Transcription factor Sox11 is essential for both embryonic and adult neurogenesis

Developmental Dynamics

Volumn 242, Issue 6, 2013, Pages 638-653

  Wang, Yong ^a   Lin, Lu ^b   Lai, Helen ^c   Parada, Luis F ^b   Lei, Lei ^d  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d UNIVERSITY OF NEW ENGLAND   (United States)

Author keywords

Forebrain; Hippocampus; Migration; Neural progenitor cell; Neurogenesis; Proliferation; Sox11; Transcriptional regulation

Indexed keywords

TRANSCRIPTION FACTOR SOX11;

ALLELE; ARTICLE; BRAIN DEVELOPMENT; BRAIN FUNCTION; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; EMBRYO; FUNCTIONAL GENOMICS; HIPPOCAMPUS; LATERAL BRAIN VENTRICLE; LOXP SITE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SUBVENTRICULAR ZONE;

ALLELES; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DEATH; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; CROSSES, GENETIC; DENTATE GYRUS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOMICS; HIPPOCAMPUS; HOMEODOMAIN PROTEINS; INTEGRASES; MALE; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NERVOUS SYSTEM; NEUROGENESIS; NEURONS; SOXC TRANSCRIPTION FACTORS; TIME FACTORS; TUMOR SUPPRESSOR PROTEINS;

MUS;

EID: 84878147851     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.23962     Document Type: Article

References (80)

