Golgi enlargement in Arf-depleted yeast cells is due to altered dynamics of cisternal maturation

Journal of Cell Science

Volumn 127, Issue 1, 2014, Pages 250-257

  Bhave, Madhura ^a   Papanikou, Effrosyni ^b   Iyer, Prasanna ^a   Pandya, Koushal ^a   Jain, Bhawik Kumar ^a   Ganguly, Abira ^a   Sharma, Chandrakala ^a   Pawar, Ketakee ^a   Austin, Jotham ^b   Day, Kasey J ^b   Rossanese, Olivia W ^b   Glick, Benjamin S ^b   Bhattacharyya, Dibyendu ^a  

^a TATA MEMORIAL HOSPITAL   (India)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Arf; Cisternal maturation; Golgi; Organelle number; Organelle size

Indexed keywords

ARF PROTEIN;

ANIMAL CELL; ARTICLE; CELL COUNT; CELL KINETICS; CELL MATURATION; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; GOLGI CISTERN; GOLGI COMPLEX; NONHUMAN; ORGANELLE SHAPE; ORGANELLE SIZE; PRIORITY JOURNAL; YEAST CELL;

ARF; CISTERNAL MATURATION; GOLGI; ORGANELLE NUMBER; ORGANELLE SIZE;

ADP-RIBOSYLATION FACTOR 1; BIOLOGICAL TRANSPORT; GENE EXPRESSION REGULATION, FUNGAL; GOLGI APPARATUS; MUTATION; MYRISTIC ACIDS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84891471994     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.140996     Document Type: Article

References (57)

