Identification of a novel sequence motif recognized by the ankyrin repeat domain of zDHHC17/13 S-acyltransferases

Journal of Biological Chemistry

Volumn 290, Issue 36, 2015, Pages 21939-21950

  Lemonidis, Kimon ^a   Sanchez Perez, Maria C ^a   Chamberlain, Luke H ^a  

^a UNIVERSITY OF STRATHCLYDE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLATION; AMINO ACIDS; ENZYMES; MAMMALS; SUBSTRATES;

ACYLTRANSFERASES; ANKYRIN-REPEAT DOMAIN; BINDING SEQUENCE; HUNTINGTON'S DISEASE; INDEPENDENT FUNCTIONS; MICROTUBULE ASSOCIATED PROTEIN; NEURONAL FUNCTION; POST-TRANSLATIONAL MODIFICATIONS;

PROTEINS;

ACYLTRANSFERASE; ANKYRIN; CYSTEINE STRING PROTEIN; CYTOPLASMIC LINKER PROTEIN 3; HUNTINGTIN; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 6; PROTEIN SNAP23; PROTEIN SNAP25; PROTEIN ZDHHC13; PROTEIN ZDHHC17; UNCLASSIFIED DRUG; HEAT SHOCK PROTEIN 40; HIP14 PROTEIN, MOUSE; HTT PROTEIN, HUMAN; MAP6 PROTEIN, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; NERVE PROTEIN; PROTEIN BINDING; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; ZDHHC13 PROTEIN, MOUSE; ZINC FINGER PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOLECULAR CLONING; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE; STRUCTURE ANALYSIS; ACYLATION; ANIMAL; BINDING SITE; BOVINE; CLASSIFICATION; GENETICS; HEK293 CELL LINE; METABOLISM; MOLECULAR GENETICS; MUTATION; PHYLOGENY; RAT; SEQUENCE HOMOLOGY; WESTERN BLOTTING;

ACYLATION; ACYLTRANSFERASES; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; ANKYRIN REPEAT; BINDING SITES; BLOTTING, WESTERN; CATTLE; HEK293 CELLS; HSP40 HEAT-SHOCK PROTEINS; HUMANS; HUNTINGTIN PROTEIN; MEMBRANE PROTEINS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; NERVE TISSUE PROTEINS; PHYLOGENY; PROTEIN BINDING; RATS; SEQUENCE HOMOLOGY, AMINO ACID; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25; ZINC FINGERS;

EID: 84941282873     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.657668     Document Type: Article

References (72)

