Identification of a transient Sox5 expressing progenitor population in the neonatal ventral forebrain by a novel cis-regulatory element

Developmental Biology

Volumn 393, Issue 1, 2014, Pages 183-193

  Hao, Hailing ^a   Li, Ying ^a   Tzatzalos, Evangeline ^a,c   Gilbert, Jordana ^a   Zala, Dhara ^a   Bhaumik, Mantu ^b   Cai, Li ^a  

^a RUTGERS UNIVERSITY   (United States)

^b CHILD HEALTH INSTITUTE OF NEW JERSEY   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

Cis element; Gene regulation; Neural stem progenitor cells; Olig2; Sox5; Trans acting factor

Indexed keywords

DNA FRAGMENT; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NG2; TRANSCRIPTION FACTOR PHOX2A; TRANSCRIPTION FACTOR PHOX2B; TRANSCRIPTION FACTOR SOX5; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL SPECIFICITY; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FEMALE; FOREBRAIN; GENE EXPRESSION REGULATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; TRANSCRIPTION INITIATION SITE;

CIS-ELEMENT; GENE REGULATION; NEURAL STEM/PROGENITOR CELLS; OLIG2; SOX5; TRANS-ACTING FACTOR;

ANIMALS; BASE SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BINDING SITES; CATTLE; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NEUROGENESIS; PROSENCEPHALON; PROTEIN BINDING; SEQUENCE ALIGNMENT; SOXD TRANSCRIPTION FACTORS;

EID: 84906101925     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.06.010     Document Type: Article

References (48)

