Synaptic changes in frontotemporal lobar degeneration: Correlation with MAPT haplotype and APOE genotype

Neuropathology and Applied Neurobiology

Volumn 37, Issue 4, 2011, Pages 366-380

  Connelly, S J ^a   Mukaetova Ladinska, E B ^a   Abdul All, Z ^a   da Silva, J Alves ^a,b,c   Brayne, C ^b   Honer, W G ^d   Mann, D M A ^e  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

APOE genotype; Frontotemporal lobar dementia; MAPT haplotype; SNAP 25; synaptophysin

Indexed keywords

SYNAPTOPHYSIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; APOLIPOPROTEIN E; MAPT PROTEIN, HUMAN; SNAP25 PROTEIN, HUMAN; TAU PROTEIN;

ADULT; AGED; ALLELE; ALZHEIMER DISEASE; APOLIPOPROTEIN E GENE; ARTICLE; BRAIN ATROPHY; CLINICAL ARTICLE; CONTROLLED STUDY; FAMILY HISTORY; FEMALE; FRONTOTEMPORAL DEMENTIA; GENE; GENOTYPE; HAPLOTYPE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MAPT GENE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RISK FACTOR; SEX DIFFERENCE; SYNAPSE; UPREGULATION; BIOSYNTHESIS; BRAIN; GENE EXPRESSION; GENETIC PREDISPOSITION; GENETICS; METABOLISM; MIDDLE AGED; PATHOLOGY; PHYSIOLOGY;

APOE GENOTYPE; FRONTOTEMPORAL LOBAR DEMENTIA; HAPLOTYPES; SNAP-25; SYNAPTOPHYSIN;

NEURODEGENERATIVE DISEASES;

ADULT; AGED; AGED, 80 AND OVER; APOLIPOPROTEINS E; BRAIN; FEMALE; FRONTOTEMPORAL LOBAR DEGENERATION; GENE EXPRESSION; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HAPLOTYPES; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; SYNAPSES; SYNAPTOPHYSIN; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25; TAU PROTEINS;

EID: 79959428085     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/j.1365-2990.2010.01150.x     Document Type: Article

References (62)

