Non-immortalized human neural stem (NS) cells as a scalable platform for cellular assays

Neurochemistry International

Volumn 59, Issue 3, 2011, Pages 432-444

  Hook, Lilian ^a,e   Vives, Joaquim ^a,f   Fulton, Norma ^a,g   Leveridge, Mathew ^a   Lingard, Sarah ^a   Bootman, Martin D ^d   Falk, Anna ^c   Pollard, Steven M ^c,h   Allsopp, Timothy E ^a,i   Dalma Weiszhausz, Dennise ^b   Tsukamoto, Ann ^b   Uchida, Nobuko ^b   Gorba, Thorsten ^a,b  

^a Stem Cell Sciences UK Ltd   (United Kingdom)

^b StemCells Inc   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d BABRAHAM INSTITUTE   (United Kingdom)

^e Plasticell Limited   (United Kingdom)

^f BANC DE SANG I TEIXITS   (Spain)

^g EDINBURGH NAPIER UNIVERSITY   (United Kingdom)

^h UNIVERSITY COLLEGE LONDON   (United Kingdom)

ⁱ Neusentis Ltd   (United Kingdom)

Author keywords

Automation; Chemical and genetic screens; Neural stem cells; Neurogenic radial glia; Neuronal maturation; Positional identity; Prospective isolation

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CELL ASSAY; CELL ISOLATION; DIAGNOSTIC VALUE; FETUS; GENE FUNCTION; GENETIC ENGINEERING; HUMAN; HUMAN CELL; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL TRANSPLANTATION; VALIDATION STUDY;

ANIMALS; CELL ADHESION; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED NOD; MICE, SCID; NEURONS; POLYMERASE CHAIN REACTION; STEM CELL TRANSPLANTATION; STEM CELLS;

ANIMALIA;

EID: 80051546467     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2011.06.024     Document Type: Article

References (65)

