Human Hippocampal Neurogenesis Persists throughout Aging

Cell Stem Cell

Volumn 22, Issue 4, 2018, Pages 589-599.e5

  Boldrini, Maura ^a,c   Fulmore, Camille A ^c   Tartt, Alexandria N ^c   Simeon, Laika R ^c   Pavlova, Ina ^c   Poposka, Verica ^d   Rosoklija, Gorazd B ^a,c,d   Stankov, Aleksandar ^d   Arango, Victoria ^a,c   Dwork, Andrew J ^a,b,c,d   Hen, René ^a,c   Mann, J John ^a,c  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b NewYork Presbyterian Hospital   (United States)

^c NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^d SS CYRIL AND METHODIUS UNIVERSITY   (Macedonia)

Author keywords

dentate gyrus; doublecortin; granule cells; Ki 67; nestin; NeuN; neural progenitor; PSA NCAM; Sox2; volume

Indexed keywords

ADOLESCENT; ADULT; AGED; AGING; ANGIOGENESIS; ARTICLE; AUTOPSY; BRAIN NERVE CELL; CAPILLARY DENSITY; COGNITION; COGNITIVE DEFECT; CORRELATION ANALYSIS; DENTATE GYRUS; EMOTION; GLIA; HIPPOCAMPUS; HUMAN; MENTAL DISEASE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NORMAL HUMAN; PRIORITY JOURNAL; CYTOLOGY; METABOLISM; MIDDLE AGED; NERVE CELL; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGING; DENTATE GYRUS; HIPPOCAMPUS; HUMANS; MIDDLE AGED; NEUROGENESIS; NEURONS; YOUNG ADULT;

EID: 85044572153     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2018.03.015     Document Type: Article

References (68)

