A 14-3-3γ 3 dimer-based scaffold bridges CtBP1-S/BARS to PI(4)KIIIβ 2 to regulate post-Golgi carrier formation

Nature Cell Biology

Volumn 14, Issue 4, 2012, Pages 343-354

  Valente, Carmen ^a,b,c   Turacchio, Gabriele ^a,c   Mariggió, Stefania ^a,c   Pagliuso, Alessandro ^a,b,c   Gaibisso, Renato ^c   Di Tullio, Giuseppe ^c   Santoro, Michele ^b,c   Formiggini, Fabio ^d,e   Spanó, Stefania ^c,g   Piccini, Daniele ^f   Polishchuk, Roman S ^b,c   Colanzi, Antonino ^a,c   Luini, Alberto ^a,b,c   Corda, Daniela ^a,c  

^a INSTITUTE OF PROTEIN BIOCHEMISTRY   (Italy)

^b TELETHON INSTITUTE OF GENETICS AND MEDICINE TIGEM   (Italy)

^c Consorzio Mario Negri Sud ^*  (Italy)

^d ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^e CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^f FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^g YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; CALYCULIN A; DYNAMIN; GLUTATHIONE TRANSFERASE; NEURONAL CALCIUM SENSOR; NEURONAL CALCIUM SENSOR 1; P21 ACTIVATED KINASE; P21 ACTIVATED KINASE 1; P21 ACTIVATED KINASE 2; P21 ACTIVATED KINASE 3; PHOSPHATIDYLINOSITOL 4 PHOSPHATE 3 KINASE; PHOSPHATIDYLINOSITOL 4 PHOSPHATE 3 KINASE BETA; PROTEIN 14 3 3; PROTEIN 14 3 3 GAMMA; PROTEIN KINASE D; PROTEIN P75; UNCLASSIFIED DRUG;

ACTIVE TRANSPORT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL MIGRATION; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GOLGI COMPLEX; IN VITRO STUDY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; REGULATORY MECHANISM; UPREGULATION; WESTERN BLOTTING;

14-3-3 PROTEINS; ALCOHOL OXIDOREDUCTASES; ANIMALS; CARRIER PROTEINS; CERCOPITHECUS AETHIOPS; COS CELLS; DIMERIZATION; DNA-BINDING PROTEINS; GOLGI APPARATUS; HUMANS; P21-ACTIVATED KINASES; PHOSPHORYLATION; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN KINASE C; RATS;

EID: 84859434555     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2445     Document Type: Article

References (70)

