The endoplasmic reticulum: Structure, function and response to cellular signaling

Cellular and Molecular Life Sciences

Volumn 73, Issue 1, 2016, Pages 79-94

  Schwarz, Dianne S ^a,b,c   Blower, Michael D ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c NEW ENGLAND BIOLABS   (United States)

Author keywords

Fertilization; Interphase; Mitosis; Organization; Phosphorylation; Unfolded protein response

Indexed keywords

ENDOPLASMIC RETICULUM; STRUCTURE ACTIVITY RELATION; ANIMAL; CHEMISTRY; FERTILIZATION; HUMAN; LIPID METABOLISM; METABOLISM; MITOSIS; PROTEIN FOLDING; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; ULTRASTRUCTURE; UNFOLDED PROTEIN RESPONSE;

CALCIUM; PROTEIN;

ANIMALS; CALCIUM; ENDOPLASMIC RETICULUM; FERTILIZATION; HUMANS; LIPID METABOLISM; MITOSIS; PROTEIN BIOSYNTHESIS; PROTEIN FOLDING; PROTEINS; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 84952895975     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-015-2052-6     Document Type: Review

References (164)

1. Reid DW, Nicchitta CV (2015) Diversity and selectivity in mRNA translation on the endoplasmic reticulum. Nat Rev Mol Cell Biol 16(4):221-231. doi: 10.1038/nrm3958
2. Rapoport TA (2007) Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450(7170):663-669. doi: 10.1038/nature06384
3. Braakman I, Hebert DN (2013) Protein folding in the endoplasmic reticulum. Cold Spring Harb Perspect Biol 5(5):a013201. doi: 10.1101/cshperspect.a013201
4. Fagone P, Jackowski S (2009) Membrane phospholipid synthesis and endoplasmic reticulum function. J Lipid Res 50(Suppl):S311-S316. doi: 10.1194/jlr.R800049-JLR200
5. Hebert DN, Garman SC, Molinari M (2005) The glycan code of the endoplasmic reticulum: asparagine-linked carbohydrates as protein maturation and quality-control tags. Trends Cell Biol 15(7):364-370. doi: 10.1016/j.tcb.2005.05.007
6. Clapham DE (2007) Calcium signaling. Cell 131(6):1047-1058. doi: 10.1016/j.cell.2007.11.028
7. Westrate LM, Lee JE, Prinz WA, Voeltz GK (2015) Form follows function: the importance of endoplasmic reticulum shape. Annu Rev Biochem 84:791-811. doi: 10.1146/annurev-biochem-072711-163501
8. Jan CH, Williams CC, Weissman JS (2014) Principles of ER cotranslational translocation revealed by proximity-specific ribosome profiling. Science 346(6210):1257521. doi: 10.1126/science.1257521
9. Walter P, Blobel G (1981) Translocation of proteins across the endoplasmic reticulum. II. Signal recognition protein (SRP) mediates the selective binding to microsomal membranes of in-vitro-assembled polysomes synthesizing secretory protein. J Cell Biol 91(2 Pt 1):551-556
10. Walter P, Ibrahimi I, Blobel G (1981) Translocation of proteins across the endoplasmic reticulum. I. Signal recognition protein (SRP) binds to in-vitro-assembled polysomes synthesizing secretory protein. J Cell Biol 91(2 Pt 1):545-550
11. Gilmore R, Blobel G, Walter P (1982) Protein translocation across the endoplasmic reticulum. I. Detection in the microsomal membrane of a receptor for the signal recognition particle. J Cell Biol 95(2 Pt 1):463-469
12. Meyer DI, Krause E, Dobberstein B (1982) Secretory protein translocation across membranes-the role of the "docking protein'. Nature 297(5868):647-650
13. Deshaies RJ, Sanders SL, Feldheim DA, Schekman R (1991) Assembly of yeast Sec proteins involved in translocation into the endoplasmic reticulum into a membrane-bound multisubunit complex. Nature 349(6312):806-808. doi: 10.1038/349806a0
14. Evans EA, Gilmore R, Blobel G (1986) Purification of microsomal signal peptidase as a complex. Proc Natl Acad Sci USA 83(3):581-585
15. Blobel G (1980) Intracellular protein topogenesis. Proc Natl Acad Sci U S A 77(3):1496-1500
16. Seiser RM, Nicchitta CV (2000) The fate of membrane-bound ribosomes following the termination of protein synthesis. J Biol Chem 275(43):33820-33827. doi: 10.1074/jbc.M004462200
