The dorsal raphe nucleus shows phospho-tau neurofibrillary changes before the transentorhinal region in Alzheimer̈s disease. A precocious onset?

Neuropathology and Applied Neurobiology

Volumn 35, Issue 4, 2009, Pages 406-416

  Grinberg, L T ^a,d,e   Rub U ^f   Ferretti, R E L ^a,c   Nitrini, R ^b   Farfel, J M ^a,c   Polichiso, L ^a,d   Gierga, K ^g   Jacob Filho, W ^c   Heinsen, H ^e  

^a Necropsy Sector   (Brazil)

^b Neurology Department   (Brazil)

^c Division of Geriatrics   (Brazil)

^d HOSPITAL ISRAELITA ALBERT EINSTEIN   (Brazil)

^e UNIVERSITY OF WÜRZBURG   (Germany)

^f GOETHE UNIVERSITY   (Germany)

^g HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Alzheimer's disease; Braak and braak staging; Brainstem; Cytoskeletal pathology; Raphe nuclei; Tau protein

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID BETA PROTEIN; TAR DNA BINDING PROTEIN; TAU PROTEIN; UBIQUITIN; UBIQUITIN 1; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ARTICLE; BRAAK AND BRAAK STAGING; BRAZIL; CYTOSKELETON; DORSAL RAPHE NUCLEUS; DORSAL RAPHE NUCLEUS SUPRATROCHLEAR SUBNUCLEUS; ENTORHINAL CORTEX; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; NEUROFIBRILLARY TANGLE; NEUROPIL THREAD; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; STAGING; TRANSENTORHINAL CORTEX; AGED; CYTOLOGY; DISEASE COURSE; EDUCATION; FEMALE; HOSPITALIZATION; MAJOR DEPRESSION; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY; PHOSPHORYLATION; RAPHE NUCLEUS;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; DEPRESSIVE DISORDER, MAJOR; DISEASE PROGRESSION; EDUCATION; ENTORHINAL CORTEX; FEMALE; HUMANS; MALE; MIDDLE AGED; NEUROFIBRILLARY TANGLES; PHOSPHORYLATION; RAPHE NUCLEI; SEVERITY OF ILLNESS INDEX; TAU PROTEINS;

EID: 67649945522     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/j.1365-2990.2008.00997.x     Document Type: Article

References (81)

