Amyloid-specific T-cells differentiate Alzheimer's disease from Lewy body dementia

Neurobiology of Aging

Volumn 33, Issue 11, 2012, Pages 2599-2611

  Lanuti, Paola ^a   Ciccocioppo, Fausta ^a   Bonanni, Laura ^a   Marchisio, Marco ^a   Lachmann, Raskit ^b   Tabet, Naji ^b,c   Pierdomenico, Laura ^a   Santavenere, Eugenio ^a   Catinella, Virginia ^d   Iacone, Antonio ^d   Thomas, Astrid ^a   Gambi, Domenico ^a   Miscia, Sebastiano ^a   Onofrj, Marco ^a   Kern, Florian ^b  

^a UNIVERSITY OF CHIETI   (Italy)

^b BRIGHTON AND SUSSEX MEDICAL SCHOOL   (United Kingdom)

^c SUSSEX PARTNERSHIP NHS FOUNDATION TRUST   (United Kingdom)

^d ASL Pescara   (Italy)

Author keywords

AD; Cytokines; DLB; Immunobiological markers; P PKC

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; PROTEIN KINASE C DELTA; PROTEIN KINASE C ZETA;

AGED; ALZHEIMER DISEASE; ARTICLE; CELL SPECIFICITY; CEREBROSPINAL FLUID ANALYSIS; CONTROLLED STUDY; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST ACCURACY STUDY; DIFFERENTIAL DIAGNOSIS; DIFFUSE LEWY BODY DISEASE; ELECTROENCEPHALOGRAPHY; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; MAJOR CLINICAL STUDY; MALE; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEIVER OPERATING CHARACTERISTIC; SENSITIVITY AND SPECIFICITY; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; BIOLOGICAL MARKERS; CYTOKINES; FEMALE; HUMANS; LEWY BODY DISEASE; MALE; MIDDLE AGED; PROTEIN KINASES; T-LYMPHOCYTES;

EID: 84865612341     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2012.01.004     Document Type: Article

References (65)

