Neural stem cell- and neurogenesis-related gene expression profiles in the young and aged dentate gyrus

Age

Volumn 35, Issue 6, 2013, Pages 2165-2176

  Shetty, Geetha A ^a,b,c   Hattiangady, Bharathi ^a,b,c,d,e   Shetty, Ashok K ^a,b,c,d,e  

^a SCOTT AND WHITE MEMORIAL HOSPITAL   (United States)

^b CTVHCS   (United States)

^c TEXAS A M COLLEGE OF MEDICINE   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

^e DURHAM VA MEDICAL CENTER   (United States)

Author keywords

Aging; Dentate gyrus; Dentate neurogenesis; Gene expression; Genes; Hippocampal neurogenesis; Hippocampus; Neural stem cells; QRT PCR; Stem cells and aging

Indexed keywords

CYTOKINE; GROWTH FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SONIC HEDGEHOG PROTEIN; STAT3 PROTEIN;

ADORA1 GENE; AGED; AGING; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN TISSUE; CDK5RAP3 GENE; CELL ADHESION; CELL CYCLE ARREST; CELL CYCLE REGULATION; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; DNA DAMAGE; FISCHER 344 RAT; GENE; GENE EXPRESSION PROFILING; GENE FUNCTION; INTRACELLULAR SIGNALING; JUVENILE ANIMAL; MALE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROMODULATION; NONHUMAN; RAT; REAL TIME POLYMERASE CHAIN REACTION; SHH GENE; STABLE EXPRESSION; STAT3 GENE; SYNAPSE; TRANSCRIPTION REGULATION;

AGING; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; DENTATE GYRUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; NEURAL STEM CELLS; NEUROGENESIS; RATS; RATS, INBRED F344; REAL-TIME POLYMERASE CHAIN REACTION; RNA;

EID: 84888644768     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-012-9507-6     Document Type: Article

References (72)

