A close-up view of membrane contact sites between the endoplasmic reticulum and the endolysosomal system: From yeast to man

Critical Reviews in Biochemistry and Molecular Biology

Volumn 49, Issue 3, 2014, Pages 262-268

  Hönscher, Carina ^a   Ungermann, Christian ^a  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

Endosome; Membrane contact site; Nuclear endoplasmic reticulum; Tether; Vacuole

Indexed keywords

CHOLESTEROL; LIPID TRANSFER PROTEIN;

BIOGENESIS; CELL CONTACT; CELL JUNCTION; CELL MEMBRANE; CELL NUCLEUS; CELL ORGANELLE; CELLULAR DISTRIBUTION; COMPARATIVE STUDY; CYTOLOGY; ENDOPLASMIC RETICULUM; ENDOSOME; HUMAN; LYSOSOME; LYSOSOME MEMBRANE; MALE; MAMMAL CELL; MEMBRANE CONTACT SITE; MITOCHONDRIAL GENOME; MITOCHONDRION; NONHUMAN; NUCLEUS VACUOLE JUNCTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROCESSING; REGULATORY MECHANISM; REVIEW; TONOPLAST; YEAST; ANIMAL; CELL VACUOLE; METABOLISM; SACCHAROMYCES CEREVISIAE; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; ENDOPLASMIC RETICULUM; ENDOSOMES; HUMANS; LYSOSOMES; SACCHAROMYCES CEREVISIAE; VACUOLES; YEASTS;

EID: 84901849884     PISSN: 10409238     EISSN: 15497798     Source Type: Journal    
DOI: 10.3109/10409238.2013.875512     Document Type: Review

References (104)

