Syk is recruited to stress granules and promotes their clearance through autophagy

Journal of Biological Chemistry

Volumn 290, Issue 46, 2015, Pages 27803-27815

  Krisenko, Mariya O ^a   Higgins, Reneé L ^a   Ghosh, Soumitra ^a   Zhou, Qing ^a   Trybula, Joy S ^a   Wang, Wen Horng ^a   Geahlen, Robert L ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ANTIGENS; BINS; CELLS; CYTOLOGY; ENZYMES; GRANULATION; PROTEINS;

ANTIGEN-ANTIBODY COMPLEX; AUTOPHAGOSOMES; BINDING PROTEINS; GRANULE FORMATIONS; INNATE IMMUNE RESPONSE; MULTIPLE FUNCTION; PROTEOMIC ANALYSIS; STRESS STIMULUS;

IMMUNE SYSTEM;

ARSENITE SODIUM; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; GROWTH FACTOR RECEPTOR BOUND PROTEIN 7; INITIATION FACTOR 2ALPHA; MESSENGER RNA; PHOSPHOTYROSINE; PROTEIN KINASE SYK; RIBONUCLEOPROTEIN; SCAFFOLD PROTEIN; ARSENOUS ACID DERIVATIVE; PROTEIN TYROSINE KINASE; RNA; SIGNAL PEPTIDE; SODIUM DERIVATIVE; SYK PROTEIN, HUMAN; TYROSINE;

ANIMAL CELL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BINDING SITE; BREAST CANCER CELL LINE; CELL GRANULE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PEPTIDE MAPPING; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; STRESS GRANULE; WESTERN BLOTTING; ENZYMOLOGY; GENETICS; HEK293 CELL LINE; MCF-7 CELL LINE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGICAL STRESS; PROTEIN TRANSPORT;

ARSENITES; AUTOPHAGY; CYTOPLASMIC GRANULES; HEK293 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MCF-7 CELLS; PHOSPHORYLATION; PROTEIN TRANSPORT; PROTEIN-TYROSINE KINASES; RNA; SODIUM COMPOUNDS; STRESS, PHYSIOLOGICAL; SYK KINASE; TYROSINE;

EID: 84946944086     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.642900     Document Type: Article

References (57)

