Role of neuronal Ras activity in adult hippocampal neurogenesis and cognition

Frontiers in Neuroscience

Volumn , Issue FEB, 2011, Pages

  Manns, Martina ^a   Leske, Oliver ^a   Gottfried, Sebastian ^a   Bichler, Zoë ^a   Lafenêtre, Pauline ^a   Wahle, Petra ^a   Heumann, Rolf ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Hippocampus; Memory; Neurogenesis; Ras

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; BRAIN DERIVED NEUROTROPHIC FACTOR; CASPASE 3; GROWTH FACTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; HORMONE; MESSENGER RNA; NEUROPEPTIDE; NEUROTRANSMITTER; RAS PROTEIN;

BEHAVIOR; BRAIN DEVELOPMENT; COGNITION; COGNITIVE DEFECT; DENTATE GYRUS; EXERCISE; GENE EXPRESSION; HIPPOCAMPUS; MEMORY; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; REVIEW; SHORT TERM MEMORY; TRANSGENIC MOUSE; WILD TYPE;

EID: 84857416456     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2011.00018     Document Type: Review

References (90)

1. Adlard, P. A., Perreau, V. M., Engesser-Cesar, C., and Cotman, C. W. (2004). The timecourse of induction of brainderived neurotrophic factor mRNA and protein in the rat hippocampus following voluntary exercise. Neurosci. Lett. 363, 43-48.
2. Ahmadian, M. R., Stege, P., Scheffzek, K., and Wittinghofer, A. (1997). Confirmation of the arginine-finger hypothesis for the GAP-stimulated GTP-hydrolysis reaction of Ras. Nat. Struct. Biol. 4, 686-689.
3. Aimone, J. B., Deng, W., and Gage, F. H. (2010). Adult neurogenesis: integrating theories and separating functions. Trends Cogn. Sci. 14, 325-337.
4. Amrein, I., and Lipp, H. P. (2009). Adult hippocampal neurogenesis of mammals: evolution and life history. Biol. Lett. 5, 141-144.
5. Amrein, I., Slomianka, L., and Lipp, H. P. (2004). Granule cell number, cell death and cell proliferation in the dentate gyrus of wild-living rodents. Eur. J. Neurosci. 20, 3342-3350.
6. Arendt, T., Gärtner, U., Seeger, G., Barmashenko, G., Palm, K., Mittmann, T., Yan, L., Hümmeke, M., Behrbohm, J., Brückner, M. K., Holzer, M., Wahle, P., and Heumann, R. (2004). Neuronal activation of Ras regulates synaptic connectivity. Eur. J. Neurosci. 19, 2953-2966.
7. Attardo, A., Fabel, K., Krebs, J., Haubensak, W., Huttner, W. B., and Kempermann, G. (2010). Tis21 expression marks not only populations of neurogenic precursor cells but also new postmitotic neurons in adult hippocampal neurogenesis. Cereb. Cortex 20, 304-314.
8. Barker, J. M., and Galea, L. A. (2008). Repeated estradiol administration alters different aspects of neurogenesis and cell death in the hippocampus of female, but not male, rats. Neuroscience 152, 888-902.
9. Berchtold, N. C., Kesslak, J. P., Pike, C. J., Adlard, P. A., and Cotman, C. W. (2001). Estrogen and exercise interact to regulate brain-derived neurotrophic factor mRNA and protein expression in the hippocampus. Eur. J. Neurosci. 14, 1992-2002.
10. Bergami, M., Rimondini, R., Santi, S., Blum, R., Götz, M., and Canossa, M. (2008). Deletion of TrkB in adult progenitors alters newborn neuron integration into hippocampal circuits and increases anxiety-like behavior. Proc. Natl. Acad. Sci. U.S.A. 105, 15570-15575.
11. Borasio, G. D., John, J., Wittinghofer, A., Barde, Y. A., Sendtner, M., and Heumann, R. (1989). ras p21 protein promotes survival and fiber outgrowth of cultured embryonic neurons. Neuron 2, 1087-1096.
12. Borasio, G. D., Markus, A., Wittinghofer, A., Barde, Y. A., and Heumann, R. (1993). Involvement of ras p21 in neurotrophin-induced response of sensory, but not sympathetic neurons. J. Cell Biol. 121, 665-672.
