Untangling the web: Mechanisms underlying ER network formation

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 11, 2013, Pages 2492-2498

  Goyal, Uma ^a   Blackstone, Craig ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Atlastin; Endoplasmic reticulum; Hereditary spastic paraplegia; Morphology; REEP; Reticulon

Indexed keywords

CALCIUM; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE;

ARABIDOPSIS; ARTICLE; CAENORHABDITIS ELEGANS; CELL DIVISION; CELL MEMBRANE; CELL NUCLEUS MEMBRANE; CYTOSKELETON; ENDOPLASMIC RETICULUM; EUKARYOTIC CELL; FERTILIZATION; GOLGI COMPLEX; HYDROLYSIS; LIPID BILAYER; MICROTUBULE; MORPHOLOGY; MYRISTYLATION; NERVE CELL PLASTICITY; NONHUMAN; NUCLEAR PORE; PHOSPHOLIPID BILAYER; POLYSOME; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PURKINJE CELL; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; TELOPHASE;

ATLASTIN; ENDOPLASMIC RETICULUM; HEREDITARY SPASTIC PARAPLEGIA; MORPHOLOGY; REEP; RETICULON;

ANIMALS; CALCIUM; CYTOSKELETON; ENDOPLASMIC RETICULUM; HUMANS; NUCLEAR ENVELOPE; PROTEINS; SIGNAL TRANSDUCTION;

EID: 84880617526     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.04.009     Document Type: Article

References (86)

