Enhanced production and dendritic growth of new dentate granule cells in the middle-aged hippocampus following intracerebroventricular FGF-2 infusions

European Journal of Neuroscience

Volumn 26, Issue 7, 2007, Pages 1765-1779

  Rai, Kiranmai S ^a,b   Hattiangady, Bharathi ^a,b   Shetty, Ashok K ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b DURHAM VA MEDICAL CENTER   (United States)

Author keywords

Dentate neurogenesis; Hippocampal aging; Hippocampal stem cells; Learning and memory; Neural stem cells

Indexed keywords

BETA TUBULIN; BROXURIDINE; DOUBLECORTIN; FIBROBLAST GROWTH FACTOR 2;

ADULTHOOD; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL LABELING; CONTINUOUS INFUSION; CONTROLLED STUDY; DENDRITIC CELL; DENTATE GYRUS; DRUG INFUSION; GRANULE CELL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LATERAL BRAIN VENTRICLE; LEARNING; LONG TERM POTENTIATION; MALE; MEMORY; NERVE CELL GROWTH; NERVE STIMULATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; OSMOTIC MINIPUMP; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT;

ANIMALS; BROMODEOXYURIDINE; CELL COUNT; CELL GROWTH PROCESSES; DENDRITES; FIBROBLAST GROWTH FACTOR 2; FUNCTIONAL LATERALITY; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; INJECTIONS, INTRAVENTRICULAR; MALE; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; NEUROPEPTIDES; RATS; RATS, INBRED F344; TUBULIN;

EID: 34848841480     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05820.x     Document Type: Article

References (86)