1. Linder, M. E., and Jennings, B. C. (2013) Mechanism and function of DHHC S-acyltransferases. Biochem. Soc. Trans. 41, 29-34
2. Tom, C. T., and Martin, B. R. (2013) Fat chance! Getting a grip on a slippery modification. ACS Chem. Biol. 8, 46-57
3. Blaskovic, S., Adibekian, A., Blanc, M., and van der Goot, G. F. (2014) Mechanistic effects of protein palmitoylation and the cellular consequences thereof. Chem. Phys. Lipids 180, 44-52
4. Fukata, M., Fukata, Y., Adesnik, H., Nicoll, R. A., and Bredt, D. S. (2004) Identification of PSD-95 palmitoylating enzymes. Neuron 44, 987-996
5. Bannan, B. A., Van Etten, J., Kohler, J. A., Tsoi, Y., Hansen, N. M., Sigmon, S., Fowler, E., Buff, H., Williams, T. S., Ault, J. G., Glaser, R. L., and Korey, C. A. (2008) The Drosophila protein palmitoylome: characterizing palmitoyl- thioesterases and DHHC palmitoyl-transferases. Fly (Austin) 2, 198-214
6. Edmonds, M. J., and Morgan, A. (2014) A systematic analysis of protein palmitoylation in Caenorhabditis elegans. BMC Genomics 15, 841
7. Frénal, K., Tay, C. L., Mueller, C., Bushell, E. S., Jia, Y., Graindorge, A., Billker, O., Rayner, J. C., and Soldati-Favre, D. (2013) Global analysis of apicomplexan protein S-acyl transferases reveals an enzyme essential for invasion. Traffic 14, 895-911
8. Roth, A. F., Wan, J., Bailey, A. O., Sun, B., Kuchar, J. A., Green, W. N., Phinney, B. S., Yates, J. R., 3rd, and Davis, N. G. (2006) Global analysis of protein palmitoylation in yeast. Cell 125, 1003-1013
9. Yang, G., and Cynader, M. S. (2011) Palmitoyl acyltransferase zD17 mediates neuronal responses in acute ischemic brain injury by regulating JNK activation in a signaling module. J. Neurosci. 31, 11980-11991
10. Harada, T., Matsuzaki, O., Hayashi, H., Sugano, S., Matsuda, A., and Nishida, E. (2003) AKRL1 and AKRL2 activate the JNK pathway. Genes Cells 8, 493-500
11. Hemsley, P. A., and Grierson, C. S. (2011) The ankyrin repeats andDHHC S-acyl transferase domain of AKR1 act independently to regulate switching from vegetative to mating states in yeast. PLoS One 6, e28799
12. Huang, K., Yanai, A., Kang, R., Arstikaitis, P., Singaraja, R. R., Metzler, M., Mullard, A., Haigh, B., Gauthier-Campbell, C., Gutekunst, C.-A., Hayden, M. R., and El-Husseini, A. (2004) Huntingtin-interacting protein HIP14 is a palmitoyl transferase involved in palmitoylation and trafficking of multiple neuronal proteins. Neuron 44, 977-986
13. Gao, T., Collins, R. E., Horton, J. R., Zhang, X., Zhang, R., Dhayalan, A., Tamas, R., Jeltsch, A., and Cheng, X. (2009) The ankyrin repeat domain of Huntingtin interacting protein 14 contains a surface aromatic cage, a potential site for methyl-lysine binding. Proteins 76, 772-777
14. Singaraja, R. R., Huang, K., Sanders, S. S., Milnerwood, A. J., Hines, R., Lerch, J. P., Franciosi, S., Drisdel, R. C., Vaid, K., Young, F. B., Doty, C., Wan, J., Bissada, N., Henkelman, R. M., Green, W. N., Davis, N. G., Raymond, L. A., and Hayden, M. R. (2011) Altered palmitoylation and neuropathological deficits in mice lacking HIP14. Hum. Mol. Genet. 20, 3899-3909
15. Sutton, L. M., Sanders, S. S., Butland, S. L., Singaraja, R. R., Franciosi, S., Southwell, A. L., Doty, C. N., Schmidt, M. E., Mui, K. K., Kovalik, V., Young, F. B., Zhang, W., and Hayden, M. R. (2013) Hip14l-deficient mice develop neuropathological and behavioural features of Huntington disease. Hum. Mol. Genet. 22, 452-465
