Psychotic Alzheimer's disease is associated with gender-specific tau phosphorylation abnormalities

Neurobiology of Aging

Volumn 35, Issue 9, 2014, Pages 2021-2028

  Koppel, Jeremy ^a,b   Acker, Chris ^a   Davies, Peter ^a   Lopez, Oscar L ^c   Jimenez, Heidy ^a   Azose, Miriam ^d   Greenwald, Blaine S ^b   Murray, Patrick S ^c   Kirkwood, Caitlin M ^c   Kofler, Julia ^c   Sweet, Robert A ^a,c,e  

^a FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b Northwell Health   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d TOURO COLLEGE   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Alpha synuclein; Alzheimer's disease; Dementia with Lewy bodies; Neurofibrillary tangles; Psychosis; Tau

Indexed keywords

ALPHA SYNUCLEIN; EPITOPE; SERINE; TAU PROTEIN; THREONINE;

AGED; ALZHEIMER DISEASE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FRONTAL CORTEX; HUMAN; HUMAN TISSUE; MALE; POSTMORTEM CHANGE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN PHOSPHORYLATION; PSYCHOSIS; SEX DIFFERENCE; SUPERIOR FRONTAL GYRUS; TAUOPATHY; COMPLICATION; FRONTAL LOBE; METABOLISM; NEUROFIBRILLARY TANGLE; PATHOLOGY; PHOSPHORYLATION; PSYCHOTIC DISORDERS; SEXUAL DEVELOPMENT; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ALPHA-SYNUCLEIN; ALZHEIMER DISEASE; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FRONTAL LOBE; HUMANS; MALE; NEUROFIBRILLARY TANGLES; PHOSPHORYLATION; PSYCHOTIC DISORDERS; SEX CHARACTERISTICS; TAU PROTEINS;

EID: 84902116675     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.03.003     Document Type: Article

References (52)

