Herpes simplex virus type 1, apolipoprotein E, and cholesterol: A dangerous liaison in Alzheimer's disease and other disorders

Progress in Lipid Research

Volumn 45, Issue 1, 2006, Pages 73-90

  Itzhaki, Ruth F ^a   Wozniak, Matthew A ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Alzheimer's disease; Apolipoprotein E; Brain; Cholesterol; Herpes simplex virus type 1; HIV; Lipid rafts; Statins

Indexed keywords

ALPHA SECRETASE; AMYLOID PRECURSOR PROTEIN; APOLIPOPROTEIN E; APOLIPOPROTEIN E2; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; BETA SECRETASE; CHOLESTEROL; GAMMA SECRETASE; GLYCOPROTEIN B; GLYCOPROTEIN D; GUANINE NUCLEOTIDE; HEPARAN SULFATE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; PROTEIN C; PYRIMIDINE NUCLEOTIDE; TAU PROTEIN; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR; VIRUS PROTEIN;

ALLELE; ALZHEIMER DISEASE; CARDIOVASCULAR DISEASE; DOWN SYNDROME; DRUG EFFECT; HEAD INJURY; HERPES SIMPLEX VIRUS 1; HUMAN; INFLAMMATION; LATENT PERIOD; LIFE CYCLE; LIPID PEROXIDATION; LIPID RAFT; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; RISK FACTOR;

AGED; ALZHEIMER DISEASE; APOLIPOPROTEINS E; BRAIN; CHOLESTEROL; GENETIC PREDISPOSITION TO DISEASE; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; LIPID PEROXIDATION; MEMBRANE MICRODOMAINS; VIRUS LATENCY;

HUMAN HERPESVIRUS 1;

EID: 31644446108     PISSN: 01637827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plipres.2005.11.003     Document Type: Review

References (85)

