Seeing beyond the average cell: Branching process models of cell proliferation, differentiation, and death during mouse brain development

Theory in Biosciences

Volumn 130, Issue 1, 2011, Pages 31-43

  MacMillan, Hugh R ^a   McConnell, Michael J ^b  

^a CLEMSON UNIVERSITY   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Branching process; Neurogenesis; Somatic mosaicism

Indexed keywords

ANIMAL; BIOLOGICAL MODEL; BRAIN CORTEX; CELL DEATH; CELL DIFFERENTIATION; CELL GROWTH; CONFERENCE PAPER; CYTOLOGY; MOUSE; NEURAL STEM CELL; PHYSIOLOGY;

ANIMALS; CELL DEATH; CELL DIFFERENTIATION; CELL GROWTH PROCESSES; CEREBRAL CORTEX; MICE; MODELS, NEUROLOGICAL; NEURAL STEM CELLS;

EID: 79952191739     PISSN: 14317613     EISSN: 16117530     Source Type: Journal    
DOI: 10.1007/s12064-010-0107-7     Document Type: Conference Paper

References (74)

1. A Alvarez-Buylla J Garcia-Verdugo A Tramontin 2001 A unified hypothesis on the lineage of neural stem cells Nat Rev Neurosci 4 287 293 10.1038/35067582 (Pubitemid 33673069)
2. J. Angevine R. Sidman 1961 Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse Nature 192 766 768 10.1038/192766b0 17533671
3. Attardo A, Calegari F, Haubensak W, Wilsch-Brauninger M, Huttner W (2008) Live imaging at the onset of cortical neurogenesis reveals differential appearance of the neuronal phenotype in apical versus basal progenitor progeny. PLoS One 3(6) e2388
4. Bayer S, Altman J (1991) Neocortical development. Raven Press Ltd., New York
5. AJ Blaschke K Staley J Chun 1996 Widespread programmed cell death in proliferative and postmitotic regions of the fetal cerebral cortex Development 122 1165 1174 1:CAS:528:DyaK28XisVOrs74%3D 8620843 (Pubitemid 26123891)
6. Brenner S (1998) Biological computation. In: The limits of reductionism in biology. Wiley, New York, pp 106-116
7. B Brouha J Schustak R Badge S Lutz-Prigge A Farley J Moran H Kazazian 2003 Hot L1s account for the bulk of retrotransposition in the human population Proc Natl Acad Sci 100 9 5280 5285 1:CAS:528:DC%2BD3sXjs1yitrg%3D 10.1073/pnas.0831042100 12682288 (Pubitemid 36542696)
8. Bruyère H, Rupps R, Kuchinka B, Friedman J, Robinson W (2000) Recurrent trisomy 21 in a couple with a child presenting trisomy 21 mosaicism and maternal uniparental disomy for chromosome 21 in the euploid cell line. Am J Med Genet 94(1):35-41
9. M Bylund E Andersson B Novitch J Muhr 2003 Vertebrate neurogenesis is counteracted by Sox1-3 activity Nat Neurosci 6 11 1162 1168 1:CAS:528: DC%2BD3sXosVOiur0%3D 10.1038/nn1131 14517545 (Pubitemid 37346036)
10. L Cai NL Hayes T Takahashi VS Caviness Jr RS Nowakowski 2002 Size distribution of retrovirally marked lineages matches prediction from population measurements of cell cycle behavior J Neurosci Res 69 731 744 1:CAS:528:DC%2BD38XntFGntLo%3D 10.1002/jnr.10398 12205666 (Pubitemid 34984690)
11. F Calegari W Haubensak C Haffner WB Huttner 2005 Selective lengthening of the cell cycle in the neurogenic subpopulation of neural progenitor cells during mouse brain development J Neurosci 25 28 6533 6538 1:CAS:528: DC%2BD2MXmslCltL0%3D 10.1523/JNEUROSCI.0778-05.2005 16014714 (Pubitemid 40995285)
