The dynamics of engineered resident proteins in the mammalian Golgi complex relies on cisternal maturation

Journal of Cell Biology

Volumn 201, Issue 7, 2013, Pages 1027-1036

  Rizzo, Riccardo ^a,b   Parashuraman, Seetharaman ^a,b   Mirabelli, Peppino ^c   Puri, Claudia ^b   Lucocq, John ^d   Luini, Alberto ^a,b  

^a CNR   (Italy)

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

^c IRCCS SDN   (Italy)

^d UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL MATURATION; DEPOLYMERIZATION; DYNAMICS; ELECTRON TOMOGRAPHY; FEMALE; GOLGI COMPLEX; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MAMMAL CELL; MORPHOLOGY; PRIORITY JOURNAL; SEDIMENTATION;

ANIMALS; CELL LINE; GOLGI APPARATUS; HELA CELLS; HUMANS; MANNOSIDASES; MICE; MODELS, BIOLOGICAL; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; RATS;

MAMMALIA;

EID: 84880021531     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201211147     Document Type: Article

References (44)

1. Antonny, B., and R. Schekman. 2001. ER export: public transportation by the COPII coach. Curr. Opin. Cell Biol. 13:438-443. http://dx.doi.org/10.1016/S0955-0674(00)00234-9
2. Bannykh, S.I., and W.E. Balch. 1997. Membrane dynamics at the endoplasmic reticulum-Golgi interface. J. Cell Biol. 138:1-4. http://dx.doi.org/10.1083/jcb.138.1.1
3. Becker, B., A. Haggarty, P.A. Romero, T. Poon, and A. Herscovics. 2000. The transmembrane domain of murine alpha-mannosidase IB is a major determinant of Golgi localization. Eur. J. Cell Biol. 79:986-992. http://dx.doi.org/10.1078/0171-9335-00127
4. Berger, E.G. 2002. Ectopic localizations of Golgi glycosyltransferases. Glycobiology. 12:29R-36R. http://dx.doi.org/10.1093/glycob/12.2.29R
5. Bonfanti, L., A.A. Mironov Jr., J.A. Martínez-Menárguez, O. Martella, A. Fusella, M. Baldassarre, R. Buccione, H.J. Geuze, A.A. Mironov, and A. Luini. 1998. Procollagen traverses the Golgi stack without leaving the lumen of cisternae: evidence for cisternal maturation. Cell. 95:993-1003. http://dx.doi.org/10.1016/S0092-8674(00)81723-7
6. Bonifacino, J.S. 2001. Metabolic labeling with amino acids. Curr. Protoc. Mol. Biol. Chapter 10:Unit 10.18.
7. Cole, N.B., N. Sciaky, A. Marotta, J. Song, and J. Lippincott-Schwartz. 1996a. Golgi dispersal during microtubule disruption: regeneration of Golgi stacks at peripheral endoplasmic reticulum exit sites. Mol. Biol. Cell. 7:631-650.
8. Cole, N.B., C.L. Smith, N. Sciaky, M. Terasaki, M. Edidin, and J. Lippincott-Schwartz. 1996b. Diffusional mobility of Golgi proteins in membranes of living cells. Science. 273:797-801. http://dx.doi.org/10.1126/science.273.5276.797
9. Copic, A., C.F. Latham, M.A. Horlbeck, J.G. D'Arcangelo, and E.A. Miller. 2012. ER cargo properties specify a requirement for COPII coat rigidity mediated by Sec13p. Science. 335:1359-1362. http://dx.doi.org/10.1126/science.1215909
10. De Matteis, M.A., and A. Luini. 2011. Mendelian disorders of membrane trafficking. N. Engl. J. Med. 365:927-938. http://dx.doi.org/10.1056/NEJMra0910494
11. Dejgaard, S.Y., A. Murshid, K.M. Dee, and J.F. Presley. 2007. Confocal microscopy-based linescan methodologies for intra-Golgi localization of proteins. J. Histochem. Cytochem. 55:709-719. http://dx.doi.org/10.1369/jhc.6A7090.2007
12. Dunphy, W.G., and J.E. Rothman. 1983. Compartmentation of asparagine-linked oligosaccharide processing in the Golgi apparatus. J. Cell Biol. 97:270-275. http://dx.doi.org/10.1083/jcb.97.1.270
13. Emr, S., B.S. Glick, A.D. Linstedt, J. Lippincott-Schwartz, A. Luini, V. Malhotra, B.J. Marsh, A. Nakano, S.R. Pfeffer, C. Rabouille, et al. 2009. Journeys through the Golgi-taking stock in a new era. J. Cell Biol. 187:449-453. http://dx.doi.org/10.1083/jcb.200909011