1. Aimone, J.B., Deng, W., Gage, F.H., Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 70 (2011), 589–596.
2. Ben Abdallah, N.M., Slomianka, L., Lipp, H.P., Reversible effect of X-irradiation on proliferation, neurogenesis, and cell death in the dentate gyrus of adult mice. Hippocampus 17 (2007), 1230–1240.
3. Bergmann, O., Liebl, J., Bernard, S., Alkass, K., Yeung, M.S., Steier, P., Kutschera, W., Johnson, L., Landén, M., Druid, H., et al. The age of olfactory bulb neurons in humans. Neuron 74 (2012), 634–639.
4. Bergmann, O., Spalding, K.L., Frisén, J., Adult Neurogenesis in Humans. Cold Spring Harb. Perspect. Biol., 7, 2015, a018994.
5. Boldrini, M., Underwood, M.D., Hen, R., Rosoklija, G.B., Dwork, A.J., John Mann, J., Arango, V., Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacology 34 (2009), 2376–2389.
6. Boldrini, M., Hen, R., Underwood, M.D., Rosoklija, G.B., Dwork, A.J., Mann, J.J., Arango, V., Hippocampal angiogenesis and progenitor cell proliferation are increased with antidepressant use in major depression. Biol. Psychiatry 72 (2012), 562–571.
7. Boldrini, M., Santiago, A.N., Hen, R., Dwork, A.J., Rosoklija, G.B., Tamir, H., Arango, V., John Mann, J., Hippocampal granule neuron number and dentate gyrus volume in antidepressant-treated and untreated major depression. Neuropsychopharmacology 38 (2013), 1068–1077.
8. Boldrini, M., Butt, T.H., Santiago, A.N., Tamir, H., Dwork, A.J., Rosoklija, G.B., Arango, V., Hen, R., Mann, J.J., Benzodiazepines and the potential trophic effect of antidepressants on dentate gyrus cells in mood disorders. Int. J. Neuropsychopharmacol. 17 (2014), 1923–1933.
9. Bonaguidi, M.A., Wheeler, M.A., Shapiro, J.S., Stadel, R.P., Sun, G.J., Ming, G.L., Song, H., In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 145 (2011), 1142–1155.
10. Bridel, C., Hoffmann, T., Meyer, A., Durieux, S., Koel-Simmelink, M.A., Orth, M., Scheltens, P., Lues, I., Teunissen, C.E., Glutaminyl cyclase activity correlates with levels of Aβ peptides and mediators of angiogenesis in cerebrospinal fluid of Alzheimer's disease patients. Alzheimers Res. Ther., 9, 2017, 38.
11. D'Amour, K.A., Gage, F.H., Genetic and functional differences between multipotent neural and pluripotent embryonic stem cells. Proc. Natl. Acad. Sci. USA 100:Suppl 1 (2003), 11866–11872.
12. Daugherty, A.M., Bender, A.R., Raz, N., Ofen, N., Age differences in hippocampal subfield volumes from childhood to late adulthood. Hippocampus 26 (2016), 220–228.
13. Dranovsky, A., Picchini, A.M., Moadel, T., Sisti, A.C., Yamada, A., Kimura, S., Leonardo, E.D., Hen, R., Experience dictates stem cell fate in the adult hippocampus. Neuron 70 (2011), 908–923.
14. Ekstrand, J., Hellsten, J., Tingström, A., Environmental enrichment, exercise and corticosterone affect endothelial cell proliferation in adult rat hippocampus and prefrontal cortex. Neurosci. Lett. 442 (2008), 203–207.
15. Encinas, J.M., Michurina, T.V., Peunova, N., Park, J.H., Tordo, J., Peterson, D.A., Fishell, G., Koulakov, A., Enikolopov, G., Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell 8 (2011), 566–579.
16. Endicott, J., Spitzer, R.L., Fleiss, J.L., Cohen, J., The global assessment scale. A procedure for measuring overall severity of psychiatric disturbance. Arch. Gen. Psychiatry 33 (1976), 766–771.
17. Erickson, K.I., Voss, M.W., Prakash, R.S., Basak, C., Szabo, A., Chaddock, L., Kim, J.S., Heo, S., Alves, H., White, S.M., et al. Exercise training increases size of hippocampus and improves memory. Proc. Natl. Acad. Sci. USA 108 (2011), 3017–3022.
18. Eriksson, P.S., Perfilieva, E., Björk-Eriksson, T., Alborn, A.M., Nordborg, C., Peterson, D.A., Gage, F.H., Neurogenesis in the adult human hippocampus. Nat. Med. 4 (1998), 1313–1317.
19. Gould, E., Reeves, A.J., Fallah, M., Tanapat, P., Gross, C.G., Fuchs, E., Hippocampal neurogenesis in adult Old World primates. Proc. Natl. Acad. Sci. USA 96 (1999), 5263–5267.
20. Harding, A.J., Halliday, G.M., Kril, J.J., Variation in hippocampal neuron number with age and brain volume. Cereb. Cortex 8 (1998), 710–718.
21. Harrison, P.J., Heath, P.R., Eastwood, S.L., Burnet, P.W.J., McDonald, B., Pearson, R.C.A., The relative importance of premortem acidosis and postmortem interval for human brain gene expression studies: selective mRNA vulnerability and comparison with their encoded proteins. Neurosci. Lett. 200 (1995), 151–154.
22. Head, D., Snyder, A.Z., Girton, L.E., Morris, J.C., Buckner, R.L., Frontal-hippocampal double dissociation between normal aging and Alzheimer's disease. Cereb. Cortex 15 (2005), 732–739.
