Intermediate progenitors are increased by lengthening of the cell cycle through calcium signaling and p53 expression in human neural progenitors

Molecular Biology of the Cell

Volumn 23, Issue 7, 2012, Pages 1167-1180

  García García, Elisa ^a   Pino Barrio, Maria José ^a   Loṕez Medina, Laura ^a   Martińez Serrano, Alberto ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; NEUROGENIN 2; PROTEIN INSULINOMA ASSOCIATED 1; PROTEIN P21; PROTEIN P53; UNCLASSIFIED DRUG;

ARTICLE; B CELL LYMPHOMA; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL CYCLE; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADENOSINE TRIPHOSPHATE; BASE SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BCL-X PROTEIN; CALCIUM SIGNALING; CELL CYCLE; CELL LINE; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYTOSOL; HUMANS; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NEUROGENESIS; RNA, SMALL INTERFERING; TUMOR SUPPRESSOR PROTEIN P53;

IPS;

EID: 84859415107     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-06-0524     Document Type: Article

References (70)

1. Alavian KN et al. (2011). Bcl-xL regulates metabolic efficiency of neurons through interaction with the mitochondrial F1FO ATP synthase. Nat Cell Biol 13, 1224-1233.
2. Ali F, Hindley C, McDowell G, Deibler R, Jones A, Kirschner M, Guillemot F, Philpott A (2011). Cell cycle-regulated multi-site phosphorylation of Neurogenin 2 coordinates cell cycling with differentiation during neurogenesis. Development 138, 4267-4277.
3. Arai Y, Pulvers JN, Haffner C, Schilling B, Nusslein I, Calegari F, Huttner WB (2011). Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat Commun 2, 154.
4. Aranha MM, Sola S, Low WC, Steer CJ, Rodrigues CM (2009). Caspases and p53 modulate FOXO3A/Id1 signaling during mouse neural stem cell differentiation. J Cell Biochem 107, 748-758.
5. Arias J, Alberts AS, Brindle P, Claret FX, Smeal T, Karin M, Feramisco J, Montminy M (1994). Activation of cAMP and mitogen responsive genes relies on a common nuclear factor. Nature 370, 226-229. (Pubitemid 24236780)
6. Arnould T, Vankoningsloo S, Renard P, Houbion A, Ninane N, Demazy C, Remacle J, Raes M (2002). CREB activation induced by mitochondrial dysfunction is a new signaling pathway that impairs cell proliferation. EMBO J 21, 53-63. (Pubitemid 34087074)
7. Besson A, Dowdy SF, Roberts JM (2008). CDK inhibitors: cell cycle regulators and beyond. Dev Cell 14, 159-169. (Pubitemid 351189186)
8. Bond J, Woods CG (2006). Cytoskeletal genes regulating brain size. Curr Opin Cell Biol 18, 95-101. (Pubitemid 43107614)
9. Boulaire J, Fotedar A, Fotedar R (2000). The functions of the cdk-cyclin kinase inhibitor p21WAF1. Pathol Biol (Paris) 48, 190-202. (Pubitemid 30318121)
10. Calegari F, Huttner WB (2003). An inhibition of cyclin-dependent kinases that lengthens, but does not arrest, neuroepithelial cell cycle induces premature neurogenesis. J Cell Sci 116, 4947-4955. (Pubitemid 38016701)
11. Chang MY et al. (2007). Bcl-XL/Bax proteins direct the fate of embryonic cortical precursor cells. Mol Cell Biol 27, 4293-4305.
12. Chrivia JC, Kwok RP, Lamb N, Hagiwara M, Montminy MR, Goodman RH (1993). Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365, 855-859. (Pubitemid 23341031)
13. Courtois ET, Castillo CG, Seiz EG, Ramos M, Bueno C, Liste I, Martinez-Serrano A (2010). In vitro and in vivo enhanced generation of human A9 dopamine neurons from neural stem cells by Bcl-XL. J Biol Chem 285, 9881-9897.