1. Geahlen, R. L. (2009) Syk and pTyr'd: Signaling through the B cell antigen receptor. Biochim. Biophys. Acta 1793, 1115-1127
2. Mócsai, A., Ruland, J., and Tybulewicz, V. L. J. (2010) The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat. Rev. Immunol. 10, 387-402
3. Geahlen, R. L. (2014) Getting Syk: spleen tyrosine kinase as a therapeutic target. Trends Pharmacol. Sci. 35, 414-422
4. Krisenko, M. O., and Geahlen, R. L. (2015) Calling in SYK: SYK's dual role as a tumor promoter and tumor suppressor in cancer. Biochim. Biophys. Acta 1853, 254-263
5. Singh, A., Greninger, P., Rhodes, D., Koopman, L., Violette, S., Bardeesy, N., and Settleman, J. (2009) A gene expression signature associated with "K-Ras addiction" reveals regulators of EMT and tumor cell survival. Cancer Cell 15, 489-500
6. Udyavar, A. R., and Hoeksema., M. D., Clark, J. E., Zou, Y., Tang, Z., Li, Z., Li, M., Chen, H., Statnikov, A., Shyr, Y., Liebler, D. C., Field, J., Eisenberg, R., Estrada, L., Massion, P. P., and Quaranta, V. (2013) Co-expression network analysis identifies spleen tyrosine kinase (SYK) as a candidate onco-genic driver in a subset of small-cell lung cancer. BMC Syst. Biol. 7, Suppl. 5, S1
7. Prinos, P., Garneau, D., Lucier, J.-F., Gendron, D., Couture, S., Boivin, M., Brosseau, J.-P., Lapointe, E., Thibault, P., Durand, M., Tremblay, K., Gervais-Bird, J., Nwilati, H., Klinck, R., Chabot, B., Perreault, J.-P., Wellinger, R. J., and Elela, S. A. (2011) Alternative splicing of SYK regulates mitosis and cell survival. Nat. Struct. Mol. Biol. 18, 673-679
8. Zhang, J., and Benavente., C. A., McEvoy, J., Flores-Otero, J., Ding, L., Chen, X., Ulyanov, A., Wu, G., Wilson, M., Wang, J., Brennan, R., Rusch, M., Manning, A. L., Ma, J., Easton, J., Shurtleff, S., Mullighan, C., Pounds, S., Mukatira, S., Gupta, P., Neale, G., Zhao, D., Lu, C., Fulton, R. S., Fulton, L. L., Hong, X., Dooling, D. J., Ochoa, K., Naeve, C., Dyson, N. J., Mardis, E. R., Bahrami, A., Ellison, D., Wilson, R. K., Downing, J. R., and Dyer, M. A. (2012) A novel retinoblastoma therapy from genomic and epigenetic analyses. Nature 481, 329-334
9. Wang, W.-H., Childress, M. O., and Geahlen, R. L. (2014) Syk interacts with and phosphorylates nucleolinto stabilize Bcl-xL mRNA and promote cell survival. Mol. Cell. Biol. 34, 3788-3799
10. Buchan, J. R., and Parker, R. (2009) Eukaryotic stress granules: the ins and outs of translation. Mol. Cell 36, 932-941
11. Anderson, P., and Kedersha, N. (2008) Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 33, 141-150
12. Kim, W. J., Back, S.H., Kim, V., Ryu, I., and Jang, S. K. (2005) Sequestration of TRAF2 into stress granules interrupts tumor necrosis factor signaling under stress conditions. Mol. Cell. Biol. 25, 2450-2462
13. Li, W., Simarro, M., Kedersha, N., and Anderson, P. (2004) FAST is a survival protein that senses mitochondrial stress and modulates TIA-1-regulated changes in protein expression. Mol. Cell. Biol. 24, 10718-10732
14. Ash, P. E. A., and Vanderweyde., T. E., Youmans, K. L., Apicco, D. J., and Wolozin, B. (2014) Pathological stress granules in Alzheimer's disease. Brain Res. 1584, 52-58
15. Dormann, D., and Haass, C. (2011) TDP-43 and FUS: a nuclear affair. Trends Neurosci. 34, 339-348
