Molecular Identity of Human Outer Radial Glia during Cortical Development

Cell

Volumn 163, Issue 1, 2015, Pages 55-67

  Pollen, Alex A ^a,b   Nowakowski, Tomasz J ^a,b   Chen, Jiadong ^a,b   Retallack, Hanna ^a,b   Sandoval Espinosa, Carmen ^a,b   Nicholas, Cory R ^a   Shuga, Joe ^c   Liu, Siyuan John ^a,b   Oldham, Michael C ^a   Diaz, Aaron ^a   Lim, Daniel A ^a   Leyrat, Anne A ^c   West, Jay A ^c   Kriegstein, Arnold R ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c FLUIDIGM CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH FACTOR; SCLEROPROTEIN; STAT3 PROTEIN;

ANIMAL CELL; ARTICLE; BRAIN DEVELOPMENT; CELL CYCLE PROGRESSION; CELL EXPANSION; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CELL RENEWAL; CLONING; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE EXPRESSION; GLIA; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL NICHE; SUBVENTRICULAR ZONE; ANIMAL; CELL CYCLE; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; MACACA; METABOLISM; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; SINGLE CELL ANALYSIS;

ANIMALS; CELL CYCLE; HUMANS; MACACA; MICE; NEOCORTEX; NEURAL STEM CELLS; NEUROGENESIS; NEUROGLIA; SIGNAL TRANSDUCTION; SINGLE-CELL ANALYSIS; STAT3 TRANSCRIPTION FACTOR; STEM CELL NICHE;

EID: 84948457494     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.09.004     Document Type: Article

References (52)

