Analysis of Mll1 deficiency identifies neurogenic transcriptional modules and brn4 as a factor for direct astrocyte-to-neuron reprogramming

Neurosurgery

Volumn 75, Issue 4, 2014, Pages 472-482

  Potts, Matthew B ^a,b   Siu, Jason J ^a,b   Price, James D ^a,b   Salinas, Ryan D ^a,b   Cho, Mathew J ^a,b   Ramos, Alexander D ^a,b   Hahn, Junghyun ^c   Margeta, Marta ^c   Oldham, Michael C ^b,c   Lim, Daniel A ^a,b,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Astrocytes; Brn4 (pou3f4); Cell transdifferentiation; Epigenomics; Mll1; Neural stem cells; Neurogenesis

Indexed keywords

BRN4 PROTEIN; MIXED LINEAGE LEUKEMIA 1 PROTEIN; MIXED LINEAGE LEUKEMIA PROTEIN; OCTAMER TRANSCRIPTION FACTOR 6; UNCLASSIFIED DRUG; HISTONE LYSINE METHYLTRANSFERASE; MLL PROTEIN, MOUSE; NERVE PROTEIN; POU3F4 PROTEIN, MOUSE; TRANSCRIPTION FACTOR POU;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL TRANSDIFFERENTIATION; CONTROLLED STUDY; GENE OVEREXPRESSION; IMMUNOCYTOCHEMISTRY; MICROARRAY ANALYSIS; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEURAL STEM CELL; NONHUMAN; OLIGODENDROGLIA; PHENOTYPE; PRIORITY JOURNAL; SUBVENTRICULAR ZONE; WILD TYPE; ANIMAL; DEFICIENCY; PHYSIOLOGY;

ANIMALS; ASTROCYTES; CELL TRANSDIFFERENTIATION; HISTONE-LYSINE N-METHYLTRANSFERASE; MICE; MICROARRAY ANALYSIS; MYELOID-LYMPHOID LEUKEMIA PROTEIN; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; POU DOMAIN FACTORS;

EID: 84924084412     PISSN: 0148396X     EISSN: 15244040     Source Type: Journal    
DOI: 10.1227/NEU.0000000000000452     Document Type: Article

References (50)

