Raloxifene increases prefrontal activity during emotional inhibition in schizophrenia based on estrogen receptor genotype

European Neuropsychopharmacology

Volumn 26, Issue 12, 2016, Pages 1930-1940

  Kindler, Jochen ^a,b,c   Weickert, Cynthia Shannon ^a,b,d   Schofield, Peter R ^a,b,d   Lenroot, Rhoshel ^a,b,d   Weickert, Thomas W ^a,b,d  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^c UNIVERSITY OF BERN   (Switzerland)

^d SCHIZOPHRENIA RESEARCH INSTITUTE   (Australia)

Author keywords

Emotions; Estrogen receptor alpha; Inhibition; Magnetic resonance imaging; Raloxifene hydrochloride; Schizophrenia

Indexed keywords

ESTROGEN RECEPTOR ALPHA; PLACEBO; RALOXIFENE; ESTROGEN RECEPTOR ALPHA, HUMAN; SELECTIVE ESTROGEN RECEPTOR MODULATOR;

ADULT; ARTICLE; ATTENTION; BOLD SIGNAL; CLINICAL ARTICLE; COMPARATIVE STUDY; COMPREHENSION; CONTROLLED STUDY; CROSSOVER PROCEDURE; DISEASE SEVERITY; DOUBLE BLIND PROCEDURE; DSM-IV; ELECTROENCEPHALOGRAM; EMOTION; EMOTIONAL INHIBITION; ESTROGEN SYNTHESIS; FACIAL RECOGNITION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; GENETIC VARIATION; GENOTYPE; HUMAN; MALE; MEDICAL HISTORY; MEMORY; MENTAL PATIENT; PREDICTION; PREFRONTAL CORTEX; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SCHIZOAFFECTIVE PSYCHOSIS; SCHIZOPHRENIA; TASK PERFORMANCE; TREATMENT DURATION; WECHSLER ADULT INTELLIGENCE SCALE; ADOLESCENT; DRUG EFFECTS; GENETICS; INHIBITION (PSYCHOLOGY); MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PSYCHOLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; EMOTIONS; ESTROGEN RECEPTOR ALPHA; FEMALE; GENETIC VARIATION; GENOTYPE; HUMANS; INHIBITION (PSYCHOLOGY); MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; PREFRONTAL CORTEX; RALOXIFENE HYDROCHLORIDE; SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY; SELECTIVE ESTROGEN RECEPTOR MODULATORS; YOUNG ADULT;

EID: 84999208551     PISSN: 0924977X     EISSN: 18737862     Source Type: Journal    
DOI: 10.1016/j.euroneuro.2016.10.009     Document Type: Article

References (52)

