ER-shaping proteins facilitate lipid exchange between the ER and mitochondria in S. cerevisiae

Journal of Cell Science

Volumn 125, Issue 20, 2012, Pages 4791-4799

  Voss, Christiane ^a   Lahiri, Sujoy ^a   Young, Barry P ^b   Loewen, Christopher J ^b   Prinz, William A ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Endoplasmic reticulum; ERMES complex; Lipid trafficking; Membrane contact sites; Mitochondria; Reticulons; Sey1p

Indexed keywords

FUNGAL PROTEIN; PHOSPHOLIPID; PROTEIN SEY1P; PROTEIN YOP1; RETICULON 1P; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE MUTATION; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; PHOSPHOLIPID TRANSFER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE; STEADY STATE; YEAST CELL;

DYNAMINS; ENDOPLASMIC RETICULUM; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MUTATION; PHOSPHOLIPIDS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; VESICULAR TRANSPORT PROTEINS;

MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 84872202122     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.105635     Document Type: Article

References (43)

1. Achleitner, G., Gaigg, B., Krasser, A., Kainersdorfer, E., Kohlwein, S. D., Perktold, A., Zellnig, G. and Daum, G. (1999). Association between the endoplasmic reticulum and mitochondria of yeast facilitates interorganelle transport of phospholipids through membrane contact. Eur. J. Biochem. 264, 545-553.
2. Anwar, K., Klemm, R. W., Condon, A., Severin, K. N., Zhang, M., Ghirlando, R., Hu, J., Rapoport, T. A. and Prinz, W. A. (2012). The dynamin-like GTPase Sey1p mediates homotypic ER fusion in S. cerevisiae. J. Cell Biol. 197, 209-217.
3. Berger, K. H., Sogo, L. F. and Yaffe, M. P. (1997). Mdm12p, a component required for mitochondrial inheritance that is conserved between budding and fission yeast. J. Cell Biol. 136, 545-553.
4. Burgess, S. M., Delannoy, M. and Jensen, R. E. (1994). MMM1 encodes a mitochondrial outer membrane protein essential for establishing and maintaining the structure of yeast mitochondria. J. Cell Biol. 126, 1375-1391.
5. Clancey, C. J., Chang, S. C. and Dowhan, W. (1993). Cloning of a gene (PSD1) encoding phosphatidylserine decarboxylase from Saccharomyces cerevisiae by complementation of an Escherichia coli mutant. J. Biol. Chem. 268, 24580-24590.
6. Dimmer, K. S., Fritz, S., Fuchs, F., Messerschmitt, M., Weinbach, N., Neupert, W. and Westermann, B. (2002). Genetic basis of mitochondrial function and morphology in Saccharomyces cerevisiae. Mol. Biol. Cell 13, 847-853.
7. Dimmer, K. S., Jakobs, S., Vogel, F., Altmann, K. and Westermann, B. (2005). Mdm31 and Mdm32 are inner membrane proteins required for maintenance of mitochondrial shape and stability of mitochondrial DNA nucleoids in yeast. J. Cell Biol. 168, 103-115.
8. Elbaz, Y. and Schuldiner, M. (2011). Staying in touch: the molecular era of organelle contact sites. Trends Biochem. Sci. 36, 616-623.
9. Henry, S. A., Kohlwein, S. D. and Carman, G. M. (2012). Metabolism and regulation of glycerolipids in the yeast Saccharomyces cerevisiae. Genetics 190, 317-349.
10. Hobbs, A. E., Srinivasan, M., McCaffery, J. M. and Jensen, R. E. (2001). Mmm1p, a mitochondrial outer membrane protein, is connected to mitochondrial DNA (mtDNA) nucleoids and required for mtDNA stability. J. Cell Biol. 152, 401-410.
11. Hu, J., Shibata, Y., Voss, C., Shemesh, T., Li, Z., Coughlin, M., Kozlov, M. M., Rapoport, T. A. and Prinz, W. A. (2008). Membrane proteins of the endoplasmic reticulum induce high-curvature tubules. Science 319, 1247-1250.
12. 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.
13. Kachar, B. and Reese, T. S. (1988). The mechanism of cytoplasmic streaming in characean algal cells: sliding of endoplasmic reticulum along actin filaments. J. Cell Biol. 106, 1545-1552.
14. Kornmann, B., Currie, E., Collins, S. R., Schuldiner, M., Nunnari, J., Weissman, J. S. and Walter, P. (2009). An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325, 477-481.
15. Kornmann, B., Osman, C. and Walter, P. (2011). The conserved GTPase Gem1 regulates endoplasmic reticulum-mitochondria connections. Proc. Natl. Acad. Sci. USA 108, 14151-14156.
16. LaMarche, A. E., Abate, M. I., Chan, S. H. and Trumpower, B. L. (1992). Isolation and characterization of COX12, the nuclear gene for a previously unrecognized subunit of Saccharomyces cerevisiae cytochrome c oxidase. J. Biol. Chem. 267, 22473-22480.
17. Lamping, E., Kohlwein, S. D., Henry, S. A. and Paltauf, F. (1991). Coordinate regulation of phosphatidylserine decarboxylase in Saccharomyces cerevisiae. J. Bacteriol. 173, 6432-6437.