17. Potter MD, Nicchitta CV (2000) Regulation of ribosome detachment from the mammalian endoplasmic reticulum membrane. J Biol Chem 275(43):33828-33835. doi: 10.1074/jbc.M005294200
18. Potter MD, Nicchitta CV (2002) Endoplasmic reticulum-bound ribosomes reside in stable association with the translocon following termination of protein synthesis. J Biol Chem 277(26):23314-23320. doi: 10.1074/jbc.M202559200
19. Jagannathan S, Reid DW, Cox AH, Nicchitta CV (2014) De novo translation initiation on membrane-bound ribosomes as a mechanism for localization of cytosolic protein mRNAs to the endoplasmic reticulum. RNA 20(10):1489-1498. doi: 10.1261/rna.045526.114
20. Cui XA, Zhang H, Palazzo AF (2012) p180 promotes the ribosome-independent localization of a subset of mRNA to the endoplasmic reticulum. PLoS Biol 10(5):e1001336. doi: 10.1371/journal.pbio.1001336
21. van der Zand A, Gent J, Braakman I, Tabak HF (2012) Biochemically distinct vesicles from the endoplasmic reticulum fuse to form peroxisomes. Cell 149(2):397-409. doi: 10.1016/j.cell.2012.01.054
22. Hartl FU, Hayer-Hartl M (2009) Converging concepts of protein folding in vitro and in vivo. Nat Struct Mol Biol 16(6):574-581. doi: 10.1038/nsmb.1591
23. Ruggiano A, Foresti O, Carvalho P (2014) Quality control: eR-associated degradation: protein quality control and beyond. J Cell Biol 204(6):869-879. doi: 10.1083/jcb.201312042
24. Ryno LM, Wiseman RL, Kelly JW (2013) Targeting unfolded protein response signaling pathways to ameliorate protein misfolding diseases. Curr Opin Chem Biol 17(3):346-352. doi: 10.1016/j.cbpa.2013.04.009
25. Glick BS, Nakano A (2009) Membrane traffic within the Golgi apparatus. Annu Rev Cell Dev Biol 25:113-132. doi: 10.1146/annurev.cellbio.24.110707.175421
26. Appenzeller-Herzog C, Hauri HP (2006) The ER-Golgi intermediate compartment (ERGIC): in search of its identity and function. J Cell Sci 119(Pt 11):2173-2183. doi: 10.1242/jcs.03019
27. Guo Y, Sirkis DW, Schekman R (2014) Protein Sorting at the trans-Golgi network. Annu Rev Cell Dev Biol 30:169-206. doi: 10.1146/annurev-cellbio-100913-013012
28. Jaffe LF (1983) Sources of calcium in egg activation: a review and hypothesis. Dev Biol 99(2):265-276 0012-1606(83)90276-2 [pii]
29. Eisen A, Reynolds GT (1985) Source and sinks for the calcium released during fertilization of single sea urchin eggs. J Cell Biol 100(5):1522-1527
30. Samtleben S, Jaepel J, Fecher C, Andreska T, Rehberg M, Blum R (2013) Direct imaging of ER calcium with targeted-esterase induced dye loading (TED). J Vis Exp 75:e50317. doi: 10.3791/50317
31. Oude Weernink PA, Han L, Jakobs KH, Schmidt M (2007) Dynamic phospholipid signaling by G protein-coupled receptors. Biochim Biophys Acta 1768(4):888-900. doi: 10.1016/j.bbamem.2006.09.012
32. Endo M (2009) Calcium-induced calcium release in skeletal muscle. Physiol Rev 89(4):1153-1176. doi: 10.1152/physrev.00040.2008
33. Fill M, Copello JA (2002) Ryanodine receptor calcium release channels. Physiol Rev 82(4):893-922. doi: 10.1152/physrev.00013.2002
34. Putney JW Jr (2005) Capacitative calcium entry: sensing the calcium stores. J Cell Biol 169(3):381-382. doi: 10.1083/jcb.200503161
35. Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel SH, Tanasa B, Hogan PG, Lewis RS, Daly M, Rao A (2006) A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441(7090):179-185. doi: 10.1038/nature04702
36. Zhang SL, Yeromin AV, Zhang XH, Yu Y, Safrina O, Penna A, Roos J, Stauderman KA, Cahalan MD (2006) Genome-wide RNAi screen of Ca(2+) influx identifies genes that regulate Ca(2+) release-activated Ca(2+) channel activity. Proc Natl Acad Sci USA 103(24):9357-9362. doi: 10.1073/pnas.0603161103
37. Parekh AB, Penner R (1997) Store depletion and calcium influx. Physiol Rev 77(4):901-930
38. 2+ channel function. J Cell Biol 169(3):435-445. doi: 10.1083/jcb.200502019
39. 2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 437(7060):902-905. doi: 10.1038/nature04147
