A transplantation study of expanded human embryonic forebrain precursors: Evidence for selection of a specific progenitor population

Molecular and Cellular Neuroscience

Volumn 23, Issue 4, 2003, Pages 531-543

  Parmar, Malin ^a   Skogh, Charlotta ^a   Englund, Ulrica ^a,b  

^a LUND UNIVERSITY   (Sweden)

^b H LUNDBECK A S   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; EPIDERMAL GROWTH FACTOR; ER81 ANTIBODY; GROWTH FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN REGION; BRAIN VENTRICLE; CELL ACTIVITY; CELL CULTURE; CELL DIFFERENTIATION; CELL ISOLATION; CELL MIGRATION; CELL POPULATION; CELL SUBPOPULATION; CELL TRANSPLANTATION; CONTROLLED STUDY; EMBRYO; EMBRYO CELL; EXPOSURE; FOREBRAIN; GANGLION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; NEWBORN; NONHUMAN; OLFACTORY BULB; PRECURSOR; PRIORITY JOURNAL; RAT; STEM CELL;

EID: 0043162074     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1044-7431(03)00097-6     Document Type: Article

References (66)

1. Alvarez-Buylla A., Garcia-Verdugo J.M., Tramontin A.D. A unified hypothesis on the lineage of neural stem cells. Nat. Rev. Neurosci. 2:2001;287-293.
2. Arsenijevic Y., Villemure J.G., Brunet J.F., Bloch J.J., Deglon N., Kostic C., Zurn A., Aebischer P. Isolation of multipotent neural precursors residing in the cortex of the adult human brain. Exp. Neurol. 170:2001;48-62.
3. Bignami A., Eng L.F., Dahl D., Uyeda C.T. Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res. 43:1972;429-435.
4. Björklund A., Lindvall O. Cell replacement therapies for central nervous system disorders. Nat. Neurosci. 3:2000;537-544.
5. Brüstle O., Choudhary K., Karram K., Huttner A., Murray K., Dubois-Dalcq M., McKay R.D. Chimeric brains generated by intraventricular transplantation of fetal human brain cells into embryonic rats. Nat. Biotechnol. 16:1998;1040-1044.
6. Buc-Caron M.H. Neuroepithelial progenitor cells explanted from human fetal brain proliferate and differentiate in vitro. Neurobiol. Dis. 2:1995;37-47.
7. Caldwell M.A., He X., Wilkie N., Pollack S., Marshall G., Wafford K.A., Svendsen C.N. Growth factors regulate the survival and fate of cells derived from human neurospheres. Nat. Biotechnol. 19:2001;475-479.
8. Carpenter M.K., Cui X., Hu Z.Y., Jackson J., Sherman S., Seiger Å., Wahlberg L.U. In vitro expansion of a multipotent population of human neural progenitor cells. Exp. Neurol. 158:1999;265-278.
9. Cunningham M.G., McKay R.D. A hypothermic miniaturized stereotaxic instrument for surgery in newborn rats. J. Neurosci. Methods. 47:1993;105-114.
10. Deacon T.W., Pakzaban P., Isacson O. The lateral ganglionic eminence is the origin of cells committed to striatal phenotypes neural transplantation and developmental evidence . Brain Res. 668:1994;211-219.
11. Doetsch F., Caille I., Lim D.A., Garcia-Verdugo J.M., Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 97:1999;703-716.
12. Englund U., Björklund A., Wictorin K. Migration patterns and phenotypic differentiation of long-term expanded human neural progenitor cells after transplantation into the adult rat brain. Brain Res. Dev. Brain Res. 134:2002;123-141.
13. Englund U., Fricker-Gates R.A., Lundberg C., Björklund A., Wictorin K. Transplantation of human neural progenitor cells into the neonatal rat brain extensive migration and differentiation with long-distance axonal projections . Exp. Neurol. 173:2002;1-21.
14. Englund U., Ericson C., Rosenblad C., Mandel R.J., Trono D., Wictorin K., Lundberg C. The use of a recombinant lentiviral vector for ex vivo gene transfer into the rat CNS. NeuroReport. 11:2000;3973-3977.
15. Eriksson C., Ericson C., Gates M.A., Wictorin K. Long-term, EGF-stimulated cultures of attached GFAP-positive cells derived from the embryonic mouse lateral ganglionic eminence in vitro and transplantation studies . Exp. Neurol. 164:2000;184-199.
16. Flax J.D., Aurora S., Yang C., Simonin C., Wills A.M., Billinghurst L.L., Jendoubi M., Sidman R.L., Wolfe J.H., Kim S.U., Snyder E.Y. Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nat. Biotechnol. 16:1998;1033-1039.
17. Francis F., Koulakoff A., Boucher D., Chafey P., Schaar B., Vinet M.C., Friocourt G., McDonnell N., Reiner O., Kahn A., McConnell S.K., Berwald-Netter Y., Denoulet P., Chelly J. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron. 23:1999;247-256.
18. Frederiksen K., McKay R.D. Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J. Neurosci. 8:1988;1144-1151.
