ER sliding dynamics and ER-mitochondrial contacts occur on acetylated microtubules
Open accessAbstract
The endoplasmic reticulum (ER) network is extremely dynamic in animal cells, yet little is known about the mechanism and function of its movements. The most common ER dynamic, termed ER sliding, involves ER tubule extension along stable microtubules (MTs). In this study, we show that ER sliding occurs on nocodazole-resistant MTs that are posttranslationally modified by acetylation. We demonstrate that high MT curvature is a good indicator of MT acetylation and show in live cells that ER sliding occurs predominantly on these curved, acetylated MTs. Furthermore, increasing MT acetylation by drug treatment increases the frequency of ER sliding. One purpose of the ER sliding on modified MT tracts could be to regulate its interorganelle contacts. We find that all mitochondria and many endosomes maintain contact with the ER despite the movements of each. However, mitochondria, but not endosomes, preferentially localize to acetylated MTs. Thus, different ER dynamics may occur on distinct MT populations to establish or maintain contacts with different organelles.
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?
Stable microtubules have a curved appearance.
“A characteristic feature of stable MTs is their curved appearance (Piperno et al., 1987; Friedman et al., 2010; Katrukha et al., 2017).”
From A live-cell marker to visualize the dynamics of stable microtubules throughout the cell cycle (2023) · cites this paper as Friedman et al., 2010
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
HDAC6 is a microtubule-associated deacetylase
Hubbert, C., Guardiola, A., Shao, R., Kawaguchi, Y., Ito, A., Nixon, A., Yoshida, M., Wang, X.-F., & Yao, T.-P. (2002) · Nature · doi:10.1038/417455a · Cited by 2,403 · see citing works
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
Microtubules containing acetylated alpha-tubulin in mammalian cells in culture.
Piperno, G., LeDizet, M., & Chang, X. J. (1987) · The Journal of cell biology · doi:10.1083/jcb.104.2.289 · Cited by 873 · 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
Mitofusins and OPA1 mediate sequential steps in mitochondrial membrane fusion
Song, Z., Ghochani, M., McCaffery, J. M., Frey, T. G., & Chan, D. C. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-03-0252 · Cited by 623 · see citing works
Hurd, D. D., & Saxton, W. M. (1996) · Genetics · doi:10.1093/genetics/144.3.1075 · Cited by 379 · see citing works
Chemical Genetic Modifier Screens
Koeller, K. M., Haggarty, S. J., Perkins, B. D., Leykin, I., Wong, J. C., Kao, M.-C. J., & Schreiber, S. L. (2003) · Chemistry & Biology · doi:10.1016/s1074-5521(03)00093-0 · Cited by 89 · see citing works
Flagged first, then by citations
Research works printed but not linked: 35
- Baumann O. Walz B. 2001 Endoplasmic reticulum of animal cells and its organization into structural and functional domains. Int. Rev. Cytol. 205: 149– 214 10.1016/S0074-7696(01)05004-5 11336391 · DOI
- Bicek A.D. Tüzel E. Kroll D.M. Odde D.J. 2007 Analysis of microtubule curvature. Methods Cell Biol. 83: 237– 268 10.1016/S0091-679X(07)83010-X 17613311 · DOI
- Boldogh I.R. Pon L.A. 2007 Mitochondria on the move. Trends Cell Biol. 17: 502– 510 10.1016/j.tcb.2007.07.008 17804238 · DOI · Paper page
- Cai D. McEwen D.P. Martens J.R. Meyhofer E. Verhey K.J. 2009 Single molecule imaging reveals differences in microtubule track selection between Kinesin motors. PLoS Biol. 7: e1000216 10.1371/journal.pbio.1000216 19823565 PMC2749942 · DOI · Paper page