1. Neary D, Snowden JS, Gustafson L, Passant U, Stuss D, Black S, Freedman M, Kertesz A, Robert PH, Albert M, Boone K, Miller BL, Cummings J, Benson DF. Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology 1998; 51: 1546-54
2. Rosso SM, Donker Kaat L, Baks T, Joosse M, de Koning I, Pijnenburg Y, de Jong D, Dooijes D, Kamphorst W, Ravid R, Niermeijer MF, Verheij F, Kremer HP, Scheltens P, van Duijn CM, Heutink P, van Swieten JC. Frontotemporal dementia in the Netherlands: patient characteristics and prevalence estimates from a population-based study. Brain 2003; 126: 2016-22
3. Snowden JS, Neary D, Mann DM. Frontotemporal dementia. Br J Psychiatry 2002; 180: 140-3
4. Haugarvoll K, Wszolek ZK, Hutton M. The genetics of frontotemporal dementia. Neurol Clin 2007; 25: 697-715
5. Rabinovici GD, Miller BL. Frontotemporal lobar degeneration: epidemiology, pathophysiology, diagmosis and management. CNS Drugs 2010; 24: 375-98
6. Galimberti D, Scarpini E. Genetics and biology of Alzheimer's disease and frontotemporal lobar degeneration. Int J Clin Exp Med 2010; 3: 129-43
7. Taylor JP, Hardy J, Fischbeck KH. Toxic proteins in neurodegenerative disease. Science 2002; 296: 1991-5
8. Arai T, Hasegawa M, Akiyama H, Ikeda K, Nonaka T, Mori H, Mann D, Tsuchiya K, Yoshida M, Hashizume Y, Oda T. TDP-43 is a component of ubiquitin-positive taunegative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem Biophys Res Commun 2006; 351: 602-11
9. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, Bruce J, Schuck T, Grossman M, Clark CM, McCluskey LF, Miller BL, Masliah E, Mackenzie IR, Feldman H, Feiden W, Kretzschmar HA, Trojanowski JQ, Lee VM. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006; 314: 130-3
10. Urwin H, Josephs KA, Rohrer JD, Mackenzie IR, Neumann M, Authier A, Seelaar H, Van Swieten JC, Brown JM, Johannsen P, Nielsen JE, Holm IE; FReJA Consortium, Dickson DW, Rademakers R, Graff-Radford NR, Parisi JE, Petersen RC, Hatanpaa KJ, White CL 3rd, Weiner MF, Geser F, Van Deerlin VM, Trojanowski JQ, Miller BL, Seeley WW, van der Zee J, Kumar-Singh S, Engelborghs S, De Deyn PP, Van Broeckhoven C, Bigio EH, Deng HX, Halliday GM, Kril JJ, Munoz DG, Mann DM, Pickering-Brown SM, Doodeman V, Adamson G, Ghazi-Noori S, Fisher EM, Holton JL, Revesz T, Rossor MN, Collinge J, Mead S, Isaacs AM. FUS pathology defines the majority of tau- and TDP-43-negative frontotemporal lobar degeneration. Acta Neuropathol 2010; 120: 33-41
11. Mackenzie IR, Neumann M, Biogio EH, Cairns NJ, Alafuzoff I, Kril J, Kovacs GG, Ghetti B, Halliday G, Holm IE, Ince PG, Kamphorst W, Revesz T, Rosemuller AJ, Kumar- Singh S, Akiyama H, Baborie A, Spina S, Dickson DW, Trojanowski JW, Mann D. Nomenclature for neuropathologic subtypes of frontotemporal lobar degeneration: consensus recommendations. Acta Neuropathol 2009; 117: 15-18
12. del Alonso CA, Li B, Grundke-Iqbal I, Iqbal K. Mechanism of tau-induced neurodegeneration in Alzheimer disease and related tauopathies. Curr Alzheimer Res 2008; 5: 375-84
13. Stefansson H, Helgason A, Thorleifsson G, Steinthorsdottir V, Masson G, Barnard J, Baker A, Jonasdottir A, Ingason A, Gudnadottir VG, Desnica N, Hicks A, Gylfason A, Gudbjartsson DF, Jonsdottir GM, Sainz J, Agnarsson K, Birgisdottir B, Ghosh S, Olafsdottir A, Cazier JB, Kristjansson K, Frigge ML, Thorgeirsson TE, Gulcher JR, Kong A, Stefansson K. A common inversion under selection in Europeans. Nat Genet 2005; 37: 129-37
