ADP ribosylation factors 1 and 4 and group VIA phospholipase A 2 regulate morphology and intraorganellar traffic in the endoplasmic reticulum-golgi intermediate compartment

Molecular Biology of the Cell

Volumn 21, Issue 23, 2010, Pages 4130-4140

  Ben Tekaya, Houchaima ^a   Kahn, Richard A ^b   Hauri, Hans Peter ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 4; PHOSPHOLIPASE A2 GROUP VI;

ARTICLE; CELL COMPARTMENTALIZATION; CELL MIGRATION; CELL ORGANELLE; CELL STRUCTURE; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; GENE SILENCING; GOLGI COMPLEX; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ADP-RIBOSYLATION FACTOR 1; ADP-RIBOSYLATION FACTORS; ENDOPLASMIC RETICULUM; GENE KNOCKDOWN TECHNIQUES; GOLGI APPARATUS; GROUP VI PHOSPHOLIPASES A2; HELA CELLS; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MICROSCOPY, FLUORESCENCE; VESICULAR TRANSPORT PROTEINS;

EID: 78650100828     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-01-0022     Document Type: Article

References (58)

1. Ackermann, E. J., Conde-Frieboes, K., and Dennis, E. A. (1995). Inhibition of macrophage Ca(2+)-independent phospholipase A2 by bromoenol lactone and trifluoromethyl ketones. J. Biol. Chem. 270, 445-450.
2. Ackermann, E. J., Kempner, E. S., and Dennis, E. A. (1994). Ca(2+)-independent cytosolic phospholipase A2 from macrophage-like P388D1 cells. Isolation and characterization. J. Biol. Chem. 269, 9227-9233.
3. Appenzeller-Herzog, C., and Hauri, H. P. (2006). The ER-Golgi intermediate compartment (ERGIC): in search of its identity and function. J. Cell Sci. 119, 2173-2183. (Pubitemid 43960307)
4. Bannykh, S. I., Rowe, T., and Balch, W. E. (1996). The organization of endoplasmic reticulum export complexes. J. Cell Biol. 135, 19-35.
5. Ben-Tekaya, H., Miura, K., Pepperkok, R., and Hauri, H. P. (2005). Live imaging of bidirectional traffic from the ERGIC. J. Cell Sci. 118, 357-367. (Pubitemid 40277348)
6. Blum, R., Stephens, D. J., and Schulz, I. (2000). Lumenal targeted GFP, used as a marker of soluble cargo, visualises rapid ERGIC to Golgi traffic by a tubulo-vesicular network. J. Cell Sci. 113, 3151-3159.
7. Breuza, L., Halbeisen, R., Jeno, P., Otte, S., Barlowe, C., Hong, W., and Hauri, H. P. (2004). Proteomics of endoplasmic reticulum-Golgi intermediate compartment (ERGIC) membranes from brefeldin A-treated HepG2 cells identifies ERGIC-32, a new cycling protein that interacts with human Erv46. J. Biol. Chem. 279, 47242-47253.
8. Brown, W. J., Chambers, K., and Doody, A. (2003). Phospholipase A2 (PLA2) enzymes in membrane trafficking: mediators of membrane shape and function. Traffic 4, 214-221. (Pubitemid 36665382)
9. Cavenagh, M. M., Whitney, J. A., Carroll, K., Zhang, C., Boman, A. L., Rosenwald, A. G., Mellman, I., and Kahn, R. A. (1996). Intracellular distribution of Arf proteins in mammalian cells. Arf6 is uniquely localized to the plasma membrane. J. Biol. Chem. 271, 21767-21774.
10. Choukroun, G. J., Marshansky, V., Gustafson, C. E., McKee, M., Hajjar, R. J., Rosenzweig, A., Brown, D., and Bonventre, J. V. (2000). Cytosolic phospholipase A(2) regulates Golgi structure and modulates intracellular trafficking of membrane proteins. J. Clin. Invest. 106, 983-993.
11. Chun, J., Shapovalova, Z., Dejgaard, S. Y., Presley, J. F., and Melancon, P. (2008). Characterization of class I and II ADP-ribosylation factors (Arfs) in live cells: GDP-bound class II Arfs associate with the ER-Golgi intermediate compartment independently of GBF1. Mol. Biol. Cell 19, 3488-3500.