1. T. Hartman Cholesterol and Alzheimer's disease: statins, cholesterol depletion in APP processing and Abeta generation Subcell Biochem 38 2005 365 380
2. N. Helbecque, and P. Amouyel Commonalities between genetics of cardiovascular disease and neurodegenerative disorders Curr Opin Lipidol 15 2004 121 127
3. I. Casserly, and E. Topol Convergence of atherosclerosis and Alzheimer's disease: inflammation, cholesterol, and misfolded proteins Lancet 363 2004 1139 1146
4. D. WuDunn, and P.G. Spear Initial interaction of herpes simplex virus with cells is binding to heparan sulfate J Virol 63 1989 52 58
5. S.I. Gerber, B.J. Belval, and B.C. Herold Differences in the role of glycoprotein C of HSV-1 and HSV-2 in viral binding may contribute to serotype differences in cell tropism Virology 214 1995 29 39
6. R.I. Montgomery, M.S. Warner, B.J. Lum, and P.G. Spear Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family Cell 87 1996 427 436
7. R.J. Geraghty, C. Krummenacher, G.H. Cohen, R.J. Eisenberg, and P.G. Spear Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor Science 280 1998 1618 1620
8. C. Krummenacher, A.V. Nicola, J.C. Whitbeck, H. Lou, W. Hou, and J.D. Lambris Herpes simplex virus glycoprotein D can bind to poliovirus receptor-related protein 1 or herpesvirus entry mediator, two structurally unrelated mediators of virus entry J Virol 72 1998 7064 7074
9. A.V. Nicola, A.M. McEvoy, and S.E. Straus Roles for endocytosis and low pH in herpes simplex virus entry into HeLa and Chinese hamster ovary cells J Virol 77 2003 5324 5332
10. F.C. Bender, J.C. Whitbeck, M. Ponce de Leon, H. Lou, R.J. Eisenberg, and G.H. Cohen Specific association of glycoprotein B with lipid rafts during herpes simplex virus entry J Virol 77 2003 9542 9552
11. A.D. Kwong, and N. Frenkel Herpes simplex virus-infected cells contain a function (s) that destabilizes both host and viral mRNAs Proc Natl Acad Sci USA 84 1987 1926 1930
12. R. Tal-Singer, T.M. Lasner, W. Podrzucki, A. Skokotas, J.J. Leary, and S.L. Berger Gene expression during reactivation of herpes simplex virus type 1 from latency in the peripheral nervous system is different from that during lytic infection of tissue cultures J Virol 71 1997 5268 5276
13. L. Hutchinson, and D.C. Johnson Herpes simplex virus glycoprotein K promotes egress of virus particles J Virol 69 1995 5401 5413
14. S.L. Deshmane, and N.W. Fraser During latency, herpes simplex virus type 1 DNA is associated with nucleosomes in a chromatin structure J Virol 63 1989 943 947
15. H. Youssoufian, S.M. Hammer, M.S. Hirsch, and C. Mulder Methylation of the viral genome in an in vitro model of herpes simplex virus latency Proc Natl Acad Sci USA 79 1982 2207 2210
16. E.K. Wagner, G. Devi-Rao, L.T. Feldman, A.T. Dobson, Y.F. Zhang, and W.M. Flanagan Physical characterization of the herpes simplex virus latency-associated transcript in neurons J Virol 62 1988 1194 1202
17. C. Wilson, M.R. Wardell, K.H. Weisgraber, R.W. Mahley, and D.A. Agard Three-dimensional structure of the LDL receptor-binding domain of human apolipoprotein E Science 252 1991 1817 1822
18. J.G. Neels, I.R. Horn, B.M.M. van der Berg, H. Pannekoek, and A.-J. van Zonneveld Ligand-receptor interactions of the low density lipoprotein receptor-related protein, a multi-ligand endocytic receptor Fibrinolysis Proteolysis 12 1998 219 240
19. R.W. Mahley, and S.C. Rall Jr. Apolipoprotein E: far more than a lipid transport protein Annu Rev Genom Hum Genet 1 2000 507 537
20. M.J. Ball Limbic predilection in Alzheimer dementia: is reactivated herpesvirus involved? Can J Neurol Sci 9 1982 303 306
21. P.E. Klapper, G.M. Cleator, and M. Longson Mild forms of herpes encephalitis J Neurol Neurosurg Psychiatry 47 1984 1247 1250
22. P.A. Fodor, M.J. Levin, A. Weinberg, E. Sandberg, J. Sylman, and K.L. Tyler A typical herpes simplex virus encephalitis diagnosed by PCR amplification of viral DNA from CSF Neurology 51 1998 554 559
