Tandem reporter assay for myristoylated proteins posttranslationally (TRAMPP) identifies novel substrates for post-translational myristoylation: PKCε, a case study

FASEB Journal

Volumn 26, Issue 1, 2012, Pages 13-28

  Martin, Dale D O ^a   Ahpin, Chrisselle Y ^a   Heit, Ryan J ^a   Perinpanayagam, Maneka A ^a   Yap, Megan C ^a   Veldhoen, Richard A ^a   Goping, Ing Swie ^a   Berthiaume, Luc G ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Apoptosis; Caspases

Indexed keywords

BIM PROTEIN; CASPASE; ENHANCED GREEN FLUORESCENT PROTEIN; MARCKS PROTEIN; PLASMID VECTOR; PROTEIN MCL 1;

APOPTOSIS; ARTICLE; HELA CELL; HUMAN; MYRISTYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION;

ANIMALS; APOPTOSIS; CASPASES; CERCOPITHECUS AETHIOPS; CLONING, MOLECULAR; COS CELLS; GENES, REPORTER; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; MYRISTIC ACID; P21-ACTIVATED KINASES; PLASMIDS; PROTEIN KINASE C-EPSILON; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84855374451     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-182360     Document Type: Article

References (63)

1. Farazi, T. A., Waksman, G., and Gordon, J. I. (2001) The biology and enzymology of protein N-myristoylation. J. Biol. Chem. 276, 39501-39504
2. Boutin, J. A. (1997) Myristoylation. Cell. Signal. 9, 15-35
3. Utsumi, T., Nakano, K., Funakoshi, T., Kayano, Y., Nakao, S., Sakurai, N., Iwata, H., and Ishisaka, R. (2004) Vertical-scanning mutagenesis of amino acids in a model N-myristoylation motif reveals the major amino-terminal sequence requirements for protein N-myristoylation. Eur. J. Biochem. 271, 863-874 (Pubitemid 38250930)
4. Zha, J., Weiler, S., Oh, K. J., Wei, M. C., and Korsmeyer, S. J. (2000) Posttranslational N-myristoylation of BID as a molecular switch for targeting mitochondria and apoptosis. Science 290, 1761-1765 (Pubitemid 32004806)
5. Utsumi, T., Sakurai, N., Nakano, K., and Ishisaka, R. (2003) C-terminal 15 kDa fragment of cytoskeletal actin is posttranslationally N-myristoylated upon caspase-mediated cleavage and targeted to mitochondria. FEBS Lett. 539, 37-44 (Pubitemid 36351284)
6. Sakurai, N., and Utsumi, T. (2006) Posttranslational N-myristoylation is required for the anti-apoptotic activity of human tGelsolin, the C-terminal caspase cleavage product of human gelsolin. J. Biol. Chem. 281, 14288-14295 (Pubitemid 43848357)
7. Vilas, G. L., Corvi, M. M., Plummer, G. J., Seime, A. M., Lambkin, G. R., and Berthiaume, L. G. (2006) Posttranslational myristoylation of caspase-activated p21-activated protein kinase 2 (PAK2) potentiates late apoptotic events. Proc. Natl. Acad. Sci. U. S. A. 103, 6542-6547
8. Yap, M. C., Kostiuk, M. A., Martin, D. D., Perinpanayagam, M. A., Hak, P. G., Siddam, A., Majjigapu, J. R., Rajaiah, G., Keller, B. O., Prescher, J. A., Wu, P., Bertozzi, C. R., Falck, J. R., and Berthiaume, L. G. (2010) Rapid and selective detection of fatty acylated proteins using ω-alkynyl-fatty acids and click chemistry. J. Lipid Res. 51, 1566-1580
9. Martin, D. D., Vilas, G. L., Prescher, J. A., Rajaiah, G., Falck, J. R., Bertozzi, C. R., and Berthiaume, L. G. (2008) Rapid detection, discovery, and identification of post-translationally myristoylated proteins during apoptosis using a bio-orthogonal azidomyristate analog. FASEB J. 22, 797-806 (Pubitemid 351348132)
10. Hang, H. C., Geutjes, E. J., Grotenbreg, G., Pollington, A. M., Bijlmakers, M. J., and Ploegh, H. L. (2007) Chemical probes for the rapid detection of fatty-acylated proteins in mammalian cells. J. Am. Chem. Soc. 129, 2744-2745 (Pubitemid 46417937)
11. Fischer, U., Janicke, R. U., and Schulze-Osthoff, K. (2003) Many cuts to ruin: a comprehensive update of caspase substrates. Cell Death Differ. 10, 76-100 (Pubitemid 36511834)
