LHX2 interacts with the NuRD complex and regulates cortical neuron subtype determinants Fezf2 and Sox11

Journal of Neuroscience

Volumn 37, Issue 1, 2017, Pages 194-203

  Muralidharan, Bhavana ^a   Khatri, Zeba ^a   Maheshwari, Upasana ^a   Gupta, Ritika ^a   Roy, Basabdatta ^a   Pradhan, Saurabh J ^b,c   Karmodiya, Krishanpal ^b   Padmanabhan, Hari ^a,d,e   Shetty, Ashwin S ^a,d   Balaji, Chinthapalli ^a   Kolthur Seetharam, Ullas ^a   Macklis, Jeffrey D ^d,e   Galande, Sanjeev ^b   Tole, Shubha ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH   (India)

^c SYMBIOSIS INTERNATIONAL DEEMED UNIVERSITY   (India)

^d Harvard University   (United States)

^e HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

Cell fate; Chromatin; Epigenetics; Lamination; Progenitor; Specification

Indexed keywords

FEZ FAMILY ZINC FINGER PROTEIN 2; HISTONE DEACETYLASE; TRANSCRIPTION FACTOR LHX2; TRANSCRIPTION FACTOR SOX11; UNCLASSIFIED DRUG; BRAIN PROTEIN; HISTONE DEACETYLASE 2; PROTEIN CTIP2; PROTEIN FEZF2; PROTEIN LHX2; PROTEIN LSD1; PROTEIN NURD; REGULATOR PROTEIN; RETINOBLASTOMA BINDING PROTEIN 4; TRANSCRIPTION FACTOR; CHROMATIN; DNA BINDING PROTEIN; LHX2 PROTEIN, MOUSE; LIM HOMEODOMAIN PROTEIN; NERVE PROTEIN; NUCLEOSOME; SOX11 PROTEIN, MOUSE; TRANSCRIPTION FACTOR SOX; ZFP312 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CHROMATIN; CONTROLLED STUDY; ELECTROPORATION; FEMALE; GENE LOCUS; GENE OVEREXPRESSION; GENE SEQUENCE; GENOTYPE; IMAGING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MICROSCOPY; MOUSE; NONHUMAN; NUCLEOSOME; POLYMERASE CHAIN REACTION; PREGNANCY; PRIORITY JOURNAL; WESTERN BLOTTING; ANIMAL CELL; BRAIN CORTEX; EMBRYO; EPIGENETIC MODIFICATION; MALE; NERVOUS SYSTEM DEVELOPMENT; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATOR GENE; REGULATORY MECHANISM; ANIMAL; CYTOLOGY; DIAGNOSTIC IMAGING; GENETIC EPIGENESIS; GENETICS; METABOLISM; NERVE CELL; PHYSIOLOGY;

ANIMALS; CEREBRAL CORTEX; CHROMATIN; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; FEMALE; HISTONE DEACETYLASES; LIM-HOMEODOMAIN PROTEINS; MALE; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; MICE; NERVE TISSUE PROTEINS; NEURONS; NUCLEOSOMES; PREGNANCY; SOXC TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS;

EID: 85008952969     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2836-16.2016     Document Type: Article

References (53)

