Optimizing culture medium composition to improve oligodendrocyte progenitor cell yields in vitro from subventricular zone-derived neural progenitor cell neurospheres

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Franco, Paula G ^a   Pasquini, Juana M ^a   Silvestroff, Lucas ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH FACTOR; HEPARIN; HOMODIMER; MYELIN BASIC PROTEIN; PLATELET DERIVED GROWTH FACTOR AA; PLATELET DERIVED GROWTH FACTOR BB; BECAPLERMIN; BIOLOGICAL MARKER; CULTURE MEDIUM; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR B; PLATELET-DERIVED GROWTH FACTOR A;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; CELL INTERACTION; CELL PROLIFERATION; CHEMICAL COMPOSITION; COCULTURE; CONTROLLED STUDY; CULTURE MEDIUM; CULTURE OPTIMIZATION; CULTURE TECHNIQUE; DEMYELINATING DISEASE; IN VITRO STUDY; MOUSE; NEURAL STEM CELL; NEWBORN; NONHUMAN; OLIGODENDROCYTE CULTURE; OLIGODENDROCYTE PRECURSOR CELL; PROTEIN EXPRESSION; STEM CELL TRANSPLANTATION; SUBVENTRICULAR ZONE; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION; GENETICS; HUMAN; LATERAL BRAIN VENTRICLE; METABOLISM; NERVE CELL; OLIGODENDROGLIA; PHARMACOLOGY; PRIMARY CELL CULTURE; REPORTER GENE; TRANSGENIC MOUSE;

MAMMALIA; MUS;

ANIMALS; ANIMALS, NEWBORN; BIOMARKERS; CELL DIFFERENTIATION; CELL PROLIFERATION; COCULTURE TECHNIQUES; CULTURE MEDIA; GENE EXPRESSION; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HEPARIN; HUMANS; LATERAL VENTRICLES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYELIN BASIC PROTEIN; NEURAL STEM CELLS; NEURONS; OLIGODENDROGLIA; PLATELET-DERIVED GROWTH FACTOR; PRIMARY CELL CULTURE; PROTO-ONCOGENE PROTEINS C-SIS;

EID: 84926512978     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0121774     Document Type: Article

References (71)

1. McCarthy KD, de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol. 1980; 85(3): 890-902. PMID: 6248568
2. Nakatsuji Y, Miller RH. Density dependent modulation of cell cycle protein expression in astrocytes. J Neurosci Res. 2001; 66(3): 487-496. PMID: 11746367
3. Yang Z, Watanabe M, Nishiyama A. Optimization of oligodendrocyte progenitor cell culture method for enhanced survival. J Neurosci Methods. 2005; 149(1): 50-56. PMID: 15975663
4. Niu J, Wang L, Liu S, Li C, Kong J, Shen HY, et al. An efficient and economical culture approach for the enrichment of purified oligodendrocyte progenitor cells. J Neurosci Methods. 2012; 209(1): 241-249. doi: 10.1016/j.jneumeth.2012.05.032 PMID: 22687939
5. Raff MC, Miller RH, Noble M. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 1983; 303(5916):390-6. PMID: 6304520
6. Barres BA, Hart IK, Coles HS, Burne JF, Voyvodic JT, Richardson WD, et al. Cell death and control of cell survival in the oligodendrocyte lineage. Cell 1992; 70(1):31-46. PMID: 1623522
7. Diers-Fenger M, Kirchhoff F, Kettenmann H, Levine JM, Trotter J. AN2/NG2 protein-expressing glial progenitor cells in the murine CNS: isolation, differentiation, and association with radial glia. Glia 2001; 34(3): 213-228. PMID: 11329183
8. Colello RJ, Sato-Bigbee C. Purification of oligodendrocytes and their progenitors using immunomagnetic separation and Percoll gradient centrifugation. Curr Protoc Neurosci. 2001;Chapter 3:Unit 3.12.