1. Akiyama H., Barger S., Barnum S., Bradt B., Bauer J., Cole G.M., Cooper N.R., Eikelenboom P., Emmerling M., Fiebich B.L., Finch C.E., Frautschy S., Griffin W.S., Hampel H., Hull M., Landreth G., Lue L., Mrak R., Mackenzie I.R., McGeer P.L., O'Banion M.K., Pachter J., Pasinetti G., Plata-Salaman C., Rogers J., Rydel R., Shen Y., Streit W., Strohmeyer R., Tooyoma I., Van Muiswinkel F.L., Veerhuis R., Walker D., Webster S., Wegrzyniak B., Wenk G., Wyss-Coray T. Inflammation and Alzheimer's disease. Neurobiol. Aging 2000, 21:383-421.
2. Askanas V., Engel W.K. Inclusion-body myositis and myopathies: different etiologies, possibly similar pathogenic mechanisms. Curr. Opin. Neurol 2002, 15:525-531.
3. Blasko I., Grubeck-Loebenstein B. Role of the immune system in the pathogenesis, prevention and treatment of Alzheimer's disease. Drugs Aging 2003, 20:101-113.
4. Bonanni L., Thomas A., Tiraboschi P., Perfetti B., Varanese S., Onofrj M. EEG comparisons in early Alzheimer's disease, dementia with Lewy bodies and Parkinson's disease with dementia patients with a 2-year follow-up. Brain 2008, 131:690-705.
5. Bonotis K., Krikki E., Holeva V., Aggouridaki C., Costa V., Baloyannis S. Systemic immune aberrations in Alzheimer's disease patients. J. Neuroimmunol 2008, 193:183-187.
6. + T-cell activation in human peripheral blood correlates with distinct antibody response patterns. Clin. Vaccine Immunol 2010, 17:705-712.
7. Chattopadhyay P.K., Hogerkorp C.M., Roederer M. A chromatic explosion: the development and future of multiparameter flow cytometry. Immunology 2008, 125:441-449.
8. Ciccocioppo F., Lanuti P., Marchisio M., Gambi F., Santavenere E., Pierdomenico L., Bascelli A., Velluto L., Gambi D., Miscia S. Expression and phosphorylation of protein kinase C isoforms in Abeta(1-42) activated T lymphocytes from Alzheimers disease. Int. J. Immunopathol. Pharmacol 2008, 21:23-33.
9. Crabtree G.R., Olson E.N. NFAT signaling: choreographing the social lives of cells. Cell 2002, 109:S67-S79.
10. Cummings J.L., Mega M., Gray K., Rosenberg-Thompson S., Carusi D.A., Gornbein J. The Neuropsychiatric Inventory: comprehensive assessment of psychopathology in dementia. Neurology 1994, 44:2308-2314.
11. Dubois B., Slachevsky A., Litvan I., Pillon B. The FAB: a Frontal Assessment Battery at bedside. Neurology 2000, 55:1621-1626.
12. Ebersbach G., Baas H., Csoti I., Müngersdorf M., Deuschl G. Scales in Parkinson's disease. J. Neurol 2006, 253:IV32-IV35.
13. Fillenbaum G.G., van Belle G., Morris J.C., Mohs R.C., Mirra S.S., Davis P.C., Tariot P.N., Silverman J.M., Clark C.M., Welsh-Bohmer K.A., Heyman A. Consortium to Establish a Registry for Alzheimer's Disease (CERAD): the first twenty years. Alzheimers Dement 2008, 4:96-109.
14. Folstein M., Folstein S., McHug P. "Mini-mental state", A practical methods for grading the cognitive state of patients for the clinician. Psychiatry Res 1975, 12:189-198.
15. Francis P.T. Biochemical and pathological correlates of cognitive and behavioural change in DLB/PDD. J. Neurol 2009, 256(Suppl 3):280-285.
16. Fuhrmann S., Streitz M., Reinke P., Volk H.D., Kern F. T cell response to the cytomegalovirus major capsid protein (UL86) is dominated by helper cells with a large polyfunctional component and diverse epitope recognition. J. Infect. Dis 2008, 197:1455-1458.
17. Gambi F., Reale M., Iarlori C., Salone A., Toma L., Paladini C., De Luca G., Feliciani C., Salvatore M., Salerno R.M., Theoharides T.C., Conti P., Exton M., Gambi D. Alzheimer patients treated with an AchE inhibitor show higher IL-4 and lower IL-1 beta levels and expression in peripheral blood mononuclear cells. J. Clin. Psychopharmacol 2004, 24:314-321.
18. Gaskin F., Finley J., Fang Q., Xu S., Fu S.M. Human antibodies reactive with beta-amyloid protein in Alzheimer's disease. J. Exp. Med 1993, 177:1181-1186.
19. + T cell response by attenuated SIV infection. J. Exp. Med 2006, 203:2661-2672.
20. Geser F., Wenning G.K., Poewe W., McKeith I. How to diagnose dementia with Lewy bodies: state of the art. Mov. Disord 2005, 20(Suppl 12):S11-S20.
21. Gustaw K.A., Garrett M.R., Lee H.G., Castellani R.J., Zagorski M.G., Prakasam A., Siedlak S.L., Zhu X., Perry G., Petersen R.B., Friedland R.P., Smith M.A. Antigen-antibody dissociation in Alzheimer disease: a novel approach to diagnosis. J. Neurochem 2008, 106:1350-1356.
22. Hanley J., McNeil B. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 1992, 143:29-36.
