Vertebrate neural progenitor cells: Subtypes and regulation

Current Opinion in Neurobiology

Volumn 6, Issue 1, 1996, Pages 11-17

  Temple, Sally ^a   Qian, Xueming ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROLIFERATION; CELL TYPE; FOREBRAIN; GENE ISOLATION; INVERTEBRATE; NERVOUS SYSTEM DEVELOPMENT; PRIORITY JOURNAL; REVIEW; STEM CELL; VERTEBRATE;

EID: 0029882104     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(96)80003-1     Document Type: Article

References (65)

1. Jacobson M: Developmental Neurobiology, edn 3. New York: Plenum Publishing Corp; 1991.
2. Kilpatrick TJ, Richards LJ, Bartlett PF: The regulation of neural precursor cells within the mammalian brain. Mol Cell Neurosci 1995, 6:2-15.
3. Leber SM, Sanes JR: Migratory paths of neurons and glia in the embryonic chick spinal cord. J Neurosci 1995, 15:1236-1248.
4. Turner DL, Cepko CL: A common progenitor for neurons and glia persists in rat retina late in development Nature 1987, 328:131-136.
5. Ono K, Bansal R, Payne J, Rutishauser U, Miller RH: Early development and dispersal of oligodendrocyte precursors in the embryonic chick spinal cord. Development 1995, 121:1743-1754.
6. McConnell SK: Constructing the cerebral cortex: neurogenesis and fate determination. Neuron 1995, 15:761-768.
7. Parnavelas JG, Barfield JA, Franke E, Luskin MB: Separate progenitor cells give rise to pyramidal and non-pyramidal neurons in the rat telencephalon. Cereb Cortex 1991, 1:463-468.
8. Hatten ME, Heintz N: Mechanisms of neural patterning and specification in the developing cerebellum. Annu Rev Neurosci 1995, 18:385-408.
9. Lumsden A, Clarke JDW, Keynes R, Fraser S: Early phenotypic choices by neuronal precursors, revealed by clonal analysis of the chick embryo hindbrain. Development 1994, 120:1581-1589. Single cells in embryonic chick hindbrain were injected with fluorescent dye and then allowed to develop in situ for 1-2 days. The resulting clones consisted of 1-46 cells. The majority contained a single neuronal cell type, suggesting that specification occurred early and was remembered through several rounds of division.
10. Potten C, Loeffler M: Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt Development 1990, 110:1001-1020.
11. Davis AA, Temple S: A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature 1994, 372:263-266. A study of the behavior of single cells of the ventricular zone of early rat cerebral cortex. Single cells grown under standardized growth conditions developed differently. The majority gave small clones of neurons, but a subpopulation of these cells generated all three major neural cell types and can self-renew. This demonstrated that a minor population of cortical progenitor cells had the characteristics of multipotential stem cells in vitro.
12. Williams BP, Price J: Evidence for multiple precursor cell types in the embryonic rat cerebral cortex. Neuron 1995, 14:1181-1188. The authors labelled clones growing in mass cultures of cortical cells with retroviral vectors. Single cells had heterogeneous fates, including some cells that had characteristics similar to multipotential cortical stem cells.
13. Reynolds BA, Weiss S: Primary and 10th passage EGF-responsive CNS stem cells exhibit similar proliferative and differentiation potential. Soc Neurosci Abstr 1994, 24:200.18.
14. Franklin RJM, Blakemore WF: Glial cell transplantation and plasticity in the O-2A lineage - implications for CNS repair. Trends Neurosci 1995, 18:151-156.
15. Dexter TM, Spooncer E: Growth and differentiation in the hemopoietic system. Annu Rev Cell Biol 1987, 3:423-441.
16. Stemple DL, Anderson DJ: Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 1992, 71:973-985.
17. Lo L, Anderson DJ: Postmigratory neural crest cells expressing c-RET display restricted developmental and proliferative capacities. Neuron 1995, 15:527-539. Using an antibody to the cell-surface receptor c-RET and FACS, the authors purified a subpopulation of postmigratory neural crest cells from gut and analyzed their developmental potentials under conditions that promote neural crest stem cell development. They demonstrated that the majority of c-RET-positive cells undergo a limited number of cell divisions and differentiate into neurons, even in the presence of glial growth factor II, which suppresses neuronal and promotes glial differentiation of neural crest stem cells, indicating the commitment of c-RET cells to neuronal differentiation.