1. L.H. Sullivan, The tall office building artistically considered, Lippincott's Magazine #57 (1896) 403-409.
2. Lynes E.M., Simmen T. Urban planning of the endoplasmic reticulum (ER): how diverse mechanisms segregate the many functions of the ER. Biochim. Biophys. Acta 2011, 1813:1893-1905.
3. Park S.H., Blackstone C. Further assembly required: construction and dynamics of the endoplasmic reticulum network. EMBO Rep. 2010, 11:515-521.
4. English A.R., Voeltz G.K. Endoplasmic reticulum structure and interconnections with other organelles. Cold Spring Harb. Perspect. Biol. 2013, 5:a013227.
5. Hu J., Prinz W.A., Rapoport T.A. Weaving the web of ER tubules. Cell 2011, 147:1226-1231.
6. Sparkes I., Hawes C., Frigerio L. FrontiERs: movers and shapers of the higher plant cortical endoplasmic reticulum. Curr. Opin. Plant Biol. 2011, 658-665.
7. Chen J., Doyle C., Qi X., Zheng H. The endoplasmic reticulum: a social network in plant cells. J. Integr. Plant Biol. 2012, 54:840-850.
8. Lin S., Sun S., Hu J. Molecular basis for sculpting the endoplasmic reticulum membrane. Int. J. Biochem. Cell Biol. 2012, 44:1436-1443.
9. Alberts B., Johnson A., Lewis J., Raff M., Roberts K., Walter P. Molecular Biology of the Cell 2002, Garland Science, New York. fourth ed.
10. Walters A.D., Bommakanti A., Cohen-Fix O. Shaping the nucleus: factors and forces. J. Cell. Biochem. 2012, 113:2813-2821.
11. Lee C., Chen L.B. Dynamic behavior of endoplasmic reticulum in living cells. Cell 1988, 54:37-46.
12. Prinz W.A., Grzyb L., Veenhuis M., Kahana J.A., Silver P.A., Rapoport T.A. Mutants affecting the structure of the cortical endoplasmic reticulum in Saccharomyces cerevisiae. J. Cell Biol. 2000, 150:461-474.
13. Puhka M., Joensuu M., Vihinen H., Belevich I., Jokitalo E. Progressive sheet-to-tubule transformation is a general mechanism for endoplasmic reticulum partitioning in dividing mammalian cells. Mol. Biol. Cell 2012, 23:2424-2432.
14. Lu L., Ladinsky M.S., Kirchhausen T. Cisternal organization of the endoplasmic reticulum during mitosis. Mol. Biol. Cell 2009, 20:3471-3480.
15. English A.R., Voeltz G.K. Rab10 GTPase regulates ER dynamics and morphology. Nat. Cell Biol. 2013, 15:169-178.
16. de Brito O.M., Scorrano L. An intimate liaison: spatial organization of the endoplasmic reticulum-mitochondria relationship. EMBO J. 2010, 29:2715-2723.
17. Manford A.G., Stefan C.J., Yuan H.L., Macgurn J.A., Emr S.D. ER-to-plasma membrane tethering proteins regulate cell signaling and ER morphology. Dev. Cell 2012, 23:1129-1140.
18. Rowland A.A., Voeltz G.K. Endoplasmic reticulum-mitochondrial contacts: function of the junction. Nat. Rev. Mol. Cell Biol. 2012, 13:607-625.
19. Spacek J., Harris K.M. Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat. J. Neurosci. 1997, 17:190-203.
20. Wagner W., Brenowitz S.D., Hammer J.A. Myosin-Va transports the endoplasmic reticulum into the dendritic spines of Purkinje neurons. Nat. Cell Biol. 2011, 13:40-48.
21. Cui-Wang T., Hanus C., Cui T., Helton T., Bourne J., Watson D., Harris K.M., Ehlers M.D. Local zones of endoplasmic reticulum complexity confine cargo in neuronal dendrites. Cell 2012, 148:309-321.
22. Voeltz G.K., Prinz W.A. Sheets, ribbons and tubules - how organelles get their shape. Nat. Rev. Mol. Cell Biol. 2007, 8:258-264.
23. Shibata Y., Hu J., Kozlov M.M., Rapoport T.A. Mechanisms shaping the membranes of cellular organelles. Annu. Rev. Cell Dev. Biol. 2009, 25:329-354.
24. Zimmerberg J., Kozlov M.M. How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 2006, 7:9-19.
25. Dannhauser P.N., Ungewickell E.J. Reconstitution of clathrin-coated bud and vesicle formation with minimal components. Nat. Cell Biol. 2012, 14:634-639.
26. Stachowiak J.C., Schmid E.M., Ryan C.J., Ann H.S., Sasaki D.Y., Sherman M.B., Geissler P.L., Fletcher D.A., Hayden C.C. Membrane bending by protein-protein crowding. Nat. Cell Biol. 2012, 14:944-949.