12. Bologna, G., Yvon, C., Duvaud, S., and Veuthey, A. L. (2004) N-Terminal myristoylation predictions by ensembles of neural networks. Proteomics 4, 1626-1632 (Pubitemid 38738321)
13. Eisenhaber, B., Eisenhaber, F., Maurer-Stroh, S., and Neuberger, G. (2004) Prediction of sequence signals for lipid post-translational modifications: insights from case studies. Proteomics 4, 1614-1625 (Pubitemid 38738320)
14. McCabe, J. B., and Berthiaume, L. G. (1999) Functional roles for fatty acylated amino-terminal domains in subcellular localization. Mol. Biol. Cell 10, 3771-3786 (Pubitemid 29534024)
15. Matheson, A. T., Yaguchi, M., and Visentin, L. P. (1975) The conservation of amino acids in the N-terminal position of ribosomal and cytosol proteins from Escherichia coli, Bacillus stearothermophilus, and Halobacterium cutirubrum. Can. J. Biochem. 53, 1323-1327
16. Ai, H. W., Hazelwood, K. L., Davidson, M. W., and Campbell, R. E. (2008) Fluorescent protein FRET pairs for ratiometric imaging of dual biosensors. Nat. Methods 5, 401-403 (Pubitemid 351619097)
17. Tyas, L., Brophy, V. A., Pope, A., Rivett, A. J., and Tavare, J. M. (2000) Rapid caspase-3 activation during apoptosis revealed using fluorescence-resonance energy transfer. EMBO Rep. 1, 266-270
18. Charron, G., Zhang, M. M., Yount, J. S., Wilson, J., Raghavan, A. S., Shamir, E., and Hang, H. C. (2009) Robust fluorescent detection of protein fatty-acylation with chemical reporters. J. Am. Chem. Soc. 131, 4967-4975
19. Hannoush, R. N., and Arenas-Ramirez, N. (2009) Imaging the lipidome: ω-alkynyl fatty acids for detection and cellular visualization of lipid-modified proteins. ACS Chem. Biol. 4, 581-587
20. Hannoush, R. N., and Sun, J. (2010) The chemical toolbox for monitoring protein fatty acylation and prenylation. Nat. Chem. Biol. 6, 498-506
21. Akita, Y. (2002) Protein kinase C-ε (PKC-ε): its unique structure and function. J. Biochem. 132, 847-852
22. Garczarczyk, D., Toton, E., Biedermann, V., Rosivatz, E., Rechfeld, F., Rybczynska, M., and Hofmann, J. (2009) Signal transduction of constitutively active protein kinase Cε. Cell. Signal. 21, 745-752
23. Saurin, A. T., Durgan, J., Cameron, A. J., Faisal, A., Marber, M. S., and Parker, P. J. (2008) The regulated assembly of a PKCεcomplex controls the completion of cytokinesis. Nat. Cell Biol. 10, 891-901
24. Basu, A., Lu, D., Sun, B., Moor, A. N., Akkaraju, G. R., and Huang, J. (2002) Proteolytic activation of protein kinase C-ε by caspase-mediated processing and transduction of antiapoptotic signals. J. Biol. Chem. 277, 41850-41856 (Pubitemid 35257496)
25. Koriyama, H., Kouchi, Z., Umeda, T., Saido, T. C., Momoi, T., Ishiura, S., and Suzuki, K. (1999) Proteolytic activation of protein kinase Cδ and ε by caspase-3 in U937 cells during chemotherapeutic agent-induced apoptosis. Cell. Signal. 11, 831-838 (Pubitemid 29507492)
26. Leverrier, S., Vallentin, A., and Joubert, D. (2002) Positive feedback of protein kinase C proteolytic activation during apoptosis. Biochem. J. 368, 905-913 (Pubitemid 36042693)
27. Wyllie, A. H. (1997) Apoptosis: an overview. Br. Med. Bull. 53, 451-465
28. Wyllie, A. H., Bellamy, C. O., Bubb, V. J., Clarke, A. R., Corbet, S., Curtis, L., Harrison, D. J., Hooper, M. L., Toft, N., Webb, S., and Bird, C. C. (1999) Apoptosis and carcinogenesis. Br. J. Cancer 80(Suppl. 1), 34-37 (Pubitemid 29389605)
29. Shaner, N. C., Steinbach, P. A., and Tsien, R. Y. (2005) A guide to choosing fluorescent proteins. Nat. Methods 2, 905-909 (Pubitemid 43108726)
30. Dix, M. M., Simon, G. M., and Cravatt, B. F. (2008) Global mapping of the topography and magnitude of proteolytic events in apoptosis. Cell 134, 679-691