1. Heins N, Malatesta P, Cecconi F, et al. Glial cells generate neurons: The role of the transcription factor Pax6. Nat Neurosci. 2002;5(4):308-315.
2. Hwang WW, Alvarez-Buylla A, Lim DA. Glial nature of adult neural stem cells: neurogenic competence in adult astrocytes. In: Rao MS, Carpenter M, Vemuri MC, eds. Neural Development and Stem Cells. 3rd ed. New York: Springer; 2012:149-172.
3. Heinrich C, Blum R, Gascón S, et al. Directing astroglia from the cerebral cortex into subtype specific functional neurons. PLoS Biol. 2010;8(5):e1000373.
4. Fuentealba LC, Obernier K, Alvarez-Buylla A. Adult neural stem cells bridge their niche. Cell Stem Cell. 2012;10(6):698-708.
5. Heinrich C, Gascón S, Masserdotti G, et al. Generation of subtype-specific neurons from postnatal astroglia of the mouse cerebral cortex. Nat Protoc. 2011;6 (2):214-228.
6. Corti S, Nizzardo M, Simone C, et al. Direct reprogramming of human astrocytes into neural stem cells and neurons. Exp Cell Res. 2012;318(13):1528-1541.
7. Kriegstein A, Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci. 2009;32:149-184.
8. Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G. Genome regulation by Polycomb and trithorax proteins. Cell 2007;128(4):735-745.
9. Zhang P, Bergamin E, Couture J-F. The many facets of MLL1 regulation. Biopolymers. 2013;99(2):136-145.
10. Lim DA, Huang YC, Swigut T, et al. Chromatin remodelling factor Mll1 is essential for neurogenesis from postnatal neural stem cells. Nature. 2009;458 (7237):529-533.
11. Berninger B, Costa MR, Koch U, et al. Functional Properties of neurons derived from in vitro reprogrammed postnatal astroglia. J Neurosci. 2007;27(32):8654-8664.
12. Niu W, Zang T, Zou Y, et al. In vivo reprogramming of astrocytes to neuroblasts in the adult brain. Nat Cell Biol. 2013;15(10):1164-1175.
13. Torper O, Pfisterer U, Wolf DA, et al. Generation of induced neurons via direct conversion in vivo. Proc Natl Acad Sci U S A. 2013;110(17):7038-7043.
14. Oldham MC, Horvath S, Geschwind DH. Conservation and evolution of gene coexpression networks in human and chimpanzee brains. Proc Natl Acad Sci U S A. 2006;103(47):17973-17978.
15. Horvath S, Dong J. Geometric interpretation of gene coexpression network analysis. PLoS Comput Biol. 2008;4(8):e1000117.
16. Oldham MC, Konopka G, Iwamoto K, et al. Functional organization of the transcriptome in human brain. Nat Neurosci. 2008;11(11):1271-1282.
17. Langfelder P, Horvath S. WGCNA: An R package for weighted correlation network analysis. BMC Bioinformatics. 2008;9:559.
18. Scheffler B. Phenotypic and functional characterization of adult brain neuropoiesis. Proc Natl Acad Sci U S A. 2005;102(26):9353-9358.
19. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 2003;31(4):e15.
20. Oldham MC, Langfelder P, Horvath S. Network methods for describing sample relationships in genomic datasets: Application to Huntington's disease. BMC Syst Biol. 2012;6:63.
21. Bachoo RM, Kim RS, Ligon KL, et al. Molecular diversity of astrocytes with implications for neurological disorders. Proc Natl Acad Sci U S A. 2004;101(22): 8384-8389.
22. Nielsen JA, Maric D, Lau P, Barker JL, Hudson LD. Identification of a novel oligodendrocyte cell adhesion protein using gene expression profiling. J Neurosci. 2006;26(39):9881-9891.
23. Cahoy JD, Emery B, Kaushal A, et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: A new resource for understanding brain development and function. J Neurosci. 2008;28(1):264-278.
24. Doyle JP, Dougherty JD, Heiman M, et al. Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell. 2008;135(4):749-762.
25. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981;391(2):85-100.
26. Lim DA, Huang Y-C, Alvarez-Buylla A. Adult subventricular zone and olfactory bulb neurogenesis. In: Gage FH, Kempermann G, Song H, eds. Adult Neurogenesis. New York: Cold Spring Harbor Laboratory Press; 2008:175-206.
27. Ming GL, Song H. Adult neurogenesis in the mammalian brain: Significant answers and significant questions. Neuron. 2011;70(4):687-702.
28. Benner EJ, Luciano D, Jo R, et al. Protective astrogenesis from the SVZ niche after injury is controlled by Notch modulator Thbs4. Nature. 2013;497(7449):369-373.
29. Menn B. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci. 2006;26(30):7907-7918.
30. Picard-Riera N, Decker L, Delarasse C, et al. Experimental autoimmune encephalomyelitis mobilizes neural progenitors from the subventricular zone to undergo oligodendrogenesis in adult mice. Proc Natl Acad Sci U S A. 2002;99(20): 13211-13216.
31. Nait-Oumesmar B, Decker L, Lachapelle F, Avellana-Adalid V, Bachelin C, Baron-Van Evercooren A. Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur J Neurosci. 1999;11(12):4357-4366.
32. Merkle FT, Mirzadeh Z, Alvarez-Buylla A. Mosaic organization of neural stem cells in the adult brain. Science. 2007;317(5836):381-384.
33. Long JE, Garel S, Álvarez-Dolado M, et al. Dlx-dependent and -independent regulation of olfactory bulb interneuron differentiation. J Neurosci. 2007;27(12): 3230-3243.
34. Allen ZJ II, Waclaw RR, Colbert MC, Campbell K. Molecular identity of olfactory bulb interneurons: Transcriptional codes of periglomerular neuron subtypes. J Mol Histol. 2007;38(6):517-525.
35. Panganiban G, Rubenstein JL. Developmental functions of the Distal-less/Dlx homeobox genes. Development. 2002;129(19):4371-4386.
36. Colasante G, Collombat P, Raimondi V, et al. Arx is a direct target of Dlx2 and thereby contributes to the tangential migration of GABAergic interneurons. J Neurosci. 2008;28(42):10674-10686.
37. Shi Y, Chichung Lie D, Taupin P, et al. Expression and function of orphan nuclear receptor TLX in adult neural stem cells. Nature. 2004;427(6969):78-83.
38. Ninkovic J, Steiner-Mezzadri A, Jawerka M, et al. The BAF complex interacts with Pax6 in adult neural progenitors to establish a neurogenic cross-regulatory transcriptional network. Cell Stem Cell. 2013;13(4):403-418.
39. Jones WD, Dafou D, McEntagart M, et al. De novo mutations in MLL cause Wiedemann-Steiner syndrome. Am J Hum Genet. 2012;91(2):358-364.
40. Liu H-K, Wang Y, Belz T, et al. The nuclear receptor tailless induces long-term neural stem cell expansion and brain tumor initiation. Genes Dev. 2010;24(7):683-695.
41. Tian L, McClafferty H, Knaus HG, Ruth P, Shipston MJ. Distinct acyl protein transferases and thioesterases control surface expression of calcium-activated potassium channels. J Biol Chem. 2012;287(18):14718-14725.
42. Saitoh F, Tian QB, Okano A, Sakagami H, Kondo H, Suzuki T. NIDD, a novel DHHC-containing protein, targets neuronal nitric-oxide synthase (nNOS) to the synaptic membrane through a PDZ-dependent interaction and regulates nNOS activity. J Biol Chem. 2004;279(28):29461-29468.
43. Phippard D, Lu L, Lee D, Saunders JC, Crenshaw EB III. Targeted mutagenesis of the POU-domain gene Brn4/Pou3f4 causes developmental defects in the inner ear. J Neurosci. 1999;19(14):5980-5989.
44. Mathis JM, Simmons DM, He X, Swanson LW, Rosenfeld MG. Brain 4: A novel mammalian POU domain transcription factor exhibiting restricted brain-specific expression. EMBO J. 1992;11(7):2551-2561.
45. Parras CM, Galli R, Britz O, et al. Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J. 2004;23(22):4495-4505.
46. Wapinski OL, Vierbuchen T, Qu K, et al. Hierarchical mechanisms for direct reprogramming of fibroblasts to neurons. Cell. 2013;155(3):621-635.
47. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131(5):861-872.
48. Yu J, Vodyanik MA, Smuga-Otto K, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007;318(5858):1917-1920.
49. Park IH, Zhao R, West JA, et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature. 2008;451(7175):141-146.
50. Gonzales-Roybal G, Lim DA. Chromatin-based epigenetics of adult subventricular zone neural stem cells. Front Genet. 2013;4:194.