9. Rivers LE, Young KM, Rizzi M, Jamen F, Psachoulia K, Wade A, et al. PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci. 2008; 11 (12): 1392-1401. doi: 10.1038/nn.2220 PMID: 18849983
10. Sim FJ, McClain CR, Schanz SJ, Protack TL, Windrem MS, Goldman SA. CD140a identifies a population of highly myelinogenic, migration-competent and efficiently engrafting human oligodendrocyte progenitor cells. Nat Biotechnol. 2011; 29(10): 934-941. doi: 10.1038/nbt.1972 PMID: 21947029
11. Calver AR, Hall AC, Yu WP, Walsh FS, Heath JK, Betsholtz C, et al. Oligodendrocyte population dynamics and the role of PDGF in vivo. Neuron 1998; 20(5): 869-82. PMID: 9620692
12. Heldin CH, Westermark B. Mechanism of action and in vivo role of platelet-derived growth factor. Physiol Rev. 1999; 79(4): 1283-1316. PMID: 10508235
13. Chen PH, Chen X, He X. Platelet-derived growth factors and their receptors: structural and functional perspectives. Biochim Biophys Acta. 2013; 1834(10): 2176-2186. doi: 10.1016/j.bbapap.2012.10.015 PMID: 23137658
14. Pringle NP, Mudhar HS, Collarini EJ, Richardson WD. PDGF receptors in the rat CNS: during late neurogenesis, PDGF alpha-receptor expression appears to be restricted to glial cells of the oligodendrocyte lineage. Development 1992; 115(2): 535-551. PMID: 1425339
15. Moore L, Bain JM, Loh JM, Levison SW. PDGF-responsive progenitors persist in the subventricular zone across the lifespan. ASN Neuro 2014; 6(2)pii: e00137. doi: 10.1042/AN20140004 PMID: 24597723
16. Demoulin JB, Essaghir A. PDGF receptor signaling networks in normal and cancer cells. Cytokine Growth Factor Rev. 2014; 25(3): 273-283. doi: 10.1016/j.cytogfr.2014.03.003 PMID: 24703957
17. Hu BY, Du ZW, Zhang SC. Differentiation of human oligodendrocytes from pluripotent stem cells. Nat Protoc. 2009; 4(11): 1614-1622. doi: 10.1038/nprot.2009.186 PMID: 19834476
18. Ball SG, Shuttleworth A, Kielty CM. Inhibition of platelet-derived growth factor receptor signaling regulates Oct4 and Nanog expression, cell shape, and mesenchymal stem cell potency. Stem Cells 2012; 30(3): 548-60. doi: 10.1002/stem.1015 PMID: 22213560
19. Gard AL, Pfeiffer SE. Glial cell mitogens bFGF and PDGF differentially regulate development of O4+GalC- oligodendrocyte progenitors. Dev Biol. 1993; 159(2): 618-630. PMID: 8405684
20. Lachapelle F, Avellana-Adalid V, Nait-Oumesmar B, Baron-Van Evercooren A. Fibroblast growth fac-tor-2 (FGF-2) and platelet-derived growth factor AB (PDGF AB) promote adult SVZ-derived oligodendrogenesis in vivo. Mol Cell Neurosci. 2002; 20(3): 390-403. PMID: 12139917
21. Woodruff RH, Fruttiger M, Richardson WD, Franklin RJ. Platelet-derived growth factor regulates oligodendrocyte progenitor numbers in adult CNS and their response following CNS demyelination. Mol Cell Neurosci. 2004; 25(2): 252-262. PMID: 15019942
22. Jackson EL, Garcia-Verdugo JM, Gil-Perotin S, Roy M, Quinones-Hinojosa A, VandenBerg S, et al. PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 2006; 51(2): 187-199. PMID: 16846854
23. Pedraza CE, Monk R, Lei J, Hao Q, Macklin WB. Production, characterization, and efficient transfection of highly pure oligodendrocyte precursor cultures from mouse embryonic neural progenitors. Glia 2008; 56(12): 1339-1352. doi: 10.1002/glia.20702 PMID: 18512250
24. Hu JG, Fu SL, Zhang KH, Li Y, Yin L, Lu PH, et al. Differential gene expression in neural stem cells and oligodendrocyte precursor cells: a cDNA microarray analysis. J Neurosci Res. 2004; 78(5): 637-646. PMID: 15499592
25. Broughton SK, Chen H, Riddle A, Kuhn SE, Nagalla S, Roberts CT Jr, et al. Large-scale generation of highly enriched neural stem-cell-derived oligodendroglial cultures: maturation-dependent differences in insulin-like growth factor-mediated signal transduction. J Neurochem. 2007; 100(3): 628-638. PMID: 17263792
