APP processing induced by herpes simplex virus type 1 (HSV-1) yields several APP fragments in human and rat neuronal cells

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  De Chiara, Giovanna ^a   Marcocci, Maria Elena ^b   Civitelli, Livia ^b   Argnani, Rafaela ^c   Piacentini, Roberto ^d   Ripoli, Cristian ^d   Manservigi, Roberto ^c   Grassi, Claudio ^d   Garaci, Enrico ^e   Palamara, Anna Teresa ^b,f  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF FERRARA   (Italy)

^d CATHOLIC UNIVERSITY   (Italy)

^e UNIVERSITY OF ROME TOR VERGATA   (Italy)

^f IRCCS SAN RAFFAELE PISANA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; CASPASE 3; GAMMA SECRETASE; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN (1 42); AMYLOID BETA-PROTEIN (1-42); PEPTIDE FRAGMENT;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; GENOMIC FRAGMENT; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; NERVE CELL; NONHUMAN; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN PROCESSING; PROTEIN SYNTHESIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; VIRUS REACTIVATION; VIRUS TITRATION; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CHEMISTRY; CONFOCAL MICROSCOPY; CYTOLOGY; GENETICS; HELA CELL; HOST PATHOGEN INTERACTION; METABOLISM; MUTATION; NEUROBLASTOMA; PATHOLOGY; PHYSIOLOGY; PROTEIN MULTIMERIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; VIROLOGY;

HUMAN HERPESVIRUS 1; RATTUS;

AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELLS, CULTURED; HELA CELLS; HERPESVIRUS 1, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; MICROSCOPY, CONFOCAL; MUTATION; NEUROBLASTOMA; NEURONS; PEPTIDE FRAGMENTS; PROTEIN MULTIMERIZATION; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 78649757007     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013989     Document Type: Article

References (57)

