Extremely low-frequency electromagnetic fields enhance the survival of newborn neurons in the mouse hippocampus

European Journal of Neuroscience

Volumn 39, Issue 6, 2014, Pages 893-903

  Podda, Maria V ^a   Leone, Lucia ^a   Barbati, Saviana A ^a   Mastrodonato, Alessia ^a   Li Puma, Domenica D ^a   Piacentini, Roberto ^a   Grassi, Claudio ^a  

^a CATHOLIC UNIVERSITY   (Italy)

Author keywords

Amyloid protein; Apoptosis; Bax Bcl 2 ratio; Neurogenesis; Spatial memory

Indexed keywords

BROXURIDINE; DOUBLECORTIN; NEURON SPECIFIC NUCLEAR PROTEIN; PROTEIN BAX; PROTEIN BCL 2;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL COUNT; CELL LABELING; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; ELECTROMAGNETIC FIELD; HIPPOCAMPUS; IN VITRO STUDY; LOW FREQUENCY ELECTROMAGNETIC FIELD; MEMORY CONSOLIDATION; MOUSE; NERVE CELL; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPATIAL LEARNING; WESTERN BLOTTING;

AMYLOID-Β PROTEIN; APOPTOSIS; BAX/BCL-2 RATIO; NEUROGENESIS; SPATIAL MEMORY;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL SURVIVAL; ELECTROMAGNETIC FIELDS; HIPPOCAMPUS; MALE; MAZE LEARNING; MEMORY; MICE; MICE, INBRED C57BL; NEUROGENESIS; NEURONS; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 84900366638     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12465     Document Type: Article

References (72)

