Increased bone morphogenetic protein signaling contributes to age-related declines in neurogenesis and cognition

Neurobiology of Aging

Volumn 38, Issue , 2016, Pages 164-175

  Meyers, Emily A ^a   Gobeske, Kevin T ^a   Bond, Allison M ^a   Jarrett, Jennifer C ^a   Peng, Chian Yu ^a   Kessler, John A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Aging; Dentate gyrus; Environmental enrichment; Neural stem cell; Novel object recognition

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 4; NOGGIN; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; BMP4 PROTEIN, MOUSE; CARRIER PROTEIN; NOGGIN PROTEIN;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; DENTATE GYRUS; ENVIRONMENTAL ENRICHMENT; HUMAN; HUMAN TISSUE; MALE; MEMORY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; Y-MAZE TEST; ANIMAL; C57BL MOUSE; COGNITION DISORDERS; GENE EXPRESSION; GENETICS; HIPPOCAMPUS; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY;

AGING; ANIMALS; BONE MORPHOGENETIC PROTEIN 4; CARRIER PROTEINS; COGNITION; COGNITION DISORDERS; DENTATE GYRUS; GENE EXPRESSION; HIPPOCAMPUS; HUMANS; MALE; MICE, INBRED C57BL; MOLECULAR TARGETED THERAPY; NEUROGENESIS; SIGNAL TRANSDUCTION;

EID: 84962255245     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2015.10.035     Document Type: Article

References (51)

