Gender difference in association of cognition with BDNF in chronic schizophrenia

Psychoneuroendocrinology

Volumn 48, Issue , 2014, Pages 136-146

  Zhang, Xiang Yang ^a,b   Chen, Da Chun ^b   Tan, Yun Long ^b   Tan, Shu ping ^b   Wang, Zhi Ren ^b   Yang, Fu De ^b   Xiu, Mei Hong ^b   Hui, Li ^b   Lv, Meng Han ^b   Zunta Soares, Giovana B ^a   Soares, Jair C ^a  

^a University of Texas Harris County Psychiatric Center   (United States)

^b PEKING UNIVERSITY   (China)

Author keywords

Association; BDNF; Cognition; Gender difference; Schizophrenia

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CHLORPROMAZINE; CLOZAPINE; HALOPERIDOL; NEUROLEPTIC AGENT; PERPHENAZINE; RISPERIDONE; SULPIRIDE;

ADULT; AGED; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; POSITIVE AND NEGATIVE SYNDROME SCALE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REPEATABLE BATTERY FOR THE ASSESSMENT OF NEUROPSYCHOLOGICAL STATUS; SCHIZOPHRENIA; SCORING SYSTEM; SEX DIFFERENCE; SHORT TERM MEMORY; BLOOD; CHRONIC DISEASE; COGNITION; CONTROLLED CLINICAL TRIAL; MEMORY; MIDDLE AGED; NEUROPSYCHOLOGICAL TEST; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGICAL RATING SCALE;

ADULT; AGED; BRAIN-DERIVED NEUROTROPHIC FACTOR; CHRONIC DISEASE; COGNITION; FEMALE; HUMANS; MALE; MEMORY; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; PSYCHIATRIC STATUS RATING SCALES; SCHIZOPHRENIA; SEX FACTORS;

EID: 84904899969     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2014.06.004     Document Type: Article

References (81)

