Herpes virus in alzheimer's disease: Relation to progression of the disease

Neurobiology of Aging

Volumn 35, Issue 1, 2014, Pages 122-129

  Carbone, Ilaria ^a   Lazzarotto, Tiziana ^b   Ianni, Manuela ^a   Porcellini, Elisa ^a   Forti, Paola ^b   Masliah, Eliezer ^c   Gabrielli, Liliana ^b   Licastro, Federico ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alzheimer's disease; Brain tissue samples; Herpes virus latency; Inflammatory plasma markers and cognitive decline; Nested PCR; Peripheral blood samples; Quantitative real time PCR

Indexed keywords

IMMUNOGLOBULIN G; VIRUS DNA;

AGED; ALZHEIMER DISEASE; ANTIGEN DETECTION; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; DISEASE ASSOCIATION; DISEASE COURSE; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; FEMALE; FOLLOW UP; HERPES VIRUS INFECTION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 6; HUMAN TISSUE; LEUKOCYTE; MAJOR CLINICAL STUDY; MALE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RISK FACTOR; SEROLOGY; VIRUS DETECTION;

ALZHEIMER'S DISEASE; BRAIN TISSUE SAMPLES; HERPES VIRUS LATENCY; INFLAMMATORY PLASMA MARKERS AND COGNITIVE DECLINE; NESTED PCR; PERIPHERAL BLOOD SAMPLES; QUANTITATIVE REAL TIME PCR;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANTIBODIES, VIRAL; BRAIN; COGNITION; DISEASE PROGRESSION; DNA, VIRAL; FEMALE; FOLLOW-UP STUDIES; HERPESVIRUS 4, HUMAN; HERPESVIRUS 6, HUMAN; HUMANS; IMMUNOGLOBULIN G; LEUKOCYTES; MALE; POLYMERASE CHAIN REACTION; RISK FACTORS;

EID: 84885174867     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.06.024     Document Type: Article

References (44)