- Cambray-Deakin M.A. Robson S.J. Burgoyne R.D. 1988 Colocalisation of acetylated microtubules, glial filaments, and mitochondria in astrocytes in vitro. Cell Motil. Cytoskeleton. 10: 438– 449 10.1002/cm.970100311 3052874 · DOI
- Csordás G. Renken C. Várnai P. Walter L. Weaver D. Buttle K.F. Balla T. Mannella C.A. Hajnóczky G. 2006 Structural and functional features and significance of the physical linkage between ER and mitochondria. J. Cell Biol. 174: 915– 921 10.1083/jcb.200604016 16982799 PMC2064383 · DOI
- de Brito O.M. Scorrano L. 2008 Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature. 456: 605– 610 10.1038/nature07534 19052620 · DOI · Paper page
- Eden E.R. White I.J. Tsapara A. Futter C.E. 2010 Membrane contacts between endosomes and ER provide sites for PTP1B-epidermal growth factor receptor interaction. Nat. Cell Biol. 12: 267– 272 20118922
- English A.R. Zurek N. Voeltz G.K. 2009 Peripheral ER structure and function. Curr. Opin. Cell Biol. 21: 596– 602 10.1016/j.ceb.2009.04.004 19447593 PMC2753178 · DOI
- Frederick R.L. Shaw J.M. 2007 Moving mitochondria: establishing distribution of an essential organelle. Traffic. 8: 1668– 1675 10.1111/j.1600-0854.2007.00644.x 17944806 PMC3739988 · DOI
- Grigoriev I. Gouveia S.M. van der Vaart B. Demmers J. Smyth J.T. Honnappa S. Splinter D. Steinmetz M.O. Putney J.W. Jr. Hoogenraad C.C. Akhmanova A. 2008 STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Curr. Biol. 18: 177– 182 10.1016/j.cub.2007.12.050 18249114 PMC2600655 · DOI
- Haggarty S.J. Koeller K.M. Wong J.C. Grozinger C.M. Schreiber S.L. 2003 Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc. Natl. Acad. Sci. USA. 100: 4389– 4394 10.1073/pnas.0430973100 12677000 PMC153564 · DOI · Paper page
- Hammond J.W. Huang C.-F. Kaech S. Jacobson C. Banker G. Verhey K.J. 2010 Posttranslational modifications of tubulin and the polarized transport of kinesin-1 in neurons. Mol. Biol. Cell. 21: 572– 583 10.1091/mbc.E09-01-0044 20032309 PMC2820422 · DOI · Paper page
- Hoepfner S. Severin F. Cabezas A. Habermann B. Runge A. Gillooly D. Stenmark H. Zerial M. 2005 Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B. Cell. 121: 437– 450 10.1016/j.cell.2005.02.017 15882625 · DOI
- Hom J.R. Gewandter J.S. Michael L. Sheu S.S. Yoon Y. 2007 Thapsigargin induces biphasic fragmentation of mitochondria through calcium-mediated mitochondrial fission and apoptosis. J. Cell. Physiol. 212: 498– 508 10.1002/jcp.21051 17443673 · DOI
- Kremer J.R. Mastronarde D.N. McIntosh J.R. 1996 Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116: 71– 76 10.1006/jsbi.1996.0013 8742726 · DOI
- Lee C. Chen L.B. 1988 Dynamic behavior of endoplasmic reticulum in living cells. Cell. 54: 37– 46 10.1016/0092-8674(88)90177-8 3383243 · DOI
- Levine T. Loewen C. 2006 Inter-organelle membrane contact sites: through a glass, darkly. Curr. Opin. Cell Biol. 18: 371– 378 10.1016/j.ceb.2006.06.011 16806880 · DOI
- Liou J. Kim M.L. Heo W.D. Jones J.T. Myers J.W. Ferrell J.E. Jr. Meyer T. 2005 STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr. Biol. 15: 1235– 1241 10.1016/j.cub.2005.05.055 16005298 PMC3186072 · DOI
- Liou J. Fivaz M. Inoue T. Meyer T. 2007 Live-cell imaging reveals sequential oligomerization and local plasma membrane targeting of stromal interaction molecule 1 after Ca2+ store depletion. Proc. Natl. Acad. Sci. USA. 104: 9301– 9306 10.1073/pnas.0702866104 17517596 PMC1890489 · DOI
- Loktev A.V. Zhang Q. Beck J.S. Searby C.C. Scheetz T.E. Bazan J.F. Slusarski D.C. Sheffield V.C. Jackson P.K. Nachury M.V. 2008 A BBSome subunit links ciliogenesis, microtubule stability, and acetylation. Dev. Cell. 15: 854– 865 10.1016/j.devcel.2008.11.001 19081074 · DOI
