Newly born cells in the ageing dentate gyrus display normal migration, survival and neuronal fate choice but endure retarded early maturation

European Journal of Neuroscience

Volumn 21, Issue 2, 2005, Pages 464-476

  Rao, Muddanna S ^a,b   Hattiangady, Bharathi ^a,b   Abdel Rahman, Ali ^b   Stanley, Dirk P ^a,b   Shetty, Ashok K ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b DURHAM VA MEDICAL CENTER   (United States)

Author keywords

5 bromodeoxyuridine; Adult neurogenesis; Ageing; Dendritic growth; Doublecortin; Hippocampus; Neural progenitors; Neural stem cells; Rat

Indexed keywords

BROXURIDINE; CELL NUCLEUS ANTIGEN; DOUBLECORTIN; NEURON SPECIFIC NUCLEAR ANTIGEN; UNCLASSIFIED DRUG;

ADOLESCENT; AGED; AGING; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FATE; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; DENDRITIC CELL; DENTATE GYRUS; GRANULE CELL; HIPPOCAMPUS; MALE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENESCENCE;

AGE FACTORS; AGING; ANALYSIS OF VARIANCE; ANIMALS; BROMODEOXYURIDINE; CELL COUNT; CELL DIFFERENTIATION; CELL ENLARGEMENT; CELL MOVEMENT; CELL SURVIVAL; DENDRITES; DENTATE GYRUS; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; MALE; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; NEUROPEPTIDES; PHOSPHOPYRUVATE HYDRATASE; RATS; RATS, INBRED F344; STEM CELLS; TIME FACTORS;

EID: 13444271905     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.03853.x     Document Type: Article

References (71)

