Recruitment of arfaptins to the trans-Golgi network by PI(4)P and their involvement in cargo export

EMBO Journal

Volumn 32, Issue 12, 2013, Pages 1717-1729

  Cruz Garcia, David ^a,b   Ortega Bellido, Maria ^a,b   Scarpa, Margherita ^a,b   Villeneuve, Julien ^a,b   Jovic, Marko ^c   Porzner, Marc ^d   Balla, Tamas ^c   Seufferlein, Thomas ^d   Malhotra, Vivek ^a,b,e  

^a CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^d UNIVERSITY OF ULM   (Germany)

^e INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

amphipathic helix; arfaptins; PI(4)P; PKD; protein secretion

Indexed keywords

ARFAPTIN; ARFAPTIN1; ARFAPTIN2; CHROMOGRANIN A; LIPOSOME; PHOSPHATIDYLINOSITOL 4 PHOSPHATE; PROTEIN KINASE D; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; GOLGI COMPLEX; GRANULE CELL; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; CERCOPITHECUS AETHIOPS; COS CELLS; DROSOPHILA MELANOGASTER; HEK293 CELLS; HELA CELLS; HUMANS; LIPOSOMES; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; TRANS-GOLGI NETWORK;

MAMMALIA;

EID: 84879460575     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.116     Document Type: Article

References (49)