13. Brandt, M. D., Maass, A., Kempermann, G., and Storch, A. (2010). Physical exercise increases Notch activity, proliferation and cell cycle exit of type-3 progenitor cells in adult hippocampal neurogenesis. Eur. J. Neurosci. 32, 1256-1264.
14. Brown, J., Cooper-Kuhn, C. M., Kempermann, G., Van Praag, H., Winkler, J., Gage, F. H., and Kuhn, H. G. (2003). Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur. J. Neurosci. 17, 2042-2046.
15. Canossa, M., Gärtner, A., Campana, G., Inagaki, N., and Thoenen, H. (2001). Regulated secretion of neurotrophins by metabotropic glutamate group I (mGluRI) and Trk receptor activation is mediated via phospholipase C signalling pathways. EMBO J. 20, 1640-1650.
16. Chakrabarty, K., Serchov, T., Mann, S. A., Dietzel, I. D., and Heumann, R. (2007). Enhancement of dopaminergic properties and protection mediated by neuronal activation of Ras in mouse ventral mesencephalic neurones. Eur. J. Neurosci. 25, 1971-1981.
17. Chan, J. P., Cordeira, J., Calderon, G. A., Iyer, L. K., and Rios, M. (2008). Depletion of central BDNF in mice impedes terminal differentiation of new granule neurons in the adult hippocampus. Mol. Cell. Neurosci. 39, 372-383.
18. Clelland, C. D., Choi, M., Romberg, C., Clemenson, G. D. Jr., Fragniere, A., Tyers, P., Jessberger, S., Saksida, L. M., Barker, R. A., Gage, F. H., and Bussey, T. J. (2009). A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325, 210-213.
19. Deisseroth, K., Singla, S., Toda, H., Monje, M., Palmer, T. D., and Malenka, R. C. (2004). Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42, 535-552.
20. Deng, W., Aimone, J. B., and Gage, F. H. (2010). New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat. Rev. Neurosci. 11, 339-350.
21. Deng, W., Saxe, M. D., Gallina, I. S., and Gage, F. H. (2009). Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J. Neurosci. 29, 13532-13542.
22. Denis-Donini, S., Dellarole, A., Crociara, P., Francese, M. T., Bortolotto, V., Quadrato, G., Canonico, P. L., Orsetti, M., Ghi, P., Memo, M., Bonini, S. A., Ferrari-Toninelli, G., and Grilli, M. (2008). Impaired adult neurogenesis associated with short-term memory defects in NF-kappaB p50-deficient mice. J. Neurosci. 28, 3911-3919.
23. Dominguez-Escriba, L., Hernendez-Rabaza, V., Soriano-Navarro, M., Barcia, J. A., Romero, F. J., Garcia-Verdugo, J. M., and Canales, J. J. (2006). Chronic cocaine exposure impairs progenitor proliferation but spares survival and maturation of neural precursors in adult rat dentate gyrus. Eur. J. Neurosci. 24, 586-594.
24. Gage, F. H. (2010). Molecular and cellular mechanisms contributing to the regulation, proliferation and differentiation of neural stem cells in the adult dentate gyrus. Keio J. Med. 59, 79-83.
25. Galea, L. A., Spritzer, M. D., Barker, J. M., and Pawluski, J. L. (2006). Gonadal hormone modulation of hippocampal neurogenesis in the adult. Hippocampus 16, 225-232.
26. Gärtner, U., Alpár, A., Behrbohm, J., Heumann, R., and Arendt, T. (2005). Enhanced Ras activity promotes spine formation in synRas mice neocortex. Neuroreport 16, 149-152.
27. Gärtner, U., Alpár, A., Seeger, G., Heumann, R., and Arendt, T. (2004). Enhanced Ras activity in pyramidal neurons induces cellular hypertrophy and changes in afferent and intrinsic connectivity in synRas mice. Int. J. Dev. Neurosci. 22, 165-173.
28. Ge, S., Goh, E. L., Sailor, K. A., Kitabatake, Y., Ming, G. L., and Song, H. (2006). GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439, 589-593.
29. Ge, S., Pradhan, D. A., Ming, G. L., and Song, H. (2007a). GABA sets the tempo for activity-dependent adult neurogenesis. Trends Neurosci. 30, 1-8.
30. Ge, S., Yang, C. H., Hsu, K. S., Ming, G. L., and Song, H. (2007b). A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54, 559-566.