1. Hyman BT, West HL, Rebeck GW, Lai F, Mann DM. Neuropathological changes in Down's syndrome hippocampal formation. Effect of age and apolipoprotein E genotype. Arch Neurol 1995 52 : 373 8
2. Gosche KM, Mortimer JA, Smith CD, Markesbery WR, Snowdon DA. Hippocampal volume as an index of Alzheimer neuropathology - findings from the Nun Study. Neurology 2002 58 : 1476 82
3. Selkoe DJ. Alzheimer's disease results from the cerebral accumulation and cytotoxicity of amyloid beta-protein. J Alzheimers Dis 2001 3 : 75 80
4. Braak H, Alafuzoff I, Arzberger T, Kretzschmar H, Del Tredici K. Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol 2006 112 : 389 404 (Pubitemid 44469160)
5. Thal DR, Rüb U, Orantes M, Braak H. Phases of Aβ-deposition in the human brain and its relevance for the development of AD. Neurology 2002 58 : 1791 800
6. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991 82 : 239 59
7. De Lacoste MC, White CL 3rd. The role of cortical connectivity in Alzheimer's disease pathogenesis: a review and model system. Neurobiol Ageing 1993 14 : 1 16
8. Appel SH. A unifying hypothesis for the cause of amyotrophic lateral sclerosis, parkinsonism, and Alzheimer disease. Ann Neurol 1981 10 : 499 505 (Pubitemid 12242175)
9. Saper CB, Wainer BH, German DC. Axonal and transneuronal transport in the transmission of neurological disease: potential role in system degenerations, including Alzheimer's disease. Neuroscience 1987 23 : 389 98
10. German DC, White CL, Sparkman DR. Alzheimer's disease: neurofibrillary tangles in nuclei that project to the cerebral cortex. Neuroscience 1987 21 : 305 12
11. Jorm AF. Is depression a risk factor for dementia or cognitive decline? A review. Gerontology 2000 46 : 219 27
12. Esiri MM. The basis for behavioural disturbances in dementia. J Neurol Neurosurg Psychiatry 1996 61 : 127 30
13. Kokmen E, Beard CM, Chandra V, Offord KP, Schoenberg BS, Ballard DJ. Clinical risk factors for Alzheimer's disease: a population-based case-control study. Neurology 1991 41 : 1393 7
14. Chen CP, Eastwood SL, Hope T, McDonald B, Francis PT, Esiri MM. Immunocytochemical study of the dorsal and median raphe nuclei in patients with Alzheimer's disease prospectively assessed for behavioural changes. Neuropathol Appl Neurobiol 2000 26 : 347 55
15. Rub U, Del Tredici K, Schultz C, Thal DR, Braak E, Braak H. The evolution of Alzheimer's disease-related cytoskeletal pathology in the human raphe nuclei. Neuropathol Appl Neurobiol 2000 26 : 553 67
16. Descarries L, Berthelet F, Garcia S, Beaudet A. Dopaminergic projection from nucleus raphe dorsalis to neostriatum in the rat. J Comp Neurol 1986 249 : 511 20, 484 5
17. Wiklund L, Leger L, Persson M. Monoamine cell distribution in the cat brain stem. A fluorescence histochemical study with quantification of indolaminergic and locus coeruleus cell groups. J Comp Neurol 1981 203 : 613 47
18. Insausti R, Amaral DG, Cowan WM. The entorhinal cortex of the monkey: III. Subcortical afferents. J Comp Neurol 1987 264 : 396 408 (Pubitemid 17150687)
19. Michelsen KA, Schmitz C, Steinbusch HW. The dorsal raphe nucleus - from silver stainings to a role in depression. Brain Res Rev 2007 55 : 329 42
20. Parvizi J, Van Hoesen GW, Damasio A. The selective vulnerability of brainstem nuclei to Alzheimer's disease. Ann Neurol 2001 49 : 53 66 (Pubitemid 32163006)
21. Curcio CA, Kemper T. Nucleus raphe dorsalis in dementia of the Alzheimer type: neurofibrillary changes and neuronal packing density. J Neuropathol Exp Neurol 1984 43 : 359 68
22. Halliday GM, Mccann HL, Pamphlett R, Brooks WS, Creasey H, Mccusker E, Cotton RGH, Broe GA, Harper CG. Brain stem serotonin-synthesizing neurons in Alzheimer's disease - a clinicopathological correlation. Acta Neuropathol 1992 84 : 638 50
