Diethylstilbestrol alters the population dynamic of neural precursor cells in the neonatal male rat dentate gyrus

Brain Research Bulletin

Volumn 71, Issue 6, 2007, Pages 619-627

  Ramos, Jorge G ^a   Varayoud, Jorgelina ^a   Monje, Lucas ^a   Moreno Piovano, Guillermo ^a   Muñoz de Toro, Mónica ^a   Luque, Enrique H ^a  

^a UNIVERSIDAD NACIONAL DEL LITORAL   (Argentina)

Author keywords

Apoptosis; DES; Hippocampus; Neural precursors; Proliferation

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIN DEPENDENT KINASE INHIBITOR 1B; DIETHYLSTILBESTROL; ESTROGEN DERIVATIVE; MESSENGER RNA; VASCULOTROPIN;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; EXPOSURE; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MITOSIS RATE; MORPHOMETRICS; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PERINATAL PERIOD; POPULATION DYNAMICS; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; RODENT;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CYCLIN-DEPENDENT KINASE INHIBITOR P27; DENTATE GYRUS; DIETHYLSTILBESTROL; ESTROGENS, NON-STEROIDAL; FEMALE; MALE; MITOTIC INDEX; NEURONS; RATS; RATS, WISTAR; RNA, MESSENGER; STEM CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 33846841149     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2006.12.004     Document Type: Article

References (57)