14. Verpillat P, Camuzat A, Hannequin D, Thomas-Anterion C, Puel M, Belliard S, Dubois B, Didic M, Michel BF, Lacomblez L, Moreaud O, Sellal F, Golfier V, Campion D, Clerget-Darpoux F, Brice A. Association between the extended tau haplotype and frontotemporal dementia. Arch Neurol 2002; 59: 935-9
15. Kwok JB, Teber ET, Loy C, Hallupp M, Nicholson G, Mellick GD, Buchanan DD, Silburn PA, Schofield PR. Tau haplotypes regulate transcription and are associated with Parkinson's disease. Ann Neurol 2004; 55: 329-34
16. Bird TD, Nochlin D, Poorkaj P, Cherrier M, Kaye J, Payami H, Peskind E, Lampe TH, Nemens E, Boyer PJ, Schellenberg GD. A clinical pathological comparison of three families with frontotemporal dementia and identical mutations in the tau gene (P301L). Brain 1999; 122: 741-56
17. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, Roses AD, Haines JL, Pericak- Vance MA. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 1993; 261: 921-3
18. Short RA, Graff-Radford NR, Adamson J, Baker M, Hutton M. Differences in tau and apolipoprotein E polymorphism frequencies in sporadic frontotemporal lobar degeneration syndromes. Arch Neurol 2002; 59: 611-15
19. Acciarri A, Masullo C, Bizzarro A, Valenza A, Quaranta D, Marra C, Tiziano FD, Brahe C, Seripa D, Matera MG, Fazio VM, Gainotti G, Daniele A. APOE epsilon-2- epsilon-4 genotype is a possible risk factor for primary progressive aphasia. Ann Neurol 2006; 59: 436-7
20. Verpillat P, Camuzat A, Hannequin D, Thomas-Anterion C, Puel M, Belliard S, Dubois B, Didic M, Lacomblez L, Moreaud O, Golfier V, Campion D, Brice A, Clerget- Darpoux F. Apolipoprotein E gene in frontotemporal dementia: an association study and meta-analysis. Eur J Hum Genet 2002; 10: 399-405
21. Morrow JA, Hatters DM, Lu B, Höchtl P, Oberg KA, Rupp B, Karl H. Apolipoprotein E4 forms a molten globule: a potential basis for its association with disease. J Biol Chem 2002; 277: 50380-5
22. Mahley RW, Weisgraber KH, Huang Y. Apolipoprotein E4: a causative factor and therapeutic target in neuropathology, including Alzheimer's. Proc Natl Acad Sci USA 2006; 103: 5644-51
23. Mukaetova-Ladinska EB, Garcia-Siera F, Hurt J, Gertz HJ, Xuereb J, Hills R, Brayne C, Huppert FA, Paykel ES, McGee M, Jakes R, Honer WG, Harrington CR, Wischik CM. Staging of cytoskeletal and beta-amyloid changes in human isocortex reveals biphasic synaptic protein response during progression of Alzheimers. Am J Pathol 2000; 157: 623-36
24. Mukaetova-Ladinska EB, Hurt J, Honer WG, Harrington CR, Wischik CM. Loss of synaptic but not cytoskeletal proteins in the cerebellum of chronic schizophrenics. Neurosci Lett 2002; 317: 161-5
25. Downes EC, Robson J, Grailly E, Abdel-All Z, Xuereb J, Brayne C, Holland A, Honer WG, Mukaetova-Ladinska EB. Loss of synaptophysin and synaptosomal-associated protein 25-kDa (SNAP-25) in elderly Down syndrome individuals. Neuropathol Appl Neurobiol 2008; 34: 12-22
26. Shi J, Shaw CL, Du Plessis D, Richardson AM, Bailey KL, Julien C, Stopford C, Thompson J, Varma A, Craufurd D, Tian J, Pickering-Brown S, Neary D, Snowden JS, Mann DM. Histopathological changes underlying frontotemporal lobar degeneration with clinicopathological correlation. Acta Neuropathol (Berl) 2005; 110: 501-12
27. Brayne C, Spiegelhalter DJ, Dufouil C, Chi LY, Dening TR, Paykel ES, O'Connor DW, Ahmed A, McGee MA, Huppert FA. Estimating the true extent of cognitive decline in the old old. J Am Geriatr Soc 1999; 47: 1283-8
28. Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brownlee LM, Vogel FS, Hughes JP, 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; 4: 479-86
