Mapping differentiation kinetics in the mouse retina reveals an extensive period of cell cycle protein expression in post-mitotic newborn neurons

Developmental Dynamics

Volumn 241, Issue 10, 2012, Pages 1525-1544

  Pacal, Marek ^a,b   Bremner, Rod ^a,b,c  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c MOUNT SINAI HOSPITAL   (Canada)

Author keywords

Cell cycle length; G2 M; Ki67; Neuronal birth; Neuronal marker induction; Retinal development

Indexed keywords

3BETA TUBULIN; BETA TUBULIN; BROXURIDINE; CALRETININ; CELL CYCLE PROTEIN; DOUBLECORTIN; HU ANTIGEN; HU ANTIGEN 2; HU ANTIGEN 3; HU ANTIGEN 4; KI 67 ANTIGEN; MICROTUBULE ASSOCIATED PROTEIN 5; RNA BINDING PROTEIN; RNA BINDING PROTEIN FOX 1 HOMOLOG; UBIQUITIN THIOLESTERASE; UBIQUITIN THIOLESTERASE L1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CYCLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL DIFFERENTIATION; EMBRYO; GANGLION; GENE SILENCING; MITOSIS; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; REACTION TIME; RETINA CELL; RETINA DEVELOPMENT; STEM CELL;

ANIMALS; ANIMALS, NEWBORN; BROMODEOXYURIDINE; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; G2 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMAGE PROCESSING, COMPUTER-ASSISTED; KI-67 ANTIGEN; MICE; MICROSCOPY, CONFOCAL; NEURONS; PROLIFERATING CELL NUCLEAR ANTIGEN; RETINA; TIME FACTORS;

MURINAE;

EID: 84866754777     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.23840     Document Type: Article

References (70)