1. Aiello A.E., Haan M., Blythe L., Moore K., Gonzalez J.M., Jagust W. The influence of latent viral infection on rate of cognitive decline over 4 years. J.Am. Geriatr. Soc. 2006, 54:1046-1054.
2. Braak H., Braak E. Frequency of stages of Alzheimer-related lesion in different age categories. Neurobiol. Aging 1997, 18:351-357.
3. Burgos J.S., Ramirez C., Sastre I., Valdivieso F. Effect of apolipoprotein E on the cerebral load of latent herpes simplex virus type 1 DNA. J.Virol. 2006, 80:5383-5387.
4. Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L., Vandesompele J., Wittwer C.T. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009, 55:611-622.
5. Carter C.J. Interactions between the products of the Herpes simplex genome and Alzheimer's disease susceptibility genes: Relevance to pathological-signalling cascades. Neurochem. Int. 2008, 52:920-934.
6. Corey-Bloom J., Tiraboschi P., Hansen L.A., Alford M., Schoocs B., Sabbagh M.N., Masliah E., Thal L.J. E4 allele dosage does not predict cholinergic activity or synapse loss in Alzheimer's disease. Neurology 2000, 54:403-406.
7. Fenner T.E., Garweg J., Hufert F.T., Boehnke M., Schmitz H. Diagnosis of human cytomegalovirus-induced retinitis in human immunodeficiency virus type 1- infected subjects by using the polymerase chain reaction. J.Clin. Microbiol. 1991, 29:2621-2622.
8. Forti P., Maioli F., Nesi B., Vettori C., Flisi E., Dalmonte E., Zanardi V., Lodi L., Macini P., Caldarera M., Ravaglia G. Conselice study: a population based survey of brain aging in a municipality of the Emilia Romagna region (A.U.S. L. Ravenna). Neuropsychological tests and nutritional status. Arch. Gerontol. Geriatr. Suppl. 2001, 7:137-144.
9. Gerna G., Baldanti F., Revello M.G. Pathogenesis of human cytomegalovirus infection and cellular targets [review]. Hum. Immunol. 2004, 65:381-386.
10. Hansen L.A., Masliah E., Galasko D., Terry R.D. Plaque-only Alzheimer disease is usually the Lewy body variant, and vice versa. J.Neuropathol. Exp. Neurol. 1993, 52:648-654.
11. Harold D., Abraham R., Hollingworth P., Sims R., Gerrish A., Hamshere M.L., Pahwa J.S., Moskvina V., Dowzell K., Williams A., Jones N., Thomas C., Stretton A., Morgan A.R., Lovestone S., Powell J., Proitsi P., Lupton M.K., Brayne C., Rubinsztein D.C., Gill M., Lawlor B., Lynch A., Morgan K., Brown K.S., Passmore P.A., Craig D., McGuinness B., Todd S., Holmes C., Mann D., Smith A.D., Love S., Kehoe P.G., Hardy J., Mead S., Fox N., Rossor M., Collinge J., Maier W., Jessen F., Schürmann B., van den Bussche H., Heuser I., Kornhuber J., Wiltfang J., Dichgans M., Frölich L., Hampel H., Hüll M., Rujescu D., Goate A.M., Kauwe J.S., Cruchaga C., Nowotny P., Morris J.C., Mayo K., Sleegers K., Bettens K., Engelborghs S., De Deyn P.P., Van Broeckhoven C., Livingston G., Bass N.J., Gurling H., McQuillin A., Gwilliam R., Deloukas P., Al-Chalabi A., Shaw C.E., Tsolaki M., Singleton A.B., Guerreiro R., Mühleisen T.W., Nöthen M.M., Moebus S., Jöckel K.H., Klopp N., Wichmann H.E., Carrasquillo M.M., Pankratz V.S., Younkin S.G., Holmans P.A., O'Donovan M., Owen M.J., Williams J. Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer's disease. Nat. Genet. 2009, 41:1088-1093.
12. Hemling N., Röyttä M., Rinne J., Pöllänen P., Broberg E., Tapio V., Vahlberg T., Hukkanen V. Herpesviruses in brains in Alzheimer's and Parkinson's diseases. Ann. Neurol. 2003, 54:267-271.