19. Fricker R.A., Carpenter M.K., Winkler C., Greco C., Gates M.A., Björklund A. Site-specific migration and neuronal differentiation of human neural progenitor cells after transplantation in the adult rat brain. J. Neurosci. 19:1999;5990-6005.
20. Gaiano N., Fishell G. Transplantation as a tool to study progenitors within the vertebrate nervous system. J. Neurobiol. 36:1998;152-161.
21. Gerfen C.R. The neostriatal mosaic multiple levels of compartmental organization . Trends Neurosci. 15:1992;133-139.
22. Gleeson J.G., Lin P.T., Flanagan L.A., Walsh C.A. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron. 23:1999;257-271.
23. Hack I., Bancila M., Loulier K., Carroll P., Cremer H. Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis. Nat. Neurosci. 5:2002;939-945.
24. Hockfield S., McKay R.D. Identification of major cell classes in the developing mammalian nervous system. J. Neurosci. 5:1985;3310-3328.
25. Johansson C.B., Svensson M., Wallstedt L., Janson A.M., Frisen J. Neural stem cells in the adult human brain. Exp. Cell. Res. 253:1999;733-736.
26. Kirschenbaum B., Nedergaard M., Preuss A., Barami K., Fraser R.A., Goldman S.A. In vitro neuronal production and differentiation by precursor cells derived from the adult human forebrain. Cereb. Cortex. 4:1994;576-589.
27. Kukekov V.G., Laywell E.D., Suslov O., Davies K., Scheffler B., Thomas L.B., O'Brien T.F., Kusakabe M., Steindler D.A. Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of adult human brain. Exp. Neurol. 156:1999;333-344.
28. Laywell E.D., Rakic P., Kukekov V.G., Holland E.C., Steindler D.A. Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc. Natl. Acad. Sci. USA. 97:2000;13883-13888.
29. Lois C., Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science. 264:1994;1145-1148.
30. Lund R.D., Banerjee R. Immunological considerations in neural transplantation. Dunnett S.B., Björklund A. Neural Transplantation A Practical Approach . 1992;161-176 Oxford University Press, Oxford, UK.
31. Lundberg C., Englund U., Trono D., Björklund A., Wictorin K. Differentiation of the RN33B cell line into forebrain projection neurons after transplantation into the neonatal rat brain. Exp. Neurol. 175:2002;370-387.
32. Luskin M.B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron. 11:1993;173-189.
33. Martinez-Serrano A., Rubio F.J., Navarro B., Bueno C., Villa A. Human neural stem and progenitor cells in vitro and in vivo properties, and potential for gene therapy and cell replacement in the CNS . Curr. Gene Ther. 1:2001;279-299.
34. Naldini L. Lentiviruses as gene transfer agents for delivery to non-dividing cells. Curr. Opin. Biotechnol. 9:1998;457-463.
35. Olsson M., Campbell K., Turnbull D.H. Specification of mouse telencephalic and mid-hindbrain progenitors following heterotopic ultrasound-guided embryonic transplantation. Neuron. 19:1997;761-772.
36. Olsson M., Björklund A., Campbell K. Early specification of striatal projection neurons and interneuronal subtypes in the lateral and medial ganglionic eminence. Neuroscience. 84:1998;867-876.
37. Olsson M., Campbell K., Wictorin K., Bjorklund A. Projection neurons in fetal striatal transplants are predominantly derived from the lateral ganglionic eminence. Neuroscience. 69:1995;1169-1182.
38. Ostenfeld T., Caldwell M.A., Prowse K.R., Linskens M.H., Jauniaux E., Svendsen C.N. Human neural precursor cells express low levels of telomerase in vitro and show diminishing cell proliferation with extensive axonal outgrowth following transplantation. Exp. Neurol. 164:2000;215-226.
39. Ourednik V., Ourednik J., Flax J.D., Zawada W.M., Hutt C., Yang C., Park K.I., Kim S.U., Sidman R.L., Freed C.R., Snyder E.Y. Segregation of human neural stem cells in the developing primate forebrain. Science. 293:2001;1820-1824.
40. Pagano S.F., Impagnatiello F., Girelli M., Cova L., Grioni E., Onofri M., Cavallaro M., Etteri S., Vitello F., Giombini S., Solero C.L., Parati E.A. Isolation and characterization of neural stem cells from the adult human olfactory bulb. Stem Cells. 18:2000;295-300.
41. Palmer T.D., Schwartz P.H., Taupin P., Kaspar B., Stein S.A., Gage F.H. Cell culture progenitor cells from human brain after death . Nature. 411:2001;42-43.
42. Peterson, D.A., 1999. The use of fluorescent probes in cell counting procedures, in: Janson, A.M., Möller, A. (Eds.), Quantitative methods in neuroscience-a neuroanatomical approach, Oxford University Press, Oxford, UK.
