JNK2 controls fragmentation of the Golgi complex and the G2/M transition through phosphorylation of GRASP65

Journal of Cell Science

Volumn 128, Issue 12, 2015, Pages 2249-2260

  Cervigni, Romina Ines ^a,c   Bonavita, Raffaella ^a,d   Barretta, Maria Luisa ^a   Spano, Daniela ^a   Ayala, Inmaculada ^a   Nakamura, Nobuhiro ^b   Corda, Daniela ^a   Colanzi, Antonino ^a  

^a INSTITUTE OF PROTEIN BIOCHEMISTRY   (Italy)

^b KYOTO SANGYO UNIVERSITY   (Japan)

^c SAN RAFFAELE HOSPITAL   (Italy)

^d HOSPITAL FOR SPECIAL SURGERY   (United States)

Author keywords

Cell cycle; Golgi complex; GRASP65; JNK

Indexed keywords

BREFELDIN A; CELL MEMBRANE PROTEIN; GRASP65 PROTEIN; JNK2 PROTEIN; SERINE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; GORASP1 PROTEIN, HUMAN; GRASP65 PROTEIN, RAT; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 9; SMALL INTERFERING RNA;

ARTICLE; CELL CYCLE PROGRESSION; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; G2 PHASE CELL CYCLE CHECKPOINT; GOLGI COMPLEX; MITOSIS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; RNA INTERFERENCE; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL CYCLE G2 PHASE; CELL DIVISION; CELL PROLIFERATION; CYTOLOGY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENETICS; HELA CELL LINE; HUMAN; KIDNEY; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; RAT; WESTERN BLOTTING;

MAMMALIA;

ANIMALS; BLOTTING, WESTERN; CELL DIVISION; CELL PROLIFERATION; CELLS, CULTURED; FLOW CYTOMETRY; G2 PHASE; GOLGI APPARATUS; HELA CELLS; HUMANS; KIDNEY; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; MITOGEN-ACTIVATED PROTEIN KINASE 9; MITOSIS; PHOSPHORYLATION; RATS; RNA, SMALL INTERFERING;

EID: 84932144744     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.164871     Document Type: Article

References (50)

