Structure and function of ER membrane contact sites with other organelles
Open accessAbstract
The endoplasmic reticulum (ER) is the largest organelle in the cell, and its functions have been studied for decades. The past several years have provided novel insights into the existence of distinct domains between the ER and other organelles, known as membrane contact sites (MCSs). At these contact sites, organelle membranes are closely apposed and tethered, but do not fuse. Here, various protein complexes can work in concert to perform specialized functions such as binding, sensing and transferring molecules, as well as engaging in organelle biogenesis and dynamics. This Review describes the structure and functions of MCSs, primarily focusing on contacts of the ER with mitochondria and endosomes.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
MAM participate in lipid synthesis, membrane stability, mitochondrial dynamics, and ROS signaling.
“Besides controlling Ca2+ flux, MAM participate in lipid synthesis, membrane stability, mitochondrial dynamics, and ROS signaling [99–101].”
From Neuronal Apolipoprotein E4 Expression Results in Proteome-Wide Alterations and Compromises Bioenergetic Capacity by Disrupting Mitochondrial Function (2019) · cites this paper as [100]
The ER–mitochondria section on lipid biosynthesis and exchange describes phospholipid synthesis and transfer at the contact interface; the Organelle biogenesis > ER–mitochondria section says contact sites help position mitochondrial fission. The passages located do not establish a role in membrane stability or ROS signaling. The discussion of stability in “MCS-bound organelles in motion” concerns the stability of contact sites, not membranes; page numbers are unavailable in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
An ER-Mitochondria Tethering Complex Revealed by a Synthetic Biology Screen
Kornmann, B., Currie, E., Collins, S. R., Schuldiner, M., Nunnari, J., Weissman, J. S., & Walter, P. (2009) · Science · doi:10.1126/science.1175088 · Cited by 1,275 · see citing works
Tanaka, Y., Kanai, Y., Okada, Y., Nonaka, S., Takeda, S., Harada, A., & Hirokawa, N. (1998) · Cell · doi:10.1016/s0092-8674(00)81459-2 · Cited by 654 · see citing works
MiD49 and MiD51, new components of the mitochondrial fission machinery
Palmer, C. S., Osellame, L. D., Laine, D., Koutsopoulos, O. S., Frazier, A. E., & Ryan, M. T. (2011) · The EMBO Reports · doi:10.1038/embor.2011.54 · Cited by 649 · see citing works
Johansson, M., Rocha, N., Zwart, W., Jordens, I., Janssen, L., Kuijl, C., Olkkonen, V. M., & Neefjes, J. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200606077 · Cited by 505 · see citing works
Hurd, D. D., & Saxton, W. M. (1996) · Genetics · doi:10.1093/genetics/144.3.1075 · Cited by 379 · see citing works
Pryor, P. R., Mullock, B. M., Bright, N. A., Gray, S. R., & Luzio, J. P. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.149.5.1053 · Cited by 347 · see citing works
Murley, A., Lackner, L. L., Osman, C., West, M., Voeltz, G. K., Walter, P., & Nunnari, J. (2013) · eLife · doi:10.7554/elife.00422 · Cited by 326 · see citing works
Self-citationMammalian Dynamin-like Protein DLP1 Tubulates Membranes
Yoon, Y., Pitts, K. R., & McNiven, M. A. (2001) · Molecular Biology of the Cell · doi:10.1091/mbc.12.9.2894 · Cited by 285 · see citing works
Flagged first, then by citations
Research works printed but not linked: 110
- [1]Fawcett DW The Cell W. B. Saunders 1981
- [2]Ogata T Yamasaki Y Ultra-high-resolution scanning electron microscopy of mitochondria and sarcoplasmic reticulum arrangement in human red, white, and intermediate muscle fibers Anat Rec 248 214 223 1997 9185987
