How to keep proliferative neural stem/progenitor cells: A critical role of asymmetric inheritance of cyclin D2

Cell Cycle

Volumn 11, Issue 19, 2012, Pages 3550-3554

  Tsunekawa, Yuji ^a   Osumi, Noriko ^b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Asymmetric cell division; Cyclin D2; mRNA localization; Post transcriptional regulation; Radial glia

Indexed keywords

CYCLIN D2; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE INHIBITOR; MESSENGER RNA;

ARTICLE; BRAIN DEVELOPMENT; CELL CYCLE REGULATION; CELL DIVISION; CELL FATE; CELL PROLIFERATION; CELLULAR DISTRIBUTION; DAUGHTER CELL; EVOLUTION; GLIA CELL; HUMAN; INHERITANCE; NEOCORTEX; NEURAL STEM CELL; NONHUMAN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TRANSCRIPTION REGULATION;

EID: 84867272850     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.21500     Document Type: Article

References (50)

1. Haubensak W, Attardo A, Denk W, Huttner WB. Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci USA 2004; 101:3196-201; PMID:14963232; http://dx.doi.org/10.1073/pnas.0308600100.
2. Kowalczyk T, Pontious A, Englund C, Daza RA, Bedogni F, Hodge R, et al. Intermediate neuronal progenitors (basal progenitors) produce pyramidalprojection neurons for all layers of cerebral cortex. Cereb Cortex 2009; 19:2439-50; PMID:19168665; http://dx.doi.org/10.1093/cercor/bhn260.
3. Götz M, Huttner WB. The cell biology of neurogenesis. Nat Rev Mol Cell Biol 2005; 6:777-88; PMID:16314867; http://dx.doi.org/10.1038/nrm1739.
4. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR. Neurons derived from radial glial cells establish radial units in neocortex. Nature 2001; 409:714-20; PMID:11217860; http://dx.doi.org/10.1038/35055553.
5. Huttner WB, Kosodo Y. Symmetric versus asymmetric cell division during neurogenesis in the developing vertebrate central nervous system. Curr Opin Cell Biol 2005; 17:648-57; PMID:16243506; http://dx.doi.org/10.1016/j.ceb.2005.10. 005.
6. Miyata T, Kawaguchi A, Saito K, Kawano M, Muto T, Ogawa M. Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 2004; 131:3133-45; PMID:15175243; http://dx.doi.org/10.1242/ dev.01173.
7. Noctor SC, Martínez-Cerdeño V, Ivic L, Kriegstein AR. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 2004; 7:136-44; PMID:14703572; http://dx.doi.org/10.1038/nn1172.
8. Fishell G, Kriegstein AR. Neurons from radial glia: the consequences of asymmetric inheritance. Curr Opin Neurobiol 2003; 13:34-41; PMID:12593980; http://dx.doi.org/10.1016/S0959-4388(03)00013-8.
9. Miyata T, Kawaguchi A, Okano H, Ogawa M. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 2001; 31:727-41; PMID:11567613; http://dx.doi.org/10.1016/S0896-6273(01)00420-2.
10. Kosodo Y, Röper K, Haubensak W, Marzesco AM, Corbeil D, Huttner WB. Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuroepithelial cells. EMBO J 2004; 23:2314-24; PMID:15141162; http://dx.doi.org/10.1038/sj.emboj.7600223.
11. Bultje RS, Castaneda-Castellanos DR, Jan LY, Jan YN, Kriegstein AR, Shi SH. Mammalian Par3 regulates progenitor cell asymmetric division via notch signaling in the developing neocortex. Neuron 2009; 63:189-202; PMID:19640478; http://dx.doi.org/10.1016/j.neuron.2009.07.004.
12. Costa MR, Wen G, Lepier A, Schroeder T, Götz M. Par-complex proteins promote proliferative progenitor divisions in the developing mouse cerebral cortex. Development 2008; 135:11-22; PMID:18032449; http://dx.doi.org/10.1242/ dev.009951.
13. Shen Q, Zhong W, Jan YN, Temple S. Asymmetric Numb distribution is critical for asymmetric cell division of mouse cerebral cortical stem cells and neuroblasts. Development 2002; 129:4843-53; PMID:12361975.
14. Matsushime H, Roussel MF, Ashmun RA, Sherr CJ. Colony-stimulating factor 1 regulates novel cyclins during the G1 phase of the cell cycle. Cell 1991; 65:701-13; PMID:1827757; http://dx.doi.org/10.1016/0092-8674(91)90101-4.
