Localization, dynamics, and function of survivin revealed by expression of functional survivinDsRed fusion proteins in the living cell

Achim Temme, Michael Rieger, Friedemann Reber, Dirk Lindemann, Bernd Weigle, Petra Diestelkoetter-Bachert, Gerhard Ehninger, Masaaki Tatsuka, Yasuhiko Terada, Ernst Peter Rieber

Research output: Contribution to journalArticle

75 Citations (Scopus)

Abstract

Survivin, a member of the inhibitor of apoptosis protein family, has attracted growing attention due to its expression in various tumors and its potential application in tumor therapy. However, its subcellular localization and function have remained controversial: Recent studies revealed that survivin is localized at the mitotic spindle, binds caspases, and could thus protect cells from apoptosis. The cell cycle-dependent expression of survivin and its antiapoptotic function led to the hypothesis that survivin connects the cell cycle with apoptosis, thus providing a death switch for the termination of defective mitosis. In other studies, survivin was detected at kinetochores, cleavage furrow, and midbody, localizations being characteristic for chromosomal passenger proteins. These proteins are involved in cytokinesis as inferred from the observation that RNA interference and expression of mutant proteins led to cytokinesis defects without an increase in apoptosis. To remedy these discrepancies, we analyzed the localizations of a survivinDsRed fusion protein in HeLa cells by using confocal laser scanning microscopy and time-lapse video imaging. SurvivinDsRed was excluded from the interphase nucleus and was detected in centrosomes and at kinetochores. It dissociated from chromosomes at the anaphase/telophase transition and accumulated at the ends of polar microtubuli where it was immediately condensed to the midbody. Overexpression of both survivinDsRed and of a phosphorylation-defective mutant conferred resistance against apoptosis-inducing reagents, but only the overexpressed mutant protein caused an aberrant cytokinesis. These data characterize in detail the dynamics of survivin in vertebrate cells and confirm that survivin represents a chromosomal passenger protein.

Original languageEnglish
Pages (from-to)78-92
Number of pages15
JournalMolecular Biology of the Cell
Volume14
Issue number1
DOIs
Publication statusPublished - 2003 Jan 1
Externally publishedYes

Fingerprint

Cytokinesis
Apoptosis
Kinetochores
Mutant Proteins
Cell Cycle
Proteins
Time-Lapse Imaging
Inhibitor of Apoptosis Proteins
Telophase
Centrosome
Anaphase
Spindle Apparatus
Interphase
Caspases
RNA Interference
HeLa Cells
Mitosis
Confocal Microscopy
Vertebrates
Neoplasms

ASJC Scopus subject areas

  • Molecular Biology
  • Genetics
  • Cell Biology

Cite this

Temme, A., Rieger, M., Reber, F., Lindemann, D., Weigle, B., Diestelkoetter-Bachert, P., ... Peter Rieber, E. (2003). Localization, dynamics, and function of survivin revealed by expression of functional survivinDsRed fusion proteins in the living cell. Molecular Biology of the Cell, 14(1), 78-92. https://doi.org/10.1091/mbc.E02-04-0182

Localization, dynamics, and function of survivin revealed by expression of functional survivinDsRed fusion proteins in the living cell. / Temme, Achim; Rieger, Michael; Reber, Friedemann; Lindemann, Dirk; Weigle, Bernd; Diestelkoetter-Bachert, Petra; Ehninger, Gerhard; Tatsuka, Masaaki; Terada, Yasuhiko; Peter Rieber, Ernst.

In: Molecular Biology of the Cell, Vol. 14, No. 1, 01.01.2003, p. 78-92.

Research output: Contribution to journalArticle

Temme, A, Rieger, M, Reber, F, Lindemann, D, Weigle, B, Diestelkoetter-Bachert, P, Ehninger, G, Tatsuka, M, Terada, Y & Peter Rieber, E 2003, 'Localization, dynamics, and function of survivin revealed by expression of functional survivinDsRed fusion proteins in the living cell', Molecular Biology of the Cell, vol. 14, no. 1, pp. 78-92. https://doi.org/10.1091/mbc.E02-04-0182
Temme, Achim ; Rieger, Michael ; Reber, Friedemann ; Lindemann, Dirk ; Weigle, Bernd ; Diestelkoetter-Bachert, Petra ; Ehninger, Gerhard ; Tatsuka, Masaaki ; Terada, Yasuhiko ; Peter Rieber, Ernst. / Localization, dynamics, and function of survivin revealed by expression of functional survivinDsRed fusion proteins in the living cell. In: Molecular Biology of the Cell. 2003 ; Vol. 14, No. 1. pp. 78-92.
@article{f2c9a4a472e844c39c9227c1dd5059c8,
title = "Localization, dynamics, and function of survivin revealed by expression of functional survivinDsRed fusion proteins in the living cell",
abstract = "Survivin, a member of the inhibitor of apoptosis protein family, has attracted growing attention due to its expression in various tumors and its potential application in tumor therapy. However, its subcellular localization and function have remained controversial: Recent studies revealed that survivin is localized at the mitotic spindle, binds caspases, and could thus protect cells from apoptosis. The cell cycle-dependent expression of survivin and its antiapoptotic function led to the hypothesis that survivin connects the cell cycle with apoptosis, thus providing a death switch for the termination of defective mitosis. In other studies, survivin was detected at kinetochores, cleavage furrow, and midbody, localizations being characteristic for chromosomal passenger proteins. These proteins are involved in cytokinesis as inferred from the observation that RNA interference and expression of mutant proteins led to cytokinesis defects without an increase in apoptosis. To remedy these discrepancies, we analyzed the localizations of a survivinDsRed fusion protein in HeLa cells by using confocal laser scanning microscopy and time-lapse video imaging. SurvivinDsRed was excluded from the interphase nucleus and was detected in centrosomes and at kinetochores. It dissociated from chromosomes at the anaphase/telophase transition and accumulated at the ends of polar microtubuli where it was immediately condensed to the midbody. Overexpression of both survivinDsRed and of a phosphorylation-defective mutant conferred resistance against apoptosis-inducing reagents, but only the overexpressed mutant protein caused an aberrant cytokinesis. These data characterize in detail the dynamics of survivin in vertebrate cells and confirm that survivin represents a chromosomal passenger protein.",
author = "Achim Temme and Michael Rieger and Friedemann Reber and Dirk Lindemann and Bernd Weigle and Petra Diestelkoetter-Bachert and Gerhard Ehninger and Masaaki Tatsuka and Yasuhiko Terada and {Peter Rieber}, Ernst",
year = "2003",
month = "1",
day = "1",
doi = "10.1091/mbc.E02-04-0182",
language = "English",
volume = "14",
pages = "78--92",
journal = "Molecular Biology of the Cell",
issn = "1059-1524",
publisher = "American Society for Cell Biology",
number = "1",