23. Heine, V.M., Zareno, J., Maslam, S., Joëls, M., Lucassen, P.J., Chronic stress in the adult dentate gyrus reduces cell proliferation near the vasculature and VEGF and Flk-1 protein expression. Eur. J. Neurosci. 21 (2005), 1304–1314.
24. Ho, N.F., Hooker, J.M., Sahay, A., Holt, D.J., Roffman, J.L., In vivo imaging of adult human hippocampal neurogenesis: progress, pitfalls and promise. Mol. Psychiatry 18 (2013), 404–416.
25. Jin, K., Peel, A.L., Mao, X.O., Xie, L., Cottrell, B.A., Henshall, D.C., Greenberg, D.A., Increased hippocampal neurogenesis in Alzheimer's disease. Proc. Natl. Acad. Sci. USA 101 (2004), 343–347.
26. Katsimpardi, L., Litterman, N.K., Schein, P.A., Miller, C.M., Loffredo, F.S., Wojtkiewicz, G.R., Chen, J.W., Lee, R.T., Wagers, A.J., Rubin, L.L., Vascular and neurogenic rejuvenation of the aging mouse brain by young systemic factors. Science 344 (2014), 630–634.
27. Kelly, T.M., Mann, J.J., Validity of DSM-III-R diagnosis by psychological autopsy: a comparison with clinician ante-mortem diagnosis. Acta Psychiatr. Scand. 94 (1996), 337–343.
28. Kempermann, G., Gast, D., Kronenberg, G., Yamaguchi, M., Gage, F.H., Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130 (2003), 391–399.
29. Knoth, R., Singec, I., Ditter, M., Pantazis, G., Capetian, P., Meyer, R.P., Horvat, V., Volk, B., Kempermann, G., Murine features of neurogenesis in the human hippocampus across the lifespan from 0 to 100 years. PLoS ONE, 5, 2010, e8809.
30. Kohler, S.J., Williams, N.I., Stanton, G.B., Cameron, J.L., Greenough, W.T., Maturation time of new granule cells in the dentate gyrus of adult macaque monkeys exceeds six months. Proc. Natl. Acad. Sci. USA 108 (2011), 10326–10331.
31. Kornack, D.R., Rakic, P., Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc. Natl. Acad. Sci. USA 96 (1999), 5768–5773.
32. Leuner, B., Kozorovitskiy, Y., Gross, C.G., Gould, E., Diminished adult neurogenesis in the marmoset brain precedes old age. Proc. Natl. Acad. Sci. USA 104 (2007), 17169–17173.
33. Lewis, D.A., The human brain revisited: opportunities and challenges in postmortem studies of psychiatric disorders. Neuropsychopharmacology 26 (2002), 143–154.
34. Louissaint, A. Jr., Rao, S., Leventhal, C., Goldman, S.A., Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 34 (2002), 945–960.
35. Maass, A., Düzel, S., Goerke, M., Becke, A., Sobieray, U., Neumann, K., Lövden, M., Lindenberger, U., Bäckman, L., Braun-Dullaeus, R., et al. Vascular hippocampal plasticity after aerobic exercise in older adults. Mol. Psychiatry 20 (2015), 585–593.
36. Malykhin, N.V., Bouchard, T.P., Camicioli, R., Coupland, N.J., Aging hippocampus and amygdala. Neuroreport 19 (2008), 543–547.
37. Manganas, L.N., Zhang, X., Li, Y., Hazel, R.D., Smith, S.D., Wagshul, M.E., Henn, F., Benveniste, H., Djuric, P.M., Enikolopov, G., Maletic-Savatic, M., Magnetic resonance spectroscopy identifies neural progenitor cells in the live human brain. Science 318 (2007), 980–985.
38. Maurya, S.K., Mishra, R., Pax6 interacts with Iba1 and shows age-associated alterations in brain of aging mice. J. Chem. Neuroanat. 82 (2017), 60–64.
39. McEwen, B.S., Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Ann. N Y Acad. Sci. 933 (2001), 265–277.
40. Mokrý, J., Ehrmann, J., Karbanová, J., Cízková, D., Soukup, T., Suchánek, J., Filip, S., Kolár, Z., Expression of intermediate filament nestin in blood vessels of neural and non-neural tissues. Acta Med. (Hradec Kralove) 51 (2008), 173–179.
41. Mouton, P.R., Long, J.M., Lei, D.L., Howard, V., Jucker, M., Calhoun, M.E., Ingram, D.K., Age and gender effects on microglia and astrocyte numbers in brains of mice. Brain Res. 956 (2002), 30–35.
42. Ngwenya, L.B., Heyworth, N.C., Shwe, Y., Moore, T.L., Rosene, D.L., Age-related changes in dentate gyrus cell numbers, neurogenesis, and associations with cognitive impairments in the rhesus monkey. Front. Syst. Neurosci., 9, 2015, 102.
43. Ní Dhúill, C.M., Fox, G.B., Pittock, S.J., O'Connell, A.W., Murphy, K.J., Regan, C.M., Polysialylated neural cell adhesion molecule expression in the dentate gyrus of the human hippocampal formation from infancy to old age. J. Neurosci. Res. 55 (1999), 99–106.
44. Pereira, A.C., Huddleston, D.E., Brickman, A.M., Sosunov, A.A., Hen, R., McKhann, G.M., Sloan, R., Gage, F.H., Brown, T.R., Small, S.A., An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc. Natl. Acad. Sci. USA 104 (2007), 5638–5643.