14. Gilchrist, A., C.E. Au, J. Hiding, A.W. Bell, J. Fernandez-Rodriguez, S. Lesimple, H. Nagaya, L. Roy, S.J. Gosline, M. Hallett, et al. 2006. Quantitative proteomics analysis of the secretory pathway. Cell. 127:1265-1281. http://dx.doi.org/10.1016/j.cell.2006.10.036
15. Glick, B.S., and A. Luini. 2011. Models for Golgi traffic: a critical assessment. Cold Spring Harb. Perspect. Biol. 3:a005215. http://dx.doi.org/10.1101/cshperspect.a005215
16. Hoe, M.H., P. Slusarewicz, T. Misteli, R. Watson, and G. Warren. 1995. Evidence for recycling of the resident medial/trans Golgi enzyme, N-acetylglucosaminyltransferase I, in ldlD cells. J. Biol. Chem. 270:25057-25063. http://dx.doi.org/10.1074/jbc.270.42.25057
17. Jarvela, T., and A.D. Linstedt. 2012. Irradiation-induced protein inactivation reveals Golgi enzyme cycling to cell periphery. J. Cell Sci. 125:973-980. http://dx.doi.org/10.1242/jcs.094441
18. Kweon, H.S., G.V. Beznoussenko, M. Micaroni, R.S. Polishchuk, A. Trucco, O. Martella, D. Di Giandomenico, P. Marra, A. Fusella, A. Di Pentima, et al. 2004. Golgi enzymes are enriched in perforated zones of Golgi cisternae but are depleted in COPI vesicles. Mol. Biol. Cell. 15:4710-4724. http://dx.doi.org/10.1091/mbc.E03-12-0881
19. Lanoix, J., J. Ouwendijk, A. Stark, E. Szafer, D. Cassel, K. Dejgaard, M. Weiss, and T. Nilsson. 2001. Sorting of Golgi resident proteins into different subpopulations of COPI vesicles: a role for ArfGAP1. J. Cell Biol. 155:1199-1212. http://dx.doi.org/10.1083/jcb.200108017
20. Lippincott-Schwartz, J., J.G. Donaldson, A. Schweizer, E.G. Berger, H.P. Hauri, L.C. Yuan, and R.D. Klausner. 1990. Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway. Cell. 60:821-836. http://dx.doi.org/10.1016/0092-8674(90)90096-W
21. Losev, E., C.A. Reinke, J. Jellen, D.E. Strongin, B.J. Bevis, and B.S. Glick. 2006. Golgi maturation visualized in living yeast. Nature. 441:1002-1006. http://dx.doi.org/10.1038/nature04717
22. Love, H.D., C.C. Lin, C.S. Short, and J. Ostermann. 1998. Isolation of functional Golgi-derived vesicles with a possible role in retrograde transport. J. Cell Biol. 140:541-551. http://dx.doi.org/10.1083/jcb.140.3.541
23. Malsam, J., A. Satoh, L. Pelletier, and G. Warren. 2005. Golgin tethers define subpopulations of COPI vesicles. Science. 307:1095-1098. http://dx.doi.org/10.1126/science.1108061
24. Marra, P., T. Maffucci, T. Daniele, G.D. Tullio, Y. Ikehara, E.K. Chan, A. Luini, G. Beznoussenko, A. Mironov, and M.A. De Matteis. 2001. The GM130 and GRASP65 Golgi proteins cycle through and define a subdomain of the intermediate compartment. Nat. Cell Biol. 3:1101-1113. http://dx.doi.org/10.1038/ncb1201-1101
25. Martinez-Menárguez, J.A., R. Prekeris, V.M. Oorschot, R. Scheller, J.W. Slot, H.J. Geuze, and J. Klumperman. 2001. Peri-Golgi vesicles contain retrograde but not anterograde proteins consistent with the cisternal progression model of intra-Golgi transport. J. Cell Biol. 155:1213-1224. http://dx.doi.org/10.1083/jcb.200108029
26. Matsuura-Tokita, K., M. Takeuchi, A. Ichihara, K. Mikuriya, and A. Nakano. 2006. Live imaging of yeast Golgi cisternal maturation. Nature. 441:1007-1010. http://dx.doi.org/10.1038/nature04737
27. Mellman, I., and G. Warren. 2000. The road taken: past and future foundations of membrane traffic. Cell. 100:99-112. http://dx.doi.org/10.1016/S0092-8674(00)81687-6
28. Mironov, A.A., and G.V. Beznoussenko. 2012. The kiss-and-run model of intra-Golgi transport. Int. J. Mol. Sci. 13:6800-6819. http://dx.doi.org/10.3390/ijms13066800