31. Gustafson, T. L., Wellberg, E., Laffin, B., Schilling, L., Metz, R. P., Zahnow, C. A., and Porter, W. W. (2009). Ha-Ras transformation of MCF10A cells leads to repression of Singleminded-2s through NOTCH and C/EBPbeta. Oncogene 28, 1561-1568.
32. Hastings, N. B., and Gould, E. (2003). Neurons inhibit neurogenesis. Nat. Med. 9, 264-266.
33. Hayes, N. L., and Nowakowski, R. S. (2000). Exploiting the dynamics of S-phase tracers in developing brain: interkinetic nuclear migration for cells entering versus leaving the S-phase. Dev. Neurosci. 22, 44-55.
34. Heumann, R. (1994). Neurotrophin signalling. Curr. Opin. Neurobiol. 4, 668-679.
35. Heumann, R., Goemans, C., Bartsch, D., Lingenhöhl, K., Waldmeier, P. C., Hengerer, B., Allegrini, P. R., Schellander, K., Wagner, E. F., Arendt, T., Kamdem, R. H., Obst-Pernberg, K., Narz, F., Wahle, P., and Berns, H. (2000). Transgenic activation of Ras in neurons promotes hypertrophy and protects from lesion-induced degeneration. J. Cell Biol. 151, 1537-1548.
36. Holzer, M., Gartner, U., Klinz, F., Narz, F., Heumann, R., and Arendt, T. (2001). Activation of mitogen-activated protein kinase cascade and phosphorylation of cytoskeletal proteins after neurone-specific activation of p21ras. I. Mitogen-activated protein kinase cascade. Neuroscience 105, 1031-1040.
37. Isgor, C., and Watson, S. J. (2005). Estrogen receptor alpha and beta mRNA expressions by proliferating and differentiating cells in the adult rat dentate gyrus and subventricular zone. Neuroscience 134, 847-856.
38. Itou, Y., Nochi, R., Kuribayashi, H., Saito, Y., and Hisatsune, T. (2010). Cholinergic activation of hippocampal neural stem cells in aged dentate gyrus. Hippocampus. [Epub ahead of print].
39. Jessberger, S., Clark, R. E., Broadbent, N. J., Clemenson, G. D. Jr., Consiglio, A., Lie, D. C., Squire, L. R., and Gage, F. H. (2009). Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn. Mem. 16, 147-154.
40. Johnson, R. A., Rhodes, J. S., Jeffrey, S. L., Garland, T. Jr., and Mitchell, G. S. (2003). Hippocampal brain-derived neurotrophic factor but not neurotrophin-3 increases more in mice selected for increased voluntary wheel running. Neuroscience 121, 1-7.
41. Kempermann, G. (2002). Why new neurons? Possible functions for adult hippocampal neurogenesis. J. Neurosci. 22, 635-638.
42. Kempermann, G. (2008). The neurogenic reserve hypothesis: what is adult hippocampal neurogenesis good for? Trends Neurosci. 31, 163-169.
43. Kempermann, G., Jessberger, S., Steiner, B., and Kronenberg, G. (2004a). Milestones of neuronal development in the adult hippocampus. Trends Neurosci. 27, 447-452.
44. Kempermann, G., Wiskott, L., and Gage, F. H. (2004b). Functional significance of adult neurogenesis. Curr. Opin. Neurobiol. 14, 186-191.
45. Kronenberg, G., Reuter, K., Steiner, B., Brandt, M. D., Jessberger, S., Yamaguchi, M., and Kempermann, G. (2003). Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J. Comp. Neurol. 467, 455-463.
46. Lafenêtre, P., Leske, O., Ma-Högemeie, Z., Haghikia, A., Bichler, Z., Wahle, P., and Heumann, R. (2010). Exercise can rescue recognition memory impairment in a model with reduced adult hippocampal neurogenesis. Front. Behav. Neurosci. 3:34. doi: 10.3389/ neuro.08.034.2009
47. Lagace, D. C., Whitman, M. C., Noonan, M. A., Ables, J. L., DeCarolis, N. A., Arguello, A. A., Donovan, M. H., Fischer, S. J., Farnbauch, L. A., Beech, R. D., DiLeone, R. J., Greer, C. A., Mandyam, C. D., and Eisch, A. J. (2007). Dynamic contribution of nestin-expressing stem cells to adult neurogenesis. J. Neurosci. 27, 12623-12629.
