The expression of Tubb2b undergoes a developmental transition in murine cortical neurons

Journal of Comparative Neurology

Volumn 523, Issue 15, 2015, Pages 2161-2186

  Breuss, Martin ^a   Morandell, Jasmin ^a   Nimpf, Simon ^a   Gstrein, Thomas ^a   Lauwers, Mattias ^a   Hochstoeger, Tobias ^a   Braun, Andreas ^a,b   Chan, Kelvin ^c   Sánchez Guajardo, Edmundo R ^d   Zhang, Lijuan ^d   Suplata, Marek ^e   Heinze, Katrin G ^e   Elsayad, Kareem ^d   Keays, David A ^a  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^c STONY BROOK UNIVERSITY MEDICAL CENTER   (United States)

^d Advanced Microscopy   (Austria)

^e UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

AB_10048713; AB_10615604; AB_2068336; AB_2088494; AB_2170714; AB_2286684; AB_2314535; AB_303395; AB_310177; AB_442102; AB_570666; AB_778267; Developing cortex; GFP reporter line; Glia; Microtubules; Neuronal migration; Tubulinopathies

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN DEVELOPMENT; CELL GROWTH; CELL POPULATION; CEREBELLUM; COCHLEA; CONTROLLED STUDY; CYTOSKELETON; DENTATE GYRUS; FETUS; GENE; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENETIC ANALYSIS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MACROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RETINA; TUBB2B GENE; ANIMAL; BRAIN; C57BL MOUSE; CONFOCAL MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; GLIA; GROWTH, DEVELOPMENT AND AGING; IMMUNOBLOTTING; METABOLISM; NERVE CELL; NEURAL STEM CELL; THREE DIMENSIONAL IMAGING; TRANSGENIC MOUSE;

ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; TUBB2B PROTEIN, MOUSE; TUBULIN;

ANIMALS; BRAIN; COCHLEA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; IMAGING, THREE-DIMENSIONAL; IMMUNOBLOTTING; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; NEURAL STEM CELLS; NEUROGLIA; NEURONS; REAL-TIME POLYMERASE CHAIN REACTION; RETINA; TUBULIN;

EID: 84939588822     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23836     Document Type: Article

References (86)

