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Intracellular organelle networks: Understanding their organization and communication through systems-level modeling and analysis |
Qinle Ba1,Ge Yang1,2( ) |
1. Department of Biomedical Engineering, Carnegie Mellon University, Pittsburgh, PA 15213, USA 2. Department of Computational Biology, Carnegie Mellon University, Pittsburgh, PA 15213, USA |
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Abstract BACKGROUND: Membrane-bound intracellular organelles are biochemically distinct compartments used by eukaryotic cells for serving specialized physiological functions and organizing their internal environment. Recent studies revealed surprisingly extensive communication between these organelles and highlighted the network nature of their organization and communication. Since organization and communication of the organelles are carried out at the systems level through their networks, systems-level studies are essential for understanding the underlying mechanisms. METHODS: We reviewed recent studies that used systems-level quantitative modeling and analysis to understand organization and communication of intracellular organelle networks. RESULTS: We first review modeling and analysis studies on how fusion/fission and degradation/biogenesis, two essential and closely related classes of activities of individual organelles, collectively mediate the dynamic organization of their networks. We then turn to another important aspect of the dynamic organization of the organelle networks, namely how organelles are physically connected within their networks, a property referred to as the topology of the networks in mathematics, and summarize some of their distinct properties. Lastly, we briefly review modeling and analysis studies that aim to understand communication between different organelle networks, focusing on cellular calcium homeostasis as an example. We conclude with a brief discussion of future directions for research in this area. CONCLUSIONS: Together, the reviewed studies provide critical insights into how diverse activities of individual organelles collectively mediate the organization and communication of their networks. They demonstrate the essential role of systems-level modeling and analysis in understanding complex behavior of such networks.
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Keywords
intracellular organelle
organelle network
organelle communication
network analysis
systems modeling
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Corresponding Author(s):
Ge Yang
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Just Accepted Date: 23 December 2016
Online First Date: 08 February 2017
Issue Date: 28 February 2017
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|
1 |
Barabasi A L, Oltvai Z N (2004). Network biology: understanding the cell’s functional organization. Nat Rev Genet, 5(2): 101–113
https://doi.org/10.1038/nrg1272
|
2 |
Barrat A, Barthelemy M, Vespignani A (2008). Dynamic Processes on Complex Networks. Cambridge University Press.
|
3 |
Barsoum M J, Yuan H, Gerencser A A, Liot G, Kushnareva Y, Gräber S, Kovacs I, Lee W D, Waggoner J, Cui J, White A D, Bossy B, Martinou J C, Youle R J, Lipton S A, Ellisman M H, Perkins G A, Bossy‐Wetzel E (2006). Nitric oxide‐induced mitochondrial fission is regulated by dynamin‐related GTPases in neurons. EMBO J, 25(16): 3900–3911
https://doi.org/10.1038/sj.emboj.7601253
|
4 |
Berridge M J, Bootman M D, Roderick H L (2003). Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol, 4(7): 517–529
https://doi.org/10.1038/nrm1155
|
5 |
