FGF signaling is necessary for neurogenesis in young mice and sufficient to reverse its decline in old mice

Journal of Neuroscience

Volumn 35, Issue 28, 2015, Pages 10217-10223

  Kang, Wenfei ^a   Hébert, Jean M ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Aging; Dentate gyrus; FGF receptor; Hippocampus; Mouse; Neurogenesis

Indexed keywords

BROXURIDINE; DOUBLECORTIN; FIBROBLAST GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 3; GLIAL FIBRILLARY ACIDIC PROTEIN; KI 67 ANTIGEN; NESTIN; TAMOXIFEN; DOUBLECORTIN PROTEIN; FGFR1 PROTEIN, MOUSE; FGFR2 PROTEIN, MOUSE; FGFR3 PROTEIN, MOUSE; FIBROBLAST GROWTH FACTOR; MICROTUBULE ASSOCIATED PROTEIN; NERVE CELL ADHESION MOLECULE L1; NEUROPEPTIDE; POLYSIALYL NEURAL CELL ADHESION MOLECULE; SIALIC ACID DERIVATIVE;

AGED; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; FEMALE; HIPPOCAMPUS; HISTOPATHOLOGY; IMMUNOFLUORESCENCE; LOSS OF FUNCTION MUTATION; MALE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; YOUNG ADULT; ANIMAL; CELL COUNT; CYTOLOGY; GENETICS; METABOLISM; NERVE CELL; PHYSIOLOGY; TRANSGENIC MOUSE;

AGING; ANIMALS; CELL COUNT; FIBROBLAST GROWTH FACTORS; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; KI-67 ANTIGEN; MICE; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; NESTIN; NEURAL CELL ADHESION MOLECULE L1; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; NEUROPEPTIDES; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 3; SIALIC ACIDS; SIGNAL TRANSDUCTION;

EID: 84937598818     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1469-15.2015     Document Type: Article

References (51)