1. Abrous DN, Koehl M, Le Moal M. 2005. Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85:523-569.
2. Altman J, Bayer SA. 1990. Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J Comp Neurol 301:325-342.
3. Alvarez-Buylla A, Lim DA. 2004. For the long run: maintaining germinal niches in the adult brain. Neuron 41:683-686.
4. Anderson DJ. 2001. Stem cells and pattern formation in the nervous system: the possible versus the actual. Neuron 30:19-35.
5. Assadi AH, Zhang G, Beffert U, McNeil RS, Renfro AL, Niu S, Quattrocchi CC, Antalffy BA, Sheldon M, Armstrong DD, Wynshaw-Boris A, Herz J, D'Arcangelo G, Clark GD. 2003. Interaction of reelin signaling and Lis1 in brain development. Nat Genet 35:270-276.
6. Ayala R, Shu T, Tsai LH. 2007. Trekking across the brain: the journey of neuronal migration. Cell 128:29-43.
7. Bagri A, Gurney T, He X, Zou YR, Littman DR, Tessier-Lavigne M, Pleasure SJ. 2002. The chemokine SDF1 regulates migration of dentate granule cells. Development 129:4249-4260.
8. Bergsland M, Werme M, Malewicz M, Perlmann T, Muhr J. 2006. The establishment of neuronal properties is controlled by Sox4 and Sox11. Genes Dev 20:3475-3486.
9. Bergsland M, Ramskold D, Zaouter C, Klum S, Sandberg R, Muhr J. 2011. Sequentially acting Sox transcription factors in neural lineage development. Genes Dev 25:2453-2464.
10. Bhattaram P, Penzo-Mendez A, Sock E, Colmenares C, Kaneko KJ, Vassilev A, Depamphilis ML, Wegner M, Lefebvre V. 2010. Organogenesis relies on SoxC transcription factors for the survival of neural and mesenchymal progenitors. Nat Commun 1:9.
11. Bix GJ, Clark GD. 1998. Platelet-activating factor receptor stimulation disrupts neuronal migration In vitro. J Neurosci 18:307-318.
12. Blaiss CA, Yu TS, Zhang G, Chen J, Dimchev G, Parada LF, Powell CM, Kernie SG. 2011. Temporally specified genetic ablation of neurogenesis impairs cognitive recovery after traumatic brain injury. J Neurosci 31:4906-4916.
13. Bowles J, Schepers G., Koopman P. 2000. Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev Biol 227:239-255.
14. Bylund M, Andersson E, Novitch BG., Muhr J. 2003. Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat Neurosci 6:1162-1168.
15. Caviness VS Jr, Sidman RL. 1973. Time of origin or corresponding cell classes in the cerebral cortex of normal and reeler mutant mice: an autoradiographic analysis. J Comp Neurol 148:141-151.
16. Chen J, Kwon CH, Lin L, Li Y, Parada LF. 2009. Inducible site-specific recombination in neural stem/progenitor cells. Genesis 47:122-131.
17. Cheung M, Briscoe J. 2003. Neural crest development is regulated by the transcription factor Sox9. Development 130:5681-5693.
18. Cheung M, Abu-Elmagd M, Clevers H, Scotting PJ. 2000. Roles of Sox4 in central nervous system development. Brain Res Mol Brain Res 79:180-191.
19. Deng W, Aimone JB, Gage FH. 2010. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 11:339-350.
20. Dy P, Penzo-Mendez A, Wang H, Pedraza CE, Macklin WB, Lefebvre V. 2008. The three SoxC proteins-Sox4, Sox11 and Sox12-exhibit overlapping expression patterns and molecular properties. Nucleic Acids Res 36:3101-3117.
21. Edlund T, Jessell TM. 1999. Progression from extrinsic to intrinsic signaling in cell fate specification: a view from the nervous system. Cell 96:211-224.
22. Forster E, Zhao S, Frotscher M. 2006. Laminating the hippocampus. Nat Rev Neurosci 7:259-267.
23. Francois M, Koopman P, Beltrame M. 2010. SoxF genes: Key players in the development of the cardio-vascular system. Int J Biochem Cell Biol 42:445-448.
24. Graham V, Khudyakov J, Ellis P, Pevny L. 2003. SOX2 functions to maintain neural progenitor identity. Neuron 39:749-765.
25. Gu H, Marth JD, Orban PC, Mossmann H, Rajewsky K. 1994. Deletion of a DNA polymerase beta gene segment in T cells using cell type-specific gene targeting. Science 265:103-106.
26. Guillemot F. 2007. Spatial and temporal specification of neural fates by transcription factor codes. Development 134:3771-3780.
27. Hargrave M, Wright E, Kun J, Emery J, Cooper L, Koopman P. 1997. Expression of the Sox11 gene in mouse embryos suggests roles in neuronal maturation and epithelio-mesenchymal induction. Dev Dyn 210:79-86.