- [3]Rolls MM Hall DH Victor M Stelzer EHK Rapoport TA Targeting of rough endoplasmic reticulum membrane proteins and ribosomes in invertebrate neurons Mol Biol Cell 13 1778 1791 2002 12006669 PMC111143
- [4]Shibata Y Voeltz GK Rapoport TA Rough sheets and smooth tubules Cell 126 435 439 2006 16901774
- [5]Shibata Y Mechanisms determining the morphology of the peripheral ER Cell 143 774 788 2010 21111237 PMC3008339
- [6]West M Zurek N Hoenger A Voeltz GK A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature J Cell Biol 193 333 346 2011 21502358 PMC3080256
- [7]Alpy F STARD3 or STARD3NL and VAP form a novel molecular tether between late endosomes and the ER J Cell Sci 126 5500 5512 2013 Measured ER–late endosome contact site distance using electron microscopy. Showed that the STARD3 and STARD3NL FFAT domain can interact with ER VAP proteins. Overexpression of STARD3 resulted in expansion of ER–endosome contact sites 24105263
- [8]Csordás G Structural and functional features and significance of the physical linkage between ER and mitochondria J Cell Biol 174 915 921 2006 16982799 PMC2064383
- [9]Friedman JR ER tubules mark sites of mitochondrial division Science 334 358 362 2011 Demonstrated that ER tubules mark the site of mitochondrial division and that ER contact occurs prior to recruitment of the mammalian division machinery DRP1 21885730 PMC3366560
- [10]Friedman JR Dibenedetto JR West M Rowland AA Voeltz GK Endoplasmic reticulum– endosome contact increases as endosomes traffic and mature Mol Biol Cell 24 1030 1040 2013 23389631 PMC3608491
- [11]Eden ER White IJ Tsapara A Futter CE Membrane contacts between endosomes and ER provide sites for PTP1B–epidermal growth factor receptor interaction Nat Cell Biol 12 267 272 2010 20118922
- [12]Swayne TC Role for cER and Mmr1p in anchorage of mitochondria at sites of polarized surface growth in budding yeast Curr Biol 21 1994 1999 2011 22119524 PMC3237857
- [13]Rowland AA Chitwood PJ Phillips MJ Voeltz GK ER contact sites define the position and timing of endosome fission Cell 159 1027 1041 2014 Demonstrated that ER tubules are recruited to pre-established endosome sorting domains that undergo fission to sort cargo, and that ER dynamics are required for endosome fission 25416943 PMC4634643
- [15]Cosson P Marchetti A Ravazzola M Orci L Mitofusin-2 independent juxtaposition of endoplasmic reticulum and mitochondria: an ultrastructural study PLoS ONE 7 e46293 2012 23029466 PMC3460865
- [17]Zajac AL Goldman YE Holzbaur ELF Ostap EM Local cytoskeletal and organelle interactions impact molecular-motor-driven early endosomal trafficking Curr Biol 23 1173 1180 2013 23770188 PMC3738301
- [18]WoŸniak MJ Role of kinesin-1 and cytoplasmic dynein in endoplasmic reticulum movement in VERO cells J Cell Sci 122 1979 1989 2009 19454478 PMC2723153
- [19]Hoepfner S Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B Cell 121 437 450 2005 15882625
- [21]Glater EE Megeath LJ Stowers RS Schwarz TL Axonal transport of mitochondria requires milton to recruit kinesin heavy chain and is light chain independent J Cell Biol 173 545 557 2006 16717129 PMC2063864
- [23]Kornmann B Osman C Walter P The conserved GTPase Gem1 regulates endoplasmic reticulum– mitochondria connections Proc Natl Acad Sci USA 108 14151 14156 2011 21825164 PMC3161550
- [24]Stowers RS Megeath LJ Górska-Andrzejak J Meinertzhagen IA Schwarz TL Axonal transport of mitochondria to synapses depends on Milton, a novel Drosophila protein Neuron 36 1063 1077 2002 12495622