18. Ogawa M, Porter PN, Nakahata T: Renewal and commitment to differentiation of hemopoietic stem cells (an interpretive review). Blood 1983, 61:823-829.
19. Temple S: Division and differentiation of isolated CNS blast cells in microculture. Nature 1989, 340:471-473.
20. Kilpatrick TJ, Bartlett PF: Cloning and growth of multipotential neural precursors: requirements for proliferation and differentiation. Neuron 1993, 10:255-265.
21. Reid CB, Liang I, Walsh C: Systematic widespread clonal organization in cerebral cortex. Neuron 1995, 15:299-310. The first study to demonstrate the existence of migratory multipotential cells in cerebral cortex in vivo using retroviral lineage tracing. The authors found that widespread clonal progeny, identified by PCR analysis of multiple retroviral tags, consisted of different neural cell types, but each sub-clone was homogeneous. Clones were spaced systematically at 2-3 mm intervals. The authors proposed the existence of multipotential migratory neural precursor cells that divide asymmetrically at intervals defined by cell cycle length, and produce non-migratory progeny in different cortical regions.
22. Kornack DR, Rakic P: Radial and horizontal deployment of clonally related cells in the primate neocortex: relationship to distinct mitotic lineages. Neuron 1995, 15:311-321. Retroviral lineage tracing reveals horizontal and radially arrayed clones. The authors suggest that horizontally arrayed clones arise from symmetric divisions of ventricular zone (VZ) cells that cease at the same time, resulting in a cohort of cell cousins migrating into the cortical plate to occupy the same lamina. In contrast, they suggest radial clones come from asymmetric divisions of a VZ progenitor cell. (An alternative hypothesis to explain horizontal clones is suggested by the Leber and Sanes article [3] in which some clones are initially radial, but then migrate on a tangential trajectory, resulting in clones that are effectively horizontally arrayed.)
23. Vescovi AL, Reynolds BA, Fraser DD, Weiss S: bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron 1993, 11:951-966.
24. Reh TA, Cagan RL: Intrinsic and extrinsic signals in the developing vertebrate and fly eyes: viewing vertebrate and invertebrate eyes in the same light Perspect Dev Neurobiol 1994, 2:183-190.
25. Chenn A, McConnell SK: Cleavage orientation and the asymmetric inheritance of Notch-1 immunoreactivity in mammalian neurogenesis. Cell 1995, 82:631-641. Time-lapse confocal microscopy of Dil-labelled cells in cortical slices reveals horizontal and vertical cleavage planes among ventricular zone (VZ) cells. Daughter cells of horizontal cleavage planes appear to be different. Antibody to human Notch-1 is used to demonstrate that it is differentially localized to basal daughter cells in horizontal divisions.
26. Hirata J, Nakagoshi H, Nabeshima YI, Matsuzaki F: Asymmetric segregation of the homeodomain protein Prospero during Drosophila development Nature 1995, 377:627-630.
27. Spana EP, Doe CQ: The prospero transcription factor is asymmetrically localized to cell cortex during neuroblast mitosis in Drosophila. Development 1995, 121:3187-3195.
28. Knoblich JA, Jan LY, Jan YN: Asymmetric segregation of Numb and Prospero during cell division. Nature 1995, 377:624-627.
29. Rhuys MS, Knoblich JA: Spindle orientation and asymmetric cell fate. Cell 1995, 82:523-526.
30. Doe CQ, Technau GM: Identification and cell lineage of individual neural precursors in the Drosophila CNS. Trends Neurosci 1993, 16:510-513.
31. Jan YN, Jan LY: Maggot's hair and bug's eye: role of cell interactions and intrinsic factors in cell fate specification. Neuron 1995, 14:1-5.
