Peripheral nervous system progenitors can be reprogrammed to produce myelinating oligodendrocytes and repair brain lesions

Journal of Neuroscience

Volumn 31, Issue 17, 2011, Pages 6379-6391

  Binder, Ellen ^a   Rukavina, Marion ^b   Hassani, Hessameh ^c   Weber, Marlen ^a   Nakatani, Hiroko ^c   Reiff, Tobias ^a   Parras, Carlos ^c   Taylor, Verdon ^b,d   Rohrer, Hermann ^a  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^b MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^c INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

^d UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; PERIPHERIN; PROTEIN P75; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LHX2; TRANSCRIPTION FACTOR NKX6.1; TRANSCRIPTION FACTOR PAX2; TRANSCRIPTION FACTOR PAX5; TRANSCRIPTION FACTOR RUNX3; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; CELL DIFFERENTIATION; CELL LINEAGE; CONTROLLED STUDY; CORPUS CALLOSUM; DNA MODIFICATION; EMBRYO; GANGLION; MORPHOLOGY; MOUSE; MYELINATION; NEURAL CREST CELL; NEURULATION; NONHUMAN; OLIGODENDROGLIA; PERIPHERAL NERVOUS SYSTEM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RANVIER NODE; STELLATE CELL; STEM CELL; SUBVENTRICULAR ZONE;

ANIMALS; ANIMALS, NEWBORN; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN INJURIES; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; DISEASE MODELS, ANIMAL; EMBRYO, MAMMALIAN; FEMALE; GANGLIA, SPINAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; MYELIN BASIC PROTEINS; MYELIN PROTEOLIPID PROTEIN; MYELIN SHEATH; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NEUROFILAMENT PROTEINS; O ANTIGENS; OLIGODENDROGLIA; STEM CELL TRANSPLANTATION; TRANSFECTION; TUBULIN;

EID: 79955798340     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0129-11.2011     Document Type: Article

References (60)