13. Hollingworth P., Harold D., Sims R., Gerrish A., Lambert J.C., Carrasquillo M.M., Abraham R., Hamshere M.L., Pahwa J.S., Moskvina V., Dowzell K., Jones N., Stretton A., Thomas C., Richards A., Ivanov D., Widdowson C., Chapman J., Lovestone S., Powell J., Proitsi P., Lupton M.K., Brayne C., Rubinsztein D.C., Gill M., Lawlor B., Lynch A., Brown K.S., Passmore P.A., Craig D., McGuinness B., Todd S., Holmes C., Mann D., Smith A.D., Beaumont H., Warden D., Wilcock G., Love S., Kehoe P.G., Hooper N.M., Vardy E.R., Hardy J., Mead S., Fox N.C., Rossor M., Collinge J., Maier W., Jessen F., Rüther E., Schürmann B., Heun R., Kölsch H., van den Bussche H., Heuser I., Kornhuber J., Wiltfang J., Dichgans M., Frölich L., Hampel H., Gallacher J., Hüll M., Rujescu D., Giegling I., Goate A.M., Kauwe J.S., Cruchaga C., Nowotny P., Morris J.C., Mayo K., Sleegers K., Bettens K., Engelborghs S., De Deyn P.P., Van Broeckhoven C., Livingston G., Bass N.J., Gurling H., McQuillin A., Gwilliam R., Deloukas P., Al-Chalabi A., Shaw C.E., Tsolaki M., Singleton A.B., Guerreiro R., Mühleisen T.W., Nöthen M.M., Moebus S., Jöckel K.H., Klopp N., Wichmann H.E., Pankratz V.S., Sando S.B., Aasly J.O., Barcikowska M., Wszolek Z.K., Dickson D.W., Graff-Radford N.R., Petersen R.C., Alzheimer's Disease Neuroimaging Initiative, van Duijn C.M., Breteler M.M., Ikram M.A., DeStefano A.L., Fitzpatrick A.L., Lopez O., Launer L.J., Seshadri S., Berr C., Campion D., Epelbaum J., Dartigues J.F., Tzourio C., Alpérovitch A., Lathrop M., Feulner T.M., Friedrich P., Riehle C., Krawczak M., Schreiber S., Mayhaus M., Nicolhaus S., Wagenpfeil S., Steinberg S., Stefansson H., Stefansson K., Snaedal J., Björnsson S., Jonsson P.V., Chouraki V., Genier-Boley B., Hiltunen M., Soininen H., Combarros O., Zelenika D., Delepine M., Bullido M.J., Pasquier F., Mateo I., Frank-Garcia A., Porcellini E., Hanon O., Coto E., Alvarez V., Bosco P., Siciliano G., Mancuso M., Panza F., Solfrizzi V., Nacmias B., Sorbi S., Bossù P., Piccardi P., Arosio B., Annoni G., Seripa D., Pilotto A., Scarpini E., Galimberti D., Brice A., Hannequin D., Licastro F., Jones L., Holmans P.A., Jonsson T., Riemenschneider M., Morgan K., Younkin S.G., Owen M.J., O'Donovan M., Amouyel P., Williams J. Common variants at ABCA7, MS4A6A/MS4A4E, EPHA1, CD33 and CD2AP are associated with Alzheimer's disease. Nat. Genet. 2011, 43:429-435. CHARGE consortium, EADI1 consortiumEADI1 consortium.
14. Itzhaki R.F., Wozniak M.A., Appelt D.M., Balin B.J. Infiltration of the brain by pathogens causes Alzheimer's disease [review]. Neurobiol. Aging 2004, 25:619-627.
15. Itzhaki R.F., Wozniak M.A. Herpes simplex virus type 1 in Alzheimer's disease: the enemy within. J.Alzheimers Dis. 2008, 13:393-405.
16. Kleines M., Schiefer J., Stienen A., Blaum M., Ritter K., Häusler M. Expanding the spectrum of neurological disease associated with Epstein-Barr virus activity. Eur. J. Clin. Microbiol. Infect. Dis. 2011, 30:1561-1569.
17. Koch S., Solana R., Dela Rosa O., Pawelec G. Human cytomegalovirus infection and T cell immunosenescence: a mini review. Mech. Ageing Dev. 2006, 127:538-543.
18. Krstic D., Madhusudan A., Doehner J., Vogel P., Notter T., Imhof C., Manalastas A., Hilfiker M., Pfister S., Schwerdel C., Riether C., Meyer U., Knuesel I. Systemic immune challenges trigger and drive Alzheimer-like neuropathology in mice. J.Neuroinflamm. 2012, 9:151.
19. Kutok J.L., Wang F. Spectrum of Epstein-Barr virus-associated diseases. Annu. Rev. Pathol. 2006, 1:375-404.
20. Lambert J.C., Heath S., Even G., Campion D., Sleegers K., Hiltunen M., Combarros O., Zelenika D., Bullido M.J., Tavernier B., Letenneur L., Bettens K., Berr C., Pasquier F., Fiévet N., Barberger-Gateau P., Engelborghs S., De Deyn P., Mateo I., Franck A., Helisalmi S., Porcellini E., Hanon O., European Alzheimer's Disease Initiative Investigators, de Pancorbo M.M., Lendon C., Dufouil C., Jaillard C., Leveillard T., Alvarez V., Bosco P., Mancuso M., Panza F., Nacmias B., Bossù P., Piccardi P., Annoni G., Seripa D., Galimberti D., Hannequin D., Licastro F., Soininen H., Ritchie K., Blanché H., Dartigues J.F., Tzourio C., Gut I., Van Broeckhoven C., Alpérovitch A., Lathrop M., Amouyel P. Genome-wide association study identities variants at CLU and CR1 associated with Alzheimer's disease. Nature Genet. 2009, 41:1094-1099.
