Age-related changes in astrocytic and ependymal cells of the subventricular zone

GLIA

Volumn 62, Issue 5, 2014, Pages 790-803

  Capilla Gonzalez, Vivian ^a   Cebrian Silla, Arantxa ^b   Guerrero Cazares, Hugo ^a   Garcia Verdugo, Jose Manuel ^b   Quiñones Hinojosa, Alfredo ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Aging; Astrocytes; Ependymal cells; Neural stem cells; Subventricular zone; Ultrastructure

Indexed keywords

BROXURIDINE; FAT DROPLET; NESTIN; THYMIDINE;

AGING; ANIMAL CELL; ARTICLE; ASTROCYTE; AUTORADIOGRAPHY; BRAIN TISSUE; CELL PROLIFERATION; CONTROLLED STUDY; DENSE BODY; ELECTRON MICROSCOPY; EPENDYMA CELL; IMMUNOHISTOCHEMISTRY; INTERMEDIATE FILAMENT; LATERAL BRAIN VENTRICLE; MOUSE; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; SENESCENCE; SUBVENTRICULAR ZONE; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CYTOLOGY; EPENDYMA; MALE; PHYSIOLOGY; ULTRASTRUCTURE;

AGING; ANIMALS; ASTROCYTES; CELL DIFFERENTIATION; CELL PROLIFERATION; EPENDYMA; LATERAL VENTRICLES; MALE; MICE; MICE, INBRED C57BL; NEURAL STEM CELLS; NEUROGENESIS;

EID: 84896316261     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22642     Document Type: Article

References (74)