1. Amin, Z., Canli, T., Epperson, C.N., Effect of estrogen-serotonin interactions on mood and cognition. Behav. Cogn. Neurosci. Rev. 4 (2005), 43–58.
2. Amin, Z., Epperson, C.N., Constable, R.T., Canli, T., Effects of estrogen variation on neural correlates of emotional response inhibition. Neuroimage. 32 (2006), 457–464.
3. Asplund, C.L., Todd, J.J., Snyder, A.P., Marois, R., A central role for the lateral prefrontal cortex in goal-directed and stimulus-driven attention. Nat. Neurosci. 13 (2010), 507–512.
4. Barch, D.M., Carter, C.S., Braver, T.S., Sabb, F.W., MacDonald, A. 3rd, Noll, D.C., Cohen, J.D., Selective deficits in prefrontal cortex function in medication-naive patients with schizophrenia. Arch. Gen. Psychiatry. 58 (2001), 280–288.
5. Becherini, L., Gennari, L., Masi, L., Mansani, R., Massart, F., Morelli, A., Falchetti, A., Gonnelli, S., Fiorelli, G., Tanini, A., Brandi, M.L., Evidence of a linkage disequilibrium between polymorphisms in the human estrogen receptor alpha gene and their relationship to bone mass variation in postmenopausal Italian women. Hum. Mol. Genet 9 (2000), 2043–2050.
6. Berman, K.F., Schmidt, P.J., Rubinow, D.R., Danaceau, M.A., Van Horn, J.D., Esposito, G., Ostrem, J.L., Weinberger, D.R., Modulation of cognition-specific cortical activity by gonadal steroids: a positron-emission tomography study in women. Proc. Natl. Acad. Sci. USA 94 (1997), 8836–8841.
7. Bookheimer, S.Y., Strojwas, M.H., Cohen, M.S., Saunders, A.M., Pericak-Vance, M.A., Mazziotta, J.C., Small, G.W., Patterns of brain activation in people at risk for Alzheimer׳s disease. N. Engl. J. Med. 343 (2000), 450–456.
8. Bradley, M.M., Lang, P.J., Affective norms for English words (ANEW): instruction manual and affective ratings. The Cenctre for Research in Psychophysiology. 1999, University of Florida, Gainesville (FL).
9. First, M.B., Structured Clinical Interview for DSM-IV-TR Axis I Disorders: scid-i. Biometrics Research Department. 2007, New York State Psychiatric Institutute, New York.
10. Glahn, D.C., Ragland, J.D., Abramoff, A., Barrett, J., Laird, A.R., Bearden, C.E., Velligan, D.I., Beyond hypofrontality: a quantitative meta-analysis of functional neuroimaging studies of working memory in schizophrenia. Hum. Brain Mapp. 25 (2005), 60–69.
11. Goekoop, R., Barkhof, F., Duschek, E.J., Netelenbos, C., Knol, D.L., Scheltens, P., Rombouts, S.A., Raloxifene treatment enhances brain activation during recognition of familiar items: a pharmacological fMRI study in healthy elderly males. Neuropsychopharmacology 31 (2006), 1508–1518.
12. Green, M.F., Kern, R.S., Braff, D.L., Mintz, J., Neurocognitive deficits and functional outcome in schizophrenia: are we measuring the “right stuff”?. Schizophr. Bull. 26 (2000), 119–136.
13. Gur, R.E., Petty, R.G., Turetsky, B.I., Gur, R.C., Schizophrenia throughout life: sex differences in severity and profile of symptoms. Schizophr. Res. 21 (1996), 1–12.
14. Hirata, S., Shoda, T., Kato, J., Hoshi, K., Isoform/variant mRNAs for sex steroid hormone receptors in humans. Trends. Endocrinol. Metab. 14 (2003), 124–129.
15. 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. 24 (2014), 223–231.
16. Ji, E., Weickert, C.S., Lenroot, R., Kindler, J., Skilleter, A.J., Vercammen, A., White, C., Gur, R.E., Weickert, T.W., Adjunctive selective estrogen receptor modulator increases neural activity in the hippocampus and inferior frontal gyrus during emotional face recognition in schizophrenia. Transl. Psychiatry, 6, 2016, e795.
17. Kay, S.R., Fiszbein, A., Opler, L.A., The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull. 13 (1987), 261–276.
18. Keedy, S.K., Reilly, J.L., Bishop, J.R., Weiden, P.J., Sweeney, J.A., Impact of antipsychotic treatment on attention and motor learning systems in first-episode schizophrenia. Schizophr. Bull. 41 (2015), 355–365.