1. Alexiades MR, Cepko C. 1996. Quantitative analysis of proliferation and cell cycle length during development of the rat retina. Dev Dyn 205: 293-307.
2. 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.
3. Barton KM, Levine EM. 2008. Expression patterns and cell cycle profiles of PCNA, MCM6, cyclin D1, cyclin A2, cyclin B1, and phosphorylated histone H3 in the developing mouse retina. Dev Dyn 237: 672-682.
4. Bates CA, Trinh N, Meyer RL. 1993. Distribution of microtubule-associated proteins (MAPs) in adult and embryonic mouse retinal explants: presence of the embryonic map, MAP5/1B, in regenerating adult retinal axons. Dev Biol 155: 533-544.
5. Baye LM, Link BA. 2007. Interkinetic nuclear migration and the selection of neurogenic cell divisions during vertebrate retinogenesis. J Neurosci 27: 10143-10152.
6. Bonfanti L, Candeo P, Piccinini M, Carmignoto G, Comelli MC, Ghidella S, Bruno R, Gobetto A, Merighi A. 1992. Distribution of protein gene product 9.5 (PGP 9.5) in the vertebrate retina: evidence that immunoreactivity is restricted to mammalian horizontal and ganglion cells. J Comp Neurol 322: 35-44.
7. Bracken AP, Ciro M, Cocito A, Helin K. 2004. E2F target genes: unraveling the biology. Trends Biochem Sci 29: 409-417.
8. Bruno S, Darzynkiewicz Z. 1992. Cell cycle dependent expression and stability of the nuclear protein detected by Ki-67 antibody in HL-60 cells. Cell Prolif 25: 31-40.
9. Bullwinkel J, Baron-Luhr B, Ludemann A, Wohlenberg C, Gerdes J, Scholzen T. 2006. Ki-67 protein is associated with ribosomal RNA transcription in quiescent and proliferating cells. J Cell Physiol 206: 624-635.
10. Burmeister M, Novak J, Liang MY, Basu S, Ploder L, Hawes NL, Vidgen D, Hoover F, Goldman D, Kalnins VI, Roderick TH, Taylor BA, Hankin MH, McInnes RR. 1996. Ocular retardation mouse caused by Chx10 homeobox null allele: impaired retinal progenitor proliferation and bipolar cell differentiation. Nat Genet 12: 376-384.
11. Cayouette M, Barres BA, Raff M. 2003. Importance of intrinsic mechanisms in cell fate decisions in the developing rat retina. Neuron 40: 897-904.
12. Chen D, Livne-Bar I, Vanderluit JL, Slack RS, Agochiya M, Bremner R. 2004. Cell-specific effects of RB or RB/p107 loss on retinal development implicate an intrinsically death-resistant cell-of-origin in retinoblastoma. Cancer Cell 5: 539-551.
13. Chen D, Opavsky R, Pacal M, Tanimoto N, Wenzel P, Seeliger MW, Leone G, Bremner R. 2007. Rb-mediated neuronal differentiation through cell-cycle-independent regulation of E2f3a. PLoS Biol 5: e179.
14. Chen D, Pacal M, Wenzel P, Knoepfler PS, Leone G, Bremner R. 2009. Division and apoptosis of E2f-deficient retinal progenitors. Nature 462: 925-929.
15. Dehay C, Kennedy H. 2007. Cell-cycle control and cortical development. Nat Rev Neurosci 8: 438-450.
16. Denham S. 1967. A cell proliferation study of the neural retina in the two-day rat. J Embryol Exp Morphol 18: 53-66.
17. Drager UC. 1985. Birth dates of retinal ganglion cells giving rise to the crossed and uncrossed optic projections in the mouse. Proc R Soc Lond B Biol Sci 224: 57-77.
18. Ekstrom P, Johansson K. 2003. Differentiation of ganglion cells and amacrine cells in the rat retina: correlation with expression of HuC/D and GAP-43 proteins. Brain Res Dev Brain Res 145: 1-8.
19. Endl E, Gerdes J. 2000. The Ki-67 protein: fascinating forms and an unknown function. Exp Cell Res 257: 231-237.
20. Esteve-Rudd J, Campello L, Herrero MT, Cuenca N, Martin-Nieto J. 2010. Expression in the mammalian retina of parkin and UCH-L1, two components of the ubiquitin-proteasome system. Brain Res 1352: 70-82.
21. Fonatsch C, Duchrow M, Rieder H, Schluter C, Gerdes J. 1991. Assignment of the human Ki-67 gene (MK167) to 10q25-qter. Genomics 11: 476-477.
22. Frank CL, Tsai LH. 2009. Alternative functions of core cell cycle regulators in neuronal migration, neuronal maturation, and synaptic plasticity. Neuron 62: 312-326.
23. Gerdes J, Schwab U, Lemke H, Stein H. 1983. Production of a mouse monoclonal antibody reactive with a human nuclear antigen associated with cell proliferation. Int J Cancer 31: 13-20.
24. Gleeson JG, Lin PT, Flanagan LA, Walsh CA. 1999. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23: 257-271.