43. Pinching A.J., Powell T.P. The neuron types of the glomerular layer of the olfactory bulb. J. Cell. Sci. 9:1971;305-345.
44. Reynolds B.A., Tetzlaff W., Weiss S. A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J. Neurosci. 12:1992;4565-4574.
45. Rosser A.E., Tyers P., Dunnett S.B. The morphological development of neurons derived from EGF- and FGF-2-driven human CNS precursors depends on their site of integration in the neonatal rat brain. Eur. J. Neurosci. 12:2000;2405-2413.
46. Rubio F.J., Bueno C., Villa A., Navarro B., Martinez-Serrano A. Genetically perpetuated human neural stem cells engraft and differentiate into the adult mammalian brain. Mol. Cell. Neurosci. 16:2000;1-13.
47. Seri B., Garcia-Verdugo J.M., McEwen B.S., Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21:2001;7153-7160.
48. Shihabuddin L.S., Hertz J.A., Holets V.R., Whittemore S.R. The adult CNS retains the potential to direct region-specific differentiation of a transplanted neuronal precursor cell line. J. Neurosci. 15:1995;6666-6678.
49. Skogh C., Eriksson C., Kokaia M., Meijer X.C., Wahlberg L.U., Wictorin K., Campbell K. Generation of regionally specified neurons in expanded glial cultures derived from the mouse and human lateral ganglionic eminence. Mol. Cell. Neurosci. 17:2001;811-820.
50. Stenman J., Toresson H., Campbell K. Identification of two distinct progenitor populations in the lateral ganglionic eminence implications for striatal and olfactory bulb neurogenesis . J. Neurosci. 23:2003;167-174.
51. Svendsen C.N., Smith A.G. New prospects for human stem-cell therapy in the nervous system. Trends Neurosci. 22:1999;357-364.
52. Svendsen C.N., Caldwell M.A. Neural stem cells in the developing central nervous system implications for cell therapy through transplantation . Prog. Brain Res. 127:2000;13-34.
53. Svendsen C.N., ter Borg M.G., Armstrong R.J., Rosser A.E., Chandran S., Ostenfeld T., Caldwell M.A. A new method for the rapid and long term growth of human neural precursor cells. J. Neurosci. Methods. 85:1998;141-152.
54. Svendsen C.N., Caldwell M.A., Shen J., ter Borg M.G., Rosser A.E., Tyers P., Karmiol S., Dunnett S.B. Long-term survival of human central nervous system progenitor cells transplanted into a rat model of Parkinson's disease. Exp. Neurol. 148:1997;135-146.
55. Tamaki S., Eckert K., He D., Sutton R., Doshe M., Jain G., Tushinski R., Reitsma M., Harris B., Tsukamoto A., Gage F., Weissman I., Uchida N. Engraftment of sorted/expanded human central nervous system stem cells from fetal brain. J. Neurosci. Res. 69:2002;976-986.
56. Thor S., Ericson J., Brännstrom T., Edlund T. The homeodomain LIM protein Isl-1 is expressed in subsets of neurons and endocrine cells in the adult rat. Neuron. 7:1991;881-889.
57. Toresson H., Campbell K. A role for Gsh1 in the developing striatum and olfactory bulb of Gsh2 mutant mice. Development. 128:2001;4769-4780.
58. Toresson H., Potter S.S., Campbell K. Genetic control of dorsal-ventral identity in the telencephalon opposing roles for Pax6 and Gsh2 . Development. 127:2000;4361-4371.
59. Uchida N., Buck D.W., He D., Reitsma M.J., Masek M., Phan T.V., Tsukamoto A.S., Gage F.H., Weissman I.L. Direct isolation of human central nervous system stem cells. Proc. Natl. Acad. Sci. USA. 97:2000;14720-14725.
60. Wang H.F., Liu F.C. Developmental restriction of the LIM homeodomain transcription factor Islet-1 expression to cholinergic neurons in the rat striatum. Neuroscience. 103:2001;999-1016.
61. Whittemore S.R., Onifer S.M. Immortalized neural cell lines for CNS transplantation. Prog. Brain Res. 127:2000;49-65.
62. Wichterle H., Garcia-Verdugo J.M., Herrera D.G., Alvarez-Buylla A. Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat. Neurosci. 2:1999;461-466.
63. Wichterle H., Turnbull D.H., Nery S., Fishell G., Alvarez-Buylla A. In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development. 128:2001;3759-3771.
64. Yun K., Potter S., Rubenstein J.L. Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development. 128:2001;193-205.
65. Zigova T., Betarbet R., Soteres B.J., Brock S., Bakay R.A., Luskin M.B. A comparison of the patterns of migration and the destinations of homotopically transplanted neonatal subventricular zone cells and heterotopically transplanted telencephalic ventricular zone cells. Dev. Biol. 173:1996;459-474.
66. Zufferey R., Nagy D., Mandel R.J., Naldini L., Trono D. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat. Biotechnol. 15:1997;871-875.