}

TY - JOUR

T1 - Localization, dynamics, and function of survivin revealed by expression of functional survivinDsRed fusion proteins in the living cell

AU - Temme, Achim

AU - Rieger, Michael

AU - Reber, Friedemann

AU - Lindemann, Dirk

AU - Weigle, Bernd

AU - Diestelkoetter-Bachert, Petra

AU - Ehninger, Gerhard

AU - Tatsuka, Masaaki

AU - Terada, Yasuhiko

AU - Peter Rieber, Ernst

PY - 2003/1/1

Y1 - 2003/1/1

N2 - Survivin, a member of the inhibitor of apoptosis protein family, has attracted growing attention due to its expression in various tumors and its potential application in tumor therapy. However, its subcellular localization and function have remained controversial: Recent studies revealed that survivin is localized at the mitotic spindle, binds caspases, and could thus protect cells from apoptosis. The cell cycle-dependent expression of survivin and its antiapoptotic function led to the hypothesis that survivin connects the cell cycle with apoptosis, thus providing a death switch for the termination of defective mitosis. In other studies, survivin was detected at kinetochores, cleavage furrow, and midbody, localizations being characteristic for chromosomal passenger proteins. These proteins are involved in cytokinesis as inferred from the observation that RNA interference and expression of mutant proteins led to cytokinesis defects without an increase in apoptosis. To remedy these discrepancies, we analyzed the localizations of a survivinDsRed fusion protein in HeLa cells by using confocal laser scanning microscopy and time-lapse video imaging. SurvivinDsRed was excluded from the interphase nucleus and was detected in centrosomes and at kinetochores. It dissociated from chromosomes at the anaphase/telophase transition and accumulated at the ends of polar microtubuli where it was immediately condensed to the midbody. Overexpression of both survivinDsRed and of a phosphorylation-defective mutant conferred resistance against apoptosis-inducing reagents, but only the overexpressed mutant protein caused an aberrant cytokinesis. These data characterize in detail the dynamics of survivin in vertebrate cells and confirm that survivin represents a chromosomal passenger protein.

AB - Survivin, a member of the inhibitor of apoptosis protein family, has attracted growing attention due to its expression in various tumors and its potential application in tumor therapy. However, its subcellular localization and function have remained controversial: Recent studies revealed that survivin is localized at the mitotic spindle, binds caspases, and could thus protect cells from apoptosis. The cell cycle-dependent expression of survivin and its antiapoptotic function led to the hypothesis that survivin connects the cell cycle with apoptosis, thus providing a death switch for the termination of defective mitosis. In other studies, survivin was detected at kinetochores, cleavage furrow, and midbody, localizations being characteristic for chromosomal passenger proteins. These proteins are involved in cytokinesis as inferred from the observation that RNA interference and expression of mutant proteins led to cytokinesis defects without an increase in apoptosis. To remedy these discrepancies, we analyzed the localizations of a survivinDsRed fusion protein in HeLa cells by using confocal laser scanning microscopy and time-lapse video imaging. SurvivinDsRed was excluded from the interphase nucleus and was detected in centrosomes and at kinetochores. It dissociated from chromosomes at the anaphase/telophase transition and accumulated at the ends of polar microtubuli where it was immediately condensed to the midbody. Overexpression of both survivinDsRed and of a phosphorylation-defective mutant conferred resistance against apoptosis-inducing reagents, but only the overexpressed mutant protein caused an aberrant cytokinesis. These data characterize in detail the dynamics of survivin in vertebrate cells and confirm that survivin represents a chromosomal passenger protein.

UR - http://www.scopus.com/inward/record.url?scp=12244293398&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=12244293398&partnerID=8YFLogxK

U2 - 10.1091/mbc.E02-04-0182

DO - 10.1091/mbc.E02-04-0182

M3 - Article

VL - 14

SP - 78

EP - 92

JO - Molecular Biology of the Cell

JF - Molecular Biology of the Cell

SN - 1059-1524

IS - 1

ER -