Multi-step down-regulation of the secretory pathway in mitosis: A fresh perspective on protein trafficking

BioEssays

Volumn 35, Issue 5, 2013, Pages 462-471

  Yeong, Foong May ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

CDK1; Cell division cycle; Endoplasmic reticulum; Golgi; Mitosis; Protein trafficking

Indexed keywords

CYCLIN B2; CYCLIN D; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6;

ACTIN FILAMENT; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CELL DIVISION; CELL VACUOLE; CYTOSKELETON; DOWN REGULATION; GOLGI COMPLEX; INHIBITION KINETICS; MITOSIS; MOLECULAR DYNAMICS; PROTEIN TRANSPORT;

ACTINS; ANIMALS; CDC2 PROTEIN KINASE; CHO CELLS; CRICETULUS; ENDOPLASMIC RETICULUM, ROUGH; GENE EXPRESSION REGULATION; GOLGI APPARATUS; HUMANS; MICROTUBULES; MITOSIS; PROTEIN TRANSPORT; SECRETORY PATHWAY;

EID: 84876339593     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201200144     Document Type: Article

References (115)

1. Lee MC, Miller EA, Goldberg J, Orci L, et al. 2004. Bi-directional protein transport between the ER and Golgi. Annu Rev Cell Dev Biol 20: 87- 123.
2. Sato K, Nakano A. 2007. Mechanisms of COPII vesicle formation and protein sorting. FEBS Lett 581: 2076- 82.
3. Lee MC, Miller EA. 2007. Molecular mechanisms of COPII vesicle formation. Semin Cell Dev Biol 18: 424- 34.
4. Mellman I, Nelson WJ. 2008. Coordinated protein sorting, targeting and distribution in polarized cells. Nat Rev Mol Cell Biol 9: 833- 45.
5. Apodaca G, Gallo LI, Bryant DM. 2012. Role of membrane traffic in the generation of epithelial cell asymmetry. Nat Cell Biol 14: 1235- 43.
6. Perrais D, Merrifield CJ. 2005. Dynamics of endocytic vesicle creation. Dev Cell 9: 581- 92.
7. Sandvig K, Pust S, Skotland T, van Deurs B. 2011. Clathrin-independent endocytosis: mechanisms and function. Curr Opin Cell Biol 23: 413- 20.
8. Houtari J, Helenius A. 2011. Endosome maturation. EMBO J 30: 3481- 500.
9. Furthauer M, Gonzalez-Gaitan M. 2009. Endocytosis and mitosis: a two-way relationship. Cell Cycle 8: 3311- 8.
10. Fielding A, Royle S. 2013. Mitotic inhibition of clathrin-mediated endocytosis. Cell Mol Life Sci, in press, DOI 10.1007/s00018-012-1250-8.
11. Zanetti G, Pahuja KB, Studer S, Shim S, et al. 2012. COPII and the regulation of protein sorting in mammals. Nat Cell Biol 14: 20- 8.
12. Obaya AJ, Sedivy JM. 2002. Regulation of cyclin-Cdk activity in mammalian cells. Cell Mol Life Sci 59: 126- 42.
13. Vermeulen K, Van Bockstaele DR, Berneman ZN. 2003. The cell cycle: a review of regulation, deregulation and therapeutic targets in cancer. Cell Prolif 36: 131- 49.
14. Miller EA, Barlowe C. 2010. Regulation of coat assembly - sorting things out at the ER. Curr Opin Cell Biol 22: 447- 53.
15. Dancourt J, Barlowe C. 2010. Protein sorting receptors in the early secretory pathway. Annu Rev Biochem 79: 777- 802.
16. Kirk SJ, Ward TH. 2007. COPII under the microscope. Semin Cell Dev Biol 18: 435- 47.
17. Budnik A, Stephens DJ. 2009. ER exit sites - localization and control of COPII vesicle formation. FEBS Lett 583: 3796- 803.
18. Orci L, Ravazzola M, Meda P, Holcomb C, et al. 1991. Mammalian Sec23p homologue is restricted to the endoplasmic reticulum transitional cytoplasm. Proc Natl Acad Sci USA 88: 8611- 5.
19. Hammond AT, Glick BS. 2000. Dynamics of transitional endoplasmic reticulum sites in vertebrate cells. Mol Biol Cell 11: 3013- 30.
20. Stephens DJ, Lin-Marq N, Pagano A, Pepperkok R, et al. 2000. COPI-coated ER-to-Golgi transport complexes segregate from COPII in close proximity to ER exit sites. J Cell Sci 113: 2177- 85.