45. Perlmutter, L.S., Chui, H.C., Saperia, D., Athanikar, J., Microangiopathy and the colocalization of heparan sulfate proteoglycan with amyloid in senile plaques of Alzheimer's disease. Brain Res. 508 (1990), 13–19.
46. Ramm, P., Couillard-Despres, S., Plötz, S., Rivera, F.J., Krampert, M., Lehner, B., Kremer, W., Bogdahn, U., Kalbitzer, H.R., Aigner, L., A nuclear magnetic resonance biomarker for neural progenitor cells: is it all neurogenesis?. Stem Cells 27 (2009), 420–423.
47. Richards, B.A., Frankland, P.W., The Persistence and Transience of Memory. Neuron 94 (2017), 1071–1084.
48. Roy, A., Pickar, D., Linnoila, M., Doran, A.R., Paul, S.M., Cerebrospinal fluid monoamine and monoamine metabolite levels and the dexamethasone suppression test in depression. Relationship to life events. Arch. Gen. Psychiatry 43 (1986), 356–360.
49. Sahay, A., Scobie, K.N., Hill, A.S., O'Carroll, C.M., Kheirbek, M.A., Burghardt, N.S., Fenton, A.A., Dranovsky, A., Hen, R., Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472 (2011), 466–470.
50. Salehi, F., Kovacs, K., Cusimano, M.D., Horvath, E., Bell, C.D., Rotondo, F., Scheithauer, B.W., Immunohistochemical expression of nestin in adenohypophysial vessels during development of pituitary infarction. J. Neurosurg. 108 (2008), 118–123.
51. Saravia, F., Beauquis, J., Pietranera, L., De Nicola, A.F., Neuroprotective effects of estradiol in hippocampal neurons and glia of middle age mice. Psychoneuroendocrinology 32 (2007), 480–492.
52. Schloesser, R.J., Lehmann, M., Martinowich, K., Manji, H.K., Herkenham, M., Environmental enrichment requires adult neurogenesis to facilitate the recovery from psychosocial stress. Mol. Psychiatry 15 (2010), 1152–1163.
53. Scholzen, T., Gerdes, J., The Ki-67 protein: from the known and the unknown. J. Cell. Physiol. 182 (2000), 311–322.
54. Simić, G., Kostović, I., Winblad, B., Bogdanović, N., Volume and number of neurons of the human hippocampal formation in normal aging and Alzheimer's disease. J. Comp. Neurol. 379 (1997), 482–494.
55. Song, J., Christian, K.M., Ming, G.L., Song, H., Modification of hippocampal circuitry by adult neurogenesis. Dev. Neurobiol. 72 (2012), 1032–1043.
56. Sorrells, S.F., Paredes, M.F., Cebrian-Silla, A., Sandoval, K., Qi, D., Kelley, K.W., James, D., Mayer, S., Chang, J., Auguste, K.I., et al. Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults. Nature 555 (2018), 377–381.
57. Spalding, K.L., Bergmann, O., Alkass, K., Bernard, S., Salehpour, M., Huttner, H.B., Boström, E., Westerlund, I., Vial, C., Buchholz, B.A., et al. Dynamics of hippocampal neurogenesis in adult humans. Cell 153 (2013), 1219–1227.
58. Thored, P., Wood, J., Arvidsson, A., Cammenga, J., Kokaia, Z., Lindvall, O., Long-term neuroblast migration along blood vessels in an area with transient angiogenesis and increased vascularization after stroke. Stroke 38 (2007), 3032–3039.
59. United States Census Bureau (2017). The Nation's Older Population Is Still Growing, Census Bureau Reports. Release Number: CB17-100. https://www.census.gov/newsroom/press-releases/2017/cb17-100.html.
60. Vagnucci, A.H. Jr., Li, W.W., Alzheimer's disease and angiogenesis. Lancet 361 (2003), 605–608.
61. Varbanov, H., Dityatev, A., Regulation of extrasynaptic signaling by polysialylated NCAM: Impact for synaptic plasticity and cognitive functions. Mol. Cell. Neurosci. 81 (2017), 12–21.
62. Warner-Schmidt, J.L., Duman, R.S., VEGF is an essential mediator of the neurogenic and behavioral actions of antidepressants. Proc. Natl. Acad. Sci. USA 104 (2007), 4647–4652.
63. West, M.J., New stereological methods for counting neurons. Neurobiol. Aging 14 (1993), 275–285.
64. West, M.J., Gundersen, H.J., Unbiased stereological estimation of the number of neurons in the human hippocampus. J. Comp. Neurol. 296 (1990), 1–22.
65. West, M.J., Coleman, P.D., Flood, D.G., Troncoso, J.C., Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet 344 (1994), 769–772.
66. Wu, M.V., Hen, R., Functional dissociation of adult-born neurons along the dorsoventral axis of the dentate gyrus. Hippocampus 24 (2014), 751–761.
67. Yang, X., Goh, A., Chen, S.H., Qiu, A., Evolution of hippocampal shapes across the human lifespan. Hum. Brain Mapp. 34 (2013), 3075–3085.
68. Yu, D.X., Di Giorgio, F.P., Yao, J., Marchetto, M.C., Brennand, K., Wright, R., Mei, A., McHenry, L., Lisuk, D., Grasmick, J.M., et al. Modeling hippocampal neurogenesis using human pluripotent stem cells. Stem Cell Reports 2 (2014), 295–310.