1. Arlotta P, Molyneaux BJ, Chen J, Inoue J, Kominami R, Macklis JD (2005) Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45:207-221. Cross Ref Medline
2. Bedogni F, Hodge RD, Elsen GE, Nelson BR, Daza RA, Beyer RP, Bammler TK, Rubenstein JL, Hevner RF (2010) Tbrl regulates regional and laminar identity ofpostmitotic neurons in developing neocortex. Proc Natl Acad SciUSA 107:13129-13134. Cross Ref Medline
3. Berger MF, Badis G, Gehrke AR, Talukder S, Philippakis AA, Pena-Castillo L, Alleyne TM, Mnaimneh S, Botvinnik OB, Chan ET, Khalid F, Zhang W, Newburger D, Jaeger SA, Morris QD, Bulyk ML, Hughes TR (2008) Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 133:1266-1276. Cross Ref Medline
4. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125:315-326. CrossRef Medline
5. Bulchand S, Subramanlan L, Tole S (2003) Dynamic spatiotemporal expression ofLIM genes and cofactors in the embryonic and postnatal cerebral cortex. DevDynam 226:460-469. Cross Ref Medline
6. Cederquist GY, Azim E, Shnider SJ, Padmanabhan H, Macklis JD (2013) Lmo4 establishes rostral motor cortex projection neuron subtype diversity. J Neurosci 33:6321-6332. Cross Ref Medline
7. Chen B, Schaevitz LR, McConnell SK (2005) Fezl regulates the differentiation and axon targeting of layer 5 subcortical projection neurons in cerebral cortex. Proc Natl Acad Sci U S A 102:17184-17189. Cross Ref Medline
8. Chen B, Wang SS, Hattox AM, Rayburn H, Nelson SB, McConnell SK (2008) The Fezf2-Ctip2 genetic pathway regulates the fate choice of subcortical projection neurons in the developing cerebral cortex. Proc Natl Acad Sci USA 105:11382-11387. Cross Ref Medline
9. Chou SJ, O’Leary DD (2013) Role for Lhx2 in corticogenesis through regulation of progenitor differentiation. Mol Cell Neurosci 56:1-9. CrossRef Medline
10. Chou SJ, Perez-Garcia CG, Kroll TT, O’Leary DD (2009) Lhx2 specifies regional fate in Emx1 lineage of telencephalic progenitors generating cerebral cortex. Nat Neurosci 12:1381-1389. Cross Ref Medline
11. Cubelos B, Sebastian-Serrano A, Beccari L, Calcagnotto ME, Cisneros E, Kim S, Dopazo A, Alvarez-Dolado M, Redondo JM, Bovolenta P, Walsh CA, Nieto M (2010) Cux1 and Cux2 regulate dendritic branching, spine morphology, and synapses of the upper layer neurons of the cortex. Neuron 66:523-535. Cross Ref Medline
12. Díaz-Alonso J, Guzman M, Galve-Roperh I (2012) Endocannabinoids via CB(1) receptors act as neurogenic niche cues during cortical development. Philos Trans R Soc Lond B Biol Sci 367:3229-3241. Cross Ref Medline
13. Díaz-Alonso J, Aguado T, de Salas-Quiroga A, Ortega Z, Guzman M, Galve- Roperh I (2015) CB1 cannabinoid receptor-dependent activation of mTORC1/Pax6 signaling drives Tbr2 expression and basal progenitor expansion in the developing mouse cortex. Cereb Cortex 25:2395-2408. Cross Ref Medline
14. Eckler MJ, Larkin KA, McKenna WL, Katzman S, Guo C, Roque R, Visel A, Rubenstein JL, Chen B (2014) Multiple conserved regulatory domains promote Fezf2 expression in the developing cerebral cortex. Neural Dev 9:6. Cross Ref Medline
15. Faedo A, Tomassy GS, Ruan Y, Teichmann H, Krauss S, Pleasure SJ, Tsai SY, Tsai MJ, Studer M, Rubenstein JL (2008) COUP-TFI coordinates cortical patterning, neurogenesis, and laminar fate and modulates MAPK/ ERK, AKT, and beta-catenin signaling. Cereb Cortex 18:2117-2131. Cross Ref Medline
16. Greig LC, Woodworth MB, Galazo MJ, Padmanabhan H, Macklis JD (2013) Molecular logic of neocortical projection neuron specification, development and diversity. Nat Rev Neurosci 14:755-769. Cross Ref Medline
17. Guo C, Eckler MJ, McKenna WL, McKinsey GL, Rubenstein JL, Chen B (2013) Fezf2 expression identifies a multipotent progenitor for neocor- tical projection neurons, astrocytes, and oligodendrocytes. Neuron 80: 1167-1174. Cross Ref Medline
