A filter at the entrance of the Golgi that selects vesicles according to size and bulk lipid composition

eLife

Volumn 5, Issue 2016JULY, 2016, Pages

  Magdeleine, Maud ^a   Gautier, Romain ^a   Gounon, Pierre ^b   Barelli, Hélène ^a   Vanni, Stefano ^a   Antonny, Bruno ^a  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b Universite Co te d'Azur Parc Valrose   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GOLGIN; GOLGIN GMAP 210; LIPOSOME; MEMBRANE PROTEIN; MONOUNSATURATED FATTY ACID; UNCLASSIFIED DRUG; MUTANT PROTEIN; NUCLEAR PROTEIN; TRIP11 PROTEIN, HUMAN;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CELL CULTURE; CONTROLLED STUDY; GOLGI COMPLEX; HUMAN; HUMAN CELL; LIPID COMPOSITION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN MOTIF; TRANSPORT VESICLE; CHEMISTRY; DNA MUTATIONAL ANALYSIS; GENETICS; METABOLISM;

DNA MUTATIONAL ANALYSIS; GOLGI APPARATUS; LIPOSOMES; MUTANT PROTEINS; NUCLEAR PROTEINS; TRANSPORT VESICLES;

EID: 84979645497     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.16988     Document Type: Article

References (54)