28. Harley VR, Lovell-Badge R, Goodfellow PN. 1994. Definition of a consensus DNA binding site for SRY. Nucleic Acids Res 22:1500-1501.
29. Haslinger A, Schwarz TJ, Covic M, Chichung Lie D. 2009. Expression of Sox11 in adult neurogenic niches suggests a stage-specific role in adult neurogenesis. Eur J Neurosci 29:2103-2114.
30. Hirotsune S, Fleck MW, Gambello MJ, Bix GJ, Chen A, Clark GD, Ledbetter DH, McBain CJ, Wynshaw-Boris A. 1998. Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nat Genet 19:333-339.
31. Hoser M, Potzner MR, Koch JM, Bosl MR, Wegner M, Sock E. 2008. Sox12 deletion in the mouse reveals non-reciprocal redundancy with the related Sox4 and Sox11 transcription factors. Mol Cell Biol 28:4675-4687.
32. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R. 2008. Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11:1153-1161.
33. Johnson GL, Lapadat R. 2002. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298:1911-1912.
34. Kamachi Y, Uchikawa M, Kondoh H. 2000. Pairing SOX off: with partners in the regulation of embryonic development. Trends Genet 16:182-187.
35. Kenney AM, Cole MD, Rowitch DH. 2003. Nmyc upregulation by sonic hedgehog signaling promotes proliferation in developing cerebellar granule neuron precursors. Development 130:15-28.
36. Kholmanskikh SS, Dobrin JS, Wynshaw-Boris A, Letourneau PC, Ross ME. 2003. Disregulated RhoGTPases and actin cytoskeleton contribute to the migration defect in Lis1-deficient neurons. J Neurosci 23:8673-8681.
37. Kholmanskikh SS, Koeller HB, Wynshaw-Boris A, Gomez T, Letourneau PC, Ross ME. 2006. Calcium-dependent interaction of Lis1 with IQGAP1 and Cdc42 promotes neuronal motility. Nat Neurosci 9:50-57.
38. Kim J, Lo L, Dormand E, Anderson DJ. 2003. SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron 38:17-31.
39. Knoepfler PS, Cheng PF, Eisenman RN. 2002. N-myc is essential during neurogenesis for the rapid expansion of progenitor cell populations and the inhibition of neuronal differentiation. Genes Dev 16:2699-2712.
40. Knoepfler PS, Kenney AM. 2006. Neural precursor cycling at sonic speed: N-Myc pedals, GSK-3 brakes. Cell Cycle 5:47-52.
41. Kuhlbrodt K, Herbarth B, Sock E, Enderich J, Hermans-Borgmeyer I, Wegner M. 1998. Cooperative function of POU proteins and SOX proteins in glial cells. J Biol Chem 273:16050-16057.
42. Lefebvre V, Smits P. 2005. Transcriptional control of chondrocyte fate and differentiation. Birth Defects Res C Embryo Today 75:200-212.
43. Lei L, Laub F, Lush M, Romero M, Zhou J, Luikart B, Klesse L, Ramirez F, Parada LF. 2005. The zinc finger transcription factor Klf7 is required for TrkA gene expression and development of nociceptive sensory neurons. Genes Dev 19:1354-1364.
44. Lei L, Zhou J, Lin L, Parada LF. 2006. Brn3a and Klf7 cooperate to control TrkA expression in sensory neurons. Dev Biol 300:758-769.
45. Li Y, Luikart BW, Birnbaum S, Chen J, Kwon CH, Kernie SG, Bassel-Duby R, Parada LF. 2008. TrkB regulates hippocampal neurogenesis and governs sensitivity to antidepressive treatment. Neuron 59:399-412.
46. Lin L, Lee VM, Wang Y, Lin JS, Sock E, Wegner M, Lei L. 2011. Sox11 regulates survival and axonal growth of embryonic sensory neurons. Dev Dyn 240:52-64.
47. Ma DK, Kim WR, Ming GL, Song H. 2009. Activity-dependent extrinsic regulation of adult olfactory bulb and hippocampal neurogenesis. Ann NY Acad Sci 1170:664-673.
48. Ma DK, Marchetto MC, Guo JU, Ming GL, Gage FH, Song H. 2010. Epigenetic choreographers of neurogenesis in the adult mammalian brain. Nat Neurosci 13:1338-1344.
49. Marin O, Rubenstein JL. 2003. Cell migration in the forebrain. Annu Rev Neurosci 26:441-483.
50. Markus A, Zhong J, Snider WD. 2002. Raf and akt mediate distinct aspects of sensory axon growth. Neuron 35:65-76.
51. McConnell SK. 1995. Constructing the cerebral cortex: neurogenesis and fate determination. Neuron 15:761-768.
52. Ming GL, Song H. 2005. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223-250.
53. Molyneaux BJ, Arlotta P, Menezes JR, Macklis JD. 2007. Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8:427-437.
54. Mu L, Berti L, Masserdotti G, Covic M, Michaelidis TM, Doberauer K, Merz K, Rehfeld F, Haslinger A, Wegner M, Sock E, Lefebvre V, Couillard-Despres S, Aigner L, Berninger B, Lie DC. 2012. SoxC transcription factors are required for neuronal differentiation in adult hippocampal neurogenesis. J Neurosci 32:3067-3080.