14. Dehay C, Kennedy H (2007). Cell-cycle control and cortical development. Nat Rev Neurosci 8, 438-450. (Pubitemid 46789227)
15. Doe CQ (2008). Neural stem cells: balancing self-renewal with differentiation. Development 135, 1575-1587.
16. Doetsch F, Verdugo JM, Caille I, Alvarez-Buylla A, Chao MV, Casaccia-Bonnefil P (2002). Lack of the cell-cycle inhibitor p27Kip1 results in selective increase of transit-amplifying cells for adult neurogenesis. J Neurosci 22, 2255-2264. (Pubitemid 35386525)
17. Englund C, Fink A, Lau C, Pham D, Daza RA, Bulfone A, Kowalczyk T, Hevner RF (2005). Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci 25, 247-251. (Pubitemid 40110787)
18. Farkas LM, Haffner C, Giger T, Khaitovich P, Nowick K, Birchmeier C, Paabo S, Huttner WB (2008). Insulinoma-associated 1 has a panneurogenic role and promotes the generation and expansion of basal progenitors in the developing mouse neocortex. Neuron 60, 40-55.
19. Farkas LM, Huttner WB (2008). The cell biology of neural stem and progenitor cells and its significance for their proliferation versus differentiation during mammalian brain development. Curr Opin Cell Biol 20, 707-715.
20. Fish JL, Dehay C, Kennedy H, Huttner WB (2008). Making bigger brains-the evolution of neural-progenitor-cell division. J Cell Sci 121, 2783-2793.
21. Garrido C, Kroemer G (2004). Life's smile, death's grin: vital functions of apoptosis-executing proteins. Curr Opin Cell Biol 16, 639-646. (Pubitemid 39463114)
22. Giorgi C et al. (2010). PML regulates apoptosis at endoplasmic reticulum by modulating calcium release. Science 330, 1247-1251.
23. Gotz M, Huttner WB (2005). The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6, 777-788. (Pubitemid 41726116)
24. Graham V, Khudyakov J, Ellis P, Pevny L (2003). SOX2 functions to maintain neural progenitor identity. Neuron 39, 749-765. (Pubitemid 37088088)
25. Guillemot F (2007). Cell fate specification in the mammalian telencephalon. Prog Neurobiol 83, 37-52.
26. Hagn F, Klein C, Demmer O, Marchenko N, Vaseva A, Moll UM, Kessler H (2010). BclxL changes conformation upon binding to wild-type but not mutant p53 DNA binding domain. J Biol Chem 285, 3439-3450.
27. Haydar TF, Wang F, Schwartz ML, Rakic P (2000). Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J Neurosci 20, 5764-5774. (Pubitemid 30636905)
28. Huttner WB, Kosodo Y (2005). Symmetric versus asymmetric cell division during neurogenesis in the developing vertebrate central nervous system. Curr Opin Cell Biol 17, 648-657. (Pubitemid 41540416)
29. Iacopetti P, Michelini M, Stuckmann I, Oback B, Aaku-Saraste E, Huttner WB (1999). Expression of the antiproliferative gene TIS21 at the onset of neurogenesis identifies single neuroepithelial cells that switch from proliferative to neuron-generating division. Proc Natl Acad Sci USA 96, 4639-4644. (Pubitemid 29190389)
30. Janumyan Y, Cui Q, Yan L, Sansam CG, Valentin M, Yang E (2008). G0 function of BCL2 and BCL-xL requires BAX, BAK, and p27 phosphorylation by Mirk, revealing a novel role of BAX and BAK in quiescence regulation. J Biol Chem 283, 34108-34120.
31. Jones RG et al. (2007). The proapoptotic factors Bax and Bak regulate T Cell proliferation through control of endoplasmic reticulum Ca(2+) homeostasis. Immunity 27, 268-280. (Pubitemid 47284916)
32. Joseph B, Hermanson O (2010). Molecular control of brain size: regulators of neural stem cell life, death and beyond. Exp Cell Res 316, 1415-1421.
