Homocysteine inhibits proliferation of neuronal precursors in the mouse adult brain by impairing the basic fibroblast growth factor signaling cascade and reducing extracellular regulated kinase 1/2-dependent cyclin E expression

FASEB Journal

Volumn 22, Issue 11, 2008, Pages 3823-3835

  Rabaneda, Luis G ^a   Carrasco, Manuel ^a   López Toledano, Miguel A ^a   Murillo Carretero, Maribel ^a   Ruiz, Félix A ^a,b   Estrada, Carmen ^a   Castro, Carmen ^a,c  

^a UNIVERSITY OF CÁDIZ   (Spain)

^b HOSPITAL UNIVERSITARIO PUERTA DEL MAR   (Spain)

^c NONE   (Spain)

Author keywords

Dementia; Dentate gyrus; Hyperhomocysteinemia; Neurogenesis; Subventricular zone

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; BROXURIDINE; CASPASE 3; CYCLIN E; FOLIC ACID; HOMOCYSTEINE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

AMNESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL ISOLATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DENTATE GYRUS; ENZYME ACTIVITY; ENZYME INACTIVATION; HIPPOCAMPUS; HYPERHOMOCYSTEINEMIA; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LEARNING; MEMORY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; OLFACTORY SYSTEM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STEM CELL; SUBVENTRICULAR ZONE;

ADULT STEM CELLS; AGED; AGED, 80 AND OVER; ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; COGNITION DISORDERS; CYCLIN E; DEMENTIA; DENTATE GYRUS; DISEASE MODELS, ANIMAL; FIBROBLAST GROWTH FACTOR 2; FOLIC ACID; GENE EXPRESSION REGULATION; HOMOCYSTEINE; HUMANS; HYPERHOMOCYSTEINEMIA; MAP KINASE SIGNALING SYSTEM; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEURODEGENERATIVE DISEASES; NEURONS; TRIGEMINAL CAUDAL NUCLEUS;

MUS;

EID: 55549117471     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.08-109306     Document Type: Article

References (57)