1. Auer A, von Blume J, Sturany S, von Wichert G, Van Lint J, Vandenheede J, Adler G, Seufferlein T (2005) Role of the regulatory domain of protein kinase D2 in phorbol ester binding, catalytic activity, and nucleocytoplasmic shuttling. Mol Biol Cell 16: 4375-4385
2. Bankaitis VA, Garcia-Mata R, Mousley CJ (2012) Golgi membrane dynamics and lipid metabolism. Curr Biol 22: R414-R424
3. Bard F, Casano L, Mallabiabarrena A, Wallace E, Saito K, Kitayama H, Guizzunti G, Hu Y, Wendler F, Dasgupta R, Perrimon N, Malhotra V (2006) Functional genomics reveals genes involved in protein secretion and Golgi organization. Nature 439: 604-607
4. Baron CL, Malhotra V (2002) Role of diacylglycerol in PKD recruitment to the TGN and protein transport to the plasma membrane. Science 295: 325-328
5. Bossard C, Bresson D, Polishchuk RS, Malhotra V (2007) Dimeric PKD regulates membrane fission to form transport carriers at the TGN. J Cell Biol 179: 1123-1131
6. Campelo F, Malhotra V (2012) Membrane fission: the biogenesis of transport carriers. Annu Rev Biochem 81: 407-427
7. Christis C, Munro S (2012) The small G protein Arl1 directs the trans-Golgi-specific targeting of the Arf1 exchange factors BIG1 and BIG2. J Cell Biol 196: 327-335
8. De Matteis MA, Luini A (2008) Exiting the Golgi complex. Nat Rev Mol Cell Biol 9: 273-284
9. Diaz Anel AM, Malhotra V (2005) PKCeta is required for beta1gam-ma2/beta3gamma2-and PKD-mediated transport to the cell surface and the organization of the Golgi apparatus. J Cell Biol 169: 83-91
10. Drin G, Antonny B (2010) Amphipathic helices and membrane curvature. FEBS Lett 584: 1840-1847
11. Duran JM, Campelo F, van Galen J, Sachsenheimer T, Sot J, Egorov MV, Rentero C, Enrich C, Polishchuk RS, Goni FM, Brugger B, Wieland F, Malhotra V (2012) Sphingomyelin organization is required for vesicle biogenesis at the Golgi complex. EMBO J 31: 4535-4546
12. Emr S, Glick BS, Linstedt AD, Lippincott-Schwartz J, Luini A, Malhotra V, Marsh BJ, Nakano A, Pfeffer SR, Rabouille C, Rothman JE, Warren G, Wieland FT (2009) Journeys through the Golgi-taking stock in a new era. J Cell Biol 187: 449-453
13. Fairn GD, Schieber NL, Ariotti N, Murphy S, Kuerschner L, Webb RI, Grinstein S, Parton RG (2011) High-resolution mapping reveals topologically distinct cellular pools of phosphatidylserine. J Cell Biol 194: 257-275
14. Fugmann T, Hausser A, Schoffler P, Schmid S, Pfizenmaier K, Olayioye MA (2007) Regulation of secretory transport by protein kinase D-mediated phosphorylation of the ceramide transfer protein. J Cell Biol 178: 15-22
15. Gautier R, Douguet D, Antonny B, Drin G (2008) HELIQUEST: a web server to screen sequences with specific alpha-helical properties. Bioinformatics 24: 2101-210 2
16. Gehart H, Goginashvili A, Beck R, Morvan J, Erbs E, Formentini I, De Matteis MA, Schwab Y, Wieland FT, Ricci R (2012) The BAR domain protein arfaptin-1 controls secretory granule biogenesis at the trans-Golgi network. Dev Cell 23: 756-768
17. Godi A, Di Campli A, Konstantakopoulos A, Di Tullio G, Alessi DR, Kular GS, Daniele T, Marra P, Lucocq JM, De Matteis MA (2004) FAPPs control Golgi-to-cell-surface membrane traffic by binding to ARF and PtdIns(4)P. Nat Cell Biol 6: 393-404
18. Godi A, Pertile P, Meyers R, Marra P, Di Tullio G, Iurisci C, Luini A, Corda D, De Matteis MA (1999) ARF mediates recruitment of PtdIns-4-OH kinase-beta and stimulates synthesis of PtdIns(4, 5)P2 on the Golgi complex. Nat Cell Biol 1: 280-287
19. Graham TR, Burd CG (2011) Coordination of Golgi functions by phosphatidylinositol 4-kinases. Trends Cell Biol 21: 113-121
20. Grainger DL, Tavelis C, Ryan AJ, Hinchliffe KA (2012) The emerging role of PtdIns5P: another signalling phosphoinositide takes its place. Biochem Soc Trans 40: 257-261
21. Hanada K, Kumagai K, Yasuda S, Miura Y, Kawano M, Fukasawa M, Nishijima M (2003) Molecular machinery for non-vesicular trafficking of ceramide. Nature 426: 803-809
22. Hausser A, Storz P, Martens S, Link G, Toker A, Pfizenmaier K (2005) Protein kinase D regulates vesicular transport by phos-phorylating and activating phosphatidylinositol-4 kinase IIIbeta at the Golgi complex. Nat Cell Biol 7: 880-886
23. Kanoh H, Williger BT, Exton JH (1997) Arfaptin 1, a putative cytosolic target protein of ADP-ribosylation factor, is recruited to Golgi membranes. J Biol Chem 272: 5421-5429
24. Levine TP, Munro S (1998) The pleckstrin homology domain of oxysterol-binding protein recognises a determinant specific to Golgi membranes. Curr Biol 8: 729-739
25. Levine TP, Munro S (2002) Targeting of Golgi-specific pleckstrin homology domains involves both PtdIns 4-kinase-dependent and-independent components. Curr Biol 12: 695-704
