High-resolution live-cell imaging reveals novel cyclin A2 degradation foci involving autophagy

Journal of Cell Science

Volumn 127, Issue 10, 2014, Pages 2145-2150

  Loukil, Abdelhalim ^a   Zonca, Manuela ^a   Rebouissou, Cosette ^a   Baldin, Véronique ^b   Coux, Olivier ^b   Biard Piechaczyk, Martine ^c   Blanchard, Jean Marie ^a   Peter, Marion ^a  

^a INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^b Centre National de la Recherche Scientifique   (France)

^c University of Montpellier I and II   (France)

Author keywords

Autophagy; Cyclin A2; FLIM; FRET; Mitosis; Ubiquitin proteasome system

Indexed keywords

CYCLIN A2; CCNA2 PROTEIN, HUMAN; PROTEASOME; UBIQUITIN;

ARTICLE; AUTOPHAGY; BLEACHING; CELL PROLIFERATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLUORESCENCE LIFETIME IMAGING MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; METAPHASE; MICROSCOPY; MITOSIS; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN DEGRADATION; PROTEIN STABILITY; STABLE TRANSFECTION; UBIQUITINATION; CELL COMMUNICATION; FLUORESCENCE MICROSCOPY; MCF 7 CELL LINE; METABOLISM; PHYSIOLOGY; PROCEDURES;

AUTOPHAGY; CELL COMMUNICATION; CYCLIN A2; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; MCF-7 CELLS; MICROSCOPY, FLUORESCENCE; PROTEASOME ENDOPEPTIDASE COMPLEX; UBIQUITIN;

EID: 84900805843     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.139188     Document Type: Article

References (34)