40. Gilkey JC, Jaffe LF, Ridgway EB, Reynolds GT (1978) A free calcium wave traverses the activating egg of the medaka, Oryzias latipes. J Cell Biol 76(2):448-466
41. Cheng H, Lederer WJ, Cannell MB (1993) Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science 262(5134):740-744
42. 2+ wave follows fertilization in eggs of the frog, Xenopus laevis. J Cell Biol 100(4):1325-1329
43. Mulkey RM, Zucker RS (1991) Action potentials must admit calcium to evoke transmitter release. Nature 350(6314):153-155. doi: 10.1038/350153a0
44. English AR, Voeltz GK (2013) Endoplasmic reticulum structure and interconnections with other organelles. Cold Spring Harb Perspect Biol 5(4):a013227. doi: 10.1101/cshperspect.a013227
45. Friedman JR, Voeltz GK (2011) The ER in 3D: a multifunctional dynamic membrane network. Trends Cell Biol 21(12):709-717. doi: 10.1016/j.tcb.2011.07.004
46. English AR, Zurek N, Voeltz GK (2009) Peripheral ER structure and function. Curr Opin Cell Biol 21(4):596-602. doi: 10.1016/j.ceb.2009.04.004
47. Shibata Y, Voeltz GK, Rapoport TA (2006) Rough sheets and smooth tubules. Cell 126(3):435-439. doi: 10.1016/j.cell.2006.07.019
48. Hu J, Prinz WA, Rapoport TA (2011) Weaving the web of ER tubules. Cell 147(6):1226-1231. doi: 10.1016/j.cell.2011.11.022
49. Bernales S, McDonald KL, Walter P (2006) Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol 4(12):e423. doi: 10.1371/journal.pbio.0040423
50. Terasaki M, Shemesh T, Kasthuri N, Klemm RW, Schalek R, Hayworth KJ, Hand AR, Yankova M, Huber G, Lichtman JW, Rapoport TA, Kozlov MM (2013) Stacked endoplasmic reticulum sheets are connected by helicoidal membrane motifs. Cell 154(2):285-296. doi: 10.1016/j.cell.2013.06.031
51. Shibata Y, Shemesh T, Prinz WA, Palazzo AF, Kozlov MM, Rapoport TA (2010) Mechanisms determining the morphology of the peripheral ER. Cell 143(5):774-788. doi: 10.1016/j.cell.2010.11.007
52. West M, Zurek N, Hoenger A, Voeltz GK (2011) A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature. J Cell Biol 193(2):333-346. doi: 10.1083/jcb.201011039
53. Staehelin LA (1997) The plant ER: a dynamic organelle composed of a large number of discrete functional domains. Plant J 11(6):1151-1165
54. Baumann O, Walz B (2001) Endoplasmic reticulum of animal cells and its organization into structural and functional domains. Int Rev Cytol 205:149-214
55. Block BA, Imagawa T, Campbell KP, Franzini-Armstrong C (1988) Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J Cell Biol 107(6 Pt 2):2587-2600
56. Takeshima H, Komazaki S, Nishi M, Iino M, Kangawa K (2000) Junctophilins: a novel family of junctional membrane complex proteins. Mol Cell 6(1):11-22 (S1097-2765(05)00005-5 [pii])
57. Voeltz GK, Prinz WA, Shibata Y, Rist JM, Rapoport TA (2006) A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124(3):573-586. doi: 10.1016/j.cell.2005.11.047
58. Shibata Y, Voss C, Rist JM, Hu J, Rapoport TA, Prinz WA, Voeltz GK (2008) The reticulon and DP1/Yop1p proteins form immobile oligomers in the tubular endoplasmic reticulum. J Biol Chem 283(27):18892-18904. doi: 10.1074/jbc.M800986200
59. De Craene JO, Coleman J, Estrada de Martin P, Pypaert M, Anderson S, Yates JR 3rd, Ferro-Novick S, Novick P (2006) Rtn1p is involved in structuring the cortical endoplasmic reticulum. Mol Biol Cell 17(7):3009-3020. doi: 10.1091/mbc.E06-01-0080
60. Anderson DJ, Hetzer MW (2008) Reshaping of the endoplasmic reticulum limits the rate for nuclear envelope formation. J Cell Biol 182(5):911-924. doi: 10.1083/jcb.200805140
61. Hu J, Shibata Y, Zhu PP, Voss C, Rismanchi N, Prinz WA, Rapoport TA, Blackstone C (2009) A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell 138(3):549-561. doi: 10.1016/j.cell.2009.05.025
62. Hu J, Shibata Y, Voss C, Shemesh T, Li Z, Coughlin M, Kozlov MM, Rapoport TA, Prinz WA (2008) Membrane proteins of the endoplasmic reticulum induce high-curvature tubules. Science 319(5867):1247-1250. doi: 10.1126/science.1153634