1. Abbott NJ, Ronnback L, Hansson E. 2006. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 7:41-53.
2. Attardo A, Calegari F, Haubensak W, Wilsch-Brauninger M, Huttner WB. 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:e2388.
3. Ayala R, Shu T, Tsai LH. 2007. Trekking across the brain: the journey of neuronal migration. Cell 128:29-43.
4. Bahi-Buisson N, Poirier K, Fourniol F, Saillour Y, Valence S, Lebrun N, Hully M, Bianco CF, Boddaert N, Elie C, Lascelles K, Souville I, Consortium LI-T, Beldjord C, Chelly J. 2014. The wide spectrum of tubulinopathies: what are the key features for the diagnosis? Brain 137:1676-1700.
5. Bamji SX, Miller FD. 1996. Comparison of the expression of a T alpha 1:nlacZ transgene and T alpha 1 alpha-tubulin mRNA in the mature central nervous system. J Comp Neurol 374:52-69.
6. Boda E, Pini A, Hoxha E, Parolisi R, Tempia F. 2009. Selection of reference genes for quantitative real-time RT-PCR studies in mouse brain. J Mol Neurosci 37:238-253.
7. Boekhoorn K, Sarabdjitsingh A, Kommerie H, de Punder K, Schouten T, Lucassen PJ, Vreugdenhil E. 2008. Doublecortin (DCX) and doublecortin-like (DCL) are differentially expressed in the early but not late stages of murine neocortical development. J Comp Neurol 507:1639-1652.
8. Braun A, Breuss M, Salzer MC, Flint J, Cowan NJ, Keays DA. 2010. Tuba8 is expressed at low levels in the developing mouse and human brain. Am J Hum Genet 86:819-822; author reply 822-823.
9. Breuss M, Keays DA. 2014. Microtubules and neurodevelopmental disease: the movers and the makers. cellular and molecular control of neuronal migration. New York: Springer. p 75-96.
10. Breuss M, Heng J, Poirier K, Tian G, Jaglin X, Qu Z, Braun A, Gstrein T, Ngo L, Haas M, Bahi-Buisson N, Moutard M, Passemard S, Verloes A, Gressens P, Xie Y, Robson KH, Rani D, Thangaraj K, Clausen T, Chelly J, Cowan N, Keays D. 2012. Mutations in the β-tubulin gene TUBB5 cause microcephaly with structural brain abnormalities. Cell Rept 2:1554-1562.
11. Burgoyne RD, Cambray-Deakin MA, Lewis SA, Sarkar S, Cowan NJ. 1988. Differential distribution of beta-tubulin isotypes in cerebellum. EMBO J 7:2311-2319.
12. Castellano B, Gonzalez B, Jensen MB, Pedersen EB, Finsen BR, Zimmer J. 1991. A double staining technique for simultaneous demonstration of astrocytes and microglia in brain sections and astroglial cell cultures. J Histochem Cytochem 39:561-568.
13. Cederquist GY, Luchniak A, Tischfield MA, Peeva M, Song Y, Menezes MP, Chan W, Andrews C, Chew S, Jamieson RV, Gomes L, Flaherty M, Grant PE, Gupta ML, Engle EC. 2012. An inherited TUBB2B mutation alters a kinesin-binding site and causes polymicrogyria, CFEOM and axon dysinnervation. Hum Mol Genet 21:5484-5499.
14. Cleveland DW. 1987. The multitubulin hypothesis revisited: what have we learned? J Cell Biol 104:381-383.
15. Cleveland D, Kirschner M, Cowan N. 1978. Isolation of separate mRNAs for α- and β-tubulin and characterization of the corresponding in vitro translation products. Cell 15:1021-1031.
16. Cleveland DW, Lopata MA, MacDonald RJ, Cowan NJ, Rutter WJ, Kirschner MW. 1980. Number and evolutionary conservation of alpha- and beta-tubulin and cytoplasmic beta- and gamma-actin genes using specific cloned cDNA probes. Cell 20:95-105.
17. Cowan NJ, Wilde CD, Chow LT, Wefald FC. 1981. Structural variation among human beta-tubulin genes. Proc Natl Acad Sci U S A 78:4877-4881.
18. Cushion TD, Dobyns WB, Mullins JG, Stoodley N, Chung SK, Fry AE, Hehr U, Gunny R, Aylsworth AS, Prabhakar P, Uyanik G, Rankin J, Rees MI, Pilz DT. 2013. Overlapping cortical malformations and mutations in TUBB2B and TUBA1A. Brain 136:536-548.