1. Aberg, M.A., Aberg, N.D., Palmer, T.D., Alborn, A.M., Carlsson-Skwirut, C., Bang, P., Rosengren, L.E., Olsson, T., Gage, F.H. Eriksson, P.S. (2003) IGF-I has a direct proliferative effect in adult hippocampal progenitor cells. Mol. Cell. Neurosci., 24, 23 40.
2. Aoyagi, A., Nishikawa, K., Saito, H. Abe, K. (1994) Characterization of basic fibroblast growth factor-mediated acceleration of axonal branching in cultured rat hippocampal neurons. Brain Res., 661, 117 126.
3. Belluardo, N., Wu, G., Mudo, G., Hansson, A.C., Pettersson, R. Fuxe, K. (1997) Comparative localization of fibroblast growth factor receptor-1-2, and -3 mRNAs in the rat brain: in situ hybridization analysis. J. Comp. Neurol., 379, 226 246.
4. 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.
5. Bizon, J.L., Lee, H.J. Gallagher, M. (2004) Neurogenesis in a rat model of age-related cognitive decline. Aging Cell, 3, 227 234.
6. 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.
7. Bull., N.D. Bartlett, P.F. (2005) The adult mouse hippocampal progenitor is neurogenic but not a stem cell. J. Neurosci., 25, 10815 10821.
8. Cameron, H.A. McKay, R.D. (1999) Restoring production of hippocampal neurons in old age. Nat. Neurosci., 2, 894 897.
9. Cao, L., Jiao, X., Zuzga, D.S., Liu, Y., Fong, D.M., Young, D. During, M.J. (2004) VEGF links hippocampal activity with neurogenesis, learning and memory. Nat. Genet., 36, 827 835.
10. Chadashvili, T. Peterson, D.A. (2006) Cytoarchitecture of fibroblast growth factor receptor 2 (FGFR-2) immunoreactivity in astrocytes of neurogenic and non-neurogenic regions of the young adult and aged rat brain. J. Comp. Neurol., 498, 1 15.
11. 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.
12. Coumoul, X. Deng, C.X. (2003) Roles of FGF receptors in mammalian development and congenital diseases. Birth Defects Res. C Embryo Today, 69, 286 304.
13. Craig, A.M., Banker, G., Chang, W., McGrath, M.E. Serpinskaya, A.S. (1996) Clustering of gephyrin at GABAergic but not glutamatergic synapses in cultured rat hippocampal neurons. J. Neurosci., 16, 3166 3177.
14. 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, 100, 14385 14390.
15. Drapeau, E., Montaron, M.F., Aguerre, S. Abrous, D.N. (2007) Learning-induced survival of new neurons depends on the cognitive status of aged rats. J. Neurosci., 27, 6037 6044.
16. Driscoll, I., Howard, S.R., Stone, J.C., Monfils, M.H., Tomanek, B., Brooks, W.M. Sutherland, R.J. (2006) The aging hippocampus: a multi-level analysis in the rat. Neuroscience, 139, 1173 1185.
17. Dupret, D., Montaron, M.F., Drapeau, E., Aurousseau, C., Le Moal, M., Piazza, P.V. Abrous, D.N. (2005) Methylazoxymethanol acetate does not fully block cell genesis in the young and aged dentate gyrus. Eur. J. Neurosci., 22, 778 783.
18. Gage, F.H., Coates, P.W., Palmer, T.D., Kuhn, H.G., Fisher, L.J., Suhonen, J.O., Peterson, D.A., Suhr, S.T. Ray, J. (1995) Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc. Natl Acad. Sci. USA, 92, 11879 11883.
19. Ge, S., Yang, C.H., Hsu, K.S., Ming, G.L. Song, H. (2007) A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron, 54, 559 566.
20. Hattiangady, B., Rao, M.S., Shetty, G.A. Shetty, A.K. (2005) Brain-derived neurotrophic factor, phosphorylated cyclic AMP response element binding protein and neuropeptide Y decline as early as middle age in the dentate gyrus and CA1 and CA3 subfields of the hippocampus. Exp. Neurol., 195, 353 371.
21. Hattiangady, B. Shetty, A.K. (2007) Aging does not alter the number or phenotype of putative stem/progenitor cells in the neurogenic region of the hippocampus. Neurobiol. Aging, PMID: 17092610.
22. Hattiangady, B., Shuai, B., Cai, J., Coksaygan, T., Rao, M.S. Shetty, A.K. (2007) Increased dentate neurogenesis after grafting of glial restricted progenitors or neural stem cells in the aging hippocampus. Stem Cells, 25, 2104 2117.
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. Greenberg, D.A. (2002) Stem cell factor stimulates neurogenesis in vitro and in vivo. J. Clin. Invest., 110, 311 319.
25. 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.
26. Johe, K.K., Hazel, T.G., Muller, T., Dugich-Djordjevic, M.M. McKay, R.D. (1996) Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev., 10, 3129 3140.
27. 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.
28. Kalil, K., Szebenyi, G. Dent, E.W. (2000) Common mechanisms underlying growth cone guidance and axon branching. J. Neurobiol., 44, 145 158.