63. Park SH, Zhu PP, Parker RL, Blackstone C (2010) Hereditary spastic paraplegia proteins REEP1, spastin, and atlastin-1 coordinate microtubule interactions with the tubular ER network. J Clin Invest 120(4):1097-1110. doi: 10.1172/JCI40979
64. Bian X, Klemm RW, Liu TY, Zhang M, Sun S, Sui X, Liu X, Rapoport TA, Hu J (2011) Structures of the atlastin GTPase provide insight into homotypic fusion of endoplasmic reticulum membranes. Proc Natl Acad Sci USA 108(10):3976-3981. doi: 10.1073/pnas.1101643108
65. Wang S, Romano FB, Field CM, Mitchison TJ, Rapoport TA (2013) Multiple mechanisms determine ER network morphology during the cell cycle in Xenopus egg extracts. J Cell Biol 203(5):801-814. doi: 10.1083/jcb.201308001
66. Byrnes LJ, Sondermann H (2011) Structural basis for the nucleotide-dependent dimerization of the large G protein atlastin-1/SPG3A. Proc Natl Acad Sci USA 108(6):2216-2221. doi: 10.1073/pnas.1012792108
67. Orso G, Pendin D, Liu S, Tosetto J, Moss TJ, Faust JE, Micaroni M, Egorova A, Martinuzzi A, McNew JA, Daga A (2009) Homotypic fusion of ER membranes requires the dynamin-like GTPase atlastin. Nature 460(7258):978-983. doi: 10.1038/nature08280
68. Dreier L, Rapoport TA (2000) In vitro formation of the endoplasmic reticulum occurs independently of microtubules by a controlled fusion reaction. J Cell Biol 148(5):883-898
69. Turner MD, Plutner H, Balch WE (1997) A Rab GTPase is required for homotypic assembly of the endoplasmic reticulum. J Biol Chem 272(21):13479-13483
70. Audhya A, Desai A, Oegema K (2007) A role for Rab5 in structuring the endoplasmic reticulum. J Cell Biol 178(1):43-56. doi: 10.1083/jcb.200701139
71. English AR, Voeltz GK (2013) Rab10 GTPase regulates ER dynamics and morphology. Nat Cell Biol 15(2):169-178. doi: 10.1038/ncb2647
72. Gerondopoulos A, Bastos RN, Yoshimura S, Anderson R, Carpanini S, Aligianis I, Handley MT, Barr FA (2014) Rab18 and a Rab18 GEF complex are required for normal ER structure. J Cell Biol 205(5):707-720. doi: 10.1083/jcb.201403026
73. Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10(8):513-525. doi: 10.1038/nrm2728
74. Bahmanyar S, Biggs R, Schuh AL, Desai A, Muller-Reichert T, Audhya A, Dixon JE, Oegema K (2014) Spatial control of phospholipid flux restricts endoplasmic reticulum sheet formation to allow nuclear envelope breakdown. Genes Dev 28(2):121-126. doi: 10.1101/gad.230599.113
75. Lee C, Chen LB (1998) Dynamic behavior of endoplasmic reticulum in living cells. Cell 54(1):37-46 (0092-8674(88)90177-8 [pii])
76. Friedman JR, Webster BM, Mastronarde DN, Verhey KJ, Voeltz GK (2010) ER sliding dynamics and ER-mitochondrial contacts occur on acetylated microtubules. J Cell Biol 190(3):363-375. doi: 10.1083/jcb.200911024
77. Chen S, Desai T, McNew JA, Gerard P, Novick PJ, Ferro-Novick S (2015) Lunapark stabilizes nascent three-way junctions in the endoplasmic reticulum. Proc Natl Acad Sci USA 112(2):418-423. doi: 10.1073/pnas.1423026112
78. Chen S, Novick P, Ferro-Novick S (2012) ER network formation requires a balance of the dynamin-like GTPase Sey1p and the Lunapark family member Lnp1p. Nat Cell Biol 14(7):707-716. doi: 10.1038/ncb2523
79. Moriya K, Nagatoshi K, Noriyasu Y, Okamura T, Takamitsu E, Suzuki T, Utsumi T (2013) Protein N-myristoylation plays a critical role in the endoplasmic reticulum morphological change induced by overexpression of protein Lunapark, an integral membrane protein of the endoplasmic reticulum. PLoS One 8(11):e78235. doi: 10.1371/journal.pone.0078235
80. Puhka M, Vihinen H, Joensuu M, Jokitalo E (2007) Endoplasmic reticulum remains continuous and undergoes sheet-to-tubule transformation during cell division in mammalian cells. J Cell Biol 179(5):895-909. doi: 10.1083/jcb.200705112
81. Laneve P, Altieri F, Fiori ME, Scaloni A, Bozzoni I, Caffarelli E (2003) Purification, cloning, and characterization of XendoU, a novel endoribonuclease involved in processing of intron-encoded small nucleolar RNAs in Xenopus laevis. J Biol Chem 278(15):13026-13032 M211937200 [pii]
