Pathophysiology
Volume 18, Issue 4 , Pages 263-272 , September 2011

Alteration of rat hippocampal neurogenesis and neuronal nitric oxide synthase expression upon prenatal exposure to tamoxifen

  • Maliheh Nobakht

      Affiliations

    • Department of Histology and Neuroscience, School of Medicine, Tehran University of Medical Science, Tehran, Iran
    • Cellular and Molecular Research Center, Tehran University of Medical Science, Tehran, Iran
    • Anti-microbial Resistance Research Center, Tehran University of Medical Science, Tehran, Iran
    • ,
  • Mohammad Javad Gharavi

      Affiliations

    • Department of Medical Parasitology, Tehran University of Medical Science, Tehran, Iran
    • ,
  • Kazem Mousavizadeh

      Affiliations

    • Oncopathology Research Center, Tehran University of Medical Science, Tehran, Iran
    • ,
  • Maasoumeh Bakhshayesh

      Affiliations

    • Cellular and Molecular Research Center, Tehran University of Medical Science, Tehran, Iran
    • ,
  • Pedram Ghafourifar

      Affiliations

    • Tri-State Institute of Pharmaceutical Sciences, Huntington, WV, USA
    • Corresponding Author InformationCorresponding author.

Received 3 March 2009 ,Revised 17 July 2009 ,Accepted 21 January 2011.