1. Bevis, B. J., Hammond, A. T., Reinke, C. A. and Glick, B. S. (2002). De novo formation of transitional ER sites and Golgi structures in Pichia pastoris. Nat. Cell Biol. 4, 750-756.
2. Castillon, G. A., Watanabe, R., Taylor, M., Schwabe, T. M. and Riezman, H. (2009). Concentration of GPI-anchored proteins upon ER exit in yeast. Traffic 10, 186-200.
3. Chan, D. C. (2012). Fusion and fission: interlinked processes critical for mitochondrial health. Annu. Rev. Genet. 46, 265-287.
4. Daboussi, L., Costaguta, G. and Payne, G. S. (2012). Phosphoinositidemediated clathrin adaptor progression at the trans-Golgi network. Nat. Cell Biol. 14, 239-248.
5. Donaldson, J. G. and Jackson, C. L. (2011). ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat. Rev. Mol. Cell Biol. 12, 362-375.
6. Epp, N., Rethmeier, R., Krämer, L. and Ungermann, C. (2011). Membrane dynamics and fusion at late endosomes and vacuoles - Rab regulation, multisubunit tethering complexes and SNAREs. Eur. J. Cell Biol. 90, 779-785.
7. Gaynor, E. C., Chen, C. Y., Emr, S. D. and Graham, T. R. (1998). ARF is required for maintenance of yeast Golgi and endosome structure and function. Mol. Biol. Cell 9, 653-670.
8. Gietz, R. D. and Sugino, A. (1988). New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74, 527-534.
9. Gietz, R. D. and Woods, R. A. (2002). Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 350, 87-96.
10. Glick, B. S. and Nakano, A. (2009). Membrane traffic within the Golgi apparatus. Annu. Rev. Cell Dev. Biol. 25, 113-132.
11. Goehring, N. W. and Hyman, A. A. (2012). Organelle growth control through limiting pools of cytoplasmic components. Curr. Biol. 22, R330-R339.
12. Guo, Y. and Linstedt, A. D. (2006). COPII-Golgi protein interactions regulate COPII coat assembly and Golgi size. J. Cell Biol. 174, 53-63.
13. Hammond, A. T. and Glick, B. S. (2000). Raising the speed limits for 4D fluorescence microscopy. Traffic 1, 935-940.
14. Johnson, D. R., Bhatnagar, R. S., Knoll, L. J. and Gordon, J. I. (1994). Genetic and biochemical studies of protein N-myristoylation. Annu. Rev. Biochem. 63, 869-914.
15. Jonikas, M. C., Collins, S. R., Denic, V., Oh, E., Quan, E. M., Schmid, V., Weibezahn, J., Schwappach, B., Walter, P., Weissman, J. S. et al. (2009). Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science 323, 1693-1697.
16. Kahn, R. A. (2009). Toward a model for Arf GTPases as regulators of traffic at the Golgi. FEBS Lett. 583, 3872-3879.
17. Kellokumpu, S., Sormunen, R. and Kellokumpu, I. (2002). Abnormal glycosylation and altered Golgi structure in colorectal cancer: dependence on intra-Golgi pH. FEBS Lett. 516, 217-224.
18. Kirk, S. J., Cliff, J. M., Thomas, J. A. and Ward, T. H. (2010). Biogenesis of secretory organelles during B cell differentiation. J. Leukoc. Biol. 87, 245-255.
19. Kukulski, W., Schorb, M., Welsch, S., Picco, A., Kaksonen, M. and Briggs, J. A. (2011). Correlated fluorescence and 3D electron microscopy with high sensitivity and spatial precision. J. Cell Biol. 192, 111-119.
20. Kunz, J., Henriquez, R., Schneider, U., Deuter-Reinhard, M., Movva, N. R. and Hall, M. N. (1993). Target of rapamycin in yeast, TOR2, is an essential phosphatidylinositol kinase homolog required for G1 progression. Cell 73, 585-596.
21. Levi, S. K., Bhattacharyya, D., Strack, R. L., Austin, J. R. I., 2nd and Glick, B. S. (2010). The yeast GRASP Grh1 colocalizes with COPII and is dispensable for organizing the secretory pathway. Traffic 11, 1168-1179.
22. Levy, D. L. and Heald, R. (2012). Mechanisms of intracellular scaling. Annu. Rev. Cell Dev. Biol. 28, 113-135.
23. Lewis, M. J., Nichols, B. J., Prescianotto-Baschong, C., Riezman, H. and Pelham, H. R. B. (2000). Specific retrieval of the exocytic SNARE Snc1p from early yeast endosomes. Mol. Biol. Cell 11, 23-38.
24. Losev, E., Reinke, C. A., Jellen, J., Strongin, D. E., Bevis, B. J. and Glick, B. S. (2006). Golgi maturation visualized in living yeast. Nature 441, 1002-1006.
25. Lu, Z., Joseph, D., Bugnard, E., Zaal, K. J. M. and Ralston, E. (2001). Golgi complex reorganization during muscle differentiation: visualization in living cells and mechanism. Mol. Biol. Cell 12, 795-808.
26. Marshall, W. (2002). Size control in dynamic organelles. Trends Cell Biol. 12, 414-419.
27. Marshall, W. F. (2012). Organelle size control systems: from cell geometry to organelle-directed medicine. Bioessays 34, 721-724.
28. Matsuura-Tokita, K., Takeuchi, M., Ichihara, A., Mikuriya, K. and Nakano, A. (2006). Live imaging of yeast Golgi cisternal maturation. Nature 441, 1007-1010.
29. Mogelsvang, S., Marsh, B. J., Ladinsky, M. S. and Howell, K. E. (2004). Predicting function from structure: 3D structure studies of the mammalian Golgi complex. Traffic 5, 338-345.