23. Hoehn M.M., Yahr M.D. Parkinsonism: onset, progression, and mortality. Neurology 2001, 1967:S11-S26. 57.
24. Hristov M., Schmitz S., Schuhmann C., Leyendecker T., von Hundelshausen P., Krötz F., Sohn H.Y., Nauwelaers F.A., Weber C. An optimized flow cytometry protocol for analysis of angiogenic monocytes and endothelial progenitor cells in peripheral blood. Cytometry A 2009, 75:848-853.
25. Iarlori C., Gambi D., Gambi F., Lucci I., Feliciani C., Salvatore M., Reale M. Expression and production of two selected beta-chemokines in peripheral blood mononuclear cells from patients with Alzheimer's disease. Exp. Gerontol 2005, 40:605-611.
26. Isakov N., Altman A. Protein kinase C(theta) in T cell activation. Annu. Rev. Immunol 2002, 20:761-794.
27. Jurica P.J., Leitten C.L., Mattis S. DRS-2 Dementia Rating Scale 2 2001, Psychological Assessment Resources, Odessa, FL.
28. Kern F., Khatamzas E., Surel I., Frömmel C., Reinke P., Waldrop S.L., Picker L.J., Volk H.D. Distribution of human CMV-specific memory T cells among the CD8pos. subsets defined by CD57, CD27, and CD45 isoforms. Eur. J. Immunol 1999, 29:2908-2915.
29. Kern F., Surel I.P., Brock C., Freistedt B., Radtke H., Scheffold A., Blasczyk R., Reinke P., Schneider-Mergener J., Radbruch A., Walden P., Volk H.D. T-cell epitope mapping by flow cytometry. Nat. Med 1998, 4:975-978.
30. Kitazawa M., Green K.N., Caccamo A., LaFerla F.M. Genetically augmenting Abeta42 levels in skeletal muscle exacerbates inclusion body myositis-like pathology and motor deficits in transgenic mice. Am. J. Pathol 2006, 168:1986-1997.
31. Lanuti P., Fuhrmann S., Lachmann R., Marchisio M., Miscia S., Kern F. Simultaneous characterization of phospho-proteins and cell cycle in activated T cell subsets. Int. J. Immunopathol. Pharmacol 2009, 22:689-698.
32. Leuner K., Pantel J., Frey C., Schindowski K., Schulz K., Wegat T., Maurer K., Eckert A., Muller W.E. Enhanced apoptosis, oxidative stress and mitochondrial dysfunction in lymphocytes as potential biomarkers for Alzheimer's disease. J. Neural Transm 2007, (Suppl.):207-215.
33. Lewczuk P., Hornegger J., Zimmermann R., Otto M., Wiltfang J., Kornhuber J. Neurochemical dementia diagnostics: assays in CSF and blood. Eur. Arch. Psychiatry Clin. Neurosci 2008, 258(Suppl 5):44-49.
34. Lugaresi A., Di Iorio A., Iarlori C., Reale M., De Luca G., Sparvieri E., Michetti A., Conti P., Gambi D., Abate G., Paganelli R. IL-4 in vitro production is upregulated in Alzheimer's disease patients treated with acetylcholinesterase inhibitors. Exp. Gerontol 2004, 39:653-657.
35. MacLeod H., Wetzler L.M. T cell activation by TLRs: a role for TLRs in the adaptive immune response. Sci. STKE 2007, 2007:e48.
36. Maecker H.T., Trotter J. Flow cytometry controls, instrument setup, and the determination of positivity. Cytometry A 2006, 69:1037-1042.
37. McKeith I., O'Brien J., Walker Z., Tatsch K., Booij J., Darcourt J., Padovani A., Giubbini R., Bonuccelli U., Volterrani D., Holmes C., Kemp P., Tabet N., Meyer I., Reininger C. Sensitivity and specificity of dopamine transporter imaging with 123I-FP-CIT SPECT in dementia with Lewy bodies: a phase III, multicentre study. Lancet Neurol 2007, 6:305-313. DLB Study Group.
38. McKeith I.G., Dickson D.W., Lowe J., Emre M., O'Brien J.T., Feldman H., Cummings J., Duda J.E., Lippa C., Perry E.K., Aarsland D., Arai H., Ballard C.G., Boeve B., Burn D.J., Costa D., Del Ser T., Dubois B., Galasko D., Gauthier S., Goetz C.G., Gomez-Tortosa E., Halliday G., Hansen L.A., Hardy J., Iwatsubo T., Kalaria R.N., Kaufer D., Kenny R.A., Korczyn A., Kosaka K., Lee V.M., Lees A., Litvan I., Londos E., Lopez O.L., Minoshima S., Mizuno Y., Molina J.A., Mukaetova-Ladinska E.B., Pasquier F., Perry R.H., Schulz J.B., Trojanowski J.Q., Yamada M. Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 2005, 65:1863-1872. Consortium on DLB.
39. 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.
40. McKhann G., Drachman D., Folstein M., Katzman R., Price D., Stadlan E.M. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 1984, 34:939-944.
41. Miscia S., Ciccocioppo F., Lanuti P., Velluto L., Bascelli A., Pierdomenico L., Genovesi D., Di Siena A., Santavenere E., Gambi F., Ausili-Cèfaro G., Grimley P.M., Marchisio M., Gambi D. Abeta(1-42) stimulated T cells express P-PKC-delta and P-PKC-zeta in Alzheimer disease. Neurobiol. Aging 2009, 30:394-406.
