Quiescent neuronal progenitors are activated in the juvenile guinea pig lateral striatum and give rise to transient neurons

Development (Cambridge)

Volumn 141, Issue 21, 2014, Pages 4065-4075

  Luzzati, Federico ^a   Nato, Giulia ^a   Oboti, Livio ^a   Vigna, Elisa ^b   Rolando, Chiara ^a   Armentano, Maria ^a   Bonfanti, Luca ^a   Fasolo, Aldo ^a   Peretto, Paolo ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Internal capsule; Neural stem cells; Parenchymal progenitors; Postnatal neurogenesis; Striatum; Transient neurons

Indexed keywords

BIOLOGICAL MARKER; BROXURIDINE; LENTIVIRUS VECTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL PROLIFERATION; CELL TYPE; CONTROLLED STUDY; CORPUS STRIATUM; EXTERNAL CAPSULE; FEMALE; GLIA CELL; GUINEA PIG; INTERNEURON; JUVENILE ANIMAL; MALE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; TROPISM; WHITE MATTER; ANIMAL; CYTOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; TISSUE CULTURE TECHNIQUE;

ANIMALS; FEMALE; GUINEA PIGS; MALE; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; TISSUE CULTURE TECHNIQUES;

EID: 84908032740     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.107987     Document Type: Article

References (60)