16. Milnerwood, A. J., Parsons, M. P., Young, F. B., Singaraja, R. R., Franciosi, S., Volta, M., Bergeron, S., Hayden, M. R., and Raymond, L. A. (2013) Memory and synaptic deficits in Hip14/DHHC17 knockout mice. Proc. Natl. Acad. Sci. U.S.A. 110, 20296-20301
17. Young, F. B., Butland, S. L., Sanders, S. S., Sutton, L. M., and Hayden, M. R. (2012) Putting proteins in their place: Palmitoylation in Huntington disease and other neuropsychiatric diseases. Prog. Neurobiol. 97, 220-238
18. Huang, K., Sanders, S., Singaraja, R., Orban, P., Cijsouw, T., Arstikaitis, P., Yanai, A., Hayden, M. R., and El-Husseini, A. (2009) Neuronal palmitoyl acyl transferases exhibit distinct substrate specificity. FASEB J. 23, 2605-2615
19. Huang, K., Sanders, S. S., Kang, R., Carroll, J. B., Sutton, L., Wan, J., Singaraja, R., Young, F. B., Liu, L., El-Husseini, A., Davis, N. G., and Hayden, M. R. (2011) Wild-type HTT modulates the enzymatic activity of the neuronal palmitoyl transferase HIP14. Hum. Mol. Genet. 20, 3356-3365
20. Yang, G., Zhou, X., Zhu, J., Liu, R., Zhang, S., Coquinco, A., Chen, Y., Wen, Y., Kojic, L., Jia, W., and Cynader, M. S. (2013) JNK3 couples the neuronal stress response to inhibition of secretory trafficking. Sci. Signal. 6, ra57
21. Lemonidis, K., Gorleku, O. A., Sanchez-Perez, M. C., Grefen, C., and Chamberlain, L. H. (2014) The Golgi S-acylation machinery comprises zDHHC enzymes with major differences in substrate affinity and S-acylation activity. Mol. Biol. Cell 25, 3870-3883
22. Sanders, S. S., Mui, K. K., Sutton, L. M., and Hayden, M. R. (2014) Identification of binding sites in Huntingtin for the Huntingtin Interacting Proteins HIP14 and HIP14L. PLoS One 9, e90669
23. Li, J., Mahajan, A., and Tsai, M.-D. (2006) Ankyrin repeat: a unique motif mediating protein-protein interactions. Biochemistry 45, 15168-15178
24. Butland, S. L., Sanders, S. S., Schmidt, M. E., Riechers, S.-P., Lin, D. T., Martin, D. D., Vaid, K., Graham, R. K., Singaraja, R. R., Wanker, E. E., Conibear, E., and Hayden, M. R. (2014) The palmitoyl acyltransferase HIP14 shares a high proportion of interactors with huntingtin: implications for a role in the pathogenesis of Huntington's disease. Hum. Mol. Genet. 23, 4142-4160
25. Greaves, J., and Chamberlain, L. H. (2006) Dual role of the cysteine-string domain in membrane binding and palmitoylation-dependent sorting of the molecular chaperone cysteine-string protein. Mol. Biol. Cell 17, 4748-4759
26. Greaves, J., Salaun, C., Fukata, Y., Fukata, M., and Chamberlain, L. H. (2008) Palmitoylation and membrane interactions of the neuroprotective chaperone cysteine-string protein. J. Biol. Chem. 283, 25014-25026
27. Greaves, J., Gorleku, O. A., Salaun, C., and Chamberlain, L. H. (2010) Palmitoylation of the SNAP25 protein family: specificity and regulation by DHHC palmitoyl transferases. J. Biol. Chem. 285, 24629-24638
28. Chi, N. W., and Lodish, H. F. (2000) Tankyrase is a Golgi-associated mitogen- activated protein kinase substrate that interacts with IRAP in GLUT4 vesicles. J. Biol. Chem. 275, 38437-38444
29. Sbodio, J. I., Lodish, H. F., and Chi, N.-W. (2002) Tankyrase-2 oligomerizes with tankyrase-1 and binds to both TRF1 (telomere-repeat-binding factor 1) and IRAP (insulin-responsive aminopeptidase). Biochem. J. 361, 451-459