12. M Case H MacMillan 2009 On simulating the generation of mosaicism during mammalian cerebral cortical development J Biol Syst 17 1 27 62 1:CAS:528:DC%2BD1MXksVOnu7k%3D 10.1142/S0218339009002740
13. V Caviness T Takahashi R Nowakowski 1995 Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model Trends Neurosci 18 9 379 383 1:CAS:528:DyaK2MXns1OitLs%3D 10.1016/0166-2236(95)93933-O 7482802
14. V Caviness Jr T Goto T Tarui T Takahashi P Bhide R Nowakowski 2003 Cell output, cell cycle duration and neuronal specification: a model of integrated mechanisms of the neocortical proliferative process Cereb Cortex 13 6 592 598 10.1093/cercor/13.6.592 12764033 (Pubitemid 36613166)
15. N Coufal J Garcia-Perez G Peng G Yeo Y Mu M Lovci M Morell K Oâ, et al. 2009 L1 retrotransposition in human neural progenitor cells Nature 460 7259 1127 1131 1:CAS:528:DC%2BD1MXpsVersLc%3D 10.1038/nature08248 19657334
16. M Dierssen Y Herault X Estivill 2009 Aneuploidy: from a physiological mechanism of variance to down syndrome Physiol Rev 89 3 887 1:CAS:528: DC%2BD1MXpslyjsLg%3D 10.1152/physrev.00032.2007 19584316
17. C Englund A Fink C Lau D Pham RAM Daza A Bulfone T Kowalczyk RF Hevner 2005 Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex J Neurosci 25 1 247 251 1:CAS:528:DC%2BD2MXhtVWrs78%3D 10.1523/JNEUROSCI.2899-04. 2005 15634788 (Pubitemid 40110787)
18. L Farkas WB Huttner 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 1:CAS:528: DC%2BD1cXhsVKrurvM 10.1016/j.ceb.2008.09.008 18930817
19. S Frank 2003 Somatic mosaicism and cancer: inference based on a conditional Luria-Delbrück distribution J Theor Biol 223 4 405 412 10.1016/S0022-5193(03)00117-6 12875820 (Pubitemid 36875739)
20. Frank S (2009) Somatic evolutionary genomics: mutations during development cause highly variable genetic mosaicism with risk of cancer and neurodegeneration. Proc Natl Acad Sci 107:1725-1730
21. FH Gage 2000 Mammalian neural stem cells Science 287 5457 1433 1438 1:CAS:528:DC%2BD3cXhsV2qtrg%3D 10.1126/science.287.5457.1433 10688783 (Pubitemid 30127128)
22. J Gair L Arbour R Rupps R Jiang H Bruyere W Robinson 2005 Recurrent trisomy 21: four cases in three generations Clin Genet 68 5 430 435 1:STN:280:DC%2BD2Mrjt1alsQ%3D%3D 10.1111/j.1399-0004.2005.00512.x 16207210 (Pubitemid 41535967)
23. L Geller H Potter 1999 Chromosome missegregation and trisomy 21 mosaicism in Alzheimer's disease Neurobiol Dis 6 3 167 179 1:CAS:528:DyaK1MXjs1Gnt7c%3D 10.1006/nbdi.1999.0236 10408806 (Pubitemid 29297818)
24. J Gohlke W Griffith S Bartell T Lewandowski E Faustman 2002 A computational model of neocortical neurogenesis predicts ethanol-induced neocortical neuron deficits Dev Brain Res 24 467 477 1:CAS:528: DC%2BD3sXivFOhsL8%3D (Pubitemid 36438781)
25. J Goodier H Kazazian 2008 Retrotransposons revisited: the restraint and rehabilitation of parasites Cell 135 1 23 35 1:CAS:528:DC%2BD1cXht1Gkt7nM 10.1016/j.cell.2008.09.022 18854152
26. M Gotz WB Huttner 2005 The cell biology of neurogenesis Nat Rev Mol Cell Biol 6 10 777 788 10.1038/nrm1739 16314867 (Pubitemid 41726116)