23. R.F. Itzhaki, W.R. Lin, D. Shang, G.K. Wilcock, B. Faragher, and G.A. Jamieson Herpes simplex virus type 1 in brain and risk of Alzheimer's disease Lancet 349 1997 241 244
24. G.A. Jamieson, N.J. Maitland, G.K. Wilcock, J. Craske, and R.F. Itzhaki Latent herpes simplex virus type 1 in normal and Alzheimer's disease brains J Med Virol 33 1991 224 227
25. L. Gordon, S. McQuaid, and S.L. Cosby Detection of herpes simplex virus types 1 and 2 and human herpes virus 6 DNA in human brain tissue by polymerase chain reaction Clin Diagnost Virol 6 1996 33 40
26. J.R. Baringer, and P. Pisani Herpes simplex virus genomes in human nervous system tissue analyzed by polymerase chain reaction Ann Neurol 36 1994 823 829
27. P. Bertrand, D. Guillaume, L. Hellauer, D. Dea, J. Lindsay, and S. Kogan Distribution of herpes simplex virus type 1 DNA in selected areas of normal and Alzheimer's disease brains: a PCR study Neurodegeneration 1993 201 208
28. G.A. Jamieson, N.J. Maitland, G.K. Wilcock, C.M. Yates, and R.F. Itzhaki Herpes simplex virus type 1 DNA is present in specific regions of brain from aged people with and without senile dementia of the Alzheimer type J Pathol 167 1992 365 368
29. W.R. Lin, I. Casas, G.K. Wilcock, and R.F. Itzhaki Neurotropic viruses and Alzheimer's disease: a search for varicella zoster virus DNA by the polymerase chain reaction J Neurol Neurosurg Psychiatry 62 1997 586 589
30. W.R. Lin, M.A. Wozniak, R.J. Cooper, G.K. Wilcock, and R.F. Itzhaki Herpesviruses in brain and Alzheimer's disease J Pathol 197 2002 395 402
31. W.R. Lin, M.A. Wozniak, G.K. Wilcock, and R.F. Itzhaki Cytomegalovirus is present in a very high proportion of brains from vascular dementia patients Neurobiol Dis 9 2002 82 87
32. H.B. Qavi Possible role of HHV-6 in the enhanced severity of HSV-1 keratitis In Vivo 13 1999 427 432
33. B. Ensoli, P. Lusso, F. Schachter, S.F. Josephs, J. Rappaport, and F. Negro Human herpes virus-6 increases HIV-1 expression in co-infected T cells via nuclear factors binding to the HIV-1 enhancer EMBO J 8 1989 3019 3027
34. K.K. Knox, and D.R. Carrigan Active human herpesvirus (HHV-6) infection of the central nervous system in patients with AIDS J Acquir Immune Defic Syndr Hum Retrovirol 9 1995 69 73
35. D.J. Mock, J.M. Powers, A.D. Goodman, S.R. Blumenthal, N. Ergin, and J.V. Baker Association of human herpesvirus 6 with the demyelinative lesions of progressive multifocal leukoencephalopathy J Neurovirol 5 1999 363 373
36. B.M. Blumberg, D.J. Mock, J.M. Powers, M. Ito, J.G. Assouline, and J.V. Baker The HHV6 paradox: ubiquitous commensal or insidious pathogen? A two-step in situ PCR approach J Clin Virol 16 2000 159 178
37. A. Kol, and P. Libby The mechanisms by which infectious agents may contribute to atherosclerosis and its clinical manifestations Trends Cardiovasc Med 8 1998 191 199
38. B.J. Balin, H.C. Gerard, E.J. Arking, D.M. Appelt, P.J. Branigan, and J.T. Abrams Identification and localization of Chlamydia pneumoniae in the Alzheimer's brain Med Microbiol Immunol (Berl) 187 1998 23 42
39. M.A. Wozniak, A. Cookson, G.K. Wilcock, and R.F. Itzhaki Absence of Chlamydia pneumoniae in brain of vascular dementia patients Neurobiol Aging 24 2003 761 765
40. A.M. Saunders, K. Schmader, J.C. Breitner, M.D. Benson, W.T. Brown, and L. Goldfarb Apolipoprotein E epsilon 4 allele distributions in late-onset Alzheimer's disease and in other amyloid-forming diseases Lancet 342 1993 710 711
41. W.R. Lin, J. Graham, S.M. MacGowan, G.K. Wilcock, and R.F. Itzhaki Alzheimer's disease, herpes virus in brain, apolipoprotein E4 and herpes labialis Alzheimers Reports 1 1998 173 178
42. S. Itabashi, H. Arai, T. Matsui, S. Higuchi, and H. Sasaki Herpes simplex virus and risk of Alzheimer's disease Lancet 349 1997 1102
43. U. Beffert, P. Bertrand, D. Champagne, S. Gauthier, and J. Poirier HSV-1 in brain and risk of Alzheimer's disease Lancet 351 1998 1330 1331 (see also: Itzhaki et al. Lancet 1998;352:238 and Corder et al. Lancet 1998;352:1312-3)