55. Nowakowski RS, Rakic P. 1979. The mode of migration of neurons to the hippocampus: a Golgi and electron microscopic analysis in foetal rhesus monkey. J Neurocytol 8:697-718.
56. Nowakowski RS, Rakic P. 1981. The site of origin and route and rate of migration of neurons to the hippocampal region of the rhesus monkey. J Comp Neurol 196:129-154.
57. O'Gorman S, Dagenais NA, Qian M, Marchuk Y. 1997. Protamine-Cre recombinase transgenes efficiently recombine target sequences in the male germ line of mice, but not in embryonic stem cells. Proc Natl Acad Sci USA 94:14602-14607.
58. Potzner MR, Tsarovina K, Binder E, Penzo-Mendez A, Lefebvre V, Rohrer H, Wegner M, Sock E. 2010. Sequential requirement of Sox4 and Sox11 during development of the sympathetic nervous system. Development 137:775-784.
59. Rakic P, Nowakowski RS. 1981. The time of origin of neurons in the hippocampal region of the rhesus monkey. J Comp Neurol 196:99-128.
60. Rodriguez CI, Buchholz F, Galloway J, Sequerra R, Kasper J, Ayala R, Stewart AF, Dymecki SM. 2000. High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat Genet 25:139-140.
61. Romero MI, Lin L, Lush ME, Lei L, Parada LF, Zhu Y. 2007. Deletion of Nf1 in neurons induces increased axon collateral branching after dorsal root injury. J Neurosci 27:2124-2134.
62. Ross SE, Greenberg ME, Stiles CD. 2003. Basic helix-loop-helix factors in cortical development. Neuron 39:13-25.
63. Sahay A, Hen R. 2007. Adult hippocampal neurogenesis in depression. Nat Neurosci 10:1110-1115.
64. Sahay A, Scobie KN, Hill AS, O'Carroll CM, Kheirbek MA, Burghardt NS, Fenton AA, Dranovsky A, Hen R. 2011. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472:466-470.
65. Sandberg M, Kallstrom M, Muhr J. 2005. Sox21 promotes the progression of vertebrate neurogenesis. Nat Neurosci 8:995-1001.
66. Sapir T, Elbaum M, Reiner O. 1997. Reduction of microtubule catastrophe events by LIS1, platelet-activating factor acetylhydrolase subunit. Embo J 16:6977-6984.
67. Schepers GE, Teasdale RD, Koopman P. 2002. Twenty pairs of sox: extent, homology, and nomenclature of the mouse and human sox transcription factor gene families. Dev Cell 3:167-170.
68. Schilham MW, Oosterwegel MA, Moerer P, Ya J, de Boer PA, van de Wetering M, Verbeek S, Lamers WH, Kruisbeek AM, Cumano A, Clevers H. 1996. Defects in cardiac outflow tract formation and pro-B-lymphocyte expansion in mice lacking Sox-4. Nature 380:711-714.
69. Sekido R, Lovell-Badge R. 2009. Sex determination and SRY: down to a wink and a nudge? Trends Genet 25:19-29.
70. Shim S, Kwan KY, Li M, Lefebvre V, Sestan N. 2012. Cis-regulatory control of corticospinal system development and evolution. Nature 486:74-79.
71. Sjostrom SK, Finn G, Hahn WC, Rowitch DH, Kenney AM. 2005. The Cdk1 complex plays a prime role in regulating N-myc phosphorylation and turnover in neural precursors. Dev Cell 9:327-338.
72. Sock E, Rettig SD, Enderich J, Bosl MR, Tamm ER, Wegner M. 2004. Gene targeting reveals a widespread role for the high-mobility-group transcription factor Sox11 in tissue remodeling. Mol Cell Biol 24:6635-6644.
73. Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663-676.
74. Temple S. 2001. The development of neural stem cells. Nature 414:112-117.
75. Thein DC, Thalhammer JM, Hartwig AC, Crenshaw EB 3rd, Lefebvre V, Wegner M, Sock E. 2010. The closely related transcription factors Sox4 and Sox11 function as survival factors during spinal cord development. J Neurochem 115:131-141.
76. Wegner M. 1999. From head to toes: the multiple facets of Sox proteins. Nucleic Acids Res 27:1409-1420.
77. Wonders CP, Anderson SA. 2006. The origin and specification of cortical interneurons. Nat Rev Neurosci 7:687-696.
78. Zhao C, Deng W, Gage FH. 2008. Mechanisms and functional implications of adult neurogenesis. Cell 132:645-660.
79. Zhong W. 2003. Diversifying neural cells through order of birth and asymmetry of division. Neuron 37:11-14.
80. Zhou CJ, Zhao C, Pleasure SJ. 2004. Wnt signaling mutants have decreased dentate granule cell production and radial glial scaffolding abnormalities. J Neurosci 24:121-126.