- [25]Saotome M Bidirectional Ca2+-dependent control of mitochondrial dynamics by the Miro GTPase Proc Natl Acad Sci USA 105 20728 20733 2008 19098100 PMC2634948
- [26]Huotari J Helenius A Endosome maturation EMBO J 30 3481 3500 2011 21878991 PMC3181477
- [27]Vihervaara T Sterol binding by OSBP-related protein 1L regulates late endosome motility and function Cell Mol Life Sci 68 537 551 2011 20690035 PMC11114714
- [28]Rocha N Cholesterol sensor ORP1L contacts the ER protein VAP to control Rab7–RILP–p150Glued and late endosome positioning J Cell Biol 185 1209 1225 2009 Discovered that late-endosome-localized ORP1L interacts with ER membrane protein VAP when cholesterol levels are low in the late endosome membrane. ORP1L–VAP interaction inhibits dynein-directed positioning of late endosomes to the cell centre, resulting in late endosomes in the cell periphery 19564404 PMC2712958
- [29]Suchanek M The mammalian oxysterol-binding protein-related proteins (ORPs) bind 25-hydroxycholesterol in an evolutionarily conserved pocket Biochem J 405 473 480 2007 17428193 PMC2267293
- [31]Tsujishita Y Hurley JH Structure and lipid transport mechanism of a StAR-related domain Nat Struct Biol 7 408 414 2000 10802740
- [32]Hölttä-Vuori M MLN64 is involved in actin-mediated dynamics of late endocytic organelles Mol Biol Cell 16 3873 3886 2005 15930133 PMC1182323
- [33]Chang J Lee S Blackstone C Protrudin binds atlastins and endoplasmic reticulum-shaping proteins and regulates network formation Proc Natl Acad Sci USA 110 14954 14959 2013 23969831 PMC3773775
- [34]Raiborg C Repeated ER–endosome contacts promote endosome translocation and neurite outgrowth Nature 520 234 238 2015 Analysis of protrudin domains showed that protrudin interacts with the late endosome through PtdIns(3)P and RAB7, creating an ER–late endosome MCS. When the ER–late endosome MCS is formed, protrudin delivers kinesin-1 to FYCO1, which links the kinesin-1 to the late endosome RAB7. This promotes trafficking of late endosomes to the cell exterior 25855459
- [35]Pankiv S FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end-directed vesicle transport J Cell Biol 188 253 269 2010 20100911 PMC2812517
- [36]Matsuzaki F Shirane M Matsumoto M Nakayama KI Protrudin serves as an adaptor molecule that connects KIF5 and its cargoes in vesicular transport during process formation Mol Biol Cell 22 4602 4620 2011 21976701 PMC3226478
- [37]Vance JE Aasman EJ Szarka R Brefeldin A does not inhibit the movement of phosphatidylethanolamine from its sites for synthesis to the cell surface J Biol Chem 266 8241 8247 1991 2022641
- [38]Wirtz KW Zilversmit DB Exchange of phospholipids between liver mitochondria and microsomes in vitro J Biol Chem 243 3596 3602 1968 4968799
- [39]Lev S Non-vesicular lipid transport by lipid-transfer proteins and beyond Nat Rev Mol Cell Biol 11 739 750 2010 20823909
- [40]Im YJ Raychaudhuri S Prinz WA Hurley JH Structural mechanism for sterol sensing and transport by OSBP-related proteins Nature 437 154 158 2005 16136145 PMC1431608
- [41]Kopec KO Alva V Lupas AN Bioinformatics of the TULIP domain superfamily Biochem Soc Trans 39 1033 1038 2011 21787343
- [42]Dennis EA Kennedy EP Intracellular sites of lipid synthesis and the biogenesis of mitochondria J Lipid Res 13 263 267 1972 5016308
- [43]Osman C Voelker DR Langer T Making heads or tails of phospholipids in mitochondria J Cell Biol 192 7 16 2011 21220505 PMC3019561
- [44]Toulmay A Prinz WA A conserved membrane-binding domain targets proteins to organelle contact sites J Cell Sci 125 49 58 2012 22250200 PMC3269022