1. Ahn S, Joyner AL (2005) In vivo analyses of quiescent adult neural stem cells responding to sonic hedgehog. Nature 437:894-897
2. Aimone JB, Wiles J, Gage FH (2006) Potential role for adult neurogenesis in the encoding of time in new memories. Not as tenants in common Neurosci 9:723-727
3. Aizawa K, Ageyama N, Terao K, Hisatsune T (2011) Primatespecific alterations in neural stem/progenitor cells in the aged hippocampus. Neurobiol Aging 32:140-150
4. Bachstetter AD, Pabon MM, Cole MJ, Hudson CE, Sanberg PR, Willing AE, Bickford PC, Gemma C (2008) Peripheral injection of human umbilical cord blood stimulates neurogenesis in the aged rat brain. BMC Neurosci 9:22
5. Bernal GM, Peterson DA (2004) Neural stem cells as therapeutic agents for age-related brain repair. Aging Cell 3:345- 351
6. Bernal GM, Peterson DA (2011) Phenotypic and gene expression modification with normal brain aging in GFAPpositive astrocytes and neural stem cells. Aging Cell 10:466-482
7. Boison D (2008) Adenosine as a neuromodulator in neurological diseases. Curr Opin Pharmacol 8:2-7
8. Brockmann R, Beyer A, Heinisch JJ, Wilhelm T (2007) Posttranscriptional expression regulation: what determines translation rates? PLoS Comput Biol 3:e57
9. Cameron HA, McKay RD (1999) Restoring production of hippocampal neurons in old age. Nat Neurosci 2:894-897
10. Chadashvili T, Peterson DA (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. Cheng N, Brantley DM, Liu H, Lin Q, Enriquez M, Gale N, Yancopoulos G, Cerretti DP, Daniel TO, Chen J (2002) Blockade of EphA receptor tyrosine kinase activation inhibits vascular endothelial cell growth factor-induced angiogenesis. Mol Cancer Res 1:2-11
12. Ching YP, Qi Z, Wang JH (2000) Cloning of three novel neuronal Cdk5 activator binding proteins. Gene 242:285- 294
13. Clelland CD, Choi M, Romberg C, Clemenson GD Jr, Fragniere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH, Bussey TJ (2009) A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325:210-213
14. Coleman GL, Barthold W, Osbaldiston GW, Foster SJ, Jonas AM (1977) Pathological changes during aging in barrierreared Fischer 344 male rats. J Gerontol 32:258-278
15. Dever TE (2002) Gene-specific regulation by general translation factors. Cell 108:545-556
16. Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza PV, Abrous DN (2003) Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc Natl Acad Sci U S A 100:14385-14390
17. Drapeau E, Nora Abrous D (2008) Stem cell review series: role of neurogenesis in age-related memory disorders. Aging Cell 7:569-589
18. Dupret D, Fabre A, Dobrossy MD, Panatier A, Rodriguez JJ, Lamarque S, Lemaire V, Oliet SH, Piazza PV, Abrous DN (2007) Spatial learning depends on both the addition and removal of new hippocampal neurons. PLoS Biol 5:e214
19. Eisch AJ, Cameron HA, Encinas JM, Meltzer LA, Ming GL, Overstreet-Wadiche LS (2008) Adult neurogenesis, mental health, and mental illness: hope or hype? J Neurosci 28:11785-11791
20. 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
21. Faigle R, Song H (2012) Signaling mechanisms regulating adult neural stem cells and neurogenesis. Biochim Biophys Acta. doi:10.1016/j.bbagen.2012.09.002
22. Gage FH (2002) Neurogenesis in the adult brain. J Neurosci 22:612-613
23. Gebauer F, Hentze MW (2004) Molecular mechanisms of translational control. Nat Rev Mol Cell Biol 5:827-835
24. Gingold H, Pilpel Y (2011) Determinants of translation efficiency and accuracy. Mol Syst Biol 7:481
25. Gould E (2007) How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 8:481-488
26. Gray PA, Fu H, Luo P, Zhao Q, Yu J, Ferrari A, Tenzen T, Yuk DI, Tsung EF, Cai Z, Alberta JA, Cheng LP, Liu Y, Stenman JM, Valerius MT, Billings N, Kim HA, Greenberg ME, McMahon AP, Rowitch DH, Stiles CD, Ma Q (2004) Mouse brain organization revealed through direct genome-scale TF expression analyses. Science 306:2255-2257
27. Hamil NE, Cock HR, Walker MC (2012) Acute downregulation of adenosine A(1) receptor activity in status epilepticus. Epilepsia 53:177-188
28. Hattiangady B, Rao MS, Shetty GA, Shetty AK (2005) Brainderived 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
29. 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
30. Hattiangady B, Shuai B, Cai J, Coksaygan T, Rao MS, Shetty AK (2007) Increased dentate neurogenesis after grafting of glial restricted progenitors or neural stem cells in the aging hippocampus. Stem Cells 25:2104-2117
31. Heine VM, Maslam S, Joels M, Lucassen PJ (2004) Prominent decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an agerelated hypothalamus-pituitary-adrenal axis activation. Neurobiol Aging 25:361-375
32. Ihle JN (2001) The stat family in cytokine signaling. Curr Opin Cell Biol 13:211-217
33. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11:1153-1161
34. Jalali A, Bassuk AG, Kan L, Israsena N, Mukhopadhyay A, McGuire T, Kessler JA (2011) HeyL promotes neuronal differentiation of neural progenitor cells. J Neurosci Res 89:299-309
35. Jessberger S, Clark RE, Broadbent NJ, Clemenson GD Jr, Consiglio A, Lie DC, Squire LR, Gage FH (2009) Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem 16:147-154
36. Jessberger S, Gage FH (2008) Stem-cell-associated structural and functional plasticity in the aging hippocampus. Psychol Aging 23:684-691