18. Han W, Kwan KY, Shim S, Lam MM, Shin Y, Xu X, Zhu Y, Li M, Sestan N (2011) TBR1 directly represses Fezf2 to control the laminar origin and development of the corticospinal tract. Proc Natl Acad Sci U S A 108: 3041-3046. Cross Ref Medline
19. Harb K, Magrinelli E, Nicolas CS, Lukianets N, Frangeul L, Pietri M, Sun T, Sandoz G, Grammont F, Jabaudon D, Studer M, Alfano C (2016) Area- specific development ofdistinct projection neuron subclasses is regulated by postnatal epigenetic modifications. Elife 5:e09531. Cross Ref Medline
20. Hevner RF, Shi L, Justice N, Hsueh Y, Sheng M, Smiga S, Bulfone A, Goffinet AM, Campagnoni AT, Rubenstein JL (2001) Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29:353-366. Cross Ref Medline
21. Hirabayashi Y, Gotoh Y (2010) Epigenetic control of neural precursor cell fate during development. Nat Rev Neurosci 11:377-388. Cross Ref Medline
22. Hirata T, Suda Y, Nakao K, Narimatsu M, Hirano T, Hibi M (2004) Zinc finger gene fez-like functions in the formation of subplate neurons and thalamocortical axons. Dev Dyn 230:546-556. Cross Ref Medline
23. Jin XL, Guo H, Mao C, Atkins N, Wang H, Avasthi PP, Tu YT, Li Y (2000) Emx1-specific expression of foreign genes using “knock-in” approach. Biochem Biophys Res Commun 270:978-982. Cross Ref Medline
24. Karmodiya K, Krebs AR, Oulad-Abdelghani M, Kimura H, Tora L (2012) H3K9 and H3K14 acetylationco-occur at manygene regulatory elements, while H3K14ac marks a subset of inactive inducible promoters in mouse embryonic stem cells. BMC Genomics 13:424. Cross Ref Medline
25. Kohwi M, Doe CQ (2013) Temporal fate specification and neural progeni-tor competence during development. Nat Rev Neurosci 14:823-838. Cross Ref Medline
26. Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D (2002) Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 16:2893-2905. Cross Ref Medline
27. Kwan KY, Lam MM, Krsnik Z, Kawasawa YI, Lefebvre V, Sestan N (2008) SOX5 postmitotically regulates migration, postmigratory differentiation, and projections ofsubplate and deep-layer neocortical neurons. Proc Natl Acad Sci U S A 105:16021-16026. Cross Ref Medline
28. Lai T, Jabaudon D, Molyneaux BJ, Azim E, Arlotta P, Menezes JR, Macklis JD (2008) SOX5 controls the sequential generation of distinct corticofugal neuron subtypes. Neuron 57:232-247. Cross Ref Medline
29. Lu CH, Rincon-Limas DE, Botas J (2000) Conserved overlapping and reciprocal expression of msh/Msx1 and apterous/Lhx2 in Drosophila and mice. Mech Dev 99:177-181. Cross Ref Medline
30. Mangale VS, Hirokawa KE, Satyaki PR, Gokulchandran N, Chikbire S, Sub- ramanian L, Shetty AS, Martynoga B, Paul J, Mai MV, Li Y, Flanagan LA, Tole S, Monuki ES (2008) Lhx2 selector activity specifies cortical identity and suppresses hippocampal organizer fate. Science 319:304-309. Cross Ref Medline
31. McKenna WL, Betancourt J, Larkin KA, Abrams B, Guo C, Rubenstein JL, Chen B (2011) Tbr1 and Fezf2 regulate alternate corticofugal neuronal identities during neocortical development. J Neurosci 31:549-564. Cross Ref Medline
32. McKenna WL, Ortiz-Londono CF, Mathew TK, Hoang K, Katzman S, Chen B (2015) Mutual regulation between Satb2 and Fezf2 promotes subcerebral projection neuron identity in the developing cerebral cortex. Proc Natl Acad SciUS A 112:11702-11707. Cross Ref Medline
33. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O’Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553-560. Cross Ref Medline
34. Molyneaux BJ, Arlotta P, Hirata T, Hibi M, Macklis JD (2005) Fezl is required for the birth and specification of corticospinal motor neurons. Neuron 47:817-831. Cross Ref Medline
35. Nakagawa Y, Johnson JE, O’Leary DD (1999) Graded and areal expression patterns of regulatory genes and cadherins in embryonic neocortex independent ofthalamocortical input. J Neurosci 19:10877-10885. Medline