References 

  1. Moreno-López B, Noval JA, González-Bonet LG, Estrada C. Morphological bases for a role of nitric oxide in adult neurogenesis. Brain Res. 2000;869:244–250
  2. Paakkari I, Lindsberg P. Nitric oxide in the central nervous system. Ann. Med. 1995;27:369–377
  3. Bayram Z, Asar M, Cayli S, Demir R. Immunocytochemical detection of neuronal nitric oxide synthase (nNOS)-IR in embryonic rat stomach between days 13 and 21 of gestation. J. Histochem. Cytochem. 2002;50:671–680
  4. Pinnock SB, Balendra R, Chan M, Hunt LT, Turner-Stokes T, Herbert J. Interactions between nitric oxide and corticosterone in the regulation of progenitor cell proliferation in the dentate gyrus of the adult Rat. Neuropsychopharmacology. 2007;32:493–504
  5. Zhou QG, Hu Y, Hua Y, Hu M, Luo CX, Han X, et al. Neuronal nitric oxide synthase contributes to chronic stress-induced depression by suppressing hippocampal neurogenesis. J. Neurochem. 2007;103:1843–1854
  6. Bredt DS, Snyder SH. Transient nitric oxide synthase neurons in embryonic cerebral cortical plate, sensory ganglia, and olfactory epithelium. Neuron. 1994;13:301–313
  7. Roskams AJ, Bredt DS, Dawson TM, Ronnett GV. Nitric oxide mediates the formation of synaptic connections in developing and regenerating olfactory receptor neurons. Neuron. 1994;13:289–299
  8. Gibbs SM. Regulation of neuronal proliferation and differentiation by nitric oxide. Mol. Neurobiol. 2000;27:107–120
  9. Packer MA, Stasiv Y, Benraiss A, Chmielnicki E, Grinberg A, Westphal H, et al. Nitric oxide negatively regulates mammalian adult neurogenesis. Proc. Natl. Acad. Sci. U.S.A. 2003;100:9566–9571
  10. Keilhoff G, Seidel B, Noack H, Tischmeyer W, Stanek D, Wolf G. Patterns of nitric oxide synthase at the messenger RNA and protein levels during early rat brain development. Neuroscience. 1996;75:1193–1201
  11. Foster JA, Phelps PE. Neurons expressing NADPH-diaphorase in the developing human spinal cord. J. Comp. Neurol. 2000;427:417–427
  12. Renodon A, Boucher JL, Sari MA, Delaforge M, Quazzani J, Mansuy D. Strong inhibition of neuronal nitric oxide synthase by the calmodulin antagonist and anti-estrogen drug tamoxifen. Biochem. Pharmacol. 1997;54:1109–1114
  13. Black SM, Bedolli MA, Martinez S, Bristow JD, Ferriero DM, Soifer SJ. Expression of neuronal nitric oxide synthase corresponds to regions of vulnerability to hypoxia-ischemia in the developing rat brain. Neurobiol. Dis. 1995;2:145–155
  14. Tanaka M, Yoshida S, Yano M, Hanaoka F. Roles of endogenous nitric oxide in cerebellar cortical development in slice cultures. Neuroreport. 1994;5:2049–2052
  15. Giuili G, Luzi A, Poyard M, Guellaen G. Expression of mouse brain soluble guanylate cyclase and NO synthase during ontogeny. Brain Res. Dev. Brain Res. 1994;81:269–283
  16. Veenman CL, Lehmann J, Stöhr T, Totterdell S, Yee B, Mura A, et al. Comparisons of the densities of NADPHd reactive and nNOS immunopositive neurons in the hippocampus of three age groups of young nonhandled and handled rats. Brain Res. Dev. Brain Res. 1999;114:229–243
  17. Wright CD, Compston JE. Tamoxifen: oestrogen or anti-oestrogenin bone?. Q. J. Med. 1995;88:307–310
  18. Robinson SP, Langan-Fahey SM, Johnson DA, Jordan VC. Metabolites, pharmacodynamics, and pharmacokinetics of tamoxifen in rats and mice compared to the breast cancer patient. Drug Metab. Dispos. 1991;19:36–43
  19. Xia Y, Krukoff TL. Estrogen induces nitric oxide production via activation of constitutive nitric oxide synthase in human neuroblastema cells. Endocrinology. 2004;145:4550–4557
  20. Shughrue PJ, Merchenthaler I. Estrogen prevents the loss of CA1 hippocampal neurons in gerbils after ischemic injury. Neuroscience. 2003;116:851–861
  21. Holtzman DM, Lee S, Li Y, Chua-Couzens J, Xia H, Bredt DS, et al. Expression of neuronal-NOS in developing basal forebrain cholinergic neurons: regulation by NGF. Neurochem. Res. 1996;2:861–868
  22. Borgna JL, Rochefort H. Hydroxylated metabolites of tamoxifen are formed in vivo and bound to estrogen receptor in target tissues. J. Biol. Chem. 1981;256:859–868
  23. Li Y, Holtzman DM, Kromer LF, Kaplan DR, Chua-Couzens J, Clay DO, et al. Regulation of TrkA and ChAT expression in developing rat basal forebrain: evidence that NGF regulate differentiation of cholinergic neurons. J. Neurosci. 1995;15:2888–2905
  24. Islam AF, Westman J, Bogdanovic N, Suliman IA, Lindell I, Winblad B, et al. Ultrastructural analysis of the hippocampus of adult rats after long-term adrenalectomy. Brain Res. 1999;849:226–230