82. Schwarz DS, Blower MD (2014) The calcium-dependent ribonuclease XendoU promotes ER network formation through local RNA degradation. J Cell Biol 207(1):41-57. doi: 10.1083/jcb.201406037
83. Seidel CW, Peck LJ (1994) Purification of a calcium dependent ribonuclease from Xenopus laevis. Nucleic Acids Res 22(8):1456-1462
84. Lorca T, Galas S, Fesquet D, Devault A, Cavadore JC, Doree M (1991) Degradation of the proto-oncogene product p39mos is not necessary for cyclin proteolysis and exit from meiotic metaphase: requirement for a Ca(2+)-calmodulin dependent event. EMBO J 10(8):2087-2093
85. Sullivan KM, Busa WB, Wilson KL (1993) Calcium mobilization is required for nuclear vesicle fusion in vitro: implications for membrane traffic and IP3 receptor function. Cell 73(7):1411-1422 0092-8674(93)90366-X [pii]
86. Shibata Y, Hu J, Kozlov MM, Rapoport TA (2009) Mechanisms shaping the membranes of cellular organelles. Annu Rev Cell Dev Biol 25:329-354. doi: 10.1146/annurev.cellbio.042308.113324
87. Senda T, Yoshinaga-Hirabayashi T (1998) Intermembrane bridges within membrane organelles revealed by quick-freeze deep-etch electron microscopy. Anat Rec 251(3):339-345. doi: 10.1002/(SICI)1097-0185(199807)251:3<339:AID-AR9>3.0.CO;2-Q
88. Foster LJ, de Hoog CL, Zhang Y, Xie X, Mootha VK, Mann M (2006) A mammalian organelle map by protein correlation profiling. Cell 125(1):187-199. doi: 10.1016/j.cell.2006.03.022
89. Nagaraj N, Wisniewski JR, Geiger T, Cox J, Kircher M, Kelso J, Paabo S, Mann M (2011) Deep proteome and transcriptome mapping of a human cancer cell line. Mol Syst Biol 7:548. doi: 10.1038/msb.2011.81
90. Beck M, Schmidt A, Malmstroem J, Claassen M, Ori A, Szymborska A, Herzog F, Rinner O, Ellenberg J, Aebersold R (2011) The quantitative proteome of a human cell line. Mol Syst Biol 7:549. doi: 10.1038/msb.2011.82
91. Klopfenstein DR, Kappeler F, Hauri HP (1998) A novel direct interaction of endoplasmic reticulum with microtubules. EMBO J 17(21):6168-6177. doi: 10.1093/emboj/17.21.6168
92. Klopfenstein DR, Klumperman J, Lustig A, Kammerer RA, Oorschot V, Hauri HP (2001) Subdomain-specific localization of CLIMP-63 (p63) in the endoplasmic reticulum is mediated by its luminal alpha-helical segment. J Cell Biol 153(6):1287-1300
93. Nikonov AV, Hauri HP, Lauring B, Kreibich G (2007) Climp-63-mediated binding of microtubules to the ER affects the lateral mobility of translocon complexes. J Cell Sci 120(Pt 13):2248-2258. doi: 10.1242/jcs.008979
94. Ogawa-Goto K, Tanaka K, Ueno T, Kurata T, Sata T, Irie S (2007) p180 is involved in the interaction between the endoplasmic reticulum and microtubules through a novel microtubule-binding and bundling domain. Mol Biol Cell 18(10):3741-3751. doi: 10.1091/mbc.E06-12-1125
95. Toyoshima I, Yu H, Steuer ER, Sheetz MP (1992) Kinectin, a major kinesin-binding protein on ER. J Cell Biol 118(5):1121-1131
96. Allan V, Vale R (1994) Movement of membrane tubules along microtubules in vitro: evidence for specialised sites of motor attachment. J Cell Sci 107(Pt 7):1885-1897
97. Allan VJ, Vale RD (1991) Cell cycle control of microtubule-based membrane transport and tubule formation in vitro. J Cell Biol 113(2):347-359
98. Lane JD, Allan VJ (1999) Microtubule-based endoplasmic reticulum motility in Xenopus laevis: activation of membrane-associated kinesin during development. Mol Biol Cell 10(6):1909-1922
99. Waterman-Storer CM, Gregory J, Parsons SF, Salmon ED (1995) Membrane/microtubule tip attachment complexes (TACs) allow the assembly dynamics of plus ends to push and pull membranes into tubulovesicular networks in interphase Xenopus egg extracts. J Cell Biol 130(5):1161-1169
100. Waterman-Storer CM, Salmon ED (1998) Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms. Curr Biol 8(14):798-806 S0960-9822(98)70321-5 [pii]
101. Terasaki M, Chen LB, Fujiwara K (1986) Microtubules and the endoplasmic reticulum are highly interdependent structures. J Cell Biol 103(4):1557-1568
