© The Rockefeller University Press,
0021-9525/1997//1199 $5.00
The Journal of Cell Biology, Volume 137, Number 6,
, 1997 1199-1210
Integral Membrane Proteins of the Nuclear Envelope Are Dispersed throughout the Endoplasmic Reticulum during Mitosis
Li Yang,
Tinglu Guan, and
Larry Gerace
Department of Cell and Molecular Biology, The Scripps Research Institute, La Jolla, California 92037
We have analyzed the fate of several integral membrane proteins of the nuclear envelope during mitosis in cultured mammalian cells to determine whether nuclear membrane proteins are present in a vesicle population distinct from bulk ER membranes after mitotic nuclear envelope disassembly or are dispersed throughout the ER. Using immunofluorescence staining and confocal microscopy, we compared the localization of two inner nuclear membrane proteins (laminaassociated polypeptides 1 and 2 [LAP1 and LAP2]) and a nuclear pore membrane protein (gp210) to the distribution of bulk ER membranes, which was determined with lipid dyes (DiOC6 and R6) and polyclonal antibodies. We found that at the resolution of this technique, the three nuclear envelope markers become completely dispersed throughout ER membranes during mitosis. In agreement with these results, we detected LAP1 in most membranes containing ER markers by immunogold electron microscopy of metaphase cells. Together, these findings indicate that nuclear membranes lose their identity as a subcompartment of the ER during mitosis. We found that nuclear lamins begin to reassemble around chromosomes at the end of mitosis at the same time as LAP1 and LAP2 and propose that reassembly of the nuclear envelope at the end of mitosis involves sorting of integral membrane proteins to chromosome surfaces by binding interactions with lamins and chromatin.
Abbreviations used in this paper: LAP, lamina-associated polypeptide; LBR, lamin binding receptor; NE, nuclear envelope; NPC, nuclear pore complex; NRK, normal rat kidney; GFP, green fluorescent protein.
Address all correspondence to Larry Gerace, Department of Cell and Molecular Biology, The Scripps Research Institute, La Jolla, CA 92037. Tel.: (619) 784-8514. Fax: (619) 784-9132.

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-
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[Full Text]
-
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-
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[Abstract]
[Full Text]
-
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(2001). A New Model for Nuclear Envelope Breakdown. Mol. Biol. Cell
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[Abstract]
[Full Text]
-
Hutchison, C., Alvarez-Reyes, M, Vaughan, O.
(2001). Lamins in disease: why do ubiquitously expressed nuclear envelope proteins give rise to tissue-specific disease phenotypes?. J. Cell Sci.
114: 9-19
[Abstract]
-
Moir, R. D., Yoon, M., Khuon, S., Goldman, R. D.
(2000). Nuclear Lamins a and B1: Different Pathways of Assembly during Nuclear Envelope Formation in Living Cells. JCB
151: 1155-1168
[Abstract]
[Full Text]
-
Lee, K. K., Gruenbaum, Y., Spann, P., Liu, J., Wilson, K. L.
(2000). C. elegans Nuclear Envelope Proteins Emerin, MAN1, Lamin, and Nucleoporins Reveal Unique Timing of Nuclear Envelope Breakdown during Mitosis. Mol. Biol. Cell
11: 3089-3099
[Abstract]
[Full Text]
-
Terasaki, M.
(2000). Dynamics of the Endoplasmic Reticulum and Golgi Apparatus during Early Sea Urchin Development. Mol. Biol. Cell
11: 897-914
[Abstract]
[Full Text]
-
Sullivan, T., Escalante-Alcalde, D., Bhatt, H., Anver, M., Bhat, N., Nagashima, K., Stewart, C. L., Burke, B.
(1999). Loss of a-Type Lamin Expression Compromises Nuclear Envelope Integrity Leading to Muscular Dystrophy. JCB
147: 913-920
[Abstract]
[Full Text]
-
Drummond, S., Ferrigno, P., Lyon, C., Murphy, J., Goldberg, M., Allen, T., Smythe, C., Hutchison, C. J.
(1999). Temporal Differences in the Appearance of NEP-B78 and an LBR-like Protein during Xenopus Nuclear Envelope Reassembly Reflect the Ordered Recruitment of Functionally Discrete Vesicle Types. JCB
144: 225-240
[Abstract]
[Full Text]
-
Broers, J., Machiels, B., van Eys, G., Kuijpers, H., Manders, E., van Driel, R, Ramaekers, F.
(1999). Dynamics of the nuclear lamina as monitored by GFP-tagged A-type lamins. J. Cell Sci.
112: 3463-3475
[Abstract]
-
Fairley, E., Kendrick-Jones, J, Ellis, J.
(1999). The Emery-Dreifuss muscular dystrophy phenotype arises from aberrant targeting and binding of emerin at the inner nuclear membrane. J. Cell Sci.
112: 2571-2582
[Abstract]
-
Gajewski, A, Krohne, G
(1999). Subcellular distribution of the Xenopus p58/lamin B receptor in oocytes and eggs. J. Cell Sci.
112: 2583-2596
[Abstract]
-
Bodoor, K, Shaikh, S, Salina, D, Raharjo, W., Bastos, R, Lohka, M, Burke, B
(1999). Sequential recruitment of NPC proteins to the nuclear periphery at the end of mitosis. J. Cell Sci.
112: 2253-2264
[Abstract]
-
Goldberg, M., Lu, H., Stuurman, N., Ashery-Padan, R., Weiss, A. M., Yu, J., Bhattacharyya, D., Fisher, P. A., Gruenbaum, Y., Wolfner, M. F.
(1998). Interactions among Drosophila Nuclear Envelope Proteins Lamin, Otefin, and YA. Mol. Cell. Biol.
18: 4315-4323
[Abstract]
[Full Text]
-
Furukawa, K., Fritze, C. E., Gerace, L.
(1998). The Major Nuclear Envelope Targeting Domain of LAP2 Coincides with Its Lamin Binding Region but Is Distinct from Its Chromatin Interaction Domain. J. Biol. Chem.
273: 4213-4219
[Abstract]
[Full Text]
-
Yang, L., Guan, T., Gerace, L.
(1997). Lamin-binding Fragment of LAP2 Inhibits Increase in Nuclear Volume during the Cell Cycle and Progression into S Phase. JCB
139: 1077-1087
[Abstract]
[Full Text]