Boccaletti S, Latora V, Moreno Y, Chavez M, Hwang D U (2006). Complex networks: Structure and dynamics. Phys Rep, 424(4-5): 175–308
https://doi.org/10.1016/j.physrep.2005.10.009
|
6 |
Bonifacino J S, Glick B S (2004). The mechanisms of vesicle budding and fusion. Cell, 116(2): 153–166
https://doi.org/10.1016/S0092-8674(03)01079-1
|
7 |
Brandhorst D, Zwilling D, Rizzoli S O, Lippert U, Lang T, Jahn R (2006). Homotypic fusion of early endosomes: SNAREs do not determine fusion specificity. Proc Natl Acad Sci USA, 103(8): 2701–2706
https://doi.org/10.1073/pnas.0511138103
|
8 |
Brini M, Calì T, Ottolini D, Carafoli E (2013). Intracellular Calcium Homeostasis and Signaling. In: Banci L, editor. Metallomics and the Cell. Springer Netherlands, Dordrecht. 119–168
|
9 |
Bucci C, Parton R G, Mather I H, Stunnenberg H, Simons K, Hoflack B, Zerial M (1992). The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell, 70(5): 715–728
https://doi.org/10.1016/0092-8674(92)90306-W
|
10 |
Campbell G E H, Lowe W H, Fagan W F (2007). Living in the branches: population dynamics and ecological processes in dendritic networks. Ecol Lett, 10(2): 165–175
https://doi.org/10.1111/j.1461-0248.2006.01007.x
|
11 |
Carafoli E (1987). Intracellular calcium homeostasis. Annu Rev Biochem, 56(1): 395–433
https://doi.org/10.1146/annurev.bi.56.070187.002143
|
12 |
Chan D C (2012). Fusion and fission: interlinked processes critical for mitochondrial health. Annu Rev Genet, 46(1): 265–287
https://doi.org/10.1146/annurev-genet-110410-132529
|
13 |
Chan Y H M, Marshall W F (2012). How cells know the size of their organelles. Science, 337(6099): 1186–1189
https://doi.org/10.1126/science.1223539
|
14 |
Chen H, Chan D C (2009). Mitochondrial dynamics–fusion, fission, movement, and mitophagy–in neurodegenerative diseases. Hum Mol Genet, 18(R2): R169–R176
https://doi.org/10.1093/hmg/ddp326
|
15 |
Collins T J, Berridge M J, Lipp P, Bootman M D (2002). Mitochondria are morphologically and functionally heterogeneous within cells. EMBO J, 21(7): 1616–1627
https://doi.org/10.1093/emboj/21.7.1616
|
16 |
Csordás G, Várnai P, Golenár T, Roy S, Purkins G, Schneider T G, Balla T, Hajnóczky G (2010). Imaging interorganelle contacts and local calcium dynamics at the ER-mitochondrial interface. Mol Cell, 39(1): 121–132
https://doi.org/10.1016/j.molcel.2010.06.029
|
17 |
Cui J, Kaandorp J A (2006). Mathematical modeling of calcium homeostasis in yeast cells. Cell Calcium, 39(4): 337–348
https://doi.org/10.1016/j.ceca.2005.12.001
|
18 |
Dupont G, Falcke M, Kirk V, Sneyd J (2016). Models of Calcium Signaling. Springer International Publishing
|
19 |
Elbaz Y, Schuldiner M (2011). Staying in touch: the molecular era of organelle contact sites. Trends Biochem Sci, 36(11): 616–623
https://doi.org/10.1016/j.tibs.2011.08.004
|
20 |
Elmore S P, Qian T, Grissom S F, Lemasters J J (2001). The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J, 15(12): 2286–2287
|
21 |
Ferraro F, Kriston-Vizi J, Daniel J (2014). A two-tier Golgi-based control of organelle size underpins the functional plasticity of endothelial cells. Dev Cell, 29(3): 292–304
https://doi.org/10.1016/j.devcel.2014.03.021
|
22 |
Figge M T, Reichert A S, Meyer-Hermann M, Osiewacz H D (2012). Deceleration of fusion-fission cycles improves mitochondrial quality control during aging. PLOS Comput Biol, 8(6): e1002576
https://doi.org/10.1371/journal.pcbi.1002576
|
23 |
Foret L, Jonathan E D, Villasenor R, Collinet C, Deutsch A, Brusch L, Zerial M, Kalaididis Y, Julicher E. (2012). A general theoretical framework to infer endosomal network dynamics from quantitative image analysis. Curr Biol, 22(15): 1381–1390
