Human neural progenitors from different foetal forebrain regions remyelinate the adult mouse spinal cord

Brain

Volumn 134, Issue 4, 2011, Pages 1168-1183

  Buchet, Delphine ^a,b,c   Garcia, Corina ^a,b,c   Deboux, Cyrille ^a,b,c   Nait Oumesmar, Brahim ^a,b,c,d   Baron Van Evercooren, Anne ^a,b,c,d  

^a SORBONNE UNIVERSITÉ   (France)

^b INSERM   (France)

^c CNRS   (France)

^d PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

human neural progenitor cells; migration; oligodendrocyte; oligodendrogenesis; remyelination

Indexed keywords

GREEN FLUORESCENT PROTEIN; MYELIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN CORTEX; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CELL MIGRATION; CELL SURVIVAL; CYTOLOGY; DEMYELINATION; ELECTRON MICROSCOPY; FETUS; FIRST TRIMESTER PREGNANCY; FOREBRAIN; GESTATIONAL AGE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN VITRO STUDY; IN VIVO STUDY; INJECTION; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; OLIGODENDROGENESIS; OLIGODENDROGLIA; PHENOTYPE; PRIORITY JOURNAL; REMYELINIZATION; SPINAL CORD; TELENCEPHALON; THALAMUS; ULTRASTRUCTURE ANALYSIS AND ELECTRON MICROSCOPY;

ANALYSIS OF VARIANCE; ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, NUDE; MYELIN SHEATH; NERVE REGENERATION; NEURAL STEM CELLS; OLIGODENDROGLIA; SPINAL CORD;

EID: 79953654634     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awr030     Document Type: Article

References (54)