27. Harris T (2002) The theory of branching processes. Dover Publications, New York
28. W Haubensak A Attardo W Denk WB Huttner 2004 Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: A major site of neurogenesis PNAS 101 9 3196 3201 1:CAS:528:DC%2BD2cXitlWhtbo%3D 10.1073/pnas.0308600100 14963232 (Pubitemid 38327757)
29. T Haydar R Nowakowski P Yarowsky B Krueger 2000 Role of founder cell deficit and delayed neuronogenesis in microencephaly of the trisomy 16 mouse J Neurosci 20 4156 4164 1:CAS:528:DC%2BD3cXjsFelurk%3D 10818151 (Pubitemid 30365686)
30. Iacopetti P, Michelini M, Stuckmann I, Oback B, Aaku-Saraste E, Huttner W (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(8):4639-4644. (Pubitemid 29190389)
31. I Iourov S Vorsanova T Liehr Y Yurov 2009 Aneuploidy in the normal, Alzheimer's disease and ataxia-telangiectasia brain: differential expression and pathological meaning Neurobiol Dis 34 2 212 220 1:CAS:528:DC%2BD1MXkslKku7Y%3D 10.1016/j.nbd.2009.01.003 19344645
32. H Kazazian J Goodier 2002 LINE drive retrotransposition and genome instability Cell 110 3 277 280 1:CAS:528:DC%2BD38Xmtl2rsr8%3D 10.1016/S0092-8674(02)00868-1 12176313
33. H Kazazian J Moran 1998 The impact of L1 retrotransposons on the human genome Nat Genet 19 1 19 24 1:CAS:528:DyaK1cXislWqurs%3D 10.1038/ng0598-19 9590283 (Pubitemid 28242017)
34. H Kazazian Jr 2004 Mobile elements: drivers of genome evolution Science 1089670 1626 303
35. Kimmel M, Axelrod D (2002) Branching processes in biology. Springer Verlag, Berlin
36. N Komarova C Lengauer B Vogelstein 2002 Dynamics of genetic instability in sporadic and familial colorectal cancer Cancer Biol Ther 1 6 685 92 1:CAS:528:DC%2BD3sXntVSltrY%3D 12642695
37. N Komarova A Sengupta M Nowak 2003 Mutation-selection networks of cancer initiation: tumor suppressor genes and chromosomal instability J Theoret Biol 223 4 433 450 1:CAS:528:DC%2BD3sXls1eqt70%3D 10.1016/S0022-5193(03)00120-6 (Pubitemid 36880758)
38. N Kraft W Cornwell C Webb D Ackerly 2007 Trait evolution, community assembly, and the phylogenetic structure of ecological communities Am Nat 170 2 271 283 10.1086/519400 17874377 (Pubitemid 47221685)
39. Kriegstein A, Alvarez-Buylla A (2009) The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149-84
40. A Kriegstein S Noctor V Martínez-Cerdeño 2006 Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion Nat Rev Neurosci 7 11 883 890 1:CAS:528:DC%2BD28XhtFShtrnE 10.1038/nrn2008 17033683 (Pubitemid 44624180)
41. T Kuwabara J Hsieh A Muotri G Yeo M Warashina D Lie L Moore K Nakashima M Asashima F Gage 2009 Wnt-mediated activation of NeuroD1 and retro-elements during adult neurogenesis Nat Neurosc 12 9 1097 1105 1:CAS:528: DC%2BD1MXhtVaksrrJ 10.1038/nn.2360
42. W Lo C Chou K Gokoffski F Wan A Lander A Calof Q Nie 2009 Feedback regulation in multistage cell lineages Math Biosci Eng 6 59 82 10.3934/mbe.2009.6.59 19292508
43. M Luskin A Pearlman J Sanes 1988 Cell lineage in the cerebral cortex of the mouse studied in vivo and in vitro with a recombinant retrovirus Neuron 1 8 635 1:STN:280:DyaK3c7ms1Gntg%3D%3D 10.1016/0896-6273(88)90163-8 3272182