https://doi.org/10.1016/j.cub.2012.06.021
|
24 |
Frazier A E, Kiu C, Stojanovski D, Hoogenraad Nicholas J, Ryan Michael T (2006). Mitochondrial morphology and distribution in mammalian cells. Biol Chem, 387(12): 1551–1558
https://doi.org/10.1515/BC.2006.193
|
25 |
Frederick R L, Shaw J M (2007). Moving mitochondria: establishing distribution of an essential organelle. Traffic, 8(12): 1668–1675
https://doi.org/10.1111/j.1600-0854.2007.00644.x
|
26 |
Friedman J R, Lackner L L, West M, DiBenedetto J R, Nunnari J, Voeltz G K (2011). ER tubules mark sites of mitochondrial division. Science, 334(6054): 358–362
https://doi.org/10.1126/science.1207385
|
27 |
Gautreau A, Oguievetskaia K, Ungermann C (2014). Function and regulation of the endosomal fusion and fission machineries. Cold Spring Harb Perspect Biol, 6(3): a016832
https://doi.org/10.1101/cshperspect.a016832
|
28 |
Gomes L C, Benedetto G D, Scorrano L (2011). During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat Cell Biol, 13(5): 589–598
https://doi.org/10.1038/ncb2220
|
29 |
Grant B D, Donaldson J G (2009). Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol, 10(9): 597–608
https://doi.org/10.1038/nrm2755
|
30 |
Helle S C J, Kanfer G, Kolar K, Lang A, Michel A H, Kornmann B (2013). Organization and function of membrane contact sites. Biochimica et Biophysica Acta (BBA) - Mol Cell Res, 1833(11): 2526–2541
|
31 |
Hoppins S, Lackner L, Nunnari J (2007). The machines that divide and fuse mitochondria. Annu Rev Biochem, 76(1): 751–780
https://doi.org/10.1146/annurev.biochem.76.071905.090048
|
32 |
Huotari J, Helenius A (2011). Endosome maturation. EMBO J, 30(17): 3481–3500
https://doi.org/10.1038/emboj.2011.286
|
33 |
Jakobs S, Schauss A C, Hell S W (2003). Photoconversion of matrix targeted GFP enables analysis of continuity and intermixing of the mitochondrial lumen. FEBS Lett, 554(1-2): 194–200
https://doi.org/10.1016/S0014-5793(03)01170-0
|
34 |
Jendrach M, Pohl S, Vöth M, Kowald A, Hammerstein P, Bereiter-Hahn J (2005). Morpho-dynamic changes of mitochondria during ageing of human endothelial cells. Mech Ageing Dev, 126(6-7): 813–821
https://doi.org/10.1016/j.mad.2005.03.002
|
35 |
Kang J S, Tian J H, Pan P Y, Zald P, Li C, Deng C, Sheng Z H (2008). Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation. Cell, 132(1): 137–148
https://doi.org/10.1016/j.cell.2007.11.024
|
36 |
Karbowski M, Arnoult D, Chen H, Chan D C, Smith C L, Youle R J (2004). Quantitation of mitochondrial dynamics by photolabeling of individual organelles shows that mitochondrial fusion is blocked during the Bax activation phase of apoptosis. J Cell Biol, 164(4): 493–499
https://doi.org/10.1083/jcb.200309082
|
37 |
Klecker T, Böckler S, Westermann B (2014). Making connections: interorganelle contacts orchestrate mitochondrial behavior. Trends Cell Biol, 24(9): 537–545
https://doi.org/10.1016/j.tcb.2014.04.004
|
38 |
Klumperman J (2011). Architecture of the mammalian Golgi. Cold Spring Harb Perspect Biol, 3(7): a005181
https://doi.org/10.1101/cshperspect.a005181
|
39 |
Knoblach B, Rachubinski R A (2015). Sharing the cell’s bounty – organelle inheritance in yeast. J Cell Sci, 128(4): 621–630
https://doi.org/10.1242/jcs.151423
|
40 |
Korolchuk V I, Saiki S, Lichtenberg M, Siddiqi F H, Roberts E A, Imarisio S, Jahreiss L, Sarkar S, Futter M, Menzies F M, O’Kane C J, Deretic V, Rubinsztein D C (2011). Lysosomal positioning coordinates cellular nutrient responses. Nat Cell Biol, 13(4): 453–460
https://doi.org/10.1038/ncb2204
|
41 |
Kuznetsov A V, Hermann M, Saks V, Hengster P, Margreiter R (2009). The cell-type specificity of mitochondrial dynamics. Int J Biochem Cell Biol, 41(10): 1928–1939