23. Mann DM, Yates PO, Marcyniuk B. Monoaminergic neurotransmitter systems in presenile Alzheimer's disease and in senile dementia of Alzheimer type. Clin Neuropathol 1984 3 : 199 205 (Pubitemid 14015453)
24. D'Amato RJ, Zweig RM, Whitehouse PJ, Wenk GL, Singer HS, Mayeux R, Price DL, Snyder SH. Aminergic systems in Alzheimer's disease and Parkinson's disease. Ann Neurol 1987 22 : 229 36
25. Ishii T. Distribution of Alzheimer's neurofibrillary changes in the brainstem and hypothalamus of senile dementia. Acta Neuropathol 1966 6 : 181 7
26. Mann DM, Yates PO, Marcyniuk B. A comparison of nerve cell loss in cortical and subcortical structures in Alzheimer's disease. J Neurol Neurosurg Psychiatry 1986 49 : 310 2
27. Grinberg LT, Ferretti RE, Farfel JM, Leite R, Pasqualucci CA, Rosemberg S, Nitrini R, Saldiva PH, Filho WJ. Brain bank of the Brazilian aging brain study group - a milestone reached and more than 1600 collected brains. Cell Tissue Bank 2007 8 : 151 62
28. Tierney MC, Fisher RH, Lewis AJ, Zorzitto ML, Snow WG, Reid DW, Nieuwstraten P. The NINCDS-ADRDA Work Group criteria for the clinical diagnosis of probable Alzheimer's disease: a clinicopathologic study of 57 cases. Neurology 1988 38 : 359 64
29. McKeith IG, Dickson DW, Lowe J, Emre M, O'Brien JT, Feldman H, Cummings J, Duda JE, Lippa C, Perry EK, Aarsland D, Arai H, Ballard CG, Boeve B, Burn DJ, Costa D, Del Ser T, Dubois B, Galasko D, Gauthier S, Goetz CG, Gomez-Tortosa E, Halliday G, Hansen LA, Hardy J, Iwatsubo T, Kalaria RN, Kaufer D, Kenny RA, Korczyn A, Kosaka K, Lee VMY, Lees A, Litvan I, Londos E, Lopez OL, Minoshima S, Mizuno Y, Molina JA, Mukaetova-Ladinska EB, Pasquier F, Perry RH, Schulz JB, Trojanowski JQ, Yamada M. Diagnosis and management of dementia with Lewy bodies - third report of the DLB consortium. Neurology 2005 65 : 1863 72
30. 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
31. 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 41 : 479 86
32. The National Institute on Aging, Reagan Institute Working Group on Diagnostic Criteria for the Neuropathological Assessment of Alzheimer's Disease. Consensus recommendations for the postmortem diagnosis of Alzheimer's disease. Neurobiol Aging 1997 18 : S1 2
33. Braak H, Ghebremedhin E, Rüb U, Bratzke H, Del Tredici K. Stages in the development of Parkinson's disease-related pathology. Cell Tissue Res 2004 318 : 121 34
34. McKeith IG, Galasko D, Kosaka K, Perry EK, Dickson DW, Hansen LA, Salmon DP, Lowe J, Mirra SS, Byrne EJ, Lennox G, Quinn NP, Edwardson JA, Ince PG, Bergeron C, Burns A, Miller BL, Lovestone S, Collerton D, Jansen EN, Ballard C, de Vos RA, Wilcock GK, Jellinger KA, Perry RH. 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 24
35. Cairns NJ, Bigio EH, Mackenzie IR, Neumann M, Lee VM, Hatanpaa KJ, White CL 3rd., Schneider JA, Grinberg LT, Halliday G, Duyckaerts C, Lowe JS, Holm IE, Tolnay M, Okamoto K, Yokoo H, Murayama S, Woulfe J, Munoz DG, Dickson DW, Ince PG, Trojanowski JQ, Mann DM. Neuropathologic diagnostic and nosologic criteria for frontotemporal lobar degeneration: consensus of the Consortium for Frontotemporal Lobar Degeneration. Acta Neuropathol 2007 114 : 5 22 (Pubitemid 47029055)
36. Braak H On the nuclei of the human brain stem. II. The raphe nuclei Z Zellforsch Mikrosk Anat 1970 107 : 123 41
37. Baker KG, Halliday GM, Hornung JP, Geffen LB, Cotton RG, Tork I. Distribution, morphology and number of monoamine-synthesizing and substance P-containing neurons in the human dorsal raphe nucleus. Neuroscience 1991 42 : 757 75
38. Ohm TG, Heilmann R, Braak H. The human oral raphe system. Architectonics and neuronal types in pigment-Nissl preparations. Anat Embryol 1989 180 : 37 43 (Pubitemid 19166314)
39. Tork I. Anatomy of the serotonergic system. Ann N Y Acad Sci 1990 600 : 9 34
40. Olszewski J, Baxter D. Cytoarchitecture of the Human Brain Stem. Basel : Karger, 1982