1. Acker C.M., Forest S.K., Zinkowski R., Davies P., d'Abramo C. Sensitive quantitative assays for tau and phospho-tau in transgenic mouse models. Neurobiol. Aging 2013, 34:338-350.
2. Arriagada P.V., Growdon J.H., Hedley-Whyte E.T., Hyman B.T. Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 1992, 42(3 Pt 1):631-639.
3. Augustinack J.C., Schneider A., Mandelkow E.M., Hyman B.T. Specific tau phosphorylation sites correlate with severity of neuronal cytopathology in Alzheimer's disease. Acta Neuropathol. 2002, 103:26-35.
4. Braak H., Braak E. Neuropahological staging of Alzheimer-related changes. Acta Neuropath. Appl. Neurobiol. 1991, 14:39-44.
5. Braak H., Braak E. Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiol. Aging 1995, 16:271-278. discussion 8-84.
6. Chien D.T., Szardenings A.K., Bahri S., Walsh J.C., Mu F., Xia C., Shankle W.R., Lerner A.J., Su M.Y., Elizarov A., Kolb H.C. Early clinical PET Imaging Results with the Novel PHF-tau Radioligand [F18]-T808. J. Alzheimers Dis. 2014, 38:171-184.
7. Emanuel J.E., Lopez O.L., Houck P.R., Becker J.T., Weamer E.A., Demichele-Sweet M.A., Kuller L., Sweet R.A. Trajectory of cognitive decline as a predictor of psychosis in early Alzheimer disease in the cardiovascular health study. Am. J. Geriatr. Psychiatry 2011, 19:160-168.
8. Farber N.B., Rubin E.H., Newcomer J.W., Kinscherf D.A., Miller J.P., Morris J.C., Olney J.W., McKeel D.W. Increased neocortical neurofibrillary tangle density in subjects with Alzheimer disease and psychosis. Arch. Gen. Psychiatry 2000, 57:1165-1173.
9. Deaths with Antipsychotics in Elderly Patients with Behavioral Disturbances. Public Health Advisory 2005, FDA.
10. Goedert M. Tau protein and the neurofibrillary pathology of Alzheimer's disease. Trends Neurosci. 1993, 16:460-465.
11. Hirono N., Mori E., Yasuda M., Ikejiri Y., Imamura T., Shimomura T., Ikeda M., Hashimoto M., Yamashita H. Factors associated with psychotic symptoms in Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 1998, 64:648-652.
12. Hollingworth P., Hamshere M.L., Holmans P.A., O'Donovan M.C., Sims R., Powell J., Lovestone S., Myers A., DeVrieze F.W., Hardy J., Goate A., Owen M., Williams J. Increased familial risk and genomewide significant linkage for Alzheimer's disease with psychosis. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2007, 144B:841-848.
13. Hollingworth P., Sweet R., Sims R., Harold D., Russo G., Abraham R., Stretton A., Jones N., Gerrish A., Chapman J., Ivanov D., Moskvina V., Lovestone S., Priotsi P., Lupton M., Brayne C., Gill M., Lawlor B., Lynch A., Craig D., McGuinness B., Johnston J., Holmes C., Livingston G., Bass N.J., Gurling H., McQuillin A., Holmans P., Jones L., Devlin B., Klei L., Barmada M.M., Demirci F.Y., Dekosky S.T., Lopez O.L., Passmore P., Owen M.J., O'Donovan M.C., Mayeux R., Kamboh M.I., Williams J. Genome-wide association study of Alzheimer's disease with psychotic symptoms. Mol. Psychiatry 2012.
14. Janocko N.J., Brodersen K.A., Soto-Ortolaza A.I., Ross O.A., Liesinger A.M., Duara R., Graff-Radford N.R., Dickson D.W., Murray M.E. Neuropathologically defined subtypes of Alzheimer's disease differ significantly from neurofibrillary tangle-predominant dementia. Acta Neuropathol. 2012, 124:681-692.
15. Jeste D.V., Wragg R.E., Salmon D.P., Harris M.J., Thal L.J. Cognitive deficits of patients with Alzheimer's disease with and without delusions. Am. J. Psychiatry 1992, 149:184-189.
16. Kimura T., Ono T., Takamatsu J., Yamamoto H., Ikegami K., Kondo A., Hasegawa M., Ihara Y., Miyamoto E., Miyakawa T. Sequential changes of tau-site-specific phosphorylation during development of paired helical filaments. Dementia 1996, 7:177-181.
17. Koppel J., Goldberg T.E., Gordon M.L., Huey E., Davies P., Keehlisen L., Huet S., Christen E., Greenwald B.S. Relationships between Behavioral Syndromes and cognitive Domains in Alzheimer disease: the Impact of Mood and psychosis. Am. J. Geriatr. Psychiatry 2012, 20:994-1000.
18. Koppel J., Sunday S., Buthorn J., Goldberg T., Davies P., Greenwald B. Elevated CSF tau is associated with psychosis in Alzheimer's disease. Am. J. Psychiatry 2013, 170:1212-1213.