48. Lai, K., Kaspar, B. K., Gage, F. H., and Schaffer, D. V. (2003). Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat. Neurosci. 6, 21-27.
49. Lessmann, V., Gottmann, K., and Malcangio, M. (2003). Neurotrophin secretion: current facts and future prospects. Prog. Neurobiol. 69, 341-374.
50. Leuner, B., and Gould, E. (2010). Structural plasticity and hippocampal function. Annu. Rev. Psychol. 61, 111-140.
51. Leuner, B., Waddell, J., Gould, E., and Shors, T. J. (2006). Temporal discontiguity is neither necessary nor sufficient for learning-induced effects on adult neurogenesis. J. Neurosci. 27, 13437-13442.
52. Li, G., and Pleasure, S. J. (2010). Ongoing interplay between the neural network and neurogenesis in the adult hippocampus. Curr. Opin. Neurobiol. 20, 126-133.
53. Li, L., Walker, T. L., Zhang, Y., Mackay, E. W., and Bartlett, P. F. (2010). Endogenous interferon gamma directly regulates neural precursors in the non-inflammatory brain. J. Neurosci. 30, 9038-9050.
54. Li, Y., Luikart, B. W., Birnbaum, S., Chen, J., Kwon, C. H., Kernie, S. G., Bassel-Duby, R., and Parada, L. F. (2008). TrkB regulates hippocampal neurogenesis and governs sensitivity to antidepressive treatment. Neuron 59, 399-412.
55. Li, Y., Mu, Y., and Gage, F. H. (2009). Development of neural circuits in the adult hippocampus. Curr. Top. Dev. Biol. 87, 149-174.
56. Lie, D. C., Colamarino, S. A., Song, H. J., Désiré, L., Mira, H., Consiglio, A., Lein, E. S., Jessberger, S., Lansford, H., Dearie, A. R., and Gage, F. H. (2005). Wnt signalling regulates adult hippocampal neurogenesis. Nature 437, 1370-1375.
57. Lledo, P. M., Alonso, M., and Grubb, M. S. (2006). Adult neurogenesis and functional plasticity in neuronal circuits. Nat. Rev. Neurosci. 7, 179-193.
58. Lugert, S., Basak, O., Knuckles, P., Haussler, U., Fabel, K., Götz, M., Haas, C. A., Kempermann, G., Taylor, V., and 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.
59. Ma, D. K., Jang, M. H., Guo, J. U., Kitabatake, Y., Chang, M. L., Pow-Ankongkul, N., Flavell, R. A., Lu, B., Ming, G. L., and Song, H. (2009). Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323, 1074-1077.
60. Makwana, M., Serchov, T., Hristova, M., Bohatschek, M., Gschwendtner, A., Kalla, R., Liu, Z., Heumann, R., and Raivich, G. (2009). Regulation and function of neuronal GTP-Ras in facial motor nerve regeneration. J. Neurochem. 108, 1453-1463.
61. Mandyam, C. D., Harburg, G. C., and Eisch, A. J. (2007). Determination of key aspects of precursor cell proliferation, cell cycle length and kinetics in the adult mouse subgranular zone. Neuroscience 146, 108-122.
62. Manns, M., Bichler, Z., Leske, O., and Heumann, R. (2010). Neuronal Ras activation inhibits adult hippocampal progenitor cell division and impairs spatial short-term memory. Genes Brain Behav. 9, 525-536.
63. Manns, M., Güntürkün, O., Heumann, R., and Blöchl, A. (2005). Photic inhibition of TrkB/Ras activity in the pigeon's tectum during development: impact on brain asymmetry formation. Eur. J. Neurosci. 22, 2180-2186.
64. McEwen, B. S. (2010). Stress, sex, and neural adaptation to a changing environment: mechanisms of neuronal remodeling. Ann. N. Y. Acad. Sci. 1204(Suppl.), E38-E59.
65. Ming, G. L., and Song, H. (2005). Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci. 28, 223-250.
66. Mira, H., Andreu, Z., Suh, H., Lie, D. C., Jessberger, S., Consiglio, A., San Emeterio, J., Hortigüela, R., Marqués-Torrejón, M. A., Nakashima, K., Colak, D., Götz, M., Fariñas, I., and Gage, F. H. (2010). Signaling through BMPR-IA regulates quiescence and long-term activity of neural stem cells in the adult hippocampus. Cell Stem Cell 7, 78-89.