18. Nguyen, T. T., Lewandowska, A., Choi, J. Y., Markgraf, D. F., Junker, M., Bilgin, M., Ejsing, C. S., Voelker, D. R., Rapoport, T. A. and Shaw, J. M. (2012). Gem1 and ERMES do not directly affect phosphatidylserine transport from ER to mitochondria or mitochondrial inheritance. Traffic 13, 880-890.
19. Nikawa, J. I. and Yamashita, S. (1981). Characterization of phosphatidylserine synthase from Saccharomyces cerevisiae and a mutant defective in the enzyme. Biochim. Biophys. Acta 665, 420-426.
20. Nunnari, J., Wong, E. D., Meeusen, S. and Wagner, J. A. (2002). Studying the behavior of mitochondria. Methods Enzymol. 351, 381-393.
21. Orso, G., Pendin, D., Liu, S., Tosetto, J., Moss, T. J., Faust, J. E., Micaroni, M., Egorova, A., Martinuzzi, A., McNew, J. A. et al. (2009). Homotypic fusion of ER membranes requires the dynamin-like GTPase atlastin. Nature 460, 978-983.
22. Parks, L. W., Bottema, C. D., Rodriguez, R. J. and Lewis, T. A. (1985). Yeast sterols: yeast mutants as tools for the study of sterol metabolism. Methods Enzymol. 111, 333-346.
23. Prinz, W. A. (2010). Lipid trafficking sans vesicles: where, why, how? Cell 143, 870-874.
24. Prinz, W. A., Grzyb, L., Veenhuis, M., Kahana, J. A., Silver, P. A. and Rapoport, T. A. (2000). Mutants affecting the structure of the cortical endoplasmic reticulum in Saccharomyces cerevisiae. J. Cell Biol. 150, 461-474.
25. Raychaudhuri, S. and Prinz, W. A. (2008). Nonvesicular phospholipid transfer between peroxisomes and the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 105, 15785-15790.
26. Shibata, Y., Hu, J., Kozlov, M. M. and Rapoport, T. A. (2009). Mechanisms shaping the membranes of cellular organelles. Annu. Rev. Cell Dev. Biol. 25, 329-354.
27. Simbeni, R., Pon, L., Zinser, E., Paltauf, F. and Daum, G. (1991). Mitochondrial membrane contact sites of yeast. Characterization of lipid components and possible involvement in intramitochondrial translocation of phospholipids. J. Biol. Chem. 266, 10047-10049.
28. Sogo, L. F. and Yaffe, M. P. (1994). Regulation of mitochondrial morphology and inheritance by Mdm10p, a protein of the mitochondrial outer membrane. J. Cell Biol. 126, 1361-1373.
29. Terasaki, M., Chen, L. B. and Fujiwara, K. (1986). Microtubules and the endoplasmic reticulum are highly interdependent structures. J. Cell Biol. 103, 1557-1568. Tong, A. H. and Boone, C. (2006). Synthetic genetic array analysis in Saccharomyces cerevisiae. Methods Mol. Biol. 313, 171-192.
30. Tong, A. H. and Boone, C. (2006). Synthetic genetic array analysis in Saccharomyces cerevisiae. Methods Mol. Biol. 313, 171-192.
31. Toulmay, A. and Prinz, W. A. (2011). Lipid transfer and signaling at organelle contact sites: the tip of the iceberg. Curr. Opin. Cell Biol. 23, 458-463.
32. Trotter, P. J., Pedretti, J. and Voelker, D. R. (1993). Phosphatidylserine decarboxylase from Saccharomyces cerevisiae. Isolation of mutants, cloning of the gene, and creation of a null allele. J. Biol. Chem. 268, 21416-21424.
33. Trotter, P. J., Pedretti, J., Yates, R. and Voelker, D. R. (1995). Phosphatidylserine decarboxylase 2 of Saccharomyces cerevisiáe. Cloning and mapping of the gene, heterologous expression, and creation of the null allele. J. Biol. Chem. 270, 6071-6080.
34. Vaden, D. L., Gohil, V. M., Gu, Z. and Greenberg, M. L. (2005). Separation of yeast phospholipids using one-dimensional thin-layer chromatography. Anal. Biochem. 338, 162-164.
35. Vance, J. E. (1990). Phospholipid synthesis in a membrane fraction associated with mitochondria. J. Biol. Chem. 265, 7248-7256.
36. Voelker, D. R. (1985). Disruption of phosphatidylserine translocation to the mitochondria in baby hamster kidney cells. J. Biol. Chem. 260, 14671-14676.
37. Voelker, D. R. (1989). Reconstitution of phosphatidylserine import into rat liver mitochondria. J. Biol. Chem. 264, 8019-8025.
38. Voelker, D. R. (2009). Genetic and biochemical analysis of non-vesicular lipid traffic. Annu. Rev. Biochem. 78, 827-856.
39. Voeltz, G. K., Prinz, W. A., Shibata, Y., Rist, J. M. and Rapoport, T. A. (2006). A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124, 573-586.
40. Wang, F., Zhao, Y. and Wang, P. (2003). Separation and determination of phospholipids in biological samples by high-performance liquid chromatography. J. Chromatogr. Sci. 41, 142-144.
41. Waterman-Storer, C. M. and Salmon, E. D. (1998). Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms. Curr. Biol. 8, 798-807.
42. West, M., Zurek, N., Hoenger, A. and Voeltz, G. K. (2011). A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature. J. Cell Biol. 193, 333-346.
43. Zinser, E., Sperka-Gottlieb, C. D., Fasch, E. V., Kohlwein, S. D., Paltauf, F. and Daum, G. (1991). Phospholipid synthesis and lipid composition of subcellular membranes in the unicellular eukaryote Saccharomyces cerevisiae. J. Bacteriol. 173, 2026-2034.