- [45]Schauder CM Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer Nature 510 552 555 2014 24847877 PMC4135724
- [46]Osman C The genetic interactome of prohibitins: coordinated control of cardiolipin and phosphatidylethanolamine by conserved regulators in mitochondria J Cell Biol 184 583 596 2009 19221197 PMC2654118
- [47]Tamura Y Role for two conserved intermembrane space proteins, Ups1p and Ups2p, [corrected] in intra-mitochondrial phospholipid trafficking J Biol Chem 287 15205 15218 2012 22403410 PMC3346110
- [48]Tan T Ozbalci C Brügger B Rapaport D Dimmer KS Mcp1 and Mcp2, two novel proteins involved in mitochondrial lipid homeostasis J Cell Sci 126 3563 3574 2013 23781023
- [49]Nguyen TT Gem1 and ERMES do not directly affect phosphatidylserine transport from ER to mitochondria or mitochondrial inheritance Traffic 13 880 890 2012 22409400 PMC3648210
- [50]Voss C Lahiri S Young BP Loewen CJ Prinz WA ER-shaping proteins facilitate lipid exchange between the ER and mitochondria in S. cerevisiae J Cell Sci 125 4791 4799 2012 22797914 PMC4074283
- [51]Elbaz-Alon Y A dynamic interface between vacuoles and mitochondria in yeast Dev Cell 30 95 102 2014 25026036
- [52]Hönscher C Cellular metabolism regulates contact sites between vacuoles and mitochondria Dev Cell 30 86 94 2014 25026035
- [53]Möbius W Recycling compartments and the internal vesicles of multivesicular bodies harbor most of the cholesterol found in the endocytic pathway Traffic 4 222 231 2003 12694561
- [54]Neufeld EB Intracellular trafficking of cholesterol monitored with a cyclodextrin J Biol Chem 271 21604 21613 1996 8702948
- [55]Liscum L Ruggiero RM Faust JR The intracellular transport of low density lipoprotein-derived cholesterol is defective in Niemann-Pick type C fibroblasts J Cell Biol 108 1625 1636 1989 2715172 PMC2115531
- [56]Infante RE NPC2 facilitates bidirectional transfer of cholesterol between NPC1 and lipid bilayers, a step in cholesterol egress from lysosomes Proc Natl Acad Sci USA 105 15287 15292 2008 18772377 PMC2563079
- [57]Kwon HJ Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol Cell 137 1213 1224 2009 19563754 PMC2739658
- [58]Du X A role for oxysterol-binding protein-related protein 5 in endosomal cholesterol trafficking J Cell Biol 192 121 135 2011 Demonstrated that depletion of tail-anchored ER protein ORP5 resulted in cholesterol accumulation in the external membranes of late endosomes, leading to the model in which ORP5 accepts cholesterol from late endosome NPC1 and transfers it to the ER 21220512 PMC3019559
- [59]Van der Kant R Zondervan I Janssen L Neefjes J Cholesterol-binding molecules MLN64 and ORP1L mark distinct late endosomes with transporters ABCA3 and NPC1 J Lipid Res 54 2153 2165 2013 23709693 PMC3708365
- [60]Peretti D Dahan N Shimoni E Hirschberg K Lev S Coordinated lipid transfer between the endoplasmic reticulum and the Golgi complex requires the VAP proteins and is essential for Golgi-mediated transport Mol Biol Cell 19 3871 3884 2008 18614794 PMC2526681
- [61]Hanada K Molecular machinery for non-vesicular trafficking of ceramide Nature 426 803 809 2003 14685229
- [62]D’Angelo G Glycosphingolipid synthesis requires FAPP2 transfer of glucosylceramide Nature 449 62 67 2007 17687330
- [63]Litvak V Dahan N Ramachandran S Sabanay H Lev S Maintenance of the diacylglycerol level in the Golgi apparatus by the Nir2 protein is critical for Golgi secretory function Nat Cell Biol 7 225 234 2005 15723057