1. Adlard P.A., Perreau V.M., Engesser-Cesar C., Cotman C.W. The timecourse of induction of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus following voluntary exercise. Neurosci. Lett. 2004, 363(1):43-48.
2. Antonova E., Sharma T., Morris R., Kumari V. The relationship between brain structure and neurocognition in schizophrenia: a selective review. Schizophr. Res. 2004, 70(2-3):117-145.
3. Asevedo E., Gadelha A., Noto C., Mansur R.B., Zugman A., Belangero S.I., Berberian A.A., Scarpato B.S., Leclerc E., Teixeira A.L., Gama C.S., Bressan R.A., Brietzke E. Impact of peripheral levels of chemokines BDNF and oxidative markers on cognition in individuals with schizophrenia. J. Psychiatr. Res. 2013, 47(10):1376-1382.
4. Beauchet O. Testosterone and cognitive function: current clinical evidence of a relationship. Eur. J. Endocrinol. 2006, 155(6):773-781.
5. Begliuomini S., Casarosa E., Pluchino N., Lenzi E., Centofanti M., Freschi L., Pieri M., Genazzani A.D., Luisi S., Genazzani A.R. Influence of endogenous and exogenous sex hormones on plasma brain-derived neurotrophic factor. Hum. Reprod. 2007, 22(4):995-1002.
6. Brébion G., David A.S., Jones H., Pilowsky L.S. Semantic organization and verbal memory efficiency in patients with schizophrenia. Neuropsychology 2004, 18(2):378-383.
7. Buckley P.F., Pillai A., Howell K.R. Brain-derived neurotrophic factor: findings in schizophrenia. Curr. Opin. Psychiatry 2011, 24(2):122-127.
8. Carlino D., Leone E., Di Cola F., Baj G., Marin R., Dinelli G., Tongiorgi E., De Vanna M. Low serum truncated-BDNF isoform correlates with higher cognitive impairment in schizophrenia. J. Psychiatr. Res. 2011, 45(2):273-279.
9. Chen D.C., Wang J., Wang B., Yang S.C., Zhang C.X., Zheng Y.L., Li Y.L., Wang N., Yang K.B., Xiu M.H., Kosten T.R., Zhang X.Y. Decreased levels of serum brain-derived neurotrophic factor in drug-naïve first-episode schizophrenia: relationship to clinical phenotypes. Psychopharmacology (Berl.) 2009, 207(3):375-380.
10. Ciammola A., Sassone J., Cannella M., Calza S., Poletti B., Frati L., Squitieri F., Silani V. Low brain-derived neurotrophic factor (BDNF) levels in serum of Huntington's disease patients. Am. J. Med. Genet. B: Neuropsychiatr. Genet. 2007, 144B(4):574-577.
11. Condray R., Yao J.K. Cognition, dopamine and bioactive lipids in schizophrenia. Front. Biosci. 2011, 3:298-330.
12. Dickerson F., Boronow J.J., Stallings C., Origoni A.E., Cole S.K., Yolken R.H. Cognitive functioning in schizophrenia and bipolar disorder: comparison of performance on the Repeatable Battery for the Assessment of Neuropsychological Status. Psychiatry Res. 2004, 129(1):45-53.
13. Diógenes M.J., Costenla A.R., Lopes L.V., Jerónimo-Santos A., Sousa V.C., Fontinha B.M., Ribeiro J.A., Sebastião A.M. Enhancement of LTP in aged rats is dependent on endogenous BDNF. Neuropsychopharmacology 2011, 36(9):1823-1836.
14. Di Paolo T. Modulation of brain dopamine transmission by sex steroids. Rev. Neurosci. 1994, 5:27-41.
15. Duff K., Humphreys Clark J.D., O'Bryant S.E., Mold J.W., Schiffer R.B., Sutker P.B. Utility of the RBANS in detecting cognitive impairment associated with Alzheimer's disease: sensitivity, specificity, and positive and negative predictive powers. Arch. Clin. Neuropsychol. 2008, 23:603-612.
16. Egan M.F., Kojima M., Callicott J.H., Goldberg T.E., Kolachana B.S., Bertolino A., Zaitsev E., Gold B., Goldman D., Dean M., Lu B., Weinberger D.R. The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 2003, 112:257-269.
17. Favalli G., Li J., Belmonte-de-Abreu P., Wong A.H., Daskalakis Z.J. The role of BDNF in the pathophysiology and treatment of schizophrenia. J. Psychiatr. Res. 2012, 46(1):1-11.
18. Fink G., Sumner B., Rosie R., Wilson H., McQueen J. Androgen actions on central serotonin neurotransmission: relevance for mood, mental state and memory. Behav. Brain Res. 1999, 105:53-68.
19. Fiszdon J.M., Silverstein S.M., Buchwald J., Hull J.W., Smith T.E. Verbal memory in schizophrenia: sex differences over repeated assessments. Schizophr. Res. 2003, 61(2-3):235-243.
20. Frye C.A., Rhodes M.E., Dudek B. Estradiol to aged female or male mice improves learning in inhibitory avoidance and water maze tasks. Brain Res. 2005, 1036(1-2):101-108.