19. Koppel J., Sunday S., Goldberg T., Davies P., Christen E., Greenwald B.S. Psychosis in Alzheimer's disease is associated with frontal Metabolic Impairment and Accelerated decline in Working Memory: Findings from the Alzheimer's disease Neuroimaging Initiative. The American Journal for Geriatric Psychiatry 2013, Epub ahead of print.
20. Leroi I., Voulgari A., Breitner J.C., Lyketsos C.G. The epidemiology of psychosis in dementia. Am. J. Geriatr. Psychiatry 2003, 11:83-91.
21. Lopez O.L., Becker J.T., Chang Y.F., Sweet R.A., Aizenstein H., Snitz B., Saxton J., McDade E., Kamboh M.I., DeKosky S.T., Reynolds C.F., Klunk W.E. The long-term effects of conventional and atypical antipsychotics in patients with probable Alzheimer's disease. Am. J. Psychiatry 2013, 170:1051-1058.
22. Magi R., Lindgren C.M., Morris A.P. Meta-analysis of sex-specific genome-wide association studies. Genet. Epidemiol. 2010, 34:846-853.
23. McKeith I.G. Consensus guidelines for the clinical and pathologic diagnosis of dementia with Lewy bodies (DLB): report of the Consortium on DLB International Workshop. J. Alzheimers Dis. 2006, 9(3 Suppl):417-423.
24. McKeith I.G., Galasko D., Kosaka K., Perry E.K., Dickson D.W., Hansen L.A., Salmon D.P., Lowe J., Mirra S.S., Byrne E.J., Lennox G., Quinn N.P., Edwardson J.A., Ince P.G., Bergeron C., Burns A., Miller B.L., Lovestone S., Collerton D., Jansen E.N., Ballard C., de Vos R.A., Wilcock G.K., Jellinger K.A., Perry R.H. Consensus guidelines for the clinical and pathologic diagnosis of dementia with Lewy bodies (DLB): report of the consortium on DLB international workshop. Neurology 1996, 47:1113-1124.
25. Mirra S.S., Heyman A., McKeel D., Sumi S.M., Crain B.J., Brownlee L.M., Vogel F.S., Hughes J.P., van Belle G., Berg L. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 1991, 41:479-486.
26. Mondragon-Rodriguez S., Basurto-Islas G., Santa-Maria I., Mena R., Binder L.I., Avila J., Smith M.A., Perry G., Garcia-Sierra F. Cleavage and conformational changes of tau protein follow phosphorylation during Alzheimer's disease. Int. J. Exp. Pathol. 2008, 89:81-90.
27. Mondragon-Rodriguez S., Perry G., Luna-Munoz J., Acevedo-Aquino M., Williams S. Phosphorylation of tau protein at sites Ser is one of the earliest events in Alzheimer's disease and Down syndrome. Neuropathol. Appl. Neurobiol 2013.
28. Moran E.K., Becker J.A., Satlin A., Lyoo I.K., Fischman A.J., Johnson K.A. Psychosis of Alzheimer's disease: Gender differences in regional perfusion. Neurobiol. Aging 2008, 29:1218-1225.
29. Murray P.S., Kirkwood C.M., Gray M.C., Fish K.N., Ikonomovic M.D., Hamilton R.L., Kofler J.K., Klunk W.E., Lopez O.L., Sweet R.A. Hyperphosphorylated tau is Elevated in Alzheimer's disease with psychosis. J. Alzheimers Dis 2013.
30. Murray P.S., Kumar S., Demichele-Sweet M.A., Sweet R.A. Psychosis in Alzheimer's disease. Biol. Psychiatry 2013.
31. Murray PS, Kirkwood CM, Gray MC, Ikonomovic MD, Paljug WR, Abrahamson EE, Henteleff RA, Hamilton RL, Kofler JK, Klunk WE, Lopez OL, Penzes P, Sweet RA. Beta-Amyloid 42/40 ratio and kalirin expression in Alzheimer disease with psychosis. Neurobiol. Aging 33, 2807-2816.
32. Paulsen J.S., Salmon D.P., Thal L.J., Romero R., Weisstein-Jenkins C., Galasko D., Hofstetter C.R., Thomas R., Grant I., Jeste D.V. Incidence of and risk factors for hallucinations and delusions in patients with probable AD. Neurology 2000, 54:1965-1971.
33. Rockwell E., Krull A.J., Dimsdale J., Jeste D.V. Late-onset psychosis with somatic delusions. Psychosomatics 1994, 35:66-72.
34. Ropacki S.A., Jeste D.V. Epidemiology of and risk factors for psychosis of Alzheimer's disease: a review of 55 studies published from 1990 to 2003. Am. J. Psychiatry 2005, 162:2022-2030.
35. Scarmeas N., Brandt J., Albert M., Hadjigeorgiou G., Papadimitriou A., Dubois B., Sarazin M., Devanand D., Honig L., Marder K., Bell K., Wegesin D., Blacker D., Stern Y. Delusions and hallucinations are associated with worse outcome in Alzheimer disease. Arch. Neurol. 2005, 62:1601-1608.