- [64]Mesmin B A four-step cycle driven by PI(4)P hydrolysis directs sterol/PI(4)P exchange by the ER–Golgi tether OSBP Cell 155 830 843 2013 Demonstrated that OSBP binding to PtdIns(4)P localizes OSBP to the Golgi. OSBP moves sterol from the ER to the Golgi. OSBP moves PtdIns(4)P to the ER, where it is hydrolysed. Depletion of PtdIns(4)P from the Golgi membrane results in OSBP dissociation from the Golgi membrane 24209621
- [65]Perry RJ Ridgway ND Oxysterol-binding protein and vesicle-associated membrane protein-associated protein are required for sterol-dependent activation of the ceramide transport protein Mol Biol Cell 17 2604 2616 2006 16571669 PMC1474796
- [66]Loewen CJR Roy A Levine TP A conserved ER targeting motif in three families of lipid binding proteins and in Opi1p binds VAP EMBO J 22 2025 2035 2003 12727870 PMC156073
- [67]Lev S Ben Halevy D Peretti D Dahan N The VAP protein family: from cellular functions to motor neuron disease Trends Cell Biol 18 282 290 2008 18468439
- [68]Amarilio R Ramachandran S Sabanay H Lev S Differential regulation of endoplasmic reticulum structure through VAP–Nir protein interaction J Biol Chem 280 5934 5944 2005 15545272
- [69]Foskett JK White C Cheung K Mak DD Inositol trisphosphate receptor Ca2+ release channels Physiol Rev 87 593 658 2007 17429043 PMC2901638
- [70]Tovey SC Dedos SG Taylor EJA Church JE Taylor CW Selective coupling of type 6 adenylyl cyclase with type 2 IP3 receptors mediates direct sensitization of IP3 receptors by cAMP J Cell Biol 183 297 311 2008 18936250 PMC2568025
- [71]Taylor CW Tovey SC IP3 receptors: toward understanding their activation Cold Spring Harb Perspect Biol 2 a004010 2010 20980441 PMC2982166
- [72]Shuai J Parker I Optical single-channel recording by imaging Ca2+ flux through individual ion channels: theoretical considerations and limits to resolution Cell Calcium 37 283 299 2005 15755490
- [73]Rizzuto R Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses Science 280 1763 1766 1998 9624056
- [74]Morgan AJ Bidirectional Ca2+ signaling occurs between the endoplasmic reticulum and acidic organelles J Cell Biol 200 789 805 2013 Demonstrated that stimulated ER Ca2+ release can activate NAADP-regulated channels on the lysosome and result in Ca2+ release from lysosomes 23479744 PMC3601362
- [75]De Stefani D Raffaello A Teardo E Szabò I Rizzuto R A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter Nature 476 336 340 2011 21685888 PMC4141877
- [76]Baughman JM Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter Nature 476 341 345 2011 21685886 PMC3486726
- [77]Rizzuto R De Stefani D Raffaello A Mammucari C Mitochondria as sensors and regulators of calcium signalling Nat Rev Mol Cell Biol 13 566 578 2012 22850819
- [78]Scorrano L BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis Science 300 135 139 2003 12624178
- [79]Zong WX Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis J Cell Biol 162 59 69 2003 12847083 PMC2172724
- [80]Rizzuto R Brini M Murgia M Pozzan T Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria Science 262 744 747 1993 8235595
- [81]Csordás G Imaging interorganelle contacts and local calcium dynamics at the ER–mitochondrial interface Mol Cell 39 121 132 2010 Adjusted ER–mitochondria contact site distance using artificial tethers and showed that distance between ER and mitochondria affects Ca2+ transfer at the ER–mitochondria MCS 20603080 PMC3178184
- [82]De Brito OM Scorrano L Mitofusin 2 tethers endoplasmic reticulum to mitochondria Nature 456 605 610 2008 19052620
- [83]Filadi R Mitofusin 2 ablation increases endoplasmic reticulum–mitochondria coupling Proc Natl Acad Sci USA 112 E2174 E2181 2015 25870285 PMC4418914
