An intron-retaining splice variant of human cyclin A2, expressed in adult differentiated tissues, induces a G1/S cell cycle arrest in vitro

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Honda, Arata ^a,b,c   Valogne, Yannick ^b,c,d   Bou Nader, Myriam ^b,c   Bréchot, Christian ^b,c   Faivre, Jamila ^b,c  

^a Department of Dentistry Oral surgery   (Japan)

^b INSERM   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d Ectycell Biotech   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A2; CYCLIN DEPENDENT KINASE 2; HISTONE H1;

ADULT; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL NUCLEUS; CELL PROLIFERATION; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; EXON; FETUS; FLOW CYTOMETRY; GENE EXPRESSION; HEART; HELA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IN VITRO STUDY; INTRON; POLYMERASE CHAIN REACTION; PROTEIN PHOSPHORYLATION; RNA SPLICING; TIME LAPSE IMAGING; TISSUE DISTRIBUTION;

CELL CYCLE; CELL DIFFERENTIATION; CYCLIN A2; FLOW CYTOMETRY; G1 PHASE; HELA CELLS; HUMANS; INTRONS; PROTEIN ISOFORMS; S PHASE;

EID: 84862702751     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039249     Document Type: Article

References (45)

1. Pines J, (1999) Four-dimensional control of the cell cycle Nat Cell Biol 1: E73-79.
2. Pagano M, Pepperkok R, Verde F, Ansorge W, Draetta G, (1992) Cyclin A is required at two points in the human cell cycle. EMBO J 11: 961-971.
3. Furuno N, den Elzen N, Pines J, (1999) Human cyclin A is required for mitosis until mid prophase. J Cell Biol 147: 295-306.
4. Jacobs HW, Keidel E, Lehner CF, (2001) A complex degradation signal in Cyclin A required for G1 arrest, and a C-terminal region for mitosis. EMBO J 20(10): 2376-2386.
5. Carbonaro-Hall D, Williams R, Wu L, Warburton D, Zeichner-David M, et al. (1993) G1 expression and multistage dynamics of cyclin A in human osteosarcoma cells. Oncogene 8: 1649-1659.
6. Girard F, Strausfeld U, Fernandez A, Lamb NJ, (1991) Cyclin A is required for the onset of DNA replication in mammalian fibroblasts. Cell 67: 1169-1179.
7. Bailly E, Pines J, Hunter T, 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.
8. Winston N, Bourgain-Guglielmetti F, Ciemerych MA, Kubiak JZ, Senamaud-Beaufort C, et al. (2000) Early development of mouse embryos null mutant for the cyclin A2 gene occurs in the absence of maternally derived cyclin A2 gene products. Dev Biol 223: 139-153.
9. Castro A, Jaumot M, Vergés M, Agell N, Bachs O, (1994) Microsomal localization of cyclin A and CDK2 in proliferating rat liver cells. Biochem Biophys Res Commun 201: 1072-1078.
10. Lu XP, Koch KS, Lew DJ, Dulic V, Pines J, et al. (1992) Induction of cyclin mRNA and cyclin-associated histone H1 kinase during liver regeneration. J Biol Chem 267: 2841-2844.
11. Vergès M, Castro A, Jaumot M, Bachs O, Enrich C, (1997) Cyclin A is present in the endocytic compartment of rat liver cells and increases during liver regeneration. Biochem Biophys Res Commun 230: 49-53.
12. Faivre J, Frank-Vaillant M, Poulhe R, Mouly H, Bréchot C, et al. (2001) Membrane-anchored cyclin A2 triggers Cdc2 activation in Xenopus oocyte. FEBS Lett 506: 243-248.
13. Faivre J, Frank-Vaillant M, Poulhe R, Mouly H, Jessus C, et al. (2002) Centrosome overduplication, increased ploidy and transformation in cells expressing endoplasmic reticulum-associated cyclin A2. Oncogene 21: 1493-1500.
14. Jackman M, Kubota Y, den Elzen N, Hagting A, Pines J, (2002) Cyclin A- and cyclin E-CDK complexes shuttle between the nucleus and the cytoplasm. Mol Biol Cell 13: 1030-1045.
15. Kaufmann H, Marone R, Olayioye MA, Bailey JE, Fussenegger M, (2001) Characterization of an N-terminally truncated cyclin A isoform in mammalian cells. J Biol Chem 276: 29987-29993.
16. Hui-Ching Wang L, Huang W, Lai MD, Su IJ, (2011) Aberrant Cyclin A Expression and Centrosome Overduplication Induced by Hepatitis B Virus Pre-S2 Mutants and Its Implication in Hepatocarcinogenesis. Carcinogenesis. 2011 Dec 9 [Epub ahead of print].
17. Graveley BR, (2001) Alternative splicing: increasing diversity in the proteomic world. Trends Genet 17: 100-107.
18. Mironov AA, Fickett JW, Gelfand MS, (1999) Frequent alternative splicing of human genes. Genome Res 9: 1288-1293.
19. Hanke J, Brett D, Zastrow I, Aydin A, Delbrück S, et al. (1999) Alternative splicing of human genes: more the rule than the exception? Trends Genet 15: 389-390.