102. Desai A, Mitchison TJ (1997) Microtubule polymerization dynamics. Annu Rev Cell Dev Biol 13:83-117. doi: 10.1146/annurev.cellbio.13.1.83
103. Guttinger S, Laurell E, Kutay U (2009) Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nat Rev Mol Cell Biol 10(3):178-191. doi: 10.1038/nrm2641
104. Bobinnec Y, Marcaillou C, Morin X, Debec A (2003) Dynamics of the endoplasmic reticulum during early development of Drosophila melanogaster. Cell Motil Cytoskeleton 54(3):217-225. doi: 10.1002/cm.10094
105. Poteryaev D, Squirrell JM, Campbell JM, White JG, Spang A (2005) Involvement of the actin cytoskeleton and homotypic membrane fusion in ER dynamics in Caenorhabditis elegans. Mol Biol Cell 16(5):2139-2153. doi: 10.1091/mbc.E04-08-0726
106. McCullough S, Lucocq J (2005) Endoplasmic reticulum positioning and partitioning in mitotic HeLa cells. J Anat 206(5):415-425. doi: 10.1111/j.1469-7580.2005.00407.x
107. Puhka M, Joensuu M, Vihinen H, Belevich I, Jokitalo E (2012) Progressive sheet-to-tubule transformation is a general mechanism for endoplasmic reticulum partitioning in dividing mammalian cells. Mol Biol Cell 23(13):2424-2432. doi: 10.1091/mbc.E10-12-0950
108. Anderson DJ, Hetzer MW (2007) Nuclear envelope formation by chromatin-mediated reorganization of the endoplasmic reticulum. Nat Cell Biol 9(10):1160-1166. doi: 10.1038/ncb1636
109. Lu L, Ladinsky MS, Kirchhausen T (2011) Formation of the postmitotic nuclear envelope from extended ER cisternae precedes nuclear pore assembly. J Cell Biol 194(3):425-440. doi: 10.1083/jcb.201012063
110. Lu L, Ladinsky MS, Kirchhausen T (2009) Cisternal organization of the endoplasmic reticulum during mitosis. Mol Biol Cell 20(15):3471-3480. doi: 10.1091/mbc.E09-04-0327
111. Olmos Y, Hodgson L, Mantell J, Verkade P, Carlton JG (2015) ESCRT-III controls nuclear envelope reformation. Nature 522(7555):236-239. doi: 10.1038/nature14503
112. Vietri M, Schink KO, Campsteijn C, Wegner CS, Schultz SW, Christ L, Thoresen SB, Brech A, Raiborg C, Stenmark H (2015) Spastin and ESCRT-III coordinate mitotic spindle disassembly and nuclear envelope sealing. Nature 522(7555):231-235. doi: 10.1038/nature14408
113. Hurley JH (2015) ESCRTs are everywhere. EMBO J. doi: 10.15252/embj.201592484
114. Bian Y, Song C, Cheng K, Dong M, Wang F, Huang J, Sun D, Wang L, Ye M, Zou H (2014) An enzyme assisted RP-RPLC approach for in-depth analysis of human liver phosphoproteome. J Proteomics 96:253-262. doi: 10.1016/j.jprot.2013.11.014
115. Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, Mortensen P, Mann M (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127(3):635-648. doi: 10.1016/j.cell.2006.09.026
116. Olsen JV, Vermeulen M, Santamaria A, Kumar C, Miller ML, Jensen LJ, Gnad F, Cox J, Jensen TS, Nigg EA, Brunak S, Mann M (2010) Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci Signal 3(104):ra3. doi: 10.1126/scisignal.2000475
117. Rigbolt KT, Prokhorova TA, Akimov V, Henningsen J, Johansen PT, Kratchmarova I, Kassem M, Mann M, Olsen JV, Blagoev B (2011) System-wide temporal characterization of the proteome and phosphoproteome of human embryonic stem cell differentiation. Sci Signal 4(164):rs3. doi: 10.1126/scisignal.2001570
118. Dephoure N, Zhou C, Villen J, Beausoleil SA, Bakalarski CE, Elledge SJ, Gygi SP (2008) A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci USA 105(31):10762-10767. doi: 10.1073/pnas.0805139105
119. Daub H, Olsen JV, Bairlein M, Gnad F, Oppermann FS, Korner R, Greff Z, Keri G, Stemmann O, Mann M (2008) Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle. Mol Cell 31(3):438-448. doi: 10.1016/j.molcel.2008.07.007
120. Mayya V, Lundgren DH, Hwang SI, Rezaul K, Wu L, Eng JK, Rodionov V, Han DK (2009) Quantitative phosphoproteomic analysis of T cell receptor signaling reveals system-wide modulation of protein-protein interactions. Sci Signal 2(84):ra46. doi: 10.1126/scisignal.2000007