15. Johnson DG, Walker CL. Cyclins and cell cycle checkpoints. Annu Rev Pharmacol Toxicol 1999; 39:295-312; PMID:10331086; http://dx.doi.org/10.1146/ annurev.pharmtox.39.1.295.
16. Sherr CJ. G1 phase progression: cycling on cue. Cell 1994; 79:551-5; PMID:7954821; http://dx.doi.org/10.1016/0092-8674(94)90540-1.
17. Lange C, Huttner WB, Calegari F. Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 2009; 5:320-31; PMID:19733543; http://dx.doi.org/10.1016/j.stem.2009.05.026.
18. Pilaz LJ, Patti D, Marcy G, Ollier E, Pfister S, Douglas RJ, et al. Forced G1-phase reduction alters mode of division, neuron number, and laminar phenotype in the cerebral cortex. Proc Natl Acad Sci USA 2009; 106:21924-9; PMID:19959663; http://dx.doi.org/10.1073/pnas.0909894106.
19. Tsunekawa Y, Britto JM, Takahashi M, Polleux F, Tan SS, Osumi N. Cyclin D2 in the basal process of neural progenitors is linked to non-equivalent cell fates. EMBO J 2012; 31:1879-92; PMID:22395070; http://dx.doi.org/10.1038/emboj. 2012.43.
20. Ali F, Hindley C, McDowell G, Deibler R, Jones A, Kirschner M, et al. Cell cycle-regulated multi-site phosphorylation of Neurogenin 2 coordinates cell cycling with differentiation during neurogenesis. Development 2011; 138:4267-77; PMID:21852393; http://dx.doi.org/10.1242/dev.067900.
21. Nguyen L, Besson A, Heng JI, Schuurmans C, Teboul L, Parras C, et al. p27kip1 independently promotes neuronal differentiation and migration in the cerebral cortex. Genes Dev 2006; 20:1511-24; PMID:16705040; http://dx.doi.org/ 10.1101/gad.377106.
22. Nguyen L, Besson A, Roberts JM, Guillemot F. Coupling cell cycle exit, neuronal differentiation and migration in cortical neurogenesis. Cell Cycle 2006; 5:2314-8; PMID:17102618; http://dx.doi.org/10.4161/cc.5.20.3381.
23. Vernon AE, Movassagh M, Horan I, Wise H, Ohnuma S, Philpott A. Notch targets the Cdk inhibitor Xic1 to regulate differentiation but not the cell cycle in neurons. EMBO Rep 2006; 7:643-8; PMID:16648822.
24. Mairet-Coello G, Tury A, Van Buskirk E, Robinson K, Genestine M, DiCicco-Bloom E. p57(KIP2) regulates radial glia and intermediate precursor cell cycle dynamics and lower layer neurogenesis in developing cerebral cortex. Development 2012; 139:475-87; PMID:22223678; http://dx.doi.org/10.1242/dev. 067314.
25. Ross ME, Risken M. MN20, a D2 cyclin found in brain, is implicated in neural differentiation. J Neurosci 1994; 14:6384-91; PMID:7965043.
26. Ross ME, Carter ML, Lee JH. MN20, a D2 cyclin, is transiently expressed in selected neural populations during embryogenesis. J Neurosci 1996; 16:210-9; PMID:8613787.
27. Glickstein SB, Alexander S, Ross ME. Differences in cyclin D2 and D1 protein expression distinguish forebrain progenitor subsets. Cereb Cortex 2007; 17:632-42; PMID:16627858; http://dx.doi.org/10.1093/cercor/bhk008.
28. Kowalczyk A, Filipkowski RK, Rylski M, Wilczynski GM, Konopacki FA, Jaworski J, et al. The critical role of cyclin D2 in adult neurogenesis. J Cell Biol 2004; 167:209-13; PMID:15504908; http://dx.doi.org/10.1083/jcb.200404181.
29. Jedynak P, Jaholkowski P, Wozniak G, Sandi C, Kaczmarek L, Filipkowski RK. Lack of cyclin D2 impairing adult brain neurogenesis alters hippocampal-dependent behavioral tasks without reducing learning ability. Behav Brain Res 2012; 227:159-66; PMID:22101301; http://dx.doi.org/10.1016/j.bbr.2011. 11.007.
30. Matsumoto Y, Tsunekawa Y, Nomura T, Suto F, Matsumata M, Tsuchiya S, et al. Differential proliferation rhythm of neural progenitor and oligodendrocyte precursor cells in the young adult hippocampus. PLoS One 2011; 6:e27628; PMID:22110700; http://dx.doi.org/10.1371/journal.pone.0027628.
31. Glickstein SB, Monaghan JA, Koeller HB, Jones TK, Ross ME. Cyclin D2 is critical for intermediate progenitor cell proliferation in the embryonic cortex. J Neurosci 2009; 29:9614-24; PMID:19641124; http://dx.doi.org/10.1523/ JNEUROSCI.2284-09.2009.