1. Aquino JB, Hjerling-Leffler J, Koltzenburg M, Edlund T, Villar MJ, Ernfors P (2006) In vitro and in vivo differentiation of boundary cap neural crest stem cells into mature Schwann cells. Exp Neurol 198:438-449.
2. Archer DR, Cuddon PA, Lipsitz D, Duncan ID (1997) Myelination of the canine central nervous system by glial cell transplantation: a model for repair of human myelin disease. Nat Med 3:54-59.
3. Baron-Van Evercooren A, Gansmuller A, Duhamel E, Pascal F, Gumpel M (1992) Repair of a myelin lesion by Schwann cells transplanted in the adult mouse spinal cord. J Neuroimmunol 40:235-242.
4. Basak O, Taylor V (2007) Identification of self-replicating multipotent progenitors in the embryonic nervous system by high Notch activity and Hes5 expression. Eur J Neurosci 25:1006-1022.
5. Bénazet JD, Bischofberger M, Tiecke E, Goncalves A, Martin JF, Zuniga A, Naef F, Zeller R (2009) A self-regulatory system of interlinked signaling feedback loops controls mouse limb patterning. Science 323:1050-1053.
6. Bixby S, Kruger GM, Mosher JT, Joseph NM, Morrison SJ (2002) Cell-intrinsic differences between stem cells from different regions of the peripheral nervous system regulate the generation of neural diversity. Neuron 35:643-656.
7. Blakemore WF (1984) Limited remyelination of CNS axons by Schwann cells transplanted into the sub-arachnoid space. J Neurol Sci 64:265-276.
8. Boiko T, Rasband MN, Levinson SR, Caldwell JH, Mandel G, Trimmer JS, Matthews G (2001) Compact myelin dictates the differential targeting of two sodium channel isoforms in the same axon. Neuron 30:91-104.
9. Busch C, Oppitz M, Sailer MH, Just L, Metzger M, Drews U (2006) BMP-2-dependent integration of adult mouse subventricular stem cells into the neural crest of chick and quail embryos. J Cell Sci 119:4467-4474.
10. Coulpier F, Le Crom S, Maro GS, Manent J, Giovannini M, Maciorowski Z, Fischer A, Gessler M, Charnay P, Topilko P (2009) Novel features of boundary cap cells revealed by the analysis of newly identified molecular markers. Glia 57:1450-1457.
11. Delfino-Machín M, Chipperfield TR, Rodrigues FS, Kelsh RN (2007) The proliferating field of neural crest stem cells. Dev Dyn 236:3242-3254.
12. De Robertis EM, Kuroda H (2004) Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu Rev Cell Dev Biol 20:285-308.
13. Dromard C, Bartolami S, Deleyrolle L, Takebayashi H, Ripoll C, Simonneau L, Prome S, Puech S, Tran VB, Duperray C,Valmier J, Privat A, Hugnot JP (2007) NG2 and Olig2 expression provides evidence for phenotypic de regulation of cultured central nervous system and peripheral nervous system neural precursor cells. Stem Cells 25:340-353.
14. Duff RS, Langtimm CJ, Richardson MK, Sieber-Blum M (1991) In vitro clonal analysis of progenitor cell patterns in dorsal root and sympathetic ganglia of the quail. Dev Biol 147:451-459.
15. Dupouey P, Jacque C, Bourre JM, Cesselin F, Privat A, Baumann N (1979) Immunochemical studies of myelin basic protein in shiverer mouse devoid of major dense line of myelin. Neurosci Lett 12:113-118.
16. Eftekharpour E, Karimi-Abdolrezaee S, Wang J, El Beheiry H, Morshead C, Fehlings MG (2007) Myelination of congenitally dysmyelinated spinal cord axons by adult neural precursor cells results in formation of nodes of Ranvier and improved axonal conduction. J Neurosci 27:3416-3428.
17. Ernsberger U, Sendtner M, Rohrer H (1989) Proliferation and differentiation of embryonic chick sympathetic neurons: effects of ciliary neu-rotrophic factor. Neuron 2:1275-1284.
18. Fairless R, Frame MC, Barnett SC (2005) N-cadherin differentially determines Schwann cell and olfactory ensheathing cell adhesion and migration responses on contact with astrocytes. Mol Cell Neurosci 28:253-263.
19. Fernandes KJ, Toma JG, Miller FD (2008) Multipotent skin-derived precursors: adult neural crest-related precursors with therapeutic potential. Phi-los Trans R Soc Lond B Biol Sci 363:185-198.
20. Fex Svenningsen A, Colman DR, Pedraza L (2004) Satellite cells of dorsal root ganglia are multipotential glial precursors. Neuron Glia Biol 1:85-93.
21. Franklin RJ, ffrench-Constant C (2008) Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 9:839-855.
22. Gabay L, Lowell S, Rubin LL, Anderson DJ (2003) Deregulation of dorso-ventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron 40:485-499.
23. Gajavelli S, Wood PM, Pennica D, Whittemore SR, Tsoulfas P (2004) BMP signaling initiates a neural crest differentiation program in embryonic rat CNS stem cells. Exp Neurol 188:205-223.
24. Gonzalez-Perez O, Romero-Rodriguez R, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A (2009) Epidermal growth factor induces the progeny of subventricular zone type B cells to migrate and differentiate into oligodendrocytes. Stem Cells 27:2032-2043.
25. Hack MA, Sugimori M, Lundberg C, Nakafuku M, Götz M (2004) Region-alization and fate specification in neurospheres: the role of Olig2 and Pax6. Mol Cell Neurosci 25:664-678.
26. Hjerling-Leffler J, Marmigère F, Heglind M, Cederberg A, Koltzenburg M, Ener-bck S, Ernfors P (2005) The boundary cap: a source of neural crest stem cells that generate multiple sensory neuron subtypes. Development 132:2623-2632.
27. Jessen KR, Mirsky R (2005) The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 6:671-682.
28. Keirstead HS, Ben-Hur T, Rogister B, O'Leary MT, Dubois-Dalcq M, Blakemore WF (1999) Polysialylated neural cell adhesion molecule-positive CNS precursors generate both oligodendrocytes and Schwann cells to remyelinate the CNS after transplantation. J Neurosci 19:7529-7536.
29. Kelly TK, Karsten SL, Geschwind DH, KornblumHI (2009) Cell lineage and regional identity of cultured spinal cord neural stem cells and comparison to brain-derived neural stem cells. PLoS One 4:e4213.