67. Mu, Y., Lee, S. W., and Gage, F. H. (2010). Signaling in adult neurogenesis. Curr. Opin. Neurobiol. 20, 416-423.
68. Nacher, J., and McEwan, B. S. (2006). The role of N-methyl-D-aspartate receptors in neurogenesis. Hippocampus 16, 267-270.
69. Ninkovic, J., Mori, T., and Götz, M. (2007). Distinct modes of neuron addition in adult mouse neurogenesis. J. Neurosci. 27, 10906-10911.
70. Patz, S., Colovic, C., Wawro, S., Lafenetre, P., Leske, O., Heumann, R., Schönfelder, S., Tomaschewski, J., Räk, A., and Wahle, P. (2009). Interneuronal growth and expression of interneuronal markers in visual cortex of mice with transgenic activation of Ras. Exp. Brain Res. 199, 265-278.
71. Scharfman, H., Goodman, J., Macleod, A., Phani, S., Antonelli, C., and Croll, S. (2005). Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp. Neurol. 192, 348-356.
72. Schmidt-Hieber, C., Jonas, P., and Bischofberger, J. (2004). Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429, 184-187.
73. Seeger, G., Gärtner, U., and Arendt, T. (2005). Transgenic activation of Ras in neurons increases synapse formation in mouse neocortex. J. Neural Transm. 112, 751-761.
74. Snyder, J. S., Kee, N., and Wojtowicz, J. M. (2001). Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J. Neurophysiol. 85, 2423-2431.
75. Spritzer, M. D., and Galea, L. A. (2007). Testosterone and dihydrotestosterone, but not estradiol, enhance survival of new hippocampal neurons in adult male rats. Dev. Neurobiol. 67, 1321-1333.
76. Squire, L. R., Wixted, J. T., and Clark, R. E. (2007). Recognition memory and the medial temporal lobe: a new perspective. Nat. Rev. Neurosci. 8, 872-883.
77. Steiner, B., Klempin, F., Wang, L., Kott, M., Kettenmann, H., and Kempermann, G. (2006). Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia 54, 805-814.
78. Suh, H., Deng, W., and Gage, F. H. (2009). Signaling in adult neurogenesis. Annu. Rev. Cell Dev. Biol. 25, 253-275.
79. Tanapat, P., Hastings, N. B., and Gould, E. (2005). Ovarian steroids influence cell proliferation in the dentate gyrus of the adult female rat in a dose- and time-dependent manner. J. Comp. Neurol. 481, 252-265.
80. Tashiro, A., Makino, H., and Gage, F. H. (2007). Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J. Neurosci. 27, 3252-3259.
81. Tashiro, A., Sandler, V. M., Toni, N., Zhao, C., and Gage, F. H. (2006). NMDA-receptor-mediated, cellspecific integration of new neurons in adult dentate gyrus. Nature 442, 929-933.
82. Toni, N., Laplagne, D. A., Zhao, C., Lombardi, G., Ribak, C. E., Gage, F. H., and Schinder, A. F. (2008). Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat. Neurosci. 11, 901-907.
83. Tozuka, Y., Fukuda, S., Namba, T., Seki, T., and Hisatsune, T. (2005). GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47, 803-815.
84. Van Praag, H., Kempermann, G., and Gage, F. H. (1999). Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 2, 266-270.
85. Wang, L. P., Kempermann, G., and Kettenmann, H. (2005). A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol. Cell. Neurosci. 29, 181-189.
86. Willert, K., and Nusse, R. (1998). Betacatenin: a key mediator of Wnt signaling. Curr. Opin. Genet. Dev. 8, 95-102.
87. Winocur, G., Wojtowicz, J. M., Sekeres, M., Snyder, J. S., and Wang, S. (2006). Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 16, 296-304.
88. Wojtowicz, J. M., Askew, M. L., and Winocur, G. (2008). The effect of running and inhibiting adult neurogenesis on learning and memory in rats. Eur. J. Neurosci. 27, 1494-1502.
89. Zhang, L., Yang, X., Yang, S., and Zhang, J. (2011). The wnt/b-catenin signaling pathway in adult neurogenesis. Eur. J. Neurosci. 33, 1-8.
90. Zhao, C., Deng, W., and Gage, F. H. (2008). Mechanisms and functional implications of adult neurogenesis. Cell 132, 645-660.