1. Seshadri, S., Beiser, A., Selhub, J., Jacques, P. F., Rosenberg, I. H., D'Agostino, R. B., Wilson, P. W., and Wolf, P. A. (2002) Plasma homocysteine as a risk factor for dementia and Alzheimer's disease. N. Engl. J. Med. 346, 476-483
2. Ravaglia, G., Forti, P., Maioli, F., Chiappelli, M., Montesi, F., Tumini, E., Mariani, E., Licastro, F., and Patterson, C. (2007) Blood inflammatory markers and risk of dementia: The Conselice Study of Brain Aging. Neurobiol. Aging 28, 1810-1820
3. Refsum, H., Ueland, P. M., Nygard, O., and Vollset, S. E. (1998) Homocysteine and cardiovascular disease. Annu. Rev. Med. 49, 31-62
4. Haan, M. N., Miller, J. W., Aiello, A. E., Whitmer, R. A., Jagust, W. J., Mungas, D. M., Allen, L. H., and Green, R. (2007) Homocysteine, B vitamins, and the incidence of dementia and cognitive impairment: results from the Sacramento Area Latino Study on Aging. Am. J. Clin. Nutr. 85, 511-517
5. Durga, J., van Boxtel, M. P., Schouten, E. G., Kok, F. J., Jolles, J., Katan, M. B., and Verhoef, P. (2007) Effect of 3-year folic acid supplementation on cognitive function in older adults in the FACIT trial: a randomised, double blind, controlled trial. Lancet 369, 208-216
6. Kruman, I. I., Kumaravel, T. S., Lohani, A., Pedersen, W. A., Cutler, R. G., Kruman, Y., Haughey, N., Lee, J., Evans, M., and Mattson, M. P. (2002) Folic acid deficiency and homocysteine impair DNA repair in hippocampal neurons and sensitize them to amyloid toxicity in experimental models of Alzheimer's disease. J. Neurosci. 22, 1752-1762
7. Kruman, I. I., Culmsee, C., Chan, S. L., Kruman, Y., Guo, Z., Penix, L., and Mattson, M. P. (2000) Homocysteine elicits a DNA damage response in neurons that promotes apoptosis and hypersensitivity to excitotoxicity. J. Neurosci. 20, 6920-6926
8. Aimone, J. B., Wiles, J., and Gage, F. H. (2006) Potential role for adult neurogenesis in the encoding of time in new memories. Nat. Neurosci. 9, 723-727
9. Kempermann, G., van Praag, H., and Gage, F. H. (2000) Activity-dependent regulation of neuronal plasticity and self repair. Prog. Brain Res. 127, 35-48
10. Kuhn, H. G., Dickinson-Anson, H., and Gage, F. H. (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 16, 2027-2033
11. Gould, E., McEwen, B. S., Tanapat, P., Galea, L. A., and Fuchs, E. (1997) Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J. Neurosci. 17, 2492-2498
12. van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., and Gage, F. H. (2002) Functional neurogenesis in the adult hippocampus. Nature 415, 1030-1034
13. Jessberger, S., and Kempermann, G. (2003) Adult-born hippocampal neurons mature into activity-dependent responsiveness. Eur. J. Neurosci. 18, 2707-2712
14. Shors, T. J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T., and Gould, E. (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410, 372-376
15. Snyder, J. S., Hong, N. S., McDonald, R. J., and Wojtowicz, J. M. (2005) A role for adult neurogenesis in spatial long-term memory. Neuroscience 130, 843-852
16. 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
17. Doetsch, F., Garcia-Verdugo, J. M., and Alvarez-Buylla, A. (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 17, 5046-5061
18. Doetsch, F., Caille, I., Lim, D. A., Garcia-Verdugo, J. M., and Alvarez-Buylla, A. (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716
19. Rochefort, C., Gheusi, G., Vincent, J. D., and Lledo, P. M. (2002) Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J. Neurosci. 22, 2679-2689
20. Kruman, I. I., Mouton, P. R., Emokpae, R., Jr., Cutler, R. G., and Mattson, M. P. (2005) Folate deficiency inhibits proliferation of adult hippocampal progenitors. Neuroreport 16, 1055-1059
21. Koury, M. J., and Horne, D. W. (1994) Apoptosis mediates and thymidine prevents erythroblast destruction in folate deficiency anemia. Proc. Natl. Acad. Sci. U. S. A. 91, 4067-4071
22. Huang, R. F., Ho, Y. H., Lin, H. L., Wei, J. S., and Liu, T. Z. (1999) Folate deficiency induces a cell cycle-specific apoptosis in HepG2 cells. J. Nutr. 129, 25-31
23. Courtemanche, C., Elson-Schwab, I., Mashiyama, S. T., Kerry, N., and Ames, B. N. (2004) Folate deficiency inhibits the proliferation of primary human CD8+ T lymphocytes in vitro. J. Immunol. 173, 3186-3192
24. Garrow, T. A. (1996) Purification, kinetic properties, and cDNA cloning of mammalian betaine-homocysteine methyltransferase. J. Biol. Chem. 271, 22831-22838
25. Doetsch, F., Petreanu, L., Caille, I., Garcia-Verdugo, J. M., and Alvarez-Buylla, A. (2002) EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36, 1021-1034
26. Torroglosa, A., Murillo-Carretero, M., Romero-Grimaldi, C., Matarredona, E. R., Campos-Caro, A., and Estrada, C. (2007) Nitric oxide decreases subventricular zone stem cell proliferation by inhibition of epidermal growth factor receptor and phosphoinositide-3-kinase/Akt pathway. Stem Cells 25, 88-97
27. Matarredona, E. R., Murillo-Carretero, M., Moreno-Lopez, B., and Estrada, C. (2004) Nitric oxide synthesis inhibition increases proliferation of neural precursors isolated from the postnatal mouse subventricular zone. Brain Res. 995, 274-284
28. Cameron, H. A., and McKay, R. D. (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol. 435, 406-417
29. Moreno-Lopez, B., Romero-Grimaldi, C., Noval, J. A., Murillo-Carretero, M., Matarredona, E. R., and Estrada, C. (2004) Nitric oxide is a physiological inhibitor of neurogenesis in the adult mouse subventricular zone and olfactory bulb. J. Neurosci. 24, 85-95