1. Balderhaar HJK, Ungermann C. (2013). CORVET and HOPS tethering complexes - coordinators of endosome and lysosome fusion. J Cell Sci 126:1307-16.
2. Baumann NA, Sullivan DP, Ohvo-Rekilä H, et al. (2005). Transport of newly synthesized sterol to the sterol-enriched plasma membrane occurs via nonvesicular equilibration. Biochemistry 44:5816-26. (Pubitemid 40525118)
3. Beh CT, McMaster CR, Kozminski KG, et al. (2012). A detour for yeast oxysterol binding proteins. J Biol Chem 287:11481-8.
4. Bodenmiller B, Campbell D, Gerrits B, et al. (2008). PhosphoPep - a database of protein phosphorylation sites in model organisms. Nature Biotechnol 26:1339-40.
5. Copeland DE, Dalton AJ. (1959). An association between mitochondria and the endoplasmic reticulum in cells of the pseudobranch gland of a teleost. J Biophys Biochem Cytol 5:393-6.
6. Cunningham KW. (2011). Acidic calcium stores of Saccharomyces cerevisiae. Cell Calcium 50:129-38.
7. Dawaliby R, Mayer A. (2010). Microautophagy of the nucleus coincides with a vacuolar diffusion barrier at nuclear-vacuolar junctions. Mol Biol Cell 21:4173-83.
8. de Brito OM, Scorrano L. (2008). Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456:605-10.
9. de Saint-Jean M, Delfosse V, Douguet D, et al. (2011). Osh4p exchanges sterols for phosphatidylinositol 4-phosphate between lipid bilayers. J Cell Biol 195:965-78.
10. Dietrich LEP, Ungermann C. (2004). On the mechanism of protein palmitoylation. EMBO Reports 5:1053-7. (Pubitemid 39600203)
11. Du X, Yang H. (2012). Endosomal cholesterol trafficking: protein factors at a glance. Acta Biochim Biophys Sinica 45:11-17.
12. 2+ by yeast vacuoles. J Biol Chem 269:7273-8.
13. Eden ER, White IJ, Tsapara A, et al. (2010). Membrane contacts between endosomes and ER provide sites for PTP1B-epidermal growth factor receptor interaction. Nature 12:267-72.
14. Elbaz Y, Schuldiner M. (2011). Staying in touch: the molecular era of organelle contact sites. Trends Biochem Sci 36:616-23.
15. Fratti RA, Jun Y, Merz AJ, et al. (2004). Interdependent assembly of specific regulatory lipids and membrane fusion proteins into the vertex ring domain of docked vacuoles. J Cell Biol 167:1087-98. (Pubitemid 40066624)
16. Friedman JR, DiBenedetto JR, West M, et al. (2013). Endoplasmic reticulum-endosome contact increases as endosomes traffic and mature. Mol Biol Cell 24:1030-40.
17. Friedman JR, Lackner LL, West M, et al. (2011). ER tubules mark sites of mitochondrial division. Science 334:358-62.
18. 2+-regulated ER-PM interactions mediated by the extended Synaptotagmins. Cell 153:1494-509.
19. Grossmann G, Opekarová M, Malinsky J, et al. (2007). Membrane potential governs lateral segregation of plasma membrane proteins and lipids in yeast. EMBO J 26:1-8. (Pubitemid 46094694)
20. Hanekamp T, Thorsness MK, Rebbapragada I, et al. (2002). Maintenance of mitochondrial morphology is linked to maintenance of the mitochondrial genome in Saccharomyces cerevisiae. Genetics 162:1147-56. (Pubitemid 35417508)
21. Helle SCJ, Kanfer G, Kolar K, et al. (2013). Organization and function of membrane contact sites. Biochim Biophys Acta Mol Cell Res 1833: 2526-41.
22. Hobbs AEA, Srinivasan M, McCaffery JM, et al. (2001). Mmm1p, a mitochondrial outer membrane protein, is connected to mitochondrial DNA (mtDNA) nucleoids and required for mtDNA stability. J Cell Biol 152:401-10. (Pubitemid 34285608)
23. Holthuis JCM, Ungermann C. (2013). Cellular microcompartments constitute general suborganellar functional units in cells. Biol Chem 394:151-61.
24. Hou H, Subramanian K, LaGrassa TJ, et al. (2005). The DHHC protein Pfa3 affects vacuole-associated palmitoylation of the fusion factor Vac8. Proc Nat Acad Sci U S A 102:17366-71. (Pubitemid 41740872)
25. Huotari J, Helenius A. (2011). Endosome maturation. EMBO J 30: 3481-500.
26. Im YJ, Raychaudhuri S, Prinz WA, et al. (2005). Structural mechanism for sterol sensing and transport by OSBP-related proteins. Nature 437: 154-8. (Pubitemid 41613443)
27. Ishihara N. (2004). Mitofusin 1 and 2 play distinct roles in mitochondrial fusion reactions via GTPase activity. J Cell Sci 117:6535-46. (Pubitemid 40214575)