29. The National Institute on Aging, and Reagan Institute Working Group on Diagnostic Criteria for the Neuropathological Assessment of Alzheimer's Disease. Consensus recommendations for the post-mortem Diagnosis of Alzheimer's disease. Neurobiol Aging 1997; 18: S1-2
30. Minger SL, Honer WG, Esiri MM, McDonald B, Keene J, Nicoll JA, Carter J, Hope T, Francis PT. Synaptic pathology in prefrontal cortex is present only with severe dementia in Alzheimer disease. J Neuropathol Exp Neurol 2001; 60: 929-36
31. Mukaetova-Ladinska EB, Xuereb JH, Garcia-Sierra F, Hurt J, Gertz HJ, Hills R, Brayne C, Huppert FA, Paykel ES, McGee MA, Jakes R, HonerWG, Harrington CR, Wischik CM. Lewy body variant of Alzheimer's disease: selective neocortical loss of t-SNARE proteins and loss of MAP2 and alpha-synuclein in medial temporal lobe. Scientific- WorldJournal 2009; 9: 1463-75
32. Trimble WS, Scheller RH. Molecular biology of synaptic vesicle-associated proteins. Trends Neurosci 1988; 11: 241-2
33. Honer WG. Pathology of presynaptic proteins in Alzheimer's disease. more than simple loss of terminals. Neurobiol Aging 2003; 24: 1047-62
34. Greber S, Lubec G, Cairns N, Fountoulakis M. Decreased levels of synaptosomal associated protein 25 in the brain of patients with Down syndrome and Alzheimer's disease. Electrophoresis 1999; 20: 928-34
35. Honer WG, Kaufmann CA, Kleinman JE, Casanova MF, Davies P. Monoclonal antibodies to study the brain in Schizophrenia. Brain Res 1989; 500: 379-83
36. Perri R, Koch G, Carlesimo GA, Serra L, Fadda L, Pasqualetti P, Pattenati C, Caltagirone C. Alzheimer's disease and frontal variant of frontotemporal dementia - a very brief battery for cognitive and behavioural distinction. J Neurol 2005; 252: 1238-44
37. Libon DJ, Xie SX, Moore P, Farmer J, Antani S, McCawley G, Cross K, Grossman M. Patterns of neuropsychological impairment in frontotemporal dementia. Neurology 2007; 68: 369-75
38. Du AT, Schuff N, Kramer JH, Rosen HJ, Gorno-Tempini ML, Rankin K, Miller BL, Weiner MW. Different regional patterns of cortical thinning in Alzheimer's disease and frontotemporal dementia. Brain 2007; 130: 1159-66
39. Kitagaki H, Mori E, Yamaji S, Ishii K, Hirono N, Kobashi S, Hata Y. Frontotemporal dementia and Alzheimer disease: evaluation of cortical atrophy with automated hemispheric surface display generated with MR images. Radiology 1998; 208: 431-9
40. Ferrer I. Neurons and their dendrites in frontotemporal dementia. Dement Geriatr Cogn Disord 1999; 10: 55-6
41. Roberson ED, Hesse JH, Rose KD, Slama H, Johnson JK, Yaffe K, Forman MS, Miller CA, Trojanowski JQ, Kramer JH, Miller BL. Frontotemporal dementia progresses to death faster than Alzheimer disease. Neurology 2005; 65: 719-25
42. Edelmann L, Hanson PI, Chapman ER, Jahn R. Synaptobrevin binding to synaptophysin: a potential mechanism for controlling the exocytotic fusion machine. EMBO J 1995; 14: 224-31
43. Lipton AM, Cullum CM, Satumtira S, Sontag E, Hynan LS, White CL 3rd, Bigio EH. Contribution of asymmetric synapse loss to lateralizing clinical deficits in frontotemporal dementias. Arch Neurol 2001; 58: 1233-9
44. Clare R, King VG, Wirenfeldt M, Vinters HV. Synapse loss in dementias. J Neurosci Res 2010; 88: 2083-90
45. Bigio EH, Hynan LS, Sontag E, Satumtira S, White CL. Synapse loss is greater in presenile than senile onset Alzheimer disease: implications for the cognitive reserve hypothesis. Neuropathol Appl Neurobiol 2002; 28: 218-27