20. Mumberg D, Wick M, Bürger C, Haas K, Funk M, et al. (1997) Cyclin ET, a new splice variant of human cyclin E with a unique expression pattern during cell cycle progression and differentiation. Nucleic Acids Res 25: 2098-2105.
21. Sewing A, Rönicke V, Bürger C, Funk M, Müller R, (1994) Alternative splicing of human cyclin E. J Cell Sci 107: 581-588.
22. Harwell RM, Porter DC, Danes C, Keyomarsi K, (2000) Processing of cyclin E differs between normal and tumor breast cells. Cancer Res 60: 481-489.
23. Keyomarsi K, Conte D Jr, Toyofuku W, Fox MP, (1995) Deregulation of cyclin E in breast cancer. Oncogene 11: 941-950.
24. Porter DC, Keyomarsi K, (2000) Novel splice variants of cyclin E with altered substrate specificity. Nucleic Acids Res 28(23): E101.
25. Solomon DA, Wang Y, Fox SR, Lambeck TC, Giesting S, Lan Z, et al. (2003) Cyclin D1 splice variants. Differential effects on localization, RB phosphorylation, and cellular transformation. J Biol Chem 278: 30339-30347.
26. Lozano JC, Schatt P, Marquès F, Peaucellier G, Fort P, et al. (1998) A presumptive developmental role for a sea urchin cyclin B splice variant. J Cell Biol 140: 283-293.
27. Lozano JC, Perret E, Schatt P, Arnould C, Peaucellier G, et al. (2002) Molecular cloning, gene localization, and structure of human cyclin B3. Biochem Biophys Res Commun 291: 406-413.
28. Resnitzky D, Hengst L, Reed SI, (1995) Cyclin A-associated kinase activity is rate limiting for entrance into S phase and is negatively regulated in G1 by p27Kip1. Mol Cell Biol 15: 4347-4352.
29. Rosenberg AR, Zindy F, Le Deist F, Mouly H, Metezeau P, et al. (1995) Overexpression of human cyclin A advances entry into S phase. Oncogene 10: 1501-1509.
30. Den Elzen N, Pines J, (2001) Cyclin A is destroyed in prometaphase and can delay chromosome alignment and anaphase. J Cell Biol 153(1): 121-136.
31. Mateo F, Vidal-Laliena1 M, Canela N, Busino L, Martinez-Balbas MA, et al (2009) Degradation of cyclin A is regulated by acetylation. Oncogene 28: 2654-2666.
32. Sherr CJ, Roberts JM, (1999) CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 13: 1501-1512.
33. Hengst L, Reed SI, (1998) Inhibitors of the Cip/Kip family. Curr Top Microbiol Immunol 227: 25-41.
34. Devoto SH, Mudryj M, Pines J, Hunter T, Nevins JR, (1992) A cyclin A-protein kinase complex possesses sequence-specific DNA binding activity: p33Cdk2 is a component of the E2F-cyclin A complex. Cell 68: 167-176.
35. Lees E, Faha B, Dulic V, Reed SI, Harlow E, (1992) Cyclin E/Cdk2 and cyclin A/CDK2 kinases associate with p107 and E2F in a temporally distinct manner. Genes Dev 6: 1874-1885.
36. Weinberg RA, (1995) The retinoblastoma protein and cell cycle control. Cell 81: 323-330.
37. Sun A, Bagella L, Tutton S, Romano G, Giordano A, (2007) From G0 to S phase: A view of the roles played by the retinoblastoma (Rb) family members in the Rb-E2F pathway. J Cell Biochem 102: 1400-1404.
38. Pagliuca FW, Collins MO, Lichawska A, Zegerman P, Choudhary JS, et al. (2011) Quantitative proteomics reveals the basis for the biochemical specificity of the cell-cycle machinery. Mol Cell 43(3): 406-17.
39. Musgrove EA, Caldon CE, Barraclough J, Stone A, Sutherland RL, (2011) Cyclin D as a therapeutic target in cancer. Nat Rev Cancer 11(8): 558-72.
40. Keyomarsi K, Tucker SL, Buchholz TA, Callister M, Ding Y, et al. (2002) Cyclin E and survival in patients with breast cancer. N Engl J Med 347(20): 1566-1575.
41. Berasain C, Patil D, Perara E, Huang SM, Mouly H, et al. (1998) Oncogenic activation of a human cyclin A2 targeted to the endoplasmic reticulum upon hepatitis B virus genome insertion. Oncogene 16: 1277-1288.
42. Yoshizumi M, Lee WS, Hsieh CM, Tsai JC, Li J, et al. (1995) Disappearance of cyclin A correlates with permanent withdrawal of cardiomyocytes from the cell cycle in human and rat hearts. J Clin Invest 95: 2275-2280.
43. Chaudhry HW, Dashoush NH, Tang H, Zhang L, Wang X, et al. (2004) Cyclin A2 mediates cardiomyocyte mitosis in the postmitotic myocardium. J Biol Chem 279: 35858-35866.
44. Kaufmann H, Marone R, Olayioye MA, Bailey JE, Fussenegger M, (2001) Characterization of an N-terminally truncated cyclin A isoform in mammalian cells. J Biol Chem 276(32): 29987-29993.
45. Bendris N, Lemmers B, Blanchard JM, Arsic N, (2011) Cyclin A2 mutagenesis analysis: a new insight into CDK activation and cellular localization requirements. PLoS One 6(7): e22879.