1. F. Autelitano, D. Loyaux, S. Roudières, C. Déon, F. Guette, P. Fabre, Q. Ping, S. Wang, R. Auvergne, V. Badarinarayana, and et al. Identification of novel tumor-associated cell surface sialoglycoproteins in human glioblastoma tumors using quantitative proteomics PLoS ONE 9 2014 e110316
2. C.S. Barros, S.J. Franco, and U. Müller Extracellular matrix: functions in the nervous system Cold Spring Harb. Perspect. Biol. 3 2011 a005108
3. N. Bayatti, J.A. Moss, L. Sun, P. Ambrose, J.F. Ward, S. Lindsay, and G.J. Clowry A molecular neuroanatomical study of the developing human neocortex from 8 to 17 postconceptional weeks revealing the early differentiation of the subplate and subventricular zone Cereb. Cortex 18 2008 1536 1548
4. C. Beadle, M.C. Assanah, P. Monzo, R. Vallee, S.S. Rosenfeld, and P. Canoll The role of myosin II in glioma invasion of the brain Mol. Biol. Cell 19 2008 3357 3368
5. M. Besser, M. Jagatheaswaran, J. Reinhard, P. Schaffelke, and A. Faissner Tenascin C regulates proliferation and differentiation processes during embryonic retinogenesis and modulates the de-differentiation capacity of Müller glia by influencing growth factor responsiveness and the extracellular matrix compartment Dev. Biol. 369 2012 163 176
6. M. Betizeau, V. Cortay, D. Patti, S. Pfister, E. Gautier, A. Bellemin-Ménard, M. Afanassieff, C. Huissoud, R.J. Douglas, H. Kennedy, and C. Dehay Precursor diversity and complexity of lineage relationships in the outer subventricular zone of the primate Neuron 80 2013 442 457
7. A. Bianchi, M.E. Gervasi, and A. Bakin Role of β5-integrin in epithelial-mesenchymal transition in response to TGF-β Cell Cycle 9 2010 1647 1659
8. M.A. Bonaguidi, T. McGuire, M. Hu, L. Kan, J. Samanta, and J.A. Kessler LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells Development 132 2005 5503 5514
9. M.A. Bonaguidi, C.Y. Peng, T. McGuire, G. Falciglia, K.T. Gobeske, C. Czeisler, and J.A. Kessler Noggin expands neural stem cells in the adult hippocampus J. Neurosci. 28 2008 9194 9204
10. J.D. Cahoy, B. Emery, A. Kaushal, L.C. Foo, J.L. Zamanian, K.S. Christopherson, Y. Xing, J.L. Lubischer, P.A. Krieg, S.A. Krupenko, and et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function J. Neurosci. 28 2008 264 278
11. S.A. Fietz, I. Kelava, J. Vogt, M. Wilsch-Bräuninger, D. Stenzel, J.L. Fish, D. Corbeil, A. Riehn, W. Distler, R. Nitsch, and W.B. Huttner OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling Nat. Neurosci. 13 2010 690 699
12. S.A. Fietz, R. Lachmann, H. Brandl, M. Kircher, N. Samusik, R. Schröder, N. Lakshmanaperumal, I. Henry, J. Vogt, A. Riehn, and et al. Transcriptomes of germinal zones of human and mouse fetal neocortex suggest a role of extracellular matrix in progenitor self-renewal Proc. Natl. Acad. Sci. USA 109 2012 11836 11841
13. M. Florio, M. Albert, E. Taverna, T. Namba, H. Brandl, E. Lewitus, C. Haffner, A. Sykes, F.K. Wong, J. Peters, and et al. Human-specific gene ARHGAP11B promotes basal progenitor amplification and neocortex expansion Science 347 2015 1465 1470
14. P. Gao, M.P. Postiglione, T.G. Krieger, L. Hernandez, C. Wang, Z. Han, C. Streicher, E. Papusheva, R. Insolera, K. Chugh, and et al. Deterministic progenitor behavior and unitary production of neurons in the neocortex Cell 159 2014 775 788
15. E. Garcion, A. Halilagic, A. Faissner, and C. ffrench-Constant Generation of an environmental niche for neural stem cell development by the extracellular matrix molecule tenascin C Development 131 2004 3423 3432
16. J. Garwood, E. Garcion, A. Dobbertin, N. Heck, V. Calco, C. ffrench-Constant, and A. Faissner The extracellular matrix glycoprotein Tenascin-C is expressed by oligodendrocyte precursor cells and required for the regulation of maturation rate, survival and responsiveness to platelet-derived growth factor Eur. J. Neurosci. 20 2004 2524 2540