1. Ambroggio E, Sorre B, Bassereau P, Goud B, Manneville JB, Antonny B. 2010. ArfGAP1 generates an Arf1 gradient on continuous lipid membranes displaying flat and curved regions. The EMBO Journal 29: 292-303. doi: 10.1038/emboj.2009.341
2. Antonny B. 2011. Mechanisms of membrane curvature sensing. Annual Review of Biochemistry 80: 101-123. doi: 10.1146/annurev-biochem-052809-155121
3. Barlowe C, Orci L, Yeung T, Hosobuchi M, Hamamoto S, Salama N, Rexach MF, Ravazzola M, Amherdt M, Schekman R. 1994. COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77: 895-907. doi: 10.1016/0092-8674(94)90138-4
4. Bigay J, Antonny B. 2012. Curvature, lipid packing, and electrostatics of membrane organelles: defining cellular territories in determining specificity. Developmental Cell 23: 886-895. doi: 10.1016/j.devcel.2012.10.009
5. Bigay J, Casella JF, Drin G, Mesmin B, Antonny B. 2005. ArfGAP1 responds to membrane curvature through the folding of a lipid packing sensor motif. The EMBO Journal 24: 2244-2253. doi: 10.1038/sj.emboj.7600714
6. Bigay J, Gounon P, Robineau S, Antonny B. 2003. Lipid packing sensed by ArfGAP1 couples COPI coat disassembly to membrane bilayer curvature. Nature 426: 563-566. doi: 10.1038/nature02108
7. Bonifacino JS, Glick BS. 2004. The mechanisms of vesicle budding and fusion. Cell 116: 153-166. doi: 10.1016/S0092-8674(03)01079-1
8. Brown FC, Pfeffer SR. 2010. An update on transport vesicle tethering. Molecular Membrane Biology 27: 457-461. doi: 10.3109/09687688.2010.501765
9. Brügger B, Sandhoff R, Wegehingel S, Gorgas K, Malsam J, Helms JB, Lehmann WD, Nickel W, Wieland FT. 2000. Evidence for segregation of sphingomyelin and cholesterol during formation of COPI-coated vesicles. Journal of Cell Biology 151: 507-518. doi: 10.1083/jcb.151.3.507
10. Cai H, Reinisch K, Ferro-Novick S. 2007. Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Developmental Cell 12: 671-682. doi: 10.1016/j.devcel.2007.04. 005
11. Cardenas J, Rivero S, Goud B, Bornens M, Rios RM. 2009. Golgi localisation of GMAP210 requires two distinct cis-membrane binding mechanisms. BMC Biology 7: 56. doi: 10.1186/1741-7007-7-56
12. Cherfils J. 2014. Arf GTPases and their effectors: assembling multivalent membrane-binding platforms. Current Opinion in Structural Biology 29: 67-76. doi: 10.1016/j.sbi.2014.09.007
13. Cheung PY, Limouse C, Mabuchi H, Pfeffer SR. 2015. Protein flexibility is required for vesicle tethering at the Golgi. eLife 4: e12790. doi: 10.7554/eLife.12790
14. Cui H, Lyman E, Voth GA. 2011. Mechanism of membrane curvature sensing by amphipathic helix containing proteins. Biophysical Journal 100: 1271-1279. doi: 10.1016/j.bpj.2011.01.036
15. Doucet CM, Esmery N, de Saint-Jean M, Antonny B. 2015. Membrane curvature sensing by amphipathic helices Is modulated by the surrounding protein backbone. PLoS One 10: e0137965. doi: 10.1371/journal.pone. 0137965
16. Drin G, Antonny B. 2010. Amphipathic helices and membrane curvature. FEBS Letters 584: 1840-1847. doi: 10. 1016/j.febslet.2009.10.022
17. Drin G, Casella JF, Gautier R, Boehmer T, Schwartz TU, Antonny B. 2007. A general amphipathic alpha-helical motif for sensing membrane curvature. Nature Structural & Molecular Biology 14: 138-146. doi: 10.1038/nsmb1194
18. Drin G, Morello V, Casella JF, Gounon P, Antonny B. 2008. Asymmetric tethering of flat and curved lipid membranes by a golgin. Science 320: 670-673. doi: 10.1126/science.1155821
19. Follit JA, San Agustin JT, Xu F, Jonassen JA, Samtani R, Lo CW, Pazour GJ. 2008. The Golgin GMAP210/TRIP11 anchors IFT20 to the Golgi complex. PLoS Genetics 4: e1000315. doi: 10.1371/journal.pgen.1000315
20. Gautier R, Douguet D, Antonny B, Drin G. 2008. HELIQUEST: a web server to screen sequences with specific -helical properties. Bioinformatics 24: 2101-2102. doi: 10.1093/bioinformatics/btn392
21. Gillingham AK, Munro S. 2016. Finding the Golgi: Golgin coiled-coil proteins show the way. Trends in Cell Biology 26: 399-408. doi: 10.1016/j.tcb.2016.02.005
22. Gillingham AK, Tong AHY, Boone C, Munro S. 2004. The GTPase Arf1p and the ER to Golgi cargo receptor Erv14p cooperate to recruit the golgin Rud3p to the cis-Golgi. Journal of Cell Biology 167: 281-292. doi: 10. 1083/jcb.200407088
23. González-Rubio P, Gautier R, Etchebest C, Fuchs PF. 2011. Amphipathic-lipid-packing-sensor interactions with lipids assessed by atomistic molecular dynamics. Biochimica Et Biophysica Acta 1808: 2119-2127. doi: 10.1016/j.bbamem.2011.05.006
24. Ho R, Stroupe C. 2015. The HOPS/class C Vps complex tethers membranes by binding to one Rab GTPase in each apposed membrane. Molecular Biology of the Cell 26: 2655-2663. doi: 10.1091/mbc.E14-04-0922
25. Horchani H, de Saint-Jean M, Barelli H, Antonny B. 2014. Interaction of the spo20 membrane-sensor motif with phosphatidic acid and other anionic lipids, and influence of the membrane environment. PLoS One 9: e113484. doi: 10.1371/journal.pone.0113484
26. Hristova K, Wimley WC, Mishra VK, Anantharamiah GM, Segrest JP, White SH. 1999. An amphipathic alpha-helix at a membrane interface: a structural study using a novel X-ray diffraction method. Journal of Molecular Biology 290: 99-117. doi: 10.1006/jmbi.1999.2840
27. Infante C, Ramos-Morales F, Fedriani C, Bornens M, Rios RM. 1999. GMAP-210, A cis-Golgi network-associated protein, is a minus end microtubule-binding protein. Journal of Cell Biology 145: 83-98. doi: 10.1083/jcb.145.1. 83
28. Ishida R, Yamamoto A, Nakayama K, Sohda M, Misumi Y, Yasunaga T, Nakamura N. 2015. GM130 is a parallel tetramer with a flexible rod-like structure and N-terminally open (Y-shaped) and closed (I-shaped) conformations. FEBS Journal 282: 2232-2244. doi: 10.1111/febs.13271
