Production and isolation of NG2+ oligodendrocyte precursors from human embryonic stem cells in defined serum-free medium

Stem Cell Research

Volumn 5, Issue 2, 2010, Pages 91-103

  Sundberg, Maria ^a   Skottman, Heli ^a   Suuronen, Riitta ^a,b   Narkilahti, Susanna ^a  

^a TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^b TAMPERE UNIVERSITY HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; HERMES ANTIGEN; MESSENGER RNA; MYELIN BASIC PROTEIN; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEOCHONDROITIN SULFATE; PROTEOLIPID PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL ISOLATION; COCULTURE; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYONIC STEM CELL; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; NERVE CELL CULTURE; OLIGODENDROGLIA; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY;

EID: 77955843135     PISSN: 18735061     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.scr.2010.04.005     Document Type: Article

References (65)

1. Adewumi O., Aflatoonian B., Ahrlund-Richter L., Amit M., Andrews P.W., Beighton G., Bello P.A., Benvenisty N., Berry L.S., Bevan S., et al. Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat. Biotechnol. 2007, 25:803-816.
2. Aguirre A., Gallo V. Postnatal neurogenesis and gliogenesis in the olfactory bulb from NG2-expressing progenitors of the subventricular zone. J. Neurosci. 2004, 24:10530-10541.
3. Aguirre A.A., Chittajallu R., Belachew S., Gallo V. NG2-expressing cells in the subventricular zone are type C-like cells and contribute to interneuron generation in the postnatal hippocampus. J. Cell Biol. 2004, 165:575-589.
4. Awatramani R., Beesley J., Yang H., Jiang H., Cambi F., Grinspan J., Garbern J., Kamholz J. Gtx, an oligodendrocyte-specific homeodomain protein, has repressor activity. J. Neurosci. Res. 2000, 61:376-387.
5. Barres B.A., Hart I.K., Coles H.S., Burne J.F., Voyvodic J.T., Richardson W.D., Raff M.C. Cell death in the oligodendrocyte lineage. J. Neurobiol. 1992, 23:1221-1230.
6. Barres B.A., Schmid R., Sendnter M., Raff M.C. Multiple extracellular signals are required for long-term oligodendrocyte survival. Development 1993, 118:283-295.
7. Brustle O., Jones K.N., Learish R.D., Karram K., Choudhary K., Wiestler O.D., Duncan I.D., McKay R.D. Embryonic stem cell-derived glial precursors: a source of myelinating transplants. Science 1999, 285:754-756.
8. Carpenter M.K., Inokuma M.S., Denham J., Mujtaba T., Chiu C.P., Rao M.S. Enrichment of neurons and neural precursors from human embryonic stem cells. Exp. Neurol. 2001, 172:383-397.
9. Carson M.J., Behringer R.R., Brinster R.L., McMorris F.A. Insulin-like growth factor I increases brain growth and central nervous system myelination in transgenic mice. Neuron 1993, 10:729-740.
10. Colognato H., Baron W., Avellana-Adalid V., Relvas J.B., Baron-Van Evercooren A., Georges-Labouesse E., ffrench-Constant C. CNS integrins switch growth factor signalling to promote target-dependent survival. Nat. Cell Biol. 2002, 4:833-841.
11. Colognato H., Galvin J., Wang Z., Relucio J., Nguyen T., Harrison D., Yurchenco P.D., French-Constant C. Identification of dystroglycan as a second laminin receptor in oligodendrocytes, with a role in myelination. Development 2007, 134:1723-1736.
12. Cui Q.L., Zheng W.H., Quirion R., Almazan G. Inhibition of Src-like kinases reveals Akt-dependent and -independent pathways in insulin-like growth factor I-mediated oligodendrocyte progenitor survival. J. Biol. Chem. 2005, 280:8918-8928.