29. Kalyani, A., Hobson, K. Rao, M.S. (1997) Neuroepithelial stem cells from the embryonic spinal cord: isolation, characterization, and clonal analysis. Dev. Biol., 186, 202 223.
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. Klempin, F. Kempermann, G. (2007) Adult hippocampal neurogenesis and aging. Eur. Arch. Psychiatry Clin. Neurosci., April 1 [Epub ahead of print], PMID: 17401726.
33. Komitova, M. Eriksson, P.S. (2004) Sox-2 is expressed by neural progenitors and astroglia in the adult rat brain. Neurosci. Lett., 369, 24 27.
34. Kronenberg, G., Bick-Sander, A., Bunk, E., Wolf, C., Ehninger, D. Kempermann, G. (2006) Physical exercise prevents age-related decline in precursor cell activity in the mouse dentate gyrus. Neurobiol. Aging, 27, 1505 1513.
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. Kuhn, H.G., Winkler, J., Kempermann, G., Thal, L.J. Gage, F.H. (1997) Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J. Neurosci., 17, 5820 5829.
37. Lee, J., Duan, W. Mattson, M.P. (2002) 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., 82, 1367 1375.
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. Lubbers, K. Frotscher, M. (1988) Differentiation of granule cells in relation to GABAergic neurons in the rat fascia dentata. Combined Golgi/EM and immunocytochemical studies. Anat. Embryol. (Berl.), 178, 119 127.
40. Madsen, T.M., Kristjansen, P.E., Bolwig, T.G. Wortwein, G. (2003) Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience, 119, 635 642.
41. Marcus, D.L., Strafaci, J.A., Miller, D.C., Masia, S., Thomas, C.G., Rosman, J., Hussain, S. Freedman, M.L. (1998) Quantitative neuronal c-fos and c-jun expression in Alzheimer's disease. Neurobiol. Aging, 19, 393 400.
42. 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.
43. McDonald, H.Y. Wojtowicz, J.M. (2005) Dynamics of neurogenesis in the dentate gyrus of adult rats. Neurosci. Lett., 385, 70 75.
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. Montaron, M.F., Drapeau, E., Dupret, D., Kitchener, P., Aurousseau, C., Le Moal, M., Piazza, P.V. Abrous, D.N. (2006) Lifelong corticosterone level determines age-related decline in neurogenesis and memory. Neurobiol. Aging, 27, 645 654.
46. 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.
47. Nakagami, Y., Saito, H. Matsuki, N. (1997) Basic fibroblast growth factor and brain-derived neurotrophic factor promote survival and neuronal circuit formation in organotypic hippocampal culture. Jpn J. Pharmacol., 75, 319 326.
48. Ohkubo, Y., Uchida, A.O., Shin, D., Partanen, J. Vaccarino, F.M. (2004) Fibroblast growth factor receptor 1 is required for the proliferation of hippocampal progenitor cells and for hippocampal growth in mouse. J. Neurosci., 24, 6057 6069.
49. Olson, A.K., Eadie, B.D., Ernst, C. Christie, B.R. (2006) Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus, 16, 250 260.
50. Palmer, T.D., Markakis, E.A., Willhoite, A.R., Safar, F. 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.
51. Palmer, T.D., Ray, J. Gage, F.H. (1995) FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol. Cell. Neurosci., 6, 474 486.
52. Patel, M.N. McNamara, J.O. (1995) Selective enhancement of axonal branching of cultured dentate gyrus neurons by neurotrophic factors. Neuroscience, 69, 763 770.
53. Pieper, A.A., Wu, X., Han, T.W., Estill, S.J., Dang, Q., Wu, L.C., Reece-Fincanon, S., Dudley, C.A., Richardson, J.A., Brat, D.J. McKnight, S.L. (2005) The neuronal PAS domain protein 3 transcription factor controls FGF-mediated adult hippocampal neurogenesis in mice. Proc. Natl Acad. Sci. USA, 102, 14052 14057.
54. Plümpe, T., Ehninger, D., Steiner, B., Klempin, F., Jessberger, S., Brandt, M., Römer, B., Rodriguez, G.R., Kronenberg, G. Kempermann, G. (2006) Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci., 7, 77.
55. van Praag, H., Kempermann, G. Gage, F.H. (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci., 2, 266 270.
56. van Praag, H., Shubert, T., Zhao, C. Gage, F.H. (2005) Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci., 25, 8680 8685.
57. Rao, M.S., Hattiangady, B., Abdel-Rahman, A., Stanley, D.P. Shetty, A.K. (2005) Newly born cells in the ageing dentate gyrus display normal migration, survival and neuronal fate choice but endure retarded early maturation. Eur. J. Neurosci., 21, 464 476.
58. Rao, M.S., Hattiangady, B. Shetty, A.K. (2006) The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell, 5, 545 558.
59. 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.