21. Spang A. 2009. On vesicle formation and tethering in the ER-Golgi shuttle. Curr Opin Cell Biol 21: 531- 6.
22. Watson P, Townley AK, Koka P, Palmer KJ, et al. 2006. Sec16 defines endoplasmic reticulum exit sites and is required for secretory cargo export in mammalian cells. Traffic 7: 1678- 87.
23. Bhattacharyya D, Glick BS. 2007. Two mammalian Sec16 homologues have nonredundant functions in endoplasmic reticulum (ER) export and transitional ER organization. Mol Biol Cell 18: 839- 49.
24. Hughes H, Budnik A, Schmidt K, Palmer KJ, et al. 2009. Organisation of human ER-exit sites: requirements for the localisation of Sec16 to transitional ER. J Cell Sci 122: 2924- 34.
25. Montegna EA, Bhave M, Liu Y, Bhattacharyya D, et al. 2012. Sec12 binds to Sec16 at transitional ER sites. PLoS ONE 7: e31156.
26. Whittle JR, Schwartz TU. 2010. Structure of the Sec13-Sec16 edge element, a template for assembly of the COPII vesicle coat. J Cell Biol 190: 347- 61.
27. Espenshade P, Gimeno RE, Holzmacher E, Teung P, et al. 1995. Yeast SEC16 gene encodes a multidomain vesicle coat protein that interacts with Sec23p. J Cell Biol 131: 311- 24.
28. Supek F, Madden DT, Hamamoto S, Orci L, et al. 2002. Sec16p potentiates the action of COPII proteins to bud transport vesicles. J Cell Biol 158: 1029- 38.
29. Cai H, Reinisch K, Ferro-Novick S. 2007. Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev Cell 12: 671- 82.
30. Lorente-Rodriguez A, Barlowe C. 2011. Entry and exit mechanisms at the cis-face of the Golgi complex. Cold Spring Harb Perspect Biol 3: a005207.
31. Lupashin V, Sztul E. 2005. Golgi tethering factors. Biochim Biophys Acta 1744: 325- 39.
32. Brocker C, Engelbrecht-Vandre S, Ungermann C. 2010. Multisubunit tethering complexes and their role in membrane fusion. Curr Biol 20: R943- 52.
33. Glick BS, Luini A. 2011. Models for Golgi traffic: a critical assessment. Cold Spring Harb Perspect Biol 3: a005215.
34. Mironov AA, Beznoussenko GV. 2012. The Kiss-and-Run model of intra-Golgi transport. Int J Mol Sci 13: 6800- 19.
35. Storrie B, Pepperkok R, Nilsson T. 2000. Breaking the COPI monopoly on Golgi recycling. Trends Cell Biol 10: 385- 90.
36. Sannerud R, Saraste J, Goud B. 2003. Retrograde traffic in the biosynthetic-secretory route: pathways and machinery. Curr Opin Cell Biol 15: 438- 45.
37. De Matteis MA, Luini A. 2008. Exiting the Golgi complex. Nat Rev Mol Cell Biol 9: 273- 84.
38. Bard F, Malhotra V. 2006. The formation of TGN-to-plasma-membrane transport carriers. Annu Rev Cell Dev Biol 22: 439- 55.
39. Luini A, Mironov AA, Polishchuk EV, Polishchuk RS. 2008. Morphogenesis of post-Golgi transport carriers. Histochem Cell Biol 129: 153- 61.
40. Anitei M, Hoflack B. 2011. Exit from the trans-Golgi network: from molecules to mechanisms. Curr Opin Cell Biol 23: 443- 51.
41. Caviston JP, Holzbaur ELF. 2006. Microtubule motors at the intersection of trafficking and transport. Trends Cell Biol 16: 530- 7.
42. Murshid A, Presley JF. 2004. ER-to-Golgi transport and cytoskeletal interactions in animal cells. Cell Mol Life Sci 61: 133- 45.
43. Loubury S, Coudrier E. 2008. Myosins in the secretory pathway: tethers or transporters? Cell Mol Life Sci 65: 2790- 800.
44. Eyster CA, Olson AL. 2009. Compartmentalization and regulation of insulin signaling to GLUT4 by the cytoskeleton. Vitam Horm 80: 193- 215.