44. M.A. Wozniak, S.J. Shipley, M. Combrinck, G.K. Wilcock, and R.F. Itzhaki Productive herpes simplex virus in brain of elderly normal subjects and Alzheimer's disease patients J Med Virol 75 2005 300 306
45. W.R. Lin, M.A. Wozniak, M.M. Esiri, P. Klenerman, and R.F. Itzhaki Herpes simplex encephalitis: involvement of apolipoprotein E genotype J Neurol Neurosurg Psychiatry 70 2001 117 119
46. M.A. Wozniak, R.F. Itzhaki, E.B. Faragher, M.W. James, S.D. Ryder, and W.L. Irving Apolipoprotein E-epsilon 4 protects against severe liver disease caused by hepatitis C virus Hepatology 36 2002 456 463
47. E.H. Corder, K. Robertson, L. Lannfelt, N. Bogdanovic, G. Eggertsen, and J. Wilkins HIV-infected subjects with the E4 allele for APOE have excess dementia and peripheral neuropathy Nat Med 4 1998 1182 1184
48. K. Bohnet, T. Pillot, S. Visvikis, N. Sabolovic, and G. Siest Apolipoprotein (apo) E genotype and apoE concentration determine binding of normal very low density lipoproteins to HepG2 cell surface receptors J Lipid Res 37 1996 1316 1324
49. C.D. Mamotte, M. Sturm, J.I. Foo, F.M. van Bockxmeer, and R.R. Taylor Comparison of the LDL-receptor binding of VLDL and LDL from apoE4 and apoE3 homozygotes Am J Physiol 276 1999 E553 E557
50. W.R. Lin, A.B. Tullo, and R.F. Itzhaki Apolipoprotein E and herpes virus diseases: herpes simplex keratitis Eur J Hum Genet 7 1999 401 403
51. M.A. Wozniak, E.B. Faragher, J.A. Todd, K.A. Koram, E.M. Riley, and R.F. Itzhaki Does apolipoprotein E polymorphism influence susceptibility to malaria? J Med Genet 40 2003 348 351
52. D.T. Laskowitz, K. Horsburgh, and A.D. Roses Apolipoprotein E and the CNS response to injury J Cereb Blood Flow Metab 18 1998 465 471
53. R.F. Itzhaki, and M.A. Wozniak Alzheimer's disease, the neuroimmune axis, and viral infection J Neuroimmunol 156 2004 1 2
54. R.F. Itzhaki, M.A. Wozniak, D.M. Appelt, and B.J. Balin Infiltration of the brain by pathogens causes Alzheimer's disease Neurobiol Aging 25 2004 619 627
55. M.I. Combrinck, V.H. Perry, and C. Cunningham Peripheral infection evokes exaggerated sickness behaviour in pre-clinical murine prion disease Neuroscience 112 2002 7 11
56. C. Holmes, M. El-Okl, A.L. Williams, C. Cunningham, D. Wilcockson, and V.H. Perry Systemic infection, interleukin 1beta, and cognitive decline in Alzheimer's disease J Neurol Neurosurg Psychiatry 74 2003 788 789
57. T.E. Strandberg, K.H. Pitkala, K.H. Linnavuori, and R.S. Tilvis Impact of viral and bacterial burden on cognitive impairment in elderly persons with cardiovascular diseases Stroke 34 2003 2126 2131
58. F.B. Dickerson, J.J. Boronow, C. Stallings, A.E. Origoni, S. Cole, and B. Krivogorsky Infection with herpes simplex virus type 1 is associated with cognitive deficits in bipolar disorder Biol Psychiatry 55 2004 588 593
59. C.B. Pocernich, R. Sultana, E. Hone, J. Turchan, R.N. Martins, and V. Calabrese Effects of apolipoprotein E on the human immunodeficiency virus protein Tat in neuronal cultures and synaptosomes J Neurosci Res 77 2004 532 539
60. J.R. Lynch, W. Tang, H. Wang, M.P. Vitek, E.R. Bennett, and P.M. Sullivan APOE genotype and an ApoE-mimetic peptide modify the systemic and central nervous system inflammatory response J Biol Chem 278 2003 48529 48533
61. J.S. Burgos, C. Ramirez, I. Sastre, M.J. Bullido, and F. Valdivieso ApoE4 is more efficient than E3 in brain access by herpes simplex virus type 1 Neuroreport 14 2003 1825 1827
62. D.H. Cribbs, B.Y. Azizeh, C.W. Cotman, and F.M. LaFerla Fibril formation and neurotoxicity by a herpes simplex virus glycoprotein B fragment with homology to the Alzheimer's A beta peptide Biochemistry 39 2000 5988 5994
63. H. Takakuwa, F. Goshima, T. Koshizuka, T. Murata, T. Daikoku, and Y. Nishiyama Herpes simplex virus encodes a virion-associated protein which promotes long cellular processes in over-expressing cells Genes Cells 6 2001 9559 9566
