Efficient neuronal in vitro and in vivo differentiation after immunomagnetic purification of mESC derived neuronal precursors

Stem Cell Research

Volumn 10, Issue 2, 2013, Pages 133-146

  Barral, Serena ^a,c   Ecklebe, Josephine ^a   Tomiuk, Stefan ^a   Tiveron, Marie Catherine ^b,c   Desoeuvre, Angélique ^b,d   Eckardt, Dominik ^a   Cremer, Harold ^b,e   Bosio, Andreas ^a  

^a MILTENYI BIOTEC GMBH   (Germany)

^b CNRS   (France)

^c AIX MARSEILLE UNIVERSITÉ   (France)

^d UNIVERSITÉ DE MONTPELLIER   (France)

^e 7288 Campus Universitaire et Technologique de Luminy ^*  (France)

Author keywords

[No Author keywords available]

Indexed keywords

NERVE CELL ADHESION MOLECULE; POLYSIALYLATED ACID; SIALOPROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ISOLATION; CELLULAR DIVERSITY; CELLULAR PARAMETERS; CONTROLLED STUDY; EMBRYONIC STEM CELL; FLOW CYTOMETRY; FOREBRAIN; GENE EXPRESSION; GENETIC ANALYSIS; GLIA CELL; IMMUNOCYTOCHEMISTRY; IMMUNOMAGNETIC PURIFICATION; IN VITRO STUDY; IN VIVO STUDY; MICROARRAY ANALYSIS; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; OLFACTORY BULB; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PURIFICATION;

ACTINS; ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL SURVIVAL; EMBRYONIC STEM CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; IMMUNOMAGNETIC SEPARATION; MICE; MICE, INBRED C57BL; NEURAL CELL ADHESION MOLECULE L1; NEURAL STEM CELLS; NEURONS; SIALIC ACIDS; STEM CELL TRANSPLANTATION;

MUS;

EID: 84870935929     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2012.10.005     Document Type: Article

References (53)