16. Kim, H. J., and Kim., N. C., Wang, Y.-D., and Scarborough., E. A., Moore, J., Diaz, Z., MacLea, K.S., Freibaum, B., Li, S., Molliex, A., Kanagaraj, A. P., Carter, R., Boylan, K.B., Wojtas, A.M., Rademakers, R., Pinkus, J.L., Greenberg, S. A., Trojanowski, J. Q., Traynor, B. J., Smith, B. N., Topp, S., Gkazi, A.-S., Miller, J., Shaw, C. E., Kottlors, M., Kirschner, J., Pestronk, A., Li, Y. R., Ford, A. F., Gitler, A. D., Benatar, M., King, O. D., Kimonis, V. E., Ross, E. D., Weihl, C. C., Shorter, J., and Taylor, J. P. (2013) Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem pro-teinopathy and ALS. Nature 495, 467-473
17. King, O. D., and Gitler., A. D., and Shorter, J. (2012) The tip of the iceberg: RNA-binding proteins with prion-like domains in neurodegenerative disease. Brain Res. 1462, 61-80
18. Watts, G. D. J., Wymer, J., Kovach, M. J., Mehta, S. G., Mumm, S., Darvish, D., Pestronk, A., Whyte, M. P., and Kimonis, V.E. (2004) Inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia is caused by mutant valosin-containing protein. Nat. Genet. 36, 377-381
19. Johnson, J. O., Mandrioli, J., Benatar, M., Abramzon, Y., Van Deerlin, V. M., Trojanowski, J. Q., Gibbs, J. R., Brunetti, M., Gronka, S., Wuu, J., Ding, J., McCluskey, L., Martinez-Lage, M., Falcone, D., Hernandez, D. G., Arepalli, S., Chong, S., Schymick, J. C., Rothstein, J., Landi, F., Wang, Y.-D., Calvo, A., Mora, G., Sabatelli, M., Monsurrò, M. R., Battistini, S., Salvi, F., Spataro, R., Sola, P., Borghero, G., The ITALSGEN Consortium, Galassi, G., Scholz, S. W., Taylor, J. P., Restagno, G., Chiò, A., and Traynor, B. J. (2010) Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron 68, 857-864
20. Buchan, J. R., Kolaitis, R.-M., and Taylor., J. P., and Parker, R. (2013) Eukaryotic stress granules are cleared by autophagy and Cdc48/VCP function. Cell 153, 1461-1474
21. Yamamoto, S., Tomita, Y., Hoshida, Y., Iizuka, N., Monden, M., Yamamoto, S., Iuchi, K., and Aozasa, K. (2004) Expression level of valosin-containing protein (p97) is correlated with progression and prognosis of non-small-cell lung carcinoma. Ann. Surg. Oncol. 11, 697-704
22. Tsujimoto, Y., Tomita, Y., Hoshida, Y., Kono, T., Oka, T., Yamamoto, S., Nonomura, N., Okuyama, A., and Aozasa, K. (2004) Elevated expression of valosin-containing protein (p97) is associated with poor prognosis of prostate cancer. Clin. Cancer Res. 10, 3007-3012
23. Laguë, M. N., Romieu-Mourez, R., Bonneil, É., Boyer, A., Pouletty, N., Mes-Masson, A.-M., Thibault, P., Nadeau, M.-È., and Boerboom, D. (2012). Proteomic profiling of a mouse model for ovarian granulosa cell tumor identifies VCP as a highly sensitive serum tumor marker in several human cancers. PLoS One 7, e42470
24. Choi, K. S. (2012) Autophagy and cancer. Exp. Mol. Med. 44, 109-120
25. Kimmelman, A. C. (2011) The dynamic nature of autophagy in cancer. Gene Dev. 25, 1999-2010
26. Chen, S., and Rehman., S. K., Zhang, W., Wen, A., Yao, L., and Zhang, J. (2010) Autophagy is a therapeutic target in anticancer drug resistance. Biochim. Biophys. Acta 1806, 220-229
27. White, E. (2012) Deconvoluting the context-dependent role for autophagy in cancer. Nat. Rev. Cancer 12, 401-410
28. Iliuk, A. B., and Martin., V. A., Alicie, B. M., Geahlen, R. L., and Tao, W.A. (2010) In-depth analyses of kinase-dependent tyrosine phosphopro-teomes based on metal ion-functionalized soluble nanopolymers. Mol. Cell. Proteomics 9, 2162-2172