1. Back SA, Luo NL, Borenstein NS, Levine JM, Volpe JJ, Kinney HC. Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury. J Neurosci 2001; 21: 1302-12. (Pubitemid 32128775)
2. Brustle O, Choudhary K, Karram K, Huttner A, Murray K, Dubois-Dalcq M, et al. Chimeric brains generated by intraventricular transplantation of fetal human brain cells into embryonic rats. Nat Biotechnol 1998; 16: 1040-4. (Pubitemid 28515896)
3. Buc-Caron MH. Neuroepithelial progenitor cells explanted from human fetal brain proliferate and differentiate in vitro. Neurobiol Dis 1995; 2: 37-47.
4. Buchet D, Baron-Van Evercooren A. In search of human oligodendroglia for myelin repair. Neurosci Lett 2009; 456: 112-9.
5. Buchet D, Buc-Caron MH, Sabate O, Lachapelle F, Mallet J. Long-term fate of human telencephalic progenitor cells grafted into the adult mouse brain: effects of previous amplification in vitro. J Neurosci Res 2002a; 68: 276-83. (Pubitemid 34462532)
6. Buchet D, Serguera C, Zennou V, Charneau P, Mallet J. Long-term expression of beta-glucuronidase by genetically modified human neural progenitor cells grafted into the mouse central nervous system. Mol Cell Neurosci 2002b; 19: 389-401. (Pubitemid 34293461)
7. Carpenter MK, Cui X, Hu ZY, Jackson J, Sherman S, Seiger A, et al. In vitro expansion of a multipotent population of human neural progenitor cells. Exp Neurol 1999; 158: 265-78. (Pubitemid 29382819)
8. Chandran S, Caldwell M, Allen N. Introduction: stem cells and brain repair. Philos Trans R Soc Lond B Biol Sci 2008; 363: 5-7. (Pubitemid 350174584)
9. Chandran S, Compston A, Jauniaux E, Gilson J, Blakemore W, Svendsen C. Differential generation of oligodendrocytes from human and rodent embryonic spinal cord neural precursors. Glia 2004; 47: 314-24. (Pubitemid 39295415)
10. Costa MR, Bucholz O, Schroeder T, Gotz M. Late origin of glia-restricted progenitors in the developing mouse cerebral cortex. Cereb Cortex 2009; 19 (Suppl 1): i135-43.
11. Cummings BJ, Uchida N, Tamaki SJ, Salazar DL, Hooshmand M, Summers R, et al. Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc Natl Acad Sci USA 2005; 102: 14069-74. (Pubitemid 41377704)
12. Duncan ID. Replacing cells in multiple sclerosis. J Neurol Sci 2008; 265: 89-92.
13. Eftekharpour E, Karimi-Abdolrezaee S, Wang J, El Beheiry H, Morshead C, Fehlings MG. 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 2007; 27: 3416-28. (Pubitemid 46515125)
14. Flax JD, Aurora S, Yang C, Simonin C, Wills AM, Billinghurst LL, et al. Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nat Biotechnol 1998; 16: 1033-9. (Pubitemid 28515895)
15. Franklin RJ, ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 2008; 9: 839-55.
16. Fricker RA, Carpenter MK, Winkler C, Greco C, Gates MA, Bjorklund A. Site-specific migration and neuronal differentiation of human neural progenitor cells after transplantation in the adult rat brain. J Neurosci 1999; 19: 5990-6005. (Pubitemid 29327933)
17. Gabay L, Lowell S, Rubin LL, Anderson DJ. Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron 2003; 40: 485-99. (Pubitemid 37494699)
18. Goldman SA, Schanz S, Windrem MS. Stem cell-based strategies for treating pediatric disorders of myelin. Hum Mol Genet 2008; 17: R76-83.
19. Grever WE, Weidenheim KM, Tricoche M, Rashbaum WK, Lyman WD. Oligodendrocyte gene expression in the human fetal spinal cord during the second trimester of gestation. J Neurosci Res 1997; 47: 332-40. (Pubitemid 27066767)
20. Gumpel M, Lachapelle F, Gansmuller A, Baulac M, Baron van Evercooren A, Baumann N. Transplantation of human embryonic oligodendrocytes into shiverer brain. Ann N Y Acad Sci 1987; 495: 71-85.
21. Hajihosseini M, Tham TN, Dubois-Dalcq M. Origin of oligodendrocytes within the human spinal cord. J Neurosci 1996; 16: 7981-94. (Pubitemid 26405060)
22. Horner PJ, Power AE, Kempermann G, Kuhn HG, Palmer TD, Winkler J, et al. Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J Neurosci 2000; 20: 2218-28. (Pubitemid 30230075)
23. Hu BY, Du ZW, Zhang SC. Differentiation of human oligodendrocytes from pluripotent stem cells. Nat Protoc 2009; 4: 1614-22.
24. Hu BY, Weick JP, Yu J, Ma LX, Zhang XQ, Thomson JA, et al. Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. Proc Natl Acad Sci USA 2010; 107: 4335-40.
25. Izrael M, Zhang P, Kaufman R, Shinder V, Ella R, Amit M, et al. 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: 310-23. (Pubitemid 46330036)
26. Jakovcevski I, Filipovic R, Mo Z, Rakic S, Zecevic N. Oligodendrocyte development and the onset of myelination in the human fetal brain. Front Neuroanat 2009; 3: 5.
27. Jakovcevski I, Zecevic N. Olig transcription factors are expressed in oligo-dendrocyte and neuronal cells in human fetal CNS. J Neurosci 2005a; 25: 10064-73. (Pubitemid 41636202)
28. Jakovcevski I, Zecevic N. Sequence of oligodendrocyte development in the human fetal telencephalon. Glia 2005b; 49: 480-91. (Pubitemid 40353834)