21. Goff D.C. Future perspectives on the treatment of cognitive deficits and negative symptoms in schizophrenia. World Psychiatry 2013, 12(2):99-107.
22. Goldberg T.E., Gold J.M., Torrey E.F., Weinberger D.R. Lack of sex differences in the neuropsychological performance of patients with schizophrenia. Am. J. Psychiatry 1995, 152(6):883-888.
23. Goldstein J.M., Seidman L.J., Goodman J.M., Koren D., Lee H., Weintraub S., Tsuang M.T. Are there sex differences in neuropsychological functions among patients with schizophrenia?. Am. J. Psychiatry 1998, 155(10):1358-1364.
24. Goldstein J.M., Seidman L.J., O'Brien L.M., Horton N.J., Kennedy D.N., Makris N., Caviness V.S., Faraone S.V., Tsuang M.T. Impact of normal sexual dimorphisms on sex differences in structural brain abnormalities in schizophrenia assessed by magnetic resonance imaging. Arch. Gen. Psychiatry 2002, 59(2):154-164.
25. Green M.J., Matheson S.L., Shepherd A., Weickert C.S., Carr V.J. Brain-derived neurotrophic factor levels in schizophrenia: a systematic review with meta-analysis. Mol. Psychiatry 2011, 16(9):960-972.
26. Grigoriadis S., Seeman M.V. The role of estrogen in schizophrenia: implications for schizophrenia practice guidelines for women. Can. J. Psychiatry 2002, 47:437-442.
27. Grillo R.W., Ottoni G.L., Leke R., Souza D.O., Portela L.V., Lara D.R. Reduced serum BDNF levels in schizophrenic patients on clozapine or typical antipsychotics. J. Psychiatr. Res. 2007, 41:31-35.
28. Gunstad J., Benitez A., Smith J., Glickman E., Spitznagel M.B., Alexander T., Juvancic-Heltzel J., Murray L. Serum brain-derived neurotrophic factor is associated with cognitive function in healthy older adults. J. Geriatr. Psychiatry Neurol. 2008, 21(3):166-170.
29. Gur R.C., Ragland J.D., Moberg P.J., Turner T.H., Bilker W.B., Kohler C., Siegel S.J., Gur R.E. Computerized neurocognitive scanning: I. Methodology and validation in healthy people. Neuropsychopharmacology 2001, 25(5):766-776.
30. Guzowski J.F., Lyford G.L., Stevenson G.D., Houston F.P., McGaugh J.L., Worley P.F., Barnes C. Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long term memory. J. Neurosci. 2000, 20(11):3993-4001.
31. Hafner H., Behrens S., De Vry J., Gattaz W.F. An animal model for the effects of estradiol on dopamine-mediated behavior: implications for sex differences in schizophrenia. Psychiatry Res. 1991, 38:125-134.
32. Häfner H. Gender differences in schizophrenia. Psychoneuroendocrinology 2003, 28(Suppl. 2):17-54.
33. Halari R., Mehrotra R., Sharma T., Ng V., Kumari V. Cognitive impairment but preservation of sexual dimorphism in cognitive abilities in chronic schizophrenia. Psychiatry Res. 2006, 141(2):129-139.
34. Hariri A.R., Goldberg T.E., Mattay V.S., Kolachana B.S., Callicott J.H., Egan M.F., Weinberger D.R. Brain-derived neurotrophic factor val66met polymorphism affects human memory-related hippocampal activity and predicts memory performance. J. Neurosci. 2003, 23(17):6690-6694.
35. Harvey P.D., Green M.F., Keefe R.S., Velligan D.I. Cognitive functioning in schizophrenia: a consensus statement on its role in the definition and evaluation of effective treatments for the illness. J. Clin. Psychiatry 2004, 65(3):361-372.
36. Hoff A.L., Wieneke M., Faustman W.O., Horon R., Sakuma M., Blankfeld H., Espinoza S., DeLisi L.E. Sex differences in neuropsychological functioning of first-episode and chronically ill schizophrenic patients. Am. J. Psychiatry 1998, 155(10):1437-1439.
37. Huang T.L., Lee C.T. Associations between serum brain-derived neurotrophic factor levels and clinical phenotypes in schizophrenia patients. J. Psychiatr. Res. 2006, 10:664-668.
38. Ikeda Y., Yahata N., Ito I., Nagano M., Toyota T., Yoshikawa T., Okubo Y., Suzuki H. Low serum levels of brain-derived neurotrophic factor and epidermal growth factor in patients with chronic schizophrenia. Schizophr. Res. 2008, 101:58-66.
39. Janowsky J.S. The role of androgens in cognition and brain aging in men. Neuroscience 2006, 138(3):1015-1020.
40. Karakaya S., Kipp M., Beyer C. Oestrogen regulates the expression and function of dopamine transporters in astrocytes of the nigrostriatal system. J. Neuroendocrinol. 2007, 19:682-690.