1. Barr, F. A., Puype, M., Vandekerckhove, J. and Warren, G. (1997). GRASP65, a protein involved in the stacking of Golgi cisternae. Cell 91, 253-262.
2. Bisel, B., Wang, Y., Wei, J.-H., Xiang, Y., Tang, D., Miron-Mendoza, M., Yoshimura, S.-i., Nakamura, N. and Seemann, J. (2008). ERK regulates Golgi and centrosome orientation towards the leading edge through GRASP65. J. Cell Biol. 182, 837-843.
3. Bogoyevitch, M. A. and Kobe, B. (2006). Uses for JNK: the many and varied substrates of the c-Jun N-terminal kinases. Microbiol. Mol. Biol. Rev. 70, 1061-1095.
4. Carcedo, C. H., Bonazzi, M., Spano, S., Turacchio, G., Colanzi, A., Luini, A. and Corda, D. (2004). Mitotic Golgi partitioning is driven by the membrane-fissioning protein CtBP3/BARS. Science 305, 93-96.
5. Cervigni, R. I., Barretta, M. L., Persico, A., Corda, D. and Colanzi, A. (2011). The role of Aurora-A kinase in the Golgi-dependent control of mitotic entry. Bioarchitecture 1, 61-65.
6. Colanzi, A. and Sutterlin, C. (2013). Signaling at the Golgi during mitosis. Methods Cell Biol. 118, 383-400.
7. Colanzi, A., Carcedo, C. H., Persico, A., Cericola, C., Turacchio, G., Bonazzi, M., Luini, A. and Corda, D. (2007). The Golgi mitotic checkpoint is controlled by BARS-dependent fission of the Golgi ribbon into separate stacks in G2. EMBO J. 26, 2465-2476.
8. Cole, N. B., Smith, C. L., Sciaky, N., Terasaki, M., Edidin, M. and Lippincott-Schwartz, J. (1996). Diffusional mobility of Golgi proteins in membranes of living cells. Science 273, 797-801.
9. Corda, D., Colanzi, A. and Luini, A. (2006). The multiple activities of CtBP/BARS proteins: the Golgi view. Trends Cell Biol. 16, 167-173.
10. Du, Y., Bock, B. C., Schachter, K. A., Chao, M. and Gallo, K. A. (2005). Cdc42 induces activation loop phosphorylation and membrane targeting of mixed lineage kinase 3. J. Biol. Chem. 280, 42984-42993.
11. Duran, J. M., Kinseth, M., Bossard, C., Rose, D. W., Polishchuk, R., Wu, C. C., Yates, J., Zimmerman, T. and Malhotra, V. (2008). The role of GRASP55 in Golgi fragmentation and entry of cells into mitosis. Mol. Biol. Cell 19, 2579-2587.
12. Farhan, H., Wendeler, M. W., Mitrovic, S., Fava, E., Silberberg, Y., Sharan, R., Zerial, M. and Hauri, H.-P. (2010). MAPK signaling to the early secretory pathway revealed by kinase/phosphatase functional screening. J. Cell Biol. 189, 997-1011.
13. Feinstein, T. N. and Linstedt, A. D. (2007). Mitogen-activated protein kinase kinase 1-dependent Golgi unlinking occurs in G(2) phase and promotes the G(2)/M cell cycle transition. Mol. Biol. Cell 18, 594-604.
14. Feinstein, T. N. and Linstedt, A. D. (2008). GRASP55 regulates Golgi ribbon formation. Mol. Biol. Cell 19, 2696-2707.
15. Gaietta, G. M., Giepmans, B. N. G., Deerinck, T. J., Smith, W. B., Ngan, L., Llopis, J., Adams, S. R., Tsien, R. Y. and Ellisman, M. H. (2006). Golgi twins in late mitosis revealed by genetically encoded tags for live cell imaging and correlated electron microscopy. Proc. Natl. Acad. Sci. USA 103, 17777-17782.
16. Gao, Y., Davies, S. P., Augustin, M., Woodward, A., Patel, U. A., Kovelman, R. and Harvey, K. J. (2013). A broad activity screen in support of a chemogenomic map for kinase signalling research and drug discovery. Biochem. J. 451, 313-328.
17. Gutierrez, G. J., Tsuji, T., Chen, M., Jiang, W. and Ronai, Z. A. (2010a). Interplay between Cdh1 and JNK activity during the cell cycle. Nat. Cell Biol. 12, 686-695.
18. Gutierrez, G. J., Tsuji, T., Cross, J. V., Davis, R. J., Templeton, D. J., Jiang, W. and Ronai, Z. A. (2010b). JNK-mediated phosphorylation of Cdc25C regulates cell cycle entry and G(2)/M DNA damage checkpoint. J. Biol. Chem. 285, 14217-14228.
19. Jarvela, T. and Linstedt, A. D. (2014). Isoform-specific tethering links the Golgi ribbon to maintain compartmentalization. Mol. Biol. Cell 25, 133-144.
20. Kellokumpu, S., Sormunen, R. and Kellokumpu, I. (2002). Abnormal glycosylation and altered Golgi structure in colorectal cancer: dependence on intra-Golgi pH. FEBS Lett. 516, 217-224.
21. Kienzle, C., Eisler, S. A., Villeneuve, J., Brummer, T., Olayioye, M. A. and Hausser, A. (2013). PKD controls mitotic Golgi complex fragmentation through a Raf-MEK1 pathway. Mol. Biol. Cell 24, 222-233.
22. Lee, K. and Song, K. (2008). Basal c-Jun N-terminal kinases promote mitotic progression through histone H3 phosphorylation. Cell Cycle 7, 216-221.
23. Lee, I., Tiwari, N., Dunlop, M. H., Graham, M., Liu, X. and Rothman, J. E. (2014). Membrane adhesion dictates Golgi stacking and cisternal morphology. Proc. Natl. Acad. Sci. USA 111, 1849-1854.
24. Lin, C.-Y., Madsen, M. L., Yarm, F. R., Jang, Y.-J., Liu, X. and Erikson, R. L. (2000). Peripheral Golgi protein GRASP65 is a target of mitotic polo-like kinase (Plk) and Cdc2. Proc. Natl. Acad. Sci. USA 97, 12589-12594.