21. Lang P.O., Govind S., Aspinall R. Reversing T cell immunosenescence: why, who, and how. Age (Dordr) 2012, 35, 609-620.
22. Lassmann H., Niedobitek G., Aloisi F., Middeldorp J.M. Epstein-Barr virus in the multiple sclerosis brain: a controversial issue-report on a focused workshop held in the Centre for Brain Research of the Medical University of Vienna, Austria. Brain 2011, 134:2772-2786. NeuroproMiSe EBV Working Group.
23. Licastro F., Pedrini S., Govoni M., Pession A., Ferri C., Annoni G., Casadei V., Veglia F., Bertolini S., Grimaldi L.M. Apolipoprotein E and alpha-1-antichymotrypsin allele polymorphism in sporadic and familial Alzheimer's disease. Neurosci. Lett. 1999, 270:129-132.
24. Licastro F., Porcellini E., Caruso C., Lio D., Corder E.H. Genetic risk profiles for Alzheimer's disease: integration of APOE genotype and variants that up-regulate inflammation. Neurobiol. Aging 2007, 28:1637-1643.
25. Licastro F., Chiappelli M., Porcellini E., Campo G., Buscema M., Grossi E., Garoia F., Ferrari R. Gene-gene and gene-clinical factors interaction in acute myocardial infarction: a new detailed risk chart. Curr. Pharm. Des. 2010, 16:783-788.
26. Licastro F., Porcellini E., Forti P., Buscema M., Carbone I., Ravaglia G., Grossi E. Multi factorial interactions in the pathogenesis pathway of Alzheimer's disease: a new risk charts for prevention of dementia. Immun. Ageing 2010, 7(Suppl1):S4.
27. Licastro F., Carbone I., Ianni M., Porcellini E. Gene signature in Alzheimer's disease and environmental factors: the virus chronicle. J.Alzheimers Dis. 2011, 27:809-817.
28. Lin W.R., Wozniak M.A., Cooper R.J., Wilcock G.K., Itzhaki R.F. Herpesviruses in brain and Alzheimer's disease. J.Pathol. 2002, 197:395-402.
29. Malorny B., Hoorfar J., Bunge C., Helmuth R. Multicenter validation of the analytical accuracy of Salmonella PCR: towards an international standard. Appl. Environ. Microbiol. 2003, 69:290-296.
30. McKahnn G., Drachmann D., Folstein M., Katzman R., Price D., Stadlan E.M. Clinical diagnosis of Alzheimer's disease: report of NINCDSADRDA work group under the auspices of Department of Health and Human Service Task Force on Alzheimer's disease. Neurology 1984, 34:934-944.
31. Mori I., Kimura Y., Naiki H., Matsubara R., Takeuchi T., Yokochi T., Nishiyama Y. Reactivation of HSV-1in the brain of patients with familial Alzheimer's disease. J.Med. Virol. 2004, 73:605-611.
32. Naj A.C., Jun G., Beecham G.W., Wang L.S., Vardarajan B.N., Buros J., Gallins P.J., Buxbaum J.D., Jarvik G.P., Crane P.K., Larson E.B., Bird T.D., Boevem B.F., Graff-Radford N.R., De Jager P.L., Evans D., Schneider J.A., Carrasquillo M.M., Ertekin-Taner N., Younkin S.G., Cruchaga C., Kauwe J.S., Nowotny P., Kramer P., Hardy J., Huentelman M.J., Myers A.J., Barmada M.M., Demirci F.Y., Baldwin C.T., Green R.C., Rogaeva E., St George-Hyslop P., Arnold S.E., Barber R., Beach T., Bigio E.H., Bowen J.D., Boxer A., Burke J.R., Cairns N.J., Carlson C.S., Carney R.M., Carroll S.L., Chui H.C., Clark D.G., Corneveaux J., Cotman C.W., Cummings J.L., DeCarli C., DeKosky S.T., Diaz-Arrastia R., Dick M., Dickson D.W., Ellis W.G., Faber K.M., Fallon K.B., Farlow M.R., Ferris S., Frosch M.P., Galasko D.R., Ganguli M., Gearing M., Geschwind D.H., Ghetti B., Gilbert J.R., Gilman S., Giordani B., Glass J.D., Growdon J.H., Hamilton R.L., Harrell L.E., Head E., Honig L.S., Hulette C.M., Hyman B.T., Jicha G.A., Jin L.W., Johnson N., Karlawish J., Karydas A., Kaye