41. Kaur P., Jodhka P.K., Underwood W.A., Bowles C.A., de Fiebre N.C., de Fiebre C.M., Singh M. Progesterone increases brain-derived neuroptrophic factor expression and protects against glutamate toxicity in a mitogen-activated protein kinase- and phosphoinositide-3 kinase-dependent manner in cerebral cortical explants. Neurosci. Res. 2007, 85(11):2441-2449.
42. Komulainen P., Pedersen M., Hänninen T., Bruunsgaard H., Lakka T.A., Kivipelto M., Hassinen M., Rauramaa T.H., Pedersen B.K., Rauramaa R. BDNF is a novel marker of cognitive function in ageing women: the DR's EXTRA Study. Neurobiol. Learn. Mem. 2008, 90(4):596-603.
43. Korte M., Griesbeck O., Gravel C., Carroll P., Staiger V., Thoenen H., Bonhoeffer T. Virus-mediated gene transfer into hippocampal CA1 region restores long-term potentiation in brain-derived neurotrophic factor mutant mice. Proc. Natl. Acad. Sci. U. S. A. 1996, 93(22):12547-12552.
44. Lewine R.R., Walker E.F., Shurett R., Caudle J., Haden C. Sex differences in neuropsychological functioning among schizophrenic patients. Am. J. Psychiatry 1996, 153(9):1178-1184.
45. Lu B., Gottschalk W. Modulation of hippocampal synaptic transmission and plasticity by neurotrophins. Prog. Brain Res. 2000, 128:231-241.
46. Lu B., Nagappan G., Lu Y. BDNF and synaptic plasticity, cognitive function, and dysfunction. Handb. Exp. Pharmacol. 2014, 220:223-250.
47. Lu Y., Christian K., Lu B. BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory?. Neurobiol. Learn. Mem. 2008, 89(3):312-323.
48. McEwen B.S., Woolley C.S. Estradiol and progesterone regulate neuronal structure and synaptic connectivity in adult as well as developing brain. Exp. Gerontol. 1994, 29:431-436.
49. Nieto R., Kukuljan M., Silva H. BDNF and schizophrenia: from neurodevelopment to neuronal plasticity, learning, and memory. Front. Psychiatry 2013, 4:45.
50. Niitsu T., Shirayama Y., Matsuzawa D., Hasegawa T., Kanahara N., Hashimoto T., Shiraishi T., Shiina A., Fukami G., Fujisaki M., Watanabe H., Nakazato M., Asano M., Kimura S., Hashimoto K., Iyo M. Associations of serum brain-derived neurotrophic factor with cognitive impairments and negative symptoms in schizophrenia. Prog. Neuropsychopharmacol. Biol. Psychiatry 2011, 35(8):1836-1840.
51. Nurjono M., Lee J., Chong S.A. A review of brain-derived neurotrophic factor as a candidate biomarker in schizophrenia. Clin. Psychopharmacol. Neurosci. 2012, 10(2):61-70.
52. Palmer B.W., Dawes S.E., Heaton R.K. What do we know about neuropsychological aspects of schizophrenia?. Neuropsychol. Rev. 2009, 19(3):365-384.
53. Palomino A.G., Pinto A.A., Gomez C., Mosquera F., Garcia G. Decreased levels of plasma BDNF levels in first-episode schizophrenia and bipolar disorder patients. Schizophr. Res. 2006, 86:321-322.
54. Pandya C.D., Kutiyanawalla A., Pillai A. BDNF-TrkB signaling and neuroprotection in schizophrenia. Asian J. Psychiatry 2013, 6(1):22-28.
55. Patterson S.L., Abel T., Deuel T.A., Martin K.C., Rose J.C., Kandel E.R. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 1996, 16(6):1137-1145.
56. Pirildar S., Gönül A.S., Taneli F., Akdeniz F. Low serum levels of brain-derived neurotrophic factor in patients with schizophrenia do not elevate after antipsychotic treatment. Prog. Neuropsychopharmacol. Biol. Psychiatry 2004, 28:709-713.
57. Pillai A., Kale A., Joshi S., Naphade N., Raju M.S., Nasrallah H., Mahadik S.P. Decreased BDNF levels in CSF of drug-naive first episode psychotic subjects: correlation with plasma BDNF and psychopathology. Int. J. Neuropsychopharmacol. 2010, 13(4):535-553.
58. Pillai A., Bruno D., Sarreal A.S., Hernando R.T., Saint-Louis L.A., Nierenberg J., Ginsberg S.D., Pomara N., Mehta P.D., Zetterberg H., Blennow K., Buckley P.F. Plasma BDNF levels vary in relation to body weight in females. PLoS ONE 2012, 7(7):e39358.
59. Pillai A., Buckley P.F. Reliable biomarkers and predictors of schizophrenia and its treatment. Psychiatr. Clin. N. Am. 2012, 35(3):645-659.
60. Poo M.M. Neurotrophins as synaptic modulators. Nat. Rev. Neurosci. 2001, 2:24-32.
61. Randolph C., Tierney M.C., Mohr E., Chase T.N. The Repeatable Battery for the Assessment of Neuropsychological Status (RBANS): preliminary clinical validity. J. Clin. Exp. Neuropsychol. 1998, 20:310-319.
62. Reis H.J., Nicolato R., Barbosa I.G., Teixeira do Prado P.H., Romano-Silva M.A., Teixeira A.L. Increased serum levels of brain derived neurotrophic factor in chronic institutionalized patients with schizophrenia. Neurosci. Lett. 2008, 439:157-159.