1. Battiste J., Helms A.W., Kim E.J., Savage T.K., Lagace D.C., Mandyam C.D., Eisch A.J., Miyoshi G., Johnson J.E. Ascl1 defines sequentially generated lineage-restricted neuronal and oligodendrocyte precursor cells in the spinal cord. Development 2007, 134:285-293.
2. Beppu H., Lei H., Bloch K.D., Li E. Generation of a floxed allele of the mouse BMP type II receptor gene. Genesis 2005, 41:133-137.
3. Birch A.M., McGarry N.B., Kelly A.M. Short-term environmental enrichment, in the absence of exercise, improves memory, and increases NGF concentration, early neuronal survival, and synaptogenesis in the dentate gyrus in a time-dependent manner. Hippocampus 2013, 23:437-450.
4. Bishop N.A., Lu T., Yankner B.A. Neural mechanisms of ageing and cognitive decline. Nature 2010, 464:529-535.
5. Bizon J.L., Lee H.J., Gallagher M. Neurogenesis in a rat model of age-related cognitive decline. Aging Cell 2004, 3:227-234.
6. Bonaguidi M.A., Peng C.Y., McGuire T., Falciglia G., Gobeske K.T., Czeisler C., Kessler J.A. Noggin expands neural stem cells in the adult hippocampus. J. Neurosci. 2008, 28:9194-9204.
7. 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 2011, 145:1142-1155.
8. Bond A.M., Bhalala O.G., Kessler J.A. The dynamic role of bone morphogenetic proteins in neural stem cell fate and maturation. Dev. Neurobiol. 2012, 72:1068-1084.
9. Bond A.M., Peng C.Y., Meyers E.A., McGuire T., Ewaleifoh O., Kessler J.A. BMP signaling regulates the tempo of adult hippocampal progenitor maturation at multiple stages of the lineage. Stem Cells 2014, 32:2201-2214.
10. Chen H.L., Lein P.J., Wang J.Y., Gash D., Hoffer B.J., Chiang Y.H. Expression of bone morphogenetic proteins in the brain during normal aging and in 6-hydroxydopamine-lesioned animals. Brain Res. 2003, 994:81-90.
11. Clelland C.D., Choi M., Romberg C., Clemenson G.D., Fragniere A., Tyers P., Jessberger S., Saksida L.M., Barker R.A., Gage F.H., Bussey T.J. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 2009, 325:210-213.
12. Clemenson G.D., Lee S.W., Deng W., Barrera V.R., Iwamoto K.S., Fanselow M.S., Gage F.H. Enrichment rescues contextual discrimination deficit associated with immediate shock. Hippocampus 2015, 25:385-392.
13. Crews L., Adame A., Patrick C., Delaney A., Pham E., Rockenstein E., Hansen L., Masliah E. Increased BMP6 levels in the brains of Alzheimer's disease patients and APP transgenic mice are accompanied by impaired neurogenesis. J. Neurosci. 2010, 30:12252-12262.
14. Deng W., Aimone J.B., Gage F.H. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?. Nat. Rev. Neurosci. 2010, 11:339-350.
15. Deng W., Saxe M.D., Gallina I.S., Gage F.H. Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J. Neurosci. 2009, 29:13532-13542.
16. 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 2011, 8:566-579.
17. Esposito M.S., Piatti V.C., Laplagne D.A., Morgenstern N.A., Ferrari C.C., Pitossi F.J., Schinder A.F. Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J. Neurosci. 2005, 25:10074-10086.
18. Fabel K., Wolf S.A., Ehninger D., Babu H., Leal-Galicia P., Kempermann G. Additive effects of physical exercise and environmental enrichment on adult hippocampal neurogenesis in mice. Front. Neurosci. 2009, 3:50.
19. Feng J.Q., Harris M.A., Ghosh-Choudhury N., Feng M., Mundy G.R., Harris S.E. Structure and sequence of mouse bone morphogenetic protein-2 gene (BMP-2): comparison of the structures and promoter regions of BMP-2 and BMP-4 genes. Biochim. Biophys. Acta 1994, 1218:221-224.
20. Furutachi S., Matsumoto A., Nakayama K.I., Gotoh Y. p57 controls adult neural stem cell quiescence and modulates the pace of lifelong neurogenesis. EMBO J. 2013, 32:970-981.
21. Ganat Y.M., Silbereis J., Cave C., Ngu H., Anderson G.M., Ohkubo Y., Ment L.R., Vaccarino F.M. Early postnatal astroglial cells produce multilineage precursors and neural stem cells in vivo. J. Neurosci. 2006, 26:8609-8621.
22. Ge S., Goh E.L., Sailor K.A., Kitabatake Y., Ming G.L., Song H. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 2006, 439:589-593.
23. Genander M., Cook P.J., Ramskold D., Keyes B.E., Mertz A.F., Sandberg R., Fuchs E. BMP signaling and its pSMAD1/5 target genes differentially regulate hair follicle stem cell lineages. Cell Stem Cell 2014, 15:619-633.
24. Gobeske K.T., Das S., Bonaguidi M.A., Weiss C., Radulovic J., Disterhoft J.F., Kessler J.A. BMP signaling mediates effects of exercise on hippocampal neurogenesis and cognition in mice. PLoS One 2009, 4:e7506.