1. A. Alvares-Buylla, J.M. Garcia-Verdugo, and A.D. Tramontin A unified hypothesis on the lineage of neural stem cells Nat. Rev. Neurosci. 2 2001 287 293 (Pubitemid 33673069)
2. S.A. Anderson, M. Qiu, and A. Bulfone Mutations of the homeobox genes Dlx1 and Dlx2 disrupt the striatal subventricular zone and differentiation of late-born striatal neurons Neuron 19 1997 27 37 (Pubitemid 27332991)
3. T.E. Anthony, C. Klein, and G. Fishell Radial glia serve as neuronal progenitors in all regions of the central nervous system Neuron 41 2004 881 890 (Pubitemid 38429732)
4. R. Batista-Brito, E. Rossignol, and J. Hjerling-Leffler The cell-intrinsic requirement of Sox6 for cortical interneuron development Neuron 63 2009 466 481
5. S.A. Bayer, and J. Altman The Human Brain During the Late First Trimester vol. 4 2006 CRC Press/Taylor & Francis Group Boca Raton
6. G. Biella, F. Di Febo, and D. Goffredo Differentiating embryonic stem-derived neural stem cells show a maturation-dependent pattern of voltage-gated sodium current expression and graded action potentials Neuroscience 149 2007 38 52 (Pubitemid 47488659)
7. J.M. Breier, N.M. Radio, and W.R. Mundy Development of a high-throughput screening assay for chemical effects on proliferation and viability of immortalized human neural progenitor cells Toxicol. Sci. 105 2008 119 133
8. L.S. Campos Neurospheres: insights into neural stem cell biology J. Neurosci. Res. 78 2004 761 769 (Pubitemid 39657564)
9. A. Capela, and S. Temple LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal Neuron 35 2002 865 875
10. A. Capela, Y. Jacobs, and X. Xie Use of lentiviral vectors for lineage specific labelling of human central nervous system stem cells (hCNS-SC) transplanted into the rodent brain 37th Annual Meeting San Diego Soc. Neurosci. 2007
11. E.M. Chan, S. Ratanasirintrawoot, and I.-H. Park Live cell imaging distinguishes bona fide human iPS cells from partially reprogrammed cells Nat. Biotechnol. 27 2009 1033 1037
12. L. Conti, S.M. Pollard, and T. Gorba Niche-independent symmetrical self-renewal of a mammalian tissue stem cell PLoS Biol. 3 2005 e283
13. I.C.W. Cromley, and S. Fox Growing market for high content analysis tools DDW 5 2004 25 34
14. B.J. Cummings, N. Uchida, and S.J. Tamaki Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice Proc. Natl. Acad. Sci. U.S.A. 102 2005 14069 14074 (Pubitemid 41377704)
15. D. Danovi, A. Falk, and P. Humphreys Imaging-based chemical screens using normal and glioma-derived neural stem cells Biochem. Soc. Trans. 38 2010 1067 1071
16. M. Davenne, M.K. Maconochie, and R. Neun Hoxa2 and Hoxb2 control dorsoventral patterns of neuronal development in the rostral hindbrain Neuron 22 1999 677 691 (Pubitemid 29203492)
17. G. Elkabetz, G. Panagiotakos, and Al Shamy Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell state Genes Dev. 22 2008 152 165
18. F.H. Gage, P.W. Coates, and T.D. Palmer Survival and differentiation of adult neural progenitor cells transplanted to the adult brain Proc. Natl. Acad. Sci. U.S.A. 92 1995 11879 11883 (Pubitemid 26014213)
19. T. Glaser, S.M. Pollard, A. Smith, and O. Brüstle Tripotential differentiation of adherently expandable neural stem (NS) cells PLoS One 2 2007 e298
20. D. Goffredo, L. Conti, and F. Di Febo Setting the conditions for efficient, robust and reproducible generation of functionally active neurons from adult subventricular zone-derived neural stem cells Cell Death Differ. 15 2008 1847 1856
21. J.L. Gomez-Skarmeta, and J. Modollel Iroquois genes: genomic organization and function in vertebrate neural development Curr. Opin. Gen. Dev. 12 2002 403 408 (Pubitemid 34722918)
22. Gorba, T., McLaren, D., Mamam, S., et al., 2010. Validation of adherent, non-immortalized mouse and human neural stem cell technology for scale-up, automated culture and high-throughput screening in a cell proliferation/ viability assay. In: ISSCR 8th Annual Meeting, San Francisco. Available from: http://www.stemcellsinc.com/Science/Publications.htm.
23. M. Götz, and W.B. Huttner The cell biology of neurogenesis Nat. Rev. Mol. Cell. Biol. 6 2005 777 788 (Pubitemid 41726116)
24. R. Guzman, N. Uchida, and T.M. Bliss Long-term monitoring of transplanted human neural stem cells in developmental and pathological context with MRI Proc. Natl. Acad. Sci. U.S.A. 104 2007 10211 10216 (Pubitemid 47175288)
25. D.V. Hansen, J.H. Lui, R.L.P. Parker, and A.R. Kriegstein Neurogenic radial glia in the outer subventricular zone of human neocortex Nature 464 2010 554 561
26. S. Horiguchi, J. Takahashi, and J. Kishi Neural precursor cells derived from human embryonic brain retain regional specificity J. Neurosci. Res. 75 2004 817 824 (Pubitemid 38296094)
27. M.J. Hooshmand, C.J. Sontag, and N. Uchida Analysis of host-mediated repair mechanisms after human CNS-stem cell transplantation for spinal cord injury: correlation of engraftment with recovery PLoS One 4 2009 e5871
28. A.L. Joyner Engrailed, Wnt and Pax genes regulate midbrain-hindbrain development Trends Genet. 12 1996 15 20 (Pubitemid 26031160)
29. M.S. Kallos, A. Sen, and L.A. Behie Large-scale expansion of mammalian neural stem cells: a review Med. Biol. Eng. Comp. 14 2003 271 282 (Pubitemid 36701030)
30. S. Kelly, T.M. Bliss, and A.K. Shah Transplanted human fetal neural stem cells survive, migrate and differentiate in ischemic rat cerebral cortex Proc. Natl. Acad. Sci. U.S.A. 101 2004 11839 11844 (Pubitemid 39095381)
31. J. Kemp, and R. McKernan NMDA receptor pathways as drug targets Nat. Neurosci. 5 2002 1039 1042 (Pubitemid 35247194)
32. H.T. Kim, I.S. Kim, and I.S. Lee Human neurospheres derived from the fetal central nervous system are regionally and temporally specified but are not committed Exp. Neurol. 199 2006 222 235