12. de Figueiredo, P., Drecktrah, D., Polizotto, R. S., Cole, N. B., Lippincott-Schwartz, J., and Brown, W. J. (2000). Phospholipase A2 antagonists inhibit constitutive retrograde membrane traffic to the endoplasmic reticulum. Traffic 1, 504-511.
13. Donaldson, J. G., Lippincott-Schwartz, J., Bloom, G. S., Kreis, T. E., and Klausner, R. D. (1990). Dissociation of a 110-kD peripheral membrane protein from the Golgi apparatus is an early event in brefeldin A action. J. Cell Biol. 111, 2295-2306.
14. Evans, J. H., Spencer, D. M., Zweifach, A., and Leslie, C. C. (2001). Intracellular calcium signals regulating cytosolic phospholipase A2 translocation to internal membranes. J. Biol. Chem. 276, 30150-30160.
15. Fensome-Green, A., Stannard, N., Li, M., Bolsover, S., and Cockcroft, S. (2007). Bromoenol lactone, an inhibitor of Group V1A calcium-independent phospholipase A2 inhibits antigen-stimulated mast cell exocytosis without blocking Ca2+ influx. Cell Calcium 41, 145-153.
16. Fullekrug, J., Sonnichsen, B., Schafer, U., Nguyen Van, P., Soling, H. D., and Mieskes, G. (1997). Characterization of brefeldin A induced vesicular structures containing cycling proteins of the intermediate compartment/cis-Golgi network. FEBS Lett. 404, 75-81.
17. Ghomashchi, F., Stewart, A., Hefner, Y., Ramanadham, S., Turk, J., Leslie, C. C., and Gelb, M. H. (2001). A pyrrolidine-based specific inhibitor of cytosolic phospholipase A(2)alpha blocks arachidonic acid release in a variety of mammalian cells. Biochim. Biophys. Acta 1513, 160-166.
18. Ghosh, M., Tucker, D. E., Burchett, S. A., and Leslie, C. C. (2006). Properties of the Group IV phospholipase A2 family. Prog. Lipid Res. 45, 487-510.
19. Glick, B. S., and Nakano, A. (2009). Membrane traffic within the Golgi apparatus. Annu. Rev. Cell Dev. Biol. 25, 113-132.
20. Grewal, S., Herbert, S. P., Ponnambalam, S., and Walker, J. H. (2005). Cytosolic phospholipase A2-alpha and cyclooxygenase-2 localize to intracellular membranes of EA.hy. 926 endothelial cells that are distinct from the endoplasmic reticulum and the Golgi apparatus. FEBS J. 272, 1278-1290.
21. Hu, J., Shibata, Y., Zhu, P. P., Voss, C., Rismanchi, N., Prinz, W. A., Rapoport, T. A., and Blackstone, C. (2009). A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell 138, 549-561.
22. Itin, C., Schindler, R., and Hauri, H. P. (1995). Targeting of protein ERGIC-53 to the ER/ERGIC/cis-Golgi recycling pathway. J. Cell Biol. 131, 57-67.
23. Jones, D. H., Bax, B., Fensome, A., and Cockcroft, S. (1999a). ADP ribosylation factor 1 mutants identify a phospholipase D effector region and reveal that phospholipase D participates in lysosomal secretion but is not sufficient for recruitment of coatomer I. Biochem. J. 341, 185-192.
24. Jones, G., Moore, C., Hashemolhosseini, S., and Brenner, H. R. (1999b). Constitutively active MuSK is clustered in the absence of agrin and induces ectopic postsynaptic-like membranes in skeletal muscle fibers. J. Neurosci. 19, 3376-3383.
25. Kinsey, G. R., McHowat, J., Beckett, C. S., and Schnellmann, R. G. (2007). Identification of calcium-independent phospholipase A2gamma in mitochondria and its role in mitochondrial oxidative stress. Am. J. Physiol. Renal Physiol. 292, F853-F860.