1. Anthony, T. E., Klein, C., Fishell, G. and Heintz, N. (2004). Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41, 881-890.
2. Arvidsson, A., Collin, T., Kirik, D., Kokaia, Z. and Lindvall, O. (2002). Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8, 963-970.
3. Bédard, A., Cossette, M., Lévesque, M. and Parent, A. (2002). Proliferating cells can differentiate into neurons in the striatum of normal adult monkey. Neurosci. Lett. 328, 213-216.
4. Bi, B., Salmaso, N., Komitova, M., Simonini, M. V., Silbereis, J., Cheng, E., Kim, J., Luft, S., Ment, L. R., Horvath, T. L. et al. (2011). Cortical glial fibrillary acidic protein-positive cells generate neurons after perinatal hypoxic injury. J. Neurosci. 31, 9205-9221.
5. Bonfanti, L. and Peretto, P. (2011). Adult neurogenesis in mammals–a theme with many variations. Eur. J. Neurosci. 34, 930-950.
6. Buffo, A., Rite, I., Tripathi, P., Lepier, A., Colak, D., Horn, A.-P., Mori, T. and Gotz, M. (2008). Origin and progeny of reactive gliosis: a source of multipotent cells in the injured brain. Proc. Natl. Acad. Sci. USA 105, 3581-3586.
7. Chen, J., Magavi, S. S. P. and Macklis, J. D. (2004). Neurogenesis of corticospinal motor neurons extending spinal projections in adult mice. Proc. Natl. Acad. Sci. USA 101, 16357-16362.
8. Cheng, L.-C., Pastrana, E., Tavazoie, M. and Doetsch, F. (2009). miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat. Neurosci. 12, 399-408.
9. Cheung, T. H. and Rando, T. A. (2013). Molecular regulation of stem cell quiescence. Nat. Rev. Mol. Cell Biol. 14, 329-340.
10. Dayer, A. G., Cleaver, K. M., Abouantoun, T. and Cameron, H. A. (2005). New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J. Cell Biol. 168, 415-427.
11. Doetsch, F., Caillé, I., Lim, D. A., García-Verdugo, J. M. and Alvarez-Buylla, A. (1999). Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716.
12. Dull, T., Zufferey, R., Kelly, M., Mandel, R. J., Nguyen, M., Trono, D. and Naldini, L. (1998). A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72, 8463-8471.
13. Emsley, J. G., Mitchell, B. D., Kempermann, G. and Macklis, J. D. (2005). Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog. Neurobiol. 75, 321-341.
14. Eriksson, C., Björklund, A. and Wictorin, K. (2003). Neuronal differentiation following transplantation of expanded mouse neurosphere cultures derived from different embryonic forebrain regions. Exp. Neurol. 184, 615-635.
15. Follenzi, A., Ailles, L. E., Bakovic, S., Geuna, M. and Naldini, L. (2000). Gene transfer by lentiviral vectors is limited by nuclear translocation and rescued by HIV-1 pol sequences. Nat. Genet. 25, 217-222.
16. Fuentealba, L. C., Obernier, K. and Alvarez-Buylla, A. (2012). Adult neural stem cells bridge their niche. Cell Stem Cell 10, 698-708.
17. Garcia, A. D. R., Doan, N. B., Imura, T., Bush, T. G. and Sofroniew, M. V. (2004). GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat. Neurosci. 7, 1233-1241.
18. Garzotto, D., Giacobini, P., Crepaldi, T., Fasolo, A. and De Marchis, S. (2008). Hepatocyte growth factor regulates migration of olfactory interneuron precursors in the rostralmigratory streamthroughMet-Grb2 coupling. J. Neurosci. 28, 5901-5909.
19. Giachino, C., Basak, O., Lugert, S., Knuckles, P., Obernier, K., Fiorelli, R., Frank, S., Raineteau, O., Alvarez-Buylla, A. and Taylor, V. (2013). Molecular diversity subdivides the adult forebrain neural stem cell population. Stem Cells 32, 70-84.
20. Götz, M., Stoykova, A. and Gruss, P. (1998). Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21, 1031-1044.
21. Gould, E., Vail, N., Wagers, M. and Gross, C. G. (2001). Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc. Natl. Acad. Sci. USA 98, 10910-10917.
22. Hack, M. A., Saghatelyan, A., de Chevigny, A., Pfeifer, A., Ashery-Padan, R., Lledo, P.-M. and Götz, M. (2005). Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat. Neurosci. 8, 865-872.
23. Kawaguchi, Y. (1997). Neostriatal cell subtypes and their functional roles. Neurosci. Res. 27, 1-8.
24. Kernie, S. G. and Parent, J. M. (2010). Forebrain neurogenesis after focal Ischemic and traumatic brain injury. Neurobiol. Dis. 37, 267-274.
25. Kohwi, M., Osumi, N., Rubenstein, J. L. R. and Alvarez-Buylla, A. (2005). Pax6 is required for making specific subpopulations of granule and periglomerular neurons in the olfactory bulb. J. Neurosci. 25, 6997-7003.
26. Kriegstein, A. and Alvarez-Buylla, A. (2009). The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 32, 149-184.
27. Künkele, J. and Trillmich, F. (1997) Are precocial young cheaper? Lactation energetics in the guinea pig. Physiol. Zool. 70, 589-596.
28. Le Magueresse, C., Alfonso, J., Khodosevich, K., Arroyo Martín, A. A., Bark, C. and Monyer, H. (2011). “Small axonless neurons”: postnatally generated neocortical interneurons with delayed functional maturation. J. Neurosci. 31, 16731-16747.
29. Lim, D. A., Tramontin, A. D., Trevejo, J. M., Herrera, D. G., García-Verdugo, J. M. and Alvarez-Buylla, A. (2000). Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28, 713-726.
30. Liu, F., You, Y., Li, X., Ma, T., Nie, Y., Wei, B., Li, T., Lin, H. and Yang, Z. (2009). Brain injury does not alter the intrinsic differentiation potential of adult neuroblasts. J. Neurosci. 29, 5075-5087.
31. Lois, C. and Alvarez-Buylla, A. (1993). Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl. Acad. Sci. USA 90, 2074-2077.
32. López-Bendito, G., Cautinat, A., Sánchez, J. A., Bielle, F., Flames, N., Garratt, A. N., Talmage, D. A., Role, L. W., Charnay, P., Marín, O. et al. (2006). Tangential neuronal migration controls axon guidance: a role for neuregulin-1 in thalamocortical axon navigation. Cell 125, 127-142.
33. Lugert, S., Basak, O., Knuckles, P., Haussler, U., Fabel, K., Götz, M., Haas, C. A., Kempermann, G., Taylor, V. and Giachino, C. (2010). Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging. Cell Stem Cell 6, 445-456.