1. Alvarez-Buylla, A. & Lim, D.A. (2004) For the long run: maintaining germinal niches in the adult brain. Neuron, 41, 683-686.
2. Bizon, J.L. & Gallagher, M. (2003) Production of new cells in the rat dentate gyrus over the lifespan: relation to cognitive decline. Eur. J. Neurosci., 18, 215-219.
3. Bondolfi, L., Ermini, F., Long, J.M., Ingram, D.K. & Jucker, M. (2004) Impact of age and caloric restriction on neurogenesis in the dentate gyrus of C57BL/6 mice. Neurobiol. Aging, 25, 333-340.
4. Brown, J.P., Couillard-Despres, S., Cooper-Kuhn, C.M., Winkler, J., Aigner, L. & Kuhn, H.G. (2003) Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol., 467, 1-10.
5. Cameron, H.A. & McKay, R.D. (1999) Restoring production of hippocampal neurons in old age. Nat. Neurosci., 2, 894-897.
6. Cameron, H.A. & McKay, R.D. (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol., 435, 406-417.
7. Cameron, H.A., Woolley, C.S., McEwen, B.S. & Gould, E. (1993) Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience, 56, 337-344.
8. Coleman, G.L., Barthold, W., Osbaldiston, G.W., Foster, S.J. & Jonas, A.M. (1977) Pathological changes during aging in barrier-reared Fischer 344 male rats. J. Gerontol., 32, 258-278.
9. Dayer, A.G., Ford, A.A., Cleaver, K.M., Yassaee, M. & Cameron, H.A. (2003) Short-term and long-term survival of new neurons in the rat dentate gyrus. J. Comp. Neurol., 460, 563-572.
10. Dobrossy, M.D., Drapeau, E., Aurousseau, C., Le Moal, M., Piazza, P.V. & Abrous, D.N. (2003) Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date. Mol. Psychiatry, 8, 974-982.
11. Dorph-Petersen, K.A., Nyengaard, J.R. & Gundersen, H.J. (2001) Tissue shrinkage and unbiased stereological estimation of particle number and size. J. Microsc., 204, 232-246.
12. Drapeau, E., Mayo, W., Aurousseau, C., Le Moal, M., Piazza, P.V. & Abrous, D.N. (2003) Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc. Natl. Acad. Sci. USA, 24, 14385-14390.
13. Eriksson, P.S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A.M., Nordborg, C., Peterson, D.A. & Gage, F.H. (1998) Neurogenesis in the adult human hippocampus. Nat. Med., 4, 1313-1317.
14. Feng, R., Rampon, C., Tang, Y.P., Shrom, D., Jin, J., Kyin, M., Sopher, B., Miller, M.W., Ware, C.B., Martin, G.M., Kim, S.H., Langdon, R.B., Sisodia, S.S. & Tsien, J.Z. (2001) Deficient neurogenesis in forebrain-specific presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces. Neuron, 32, 911-926.
15. Gage, F.H. (2002) Neurogenesis in the adult brain. J. Neurosci., 22, 612-613.
16. Gould, E. (1999) Serotonin and hippocampal neurogenesis. Neuropsychopharmacology, 11, S46-S51.
17. Gould, E., Beylin, A., Tanapat, P., Reeves, A. & Shors, T.J. (1999) Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci., 2, 260-265.
18. Gould, E. & Gross, C.G. (2002) Neurogenesis in adult mammals: some progress and problems. J. Neurosci., 22, 619-623.
19. Gould, E. & Tanapat, P. (1997) Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat. Neuroscience, 80, 427-436.
20. Gould, E., Tanapat, P., McEwen, B.S., Flugge, G. & Fuchs, E. (1998) Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc. Natl. Acad. Sci. USA, 95, 3168-3171.
21. Gray, W.P. & Sundstrom, L.E. (1998) Kainic acid increases the proliferation of granule cell progenitors in the dentate gyrus of the adult rat. Brain Res., 790, 52-59.
22. Gross, C.G. (2000) Neurogenesis in the adult brain: death of a dogma. Nat. Rev. Neurosci., 1, 67-73.
23. Heine, V.M., Maslam, S., Joels, M. & Lucassen, P.J. (2004) Prominent decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitary-adrenal axis activation. Neurobiol. Aging, 25, 361-375.
24. Jin, K., Mao, X.O., Sun, Y., Xie, L., Jin, L., Nishi, E., Klagsbrun, M. & Greenberg, D.A. (2002a) Heparin-binding epidermal growth factor-like growth factor: hypoxia-inducible expression in vitro and stimulation of neurogenesis in vitro and in vivo. J. Neurosci., 22, 5365-5373.