26. Klumperman, J., Schweizer, A., Clausen, H., Tang, B. L., Hong, W., Oorschot, V., and Hauri, H. P. (1998). The recycling pathway of protein ERGIC-53 and dynamics of the ER-Golgi intermediate compartment. J. Cell Sci. 111, 3411-3425.
27. Kreis, T. E. (1987). Microtubules containing detyrosinated tubulin are less dynamic. EMBO J. 6, 2597-2606.
28. Kuismanen, E., and Saraste, J. (1989). Low temperature-induced transport blocks as tools to manipulate membrane traffic. Methods Cell Biol. 32, 257-274.
29. Larsson, P. K., Claesson, H. E., and Kennedy, B. P. (1998). Multiple splice variants of the human calcium-independent phospholipase A2 and their effect on enzyme activity. J. Biol. Chem. 273, 207-214.
30. Linstedt, A. D., Mehta, A., Suhan, J., Reggio, H., and Hauri, H. P. (1997). Sequence and overexpression of GPP130/GIMPc: evidence for saturable pH-sensitive targeting of a type II early Golgi membrane protein. Mol. Biol. Cell 8, 1073-1087.
31. Lippincott-Schwartz, J., Donaldson, J. G., Schweizer, A., Berger, E. G., Hauri, H. P., Yuan, L. C., and Klausner, R. D. (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.
32. Lotti, L. V., Torrisi, M. R., Pascale, M. C., and Bonatti, S. (1992). Immunocytochemical analysis of the transfer of vesicular stomatitis virus G glycoprotein from the intermediate compartment to the Golgi complex. J. Cell Biol. 118, 43-50.
33. Manguikian, A. D., and Barbour, S. E. (2004). Cell cycle dependence of group VIA calcium-independent phospholipase A2 activity. J. Biol. Chem. 279, 52881-52892.
34. Marie, M., Dale, H. A., Sannerud, R., and Saraste, J. (2009). The function of the intermediate compartment in pre-Golgi trafficking involves its stable connection with the centrosome. Mol. Biol. Cell 20, 4458-4470.
35. Marra, P., Maffucci, T., Daniele, T., Tullio, G. D., Ikehara, Y., Chan, E. K., Luini, A., Beznoussenko, G., Mironov, A., and De Matteis, M. A. (2001). The GM130 and GRASP65 Golgi proteins cycle through and define a subdomain of the intermediate compartment. Nat. Cell Biol. 3, 1101-1113.
36. Mironov, A. A., et al. (2003). ER-to-Golgi carriers arise through direct en bloc protrusion and multistage maturation of specialized ER exit domains. Dev. Cell 5, 583-594.
37. Morikawa, R. K., Aoki, J., Kano, F., Murata, M., Yamamoto, A., Tsujimoto, M., and Arai, H. (2009). Intracellular phospholipase A1gamma (iPLA1gamma) is a novel factor involved in coat protein complex I- and Rab6-independent retrograde transport between the endoplasmic reticulum and the Golgi complex. J. Biol. Chem. 284, 26620-26630.
38. Orso, G., Pendin, D., Liu, S., Tosetto, J., Moss, T. J., Faust, J. E., Micaroni, M., Egorova, A., Martinuzzi, A., McNew, J. A., and Daga, A. (2009). Homotypic fusion of ER membranes requires the dynamin-like GTPase Atlastin. Nature 460, 978-983.
39. Palade, G. (1975). Intracellular aspects of the process of protein transport. Science 189, 347-358.
40. Poulsen, K. A., Pedersen, S. F., Kolko, M., and Lambert, I. H. (2007). Induction of group VIA phospholipase A2 activity during in vitro ischemia in C2C12 myotubes is associated with changes in the level of its splice variants. Am. J. Physiol. Cell Physiol. 293, C1605-C1615.
41. Renault, L., Guibert, B., and Cherfils, J. (2003). Structural snapshots of the mechanism and inhibition of a guanine nucleotide exchange factor. Nature 426, 525-530. (Pubitemid 37522634)
42. San Pietro, E., et al. (2009). Group IV phospholipase A(2)alpha controls the formation of inter-cisternal continuities involved in intra-Golgi transport. PLoS Biol. 7, e1000194.