27. Waterman-Storer C.M., Salmon E.D. Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms. Curr. Biol. 1998, 8:798-806.
28. Grigoriev I., Gouveia S.M., van der Vaart B., Demmers J., Smyth J.T., Honnappa S., Splinter D., Steinmetz M.O., Putney J.W., Hoogenraad C.C., Akhmanova A. STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Curr. Biol. 2008, 18:177-182.
29. Voeltz G.K., Prinz W.A., Shibata Y., Rist J.M., Rapoport T.A. A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 2006, 124:573-586.
30. Hu J., Shibata Y., Voss C., Shemesh T., Li Z., Coughlin M., Kozlov M.M., Rapoport T.A., Prinz W.A. Membrane proteins of the endoplasmic reticulum induce high-curvature tubules. Science 2008, 319:1247-1250.
31. Shibata Y., Voss C., Rist J.M., Hu J., Rapoport T.A., Prinz W.A., Voeltz G.K. The reticulon and Dp1/Yop1p proteins form immobile oligomers in the tubular endoplasmic reticulum. J. Biol. Chem. 2008, 283:18892-18904.
32. Sparkes I., Tolley N., Aller I., Svozil J., Osterrieder A., Botchway S., Mueller C., Frigerio L., Hawes C. Five Arabidopsis reticulon isoforms share endoplasmic reticulum location, topology, and membrane-shaping properties. Plant Cell 2010, 22:1333-1343.
33. Tolley N., Sparkes I., Craddock C.P., Eastmond P.J., Runions J., Hawes C., Frigerio L. Transmembrane domain length is responsible for the ability of a plant reticulon to shape endoplasmic reticulum tubules in vivo. Plant J. 2010, 64:411-418.
34. Tolley N., Sparkes I.A., Hunter P.R., Craddock C.P., Nuttall J., Roberts L.M., Hawes C., Pedrazzini E., Frigerio L. Overexpression of a plant reticulon remodels the lumen of the cortical endoplasmic reticulum but does not perturb protein transport. Traffic 2008, 9:94-102.
35. West M., Zurek N., Hoenger A., Voeltz G.K. A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature. J. Cell Biol. 2011, 193:333-346.
36. Ronchi P., Colombo S., Francolini M., Borgese N. Transmembrane domain-dependent partitioning of membrane proteins within the endoplasmic reticulum. J. Cell Biol. 2008, 181:105-118.
37. Anderson D.J., Hetzer M.W. Reshaping of the endoplasmic reticulum limits the rate for nuclear envelope formation. J. Cell Biol. 2008, 182:911-924.
38. Shibata Y., Shemesh T., Prinz W.A., Palazzo A.F., Kozlov M.M., Rapoport T.A. Mechanisms determining the morphology of the peripheral ER. Cell 2010, 143:774-788.
39. Klopfenstein D.R., Klumperman J., Lustig A., Kammerer R.A., Oorschot V., Hauri H.-P. Subdomain-specific localization of Climp-63 (P63) in the endoplasmic reticulum is mediated by its luminal α-helical segment. J. Cell Biol. 2001, 153:1287-1300.
40. Snapp E.L., Hegde R.S., Francolini M., Lombardo F., Colombo S., Pedrazzini E., Borgese N., Lippincott-Schwartz J. Formation of stacked ER cisternae by low affinity protein interactions. J. Cell Biol. 2003, 163:257-269.
41. Raices M., D'Angelo M.A. Nuclear pore complex composition: a new regulator of tissue-specific and developmental functions. Nat. Rev. Mol. Cell Biol. 2012, 13:687-699.
42. Dawson T.R., Lazarus M.D., Hetzer M.W., Wente S.R. ER membrane-bending proteins are necessary for de novo nuclear pore formation. J. Cell Biol. 2009, 184:659-675.
43. Sosa B.A., Rothballer A., Kutay U., Schwartz T.U. LINC complexes form by binding of three KASH peptides to domain interfaces of trimeric SUN proteins. Cell 2012, 149:1035-1047.
44. Zhu P.-P., Patterson A., Lavoie B., Stadler J., Shoeb M., Patel R., Blackstone C. Cellular localization, oligomerization, and membrane association of the hereditary spastic paraplegia 3A (SPG3A) protein atlastin. J. Biol. Chem. 2003, 278:49063-49071.
45. Zhu P.-P., Soderblom C., Tao-Cheng J.-H., Stadler J., Blackstone C. SPG3A protein atlastin-1 is enriched in growth cones and promotes axon elongation during neuronal development. Hum. Mol. Genet. 2006, 15:1343-1353.
