Age-related neurogenesis decline in the subventricular zone is associated with specific cell cycle regulation changes in activated neural stem cells

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Daynac, Mathieu ^a,b,c,d   Morizur, Lise ^a,b,c,d   Chicheportiche, Alexandra ^a,b,c,d   Mouthon, Marc André ^a,b,c,d   Boussin, François D ^a,b,c,d  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^b Universite Paris Sud   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER;

AGE; AGING; ANIMAL; BIOLOGY; CELL COUNT; CELL CYCLE; CLUSTER ANALYSIS; CYTOLOGY; GENE EXPRESSION PROFILING; LATERAL BRAIN VENTRICLE; METABOLISM; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; PROCEDURES; TRANSGENIC MOUSE;

AGE FACTORS; AGING; ANIMALS; BIOMARKERS; CELL COUNT; CELL CYCLE; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; GENE EXPRESSION PROFILING; LATERAL VENTRICLES; MICE; MICE, TRANSGENIC; NEURAL STEM CELLS; NEUROGENESIS;

EID: 84958953576     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep21505     Document Type: Article

References (46)

1. Fuentealba, L. C., Obernier, K., Alvarez-Buylla, A. Adult neural stem cells bridge their niche. Cell Stem Cell 10, 698-708, doi: 10.1016/j.stem.2012.05.012 (2012).
2. Aimone, J. B. et al. Regulation and function of adult neurogenesis: from genes to cognition. Physiol Rev 94, 991-1026 (2014).
3. Morshead, C. M. et al. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13, 1071-1082 (1994).
4. Pastrana, E., Cheng, L. C., Doetsch, F. Simultaneous prospective purification of adult subventricular zone neural stem cells and their progeny. Proc Natl Acad Sci USA 106, 6387-6392 (2009).
5. Daynac, M. et al. Quiescent neural stem cells exit dormancy upon alteration of GABAAR signaling following radiation damage. Stem Cell Res 11, 516-528, doi: 10.1016/j.scr.2013.02.008 (2013).
6. Codega, P. et al. Prospective identification and purification of quiescent adult neural stem cells from their in vivo niche. Neuron 82, 545-559, doi: 10.1016/j.neuron.2014.02.039 (2014).
7. Luo, Y. et al. Single-cell transcriptome analyses reveal signals to activate dormant neural stem cells. Cell 161, 1175-1186, doi: 10.1016/j.cell.2015.04.001 (2015).
8. Llorens-Bobadilla, E. et al. Single-Cell Transcriptomics Reveals a Population of Dormant Neural Stem Cells that Become Activated upon Brain Injury. Cell Stem Cell, 329-40, doi: 10.1016/j.stem.2015.07.002 (2015).
9. 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, 703-716. (1999).
10. Lois, C., GarciaVerdugo, J. M., AlvarezBuylla, A. Chain migration of neuronal precursors. Science 271, 978-981, doi: 10.1126/science.271.5251.978 (1996).
11. Kriegstein, A., Alvarez-Buylla, A. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32, 149-184 (2009).
12. Tropepe, V., Craig, C. G., Morshead, C. M., vanderKooy, D. Transforming growth factor-alpha null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma. J Neurosci 17, 7850-7859 (1997).
13. Enwere, E. et al. Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J Neurosci 24, 8354-8365, doi: 10.1523/Jneurosci.2751-04.2004 (2004).
14. Maslov, A. Y., Barone, T. A., Plunkett, R. J., Pruitt, S. C. Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice. J Neurosci 24, 1726-1733, doi: 10.1523/Jneurosci.4608-03.2004 (2004).
15. Blackmore, D. G., Golmohammadi, M. G., Large, B., Waters, M. J., Rietze, R. L. Exercise Increases Neural Stem Cell Number in a Growth Hormone-Dependent Manner, Augmenting the Regenerative Response in Aged Mice. Stem Cells 27, 2044-2052, doi: 10.1002/stem.120 (2009).
16. Bouab, M., Paliouras, G. N., Aumont, A., Forest-Berard, K., Fernandes, K. J. L. Aging of the Subventricular Zone Neural Stem Cell Niche: Evidence for Quiescence-Associated Changes between Early and Mid-Adulthood. Neuroscience 173, 135-149, doi: 10.1016/j. neuroscience.2010.11.032 (2011).
17. Piccin, D., Tufford, A., Morshead, C. M. Neural stem and progenitor cells in the aged subependyma are activated by the young niche. Neurobiol Aging 35, 1669-1679, doi: 10.1016/j.neurobiolaging.2014.01.026 (2014).
18. Daynac, M. et al. TGFbeta lengthens the G1 phase of stem cells in aged mouse brain. Stem Cells 32, 3257-3265, doi: 10.1002/stem.1815 (2014).
19. Ahlenius, H., Visan, V., Kokaia, M., Lindvall, O., Kokaia, Z. Neural Stem and Progenitor Cells Retain Their Potential for Proliferation and Differentiation into Functional Neurons Despite Lower Number in Aged Brain. J Neurosci 29, 4408-4419, doi: 10.1523/Jneurosci.6003-08.2009 (2009).
20. Capilla-Gonzalez, V., Cebrian-Silla, A., Guerrero-Cazares, H., Garcia-Verdugo, J. M., Quinones-Hinojosa, A. Age-Related Changes in Astrocytic and Ependymal Cells of the Subventricular Zone. Glia 62, 790-803, doi: 10.1002/glia.22642 (2014).
21. Lugert, S. et al. 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, doi: 10.1016/j.stem.2010.03.017 (2010).
