICS; METABOLISM; PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SINGLE CELL ANALYSIS;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CELL ADHESION; CELL MOVEMENT; EXTRACELLULAR MATRIX; HUMANS; ONCOGENE PROTEINS; PEPTIDES; PHOSPHORYLATION; PROTEIN INTERACTION MAPS; SINGLE-CELL ANALYSIS; SUBSTRATE SPECIFICITY;

EID: 84948425160     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2015.09.009     Document Type: Article

References (61)

1. Amato, S., Liu, X., Zheng, B., Cantley, L., Rakic, P., and Man, H. Y. (2011). AMP-activated protein kinase regulates neuronal polarization by interfering with PI 3-kinase localization. Science 332, 247-251.
2. Andersson, U., Filipsson, K., Abbott, C. R., Woods, A., Smith, K., Bloom, S. R., Carling, D., and Small, C. J. (2004). AMP-activated protein kinase plays a role in the control of food intake. J. Biol. Chem. 279, 12005-12008.
3. Apfeld, J., O'Connor, G., McDonagh, T., DiStefano, P. S., and Curtis, R. (2004). The AMP-activated protein kinase AAK-2 links energy levels and insulin-like signals to lifespan in C. elegans. Genes Dev. 18, 3004-3009.
4. Bailey, T. L., Boden, M., Buske, F. A., Frith, M., Grant, C. E., Clementi, L., Ren, J., Li, W. W., and Noble, W. S. (2009). MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37, W202-W208.
5. Banko, M. R., Allen, J. J., Schaffer, B. E., Wilker, E. W., Tsou, P., White, J. L., Villén, J., Wang, B., Kim, S. R., Sakamoto, K., et al. (2011). Chemical genetic screen for AMPKa2 substrates uncovers a network of proteins involved in mitosis. Mol. Cell 44, 878-892.
6. Bettencourt-Dias, M., Giet, R., Sinka, R., Mazumdar, A., Lock, W. G., Balloux, F., Zafiropoulos, P. J., Yamaguchi, S., Winter, S., Carthew, R. W., et al. (2004). Genome-wide survey of protein kinases required for cell cycle progression. Nature 432, 980-987.
7. Blethrow, J. D., Glavy, J. S., Morgan, D. O., and Shokat, K. M. (2008). Covalent capture of kinase-specific phosphopeptides reveals Cdk1-cyclin B substrates. Proc. Natl. Acad. Sci. USA 105, 1442-1447.
8. Bowden, E. T., Coopman, P. J., and Mueller, S. C. (2001). Invadopodia: unique methods for measurement of extracellular matrix degradation in vitro. Methods Cell Biol. 63, 613-627.
9. Burkewitz, K., Zhang, Y., and Mair, W. B. (2014). AMPK at the nexus of energetics and aging. Cell Metab. 20, 10-25.
10. Carr, H. S., Zuo, Y., Oh, W., and Frost, J. A. (2013). Regulation of focal adhesion kinase activation, breast cancer cell motility, and amoeboid invasion by the RhoA guanine nucleotide exchange factor Net1. Mol. Cell. Biol. 33, 2773-2786.
11. Chan, K. T., Cortesio, C. L., and Huttenlocher, A. (2009). FAK alters invadopodia and focal adhesion composition and dynamics to regulate breast cancer invasion. J. Cell Biol. 185, 357-370.
12. Chen, S., Murphy, J., Toth, R., Campbell, D. G., Morrice, N. A., and Mackintosh, C. (2008). Complementary regulation of TBC1D1 and AS160 by growth factors, insulin and AMPK activators. Biochem. J. 409, 449-459.
13. Cool, B., Zinker, B., Chiou, W., Kifle, L., Cao, N., Perham, M., Dickinson, R., Adler, A., Gagne, G., Iyengar, R., et al. (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.
14. Crooks, G. E., Hon, G., Chandonia, J. M., and Brenner, S. E. (2004). WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190.
15. Dale, S., Wilson, W. A., Edelman, A. M., and Hardie, D. G. (1995). Similar substrate recognition motifs for mammalian AMP-activated protein kinase, higher plant HMG-CoA reductase kinase-A, yeast SNF1, and mammalian calmodulin-dependent protein kinase I. FEBS Lett. 361, 191-195.