13. Dakubo G.D., Beug S.T., Mazerolle C.J., Thurig S., Wang Y., Wallace V.A. Control of glial precursor cell development in the mouse optic nerve by sonic hedgehog from retinal ganglion cells. Brain Res. 2008, 1228:27-42.
14. Dugas J.C., Ibrahim A., Barres B.A. A crucial role for p57(Kip2) in the intracellular timer that controls oligodendrocyte differentiation. J. Neurosci. 2007, 27:6185-6196.
15. Gilbertson J.A., Sen A., Behie L.A., Kallos M.S. Scaled-up production of mammalian neural precursor cell aggregates in computer-controlled suspension bioreactors. Biotechnol. Bioeng. 2006, 94:783-792.
16. Glaser T., Perez-Bouza A., Klein K., Brustle O. Generation of purified oligodendrocyte progenitors from embryonic stem cells. FASEB J. 2005, 19:112-114.
17. Grinspan J. Cells and signaling in oligodendrocyte development. J. Neuropathol. Exp. Neurol. 2002, 61:297-306.
18. Heiskanen A., Satomaa T., Tiitinen S., Laitinen A., Mannelin S., Impola U., Mikkola M., Olsson C., Miller-Podraza H., Blomqvist M., et al. N-Glycolylneuraminic acid xenoantigen contamination of human embryonic and mesenchymal stem cells is substantially reversible. Stem Cells 2007, 25:197-202.
19. Horiuchi M., Lindsten T., Pleasure D., Itoh T. Differing in vitro survival dependency of mouse and rat NG2(+) oligodendroglial progenitor cells. J. Neurosci. Res. 2009, 88:957-970.
20. Hovatta O., Mikkola M., Gertow K., Stromberg A.M., Inzunza J., Hreinsson J., Rozell B., Blennow E., Andang M., Ahrlund-Richter L. A culture system using human foreskin fibroblasts as feeder cells allows production of human embryonic stem cells. Hum. Reprod. 2003, 18:1404-1409.
21. Hsieh J., Aimone J.B., Kaspar B.K., Kuwabara T., Nakashima K., Gage F.H. IGF-I instructs multipotent adult neural progenitor cells to become oligodendrocytes. J. Cell Biol. 2004, 164:111-122.
22. Hu B.Y., Du Z.W., Li X.J., Ayala M., Zhang S.C. Human oligodendrocytes from embryonic stem cells: conserved SHH signaling networks and divergent FGF effects. Development 2009, 136:1443-1452.
23. Inzunza J., Gertow K., Stromberg M.A., Matilainen E., Blennow E., Skottman H., Wolbank S., Ahrlund-Richter L., Hovatta O. Derivation of human embryonic stem cell lines in serum replacement medium using postnatal human fibroblasts as feeder cells. Stem Cells 2005, 23:544-549.
24. Izrael M., Zhang P., Kaufman R., Shinder V., Ella R., Amit M., Itskovitz-Eldor J., Chebath J., Revel M. Human oligodendrocytes derived from embryonic stem cells: effect of noggin on phenotypic differentiation in vitro and on myelination in vivo. Mol. Cell. Neurosci. 2007, 34:310-323.
25. Jiang X., Gwye Y., McKeown S.J., Bronner-Fraser M., Lutzko C., Lawlor E.R. Isolation and characterization of neural crest stem cells derived from in vitro-differentiated human embryonic stem cells. Stem Cells Dev. 2009, 18:1059-1070.
26. Kang S.M., Cho M.S., Seo H., Yoon C.J., Oh S.K., Choi Y.M., Kim D.W. Efficient induction of oligodendrocytes from human embryonic stem cells. Stem Cells 2007, 25:419-424.
27. Keirstead H.S., Nistor G., Bernal G., Totoiu M., Cloutier F., Sharp K., Steward O. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J. Neurosci. 2005, 25:4694-4705.
28. Kulbatski I., Tator C.H. Region-specific differentiation potential of adult rat spinal cord neural stem/precursors and their plasticity in response to in vitro manipulation. J. Histochem. Cytochem. 2009, 57:405-423.