29. Klemm RW, Ejsing CS, Surma MA, Kaiser HJ, Gerl MJ, Sampaio JL, de Robillard Q, Ferguson C, Proszynski TJ, Shevchenko A, Simons K. 2009. Segregation of sphingolipids and sterols during formation of secretory vesicles at the trans-Golgi network. Journal of Cell Biology 185: 601-612. doi: 10.1083/jcb.200901145
30. Kobayashi T, Pagano RE. 1988. ATP-dependent fusion of liposomes with the Golgi apparatus of perforated cells. Cell 55: 797-805. doi: 10.1016/0092-8674(88)90135-3
31. Kuhlee A, Raunser S, Ungermann C. 2015. Functional homologies in vesicle tethering. FEBS Letters 589: 2487-2497. doi: 10.1016/j.febslet.2015.06.001
32. Ladinsky MS, Mastronarde DN, McIntosh JR, Howell KE, Staehelin LA. 1999. Golgi structure in three dimensions: functional insights from the normal rat kidney cell. Journal of Cell Biology 144: 1135-1149. doi: 10.1083/jcb. 144.6.1135
33. Malhotra V, Erlmann P. 2015. The pathway of collagen secretion. Annual Review of Cell and Developmental Biology 31: 109-124. doi: 10.1146/annurev-cellbio-100913-013002
34. Malhotra V, Serafini T, Orci L, Shepherd JC, Rothman JE. 1989. Purification of a novel class of coated vesicles mediating biosynthetic protein transport through the Golgi stack. Cell 58: 329-336. doi: 10.1016/0092-8674(89) 90847-7
35. Malsam J, Satoh A, Pelletier L, Warren G. 2005. Golgin tethers define subpopulations of COPI vesicles. Science 307: 1095-1098. doi: 10.1126/science.1108061
36. Marsh BJ, Mastronarde DN, Buttle KF, Howell KE, McIntosh JR. 2001. Organellar relationships in the Golgi region of the pancreatic beta cell line, HIT-T15, visualized by high resolution electron tomography. PNAS 98: 2399-2406. doi: 10.1073/pnas.051631998
37. Mesmin B, Drin G, Levi S, Rawet M, Cassel D, Bigay J, Antonny B. 2007. Two lipid-packing sensor motifs contribute to the sensitivity of ArfGAP1 to membrane curvature. Biochemistry 46: 1779-1790. doi: 10.1021/bi062288w
38. Munro S. 2011. The Golgin coiled-coil proteins of the Golgi apparatus. Cold Spring Harbor Perspectives in Biology 3: a005256. doi: 10.1101/cshperspect.a005256
39. Ohya T, Miaczynska M, Coskun U, Lommer B, Runge A, Drechsel D, Kalaidzidis Y, Zerial M. 2009. Reconstitution of Rab-and SNARE-dependent membrane fusion by synthetic endosomes. Nature 459: 1091-1097. doi: 10. 1038/nature08107
40. Pernet-Gallay K, Antony C, Johannes L, Bornens M, Goud B, Rios RM. 2002. The overexpression of GMAP-210 blocks anterograde and retrograde transport between the ER and the Golgi apparatus. Traffic 3: 822-832. doi: 10.1034/j.1600-0854.2002.31107.x
41. Pranke IM, Morello V, Bigay J, Gibson K, Verbavatz JM, Antonny B, Jackson CL. 2011. α-Synuclein and ALPS motifs are membrane curvature sensors whose contrasting chemistry mediates selective vesicle binding. Journal of Cell Biology 194: 89-103. doi: 10.1083/jcb.201011118
42. Risselada HJ, Marrink SJ. 2009. Curvature effects on lipid packing and dynamics in liposomes revealed by coarse grained molecular dynamics simulations. Physical Chemistry Chemical Physics 11: 2056-2067. doi: 10.1039/b818782g
43. Roboti P, Sato K, Lowe M. 2015. The golgin GMAP-210 is required for efficient membrane trafficking in the early secretory pathway. Journal of Cell Science 128: 1595-1606. doi: 10.1242/jcs.166710
44. Sato K, Roboti P, Mironov AA, Lowe M. 2015. Coupling of vesicle tethering and Rab binding is required for in vivo functionality of the golgin GMAP-210. Molecular Biology of the Cell 26: 537-553. doi: 10.1091/mbc.E14-10-1450
45. Simons K, Virta H. 1987. Perforated MDCK cells support intracellular transport. The EMBO Journal 6: 2241-2247.
46. Sinka R, Gillingham AK, Kondylis V, Munro S. 2008. Golgi coiled-coil proteins contain multiple binding sites for Rab family G proteins. Journal of Cell Biology 183: 607-615. doi: 10.1083/jcb.200808018
47. Smits P, Bolton AD, Funari V, Hong M, Boyden ED, Lu L, Manning DK, Dwyer ND, Moran JL, Prysak M, Merriman B, Nelson SF, Bonafé L, Superti-Furga A, Ikegawa S, Krakow D, Cohn DH, Kirchhausen T, Warman ML, Beier DR. 2010. Lethal skeletal dysplasia in mice and humans lacking the Golgin GMAP-210. New England Journal of Medicine 362: 206-216. doi: 10.1056/NEJMoa0900158
48. Vamparys L, Gautier R, Vanni S, Bennett WF, Tieleman DP, Antonny B, Etchebest C, Fuchs PF. 2013. Conical lipids in flat bilayers induce packing defects similar to that induced by positive curvature. Biophysical Journal 104: 585-593. doi: 10.1016/j.bpj.2012.11.3836
49. van Meer G, Voelker DR, Feigenson GW. 2008. Membrane lipids: where they are and how they behave. Nature Reviews Molecular Cell Biology 9: 112-124. doi: 10.1038/nrm2330
50. Vanni S, Hirose H, Barelli H, Antonny B, Gautier R. 2014. A sub-nanometre view of how membrane curvature and composition modulate lipid packing and protein recruitment. Nature Communications 5: 4916. doi: 10.1038/ncomms5916
51. Vanni S, Vamparys L, Gautier R, Drin G, Etchebest C, Fuchs PF, Antonny B. 2013. Amphipathic lipid packing sensor motifs: probing bilayer defects with hydrophobic residues. Biophysical Journal 104: 575-584. doi: 10. 1016/j.bpj.2012.11.3837
52. Verhey KJ, Yang W. 2016. Permeability barriers for generating a unique ciliary protein and lipid composition. Current Opinion in Cell Biology 41: 109-116. doi: 10.1016/j.ceb.2016.05.004
53. Witkos TM, Lowe M. 2015. The Golgin family of coiled-coil tethering proteins. Frontiers in Cell and Developmental Biology 3: 86. doi: 10.3389/fcell.2015.00086
54. Wong M, Munro S. 2014. Membrane trafficking. The specificity of vesicle traffic to the Golgi is encoded in the golgin coiled-coil proteins. Science 346: 1256898. doi: 10.1126/science.1256898