Review point on neural stem cells and neurogenic areas of the central nervous system

Erika Toledo da Fonseca, Ana Carolina Furlanetto Mançanares, Carlos Eduardo Ambrósio, Maria Angélica Miglino

Department of Basic Sciences of the School of Animal Science and Food Engineering, University of S?o Paulo, S?o Paulo, Brazil.
Department of Surgery, School of Veterinary Medicine and Animal Science, University of S?o Paulo, S?o Paulo, Brazil;.

DOI: 10.4236/ojas.2013.33036                

Abstract

The potential applications of neural stem cells (NSC) in the therapy of degenerative and traumatic diseases of the central nervous system (CNS) have aroused great scientific interest. NSCs can be recovered from specific areas of the CNS from fetuses, embryos and from adult brain as well, and under appropriate culture conditions, may be induced to differentiate into the three major neural cell types, neurons, astrocytes and oligodendrocytes. The main neurogenic areas of mammals are the subventricular zone (SVZ) and the dentate gyrus (DG) of the hippocampus, yet other areas of neurogenic potential have been identified, including frontal and parietal cortices, hippocampus and lateral wall of the lateral ventricle. Neural stem cells and differentiated neural cells are usually identified by expression of specific markers, proteins that are expressed by different cell types and/or at different stages of differentiation. The main cell markers are nestin and Sox-2 for undifferentiated NSCs, beta-III tubulin (B-III tubulin) for neurons, Galactocerebroside (GalC) for oligodendrocytes and Glial fibrillary acid protein (GFAP) for astrocytes. In general, the main neurogenic areas, the neurogenic potential of NSC and the morphological and biological characteristics of differentiated neural cells are strikingly similar among species, yet some differences have been reported. This article presents a brief review of NSCs, neurogenic areas and techniques used for their identification and characterization in humans and experimental animals.