64. L. Benboudjema, M. Mulvey, Y. Gao, S.W. Pimplikar, and I. Mohr Association of the herpes simplex virus type 1 Us11 gene product with the cellular kinesin light-chain-related protein PAT1 results in the redistribution of both polypeptides J Virol 77 2003 9192 9203
65. P. Satpute-Krishnan, J.A. DeGiorgis, and E.L. Bearer Fast anterograde transport of herpes simplex virus: role for the amyloid precursor protein of Alzheimer's disease Aging Cell 2 2003 305 318
66. J. Poirier Apolipoprotein E, cholesterol transport and synthesis in sporadic Alzheimer's disease Neurobiol Aging 26 2005 355 361
67. A.M. Manelli, W.B. Stine, L.J. Van Eldik, and M.J. LaDu ApoE and Abeta1-42 interactions: effects of isoform and conformation on structure and function J Mol Neurosci 23 2004 235 246
68. D.B. Carter The interaction of amyloid-beta with ApoE Subcell Biochem 38 2005 255 272
69. D.H. Mauch, K. Nagler, S. Schumacher, C. Goritz, E.C. Muller, and A. Otto CNS synaptogenesis promoted by glia-derived cholesterol Science 294 2001 1354 1357
70. F.W. Pfrieger Cholesterol homeostasis and function in neurons of the central nervous system Cell Mol Life Sci 60 2003 1158 1171
71. I. Bjorkhem, and S. Meaney Brain cholesterol: long secret life behind a barrier Arterioscler Thromb Vasc Biol 24 2004 806 815
72. M.D. Ledesma, and C.G. Dotti The conflicting role of brain cholesterol in Alzheimer's disease: lessons from the brain plasminogen system Biochem Soc Symp 2005 129 138
73. H.Y. Hsu, A.C. Nicholson, K.B. Pomerantz, R.J. Kaner, and D.P. Hajjar Altered cholesterol trafficking in herpesvirus-infected arterial cells. Evidence for viral protein kinase-mediated cholesterol accumulation J Biol Chem 270 1995 19630 19637
74. Statin use and Alzheimer disease: a tale of two methodologies. Available from: www.alzforum.com; 2005.
75. Philadelphia: All is not well with the statin story. Available from: www.alzforum.com; 2005.
76. J.M. Hill, I. Steiner, K.E. Matthews, S.G. Trahan, T.P. Foster, and M.J. Ball Statins lower the risk of developing Alzheimer's disease by limiting lipid raft endocytosis and decreasing the neuronal spread of Herpes simplex virus type 1 Med Hypotheses 64 2005 53 58
77. H. Hayashi, U. Igbavboa, H. Hamanaka, M. Kobayashi, S.C. Fujita, and W.G. Wood Cholesterol is increased in the exofacial leaflet of synaptic plasma membranes of human apolipoprotein E4 knock-in mice Neuroreport 13 2002 383 386
78. R.F. Itzhaki, and M.A. Wozniak Comment on: Hill JM et al. Statins lower the risk of developing Alzheimer's disease by limiting lipid raft endocytosis and decreasing the neuronal spread of Herpes simplex virus type 1 Med Hypotheses 64 2005 53 58 Alzheimer's Research Forum - Available from: http://www.alzforum. org
79. H. Koprowski, Y.M. Zheng, E. Heber-Katz, N. Fraser, L. Rorke, and Z.F. Fu In vivo expression of inducible nitric oxide synthase in experimentally induced neurologic diseases Proc Natl Acad Sci USA 90 1993 3024 3027
80. E.M. Cantin, D.R. Hinton, J. Chen, and H. Openshaw Gamma interferon expression during acute and latent nervous system infection by herpes simplex virus type1 J Virol 69 1995 4898 4905
81. U. Meyding-Lamade, J. Haas, W. Lamade, K. Stingele, R. Kehm, and A. Fath Herpes simplex virus encephalitis: long-term comparative study of viral load and the expression of immunologic nitric oxide synthase in mouse brain tissue Neurosci Lett 244 1998 9 12
82. T. Valyi-Nagi, and T.S. Dermody Role of oxidative damage in the pathogenesis of viral infections of the nervous system Histol Histopathol 20 2005 957 967
83. C.N. Bassett, and T.J. Montine Lipoproteins and lipid peroxidation in Alzheimer's disease J Nutr Health Aging 7 2003 24 29
84. C.A. Colton, C.M. Brown, D. Cook, L.K. Needham, Q. Xu, and M. Czapiga APOE and the regulation of microglial nitric oxide production: a link between genetic risk and oxidative stress Neurobiol Aging 23 2002 777 785
85. W.R. Lin, R. Jennings, T.L. Smith, M.A. Wozniak, and R.F. Itzhaki Vaccination prevents latent HSV1 infection of mouse brain Neurobiol Aging 22 2001 699 703