121. Vedrenne C, Klopfenstein DR, Hauri HP (2005) Phosphorylation controls CLIMP-63-mediated anchoring of the endoplasmic reticulum to microtubules. Mol Biol Cell 16(4):1928-1937. doi: 10.1091/mbc.E04-07-0554
122. Grigoriev I, Gouveia SM, van der Vaart B, Demmers J, Smyth JT, Honnappa S, Splinter D, Steinmetz MO, Putney JW Jr, Hoogenraad CC, Akhmanova A (2008) STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Curr Biol 18(3):177-182. doi: 10.1016/j.cub.2007.12.050
123. Smyth JT, Beg AM, Wu S, Putney JW Jr, Rusan NM (2012) Phosphoregulation of STIM1 leads to exclusion of the endoplasmic reticulum from the mitotic spindle. Curr Biol 22(16):1487-1493. doi: 10.1016/j.cub.2012.05.057
124. Schlaitz AL, Thompson J, Wong CC, Yates JR 3rd, Heald R (2013) REEP3/4 ensure endoplasmic reticulum clearance from metaphase chromatin and proper nuclear envelope architecture. Dev Cell 26(3):315-323. doi: 10.1016/j.devcel.2013.06.016
125. Vacquier VD (1981) Dynamic changes of the egg cortex. Dev Biol 84(1):1-26 (0012-1606(81)90366-3 [pii])
126. Whitaker M (2006) Calcium at fertilization and in early development. Physiol Rev 86(1):25-88. doi: 10.1152/physrev.00023.2005
127. Horner VL, Wolfner MF (2008) Transitioning from egg to embryo: triggers and mechanisms of egg activation. Dev Dyn 237(3):527-544. doi: 10.1002/dvdy.21454
128. Perry AC, Verlhac MH (2008) Second meiotic arrest and exit in frogs and mice. EMBO Rep 9(3):246-251. doi: 10.1038/embor.2008.22
129. Stricker SA (2006) Structural reorganizations of the endoplasmic reticulum during egg maturation and fertilization. Semin Cell Dev Biol 17(2):303-313. doi: 10.1016/j.semcdb.2006.02.002
130. Terasaki M, Runft LL, Hand AR (2001) Changes in organization of the endoplasmic reticulum during Xenopus oocyte maturation and activation. Mol Biol Cell 12(4):1103-1116
131. Kume S, Yamamoto A, Inoue T, Muto A, Okano H, Mikoshiba K (1997) Developmental expression of the inositol 1,4,5-trisphosphate receptor and structural changes in the endoplasmic reticulum during oogenesis and meiotic maturation of Xenopus laevis. Dev Biol 182(2):228-239. doi: 10.1006/dbio.1996.8479
132. Henson JH, Beaulieu SM, Kaminer B, Begg DA (1990) Differentiation of a calsequestrin-containing endoplasmic reticulum during sea urchin oogenesis. Dev Biol 142(2):255-269
133. Jaffe LA, Terasaki M (1994) Structural changes in the endoplasmic reticulum of starfish oocytes during meiotic maturation and fertilization. Dev Biol 164(2):579-587. doi: 10.1006/dbio.1994.1225
134. Mehlmann LM, Terasaki M, Jaffe LA, Kline D (1995) Reorganization of the endoplasmic reticulum during meiotic maturation of the mouse oocyte. Dev Biol 170(2):607-615. doi: 10.1006/dbio.1995.1240
135. FitzHarris G, Marangos P, Carroll J (2007) Changes in endoplasmic reticulum structure during mouse oocyte maturation are controlled by the cytoskeleton and cytoplasmic dynein. Dev Biol 305(1):133-144. doi: 10.1016/j.ydbio.2007.02.006
136. Mendez R, Richter JD (2001) Translational control by CPEB: a means to the end. Nat Rev Mol Cell Biol 2(7):521-529. doi: 10.1038/35080081
137. Kessel RG (1992) Annulate lamellae: a last frontier in cellular organelles. Int Rev Cytol 133:43-120
138. 2+ wave following fertilization of the Xenopus egg requires the production of Ins(1, 4, 5)P3. Dev Biol 158(1):200-212. doi: 10.1006/dbio.1993.1179
139. Han JK, Nuccitelli R (1990) Inositol 1,4,5-trisphosphate-induced calcium release in the organelle layers of the stratified, intact egg of Xenopus laevis. J Cell Biol 110(4):1103-1110
140. Steinhardt R, Zucker R, Schatten G (1977) Intracellular calcium release at fertilization in the sea urchin egg. Dev Biol 58(1):185-196 0012-1606(77)90084-7 [pii]
141. Ridgway EB, Gilkey JC, Jaffe LF (1977) Free calcium increases explosively in activating medaka eggs. Proc Natl Acad Sci USA 74(2):623-627
142. 2+ oscillation by antibody to the inositol 1,4,5-trisphosphate receptor in fertilized hamster eggs. Science 257(5067):251-255