45. Warren G, Featherstone C, Griffiths G, Burke B. 1983. Newly synthesized G protein of vesicular stomatitis virus is not transported to the cell surface during mitosis. J Cell Biol 97: 1623- 8.
46. Featherstone C, Griffiths G, Warren G. 1985. Newly synthesized G protein of vesicular stomatitis virus is not transported to the Golgi complex in mitotic cells. J Cell Biol 101: 2036- 46.
47. Hauri HP, Kappeler F, Andersson H, Appenzeller C. 2000. ERGIC-53 and traffic in the secretory pathway. J Cell Sci 113: 587- 96.
48. Farmaki T, Ponnambalam S, Prescott AR, Clausen H, et al. 1999. Forward and retrograde trafficking in mitotic animal cells. ER-Golgi transport arrest restricts protein export from the ER into COPII-coated structures. J Cell Sci 112: 589- 600.
49. Kreiner T, Moore HP. 1990. Membrane traffic between secretory compartments is differentially affected during mitosis. Cell Regul 1: 415- 24.
50. Hesketh TR, Beaven MA, Rogers J, Burke B, et al. 1984. Stimulated release of histamine by a rat mast cell line is inhibited during mitosis. J Cell Biol 98: 2250- 4.
51. Dudognon P, Maeder-Garavaglia C, Carpentier J-L, Paccaud J-P. 2004. Regulation of a COPII component by cytosolic O-glycosylation during mitosis. FEBS Lett 561: 44- 50.
52. Prescott AR, Farmaki T, Thomson C, James J, et al. 2001. Evidence for prebudding arrest of ER export in animal cell mitosis and its role in generating Golgi partitioning intermediates. Traffic 2: 321- 35.
53. Stephens DJ. 2003. De novo formation, fusion and fission of mammalian COPII-coated endoplasmic reticulum exit sites. EMBO Rep 4: 210- 7.
54. Hughes H, Stephens DJ. 2010. Sec16A defines the site for vesicle budding from the endoplasmic reticulum on exit from mitosis. J Cell Sci 123: 4032- 8.
55. Kano F, Tanaka AR, Yamauchi S, Kondo H, et al. 2004. Cdc2 kinase-dependent disassembly of endoplasmic reticulum (ER) exit sites inhibits ER-to-Golgi vesicular transport during mitosis. Mol Biol Cell 15: 4289- 98.
56. Dykstra KM, Pokusa JE, Suhan J, Lee TH. 2010. Yip1A structures the mammalian endoplasmic reticulum. Mol Biol Cell 21: 1556- 68.
57. Uchiyama K, Kondo H. 2005. p97/p47-mediated biogenesis of Golgi and ER. J Biochem 137: 115- 9.
58. Forster R, Weiss M, Zimmermann T, Reynaud EG, et al. 2006. Secretory cargo regulates the turnover of COPII subunits at single ER exit sites. Curr Biol 16: 173- 9.
59. Farhan H, Weiss M, Tani K, Kaufman RJ, et al. 2008. Adaptation of endoplasmic reticulum exit sites to acute and chronic increases in cargo load. EMBO J 27: 2043- 54.
60. Le Breton M, Cormier P, Belle R, Mulner-Lorillon O, et al. 2005. Translational control during mitosis. Biochimie 87: 805- 11.
61. Scharff MD, Robbins E. 1966. Polyribosome disaggregation during metaphase. Science 151: 992- 5.
62. Hernandez-Verdun D. 2011. Assembly and disassembly of the nucleolus during the cell cycle. Nucleus 2: 189- 94.
63. Sivan G, Elroy-Stein O. 2008. Regulation of mRNA translation during cellular division. Cell Cycle 7: 741- 4.
64. Balch WE, Dunphy WG, Braell WA, Rothman JE. 1984. Reconstitution of the transport of protein between successive compartments of the Golgi measured by the coupled incorporation of N-acetylglucosamine. Cell 39: 405- 16.
65. Mackay D, Kieckbusch R, Adamczewski J, Warren G. 1993. Cyclin A-mediated inhibition of intra-Golgi transport requires p34cdc2. FEBS Lett 336: 549- 54.
66. Stuart RA, Mackay D, Adamczewski J, Warren G. 1993. Inhibition of intra-Golgi transport in vitro by mitotic kinase. J Biol Chem 268: 4050- 4.