26. Lu L, Horstmann H, Ng C, Hong W (2001) Regulation of Golgi structure and function by ARF-like protein 1 (Arl1). J Cell Sci 11 4 (Pt 24): 4543-4555
27. Maeda Y, Beznoussenko GV, Van Lint J, Mironov AA, Malhotra V (2001) Recruitment of protein kinase D to the trans-Golgi network via the first cysteine-rich domain. EMBO J 20: 5982-5990
28. Man Z, Kondo Y, Koga H, Umino H, Nakayama K, Shin HW (2011) Arfaptins are localized to the trans-Golgi by interaction with Arl1, but not Arfs. J Biol Chem 286: 11569-11578
29. Mellman I, Nelson WJ (2008) Coordinated protein sorting, targeting and distribution in polarized cells. Nat Rev Mol Cell Biol 9: 833-845
30. Nakamura K, Man Z, Xie Y, Hanai A, Makyio H, Kawasaki M, Kato R, Shin HW, Nakayama K, Wakatsuki S (2012) Structural basis for membrane binding specificity of the Bin/Amphiphysin/Rvs (BAR) Domain of Arfaptin-2 Determined by Arl1 GTPase. J Biol Chem 287: 25478-25489
31. Nhek S, Ngo M, Yang X, Ng MM, Field SJ, Asara JM, Ridgway ND, Toker A (2010) Regulation of oxysterol-binding protein Golgi localization through protein kinase D-mediated phosphorylation. Mol Biol Cell 21: 2327-2337
32. Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJ, Evans PR, McMahon HT (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303: 495-499
33. Pusapati GV, Krndija D, Armacki M, von Wichert G, von Blume J, Malhotra V, Adler G, Seufferlein T (2010) Role of the second cysteine-rich domain and Pro275 in protein kinase D2 interaction with ADP-ribosylation factor 1, trans-Golgi network recruitment, and protein transport. Mol Biol Cell 21: 1011-1022
34. Qualmann B, Koch D, Kessels MM (2011) Let's go bananas: revisiting the endocytic BAR code. EMBO J 30: 3501-3515
35. Rao Y, Haucke V (2011) Membrane shaping by the Bin/amphiphy-sin/Rvs (BAR) domain protein superfamily. Cell Mol Life Sci 68: 3983-3993
36. Shin OH, Exton JH (2001) Differential binding of arfaptin 2/POR1 to ADP-ribosylation factors and Rac1. Biochem Biophys Res Commun 285: 1267-1273
37. Szentpetery Z, Varnai P, Balla T (2010) Acute manipulation of Golgi phosphoinositides to assess their importance in cellular trafficking and signaling. Proc Natl Acad Sci USA 107: 8225-8230
38. Tsai SC, Adamik R, Hong JX, Moss J, Vaughan M, Kanoh H, Exton JH (1998) Effects of arfaptin 1 on guanine nucleotide-dependent activation of phospholipase D and cholera toxin by ADP-ribosyla-tion factor. J Biol Chem 273: 20697-20701
39. Valente C, Turacchio G, Mariggio S, Pagliuso A, Gaibisso R, Di Tullio G, Santoro M, Formiggini F, Spano S, Piccini D, Polishchuk RS, Colanzi A, Luini A, Corda D (2012) A 14-3-3gamma dimer-based scaffold bridges CtBP1-S/BARS to PI(4)KIIIbeta to regulate post-Golgi carrier formation. Nat Cell Biol 14: 343-354
40. van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9: 112-124
41. von Blume J, Duran JM, Forlanelli E, Alleaume AM, Egorov M, Polishchuk R, Molina H, Malhotra V (2009) Actin remodeling by ADF/cofilin is required for cargo sorting at the trans-Golgi network. J Cell Biol 187: 1055-1069
42. von Blume J, Knippschild U, Dequiedt F, Giamas G, Beck A, Auer A, Van Lint J, Adler G, Seufferlein T (2007) Phosphorylation at Ser244 by CK1 determines nuclear localization and substrate targeting of PKD2. EMBO J 26: 4619-4633
43. von Wichert G, Edenfeld T, von Blume J, Krisp H, Krndija D, Schmid H, Oswald F, Lother U, Walther P, Adler G, Seufferlein T (2008) Protein kinase D2 regulates chromogranin A secretion in human BON neuroendocrine tumour cells. Cell Signal 20: 925-934
44. Wakana Y, van Galen J, Meissner F, Scarpa M, Polishchuk RS, Mann M, Malhotra V (2012) A new class of carriers that transport selective cargo from the trans Golgi network to the cell surface. EMBO J 31: 3976-3990
45. Wang J, Sun HQ, Macia E, Kirchhausen T, Watson H, Bonifacino JS, Yin HL (2007) PI4P promotes the recruitment of the GGA adaptor proteins to the trans-Golgi network and regulates their recognition of the ubiquitin sorting signal. Mol Biol Cell 18: 2646-2655
46. Wang YJ, Wang J, Sun HQ, Martinez M, Sun YX, Macia E, Kirchhausen T, Albanesi JP, Roth MG, Yin HL (2003) Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 114: 299-310
47. Wiedemann C, Schafer T, Burger MM (1996) Chromaffin granule-associated phosphatidylinositol 4-kinase activity is required for stimulated secretion. EMBO J 15: 2094-2101
48. Williger BT, Ostermann J, Exton JH (1999) Arfaptin 1, an ARF-binding protein, inhibits phospholipase D and endoplasmic reticulum/Golgi protein transport. FEBS Lett 443: 197-200
49. Yeaman C, Ayala MI, Wright JR, Bard F, Bossard C, Ang A, Maeda Y, Seufferlein T, Mellman I, Nelson WJ, Malhotra V (2004) Protein kinase D regulates basolateral membrane protein exit from trans-Golgi network. Nat Cell Biol 6: 106-112