46. Alder J, Kanki H, Valtorta F, Greengard P, Poo MM. Overexpression of synaptophysin enhances neurotransmitter secretion at Xenopus neuromuscular synapses. J Neurosci 1995; 15: 511-19
47. Siso S, Puig B, Varea R, Vidal E, Acin C, Prinz M, Montrasio F, Badiola J, Aguzzi A, Pumarola M, Ferrer I. Abnormal synaptic protein expression and cell death in murine scrapie. Acta Neuropathol (Berl) 2002; 103: 615-26
48. Ferrer I. Synaptic pathology and cell death in the cerebellum in Creutzfeldt-Jakob disease. Cerebellum 2002; 1: 213-22
49. Yuan J, Yankner BA. Caspase activity sows the seeds of neuronal death. Nat Cell Biol 1999; 1: E44-45
50. Mouser PE, Head E, Kwang-Ho Ha K-H, Rohn TT. Caspase-mediated cleavage of glial fibrillary acidic protein within degenerating astrocytes of the Alzheimer's disease brain. Am J Pathol 2006; 168: 936-46
51. Baba Y, Baker MC, Le Ber I, Brice A, Maeck L, Kohlhase J, Yasuda M, Stoppe G, Bugiani O, Sperfeld AD, Tsuboi Y, Uitti RJ, Farrer MJ, Ghetti B, Hutton ML, Wszolek ZK. Clinical and genetic features of families with frontotemporal dementia and parkinsonism linked to chromosome 17 with a P301S tau mutation. J Neural Transm 2007; 114: 947-50
52. Laws SM, Perneczky R, Drzezga A, Diehl-Schmid J, Ibach B, Bäumi J, Eisele T, Förstl H, Kurz A, Riemenschneider M. Association of the tau haplotype H2 with age at onset and functional alterations of glucose utilization in frontotemporal dementia. Am J Psychiatry 2007; 164: 1577-84
53. Ghidoni R, Signorini S, Barbiero L, Sina E, Cominelli P, Villa A, Benussi L, Binetti G. The H2 MAPT haplotype is associated with familial frontotemporal dementia. Neurobiol Dis 2006; 22: 357-62
54. Borroni B, Yancopoulou D, Tsutsui M, Padovani A, Sawcer SJ, Hodges JR, Spillantini MG. Association between tau H2 haplotype and age at onset in frontotemporal dementia. Arch Neurol 2005; 62: 1419-22
55. Pickering-Brown SM, Richardson AM, Snowden JS, McDonagh AM, Burns A, Braude W, Baker M, Liu WK, Yen SH, Hardy J, Hutton M, Davies Y, Allsop D, Craufurd D, Neary D, Mann DM. Inherited frontotemporal dementia in nine British families associated with intronic mutations in the tau gene. Brain 2002; 125: 732-51
56. Raz N. Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional difference. Neurobiol Aging 2004; 25: 377-96
57. Smith CD. Frontal lobe phosphorus metabolism and neuropsychological function in aging and in Alzheimer's disease. Ann Neurol 1995; 38: 194-201
58. Ott BR, Tate CA, Gordon NM, HeindelWC. Gender differences in the behavioral manifestations of Alzheimer's disease. J Am Geriatr Soc 1996; 44: 583-7
59. Agosta F, Vossel KA, Miller BL, Migliaccio R, Bonasera SJ, Filippi M, Boxer AL, Karydas A, Possin KL, Gorno- Tempini ML. Apolipoprotein E ε4 is associated with disease-specific effects on brain atrophy in Alzheimer's disease and frontotemporal dementia. Proc Natl Acad Sci USA 2009; 106: 2018-22
60. Gustafson L, Abrahamson M, Grubb A, Nilsson K, Fex G. Apolipoprotein-E genotyping in Alzheimer's disease and frontotemporal dementia. Dement Geriatr Cogn Disord 1997; 8: 240-3
61. Pickering-Brown SM, Owen F, Isaacs A, Snowden JS, Varma A, Neary D, Furlong R, Daniel SE, Cairns NJ, Mann DMA. Apolipoprotein E ε4 allele has no effect on age at onset or duration of disease in cases of frontotemporal dementia with Pick- or microvacuolar-type histology. Exp Neurol 2000; 163: 452-6
62. Honer WG, Falkai P, Young C, Wang T, Xie J, Bonner J, Hu L, Boulianne GL, Luo Z, Trimble WS. Cingulate cortex synaptic terminal proteins and neural cell adhesion molecule in schizophrenia. Neuroscience 1997; 78: 99-110