32. Takahashi T, Nowakowski RS, Caviness VS Jr. Mode of cell proliferation in the developing mouse neocortex. Proc Natl Acad Sci USA 1994; 91:375-9; PMID:8278397; http://dx.doi.org/10.1073/pnas.91.1.375.
33. Takahashi T, Nowakowski RS, Caviness VS Jr. The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 1995; 15:6046-57; PMID:7666188.
34. Calegari F, Huttner WB. An inhibition of cyclin-dependent kinases that lengthens, but does not arrest, neuroepithelial cell cycle induces premature neurogenesis. J Cell Sci 2003; 116:4947-55; PMID:14625388; http://dx.doi.org/10. 1242/jcs.00825.
35. Dehay C, Kennedy H. Cell-cycle control and cortical development. Nat Rev Neurosci 2007; 8:438-50; PMID:17514197; http://dx.doi.org/10.1038/nrn2097.
36. Lange C, Calegari F. Cdks and cyclins link G1 length and differentiation of embryonic, neural and hematopoietic stem cells. Cell Cycle 2010; 9:1893-900; PMID:20436288; http://dx.doi.org/10.4161/cc.9.10.11598.
37. Salomoni P, Calegari F. Cell cycle control of mammalian neural stem cells: putting a speed limit on G1. Trends Cell Biol 2010; 20:233-43; PMID:20153966; http://dx.doi.org/10.1016/j.tcb.2010.01.006.
38. Arai Y, Pulvers JN, Haffner C, Schilling B, Nüsslein I, Calegari F, et al. Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat Commun 2011; 2:154; PMID:21224845; http://dx.doi.org/10.1038/ ncomms1155.
39. Shitamukai A, Konno D, Matsuzaki F. Oblique radial glial divisions in the developing mouse neocortex induce self-renewing progenitors outside the germinal zone that resemble primate outer subventricular zone progenitors. J Neurosci 2011; 31:3683-95; PMID:21389223; http://dx.doi.org/10.1523/JNEUROSCI. 4773-10.2011.
40. Wang X, Tsai JW, LaMonica B, Kriegstein AR. A new subtype of progenitor cell in the mouse embryonic neocortex. Nat Neurosci 2011; 14:555-61; PMID:21478886; http://dx.doi.org/10.1038/nn.2807.
41. Susaki E, Nakayama K, Nakayama KI. Cyclin D2 translocates p27 out of the nucleus and promotes its degradation at the G0-G1 transition. Mol Cell Biol 2007; 27:4626-40; PMID:17452458; http://dx.doi.org/10.1128/MCB.00862-06.
42. Susaki E, Nakayama KI. Multiple mechanisms for p27(Kip1) translocation and degradation. Cell Cycle 2007; 6:3015-20; PMID:18075313; http://dx.doi.org/ 10.4161/cc.6.24.5087.
43. Ratineau C, Petry MW, Mutoh H, Leiter AB. Cyclin D1 represses the basic helix-loop-helix transcription factor, BETA2/NeuroD. J Biol Chem 2002; 277:8847-53; PMID:11788592; http://dx.doi.org/10.1074/jbc.M110747200.
44. Bienvenu F, Jirawatnotai S, Elias JE, Meyer CA, Mizeracka K, Marson A, et al. Transcriptional role of cyclin D1 in development revealed by a genetic-proteomic screen. Nature 2010; 463:374-8; PMID:20090754; http://dx.doi.org/10.1038/nature08684.
45. Fietz SA, Kelava I, Vogt J, Wilsch-Bräuninger M, Stenzel D, Fish JL, et al. OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat Neurosci 2010; 13:690-9; PMID:20436478; http://dx.doi.org/10.1038/nn.2553.
46. Hansen DV, Lui JH, Parker PR, Kriegstein AR. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 2010; 464:554-61; PMID:20154730; http://dx.doi.org/10.1038/nature08845.
47. Lui JH, Hansen DV, Kriegstein AR. Development and evolution of the human neocortex. Cell 2011; 146:18-36; PMID:21729779; http://dx.doi.org/10.1016/j. cell.2011.06.030.
48. García-Moreno F, Vasistha NA, Trevia N, Bourne JA, Molnár Z. Compartmentalization of cerebral cortical germinal zones in a lissencephalic primate and gyrencephalic rodent. Cereb Cortex 2012; 22:482-92; PMID:22114081; http://dx.doi.org/10.1093/cercor/bhr312.
49. Siegenthaler JA, Ashique AM, Zarbalis K, Patterson KP, Hecht JH, Kane MA, et al. Retinoic acid from the meninges regulates cortical neuron generation. Cell 2009; 139:597-609; PMID:19879845; http://dx.doi.org/10.1016/j.cell.2009.10. 004.
50. Reillo I, de Juan Romero C, García-Cabezas MA, Borrell V. A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. Cereb Cortex 2011; 21:1674-94; PMID:21127018; http://dx.doi.org/10.1093/cercor/bhq238.