60. Ray, J., Peterson, D.A., Schinstine, M. Gage, F.H. (1993) Proliferation, differentiation, and long-term culture of primary hippocampal neurons. Proc. Natl Acad. Sci. USA, 90, 3602 3606.
61. 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.
62. Ribak, C.E. Shapiro, L.A. (2006) Dendritic development of newly generated neurons in the adult brain. Brain Res. Brain Res. Rev., [Epub ahead of Print], PMID: 17239443.
63. Rola, R., Raber, J., Rizk, A., Otsuka, S., VandenBerg, S.R., Morhardt, D.R. Fike, J.R. (2004) Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Exp. Neurol., 188, 316 330.
64. Ruel, L., Bourouis, M., Heitzler, P., Pantesco, V. Simpson, P. (1993) Drosophila shaggy kinase and rat glycogen synthase kinase-3 have conserved activities and act downstream of Notch. Nature, 362, 557 560.
65. Schmidt-Hieber, C., Jonas, P. Bischofberger, J. (2004) Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature, 429, 184 187.
66. 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.
67. Shetty, A.K. (2004) Progenitor cells from the CA3 region of the embryonic day 19 rat hippocampus generate region-specific neuronal phenotypes in vitro. Hippocampus, 14, 595 614.
68. Shetty, A.K. Hattiangady, B. (2007) Restoration of calbindin after fetal hippocampal CA3 cell grafting into the injured hippocampus in a rat model of temporal lobe epilepsy. Hippocampus, June 29 [Epub ahead of print], PMID: 17604349.
69. Shetty, A.K., Hattiangady, B. Shetty, G.A. (2005) Stem/progenitor cell proliferation factors FGF-2, IGF-1, and VEGF exhibit early decline during the course of aging in the hippocampus: role of astrocytes. Glia, 51, 173 186.
70. Shetty, A.K., Rao, M.S., Hattiangady, B., Zaman, V. Shetty, G.A. (2004) Hippocampal neurotrophin levels after injury: relationship to the age of the hippocampus at the time of injury. J. Neurosci. Res., 78, 520 532.
71. 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.
72. 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.
73. Sholl, D.A. (1953) Dendritic organization in the neurons of the visual and motor cortices of the cat. J. Anat., 87, 387 406.
74. 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.
75. Stanley, D.P. Shetty, A.K. (2004) Aging in the rat hippocampus is associated with widespread reductions in the number of glutamate decarboxylase-67 positive interneurons but not interneuron degeneration. J. Neurochem., 89, 204 216.
76. Steiner, B., Klempin, F., Wang, L., Kott, M., Kettenmann, H. Kempermann, G. (2006) Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia, 54, 805 814.
77. Tao, Y., Black, I.B. DiCicco-Bloom, E. (1997) In vivo neurogenesis is inhibited by neutralizing antibodies to basic fibroblast growth factor. J. Neurobiol., 33, 289 296.
78. Tatebayashi, Y., Iqbal, K. Grundke-Iqbal, I. (1999) Dynamic regulation of expression and phosphorylation of tau by fibroblast growth factor-2 in neural progenitor cells from adult rat hippocampus. J. Neurosci., 19, 5245 5254.
79. Tatebayashi, Y., Lee, M.H., Li, L., Iqbal, K. Grundke-Iqbal, I. (2003) The dentate gyrus neurogenesis: a therapeutic target for Alzheimer's disease. Acta Neuropathol. (Berl.), 105, 225 232.
80. Temple, S. Qian, X. (1995) bFGF, neurotrophins, and the control or cortical neurogenesis. Neuron, 15, 249 252.
81. Vaccarino, F.M., Schwartz, M.L., Hartigan, D. Leckman, J.F. (1995) Basic fibroblast growth factor increases the number of excitatory neurons containing glutamate in the cerebral cortex. Cereb. Cortex, 5, 64 78.
82. Vescovi, A.L., Reynolds, B.A., Fraser, D.D. Weiss, S. (1993) bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron, 11, 951 966.
83. Vicario-Abejon, C., Johe, K.K., Hazel, T.G., Collazo, D. McKay, R.D. (1995) Functions of basic fibroblast growth factor and neurotrophins in the differentiation of hippocampal neurons. Neuron, 15, 105 114.
84. Wang, S., Wojtowicz, J.M. Atwood, H.L. (2000) Synaptic recruitment during long-term potentiation at synapses of the medial perforant pathway in the dentate gyrus of the rat brain. Synapse, 22, 78 86.
85. Yoshimura, S., Takagi, Y., Harada, J., Teramoto, T., Thomas, S.S., Waeber, C., Bakowska, J.C., Breakefield, X.O. Moskowitz, M.A. (2001) FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc. Natl Acad. Sci. USA, 98, 5874 5879.
86. Zhao, M., Li, D., Shimazu, K., Zhou, Y.X., Lu, B. Deng, C.X. (2007) Fibroblast growth factor receptor-1 is required for long-term potentiation, memory consolidation, and neurogenesis. Biol. Psychiatry. January 17 [Epub ahead of print], PMID: 17239352.