41. Dickson DW, Bergeron C, Chin SS, Duyckaerts C, Horoupian D, Ikeda K, Jellinger K, Lantos PL, Lippa CF, Mirra SS, Tabaton M, Vonsattel JP, Wakabayashi K, Litvan I. Office of Rare Diseases neuropathologic criteria for corticobasal degeneration. J Neuropathol Exp Neurol 2002 61 : 935 46
42. Hauw JJ, Daniel SE, Dickson D, Horoupian DS, Jellinger K, Lantos PL, McKee A, Tabaton M, Litvan I. Preliminary NINDS neuropathologic criteria for Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). Neurology 1994 44 : 2015 19
43. Morris JC. The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology 1993 43 : 2412 14
44. Jorm AF. A short form of the Informant Questionnaire on Cognitive Decline in the Elderly (IQCODE): development and cross-validation. Psychol Med 1994 24 : 145 53
45. Cummings JL, Mega M, Gray K, Rosenberg-Thompson S, Carusi DA, Gornbein J. The Neuropsychiatric Inventory: comprehensive assessment of psychopathology in dementia. Neurology 1994 44 : 2308 14
46. Tanner CM, Ben-Shlomo Y. Epidemiology of Parkinson's disease. Adv Neurol 1999 80 : 153 9
47. Hornung JP. The human raphe nuclei and the serotonergic system. J Chem Neuroanat 2003 26 : 331 43
48. Sassin I, Schultz C, Thal DR, Rüb U, Arai K, Braak E, Braak H. Evolution of Alzheimer's disease-related cytoskeletal changes in the basal nucleus of Meynert. Acta Neuropathol 2000 100 : 259 69
49. Parvizi J, Van Hoesen GW, Damasio A. Severe pathological changes of parabrachial nucleus in Alzheimer's disease. Neuroreport 1998 9 : 4151 4
50. Rüb U, Del Tredici K, Schultz C, Thal DR, Braak E, Braak H. The autonomic higher order processing nuclei of the lower brain stem are among the early targets of the Alzheimer's disease-related cytoskeletal pathology. Acta Neuropathol 2001 101 : 555 64
51. Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 2003 24 : 197 211 (Pubitemid 36007810)
52. Braak H, Rüb U, Gai WP, Del Tredici K. Idiopathic Parkinson's disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen. J Neural Transm 2003 110 : 517 36
53. Rossor MN. Parkinson's disease and Alzheimer's disease as disorders of the isodendritic core. Br Med J 1981 283 : 1588 90
54. Castellani RJ, Lee HG, Zhu XW, Nunomura A, Perry G, Smith MA. Neuropathology of Alzheimer disease: pathognomonic but not pathogenic. Acta Neuropathol 2006 111 : 503 9
55. Zhu X, Avila J, Perry G, Smith MA. Treating the lesions, not the disease. Am J Pathol 2007 170 : 1457 9
56. Spillantini MG, Murrell JR, Goedert M, Farlow M, Klug A, Ghetti B. Mutations in the tau gene (MAPT) in FTDP-17: the family with Multiple System Tauopathy with Presenile Dementia (MSTD). J Alzheimers Dis 2006 9 : 373 80
57. Foster NL, Wilhelmsen K, Sima AA, Jones MZ, D'Amato CJ, Gilman S. Frontotemporal dementia and parkinsonism linked to chromosome 17: a consensus conference. Conference participants. Ann Neurol 1997 41 : 706 15
58. Berg L, McKeel DW Jr., Miller, JP, Storandt M, Rubin EH, Morris JC, Baty J, Coats M, Norton J, Goate AM, Price JL, Gearing M, Mirra SS, Saunders AM. Clinicopathologic studies in cognitively healthy aging and Alzheimer's disease: relation of histologic markers to dementia severity, age, sex, and apolipoprotein E genotype. Arch Neurol 1998 55 : 326 35
59. Giannakopoulos P, Gold G, Kovari E, von Gunten A, Imhof A, Bouras C, Hof PR. Assessing the cognitive impact of Alzheimer disease pathology and vascular burden in the aging brain: the Geneva experience. Acta Neuropathol 2007 113 : 1 12 (Pubitemid 44782924)
60. Duyckaerts C. Looking for the link between plaques and tangles. Neurobiol Aging 2004 25 : 735 9
61. Riley KP, Snowdon DA, Desrosiers MF, Markesbery WR. Early life linguistic ability, late life cognitive function, and neuropathology: findings from the Nun Study. Neurobiol Aging 2005 26 : 341 7
62. Supprian T, Reiche W, Schmitz B, Grunwald I, Backens M, Hofmann E, Georg T, Falkai P, Reith W. MRI of the brainstern in patients with major depression, bipolar affective disorder and normal controls. Psychiatry Res Neuroimaging 2004 131 : 269 76