1. Abrous, D.N., Koehl, M. & Le Moal, M. (2005) Adult neurogenesis: from precursors to network and physiology. Physiol. Rev., 85, 523-569.
2. 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.
3. Alvarez-Buylla, A. & Garcia-Verdugo, J.M. (2002) Neurogenesis in adult subventricular zone. J. Neurosci., 22, 629-634.
4. Arias-Carrión, O., Verdugo-Díaz, L., Feria-Velasco, A., Millán-Aldaco, D., Gutiérrez, A.A., Hernández-Cruz, A. & Drucker-Colín, R. (2004) Neurogenesis in the subventricular zone following transcranial magnetic field stimulation and nigrostriatal lesions. J. Neurosci. Res., 78, 16-28.
5. Bellenchi, G.C., Volpicelli, F., Piscopo, V., Perrone-Capano, C. & di Porzio, U. (2013) Adult neural stem cells: an endogenous tool to repair brain injury? J. Neurochem., 124, 159-167.
6. Biebl, M., Cooper, C.M., Winkler, J. & Kuhn, H.G. (2000) Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci. Lett., 291, 17-20.
7. Biscaro, B., Lindvall, O., Hock, C., Ekdahl, C.T. & Nitsch, R.M. (2009) Abeta immunotherapy protects morphology and survival of adult-born neurons in doubly transgenic APP/PS1 mice. J. Neurosci., 29, 14108-14119.
8. Bissonnette, R.P., Echeverri, F., Mahboubi, A. & Green, D.R. (1992) Apoptotic cell death induced by c-myc is inhibited by bcl-2. Nature, 359, 552-554.
9. Brown, J., Cooper-Kuhn, C.M., Kempermann, G., Van Praag, H., Winkler, J., Gage, F.H. & Kuhn, H.G. (2003) Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur. J. Neurosci., 17, 2042-2046.
10. Bruel-Jungerman, E., Laroche, S. & Rampon, C. (2005) New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur. J. Neurosci., 21, 513-521.
11. Cameron, H.A. & McKay, R.D. (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol., 435, 406-417.
12. Capilla-Gonzalez, V., Gil-Perotin, S., Ferragud, A., Bonet-Ponce, L., Canales, J. & Garcia-Verdugo, J. (2012) Exposure to N-ethyl-N-nitrosourea in adult mice alters structural and functional integrity of neurogenic sites. PLoS ONE, 7, e29891.
13. Corvino, V., Marchese, E., Giannetti, S., Lattanzi, W., Bonvissuto, D., Biamonte, F., Mongiovì, A.M., Michetti, F. & Geloso, M.C. (2012) The neuroprotective and neurogenic effects of neuropeptide Y administration in an animal model of hippocampal neurodegeneration and temporal lobe epilepsy induced by trimethyltin. J. Neurochem., 122, 415-426.
14. Cuccurazzu, B., Leone, L., Podda, M.V., Piacentini, R., Riccardi, E., Ripoli, C., Azzena, G.B. & Grassi, C. (2010) Exposure to extremely low-frequency (50 Hz) electromagnetic fields enhances adult hippocampal neurogenesis in C57BL/6 mice. Exp. Neurol., 226, 173-182.
15. Cunningham, J., Estrella, V., Lloyd, M., Gillies, R., Frieden, B.R. & Gatenby, R. (2012) Intracellular electric field and pH optimize protein localization and movement. PLoS ONE, 7, e36894.
16. Curcio, L., Podda, M.V., Leone, L., Piacentini, R., Mastrodonato, A., Cappelletti, P., Sacchi, S., Pollegioni, L., Grassi, C. & D'Ascenzo, M. (2013) Reduced D-serine levels in the nucleus accumbens of cocaine-treated rats hinder the induction of NMDA receptor-dependent synaptic plasticity. Brain, 136, 1216-1230.
17. Curlik, D.M. 2nd. & Shors, T.J. (2011) Learning increases the survival of newborn neurons provided that learning is difficult to achieve and successful. J. Cognitive Neurosci., 23, 2159-2170.
18. Czéh, B., Welt, T., Fischer, A.K., Erhardt, A., Schmitt, W., Müller, M.B., Toschi, N., Fuchs, E. & Keck, M.E. (2002) Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis. Biol. Psychiat., 52, 1057-1065.
19. Dayer, A.G., Ford, A.A., Cleaver, K.M., Yassaee, M. & Cameron, H.A. (2003) Short-term and long-term survival of new neurons in the rat dentate gyrus. J. Comp. Neurol., 460, 563-572.
20. Demars, M., Hu, Y.S., Gadadhar, A. & Lazarov, O. (2010) Impaired neurogenesis is an early event in the etiology of familial Alzheimer's disease in transgenic mice. J. Neurosci. Res., 88, 2103-2117.
21. Di Lazzaro, V., Capone, F., Apollonio, F., Borea, P.A., Cadossi, R., Fassina, L., Grassi, C., Liberti, M., Paffi, A., Parazzini, M., Varani, K. & Ravazzani, P. (2013) A consensus panel review of central nervous system effects of the exposure to low-intensity extremely low-frequency magnetic fields. Brain Stimul., 6, 469-476.
22. Dupret, D., Revest, J.M., Koehl, M., Ichas, F., De Giorgi, F., Costet, P., Abrous, D.N. & Piazza, P.V. (2008) Spatial relational memory requires hippocampal adult neurogenesis. PLoS ONE, 3, e1959.
