Comparing the effects of 17β-oestradiol and the selective oestrogen receptor modulators, raloxifene and tamoxifen, on prepulse inhibition in female rats

Schizophrenia Research

Volumn 168, Issue 3, 2015, Pages 634-639

  Gogos, Andrea ^a   van den Buuse, Maarten ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b LA TROBE UNIVERSITY   (Australia)

Author keywords

17 Estradiol; Female rats; Prepulse inhibition (PPI); Raloxifene; SERMs; Tamoxifen

Indexed keywords

APOMORPHINE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; ESTRADIOL; RALOXIFENE; TAMOXIFEN; DOPAMINE RECEPTOR STIMULATING AGENT; DRD2 PROTEIN, RAT; ESTROGEN; SELECTIVE ESTROGEN RECEPTOR MODULATOR;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG MEGADOSE; FEMALE; LOW DRUG DOSE; NONHUMAN; OVARIECTOMY; PREPULSE INHIBITION; PRIORITY JOURNAL; RAT; SCHIZOPHRENIA; SENSORY GATING; STARTLE REFLEX; AGONISTS; ANIMAL; AUDITORY STIMULATION; COMPARATIVE STUDY; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; RANDOMIZATION; SPRAGUE DAWLEY RAT;

ACOUSTIC STIMULATION; ANIMALS; APOMORPHINE; DOPAMINE AGONISTS; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; ESTROGENS; FEMALE; OVARIECTOMY; PREPULSE INHIBITION; RALOXIFENE HYDROCHLORIDE; RANDOM ALLOCATION; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D2; REFLEX, STARTLE; SCHIZOPHRENIA; SELECTIVE ESTROGEN RECEPTOR MODULATORS; TAMOXIFEN;

EID: 84941741532     PISSN: 09209964     EISSN: 15732509     Source Type: Journal    
DOI: 10.1016/j.schres.2015.04.029     Document Type: Article

References (59)