- Perktold A. Zechmann B. Daum G. Zellnig G. 2007 Organelle association visualized by three-dimensional ultrastructural imaging of the yeast cell. FEMS Yeast Res. 7: 629– 638 10.1111/j.1567-1364.2007.00226.x 17419771 · DOI
- Reed N.A. Cai D. Blasius T.L. Jih G.T. Meyhofer E. Gaertig J. Verhey K.J. 2006 Microtubule acetylation promotes kinesin-1 binding and transport. Curr. Biol. 16: 2166– 2172 10.1016/j.cub.2006.09.014 17084703 · DOI · Paper page
- Rink J. Ghigo E. Kalaidzidis Y. Zerial M. 2005 Rab conversion as a mechanism of progression from early to late endosomes. Cell. 122: 735– 749 10.1016/j.cell.2005.06.043 16143105 · DOI
- Rizzuto R. Pinton P. Carrington W. Fay F.S. Fogarty K.E. Lifshitz L.M. Tuft R.A. Pozzan T. 1998 Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science. 280: 1763– 1766 10.1126/science.280.5370.1763 9624056 · DOI · Paper page
- Rocha N. Kuijl C. van der Kant R. Janssen L. Houben D. Janssen H. Zwart W. Neefjes J. 2009 Cholesterol sensor ORP1L contacts the ER protein VAP to control Rab7–RILP–p150Glued and late endosome positioning. J. Cell Biol. 185: 1209– 1225 10.1083/jcb.200811005 19564404 PMC2712958 · DOI
- Staehelin L.A. 1997 The plant ER: a dynamic organelle composed of a large number of discrete functional domains. Plant J. 11: 1151– 1165 10.1046/j.1365-313X.1997.11061151.x 9225461 · DOI
- Stepanova T. Slemmer J. Hoogenraad C.C. Lansbergen G. Dortland B. De Zeeuw C.I. Grosveld F. van Cappellen G. Akhmanova A. Galjart N. 2003 Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J. Neurosci. 23: 2655– 2664 12684451 PMC6742099
- Subramanian K. Meyer T. 1997 Calcium-induced restructuring of nuclear envelope and endoplasmic reticulum calcium stores. Cell. 89: 963– 971 10.1016/S0092-8674(00)80281-0 9200614 · DOI
- Terasaki M. Chen L.B. Fujiwara K. 1986 Microtubules and the endoplasmic reticulum are highly interdependent structures. J. Cell Biol. 103: 1557– 1568 10.1083/jcb.103.4.1557 3533956 PMC2114338 · DOI
- Vance J.E. 2008 Phosphatidylserine and phosphatidylethanolamine in mammalian cells: two metabolically related aminophospholipids. J. Lipid Res. 49: 1377– 1387 10.1194/jlr.R700020-JLR200 18204094 · DOI
- Vedrenne C. Hauri H.-P. 2006 Morphogenesis of the endoplasmic reticulum: beyond active membrane expansion. Traffic. 7: 639– 646 10.1111/j.1600-0854.2006.00419.x 16683914 · DOI
- Voeltz G.K. Prinz W.A. Shibata Y. Rist J.M. Rapoport T.A. 2006 A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell. 124: 573– 586 10.1016/j.cell.2005.11.047 16469703 · DOI
- Waterman-Storer C.M. Salmon E.D. 1998 Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms. Curr. Biol. 8: 798– 806 10.1016/S0960-9822(98)70321-5 9663388 · DOI
- Woźniak M.J. Bola B. Brownhill K. Yang Y.-C. Levakova V. Allan V.J. 2009 Role of kinesin-1 and cytoplasmic dynein in endoplasmic reticulum movement in VERO cells. J. Cell Sci. 122: 1979– 1989 10.1242/jcs.041962 19454478 PMC2723153 · DOI
Cited by
Sorted by citations
ER Tubules Mark Sites of Mitochondrial Division
Friedman, J. R., Lackner, L. L., West, M., DiBenedetto, J. R., Nunnari, J., & Voeltz, G. K. (2011) · Science · doi:10.1126/science.1207385 · Cited by 2,072 · see citing works
Self-citationThe cell biology of mitochondrial membrane dynamics
Giacomello, M., Pyakurel, A., Glytsou, C., & Scorrano, L. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0210-7 · Cited by 1,550 · see citing works
Endoplasmic reticulum-mitochondria contacts: Function of the junction
Rowland, A. A., & Voeltz, G. K. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3440 · Cited by 1,018 · see citing works
