Skip to main content
SpringerLink
Log in

Differential nuclear envelope assembly at the end of mitosis in suspension-cultured Apium graveolens cells

  • Research Article
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

NMCP1 is a plant protein that has a long coiled-coil domain within the molecule. Newly identified NMCP2 of Daucus carota and Apium graveolens showed similar peripheral localization in the interphase nucleus, and the sequence spanning the coiled-coil domain exhibited significant similarity with the corresponding region of NMCP1. To better understand disassembly and assembly of the nuclear envelope (NE) during mitosis, subcellular distribution of NMCP1 and NMCP2 was examined using A. graveolens cells. AgNMCP1 (NMCP1 in Apium) disassembled at prometaphase, dispersed mainly within the spindle, and accumulated on segregating chromosomes, while AgNMCP2 (NMCP2 in Apium), following disassembly at prometaphase with timing similar to that of AgNMCP1, dispersed throughout the mitotic cytoplasm at metaphase and anaphase. The protein accumulated at the periphery of reforming nuclei at telophase. A probe for the endomembrane indicated that the nuclear membrane (NM) disappears at prometaphase and begins to reappear at early telophase. Growth of the NM continued after mitosis was completed. NMCP2 in the mitotic cytoplasm localized in vesicular structures that could be distinguished from the bulk endomembrane system. These results suggest that NMCP1 and NMCP2 are recruited for NE assembly in different pathways in mitosis and that NMCP2 associates with NM-derived vesicles in the mitotic cytoplasm.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bollman KM, Aukerman MJ, Park MY, Hunte C, Berardini TZ, Poethig RS (2003) HASTY, the Arabidopsis ortholog of exportin 5/MSN5, regulates phase change and morphogenesis. Development 130:1493–1504

    Article  CAS  PubMed  Google Scholar 

  • Clarke PR, Zhang C (2008) Spatial and temporal coordination of mitosis by Ran GTPase. Nat Rev Mol Cell Biol 9:464–477

    Article  CAS  PubMed  Google Scholar 

  • Cohen M, Lee KK, Wilson KL, Gruenbaum Y (2001) Transcriptional repression, apoptosis, human disease and the functional evolution of the nuclear lamina. Trends Biochem Sci 26:41–47

    Article  CAS  PubMed  Google Scholar 

  • Demidov D, Van Damme D, Geelen D, Blattner FR, Houben A (2005) Identification and dynamics of two classes of aurora-like kinases in Arabidopsis and other plants. Plant Cell 17:836–848

    Article  CAS  PubMed  Google Scholar 

  • Dittmer TA, Stacey NJ, Sugimoto-Shirasu K, Richards EJ (2007) LITTLE NUCLEI genes affecting nuclear morphology in Arabidopsis thaliana. Plant Cell 19:2793–2803

    Article  CAS  PubMed  Google Scholar 

  • Dixit R, Cyr RJ (2002) Spatio-temporal relationship between nuclear-envelope breakdown and preprophase band disappearance in cultured tobacco cells. Protoplasma 219:116–121

    Article  CAS  PubMed  Google Scholar 

  • Drummond S, Ferrigno P, Lyon C, Murphy J, Goldberg M, Allen T, Smythe C, Hutchison CJ (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. J Cell Biol 144:225–240

    Article  CAS  PubMed  Google Scholar 

  • Ellenberg J, Siggia ED, Moreira JE, Smith CL, Presley JF, Worman H, Lippincott-Schwartz J (1997) Nuclear membrane dynamics and reassembly in living cells: targeting of an inner nuclear membrane protein in interphase and mitosis. J Cell Biol 138:1193–1206

    Article  CAS  PubMed  Google Scholar 

  • Evans DE, Irons SL, Graumann K, Runions J (2009) The plant nuclear envelope. In: Meier I (ed) Functional organization of the plant nucleus. Plant cell monographs 14. Springer, Berlin, pp 9–28

    Chapter  Google Scholar 

  • Fisher DZ, Chaudhary N, Blobel G (1986) cDNA sequencing of nuclear lamins A and C reveals primary and secondary structural homology to intermediate filament proteins. Proc Natl Acad Sci USA 83:6450–6454

    Article  CAS  PubMed  Google Scholar 

  • Frederick SE, Mangan ME, Carey JB, Gruber PJ (1992) Intermediate filament antigens of 60 and 65 kDa in the nuclear matrix of plants: their detection and localization. Exp Cell Res 1199:213–222

    Article  Google Scholar 

  • Fujimoto S, Matsunaga S, Yonemura M, Uchiyama S, Azuma T, Fukui K (2004) Identification of a novel plant MAR DNA binding protein localized on chromosomal surfaces. Plant Mol Biol 56:225–239

    Article  CAS  PubMed  Google Scholar 

  • Gerace L, Blobel G (1980) The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell 19:277–287

    Article  CAS  PubMed  Google Scholar 

  • Graumann K, Irons SL, Runions J, Evans DE (2007) Retention and mobility of the mammalian lamin B receptor in the plant nuclear envelope. Biol Cell 99:553–562