143. Terasaki M, Sardet C (1991) Demonstration of calcium uptake and release by sea urchin egg cortical endoplasmic reticulum. J Cell Biol 115(4):1031-1037
144. Terasaki M, Jaffe LA, Hunnicutt GR, Hammer JA 3rd (1996) Structural change of the endoplasmic reticulum during fertilization: evidence for loss of membrane continuity using the green fluorescent protein. Dev Biol 179(2):320-328 S0012160696902638 [pii]
145. Kline D, Mehlmann L, Fox C, Terasaki M (1999) The cortical endoplasmic reticulum (ER) of the mouse egg: localization of ER clusters in relation to the generation of repetitive calcium waves. Dev Biol 215(2):431-442. doi: 10.1006/dbio.1999.9445
146. Mehlmann LM, Mikoshiba K, Kline D (1996) Redistribution and increase in cortical inositol 1,4,5-trisphosphate receptors after meiotic maturation of the mouse oocyte. Dev Biol 180(2):489-498. doi: 10.1006/dbio.1996.0322
147. Tabas I, Ron D (2011) Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 13(3):184-190. doi: 10.1038/ncb0311-184
148. Nilsson IM, von Heijne G (1993) Determination of the distance between the oligosaccharyltransferase active site and the endoplasmic reticulum membrane. J Biol Chem 268(8):5798-5801
149. Jitsuhara Y, Toyoda T, Itai T, Yamaguchi H (2002) Chaperone-like functions of high-mannose type and complex-type N-glycans and their molecular basis. J Biochem 132(5):803-811
150. Hanson SR, Culyba EK, Hsu TL, Wong CH, Kelly JW, Powers ET (2009) The core trisaccharide of an N-linked glycoprotein intrinsically accelerates folding and enhances stability. Proc Natl Acad Sci USA 106(9):3131-3136. doi: 10.1073/pnas.0810318105
151. Kaufman RJ (1999) Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 13(10):1211-1233
152. Kaufman RJ, Scheuner D, Schroder M, Shen X, Lee K, Liu CY, Arnold SM (2002) The unfolded protein response in nutrient sensing and differentiation. Nat Rev Mol Cell Biol 3(6):411-421. doi: 10.1038/nrm829
153. Lee AS (1992) Mammalian stress response: induction of the glucose-regulated protein family. Curr Opin Cell Biol 4(2):267-273
154. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8(7):519-529. doi: 10.1038/nrm2199
155. Walter P, Ron D (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334(6059):1081-1086. doi: 10.1126/science.1209038
156. Schuck S, Prinz WA, Thorn KS, Voss C, Walter P (2009) Membrane expansion alleviates endoplasmic reticulum stress independently of the unfolded protein response. J Cell Biol 187(4):525-536. doi: 10.1083/jcb.200907074
157. Yanagitani K, Imagawa Y, Iwawaki T, Hosoda A, Saito M, Kimata Y, Kohno K (2009) Cotranslational targeting of XBP1 protein to the membrane promotes cytoplasmic splicing of its own mRNA. Mol Cell 34(2):191-200. doi: 10.1016/j.molcel.2009.02.033
158. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107(7):881-891 S0092-8674(01)00611-0 [pii]
159. Lee K, Tirasophon W, Shen X, Michalak M, Prywes R, Okada T, Yoshida H, Mori K, Kaufman RJ (2002) IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev 16(4):452-466. doi: 10.1101/gad.964702
160. Hollien J, Weissman JS (2006) Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313(5783):104-107. doi: 10.1126/science.1129631
161. Gaddam D, Stevens N, Hollien J (2013) Comparison of mRNA localization and regulation during endoplasmic reticulum stress in Drosophila cells. Mol Biol Cell 24(1):14-20. doi: 10.1091/mbc.E12-06-0491
162. Cao Y, Knochel S, Oswald F, Donow C, Zhao H, Knochel W (2006) XBP1 forms a regulatory loop with BMP-4 and suppresses mesodermal and neural differentiation in Xenopus embryos. Mech Dev 123(1):84-96. doi: 10.1016/j.mod.2005.09.003
163. Brar GA, Yassour M, Friedman N, Regev A, Ingolia NT, Weissman JS (2012) High-resolution view of the yeast meiotic program revealed by ribosome profiling. Science 335(6068):552-557. doi: 10.1126/science.1215110
164. Davidowitz J, Philips GH, Pachter BR, Breinin GM (1975) Particle-free and glycogen-bearing double membrane arrays in extraocular muscle of rabbit. Am J Pathol 78(2):191-198