Self-citationEndoplasmic 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
Organization and Function of Membrane Contact Sites
Helle, S. C. J., Kanfer, G., Kolar, K., Lang, A., Michel, A. H., & Kornmann, B. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2013.01.028 · Cited by 453 · see citing works
Intercellular mitochondrial transfer as a means of tissue revitalization
Liu, D., Gao, Y., Liu, J., Huang, Y., Yin, J., Feng, Y., Shi, L., Meloni, B. P., Zhang, C., Zheng, M., et al. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00440-z · Cited by 403 · see citing works
HDAC6 inhibition reverses axonal transport defects in motor neurons derived from FUS-ALS patients
Guo, W., Naujock, M., Fumagalli, L., Vandoorne, T., Baatsen, P., Boon, R., Ordovás, L., Patel, A., Welters, M., Vanwelden, T., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00911-y · Cited by 373 · see citing works
The Conserved GTPase Gem1 Regulates Endoplasmic Reticulum–Mitochondria Connections
Kornmann, B., Osman, C., & Walter, P. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1111314108 · Cited by 335 · see citing works
Kinesin Assembly and Movement in Cells
Verhey, K. J., Kaul, N., & Soppina, V. (2011) · Annual Review of Biophysics · doi:10.1146/annurev-biophys-042910-155310 · Cited by 231 · see citing works
Self-citationProteostasis 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
Sequential formation of different layers of dystrophic neurites in Alzheimer’s brains
Sharoar, M. G., Hu, X., Ma, X.-M., Zhu, X., & Yan, R. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0396-2 · Cited by 87 · see citing works
Detyrosinated microtubules spatially constrain lysosomes facilitating lysosome-autophagosome fusion
Mohan, N., Sorokina, E. M., Verdeny, I. V., Alvarez, A. S., & Lakadamyali, M. (2019) · Journal of Cell Biology · doi:10.1083/jcb.201807124 · Cited by 92 · 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
A live-cell marker to visualize the dynamics of stable microtubules throughout the cell cycle
Jansen, K. I., Iwanski, M. K., Burute, M., & Kapitein, L. C. (2023) · Journal of Cell Biology · doi:10.1083/jcb.202106105 · Cited by 39 · 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
- Friedman, J. R., Webster, B. M., Mastronarde, D. N., Verhey, K. J., & Voeltz, G. K.
- Affiliations
- University of Colorado Boulder (US)
- University of Michigan (US)
- Corresponding author
- Voeltz, Gia K.
- Venue
- Journal of Cell Biology
- Publisher
- Rockefeller University Press
- Published
- 2010-08-09
- Volume
- 190
- Issue
- 3
- Pages
- 363-375
- ISSN
- 0021-9525 (ISSN-L)
- 1540-8140
- PMC
- PMC2922647
- OpenAlex
- W2105176187
- Cited by
- 393
- References
- 7
- Citations by year
- 2026: 18 · 2025: 17 · 2024: 29 · 2023: 26 · 2022: 25 · 2021: 27 · 2020: 25 · 2019: 22 · 2018: 31 · 2017: 29 · 2016: 24 · 2015: 25 · 2014: 24 · 2013: 27 · 2012: 17
- FWCI
- 9.41
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-sa
- Locations
- The Journal of Cell Biology (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (n01co12400-79-0-22, N01-CO-12400, RR000592)
- National Cancer Institute (N01CO12400, N01-CO-012400)
- National Institute of General Medical Sciences (GM083254, R01GM083977, R01GM083254, T32GM008759, GM08759, GM083977, T32GM142607)
- National Center for Research Resources (P41RR000592)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Keywords
- endoplasmic reticulum dynamics, microtubule acetylation, microtubule curvature, ER-mitochondria contact sites
- MeSH terms
- Acetylation, Animals, Chlorocebus aethiops, Endoplasmic Reticulum, Microtubules, Mitochondria, COS Cells
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