25. Lippincott-Schwartz, J. and Patterson, G. H. (2003). Development and use of fluorescent protein markers in living cells. Science 300, 87-91.
26. Lowe, M. and Barr, F. A. (2007). Inheritance and biogenesis of organelles in the secretory pathway. Nat. Rev. Mol. Cell Biol. 8, 429-439.
27. MacCorkle-Chosnek, R. A., Van Hooser, A., Goodrich, D.W., Brinkley, B. R. and Tan, T.-H. (2001). Cell cycle regulation of c-Jun N-terminal kinase activity at the centrosomes. Biochem. Biophys. Res. Commun. 289, 173-180.
28. Millarte, V. and Farhan, H. (2012). The Golgi in cell migration: regulation by signal transduction and its implications for cancer cell metastasis. ScientificWorldJournal 2012, 498278.
29. Mingo-Sion, A. M., Marietta, P. M., Koller, E., Wolf, D. M. and Van Den Berg, C. L. (2004). Inhibition of JNK reduces G2/M transit independent of p53, leading to endoreduplication, decreased proliferation, and apoptosis in breast cancer cells. Oncogene 23, 596-604.
30. Oktay, K., Buyuk, E., Oktem, O., Oktay, M. and Giancotti, F. G. (2008). The c-Jun N-terminal kinase JNK functions upstream of Aurora B to promote entry into mitosis. Cell Cycle 7, 533-541.
31. Persico, A., Cervigni, R. I., Barretta, M. L., Corda, D. and Colanzi, A. (2010). Golgi partitioning controls mitotic entry through Aurora-A kinase. Mol. Biol. Cell 21, 3708-3721.
32. Preisinger, C., Korner, R., Wind, M., Lehmann, W. D., Kopajtich, R. and Barr, F. A. (2005). Plk1 docking to GRASP65 phosphorylated by Cdk1 suggests a mechanism for Golgi checkpoint signalling. EMBO J. 24, 753-765.
33. Puthenveedu, M. A. and Linstedt, A. D. (2004). Gene replacement reveals that p115/SNARE interactions are essential for Golgi biogenesis. Proc. Natl. Acad. Sci. USA 101, 1253-1256.
34. Puthenveedu, M. A., Bachert, C., Puri, S., Lanni, F. and Linstedt, A. D. (2006). GM130 and GRASP65-dependent lateral cisternal fusion allows uniform Golgienzyme distribution. Nat. Cell Biol. 8, 238-248.
35. Sengupta, D. and Linstedt, A. D. (2010). Mitotic inhibition of GRASP65 organelle tethering involves Polo-like kinase 1 (PLK1) phosphorylation proximate to an internal PDZ ligand. J. Biol. Chem. 285, 39994-40003.
36. Sengupta, D., Truschel, S., Bachert, C. and Linstedt, A. D. (2009). Organelle tethering by a homotypic PDZ interaction underlies formation of the Golgi membrane network. J. Cell Biol. 186, 41-55.
37. Shorter, J. and Warren, G. (2002). Golgi architecture and inheritance. Annu. Rev. Cell Dev. Biol. 18, 379-420.
38. Sutterlin, C., Hsu, P., Mallabiabarrena, A. and Malhotra, V. (2002). Fragmentation and dispersal of the pericentriolar Golgi complex is required for entry into mitosis in mammalian cells. Cell 109, 359-369.
39. Sutterlin, C., Polishchuk, R., Pecot, M. and Malhotra, V. (2005). The Golgiassociated protein GRASP65 regulates spindle dynamics and is essential for cell division. Mol. Biol. Cell 16, 3211-3222.
40. Tang, D., Yuan, H., Vielemeyer, O., Perez, F. and Wang, Y. (2012). Sequential phosphorylation of GRASP65 during mitotic Golgi disassembly. Biol. Open 1, 1204-1214.
41. Truschel, S. T., Zhang, M., Bachert, C., Macbeth, M. R. and Linstedt, A. D. (2012). Allosteric regulation of GRASP protein-dependent Golgi membrane tethering by mitotic phosphorylation. J. Biol. Chem. 287, 19870-19875.
42. Vassilev, L. T. (2006). Cell cycle synchronization at the G2/M phase border by reversible inhibition of CDK1. Cell Cycle 5, 2555-2556.
43. Veenendaal, T., Jarvela, T., Grieve, A. G., van Es, J. H., Linstedt, A. D. and Rabouille, C. (2014). GRASP65 controls the cis Golgi integrity in vivo. Biol. Open 3, 431-443.
44. Villeneuve, J., Scarpa, M., Ortega-Bellido, M. and Malhotra, V. (2013). MEK1 inactivates Myt1 to regulate Golgi membrane fragmentation and mitotic entry in mammalian cells. EMBO J. 32, 72-85.
45. Vinke, F. P., Grieve, A. G. and Rabouille, C. (2011). The multiple facets of the Golgi reassembly stacking proteins. Biochem. J. 433, 423-433.
46. Waetzig, V. and Herdegen, T. (2005). Context-specific inhibition of JNKs: overcoming the dilemma of protection and damage. Trends Pharmacol. Sci. 26, 455-461.
47. Wang, Y., Seemann, J., Pypaert, M., Shorter, J. andWarren, G. (2003). A direct role forGRASP65 as a mitotically regulated Golgi stacking factor.EMBOJ.22, 3279-3290.
48. Wang, Y., Satoh, A. andWarren, G. (2005). Mapping the functional domains of the Golgi stacking factor GRASP65. J. Biol. Chem. 280, 4921-4928.
49. Wei, J.-H. and Seemann, J. (2009). Mitotic division of the mammalian Golgi apparatus. Semin. Cell Dev. Biol. 20, 810-816.
50. Yoshimura, S.-i., Yoshioka, K., Barr, F. A., Lowe, M., Nakayama, K., Ohkuma, S. and Nakamura, N. (2005). Convergence of cell cycle regulation and growth factor signals on GRASP65. J. Biol. Chem. 280, 23048-23056.