26. Hu JG, Wu XJ, Feng YF, Xi GM, Wang ZH, Zhou JS, et al. PDGF-AA and bFGF mediate B104CM-induced proliferation of oligodendrocyte precursor cells. Int J Mol Med. 2012; 30(5): 1113-1118. doi: 10. 3892/ijmm.2012.1110 PMID: 22922759
27. Erlandsson A, Brännvall K, Gustafsdottir S, Westermark B, Forsberg-Nilsson K. Autocrine/paracrine platelet-derived growth factor regulates proliferation of neural progenitor cells. Cancer Res. 2006; 66 (16): 8042-8048. PMID: 16912180
28. Assanah M, Lochhead R, Ogden A, Bruce J, Goldman J, Canoll P. Glial progenitors in adult white matter are driven to form malignant gliomas by platelet-derived growth factor-expressing retroviruses. J Neurosci. 2006; 26(25): 6781-90. PMID: 16793885
29. Chojnacki A, Weiss S. Isolation of a novel platelet-derived growth factor-responsive precursor from the embryonic ventral forebrain. J Neurosci. 2004; 24(48): 10888-10899. PMID: 15574739
30. Kessaris N, Jamen F, Rubin LL, Richardson WD. Cooperation between sonic hedgehog and fibroblast growth factor/MAPK signalling pathways in neocortical precursors. Development 2004; 131(6):1289-98. PMID: 14960493
31. Bilican B, Fiore-Heriche C, Compston A, Allen ND, Chandran S. Induction of Olig2 precursors by FGF involves BMP signalling blockade at the Smad level. PLoS One 2008; 3(8):e2863. doi: 10.1371/journal. pone.0002863 PMID: 18682850
32. Naruse M, Nakahira E, Miyata T, Hitoshi S, Ikenaka K, Bansal R. Induction of oligodendrocyte progenitors in dorsal forebrain by intraventricular microinjection of FGF-2. Dev Biol. 2006; 297(1):262-73. PMID: 16782086
33. Azim K, Raineteau O, Butt AM. Intraventricular injection of FGF-2 promotes generation of oligodendro-cyte-lineage cells in the postnatal and adult forebrain. Glia 2012; 60: 1977-1990. doi: 10.1002/glia. 22413 PMID: 22951928
34. Furusho M, Kaga Y, Ishii A, Hebert JM, Bansal R. Fibroblast growth factor signaling is required for the generation of oligodendrocyte progenitors from the embryonic forebrain. J Neurosci. 2011; 31(13): 5055-66. doi: 10.1523/JNEUROSCI.4800-10.2011 PMID: 21451043
35. Mason JL, Goldman JE. A2B5+ and O4+ Cycling progenitors in the adult forebrain white matter respond differentially to PDGF-AA, FGF-2, and IGF-1. Mol Cell Neurosci. 2002; 20(1):30-42. PMID: 12056838
36. McKinnon RD, Matsui T, Dubois-Dalcq M, Aaronson SA. FGF modulates the PDGF-driven pathway of oligodendrocyte development. Neuron 1990; 5(5):603-14. PMID: 2171589
37. Zhang SC, Lundberg C, Lipsitz D, O'Connor LT, Duncan ID. Generation of oligodendroglial progenitors from neural stem cells. OPC expresan PDGFR y FGFR pero apagan EGFR. J Neurocytol. 1998; 27(7): 475-89. PMID: 11246488
38. Kelly JD, Haldeman BA, Grant FJ, Murray MJ, Seifert RA, Bowen-Pope DF, et al. Platelet-derived growth factor (PDGF) stimulates PDGF receptor subunit dimerization and intersubunit trans-phosphorylation. J Biol Chem. 1991; 266(14):8987-92. PMID: 1709159
39. Ray J, Gage FH. Differential properties of adult rat and mouse brain-derived neural stem/progenitor cells. Mol Cell Neurosci. 2006; 31(3): 560-573. PMID: 16426857
40. Yuan X, Chittajallu R, Belachew S, Anderson S, McBain CJ, Gallo V. Expression of the green fluorescent protein in the oligodendrocyte lineage: a transgenic mouse for developmental and physiological studies. J Neurosci Res. 2002; 70(4): 529-545. PMID: 12404507
41. Belachew S, Yuan X, Gallo V. Unraveling oligodendrocyte origin and function by cell-specific transgenesis. Dev Neurosci. 2001; 23(4-5): 287-298. PMID: 11872939
42. Mirzadeh Z, Doetsch F, Sawamoto K, Wichterle H, Alvarez-Buylla A. The subventricular zone en-face: wholemount staining and ependymal flow. J Vis Exp. 2010; 39. pii: 1938.