1. Achanta P, Capilla-Gonzalez V, Purger D, Reyes J, Sailor K, Song H, Garcia-Verdugo JM, Gonzalez-Perez O, Ford E, Quinones-Hinojosa A. 2012. Subventricular zone localized irradiation affects the generation of proliferating neural precursor cells and the migration of neuroblasts. Stem Cells 30:2548-2560.
2. Ahlenius H, Visan V, Kokaia M, Lindvall O, Kokaia Z. 2009. 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.
3. Alfaro-Cervello C, Soriano-Navarro M, Mirzadeh Z, Alvarez-Buylla A, Garcia-Verdugo JM. 2012. Biciliated ependymal cell proliferation contributes to spinal cord growth. J Comp Neurol 520:3528-3552.
4. Alvarez-Buylla A, Garcia-Verdugo JM. 2002. Neurogenesis in adult subventricular zone. J Neurosci 22:629-634.
5. Batiz LF, Jimenez AJ, Guerra M, Rodriguez-Perez LM, Toledo CD, Vio K, Paez P, Perez-Figares JM, Rodriguez EM. 2011. New ependymal cells are born postnatally in two discrete regions of the mouse brain and support ventricular enlargement in hydrocephalus. Acta Neuropathol 121:721-735.
6. Bouab M, Paliouras GN, Aumont A, Forest-Berard K, Fernandes KJ. 2011. Aging of the subventricular zone neural stem cell niche: Evidence for quiescence-associated changes between early and mid-adulthood. Neuroscience 173:135-149.
7. Capela A, Temple S. 2002. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 35:865-875.
8. Capilla-Gonzalez V, Cebrian-Silla A, Guerrero-Cazares H, Garcia-Verdugo JM, Quinones-Hinojosa A. 2013a. The generation of oligodendroglial cells is preserved in the rostral migratory stream during aging. Front Cell Neurosci 7:147.
9. Capilla-Gonzalez V, Gil-Perotin S, Ferragud A, Bonet-Ponce L, Canales JJ, Garcia-Verdugo JM. 2012. Exposure to N-ethyl-N-nitrosourea in adult mice alters structural and functional integrity of neurogenic sites. PLoS One 7:e29891.
10. Capilla-Gonzalez V, Gil-Perotin S, Garcia-Verdugo JM. 2010. Postnatal exposure to N-ethyl-N-nitrosurea disrupts the subventricular zone in adult rodents. Eur J Neurosci 32:1789-1799.
11. Capilla-Gonzalez V, Guerrero-Cazares H, Bonsu JM, Gonzalez-Perez O, Achanta P, Wong J, Garcia-Verdugo JM, Quinones-Hinojosa A. 2013b. The subventricular zone is able to respond to a demyelinating lesion after localized radiation. Stem Cells 32:59-69.
12. Carlen M, Meletis K, Goritz C, Darsalia V, Evergren E, Tanigaki K, Amendola M, Barnabe-Heider F, Yeung MS, Naldini L, Honjo T, Kokaia Z, Shupliakov O, Cassidy RM, Lindvall O, Frisen J. 2009. Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke. Nat Neurosci 12:259-267.
13. Chen CT, Shih YR, Kuo TK, Lee OK, Wei YH. 2008. Coordinated changes of mitochondrial biogenesis and antioxidant enzymes during osteogenic differentiation of human mesenchymal stem cells. Stem Cells 26:960-968.
14. Conover JC, Shook BA. 2011. Aging of the subventricular zone neural stem cell niche. Aging Dis 2:49-63.
15. Del Carmen Gomez-Roldan M, Perez-Martin M, Capilla-Gonzalez V, Cifuentes M, Perez J, Garcia-Verdugo JM, Fernandez-Llebrez P. 2008. Neuroblast proliferation on the surface of the adult rat striatal wall after focal ependymal loss by intracerebroventricular injection of neuraminidase. J Comp Neurol 507:1571-1587.
16. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A. 1999a. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-716.
17. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. 1997. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17:5046-5061.
18. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. 1999b. Regeneration of a germinal layer in the adult mammalian brain. Proc Natl Acad Sci USA 96:11619-11624.
19. Encinas JM, Sierra A. 2012. Neural stem cell deforestation as the main force driving the age-related decline in adult hippocampal neurogenesis. Behav Brain Res 227:433-439.
20. Facucho-Oliveira JM, St John JC. 2009. The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation. Stem Cell Rev 5:140-158.
21. Garden GA, Moller T. 2006. Microglia biology in health and disease. J Neuroimmune Pharmacol 1:127-137.
22. Gil-Perotin S, Alvarez-Buylla A, Garcia-Verdugo JM. 2009. Identification and characterization of neural progenitor cells in the adult mammalian brain. Adv Anat Embryol Cell Biol 203:1-101.
23. Gonzalez-Perez O, Gutierrez-Fernandez F, Lopez-Virgen V, Collas-Aguilar J, Quinones-Hinojosa A, Garcia-Verdugo JM. 2012. Immunological regulation of neurogenic niches in the adult brain. Neuroscience 226:270-281.
24. Gritti A, Dal Molin M, Foroni C, Bonfanti L. 2009. Effects of developmental age, brain region, and time in culture on long-term proliferation and multipotency of neural stem cell populations. J Comp Neurol 517:333-349.
25. Guerrero-Cazares H, Gonzalez-Perez O, Soriano-Navarro M, Zamora-Berridi G, Garcia-Verdugo JM, Quinones-Hinojosa A. 2011. Cytoarchitecture of the lateral ganglionic eminence and rostral extension of the lateral ventricle in the human fetal brain. J Comp Neurol 519:1165-1180.
