Calorie restriction alleviates the age-related decrease in neural progenitor cell division in the aging brain

European Journal of Neuroscience

Volumn 37, Issue 12, 2013, Pages 1987-1993

  Park, June Hee ^a   Glass, Zachary ^a   Sayed, Kasim ^a   Michurina, Tatyana V ^a,b   Lazutkin, Alexander ^a,b   Mineyeva, Olga ^a,b   Velmeshev, Dmitry ^a   Ward, Walter F ^c   Richardson, Arlan ^c   Enikolopov, Grigori ^a,b  

^a Simons Center for Quantitative Biology   (United States)

^b MOSCOW INSTITUTE OF PHYSICS AND TECHNOLOGY   (Russian Federation)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Adult neurogenesis; Aging; Calorie restriction; Rapamycin; Stem cells

Indexed keywords

DOUBLECORTIN; GREEN FLUORESCENT PROTEIN; NESTIN; RAPAMYCIN;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALORIC RESTRICTION; CELL COUNT; CELL DIVISION; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; DRUG EFFECT; FEMALE; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AGING; ANIMALS; CALORIC RESTRICTION; FEMALE; HIPPOCAMPUS; MALE; MICE; MICE, TRANSGENIC; NEURAL STEM CELLS; NEUROGENESIS; SIROLIMUS;

EID: 84879228410     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12249     Document Type: Article

References (43)