1. Banasr M., Hery M., Brezun J.M., and Daszuta A. Serotonin mediates oestrogen stimulation of cell proliferation in the adult dentate gyrus. Eur. J. Neurosci. 14 (2001) 1417-1424
2. Bora S.H., Liu Z., Kecojevic A., Merchenthaler I., and Koliatsos V.E. Direct, complex effects of estrogens on basal forebrain cholinergic neurons. Exp. Neurol. 194 (2005) 506-522
3. Cao L., Jiao X., Zuzga D.S., Liu Y., Fong D.M., Young D., and During M.J. VEGF links hippocampal activity with neurogenesis, learning and memory. Nat. Genet. 36 (2004) 827-835
4. Carr R., Bertasi F., Betancourt A., Bowers S., Gandy B.S., Ryan P., and Willard S. Effect of neonatal rat bisphenol a exposure on performance in the Morris water maze. J. Toxicol. Environ. Health A 66 (2003) 2077-2088
5. Caviness Jr. V.S., Takahashi T., and Nowakowski R.S. The G1 restriction point as critical regulator of neocortical neuronogenesis. Neurochem. Res. 24 (1999) 497-506
6. Ciaroni S., Cuppini R., Cecchini T., Ferri P., Ambrogini P., Cuppini C., and Del Grande P. Neurogenesis in the adult rat dentate gyrus is enhanced by vitamin E deficiency. J. Comp. Neurol. 411 (1999) 495-502
7. Cooper-Kuhn C.M., Winkler J., and Kuhn H.G. Decreased neurogenesis after cholinergic forebrain lesion in the adult rat. J. Neurosci. Res. 77 (2004) 155-165
8. Cordoba Montoya D.A., and Carrer H.F. Estrogen facilitates induction of long term potentiation in the hippocampus of awake rats. Brain Res. 778 (1997) 430-438
9. Crespo D., Stanfield B.B., and Cowan W.M. Evidence that late-generated granule cells do not simply replace earlier formed neurons in the rat dentate gyrus. Exp. Brain Res. 62 (1986) 541-548
10. Davies A.M. The role of neurotrophins in the developing nervous system. J. Neurobiol. 25 (1994) 1334-1348
11. Doetsch F., Verdugo J.M., Caille I., Alvarez-Buylla A., Chao M.V., and Casaccia-Bonnefil P. Lack of the cell-cycle inhibitor p27Kip1 results in selective increase of transit-amplifying cells for adult neurogenesis. J. Neurosci. 22 (2002) 2255-2264
12. DonCarlos L.L., McAbee M., Ramer-Quinn D.S., and Stancik D.M. Estrogen receptor mRNA levels in the preoptic area of neonatal rats are responsive to hormone manipulation. Brain Res. Dev. Brain Res. 84 (1995) 253-260
13. Emsley J.G., Mitchell B.D., Kempermann G., and Macklis J.D. Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog. Neurobiol. 75 (2005) 321-341
14. Eriksson P.S., Perfilieva E., Bjork-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., and Gage F.H. Neurogenesis in the adult human hippocampus. Nat. Med. 4 (1998) 1313-1317
15. Farabollini F., Porrini S., Della S.D., Bianchi F., and Dessi-Fulgheri F. Effects of perinatal exposure to bisphenol A on sociosexual behavior of female and male rats. Environ. Health Perspect. 3 Suppl. 110 (2002) 409-414
16. Filippov V., Kronenberg G., Pivneva T., Reuter K., Steiner B., Wang L.P., Yamaguchi M., Kettenmann H., and Kempermann G. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol. Cell. Neurosci. 23 (2003) 373-382
17. Fujimoto T., Kubo K., and Aou S. Prenatal exposure to bisphenol A impairs sexual differentiation of exploratory behavior and increases depression-like behavior in rats. Brain Res. 1068 (2006) 49-55
18. Gould E., and Tanapat P. Stress and hippocampal neurogenesis. Biol. Psychiatry 46 (1999) 1472-1479
19. Hastings N.B., and Gould E. Rapid extension of axons into the CA3 region by adult-generated granule cells. J. Comp. Neurol. 413 (1999) 146-154
20. Higuchi R., Fockler C., Dollinger G., and Watson R. Kinetic PCR analysis: real-time monitoring of DNA amplification reactions. Biotechnology (NY) 11 (1993) 1026-1030
21. Isgor C., and Sengelaub D.R. Prenatal gonadal steroids affect adult spatial behavior CA1 and CA3 pyramidal cell morphology in rats. Horm. Behav. 34 (1998) 183-198
22. Jin K., Zhu Y., Sun Y., Mao X.O., Xie L., and Greenberg D.A. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 11946-11950
23. Kaplan M.S., and Hinds J.W. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197 (1977) 1092-1094
24. Karishma K.K., and Herbert J. Dehydroepiandrosterone (DHEA) stimulates neurogenesis in the hippocampus of the rat, promotes survival of newly formed neurons and prevents corticosterone-induced suppression. Eur. J. Neurosci. 16 (2002) 445-453
25. Kass L., Varayoud J., Ortega H., Munoz d.T., and Luque E.H. Detection of bromodeoxyuridine in formalin-fixed tissue DNA denaturation following microwave or enzymatic digestion pretreatment is required. Eur. J. Histochem. 44 (2000) 185-191
26. Kronenberg G., Reuter K., Steiner B., Brandt M.D., Jessberger S., Yamaguchi M., and Kempermann G. Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J. Comp. Neurol. 467 (2003) 455-463
27. Kuhn H.G., Dickinson-Anson H., and Gage F.H. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 16 (1996) 2027-2033
28. Levine E.S., Dreyfus C.F., Black I.B., and Plummer M.R. Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 8074-8077