- [84]Szabadkai G Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels J Cell Biol 175 901 911 2006 17178908 PMC2064700
- [85]Giorgi C PML regulates apoptosis at endoplasmic reticulum by modulating calcium release Science 330 1247 1251 2010 21030605 PMC3017677
- [86]Marchi S Akt kinase reducing endoplasmic reticulum Ca2+ release protects cells from Ca2+-dependent apoptotic stimuli Biochem Biophys Res Commun 375 501 505 2008 18723000 PMC2576286
- [87]Marchi S Selective modulation of subtype III IP3R by Akt regulates ER Ca2+ release and apoptosis Cell Death Dis 3 e304 2012 22552281 PMC3366079
- [88]Gerasimenko JV Tepikin aV Petersen OH Gerasimenko OV Calcium uptake via endocytosis with rapid release from acidifying endosomes Curr Biol 8 1335 1338 1998 9843688
- [90]Morgan AJ Platt FM Lloyd-Evans E Galione A Molecular mechanisms of endolysosomal Ca2+ signalling in health and disease Biochem J 439 349 374 2011 21992097
- [91]Albrecht T Zhao Y Nguyen TH Campbell RE Johnson JD Fluorescent biosensors illuminate calcium levels within defined beta-cell endosome subpopulations Cell Calcium 57 263 274 2015 25682167
- [92]Christensen KA Myers JT Swanson J A pH-dependent regulation of lysosomal calcium in macrophages 115 599 607 2002 11861766
- [93]Lloyd-Evans E Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium Nat Med 14 1247 1255 2008 18953351
- [94]Abe K Puertollano R Role of TRP channels in the regulation of the endosomal pathway Physiology 26 14 22 2011 21357899 PMC3408074
- [95]Lelouvier B Puertollano R Mucolipin-3 regulates luminal calcium, acidification, and membrane fusion in the endosomal pathway J Biol Chem 286 9826 9832 2011 21245134 PMC3058973
- [96]Ruas M Purified TPC isoforms form NAADP receptors with distinct roles for Ca2+ signaling and endolysosomal trafficking Curr Biol 20 703 709 2010 20346675 PMC2861162
- [97]Kilpatrick BS Eden ER Schapira AH Futter CE Patel S Direct mobilisation of lysosomal Ca2+ triggers complex Ca2+ signals J Cell Sci 126 60 66 2013 23108667 PMC4208295
- [98]López-Sanjurjo CI Tovey SC Prole DL Taylor CW Lysosomes shape Ins(1,4,5)P3-evoked Ca2+ signals by selectively sequestering Ca2+ released from the endoplasmic reticulum J Cell Sci 126 289 300 2013 Measured pH-adjusted Ca2+ levels in the lysosome and demonstrated that Ca2+ levels increase in the lysosome upon ER Ins(1,4,5)P3R stimulation, leading to the idea that lysosomes can sequester ER Ca2+ 23097044 PMC3603520
- [99]Nunnari J Suomalainen A Mitochondria: in sickness and in health Cell 148 1145 1159 2012 22424226 PMC5381524
- [100]Otsuga D The dynamin-related GTPase, Dnm1p, controls mitochondrial morphology in yeast J Cell Biol 143 333 349 1998 9786946 PMC2132834
- [101]Bleazard W The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast Nat Cell Biol 1 298 304 1999 10559943 PMC3739991
- [102]Smirnova E Griparic L Shurland DL van der Bliek AM Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells Mol Biol Cell 12 2245 2256 2001 11514614 PMC58592
- [103]Mears JA Conformational changes in Dnm1 support a contractile mechanism for mitochondrial fission Nat Struct Mol Biol 18 20 26 2011 21170049 PMC3059246
- [104]Ingerman E Dnm1 forms spirals that are structurally tailored to fit mitochondria J Cell Biol 170 1021 1027 2005 16186251 PMC2171542
- [106]Legesse-Miller A Massol RH Kirchhausen T Constriction and Dnm1p recruitment are distinct processes in mitochondrial fission Mol Biol Cell 14 1953 1963 2003 12802067 PMC165089
- [107]Korobova F Ramabhadran V Higgs HN An actin-dependent step in mitochondrial fission mediated by the ER-associated formin INF2 Science 339 464 467 2013 23349293 PMC3843506