Keywords

Neurogenesis; Neural Stem Cells; Subventricular Zone; Hippocampus

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Chou Gage, F.H. (2000) Mammalian neural stem cells. Science, 287, 1433-1438. doi:10.1126/science.287.5457.1433
[2]	Taupin, P. and Gage, F.H. (2002) Adult neurogenesis and neural stem cells of the central nervous system in mammals. Journal of Neuroscience Research, 69, 745-749. doi:10.1002/jnr.10378
[3]	Jandial, R., Singec, I., Duenas, V.J., Ho, A.L., Levy, M.L. and Snyder, E.Y. (2007) Central nervous system repair and stem cells. International Congress Series, 1302, 154163. doi:10.1016/j.ics.2007.02.062
[4]	Doetsch, F. (2003) The glial identity of neural stem cells. Nature Neuroscience, 6, 1127-1134. doi:10.1038/nn1144
[5]	Gotz, M. and Huttner, W.B. (2005) The cell biology of neurogenesis. Nature Reviews Molecular Cell Biology, 6, 777-788. doi:10.1038/nrm1739
[6]	Alvarez-Buylla, A. and Lois, C. (1995) Neuronal stem cells in the brain of adult vertebrates. Stem Cells, 13, 263-272. doi:10.1002/stem.5530130307
[7]	Bonaguidi, M.A., Peng, C.Y., McGuire, T., Falciglia, G., Gobeske, K.T., Czeisler, C. and Kessler, J.A. (2008) Noggin expands neural stem cells in the adult hippocampus. The Journal of Neuroscience, 28, 9194-9204. doi:10.1523/JNEUROSCI.3314-07.2008
[8]	Buddensiek, J., Dressel, A., Kowalski, M., Runge, U., Schroeder, H., Hermann, A., Kirsch, M., Storch, A. and Sabolek, M. (2010) Cerebrospinal fluid promotes survival and astroglial differentiation of adult human neural progenitor cells but inhibits proliferation and neuronal differentiation. BMC Neuroscience, 11, 48. doi:10.1186/1471-2202-11-48
[9]	Arsenijevic, Y., Villemure, J.G., Brunet, J.F., Bloch, J.J., Deglon, N., Kostic, C., Zurn, A. and Aebischer, P. (2001) Isolation of multipotent neural precursors residing in the cortex of the adult human brain. Experimental Neurology, 170, 48-62. doi:10.1006/exnr.2001.7691
[10]	Frisen, J., Johansson, C.B., Lothian, C. and Lendahl, U. (1998) Central nervous system stem cells in the embryo and adult. Cellular and Molecular Life Sciences, 54, 935945. doi:10.1007/s000180050224
[11]	Johansson, C.B., Momma, S., Clarke, D.L., Risling, M., Lendahl, U. and Frisen, J. (1999) Identification of a neural stem cell in the adult mammalian central nervous system. Cell, 96, 25-34. doi:10.1016/S0092-8674(00)80956-3
[12]	Johansson, C.B., Svensson, M., Wallstedt, L., Janson, A.M. and Frisen, J. (1999) Neural stem cells in the adult human brain. Experimental Cell Research, 253, 733-736. doi:10.1006/excr.1999.4678
[13]	Mansergh, F.C., Wride, M.A. and Rancourt, D.E. (2003) Neurons stem cells and potential therapies. In: Sell, S., Ed., Stem Cells Handbook. Humana Press, New Jersey, 177-190. doi:10.1385/1-59259-411-5:177
[14]	Shamblott, M.J., Axelman, J., Wang, S., Bugg, E.M., Littlefield, J.W., Donovan, P.J., Blumenthal, P.D., Huggins, G.R. and Gearhart, J.D. (1998) Derivation of pluripotent stem cells from cultured human primordial germ cells. Proceedings of the National Academy of Sciences, 95, 13726-13731. doi:10.1073/pnas.95.23.13726
[15]	Thomson, J.A., Itskovitz-Eldor, J., Shapiro, S.S., Waknitz, M.A., Swiergiel, J.J., Marshall, V.S. and Jones, J.M. (1998) Embryonic stem cell lines derived from human blastocysts. Science, 282, 1145-1147. doi:10.1126/science.282.5391.1145
[16]	Vescovi, A.L., Parati, E.A., Gritti, A., Poulin, P., Ferrario, M., Wanke, E., Frolichsthal-Schoeller, P., Cova, L., Arcellana-Panlilio, M., Colombo, A. and Galli, R. (1999) Isolation and cloning of multipotential stem cells from the embryonic human CNS and establishment of transplantable human neural stem cell lines by epigenetic stimulation. Experimental Neurology, 156, 71-83. doi:10.1006/exnr.1998.6998
[17]	Piper, D.R., Mujtaba, T., Keyoung, H., Roy, N.S., Goldman, S.A., Rao, M.S. and Lucero, M.T. (2001) Identification and characterization of neuronal precursors and their progeny from human fetal tissue. Journal of Neuroscience Research, 66, 356-368. doi:10.1002/jnr.1228
[18]	Uchida, N., Buck, D.W., He, D., Reitsma, M.J., Masek, M., Phan, T.V., Tsukamoto, A.S., Gage, F.H. and Weissman, I.L. (2000) Direct isolation of human central nervous system stem cells. Proceedings of the National Academy of Sciences, 97, 14720-14725. doi:10.1073/pnas.97.26.14720
[19]	Suslov, O.N., Kukekov, V.G., Ignatova, T.N. and Steindler, D.A. (2002) Neural stem cell heterogeneity demonstrated by molecular phenotyping of clonal neurospheres. Proceedings of the National Academy of Sciences of the United States of America, 99, 14506-14511. doi:10.1073/pnas.212525299