43. Gallagher S. Quantification of DNA and RNA with absorption and fluorescence spectroscopy. Curr Protoc Cell Biol. 2000;A.3D.1-A.3D.8.
44. Kaech S, Banker G. Culturing hippocampal neurons. Nat Protoc. 2006; 1(5): 2406-2415. PMID: 17406484
45. Gardner A, Jukkola P, Gu C. Myelination of rodent hippocampal neurons in culture. Nat Protoc. 2012; 7 (10): 1774-1782. doi: 10.1038/nprot.2012.100 PMID: 22955693
46. Xu SY, Wu YM, Ji Z, Gao XY, Pan SY. A modified technique for culturing primary fetal rat cortical neurons. J Biomed Biotechnol. 2012: 803930.
47. Wang J, O'Bara MA, Pol SU, Sim FJ. CD133/CD140a-based isolation of distinct human multipotent neural progenitor cells and oligodendrocyte progenitor cells. Stem Cells Dev. 2013; 22(15): 2121-2131. doi: 10.1089/scd.2013.0003 PMID: 23488628
48. Aguirre AA, 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(4): 575-89. PMID: 15159421
49. Kang SH, Fukaya M, Yang JK, Rothstein JD, Bergles DE. NG2+ CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration. Neuron 2010; 68 (4): 668-681. doi: 10.1016/j.neuron.2010.09.009 PMID: 21092857
50. Aguirre A, Gallo V. Postnatal neurogenesis and gliogenesis in the olfactory bulb from NG2-expressing progenitors of the subventricular zone. J Neurosci. 2004; 24(46): 10530-41. PMID: 15548668
51. Nishiyama A, Komitova M, Suzuki R, Zhu X. Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci. 2009; 10(1): 9-22. doi: 10.1038/nrn2495 PMID: 19096367
52. Hill RA, Nishiyama A. NG2 cells (polydendrocytes): Listeners to the neural network with diverse properties. Glia 2014; 62(8): 1195-1210. doi: 10.1002/glia.22664 PMID: 24753030
53. Baracskay KL, Kidd GJ, Miller RH, Trapp BD. NG2-positive cells generate A2B5-positive oligodendrocyte precursor cells. Glia 2007; 55(10): 1001-1010. PMID: 17503442
54. Zhu X, Hill RA, Dietrich D, Komitova M, Suzuki R, Nishiyama A. Age-dependent fate and lineage restriction of single NG2 cells. Development 2011; 138(4): 745-753. doi: 10.1242/dev.047951 PMID: 21266410
55. Marshall CA, Novitch BG, Goldman JE. Olig2 directs astrocyte and oligodendrocyte formation in postnatal subventricular zone cells. J Neurosci. 2005; 25(32): 7289-98. PMID: 16093378
56. Cai J, Chen Y, Cai WH, Hurlock EC, Wu H, Kernie SG, et al. A crucial role for Olig2 in white matter astrocyte development. Development 2007; 134(10): 1887-99. PMID: 17428828
57. Chen Y, Miles DK, Hoang T, Shi J, Hurlock E, Kernie SG, et al. The basic helix-loop-helix transcription factor olig2 is critical for reactive astrocyte proliferation after cortical injury. J Neurosci. 2008; 28(43): 10983-9. doi: 10.1523/JNEUROSCI.3545-08.2008 PMID: 18945906
58. Dimou L, Simon C, Kirchhoff F, Takebayashi H, Götz M. Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J Neurosci. 2008; 28(41): 10434-42. doi: 10. 1523/JNEUROSCI.2831-08.2008 PMID: 18842903