https://doi.org/10.1016/j.biocel.2009.03.007
|
42 |
Kuznetsov A V, Margreiter R (2009). Heterogeneity of mitochondria and mitochondrial function within cells as another level of mitochondrial complexity. Int J Mol Sci, 10(4): 1911–1929
https://doi.org/10.3390/ijms10041911
|
43 |
Labbé K, Murley A, Nunnari J (2014). Determinants and functions of mitochondrial behavior. Annu Rev Cell Dev Biol, 30(1): 357–391
https://doi.org/10.1146/annurev-cellbio-101011-155756
|
44 |
Lee M C S, Miller E A, Goldberg J, Orci L, Schekman R (2004). Bi-directional protein transport between the ER and Golgi. Annu Rev Cell Dev Biol, 20(1): 87–123
https://doi.org/10.1146/annurev.cellbio.20.010403.105307
|
45 |
Levine T P, Patel S (2016). Signalling at membrane contact sites: two membranes come together to handle second messengers. Curr Opin Cell Biol, 39: 77–83
https://doi.org/10.1016/j.ceb.2016.02.011
|
46 |
Li X, Rydzewski N, Hider A, Zhang X, Yang J, Wang W, Gao Q, Cheng X, Xu H (2016). A molecular mechanism to regulate lysosome motility for lysosome positioning and tubulation. Nat Cell Biol, 18(4): 404–417
https://doi.org/10.1038/ncb3324
|
47 |
Liu X, Weaver D, Shirihai O, Hajnóczky G (2009). Mitochondrial ‘kiss‐and‐run’: interplay between mitochondrial motility and fusion–fission dynamics. EMBO J, 28(20): 3074–3089
https://doi.org/10.1038/emboj.2009.255
|
48 |
Luzio J P, Pryor P R, Bright N A (2007). Lysosomes: fusion and function. Nat Rev Mol Cell Biol, 8(8): 622–632
https://doi.org/10.1038/nrm2217
|
49 |
Ma X, Gong N, Zhong L, Sun J, Liang X J (2016). Future of nanotherapeutics: targeting the cellular sub-organelles. Biomat, 97: 10–21
https://doi.org/10.1016/j.biomaterials.2016.04.026
|
50 |
Marshall W F (2015). How cells measure length on subcellular scales. Trends Cell Biol, 25(12): 760–768
https://doi.org/10.1016/j.tcb.2015.08.008
|
51 |
Martens S, McMahon H T (2008). Mechanisms of membrane fusion: disparate players and common principles. Nat Rev Mol Cell Biol, 9(7): 543–556
https://doi.org/10.1038/nrm2417
|
52 |
McNew J A, Sondermann H, Lee T, Stern M, Brandizzi F (2013). GTP-dependent membrane fusion. Annu Rev Cell Dev Biol, 29(1): 529–550
https://doi.org/10.1146/annurev-cellbio-101512-122328
|
53 |
Means S, Smith A J, Shepherd J, Shadid J, Fowler J, Wojcikiewicz R J H, Mazel T, Smith G D, Wilson B S (2006). Reaction diffusion modeling of calcium dynamics with realistic ER geometry. Biophys J, 91(2): 537–557
https://doi.org/10.1529/biophysj.105.075036
|
54 |
Mizushima N (2007). Autophagy: process and function. Genes Dev, 21(22): 2861–2873
https://doi.org/10.1101/gad.1599207
|
55 |
Mouli P K, Twig G, Shirihai O S (2009). Frequency and selectivity of mitochondrial fusion are key to its quality maintenance function. Biophys J, 96(9): 3509–3518
https://doi.org/10.1016/j.bpj.2008.12.3959
|
56 |
Murley A, Nunnari J (2016). The emerging network of mitochondria-organelle contacts. Mol Cell, 61(5): 648–653
https://doi.org/10.1016/j.molcel.2016.01.031
|
57 |
Nakamura N, Wei J H, Seemann J (2012). Modular organization of the mammalian Golgi apparatus. Curr Opin Cell Biol, 24(4): 467–474
https://doi.org/10.1016/j.ceb.2012.05.009
|
58 |
Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y (2009). Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol, 10(7): 458–467
https://doi.org/10.1038/nrm2708
|
59 |
Namtame A, Chen S H (2016). Agent-based Modeling and Network Analysis. Oxford University Press
|
60 |
Newman M E J (2003). The structure and function of complex networks. SIAM Rev, 45(2): 167–256
https://doi.org/10.1137/S003614450342480
|
61 |
Newman M E J 2010. Networks. Oxford University Press.