30. Grefen, C., Obrdlik, P., and Harter, K. (2009) The determination of protein- protein interactions by the mating-based split-ubiquitin system (mb- SUS). Methods Mol. Biol. 479, 217-233
31. Monastyrskyy, B., Kryshtafovych, A., Moult, J., Tramontano, A., and Fidelis, K. (2014) Assessment of protein disorder region predictions in CASP10. Proteins 82, 127-137
32. Jones, D. T., and Cozzetto, D. (2015) DISOPRED3: precise disordered region predictions with annotated protein-binding activity. Bioinformatics 31, 857-863
33. Ishida, T., and Kinoshita, K. (2007) PrDOS: prediction of disordered protein regions from amino acid sequence. Nucleic Acids Res. 35, W460-W464
34. Wan, J., Savas, J. N., Roth, A. F., Sanders, S. S., Singaraja, R. R., Hayden, M. R., Yates, J. R., 3rd, and Davis, N. G. (2013) Tracking brain palmitoylation change: predominance of glial change in a mouse model of Huntington's disease. Chem. Biol. 20, 1421-1434
35. Song, I.-W., Li, W.-R., Chen, L.-Y., Shen, L.-F., Liu, K.-M., Yen, J. J. Y., Chen, Y.-J., Chen, Y.-J., Kraus, V. B., Wu, J.-Y., Lee, M. T., and Chen, Y.-T. (2014) Palmitoyl acyltransferase, Zdhhc13, facilitates bone mass acquisition by regulating postnatal epiphyseal development and endochondral ossification: a mouse model. PLoS One 9, e92194
36. Gonzalo, S., Greentree, W. K., and Linder, M. E. (1999) SNAP-25 is targeted to the plasma membrane through a novel membrane-binding domain. J. Biol. Chem. 274, 21313-21318
37. Greaves, J., Prescott, G. R., Fukata, Y., Fukata, M., Salaun, C., and Chamberlain, L. H. (2009) The hydrophobic cysteine-rich domain of SNAP25 couples with downstream residues to mediate membrane interactions and recognition by DHHC palmitoyl transferases. Mol. Biol. Cell 20, 1845-1854
38. Ren, W., Sun, Y., and Du, K. (2013) DHHC17 palmitoylates ClipR-59 and modulates ClipR-59 association with the plasma membrane. Mol. Cell. Biol. 33, 4255-4265
39. Gory-Fauré, S., Windscheid, V., Bosc, C., Peris, L., Proietto, D., Franck, R., Denarier, E., Job, D., and Andrieux, A. (2006) STOP-like protein 21 is a novel member of the STOP family, revealing a golgi localization of STOP proteins. J. Biol. Chem. 281, 28387-28396
40. Guillaud, L., Bosc, C., Fourest-Lieuvin, A., Denarier, E., Pirollet, F., Lafaneche re, L., and Job, D. (1998) STOP proteins are responsible for the high degree of microtubule stabilization observed in neuronal cells. J. Cell Biol. 142, 167-179
41. Sbodio, J. I., and Chi, N.-W. (2002) Identification of a tankyrase-binding motif shared by IRAP, TAB182, and human TRF1 but not mouse TRF1. NuMA contains this RXXPDG motif and is a novel tankyrase partner. J. Biol. Chem. 277, 31887-31892
42. Dubois, T., Paléotti, O., Mironov, A. A., Fraisier, V., Stradal, T. E., De Matteis, M. A., Franco, M., and Chavrier, P. (2005) Golgi-localized GAP for Cdc42 functions downstream of ARF1 to control Arp2/3 complex and F-actin dynamics. Nat. Cell Biol. 7, 353-364
43. Gilley, J., and Coleman, M. P. (2010) Endogenous Nmnat2 is an essential survival factor for maintenance of healthy axons. PLos Biol. 8, e1000300
44. Milde, S., and Coleman, M. P. (2014) Identification of palmitoyltransferase and thioesterase enzymes that control the subcellular localisation of axon survival factor nicotinamide mononucleotide adenylyltransferase 2 (NMNAT2). J. Biol. Chem. 289, 32858-32870
45. Bundschu, K., Walter, U., and Schuh, K. (2007) Getting a first clue about SPRED functions. BioEssays 29, 897-907