J.A., Kim R., Koo E.H., Kowall N.W., Lah J.J., Levey A.I., Lieberman A.P., Lopez O.L., Mack W.J., Marson D.C., Martiniuk F., Mash D.C., Masliah E., McCormick W.C., McCurry S.M., McDavid A.N., McKee A.C., Mesulam M., Miller B.L., Miller C.A., Miller J.W., Parisi J.E., Perl D.P., Peskind E., Petersen R.C., Poon W.W., Quinn J.F., Rajbhandary R.A., Raskind M., Reisberg B., Ringman J.M., Roberson E.D., Rosenberg R.N., Sano M., Schneider L.S., Seeley W., Shelanski M.L., Slifer M.A., Smith C.D., Sonnen J.A., Spina S., Stern R.A., Tanzi R.E., Trojanowski J.Q., Troncoso J.C., Van Deerlin V.M., Vinters H.V., Vonsattel J.P., Weintraub S., Welsh-Bohmer K.A., Williamson J., Woltjer R.L., Cantwell L.B., Dombroski B.A., Beekly D., Lunetta K.L., Martin E.R., Kamboh M.I., Saykin A.J., Reiman E.M., Bennett D.A., Morris J.C., Montine T.J., Goate A.M., Blacker D., Tsuang D.W., Hakonarson H., Kukull W.A., Foroud T.M., Haines J.L., Mayeux R., Pericak-Vance M.A., Farrer L.A., Schellenberg G.D. Common variants at MS4A4/MS4A6E, CD2AP, CD33 and EPHA1 are associated with late-onset Alzheimer's disease. Nat. Genet. 2011, 43:436-441.
33. Pawelec G., Derhovanessian E., Larbi A., Strindhall J., Wikby A. Cytomegalovirus and human immunosenescence. Rev. Med. Virol. 2009, 19:47-56.
34. Porcellini E., Davis E.J., Chiappelli M., Ianni E., Di Stefano G., Forti P., Ravaglia G., Licastro F. Elevated plasma levels of alpha-1-anti-chymotrypsin in age-related cognitive decline and Alzheimer's disease: a potential therapeutic target. Curr. Pharm. Des. 2008, 14:2659-2664.
35. Porcellini E., Carbone I., Ianni M., Licastro F. Alzheimer's disease gene signature says: beware of brain viral infections. Immun. Ageing 2010, 7:16.
36. Ravaglia G., Forti P., Maioli F., Orlanducci P., Sacchetti L., Flisi E., Dalmonte E., Martignani A., Cucinotta D., Cavalli G. Conselice study: a population based survey of brain aging in a municipality of the Emilia Romagna region (A.U.S.L. Ravenna). Design and methods. Arch. Gerontol. Geriatr. Suppl. 2001, 7:313-324.
37. Ravaglia G., Forti P., Maioli F., Chiappelli M., Montesi F., Tumini E., Mariani E., Licastro F., Patterson C. Blood inflammatory markers and risk of dementia: the Conselice Study of Brain Aging. Neurobiol. Aging 2007, 28:1810-1820.
38. Rymkiewicz P.D., Heng Y.X., Vasudev A., Larbi A. The immune system in the aging human. Immunol. Res. 2012, 53:235-250.
39. Simanek A.M., Dowd J.B., Pawelec G., Melzer D., Dutta A., Aiello A.E. Seropositivity to cytomegalovirus, inflammation, all-cause and cardiovascular disease-related mortality in the United States. PLoS One 2011, 17:e16103.
40. Tsutsui Y., Kosugi I., Kawasaki H., Arai Y., Han G.P., Li L., Kaneta M. Roles of neural stem progenitor cells in cytomegalovirus infection of the brain in mouse models [review]. Pathol. Int. 2008, 58:257-267.
41. Vogl B.A., Fagin U., Nerbas L., Schlenke P., Lamprecht P., Jabs W.J. Longitudinal analysis of frequency and reactivity of Epstein-Barr virus-specific T lymphocytes and their association with intermittent viral reactivation. J.Med. Virol. 2012, 84:119-131.
42. Wakefield A.J., Fox J.D., Sawyerr A.M., Taylor J.E., Sweenie C.H., Smith M., Emery V.C., Hudson M., Tedder R.S., Pounder R.E. Detection of Herpesvirus DNA in the large intestine of patients with ulcerative colitis and Crohn's disease using the nested polymerase chain reaction. J.Med. Virol. 1992, 38:183-190.
43. Wozniak M.A., Mee A.P., Itzhaki R.F. Herpes simplex virus type 1 DNA is located within Alzheimer's disease amyloid plaques. J.Pathol. 2009, 217:131-138.
44. Yao K., Crawford J.R., Komaroff A.L., Ablashi D.V., Jacobson S. Review part 2: human herpesvirus-6 in central nervous system diseases. J.Med. Virol. 2010, 82:1669-1678.