29. Mironov, A.A., G.V. Beznoussenko, P. Nicoziani, O. Martella, A. Trucco, H.S. Kweon, D. Di Giandomenico, R.S. Polishchuk, A. Fusella, P. Lupetti, et al. 2001. Small cargo proteins and large aggregates can traverse the Golgi by a common mechanism without leaving the lumen of cisternae. J. Cell Biol. 155:1225-1238. http://dx.doi.org/10.1083/jcb.200108073
30. Nakano, A., and A. Luini. 2010. Passage through the Golgi. Curr. Opin. Cell Biol. 22:471-478. http://dx.doi.org/10.1016/j.ceb.2010.05.003
31. Orci, L., M. Amherdt, M. Ravazzola, A. Perrelet, and J.E. Rothman. 2000. Exclusion of golgi residents from transport vesicles budding from Golgi cisternae in intact cells. J. Cell Biol. 150:1263-1270. http://dx.doi.org/10.1083/jcb.150.6.1263
32. Patterson, G.H., K. Hirschberg, R.S. Polishchuk, D. Gerlich, R.D. Phair, and J. Lippincott-Schwartz. 2008. Transport through the Golgi apparatus by rapid partitioning within a two-phase membrane system. Cell. 133:1055-1067. http://dx.doi.org/10.1016/j.cell.2008.04.044
33. Pfeffer, S.R. 2007. Unsolved mysteries in membrane traffic. Annu. Rev. Biochem. 76:629-645. http://dx.doi.org/10.1146/annurev.biochem.76.061705.130002
34. Pfeffer, S.R. 2010. How the Golgi works: a cisternal progenitor model. Proc. Natl. Acad. Sci. USA. 107:19614-19618. http://dx.doi.org/10.1073/pnas.1011016107
35. Pryor, P.R., and J.P. Luzio. 2009. Delivery of endocytosed membrane proteins to the lysosome. Biochim. Biophys. Acta. 1793:615-624. http://dx.doi.org/10.1016/j.bbamcr.2008.12.022
36. Rivera, V.M., X. Wang, S. Wardwell, N.L. Courage, A. Volchuk, T. Keenan, D.A. Holt, M. Gilman, L. Orci, F. Cerasoli Jr., et al. 2000. Regulation of protein secretion through controlled aggregation in the endoplasmic reticulum. Science. 287:826-830. http://dx.doi.org/10.1126/science.287.5454.826
37. Rothman, J.E., and F.T. Wieland. 1996. Protein sorting by transport vesicles. Science. 272:227-234. http://dx.doi.org/10.1126/science.272.5259.227
38. Sciaky, N., J. Presley, C. Smith, K.J. Zaal, N. Cole, J.E. Moreira, M. Terasaki, E. Siggia, and J. Lippincott-Schwartz. 1997. Golgi tubule traffic and the effects of brefeldin A visualized in living cells. J. Cell Biol. 139:1137-1155. http://dx.doi.org/10.1083/jcb.139.5.1137
39. Shima, D.T., K. Haldar, R. Pepperkok, R. Watson, and G. Warren. 1997. Partitioning of the Golgi apparatus during mitosis in living HeLa cells. J. Cell Biol. 137:1211-1228. http://dx.doi.org/10.1083/jcb.137.6.1211
40. Teasdale, R.D., G. D'Agostaro, and P.A. Gleeson. 1992. The signal for Golgi retention of bovine beta 1,4-galactosyltransferase is in the transmembrane domain. J. Biol. Chem. 267:4084-4096.
41. Trucco, A., R.S. Polishchuk, O. Martella, A. Di Pentima, A. Fusella, D. Di Giandomenico, E. San Pietro, G.V. Beznoussenko, E.V. Polishchuk, M. Baldassarre, et al. 2004. Secretory traffic triggers the formation of tubular continuities across Golgi sub-compartments. Nat. Cell Biol. 6:1071-1081. http://dx.doi.org/10.1038/ncb1180
42. Venditti, R., T. Scanu, M. Santoro, G. Di Tullio, A. Spaar, R. Gaibisso, G.V. Beznoussenko, A.A. Mironov, A. Mironov Jr., L. Zelante, et al. 2012. Sedlin controls the ER export of procollagen by regulating the Sar1 cycle. Science. 337:1668-1672. http://dx.doi.org/10.1126/science.1224947
43. Volchuk, A., M. Amherdt, M. Ravazzola, B. Brügger, V.M. Rivera, T. Clackson, A. Perrelet, T.H. Söllner, J.E. Rothman, and L. Orci. 2000. Megavesicles implicated in the rapid transport of intracisternal aggregates across the Golgi stack. Cell. 102:335-348. http://dx.doi.org/10.1016/S0092-8674(00)00039-8
44. Yang, J.S., C. Valente, R.S. Polishchuk, G. Turacchio, E. Layre, D.B. Moody, C.C. Leslie, M.H. Gelb, W.J. Brown, D. Corda, et al. 2011. COPI acts in both vesicular and tubular transport. Nat. Cell Biol. 13:996-1003. http://dx.doi.org/10.1038/ncb2273