19. Dent EW, Gertler FB. 2003. Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40:209-227.
20. Emmenlauer M, Ronneberger O, Ponti A, Schwarb P, Griffa A, Filippi A, Nitschke R, Driever W, Burkhardt H. 2009. XuvTools: free, fast and reliable stitching of large 3D datasets. J Microsc 233:42-60.
21. Fagoe ND, Eggers R, Verhaagen J, Mason MR. 2014. A compact dual promoter adeno-associated viral vector for efficient delivery of two genes to dorsal root ganglion neurons. Gene Ther 21:242-252.
22. Fietz SA, Huttner WB. 2011. Cortical progenitor expansion, self-renewal and neurogenesis-a polarized perspective. Curr Opin Neurobiol 21:23-35.
23. Florio M, Huttner WB. 2014. Neural progenitors, neurogenesis and the evolution of the neocortex. Development 141:2182-2194.
24. Franco SJ, Muller U. 2013. Shaping our minds: stem and progenitor cell diversity in the mammalian neocortex. Neuron 77:19-34.
25. Fukushige T, Siddiqui ZK, Chou M, Culotti JG, Gogonea CB, Siddiqui SS, Hamelin M. 1999. MEC-12, an alpha-tubulin required for touch sensitivity in C. elegans. J Cell Sci 112:395-403.
26. Fulton C, Simpson PA. 1976. Selective synthesis and utilization of flagellar tubulin. The multi-tubulin hypothesis. In: Goldman R, Pollard T, Rosenbaum J, editors. Cell motility. New York: Cold Spring Harbor Publications. p 987-1005.
27. Gage FH. 2000. Mammalian neural stem cells. Science 287:1433-1438.
28. Gleeson JG, Walsh CA. 2000. Neuronal migration disorders: from genetic diseases to developmental mechanisms. Trends Neurosci 23:352-359.
29. Gloster A, Wu W, Speelman A, Weiss S, Causing C, Pozniak C, Reynolds B, Chang E, Toma JG, Miller FD. 1994. The T alpha 1 alpha-tubulin promoter specifies gene expression as a function of neuronal growth and regeneration in transgenic mice. J Neurosci 14:7319-7330.
30. Gloster A, El-Bizri H, Bamji SX, Rogers D, Miller FD. 1999. Early induction of Talpha1 alpha-tubulin transcription in neurons of the developing nervous system. J Comp Neurol 405:45-60.
31. Gotz M, Huttner WB. 2005. The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6:777-788.
32. Hama H, Kurokawa H, Kawano H, Ando R, Shimogori T, Noda H, Fukami K, Sakaue-Sawano A, Miyawaki A. 2011. Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain. Nat Neurosci 14:1481-1488.
33. Heimer-McGinn V, Young P. 2011. Efficient inducible Pan-neuronal cre-mediated recombination in SLICK-H transgenic mice. Genesis 49:942-949.
34. 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.
35. Hoyle HD, Raff EC. 1990. Two Drosophila beta tubulin isoforms are not functionally equivalent. J Cell Biol 111:1009-1026.
36. Hutchens JA, Hoyle HD, Turner FR, Raff EC. 1997. Structurally similar Drosophila alpha-tubulins are functionally distinct in vivo. Mol Biol Cell 8:481-500.
37. Jaglin XH, Poirier K, Saillour Y, Buhler E, Tian G, Bahi-Buisson N, Fallet-Bianco C, Phan-Dinh-Tuy F, Kong XP, Bomont P, Castelnau-Ptakhine L, Odent S, Loget P, Kossorotoff M, Snoeck I, Plessis G, Parent P, Beldjord C, Cardoso C, Represa A, Flint J, Keays DA, Cowan NJ, Chelly J. 2009. Mutations in the beta-tubulin gene TUBB2B result in asymmetrical polymicrogyria. Nat Genet 41:746-752.
38. Jaglin X, Chelly J, Bahi-Buisson N. 2012. Tubulin-related malformations of cortical development. Cytoskeleton Hum Dis. Human Press. p 315-341.
39. Janke C, Bulinski JC. 2011. Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions. Nat Rev Mol Cell Biol 12:773-786.
40. Keays DA. 2007. Neuronal migration: unraveling the molecular pathway with humans, mice, and a fungus. Mamm Genome 18:425-430.