29. Kessaris N, Fogarty M, Iannarelli P, Grist M, Wegner M, Richardson WD. Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat Neurosci 2006; 9: 173-9. (Pubitemid 43164539)
30. Lasiene J, Matsui A, Sawa Y, Wong F, Horner PJ. Age-related myelin dynamics revealed by increased oligodendrogenesis and short inter-nodes. Aging Cell 2009; 8: 201-13.
31. Ligon KL, Alberta JA, Kho AT, Weiss J, Kwaan MR, Nutt CL, et al. The oligodendroglial lineage marker OLIG2 is universally expressed in diffuse gliomas. J Neuropathol Exp Neurol 2004; 63: 499-509. (Pubitemid 38669670)
32. LoPresti P. Regulation and differential expression of tau mRNA isoforms as oligodendrocytes mature in vivo: implications for myelination. Glia 2002; 37: 250-7.
33. LoPresti P, Szuchet S, Papasozomenos SC, Zinkowski RP, Binder LI. Functional implications for the microtubule-associated protein tau: localization in oligodendrocytes. Proc Natl Acad Sci USA 1995; 92: 10369-73.
34. Maire CL, Buchet D, Kerninon C, Deboux C, Baron-Van Evercooren A, Nait-Oumesmar B. Directing human neural stem/precursor cells into oligodendrocytes by overexpression of Olig2 transcription factor. J Neurosci Res 2009; 87: 3438-46.
35. Martino G, Franklin RJ, Van Evercooren AB, Kerr DA. Stem cell transplantation in multiple sclerosis: current status and future prospects. Nat Rev Neurol 2010; 6: 247-55.
36. Murray K, Dubois-Dalcq M. Emergence of oligodendrocytes from human neural spheres. J Neurosci Res 1997; 50: 146-56. (Pubitemid 27473631)
37. Nishiyama A, Komitova M, Suzuki R, Zhu X. Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci 2009; 10: 9-22.
38. Nistor GI, Totoiu MO, Haque N, Carpenter MK, Keirstead HS. Human embryonic stem cells differentiate into oligodendrocytes in high purity and myelinate after spinal cord transplantation. Glia 2005; 49: 385-96. (Pubitemid 40222916)
39. Palmer TD, Schwartz PH, Taupin P, Kaspar B, Stein SA, Gage FH. Cell culture. Progenitor cells from human brain after death. Nature 2001; 411: 42-3. (Pubitemid 32428181)
40. Peru RL, Mandrycky N, Nait-Oumesmar B, Lu QR. Paving the axonal highway: from stem cells to myelin repair. Stem Cell Rev 2008; 4: 304-18.
41. Quinn SM, Walters WM, Vescovi AL, Whittemore SR. Lineage restriction of neuroepithelial precursor cells from fetal human spinal cord. J Neurosci Res 1999; 57: 590-602. (Pubitemid 29411474)
42. Rakic S, Zecevic N. Early oligodendrocyte progenitor cells in the human fetal telencephalon. Glia 2003; 41: 117-27. (Pubitemid 36262189)
43. Richardson WD, Kessaris N, Pringle N. Oligodendrocyte wars. Nat Rev Neurosci 2006; 7: 11-8. (Pubitemid 41828927)
44. Rowitch DH. Glial specification in the vertebrate neural tube. Nat Rev Neurosci 2004; 5: 409-19. (Pubitemid 38568501)
45. Roy NS, Wang S, Harrison-Restelli C, Benraiss A, Fraser RA, Gravel M, et al. Identification, isolation, and promoter-defined separation of mi-totic oligodendrocyte progenitor cells from the adult human subcortical white matter. J Neurosci 1999; 19: 9986-95. (Pubitemid 30226670)
46. Spassky N, Goujet-Zalc C, Parmantier E, Olivier C, Martinez S, Ivanova A, et al. Multiple restricted origin of oligodendrocytes. J Neurosci 1998; 18: 8331-43. (Pubitemid 28465009)
47. Svendsen CN, ter Borg MG, Armstrong RJ, Rosser AE, Chandran S, Ostenfeld T, et al. A new method for the rapid and long term growth of human neural precursor cells. J Neurosci Methods 1998; 85: 141-52. (Pubitemid 29003064)
48. Tepavcevic V, Baron-Van Evercooren A. Transplantation of myelin-forming cells. In: Squire LR, editor. Encyclopedia of neuroscience. Oxford: Academic Press; 2008.
49. Windrem MS, Nunes MC, Rashbaum WK, Schwartz TH, Goodman RA, McKhann G 2nd. Fetal and adult human oligodendrocyte progenitor cell isolates myelinate the congenitally dysmyelinated brain. Nat Med 2004; 10: 93-7. (Pubitemid 38524704)
50. Windrem MS, Roy NS, Wang J, Nunes M, Benraiss A, Goodman R, et al. Progenitor cells derived from the adult human subcortical white matterdisperse and differentiate as oligodendrocytes within demyeli-nated lesions of the rat brain. J Neurosci Res 2002; 69: 966-75. (Pubitemid 34984714)
51. Windrem MS, Schanz SJ, Guo M, Tian GF, Washco V, Stanwood N, et al. Neonatal chimerization with human glial progenitor cells can both remyelinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell 2008; 2: 553-65. (Pubitemid 351729215)
52. Woodruff RH, Tekki-Kessaris N, Stiles CD, Rowitch DH, Richardson WD. Oligodendrocyte development in the spinal cord and telencephalon: common themes and new perspectives. Int J Dev Neurosci 2001; 19: 379-85. (Pubitemid 32500334)
53. Yandava BD, Billinghurst LL, Snyder EY. "Global" cell replacement is feasible via neural stem cell transplantation: evidence from the dysmyeli-nated shiverer mouse brain. Proc Natl Acad Sci USA 1999; 96: 7029-34. (Pubitemid 29275004)
54. Zhang SC, Ge B, Duncan ID. Tracing human oligodendroglial development in vitro. J Neurosci Res 2000; 59: 421-9. (Pubitemid 30107983)