29. Laszkiewicz I., Wiggins R.C., Konat G. Ascorbic acid upregulates myelin gene expression in C6 glioma cells. Metab. Brain Dis. 1992, 7:157-164.
30. Levine J.M., Reynolds R., Fawcett J.W. The oligodendrocyte precursor cell in health and disease. Trends Neurosci. 2001, 24:39-47.
31. Martin M.J., Muotri A., Gage F., Varki A. Human embryonic stem cells express an immunogenic nonhuman sialic acid. Nat. Med. 2005, 11:228-232.
32. Matise M.P., Joyner A.L. Gli genes in development and cancer. Oncogene 1999, 18:7852-7859.
33. McMorris F.A., Dubois-Dalcq M. Insulin-like growth factor I promotes cell proliferation and oligodendroglial commitment in rat glial progenitor cells developing in vitro. J. Neurosci. Res. 1988, 21:199-209.
34. Mi H., Barres B.A. Purification and characterization of astrocyte precursor cells in the developing rat optic nerve. J. Neurosci. 1999, 19:1049-1061.
35. Miller R.H. Regulation of oligodendrocyte development in the vertebrate CNS. Prog. Neurobiol. 2002, 67:451-467.
36. Nat R., Nilbratt M., Narkilahti S., Winblad B., Hovatta O., Nordberg A. Neurogenic neuroepithelial and radial glial cells generated from six human embryonic stem cell lines in serum-free suspension and adherent cultures. Glia 2007, 55:385-399.
37. Ness J.K., Scaduto R.C., Wood T.L. IGF-I prevents glutamate-mediated bax translocation and cytochrome C release in O4+ oligodendrocyte progenitors. Glia 2004, 46:183-194.
38. Ng V.Y., Ang S.N., Chan J.X., Choo A.B. Characterization of epithelial cell adhesion molecule as a surface marker on undifferentiated human embryonic stem cells. Stem Cells 2010, 28:29-35.
39. Nicolay D.J., Doucette J.R., Nazarali A.J. Transcriptional control of oligodendrogenesis. Glia 2007, 55:1287-1299.
40. Nishiyama A., Komitova M., Suzuki R., Zhu X. Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat. Rev. Neurosci. 2009, 10:9-22.
41. Nishiyama A., Lin X.H., Giese N., Heldin C.H., Stallcup W.B. Co-localization of NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells in the developing rat brain. J. Neurosci. Res. 1996, 43:299-314.
42. Nistor G.I., Totoiu M.O., Haque N., Carpenter M.K., Keirstead H.S. Human embryonic stem cells differentiate into oligodendrocytes in high purity and myelinate after spinal cord transplantation. Glia 2005, 49:385-396.
43. Pang Y., Zheng B., Fan L.W., Rhodes P.G., Cai Z. IGF-1 protects oligodendrocyte progenitors against TNFalpha-induced damage by activation of PI3K/Akt and interruption of the mitochondrial apoptotic pathway. Glia 2007, 55:1099-1107.
44. Portner R., Nagel-Heyer S., Goepfert C., Adamietz P., Meenen N.M. Bioreactor design for tissue engineering. J. Biosci. Bioeng. 2005, 100:235-245.
45. Pujuguet P., Simian M., Liaw J., Timpl R., Werb Z., Bissell M.J. Nidogen-1 regulates laminin-1-dependent mammary-specific gene expression. J. Cell Sci. 2000, 113(Pt 5):849-858.
46. Qi Y., Cai J., Wu Y., Wu R., Lee J., Fu H., Rao M., Sussel L., Rubenstein J., Qiu M. Control of oligodendrocyte differentiation by the Nkx2.2 homeodomain transcription factor. Development 2001, 128:2723-2733.
47. Qi Y., Tan M., Hui C.C., Qiu M. Gli2 is required for normal Shh signaling and oligodendrocyte development in the spinal cord. Mol. Cell. Neurosci. 2003, 23:440-450.
48. Rajala K., Hakala H., Panula S., Aivio S., Pihlajamaki H., Suuronen R., Hovatta O., Skottman H. Testing of nine different xeno-free culture media for human embryonic stem cell cultures. Hum. Reprod. 2007, 22:1231-1238.