30. Svedin, P., Hagberg, H., Savman, K., Zhu, C., and Mallard, C. (2007) Matrix metalloproteinase-9 gene knock-out protects the immature brain after cerebral hypoxia-ischemia. J. Neurosci. 27, 1511-1518
31. Keilhoff, G., Becker, A., Grecksch, G., Bernstein, H. G., and Wolf, G. (2006) Cell proliferation is influenced by bulbectomy and normalized by imipramine treatment in a region-specific manner. Neuropsychopharmacology 31, 1165-1176
32. Bull, N. D., and Bartlett, P. F. (2005) The adult mouse hippocampal progenitor is neurogenic but not a stem cell. J. Neurosci. 25, 10815-10821
33. Heo, J. S., Lee, Y. J., and Han, H. J. (2006) EGF stimulates proliferation of mouse embryonic stem cells: involvement of Ca2+ influx and p44/42 MAPKs. Am. J. Physiol. 290, C123-C133
34. Seaberg, R. M., and van der Kooy, D. (2002) Adult rodent neurogenic regions: the ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. J. Neurosci. 22, 1784-1793
35. Reynolds, B. A., and Weiss, S. (1996) Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev. Biol. 175, 1-13
36. Reynolds, B. A., and Rietze, R. L. (2005) Neural stem cells and neurospheres-re-evaluating the relationship. Nat. Methods 2, 333-336
37. Schlessinger, J. (2004) Common and distinct elements in cellular signaling via EGF and FGF receptors. Science 306, 1506-1507
38. Robert, K., Pages, C., Ledru, A., Delabar, J., Caboche, J., and Janel, N. (2005) Regulation of extracellular signal-regulated kinase by homocysteine in hippocampus. Neuroscience 133, 925-935
39. Brown, J. C., Rosenquist, T. H., and Monaghan, D. T. (1998) ERK2 activation by homocysteine in vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 251, 669-676
40. Shi, S. S., Day, R. M., Halpner, A. D., Blumberg, J. B., and Suzuki, Y. J. (1999) Homocysteine and alpha-lipoic acid regulate p44/42 MAP kinase phosphorylation in NIH/3T3 cells. Antioxid. Redox. Signal. 1, 123-128
41. Alvarez-Maqueda, M., El Bekay, R., Monteseirin, J., Alba, G., Chacon, P., Vega, A., Santa Maria, C., Tejedo, J. R., Martin-Nieto, J., Bedoya, F. J., Pintado, E., and Sobrino, F. (2004) Homocysteine enhances superoxide anion release and NADPH oxidase assembly by human neutrophils. Effects on MAPK activation and neutrophil migration. Atherosclerosis 172, 229-238
42. Schwahn, B. C., Chen, Z., Laryea, M. D., Wendel, U., Lussier-Cacan, S., Genest, J., Jr., Mar, M. H., Zeisel, S. H., Castro, C., Garrow, T., and Rozen, R. (2003) Homocysteine-betaine interactions in a murine model of 5,10-methylenetetrahydrofolate reductase deficiency. FASEB J. 17, 512-514
43. Clarke, R., Smith, A. D., Jobst, K. A., Refsum, H., Sutton, L., and Ueland, P. M. (1998) Folate, vitamin B12, and serum total homocysteine levels in confirmed Alzheimer disease. Arch. Neurol. 55, 1449 -1455
44. Quadri, P., Fragiacomo, C., Pezzati, R., Zanda, E., Forloni, G., Tettamanti, M., and Lucca, U. (2004) Homocysteine, folate, and vitamin B-12 in mild cognitive impairment, Alzheimer disease, and vascular dementia. Am. J. Clin. Nutr. 80, 114-122
45. Moser, M. B., and Moser, E. I. (1998) Distributed encoding and retrieval of spatial memory in the hippocampus. J. Neurosci. 18, 7535-7542
46. Lepage, M., Habib, R., and Tulving, E. (1998) Hippocampal PET activations of memory encoding and retrieval: the HIPER model. Hippocampus 8, 313-322
47. Greicius, M. D., Krasnow, B., Boyett-Anderson, J. M., Eliez, S., Schatzberg, A. F., Reiss, A. L., and Menon, V. (2003) Regional analysis of hippocampal activation during memory encoding and retrieval: fMRI study. Hippocampus 13, 164-174
48. Chen, Z., Schwahn, B. C., Wu, Q., He, X., and Rozen, R. (2005) Postnatal cerebellar defects in mice deficient in methylenetetrahydrofolate reductase. Int. J. Dev. Neurosci. 23, 465-474
49. Zhao, M., Li, D., Shimazu, K., Zhou, Y. X., Lu, B., and Deng, C. X. (2007) Fibroblast growth factor receptor-1 is required for long-term potentiation, memory consolidation, and neurogenesis. Biol. Psychiatry 62, 381-390
50. Ravaglia, G., Forti, P., Maioli, F., Martelli, M., Servadei, L., Brunetti, N., Pantieri, G., and Mariani, E. (2006) Conversion of mild cognitive impairment to dementia: predictive role of mild cognitive impairment subtypes and vascular risk factors. Dement. Geriatr. Cogn. Disord. 21, 51-58
51. Algaidi, S. A., Christie, L. A., Jenkinson, A. M., Whalley, L., Riedel, G., and Platt, B. (2006) Long-term homocysteine exposure induces alterations in spatial learning, hippocampal signalling and synaptic plasticity. Exp. Neurol. 197, 8 -21
52. Gould, E., Tanapat, P., Hastings, N. B., and Shors, T. J. (1999) Neurogenesis in adulthood: a possible role in learning. Trends Cogn. Sci. 3, 186-192
53. van Praag, H., Christie, B. R., Sejnowski, T. J., and Gage, F. H. (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl. Acad. Sci. U. S. A. 96, 13427-13431
54. 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
55. Maguire, E. A., Frackowiak, R. S., and Frith, C. D. (1997) Recalling routes around london: activation of the right hippocampus in taxi drivers. J. Neurosci. 17, 7103-7110
56. Maguire, E. A., Gadian, D. G., Johnsrude, I. S., Good, C. D., Ashburner, J., Frackowiak, R. S., and Frith, C. D. (2000) Navigation-related structural change in the hippocampi of taxi drivers. Proc. Natl. Acad. Sci. U. S. A. 97, 4398-4403
57. Shors, T. J., Townsend, D. A., Zhao, M., Kozorovitskiy, Y., and Gould, E. (2002) Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12, 578-584