The Terminal Basal Mitosis of Chicken Retinal Lim1 Horizontal Cells is Not Sensitive to Cisplatin-induced Cell Cycle Arrest

Overview

Journal Cell Cycle

Specialty Cell Biology

Date 2014 Dec 9

PMID 25483080

Citations 12

Authors

Shahrzad Shirazi Fard

Malin Thyselius

Charlotta All-Ericsson

Finn Hallbook

Affiliations

Soon will be listed here.

Abstract

For proper development, cells need to coordinate proliferation and cell cycle-exit. This is mediated by a cascade of proteins making sure that each phase of the cell cycle is controlled before the initiation of the next. Retinal progenitor cells divide during the process of interkinetic nuclear migration, where they undergo S-phase on the basal side, followed by mitoses on the apical side of the neuroepithelium. The final cell cycle of chicken retinal horizontal cells (HCs) is an exception to this general cell cycle behavior. Lim1 expressing (+) horizontal progenitor cells (HPCs) have a heterogenic final cell cycle, with some cells undergoing a terminal mitosis on the basal side of the retina. The results in this study show that this terminal basal mitosis of Lim1+ HPCs is not dependent on Chk1/2 for its regulation compared to retinal cells undergoing interkinetic nuclear migration. Neither activating nor blocking Chk1 had an effect on the basal mitosis of Lim1+ HPCs. Furthermore, the Lim1+ HPCs were not sensitive to cisplatin-induced DNA damage and were able to continue into mitosis in the presence of γ-H2AX without activation of caspase-3. However, Nutlin3a-induced expression of p21 did reduce the mitoses, suggesting the presence of a functional p53/p21 response in HPCs. In contrast, the apical mitoses were blocked upon activation of either Chk1/2 or p21, indicating the importance of these proteins during the process of interkinetic nuclear migration. Inhibiting Cdk1 blocked M-phase transition both for apical and basal mitoses. This confirmed that the cyclin B1-Cdk1 complex was active and functional during the basal mitosis of Lim1+ HPCs. The regulation of the final cell cycle of Lim1+ HPCs is of particular interest since it has been shown that the HCs are able to sustain persistent DNA damage, remain in the cell cycle for an extended period of time and, consequently, survive for months.

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References

Scoumanne A, Cho S, Zhang J, Chen X . The cyclin-dependent kinase inhibitor p21 is regulated by RNA-binding protein PCBP4 via mRNA stability. Nucleic Acids Res. 2010; 39(1):213-24. PMC: 3017617. DOI: 10.1093/nar/gkq778. View

Gotz M, Huttner W . The cell biology of neurogenesis. Nat Rev Mol Cell Biol. 2005; 6(10):777-88. DOI: 10.1038/nrm1739. View

Fragel-Madeira L, Meletti T, Mariante R, Monteiro R, Einicker-Lamas M, Bernardo R . Platelet activating factor blocks interkinetic nuclear migration in retinal progenitors through an arrest of the cell cycle at the S/G2 transition. PLoS One. 2011; 6(1):e16058. PMC: 3029264. DOI: 10.1371/journal.pone.0016058. View

Bohlig L, Rother K . One function--multiple mechanisms: the manifold activities of p53 as a transcriptional repressor. J Biomed Biotechnol. 2011; 2011:464916. PMC: 3062963. DOI: 10.1155/2011/464916. View

Vuong L, Conley S, Al-Ubaidi M . Expression and role of p53 in the retina. Invest Ophthalmol Vis Sci. 2012; 53(3):1362-71. DOI: 10.1167/iovs.11-8909. View

Chang L, Eastman A . Decreased translation of p21waf1 mRNA causes attenuated p53 signaling in some p53 wild-type tumors. Cell Cycle. 2012; 11(9):1818-26. PMC: 3372393. DOI: 10.4161/cc.20208. View

Donovan S, Corbo J . Retinal horizontal cells lacking Rb1 sustain persistent DNA damage and survive as polyploid giant cells. Mol Biol Cell. 2012; 23(22):4362-72. PMC: 3496610. DOI: 10.1091/mbc.E12-04-0293. View

Shirazi Fard S, Jarrin M, Boije H, Fillon V, All-Eriksson C, Hallbook F . Heterogenic final cell cycle by chicken retinal Lim1 horizontal progenitor cells leads to heteroploid cells with a remaining replicated genome. PLoS One. 2013; 8(3):e59133. PMC: 3602602. DOI: 10.1371/journal.pone.0059133. View

Hamburger V, HAMILTON H . A series of normal stages in the development of the chick embryo. J Morphol. 2014; 88(1):49-92. View

10.

Shirazi Fard S, All-Ericsson C, Hallbook F . The heterogenic final cell cycle of chicken retinal Lim1 horizontal cells is not regulated by the DNA damage response pathway. Cell Cycle. 2013; 13(3):408-17. PMC: 3956536. DOI: 10.4161/cc.27200. View

11.

Zdzalik M, Pustelny K, Kedracka-Krok S, Huben K, Pecak A, Wladyka B . Interaction of regulators Mdm2 and Mdmx with transcription factors p53, p63 and p73. Cell Cycle. 2010; 9(22):4584-91. DOI: 10.4161/cc.9.22.13871. View

12.

Sheikh M, Fornace Jr A . Role of p53 family members in apoptosis. J Cell Physiol. 2000; 182(2):171-81. DOI: 10.1002/(SICI)1097-4652(200002)182:2<171::AID-JCP5>3.0.CO;2-3. View

13.

Jackson J, Gilmartin A, Imburgia C, Winkler J, Marshall L, Roshak A . An indolocarbazole inhibitor of human checkpoint kinase (Chk1) abrogates cell cycle arrest caused by DNA damage. Cancer Res. 2000; 60(3):566-72. View

14.

Levrero M, De Laurenzi V, Costanzo A, Gong J, Wang J, Melino G . The p53/p63/p73 family of transcription factors: overlapping and distinct functions. J Cell Sci. 2000; 113 ( Pt 10):1661-70. DOI: 10.1242/jcs.113.10.1661. View

15.

Yang A, McKeon F . P63 and P73: P53 mimics, menaces and more. Nat Rev Mol Cell Biol. 2001; 1(3):199-207. DOI: 10.1038/35043127. View

16.

Taylor W, Stark G . Regulation of the G2/M transition by p53. Oncogene. 2001; 20(15):1803-15. DOI: 10.1038/sj.onc.1204252. View

17.

Damia G, Filiberti L, Vikhanskaya F, Carrassa L, Taya Y, DIncalci M . Cisplatinum and taxol induce different patterns of p53 phosphorylation. Neoplasia. 2001; 3(1):10-6. PMC: 1505020. DOI: 10.1038/sj.neo.7900122. View

18.

Dyer M, Cepko C . p27Kip1 and p57Kip2 regulate proliferation in distinct retinal progenitor cell populations. J Neurosci. 2001; 21(12):4259-71. PMC: 6762752. View

19.

Burma S, Chen B, Murphy M, Kurimasa A, Chen D . ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J Biol Chem. 2001; 276(45):42462-7. DOI: 10.1074/jbc.C100466200. View

20.

Bartek J, Lukas J . Mammalian G1- and S-phase checkpoints in response to DNA damage. Curr Opin Cell Biol. 2001; 13(6):738-47. DOI: 10.1016/s0955-0674(00)00280-5. View