19. Kindler, J., Weickert, C.S., Skilleter, A.J., Catts, S.V., Lenroot, R., Weickert, T.W., Selective estrogen receptor modulation increases hippocampal activity during probabilistic association learning in schizophrenia. Neuropsychopharmacology 40 (2015), 2388–2397.
20. Ko, Y.H., Joe, S.H., Cho, W., Park, J.H., Lee, J.J., Jung, I.K., Kim, L., Kim, S.H., Estrogen, cognitive function and negative symptoms in female schizophrenia. Neuropsychobiology 53 (2006), 169–175.
21. Kohler, C.G., Turner, T.H., Bilker, W.B., Brensinger, C.M., Siegel, S.J., Kanes, S.J., Gur, R.E., Gur, R.C., Facial emotion recognition in schizophrenia: intensity effects and error pattern. Am. J. Psychiatry 160 (2003), 1768–1774.
22. Kulkarni, J., Gavrilidis, E., Wang, W., Worsley, R., Fitzgerald, P.B., Gurvich, C., Van Rheenen, T., Berk, M., Burger, H., Estradiol for treatment-resistant schizophrenia: a large-scale randomized-controlled trial in women of child-bearing age. Mol. Psychiatry, 2014.
23. 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. 35 (2010), 1142–1147.
24. Leucht, S., Wahlbeck, K., Hamann, J., Kissling, W., New generation antipsychotics versus low-potency conventional antipsychotics: a systematic review and meta-analysis. Lancet 361 (2003), 1581–1589.
25. Lieberman, J.A., Perkins, D., Belger, A., Chakos, M., Jarskog, F., Boteva, K., Gilmore, J., The early stages of schizophrenia: speculations on pathogenesis, pathophysiology, and therapeutic approaches. Biol. Psychiatry 50 (2001), 884–897.
26. Lilly, Ea.C., Product Information. (Evista (raloxifene), 2007, Indianapolis, IN.
27. Lonard, D.M., Smith, C.L., Molecular perspectives on selective estrogen receptor modulators (SERMs): progress in understanding their tissue-specific agonist and antagonist actions. Steroids. 67 (2002), 15–24.
28. Maruyama, H., Toji, H., Harrington, C.R., Sasaki, K., Izumi, Y., Ohnuma, T., Arai, H., Yasuda, M., Tanaka, C., Emson, P.C., Nakamura, S., Kawakami, H., Lack of an association of estrogen receptor alpha gene polymorphisms and transcriptional activity with Alzheimer׳s disease. Arch. Neurol. 57 (2000), 236–240.
29. Minzenberg, M.J., Yoon, J.H., Cheng, Y., Carter, C.S., Sustained modafinil treatment effects on control-related gamma oscillatory power in schizophrenia. Neuropsychopharmacology, 2015.
30. Moore, L., Kyaw, M., Vercammen, A., Lenroot, R., Kulkarni, J., Curtis, J., O׳Donnell, M., Carr, V.J., Shannon Weickert, C., Weickert, T.W., Serum testosterone levels are related to cognitive function in men with schizophrenia. Psychoneuroendocrinology 38 (2013), 1717–1728.
31. Perlman, W.R., Tomaskovic-Crook, E., Montague, D.M., Webster, M.J., Rubinow, D.R., Kleinman, J.E., Weickert, C.S., Alteration in estrogen receptor alpha mRNA levels in frontal cortex and hippocampus of patients with major mental illness. Biol. Psychiatry. 58 (2005), 812–824.
32. Ravizza, S.M., Moua, K.C., Long, D., Carter, C.S., The impact of context processing deficits on task-switching performance in schizophrenia. Schizophr. Res. 116 (2010), 274–279.
33. Ryan, J., Carriere, I., Amieva, H., Rouaud, O., Berr, C., Ritchie, K., Scarabin, P.Y., Ancelin, M.L., Prospective analysis of the association between estrogen receptor gene variants and the risk of cognitive decline in elderly women. Eur. Neuropsychopharmacol. 23 (2013), 1763–1768.
34. Schneider, F., Gur, R.C., Gur, R.E., Shtasel, D.L., Emotional processing in schizophrenia: neurobehavioral probes in relation to psychopathology. Schizophr. Res. 17 (1995), 67–75.
35. Shtasel, D.L., Gur, R.E., Gallacher, F., Heimberg, C., Gur, R.C., Gender differences in the clinical expression of schizophrenia. Schizophr. Res. 7 (1992), 225–231.