- [108]Korobova F Gauvin TJ Higgs HN A role for myosin II in mammalian mitochondrial fission Curr Biol 24 409 414 2014 24485837 PMC3958938
- [109]Losón OC Song Z Chen H Chan DC Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission Mol Biol Cell 24 659 667 2013 23283981 PMC3583668
- [110]Tieu Q Nunnari J Mdv1p is a WD repeat protein that interacts with the dynamin-related GTPase, Dnm1p, to trigger mitochondrial division J Cell Biol 151 353 366 2000 11038182 PMC2192646
- [111]Gandre-Babbe S van der Bliek AM The novel tail-anchored membrane protein Mff controls mitochondrial and peroxisomal fission in mammalian cells Mol Biol Cell 19 2402 2412 2008 18353969 PMC2397315
- [113]Mozdy AD McCaffery JM Shaw JM Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fis1p J Cell Biol 151 367 380 2000 11038183 PMC2192649
- [114]De Vos KJ VAPB interacts with the mitochondrial protein PTPIP51 to regulate calcium homeostasis Hum Mol Genet 21 1299 1311 2012 22131369 PMC3284118
- [115]Iwasawa R Mahul-Mellier AL Datler C Pazarentzos E Grimm S Fis1 and Bap31 bridge the mitochondria–ER interface to establish a platform for apoptosis induction EMBO J 30 556 568 2011 21183955 PMC3034017
- [116]Palande K Peroxiredoxin-controlled G-CSF signalling at the endoplasmic reticulum–early endosome interface J Cell Sci 124 3695 3705 2011 22045733 PMC3215578
- [117]Xu N The FATP1–DGAT2 complex facilitates lipid droplet expansion at the ER–lipid droplet interface J Cell Biol 198 895 911 2012 22927462 PMC3432760
- [118]Knoblach B An ER–peroxisome tether exerts peroxisome population control in yeast EMBO J 32 2439 2453 2013 23900285 PMC3770948
Cited by
Sorted by citations
Galluzzi, L., Vitale, I., Aaronson, S. A., Abrams, J. M., Adam, D., Agostinis, P., Alnemri, E. S., Altucci, L., Amelio, I., Andrews, D. W., et al. (2018) · Cell Death & Differentiation · doi:10.1038/s41418-017-0012-4 · Cited by 6,680 · see citing works
Mechanisms, regulation and functions of the unfolded protein response
Hetz, C., Zhang, K., & Kaufman, R. J. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0250-z · Cited by 2,666 · see citing works
α-synuclein toxicity in neurodegeneration: mechanism and therapeutic strategies
Wong, Y. C., & Krainc, D. (2017) · Nature Medicine · doi:10.1038/nm.4269 · Cited by 897 · see citing works
Biochemical and cellular properties of insulin receptor signalling
Haeusler, R. A., McGraw, T. E., & Accili, D. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.89 · Cited by 739 · see citing works
Endoplasmic reticulum-mitochondrial contactology: structure and signaling functions
Csordás, G., Weaver, D., & Hajnóczky, G. (2018) · Trends in Cell Biology · doi:10.1016/j.tcb.2018.02.009 · Cited by 625 · see citing works
Chakrabarti, R., Ji, W.-K., Stan, R. V., de Juan Sanz, J., Ryan, T. A., & Higgs, H. N. (2018) · Journal of Cell Biology · doi:10.1083/jcb.201709111 · Cited by 349 · see citing works
BCL-2 family: integrating stress responses at the ER to control cell demise
Pihán, P., Carreras-Sureda, A., & Hetz, C. (2017) · Cell Death & Differentiation · doi:10.1038/cdd.2017.82 · Cited by 274 · see citing works
The constriction and scission machineries involved in mitochondrial fission
Kraus, F., & Ryan, M. T. (2017) · Journal of Cell Science · doi:10.1242/jcs.199562 · Cited by 244 · see citing works
Barrera, M.-J., Aguilera, S., Castro, I., Carvajal, P., Jara, D., Molina, C., González, S., & González, M.-J. (2021) · Autoimmunity Reviews · doi:10.1016/j.autrev.2021.102867 · Cited by 213 · see citing works