46. Masoumi-Moghaddam, S., Amini, A., and Morris, D. L. (2014) The developing story of Sprouty and cancer. Cancer Metastasis Rev. 33, 695-720
47. Yokoyama, C., Wang, X., Briggs, M. R., Admon, A., Wu, J., Hua, X., Goldstein, J. L., and Brown, M. S. (1993) SREBP-1, a basic-helix-loop-helixleucine zipper protein that controls transcription of the low density lipoprotein receptor gene. Cell 75, 187-197
48. Hua, X., Yokoyama, C., Wu, J., Briggs, M. R., Brown, M. S., Goldstein, J. L., and Wang, X. (1993) SREBP-2, a second basic-helix-loop-helix-leucine zipper protein that stimulates transcription by binding to a sterol regulatory element. Proc. Natl. Acad. Sci. U.S.A. 90, 11603-11607
49. Nohturfft, A., DeBose-Boyd, R. A., Scheek, S., Goldstein, J. L., and Brown, M. S. (1999) Sterols regulate cycling of SREBP cleavage-activating protein (SCAP) between endoplasmic reticulum and Golgi. Proc. Natl. Acad. Sci. U.S.A. 96, 11235-11240
50. Davey, N. E., Van Roey, K., Weatheritt, R. J., Toedt, G., Uyar, B., Altenberg, B., Budd, A., Diella, F., Dinkel, H., and Gibson, T. J. (2012) Attributes of short linear motifs. Mol. Biosyst. 8, 268-281
51. Van Roey, K., Uyar, B., Weatheritt, R. J., Dinkel, H., Seiler, M., Budd, A., Gibson, T. J., and Davey, N. E. (2014) Short linear motifs: ubiquitous and functionally diverse protein interaction modules directing cell regulation. Chem. Rev. 114, 6733-6778
52. van der Lee, R., Buljan, M., Lang, B., Weatheritt, R. J., Daughdrill, G. W., Dunker, A. K., Fuxreiter, M., Gough, J., Gsponer, J., Jones, D. T., Kim, P. M., Kriwacki, R. W., Oldfield, C. J., Pappu, R. V., Tompa, P., Uversky, V. N., Wright, P. E., and Babu, M. M. (2014) Classification of intrinsically disordered regions and proteins. Chem. Rev. 114, 6589-6631
53. Stengel, K. F., Holdermann, I., Cain, P., Robinson, C., Wild, K., and Sinning, I. (2008) Structural basis for specific substrate recognition by the chloroplast signal recognition particle protein cpSRP43. Science 321, 253-256
54. Collins, R. E., Northrop, J. P., Horton, J. R., Lee, D. Y., Zhang, X., Stallcup, M. R., and Cheng, X. (2008) The ankyrin repeats of G9a and GLP histone methyltransferases are mono- and dimethyllysine binding modules. Nat. Struct. Mol. Biol. 15, 245-250
55. Bennett, V., and Healy, J. (2009) Membrane domains based on ankyrin and spectrin associated with cell-cell interactions. Cold Spring Harb. Perspect. Biol. 1, a003012
56. Bennett, V., and Lorenzo, D. N. (2013) Spectrin- and ankyrin-based membrane domains and the evolution of vertebrates. Curr. Top. Membr. 72, 1-37
57. Guettler, S., LaRose, J., Petsalaki, E., Gish, G., Scotter, A., Pawson, T., Rottapel, R., and Sicheri, F. (2011) Structural basis and sequence rules for substrate recognition by Tankyrase explain the basis for cherubism disease. Cell 147, 1340-1354
58. Xu, C., Jin, J., Bian, C., Lam, R., Tian, R., Weist, R., You, L., Nie, J., Bochkarev, A., Tempel, W., Tan, C. S., Wasney, G. A., Vedadi, M., Gish, G. D., Arrowsmith, C. H., Pawson, T., Yang, X.-J., and Min, J. (2012) Sequencespecific recognition of a PxLPxI/L motif by an ankyrin repeat tumbler lock. Sci. Signal. 5, ra39
59. Liu, Z., and Huang, Y. (2014) Advantages of proteins being disordered. Protein Sci. 23, 539-550