16. Davies, S. P., Sim, A. T., and Hardie, D. G. (1990). Location and function of three sites phosphorylated on rat acetyl-CoA carboxylase by the AMP-activated protein kinase. Eur. J. Biochem. 187, 183-190.
17. Ducharme, N. A., Hales, C. M., Lapierre, L. A., Ham, A. J., Oztan, A., Apodaca, G., and Goldenring, J. R. (2006). MARK2/EMK1/Par-1Balpha phosphorylation of Rab11-family interacting protein 2 is necessary for the timely establishment of polarity in Madin-Darby canine kidney cells. Mol. Biol. Cell 17, 3625-3637.
18. Ducommun, S., Deak, M., Sumpton, D., Ford, R. J., Núņez Galindo, A., Kussmann, M., Viollet, B., Steinberg, G. R., Foretz, M., Dayon, L., et al. (2015). Motif affinity and mass spectrometry proteomic approach for the discovery of cellular AMPK targets: identification of mitochondrial fission factor as a new AMPK substrate. Cell. Signal. 27, 978-988.
19. Eckert, M. A., Lwin, T. M., Chang, A. T., Kim, J., Danis, E., Ohno-Machado, L., and Yang, J. (2011). Twist1-induced invadopodia formation promotes tumor metastasis. Cancer Cell 19, 372-386.
20. Egan, D. F., Shackelford, D. B., Mihaylova, M. M., Gelino, S., Kohnz, R. A., Mair, W., Vasquez, D. S., Joshi, A., Gwinn, D. M., Taylor, R., et al. (2011). Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331, 456-461.
21. Goodwin, J. M., Svensson, R. U., Lou, H. J., Winslow, M. M., Turk, B. E., and Shaw, R. J. (2014). An AMPK-independent signaling pathway downstream of the LKB1 tumor suppressor controls Snail1 and metastatic potential. Mol. Cell 55, 436-450.
22. Grant, C. E., Bailey, T. L., and Noble, W. S. (2011). FIMO: scanning for occurrences of a given motif. Bioinformatics 27, 1017-1018.
23. Greer, E. L., Dowlatshahi, D., Banko, M. R., Villen, J., Hoang, K., Blanchard, D., Gygi, S. P., and Brunet, A. (2007). An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr. Biol. 17, 1646-1656.
24. Gwinn, D. M., Shackelford, D. B., Egan, D. F., Mihaylova, M. M., Mery, A., Vasquez, D. S., Turk, B. E., and Shaw, R. J. (2008). AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol. Cell 30, 214-226.
25. Hardie, D. G., and Ashford, M. L. (2014). AMPK: regulating energy balance at the cellular and whole body levels. Physiology (Bethesda) 29, 99-107.
26. Hardie, D. G., and Carling, D. (1997). The AMP-activated protein kinase-fuel gauge of the mammalian cell? Eur. J. Biochem. 246, 259-273.
27. 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., et al. (2012). The ancient drug salicylate directly activates AMP-activated protein kinase. Science 336, 918-922.
28. Hengeveld, R. C., Hertz, N. T., Vromans, M. J., Zhang, C., Burlingame, A. L., Shokat, K. M., and Lens, S. M. (2012). Development of a chemical genetic approach for human aurora B kinase identifies novel substrates of the chromosomal passenger complex. Mol. Cell. Proteomics 11, 47-59.
29. Hertz, N. T., Wang, B. T., Allen, J. J., Zhang, C., Dar, A. C., Burlingame, A. L., and Shokat, K. M. (2010). Chemical genetic approach for kinase-substrate mapping by covalent capture of thiophosphopeptides and analysis by mass spectrometry. Curr. Protoc. Chem. Biol. 2, 15-36.
30. Johnson, C., Tinti, M., Wood, N. T., Campbell, D. G., Toth, R., Dubois, F., Geraghty, K. M., Wong, B. H., Brown, L. J., Tyler, J., et al. (2011). Visualization and biochemical analyses of the emerging mammalian 14-3-3-phosphoproteome. Mol. Cell. Proteomics 10, 005751.
31. Kato, K., Ogura, T., Kishimoto, A., Minegishi, Y., Nakajima, N., Miyazaki, M., and Esumi, H. (2002). Critical roles of AMP-activated protein kinase in constitutive tolerance of cancer cells to nutrient deprivation and tumor formation. Oncogene 21, 6082-6090.