41. Keays DA, Cleak J, Huang GJ, Edwards A, Braun A, Treiber CD, Pidsley R, Flint J. 2010. The role of Tuba1a in adult hippocampal neurogenesis and the formation of the dentate gyrus. Dev Neurosci 32:268-277.
42. Keller PJ, Schmidt AD, Wittbrodt J, Stelzer EH. 2008. Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy. Science 322:1065-1069.
43. Kim KK, Adelstein RS, Kawamoto S. 2009. Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors. J Biol Chem 284:31052-31061.
44. Kirshner H, Aguet F, Sage D, Unser M. 2013. 3-D PSF fitting for fluorescence microscopy: implementation and localization application. J Microsc 249:13-25.
45. Kuijpers M, Hoogenraad CC. 2011. Centrosomes, microtubules and neuronal development. Mol Cell Neurosci 48:349-358.
46. Kunishima S, Kobayashi R, Itoh TJ, Hamaguchi M, Saito H. 2009. Mutation of the beta1-tubulin gene associated with congenital macrothrombocytopenia affecting microtubule assembly. Blood 113:458-461.
47. Lewis SA, Lee MG, Cowan NJ. 1985. Five mouse tubulin isotypes and their regulated expression during development. J Cell Biol 101:852-861.
48. Lewis SA, Tian G, Cowan NJ. 1997. The alpha- and beta-tubulin folding pathways. Trends Cell Biol 7:479-484.
49. Liu L, Geisert EE, Frankfurter A, Spano AJ, Jiang CX, Yue J, Dragatsis I, Goldowitz D. 2007. A transgenic mouse class-III beta tubulin reporter using yellow fluorescent protein. Genesis 45:560-569.
50. Malatesta P, Gotz M. 2013. Radial glia-from boring cables to stem cell stars. Development 140:483-486.
51. Mathews EA, Morgenstern NA, Piatti VC, Zhao C, Jessberger S, Schinder AF, Gage FH. 2010. A distinctive layering pattern of mouse dentate granule cells is generated by developmental and adult neurogenesis. J Comp Neurol 518:4479-4490.
52. McKean PG, Vaughan S, Gull K. 2001. The extended tubulin superfamily. J Cell Sci 114:2723-2733.
53. Miller FD, Gauthier AS. 2007. Timing is everything: making neurons versus glia in the developing cortex. Neuron 54:357-369.
54. Mullen RJ, Buck CR, Smith AM. 1992. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
55. Murtaugh LC, Chyung JH, Lassar AB. 1999. Sonic hedgehog promotes somitic chondrogenesis by altering the cellular response to BMP signaling. Genes Dev 13:225-237.
56. Navarro-Quiroga I, Hernandez-Valdes M, Lin SL, Naegele JR. 2006. Postnatal cellular contributions of the hippocampus subventricular zone to the dentate gyrus, corpus callosum, fimbria, and cerebral cortex. J Comp Neurol 497:833-845.
57. Ngo L, Haas M, Qu Z, Li SS, Zenker J, Teng KSL, Gunnersen JM, Breuss M, Habgood M, Keays D. 2014. TUBB5 and its disease-associated mutations influence the terminal differentiation and dendritic spine densities of cerebral cortical neurons. Hum Mol Genet ddu238.
58. Nobrega C, Nascimento-Ferreira I, Onofre I, Albuquerque D, Hirai H, Deglon N, de Almeida LP. 2013. Silencing mutant ataxin-3 rescues motor deficits and neuropathology in Machado-Joseph disease transgenic mice. PloS One 8:e52396.
59. Pinto D, Pagnamenta AT, Klei L, Anney R, Merico D, Regan R, Conroy J, Magalhaes TR, Correia C, Abrahams BS, Almeida J, Bacchelli E, Bader GD, Bailey AJ, Baird G, Battaglia A, Berney T, Bolshakova N, Bolte S, Bolton PF, Bourgeron T, Brennan S, Brian J, Bryson SE, Carson AR, Casallo G, Casey J, Chung BH, Cochrane L, Corsello C, Crawford EL, Crossett A, Cytrynbaum C, Dawson G, de Jonge M, Delorme R, Drmic I, Duketis E, Duque F, Estes A, Farrar P, Fernandez BA, Folstein SE, Fombonne E, Freitag CM, Gilbert J, Gillberg C, Glessner JT, Goldberg J, Green A, Green J, Guter SJ, Hakonarson H, Heron EA, Hill M, Holt R, Howe JL, Hughes G, Hus