29. Galan, J. A., and Paris., L. L., Zhang, H.-J., Adler, J., and Geahlen., R. L., and Tao, W. A. (2011) Identification of Syk-interacting proteins using a novel amine-specific isotope tag and GFP nanotrap. J. Am. Soc. Mass Spectrom. 22, 319-328
30. Xue, L., Wang, W.-H., Iliuk, A., Hu, L., Galan, J. A., Yu, S., Hans, M., and Geahlen., R. L., and Tao, W. A. (2012) Sensitive kinase assay linked with phosphoproteomics for identifying direct kinase substrates. Proc. Natl. Acad. Sci. U.S.A. 109, 5615-5620
31. Mazroui, R., Di Marco, S., Kaufman, R. J., and Gallouzi, I. E. (2007) Inhibition of the ubiquitin-proteasome system induces stress granule formation. Mol. Biol. Cell 18, 2603-2618
32. Oh, H., Ozkirimli, E., Shah, K., Harrison, M. L., and Geahlen, R. L. (2007) Generation of an analog-sensitive Syk tyrosine kinase for the study of signaling dynamics from the B cell antigen receptor. J. Biol. Chem. 282, 33760-33768
33. Zhou, Q., and Geahlen, R. L. (2009) Interaction of the protein tyrosine kinase Syk and TRAF-interacting protein (TRIP) in the tumor necrosis factor (TNF)-mediated survival pathway in breast epithelial cells. Oncogene 28, 1348-1356
34. Zhou, F., Hu, J., Ma, H., Harrison, M. L., and Geahlen, R. L. (2006) Nucle-ocytoplasmic trafficking of the Syk protein-tyrosine kinase. Mol. Cell. Biol. 26, 3478-3491
35. Machida, K., and Thompson., C. M., Dierck, K., Jablonowski, K., Kärkkäinen, S., Liu, B., Zhang, H., Nash, P. D., Newman, D. K., Nollau, P., Pawson, T., and Renkema., G. H., Saksela, K., Schiller, M. R., Shin, D. G., and Mayer, B. J. (2007) High-throughput phosphotyrosine profiling using SH2 domains. Mol. Cell 26, 899-915
36. Kedersha, N., and Cho., M. R., Li, W., Yacono, P. W., Chen, S., Gilks, N., and Golan., D. E., and Anderson, P. (2000) Dynamic shuttling of Tia-1 accompanies the recruitment of mRNA to mammalian stress granules. J. Cell Biol. 151, 1257-1268
37. Kwon, S., Zhang, Y., and Matthias, P. (2007) The deacetylase HDAC6 is a novel critical component ofstress granules involved inthe stress response. Genes Dev. 21, 3381-3394
38. Bishop, A. C., and Ubersax., J. A., Petsch, D. T., Matheos, D. P., Gray, N. S., Blethrow, J., Shimizu, E., and Tsien., J. Z., Schultz, P. G., Rose, M. D., Wood, J. L., Morgan, D. O., and Shokat, K. M. (2000) A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 407, 395-401
39. Keshvara, L. M., and Isaacson., C. C., Yankee, T. M., Sarac, R., Harrison, M. L., and Geahlen, R. L. (1998) Syk- and Lyn-dependent phosphorylation of Syk on multiple tyrosines following B-cell activation includes a site that negatively regulates signaling. J. Immunol. 161, 5276-5283
40. Tsai, N.-P., Ho, P.-C., and Wei, L.-N. (2008) Regulation of stress granule dynamics by Grb7 and FAK signalling pathway. EMBO J. 27, 715-726
41. Groesch, T. D., Zhou, F., Mattila, S., Geahlen, R. L., and Post, C. B. (2006) Structural basis for the requirement of two phosphotyrosine residues in signaling mediated by Syk tyrosine kinase. J. Mol. Biol. 356, 1222-1236
42. Levin, S. E., Zhang, C., Kadlecek, T. A., Shokat, K. M., and Weiss, A. (2008) Inhibition of ZAP-70 kinase activity via an analog-sensitive allele blocks T cell receptor and CD28 superagonist signaling. J. Biol. Chem. 283, 15419-15430
43. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., and Yoshimori, T. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBOJ. 19, 5720-5728