42. Miscia S., Di Baldassarre A., Cataldi A., Rana R.A., Di Pietro R., Bosco D., Grilli A., Amerio G., Sabatino G. Immunocytochemical localization of phospholipase C isozymes in cord blood and adult T-lymphocytes. J. Histochem. Cytochem 1999, 47:929-936.
43. Monsonego A., Zota V., Karni A., Krieger J.I., Bar-Or A., Bitan G., Budson A.E., Sperling R., Selkoe D.J., Weiner H.L. Increased T cell reactivity to amyloid beta protein in older humans and patients with Alzheimer disease. J. Clin. Invest 2003, 112:415-422.
44. Morgan D. The role of microglia in antibody-mediated clearance of amyloid-beta from the brain. CNS Neurol. Disord. Drug Targets 2009, 8:7-15.
45. Onofrj M., Luciano A.L., Iacono D., Thomas A., Stocchi F., Papola F., Adorno D., Di Mascio R. HLA typing does not predict REM sleep behaviour disorder and hallucinations in Parkinson's disease. Mov. Disord 2003, 18:337-340.
46. Parnetti L., Lanari A., Amici S., Gallai V., Vanmechelen E., Hulstaert F. CSF phosphorylated tau is a possible marker for discriminating Alzheimer's disease from dementia with Lewy bodies. Phospho-Tau International Study Group. Neurol. Sci 2001, 22:77-78. Phospho-Tau International Study Group.
47. Perfetto S.P., Ambrozak D., Nguyen R., Chattopadhyay P., Roederer M. Quality assurance for polychromatic flow cytometry. Nat. Protoc 2006, 1:1522-1530.
48. Preston S.D., Steart P.V., Wilkinson A., Nicoll J.A., Weller R.O. Capillary and arterial cerebral amyloid angiopathy in Alzheimer's disease: defining the perivascular route for the elimination of amyloid beta from the human brain. Neuropathol. Appl. Neurobiol 2003, 29:106-117.
49. Rambaran R.N., Serpell L.C. Amyloid fibrils: abnormal protein assembly. Prion 2008, 2:112-117.
50. Reale M., Iarlori C., Gambi F., Lucci I., Salvatore M., Gambi D. Acetylcholinesterase inhibitors effects on oncostatin-M, interleukin-1 beta and interleukin-6 release from lymphocytes of Alzheimer's disease patients. Exp. Gerontol 2005, 40:165-171.
51. Roederer M. Spectral compensation for flow cytometry: visualization artifacts, limitations, and caveats. Cytometry 2001, 45:194-205.
52. Roederer M., Nozzi J.L., Nason M.X. SPICE: Exploration and analysis of post-cytometric complex multivariate datasets. Cytometry A 2011, 79A:167-174.
53. San-Antonio B., Iñiguez M.A., Fresno M. Protein kinase Czeta phosphorylates nuclear factor of activated T cells and regulates its transactivating activity. J. Biol. Chem 2002, 277:27073-27080.
54. Savkovic S.D., Koutsouris A., Hecht G. PKC zeta participates in activation of inflammatory response induced by enteropathogenic E. coli. Am. J. Physiol. Cell Physiol 2003, 285:C512-C521.
55. Schoojans F. MedCalc 1998, MedCalc Software, Belgium.
56. Schwartz M., Shechter R. Systemic inflammatory cells fight off neurodegenerative disease. Nat. Rev. Neurol 2010, 6:405-410.
57. Speciale L., Calabrese E., Saresella M., Tinelli C., Mariani C., Sanvito L., Longhi R., Ferrante P. Lymphocyte subset patterns and cytokine production in Alzheimer's disease patients. Neurobiol. Aging 2007, 28:1163-1169.
58. Szabo P., Relkin N., Weksler M.E. Natural human antibodies to amyloid beta peptide. Autoimmun. Rev 2008, 7:415-420.
59. Tan S.L., Parker P.J. Emerging and diverse roles of protein kinase C in immune cell signalling. Biochem. J 2003, 376:545-552.
60. Togo T., Akiyama H., Iseki E., Kondo H., Ikeda K., Kato M., Oda T., Tsuchiya K., Kosaka K. Occurrence of T cells in the brain of Alzheimer's disease and other neurological diseases. J. Neuroimmunol 2002, 124:83-92.
61. Town T., Tan J., Flavell R.A., Mullan M. T-cells in Alzheimer's disease. Neuromol. Med 2005, 7:255-264.
62. Udan M.L., Ajit D., Crouse N.R., Nichols M.R. Toll-like receptors 2 and 4 mediate Abeta(1-42) activation of the innate immune response in a human monocytic cell line. J. Neurochem 2008, 104:524-533.
63. Walker M.P., Ayre G.A., Cummings J.L., Wesnes K., McKeith I.G., O'Brien J.T., Ballard C.G. The Clinician Assessment of Fluctuation and the One Day Fluctuation Assessment Scale. Two methods to assess fluctuating confusion in dementia. Br. J. Psychiatry 2000, 177:252-256.
64. Yamada M., Itoh Y., Shintaku M., Kawamura J., Jensson O., Thorsteinsson L., Suematsu N., Matsushita M., Otomo E. Immune reactions associated with cerebral amyloid angiopathy. Stroke 1996, 27:1155-1162.
65. Yonezawa T., Kurata R., Kimura M., Inoko H. PKC delta and epsilon in drug targeting and therapeutics. Recent Pat. DNA Genes Seq 2009, 3:96-101.