    Article  CAS  PubMed  Google Scholar 

  • Gruenbaum Y, Margalit A, Goldman RD, Shumaker DK, Wilson KL (2005) The nuclear lamina comes of age. Nat Rev Mol Cell Biol 6:21–31

    Article  CAS  PubMed  Google Scholar 

  • Güttinger S, Laurell E, Kutay U (2009) Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nat Rev Mol Cell Biol 10:178–191

    Article  PubMed  Google Scholar 

  • Haraguchi T, Koujin T, Hayakawa T, Kaneda T, Tsutsumi C, Imamoto N, Akazawa C, Sukegawa J, Yoneda Y, Hiraoka Y (2000) Live fluorescence imaging reveals early recruitment of emerin, LBR, RanBP2, and Nup153 to reforming functional nuclear envelopes. J Cell Sci 113:779–794

    CAS  PubMed  Google Scholar 

  • Harel A, Chan RC, Lachish-Zalait A, Zimmerman E, Elbaum M, Forbes DJ (2003) Importin beta negatively regulates nuclear membrane fusion and nuclear pore complex assembly. Mol Biol Cell 4:4387–4396

    Article  Google Scholar 

  • Heald R, McKeon F (1990) Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 61:579–589

    Article  CAS  PubMed  Google Scholar 

  • Heitlinger E, Peter M, Häner M, Lustig A, Aebi U, Nigg EA (1991) Expression of chicken lamin B2 in Escherichia coli: characterization of its structure, assembly, and molecular interactions. J Cell Biol 113:485–495

    Article  CAS  PubMed  Google Scholar 

  • Heitlinger E, Peter M, Lustig A, Villiger W, Nigg EA, Aebi U (1992) The role of the head and tail domain in lamin structure and assembly: analysis of bacterially expressed chicken lamin A and truncated B2 lamins. J Struct Biol 108:74–89

    Article  CAS  PubMed  Google Scholar 

  • Herman EM, Tague BW, Hoffman LM, Kjemtrup SE, Chrispeels MJ (1990) Retention of phytohemagglutinin with carboxyterminal tetrapeptide KDEL in the nuclear envelope and the endoplasmic reticulum. Planta 182:305–312

    Article  CAS  Google Scholar 

  • Hetzer MW, Walther TC, Mattaj IW (2005) Pushing the envelope: structure, function, and dynamics of the nuclear periphery. Annu Rev Cell Dev Biol 21:347–380

    Article  CAS  PubMed  Google Scholar 

  • Höger TH, Krohne G, Kleinschmidt JA (1991) Interaction of Xenopus lamins A and LII with chromatin in vitro mediated by a sequence element in the carboxyterminal domain. Exp Cell Res 197:280–289

    Article  PubMed  Google Scholar 

  • Holaska JM, Wilson KL, Mansharamani M (2002) The nuclear envelope, lamins and nuclear assembly. Curr Opin Cell Biol 14:357–364

    Article  CAS  PubMed  Google Scholar 

  • Holmer L, Worman HJ (2001) Inner nuclear membrane proteins: functions and targeting. Cell Mol Life Sci 58:1741–1747

    Article  CAS  PubMed  Google Scholar 

  • Isobe K, Gohara R, Ueda T, Takasaki Y, Ando S (2007) The last twenty residues in the head domain of mouse lamin A contain important structural elements for formation of head-to-tail polymers in vitro. Biosci Biotechnol Biochem 71:1252–1259

    Article  CAS  PubMed  Google Scholar 

  • Jiang CJ, Imamoto N, Matsuki R, Yoneda Y, Yamamoto N (1998) In vitro characterization of rice importin beta1: molecular interaction with nuclear transport factors and mediation of nuclear protein import. FEBS Lett 437:127–130

    Article  CAS  PubMed  Google Scholar 

  • Kawabe A, Matsunaga S, Nakagawa K, Kurihara D, Yoneda A, Hasezawa S, Uchiyama S, Fukui K (2005) Characterization of plant Aurora kinases during mitosis. Plant Mol Biol 58:1–13

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Cai S, Lv Q, Jiang Q, Zhang Q (2007) Lamin B receptor plays a role in stimulating nuclear envelope production and targeting membrane vesicles to chromatin during nuclear envelope assembly through direct interaction with importin beta. J Cell Sci 120:520–530

    Article  CAS  PubMed  Google Scholar 

  • Masuda K, Takahashi S, Nomura K, Arimoto M, Inoue M (1993) Residual structure and constituent proteins of the peripheral framework of the cell nucleus in somatic embryos from Daucus carota L. Planta 191:532–540

    Article  CAS  Google Scholar 

  • Masuda K, Xu ZJ, Takahashi S, Ito A, Ono M, Nomura K, Inoue M (1997) Peripheral framework of carrot cell nucleus contains a novel protein predicted to exhibit a long alpha-helical domain. Exp Cell Res 10:173–181

    Article  Google Scholar 

  • Masuda K, Haruyama S, Fujino K (1999) Assembly and disassembly of the peripheral architecture of the plant cell nucleus during mitosis. Planta 210:165–167