33. Kriegstein A, Noctor S, Martinez-Cerdeno V (2006). Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 7, 883-890.
34. Kuranaga E (2011). Caspase signaling in animal development. Dev Growth Differ 53, 137-148.
35. Kuranaga E, Miura M (2007). Nonapoptotic functions of caspases: caspases as regulatory molecules for immunity and cell-fate determination. Trends Cell Biol 17, 135-144. (Pubitemid 46341825)
36. Lamb HM, Hardwick M (2010). Noncanonical functions of BCL-2 proteins in the nervous system. Adv Exp Med Biol 687, 115-129.
37. Lenos MG, Tsaniklidou SM (2010). Calcium oscillations, G1 phase duration and neurogenesis timing. Trends Cell Biol 20, 577; author reply 578.
38. Li C, Wang X, Vais H, Thompson CB, Foskett JK, White C (2007). Apoptosis regulation by Bcl-x(L) modulation of mammalian inositol 1,4,5-trisphosphate receptor channel isoform gating. Proc Natl Acad Sci USA 104, 12565-12570. (Pubitemid 47206178)
39. Lindsten T, Golden JA, Zong WX, Minarcik J, Harris MH, Thompson CB (2003). The proapoptotic activities of Bax and Bak limit the size of the neural stem cell pool. J Neurosci 23, 11112-11119. (Pubitemid 37548946)
40. Lipskaia L, Hulot JS, Lompre AM (2009). Role of sarco/endoplasmic reticulum calcium content and calcium ATPase activity in the control of cell growth and proliferation. Pflugers Arch 457, 673-685.
41. Liste I, Garcia-Garcia E, Bueno C, Martinez-Serrano A (2007). Bcl-XL modulates the differentiation of immortalized human neural stem cells. Cell Death Differ 14, 1880-1892. (Pubitemid 350011664)
42. Liste I, Garcia-Garcia E, Martinez-Serrano A (2004). The generation of dopaminergic neurons by human neural stem cells is enhanced by Bcl-XL, both in vitro and in vivo. J Neurosci 24, 10786-10795. (Pubitemid 39602390)
43. Mandal S, Guptan P, Owusu-Ansah E, Banerjee U (2005). Mitochondrial regulation of cell cycle progression during development as revealed by the tenured mutation in Drosophila. Dev Cell 9, 843-854. (Pubitemid 41724111)
44. Martins RA, Pearson RA (2008). Control of cell proliferation by neurotransmitters in the developing vertebrate retina. Brain Res 4, 119237-60.
45. Martinez-Serrano A, Borner C, Pereira R, Villalba M, Satrustegui J (1996). Modulation of presynaptic calcium homeostasis by nitric oxide. Cell Calcium 20, 293-302. (Pubitemid 26341085)
46. Miyata T, Kawaguchi A, Saito K, Kawano M, Muto T, Ogawa M (2004). Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131, 3133-3145. (Pubitemid 39077437)
47. Nguyen L, Besson A, Roberts JM, Guillemot F (2006). Coupling cell cycle exit, neuronal differentiation and migration in cortical neurogenesis. Cell Cycle 5, 2314-2318. (Pubitemid 44785839)
48. Noctor SC, Martinez-Cerdeno V, Kriegstein AR (2008). Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. J Comp Neurol 508, 28-44. (Pubitemid 351532566)
49. Nowakowski RS, Lewin SB, Miller MW (1989). Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocytol 18, 311-318. (Pubitemid 19147398)
50. Ohnuma S, Philpott A, Harris WA (2001). Cell cycle and cell fate in the nervous system. Curr Opin Neurobiol 11, 66-73. (Pubitemid 32155951)
51. Owusu-Ansah E, Yavari A, Mandal S, Banerjee U (2008). Distinct mitochondrial retrograde signals control the G1-S cell cycle checkpoint. Nat Genet 40, 356-361. (Pubitemid 351311760)
52. Qian X, Shen Q, Goderie SK, He W, Capela A, Davis AA, Temple S (2000). Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron 28, 69-80.