1. Akhondzadeh S., Nejatisafa A.A., Amini H., Mohammadi M.R., Larijani B., Kashani L., Raisi F., Kamalipour A. Adjunctive estrogen treatment in women with chronic schizophrenia: a double-blind, randomized, and placebo-controlled trial. Prog. Neuropsychopharmacol. Biol. Psychiatry 2003, 27(6):1007-1012.
2. Albert D.J., Jonik R.H., Gorzalka B.B., Newlove T., Webb B., Walsh M.L. Serum estradiol concentration required to maintain body weight, attractivity, proceptivity, and receptivity in the ovariectomized female rat. Physiol. Behav. 1991, 49(2):225-231.
3. Amrollahi Z., Rezaei F., Salehi B., Modabbernia A.H., Maroufi A., Esfandiari G.R., Naderi M., Ghebleh F., Ahmadi-Abhari S.A., Sadeghi M., Tabrizi M., Akhondzadeh S. Double-blind, randomized, placebo-controlled 6-week study on the efficacy and safety of the tamoxifen adjunctive to lithium in acute bipolar mania. J. Affect. Disord. 2011, 129(1-3):327-331.
4. Anderson G.L., Limacher M., Assaf A.R., Bassford T., Beresford S.A., Black H., Bonds D., Brunner R., Brzyski R., Caan B., Chlebowski R., Curb D., Gass M., Hays J., Heiss G., Hendrix S., Howard B.V., Hsia J., Hubbell A., Jackson R., Johnson K.C., Judd H., Kotchen J.M., Kuller L., LaCroix A.Z., Lane D., Langer R.D., Lasser N., Lewis C.E., Manson J., Margolis K., Ockene J., O'Sullivan M.J., Phillips L., Prentice R.L., Ritenbaugh C., Robbins J., Rossouw J.E., Sarto G., Stefanick M.L., Van Horn L., Wactawski-Wende J., Wallace R., Wassertheil-Smoller S. Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled trial. JAMA 2004, 291(14):1701-1712.
5. Arad M., Weiner I. Sex-dependent antipsychotic capacity of 17beta-estradiol in the latent inhibition model: a typical antipsychotic drug in both sexes, atypical antipsychotic drug in males. Neuropsychopharmacology 2010, 35(11):2179-2192.
6. Baraka A.M., Korish A.A., Soliman G.A., Kamal H. The possible role of estrogen and selective estrogen receptor modulators in a rat model of Parkinson's disease. Life Sci. 2011, 88(19-20):879-885.
7. Bergemann N., Mundt C., Parzer P., Jannakos I., Nagl I., Salbach B., Klinga K., Runnebaum B., Resch F. Plasma concentrations of estradiol in women suffering from schizophrenia treated with conventional versus atypical antipsychotics. Schizophr. Res. 2005, 73(2-3):357-366.
8. Bethea C.L., Mirkes S.J., Su A., Michelson D. Effects of oral estrogen, raloxifene and arzoxifene on gene expression in serotonin neurons of macaques. Psychoneuroendocrinology 2002, 27(4):431-445.
9. Braff D.L., Geyer M.A., Swerdlow N.R. Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berlin) 2001, 156(2-3):234-258.
10. Calabrese E.J. Dopamine: biphasic dose responses. Crit. Rev. Toxicol. 2001, 31(4-5):563-583.
11. Callier S., Morissette M., Grandbois M., Pelaprat D., Di Paolo T. Neuroprotective properties of 17beta-estradiol, progesterone, and raloxifene in MPTP C57Bl/6 mice. Synapse 2001, 41(2):131-138.
12. Canuso C.M., Pandina G. Gender and schizophrenia. Psychopharmacol. Bull. 2007, 40(4):178-190.
13. Castle D., Sham P., Murray R. Differences in distribution of ages of onset in males and females with schizophrenia. Schizophr. Res. 1998, 33(3):179-183.
14. Chaurasia C.S., Chen C.E., Rubin J., Dewey S.L. Effects of tamoxifen on striatal dopamine and 5-hydroxytryptamine release in freely moving male rats: an in-vivo microdialysis investigation. J. Pharm. Pharmacol. 1998, 50(12):1377-1385.
15. Chavez C., Hollaus M., Scarr E., Pavey G., Gogos A., van den Buuse M. The effect of estrogen on dopamine and serotonin receptor and transporter levels in the brain: an autoradiography study. Brain Res. 2010, 1321:51-59.
16. Cyr M., Landry M., Di Paolo T. Modulation by estrogen-receptor directed drugs of 5-hydroxytryptamine-2A receptors in rat brain. Neuropsychopharmacology 2000, 23(1):69-78.
17. Dluzen D.E. Neuroprotective effects of estrogen upon the nigrostriatal dopaminergic system. J. Neurocytol. 2000, 29(5-6):387-399.
18. Dluzen D.E., McDermott J.L., Anderson L.I. Tamoxifen diminishes methamphetamine-induced striatal dopamine depletion in intact female and male mice. J. Neuroendocrinol. 2001, 13(7):618-624.
19. Geyer M.A., Krebs-Thomson K., Braff D.L., Swerdlow N.R. Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review. Psychopharmacology 2001, 156(2-3):117-154.