29. Lie D.C., Song H., Colamarino S.A., Ming G.L., and Gage F.H. Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annu. Pharmacol. Rev. Toxicol. 44 (2004) 399-421
30. Luine V.N., Richards S.T., Wu V.Y., and Beck K.D. Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters. Horm. Behav. 34 (1998) 149-162
31. Matsuzaki H., Tamatani M., Yamaguchi A., Namikawa K., Kiyama H., Vitek M.P., Mitsuda N., and Tohyama M. Vascular endothelial growth factor rescues hippocampal neurons from glutamate-induced toxicity: signal transduction cascades. FASEB J. 15 (2001) 1218-1220
32. McEwen B.S., and Alves S.E. Estrogen actions in the central nervous system. Endocr. Rev. 20 (1999) 279-307
33. Mohapel P., Leanza G., Kokaia M., and Lindvall O. Forebrain acetylcholine regulates adult hippocampal neurogenesis and learning. Neurobiol. Aging 26 (2005) 939-946
34. Montaron M.F., Petry K.G., Rodriguez J.J., Marinelli M., Aurousseau C., Rougon G., Le Moal M., and Abrous D.N. Adrenalectomy increases neurogenesis but not PSA-NCAM expression in aged dentate gyrus. Eur. J. Neurosci. 11 (1999) 1479-1485
35. Naylor M., Bowen K.K., Sailor K.A., Dempsey R.J., and Vemuganti R. Preconditioning-induced ischemic tolerance stimulates growth factor expression and neurogenesis in adult rat hippocampus. Neurochem. Int. 47 (2005) 565-572
36. Ogunshola O.O., Antic A., Donoghue M.J., Fan S.Y., Kim H., Stewart W.B., Madri J.A., and Ment L.R. Paracrine and autocrine functions of neuronal vascular endothelial growth factor (VEGF) in the central nervous system. J. Biol. Chem. 277 (2002) 11410-11415
37. Ormerod B.K., and Galea L.A. Reproductive status influences cell proliferation and cell survival in the dentate gyrus of adult female meadow voles: a possible regulatory role for estradiol. Neuroscience 102 (2001) 369-379
38. Ormerod B.K., Lee T.T., and Galea L.A. Estradiol initially enhances but subsequently suppresses (via adrenal steroids) granule cell proliferation in the dentate gyrus of adult female rats. J. Neurobiol. 55 (2003) 247-260
39. Palkovits M., and Brownstein M.J. Microdissection of brain areas by the punch technique. In: Cuello A.C. (Ed). Brain Microdissection Techniques Chichester (1983), John Wiley and Sons 1-36
40. Palmer T.D., Willhoite A.R., and Gage F.H. Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 425 (2000) 479-494
41. Perez-Martin M., Salazar V., Castillo C., Ariznavarreta C., Azcoitia I., Garcia-Segura L.M., and Tresguerres J.A. Estradiol and soy extract increase the production of new cells in the dentate gyrus of old rats. Exp. Gerontol. 40 (2005) 450-453
42. Pombo M., and Castro-Feijoo L. Endocrine disruptors. J. Pediatr. Endocrinol. Metab. 18 Suppl. 1 (2005) 1145-1155
43. Porrini S., Belloni V., Della S.D., Farabollini F., Giannelli G., and Dessi-Fulgheri F. Early exposure to a low dose of bisphenol A affects socio-sexual behavior of juvenile female rats. Brain Res. Bull. 65 (2005) 261-266
44. Sapolsky R.M., and Meaney M.J. Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res. 396 (1986) 64-76
45. Sato K., Matsuki N., Ohno Y., and Nakazawa K. Effects of 17beta-estradiol and xenoestrogens on the neuronal survival in an organotypic hippocampal culture. Neuroendocrinology 76 (2002) 223-234
46. Savu L., Benassayag C., Vallette G., and Nunez E.A. Ligand properties of diethylstilbestrol: studies with purified native and fatty acid-free rat alpha 1-fetoprotein and albumin. Steroids 34 (1979) 737-748
47. Shors T.J., Townsend D.A., Zhao M., Kozorovitskiy Y., and Gould E. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12 (2002) 578-584
48. Solum D.T., and Handa R.J. Estrogen regulates the development of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus. J. Neurosci. 22 (2002) 2650-2659
49. Tanapat P., Hastings N.B., Reeves A.J., and Gould E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci. 19 (1999) 5792-5801
50. Tanapat P., Hastings N.B., and Gould E. 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 (2005) 252-265
51. Vallieres L., Campbell I.L., Gage F.H., and Sawchenko P.E. Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6. J. Neurosci. 22 (2002) 486-492
52. Van der B.K., Mulder J., Keijser J.N., Eggen B.J., Luiten P.G., and Van der Zee E.A. Input from the medial septum regulates adult hippocampal neurogenesis. Brain Res. Bull. 67 (2005) 117-125
53. van Praag H., Christie B.R., Sejnowski T.J., and Gage F.H. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 13427-13431
54. Vemuri M.C., and Chetty C.S. Alcohol impairs astrogliogenesis by stem cells in rodent neurospheres. Neurochem. Int. 47 (2005) 129-135
55. Vizi E.S., and Kiss J.P. Neurochemistry and pharmacology of the major hippocampal transmitter systems: synaptic and non-synaptic interactions. Hippocampus 8 (1998) 566-607
56. Wasterlain C.G., and Plum F. Vulnerability of developing rat brain to electroconvulsive seizures. Arch. Neurol. 29 (1973) 38-45
57. Woolley C.S., and McEwen B.S. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J. Neurosci. 12 (1992) 2549-2554