25. Jin, K., Peel, A.L., Mao, X.O., Xie, L., Cottrell, B.A., Henshall, D.C. & Greenberg, D.A. (2004) Increased hippocampal neurogenesis in Alzheimer's disease. Proc. Natl. Acad. Sci. USA, 101, 343-347.
26. Jin, K., Sun, Y., Xie, L., Batteur, S., Mao, X.O., Smelick, C., Logvinova, A. & Greenberg, D.A. (2003) Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell, 2, 175-183.
27. Jin, K., Zhu, Y., Sun, Y, Mao, X.O., Xie, L. & Greenberg, D.A. (2002b) Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc. Natl. Acad. Sci. USA, 99, 11946-11950.
28. Jones, S.P., Rahimi, O., O'Boyle, M.P., Diaz, D.L. & Claiborne, B.J. (2003) Maturation of granule cell dendrites after mossy fiber arrival in hippocampal field CA3. Hippocampus, 13, 413-427.
29. Kaplan, M.S. & Hinds, J.W. (1977) Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science, 197, 1092-1094.
30. Kempermann, G., Gast, D. & Gage, F.H. (2002) Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann. Neurol., 52, 135-143.
31. Kempermann, G., Gast, D., Kronenberg, G., Yamaguchi, M. & Gage, F.H. (2003) Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development, 130, 391-399.
32. Kempermann, G., Jesberger, S., Steiner, B. & Kronenberg, G. (2004b) Milestones of neuronal development in the adult hippocampus. Trends Neurosci., 27, 447-452.
33. Kempermann, G., Kuhn, H.G. & Gage, F.H. (1998) Experience-induced neurogenesis in the senescent dentate gyrus. J. Neurosci., 18, 3206-3212.
34. Kempermann, G., Wiskott, L. & Gage, F.H. (2004a) Functional significance of adult neurogenesis. Curr. Opin. Neurobiol., 14, 1-6.
35. Kuhn, H.G., Dickinson-Anson, H. & Gage, F.H. (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci., 16, 2027-2033.
36. Lee, J., Duan, W. & Mattson, M.P. (2002a) Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J. Neurochem., 2, 1367-1375.
37. Lee, J., Seroogy, K.B. & Mattson, M.P. (2002b) Dietary restriction enhances neurotrophin expression and neurogenesis in the hippocampus of adult mice. J. Neurochem., 80, 539-547.
38. Lichtenwalner, R.J., Forbes, M.E., Bennett, S.A., Lynch, C.D., Sonntag, W.E. & Riddle, D.R. (2001) Intracerebroventricular infusion of insulin-like growth factor-I ameliorates the age-related decline in hippocampal neurogenesis. Neuroscience, 107, 603-613.
39. Limke, T.L. & Rao, M.S. (2003) Neural stem cell therapy in the aging brain: pitfalls and possibilities. J. Hematother. Stem Cell. Res., 12, 615-623.
40. Liu, Y.B., Lio, P.A., Pasternak, J.F. & Trommer, B.L. (1996) Developmental changes in membrane properties and postsynaptic currents of granule cells in rat dentate gyrus. J. Neurophysiol., 76, 1074-1088.
41. Lubbers, K. & Frotscher, M. (1988) Differentiation of granule cells in relation to GABA-ergic neurons in the rat fascia dentata. Combined Golgi/EM and immunocytochemical studies. Anat. Embryol., 178, 119-127.
42. Markakis, E.A. & Gage, F.H. (1999) Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. J. Comp. Neurol., 406, 449-460.
43. Marti-Subirana, A., Soriano, E. & Garcia-Verdugo, J.M. (1986) Morphological aspects of the ectopic granule-like cellular populations in the albino rat hippocampal formation: a Golgi study. J. Anat., 144, 31-47.
44. Merrill, D.A., Karim, R., Darraq, M., Chiba, A.A. & Tuszynski, M.H. (2003) Hippocampal cell genesis does not correlate with spatial learning ability in aged rats. J. Comp. Neurol., 459, 201-207.
45. Monje, M.L., Mizumatsu, S., Fike, J.R. & Palmer, T.D. (2002) Irradiation induces neural precursor-cell dysfunction. Nat. Med., 8, 955-962.
46. Monje, M.L., Toda, H. & Palmer, T.D. (2003) Inflammatory blockade restores adult hippocampal neurogenesis. Science, 302, 1760-1765.
47. Nacher, J., Alonso-Llosa, G., Rosell, D.R. & McEwen, B.S. (2003) NMDA receptor antagonist treatment increases the production of new neurons in the aged rat hippocampus. Neurobiol. Aging, 24, 273-284.
48. Palmer, T.D., Willhoite, A.R. & Gage, F.H. (2000) Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol., 425, 479-494.