43. Sannerud, R., Marie, M., Nizak, C., Dale, H. A., Pernet-Gallay, K., Perez, F., Goud, B., and Saraste, J. (2006). Rab1 defines a novel pathway connecting the pre-Golgi intermediate compartment with the cell periphery. Mol. Biol. Cell 17, 1514-1526.
44. Saraste, J., Dale, H. A., Bazzocco, S., and Marie, M. (2009). Emerging new roles of the pre-Golgi intermediate compartment in biosynthetic-secretory trafficking. FEBS Lett. 583, 3804-3810.
45. Scheel, J., Pepperkok, R., Lowe, M., Griffiths, G., and Kreis, T. E. (1997). Dissociation of coatomer from membranes is required for brefeldin A-induced transfer of Golgi enzymes to the endoplasmic reticulum. J. Cell Biol. 137, 319-333.
46. Schmidt, J. A., and Brown, W. J. (2009). Lysophosphatidic acid acyltransferase 3 regulates Golgi complex structure and function. J. Cell Biol. 186, 211-218.
47. Schweizer, A., Ericsson, M., Bachi, T., Griffiths, G., and Hauri, H. P. (1993). Characterization of a novel 63 kDa membrane protein. Implications for the organization of the ER-to-Golgi pathway. J. Cell Sci. 104, 671-683.
48. Schweizer, A., Fransen, J. A., Bachi, T., Ginsel, L., and Hauri, H. P. (1988). Identification, by a monoclonal antibody, of a 53-kD protein associated with a tubulo-vesicular compartment at the cis-side of the Golgi apparatus. J. Cell Biol. 107, 1643-1653. (Pubitemid 18263538)
49. Schweizer, A., Fransen, J. A., Matter, K., Kreis, T. E., Ginsel, L., and Hauri, H. P. (1990). Identification of an intermediate compartment involved in protein transport from endoplasmic reticulum to Golgi apparatus. Eur. J. Cell Biol. 53, 185-196.
50. Seno, K., et al. (2000). Pyrrolidine inhibitors of human cytosolic phospholipase A(2). J. Med. Chem. 43, 1041-1044.
51. Shugrue, C. A., Kolen, E. R., Peters, H., Czernik, A., Kaiser, C., Matovcik, L., Hubbard, A. L., and Gorelick, F. (1999). Identification of the putative mammalian orthologue of Sec31P, a component of the COPII coat. J. Cell Sci. 112, 4547-4556.
52. Simpson, J. C., Nilsson, T., and Pepperkok, R. (2006). Biogenesis of tubular ER-to-Golgi transport intermediates. Mol. Biol. Cell 17, 723-737.
53. Skippen, A., Jones, D. H., Morgan, C. P., Li, M., and Cockcroft, S. (2002). Mechanism of ADP ribosylation factor-stimulated phosphatidylinositol 4,5-bisphosphate synthesis in HL60 cells. J. Biol. Chem. 277, 5823-5831.
54. Szul, T., Grabski, R., Lyons, S., Morohashi, Y., Shestopal, S., Lowe, M., and Sztul, E. (2007). Dissecting the role of the ARF guanine nucleotide exchange factor GBF1 in Golgi biogenesis and protein trafficking. J. Cell Sci. 120, 3929-3940.
55. Vedrenne, C., Klopfenstein, D. R., and Hauri, H. P. (2005). Phosphorylation controls CLIMP-63-mediated anchoring of the endoplasmic reticulum to microtubules. Mol. Biol. Cell 16, 1928-1937.
56. Volpicelli-Daley, L. A., Li, Y., Zhang, C. J., and Kahn, R. A. (2005). Isoform-selective effects of the depletion of ADP-ribosylation factors 1-5 on membrane traffic. Mol. Biol. Cell 16, 4495-4508.
57. Yang, J., Han, X., and Gross, R. W. (2003). Identification of hepatic peroxisomal phospholipase A(2) and characterization of arachidonic acid-containing choline glycerophospholipids in hepatic peroxisomes. FEBS Lett. 546, 247-250.
58. Zeghouf, M., Guibert, B., Zeeh, J. C., and Cherfils, J. (2005). Arf, Sec7 and Brefeldin A: a model towards the therapeutic inhibition of guanine nucleotide-exchange factors. Biochem. Soc. Trans. 33, 1265-1268.