30. Mowbrey, K. and Dacks, J. B. (2009). Evolution and diversity of the Golgi body. FEBS Lett. 583, 3738-3745.
31. Papanikou, E. and Glick, B. S. (2009). The yeast Golgi apparatus: insights and mysteries. FEBS Lett. 583, 3746-3751.
32. Peyroche, A., Courbeyrette, R., Rambourg, A. and Jackson, C. L. (2001). The ARF exchange factors Gea1p and Gea2p regulate Golgi structure and function in yeast. J. Cell Sci. 114, 2241-2253.
33. Preuss, D., Mulholland, J., Franzusoff, A., Segev, N. and Botstein, D. (1992). Characterization of the Saccharomyces Golgi complex through the cell cycle by immunoelectron microscopy. Mol. Biol. Cell 3, 789-803.
34. Rambourg, A. and Clermont, Y. (1997). Three-dimensional structure of the Golgi apparatus in mammalian cells. In The Golgi Apparatus (ed. E. G. Berger and J. Roth), pp. 37-61. Basel: Birkhäuser Verlag.
35. Rossanese, O. W., Soderholm, J., Bevis, B. J., Sears, I. B., O'Connor, J., Williamson, E. K. and Glick, B. S. (1999). Golgi structure correlates with transitional endoplasmic reticulum organization in Pichia pastoris and Saccharomyces cerevisiae. J. Cell Biol. 145, 69-81.
36. Rossanese, O. W., Reinke, C. A., Bevis, B. J., Hammond, A. T., Sears, I. B., O'Connor, J. and Glick, B. S. (2001). A role for actin, Cdc1p, and Myo2p in the inheritance of late Golgi elements in Saccharomyces cerevisiae. J. Cell Biol. 153, 47-62.
37. Rothstein, R. (1991). Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 194, 281-301.
38. Sengupta, D. and Linstedt, A. D. (2011). Control of organelle size: the Golgi complex. Annu. Rev. Cell Dev. Biol. 27, 57-77.
39. Shaner, N. C., Campbell, R. E., Steinbach, P. A., Giepmans, B. N. G., Palmer, A. E. and Tsien, R. Y. (2004). Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22, 1567-1572.
40. Sherman, F. (1991). Getting started with yeast. Methods Enzymol. 194, 3-21.
41. Shindiapina, P. and Barlowe, C. (2010). Requirements for transitional endoplasmic reticulum site structure and function in Saccharomyces cerevisiae. Mol. Biol. Cell 21, 1530-1545.
42. Staehelin, L. A. and Kang, B. H. (2008). Nanoscale architecture of endoplasmic reticulum export sites and of Golgi membranes as determined by electron tomography. Plant Physiol. 147, 1454-1468.
43. Stalder, D. and Antonny, B. (2013). Arf GTPase regulation through cascade mechanisms and positive feedback loops. FEBS Lett. 587, 2028-2035.
44. Stearns, T., Kahn, R. A., Botstein, D. and Hoyt, M. A. (1990a). ADP ribosylation factor is an essential protein in Saccharomyces cerevisiae and is encoded by two genes. Mol. Cell. Biol. 10, 6690-6699.
45. Stearns, T., Willingham, M. C., Botstein, D. and Kahn, R. A. (1990b). ADPribosylation factor is functionally and physically associated with the Golgi complex. Proc. Natl. Acad. Sci. USA 87, 1238-1242.
46. Storrie, B., Micaroni, M., Morgan, G. P., Jones, N., Kamykowski, J. A., Wilkins, N., Pan, T. H. and Marsh, B. J. (2012). Electron tomography reveals Rab6 is essential to the trafficking of trans-Golgi clathrin and COPI-coated vesicles and the maintenance of Golgi cisternal number. Traffic 13, 727-744.
47. Tang, X., Punch, J. J. and Lee, W. L. (2009). A CAAX motif can compensate for the PH domain of Num1 for cortical dynein attachment. Cell Cycle 8, 3182-3190.
48. Travers, K. J., Patil, C. K., Wodicka, L., Lockhart, D. J., Weissman, J. S. and Walter, P. (2000). Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101, 249-258.
49. Vida, T. A. and Emr, S. D. (1995). A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol. 128, 779-792.
50. Wach, A., Brachat, A., Pöhlmann, R. and Philippsen, P. (1994). New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793-1808.
51. Warren, G. and Rothman, J. (2011). The Golgi, pp. 322. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
52. Weller, S. G., Capitani, M., Cao, H., Micaroni, M., Luini, A., Sallese, M. and McNiven, M. A. (2010). Src kinase regulates the integrity and function of the Golgi apparatus via activation of dynamin 2. Proc. Natl. Acad. Sci. USA 107, 5863-5868.
53. Westermann, B. (2010). Mitochondrial dynamics in model organisms: what yeasts, worms and flies have taught us about fusion and fission of mitochondria. Semin. Cell Dev. Biol. 21, 542-549.
54. Wooding, S. and Pelham, H. R. B. (1998). The dynamics of golgi protein traffic visualized in living yeast cells. Mol. Biol. Cell 9, 2667-2680.
55. Wu, C. C., Yates, J. R., 3rd, Neville, M. C. and Howell, K. E. (2000). Proteomic analysis of two functional states of the Golgi complex in mammary epithelial cells. Traffic 1, 769-782.
56. Zacharias, D. A., Violin, J. D., Newton, A. C. and Tsien, R. Y. (2002). Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296, 913-916.
57. Zink, D., Fischer, A. H. and Nickerson, J. A. (2004). Nuclear structure in cancer cells. Nat. Rev. Cancer 4, 677-687.