53. Regad T, Bellodi C, Nicotera P, Salomoni P (2009). The tumor suppressor Pml regulates cell fate in the developing neocortex. Nat Neurosci 12, 132-140.
54. Resende RR, Adhikari A, da Costa JL, Lorencon E, Ladeira MS, Guatimosim S, Kihara AH, Ladeira LO (2010). Influence of spontaneous calcium events on cell-cycle progression in embryonal carcinoma and adult stem cells. Biochim Biophys Acta 1803, 246-260.
55. Resende RR, Britto LR, Ulrich H (2008a). Pharmacological properties of purinergic receptors and their effects on proliferation and induction of neuronal differentiation of P19 embryonal carcinoma cells. Int J Dev Neurosci 26, 763-777.
56. Resende RR, Gomes KN, Adhikari A, Britto LR, Ulrich H (2008b). Mechanism of acetylcholine-induced calcium signaling during neuronal differentiation of P19 embryonal carcinoma cells in vitro. Cell Calcium 43, 107-121.
57. Ryu JK, Choi HB, Hatori K, Heisel RL, Pelech SL, McLarnon JG, Kim SU (2003). Adenosine triphosphate induces proliferation of human neural stem cells: Role of calcium and p70 ribosomal protein S6 kinase. J Neurosci Res 72, 352-362. (Pubitemid 36504704)
58. Salomoni P, Calegari F (2010). Cell cycle control of mammalian neural stem cells: putting a speed limit on G1. Trends Cell Biol 20, 233-243.
59. Scemes E, Duval N, Meda P (2003). Reduced expression of P2Y1 receptors in connexin43-null mice alters calcium signaling and migration of neural progenitor cells. J Neurosci 23, 11444-11452. (Pubitemid 37549701)
60. Schuurmans C et al. (2004). Sequential phases of cortical specification involve Neurogenin-dependent and -independent pathways. EMBO J 23, 2892-2902. (Pubitemid 39013561)
61. Shen Q, Wang Y, Dimos JT, Fasano CA, Phoenix TN, Lemischka IR, Ivanova NB, Stifani S, Morrisey EE, Temple S (2006). The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat Neurosci 9, 743-751.
62. Shim JW, Koh HC, Chang MY, Roh E, Choi CY, Oh YJ, Son H, Lee YS, Studer L, Lee SH (2004). Enhanced in vitro midbrain dopamine neuron differentiation, dopaminergic function, neurite outgrowth, and 1-methyl-4-phenylpyridium resistance in mouse embryonic stem cells overexpressing Bcl-XL. J Neurosci 24, 843-852. (Pubitemid 38146595)
63. Swanson CA, Arkin AP, Ross J (1997). An endogenous calcium oscillator may control early embryonic division. Proc Natl Acad Sci USA 94, 1194-1199.
64. Tedeschi A, Di Giovanni S (2009). The non-apoptotic role of p53 in neuronal biology: enlightening the dark side of the moon. EMBO Rep 10, 576-583.
65. Villa A, Snyder EY, Vescovi A, Martinez-Serrano A (2000). Establishment and properties of a growth factor-dependent, perpetual neural stem cell line from the human CNS. Exp Neurol 161, 67-84. (Pubitemid 30136530)
66. Weissman TA, Riquelme PA, Ivic L, Flint AC, Kriegstein AR (2004). Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 43, 647-661. (Pubitemid 39179725)
67. White C, Li C, Yang J, Petrenko NB, Madesh M, Thompson CB, Foskett JK (2005). The endoplasmic reticulum gateway to apoptosis by Bcl-X(L) modulation of the InsP3R. Nat Cell Biol 7, 1021-1028. (Pubitemid 41486277)
68. Youle RJ, Strasser A (2008). The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9, 47-59.
69. Zhong W, Chia W (2008). Neurogenesis and asymmetric cell division. Curr Opin Neurobiol 18, 4-11.
70. Zinkel S, Gross A, Yang E (2006). BCL2 family in DNA damage and cell cycle control. Cell Death Differ 13, 1351-1359. (Pubitemid 44057470)