44. Chen, C.-H., Martin, V. A., and Gorenstein., N. M., Geahlen, R. L., and Post, C. B. (2011) Two closely-spaced tyrosines regulate NFAT signaling in B cells via Syk association with Vav. Mol. Cell. Biol. 31, 2984-2996
45. Porter, C. J., and Matthews., J. M., Mackay, J. P., Pursglove, S. E., Schmidberger, J. W., Leedman, P. J., Pero, S. C, Krag, D. N., Wilce, M. C. J., and Wilce, J. A. (2007) Grb7 SH2 domain structure and interactions with a cyclic peptide inhibtor of cancer cell migration and proliferation. BMC Struct. Biol. 7, 58
46. Porter, C. J., Wilce, M. C. J., Mackay, J. P., Leedman, P., and Wilce, J. A. (2005) Grb7-SH2 domain dimerisation is affected by a single point mutation. Eur. Biophys. J. 34, 454-460
47. Oligino, L., and Lung., F. D., Sastry, L., Bigelow, J., Cao, T., Curran, M., Burke, T. R., Jr., Wang, S., Krag, D., Roller, P. P., and King, C. R. (1997) Nonphos-phorylated peptide ligands for the Grb2 Src homology 2 domain. J. Biol. Chem. 272, 29046-29052
48. Hart, C. P., and Martin., J. E., Reed, M. A., Keval, A. A., Pustelnik, M.J., Northrop, J. P., Patel, D. V., and Grove, J. R. (1999) Potent inhibitory ligands of the GRB2 SH2 domain from recombinant peptide libraries. Cell. Signal. 11, 453-464
49. Fumagalli, S., and Totty., N. F., Hsuan, J. J., and Courtneidge, S. A. (1994) A target for Src in mitosis. Nature 368, 871-874
50. Baudot, A. D., and Jeandel., P. Y., Mouska, X., Maurer, U., Tartare-Deckert, S., Raynaud, S. D., and Cassuto., J. P., Ticchioni, M., and Deckert, M. (2009) The tyrosine kinase Syk regulates the survival of chronic lymphocytic leukemia B cells through PKCS and proteasome-dependent regulation of Mcl-1 expression. Oncogene 28, 3261-3273
51. Chen, L., Monti, S., Juszczynski, P., Ouyang, J., Chapuy, B., Neuberg, D., Doench, J. G., Bogusz, A. M., Habermann, T. M., Dogan, A., Witzig, T. E., Kutok, J. L., Rodig, S.J., Golub, T., and Shipp, M. A. (2013) SYK inhibition modulates distinct PI3K/AKT-dependent survival pathways and cholesterol biosynthesis in diffuse large B cell lymphomas. Cancer Cell 23, 826-838
52. Caldwell, R. G., and Wilson., J. B., Anderson, S. J., and Longnecker, R. (1998) Epstein-Barr virus LMP2A drives B cell development and survival in the absence of normal B cell receptor signals. Immunity 9, 405-411
53. Carnevale, J., Ross, L., Puissant, A., Banerji, V., and Stone., R. M., DeAngelo, D. J., Ross, K. N., and Stegmaier, K. (2013) SYK regulates mTOR signaling in AML. Leukemia 27, 2118-2128
54. 2 integrin-derived signals induce cell survival and proliferation of AML blasts by activating a Syk/STAT signaling axis. Blood 121, 3889-3899, S1-S66
55. Kanie, T., Abe, A., Matsuda, T., Kuno, Y., Towatari, M., Yamamoto, T., Saito, H., Emi, N., and Naoe, T. (2004) TEL-Syk fusion constitutively activates PI3-K/Akt, MAPK and JAK2-independent STAT5 signal pathways. Leukemia 18, 548-555
56. Uckun, F. M., Qazi, S., Ma, H., Tuel-Ahlgren, L., and Ozer, Z. (2010) STAT3 is a substrate of SYK tyrosine kinase in B-lineage leukemia/lym-phoma cells exposed to oxidative stress. Proc. Natl. Acad. Sci. U.S.A. 107, 2902-2907
57. Maycotte, P., Gearheart, CM., Barnard, R., Aryal, S., MulcahyLevy, J.M., and Fosmire., S. P., Hansen, R. J., Morgan, M. J., Porter, C. C, Gustafson, D. L., and Thorburn, A. (2014) STAT3-mediated autophagy dependence identifies subtypes of breast cancer where autophagy inhibition can be efficacious. Cancer Res. 74, 2579-2590