25. Gloor BP, Rokos L, Kaldarar-Pedotti S. 1985. Cell cycle time and life-span of cells in the mouse eye. Measurements during the postfetal period using repeated 3H-thymidine injections. Dev Ophthalmol 12: 70-129.
26. Gomes FL, Zhang G, Carbonell F, Correa JA, Harris WA, Simons BD, Cayouette M. 2011. Reconstruction of rat retinal progenitor cell lineages in vitro reveals a surprising degree of stochasticity in cell fate decisions. Development 138: 227-235.
27. Gotz M, Huttner WB. 2005. The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6: 777-788.
28. Haverkamp S, Wassle H. 2000. Immunocytochemical analysis of the mouse retina. J Comp Neurol 424: 1-23.
29. Heidebrecht HJ, Buck F, Haas K, Wacker HH, Parwaresch R. 1996. Monoclonal antibodies Ki-S3 and Ki-S5 yield new data on the 'Ki-67' proteins. Cell Prolif 29: 413-425.
30. Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD. 1997. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106: 348-360.
31. Hinds JW, Hinds PL. 1974. Early ganglion cell differentiation in the mouse retina: an electron microscopic analysis utilizing serial sections. Dev Biol 37: 381-416.
32. Ishida S, Huang E, Zuzan H, Spang R, Leone G, West M, Nevins JR. 2001. Role for E2F in control of both DNA replication and mitotic functions as revealed from DNA microarray analysis. Mol Cell Biol 21: 4684-4699.
33. Kausch I, Lingnau A, Endl E, Sellmann K, Deinert I, Ratliff TL, Jocham D, Sczakiel G, Gerdes J, Bohle A. 2003. Antisense treatment against Ki-67 mRNA inhibits proliferation and tumor growth in vitro and in vivo. Int J Cancer 105: 710-716.
34. Kausch I, Jiang H, Brocks C, Bruderek K, Kruger S, Sczakiel G, Jocham D, Bohle A. 2004. Ki-67-directed antisense therapy in an orthotopic renal cell carcinoma model. Eur Urol 46: 118-124; discussion 124-115.
35. Kausch I, Jiang H, Ewerdwalbesloh N, Doehn C, Kruger S, Sczakiel G, Jocham D. 2005. Inhibition of Ki-67 in a renal cell carcinoma severe combined immunodeficiency disease mouse model is associated with induction of apoptosis and tumour growth inhibition. BJU Int 95: 416-420.
36. Lange C, Calegari F. 2010. Cdks and cyclins link G1 length and differentiation of embryonic, neural and hematopoietic stem cells. Cell Cycle 9: 1893-1900.
37. Lee EJ, Kim IB, Lee E, Kwon SO, Oh SJ, Chun MH. 2003. Differential expression and cellular localization of doublecortin in the developing rat retina. Eur J Neurosci 17: 1542-1548.
38. Leung L, Klopper AV, Grill SW, Harris WA, Norden C. 2011. Apical migration of nuclei during G2 is a prerequisite for all nuclear motion in zebrafish neuroepithelia. Development 138: 5003-5013.
39. Li DW, Yang Q, Chen JT, Zhou H, Liu RM, Huang XT. 2005. Dynamic distribution of Ser-10 phosphorylated histone H3 in cytoplasm of MCF-7 and CHO cells during mitosis. Cell Res 15: 120-126.
40. Livne-Bar I, Pacal M, Cheung MC, Hankin M, Trogadis J, Chen D, Dorval KM, Bremner R. 2006. Chx10 is required to block photoreceptor differentiation but is dispensable for progenitor proliferation in the postnatal retina. Proc Natl Acad Sci USA 103:4988-4993.
41. Locker M, Agathocleous M, Amato MA, Parain K, Harris WA, Perron M. 2006. Hedgehog signaling and the retina: insights into the mechanisms controlling the proliferative properties of neural precursors. Genes Dev 20: 3036-3048.
42. Lyons DA, Guy AT, Clarke JD. 2003. Monitoring neural progenitor fate through multiple rounds of division in an intact vertebrate brain. Development 130: 3427-3436.
43. MacPherson D, Sage J, Kim T, Ho D, McLaughlin ME, Jacks T. 2004. Cell type-specific effects of Rb deletion in the murine retina. Genes Dev 18: 1681-1694.
44. Marquardt T, Ashery-Padan R, Andrejewski N, Scardigli R, Guillemot F, Gruss P. 2001. Pax6 is required for the multipotent state of retinal progenitor cells. Cell 105: 43-55.
45. Meixner A, Haverkamp S, Wassle H, Fuhrer S, Thalhammer J, Kropf N, Bittner RE, Lassmann H, Wiche G, Propst F. 2000. MAP1B is required for axon guidance and Is involved in the development of the central and peripheral nervous system. J Cell Biol 151: 1169-1178.
46. Morrow EM, Belliveau MJ, Cepko CL. 1998. Two phases of rod photoreceptor differentiation during rat retinal development. J Neurosci 18: 3738-3748.