25. Hashimoto K., Fujita Y., Shimizu E., Iyo M. Phencyclidine-induced cognitive deficits in mice are improved by subsequent subchronic administration of clozapine, but not haloperidol. Eur. J. Pharmacol. 2005, 519:114-117.
26. Jessberger S., Clark R.E., Broadbent N.J., Clemenson G.D., Consiglio A., Lie D.C., Squire L.R., Gage F.H. Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn. Mem. 2009, 16:147-154.
27. Kempermann G., Gast D., Gage F.H. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann. Neurol. 2002, 52:135-143.
28. Kempermann G., Kuhn H.G., Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997, 386:493-495.
29. Kim E.J., Ables J.L., Dickel L.K., Eisch A.J., Johnson J.E. Ascl1 (Mash1) defines cells with long-term neurogenic potential in subgranular and subventricular zones in adult mouse brain. PLoS One 2011, 6:e18472.
30. Kobilo T., Liu Q.R., Gandhi K., Mughal M., Shaham Y., van Praag H. Running is the neurogenic and neurotrophic stimulus in environmental enrichment. Learn. Mem. 2011, 18:605-609.
31. Kronenberg G., Bick-Sander A., Bunk E., Wolf C., Ehninger D., Kempermann G. Physical exercise prevents age-related decline in precursor cell activity in the mouse dentate gyrus. Neurobiol. Aging 2006, 27:1505-1513.
32. Kuhn H.G., Dickinson-Anson H., Gage F.H. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 1996, 16:2027-2033.
33. Lazarov O., Mattson M.P., Peterson D.A., Pimplikar S.W., van Praag H. When neurogenesis encounters aging and disease. Trends Neurosci. 2010, 33:569-579.
34. Li D., Tang J., Xu H., Fan X., Bai Y., Yang L. Decreased hippocampal cell proliferation correlates with increased expression of BMP4 in the APPswe/PS1DeltaE9 mouse model of Alzheimer's disease. Hippocampus 2008, 18:692-698.
35. Lim D.A., Tramontin A.D., Trevejo J.M., Herrera D.G., Garcia-Verdugo J.M., Alvarez-Buylla A. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 2000, 28:713-726.
36. Marin-Burgin A., Schinder A.F. Requirement of adult-born neurons for hippocampus-dependent learning. Behav. Brain Res. 2012, 227:391-399.
37. Masuhara K., Nakase T., Suzuki S., Takaoka K., Matsui M., Anderson H.C. Use of monoclonal antibody to detect bone morphogenetic protein-4 (BMP-4). Bone 1995, 16:91-96.
38. Mikawa S., Sato K. Noggin expression in the adult rat brain. Neuroscience 2011, 184:38-53.
39. Mikawa S., Wang C., Sato K. Bone morphogenetic protein-4 expression in the adult rat brain. J. Comp. Neurol. 2006, 499:613-625.
40. Ming G.L., Song H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 2011, 70:687-702.
41. Mira H., Andreu Z., Suh H., Lie D.C., Jessberger S., Consiglio A., San Emeterio J., Hortiguela R., Marques-Torrejon M.A., Nakashima K., Colak D., Gotz M., Farinas I., Gage F.H. Signaling through BMPR-IA regulates quiescence and long-term activity of neural stem cells in the adult hippocampus. Cell Stem Cell 2010, 7:78-89.
42. Mustroph M.L., Chen S., Desai S.C., Cay E.B., DeYoung E.K., Rhodes J.S. Aerobic exercise is the critical variable in an enriched environment that increases hippocampal neurogenesis and water maze learning in male C57BL/6J mice. Neuroscience 2012, 219:62-71.
43. Olson A.K., Eadie B.D., Ernst C., Christie B.R. Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus 2006, 16:250-260.
44. Saxe M.D., Battaglia F., Wang J.W., Malleret G., David D.J., Monckton J.E., Garcia A.D., Sofroniew M.V., Kandel E.R., Santarelli L., Hen R., Drew M.R. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:17501-17506.
45. Shors T.J., Miesegaes G., Beylin A., Zhao M., Rydel T., Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature 2001, 410:372-376.
46. Tang J., Song M., Wang Y., Fan X., Xu H., Bai Y. Noggin and BMP4 co-modulate adult hippocampal neurogenesis in the APP(swe)/PS1(DeltaE9) transgenic mouse model of Alzheimer's disease. Biochem. Biophys. Res. Commun. 2009, 385:341-345.
47. Toni N., Sultan S. Synapse formation on adult-born hippocampal neurons. Eur. J. Neurosci. 2011, 33:1062-1068.
48. van Praag H., Shubert T., Zhao C., Gage F.H. Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci. 2005, 25:8680-8685.
49. Yassa M.A., Stark C.E. Pattern separation in the hippocampus. Trends Neurosci 2011, 34:515-525.
50. Zhang C.L., Zou Y., He W., Gage F.H., Evans R.M. A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 2008, 451:1004-1007.
51. Zhao C., Jou J., WolffL.J., Sun H., Gage F.H. Spine morphogenesis in newborn granule cells is differentially regulated in the outer and middle molecular layers. J. Comp. Neurol. 2014, 522:2756-2766.