20. Gogos A. Natural and synthetic sex hormones: effects on higher-order cognitive function and prepulse inhibition. Biol. Psychol. 2013, 93(1):17-23.
21. Gogos A., Van den Buuse M. Castration reduces the effect of serotonin-1A receptor stimulation on prepulse inhibition in rats. Behav. Neurosci. 2003, 117(6):1407-1415.
22. Gogos A., Van den Buuse M. Estrogen and progesterone prevent disruption of prepulse inhibition by the serotonin-1A receptor agonist 8-hydroxy-2-dipropylaminotetralin. J. Pharmacol. Exp. Ther. 2004, 309(1):267-274.
23. 1A receptor-induced disruptions of prepulse inhibition in healthy women. Neuropsychopharmacology 2006, 31(4):885-889.
24. Gogos A., Kwek P., Chavez C., van den Buuse M. Estrogen treatment blocks 8-hydroxy-2-dipropylaminotetralin- and apomorphine-induced disruptions of prepulse inhibition: involvement of dopamine D1 or D2 or serotonin 5-HT1A, 5-HT2A, or 5-HT7 receptors. J. Pharmacol. Exp. Ther. 2010, 333(1):218-227.
25. Gogos A., Kwek P., van den Buuse M. The role of estrogen and testosterone in female rats in behavioral models of relevance to schizophrenia. Psychopharmacology (Berlin) 2012, 219(1):213-224.
26. Gogos A., Wu Y.C., Williams A.S., Byrne L.K. The effects of ethinylestradiol and progestins ("the pill") on cognitive function in pre-menopausal women. Neurochem. Res. 2014, 39(12):2288-2300.
27. Grandbois M., Morissette M., Callier S., Di Paolo T. Ovarian steroids and raloxifene prevent MPTP-induced dopamine depletion in mice. Neuroreport 2000, 11(2):343-346.
28. Gray J.M., Schrock S., Bishop M. Estrogens and antiestrogens: actions and interactions with fluphenazine on food intake and body weight in rats. Am. J. Physiol. 1993, 264(6 Pt 2):R1214-R1218.
29. Häfner H., Riecher-Rossler A., An Der Heiden W., Maurer K., Fatkenheuer B., Loffler W. Generating and testing a causal explanation of the gender difference in age at first onset of schizophrenia. Psychol. Med. 1993, 23(4):925-940.
30. Huerta-Ramos E., Iniesta R., Ochoa S., Cobo J., Miquel E., Roca M., Serrano-Blanco A., Teba F., Usall J. Effects of raloxifene on cognition in postmenopausal women with schizophrenia: a double-blind, randomized, placebo-controlled trial. Eur. Neuropsychopharmacol. 2014, 24(2):223-231.
31. Jacobsen D.E., Samson M.M., Emmelot-Vonk M.H., Verhaar H.J. Raloxifene improves verbal memory in late postmenopausal women: a randomized, double-blind, placebo-controlled trial. Menopause 2010, 17(2):309-314.
32. Karahancer M., Cirpan T., Kanit L., Terek M.C., Dikmen Y., Ozsener S. The effects of raloxifen on depression and cognition in ovariectomized rats. Fertil. Steril. 2008, 89(1):240-242.
33. Kianimehr G., Fatehi F., Hashempoor S., Khodaei-Ardakani M.R., Rezaei F., Nazari A., Kashani L., Akhondzadeh S. Raloxifene adjunctive therapy for postmenopausal women suffering from chronic schizophrenia: a randomized double-blind and placebo controlled trial. Daru 2014, 22:55.
34. Kulkarni J., de Castella A., Fitzgerald P.B., Gurvich C.T., Bailey M., Bartholomeusz C., Burger H. Estrogen in severe mental illness: a potential new treatment approach. Arch. Gen. Psychiatry 2008, 65(8):955-960.
35. Kulkarni J., Gurvich C., Gilbert H., Mehmedbegovic F., Mu L., Marston N., Gavrilidis E., de Castella A. Hormone modulation: a novel therapeutic approach for women with severe mental illness. Aust. N. Z. J. Psychiatry 2008, 42(1):83-88.
36. Kulkarni J., Gurvich C., Lee S.J., Gilbert H., Gavrilidis E., de Castella A., Berk M., Dodd S., Fitzgerald P.B., Davis S.R. Piloting the effective therapeutic dose of adjunctive selective estrogen receptor modulator treatment in postmenopausal women with schizophrenia. Psychoneuroendocrinology 2010, 35(8):1142-1147.
37. Kumari V., Aasen I., Sharma T. Sex differences in prepulse inhibition deficits in chronic schizophrenia. Schizophr. Res. 2004, 69(2-3):219-235.
38. Lagunas N., Calmarza-Font I., Grassi D., Garcia-Segura L.M. Estrogen receptor ligands counteract cognitive deficits caused by androgen deprivation in male rats. Horm. Behav. 2011, 59(4):581-584.
39. Landry M., Levesque D., Di Paolo T. Estrogenic properties of raloxifene, but not tamoxifen, on D2 and D3 dopamine receptors in the rat forebrain. Neuroendocrinology 2002, 76(4):214-222.