31. Luthi, A. U., and Martin, S. J. (2007) The CASBAH: a searchable database of caspase substrates. Cell Death Differ. 14, 641-650 (Pubitemid 46444502)
32. Mahrus, S., Trinidad, J. C., Barkan, D. T., Sali, A., Burlingame, A. L., and Wells, J. A. (2008) Global sequencing of proteolytic cleavage sites in apoptosis by specific labeling of protein N termini. Cell 134, 866-876
33. Martin, D. D., Beauchamp, E., and Berthiaume, L. G. (2010) Post-translational myristoylation: fat matters in cellular life and death. Biochimie 93, 18-31
34. Xu, T. R., He, G., and Rumsby, M. G. (2009) Adenosine triggers the nuclear translocation of protein kinase Cε in H9c2 cardiomyoblasts with the loss of phosphorylation at Ser729. J. Cell. Biochem. 106, 633-642
35. Sallese, M., Pulvirenti, T., and Luini, A. (2006) The physiology of membrane transport and endomembrane-based signalling. EMBO J. 25, 2663-2673 (Pubitemid 43980375)
36. Kronebusch, P. J., and Singer, S. J. (1987) The microtubuleorganizing complex and the Golgi apparatus are co-localized around the entire nuclear envelope of interphase cardiac myocytes. J. Cell Sci. 88(Pt. 1), 25-34
37. Guasch, R. M., Guerri, C., and O'Connor, J. E. (1993) Flow cytometric analysis of concanavalin A binding to isolated Golgi fractions from rat liver. Exp. Cell Res. 207, 136-141 (Pubitemid 23192173)
38. Shnyder, S. D., and Hubbard, M. J. (2002) ERp29 is a ubiquitous resident of the endoplasmic reticulum with a distinct role in secretory protein production. J. Histochem. Cytochem. 50, 557-566 (Pubitemid 34250595)
39. Luciano, F., Jacquel, A., Colosetti, P., Herrant, M., Cagnol, S., Pages, G., and Auberger, P. (2003) Phosphorylation of Bim-EL by Erk1/2 on serine 69 promotes its degradation via the proteasome pathway and regulates its proapoptotic function. Oncogene 22, 6785-6793 (Pubitemid 37372218)
40. Tan, Y., Ruan, H., Demeter, M. R., and Comb, M. J. (1999) p90RSK blocks bad-mediated cell death via a protein kinase C-dependent pathway. J. Biol. Chem. 274, 34859-34867 (Pubitemid 129509532)
41. Ducker, C. E., Upson, J. J., French, K. J., and Smith, C. D. (2005) Two N-myristoyltransferase isozymes play unique roles in protein myristoylation, proliferation, and apoptosis. Mol. Cancer Res. 3, 463-476 (Pubitemid 41232608)
42. Giang, D. K., and Cravatt, B. F. (1998) A second mammalian N-myristoyltransferase. J. Biol. Chem. 273, 6595-6598 (Pubitemid 28160313)
43. Selvakumar, P., Smith-Windsor, E., Bonham, K., and Sharma, R. K. (2006) N-Myristoyltransferase 2 expression in human colon cancer: cross-talk between the calpain and caspase system. FEBS Lett. 580, 2021-2026
44. Lane, J. D., Vergnolle, M. A., Woodman, P. G., and Allan, V. J. (2001) Apoptotic cleavage of cytoplasmic dynein intermediate chain and p150Glued stops dynein-dependent membrane motility. J. Cell Biol. 153, 1415-1426 (Pubitemid 34286126)
45. Puthalakath, H., Huang, D. C., O'Reilly, L. A., King, S. M., and Strasser, A. (1999) The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol. Cell 3, 287-296 (Pubitemid 29290669)
46. Aslan, J. E., and Thomas, G. (2009) Death by committee: organellar trafficking and communication in apoptosis. Traffic 10, 1390-1404
47. Weng, C., Li, Y., Xu, D., Shi, Y., and Tang, H. (2005) Specific cleavage of Mcl-1 by caspase-3 in tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis in Jurkat leukemia T cells. J. Biol. Chem. 280, 10491-10500 (Pubitemid 40395908)
48. Koya, R. C., Fujita, H., Shimizu, S., Ohtsu, M., Takimoto, M., Tsujimoto, Y., and Kuzumaki, N. (2000) Gelsolin inhibits apoptosis by blocking mitochondrial membrane potential loss and cytochrome c release. J. Biol. Chem. 275, 15343-15349 (Pubitemid 30337262)