V, Igliozzi R, Kim C, Klauck SM, Kolevzon A, Korvatska O, Kustanovich V, Lajonchere CM, Lamb JA, Laskawiec M, Leboyer M, Le Couteur A, Leventhal BL, Lionel AC, Liu XQ, Lord C, Lotspeich L, Lund SC, Maestrini E, Mahoney W, Mantoulan C, Marshall CR, McConachie H, McDougle CJ, McGrath J, McMahon WM, Merikangas A, Migita O, Minshew NJ, Mirza GK, Munson J, Nelson SF, Noakes C, Noor A, Nygren G, Oliveira G, Papanikolaou K, Parr JR, Parrini B, Paton T, Pickles A, Pilorge M, Piven J, Ponting CP, Posey DJ, Poustka A, Poustka F, Prasad A, Ragoussis J, Renshaw K, Rickaby J, Roberts W, Roeder K, Roge B, Rutter ML, Bierut LJ, Rice JP, Salt J, Sansom K, Sato D, Segurado R, Sequeira AF, Senman L, Shah N, Sheffield VC, Soorya L, Sousa I, Stein O, Sykes N, Stoppioni V, Strawbridge C, Tancredi R, Tansey K, Thiruvahindrapduram B, Thompson AP, Thomson S, Tryfon A, Tsiantis J, Van Engeland H, Vincent JB, Volkmar F, Wallace S, Wang K, Wang Z, Wassink TH, Webber C, Weksberg R, Wing K, Wittemeyer K, Wood S, Wu J, Yaspan BL, Zurawiecki D, Zwaigenbaum L, Buxbaum JD, Cantor RM, Cook EH, Coon H, Cuccaro ML, Devlin B, Ennis S, Gallagher L, Geschwind DH, Gill M, Haines JL, Hallmayer J, Miller J, Monaco AP, Nurnberger JI Jr, Paterson AD, Pericak-Vance MA, Schellenberg GD, Szatmari P, Vicente AM, Vieland VJ, Wijsman EM, Scherer SW, Sutcliffe JS, Betancur C. 2010. Functional impact of global rare copy number variation in autism spectrum disorders. Nature 466:368-372.
60. Poirier K, Saillour Y, Bahi-Buisson N, Jaglin XH, Fallet-Bianco C, Nabbout R, Castelnau-Ptakhine L, Roubertie A, Attie-Bitach T, Desguerre I, Genevieve D, Barnerias C, Keren B, Lebrun N, Boddaert N, Encha-Razavi F, Chelly J. 2010. Mutations in the neuronal ss-tubulin subunit TUBB3 result in malformation of cortical development and neuronal migration defects. Hum Mol Genet 19:4462-4473.
61. Preitner N, Quan J, Nowakowski DW, Hancock ML, Shi J, Tcherkezian J, Young-Pearse TL, Flanagan JG. 2014. APC is an RNA-binding protein, and its interactome provides a link to neural development and microtubule assembly. Cell 158:368-382.
62. Pulvers JN, Huttner WB. 2009. Brca1 is required for embryonic development of the mouse cerebral cortex to normal size by preventing apoptosis of early neural progenitors. Development 136:1859-1868.
63. Romaniello R, Tonelli A, Arrigoni F, Baschirotto C, Triulzi F, Bresolin N, Bassi MT, Borgatti R. 2012. A novel mutation in the β-tubulin gene TUBB2B associated with complex malformation of cortical development and deficits in axonal guidance. Dev Med Child Neurol 54:765-769.
64. Rowitch DH, Kriegstein AR. 2010. Developmental genetics of vertebrate glial-cell specification. Nature 468:214-222.
65. Saillour Y, Broix L, Bruel-Jungerman E, Lebrun N, Muraca G, Rucci J, Poirier K, Belvindrah R, Francis F, Chelly J. 2014. Beta tubulin isoforms are not interchangeable for rescuing impaired radial migration due to Tubb3 knockdown. Hum Mol Genet 23:1516-1526.
66. Savage C, Hamelin M, Culotti JG, Coulson A, Albertson DG, Chalfie M. 1989. Mec-7 is a beta-tubulin gene required for the production of 15-protofilament microtubules in Caenorhabditis elegans. Genes Dev 3:870-881.
67. Savage C, Xue Y, Mitani S, Hall D, Zakhary R, Chalfie M. 1994. Mutations in the Caenorhabditis elegans beta-tubulin gene mec-7: effects on microtubule assembly and stability and on tubulin autoregulation. J Cell Sci 107:2165-2175.
68. Sirajuddin M, Rice LM, Vale RD. 2014. Regulation of microtubule motors by tubulin isotypes and post-translational modifications. Nat Cell Biol 16:335-344.