49. Parent, J.M., Tada, E., Fike, J.R. & Lowenstein, D.H. (1999) Inhibition of dentate granule cell neurogenesis with brain irradiation does not prevent seizure-induced mossy fiber synaptic reorganization in the rat. J. Neurosci., 19, 4508-4519.
50. van Praag, H., Schinder, A.F., Christie, B.R., Toni, N., Palmer, T.D. & Gage, F.H. (2002) Functional neurogenesis in the adult hippocampus. Nature, 415, 1030-1034.
51. Quinn, C.C., Gray, G.E. & Hockfield, S. (1999) A family of proteins implicated in axon guidance and outgrowth. J. Neurobiol., 41, 158-164.
52. Rao, M.S. & Shetty, A.K. (2004) Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur. J. Neurosci., 19, 234-246.
53. Ribak, C.E., Korn, M.J., Shan, Z. & Obenaus, A. (2004) Dendritic growth cones and recurrent basal dendrites are typical features of newly generated dentate granule cells in the adult hippocampus. Brain Res., 1000, 195-199.
54. Rihn, L.L. & Claiborne, B.J. (1990) Dendritic growth and regression in rat dentate granule cells during late postnatal development. Dev. Brain Res., 54, 115-124.
55. Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., Weisstaub, N., Lee, J., Duman, R., Arancio, O., Beizung, C. & Hen, R. (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science, 301, 805-809.
56. Sapolsky, R.M. (1992) Do glucocorticoid concentrations rise with age in the rat? Neurobiol. Aging, 13, 171-174.
57. Seki, T. (2002) Expression patterns of immature neuronal markers PSA-NCAM, CRMP-4 and NeuroD in the hippocampus of young adult and aged rodents. J. Neurosci. Res., 70, 327-334.
58. Seki, T. & Arai, Y. (1995) Age-related production of new granule cells in the adult dentate gyrus. Neuroreport, 6, 2479-2482.
59. Seress, L. & Pokorny, J. (1981) Structure of the granular layer of the rat dentate gyrus. A light microscopic and Golgi study. J. Anat., 133, 181-195.
60. Seri, B., Garcia-Verdugo, J.M., McEwen, B.S. & Alvarez-Buylla, A. (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci., 21, 7153-7160.
61. Shetty, A.K., Hattiangady, B. & Shetty, G.A. (2004b) Stem/progenitor cell proliferation factors FGF-2, IGF-1 and VEGF exhibit early decline in the hippocampus during aging. J. Neurochem., 90 (Suppl. 1), 34.
62. Shetty, A.K., Rao, M.S., Hattiangady, B., Zaman, V. & Shetty, G.A. (2004a) Hippocampal neurotrophin levels after injury: relationship to the age of the hippocampus at the time of injury. J. Neurosci. Res., 78, 520-532.
63. Shetty, A.K. & Turner, D.A. (1998) In vitro survival and differentiation of neurons derived from epidermal growth factor-responsive postnatal hippocampal stem cells: inducing effects of brain-derived neurotrophic factor. J. Neurobiol., 35, 395-425.
64. Shetty, A.K. & Turner, D.A. (2000) Fetal hippocampal grafts containing CA3 cells restore host hippocampal glutamate decarboxylase-positive interneuron numbers in a rat model of temporal lobe epilepsy. J. Neurosci., 20, 8788-8801.
65. Sholl, D.A. (1953) Dendritic organization of the neurons of the visual and motor cortices of the cat. J. Anat., 87, 387-406.
66. Shors, T.J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T. & Gould, E. (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature, 410, 372-376.
67. Stanfield, B.B. & Trice, J.E. (1998) Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections. Exp. Brain Res., 72, 399-406.
68. Steindler, D.A. & Pincus, D.W. (2002) Stem cells and neuropoiesis in the adult human brain. Lancet, 359, 1047-1054.
69. Steiner, B., Kronenberg, G., Jessberger, S., Brandt, M.D., Reuter, K. & Kempermann, G. (2004) Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia, 46, 41-52.
70. Stemmelin, J., Lazarus, C., Cassel, S., Kelche, C. & Cassel, J.C. (2000) Immunohistochemical and neurochemical correlates of learning deficits in aged rats. Neuroscience, 96, 275-289.
71. Ueki, T., Tanaka, M., Yamashita, K., Mikawa, S., Qiu, Z., Maragakis, N.J., Hevner, R.F., Miura, N., Sugimura, H. & Sato, K. (2003) A novel secretory factor, Neurogenesin-1, provides neurogenic environmental cues for neural stem cells in the adult hippocampus, secretory factor, neurogenesin. J. Neurosci., 23, 11732-11740.