1. Angata K., Fukuda M. Polysialyltransferases: major players in polysialic acid synthesis on the neural cell adhesion molecule. Biochimie 2003, 85(1-2):195-206.
2. Ben-Hur T., Rogister B., Murray K., Rougon G., Dubois-Dalcq M. Growth and fate of PSA-NCAM+ precursors of the postnatal brain. J. Neurosci. 1998, 18(15):5777-5788.
3. Bjorklund L.M., Sanchez-Pernaute R., Chung S., Andersson T., Chen I.Y., McNaught K.S., Isacson O. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc. Natl. Acad. Sci. U. S. A. 2002, 99(4):2344-2349.
4. Bonfanti L. PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog. Neurobiol. 2006, 80(3):129-164.
5. Bonfanti L., Theodosis D.T. Expression of polysialylated neural cell adhesion molecule by proliferating cells in the subependymal layer of the adult rat, in its rostral extension and in the olfactory bulb. Neuroscience 1994, 62(1):291-305.
6. Bonfanti L., Merighi A., Theodosis D.T. Dorsal rhizotomy induces transient expression of the highly sialylated isoform of the neural cell adhesion molecule in neurons and astrocytes of the adult rat spinal cord. Neuroscience 1996, 74(3):619-623.
7. Bosio A., Huppert V., Donath S., Hennemann P., Malchow M., Heinlein U.A. Isolation and enrichment of stem cells. Adv. Biochem. Eng. Biotechnol. 2009, 114:23-72.
8. Brustle O., Jones K.N., Learish R.D., Karram K., Choudhary K., Wiestler O.D., McKay R.D. Embryonic stem cell-derived glial precursors: a source of myelinating transplants. Science 1999, 285(5428):754-756.
9. Chung S., Sonntag K.C., Andersson T., Bjorklund L.M., Park J.J., Kim D.W., Kim K.S. Genetic engineering of mouse embryonic stem cells by Nurr1 enhances differentiation and maturation into dopaminergic neurons. Eur. J. Neurosci. 2002, 16(10):1829-1838.
10. Chung S., Moon J.I., Leung A., Aldrich D., Lukianov S., Kitayama Y., Kim K.S. ES cell-derived renewable and functional midbrain dopaminergic progenitors. Proc. Natl. Acad. Sci. U. S. A. 2011, 23:9703-9708.
11. Cremer H., Lange R., Christoph A., Plomann M., Vopper G., Roes J., et al. Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 1994, 367(6462):455-459.
12. Cremer H., Chazal G., Carleton A., Goridis C., Vincent J.D., Lledo P.M. Long-term but not short-term plasticity at mossy fiber synapses is impaired in neural cell adhesion molecule-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 1998, 95(22):13242-13247.
13. Durbec P., Cremer H. Revisiting the function of PSA-NCAM in the nervous system. Mol. Neurobiol. 2001, 24(1-3):53-64.
14. Duveau V., Arthaud S., Rougier A., Le Gal La Salle G. Polysialylation of NCAM is upregulated by hyperthermia and participates in heat shock preconditioning-induced neuroprotection. Neurobiol. Dis. 2007, 26(2):385-395.
15. El Maarouf A., Rutishauser U. Removal of polysialic acid induces aberrant pathways, synaptic vesicle distribution, and terminal arborization of retinotectal axons. J. Comp. Neurol. 2003, 460(2):203-211.
16. El Maarouf A., Petridis A.K., Rutishauser U. Use of polysialic acid in repair of the central nervous system. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(45):16989-16994.
17. Finne J. Occurrence of unique polysialosyl carbohydrate units in glycoproteins of developing brain. J. Biol. Chem. 1982, 257(20):11966-11970.
18. Finne J., Finne U., Deagostini-Bazin H., Goridis C. Occurrence of alpha 2-8 linked polysialosyl units in a neural cell adhesion molecule. Biochem. Biophys. Res. Commun. 1983, 112(2):482-487.
19. Franz C.K., Rutishauser U., Rafuse V.F. Polysialylated neural cell adhesion molecule is necessary for selective targeting of regenerating motor neurons. J. Neurosci. 2005, 25(8):2081-2091.
20. Friling S., Andersson E., Thompson L.H., Jonsson M.E., Hebsgaard J.B., Nanou E., Ericson J. Efficient production of mesencephalic dopamine neurons by Lmx1a expression in embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(18):7613-7618.
21. Glaser T., Brose C., Franceschini I., Hamann K., Smorodchenko A., Zipp F., Brustle O. Neural cell adhesion molecule polysialylation enhances the sensitivity of embryonic stem cell-derived neural precursors to migration guidance cues. Stem Cells 2007, 25(12):3016-3025.
22. Golebiewska A., Atkinson S.P., Lako M., Armstrong L. Epigenetic landscaping during hESC differentiation to neural cells. Stem Cells 2009, 27(6):1298-1308.
23. Hadjantonakis A.K., Gertsenstein M., Ikawa M., Okabe M., Nagy A. Generating green fluorescent mice by germline transmission of green fluorescent ES cells. Mech. Dev. 1998, 76(1-2):79-90.
24. Hedlund E., Pruszak J., Ferree A., Vinuela A., Hong S., Isacson O., Kim K.S. Selection of embryonic stem cell-derived enhanced green fluorescent protein-positive dopamine neurons using the tyrosine hydroxylase promoter is confounded by reporter gene expression in immature cell populations. Stem Cells 2007, 25(5):1126-1135.
25. Hedlund E., Pruszak J., Lardaro T., Ludwig W., Vinuela A., Kim K.S., Isacson O. Embryonic stem cell-derived Pitx3-enhanced green fluorescent protein midbrain dopamine neurons survive enrichment by fluorescence-activated cell sorting and function in an animal model of Parkinson's disease. Stem Cells 2008, 26(6):1526-1536.
26. Karaca M., Castel J., Tourrel-Cuzin C., Brun M., Geant A., Dubois M., Ctesson S., Rodriguez M., Luquet S., Cattan P., Lockhart B., Lang J., Ktorza A., Magnan C., Kargar C. Exploring functional beta-cell heterogeneity in vivo using PSA-NCAM as a specific marker. PLoS One 2009, 4(5):e5555.