1. Aimone JB, Deng W, Gage FH (2011) Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 70:589 -596. CrossRef Medline
2. Alvarez-Buylla A, Lim DA (2004) For the long run: maintaining germinal niches in the adult brain. Neuron 41:683- 686. CrossRef Medline
3. Balordi F, Fishell G (2007) 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. CrossRef Medline
4. Biebl M, Cooper CM, Winkler J, Kuhn HG (2000) Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci Lett 291:17-20. CrossRef Medline
5. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA (2003) Shortterm and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460:563-572. CrossRef Medline
6. Deng C, Wynshaw-Boris A, Zhou F, Kuo A, Leder P (1996) Fibroblast growth factor receptor 3 is a negative regulator of bone growth. Cell 84:911-921. CrossRef Medline
7. Dono R, Texido G, Dussel R, Ehmke H, Zeller R (1998) Impaired cerebral cortex development and blood pressure regulation in FGF-2-deficient mice. EMBO J 17:4213- 4225. CrossRef Medline
8. Eisch AJ, Petrik D (2012) Depression and hippocampal neurogenesis: a road to remission? Science 338:72-75. CrossRef Medline
9. Encinas JM, Michurina TV, Peunova N, Park JH, Tordo J, Peterson DA, Fishell G, Koulakov A, Enikolopov G (2011) Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell 8:566 -579. CrossRef Medline
10. Faigle R, SongH (2013) Signaling mechanisms regulating adult neural stem cells and neurogenesis. Biochim Biophys Acta 1830:2435-2448. CrossRef Medline
11. Hattiangady B, Shetty AK (2008) Aging does not alter the number or phenotype of putative stem/progenitor cells in the neurogenic region of the hippocampus. Neurobiol Aging 29:129 -147. CrossRef Medline
12. Jessberger S, Gage FH (2008) Stem-cell-associated structural and functional plasticity in the aging hippocampus. Psychol Aging 23:684-691. CrossRef Medline
13. Jin K, Sun Y, Xie L, Batteur S, Mao XO, Smelick C, Logvinova A, Greenberg DA (2003) Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell 2:175-183. CrossRef Medline
14. Kang W, Wong LC, Shi SH, Hébert JM (2009) The transition from radial glial to intermediate progenitor cell is inhibited by FGF signaling during corticogenesis. J Neurosci 29:14571-14580. CrossRef Medline
15. Kang W, Balordi F, Su N, Chen L, Fishell G, Hébert JM (2014) Astrocyte activation is suppressed in both normal and injured brain by FGF signaling. Proc Natl Acad Sci U S A 111:E2987-E2995. CrossRef Medline
16. Kempermann G, Gast D, Gage FH (2002) Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann Neurol 52:135-143. CrossRef Medline
17. Korada S, Zheng W, Basilico C, Schwartz ML, Vaccarino FM (2002) Fibroblast growth factor 2 is necessary for the growth of glutamate projection neurons in the anterior neocortex. J Neurosci 22:863- 875. Medline
18. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033. Medline
19. Kuipers SD, Schroeder JE, Trentani A (2015) Changes in hippocampal neurogenesis throughout early development. Neurobiol Aging 36:365-379. CrossRef Medline
20. Lugert S, Basak O, Knuckles P, Haussler U, Fabel K, Götz M, Haas CA, Kempermann G, Taylor V, GiachinoC (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. CrossRef Medline
21. Ohkubo Y, Uchida AO, Shin D, Partanen J, VaccarinoFM (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. CrossRef Medline
22. Ortega S, Ittmann M, Tsang SH, Ehrlich M, Basilico C (1998) Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor 2. Proc Natl Acad Sci U S A 95:5672-5677. CrossRef Medline
23. Ota S, Tonou-Fujimori N, Yamasu K (2009) The roles of the FGF signal in zebrafish embryos analyzed using constitutive activation and dominantnegative suppression of different FGF receptors. Mech Dev 126:1-17. CrossRef Medline
24. Paek H, Gutin G, Hébert JM (2009) FGF signaling is strictly required to maintain early telencephalic precursor cell survival. Development 136: 2457-2465. CrossRef Medline
25. Palmer TD, Willhoite AR, Gage FH (2000) Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425:479-494. CrossRef Medline
26. Raballo R, Rhee J, Lyn-Cook R, Leckman JF, Schwartz ML, Vaccarino FM (2000) Basic fibroblast growth factor (Fgf2) is necessary for cell proliferation and neurogenesis in the developing cerebral cortex. J Neurosci 20: 5012-5023. Medline
27. Rai KS, Hattiangady B, Shetty AK (2007) Enhanced production and dendritic growth of new dentate granule cells in the middle-aged hippocampus following intracerebroventricular FGF-2 infusions. Eur J Neurosci 26:1765-1779. CrossRef Medline
28. Rao MS, Hattiangady B, Shetty AK (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. CrossRef Medline