67. Collins RN, Warren G. 1992. Sphingolipid transport in mitotic HeLa cells. J Biol Chem 267: 24906- 11.
68. Shorter J, Warren G. 2002. Golgi architecture and inheritance. Annu Rev Cell Dev Biol 18: 379- 420.
69. Persico A, Cervigni RI, Barretta ML, Colanzi A. 2009. Mitotic inheritance of the Golgi complex. FEBS Lett 583: 3857- 62.
70. Sengupta D, Linstedt AD. 2011. Control of organelle size: the Golgi complex. Annu Rev Cell Dev Biol 27: 57- 77.
71. Wei JH, Seemann J. 2009. Mitotic division of the mammalian Golgi apparatus. Semin Cell Dev Biol 20: 810- 6.
72. Vinke FP, Grieve AG, Rabouille C. 2011. The multiple facets of the Golgi reassembly stacking proteins. Biochem J 433: 423- 33.
73. Klumperman J. 2011. Architecture of the mammalian Golgi. Cold Spring Harb Perspect Biol 3: a005181.
74. Wang Y, Seemann J. 2011. Golgi biogenesis. Cold Spring Harb Perspect Biol 3: a005330.
75. Draviam VM, Orrechia S, Lowe M, Pardi R, et al. 2001. The localization of human cyclins B1 and B2 determines CDK1 substrate specificity and neither enzyme requires Mek to disassemble the Golgi apparatus. J Cell Biol 152: 945- 58.
76. Borgonovo B, Ouwendijk J, Solimena M. 2006. Biogenesis of secretory granules. Curr Opin Cell Biol 18: 365- 70.
77. Bukoreshtliev NV, Hodneland E, Eichler TW, Eifart P, et al. 2012. Partitioning and exocytosis of secretory granules during division of PC12 cells. Int J Cell Biol 2012: 1- 14.
78. English AR, Zurek N, Voeltz GK. 2009. Peripheral ER structure and function. Curr Opin Cell Biol 21: 596- 602.
79. Guttinger S, Laura E, Kutay U. 2009. Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nat Rev Mol Cell Biol 10: 178- 91.
80. Lu L, Landinsky MD, Kirchhausen T. 2009. Cisternal organization of the endoplasmic reticulum during mitosis. Mol Biol Cell 20: 3471- 80.
81. Puhka M, Joensuu M, Vihinen H, Belevich I, et al. 2012. Progressive sheet-to-tubule transformation is a general mechanism for endoplasmic reticulum partitioning in dividing mammalian cells. Mol Biol Cell 23: 2424- 32.
82. 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: 895- 909.
83. Barr FA. 2002. Inheritance of the endoplasmic reticulum and Golgi apparatus. Curr Opin Cell Biol 14: 496- 9.
84. Nevalainen LT, Louhelainen J, Makarow M. 1989. Post-translational modifications in mitotic yeast cells. Eur J Biochem 184: 165- 72.
85. Makarow M. 1988. Secretion of invertase in mitotic yeast cells. EMBO J 7: 1475- 82.
86. Wei J-H, Seemann J. 2010. Unraveling the Golgi ribbon. Traffic 11: 1391- 400.
87. Nakamura N, Lowe M, Levine TP, Rabouille C, et al. 1997. The vesicle docking protein p115 binds GM130, a cis-Golgi matrix protein, in a mitotically regulated manner. Cell 89: 445- 55.
88. Lowe M, Rabouille C, Nakamura N, Watson R, et al. 1998. Cdc2 kinase directly phosphorylates the cis-Golgi matrix protein GM130 and is required for Golgi fragmentation in mitosis. Cell 94: 783- 93.
89. Lin C-Y, Madsen ML, Yarm FR, Jang Y-J et al. 2000. Peripheral Golgi protein GRASP65 is a target of mitotic polo-like kinase (Plk) and Cdc2. Proc Natl Acad Sci USA 97: 12589- 94.
90. Wang Y, Seemann J, Pypaert M, Shorter J, et al. 2003. A direct role for GRASP65 as a mitotically regulated Golgi stacking factor. EMBO J 22: 3279- 90.
91. Tang D, Mar K, Warren G, Wang Y. 2008. Molecular mechanism of mitotic Golgi disassembly and reassembly revealed by a defined reconstitution assay. J Biol Chem 283: 6085- 94.
92. Xiang Y, Wang Y. 2010. GRASP55 and GRASP65 play complementary and essential roles in Golgi cisternal stacking. J Cell Biol 188: 237- 51.