27. Kawasaki H., Mizuseki K., Nishikawa S., Kaneko S., Kuwana Y., Nakanishi S., Sasai Y. Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 2000, 28(1):31-40.
28. Keirstead H.S., Ben-Hur T., Rogister B., O'Leary M.T., Dubois-Dalcq M., Blakemore W.F. Polysialylated neural cell adhesion molecule-positive CNS precursors generate both oligodendrocytes and Schwann cells to remyelinate the CNS after transplantation. J. Neurosci. 1999, 19(17):7529-7536.
29. Kiss J.Z., Rougon G. Cell biology of polysialic acid. Curr. Opin. Neurobiol. 1997, 7(5):640-646.
30. Lee S.H., Lumelsky N., Studer L., Auerbach J.M., McKay R.D. Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat. Biotechnol. 2000, 18(6):675-679.
31. Liu S., Qu Y., Stewart T.J., Howard M.J., Chakrabortty S., Holekamp T.F., McDonald J.W. Embryonic stem cells differentiate into oligodendrocytes and myelinate in culture and after spinal cord transplantation. Proc. Natl. Acad. Sci. U. S. A. 2000, 97(11):6126-6131.
32. MacLaren R.E., Pearson R.A., MacNeil A., Douglas R.H., Salt T.E., Akimoto M., Ali R.R. Retinal repair by transplantation of photoreceptor precursors. Nature 2006, 444(7116):203-207.
33. Mak S.K., Huang Y.A., Iranmanesh S., Vangipuram M., Sundararajan R., Nguyen L., Langston J.W., Schüle B. Small molecules greatly improve conversion of human-induced pluripotent stem cells to the neuronal lineage. Stem Cells Int. 2012, 140427.
34. Martinat C., Bacci J.J., Leete T., Kim J., Vanti W.B., Newman A.H., Abeliovich A. Cooperative transcription activation by Nurr1 and Pitx3 induces embryonic stem cell maturation to the midbrain dopamine neuron phenotype. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(8):2874-2879.
35. Muller D., Wang C., Skibo G., Toni N., Cremer H., Calaora V., Kiss J.Z. PSA-NCAM is required for activity-induced synaptic plasticity. Neuron 1996, 17(3):413-422.
36. Nguyen L., Rigo J.M., Malgrange B., Moonen G., Belachew S. Untangling the functional potential of PSA-NCAM-expressing cells in CNS development and brain repair strategies. Curr. Med. Chem. 2003, 10(20):2185-2196.
37. Okabe S., Forsberg-Nilsson K., Spiro A.C., Segal M., McKay R.D. Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech. Dev. 1996, 59(1):89-102.
38. Pham K., Nacher J., Hof P.R., McEwen B.S. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur. J. Neurosci. 2003, 17(4):879-886.
39. Pruszak J., Sonntag K.C., Aung M.H., Sanchez-Pernaute R., Isacson O. Markers and methods for cell sorting of human embryonic stem cell-derived neural cell populations. Stem Cells 2007, 25(9):2257-2268.
40. Pruszak J., Ludwig W., Blak A., Alavian K., Isacson O. CD15, CD24, and CD29 define a surface biomarker code for neural lineage differentiation of stem cells. Stem Cells 2009, 27(12):2928-2940.
41. Rousselot P., Lois C., Alvarez-Buylla A. Embryonic (PSA) N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of adult mice. J. Comp. Neurol. 1995, 351(1):51-61.
42. Roy N.S., Cleren C., Singh S.K., Yang L., Beal M.F., Goldman S.A. Functional engraftment of human ES cell-derived dopaminergic neurons enriched by coculture with telomerase-immortalized midbrain astrocytes. Nat. Med. 2006, 12(11):1259-1268.
43. Rutishauser U., Landmesser L. Polysialic acid in the vertebrate nervous system: a promoter of plasticity in cell-cell interactions. Trends Neurosci. 1996, 19(10):422-427.
44. Schwartz C.M., Spivak C.E., Baker S.C., McDaniel T.K., Loring J.F., Nguyen C., Rao M.S. NTera2: a model system to study dopaminergic differentiation of human embryonic stem cells. Stem Cells Dev. 2005, 14(5):517-534.
45. Seidenfaden R., Desoeuvre A., Bosio A., Virard I., Cremer H. Glial conversion of SVZ-derived committed neuronal precursors after ectopic grafting into the adult brain. Mol. Cell. Neurosci. 2006, 32(1-2):187-198.
46. Sharp J., Keirstead H.S. Stem cell-based cell replacement strategies for the central nervous system. Neurosci. Lett. 2009, 456(3):107-111.
47. Tabar V., Panagiotakos G., Greenberg E.D., Chan B.K., Sadelain M., Gutin P.H., Studer L. Migration and differentiation of neural precursors derived from human embryonic stem cells in the rat brain. Nat. Biotechnol. 2005, 23(5):601-606.
48. Thomson J.A., Itskovitz-Eldor J., Shapiro S.S., Waknitz M.A., Swiergiel J.J., Marshall V.S., Jones J.M. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282(5391):1145-1147.
49. Tropepe V., Hitoshi S., Sirard C., Mak T.W., Rossant J., van der Kooy D. Direct neural fate specification from embryonic stem cells: a primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron 2001, 30(1):65-78.
50. Wichterle H., Lieberam I., Porter J.A., Jessell T.M. Directed differentiation of embryonic stem cells into motor neurons. Cell 2002, 110(3):385-397.
51. Xian H.Q., McNichols E., St Clair A., Gottlieb D.I. A subset of ES-cell-derived neural cells marked by gene targeting. Stem Cells 2003, 21(1):41-49.
52. Ying Q.L., Stavridis M., Griffiths D., Li M., Smith A. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol. 2003, 21(2):183-186.
53. Yuan S.H., Martin J., Elia J., Flippin J., Paramban R.I., Hefferan M.P., Carson C.T. Cell-surface marker signatures for the isolation of neural stem cells, glia and neurons derived from human pluripotent stem cells. PLoS One 2011, 6(3):e17540.