1. Akagi T., Inoue T., Miyoshi G., Bessho Y., Takahashi M., Lee J.E., Guillemot F., Kageyama R. Requirement of multiple basic helix-loop-helix genes for retinal neuronal subtype specification. J. Biol. Chem. 2004, 279:28492-28498.
2. Azim E., Jabaudon D., Fame R.M., Macklis J.D. SOX6 controls dorsal progenitor identity and interneuron diversity during neocortical development. Nat. Neurosci. 2009, 12:1238-1247.
3. Batista-Brito R., Rossignol E., Hjerling-Leffler J., Denaxa M., Wegner M., Lefebvre V., Pachnis V., Fishell G. The cell-intrinsic requirement of Sox6 for cortical interneuron development. Neuron 2009, 63:466-481.
4. Bertrand N., Castro D.S., Guillemot F. Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 2002, 3:517-530.
5. Blackwood E.M., Kadonaga J.T. Going the distance: a current view of enhancer action. Science 1998, 281:60-63.
6. Brill M.S., Snapyan M., Wohlfrom H., Ninkovic J., Jawerka M., Mastick G.S., Ashery-Padan R., Saghatelyan A., Berninger B., Gotz M. A dlx2- and pax6-dependent transcriptional code for periglomerular neuron specification in the adult olfactory bulb. J. Neurosci.: Off. J. Soc. Neurosci. 2008, 28:6439-6452.
7. Butt S.J., Fuccillo M., Nery S., Noctor S., Kriegstein A., Corbin J.G., Fishell G. The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 2005, 48:591-604.
8. Cartharius K., Frech K., Grote K., Klocke B., Haltmeier M., Klingenhoff A., Frisch M., Bayerlein M., Werner T. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 2005, 21:2933-2942.
9. Dessaud E., McMahon A.P., Briscoe J. Pattern formation in the vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network. Development 2008, 135:2489-2503.
10. Doh S.T., Hao H., Loh S.C., Patel T., Tawil H.Y., Chen D.K., Pashkova A., Shen A., Wang H., Cai L. Analysis of retinal cell development in chick embryo by immunohistochemistry and in ovo electroporation techniques. BMC. Dev. Biol. 2010, 10:8.
11. Doh S.T., Zhang Y., Temple M.H., Cai L. Non-coding sequence retrieval system for comparative genomic analysis of gene regulatory elements. BMC Bioinform. 2007, 8:94.
12. Finlay B.L., Darlington R.B. Linked regularities in the development and evolution of mammalian brains. Science 1995, 268:1578-1584.
13. Fode C., Ma Q., Casarosa S., Ang S.L., Anderson D.J., Guillemot F. A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev. 2000, 14:67-80.
14. Frazer K.A., Pachter L., Poliakov A., Rubin E.M., Dubchak I. VISTA: computational tools for comparative genomics. Nucl. Acids Res. 2004, 32:W273-W279.
15. Friedli M., Barde I., Arcangeli M., Verp S., Quazzola A., Zakany J., Lin-Marq N., Robyr D., Attanasio C., Spitz F., Duboule D., Trono D., Antonarakis S.E. A systematic enhancer screen using lentivector transgenesis identifies conserved and non-conserved functional elements at the Olig1 and Olig2 locus. PLoS One 2010, 5:e15741.
16. Gomez-Skarmeta J.L., Lenhard B., Becker T.S. New technologies, new findings, and new concepts in the study of vertebrate cis-regulatory sequences. Dev. Dyn. 2006, 235:870-885.
17. Greig L.C., Woodworth M.B., Galazo M.J., Padmanabhan H., Macklis J.D. Molecular logic of neocortical projection neuron specification, development and diversity. Nat. Rev. Neurosci. 2013, 14:755-769.
18. Guth S.I., Wegner M. Having it both ways: Sox protein function between conservation and innovation. Cell. Mol. Life Sci.: CMLS 2008, 65:3000-3018.
19. Hoshino M. Neuronal subtype specification in the cerebellum and dorsal hindbrain. Dev. Growth Differ. 2012, 54:317-326.
20. Jeziorska D.M., Jordan K.W., Vance K.W. A systems biology approach to understanding cis-regulatory module function. Semin. Cell Dev. Biol. 2009, 20:856-862.
21. Lai T., Jabaudon D., Molyneaux B.J., Azim E., Arlotta P., Menezes J.R., Macklis J.D. SOX5 controls the sequential generation of distinct corticofugal neuron subtypes. Neuron 2008, 57:232-247.
22. Lledo P.M., Merkle F.T., Alvarez-Buylla A. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci. 2008, 31:392-400.
23. Lo L., Dormand E., Greenwood A., Anderson D.J. Comparison of the generic neuronal differentiation and neuron subtype specification functions of mammalian achaete-scute and atonal homologs in cultured neural progenitor cells. Development 2002, 129:1553-1567.
24. Long X., Miano J.M. Remote control of gene expression. J. Biol. Chem. 2007, 282:15941-15945.