59. Silvestroff L, Franco PG, Pasquini JM. Neural and oligodendrocyte progenitor cells: transferrin effects on cell proliferation. ASN Neuro 2013; 5(1):e00107. doi: 10.1042/AN20120075 PMID: 23368675
60. Grinspan JB, Reddy UR, Stern JL, Hardy M, Williams M, Baird L, et al. Oligodendroglia express PDGF beta-receptor protein and are stimulated to proliferate by PDGF. Ann N Y Acad Sci. 1990; 605: 71-80. PMID: 2176446
61. Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 2002; 36(6): 1021-1034. PMID: 12495619
62. Sun Y, Goderie SK, Temple S. Asymmetric distribution of EGFR receptor during mitosis generates diverse CNS progenitor cells. Neuron 2005; 45(6): 873-886. PMID: 15797549
63. Cohen RI, Mckay R, Almazan G. Cyclic AMP regulates PDGF-stimulated signal transduction and differentiation of an immortalized optic-nerve-derived cell line. J Exp Biol. 1999; 202(Pt 4): 461-473.
64. Kulbatski I, Mothe AJ, Keating A, Hakamata Y, Kobayashi E, Tator CH. Oligodendrocytes and radial glia derived from adult rat spinal cord progenitors: morphological and immunocytochemical characterization. J Histochem Cytochem. 2007; 55(3): 209-222. PMID: 17101728
65. Silvestroff L, Franco PG, Pasquini JM. ApoTransferrin: dual role on adult subventricular zone-derived neurospheres. PLoS One 2012; 7(3): e33937. doi: 10.1371/journal.pone.0033937 PMID: 22479482
66. He Y, Cai W, Wang L, Chen P. A developmental study on the expression of PDGFalphaR immunoreactive cells in the brain of postnatal rats. Neurosci Res. 2009; 65(3): 272-279. doi: 10.1016/j.neures. 2009.07.011 PMID: 19665498
67. Gil-Perotín S, Duran-Moreno M, Cebrián-Silla A, Ramírez M, García-Belda P, García-Verdugo JM. Adult neural stem cells from the subventricular zone: a review of the neurosphere assay. Anat Rec. 2013; 296(9): 1435-1452. doi: 10.1002/ar.22746 PMID: 23904071
68. Coles-Takabe BL, Brain I, Purpura KA, Karpowicz P, Zandstra PW, Morshead CM, et al. Don't look: growing clonal versus nonclonal neural stem cell colonies. Stem Cells 2008; 26(11): 2938-2944. doi: 10.1634/stemcells.2008-0558 PMID: 18757294
69. Singec I, Knoth R, Meyer RP, Maciaczyk J, Volk B, Nikkhah G, et al. Defining the actual sensitivity and specificity of the neurosphere assay in stem cell biology. Nat Methods. 2006; 3(10): 801-806. PMID: 16990812
70. Moors M, Rockel TD, Abel J, Cline JE, Gassmann K, Schreiber T, et al. Research Human Neurospheres as Three-Dimensional Cellular Systems for Developmental Neurotoxicity Testing. Environ Health Perspect. 2009; 117(7): 1131-1138. doi: 10.1289/ehp.0800207 PMID: 19654924
71. Caldwell MA, Garcion E, terBorg MG, He X, Svendsen CN. Heparin stabilizes FGF-2 and modulates striatal precursor cell behavior in response to EGF. Exp Neurol. 2004; 188(2): 408-420. PMID: 15246840