17. C.C. Gertz, J.H. Lui, B.E. LaMonica, X. Wang, and A.R. Kriegstein Diverse behaviors of outer radial glia in developing ferret and human cortex J. Neurosci. 34 2014 2559 2570
18. M. Götz, A. Stoykova, and P. Gruss Pax6 controls radial glia differentiation in the cerebral cortex Neuron 21 1998 1031 1044
19. D.V. Hansen, J.H. Lui, P.R. Parker, and A.R. Kriegstein Neurogenic radial glia in the outer subventricular zone of human neocortex Nature 464 2010 554 561
20. R.F. Hevner, R.D. Hodge, R.A. Daza, and C. Englund Transcription factors in glutamatergic neurogenesis: conserved programs in neocortex, cerebellum, and adult hippocampus Neurosci. Res. 55 2006 223 233
21. S. Hong, and M.R. Song Signal transducer and activator of transcription-3 maintains the stemness of radial glia at mid-neurogenesis J. Neurosci. 35 2015 1011 1023
22. G. Huang, H. Yan, S. Ye, C. Tong, and Q.L. Ying STAT3 phosphorylation at tyrosine 705 and serine 727 differentially regulates mouse ESC fates Stem Cells 32 2014 1149 1160
23. Y. Itoh, Y. Moriyama, T. Hasegawa, T.A. Endo, T. Toyoda, and Y. Gotoh Scratch regulates neuronal migration onset via an epithelial-mesenchymal transition-like mechanism Nat. Neurosci. 16 2013 416 425
24. M.B. Johnson, P.P. Wang, K.D. Atabay, E.A. Murphy, R.N. Doan, J.L. Hecht, and C.A. Walsh Single-cell analysis reveals transcriptional heterogeneity of neural progenitors in human cortex Nat. Neurosci. 18 2015 637 646
25. D. Katoh, K. Nagaharu, N. Shimojo, N. Hanamura, M. Yamashita, Y. Kozuka, K. Imanaka-Yoshida, and T. Yoshida Binding of αvβ1 and αvβ6 integrins to tenascin-C induces epithelial-mesenchymal transition-like change of breast cancer cells Oncogenesis 2 2013 e65
26. A. Kawaguchi, T. Ikawa, T. Kasukawa, H.R. Ueda, K. Kurimoto, M. Saitou, and F. Matsuzaki Single-cell gene profiling defines differential progenitor subclasses in mammalian neurogenesis Development 135 2008 3113 3124
27. D. Kyuno, T. Kojima, H. Yamaguchi, T. Ito, Y. Kimura, M. Imamura, A. Takasawa, M. Murata, S. Tanaka, K. Hirata, and N. Sawada Protein kinase Cα inhibitor protects against downregulation of claudin-1 during epithelial-mesenchymal transition of pancreatic cancer Carcinogenesis 34 2013 1232 1243
28. P.U. Le, A. Angers-Loustau, R.M. de Oliveira, A. Ajlan, C.L. Brassard, A. Dudley, H. Brent, V. Siu, G. Trinh, G. Mölenkamp, and et al. DRR drives brain cancer invasion by regulating cytoskeletal-focal adhesion dynamics Oncogene 29 2010 4636 4647
29. M.K. Lehtinen, M.W. Zappaterra, X. Chen, Y.J. Yang, A.D. Hill, M. Lun, T. Maynard, D. Gonzalez, S. Kim, P. Ye, and et al. The cerebrospinal fluid provides a proliferative niche for neural progenitor cells Neuron 69 2011 893 905
30. E. Lewitus, I. Kelava, and W.B. Huttner Conical expansion of the outer subventricular zone and the role of neocortical folding in evolution and development Front. Hum. Neurosci. 7 2013 424
31. D.A. Lim, A.D. Tramontin, J.M. Trevejo, D.G. Herrera, J.M. García-Verdugo, and A. Alvarez-Buylla Noggin antagonizes BMP signaling to create a niche for adult neurogenesis Neuron 28 2000 713 726
32. J.H. Lui, T.J. Nowakowski, A.A. Pollen, A. Javaherian, A.R. Kriegstein, and M.C. Oldham Radial glia require PDGFD-PDGFRβ signalling in human but not mouse neocortex Nature 515 2014 264 268
33. V. Martínez-Cerdeño, C.L. Cunningham, J. Camacho, J.L. Antczak, A.N. Prakash, M.E. Cziep, A.I. Walker, and S.C. Noctor Comparative analysis of the subventricular zone in rat, ferret and macaque: evidence for an outer subventricular zone in rodents PLoS ONE 7 2012 e30178
34. P. Milev, H. Monnerie, S. Popp, R.K. Margolis, and R.U. Margolis The core protein of the chondroitin sulfate proteoglycan phosphacan is a high-affinity ligand of fibroblast growth factor-2 and potentiates its mitogenic activity J. Biol. Chem. 273 1998 21439 21442