36. Sundermann, E.E., Maki, P.M., Bishop, J.R., A review of estrogen receptor alpha gene (ESR1) polymorphisms, mood, and cognition. Menopause 17 (2010), 874–886.
37. Usall, J., Huerta-Ramos, E., Labad, J., Cobo, J., Nunez, C., Creus, M., Pares, G.G., Cuadras, D., Franco, J., Miquel, E., Reyes, J.C., Roca, M., Group, R., Raloxifene as an adjunctive treatment for postmenopausal women with schizophrenia: a 24-week double-blind, randomized, parallel, placebo-controlled trial. Schizophr. Bull., 2015.
38. Vercammen, A., Morris, R., Green, M.J., Lenroot, R., Kulkarni, J., Carr, V.J., Weickert, C.S., Weickert, T.W., Reduced neural activity of the prefrontal cognitive control circuitry during response inhibition to negative words in people with schizophrenia. J. Psychiatry Neurosci. 37 (2012), 379–388.
39. Vercammen, A., Rushby, J.A., Loo, C., Short, B., Weickert, C.S., Weickert, T.W., Transcranial direct current stimulation influences probabilistic association learning in schizophrenia. Schizophr. Res. 131 (2011), 198–205.
40. Vercammen, A., Skilleter, A.J., Lenroot, R., Catts, S.V., Weickert, C.S., Weickert, T.W., Testosterone is inversely related to brain activity during emotional inhibition in schizophrenia. PLoS One, 8, 2013, e77496.
41. Vercammen, A., Weickert, C.S., Skilleter, A.J., Lenroot, R., Schofield, P.R., Weickert, T.W., Common polymorphisms in dopamine-related genes combine to produce a ׳schizophrenia-like׳ prefrontal hypoactivity. Transl. Psychiatry, 4, 2014, e356.
42. Wang, J., Cheng, C.M., Zhou, J., Smith, A., Weickert, C.S., Perlman, W.R., Becker, K.G., Powell, D., Bondy, C.A., Estradiol alters transcription factor gene expression in primate prefrontal cortex. J. Neurosci. Res. 76 (2004), 306–314.
43. Wechsler, D., Wechsler Adult Intelligence Scale. 1997, The Psychological Corporation: San Antonio, Texas.
44. Wechsler, D., Wechsler Test of Adult Reading. 2001, The Pscyhological Corporation: San Antonio, Texas.
45. Weickert, C.S., Miranda-Angulo, A.L., Wong, J., Perlman, W.R., Ward, S.E., Radhakrishna, V., Straub, R.E., Weinberger, D.R., Kleinman, J.E., Variants in the estrogen receptor alpha gene and its mRNA contribute to risk for schizophrenia. Hum. Mol. Genet. 17 (2008), 2293–2309.
46. Weickert, T.W., Goldberg, T.E., Callicott, J.H., Chen, Q., Apud, J.A., Das, S., Zoltick, B.J., Egan, M.F., Meeter, M., Myers, C., Gluck, M.A., Weinberger, D.R., Mattay, V.S., Neural correlates of probabilistic category learning in patients with schizophrenia. J. Neurosci. 29 (2009), 1244–1254.
47. Weickert, T.W., Goldberg, T.E., Gold, J.M., Bigelow, L.B., Egan, M.F., Weinberger, D.R., Cognitive impairments in patients with schizophrenia displaying preserved and compromised intellect. Arch. Gen. Psychiatry. 57 (2000), 907–913.
48. Weickert, T.W., Weinberg, D., Lenroot, R., Catts, S.V., Wells, R., Vercammen, A., O׳Donnell, M., Galletly, C., Liu, D., Balzan, R., Short, B., Pellen, D., Curtis, J., Carr, V.J., Kulkarni, J., Schofield, P.R., Weickert, C.S., Adjunctive raloxifene treatment improves attention and memory in men and women with schizophrenia. Mol. Psychiatry. 20 (2015), 685–694.
49. Weisbrod, M., Kiefer, M., Marzinzik, F., Spitzer, M., Executive control is disturbed in schizophrenia: evidence from event-related potentials in a Go/NoGo task. Biol. Psychiatry. 47 (2000), 51–60.
50. 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. 162 (2005), 683–690.
51. Yaffe, K., Lindquist, K., Sen, S., Cauley, J., Ferrell, R., Penninx, B., Harris, T., Li, R., Cummings, S.R., Estrogen receptor genotype and risk of cognitive impairment in elders: findings from the health ABC study. Neurobiol. Aging. 30 (2009), 607–614.
52. Yaffe, K., Lui, L.Y., Grady, D., Stone, K., Morin, P., Estrogen receptor 1 polymorphisms and risk of cognitive impairment in older women. Biol. Psychiatry. 51 (2002), 677–682.