44. Mandal P, Kazazian H (2008) SnapShot: vertebrate transposons. Cell 135(1):192-192.e1
45. McConnell MJ, MacMillan H, Chun J (2009) Mathematical modeling supports substantial mouse neural progenitor cell death. Neural Dev 4(1):28
46. RM Merks JA Glazier 2005 A cell-centered approach to developmental biology Physica A Stat Mech Appl 352 1 113 130 1:CAS:528:DC%2BD2MXjs1Cqtr8%3D 10.1016/j.physa.2004.12.028 (Pubitemid 40584061)
47. 1 phase in the murine neocortical proliferative epithelium. Cereb Cortex 7:678-689 (Pubitemid 27467978)
48. T Miyata A Kawaguchi K Saito M Kawano T Muto M Ogawa 2004 Asymmetric production of surface-dividing and non-surface dividing cortical progenitor cells Development 131 3133 3145 1:CAS:528:DC%2BD2cXmtFKlsbc%3D 10.1242/dev.01173 15175243 (Pubitemid 39077437)
49. C Mode 1969 Applications of generalized multi-type age-dependent branching processes in population genetics Bull Math Biol 31 3 575 589 1:STN:280:DyaE3c%2FjtVOguw%3D%3D
50. AR Muotri V Chu M Marchetto W Deng JV Moran FH Gage 2005 Somatic mosaicism in neuronal precursor cells mediated by l1 retrotransposition Nature 435 903 910 1:CAS:528:DC%2BD2MXltFeltb0%3D 10.1038/nature03663 15959507 (Pubitemid 40896309)
51. AR Muotri FH Gage 2006 Generation of neuronal variability and complexity Nature 441 7097 1087 1093 1:CAS:528:DC%2BD28Xmtlahs74%3D 10.1038/nature04959 16810244 (Pubitemid 43990721)
52. T Naas R DeBerardinis J Moran E Ostertag S Kingsmore M Seldin Y Hayashizaki S Martin H Kazazian 1998 An actively retrotransposing, novel subfamily of mouse L1 elements EMBO J 17 2 590 1:CAS:528:DyaK1cXos1ersA%3D%3D 10.1093/emboj/17.2.590 9430649 (Pubitemid 28045498)
53. Noble D (2006) The music of life: biology beyond the genome. Oxford University Press, Oxford
54. SC Noctor AC Flint TA Weissman WS Wong BK Clinton AR Kriegstein 2002 Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia J Neurosci 22 8 3161 3173 1:CAS:528:DC%2BD38XjtF2gt70%3D 11943818 (Pubitemid 35379204)
55. SC Noctor V Martinez-Cerdeno L Ivic AR Kriegstein 2004 Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases Nat Neurosci 7 2 136 134 1:CAS:528:DC%2BD2cXmvVGmtg%3D%3D 10.1038/nn1172 14703572 (Pubitemid 38129789)
56. M Nowak N Komarova A Sengupta P Jallepalli I Shih B Vogelstein C Lengauer 2002 The role of chromosomal instability in tumor initiation Proc Natl Acad Sci 99 25 16,226 16,231 1:CAS:528:DC%2BD38Xps1ensbk%3D 10.1073/pnas.202617399 (Pubitemid 35462777)
57. R Oppenheim 1991 Cell death during development of the nervous system Annu Rev Neurosci 14 453 501 1:STN:280:DyaK3M3jsVSnsw%3D%3D 10.1146/annurev.ne.14. 030191.002321 2031577
58. D Pushkarev NF Neff SR Quake 2009 Single-molecule sequencing of an individual human genome Nat Biotechnol 27 9 847 52 1:CAS:528: DC%2BD1MXps1aht7g%3D 10.1038/nbt.1561 19668243
59. Rehen SK, McConnell MJ, Kaushal D, Kingsbury MA, Yang AH, Chun J (2001) Chromosomal variation in neurons of the developing and adult mammalian nervous system. Proc Natl Acad Sci 98(23):13,361-13,366 (Pubitemid 33051368)