25. Lopez-Juarez A., Howard J., Ullom K., Howard L., Grande A., Pardo A., Waclaw R., Sun Y.Y., Yang D., Kuan C.Y., Campbell K., Nakafuku M. Gsx2 controls region-specific activation of neural stem cells and injury-induced neurogenesis in the adult subventricular zone. Genes Dev. 2013, 27:1272-1287.
26. Lu Q.R., Cai L., Rowitch D., Cepko C.L., Stiles C.D. Ectopic expression of Olig1 promotes oligodendrocyte formation and reduces neuronal survival in developing mouse cortex. Nat. Neurosci. 2001, 4:973-974.
27. Lu Q.R., Sun T., Zhu Z., Ma N., Garcia M., Stiles C.D., Rowitch D.H. Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 2002, 109:75-86.
28. Lu Q.R., Yuk D., Alberta J.A., Zhu Z., Pawlitzky I., Chan J., McMahon A.P., Stiles C.D., Rowitch D.H. Sonic hedgehog--regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 2000, 25:317-329.
29. Marin O., Rubenstein J.L. A long, remarkable journey: tangential migration in the telencephalon. Nat. Rev. Neurosci. 2001, 2:780-790.
30. Marshall C.A., Novitch B.G., Goldman J.E. Olig2 directs astrocyte and oligodendrocyte formation in postnatal subventricular zone cells. J. Neuroscin: Off. J. Soc. Neurosci. 2005, 25:7289-7298.
31. Marshall C.A., Suzuki S.O., Goldman J.E. Gliogenic and neurogenic progenitors of the subventricular zone: who are they, where did they come from, and where are they going?. Glia 2003, 43:52-61.
32. Martinez-Morales P.L., Quiroga A.C., Barbas J.A., Morales A.V. SOX5 controls cell cycle progression in neural progenitors by interfering with the WNT-beta-catenin pathway. EMBO Rep. 2010, 11:466-472.
33. Menn B., Garcia-Verdugo J.M., Yaschine C., Gonzalez-Perez O., Rowitch D., Alvarez-Buylla A. Origin of oligodendrocytes in the subventricular zone of the adult brain. J. Neurosci.: Off. J. Soc. Neurosci. 2006, 26:7907-7918.
34. Merkle F.T., Mirzadeh Z., Alvarez-Buylla A. Mosaic organization of neural stem cells in the adult brain. Science 2007, 317:381-384.
35. Middeldorp J., Boer K., Sluijs J.A., De Filippis L., Encha-Razavi F., Vescovi A.L., Swaab D.F., Aronica E., Hol E.M. GFAPdelta in radial glia and subventricular zone progenitors in the developing human cortex. Development 2010, 137:313-321.
36. Molyneaux B.J., Arlotta P., Menezes J.R., Macklis J.D. Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 2007, 8:427-437.
37. Panman L., Andersson E., Alekseenko Z., Hedlund E., Kee N., Mong J., Uhde C.W., Deng Q., Sandberg R., Stanton L.W., Ericson J., Perlmann T. Transcription factor-induced lineage selection of stem-cell-derived neural progenitor cells. Cell Stem Cell. 2011, 8:663-675.
38. Parras C.M., Schuurmans C., Scardigli R., Kim J., Anderson D.J., Guillemot F. Divergent functions of the proneural genes Mash1 and Ngn2 in the specification of neuronal subtype identity. Genes Dev. 2002, 16:324-338.
39. Perez-Alcala S., Nieto M.A., Barbas J.A. LSox5 regulates RhoB expression in the neural tube and promotes generation of the neural crest. Development 2004, 131:4455-4465.
40. Quandt K., Frech K., Karas H., Wingender E., Werner T. MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucl. Acids Res. 1995, 23:4878-4884.
41. Stolt C.C., Schlierf A., Lommes P., Hillgartner S., Werner T., Kosian T., Sock E., Kessaris N., Richardson W.D., Lefebvre V., Wegner M. SoxD proteins influence multiple stages of oligodendrocyte development and modulate SoxE protein function. Dev Cell 2006, 11:697-709.
42. Sun T., Hafler B.P., Kaing S., Kitada M., Ligon K.L., Widlund H.R., Yuk D.I., Stiles C.D., Rowitch D.H. Evidence for motoneuron lineage-specific regulation of Olig2 in the vertebrate neural tube. Dev. Biol. 292 2006, 152-164.
43. Wegner M., Stolt C.C. From stem cells to neurons and glia: a Soxist's view of neural development. Trends Neurosci. 2005, 28:583-588.
44. Werner T. Computer-assisted analysis of transcription control regions. Matinspector and other programs. Methods Mol. Biol. 2000, 132:337-349.
45. Yu Y., Chen Y., Kim B., Wang H., Zhao C., He X., Liu L., Liu W., Wu L.M., Mao M., Chan J.R., Wu J., Lu Q.R. Olig2 targets chromatin remodelers to enhancers to initiate oligodendrocyte differentiation. Cell 2013, 152:248-261.
46. Zhou Q., Anderson D.J. The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 2002, 109:61-73.
47. Zhou Q., Wang S., Anderson D.J. Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 2000, 25:331-343.
48. Zhu X., Zuo H., Maher B.J., Serwanski D.R., LoTurco J.J., Lu Q.R., Nishiyama A. Olig2-dependent developmental fate switch of NG2 cells. Development 2012, 139:2299-2307.