1. De Matteis, M. A. & Luini, A. Exiting the Golgi complex. Nat. Rev. Mol. Cell Biol. 9, 273-284 (2008). (Pubitemid 351430855)
2. Hirschberg, K. et al. Kinetic analysis of secretory protein trafic and characterization of golgi to plasma membrane transport intermediates in living cells. J. Cell Biol. 143, 1485-1503 (1998). (Pubitemid 29006498)
3. Polishchuk, E. V., Di Pentima, A., Luini, A. & Polishchuk, R. S. Mechanism of constitutive export from the golgi: bulk flow via the formation, protrusion, and en bloc cleavage of large trans-golgi network tubular domains. Mol. Biol. Cell 14, 4470-4485 (2003). (Pubitemid 37444649)
4. Rodriguez-Boulan, E., Kreitzer, G. & Musch, A. Organization of vesicular traficking in epithelia. Nat. Rev. Mol. Cell Biol. 6, 233-247 (2005).
5. Rothman, J. E. Lasker Basic Medical Research Award. The machinery and principles of vesicle transport in the cell. Nat. Med. 8, 1059-1062 (2002). (Pubitemid 35175951)
6. Schekman, R. Lasker Basic Medical Research Award. SEC mutants and the secretory apparatus. Nat. Med. 8, 1055-1058 (2002). (Pubitemid 35175950)
7. Haynes, L. P., Thomas, G. M. & Burgoyne, R. D. Interaction of neuronal calcium sensor-1 and ADP-ribosylation factor 1 allows bidirectional control of phosphatidylinositol 4-kinase and trans-Golgi network plasma membrane trafic. J. Biol. Chem. 280, 6047-6054 (2005). (Pubitemid 40280088)
8. Bruns, J. R., Ellis, M. A., Jeromin, A. & Weisz, O. A. Multiple roles for phosphatidylinositol 4-kinase in biosynthetic transport in polarized Madin-Darby canine kidney cells. J. Biol. Chem. 277, 2012-2018 (2002). (Pubitemid 34968782)
9. Godi, A. et al. FAPPs control Golgi-to-cell-surface membrane trafic by binding to ARF and PtdIns(4)P. Nat. Cell Biol. 6, 393-404 (2004). (Pubitemid 38607499)
10. Godi, A. et al. ARF mediates recruitment of PtdIns-4-OH kinase-and stimulates synthesis of PtdIns(4,5)P2 on the Golgi complex. Nat. Cell Biol. 1, 280-287 (1999). (Pubitemid 129495778)
11. D'Angelo, G. et al. Glycosphingolipid synthesis requires FAPP2 transfer of glucosylceramide. Nature 449, 62-67 (2007). (Pubitemid 47373773)
12. Cao, X. et al. Golgi protein FAPP2 tubulates membranes. Proc. Natl Acad. Sci. USA 106, 21121-21125 (2009).
13. Diaz Anel, A. M. Phospholipase C23 is a key component in the G=PKC, =PKDmediated regulation of trans-Golgi network to plasma membrane transport. Biochem. J. 406, 157-165 (2007). (Pubitemid 47264746)
14. Liljedahl, M. et al. Protein kinase D regulates the Cssion of cell surface destined transport carriers from the trans-Golgi network. Cell 104, 409-420 (2001). (Pubitemid 32206461)
15. Yeaman, C. et al. Protein kinase D regulates basolateral membrane protein exit from trans-Golgi network. Nat. Cell Biol. 6, 106-112 (2004). (Pubitemid 38425709)
16. Miserey-Lenkei, S. et al. Rab and actomyosin-dependent Cssion of transport vesicles at the Golgi complex. Nat. Cell Biol. 12, 645-654 (2010).
17. Bonazzi, M. et al. CtBP3/BARS drives membrane Cssion in dynamin-independent transport pathways. Nat. Cell Biol. 7, 570-580 (2005). (Pubitemid 40796980)
18. Nardini, M. et al. CtBP/BARS: a dual-function protein involved in transcription co-repression and Golgi membrane Cssion. EMBO J. 22, 3122-3130 (2003). (Pubitemid 36758632)
19. Corda, D., Colanzi, A. & Luini, A. The multiple activities of CtBP/BARS proteins: the Golgi view. Trends Cell Biol. 16, 167-173 (2006). (Pubitemid 43358005)
20. Colanzi, A. & Corda, D. Mitosis controls the Golgi and the Golgi controls mitosis. Curr. Opin. Cell Biol. 19, 386-393 (2007). (Pubitemid 47277505)
21. Aitken, A. 14-3-3 proteins: a historic overview. Semin. Cancer Biol. 16, 162-172 (2006). (Pubitemid 43796128)
22. Hausser, A. et al. Phospho-specific binding of 14-3-3 proteins to phosphatidylinositol 4-kinase III protects from dephosphorylation and stabilises lipid kinase activity. J. Cell Sci. 119, 3613-3621 (2006). (Pubitemid 44501865)
23. Demmel, L. et al. Nucleocytoplasmic shuttling of the Golgi phosphatidylinositol 4-kinase Pik1 is regulated by 14-3-3 proteins and coordinates Golgi function with cell growth. Mol. Biol. Cell 19, 1046-1061 (2008). (Pubitemid 351481818)