26. Han YG, Spassky N, Romaguera-Ros M, Garcia-Verdugo JM, Aguilar A, Schneider-Maunoury S, Alvarez-Buylla A. 2008. Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat Neurosci 11:277-284.
27. Hatten ME, Liem RK, Shelanski ML, Mason CA. 1991. Astroglia in CNS injury. Glia 4:233-243.
28. Henry CJ, Huang Y, Wynne AM, Godbout JP. 2009. Peripheral lipopolysaccharide (LPS) challenge promotes microglial hyperactivity in aged mice that is associated with exaggerated induction of both pro-inflammatory IL-1beta and anti-inflammatory IL-10 cytokines. Brain Behav Immun 23:309-317.
29. Ihrie RA, Alvarez-Buylla A. 2008. Cells in the astroglial lineage are neural stem cells. Cell Tissue Res 331:179-191.
30. Ihrie RA, Alvarez-Buylla A. 2011. Lake-front property: A unique germinal niche by the lateral ventricles of the adult brain. Neuron 70:674-686.
31. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R. 2008. Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11:1153-1161.
32. Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisen J. 1999. Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96:25-34.
33. Kang SS, Keasey MP, Arnold SA, Reid R, Geralds J, Hagg T. 2012. Endogenous CNTF mediates stroke-induced adult CNS neurogenesis in mice. Neurobiol Dis 49C:68-78.
34. Kazanis I, Lathia JD, Vadakkan TJ, Raborn E, Wan R, Mughal MR, Eckley DM, Sasaki T, Patton B, Mattson MP, Hirschi KK, Dickinson ME, ffrench-Constant C. 2010. Quiescence and activation of stem and precursor cell populations in the subependymal zone of the mammalian brain are associated with distinct cellular and extracellular matrix signals. J Neurosci 30:9771-9781.
35. Kerever A, Schnack J, Vellinga D, Ichikawa N, Moon C, Arikawa-Hirasawa E, Efird JT, Mercier F. 2007. Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor fibroblast growth factor 2 from the extracellular milieu. Stem Cells 25:2146-2157.
36. L'Episcopo F, Tirolo C, Testa N, Caniglia S, Morale MC, Deleidi M, Serapide MF, Pluchino S, Marchetti B. 2012. Plasticity of subventricular zone neuroprogenitors in MPTP (1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine) mouse model of Parkinson's disease involves cross talk between inflammatory and Wnt/beta-catenin signaling pathways: Functional consequences for neuroprotection and repair. J Neurosci 32:2062-2085.
37. L'Episcopo F, Tirolo C, Testa N, Caniglia S, Morale MC, Impagnatiello F, Pluchino S, Marchetti B. 2013. Aging-induced Nrf2-ARE pathway disruption in the subventricular zone drives neurogenic impairment in parkinsonian mice via PI3K-Wnt/beta-catenin dysregulation. J Neurosci 33:1462-1485.
38. Lazarini F, Lledo PM. 2011. Is adult neurogenesis essential for olfaction? Trends Neurosci 34:20-30.
39. Lim DA, Tramontin AD, Trevejo JM, Herrera DG, Garcia-Verdugo JM, Alvarez-Buylla A. 2000. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28:713-726.
40. Logan TT, Villapol S, Symes AJ. 2013. TGF-beta superfamily gene expression and induction of the Runx1 transcription factor in adult neurogenic regions after brain injury. PLoS One 8:e59250.
41. Lonergan T, Brenner C, Bavister B. 2006. Differentiation-related changes in mitochondrial properties as indicators of stem cell competence. J Cell Physiol 208:149-153.
42. Lorez HP, Richards JG. 1982. Supra-ependymal serotoninergic nerves in mammalian brain: Morphological, pharmacological and functional studies. Brain Res Bull 9:727-741.
43. Luo J, Daniels SB, Lennington JB, Notti RQ, Conover JC. 2006. The aging neurogenic subventricular zone. Aging Cell 5:139-152.
44. Luo J, Shook BA, Daniels SB, Conover JC. 2008. Subventricular zone-mediated ependyma repair in the adult mammalian brain. J Neurosci 28:3804-3813.
45. Luskin MB, Zigova T, Soteres BJ, Stewart RR. 1997. Neuronal progenitor cells derived from the anterior subventricular zone of the neonatal rat forebrain continue to proliferate in vitro and express a neuronal phenotype. Mol Cell Neurosci 8:351-366.
46. Marichal N, Garcia G, Radmilovich M, Trujillo-Cenoz O, Russo RE. 2009. Enigmatic central canal contacting cells: Immature neurons in "standby mode"? J Neurosci 29:10010-10024.
47. Maslov AY, Barone TA, Plunkett RJ, Pruitt SC. 2004. Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice. J Neurosci 24:1726-1733.
48. McGinn MJ, Colello RJ, Sun D. 2012. Age-related proteomic changes in the subventricular zone and their association with neural stem/progenitor cell proliferation. J Neurosci Res 90:1159-1168.
49. Mirzadeh Z, Merkle FT, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A. 2008. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3:265-278.
50. Mokry J, Karbanova J. 2006. Foetal mouse neural stem cells give rise to ependymal cells in vitro. Folia Biol (Praha) 52:149-155.
51. Morrens J, Van Den Broeck W, Kempermann G. 2012. Glial cells in adult neurogenesis. Glia 60:159-174.