28. Itoh T, Toh-E A, Matsui Y. (2004). Mmr1p is a mitochondrial factor for Myo2p-dependent inheritance of mitochondria in the budding yeast. EMBO J 23:2520-30. (Pubitemid 38988224)
29. Iwanaga T, Tsutsumi R, Noritake J, et al. (2009). Dynamic protein palmitoylation in cellular signaling. Prog Lipid Res 48:117-27.
30. Johansson M, Lehto M, Tanhuanpää K, et al. (2005). The oxysterolbinding protein homologue ORP1L interacts with Rab7 and alters functional properties of late endocytic compartments. Mol Biol Cell 16:5480-92. (Pubitemid 41752200)
31. Kaplan MR, Simoni RD. (1985). Intracellular transport of phosphatidylcholine to the plasma membrane. J Cell Biol 101:441-5. (Pubitemid 15239119)
32. Kawano M. (2006). Efficient trafficking of ceramide from the endoplasmic reticulum to the Golgi apparatus requires a VAMP-associated protein-interacting FFAT motif of CERT. J Biol Chem 281:30279-88. (Pubitemid 44537035)
33. 2+ signals. J Cell Sci 126:60-6.
34. Klecker T, Scholz D, Fortsch J, et al. (2013). The yeast cell cortical protein Num1 integrates mitochondrial dynamics into cellular architecture. J Cell Sci 126:2924-30.
35. Kohlwein SD, Eder S, Oh CS, et al. (2001). Tsc13p is required for fatty acid elongation and localizes to a novel structure at the nuclearvacuolar interface in Saccharomyces cerevisiae. Mol Cell Biol 21: 109-25.
36. Kopec KO, Alva V, Lupas AN. (2010). Homology of SMP domains to the TULIP superfamily of lipid-binding proteins provides a structural basis for lipid exchange between ER and mitochondria. Bioinformatics 26:1927-31.
37. Kopec KO, Alva V, Lupas AN. (2011). Bioinformatics of the TULIP domain superfamily. Biochem Soc Trans 39:1033-8.
38. Kormanec J, Schaaff-Gerstenschläger I, Zimmermann FK, et al. (1991). Nuclear migration in Saccharomyces cerevisiae is controlled by the highly repetitive 313 kDa NUM1 protein. Mol General Genet 230:277-87.
39. Kornmann B. (2013). The molecular hug between the ER and the mitochondria. Curr Opin Cell Biol 25:443-8.
40. Kornmann B, Walter P. (2010). ERMES-mediated ER-mitochondria contacts: molecular hubs for the regulation of mitochondrial biology. J Cell Sci 123:1389-93.
41. Kornmann B, Currie E, Collins SR, et al. (2009). An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325:1033-8.
42. Kornmann B, Osman C, Walter P. (2011). The conserved GTPase Gem1 regulates endoplasmic reticulum-mitochondria connections. Proc Nat Acad Sci U S A 108:14151-6.
43. Koshiba T. (2004). Structural basis of mitochondrial tethering by mitofusin complexes. Science 305:858-62. (Pubitemid 39038419)
44. Kvam E. (2004). Nvj1p is the outer-nuclear-membrane receptor for oxysterol-binding protein homolog Osh1p in Saccharomyces cerevisiae. J Cell Sci 117:4959-68. (Pubitemid 39517512)
45. Kvam E, Goldfarb DS. (2007). Nucleus-vacuole junctions and piecemeal microautophagy of the nucleus in S. cerevisiae. Autophagy 3:85-92. (Pubitemid 46449095)
46. Kvam E, Gable K, Dunn TM, et al. (2005). Targeting of Tsc13p to nucleus-vacuole junctions: a role for very-long-chain fatty acids in the biogenesis of microautophagic vesicles. Mol Biol Cell 16: 3987-98. (Pubitemid 41262872)
47. Lackner LL. (2013). Determining the shape and cellular distribution of mitochondria: the integration of multiple activities. Curr Opin Cell Biol 25:471-6.
48. Lee I. (2006). Diverse membrane-associated proteins contain a novel SMP domain. FASEB J 20:202-6. (Pubitemid 44933166)
49. Lev S, Halevy DB, Peretti D, et al. (2008). The VAP protein family: from cellular functions to motor neuron disease. Trends Cell Biol 18: 282-90.
50. Levental I, Lingwood D, Grzybek M, et al. (2010). Palmitoylation regulates raft affinity for the majority of integral raft proteins. Proc Nat Acad Sci U S A 107:22050-4.
51. Levine TP, Munro S. (2001). Dual targeting of Osh1p, a yeast homologue of oxysterol-binding protein, to both the Golgi and the nucleus-vacuole junction. Mol Biol Cell 12:1633-44. (Pubitemid 33049719)
52. Li SC, Kane PM. (2009). The yeast lysosome-like vacuole: Endpoint and crossroads. Biochim Biophys Acta Mol Cell Res 1793:650-63.
53. Loewen CJR. (2004). Phospholipid metabolism regulated by a transcription factor sensing phosphatidic acid. Science 304:1644-7.