24. Valente, C., Spanò, S., Luini, A. & Corda, D. Purification and functional properties of the membrane Cssioning protein CtBP3/BARS. Methods Enzymol. 404, 296-316 (2005).
25. Zhao, X. et al. Interaction of neuronal calcium sensor-1 (NCS-1) with phosphatidylinositol 4-kinase stimulates lipid kinase activity and affects membrane traficking in COS-7 cells. J. Biol. Chem. 276, 40183-40189 (2001).
26. Hausser, A. et al. Protein kinase D regulates vesicular transport by phosphorylating and activating phosphatidylinositol-4 kinase III at the Golgi complex. Nat. Cell Biol. 7, 880-886 (2005). (Pubitemid 41486288)
27. Eswaran, J., Soundararajan, M., Kumar, R. & Knapp, S. UnPAKing the class differences among p21-activated kinases. Trends Biochem. Sci. 33, 394-403 (2008).
28. Rodriguez Boulan, E. & Pendergast, M. Polarized distribution of viral envelope proteins in the plasma membrane of infected epithelial cells. Cell 20, 45-54 (1980). (Pubitemid 10117299)
29. Matlin, K. S. & Simons, K. Reduced temperature prevents transfer of a membrane glycoprotein to the cell surface but does not prevent terminal glycosylation. Cell 34, 233-243 (1983).
30. Polishchuk, R., Di Pentima, A. & Lippincott-Schwartz, J. Delivery of raft-associated, GPI-anchored proteins to the apical surface of polarized MDCK cells by a transcytotic pathway. Nat. Cell Biol. 6, 297-307 (2004). (Pubitemid 38584819)
31. Marra, P. et al. The GM130 and GRASP65 Golgi proteins cycle through and dëne a subdomain of the intermediate compartment. Nat. Cell Biol. 3, 1101-1113 (2001). (Pubitemid 33130461)
32. Pelkmans, L. & Helenius, A. Insider information: what viruses tell us about endocytosis. Curr. Opin. Cell Biol. 15, 414-422 (2003). (Pubitemid 36928043)
33. Steinacker, P. et al. Unchanged survival rates of 14-3-3 knockout mice after inoculation with pathological prion protein. Mol. Cell Biol. 25, 1339-1346 (2005). (Pubitemid 40204911)
34. Chaudhri, M., Scarabel, M. & Aitken, A. Mammalian and yeast 14-3-3 isoforms form distinct patterns of dimers in vivo. Biochem. Biophys. Res. Commun. 300, 679-685 (2003). (Pubitemid 36268890)
35. Yaffe, M. B. et al. The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 91, 961-971 (1997). (Pubitemid 28027829)
36. Braselmann, S. & McCormick, F. Bcr and Raf form a complex in vivo via 14-3-3 proteins. EMBO J. 14, 4839-4848 (1995).
37. Vincenz, C. & Dixit, V. M. 14-3-3 proteins associate with A20 in an isoform-specific manner and function both as chaperone and adapter molecules. J. Biol. Chem. 271, 20029-20034 (1996). (Pubitemid 26281752)
38. Van Der Hoeven, P. C., Van Der Wal, J. C., Ruurs, P., Van Dijk, M. C. & Van Blitterswijk, J. 14-3-3 isotypes facilitate coupling of protein kinase C-to Raf-1: negative regulation by 14-3-3 phosphorylation. Biochem. J. 345 Pt 2, 297-306 (2000).
39. Liberali, P. et al. The closure of Pak1-dependent macropinosomes requires the phosphorylation of CtBP1/BARS. EMBO J. 27, 970-981 (2008). (Pubitemid 351508162)
40. Liu, D. et al. Crystal structure of the isoform of the 14-3-3 protein. Nature 376, 191-194 (1995).
41. Ottmann, C. et al. Phosphorylation-independent interaction between 14-3-3 and exoenzyme S: from structure to pathogenesis. EMBO J. 26, 902-913 (2007).
42. Barnes, C. J. et al. Functional inactivation of a transcriptional corepressor by a signaling kinase. Nat. Struct. Biol. 10, 622-628 (2003). (Pubitemid 36944715)
43. Dharmawardhane, S. et al. Regulation of macropinocytosis by p21-activated kinase-1. Mol. Biol. Cell 11, 3341-3352 (2000).
44. Paglini, G., Peris, L., Diez-Guerra, J., Quiroga, S. & Caceres, A. The Cdk5-p35 kinase associates with the Golgi apparatus and regulates membrane trafic. EMBO Rep. 2, 1139-1144 (2001). (Pubitemid 34055962)
45. Deacon, S. W. et al. An isoform-selective, small-molecule inhibitor targets the autoregulatory mechanism of p21-activated kinase . Chem. Biol. 15, 322-331 (2008). (Pubitemid 351508427)
46. Yang, J. S. et al. A role for BARS at the Cssion step of COPI vesicle formation from Golgi membrane. EMBO J. 24, 4133-4143 (2005).
47. Yang, J. S. et al. COPI acts in both vesicular and tubular transport. Nat. Cell Biol. 13, 996-1003 (2011).