46. Rismanchi N., Soderblom C., Stadler J., Zhu P.-P., Blackstone C. Atlastin GTPases are required for Golgi apparatus and ER morphogenesis. Hum. Mol. Genet. 2008, 17:1591-1604.
47. Hu J., Shibata Y., Zhu P.-P., Voss C., Rismanchi N., Prinz W.A., Rapoport T.A., Blackstone C. A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell 2009, 138:549-561.
48. Orso G., Pendin D., Liu S., Tosetto J., Moss T.J., Faust J.E., Micaroni M., Egorova A., Martinuzzi A., McNew J.A., Daga A. Homotypic fusion of ER membranes requires the dynamin-like GTPase Atlastin. Nature 2009, 460:978-983.
49. Lee H., Sparkes I., Gattolin S., Dzimitrowicz N., Roberts L.M., Hawes C., Frigerio L. An Arabidopsis reticulon and the atlastin homologue RHD3-like2 act together in shaping the tubular endoplasmic reticulum. New Phytol. 2013, 197:481-489.
50. Anwar K., Klemm R.W., Condon A., Severin K.N., Zhang M., Ghirlando R., Hu J., Rapoport T.A., Prinz W.A. The dynamin-like GTPase Sey1p mediates homotypic ER fusion in S. cerevisiae. J. Cell Biol. 2012, 197:209-217.
51. Moss T.J., Andreazza C., Verma A., Daga A., McNew J.A. Membrane fusion by the GTPase atlastin requires a conserved C-terminal cytoplasmic tail and dimerization through the middle domain. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:11133-11138.
52. Liu T.Y., Bian X., Sun S., Hu X., Klemm R.W., Prinz W.A., Rapoport T.A., Hu J. Lipid interaction of the C terminus and association of the transmembrane segments facilitate atlastin-mediated homotypic endoplasmic reticulum fusion. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E2146-E2154.
53. Byrnes L.J., Singh A., Szeto K., Benvin N.M., O'Donnell J.P., Zipfel W.R., Sondermann H. Structural basis for conformational switching and GTP loading of the large G protein atlastin. EMBO J. 2013, 32:369-384.
54. Chen S., Novick P., Ferro-Novick S. ER network formation requires a balance of the dynamin-like GTPase Sey1p and the Lunapark family member Lnp1p. Nat. Cell Biol. 2012, 14:707-716.
55. Terasaki M., Chen L.B., Fujiwara K. Microtubules and the endoplasmic reticulum are highly interdependent structures. J. Cell Biol. 1986, 103:1557-1568.
56. Chen S., Novick P., Ferro-Novick S. ER structure and function. Curr. Opin. Cell Biol. 2013, 25. (doi:pii: S0955-0674(13)00029-X). 10.1016/j.ceb.2013.02.006.
57. Bola B., Allan V. How and why does the endoplasmic reticulum move?. Biochem. Soc. Trans. 2009, 37:961-965.
58. Dreier L., Rapoport T.A. In vitro formation of the endoplasmic reticulum occurs independently of microtubules by a controlled fusion reaction. J. Cell Biol. 2000, 148:883-898.
59. Terasaki M., Reese T.S. Interactions among endoplasmic reticulum, microtubules, and retrograde movements of the cell surface. Cell Motil. Cytoskeleton 1994, 29:291-300.
60. Evans K., Keller C., Pavur K., Glasgow K., Conn B., Lauring B. Interaction of two hereditary spastic paraplegia gene products, spastin and atlastin, suggests a common pathway for axonal maintenance. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:10666-10671.
61. Sanderson C.M., Connell J.W., Edwards T.L., Bright N.A., Duley S., Thompson A., Luzio J.P., Reid E. Spastin and atlastin, two proteins mutated in autosomal-dominant hereditary spastic paraplegia, are binding partners. Hum. Mol. Genet. 2006, 15:307-318.
62. Park S.H., Zhu P.-P., Parker R.L., Blackstone C. Hereditary spastic paraplegia proteins REEP1, spastin, and atlastin-1 coordinate microtubule interactions with the tubular ER network. J. Clin. Invest. 2010, 120:1097-1110.
63. Klopfenstein D.R., Kappeler F., Hauri H.-P. A novel direct interaction of endoplasmic reticulum with microtubules. EMBO J. 1998, 17:6168-6177.
64. Estrada P., Kim J., Coleman J., Walker L., Dunn B., Takizawa P., Novick P., Ferro-Novick S. Myo4p and She3p are required for cortical ER inheritance in Saccharomyces cerevisiae. J. Cell Biol. 2003, 163:1255-1266.