47. Mullen RJ, Buck CR, Smith AM. 1992. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116: 201-211.
48. Okabe S, Shiomura Y, Hirokawa N. 1989. Immunocytochemical localization of microtubule-associated proteins 1A and 2 in the rat retina. Brain Res 483: 335-346.
49. Pan L, Deng M, Xie X, Gan L. 2008. ISL1 and BRN3B co-regulate the differentiation of murine retinal ganglion cells. Development 135: 1981-1990.
50. Pasteels B, Rogers J, Blachier F, Pochet R. 1990. Calbindin and calretinin localization in retina from different species. Vis Neurosci 5: 1-16.
51. Peco E, Escude T, Agius E, Sabado V, Medevielle F, Ducommun B, Pituello F. 2012. The CDC25B phosphatase shortens the G2 phase of neural progenitors and promotes efficient neuron production. Development 139: 1095--1104.
52. Prigent C, Dimitrov S. 2003. Phosphorylation of serine 10 in histone H3, what for? J Cell Sci 116: 3677-3685.
53. Quastler H, Sherman FG. 1959. Cell population kinetics in the intestinal epithelium of the mouse. Exp Cell Res 17: 420-438.
54. Rahmanzadeh R, Huttmann G, Gerdes J, Scholzen T. 2007. Chromophore-assisted light inactivation of pKi-67 leads to inhibition of ribosomal RNA synthesis. Cell Prolif 40: 422-430.
55. Raymond ID, Vila A, Huynh UC, Brecha NC. 2008. Cyan fluorescent protein expression in ganglion and amacrine cells in a thy1-CFP transgenic mouse retina. Mol Vis 14: 1559-1574.
56. Rowan S, Cepko CL. 2004. Genetic analysis of the homeodomain transcription factor Chx10 in the retina using a novel multifunctional BAC transgenic mouse reporter. Dev Biol 271: 388-402.
57. Sakaue-Sawano A, Kurokawa H, Morimura T, Hanyu A, Hama H, Osawa H, Kashiwagi S, Fukami K, Miyata T, Miyoshi H, Imamura T, Ogawa M, Masai H, Miyawaki A. 2008. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 132: 487-498.
58. Schluter C, Duchrow M, Wohlenberg C, Becker MH, Key G, Flad HD, Gerdes J. 1993. The cell proliferation-associated antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle-maintaining proteins. J Cell Biol 123: 513-522.
59. Scholzen T, Endl E, Wohlenberg C, van der Sar S, Cowell IG, Gerdes J, Singh PB. 2002. The Ki-67 protein interacts with members of the heterochromatin protein 1 (HP1) family: a potential role in the regulation of higher-order chromatin structure. J Pathol 196: 135-144.
60. Schonk DM, Kuijpers HJ, van Drunen E, van Dalen CH, Geurts van Kessel AH, Verheijen R, Ramaekers FC. 1989. Assignment of the gene(s) involved in the expression of the proliferation-related Ki-67 antigen to human chromosome 10. Hum Genet 83: 297-299.
61. Sharma RK, Netland PA. 2007. Early born lineage of retinal neurons express class III beta-tubulin isotype. Brain Res 1176: 11-17.
62. Slack RS, El-Bizri H, Wong J, Belliveau DJ, Miller FD. 1998. A critical temporal requirement for the retinoblastoma protein family during neuronal determination. J Cell Biol 140: 1497-1509.
63. Starborg M, Gell K, Brundell E, Hoog C. 1996. The murine Ki-67 cell proliferation antigen accumulates in the nucleolar and heterochromatic regions of interphase cells and at the periphery of the mitotic chromosomes in a process essential for cell cycle progression. J Cell Sci 109: 143-153.
64. Takahashi T, Nowakowski RS, Caviness VS, Jr. 1995. The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 15: 6046-6057.
65. Tram U, Sullivan W. 2002. Role of delayed nuclear envelope breakdown and mitosis in Wolbachia-induced cytoplasmic incompatibility. Science 296: 1124-1126.
66. Trimarchi JM, Stadler MB, Cepko CL. 2008. Individual retinal progenitor cells display extensive heterogeneity of gene expression. PLoS ONE 3: e1588.
67. Wilcock AC, Swedlow JR, Storey KG. 2007. Mitotic spindle orientation distinguishes stem cell and terminal modes of neuron production in the early spinal cord. Development 134: 1943-1954.
68. Wolf HK, Buslei R, Schmidt-Kastner R, Schmidt-Kastner PK, Pietsch T, Wiestler OD, Blumcke I. 1996. NeuN: a useful neuronal marker for diagnostic histopathology. J Histochem Cytochem 44: 1167-1171.
69. Young RW. 1985a. Cell differentiation in the retina of the mouse. Anat Rec 212: 199-205.
70. Young RW. 1985b. Cell proliferation during postnatal development of the retina in the mouse. Brain Res 353: 229-239.