54. Loewen CJR, Roy A, Levine TP. (2003). A conserved ER targeting motif in three families of lipid binding proteins and in Opi1p binds VAP. EMBO J 22:2025-35. (Pubitemid 36565528)
55. Lynch-Day MA, Klionsky DJ. (2010). The Cvt pathway as a model for selective autophagy. FEBS Lett 584:1359-66.
56. Lynes EM, Bui M, Yap MC, et al. (2011). Palmitoylated TMX and calnexin target to the mitochondria-associated membrane. EMBO J 31:457-70.
57. Manford AG, Stefan CJ, Yuan HL, et al. (2012). ER-to-plasma membrane tethering proteins regulate cell signaling and ER morphology. Develop Cell 23:1129-40.
58. Meeusen S. (2003). Evidence for a two membrane-spanning autonomous mitochondrial DNA replisome. J Cell Biol 163:503-10. (Pubitemid 37429864)
59. Meisinger C, Rissler M, Chacinska A, et al. (2004). The mitochondrial morphology protein Mdm10 functions in assembly of the preprotein translocase of the outer membrane. Develop Cell 7:61-71. (Pubitemid 39172688)
60. Meisinger C, Wiedemann N, Rissler M, et al. (2006). Mitochondrial protein sorting: differentiation of beta-barrel assembly by Tom7- mediated segregation of Mdm10. J Biol Chem 281:22819-26.
61. Mesmin B, Bigay J, von Filseck JM, et al. (2013). A four-step cycle driven by PI(4)P hydrolysis directs sterol/PI(4)P exchange by the ERGolgi tether OSBP. Cell 155:830-43.
62. Mijaljica D, Prescott M, Devenish RJ. (2010). The intricacy of nuclear membrane dynamics during nucleophagy. Nucleus 1:213-23.
63. Millen JI, Pierson J, Kvam E, et al. (2008). The luminal N-terminus of yeast Nvj1 is an inner nuclear membrane anchor. Traffic 9:1653-64.
64. Murley A, Lackner LL, Osman C, et al. (2013). ER-associated mitochondrial division links the distribution of mitochondria and mitochondrial DNA in yeast. eLife 2:e00422.
65. Nguyen TT, Lewandowska A, Choi J-Y, et al. (2012). Gem1 and ERMES do not directly affect phosphatidylserine transport from ER to mitochondria or mitochondrial inheritance. Traffic 13:880-90.
66. Pan X, Roberts P, Chen Y, et al. (2000). Nucleus-vacuole junctions in Saccharomyces cerevisiae are formed through the direct interaction of Vac8p with Nvj1p. Mol Biol Cell 11:2445-57. (Pubitemid 30489926)
67. Paschen SA, Neupert W, Rapaport D. (2005). Biogenesis of b-barrel membrane proteins of mitochondria. Trends Biochem Sci 30:575-82. (Pubitemid 41356496)
68. Peng Y, Tang F, Weisman LS. (2006). Palmitoylation plays a role in targeting Vac8p to specific membrane subdomains. Traffic 7:1378-87. (Pubitemid 44364175)
69. Pfeffer SR. (2013). Rab GTPase regulation of membrane identity. Curr Opin Cell Biol 25:414-19.
70. Platt FM, Boland B, van der Spoel AC. (2012). The cell biology of disease: Lysosomal storage disorders: The cellular impact of lysosomal dysfunction. J Cell Biol 199:723-34.
71. Roberts P, Moshitch-Moshkovitz S, Kvam E, et al. (2003). Piecemeal microautophagy of nucleus in Saccharomyces cerevisiae. Mol Biol Cell 14:129-141. (Pubitemid 36106025)
72. Rocha N, Kuijl C, van der Kant R, et al. (2009). Cholesterol sensor ORP1L contacts the ER protein VAP to control Rab7-RILPp150Glued and late endosome positioning. J Cell Biol 185:1209-25.
73. Rowland AA, Voeltz GK. (2012). Endoplasmic reticulum-mitochondria contacts: function of the junction. Nat Rev Mol Cell Biol 13:607-15.
74. Schulz TA, Prinz WA. (2007). Sterol transport in yeast and the oxysterol binding protein homologue (OSH) family. Biochim Biophys Acta 1771:769-80. (Pubitemid 46863503)
75. Scott SV, Nice DC, Nau JJ, et al. (2000). Apg13p and Vac8p are part of a complex of phosphoproteins that are required for cytoplasm to vacuole targeting. J Biol Chem 275:25840-9.
76. Sleight RG, Pagano RE. (1983). Rapid appearance of newly synthesized phosphatidylethanolamine at the plasma membrane. J Biol Chem 258: 9050-8.
77. Smotrys JE, Linder ME. (2004). Palmitoylation of intracellular signaling proteins: regulation and function. Ann Rev Biochem 73:559-87. (Pubitemid 39050380)
78. Solinger JA, Spang A. (2013). Tethering complexes in the endocytic pathway: CORVET and HOPS. FEBS J 280:2743-57.
