Cell Stress and Chaperones

, Volume 22, Issue 4, pp 553–567 | Cite as

Fine-tuning of actin dynamics by the HSPB8-BAG3 chaperone complex facilitates cytokinesis and contributes to its impact on cell division

  • Alice Anaïs Varlet
  • Margit Fuchs
  • Carole Luthold
  • Herman Lambert
  • Jacques Landry
  • Josée N. Lavoie
SMALL HEAT SHOCK PROTEINS

Abstract

The small heat shock protein HSPB8 and its co-chaperone BAG3 are proposed to regulate cytoskeletal proteostasis in response to mechanical signaling in muscle cells. Here, we show that in dividing cells, the HSPB8-BAG3 complex is instrumental to the accurate disassembly of the actin-based contractile ring during cytokinesis, a process required to allow abscission of daughter cells. Silencing of HSPB8 markedly decreased the mitotic levels of BAG3 in HeLa cells, supporting its crucial role in BAG3 mitotic functions. Cells depleted of HSPB8 were delayed in cytokinesis, remained connected via a disorganized intercellular bridge, and exhibited increased incidence of nuclear abnormalities that result from failed cytokinesis (i.e., bi- and multi-nucleation). Such phenotypes were associated with abnormal accumulation of F-actin at the intercellular bridge of daughter cells at telophase. Remarkably, the actin sequestering drug latrunculin A, like the inhibitor of branched actin polymerization CK666, normalized F-actin during cytokinesis and restored proper cell division in HSPB8-depleted cells, implicating deregulated actin dynamics as a cause of abscission failure. Moreover, this HSPB8-dependent phenotype could be corrected by rapamycin, an autophagy-promoting drug, whereas it was mimicked by drugs impairing lysosomal function. Together, the results further support a role for the HSPB8-BAG3 chaperone complex in quality control of actin-based structure dynamics that are put under high tension, notably during cell cytokinesis. They expand a so-far under-appreciated connection between selective autophagy and cellular morphodynamics that guide cell division.

Keywords

Cytokinesis BAG3 HSPB8 Actin Autophagy 

Notes

Acknowledgements

We are grateful to Sabine Elowe (Centre Hospitalier de l’Université Laval, Quebec, Canada), John A. Cooper (Dept of Biochemistry and Molecular Biophysics Washington University, St Louis, USA), and Laurence Pelletier (the Lunenfeld-Tanenbaum Research Institute, Toronto, Canada) for providing critical reagents. We thank Carl St-Pierre and Anne Loranger (Centre de recherche sur le cancer de lUniversité Laval, HDQ) for their assistance in microscopic analyses. This work was supported by the Canadian Institutes of Health Research Grant No 7088.

Supplementary material

12192_2017_780_MOESM1_ESM.avi (84 kb)
Movie S1 Related to Fig. 1BSpreading in control HeLa-GFP-H2B cells. Video microscopy of a representative HeLa-GFP-H2B cell transfected with control siRNA (siCtl) undergoing cytokinesis. Cells were imaged for 72 h at 10 min intervals using a Nikon TE-2000 inverted microscope equipped with CO2/thermo-regulated chamber and a X40 0.6 NA objective; single plane images are displayed at 2 frames/s. (AVI 84 kb)
12192_2017_780_MOESM2_ESM.avi (1.5 mb)
Movie S2 Related to Fig. 1BBAG3 depletion impairs daughter cells spreading and is associated with prolonged blebbing. Hela-GFP-H2B cells that have been transfected with BAG3-specific siRNAs were imaged for 72 h at 10 min intervals using a Nikon TE-2000 inverted microscope equipped with CO2/thermo-regulated chamber and a X40 0.6 NA objective; single plane images are displayed at 2 frames/s. (AVI 1565 kb)
12192_2017_780_MOESM3_ESM.avi (500 kb)
Movie S3 Related to Fig. 1BHSPB8 depletion impairs daughter cells spreading and is associated with prolonged blebbing. Hela-GFP-H2B cells that have been transfected with HSPB8-specific siRNAs were imaged for 72 h at 10 min intervals using a Nikon TE-2000 inverted microscope equipped with CO2/thermo-regulated chamber and a X40 0.6 NA objective; single plane images are displayed at 2 frames/s. (AVI 500 kb)
12192_2017_780_MOESM4_ESM.avi (343 kb)
Movie S4 Related to Fig. 1DDynamics of ICB disappearance in HeLa-GFP-H2B cells transfected with control siRNA. The ICB of representative daughter cells is pointed by an arrowhead. Cell imaging was performed for 72 h at 10 min intervals using a Nikon TE-2000 inverted microscope equipped with CO2/thermo-regulated chamber and a X40 0.6 NA objective; single plane images are displayed at 2 frames/s. (AVI 342 kb)
12192_2017_780_MOESM5_ESM.avi (679 kb)
Movie S5 Related to Fig. 1DBAG3 depletion is associated with abnormal and persistent ICB. The ICB of representative daughter cells is pointed by an arrowhead. Cell imaging was performed for 72 h at 10 min intervals using a Nikon TE-2000 inverted microscope equipped with CO2/thermo-regulated chamber and a X40 0.6 NA objective; single plane images are displayed at 2 frames/s. (AVI 679 kb)
12192_2017_780_MOESM6_ESM.avi (316 kb)
Movie S6 Related to Fig. 1DHSPB8 depletion is associated with abnormal and persistent ICB. The ICB of representative daughter cells is pointed by an arrowhead. Cell imaging was performed for 72 h at 10 min intervals using a Nikon TE-2000 inverted microscope equipped with CO2/thermo-regulated chamber and a X40 0.6 NA objective; single plane images are displayed at 2 frames/s. (AVI 316 kb)
12192_2017_780_MOESM7_ESM.avi (475 kb)
Movie S7 Related to Fig. 3CActin ring dynamics in HeLa-RFP-H2B cells adenofected with Ad-LifeAct-GFP and control siRNA. Mitotic cells expressing Lifeact-GFP (green) and RFP-H2B (red) were imaged for 2 h at 5 min intervals using a Perkin Elmer UltraVIEW Spinning Disk Confocal equipped with CO2/thermo-regulated chamber and 40 × 0.75NA objective; single plane images are displayed at 2 frames/s. (AVI 475 kb)
12192_2017_780_MOESM8_ESM.avi (473 kb)
Movie S8 Related to Fig. 3CActin ring dynamics in HeLa-RFP-H2B cells adenofected with Ad-LifeAct-GFP and HSPB8-specific siRNA. Mitotic cells expressing Lifeact-GFP (green) and RFP-H2B (red) were imaged for 2 h at 5 min intervals using a Perkin Elmer UltraVIEW Spinning Disk Confocal equipped with CO2/thermo-regulated chamber and 40 × 0.75NA objective; single plane images are displayed at 2 frames/s. (AVI 472 kb)

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Copyright information

© Cell Stress Society International 2017

Authors and Affiliations

  • Alice Anaïs Varlet
    • 1
    • 2
  • Margit Fuchs
    • 1
    • 2
  • Carole Luthold
    • 1
    • 2
  • Herman Lambert
    • 1
    • 2
  • Jacques Landry
    • 1
    • 2
    • 3
  • Josée N. Lavoie
    • 1
    • 2
    • 3
  1. 1.Centre de recherche sur le cancer de lʼUniversité LavalQuébecCanada
  2. 2.OncologyCentre de recherche du CHU de Québec-Université LavalQuébecCanada
  3. 3.Département de Biologie MoléculaireBiochimie Médicale et Pathologie Université LavalQuébecCanada

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