37. Jiao J, Chen DF (2008) Induction of neurogenesis in nonconventional neurogenic regions of the adult central nervous system by niche astrocyte-produced signals. Stem Cells 26:1221-1230
38. Jiang H, Wu J, He C, Yang W, Li H (2009) Tumor suppressor protein C53 antagonizes checkpoint kinases to promote cyclin-dependent kinase 1 activation. Cell Res 19:458-468
39. 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
40. Kee N, Teixeira CM, Wang AH, Frankland PW (2007) Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Not as tenants in common Neurosci 10:355-362
41. Koh MT, Haberman RP, Foti S, McCown TJ, Gallagher M (2010) Treatment strategies targeting excess hippocampal activity benefit aged rats with cognitive impairment. Neuropsychopharmacol 35:1016-1025
42. 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
43. Lai K, Kaspar BK, Gage FH, Schaffer DV (2003) Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat Neurosci 6:21-27
44. Larsson C, Lardelli M, White I, Lendahl U (1994) The human NOTCH1, 2, and 3 genes are located at chromosome positions 9q34, 1p13-p11, and 19p13.2-p13.1 in regions of neoplasia-associated translocation. Genomics 24:253-258
45. Lauri SE, Taira T, Kaila K, Rauvala H (1996) Activity-induced enhancement of HB-GAM expression in rat hippocampal slices. Neuroreport 7:1670-1674
46. Leuner B, Gould E (2010) Structural plasticity and hippocampal function. Annu Rev Psychol 61:111-140
47. Leuner B, Gould E, Shors TJ (2006) Is there a link between adult neurogenesis and learning? Hippocampus 16:216- 224
48. Lie DC, Colamarino SA, Song HJ, Desire L, Mira H, Consiglio A, Lein ES, Jessberger S, Lansford H, Dearie AR, Gage FH (2005) Wnt signalling regulates adult hippocampal neurogenesis. Nature 437:1370-1375
49. Lindner AB, Demarez A (2009) Protein aggregation as a paradigm of aging. Biochim Biophys Acta 1790:980-996
50. Maroney PA, Yu Y, Nilsen TW (2006) MicroRNAs, mRNAs, and translation. Cold Spring Harb Symp Quant Biol 71:531-535
51. Mata J, Marguerat S, Bahler J (2005) Post-transcriptional control of gene expression: A genome-wide perspective. Trends Biochem Sci 30:506-514
52. McDonald HY, Wojtowicz JM (2005) Dynamics of neurogenesis in the dentate gyrus of adult rats. Neurosci Lett 385:70-75
53. Miranda CJ, Braun L, Jiang Y, Hester ME, Zhang L, Riolo M, Wang H, Rao M, Altura RA, Kaspar BK (2012) Aging brain microenvironment decreases hippocampal neurogenesis through Wnt-mediated survivin signaling. Aging Cell 11:542-552
54. Muller S, Chakrapani BPS, Schwegler H, Hofmann H-D, Kirsch M (2009) Neurogenesis in the dentate gyrus depends on ciliary neurotrophic factor and signal transducer and activator of transcription 3 signaling. Stem Cells 27:431-441
55. Nacher J, Alonso-Llosa G, Rosell DR, McEwen BS (2003) NMDA receptor antagonist treatment increases the production of new neurons in the aged rat hippocampus. Neurobiol Aging 24:273-284
56. Olariu A, Cleaver KM, Cameron HA (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
57. Pavlov I, Voikar V, Kaksonen M, Lauri SE, Hienola A, Taira T, Rauvala H (2002) Role of heparin-binding growthassociated molecule (HB-GAM) in hippocampal LTP and spatial learning revealed by studies on overexpressing and knockout mice. Mol Cell Neurosci 20:330-342
58. Petersen CP, Bordeleau ME, Pelletier J, Sharp PA (2006) Short RNAs repress translation after initiation in mammalian cells. Mol Cell 21:533-542
59. Raghavan A, Ogilvie RL, Reilly C, Abelson ML, Raghavan S, Vasdewani J, Krathwohl M, Bohjanen PR (2002) Genomewide analysis of mRNA decay in resting and activated primary human T lymphocytes. Nucleic Acids Res 30:5529-5538
60. Rao MS, Hattiangady B, Abdel-Rahman A, Stanley DP, Shetty AK (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
61. 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
62. Rauvala H, Pihlaskari R (1987) Isolation and some characteristics of an adhesive factor of brain that enhances neurite outgrowth in central neurons. J Biol Chem 262:16625- 16635
63. Ruiz A, Altaba I, Palma V, Dahmane N (2002) Hedgehog-Gli signaling and the growth of the brain. Nat Rev Neurosci 3:24-33
64. Sahay A, Hen R (2007) Adult hippocampal neurogenesis in depression. Nat Neurosci 10:1110-1115
65. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:805-809
66. Schouten M, Buijink MR, Lucassen PJ, Fitzsimons CP (2012) New neurons in aging brains: molecular control by small non-coding RNAs. Front Neurosci 6:25
67. Seki T, Arai Y (1995) Age-related production of new granule cells in the adult dentate gyrus. Neuroreport 6:2479-2482
68. 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
69. Townsend-Nicholson A, Baker E, Schofield PR, Sutherland GR (1995) Localization of the adenosine A1 receptor subtype gene (ADORA1) to chromosome 1q32.1. Genomics 26:423-425
70. Walter J, Keiner S, Witte OW, Redecker C (2011) Age-related effects on hippocampal precursor cell subpopulations and neurogenesis. Neurobiol Aging 32:1906-1914
71. Wu J, Lei G, Mei M, Tang Y, Li H (2010) A novel C53/LZAPinteracting protein regulates stability of C53/LZAP and DDRGK domain-containing Protein 1 (DDRGK1) and modulates NF-kappaB signaling. J Biol Chem 285:15126- 15136
72. Zeng Y, Tan M, Kohyama J, Sneddon M, Watson JB, Sun YE, Xie CW (2011) Epigenetic enhancement of BDNF signaling rescues synaptic plasticity in aging. J Neurosci 31:17800-17810