23. Eisch, A.J. & Petrik, D. (2012) Depression and hippocampal neurogenesis: a road to remission? Science, 338, 72-75.
24. El Beltagy, M., Mustafa, S., Umka, J., Lyons, L., Salman, A., Dormon, K., Allcock, C., Bennett, G. & Wigmore, P. (2012) The effect of 5-fluorouracil on the long term survival and proliferation of cells in the rat hippocampus. Brain Res. Bull., 88, 514-518.
25. Emre, M., Cetiner, S., Zencir, S., Unlukurt, I., Kahraman, I. & Topcu, Z. (2011) Oxidative stress and apoptosis in relation to exposure to magnetic field. Cell Biochem. Biophys., 59, 71-77.
26. 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.
27. Fetoni, A.R., Piacentini, R., Fiorita, A., Paludetti, G. & Troiani, D. (2009) Water-soluble coenzyme Q10 formulation (Q-ter) promotes outer hair cell survival in a guinea pig model of noise induced hearing loss (NIHL). Brain Res., 1257, 108-116.
28. Fusco, S., Ripoli, C., Podda, M.V., Ranieri, S.C., Leone, L., Toietta, G., McBurney, M.W., Schütz, G., Riccio, A., Grassi, C., Galeotti, T. & Pani, G. (2012) A role for neuronal CREB (cAMP responsive element binding)-1 in brain responses to calorie restriction. Proc. Natl. Acad. Sci. USA, 109, 621-626.
29. Gage, F.H. (2000) Mammalian neural stem cells. Science, 287, 1433-1438.
30. Garthe, A., Behr, J. & Kempermann, G. (2009) Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS ONE, 4, e5464.
31. Goodman, T., Trouche, S., Massou, I., Verret, L., Zerwas, M., Roullet, P. & Rampon, C. (2010) Young hippocampal neurons are critical for recent and remote spatial memory in adult mice. Neuroscience, 171, 769-778.
32. Gould, E., Beylin, A., Tanapat, P., Reeves, A. & Shors, T.J. (1999) Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci., 2, 260-265.
33. 2+ channels and their role in modulation of neuroendocrine cell proliferation and death. Cell Calcium, 35, 307-315.
34. Karkkainen, V., Magga, J., Koistinaho, J. & Malm, T. (2012) Brain environment and Alzheimer's disease mutations affect the survival, migration and differentiation of neural progenitor cells. Curr. Alzheimer Res., 9, 1030-1042.
35. Kempermann, G. (2006) Adult Hippocampal Neurogenesis. Adult Neurogenesis: Stem Cells and Neuronal Development in the Adult Brain. Oxford University Press, New York.
36. Kempermann, G. (2012) New neurons for 'survival of the fittest'. Nat. Rev. Neurosci., 13, 727-736.
37. Kempermann, G. & Gage, F.H. (2002) Genetic determinants of adult hippocampal neurogenesis correlate with acquisition, but not probe trial performance, in the water maze task. Eur. J. Neurosci., 16, 129-136.
38. Kempermann, G., Kuhn, H.G. & Gage, F.H. (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature, 386, 493-495.
39. Kempermann, G., Gast, D., Kronenberg, G., Yamaguchi, M. & Gage, F.H. (2003) Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development, 130, 391-399.
40. Kim, W.R., Christian, K., Ming, G.L. & Song, H. (2012) Time-dependent involvement of adult-born dentate granule cells in behavior. Behav. Brain Res., 227, 470-479.
41. Kuhn, H.G., Biebl, M., Wilhelm, D., Li, M., Friedlander, R.M. & Winkler, J. (2005) Increased generation of granule cells in adult Bcl-2-overexpressing mice: a role for cell death during continued hippocampal neurogenesis. Eur. J. Neurosci., 22, 1907-1915.
42. Lazarov, O., Demars, M.P., Zhao Kda, T., Ali, H.M., Grauzas, V., Kney, A. & Larson, J. (2012) Impaired survival of neural progenitor cells in dentate gyrus of adult mice lacking fMRP. Hippocampus, 22, 1220-1224.
43. Martinou, J.C., Dubois-Dauphin, M., Staple, J.K., Rodriguez, I., Frankowski, H., Missotten, M., Albertini, P., Talabot, D., Catsicas, S., Pietra, C. & Huarte, J. (1994) Overexpression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron, 13, 1017-1030.
44. Ming, G.L. & Song, H. (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron, 70, 687-702.
45. Nickells, R.W., Semaan, S.J. & Schlamp, C.L. (2008) Involvement of the Bcl2 gene family in the signaling and control of retinal ganglion cell death. Prog. Brain Res., 173, 423-435.
46. Oda, T. & Koike, T. (2004) Magnetic field exposure saves rat cerebellar granule neurons from apoptosis in vitro. Neurosci. Lett., 365, 83-86.
47. Pall, M.L. (2013) Electromagnetic fields act via activation of voltage-gated calcium channels to produce beneficial or adverse effects. J. Cell. Mol. Med., 17, 958-965.