1. Aimone, J.B., Deng, W. & Gage, F.H. (2011) Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron, 70, 589-596.
2. Anderson, R.M. & Weindruch, R. (2010) Metabolic reprogramming, caloric restriction and aging. Trends Endocrin. Met., 21, 134-141.
3. Anderson, R.M. & Weindruch, R. (2012) The caloric restriction paradigm: implications for healthy human aging. Am. J. Hum. Biol., 24, 101-106.
4. Bonaguidi, M.A., Wheeler, M.A., Shapiro, J.S., Stadel, R.P., Sun, G.J., Ming, G.L. & Song, H. (2011) In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell, 145, 1142-1155.
5. 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.
6. Cameron, H.A. & McKay, R.D. (1999) Restoring production of hippocampal neurons in old age. Nat. Neurosci., 2, 894-897.
7. Cerletti, M., Jang, Y.C., Finley, L.W., Haigis, M.C. & Wagers, A.J. (2012) Short-term calorie restriction enhances skeletal muscle stem cell function. Cell Stem Cell, 10, 515-519.
8. Day, K., Shefer, G., Richardson, J.B., Enikolopov, G. & Yablonka-Reuveni, Z. (2007) Nestin-GFP reporter expression defines the quiescent state of skeletal muscle satellite cells. Dev. Biol., 304, 246-259.
9. Deng, W., Aimone, J.B. & Gage, F.H. (2010) New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat. Rev. Neurosci., 11, 339-350.
10. Encinas, J.M. & Enikolopov, G. (2008) Identifying and quantitating neural stem and progenitor cells in the adult brain. Method. Cell Biol., 85, 243-272.
11. Encinas, J.M. & 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.
12. Encinas, J.M., Vaahtokari, A. & Enikolopov, G. (2006) Fluoxetine targets early progenitor cells in the adult brain. Proc. Natl. Acad. Sci. USA, 103, 8233-8238.
13. Encinas, J.M., Hamani, C., Lozano, A.M. & Enikolopov, G. (2011a) Neurogenic hippocampal targets of deep brain stimulation. J. Comp. Neurol., 519, 6-20.
14. Encinas, J.M., Michurina, T.V., Peunova, N., Park, J.H., Tordo, J., Peterson, D.A., Fishell, G., Koulakov, A. & Enikolopov, G. (2011b) Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell, 8, 566-579.
15. Enikolopov, G. & Overstreet-Wadiche, L. (2008) Transgenic reporter lines for studying adult neurogenesis. In Gage, F.H., Kempermann, G. & Song, H. (Eds), Adult Neurogenesis. CSHL Press, pp. 81-100.
16. Fok, W., Zhang, Y., Salmon, A.B., Bhattacharya, A., Gunda, R., Jones, D., Ward, W.F., Richardson, A. & Perez, V. (2012) Short-term treatment with rapamycin and dietary restriction have overlapping and distinctive effects in young mice. J. Gerontol. A-Biol., 68, 108-116.
17. Galea, L.A. (2008) Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents. Brain Res. Rev., 57, 332-341.
18. Gleiberman, A.S., Encinas, J.M., Mignone, J.L., Michurina, T., Rosenfeld, M.G. & Enikolopov, G. (2005) Expression of nestin-green fluorescent protein transgene marks oval cells in the adult liver. Dev. Dynam., 234, 413-421.
19. Gleiberman, A.S., Michurina, T., Encinas, J.M., Roig, J.L., Krasnov, P., Balordi, F., Fishell, G., Rosenfeld, M.G. & Enikolopov, G. (2008) Genetic approaches identify adult pituitary stem cells. Proc. Natl. Acad. Sci. USA, 105, 6332-6337.
20. Harrison, D.E., Strong, R., Sharp, Z.D., Nelson, J.F., Astle, C.M., Flurkey, K., Nadon, N.L., Wilkinson, J.E., Frenkel, K., Carter, C.S., Pahor, M., Javors, M.A., Fernandez, E. & Miller, R.A. (2009) Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature, 460, 392-395.
21. Hattiangady, B. & Shetty, A.K. (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.
22. Hayes, N.L. & Nowakowski, R.S. (2002) Dynamics of cell proliferation in the adult dentate gyrus of two inbred strains of mice. Brain Res. Dev. Brain Res., 134, 77-85.
23. Houtkooper, R.H., Williams, R.W. & Auwerx, J. (2010) Metabolic networks of longevity. Cell, 142, 9-14.
24. 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.
25. Lagace, D.C., Fischer, S.J. & Eisch, A.J. (2007) Gender and endogenous levels of estradiol do not influence adult hippocampal neurogenesis in mice. Hippocampus, 17, 175-180.
26. Leuner, B., Kozorovitskiy, Y., Gross, C.G. & Gould, E. (2007) Diminished adult neurogenesis in the marmoset brain precedes old age. Proc. Natl. Acad. Sci. USA, 104, 17169-17173.
27. Lugert, S., Basak, O., Knuckles, P., Haussler, U., Fabel, K., Gotz, M., Haas, C.A., Kempermann, G., Taylor, V. & Giachino, C. (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.
28. Mendez-Ferrer, S., Michurina, T.V., Ferraro, F., Mazloom, A.R., Macarthur, B.D., Lira, S.A., Scadden, D.T., Ma'ayan, A., Enikolopov, G.N. & Frenette, P.S. (2010) Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature, 466, 829-834.
29. Mercken, E.M., Carboneau, B.A., Krzysik-Walker, S.M. & de Cabo, R. (2012) Of mice and men: the benefits of caloric restriction, exercise, and mimetics. Ageing Res. Rev., 11, 390-398.
30. Mignone, J.L., Kukekov, V., Chiang, A.S., Steindler, D. & Enikolopov, G. (2004) Neural stem and progenitor cells in nestin-GFP transgenic mice. J. Comp. Neurol., 469, 311-324.
31. Mignone, J.L., Roig-Lopez, J.L., Fedtsova, N., Schones, D.E., Manganas, L.N., Maletic-Savatic, M., Keyes, W.M., Mills, A.A., Gleiberman, A., Zhang, M.Q. & Enikolopov, G. (2007) Neural potential of a stem cell population in the hair follicle. Cell Cycle, 6, 2161-2170.
32. Miller, R.A., Harrison, D.E., Astle, C.M., Baur, J.A., Boyd, A.R., de Cabo, R., Fernandez, E., Flurkey, K., Javors, M.A., Nelson, J.F., Orihuela, C.J., Pletcher, S., Sharp, Z.D., Sinclair, D., Starnes, J.W., Wilkinson, J.E., Nadon, N.L. & Strong, R. (2011) Rapamycin, but not resveratrol or simvastatin, extends life span of genetically heterogeneous mice. J. Gerontol. A-Biol., 66, 191-201.
33. Ming, G.L. & Song, H. (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron, 70, 687-702.
34. Olariu, A., Cleaver, K.M. & Cameron, H.A. (2007) Decreased neurogenesis in aged rats results from loss of granule cell precursors without lengthening of the cell cycle. J. Comp. Neurol., 501, 659-667.
35. Paliouras, G.N., Hamilton, L.K., Aumont, A., Joppe, S.E., Barnabe-Heider, F. & Fernandes, K.J. (2012) Mammalian target of rapamycin signaling is a key regulator of the transit-amplifying progenitor pool in the adult and aging forebrain. J. Neurosci., 32, 15012-15026.
36. Park, J.H. & Enikolopov, G. (2010) Transient elevation of adult hippocampal neurogenesis after dopamine depletion. Exp. Neurol., 222, 267-276.
37. Plumpe, T., Ehninger, D., Steiner, B., Klempin, F., Jessberger, S., Brandt, M., Romer, 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.
38. Sahay, A. & Hen, R. (2007) Adult hippocampal neurogenesis in depression. Nat. Neurosci., 10, 1110-1115.
39. Sahay, A., Wilson, D.A. & Hen, R. (2011) Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron, 70, 582-588.
40. Samuels, B.A. & Hen, R. (2011) Neurogenesis and affective disorders. Eur. J. Neurosci., 33, 1152-1159.
41. Stangl, D. & Thuret, S. (2009) Impact of diet on adult hippocampal neurogenesis. Genes Nutr., 4, 271-282.
42. Tanapat, P., Hastings, N.B., Reeves, A.J. & Gould, E. (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci., 19, 5792-5801.
43. Zhao, C., Deng, W. & Gage, F.H. (2008) Mechanisms and functional implications of adult neurogenesis. Cell, 132, 645-660.