40. Le Saux M., Di Paolo T. Influence of oestrogenic compounds on monoamine transporters in rat striatum. J. Neuroendocrinol. 2006, 18(1):25-32.
41. Littleton-Kearney M.T., Ostrowski N.L., Cox D.A., Rossberg M.I., Hurn P.D. Selective estrogen receptor modulators: tissue actions and potential for CNS protection. CNS Drug Rev. 2002, 8(3):309-330.
42. Maki P.M., Rich J.B., Rosenbaum R.S. Implicit memory varies across the menstrual cycle: estrogen effects in young women. Neuropsychologia 2002, 40(5):518-529.
43. McDermott J.L., Liu B., Dluzen D.E. Tamoxifen treatment of ovariectomized mice alters dopamine release from striatal tissue fragments superfused in vitro. Brain Res. 1995, 698(1-2):248-252.
44. McGrath J., Saha S., Welham J., El Saadi O., MacCauley C., Chant D. A systematic review of the incidence of schizophrenia: the distribution of rates and the influence of sex, urbanicity, migrant status and methodology. BMC Med. 2004, 2:13.
45. Moretti M., Valvassori S.S., Steckert A.V., Rochi N., Benedet J., Scaini G., Kapczinski F., Streck E.L., Zugno A.I., Quevedo J. Tamoxifen effects on respiratory chain complexes and creatine kinase activities in an animal model of mania. Pharmacol. Biochem. Behav. 2011, 98(2):304-310.
46. Pinkerton J.V., Thomas S. Use of SERMs for treatment in postmenopausal women. J. Steroid Biochem. Mol. Biol. 2014, 142:142-154.
47. Sanchez M.G., Bourque M., Morissette M., Di Paolo T. Steroids-dopamine interactions in the pathophysiology and treatment of CNS disorders. CNS Neurosci. Ther. 2010, 16(3):e43-e71.
48. Seeman M.V. The role of estrogen in schizophrenia. J. Psychiatry Neurosci. 1996, 21(2):123-127.
49. Sherwin B.B. Estrogen and cognitive functioning in women: lessons we have learned. Behav. Neurosci. 2012, 126(1):123-127.
50. Steckert A.V., Valvassori S.S., Mina F., Lopes-Borges J., Varela R.B., Kapczinski F., Dal-Pizzol F., Quevedo J. Protein kinase C and oxidative stress in an animal model of mania. Curr. Neurovasc. Res. 2012, 9(1):47-57.
51. Szymanski S., Lieberman J.A., Alvir J.M., Mayerhoff D., Loebel A., Geisler S., Chakos M., Koreen A., Jody D., Kane J., Woerner M., Cooper T. Gender differences in onset of illness, treatment response, course, and biologic indexes in first-episode schizophrenic patients. Am. J. Psychiatry 1995, 152(5):698-703.
52. Thwaites S.J., van den Buuse M., Gogos A. Differential effects of estrogen and testosterone on auditory sensory gating in rats. Psychopharmacology (Berlin) 2014, 231(1):243-256.
53. Usall J., Huerta-Ramos E., Iniesta R., Cobo J., Araya S., Roca M., Serrano-Blanco A., Teba F., Ochoa S. Raloxifene as an adjunctive treatment for postmenopausal women with schizophrenia: a double-blind, randomized, placebo-controlled trial. J. Clin. Psychiatry 2011, 72(11):1552-1557.
54. Velazquez-Zamora D.A., Garcia-Segura L.M., Gonzalez-Burgos I. Effects of selective estrogen receptor modulators on allocentric working memory performance and on dendritic spines in medial prefrontal cortex pyramidal neurons of ovariectomized rats. Horm. Behav. 2012, 61(4):512-517.
55. Walf A.A., Frye C.A. Raloxifene and/or estradiol decrease anxiety-like and depressive-like behavior, whereas only estradiol increases carcinogen-induced tumorigenesis and uterine proliferation among ovariectomized rats. Behav. Pharmacol. 2010, 21(3):231-240.
56. Wong J., Seeman M.V., Shapiro H. Case report: raloxifene in postmenopausal women with psychosis: preliminary findings. Am. J. Geriatr. Psychiatry 2003, 11(6):697-698.
57. Wu Y.C., Hill R.A., Gogos A., van den Buuse M. Sex differences and the role of estrogen in animal models of schizophrenia: interaction with BDNF. Neuroscience 2013, 239:67-83.
58. Yaffe K., Krueger K., Cummings S.R., Blackwell T., Henderson V.W., Sarkar S., Ensrud K., Grady D. Effect of raloxifene on prevention of dementia and cognitive impairment in older women: the Multiple Outcomes of Raloxifene Evaluation (MORE) randomized trial. Am. J. Psychiatry 2005, 162(4):683-690.
59. Zhou W., Koldzic-Zivanovic N., Clarke C.H., de Beun R., Wassermann K., Bury P.S., Cunningham K.A., Thomas M.L. Selective estrogen receptor modulator effects in the rat brain. Neuroendocrinology 2002, 75(1):24-33.