60. Pan, Z., Kao, T., Horvath, Z., Lemos, J., Sul, J.-Y., Cranstoun, S. D., Bennett, V., Scherer, S. S., and Cooper, E. C. (2006) A common ankyrin-G-based mechanism retains KCNQ and NaV channels at electrically active domains of the axon. J. Neurosci. 26, 2599-2613
61. Chen, L., Ong, B., and Bennett, V. (2001) LAD-1, the Caenorhabditis elegans L1CAM homologue, participates in embryonic and gonadal morphogenesis and is a substrate for fibroblast growth factor receptor pathway-dependent phosphotyrosine-based signaling. J. Cell Biol. 154, 841-855
62. Chamberlain, L. H., andBurgoyne, R. D. (1996) Identification of a novel cysteine string protein variant and expression of cysteine string proteins in non-neuronal cells. J. Biol. Chem. 271, 7320-7323
63. Arnold, C., Reisch, N., Leibold, C., Becker, S., Prüfert, K., Sautter, K., Palm, D., Jatzke, S., Buchner, S., and Buchner, E. (2004) Structure-function analysis of the cysteine string protein in Drosophila: cysteine string, linker and C terminus. J. Exp. Biol. 207, 1323-1334
64. Stowers, R. S., and Isacoff, E. Y. (2007) Drosophila huntingtin-interacting protein 14 is a presynaptic protein required for photoreceptor synaptic transmission and expression of the palmitoylated proteins synaptosomeassociated protein 25 and cysteine string protein. J. Neurosci. 27, 12874-12883
65. Ohyama, T., Verstreken, P., Ly, C. V., Rosenmund, T., Rajan, A., Tien, A. C., Haueter, C., Schulze, K. L., and Bellen, H. J. (2007) Huntingtininteracting protein 14, a palmitoyl transferase required for exocytosis and targeting of CSP to synaptic vesicles. J. Cell Biol. 179, 1481-1496
66. Yang, G., Liu, Y., Yang, K., Liu, R., Zhu, S., Coquinco, A., Wen, W., Kojic, L., Jia, W., and Cynader, M. (2012) Isoform-specific palmitoylation of JNK regulates axonal development. Cell Death Differ. 19, 553-561
67. Gory-Fauré, S., Windscheid, V., Brocard, J., Montessuit, S., Tsutsumi, R., Denarier, E., Fukata, Y., Bosc, C., Delaroche, J., Collomb, N., Fukata, M., Martinou, J.-C., Pernet-Gallay, K., and Andrieux, A. (2014) Non-microtubular localizations of microtubule-associated protein 6 (MAP6). PLoS One 9, e114905
68. Tian, L., McClafferty, H., Jeffries, O., and Shipston, M. J. (2010) Multiple palmitoyltransferases are required for palmitoylation-dependent regulation of large conductance calcium- and voltage-activated potassium channels. J. Biol. Chem. 285, 23954-23962
69. Iakoucheva, L. M., Radivojac, P., Brown, C. J., O'Connor, T. R., Sikes, J. G., Obradovic, Z., and Dunker, A. K. (2004) The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res. 32, 1037-1049
70. Collins, M. O., Yu, L., Campuzano, I., Grant, S. G., and Choudhary, J. S. (2008) Phosphoproteomic analysis of the mouse brain cytosol reveals a predominance of protein phosphorylation in regions of intrinsic sequence disorder. Mol. Cell. Proteomics 7, 1331-1348
71. Yanai, A., Huang, K., Kang, R., Singaraja, R. R., Arstikaitis, P., Gan, L., Orban, P. C., Mullard, A., Cowan, C. M., Raymond, L. A., Drisdel, R. C., Green, W. N., Ravikumar, B., Rubinsztein, D. C., El-Husseini, A., and Hayden, M. R. (2006) Palmitoylation of huntingtin by HIP14 is essential for its trafficking and function. Nat. Neurosci. 9, 824-831
72. Bandyopadhyay, S., Chiang, C. Y., Srivastava, J., Gersten, M., White, S., Bell, R., Kurschner, C., Martin, C., Smoot, M., Sahasrabudhe, S., Barber, D. L., Chanda, S. K., and Ideker, T. (2010) A human MAP kinase interactome. Nat. Methods 7, 801-805