93. Uchiyama K, Totsukawa G, Puhka M, Kaneko Y, et al. 2006. p37 is a p97 adaptor required for Golgi and ER biogenesis in interphase and at the end of mitosis. Dev Cell 11: 803- 16.
94. Uchiyama K, Jokitalo E, Lindman M, Jackman M, et al. 2003. The localization and phosphorylation of p47 are important for Golgi disassembly-assembly during the cell cycle. J Cell Biol 161: 1067- 79.
95. Kaneko Y, Tamura K, Totsukawa G, Kondo H. 2010. Phosphorylation of p37 is important for Golgi disassembly at mitosis. Biochem Biophys Res Commun 402: 37- 41.
96. Puthenveedu MA, Bachert C, Puri S, Lanni F, et al. 2006. GM130 and GRASP65-dependent lateral cisternal fusion allows uniform Golgi-enzyme distribution. Nat Cell Biol 8: 238- 48.
97. de Forges H, Bouissou A, Perez F. 2012. Interplay between microtubule dynamics and intracellular organization. Int J Biochem Cell Biol 44: 266- 74.
98. Walczak CE, Heald R. 2008. Mechanisms of mitotic spindle assembly and function. Int Rev Cytol 265: 111- 58.
99. Heng Y-W, Koh C-G. 2010. Actin cytoskeleton dynamics and the cell division cycle. Int J Biochem Cell Biol 42: 1622- 33.
100. Fourest-Lieuvin A, Peris L, Gache V, Garcia-Saez I, et al. 2006. Microtubule regulation in mitosis: tubulin phosphorylation by the cyclin-dependent kinase Cdk1. Mol Biol Cell 17: 1041- 50.
101. Cukier IH, Li Y, Lee JM. 2007. Cyclin B1/Cdk1 binds and phosphorylates Filamin A and regulates its ability to cross-link actin. FEBS Lett 581: 1661- 72.
102. Sullivan M, Morgan DO. 2007. Finishing mitosis, one step at a time. Nat Rev Mol Cell Biol 8: 894- 903.
103. Nigg EA. 2001. Mitotic kinases as regulators of cell division and its checkpoints. Nat Rev Mol Cell Biol 2: 21- 32.
104. Jin P, Hardy S, Morgan DO. 1998. Nuclear localization of cyclin B1 controls mitotic entry after DNA damage. J Cell Biol 141: 875- 85.
105. Nakajima H, Yonemura S, Murata M, Nakamura N, et al. 2008. Myt1 protein kinase is essential for Golgi and ER assembly during mitotic exit. J Cell Biol 181: 89- 103.
106. Souter E, Pypaert M, Warren G. 1993. The Golgi stack reassembles during telophase before arrival of proteins transported from the endoplasmic reticulum. J Cell Biol 122: 533- 40.
107. McKay HF, Burgess DR. 2011. 'Life is a highway': membrane trafficking during cytokinesis. Traffic 12: 247- 51.
108. Montagnac G, Echard A, Chavrier P. 2008. Endocytic traffic in animal cell cytokinesis. Curr Opin Cell Biol 20: 454- 61.
109. Prekeris R, Gould GW. 2008. Breaking up is hard to do - membrane traffic in cytokinesis. J Cell Sci 121: 1569- 76.
110. Schweitzer JK, Burke EE, Goodson HV, D'Souza-Schorey C. 2005. Endocytosis resumes during late mitosis and is required for cytokinesis. J Biol Chem 280: 41628- 35.
111. Schiel JA, Prekeris R. 2010. Making the final cut - mechanisms mediating the abscission step of cytokinesis. Sci World J 10: 1424- 34.
112. Chen C-T, Hehnly H, Doxsey SJ. 2012. Orchestrating vesicle transport, ESCRTs and kinase surveillance during abscission. Nat Rev Mol Cell Biol 13: 483- 8.
113. Kim J, Hamamoto S, Ravazzola M, Orci L, et al. 2005. Uncoupled packaging of amyloid precursor protein and presenilin 1 into coat protein complex II vesicles. J Biol Chem 280: 7758- 68.
114. Friedman JR, Voeltz GK. 2011. The ER in 3D: a multifunctional dynamic membrane network. Trends Cell Biol 21: 709- 17.
115. Blethrow JD, Glavy JS, Morgan DO, Shokat KM. 2008. Covalent capture of kinase-specific phosphopeptides reveals Cdk1-cyclin B substrates. Proc Natl Acad Sci USA 105: 1442- 7.