63. Walter U, Prudente-Morrissey L, Herpertz SC, Benecke R, Hoeppner J. Relationship of brainstem raphe echogenicity and clinical findings in depressive states. Psychiatry Res 2007 155 : 67 73 (Pubitemid 46561250)
64. Nagae-Poetscher LM, Jiang HY, Wakana S, Golay X, van Zijl PCM, Mori S. High-resolution diffusion tensor imaging of the brain stem at 3 T. Am J Neuroradiol 2004 25 : 1325 30
65. Habas C, Cabanis EA. Anatomical parcellation of the brainstem and cerebellar white matter: a preliminary probabilistic tractography study at 3 T. Neuroradiology 2007 49 : 849 63
66. Stieltjes B, Kaufmann WE, van Zijl PC, Fredericksen K, Pearlson GD, Solaiyappan M, Mori S. Diffusion tensor imaging and axonal tracking in the human brainstem. Neuroimage 2001 14 : 723 35
67. Small GW, Kepe V, Ercoli LM, Siddarth P, Bookheimer SY, Miller KJ, Lavretsky H, Burggren AC, Cole GM, Vinters HV, Thompson PM, Huang SC, Satyamurthy N, Phelps ME, Barrio JR. PET of brain amyloid and tau in mild cognitive impairment. N Engl J Med 2006 355 : 2652 63
68. Yamamoto T, Hirano A. Nucleus raphe dorsalis in Alzheimer's disease: neurofibrillary tangles and loss of large neurons. Ann Neurol 1985 17 : 573 7
69. Zweig RM, Ross CA, Hedreen JC, Steele C, Cardillo JE, Whitehouse PJ, Folstein MF, Price DL. The neuropathology of aminergic nuclei in Alzheimer's disease. Ann Neurol 1988 24 : 233 42
70. Khachaturian ZS. Diagnosis of Alzheimer's disease. Arch Neurol 1985 42 : 1097 105
71. Bancher C, Braak H, Fischer P, Jellinger KA. Neuropathological staging of Alzheimer lesions and intellectual status in Alzheimer's and Parkinson's disease patients. Neurosci Lett 1993 162 : 179 82
72. Bancher C, Jellinger K, Lassmann H, Fischer P, Leblhuber F. Correlations between mental state and quantitative neuropathology in the Vienna longitudinal study on dementia. Eur Arch Psychiatry Clin Neurosci 1996 246 : 137 46
73. Azmitia EC, Whitaker-Azmitia PM. Awakening the sleeping giant: anatomy and plasticity of the brain serotonergic system. J Clin Psychiatry 1991 52 (Suppl. 4 16
74. Chan-Palay V, Asan E. Alterations in catecholamine neurons of the locus coeruleus in senile dementia of the Alzheimer type and in Parkinson's disease with and without depression. J Comp Neurol 1989 287 : 373 92
75. Heinsen H, Arzberger T, Schmitz C. Celloidin mounting (embedding without infiltration) - a new, simple and reliable method for producing serial sections of high thickness through complete human brains and its application to stereological and immunohistochemical investigations. J Chem Neuroanat 2000 20 : 49 59 (Pubitemid 30802255)
76. Del-Ben CM, Rodrigues CR, Zuardi AW. Reliability of the Portuguese version of the structured clinical interview for DSM-III-R (SCID) in a Brazilian sample of psychiatric outpatients. Braz J Med Biol Res 1996 29 : 1675 82
77. Spitzer RL, Williams JB, Gibbon M, First MB. The Structured Clinical Interview for DSM-III-R (SCID). I: history, rationale, and description. Arch Gen Psychiatry 1992 49 : 624 9
78. Katz S, Ford AB, Moskowitz RW, Jackson BA, Jaffe MW. Studies of illness in the aged. The index of Adl: a standardized measure of biological and psychosocial function. JAMA 1963 185 : 914 19
79. Lawton MP, Brody EM. Assessment of older people: self-maintaining and instrumental activities of daily living. Gerontologist 1969 9 : 179 86
80. Tanner CM, Chen B, Wang W, Peng M, Liu Z, Liang X, Kao LC, Gilley DW, Goetz CG, Schoenberg BS. Environmental factors and Parkinson's disease: a case-control study in China. Neurology 1989 39 : 660 4
81. Almeida PM, Wickerhauser H. [O critério ABA/ABIPEME - em busca de uma solução. Um estudo e uma proposta submetidos à ABA - Associação Brasileira de Anunciantes e ABIPEME]. São Paulo : Associação Brasileira dos Institutos de Pesquisa de Mercado, 1991