49. Kusano, H., Shimizu, S., Koya, R. C., Fujita, H., Kamada, S., Kuzumaki, N., and Tsujimoto, Y. (2000) Human gelsolin prevents apoptosis by inhibiting apoptotic mitochondrial changes via closing VDAC. Oncogene 19, 4807-4814
50. Wright, M. M., Howe, A. G., and Zaremberg, V. (2004) Cell membranes and apoptosis: role of cardiolipin, phosphatidylcholine, and anticancer lipid analogues. Biochem. Cell Biol. 82, 18-26 (Pubitemid 38580871)
51. Yim, H., Hwang, I. S., Choi, J. S., Chun, K. H., Jin, Y. H., Ham, Y. M., Lee, K. Y., and Lee, S. K. (2006) Cleavage of Cdc6 by caspase-3 promotes ATM/ATR kinase-mediated apoptosis of HeLa cells. J. Cell Biol. 174, 77-88 (Pubitemid 43992898)
52. Yim, H., Jin, Y. H., Park, B. D., Choi, H. J., and Lee, S. K. (2003) Caspase-3-mediated cleavage of Cdc6 induces nuclear localization of p49-truncated Cdc6 and apoptosis. Mol. Biol. Cell 14, 4250-4259 (Pubitemid 37186325)
53. Chen, H. J., Lin, C. M., Lin, C. S., Perez-Olle, R., Leung, C. L., and Liem, R. K. (2006) The role of microtubule actin cross-linking factor 1 (MACF1) in the Wnt signaling pathway. Genes Dev. 20, 1933-1945 (Pubitemid 44079330)
54. Fryer, J. D., and Zoghbi, H. Y. (2006) Huntingtin's critical cleavage. Nat. Neurosci. 9, 1088-1089 (Pubitemid 44306298)
55. Graham, R. K., Deng, Y., Slow, E. J., Haigh, B., Bissada, N., Lu, G., Pearson, J., Shehadeh, J., Bertram, L., Murphy, Z., Warby, S. C., Doty, C. N., Roy, S., Wellington, C. L., Leavitt, B. R., Raymond, L. A., Nicholson, D. W., and Hayden, M. R. (2006) Cleavage at the caspase-6 site is required for neuronal dysfunction and degeneration due to mutant huntingtin. Cell 125, 1179-1191 (Pubitemid 43866195)
56. Wellington, C. L., Ellerby, L. M., Gutekunst, C. A., Rogers, D., Warby, S., Graham, R. K., Loubser, O., van Raamsdonk, J., Singaraja, R., Yang, Y. Z., Gafni, J., Bredesen, D., Hersch, S. M., Leavitt, B. R., Roy, S., Nicholson, D. W., and Hayden, M. R. (2002) Caspase cleavage of mutant huntingtin precedes neurodegeneration in Huntington's disease. J. Neurosci. 22, 7862-7872 (Pubitemid 35379091)
57. Kim, Y. J., Yi, Y., Sapp, E., Wang, Y., Cuiffo, B., Kegel, K. B., Qin, Z. H., Aronin, N., and DiFiglia, M. (2001) Caspase 3-cleaved N-terminal fragments of wild-type and mutant huntingtin are present in normal and Huntington's disease brains, associate with membranes, and undergo calpain-dependent proteolysis. Proc. Natl. Acad. Sci. U. S. A. 98, 12784-12789 (Pubitemid 33020022)
58. Ehrnhoefer, D. E., Sutton, L., and Hayden, M. R. (2011) Small changes, big impact: posttranslational modifications and function of huntingtin in Huntington disease. [E-pub ahead of print] Neuroscientist doi:10.1177/ 1073858410390378
59. Dasgupta, S., Bhattacharya, S., Maitra, S., Pal, D., Majumdar, S. S., and Datta, A. (2011) Mechanism of lipid induced insulin resistance: activated PKCε is a key regulator. Biochim. Biophys. Acta 1812, 495-506
60. O'Reilly, L. A., Kruse, E. A., Puthalakath, H., Kelly, P. N., Kaufmann, T., Huang, D. C., and Strasser, A. (2009) MEK/ERK-mediated phosphorylation of Bim is required to ensure survival of T and B lymphocytes during mitogenic stimulation. J. Immunol. 183, 261-269
61. Ley, R., Ewings, K. E., Hadfield, K., and Cook, S. J. (2005) Regulatory phosphorylation of Bim: sorting out the ERK from the JNK. Cell Death Differ. 12, 1008-1014 (Pubitemid 41065418)
62. Lei, K., and Davis, R. J. (2003) JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc. Natl. Acad. Sci. U. S. A. 100, 2432-2437 (Pubitemid 36297516)
63. Putcha, G. V., Le, S., Frank, S., Besirli, C. G., Clark, K., Chu, B., Alix, S., Youle, R. J., LaMarche, A., Maroney, A. C., and Johnson, E. M., Jr. (2003) JNK-mediated BIM phosphorylation potentiates BAX-dependent apoptosis. Neuron 38, 899-914 (Pubitemid 36782382)