22. Balordi, F., Fishell, G. Mosaic removal of hedgehog signaling in the adult SVZ reveals that the residual wild-type stem cells have a limited capacity for self-renewal. J Neurosci 27, 14248-14259 (2007).
23. Shook, B. A., Manz, D. H., Peters, J. J., Kang, S., Conover, J. C. Spatiotemporal Changes to the Subventricular Zone Stem Cell Pool through Aging. J Neurosci 32, 6947-6956, doi: 10.1523/Jneurosci.5987-11.2012 (2012).
24. Pineda, J. R. et al. Vascular-derived TGF-beta increases in the stem cell niche and perturbs neurogenesis during aging and following irradiation in the adult mouse brain. Embo Mol Med 5, 548-562 (2013).
25. Fischer, J. et al. Prospective isolation of adult neural stem cells from the mouse subependymal zone. Nat Protoc 6, 1981-1989, doi: 10.1038/nprot.2011.412 (2011).
26. Mich, J. K. et al. Prospective identification of functionally distinct stem cells and neurosphere-initiating cells in adult mouse forebrain. Elife 3, e02669 (2014).
27. Capela, A., Temple, S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 35, 865-875 (2002).
28. Obermair, F. J. et al. A novel classification of quiescent and transit amplifying adult neural stem cells by surface and metabolic markers permits a defined simultaneous isolation. Stem Cell Res 5, 131-143, doi: 10.1016/j.scr.2010.05.001 (2010).
29. Daynac, M., Morizur, L., Kortulewski, T., Gauthier, L. R., Ruat, M., Mouthon, M. A., Boussin, F. D. Cell Sorting of Neural Stem and Progenitor Cells from the Adult Mouse Subventricular Zone and Live-imaging of their Cell Cycle Dynamics. J. Vis. Exp, doi: 10.3791/53247 (2015).
30. Sakaue-Sawano, A. et al. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 132, 487-498 (2008).
31. Mouthon, M. A. et al. Neural stem cells from mouse forebrain are contained in a population distinct from the 'side population'. J Neurochem 99, 807-817 (2006).
32. Reynolds, B. A., Weiss, S. Generation of Neurons and Astrocytes from Isolated Cells of the Adult Mammalian Central-Nervous-System. Science 255, 1707-1710, doi: 10.1126/science.1553558 (1992).
33. Costa, M. R. et al. Continuous live imaging of adult neural stem cell division and lineage progression in vitro. Development 138, 1057-1068, doi: 10.1242/dev.061663 (2011).
34. Mi, H. Y., Muruganujan, A., Thomas, P. D. PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees. Nucleic Acids Research 41, D377-D386, doi: 10.1093/nar/gks1118 (2013).
35. Beckervordersandforth, R. et al. In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. Cell Stem Cell 7, 744-758, doi: 10.1016/j.stem.2010.11.017 (2010).
36. Whitfield, M. L. et al. Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Mol Biol Cell 13, 1977-2000, doi: 10.1091/mbc.02-02-0030. (2002).
37. Bar-Joseph, Z. et al. Genome-wide transcriptional analysis of the human cell cycle identifies genes differentially regulated in normal and cancer cells. Proc Natl Acad Sci USA 105, 955-960, doi: 10.1073/pnas.0704723105 (2008).
38. Ishida, S. et al. Role for E2F in control of both DNA replication and mitotic functions as revealed from DNA microarray analysis. Mol Cell Biol 21, 4684-4699, doi: 10.1128/MCB.21.14.4684-4699.2001 (2001).
39. Oka, C. et al. HtrA1 serine protease inhibits signaling mediated by Tgf beta family proteins. Development 131, 1041-1053, |doi: 10.1242/dev.00999 (2004).
40. Graham, J. R. et al. Serine Protease HTRA1 Antagonizes Transforming Growth Factor-beta Signaling by Cleaving Its Receptors and Loss of HTRA1 In Vivo Enhances Bone Formation. Plos One 8, doi: ARTN e7409410.1371/journal.pone.0074094 (2013).
41. Shiga, A. et al. Cerebral small-vessel disease protein HTRA1 controls the amount of TGF-beta 1 via cleavage of proTGF-beta 1. Hum Mol Genet 20, 1800-1810, doi: 10.1093/hmg/ddr063 (2011).
42. Mirzadeh, Z., Merkle, F. T., Soriano-Navarro, M., Garcia-Verdugo, J. M., Alvarez-Buylla, A. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3, 265-278, doi: 10.1016/j. stem.2008.07.004 (2008).
43. Capilla-Gonzalez, V., Cebrian-Silla, A., Guerrero-Cazares, H., Garcia-Verdugo, J. M., Quinones-Hinojosa, A. Age-related changes in astrocytic and ependymal cells of the subventricular zone. Glia 62, 790-803, doi: 10.1002/glia.22642 (2014).
44. Ponti, G. et al. Cell cycle and lineage progression of neural progenitors in the ventricular-subventricular zones of adult mice. Proc Natl Acad Sci USA 110, E1045-1054, doi: 10.1073/pnas.1219563110 (2013).
45. Salomoni, P., Calegari, F. Cell cycle control of mammalian neural stem cells: putting a speed limit on G1. Trends Cell Biol 20, 233-243, doi: 10.1016/j.tcb.2010.01.006 (2010).
46. Hamilton, L. K., Joppe, S. E., Cochard, L. M., Fernandes, K. J. L. Aging and neurogenesis in the adult forebrain: what we have learned and where we should go from here. Eur J Neurosci 37, 1978-1986, doi: 10.1111/ejn.12207 (2013).