[20]	Schwartz, P.H., Bryant, P.J., Fuja, T.J., Su, H., O’Dowd, D.K. and Klassen, H. (2003) Isolation and characterization of neural progenitor cells from post-mortem human cortex. Journal of Neuroscience Research, 74, 838-851. doi:10.1002/jnr.10854
[21]	Palmer, T.D., Schwartz, P.H., Taupin, P., Kaspar, B., Stein, S.A. and Gage, F.H. (2001) Cell culture: Progenitor cells from human brain after death. Nature, 411, 42-43. doi:10.1038/35075141
[22]	Altman, J. and Bayer, S.A. (1990) Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. The Journal of Comparative Neurology, 301, 325-342. doi:10.1002/cne.903010302
[23]	Crespo, D., Stanfield, B.B. and Cowan, W.M. (1986) Evidence that late-generated granule cells do not simply replace earlier formed neurons in the rat dentate gyrus. Experimental Brain Research, 62, 541-548. doi:10.1007/BF00236032
[24]	Schlessinger, A.R., Cowan, W.M. and Gottlieb, D.I. (1975) An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. The Journal of Comparative Neurology, 159, 149175. doi:10.1002/cne.901590202
[25]	Ara, J., Fekete, S., Zhu, A. and Frank, M. (2010) Characterization of neural stem/progenitor cells expressing VEGF and its receptors in the subventricular zone of newborn piglet brain. Neurochemical Research, 35, 1455-1470. doi:10.1007/s11064-010-0207-2
[26]	Baizabal, J.M. and Covarrubias, L. (2009) The embryonic midbrain directs neuronal specification of embryonic stem cells at early stages of differentiation. Developmental Biology, 325, 49-59. doi:10.1016/j.ydbio.2008.09.024
[27]	Li, H.W., Liu, H., Corrales, C.E., Risner, J.R., Forrester, J., Holt, J.R., Heller, S. and Edge, A.S.B. (2009) Differentiation of neurons from neural precursors generated in floating spheres from embryonic stem cells. BMC Neuroscience, 10, 122. doi:10.1186/1471-2202-10-122
[28]	Yokoyama, A., Yang, L., Itoh, S., Mori, K. and Tanaka, J. (2004) Microglia, a potential source of neurons, astrocytes, and oligodendrocytes. Glia, 45, 96-104. doi:10.1002/glia.10306
[29]	Komitova, M. and Eriksson, P.S. (2004) Sox-2 is expressed by neural progenitors and astroglia in the adult rat brain. Neuroscience Letters, 369, 24-27. doi:10.1016/j.neulet.2004.07.035
[30]	Kornack, D.R. and Rakic, P. (2001) The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proceedings of the National Academy of Sciences, 98, 4752-4757. doi:10.1073/pnas.081074998
[31]	Guidi, S., Ciani, E., Severi, S., Contestabile, A. and Bartesaghi, R. (2005) Postnatal neurogenesis in the dentate gyrus of the guinea pig. Hippocampus, 15, 285-301. doi:10.1002/hipo.20050
[32]	Jiao, J. and Chen, D.F. (2008) Induction of neurogenesis in nonconventional neurogenic regions of the adult central nervous system by niche astrocyte-produced signals. Stem Cells, 26, 1221-1230. doi:10.1634/stemcells.2007-0513
[33]	Conti, L., Reitano, E. and Cattaneo, E. (2006) Neural stem cell systems: Diversities and properties after transplantation in animal models of diseases. Brain Pathology, 16, 143-154. doi:10.1111/j.1750-3639.2006.00009.x
[34]	Liu, S.Y., Zhang, Z.Y., Song, Y.C., Qiu, K.J., Zhang, K.C., An, N., Zhou, Z., Cal, W.Q. and Yang, H. (2004) SVZa neural stem cells differentiate into distinct lineages in response to BMP4. Experimental Neurology, 190, 109-121. doi:10.1016/j.expneurol.2004.07.015
[35]	Seaberg, R.M. and van der Kooy, D. (2002) Adult rodent neurogenic regions: The ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. The Journal of Neuroscience, 22, 1784-1793.
[36]	Alvarez-Buylla, A. and Garcia-Verdugo, J.M. (2002) Neurogenesis in adult subventricular zone. The Journal of neuroscience, 22, 629-634.
[37]	Smith, R., Bagga, V. and Fricker-Gates, R.A. (2003) Embryonic neural progenitor cells: the effects of species, region, and culture conditions on long-term proliferation and neuronal differentiation. Journal of Hematotherapy & Stem Cell Research, 12, 713-725. doi:10.1089/15258160360732731
[38]	Yokoyama, A., Sakamoto, A., Kameda, K., Imai, Y. and Tanaka, J. (2006) NG2 proteoglycan-expressing microglia as multipotent neural progenitors in normal and pathologic brains. Glia, 53, 754-768. doi:10.1002/glia.20332
[39]	Ren, Y.J., Zhang, H., Huang, H., Wang, X.M., Zhou, Z.Y., Cui, F.Z. and An, Y.H. (2009) In vitro behavior of neural stem cells in response to different chemical functional groups. Biomaterials, 30, 1036-1044. doi:10.1016/j.biomaterials.2008.10.028
[40]	Altman, J. and Das, G.D. (1967) Postnatal neurogenesis in the guinea-pig. Nature, 214, 1098-1101. doi:10.1038/2141098a0
[41]	Skalnikova, H., Vodicka, P., Pelech, S., Motlik, J., Gadher, S.J. and Kovarova, H. (2008) Protein signaling pathways in differentiation of neural stem cells. Proteomics, 8, 4547-4559. doi:10.1002/pmic.200800096