48. Hidalgo Carcedo, C. et al. Mitotic Golgi partitioning is driven by the membrane-Cssioning protein CtBP3/BARS. Science 305, 93-96 (2004). (Pubitemid 38869379)
49. Colanzi, A. et al. The Golgi mitotic checkpoint is controlled by BARS-dependent Cssion of the Golgi ribbon into separate stacks in G2. EMBO J. 26, 2465-2476 (2007). (Pubitemid 46788313)
50. Saeed, M. F., Kolokoltsov, A. A., Albrecht, T. & Davey, R. A. Cellular entry of ebola virus involves uptake by a macropinocytosis-like mechanism and subsequent traficking through early and late endosomes. PLoS Pathog. 6, e1001110 (2010).
51. Haga, Y., Miwa, N., Jahangeer, S., Okada, T. & Nakamura, S. CtBP1/BARS is an activator of phospholipase D1 necessary for agonist-induced macropinocytosis. EMBO J. 28, 1197-1207 (2009).
52. Moreau, D. et al. Genome-wide RNAi screens identify genes required for ricin and PE intoxications. Dev. Cell 21, 231-244 (2011).
53. Tzivion, G. & Avruch, J. 14-3-3 proteins: active cofactors in cellular regulation by serine/threonine phosphorylation. J. Biol. Chem. 277, 3061-3064 (2002). (Pubitemid 34953163)
54. Ponsioen, B. et al. Detecting cAMP-induced Epac activation by uorescence resonance energy transfer: Epac as a novel cAMP indicator. EMBO Rep. 5, 1176-1180 (2004). (Pubitemid 40103613)
55. Pusapati, G. V. et al. Role of the second cysteine-rich domain and Pro275 in PKD2 interaction with ARF1, TGN recruitment and protein transport. Mol. Biol. Cell 21, 1011-1022 (2010).
56. Beck, R. et al. Membrane curvature induced by Arf1-GTP is essential for vesicle formation. Proc. Natl Acad. Sci. USA 105, 11731-11736 (2008).
57. Krauss, M. et al. Arf1-GTP-induced tubule formation suggests a function of Arf family proteins in curvature acquisition at sites of vesicle budding. J. Biol. Chem. 283, 27717-27723 (2008).
58. Lundmark, R., Doherty, G. J., Vallis, Y., Peter, B. J. & McMahon, H. T. Arf family GTP loading is activated by, and generates, positive membrane curvature. Biochem. J. 414, 189-194 (2008).
59. Vieira, O. V., Verkade, P., Manninen, A. & Simons, K. FAPP2 is involved in the transport of apical cargo in polarized MDCK cells. J. Cell Biol. 170, 521-526 (2005). (Pubitemid 41186927)
60. Schmidt, J. A. & Brown, W. J. Lysophosphatidic acid acyltransferase 3 regulates Golgi complex structure and function. J. Cell Biol. 186, 211-218 (2009).
61. Schwarz, K., Natarajan, S., Kassas, N., Vitale, N. & Schmitz, F. The synaptic ribbon is a site of phosphatidic acid generation in ribbon synapses. J. Neurosci. 31, 15996-16011 (2011).
62. Weigert, R. et al. CtBP/BARS induces Cssion of Golgi membranes by acylating lysophosphatidic acid. Nature 402, 429-433 (1999). (Pubitemid 129544833)
63. Gallop, J. L., Butler, P. J. & McMahon, H. T. Endophilin and CtBP/BARS are not acyl transferases in endocytosis or Golgi Cssion. Nature 438, 675-678 (2005). (Pubitemid 41740578)
64. Pulvirenti, T. et al. A trafic-activated Golgi-based signalling circuit coordinates the secretory pathway. Nat. Cell Biol. 10, 912-922 (2008).
65. Harlow, E. & Lane, D. Antibodies: A Laboratory Manual (CSH Press, 1988).
66. Malhotra, V., Serãni, T., Orci, L., Shepherd, J. C. & Rothman, J. E. Purification of a novel class of coated vesicles mediating biosynthetic protein transport through the Golgi stack. Cell 58, 329-336 (1989). (Pubitemid 19191415)
67. Leelavathi, D. E., Estes, L. V., Feingold, D. S. & Lombardi, B. Isolation of a Golgi rich fraction from rat liver. BBA 211, 124-138 (1970).
68. Verdoodt, B., Benzinger, A., Popowicz, G. M., Holak, T. A. & Hermeking, H. Characterization of 14-3-3 dimerization determinants: requirement of homodimerization for inhibition of cell proliferation. Cell Cycle 5, 2920-2926 (2006). (Pubitemid 44953948)
69. Zhou, Y., Reddy, S., Murrey, H., Fei, H. & Levitan, I. B. Monomeric 14-3-3 protein is suficient to modulate the activity of the Drosophila slowpoke calcium-dependent potassium channel. J. Biol. Chem. 278, 10073-10080 (2003). (Pubitemid 36800263)
70. Keller, P., Toomre, D., Diaz, E., White, J. & Simons, K. Multicolour imaging of post-Golgi sorting and traficking in live cells. Nat. Cell Biol. 3, 140-149 (2001). (Pubitemid 32118367)