63. Riecher-Rössler A., Häfner H. Gender aspects in schizophrenia: bridging the border between social and biological psychiatry. Acta Psychiatr. Scand. 2000, 407(Suppl.):58-62.
64. Rizos E.N., Rontos I., Laskos E., Arsenis G., Michalopoulou P.G., Vasilopoulos D., Gournellis R., Lykouras L. Investigation of serum BDNF levels in drug-naive patients with schizophrenia. Prog. Neuropsychopharmacol. Biol. Psychiatry 2008, 32:1308-1311.
65. Rizos E.N., Papadopoulou A., Laskos E., Michalopoulou P.G., Kastania A., Vasilopoulos D., Katsafouros K., Lykouras L. Reduced serum BDNF levels in patients with chronic schizophrenic disorder in relapse, who were treated with typical or atypical antipsychotics. World J. Biol. Psychiatry 2010, 11:251-255.
66. Rubin L.H., Haas G.L., Keshavan M.S., Sweeney J.A., Maki P.M. Sex difference in cognitive response to antipsychotic treatment in first episode schizophrenia. Neuropsychopharmacology 2008, 33:290-297.
67. Rubin L.H., Carter C.S., Drogos L., Jamadar R., Pournajafi-Nazarloo H., Sweeney J.A., Maki P.M. Sex-specific associations between peripheral oxytocin and emotion perception in schizophrenia. Schizophr. Res. 2011, 130(1-3):266-270.
68. Scharfman H.E., Maclusky N.J. Similarities between actions of estrogen and BDNF in the hippocampus: coincidence or clue?. Trends Neurosci. 2005, 28(2):79-85.
69. Sharma T., Antonova L. Cognitive function in schizophrenia. Deficits, functional consequences, and future treatment. Psychiatr. Clin. N. Am. 2003, 26(1):25-40.
70. Shimizu E., Hashimoto K., Watanabe H., Komatsu N., Okamura N., Koike K., Shinoda N., Nakazato M., Kumakiri C., Okada S., Iyo M. Serum brain-derived neurotrophic factor (BDNF) levels in schizophrenia are indistinguishable from controls. Neurosci. Lett. 2003, 351:111-114.
71. Sohrabji F., Lewis D.K. Estrogen-BDNF interactions: implications for neurodegenerative diseases. Front. Neuroendocrinol. 2006, 27(4):404-414.
72. Sota T.L., Heinrichs R.W. Sex differences in verbal memory in schizophrenia patients treated with "typical" neuroleptics. Schizophr. Res. 2003, 62:175-182.
73. Tan Y.L., Zhou D.F., Cao L.Y., Zou Y.Z., Zhang X.Y. Decreased BDNF in serum of patients with chronic schizophrenia on long term treatment with antipsychotics. Neurosci. Lett. 2005, 382:27-32.
74. Toyooka K., Asama K., Watanabea Y., Muratakeb T., Takahashib M., Someyab T., Nawaa H. Decreased levels of brain-derived neurotrophic factor in serum of chronic schizophrenic patients. Psychiatry Res. 2002, 110:249-257.
75. Tyler W.J., Alonso M., Bramham C.R., Pozzo-Miller L.D. From acquisition to consolidation: on the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning. Learn. Mem. 2002, 9(5):224-237.
76. Vinogradov S., Fisher M., Holland C., Shelly W., Wolkowitz O., Mellon S.H. Is serum brain-derived neurotrophic factor a biomarker for cognitive enhancement in schizophrenia?. Biol. Psychiatry 2009, 66(6):549-553.
77. Wisner K.M., Elvevåg B., Gold J.M., Weinberger D.R., Dickinson D. A closer look at siblings of patients with schizophrenia: the association of depression history and sex with cognitive phenotypes. Schizophr. Res. 2011, 126(1-3):164-173.
78. Xiu M.H., Hui L., Dang Y.F., Hou T.D., Zhang C.X., Zheng Y.L., da Chen C., Kosten T.R., Zhang X.Y. Decreased serum BDNF levels in chronic institutionalized schizophrenia on long-term treatment with typical and atypical antipsychotics. Prog. Neuropsychopharmacol. Biol. Psychiatry 2009, 33(8):1508-1512.
79. Yu H., Zhang Z., Shi Y., Bai F., Xie C., Qian Y., Yuan Y., Deng L. Association study of the decreased serum BDNF concentrations in amnestic mild cognitive impairment and the Val66Met polymorphism in Chinese Han. J. Clin. Psychiatry 2008, 69(7):1104-1111.
80. Zhang B.H., Tan Y.L., Zhang W.F., Wang Z.R., Yang G.G., Shi C., Zhang X.Y., Zhou D.F. Repeatable battery for the assessment of neuropsychological status (RBANS) as a screening test in Chinese: reliability and validity. Chin. Ment. Health J. 2009, 28:865-869.
81. Zhang X.Y., Chen da C., Xiu M.H., Haile C.N., Luo X., Xu K., Zhang H.P., Zuo L., Zhang Z., Zhang X., Kosten T.A., Kosten T.R. Cognitive and serum BDNF correlates of BDNF Val66Met gene polymorphism in patients with schizophrenia and normal controls. Hum. Genet. 2012, 131(7):1187-1195.