    Article  CAS  PubMed  Google Scholar 

  • Mattout A, Goldberg M, Tzur Y, Margalit A, Gruenbaum Y (2007) Specific and conserved sequences in D. melanogaster and C. elegans lamins and histone H2A mediate the attachment of lamins to chromosomes. J Cell Sci 120:77–85

    Article  CAS  PubMed  Google Scholar 

  • McKeon FD, Kirschner MW, Caput D (1986) Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins. Nature 319:463–468

    Article  CAS  PubMed  Google Scholar 

  • Meier I (2007) Composition of the plant nuclear envelope: theme and variations. J Exp Bot 58:27–34

    Article  CAS  PubMed  Google Scholar 

  • Moir RD, Yoon M, Khuon S, Goldman RD (2000) Nuclear lamins A and B1: different pathways of assembly during nuclear envelope formation in living cells. J Cell Biol 151:1155–1168

    Article  CAS  PubMed  Google Scholar 

  • Moreno Díaz de la Espina S, Barthellemy I, Cerezuela MA (1991) Isolation and ultrastructural characterization of the residual nuclear matrix in a plant cell system. Chromosoma 100:110–117

    Article  Google Scholar 

  • Moriguchi K, Suzuki T, Ito Y, Yamazaki Y, Niwa Y, Kurata N (2005) Functional isolation of novel nuclear proteins showing a variety of subnuclear localizations. Plant Cell 17:389–403

    Article  CAS  PubMed  Google Scholar 

  • Pay A, Resch K, Frohnmeyer H, Fejes E, Nagy F, Nick P (2002) Plant RanGAPs are localized at the nuclear envelope in interphase and associated with microtubules in mitotic cells. Plant J 30:699–709

    Article  CAS  PubMed  Google Scholar 

  • Peter M, Nakagawa J, Dorée M, Labbé JC, Nigg EA (1990) In vitro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 kinase. Cell 61:591–602

    Article  CAS  PubMed  Google Scholar 

  • Peter M, Heitlinger E, Häner M, Aebi U, Nigg EA (1991) Disassembly of in vitro formed lamin head-to-tail polymers by CDC2 kinase. EMBO J 10:1535–1544

    CAS  PubMed  Google Scholar 

  • Prunuske AJ, Ullman KS (2006) The nuclear envelope: form and reformation. Curr Opin Cell Biol 18:108–116

    Article  CAS  PubMed  Google Scholar 

  • Rose A, Meier I (2001) A domain unique to plant RanGAP is responsible for its targeting to the plant nuclear rim. Proc Natl Acad Sci USA 98:15377–15382

    Article  CAS  PubMed  Google Scholar 

  • Van Damme D, Bouget FY, Van Poucke K, Inzé D, Geelen D (2004) Molecular dissection of plant cytokinesis and phragmoplast structure: a survey of GFP-tagged proteins. Plant J 40:386–398

    Article  PubMed  Google Scholar 

  • Vigers GP, Lohka MJ (1991) A distinct vesicle population targets membranes and pore complexes to the nuclear envelope in Xenopus eggs. J Cell Biol 112:545–556

    Article  CAS  PubMed  Google Scholar 

  • Yamada T, Chimera K, van Doorn WG (2006) DNA degradation and nuclear degeneration during programmed cell death in petals of Antirrhinum, Argyranthemum, and Petunia. J Exp Bot 57:3543–3552

    Article  CAS  PubMed  Google Scholar 

  • Yang L, Guan T, Gerace L (1997) Integral membrane proteins of the nuclear envelope are dispersed throughout the endoplasmic reticulum during mitosis. J Cell Biol 137:1199–1210

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Hutchins JR, Mühlhäusser P, Kutay U, Clarke PR (2002) Role of importin-beta in the control of nuclear envelope assembly by Ran. Curr Biol 12:498–502

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Professor M. Inoue (Akita Prefectural University) for technical advice and helpful discussions, and Mr. T. Ito and Mr. M. Yasui (Hokkaido University) for excellent technical assistance in CLSM.

Author information

Authors and Affiliations

  1. Laboratory of Plant Functional Biology, Graduate School of Agriculture, Hokkaido University, Kita 9 Nishi 9, Sapporo, 060-8589, Hokkaido, Japan

    Yuta Kimura, Chie Kuroda & Kiyoshi Masuda

Authors
  1. Yuta Kimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chie Kuroda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kiyoshi Masuda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kiyoshi Masuda.

Additional information

Communicated by Y. Hiraoka.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

The combination of primers used for amplification of cDNAs for NMCP2, DcPDI1, AgNMCP1, and AgNMCP2 (DOC 32 kb)

Table S2

Sequences of primers (DOC 41 kb)

Fig. S1

(PDF 79.8 kb)

Fig. S2

(PDF 279 kb)

Fig. S3

(PDF 134 kb)

Fig. S4

(PDF 129 kb)

Fig. S5

(PDF 304 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kimura, Y., Kuroda, C. & Masuda, K. Differential nuclear envelope assembly at the end of mitosis in suspension-cultured Apium graveolens cells. Chromosoma 119, 195–204 (2010). https://doi.org/10.1007/s00412-009-0248-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-009-0248-y

Keywords

Search

Navigation