1. Schmutzhard E (2001) Viral infections of the CNS with special emphasis on herpes simplex infections. J Neurol 248: 469-477.
2. Jamieson GA, Maitland NJ, Wilcock GK, Craske J, Itzhaki RF (1991) Latent herpes simplex virus type 1 in normal and Alzheimer's disease brains. J Med Virol 33: 224-227.
3. Itabashi S, Arai H, Matsui T, Higuchi S, Sasaki H (1997) Herpes simplex virus and risk of Alzheimer's disease. Lancet 349: 1102.
4. Wozniak MA, Shipley SJ, Combrinck M, Wilcock GK, Itzhaki RF (2005) Productive herpes simplex virus in brain of elderly normal subjects andAlzheimer's disease patients. J Med Virol 75: 300-306.
5. Kastrukoff L, Hamada T, Schumacher U, Long C, Doherty PC, et al. (1982) Central nervous system infection and immune response in mice inoculated into the lip with herpes simplex virus type 1. J Neuroimmunol 2: 295-305.
6. Dobson CB, Itzhaki RF (1999) Herpes Simplex virus type 1 and Alzheimer's disease. Neurobiol Aging 20: 457-465.
7. Lewandowski G, Zimmerman MN, Denk LL, Porter DD, Prince GA (2002) Herpes simplex type 1 infects and establishes latency in the brain and trigeminal ganglia during primary infection of the lip in cotton rats and mice. Arch Virol 147: 167-179.
8. Ball MJ (1982) Limbic predilection in Alzheimer dementia: is reactivated herpes virus involved? Can J Neurol Sci 9: 303-306.
9. Selkoe DJ (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 81: 741-766.
10. Deatly AM, Haase AT, Fewster PH, Lewis E, Ball MJ (1990) Human herpes virus infections and Alzheimer's disease. Neuropathol Appl Neurobiol 16: 213-223.
11. Jamieson GA, Maitland NJ, Craske J, Wilcock GK, Itzhaki RF (1991) Detection of herpes simplex virus type 1 DNA sequences in normal and Alzheimer's disease brains using polymerase chain reaction. Biochem Soc Trans 19: 122S.
12. Hill JM, Gebhardt BM, Azcuy AM, Matthews KE, Lukiw WJ, et al. (2005) Can a herpes simplex virus type 1 neuroinvasive score be correlated to other risk factors in Alzheimer's disease? Med Hypotheses 64: 320-327.
13. Mori I, Kimura Y, Naiki H, Matsubara R, Takeuchi T, et al. (2004)Reactivation of HSV-1 in the brain of patients with familial Alzheimer's disease. J Med Virol 73: 605-611.
14. Itzhaki RF (2004) Herpes simplex virus type 1, apolipoprotein E and Alzheimer' disease. Herpes 11(Suppl 2): 77A-82A.
15. Letenneur L, Peres K, Fleuri H, Garrigue I, Barberger-Gateau P, et al. (2008) Sieropositive to herpes virus antibodies and risk of Alzheimer's disease: a population-based cohort study. Plos One 3: e3637.
16. Sinha S, Anderson JP, Barbour R, Basi GS, Caccavello R, et al. (1999) Purification and cloning of amyloid precursor protein beta-secretase from human brain. Nature 402: 537-540.
17. Vassar R (2001) The beta-secretase, BACE: a prime drug target for Alzheimer's disease. J Mol Neurosci 17: 157-170.
18. MÜller T, Meyer HE, Egensperger R, Marcus K (2008) The amyloid precursor protein intracellular domain (AICD) as modulator of gene expression, apoptosis, and cytoskeletal dynamics-relevance for Alzheimer's disease. Prog Neurobiol 85: 393-406.
19. Chyung AS, Greenberg BD, Cook DG, Doms RW, Lee VM (1997) Novel betasecretase cleavage of beta-amyloid precursor protein in the endoplasmic reticulum/intermediate compartment of NT2N cells. J Cell Biol 138: 671-680.
20. Cook DG, Forman MS, Sung JC, Leight S, Kolson DL, et al. (1997) Alzheimer's Abeta (1-42) is generated in the endoplasmic reticulum/intermediate compartment of NT2N cells. Nat Med 3: 1021-1023.
21. Hartman T, Bieger SC, Bruhl B, Tienari PJ, Ida N, et al. (1997) Distinct sites of intracellular production for Alzheimer's disease Abeta 40/42 amyloid peptides. Nat Med 3: 1016-1020.
22. Xu H, Sweeney D, Wang R, Thinakaran C, Lo AC, et al. (1997) Generation of Alzheimer beta-amyloid protein in the trans-Golgi network in the apparent absence of vesicle formation. Proc Natl Acad Sci USA 94: 3748-3752.
23. Koo EH, Squazzo SL (1994) Evidence that production and release of amyloid beta-protein involves the endocytic pathway. J Biol Chem 269: 17386-17389.
24. LaFerla FM, Green KN, Oddo S (2007) Intracellular amyloid-beta in Alzheimer's disease. Nat Rev Neurosci 8: 499-509.
25. Lu DC, Rabizadeh S, Chandra S, Shayya RF, Ellerby LM, et al. (2000) A second cytotoxic proteolytic peptide derived from amyloid beta-protein precursor. Nat Med 6: 397-404.
26. Park SH, Shaked GM, Bredesen DE, Koo EH (2009) Mechanism of cytotoxicity mediated by the C31 fragment of amyloid precursor protein. Biochem Biophys Res Comm 388: 450-455.
27. Cribbs DH, Azizeh BY, Cotman CW, LaFerla FM (2000) Fibril formation and neurotoxicity by a herpes simplex virus glycoprotein B fragment with homology to the Alzheimer's A beta peptide. Biochemistry 39: 5988-5994.
28. Bearer EL (2004) Perspectives on herpes-APP interactions. Aging cell 3: 81-84.
29. Satpute-Krishnan P, De Giorgis JA, Bearer EL (2003) Fast anterograde transport of herpes simplex virus: role for the amyloid precursor protein of Alzheimer disease. Aging cell 2: 305-318.
30. Satpute-Krishnan P, De Giorgis JA, Conley MP, Jang M, Bearer EL (2006) A peptide zipcode sufficient for anterograde transport within amyloid precursor protein. Proc Natl Acad Sci USA 103: 16532-16537.