65. Schulz T.A., Creutz C.E. The tricalbin C2 domains: lipid-binding properties of a novel, synaptotagmin-like yeast protein family. Biochemistry 2004, 43:3987-3995.
66. Stefan C.J., Manford A.G., Baird D., Yamada-Hanff J., Mao Y., Emr S.D. Osh proteins regulate phosphoinositide metabolism at ER-plasma membrane contact sites. Cell 2011, 144:389-401.
67. Wolf W., Kilic A., Schrul B., Lorenz H., Schwappach B., Seedorf M. Yeast Ist2 recruits the endoplasmic reticulum to the plasma membrane and creates a ribosome-free membrane microcompartment. PLoS One 2012, 7:e39703.
68. 2+-binding requirements. Mol. Biol. Cell 2004, 15:481-496.
69. Soboloff J., Rothberg B.S., Madesh M., Gill D.L. STIM proteins: dynamic calcium signal transducers. Nat. Rev. Mol. Cell Biol. 2012, 13:549-565.
70. Smyth J.T., Beg A.M., Wu S., Putney J.W., Rusan N.M. Phosphoregulation of STIM1 leads to exclusion of the endoplasmic reticulum from the mitotic spindle. Curr. Biol. 2012, 22:1487-1493.
71. Terasaki M., Jaffe L.A., Hunnicutt G.R., Hammer J.A. Structural change of the endoplasmic reticulum during fertilization: evidence for loss of membrane continuity using the green fluorescent protein. Dev. Biol. 1996, 179:320-328.
72. Subramanian K., Meyer T. Calcium-induced restructuring of nuclear envelope and endoplasmic reticulum calcium stores. Cell 1997, 89:963-971.
73. Kucharz K., Krogh M., Ng A.N., Toresson H. NMDA receptor stimulation induces reversible fission of the neuronal endoplasmic reticulum. PLoS One 2009, 4:e5250.
74. Chang J., Blackstone C. Rab10 joins the ER social network. Nat. Cell Biol. 2013, 15:135-136.
75. Kim Y.J., Guzman-Hernandez M.-L., Balla T. A highly dynamic ER-derived phosphatidylinositol-synthesizing organelle supplies phosphoinositides to cellular membranes. Dev. Cell 2011, 21:813-824.
76. Audhya A., Desai A., Oegema K. A role for Rab5 in structuring the endoplasmic reticulum. J. Cell Biol. 2007, 178:43-56.
77. Sasidharan N., Sumakovic M., Hannemann M., Hegermann J., Liewald J.F., Olendrowitz C., Koenig S., Grant B.D., Rizzoli S.O., Gottschalk A., Eimer S. RAB-5 and RAB-10 cooperate to regulate neuropeptide release in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:18944-18949.
78. Shi A., Liu O., Koenig S., Banerjee R., Chen C.C., Eimer S., Grant B.D. RAB-10-GTPase-mediated regulation of endosomal phosphatidylinositol-4,5-bisphosphate. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E2306-E2315.
79. Turner M.D., Plutner H., Balch W.E. A Rab GTPase is required for homotypic assembly of the endoplasmic reticulum. J. Biol. Chem. 1997, 272:13479-13483.
80. Sandoval C.O., Simmen T. Rab proteins of the endoplasmic reticulum: functions and interactors. Biochem. Soc. Trans. 2012, 40:1426-1432.
81. Renvoisé B., Blackstone C. Emerging themes of ER organization in the development and maintenance of axons. Curr. Opin. Neurobiol. 2010, 20:531-537.
82. Blackstone C. Cellular pathways of hereditary spastic paraplegia. Annu. Rev. Neurosci. 2012, 35:25-47.
83. Yang Y.S., Harel N.Y., Strittmatter S.M. Reticulon-4A (Nogo-A) redistributes protein disulfide isomerase to protect mice from SOD1-dependent amyotrophic lateral sclerosis. J. Neurosci. 2009, 29:13850-13859.
84. Fasana E., Fossati M., Ruggiano A., Brambillasca S., Hoogenraad C.C., Navone F., Francolini M., Borgese N. A VAPB mutant linked to amyotrophic lateral sclerosis generates a novel form of organized smooth endoplasmic reticulum. FASEB J. 2010, 24:1419-1430.
85. Tran D., Chalhoub A., Schooley A., Zhang W., Ngsee J.K. A mutation in VAPB that causes amyotrophic lateral sclerosis also causes a nuclear envelope defect. J. Cell Sci. 2012, 125:2831-2836.
86. Pendin D., McNew J.A., Daga A. Balancing ER dynamics: shaping, bending, severing, and mending membranes. Curr. Opin. Cell Biol. 2011, 23:435-442.