36. Schneider L.S., Dagerman K.S. Psychosis of Alzheimer's disease: clinical characteristics and history. J. Psychiatr. Res. 2004, 38:105-111.
37. Schneider L.S., Dagerman K., Insel P.S. Efficacy and adverse effects of atypical antipsychotics for dementia: meta-analysis of randomized, placebo-controlled trials. Am. J. Geriatr. Psychiatry 2006, 14:191-210.
38. Sultzer D.L., Brown C.V., Mandelkern M.A., Mahler M.E., Mendez M.F., Chen S.T., Cummings J.L. Delusional thoughts and regional frontal/temporal cortex metabolism in Alzheimer's disease. Am. J. Psychiatry 2003, 160:341-349.
39. Sweet R.A., Hamilton R.L., Lopez O.L., Klunk W.E., Wisniewski S.R., Kaufer D.I., Healy M.T., DeKosky S.T. Psychotic symptoms in Alzheimer's disease are not associated with more severe neuropathologic features. Int. Psychogeriatr. 2000, 12:547-558.
40. Sweet R.A., Hamilton R.L., Healy M.T., Wisniewski S.R., Henteleff R., Pollock B.G., Lewis D.A., DeKosky S.T. Alterations of striatal dopamine receptor binding in Alzheimer disease are associated with Lewy body pathology and antemortem psychosis. Arch. Neurol. 2001, 58:466-472.
41. Sweet R.A., Nimgaonkar V.L., Devlin B., Lopez O.L., DeKosky S.T. Increased familial risk of the psychotic phenotype of Alzheimer disease. Neurology 2002, 58:907-911.
42. Sweet R.A., Bennett D.A., Graff-Radford N.R., Mayeux R. Assessment and familial aggregation of psychosis in Alzheimer's disease from the National Institute on Aging Late Onset Alzheimer's Disease Family Study. Brain 2010, 133(Pt 4):1155-1162.
43. Sweet R.A., Seltman H., Emanuel J.E., Lopez O.L., Becker J.T., Bis J.C., Weamer E.A., DeMichele-Sweet M.A., Kuller L.H. Effect of Alzheimer's disease risk genes on trajectories of cognitive function in the Cardiovascular Health Study. Am. J. Psychiatry 2012, 169:954-962.
44. Tariot P.N., Mack J.L., Patterson M.B., Edland S.D., Weiner M.F., Fillenbaum G., Blazina L., Teri L., Rubin E., Mortimer J.A., et al. The Behavior Rating Scale for Dementia of the Consortium to Establish a Registry for Alzheimer's Disease. The Behavioral Pathology Committee of the Consortium to Establish a Registry for Alzheimer's Disease. Am. J. Psychiatry 1995, 152:1349-1357.
45. Tiraboschi P., Salmon D.P., Hansen L.A., Hofstetter R.C., Thal L.J., Corey-Bloom J. What best differentiates Lewy body from Alzheimer's disease in early-stage dementia?. Brain 2006, 129(Pt 3):729-735.
46. Vigen C.L., Mack W.J., Keefe R.S., Sano M., Sultzer D.L., Stroup T.S., Dagerman K.S., Hsiao J.K., Lebowitz B.D., Lyketsos C.G., Tariot P.N., Zheng L., Schneider L.S. Cognitive effects of atypical antipsychotic medications in patients with Alzheimer's disease: outcomes from CATIE-AD. Am. J. Psychiatry 2011, 168:831-839.
47. Weamer E.A., Emanuel J.E., Varon D., Miyahara S., Wilkosz P.A., Lopez O.L., Dekosky S.T., Sweet R.A. The relationship of excess cognitive impairment in MCI and early Alzheimer's disease to the subsequent emergence of psychosis. Int. Psychogeriatr. 2009, 21:78-85.
48. Whitehead D., Tunnard C., Hurt C., Wahlund L.O., Mecocci P., Tsolaki M., Vellas B., Spenger C., Kloszewska I., Soininen H., Cromb D., Lovestone S., Simmons A. Frontotemporal atrophy associated with paranoid delusions in women with Alzheimer's disease. Int. Psychogeriatr. 2012, 24:99-107.
49. Wilkosz P.A., Seltman H.J., Devlin B., Weamer E.A., Lopez O.L., DeKosky S.T., Sweet R.A. Trajectories of cognitive decline in Alzheimer's disease. Int. Psychogeriatr. 2010, 22:281-290.
50. Wilson R.S., Krueger K.R., Kamenetsky J.M., Tang Y., Gilley D.W., Bennett D.A., Evans D.A. Hallucinations and mortality in Alzheimer disease. Am. J.Geriatr. Psychiatry 2005, 13:984-990.
51. Yamamoto T., Hirano A. A comparative study of modified Bielschowsky, Bodian and thioflavin S stains on Alzheimer's neurofibrillary tangles. Neuropathol. Appl. Neurobiol. 1986, 12:3-9.
52. Zubenko G.S., Moossy J., Martinez A.J., Rao G., Claassen D., Rosen J., Kopp U. Neuropathologic and neurochemical correlates of psychosis in primary dementia. Arch. Neurol. 1991, 48:619-624.