36. Nieto M, Monuki ES, Tang H, Imitola J, Haubst N, Khoury SJ, Cunningham J, Gotz M, Walsh CA (2004) Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IVof the cerebral cortex. J Comp Neurol 479:168-180. Cross Ref Medline
37. Rincon-Limas DE, Lu CH, Canal I, Calleja M, Rodríguez-Esteban C, Izpisua- Belmonte JC, Botas J (1999) Conservation of the expression and function of apterous orthologs in Drosophila and mammals. Proc Natl Acad SciU S A 96:2165-2170. Cross Ref Medline
38. Rodríguez-Tornos FM, Briz CG, Weiss LA, Sebastian-Serrano A, Ares S, Na- varrete M, Frangeul L, Galazo M, Jabaudon D, Esteban JA, Nieto M (2016) Cux1 enables interhemispheric connections of layer II/III Neurons by regulating Kv1-dependent firing. Neuron 89:494-506. Cross Ref Medline
39. Rouaux C, Arlotta P (2013) Direct lineage reprogramming of post-mitotic callosal neurons into corticofugal neurons in vivo. Nat Cell Biol 15:214221. Cross Ref Medline
40. Shetty AS, Godbole G, Maheshwari U, Padmanabhan H, Chaudhary R, Mu- ralidharanB, Hou PS, Monuki ES, Kuo HC, Rema V, Tole S (2013) Lhx2 regulates a cortex-specific mechanism for barrel formation. P Natl Acad Sci U S A 110:E4913-E4921. Cross Ref Medline
41. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850-858. Cross Ref Medline
42. Shim S, Kwan KY, Li M, Lefebvre V, Sestan N (2012) Cis-regulatory control of corticospinal system development and evolution. Nature 486:74-79. Cross Ref Medline
43. Subramanian L, Sarkar A, Shetty AS, Muralidharan B, Padmanabhan H, Piper M, Monuki ES, Bach I, Gronostajski RM, Richards LJ, Tole S (2011) Transcription factor Lhx2 is necessary and sufficient to suppress astro-gliogenesis and promote neurogenesis in the developing hippocampus. Proc Natl Acad Sci USA 108:E265-E274. Cross Ref Medline
44. Tomassy GS, De Leonibus E, Jabaudon D, Lodato S, Alfano C, Mele A, Macklis JD, Studer M (2010) Area-specific temporal control of corticospinal motor neuron differentiation by COUP-TFI. Proc Natl Acad Sci U S A 107:3576-3581. Cross Ref Medline
45. Vernimmen D, Bickmore WA (2015) The hierarchy of transcriptional activation: from enhancer to promoter. Trends Genet 31:696-708. Cross Ref Medline
46. Wang J, Scully K, Zhu X, Cai L, Zhang J, Prefontaine GG, Krones A, Ohgi KA, Zhu P, Garcia-Bassets I, Liu F, Taylor H, Lozach J, Jayes FL, Korach KS, Glass CK, Fu XD, Rosenfeld MG (2007) Opposing LSD1 complexes function in developmental gene activation and repression programmes. Nature 446:882-887. Cross Ref Medline
47. Wang Y, Zhang H, Chen Y, Sun Y, Yang F, Yu W, Liang J, Sun L, Yang X, Shi L, Li R, Li Y, Zhang Y, Li Q, Yi X, Shang Y (2009) LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell 138:660-672. Cross Ref Medline
48. Wilson S, Shafer B, Lee K, Dodd J (2008) A molecular program for contralateral trajectory: Rig-1 control by LIM homeodomain transcription factors. Neuron 59:413-424. Cross Ref Medline
49. Woodworth MB, Custo Greig L, Kriegstein AR, Macklis JD (2012) SnapShot: cortical development. Cell 151:918-918e1. Cross Ref Medline
50. Woodworth MB, Greig LC, Liu KX, Ippolito GC, Tucker HO, Macklis JD (2016) Ctip1 regulates the balance between specification of distinct projection neuron subtypes in deep cortical layers. Cell Rep 15:999-1012. Cross Ref Medline
51. Yang M, Gocke CB, Luo X, Borek D, Tomchick DR, Machius M, Otwinowski Z, Yu H (2006) Structural basis for CoREST-dependent demethylation of nucleosomes by the human LSD1 histone demethylase. Mol Cell 23: 377-387. Cross Ref Medline
52. Zembrzycki A, Perez-Garcia CG, Wang CF, Chou SJ, O’Leary DD (2015) Postmitotic regulation of sensory area patterning in the mammalian neocortex by Lhx2. Proc Natl Acad Sci U S A 112:6736-6741. Cross Ref Medline
53. Zimmer C, Tiveron MC, Bodmer R, Cremer H (2004) Dynamics of Cux2 expression suggests that an early pool of SVZ precursors is fated to become upper cortical layer neurons. Cereb Cortex 14:1408-1420. Cross Ref Medline