33. J. Kimura, Y. Suda, and D. Kurokawa Emx2 and Pax6 function in cooperation with Otx2 and Otx1 to develop caudal forebrain epithelium that includes future archipallium J. Neurosci. 25 2005 5097 5108 (Pubitemid 40726963)
34. P. Koch, T. Opitz, and J.A. Steinbeck A rosette-type, self-renewing human ES cell-derived neural stem cell with potential for in vitro instruction and synaptic integration Proc. Natl. Acad. Sci. U.S.A. 106 2009 3225 3230
35. H. Li, J.C. Radford, and M.J. Ragusa Transcription factor MEF2C influences neural stem/progenitor cell differentiation and maturation in vivo Proc. Natl. Acad. Sci. U.S.A. 105 2008 9397 9402
36. P. Malatesta, E. Hartfuss, and M. Götz Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage Development 127 2000 5253 5263 (Pubitemid 32049182)
37. P. Malatesta, M.A. Hack, and E. Hartfuss Neuronal or glial progeny: regional differences in radial glial fate Neuron 37 2003 751 764 (Pubitemid 36288548)
38. M. Monotoute, M. Fisher, and S. Lin GSK, application of cell culture automation for cell-based HTS using SelecT Proc. Eur. Soc. Animal Cell Technol. 2003
39. T. Miyata, A. Kawaguchi, and H. Okano Assymetric inheritance of radial glial fibers by cortical neurons Neuron 31 2001 727 741 (Pubitemid 32907370)
40. S.C. Noctor, A.C. Flint, and T.A. Weissman Neurons derived from radial glial cells establish radial units in neocortex Nature 409 2001 714 720 (Pubitemid 32144516)
41. M. Onorati, S. Cammasio, and M. Binetti Neuropotent self-renewing neural stem (NS) cells derived from mouse induced pluripotent stem (iPS) cells Mol. Cell. Neurosci. 43 2010 287 295
42. M. Onorati, M. Binetti, and L. Conti Preservation of positional identity in fetus-derived neural stem cells from different mouse central nervous system compartments Cell. Mol. Life Sci. 2010 10.1007/s00018-010-0548-7
43. Polkingthorne Report Review of the Guidance on the Research Use of Fetuses and Fetal Material 1989 HMSO London
44. S. Pollard, L. Conti, and A. Smith Exploitation of adherent neural stem cells in basic and applied neurobiology Regen. Med. 1 2006 111 118
45. S.M. Pollard, L. Conti, and Y. Sun Adherent neural stem (NS) cells from fetal and adult forebrain Cereb. Cortex 16 Suppl 1 2006 i112 i120
46. S.M. Pollard, and L. Conti Investigating radial glia in vitro Prog. Neurobiol. 83 2007 53 67 (Pubitemid 47239229)
47. S.M. Pollard, R. Wallbank, and S. Tomlinson Fibroblast growth factor induces a neural stem cell phenotype in foetal forebrain progenitors and during embryonic stem cell differentiation Mol. Cell. Neurosci. 38 2008 393 403
48. K. Pollock, P. Stroemer, and S. Patel A conditionally immortal clonal stem cell line from human cortical neuroepithelium for the treatment of ischemic stroke Exp. Neurol. 199 2006 143 155 (Pubitemid 43959830)
49. P. Rakic Guidance of neurons migrating to the fetal monkey neocortex Brain Res. 33 1971 471 476
50. J. Ray, H.K. Raymon, and F.H. Gage Generation and culturing of precursor cells from embryonic and adult central nervous system Methods Enzymol. 254 1995 20 37
51. B.A. Reynolds, W. Tetzlaff, and S. Weiss A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes J. Neurosci. 12 1992 4565 4574
52. B.A. Reynolds, and S. Weiss Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system Science 255 1992 1707 1710
53. B.A. Reynolds, and R.L. Rietze Neural stem cells and neurospheres: re-evaluating the relationship Nat. Methods 2 2005 333 336 (Pubitemid 41130977)
54. D.L. Salazar, N. Uchida, and F.P.T. Hamers Human neural stem cells differentiate and promote locomotor recovery in an early chronic spinal cord injury NOD-scid mouse model PLoS One 5 2010 e12272
55. C.D. Stern Initial patterning of the central nervous system: how many organizers? Nat. Rev. Neurosci. 2 2001 92 98 (Pubitemid 33673363)
56. Y. Sun, S. Pollard, and L. Conti Long-term tripotent differentiation capacity of human neural stem (NS) cells in adherent culture Mol. Cell. Neurosci. 38 2008 245 258
57. C.N. Svendsen, M.G. ter Borg, and R.J. Armstrong A new method for the rapid and long term growth of human neural precursor cells J. Neurosci. Methods 85 1998 141 152 (Pubitemid 29003064)
58. S. Tamaki, K. Eckert, and D. He Engraftment of sorted/expanded human central nervous system stem cells from fetal brain J. Neurosci. Res. 69 2002 976 986 (Pubitemid 34984715)
59. S.J. Tamaki, Y. Jacobs, and M. Dohse Neuroprotection of host cells by human cental nervous system stem cells in a mouse model of infantile neuronal ceroid lipofuscinosis Cell Stem Cell 5 2009 310 319
60. W. Tao, and E. Lai Telencephalon restricted expression of BF-1, a new member of the HNF-2/fork head gene family, in the developing rat brain Neuron 8 1992 957 966
61. R. Torp, F. Hoover, and N.C. Danbolt Differential distribution of the glutamte transporters GLT1 and rEAAC1 in rat cerebral cortex and thalamus: an in situ hybridization analysis Anat. Embryol. 195 1997 317 326 (Pubitemid 27156255)
62. N. Uchida, D.W. Buck, and D. He Direct isolation of human central nervous system stem cells Proc. Natl. Acad. Sci. U.S.A. 97 2000 14720 14725 (Pubitemid 32016642)
63. A.L. Vescovi, E.A. Parati, and A. Gritti Isolation and cloning of multipotential stem cells from the embryonic human CNS and establishment of transplantable human neural stem cell lines by epigenetic stimulation Exp. Neurol. 156 1999 71 83 (Pubitemid 29152984)
64. S. Weiss, C. Dunne, and J. Hewson Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis J. Neurosci. 16 1996 7599 7609 (Pubitemid 26389699)
65. Q.-L. Ying, J. Wray, and J. Nichols The ground state of embryonic stem cell self-renewal Nature 453 2008 519 523 (Pubitemid 351733324)