30. Kessaris N, Fogarty M, Iannarelli P, Grist M, Wegner M, Richardson WD (2006) Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat Neurosci 9:173-179.
31. Kruger GM, Mosher JT, Bixby S, Joseph N, Iwashita T, Morrison SJ (2002) Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness. Neuron 35:657-669.
32. Le Douarin NM, Kalcheim C (1999) The neural crest, Ed 2.Cambridge, UK: Cambridge UP.
33. Lütolf S, Radtke F, Aguet M, Suter U, Taylor V (2002) Notch1isrequired for neuronal and glial differentiation in the cerebellum. Development 129:373-385.
34. Marshall OJ (2004) PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics 20:2471-2472.
35. Martino G, Franklin RJ, Van Evercooren AB, Kerr DA (2010) Stem cell transplantation in multiple sclerosis: current status and future prospects. Nat Rev Neurol 6:247-255.
36. Menegoz M, Gaspar P, Le Bert M, Galvez T, Burgaya F, Palfrey C, Ezan P, Arnos F, Girault JA (1997) Paranodin, a glycoprotein of neuronal para-nodal membranes. Neuron 19:319-331.
37. Molofsky AV, Pardal R, Iwashita T, Park IK, Clarke MF, Morrison SJ (2003) Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 425:962-967.
38. Mori S, Leblond CP (1970) Electron microscopic identification of three classes of oligodendrocytes and a preliminary study of their proliferative activity in the corpus callosum of young rats. J Comp Neurol 139:1-28.
39. Morrison SJ, White PM, Zock C, Anderson DJ (1999) Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipo-tent mammalian neural crest stem cells. Cell 96:737-749.
40. Mosher JT, Yeager KJ, Kruger GM, Joseph NM, Hutchin ME, Dlugosz AA, Morrison SJ (2007) Intrinsic differences among spatially distinct neural crest stem cells in terms of migratory properties, fate determination, and ability to colonize the enteric nervous system. Dev Biol 303:1-15.
41. Nait-Oumesmar B, Decker L, Lachapelle F, Avellana-Adalid V, Bachelin C, Van Evercooren AB (1999) Progenitor cells of the adult mouse subven-tricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur J Neurosci 11:4357-4366.
42. Nern C, Wolff I, Macas J, von Randow J, Scharenberg C, Priller J, Momma S (2009) Fusionofhematopoietic cells with Purkinje neurons does not lead to stable heterokaryon formation under noninvasive conditions. J Neu-rosci 29:3799-3807.
43. Neumeister B, Grabosch A, Basak O, Kemler R, Taylor V (2009) Neural progenitors of the postnatal and adult mouse forebrain retain the ability to self-replicate, form neurospheres and undergo multipotent differentiation in vivo. Stem Cells 27:714-723.
44. Nyfeler Y, Kirch RD, Mantei N, Leone DP, Radtke F, Suter U, Taylor V (2005) Jagged1 signals in the postnatal subventricular zone are required for enrual stem cell self-renewal. EMBO J 24:3504-3515.
45. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y (1997) "Green mice" as a source of ubiquitous green cells. FEBS Lett 407:313-319.
46. Piaton G, Gould RM, Lubetzki C (2010) Axon-oligodendrocyte interactions during developmental myelination, demyelination and repair. J Neuro-chem 114:1243-1260.
47. Poliak S, Peles E (2003) The local differentiation of myelinated axons at nodes of Ranvier. Nat Rev Neurosci 4:968-980.
48. Privat A, Jacque C, Bourre JM, Dupouey P, Baumann N (1979) Absence of the major dense line in myelin of the mutant mouse "shiverer." Neurosci Lett 12:107-112.
49. Rasband MN, Peles E, Trimmer JS, Levinson SR, Lux SE, Shrager P (1999) Dependence of nodal sodium channel clustering on paranodal axoglial contact in the developing CNS. J Neurosci 19:7516-7528.
50. Rosenbluth J (1980) Central myelin in the mouse mutant shiverer. J Comp Neurol 194:639-648.
51. Sailer MH, Hazel TG, Panchision DM, Hoeppner DJ, Schwab ME, McKay RD (2005) BMP2 and FGF2 cooperate to induce neural-crest-like fates from fetal and adult CNS stem cells. J Cell Sci 118:5849-5860.
52. Sauka-Spengler T, Bronner-Fraser M (2008) A gene regulatory network orchestrates neural crest formation. Nat Rev Mol Cell Biol 9:557-568.
53. Shields SA, Blakemore WF, Franklin RJ (2000) Schwann cell remyelination is restricted to astrocyte-deficient areas after transplantation into demy-elinated adult rat brain. J Neurosci Res 60:571-578.
54. Sieber-Blum M, Grim M, Hu YF, Szeder V (2004) Pluripotent neural crest stem cells in the adult hair follicle. Dev Dyn 231:258-269.
55. Stemple DL, Anderson DJ (1992) Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 71:973-985.
56. Trentin A, Glavieux-Pardanaud C, Le Douarin NM, Dupin E (2004) Self-renewal capacity is a widespread property of various types of neural crest precursor cells. Proc Natl Acad Sci USA 101:4495-4500.
57. Windrem MS, Nunes MC, Rashbaum WK, Schwartz TH, Goodman RA, McKhann G 2nd, Roy NS, Goldman SA (2004) Fetal and adult human oligodendrocyte progenitor cell isolates myelinate the congenitally dys-myelinated brain. Nat Med 10:93-97.
58. Windrem MS, Schanz SJ, Guo M, Tian GF, Washco V, Stanwood N, Rasband M, Roy NS, Nedergaard M, Havton LA, Wang S, Goldman SA (2008) Neonatal chimerization with human glial progenitor cells can both remy-elinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell 2:553-565.
59. Zawadzka M, Rivers LE, Fancy SP, Zhao C, Tripathi R, Jamen F, Young K, Goncharevich A, Pohl H, Rizzi M, Rowitch DH, Kessaris N, Suter U, Richardson WD, Franklin RJ (2010) CNS-resident glial progenitor/ stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell 6:578-590.
60. Zujovic V, Thibaud J, Bachelin C, Vidal M, Coulpier F, Charnay P, Topilko P, Baron-Van Evercooren A (2010) Boundary cap cells are highly competitive for CNS remyelination: fast migration and efficient differentiation in PNS and CNS myelin-forming cells. Stem Cells 28:470-479.