32. Skeath JB, Zhang Y, Holmgren R, Carroll SB, Doe CQ: Specification of neuroblast identity in the Drosophila embryonic central nervous system by gooseberry-distal. Nature 1995, 376:427-430.
33. Yang X, Yeo S, Dick T, Chia W: The role of a Drosophila POU homeodomain gene in the specification of neural precursor cell identity in the developing embryonic central nervous system. Genes Dev 1993, 7:504-516.
34. Yeo SL, Lloyd A, Kozak K, Dinh A, Dick T, Yand X, Sakonju S, Chia W: On the functional overlap between two Drosophila POU homeodomain genes and the cell fate specification of a CNS neural precursor. Genes Dev 1995, 9:1223-1236.
35. Roelink H, Augsburger A, Heemskerk J, Korzh V, Norlin S, Ruiz I Altaba A, Tanabe Y, Placzek M, Edlund T, Jessell T, Dodd J: Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 1994, 76:761-775.
36. Hynes M, Porter JA, Chiang C, Chang D, Tessier-Lavigne M, Beachy PA, Rosenthal A: Induction of midbrain dopaminergic neurons by Sonic Hedgehog. Neuron 1995, 15:35-44.
37. Ericson J, Muhr J, Placzek M, Lints T, Jessell TM, Edlund T: Sonic hedgehog induces the differentiation of ventral forebrain neurons: a common signal for ventral patterning along the rostrocaudal axis of the neural tube. Cell 1995, 81:747-756.
38. Rubenstein JL, Martinez S, Shimamura KP, Puelles L: The embryonic vertebrate forebrain: the prosomeric model. Science 1994, 266:578-580.
39. Thor S: The genetics of brain development: conserved programs in flies and mice. Neuron 1995, 15:975-977.
40. Shimizu C, Akazawa S, Nakanishi S, Kageyama R: MATH-2, a mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal, is specifically expressed in the nervous system. Eur J Biochem 1995, 229:239-248.
41. Akazawa C, Ishibashi M, Shimizu C, Nakanishi S, Kageyama R: A mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal is a positive transcriptional regulator expressed in the developing nervous system. J Biol Chem 1995, 15:8730-8738.
42. Xuan S, Baptista CA, Balas G, Tao W, Soares VC, Lai E: Winged helix transcription factor BF-1 is essential for the development of the cerebral hemispheres. Neuron 1995, 14:1141-1152. Gene targeting provides evidence that BF-1 is important for development of the telencephalon. The authors propose that BF-1 is involved in the regulation of neural progenitor cell proliferation.
43. -l- mutants due to a defective anterior neuroectoderm specification during gastrulation. Development 1995, 121:3279-3290.
44. Ruiz I Altaba A: Pattern formation in the vertebrate neural plate. Trends Neurosci 1994, 7:233-243.
45. Fishell G: Striatal precursors adopt cortical identities in response to local cues. Development 1995, 121:803-812. Labelled embryonic striatal cells transplanted into cerebral cortex take on cortical morphologies and adopt cortical-specific axonal trajectories. This demonstrates that although regional neural characteristics are established early in development, individual progenitor cells are not yet committed to a particular regional identity at the ages examined. By the same token, environmental signals appear to play an instructive role in determining regional phenotype.
46. Campbell K, Olsson M, Bjorklund A: Regional incorporation and site-specific differentiation of striatal precursors transplanted to the embryonic forebrain ventricle. Neuron 1995, 15:1259-1273.
47. Brustle O, Maskos U, McKay RDG: Host-guided migration allows targeted introduction of neurons into the embryonic brain. Neuron 1995, 15:1275-1285.
48. Schoenherr CJ, Anderson DJ: The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science 1995, 267:1360-1363.
49. •].
50. •] provided evidence that glial cells missing (gcm) plays an important role in the cell fate switch between neurons and glia. Loss of function results in a failure of glial differentiation, whereas gain of function promotes presumptive neuroblast to a glial fate. The gcm gene encodes a novel nuclear protein, and analysis of its downstream targets is likely to provide insights into the molecular mechanisms that control neural cell fate determination.