34. Luzzati, F., De Marchis, S., Fasolo, A. and Peretto, P. (2006). Neurogenesis in the caudate nucleus of the adult rabbit. J. Neurosci. 26, 609-621.
35. Luzzati, F., De Marchis, S., Parlato, R., Gribaudo, S., Schütz, G., Fasolo, A. and Peretto, P. (2011a). New striatal neurons in a mouse model of progressive striatal degeneration are generated in both the subventricular zone and the striatal parenchyma. PLoS ONE 6, e25088.
36. Luzzati, F., Fasolo, A. and Peretto, P. (2011b). Combining confocal laser scanning microscopy with serial section reconstruction in the study of adult neurogenesis. Front. Neurosci. 5, 70.
37. Ma, T., Zhang, Q., Cai, Y., You, Y., Rubenstein, J. L. R. and Yang, Z. (2012). A subpopulation of dorsal lateral/caudal ganglionic eminence-derived neocortical interneurons expresses the transcription factor Sp8. Cereb. Cortex 22, 2120-2130.
38. Maekawa, M., Takashima, N., Arai, Y., Nomura, T., Inokuchi, K., Yuasa, S. and Osumi, N. (2005). Pax6 is required for production and maintenance of progenitor cells in postnatal hippocampal neurogenesis. Genes Cells 10, 1001-1014.
39. Marin, O., Anderson, S. A. and Rubenstein, J. L. (2000). Origin and molecular specification of striatal interneurons. J. Neurosci. 20, 6063-6076.
40. Merkle, F. T., Mirzadeh, Z. and Alvarez-Buylla, A. (2007). Mosaic organization of neural stem cells in the adult brain. Science 317, 381-384.
41. Ming, G.-L. and Song, H. (2011). Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70, 687-702.
42. Ninkovic, J. and Götz, M. (2013). Fate specification in the adult brain–lessons for eliciting neurogenesis from glial cells. BioEssays 35, 242-252.
43. Niquille, M., Garel, S., Mann, F., Hornung, J.-P., Otsmane, B., Chevalley, S., Parras, C., Guillemot, F., Gaspar, P., Yanagawa, Y. et al. (2009). Transient neuronal populations are required to guide callosal axons: a role for semaphorin 3C. PLoS Biol. 7, e1000230.
44. Niquille, M., Minocha, S., Hornung, J.-P., Rufer, N., Valloton, D., Kessaris, N., Alfonsi, F., Vitalis, T., Yanagawa, Y., Devenoges, C. et al. (2013). Two specific populations of GABAergic neurons originating from the medial and the caudal ganglionic eminences aid in proper navigation of callosal axons. Dev. Neurobiol. 73, 647-672.
45. Ohira, K., Furuta, T., Hioki, H., Nakamura, K. C., Kuramoto, E., Tanaka, Y., Funatsu, N., Shimizu, K., Oishi, T., Hayashi, M. et al. (2010). Ischemia-induced neurogenesis of neocortical layer 1 progenitor cells. Nat. Neurosci. 13, 173-179.
46. 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. et al. (2001). Segregation of human neural stem cells in the developing primate forebrain. Science 293, 1820-1824.
47. Palmer, T. D., Markakis, E. A., Willhoite, A. R., Safar, F. and Gage, F. H. (1999). Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J. Neurosci. 19, 8487-8497.
48. Ponti, G., Peretto, P. and Bonfanti, L. (2008). Genesis of neuronal and glial progenitors in the cerebellar cortex of peripuberal and adult rabbits. PLoS ONE 3, e2366.
49. Ponti, G., Obernier, K., Guinto, C., Jose, L., Bonfanti, L. and Alvarez-Buylla, A. (2013). Cell cycle and lineage progression of neural progenitors in the ventricularsubventricular zones of adult mice. Proc. Natl. Acad. Sci. USA 110, E1045-E1054.
50. Sato, Y., Hirata, T., Ogawa, M. and Fujisawa, H. (1998). Requirement for earlygenerated neurons recognized by monoclonal antibody Lot1 in the formation of lateral olfactory tract. J. Neurosci. 18, 7800-7810.
51. Schnitzer, J., Franke, W. W. and Schachner, M. (1981). Immunocytochemical demonstration of vimentin in astrocytes and ependymal cells of developing and adult mouse nervous system. J. Cell Biol. 90, 435-447.
52. Scholzen, T. and Gerdes, J. (2000). The Ki-67 protein: from the known and the unknown. J. Cell. Physiol. 182, 311-322.
53. Shihabuddin, L. S., Horner, P. J., Ray, J. and Gage, F. H. (2000). Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. J. Neurosci. 20, 8727-8735.
54. Shin, J. J., Fricker-Gates, R. A., Perez, F. A., Leavitt, B. R., Zurakowski, D. and Macklis, J. D. (2000). Transplanted neuroblasts differentiate appropriately into projection neurons with correct neurotransmitter and receptor phenotype in neocortex undergoing targeted projection neuron degeneration. J. Neurosci. 20, 7404-7416.
55. Sirko, S., Behrendt, G., Johansson, P. A., Tripathi, P., Costa, M. R., Bek, S., Heinrich, C., Tiedt, S., Colak, D., Dichgans, M. et al. (2013). Reactive glia in the injured brain acquire stem cell properties in response to sonic hedgehog. Cell Stem Cell 12, 426-439.
56. Southwell, D. G., Paredes, M. F., Galvao, R. P., Jones, D. L., Froemke, R. C., Sebe, J. Y., Alfaro-Cervello, C., Tang, Y., Garcia-Verdugo, J. M., Rubenstein, J. L. et al. (2012). Intrinsically determined cell death of developing cortical interneurons. Nature 491, 109-113.
57. Tattersfield, A. S., Croon, R. J., Liu, Y.W., Kells, A. P., Faull, R. L. M. and Connor, B. (2004). Neurogenesis in the striatum of the quinolinic acid lesion model of Huntington’s disease. Neuroscience 127, 319-332.
58. Teissier, A., Waclaw, R. R., Griveau, A., Campbell, K. and Pierani, A. (2012). Tangentially migrating transient glutamatergic neurons control neurogenesis and maintenance of cerebral cortical progenitor pools. Cereb. Cortex 22, 403-416.
59. Waclaw, R. R., Allen, Z. J., Bell, S. M., Erdélyi, F., Szabó, G., Potter, S. S. and Campbell, K. (2006). The zinc finger transcription factor Sp8 regulates the generation and diversity of olfactory bulb interneurons. Neuron 49, 503-516.
60. Wang, Y.-Z., Plane, J. M., Jiang, P., Zhou, C. J. and Deng, W. (2011). Concise review: quiescent and active states of endogenous adult neural stem cells: identification and characterization. Stem Cells 29, 907-912.