Proteostasis in cardiac health and disease
Henning, R. H., & Brundel, B. J. J. M. (2017) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2017.89 · Cited by 193 · see citing works
Mitochondrial aspartate regulates TNF biogenesis and autoimmune tissue inflammation
Wu, B., Zhao, T. V., Jin, K., Hu, Z., Abdel, M. P., Warrington, K. J., Goronzy, J. J., & Weyand, C. M. (2021) · Nature Immunology · doi:10.1038/s41590-021-01065-2 · Cited by 141 · see citing works
Vincent, A. E., Turnbull, D. M., Eisner, V., Hajnóczky, G., & Picard, M. (2017) · Trends in Cell Biology · doi:10.1016/j.tcb.2017.08.009 · Cited by 135 · see citing works
Orr, A. L., Kim, C., Jimenez-Morales, D., Newton, B. W., Johnson, J. R., Krogan, N. J., Swaney, D. L., & Mahley, R. W. (2019) · Journal of Alzheimer's Disease · doi:10.3233/jad-181184 · Cited by 103 · see citing works
Mitochondria-cytosol-nucleus crosstalk: learning from Saccharomyces cerevisiae
Guaragnella, N., Coyne, L. P., Chen, X. J., & Giannattasio, S. (2018) · FEMS Yeast Research · doi:10.1093/femsyr/foy088 · Cited by 72 · see citing works
Tubbs, E., & Rieusset, J. (2016) · Journal of Visualized Experiments · doi:10.3791/54899 · Cited by 60 · see citing works
Sigma-1 receptor: a potential therapeutic target for traumatic brain injury
Shi, M., Chen, F., Chen, Z., Yang, W., Yue, S., Zhang, J., & Chen, X. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.685201 · Cited by 58 · see citing works
Krols, M., Asselbergh, B., De Rycke, R., De Winter, V., Seyer, A., Müller, F.-J., Kurth, I., Bultynck, G., Timmerman, V., & Janssens, S. (2019) · Human Molecular Genetics · doi:10.1093/hmg/ddy352 · Cited by 40 · see citing works
Multi-resolution analysis enables fidelity-ensured deconvolution for fluorescence microscopy
Hou, Y., Wang, W., Fu, Y., Ge, X., Li, M., & Xi, P. (2024) · eLight · doi:10.1186/s43593-024-00073-7 · Cited by 42 · see citing works
Molecular Perspectives of Mitochondrial Adaptations and Their Role in Cardiac Proteostasis
Alam, S., Abdullah, C. S., Aishwarya, R., Morshed, M., & Bhuiyan, M. S. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.01054 · Cited by 12 · see citing works
- Authors
- Phillips, M. J., & Voeltz, G. K.
- Affiliations
- University of Colorado Boulder (US)
- Corresponding author
- Voeltz, Gia K.
- ORCID
- Voeltz, Gia K.
- Venue
- Nature Reviews Molecular Cell Biology
- Published
- 2015-12-02
- Volume
- 17
- Issue
- 2
- Pages
- 69-82
- ISSN
- 1471-0072 (ISSN-L)
- 1471-0080
- PMC
- PMC5117888
- OpenAlex
- W2182369134
- Cited by
- 933
- References
- 8
- Citations by year
- 2026: 51 · 2025: 78 · 2024: 100 · 2023: 81 · 2022: 98 · 2021: 107 · 2020: 100 · 2019: 86 · 2018: 97 · 2017: 93 · 2016: 40 · 2015: 2
- FWCI
- 7.80
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Molecular Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- American Cancer Society
- National Institutes of Health
- National Institute of General Medical Sciences (R01GM083977, T32GM008759, GM083977)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- membrane contact sites, endoplasmic reticulum, ER-mitochondria contact sites, organelle tethering, lipid transfer, calcium signaling, organelle biogenesis, organelle dynamics, protein complexes
- MeSH terms
- Animals, Organelle Biogenesis, Biological Transport, Calcium, Cell Membrane, Endoplasmic Reticulum, Eukaryotic Cells, Gene Expression Regulation, Humans, Membrane Proteins, Mitochondria, Endosomes, Saccharomyces cerevisiae, Lipid Metabolism, Mitochondrial Membranes
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review