35. J.A. Miller, S.L. Ding, S.M. Sunkin, K.A. Smith, L. Ng, A. Szafer, A. Ebbert, Z.L. Riley, J.J. Royall, K. Aiona, and et al. Transcriptional landscape of the prenatal human brain Nature 508 2014 199 206
36. S. Nie, M. Gurrea, J. Zhu, S. Thakolwiboon, J.A. Heth, K.M. Muraszko, X. Fan, and D.M. Lubman Tenascin-C: a novel candidate marker for cancer stem cells in glioblastoma identified by tissue microarrays J. Proteome Res. 14 2015 814 822
37. B.E. Ostrem, J.H. Lui, C.C. Gertz, and A.R. Kriegstein Control of outer radial glial stem cell mitosis in the human brain Cell Rep. 8 2014 656 664
38. A.P. Patel, I. Tirosh, J.J. Trombetta, A.K. Shalek, S.M. Gillespie, H. Wakimoto, D.P. Cahill, B.V. Nahed, W.T. Curry, R.L. Martuza, and et al. Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma Science 344 2014 1396 1401
39. P. Perez-Pinera, S. Alcantara, T. Dimitrov, J.A. Vega, and T.F. Deuel Pleiotrophin disrupts calcium-dependent homophilic cell-cell adhesion and initiates an epithelial-mesenchymal transition Proc. Natl. Acad. Sci. USA 103 2006 17795 17800
40. A.A. Pollen, T.J. Nowakowski, J. Shuga, X. Wang, A.A. Leyrat, J.H. Lui, N. Li, L. Szpankowski, B. Fowler, P. Chen, and et al. Low-coverage single-cell mRNA sequencing reveals cellular heterogeneity and activated signaling pathways in developing cerebral cortex Nat. Biotechnol. 32 2014 1053 1058
41. X. Qian, Q. Shen, S.K. Goderie, W. He, A. Capela, A.A. Davis, and S. Temple Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells Neuron 28 2000 69 80
42. I. Reillo, C. de Juan Romero, M.A. García-Cabezas, and V. Borrell A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex Cereb. Cortex 21 2011 1674 1694
43. A. Shitamukai, D. Konno, and F. Matsuzaki Oblique radial glial divisions in the developing mouse neocortex induce self-renewing progenitors outside the germinal zone that resemble primate outer subventricular zone progenitors J. Neurosci. 31 2011 3683 3695
44. F.J. Sim, J.K. Lang, B. Waldau, N.S. Roy, T.E. Schwartz, W.H. Pilcher, K.J. Chandross, S. Natesan, J.E. Merrill, and S.A. Goldman Complementary patterns of gene expression by human oligodendrocyte progenitors and their environment predict determinants of progenitor maintenance and differentiation Ann. Neurol. 59 2006 763 779
45. I.H. Smart, C. Dehay, P. Giroud, M. Berland, and H. Kennedy Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey Cereb. Cortex 12 2002 37 53
46. D. Szklarczyk, A. Franceschini, S. Wyder, K. Forslund, D. Heller, J. Huerta-Cepas, M. Simonovic, A. Roth, A. Santos, K.P. Tsafou, and et al. STRING v10: protein-protein interaction networks, integrated over the tree of life Nucleic Acids Res. 43 2015 D447 D452
47. N.A. Vasistha, F. Garcia-Moreno, S. Arora, A.F. Cheung, S.J. Arnold, E.J. Robertson, and Z. Molnar Cortical and clonal contribution of Tbr2 expressing progenitors in the developing mouse brain Cereb. Cortex 2014 10.1093/cercor/bhu125 Published online June 13, 2014
48. A. von Holst Tenascin C in stem cell niches: redundant, permissive or instructive? Cells Tissues Organs (Print) 188 2008 170 177
49. W.Z. Wang, F.M. Oeschger, J.F. Montiel, F. García-Moreno, A. Hoerder-Suabedissen, L. Krubitzer, C.J. Ek, N.R. Saunders, K. Reim, A. Villalón, and Z. Molnár Comparative aspects of subplate zone studied with gene expression in sauropsids and mammals Cereb. Cortex 21 2011 2187 2203
50. X. Wang, J.W. Tsai, B. LaMonica, and A.R. Kriegstein A new subtype of progenitor cell in the mouse embryonic neocortex Nat. Neurosci. 14 2011 555 561
51. S. Wiese, M. Karus, and A. Faissner Astrocytes as a source for extracellular matrix molecules and cytokines Front. Pharmacol. 3 2012 120
52. N. Zecevic, Y. Chen, and R. Filipovic Contributions of cortical subventricular zone to the development of the human cerebral cortex J. Comp. Neurol. 491 2005 109 122