52. Njie EG, Boelen E, Stassen FR, Steinbusch HW, Borchelt DR, Streit WJ. 2012. Ex vivo cultures of microglia from young and aged rodent brain reveal age-related changes in microglial function. Neurobiol Aging 33:195 e1-12.
53. Pluchino S, Muzio L, Imitola J, Deleidi M, Alfaro-Cervello C, Salani G, Porcheri C, Brambilla E, Cavasinni F, Bergamaschi A, Garcia-Verdugo JM, Comi G, Khoury SJ, Martino G. 2008. Persistent inflammation alters the function of the endogenous brain stem cell compartment. Brain 131 (Part 10):2564-2578.
54. Ponti G, Obernier K, Guinto C, Jose L, Bonfanti L, Alvarez-Buylla A. 2013. Cell cycle and lineage progression of neural progenitors in the ventricular-subventricular zones of adult mice. Proc Natl Acad Sci USA 110:E1045-E1054.
55. Qin L, Liu Y, Hong JS, Crews FT. 2013. NADPH oxidase and aging drive microglial activation, oxidative stress, and dopaminergic neurodegeneration following systemic LPS administration. Glia 61:855-868.
56. Quinones-Hinojosa A, Sanai N, Soriano-Navarro M, Gonzalez-Perez O, Mirzadeh Z, Gil-Perotin S, Romero-Rodriguez R, Berger MS, Garcia-Verdugo JM, Alvarez-Buylla A. 2006. Cellular composition and cytoarchitecture of the adult human subventricular zone: A niche of neural stem cells. J Comp Neurol 494:415-434.
57. Robel S, Berninger B, Gotz M. 2011. The stem cell potential of glia: Lessons from reactive gliosis. Nat Rev Neurosci 12:88-104.
58. Sanai N, Nguyen T, Ihrie RA, Mirzadeh Z, Tsai HH, Wong M, Gupta N, Berger MS, Huang E, Garcia-Verdugo JM, Rowitch DH, Alvarez-Buylla A. 2011. Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478:382-386.
59. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Garcia-Verdugo JM, Berger MS, Alvarez-Buylla A. 2004. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427:740-744.
60. Sawamoto K, Hirota Y, Alfaro-Cervello C, Soriano-Navarro M, He X, Hayakawa-Yano Y, Yamada M, Hikishima K, Tabata H, Iwanami A, Nakajima K, Toyama Y, Itoh T, Alvarez-Buylla A, Garcia-Verdugo JM, Okano H. 2011. Cellular composition and organization of the subventricular zone and rostral migratory stream in the adult and neonatal common marmoset brain. J Comp Neurol 519:690-713.
61. Sawamoto K, Wichterle H, Gonzalez-Perez O, Cholfin JA, Yamada M, Spassky N, Murcia NS, Garcia-Verdugo JM, Marin O, Rubenstein JL, Tessier-Lavigne M, Okano H, Alvarez-Buylla A. 2006. New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 311:629-632.
62. Schiffer D, Giordana MT, Migheli A, Giaccone G, Pezzotta S, Mauro A. 1986. Glial fibrillary acidic protein and vimentin in the experimental glial reaction of the rat brain. Brain Res 374:110-118.
63. Shen Q, Wang Y, Kokovay E, Lin G, Chuang SM, Goderie SK, Roysam B, Temple S. 2008. Adult SVZ stem cells lie in a vascular niche: A quantitative analysis of niche cell-cell interactions. Cell Stem Cell 3:289-300.
64. Shook BA, Manz DH, Peters JJ, Kang S, Conover JC. 2012. Spatiotemporal changes to the subventricular zone stem cell pool through aging. J Neurosci 32:6947-6956.
65. Spassky N, Merkle FT, Flames N, Tramontin AD, Garcia-Verdugo JM, Alvarez-Buylla A. 2005. Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J Neurosci 25:10-18.
66. Stoll EA, Habibi BA, Mikheev AM, Lasiene J, Massey SC, Swanson KR, Rostomily RC, Horner PJ. 2011. Increased re-entry into cell cycle mitigates age-related neurogenic decline in the murine subventricular zone. Stem Cells 29:2005-2017.
67. Streit WJ, Walter SA, Pennell NA. 1999. Reactive microgliosis. Prog Neurobiol 57:563-581.
68. Tatar C, Bessert D, Tse H, Skoff RP. 2013. Determinants of central nervous system adult neurogenesis are sex, hormones, mouse strain, age, and brain region. Glia 61:192-209.
69. Tavazoie M, Van der Veken L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B, Garcia-Verdugo JM, Doetsch F. 2008. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3:279-288.
70. Thored P, Heldmann U, Gomes-Leal W, Gisler R, Darsalia V, Taneera J, Nygren JM, Jacobsen SE, Ekdahl CT, Kokaia Z, Lindvall O. 2009. Long-term accumulation of microglia with proneurogenic phenotype concomitant with persistent neurogenesis in adult subventricular zone after stroke. Glia 57:835-849.
71. Tonchev AB. 2011. Brain ischemia, neurogenesis, and neurotrophic receptor expression in primates. Arch Ital Biol 149:225-231.
72. Walton NM, Sutter BM, Laywell ED, Levkoff LH, Kearns SM, Marshall GP II, Scheffler B, Steindler DA. 2006. Microglia instruct subventricular zone neurogenesis. Glia 54:815-825.
73. Yan YP, Sailor KA, Vemuganti R, Dempsey RJ. 2006. Insulin-like growth factor-1 is an endogenous mediator of focal ischemia-induced neural progenitor proliferation. Eur J Neurosci 24:45-54.
74. Young CC, van der Harg JM, Lewis NJ, Brooks KJ, Buchan AM, Szele FG. 2012. Ependymal ciliary dysfunction and reactive astrocytosis in a reorganized subventricular zone after stroke. Cereb Cortex 23:647-659.