60. J Shendure H Ji 2008 Next-generation DNA sequencing Nat Biotechnol 26 10 1135 1145 1:CAS:528:DC%2BD1cXht1aisrzK 10.1038/nbt1486 18846087
61. JL Slater KA Landman BD Hughes Q Shen S Temple 2009 Cell lineage tree models of neurogenesis J Theoret Biol 256 164 179 10.1016/j.jtbi.2008.09.034
62. S Spencer R Gerety K Pienta S Forrest 2006 Modeling somatic evolution in tumorigenesis PLoS Comput Biol 2 8 e108 10.1371/journal.pcbi.0020108 16933983 (Pubitemid 44298482)
63. Suh H, Deng W, Gage F (2009) Signaling in adult neurogenesis. Annu Rev Cell Dev Biol 25(1):253-275
64. T Takahashi RS Nowakowski VS Caviness Jr 1995 The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall J Neurosci 15 9 6046 6057 1:CAS:528:DyaK2MXnvFChtLg%3D 7666188
65. T Takahashi RS Nowakowski VS Caviness Jr 1996 The leaving or Q fraction of the murine cerebral proliferative epithelium: a general model of neocortical neuronogenesis J Neurosci 16 19 6183 6196 1:CAS:528:DyaK28XntlehsLY%3D 8815900 (Pubitemid 26313993)
66. Takahashi T, S, NR, Caviness Jr VS (1997) The mathematics of neocortical neuronogenesis. Dev Neurosci 19(1):17-22
67. S Temple 2001 The development of neural stem cells Nature 414 112 117 1:CAS:528:DC%2BD3MXot1ahu7c%3D 10.1038/35102174 11689956 (Pubitemid 33041635)
68. F Vaccarino ML Schwartz R Raballo J Rhee R Lyn-Cook 1999 Fibroblast growth factor signaling regulates growth and morphogenesis at multiple steps during brain development Curr Topics Dev Biol 46 179 200 1:CAS:528: DyaK1MXmsVGjtbs%3D 10.1016/S0070-2153(08)60329-4
69. C Walsh CL Cepko 1992 Widespread dispersion of neuronal clones across functional regions of the cerebral cortex Science 255 434 440 1:STN:280:DyaK387jt1GntQ%3D%3D 10.1126/science.1734520 1734520
70. AL Wilkie SA Jordan JA Sharpe D Price IJ Jackson 2004 Widespread tangential dispersion and extensive cell death during early neurogenesis in the mouse neocortex Dev Biol 267 109 118 1:CAS:528:DC%2BD2cXht1yhsrw%3D 10.1016/j.ydbio.2003.11.006 14975720 (Pubitemid 38234737)
71. F Yu N Zingler G Schumann W Stratling 2001 Methyl-CpG-binding protein 2 represses LINE-1 expression and retrotransposition but not Alu transcription Nucl Acids Res 29 21 4493 1:CAS:528:DC%2BD3MXovFaksbg%3D 10.1093/nar/29.21.4493 11691937
72. Y Yurov I Iourov S Vorsanova I Demidova V Kravetz A Beresheva A Kolotii V Monakchov N Uranova V Vostrikov, et al. 2008 The schizophrenia brain exhibits low-level aneuploidy involving chromosome 1 Schizophrenia Res 98 1-3 139 147 10.1016/j.schres.2007.07.035 (Pubitemid 350245588)
73. Y Yurov S Vorsanova I Iourov I Demidova A Beresheva V Kravetz V Monakhov A Kolotii V Voinova-Ulas N Gorbachevskaya 2007 Unexplained autism is frequently associated with low-level mosaic aneuploidy Br Med J 44 8 521 1:STN:280:DC%2BD2svltl2nsg%3D%3D
74. X Zhao T Ueba B Christie B Barkho M McConnell K Nakashima E Lein B Eadie A Willhoite A Muotri, et al. 2003 Mice lacking methyl-CpG binding protein 1 have deficits in adult neurogenesis and hippocampal function Proc Natl Acad Sci 100 11 6777 6782 1:CAS:528:DC%2BD3sXktlygsbo%3D 10.1073/pnas.1131928100 12748381 (Pubitemid 36666656)