32. Kudo, N., Barr, A. J., Barr, R. L., Desai, S., and Lopaschuk, G. D. (1995). High rates of fatty acid oxidation during reperfusion of ischemic hearts are associated with a decrease in malonyl-CoA levels due to an increase in 50-AMP-activated protein kinase inhibition of acetyl-CoA carboxylase. J. Biol. Chem. 270, 17513-17520.
33. Kurth-Kraczek, E. J., Hirshman, M. F., Goodyear, L. J., and Winder, W. W. (1999). 50 AMP-activated protein kinase activation causes GLUT4 translocation in skeletal muscle. Diabetes 48, 1667-1671.
34. Lee, J. H., Koh, H., Kim, M., Kim, Y., Lee, S. Y., Karess, R. E., Lee, S. H., Shong, M., Kim, J. M., Kim, J., and Chung, J. (2007). Energy-dependent regulation of cell structure by AMP-activated protein kinase. Nature 447, 1017-1020.
35. Liang, J., and Mills, G. B. (2013). AMPK: a contextual oncogene or tumor suppressor? Cancer Res. 73, 2929-2935.
36. Liu, D., Shi, M., Duan, C., Chen, H., Hu, Y., Yang, Z., Duan, H., and Guo, N. (2013). Downregulation of Erbin in Her2-overexpressing breast cancer cells promotes cell migration and induces trastuzumab resistance. Mol. Immunol. 56, 104-112.
37. Mair, W., Morantte, I., Rodrigues, A. P., Manning, G., Montminy, M., Shaw, R. J., and Dillin, A. (2011). Lifespan extension induced by AMPK and calcineurin is mediated by CRTC-1 and CREB. Nature 470, 404-408.
38. Marin, T. L., Gongol, B., Martin, M., King, S. J., Smith, L., Johnson, D. A., Subramaniam, S., Chien, S., and Shyy, J. Y. (2015). Identification of AMP-activated protein kinase targets by a consensus sequence search of the proteome. BMC Syst. Biol. 9, 13.
39. Mertins, P., Yang, F., Liu, T., Mani, D. R., Petyuk, V. A., Gillette, M. A., Clauser, K. R., Qiao, J. W., Gritsenko, M. A., Moore, R. J., et al. (2014). Ischemia in tumors induces early and sustained phosphorylation changes in stress kinase pathways but does not affect global protein levels. Mol. Cell. Proteomics 13, 1690-1704.
40. Nakano, A., Kato, H., Watanabe, T., Min, K. D., Yamazaki, S., Asano, Y., Seguchi, O., Higo, S., Shintani, Y., Asanuma, H., et al. (2010). AMPK controls the speed of microtubule polymerization and directional cell migration through CLIP-170 phosphorylation. Nat. Cell Biol. 12, 583-590.
41. Obenauer, J. C., Cantley, L. C., and Yaffe, M. B. (2003). Scansite 2. 0: Proteomewide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31, 3635-3641.
42. Olsen, J. V., Vermeulen, M., Santamaria, A., Kumar, C., Miller, M. L., Jensen, L. J., Gnad, F., Cox, J., Jensen, T. S., Nigg, E. A., et al. (2010). Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 3, ra3.
43. Russell, R. R., 3rd, Li, J., Coven, D. L., Pypaert, M., Zechner, C., Palmeri, M., Giordano, F. J., Mu, J., Birnbaum, M. J., and Young, L. H. (2004). AMP-activated protein kinase mediates ischemic glucose uptake and prevents postischemic cardiac dysfunction, apoptosis, and injury. J. Clin. Invest. 114, 495-503.
44. Schneider, T. D., and Stephens, R. M. (1990). Sequence logos: a new way to display consensus sequences. Nucleic Acids Res. 18, 6097-6100.
45. Scott, J. W., Norman, D. G., Hawley, S. A., Kontogiannis, L., and Hardie, D. G. (2002). Protein kinase substrate recognition studied using the recombinant catalytic domain of AMP-activated protein kinase and a model substrate. J. Mol. Biol. 317, 309-323.
46. Scott, K. E., Wheeler, F. B., Davis, A. L., Thomas, M. J., Ntambi, J. M., Seals, D. F., and Kridel, S. J. (2012). Metabolic regulation of invadopodia and invasion by acetyl-CoA carboxylase 1 and de novo lipogenesis. PLoS ONE 7, e29761.