51. Jin Y, Hoskins R, Horvitz HR: Control of type-D GABAergic neuron differentiation by C. elegans UNC-30 homeodomain protein. Nature 1994, 372:780-783.
52. Dehamer MK, Guevara JL, Hannon K, Olwin BB, Calof AL: Genesis of olfactory receptor neurons in vitro: regulation of progenitor cell divisions by fibroblast growth factors. Neuron 1994, 13:1083-1097.
53. Gritti A, Parati EA, Cova L, Frolichsthal P, Galli R, Wanke E, Faravelli L, Morassutti DJ, Roisen P, Nickel DD, Vescovi AL: Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J Neurosci 1995, 16:1091-1100. Cells isolated from the adult striatum proliferate and differentiate into neurons, astrocytes and oligodendrocytes in response to bFGF. Neurons also express major neurotransmitters and neuropeptides. These cells self-renew extensively, demonstrating that they are stem cells.
54. Vaccarino FM, Schwartz ML, Hartigan D, Leckman JF: Basic fibroblast growth factor increases the number of excitatory neurons containing glutamate in the cerebral cortex. Cereb Cortex 1995, 5:64-78.
55. Ghosh A, Greenberg ME: Distinct roles for bFGF and NT-3 in the regulation of cortical neurogenesis. Neuron 1995, 15:89-103.
56. Vicario-Abejon C, Johe KK, Hazel TG, Collazo D, McKay RDG: Functions of basis fibroblast growth factor and neurotrophins in the differentiation of hippocampal neurons. Neuron 1995, 15:105-114.
57. LoTurco JJ, Owens DF, Heath MJS, Davis MBE, Kriegstein AR: GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 1995, 15:1287-1298. The authors demonstrate that ventricular zone cells of the cerebral cortex are depolarized by both GABA and glutamate. Depolarization is accompanied by an increase in intracellular calcium. These acute events are linked to a decrease in progenitor cell division, suggesting that these neurotransmitters may regulate exit of precursor cells from the cell cycle.
58. Kilpatrick TJ, Bartlett PF: Cloned multipotential precursors from the mouse cerebrum require FGF-2, whereas glial restricted precursors are stimulated with either FGF-2 or EGF. J Neurosci 1995, 15:3653-3661.
59. Lillien L: Changes in retinal cell fate induced by overexpression of EGF receptor. Nature 1995, 377:158-162. A wild-type EGF receptor is introduced into retinal progenitor cells using a retroviral vector. The resulting clones contain an increased proportion of Müller glia, demonstrating that modulating the level of EGF receptors normally expressed can influence cell-fate choices.
60. Shah NM, Marchionni MA, Isaaca I, Stroobant P, Anderson DJ: Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 1994, 77:349-360. Multipotential neural crest stem cells, cultured in the presence of glial growth factor (GGF) do not generate neuronal progeny, whereas in the absence of GGF, both neurons and glial cells are generated. The authors also demonstrate that GGF inhibits Mash-1 expression in the stem cell progeny. Their data suggest that the effect of GGF is instructive rather than selective, and they propose that neuron-derived GGF might serve as a feedback mechanism to influence neural crest stem cells to generate diverse progeny.
61. Rougvie AE, Ambros V: The heterochronic gene Lin-29 encodes a zinc finger protein that controls a terminal differentiation event in Caenorhabditis elegans. Development 1995, 121:2491-2500.
62. Louis C, Alvarez-Buylla A: Long distance neuronal migration in the adult mammalian brain. Science 1994, 264:1145-1148. Transplanting labelled subventricular zone (SVZ) cells back into adult host reveals that cells migrate long distances to differentiate into olfactory bulb neurons. No other type of neuronal differentiation is observed, suggesting some restriction in SVZ cell fate.
63. Luskin MB: Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 1993, 11:173-189.
64. 3H-thymidine. A relatively quiescent population of SVZ cells was shown to reconstitute this population. The constitutively dividing population appear to correspond to EGF-responsive stem cells, identified in vitro, the precursors to neurospheres.
65. Gage FH, Ray J, Fisher LJ: Isolation, characterization and use of stem cells from the CNS. Annu Rev Neurosci 1995, 18:159-192.