49. Reubinoff B.E., Itsykson P., Turetsky T., Pera M.F., Reinhartz E., Itzik A., Ben-Hur T. Neural progenitors from human embryonic stem cells. Nat. Biotechnol. 2001, 19:1134-1140.
50. Rivera F.J., Kandasamy M., Couillard-Despres S., Caioni M., Sanchez R., Huber C., Weidner N., Bogdahn U., Aigner L. Oligodendrogenesis of adult neural progenitors: differential effects of ciliary neurotrophic factor and mesenchymal stem cell derived factors. J. Neurochem. 2008, 107:832-843.
51. Robinson S., Miller R. Environmental enhancement of growth factor-mediated oligodendrocyte precursor proliferation. Mol. Cell. Neurosci. 1996, 8:38-52.
52. Sen A., Kallos M.S., Behie L.A. New tissue dissociation protocol for scaled-up production of neural stem cells in suspension bioreactors. Tissue Eng. 2004, 10:904-913.
53. Southwood C., He C., Garbern J., Kamholz J., Arroyo E., Gow A. CNS myelin paranodes require Nkx6-2 homeoprotein transcriptional activity for normal structure. J. Neurosci. 2004, 24:11215-11225.
54. Spassky N., Olivier C., Cobos I., LeBras B., Goujet-Zalc C., Martinez S., Zalc B., Thomas J.L. The early steps of oligodendrogenesis: insights from the study of the plp lineage in the brain of chicks and rodents. Dev. Neurosci. 2001, 23:318-326.
55. Stolt C.C., Lommes P., Sock E., Chaboissier M.C., Schedl A., Wegner M. The Sox9 transcription factor determines glial fate choice in the developing spinal cord. Genes Dev. 2003, 17:1677-1689.
56. Sundberg M., Jansson L., Ketolainen J., Pihlajamaki H., Suuronen R., Skottman H., Inzunza J., Hovatta O., Narkilahti S. CD marker expression profiles of human embryonic stem cells and their neural derivatives, determined using flow-cytometric analysis, reveal a novel CD marker for exclusion of pluripotent stem cells. Stem Cell Res. 2009, 2:113-124.
57. Thomson A., Wojtacha D., Hewitt Z., Priddle H., Sottile V., Di Domenico A., Fletcher J., Waterfall M., Corrales N.L., Ansell R., et al. Human embryonic stem cells passaged using enzymatic methods retain a normal karyotype and express CD30. Cloning Stem Cells 2008, 10:89-106.
58. 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, 282:1145-1147.
59. Wilson H.C., Scolding N.J., Raine C.S. Co-expression of PDGF alpha receptor and NG2 by oligodendrocyte precursors in human CNS and multiple sclerosis lesions. J. Neuroimmunol. 2006, 176:162-173.
60. Zaka M., Rafi M.A., Rao H.Z., Luzi P., Wenger D.A. Insulin-like growth factor-1 provides protection against psychosine-induced apoptosis in cultured mouse oligodendrocyte progenitor cells using primarily the PI3K/Akt pathway. Mol. Cell. Neurosci. 2005, 30:398-407.
61. Zhang P.L., Izrael M., Ainbinder E., Ben-Simchon L., Chebath J., Revel M. Increased myelinating capacity of embryonic stem cell derived oligodendrocyte precursors after treatment by interleukin-6/soluble interleukin-6 receptor fusion protein. Mol. Cell. Neurosci. 2006, 31:387-398.
62. Zhang S.C., Ge B., Duncan I.D. Tracing human oligodendroglial development in vitro. J. Neurosci. Res. 2000, 59:421-429.
63. Zhang S.C., Wernig M., Duncan I.D., Brustle O., Thomson J.A. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat. Biotechnol. 2001, 19:1129-1133.
64. Zhang X., Cai J., Klueber K.M., Guo Z., Lu C., Qiu M., Roisen F.J. Induction of oligodendrocytes from adult human olfactory epithelial-derived progenitors by transcription factors. Stem Cells 2005, 23:442-453.
65. Zhang Y.W., Denham J., Thies R.S. Oligodendrocyte progenitor cells derived from human embryonic stem cells express neurotrophic factors. Stem Cells Dev. 2006, 15:943-952.