|
62 |
Ni H M, Williams J A, Ding W X (2015). Mitochondrial dynamics and mitochondrial quality control. Redox Biol, 4: 6–13
https://doi.org/10.1016/j.redox.2014.11.006
|
63 |
Nunnari J, Walter P (1996). Regulation of organelle biogenesis. Cell, 84(3): 389–394
https://doi.org/10.1016/S0092-8674(00)81283-0
|
64 |
Okamoto K, Shaw J M (2005). Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annu Rev Genet, 39(1): 503–536
https://doi.org/10.1146/annurev.genet.38.072902.093019
|
65 |
Palikaras K, Tavernarakis N (2014). Mitochondrial homeostasis: The interplay between mitophagy and mitochondrial biogenesis. Exp Gerontol, 56: 182–188
https://doi.org/10.1016/j.exger.2014.01.021
|
66 |
Patel P K, Shirihai O, Huang K C (2013). Optimal dynamics for quality control in spatially distributed mitochondrial networks. PLOS Comput Biol, 9(7): e1003108
https://doi.org/10.1371/journal.pcbi.1003108
|
67 |
Penny C J, Kilpatrick B S, Han J M, Sneyd J, Patel S (2014). A computational model of lysosome–ER Ca2+ microdomains. J Cell Sci, 127(13): 2934–2943
https://doi.org/10.1242/jcs.149047
|
68 |
Phillips M J, Voeltz G K (2016). Structure and function of ER membrane contact sites with other organelles. Nat Rev Mol Cell Biol, 17(2): 69–82
https://doi.org/10.1038/nrm.2015.8
|
69 |
Posakony J W, England J M, Attardi G (1977). Mitochondrial growth and division during the cell cycle in HeLa cells. J Cell Biol, 74(2): 468–491
https://doi.org/10.1083/jcb.74.2.468
|
70 |
Priault M, Salin B, Schaeffer J, Vallette F M, di Rago J P, Martinou J C (2005). Impairing the bioenergetic status and the biogenesis of mitochondria triggers mitophagy in yeast. Cell Death Differ, 12(12): 1613–1621
https://doi.org/10.1038/sj.cdd.4401697
|
71 |
Prinz W A (2014). Bridging the gap: membrane contact sites in signaling, metabolism, and organelle dynamics. J Cell Biol, 205(6): 759–769
https://doi.org/10.1083/jcb.201401126
|
72 |
Rafelski S M, Viana M P, Zhang Y, Chan Y H M, Thorn K S, Yam P, Fung J C, Li H, Costa L D F, Marshall W F (2012). Mitochondrial network size scaling in budding yeast. Science, 338(6108): 822–824
https://doi.org/10.1126/science.1225720
|
73 |
Rambold A S, Kostelecky B, Elia N, Lippincott-Schwartz J (2011). Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc Natl Acad Sci USA, 108(25): 10190–10195
https://doi.org/10.1073/pnas.1107402108
|
74 |
Rink J, Ghigo E, Kalaidzidis Y, Zerial M (2005). Rab conversion as a mechanism of progression from early to late endosomes. Cell, 122(5): 735–749
https://doi.org/10.1016/j.cell.2005.06.043
|
75 |
Rohn J L, Patel J V, Neumann B, Bulkescher J, Mchedlishvili N, McMullan R C, Quintero O A, Ellenberg J, Baum B (2014). Myo19 ensures symmetric partitioning of mitochondria and coupling of mitochondrial segregation to cell division. Curr Biol, 24(21): 2598–2605
https://doi.org/10.1016/j.cub.2014.09.045
|
76 |
Rutter G A, Rizzuto R (2000). Regulation of mitochondrial metabolism by ER Ca2+ release: an intimate connection. Trends Biochem Sci, 25(5): 215–221
https://doi.org/10.1016/S0968-0004(00)01585-1
|
77 |
Scheckhuber C Q, Erjavec N, Tinazli A, Hamann A, Nystrom T, Osiewacz H D (2007). Reducing mitochondrial fission results in increased life span and fitness of two fungal ageing models. Nat Cell Biol, 9(1): 99–105
https://doi.org/10.1038/ncb1524
|
78 |
Schrader M, Godinho L F, Costello J, Islinger M (2015). The different facets of organelle interplay-an overview of organelle interactions. Front Cell Dev Biol, 3: 56
https://doi.org/10.3389/fcell.2015.00056
|
79 |
Sengupta D, Linstedt A D (2011). Control of organelle size: The Golgi complex. Annu Rev Cell Dev Biol, 27(1): 57–77