47. Seals, D. F., Azucena, E. F., Jr., Pass, I., Tesfay, L., Gordon, R., Woodrow, M., Resau, J. H., and Courtneidge, S. A. (2005). The adaptor protein Tks5/Fish is required for podosome formation and function, and for the protease-driven invasion of cancer cells. Cancer Cell 7, 155-165.
48. Shah, K., Liu, Y., Deirmengian, C., and Shokat, K. M. (1997). Engineering unnatural nucleotide specificity for Rous sarcoma virus tyrosine kinase to uniquely label its direct substrates. Proc. Natl. Acad. Sci. USA 94, 3565-3570.
49. Sim, A. T., and Hardie, D. G. (1988). The low activity of acetyl-CoA carboxylase in basal and glucagon-stimulated hepatocytes is due to phosphorylation by the AMP-activated protein kinase and not cyclic AMP-dependent protein kinase. FEBS Lett. 233, 294-298.
50. Simonsen, A., Birkeland, H. C., Gillooly, D. J., Mizushima, N., Kuma, A., Yoshimori, T., Slagsvold, T., Brech, A., and Stenmark, H. (2004). Alfy, a novel FYVE-domain-containing protein associated with protein granules and autophagic membranes. J. Cell Sci. 117, 4239-4251.
51. Towler, M. C., and Hardie, D. G. (2007). AMP-activated protein kinase in metabolic control and insulin signaling. Circ. Res. 100, 328-341.
52. Vazquez-Martin, A., Oliveras-Ferraros, C., and Menendez, J. A. (2009). The active form of the metabolic sensor: AMP-activated protein kinase (AMPK) directly binds the mitotic apparatus and travels from centrosomes to the spindle midzone during mitosis and cytokinesis. Cell Cycle 8, 2385-2398.
53. Wang, Z., Wilson, W. A., Fujino, M. A., and Roach, P. J. (2001). Antagonistic controls of autophagy and glycogen accumulation by Snf1p, the yeast homolog of AMP-activated protein kinase, and the cyclin-dependent kinase Pho85p. Mol. Cell. Biol. 21, 5742-5752.
54. Winder, W. W., and Hardie, D. G. (1999). AMP-activated protein kinase, a metabolic master switch: possible roles in type 2 diabetes. Am. J. Physiol. 277, E1-E10.
55. Xiang, X., Saha, A. K., Wen, R., Ruderman, N. B., and Luo, Z. (2004). AMP-activated protein kinase activators can inhibit the growth of prostate cancer cells by multiple mechanisms. Biochem. Biophys. Res. Commun. 321, 161-167.
56. Yuan, J., Ossendorf, C., Szatkowski, J. P., Bronk, J. T., Maran, A., Yaszemski, M., Bolander, M. E., Sarkar, G., and Fuchs, B. (2009). Osteoblastic and osteolytic human osteosarcomas can be studied with a new xenograft mouse model producing spontaneous metastases. Cancer Invest. 27, 435-442.
57. Zadra, G., Photopoulos, C., Tyekucheva, S., Heidari, P., Weng, Q. P., Fedele, G., Liu, H., Scaglia, N., Priolo, C., Sicinska, E., et al. (2014). A novel direct activator of AMPK inhibits prostate cancer growth by blocking lipogenesis. EMBO Mol. Med. 6, 519-538.
58. Zhang, H., Zha, X., Tan, Y., Hornbeck, P. V., Mastrangelo, A. J., Alessi, D. R., Polakiewicz, R. D., and Comb, M. J. (2002). Phosphoprotein analysis using antibodies broadly reactive against phosphorylated motifs. J. Biol. Chem. 277, 39379-39387.
59. Zhang, L., Li, J., Young, L. H., and Caplan, M. J. (2006). AMP-activated protein kinase regulates the assembly of epithelial tight junctions. Proc. Natl. Acad. Sci. USA 103, 17272-17277.
60. Zheng, B., and Cantley, L. C. (2007). Regulation of epithelial tight junction assembly and disassembly by AMP-activated protein kinase. Proc. Natl. Acad. Sci. USA 104, 819-822.
61. Zhou, G., Myers, R., Li, Y., Chen, Y., Shen, X., Fenyk-Melody, J., Wu, M., Ventre, J., Doebber, T., Fujii, N., et al. (2001). Role of AMP-activated protein kinase in mechanism of metformin action. J. Clin. Invest. 108, 1167-1174.