29. Rao MS, Hattiangady B, Shetty AK (2008) Status epilepticus during old age is not associated with enhanced hippocampal neurogenesis. Hippocampus 18:931-944. CrossRef Medline
30. Rolando C, Taylor V (2014) Neural stem cell of the hippocampus: development, physiology regulation, and dysfunction in disease. Curr Top Dev Biol 107:183-206. CrossRef Medline
31. Saarimäki-Vire J, Peltopuro P, Lahti L, Naserke T, Blak AA, Vogt Weisenhorn DM, Yu K, Ornitz DM, Wurst W, Partanen J (2007) Fibroblast growth factor receptors cooperate to regulate neural progenitor properties in the developing midbrain and hindbrain. J Neurosci 27:8581- 8592. CrossRef Medline
32. Sato T, Joyner AL, Nakamura H (2004) How does FGF signaling from the isthmic organizer induce midbrain and cerebellum development? Dev Growth Differ 46:487- 494. CrossRef Medline
33. Shetty AK, Hattiangady B, Shetty GA (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. CrossRef Medline
34. Smith KM, Ohkubo Y, Maragnoli ME, Rasin MR, Schwartz ML, Sestan N, Vaccarino FM (2006) Midline radial glia translocation and corpus callosum formation require FGF signaling. Nat Neurosci 9:787-797. CrossRef Medline
35. Smith KM, Maragnoli ME, Phull PM, Tran KM, Choubey L, Vaccarino FM (2014) Fgfr1 inactivation in the mouse telencephalon results in impaired maturation of interneurons expressing parvalbumin. PLoS One 9:e103696. CrossRef Medline
36. Stevens HE, Jiang GY, Schwartz ML, Vaccarino FM (2012) Learning and memory depend on fibroblast growth factor receptor 2 functioning in hippocampus. Biol Psychiatry 71:1090 -1098. CrossRef Medline
37. Su N, Xu X, Li C, He Q, Zhao L, Li C, Chen S, Luo F, Yi L, Du X, Huang H, Deng C, Chen L (2010) Generation of Fgfr3 conditional knockout mice. Int J Biol Sci 6:327-332. CrossRef Medline
38. Suh H, Deng W, Gage FH (2009) Signaling in adult neurogenesis. Annu Rev Cell Dev Biol 25:253-275. CrossRef Medline
39. Taupin P, Ray J, Fischer WH, Suhr ST, Hakansson K, Grubb A, Gage FH (2000) FGF-2-responsive neural stem cell proliferation requires CCg, a novel autocrine/ paracrine cofactor. Neuron 28:385-397. CrossRef Medline
40. Tole S, Gutin G, Bhatnagar L, Remedios R, Hébert JM (2006) Development of midline cell types and commissural axon tracts requires Fgfr1 in the cerebrum. Dev Biol 289:141-151. CrossRef Medline
41. Trokovic R, Trokovic N, Hernesniemi S, Pirvola U, Vogt Weisenhorn DM, Rossant J, McMahon AP, Wurst W, Partanen J (2003) FGFR1 is independently required in both developing mid- and hindbrain for sustained response to isthmic signals. EMBO J 22:1811-1823. CrossRef Medline
42. Vaccarino FM, Schwartz ML, Raballo R, Nilsen J, Rhee J, Zhou M, Doetschman T, Coffin JD, Wyland JJ, Hung YT (1999) Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nat Neurosci 2:848. CrossRef Medline
43. van Praag H, Shubert T, Zhao C, Gage FH (2005) Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25:8680- 8685. CrossRef Medline
44. Wang Q, Green RP, Zhao G, Ornitz DM (2001) Differential regulation of endochondral bone growth and joint development by FGFR1 and FGFR3 tyrosine kinase domains. Development 128:3867-3876. Medline
45. Werner S, Unsicker K, von Bohlen und HalbachO (2011) Fibroblast growth factor-2 deficiency causes defects in adult hippocampal neurogenesis, which are not rescued by exogenous fibroblast growth factor-2. J Neurosci Res 89:1605-1617. CrossRef Medline
46. White LD, Barone S Jr (2001) Qualitative and quantitative estimates of apoptosis from birth to senescence in the rat brain. Cell Death Differ 8:345- 356. CrossRef
47. Yoshimura S, Takagi Y, Harada J, Teramoto T, Thomas SS, Waeber C, Bakowska JC, Breakefield XO, Moskowitz MA (2001) FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc Natl Acad Sci U S A 98:5874 -5879. CrossRef Medline
48. Yu K, Xu J, Liu Z, Sosic D, Shao J, Olson EN, Towler DA, Ornitz DM (2003) Conditional inactivation of FGF receptor 2 reveals an essential role for FGF signaling in the regulation of osteoblast function and bone growth. Development 130:3063-3074. CrossRef Medline
49. Zervas M, Blaess S, Joyner AL (2005) Classical embryological studies and modern genetic analysis of midbrain and cerebellum development. Curr Top Dev Biol 69:101-138. CrossRef Medline
50. Zhao M, Li D, Shimazu K, Zhou YX, Lu B, Deng CX (2007) Fibroblast growth factor receptor-1 is required for long-term potentiation, memory consolidation, and neurogenesis. Biol Psychiat 62:381-390. CrossRef Medline
51. Zucchini S, Buzzi A, Barbieri M, Rodi D, Paradiso B, Binaschi A, Coffin JD, Marzola A, Cifelli P, Belluzzi O, Simonato M (2008) Fgf-2 overexpression increases excitability and seizure susceptibility but decreases seizureinduced cell loss. J Neurosci 28:13112-13124. CrossRef Medline