https://doi.org/10.1146/annurev-cellbio-100109-104003
|
80 |
Sheng Z H (2014). Mitochondrial trafficking and anchoring in neurons: new insight and implications. J Cell Biol, 204(7): 1087–1098
https://doi.org/10.1083/jcb.201312123
|
81 |
Sheng Z H, Cai Q (2012). Mitochondrial transport in neurons: impact on synaptic homeostasis and neurodegeneration. Nat Rev Neurosci, 13(2): 77–93
|
82 |
Shneyer B I, Ušaj M, Henn A (2016). Myo19 is an outer mitochondrial membrane motor and effector of starvation-induced filopodia. J Cell Sci, 129(3): 543–556
https://doi.org/10.1242/jcs.175349
|
83 |
Sukhorukov V M, Dikov D, Reichert A S, Meyer-Hermann M (2012). Emergence of the mitochondrial reticulum from fission and fusion dynamics. PLOS Comput Biol, 8(10): e1002745
https://doi.org/10.1371/journal.pcbi.1002745
|
84 |
Sukhorukov V M, Meyer-Hermann M (2015). Structural heterogeneity of mitochondria induced by the microtubule cytoskeleton. Sci Rep, 5: 13924
https://doi.org/10.1038/srep13924
|
85 |
Tam Z Y, Gruber J, Halliwell B, Gunawan R (2013). Mathematical modeling of the role of mitochondrial fusion and fission in mitochondrial DNA maintenance. PLoS One, 8(10): e76230
https://doi.org/10.1371/journal.pone.0076230
|
86 |
Torchilin V P (2006). Recent approaches to intracellular delivery of drugs and DNA and organelle targeting. Annu Rev Biomed Eng, 8(1): 343–375
https://doi.org/10.1146/annurev.bioeng.8.061505.095735
|
87 |
Twig G, Elorza A, Molina A J A, Mohamed H, Wikstrom J D, Walzer G, Stiles L, Haigh S E, Katz S, Las G, Alroy J, Wu M, Py B F, Yuan J, Deeney J T, Corkey B E, Shirihai O S (2008a). Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J, 27(2): 433–446
https://doi.org/10.1038/sj.emboj.7601963
|
88 |
Twig G, Hyde B, Shirihai O S (2008b). Mitochondrial fusion, fission and autophagy as a quality control axis: The bioenergetic view. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1777(9): 1092–1097
https://doi.org/10.1016/j.bbabio.2008.05.001
|
89 |
Twig G, Liu X, Liesa M, Wikstrom J D, Molina A J A, Las G, Yaniv G, Hajnóczky G, Shirihai O S (2010). Biophysical properties of mitochondrial fusion events in pancreatic β-cells and cardiac cells unravel potential control mechanisms of its selectivity. Am J Physiol Cell Physiol, 299(2): C477–C487
https://doi.org/10.1152/ajpcell.00427.2009
|
90 |
Warren G, Wickner W (1996). Organelle inheritance. Cell, 84(3): 395–400
https://doi.org/10.1016/S0092-8674(00)81284-2
|
91 |
Westrate L M, Lee J E, Prinz W A, Voeltz G K (2015). Form follows function: The importance of endoplasmic reticulum shape. Annu Rev Biochem, 84(1): 791–811
https://doi.org/10.1146/annurev-biochem-072711-163501
|
92 |
Wikstrom J D, Twig G, Shirihai O S (2009). What can mitochondrial heterogeneity tell us about mitochondrial dynamics and autophagy? Int J Biochem Cell Biol, 41(10): 1914–1927
https://doi.org/10.1016/j.biocel.2009.06.006
|
93 |
Youle R J, Narendra D P (2011). Mechanisms of mitophagy. Nat Rev Mol Cell Biol, 12(1): 9–14
https://doi.org/10.1038/nrm3028
|
94 |
Youle R J, van der Bliek A M (2012). Mitochondrial fission, fusion, and stress. Science, 337(6098): 1062–1065
https://doi.org/10.1126/science.1219855
|
95 |
Yu Y, Lee H C, Chen K C, Suhan J, Qiu M, Ba Q, Yang G (2016). Inner membrane fusion mediates spatial distribution of axonal mitochondria. Sci Rep, 6: 18981
https://doi.org/10.1038/srep18981
|
96 |
Zhu X, Gerstein M, Snyder M (2007). Getting connected: analysis and principles of biological networks. Genes Dev, 21: 1010–1024
|
|
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