31. Wozniak MA, Mee AP, Itzhaki RF (2009) Herpes simplex virus type 1 DNA is located within Alzheimer's disease amyloid plaques. J Pathol 217: 131-138.
32. Shipley SJ, Parkin ET, Ithzaki RF, Dobson CB (2005) Herpes simplex virus interferes with amyloid precursor protein processing. BMC Microbiol 5: 48.
33. Wozniak MA, Itzhaki RF, Shipley SJ, Dobson CB (2007) Herpes simplex virus infection causes cellular -amyloid accumulation and secretase upregulation. Neuroscience Letters 429: 95-100.
34. Piacentini R, Civitelli L, Ripoli C, Marcocci ME, De Chiara G, et al. (2010) HSV-1 promotes Ca2+-mediated APP phosphorylation and Ab accumulation in rat cortical neurons. Neurobiol Aging. In press.
35. Fan YW, Cui FZ, Hou SP, Xu QY, Chen LN, et al. (2002) Culture of neural cells on silicon wafers with nano-scale surface topograph. J Neurosci Methods 120: 17-23.
36. Killington RA, Powell KL (1991) Growth, Assay and Purification of Herpesviruses. In: Mahy BWJ, ed. Virology: a pratical approach. Oxford: IRL Press. pp 212-213.
37. Gianni D, Zambrano N, Bimonte M, Minopoli G, Mercken L, et al. (2003) Platelet-derived growth factor induces the beta-gamma-secretase-mediated cleavage of alzheimer's amyloid precursor protein through a Src-Rac-dependent pathway. J Biol Chem 278: 9290-9297.
38. Piacentini R, Ripoli C, Mezzogori D, Azzera GB, Grassi C (2008) Extremely low-frequency electromagnetic fields promote in vitro neurogenesis via upregulation of Cav1-channel activity. J Cell Physiol 215: 129-193.
39. Matis J, Kudelova M (2001) Early shutoff of host protein synthesis in cells infected with herpes simplex viruses. Acta Virol 45: 269-277.
40. Kwong AD, Frenkel N (1989) The herpes simplex virus virion host shutoff function. J Virol 63: 4834-4839.
41. Roizmann B, Knipe DM (2001) Herpes Simplex Virus and Their Replication. In: Knipe DM, Howley PM, eds. Fields Virology. Philadelphia, PA, USA: Lippincott Williams and Wilkins. pp 2432-2434.
42. He B, Gross M, Roizman B (1998) The c134.5 protein of herpes simplex virus 1 has the structural and functional attributes of a protein phosphatase 1 regulatory subunit and is present in a high molecular weight complex with the enzyme in infected cells. J Biol Chem 273: 20737-20743.
43. Lesné S, Koh MT, Kotilinek L, Kayed R, Glabe CG, et al. (2006) A specific amyloid-b protein assembly in the brain impairs memory. Nature 440: 352-357.
44. Skovronsky DM, Doms RW, Lee VMY (1998) Detection of a novel intraneuronal pool of insoluble amyloid beta protein that accumulates with time in culture. J Cell Biol 141: 1031-1039.
45. Ohyagi Y, Asahara H, Chui DH, Tsuruta Y, Sakae N, et al. (2005) Intracellular Abeta42 activates p53 promoter: a pathway to neurodegeneration in Alzheimer's disease. FASEB J 19: 255-257.
46. Tamagno E, Bardini P, Obbili A, Vitali A, Borghi R, et al. (2002) Oxidative stress increases expression and activity of BACE in NT2 neurons. Neurobiol Dis 10: 279-288.
47. Tamagno E, Parola M, Bardini P, Piccini A, Borghi R, et al. (2005) Beta-site APP cleaving enzyme up-regulation induced by 4-hydroxynonenal is mediated by stress-activated protein kinases pathways. J Neurochem 92: 628-636.
48. Tamagno E, Guglielmotto M, Aragno M, Borghi R, Autelli R, et al. (2008) Oxidative stress activates a positive feedback between the gamma- and betasecretase cleavages of the beta-amyloid precursor protein. J Neurochem 104: 683-695.
49. Palamara AT, Perno CF, Ciriolo MR, Dini L, Balestra E, et al. (1995) Evidence for antiviral activity of glutathione: in vitro inhibition of herpes simplex virus type 1 replication. Antiviral Res 27: 237-253.
50. Valyi-Nagy T, Dermody TS (2005) Role of oxidative damage in the pathogenesis of viral infections of the nervous system. Histol Histopathol 20: 957-967.
51. Kavouras JH, Prandovszky E, Valyi-Nagy K, Kovacs SK, Tiwari V, et al. (2007) Herpes simplex virus type 1 infection induces oxidative stress and the release of bioactive lipid peroxidation by-products in mouse P19N neural cell cultures. J Neurovirol 13: 416-425.
52. Fujii S, Akaike T, Maeda H (1999) Role of nitric oxide in pathogenesis of herpes simplex virus encephalitis in rats. Virology 256: 203-212.
53. Valyi-Nagy T, Olson SJ, Valyi-Nagy K, Montine TJ, Dermody TS (2000) Herpes simplex virus type 1 latency in the murine nervous system is associated with oxidative damage to neurons. Virology 278: 309-321.
54. Lu DC, Rabizadeh S, Chandra S, Shayya RF, Ellerby LM, et al. (2000) A second cytotoxic proteolytic peptide derived from amyloid beta-protein precursor. Nat Med 4: 397-404.
55. Chang KA, Suh YH (2005) Pathophysiological roles of amyloidogenic carboxyterminal fragments of the beta amyloid precursor protein in Alzheimer's disease. J Pharmacol Sci 97: 461-471.
56. Muller T, Concannon CG, Word MW, Walsh CN, Tirniceriu AL, et al. (2007) Modulation f gene expression and cytoskeletal dynamics by amyloid precursor protein intracellular domain (AICD). Mol Biol Cell 18: 201-210.
57. Goodger ZV, Rajendran L, Trutzell A, Kohli BM, Nitsck RM, et al. (2009) Nuclear signalling by the APP intracellular domain occurs predominantlythrough the amyloidogenic processing pathway. J Cell Sci 122: 3703-3714.