79. Stark C, Su TC, Breitkreutz A, et al. (2010). PhosphoGRID: a database of experimentally verified in vivo protein phosphorylation sites from the budding yeast Saccharomyces cerevisiae. Database 2010: bap026-bap026.
80. Stefan CJ, Manford AG, Emr SD. (2013). ER-PM connections: sites of information transfer and inter-organelle communication. Curr Opin Cell Biol 25:1-9.
81. Stefan CJ, Manford AG, Baird D, et al. (2011). Osh proteins regulate phosphoinositide metabolism at ER-plasma membrane contact sites. Cell 144:389-401.
82. Subramanian K, Dietrich LEP, Hou H, et al. (2006). Palmitoylation determines the function of Vac8 at the yeast vacuole. J Cell Sci 119: 2477-85. (Pubitemid 44070429)
83. Swayne TC, Zhou C, Boldogh IR, et al. (2011). Role for cER and Mmr1p in anchorage of mitochondria at sites of polarized surface growth in budding yeast. Curr Biol 21:1994-9.
84. Tang F, Kauffman EJ, Novak JL, et al. (2003). Regulated degradation of a class V myosin receptor directs movement of the yeast vacuole. Nature 422:87-92. (Pubitemid 36323301)
85. Tang F, Peng Y, Nau JJ, et al. (2006). Vac8p, an armadillo repeat protein, coordinates vacuole inheritance with multiple vacuolar processes. Traffic 7:1368-77. (Pubitemid 44364174)
86. Tavassoli S, Chao JT, Young BP, et al. (2013). Plasma membrane - endoplasmic reticulum contact sites regulate phosphatidylcholine synthesis. EMBO Reports 14:434-40.
87. Tewari R, Bailes E, Bunting KA, et al. (2010). Armadillo-repeat protein functions: questions for little creatures. Trends Cell Biol 20:470-81.
88. Toulmay A, Prinz WA. (2013). Direct imaging reveals stable, micrometer- scale lipid domains that segregate proteins in live cells. J Cell Biol 202:35-44.
89. Toulmay A, Prinz WA. (2012). A conserved membrane-binding domain targets proteins to organelle contact sites. J Cell Sci 125:49-58.
90. van der Kant R, Fish A, Janssen L, et al. (2013a). Late endosomal transport and tethering are coupled processes controlled by RILP and the cholesterol sensor ORP1L. J Cell Sci 126:3462-74.
91. van der Kant R, Zondervan I, Janssen L, et al. (2013b). Cholesterolbinding molecules MLN64 and ORP1L mark distinct late endosomes with transporters ABCA3 and NPC1. J Lipid Res 54:2153-65.
92. Vance JE. (1990). Phospholipid synthesis in a membrane fraction associated with mitochondria. J Biol Chem 265:7248-56.
93. Vance JE. (2010). Transfer of cholesterol by the NPC team. Cell Metabol 12:105-6.
94. Veit M, Laage R, Dietrich L, et al. (2001). Vac8p release from the SNARE complex and its palmitoylation are coupled and essential for vacuole fusion. EMBO J 20:3145-55. (Pubitemid 32612002)
95. Vihervaara T, Jansen M, Uronen R-L, et al. (2011). Cytoplasmic oxysterol-binding proteins: sterol sensors or transporters? Chem Phys Lipids 164:443-50.
96. Wang YX. (2001). Fusion of docked membranes requires the armadillo repeat protein Vac8p. J Biol Chem 276:35133-40.
97. Wang YX, Catlett NL, Weisman LS. (1998). Vac8p, a vacuolar protein with armadillo repeats, functions in both vacuole inheritance and protein targeting from the cytoplasm to vacuole. J Cell Biol 140: 1063-74. (Pubitemid 28128867)
98. Wang T, Ming Z, Xiaochun W, Hong W. (2011). Rab7: role of its protein interaction cascades in endo-lysosomal traffic. Cell Signal 23:516-21.
99. Warnock DE, Lutz MS, Blackburn WA, et al. (1994). Transport of newly synthesized glucosylceramide to the plasma membrane by a non- Golgi pathway. Proc Nat Acad Sci U S A 91:2708-12. (Pubitemid 24139417)
100. Westermann B. (2008). Molecular machinery of mitochondrial fusion and fission. J Biol Chem 283:13501-5.
101. Wickner WT. (2013). Profile of Thomas Sudh of, James Rothman, and Randy Schekman, 2013 Nobel Laureates in Physiology or Medicine. Proc Nat Acad Sci U S A 110:18349-50.
102. Woodman PG, Futter CE. (2008). Multivesicular bodies: co-ordinated progression to maturity. Curr Opin Cell Biol 20:408-14.
103. Wullschleger S, Loewith R, Hall MN. (2006). TOR signaling in growth and metabolism. Cell 124:471-84. (Pubitemid 43199434)
104. Yamano K, Tanaka-Yamano S, Endo T. (2010). Tom7 regulates Mdm10- mediated assembly of the mitochondrial import channel protein Tom40. J Biol Chem 285:41222-31.