1. Arsic, N., Bendris, N., Peter, M., Begon-Pescia, C., Rebouissou, C., Gadéa, G., Bouquier, N., Bibeau, F., Lemmers, B. and Blanchard, J. M. (2012). A novel function for Cyclin A2: control of cell invasion via RhoA signaling. J. Cell Biol. 196, 147-162.
2. Bailly, E., Pines, J., Hunter, T. and Bornens, M. (1992). Cytoplasmic accumulation of cyclin B1 in human cells: association with a detergent- resistant compartment and with the centrosome. J. Cell Sci. 101, 529-545.
3. Baldin, V., Militello, M., Thomas, Y., Doucet, C., Fic, W., Boireau, S., Jariel-Encontre, I., Piechaczyk, M., Bertrand, E., Tazi, J. et al. (2008). A novel role for PA28gamma-proteasome in nuclear speckle organization and SR protein trafficking. Mol. Biol. Cell 19, 1706-1716.
4. Bjørkøy, G., Lamark, T., Brech, A., Outzen, H., Perander, M., Overvatn, A., Stenmark, H. and Johansen, T. (2005). p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin- induced cell death. J. Cell Biol. 171, 603-614.
5. Cardoso, M. C., Leonhardt, H. and Nadal-Ginard, B. (1993). Reversal of terminal differentiation and control of DNA replication: cyclin A and Cdk2 specifically localize at subnuclear sites of DNA replication. Cell 74, 979-992.
6. den Elzen, N. and Pines, J. (2001). Cyclin A is destroyed in prometaphase and can delay chromosome alignment and anaphase. J. Cell Biol. 153, 121-136.
7. Di Fiore, B. and Pines, J. (2010). How cyclin A destruction escapes the spindle assembly checkpoint. J. Cell Biol. 190, 501-509.
8. Dulić, V., Stein, G. H., Far, D. F. and Reed, S. I. (1998). Nuclear accumulation of p21Cip1 at the onset of mitosis: a role at the G2/M-phase transition. Mol. Cell. Biol. 18, 546-557.
9. Fung, T. K., Ma, H. T. and Poon, R. Y. (2007). Specialized roles of the two mitotic cyclins in somatic cells: cyclin A as an activator of M phase-promoting factor. Mol. Biol. Cell 18, 1861-1873.
10. Geley, S., Kramer, E., Gieffers, C., Gannon, J., Peters, J. M. and Hunt, T. (2001). Anaphase-promoting complex/cyclosome-dependent proteolysis of human cyclin A starts at the beginning of mitosis and is not subject to the spindle assembly checkpoint. J. Cell Biol. 153, 137-148.
11. Izawa, D. and Pines, J. (2011). How APC/C-Cdc20 changes its substrate specificity in mitosis. Nat. Cell Biol. 13, 223-233.
12. Jackman, M., Kubota, Y., den Elzen, N., Hagting, A. and Pines, J. (2002). Cyclin A- and cyclin E-Cdk complexes shuttle between the nucleus and the cytoplasm. Mol. Biol. Cell 13, 1030-1045.
13. Kallio, M., Weinstein, J., Daum, J. R., Burke, D. J. and Gorbsky, G. J. (1998). Mammalian p55CDC mediates association of the spindle checkpoint protein Mad2 with the cyclosome/anaphase-promoting complex, and is involved in regulating anaphase onset and late mitotic events. J. Cell Biol. 141, 1393-1406.
14. Mateo, F., Vidal-Laliena, M., Canela, N., Busino, L., Martinez-Balbas, M. A., Pagano, M., Agell, N. and Bachs, O. (2009). Degradation of cyclin A is regulated by acetylation. Oncogene 28, 2654-2666.
15. Morgan,D.O.(1997). Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu. Rev. Cell Dev. Biol. 13, 261-291.
16. Nishiyama, A., Tachibana, K., Igarashi, Y., Yasuda, H., Tanahashi, N., Tanaka, K., Ohsumi, K. and Kishimoto, T. (2000). A nonproteolytic function of the proteasome is required for the dissociation of Cdc2 and cyclin B at the end of M phase. Genes Dev. 14, 2344-2357.
17. Pagano, M., Pepperkok, R., Verde, F., Ansorge, W. and Draetta, G. (1992). Cyclin A is required at two points in the human cell cycle. EMBO J. 11, 961-971.
18. Pankiv, S., Clausen, T. H., Lamark, T., Brech, A., Bruun, J. A., Outzen, H., Øvervatn, A., Bjørkøy, G. and Johansen, T. (2007). p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282, 24131-24145.
19. Pascreau, G., Eckerdt, F., Churchill, M. E. and Maller, J. L. (2010). Discovery of a distinct domain in cyclin A sufficient for centrosomal localization independently of Cdk binding. Proc. Natl. Acad. Sci. USA 107, 2932-2937.
20. Peter, M. and Ameer-Beg, S. M. (2004). Imaging molecular interactions by multiphoton FLIM. Biol. Cell 96, 231-236.
21. Peter, M., Ameer-Beg, S. M., Hughes, M. K., Keppler, M. D., Prag, S., Marsh, M., Vojnovic, B. and Ng, T. (2005). Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions. Biophys. J. 88, 1224-1237.
22. Pines, J. and Hunter, T. (1991). Human cyclins A and B1 are differentially located in the cell and undergo cell cycle-dependent nuclear transport. J. Cell Biol. 115, 1-17.
23. Rockel, T. D., Stuhlmann, D. and von Mikecz, A. (2005). Proteasomes degrade proteins in focal subdomains of the human cell nucleus. J. Cell Sci. 118, 5231-5242.
24. Seeger, M., Hartmann-Petersen, R., Wilkinson, C. R., Wallace, M., Samejima, I., Taylor, M. S. and Gordon, C. (2003). Interaction of the anaphase-promoting complex/cyclosome and proteasome protein complexes with multiubiquitin chain-binding proteins. J. Biol. Chem. 278, 16791-16796.
25. Sobczak-Thepot, J., Harper, F., Florentin, Y., Zindy, F., Brechot, C. and Puvion, E. (1993). Localization of cyclin A at the sites of cellular DNA replication. Exp. Cell Res. 206, 43-48.
26. Sudakin, V., Ganoth, D., Dahan, A., Heller, H., Hershko, J., Luca, F. C., Ruderman, J. V. and Hershko, A. (1995). The cyclosome, a large complex containing cyclin-selective ubiquitin ligase activity, targets cyclins for destruction at the end of mitosis. Mol. Biol. Cell 6, 185-197.
27. Tanida, I., Tanida-Miyake, E., Ueno, T. and Kominami, E. (2001). The human homolog of Saccharomyces cerevisiae Apg7p is a Protein-activating enzyme for multiple substrates including human Apg12p, GATE-16, GABARAP, and MAP- LC3. J. Biol. Chem. 276, 1701-1706.
28. Theis-Febvre, N., Filhol, O., Froment, C., Cazales, M., Cochet, C., Monsarrat, B., Ducommun, B. and Baldin, V. (2003). Protein kinase CK2 regulates CDC25B phosphatase activity. Oncogene 22, 220-232.
29. Thomas, Y., Coux, O. and Baldin, V. (2010). bTrCP-dependent degradation of CDC25B phosphatase at the metaphase-anaphase transition is a pre-requisite for correct mitotic exit. Cell Cycle 9, 4338-4350.
30. Tramier, M., Zahid, M., Mevel, J. C., Masse, M. J. and Coppey-Moisan, M. (2006). Sensitivity of CFP/YFP and GFP/mCherry pairs to donor photobleaching on FRET determination by fluorescence lifetime imaging microscopy in living cells. Microsc. Res. Tech. 69, 933-939.
31. Walker, A., Acquaviva, C., Matsusaka, T., Koop, L. and Pines, J. (2008). UbcH10 has a rate-limiting role in G1 phase but might not act in the spindle checkpoint or as part of an autonomous oscillator. J. Cell Sci. 121, 2319-2326.
32. Wolthuis, R., Clay-Farrace, L., van Zon, W., Yekezare, M., Koop, L., Ogink, J., Medema, R. and Pines, J. (2008). Cdc20 and Cks direct the spindle checkpoint-independent destruction of cyclin A. Mol. Cell 30, 290-302.
33. Yamamoto, A., Tagawa, Y., Yoshimori, T., Moriyama, Y., Masaki, R. and Tashiro, Y. (1998). Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct. Funct. 23, 33-42.
34. Yoshimori, T., Yamamoto, A., Moriyama, Y., Futai, M. and Tashiro, Y. (1991). Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J. Biol. Chem. 266, 17707-17712.