69. Stottmann RW, Donlin M, Hafner A, Bernard A, Sinclair DA, Beier DR. 2013. A mutation in Tubb2b, a human polymicrogyria gene, leads to lethality and abnormal cortical development in the mouse. Hum Mol Genet 22:4053-4063.
70. + neural stem cells in the adult hippocampus. Cell Stem Cell 1:515-528.
71. Swanson DJ, Goldowitz D. 2011. Experimental Sey mouse chimeras reveal the developmental deficiencies of Pax6-null granule cells in the postnatal cerebellum. Dev Biol 351:1-12.
72. Tian G, Lewis SA, Feierbach B, Stearns T, Rommelaere H, Ampe C, Cowan NJ. 1997. Tubulin subunits exist in an activated conformational state generated and maintained by protein cofactors. J Cell Biol 138:821-832.
73. Tischfield MA, Baris HN, Wu C, Rudolph G, Van Maldergem L, He W, Chan WM, Andrews C, Demer JL, Robertson RL, Mackey DA, Ruddle JB, Bird TD, Gottlob I, Pieh C, Traboulsi EI, Pomeroy SL, Hunter DG, Soul JS, Newlin A, Sabol LJ, Doherty EJ, de Uzcategui CE, de Uzcategui N, Collins ML, Sener EC, Wabbels B, Hellebrand H, Meitinger T, de Berardinis T, Magli A, Schiavi C, Pastore-Trossello M, Koc F, Wong AM, Levin AV, Geraghty MT, Descartes M, Flaherty M, Jamieson RV, Moller HU, Meuthen I, Callen DF, Kerwin J, Lindsay S, Meindl A, Gupta ML Jr, Pellman D, Engle EC. 2010. Human TUBB3 mutations perturb microtubule dynamics, kinesin interactions, and axon guidance. Cell 140:74-87.
74. Tischfield MA, Cederquist GY, Gupta ML Jr, Engle EC. 2011. Phenotypic spectrum of the tubulin-related disorders and functional implications of disease-causing mutations. Curr Opin Genet Dev 21:286-294.
75. Tsai LH, Gleeson JG. 2005. Nucleokinesis in neuronal migration. Neuron 46:383-388.
76. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034.
77. Vasistha NA, Garcia-Moreno F, Arora S, Cheung AF, Arnold SJ, Robertson EJ, Molnar Z. 2014. Cortical and clonal contribution of Tbr2 expressing progenitors in the developing mouse brain. Cereb Cortex (in press).
78. Vernerey J, Macchi M, Magalon K, Cayre M, Durbec P. 2013. Ciliary neurotrophic factor controls progenitor migration during remyelination in the adult rodent brain. J Neurosci 33:3240-3250.
79. Villasante A, Wang D, Dobner P, Dolph P, Lewis SA, Cowan NJ. 1986. Six mouse alpha-tubulin mRNAs encode five distinct isotypes: testis-specific expression of two sister genes. Mol Cell Biol 6:2409-2419.
80. von Bohlen Und Halbach O. 2007. Immunohistological markers for staging neurogenesis in adult hippocampus. Cell Tissue Res 329:409-420.
81. Vonesch C, Unser M. 2008. A fast thresholded landweber algorithm for wavelet-regularized multidimensional deconvolution. IEEE Transact Image Process 17:539-549.
82. Wang D, Villasante A, Lewis SA, Cowan NJ. 1986. The mammalian beta-tubulin repertoire: hematopoietic expression of a novel, heterologous beta-tubulin isotype. J Cell Biol 103:1903-1910.
83. Wang X, Lui JH, Kriegstein AR. 2011. Orienting fate: spatial regulation of neurogenic divisions. Neuron 72:191-193.
84. Yamada M, Johannesson B, Sagi I, Burnett LC, Kort DH, Prosser RW, Paull D, Nestor MW, Freeby M, Greenberg E, Goland RS, Leibel RL, Solomon SL, Benvenisty N, Sauer MV, Egli D. 2014. Human oocytes reprogram adult somatic nuclei of a type 1 diabetic to diploid pluripotent stem cells. Nature 510:533-536.
85. Yu DX, Marchetto MC, Gage FH. 2014. How to make a hippocampal dentate gyrus granule neuron. Development 141:2366-2375.
86. Yutsudo N, Kamada T, Kajitani K, Nomaru H, Katogi A, Ohnishi YH, Ohnishi YN, Takase K, Sakumi K, Shigeto H, Nakabeppu Y. 2013. fosB-null mice display impaired adult hippocampal neurogenesis and spontaneous epilepsy with depressive behavior. Neuropsychopharmacology 38:895-906.