48. v1-channel activity. J. Cell. Physiol., 215, 129-139.
49. + -dependent apoptosis induced by amyloid beta-peptide in human neuroblastoma IMR32 cells. J. Neurochem., 107, 1070-1082.
50. Podda, M.V., D'Ascenzo, M., Leone, L., Piacentini, R., Azzena, G.B. & Grassi, C. (2008) Functional role of cyclic nucleotide-gated channels in rat medial vestibular nucleus neurons. J. Physiol. (Lond.), 586, 803-815.
51. Podda, M.V., Leone, L., Piacentini, R., Cocco, S., Mezzogori, D., D'Ascenzo, M. & Grassi, C. (2012) Expression of olfactory-type cyclic nucleotide-gated channels in rat cortical astrocytes. Glia, 60, 1391-1405.
52. Podda, M.V., Piacentini, R., Barbati, S.A., Mastrodonato, A., Puzzo, D., D'Ascenzo, M., Leone, L. & Grassi, C. (2013) Role of cyclic nucleotide-gated channels in the modulation of mouse hippocampal neurogenesis. PLoS ONE, 8, e73246.
53. Puzzo, D. & Arancio, O. (2013) Amyloid-β peptide: Dr. Jekyll or Mr. Hyde? J. Alzheimers Dis., 33, S111-S120.
54. Querfurth, H.W. & LaFerla, F.M. (2010) Alzheimer's disease. New Engl. J. Med., 362, 329-344.
55. Ripoli, C., Piacentini, R., Riccardi, E., Leone, L., Li Puma, D.D., Bitan, G. & Grassi, C. (2013) Effects of different amyloid β-protein analogues on synaptic function. Neurobiol. Aging, 34, 1032-1044.
56. Saaltink, D.J., Håvik, B., Verissimo, C.S., Lucassen, P.J. & Vreugdenhil, E. (2012) Doublecortin and doublecortin-like are expressed in overlapping and non-overlapping neuronal cell population: implications for neurogenesis. J. Comp. Neurol., 520, 2805-2823.
57. 2+ signal dysregulation in DM1 and DM2 myotubes. Neuropath. Appl. Neuro., doi:10.1111/nan.12076. [Epub ahead of print].
58. Sasaki, T., Kitagawa, K., Yagita, Y., Sugiura, S., Omura-Matsuoka, E., Tanaka, S., Matsushita, K., Okano, H., Tsujimoto, Y. & Hori, M. (2006) Bcl2 enhances survival of newborn neurons in the normal and ischemic hippocampus. J. Neurosci. Res., 84, 1187-1196.
59. Shors, T.J. (2009) Saving new brain cells. Sci. Am., 300, 46-52.
60. Shors, T.J., Anderson, M.L., Curlik, D.M. 2nd. & Nokia, M.S. (2012) Use it or lose it: how neurogenesis keeps the brain fit for learning. Behav. Brain Res., 227, 450-458.
61. Snyder, J.S., Glover, L.R., Sanzone, K.M., Kamhi, J.F. & Cameron, H.A. (2009) The effects of exercise and stress on the survival and maturation of adult-generated granule cells. Hippocampus, 19, 898-906.
62. Sun, W., Winseck, A., Vinsant, S., Park, O.H., Kim, H. & Oppenheim, R.W. (2004) Programmed cell death of adult-generated hippocampal neurons is mediated by the proapoptotic gene Bax. J. Neurosci., 24, 11205-11213.
63. Tanaka, T., Serneo, F.F., Tseng, H.C., Kulkarni, A.B., Tsai, L.H. & Gleeson, J.G. (2004) Cdk5 phosphorylation of doublecortin ser297 regulates its effect on neuronal migration. Neuron, 41, 215-227.
64. Tashiro, A., Makino, H. & 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.
65. Taylor, C.J., Jhaveri, D.J. & Bartlett, P.F. (2013) The therapeutic potential of endogenous hippocampal stem cells for the treatment of neurological disorders. Front. Cell. Neurosci., 7, 5.
66. Tian, F., Nakahara, T., Yoshida, M., Honda, N., Hirose, H. & Miyakoshi, J. (2002) Exposure to power frequency magnetic fields suppresses X-ray-induced apoptosis transiently in Ku80-deficient xrs5 cells. Biochem. Bioph. Res. Co., 292, 355-361.
67. Tronel, S., Fabre, A., Charrier, V., Oliet, S.H., Gage, F.H. & Abrous, D.N. (2010) Spatial learning sculpts the dendritic arbor of adult-born hippocampal neurons. Proc. Natl. Acad. Sci. USA, 107, 7963-7968.
68. Van Praag, H., Christie, B.R., Sejnowski, T.J. & Gage, F.H. (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl. Acad. Sci. USA, 96, 13427-13431.
69. Veena, J., Srikumar, B.N., Mahati, K., Bhagya, V., Raju, T.R. & Shankaranarayana Rao, B.S. (2009) Enriched environment restores hippocampal cell proliferation and ameliorates cognitive deficits in chronically stressed rats. J. Neurosci. Res., 87, 831-843.
70. West, M.J. (1999) Stereological methods for estimating the total number of neurons and synapses: issues of precision and bias. Trends Neurosci., 22, 51-61.
71. Winner, B., Cooper-Kuhn, C.M., Aigner, R., Winkler, J. & Kuhn, H.G. (2002) Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur. J. Neurosci., 16, 1681-1689.
72. Winner, B., Kohl, Z. & Gage, F.H. (2011) Neurodegenerative disease and adult neurogenesis. Eur. J. Neurosci., 33, 1139-1151.