  25. Silva I, Mello LE, Freymuller E, Haidar MA, Baracat EC. Estrogen, progestogen and tamoxifen increase synaptic density of the hippocampus of ovariectomized rats. Neurosci. Lett. 2000;291:183–186
  26. Landfield PW, Braun LD, Pitler TA, Lindsey JD, Lynch G. Hippocampal aging in rats: a morphometric study of multiple variables in semithin sections. Neurobiol. Aging. 1981;2:265–275
  27. Parihar A, Parihar MS, Ghafourifar P. Significance of mitochondrial calcium and nitric oxide for apoptosis of human breast cancer cells induced by tamoxifen and etoposide. Int. J. Mol. Med. 2008;21:317–324
  28. Kimura KA, Parr AM, Brien JF. Effect of chronic maternal ethanol administration on nitric oxide synthase activity in the hippocampus of the mature fetal guinea pig. Alcohol. Clin. Exp. Res. 1996;20:948–953
  29. Wilcox BJ, Applegate MD, Portera-Caillau C, Koliatsos VE. Nerve growth factor prevents apoptotic cell death in injured central cholinergic neurons. J. Comp. Neurol. 1995;395:573–585
  30. Shughrue PJ, Merchenthaler I. Evidence for novel estrogen binding sites in the rat hippocampus. Neuroscience. 2000;99:605–612
  31. Poe BH, Linville C, Riddle DR, Sonntag WE, Brunso-Bechtold JK. Effects of age and insulin-like growth factor-1 on neuron and synapse numbers in area CA3 of hippocampus. Neuroscience. 2001;107:231–238
  32. Devaney KO, Johnson HA. Changes in cell density within the human hippocampal formation as a function of age. Gerontology. 1984;30:100–108
  33. Meaney MJ, Aitken DH, Bhatnagar S, Sapolsky RM. Postnatal handling attenuates certain neuroendocrine, anatomical and cognitive dysfunctions associated with aging in female rats. Neurobiol. Aging. 1991;12:31–38
  34. Satake A, Takaoka M, Nishikawa M, Yuba M, Shibata Y, Okumura K, et al. Protective effect of 17beta-estradiol on ischemic acute renal failure through the PI3K/Akt/eNOS pathway. Kidney Int. 2008;73:308–317
  35. Peters A, Rosene DL, Moss MB, Kemper TL, Abraham CR, Tigges J, et al. Neurobiological bases of age-related cognitive decline in the rhesus monkey. J. Neuropathol. Exp. Neurol. 1996;55:861–874
  36. Kadar T, Silbermann M, Brandeis R, Levy A. Age-related structural changes in the rat hippocampus: correlation with working memory deficiency. Brain Res. 1990;512:113–120
  37. Luine VN, McEwen BS. Effects of stradiol on turnover of type A monoamine oxidase in brain. J. Neurochem. 1977;28:1221–1227
  38. Curcio CA, Hinds JW. Stability of synaptic density and spine volume in dentate gyrus of aged rats. Neurobiol. Aging. 1983;4:77–87
  39. Pliss L, Balcar VJ, Bubenikova V, Pokorny J, Fitzgibbon T, Stastny F. Morphology and ultrastructure of rat hippocampal formation after I.C.V. administration of n-acetyl-l-aspartyl-l-glutamate. Neuroscience. 2003;122:93–101
  40. Weiland NG. Glutamic acid decarboxylase messenger ribonucleic acid is regulated by estradiol and progesterone in the hippocampus. Endocrinology. 1992;131:2697–2702
  41. Ellerby HM, Martin SJ, Ellerby LM, Naiem SS, Rabizadeh S, Salvesen GS, et al. Establishment of a cell-free system of neuronal apoptosis: comparison of premitochondrial, mitochondrial, and postmitochondrial phases. J. Neurosci. 1997;17:6165–6178
  42. Weiner CP, Lizasonia I, Baylis SA, Knowles RG, Charles IG, Moncada S. Induction of calcium-dependent nitric oxide synthases by sex hormones. Proc. Natl. Acad. Sci. U.S.A. 1994;91:5212–5216
  43. Anglade P, Vyas S, Javoy-Agid F, Herrero MT, Michel PP, Marquez J, et al. Appoptosis and autophagy in nigra neurons of patients with Parkinson's disease. J. Histochem. Cytochem. 1997;12:25–31
  44. Sapolsky RM, Kery LC, McEwen BS. Prolonged glucocorticoid exposure reduces hippocampal neuron number: implication for aging. J. Neurosci. 1985;5:1222–1227
  45. Clarke PG. Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. 1990;181:195–213
  46. Shughrue PJ, Merchenthaler I. Distribution of estrogen receptor ß immunoreactivity in the rat central nervous system. J. Comp. Neurol. 2001;436:64–81
  47. Sourla A, Luo S, Labrie C, Belanger A, Labrie F. Morphological changes induced by 6-month treatment of intact and ovariectomized mice with tamoxifen and the pure antiestrogen EM-800. Endocrinology. 1997;138:5605–5617
  48. Nobakht M, Majidzadeh S, Fattahi M, Samadi M, Tabatabaei P. Expression of neuronal nitric oxide synthase during embryonic development of the rat optic vesicle. Pakistan J. Biol. Sci. 2007;10:1078–1082

PII: S0928-4680(11)00030-7

doi: 10.1016/j.pathophys.2011.01.002

Pathophysiology
Volume 18, Issue 4 , Pages 263-272 , September 2011

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