Intracerebral adeno-associated virus gene delivery of apolipoprotein E2 markedly reduces brain amyloid pathology in Alzheimer's disease mouse models

Neurobiology of Aging

Volumn 44, Issue , 2016, Pages 159-172

  Zhao, Lingzhi ^a   Gottesdiener, Andrew J ^a   Parmar, Mayur ^a   Li, Mingjie ^b   Kaminsky, Stephen M ^c   Chiuchiolo, Maria J ^c   Sondhi, Dolan ^c   Sullivan, Patrick M ^d   Holtzman, David M ^b   Crystal, Ronald G ^c   Paul, Steven M ^a  

^a FEIL FAMILY BRAIN AND MIND RESEARCH INSTITUTE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Adeno associated virus; Alzheimer's disease; Amyloid pathology; Apolipoprotein E2; Gene delivery

Indexed keywords

ADENOVIRUS VECTOR; AMYLOID BETA PROTEIN; APOLIPOPROTEIN E2; APOLIPOPROTEIN E4;

ADULT; ALZHEIMER DISEASE; AMYLOIDOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOE2 GENE; APOE4 GENE; ARTICLE; BRAIN LEVEL; CONTROLLED STUDY; DRUG EFFICACY; GENE EXPRESSION; INTRACEREBRAL DRUG ADMINISTRATION; INTRATHALAMIC DRUG ADMINISTRATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIRAL GENE DELIVERY SYSTEM; ALLELE; ANIMAL; BRAIN; DEPENDOPARVOVIRUS; DISEASE MODEL; GENE THERAPY; GENE TRANSFER; GENE VECTOR; GENETICS; GENOTYPE; KNOCKOUT MOUSE; METABOLISM; MOLECULARLY TARGETED THERAPY; ONSET AGE; PATHOLOGY; PROCEDURES; RISK FACTOR;

AGE OF ONSET; ALLELES; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; APOLIPOPROTEIN E2; BRAIN; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GENETIC VECTORS; GENOTYPE; MICE, KNOCKOUT; MOLECULAR TARGETED THERAPY; RISK FACTORS;

EID: 84973342068     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2016.04.020     Document Type: Article

References (51)

1. Baek R.C., Broekman M.L., Leroy S.G., Tierney L.A., Sandberg M.A., D'Azzo A., Seyfried T.N., Sena-Esteves M. AAV-mediated gene delivery in adult GM1-gangliosidosis mice corrects lysosomal storage in CNS and improves survival. PLoS One 2010, 5:e13468.
2. Bales K.R., Liu F., Wu S., Lin S., Koger D., DeLong C., Hansen J.C., Sullivan P.M., Paul S.M. Human APOE isoform-dependent effects on brain β-amyloid levels in PDAPP transgenic mice. J. Neurosci. 2009, 29:6771-6779.
3. Bales K.R., Verina T., Dodel R.C., Du Y., Altstiel L., Bender M., Hyslop P., Johnstone E.M., Little S.P., Cummins D.J., Piccardo P., Ghetti B., Paul S.M. Lack of apolipoprotein E dramatically reduces amyloid β-peptide deposition. Nat. Genet. 1997, 17:263-264.
4. Boyles J.K., Pitas R.E., Wilson E., Mahley R.W., Taylor J.M. Apolipoprotein E associated with astrocytic glia of the central nervous system and with nonmyelinating glia of the peripheral nervous system. J. Clin. Invest. 1985, 76:1501-1513.
5. Carrasquillo M.M., Crook J.E., Pedraza O., Thomas C.S., Pankratz V.S., Allen M., Nguyen T., Malphrus K.G., Ma L., Bisceglio G.D., Roberts R.O., Lucas J.A., Smith G.E., Ivnik R.J., Machulda M.M., Graff-Radford N.R., Petersen R.C., Younkin S.G., Ertekin-Taner N. Late-onset Alzheimer's risk variants in memory decline, incident mild cognitive impairment, and Alzheimer's disease. Neurobiol. Aging 2015, 36:60-67.
6. Castellano J.M., Kim J., Stewart F.R., Jiang H., DeMattos R.B., Patterson B.W., Fagan A.M., Morris J.C., Mawuenyega K.G., Cruchaga C., Goate A.M., Bales K.R., Paul S.M., Bateman R.J., Holtzman D.M. Human apoE isoforms differentially regulate brain amyloid-β peptide clearance. Sci. Transl. Med. 2011, 3:89ra57.
7. Cearley C.N., Wolfe J.H. A single injection of an adeno-associated virus vector into nuclei with divergent connections results in widespread vector distribution in the brain and global correction of a neurogenetic disease. J. Neurosci. 2007, 27:9928-9940.
8. Corder E., Saunders A., Risch N., Strittmatter W., Schmechel D., Gaskell P., Rimmler J.B., Locke P.A., Conneally P.M., Schmader K.E., Small G.W., Roses A.D., Haines J.L., Pericak-Vance M.A. Protective effect of apolipoprotein E type 2 allele for late onset Alzheimer disease. Nat. Genet. 1994, 7:180-184.
9. Corder E.H., Saunders A.M., Strittmatter W.J., Schmechel D.E., Gaskell P.C., Small G.W., Roses A.D., Haines J.L., Pericak-Vance M.A. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 1993, 261:921-923.
10. Deane R., Sagare A., Hamm K., Parisi M., Lane S., Finn M.B., Holtzman D.M., Zlokovic B.V. ApoE isoform-specific disruption of amyloid beta peptide clearance from mouse brain. J. Clin. Invest. 2008, 118:4002-4013.
11. DeMattos R.B., Brendza R.P., Heuser J.E., Kierson M., Cirrito J.R., Fryer J., Sullivan P.M., Fagan A.M., Han X., Holtzman D.M. Purification and characterization of astrocyte-secreted apolipoprotein E and J-containing lipoproteins from wild-type and human apoE transgenic mice. Neurochem. Int. 2001, 39:415-425.
12. Dodart J.C., Marr R.A., Koistinaho M., Gregersen B.M., Malkani S., Verma I.M., Paul S.M. Gene delivery of human apolipoprotein E alters brain Aβ burden in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:1211-1216.
13. Fagan A.M., Watson M., Parsadanian M., Bales K.R., Paul S.M., Holtzman D.M. Human and murine ApoE markedly alters Aβ metabolism before and after plaque formation in a mouse model of Alzheimer's disease. Neurobiol. Dis. 2002, 9:305-318.
14. Fan J., Donkin J., Wellington C. Greasing the wheels of Aβ clearance in Alzheimer's disease: the role of lipids and apolipoprotein E. Biofactors 2009, 35:239-248.
15. Farrer L.A., Cupples L.A., Haines J.L., Hyman B., Kukull W.A., Mayeux R., Myers R.H., Pericak-Vance M.A., Risch N., van Duijn C.M. Effects of age, sex, and ethnicity on the association between apolipoprotein E genotype and Alzheimer disease: a meta-analysis. JAMA 1997, 278:1349-1356.
16. Franklin K.B.J., Paxinos G. The mouse brain in Stereotaxic Coordinates 2007, Elsevier Inc, New York. 3rd edition.
17. Games D., Adams D., Alessandrini R., Barbour R., Berthelette P., Blackwell C., Carr T., Clemens J., Donaldson T., Gillespie F., Guido T., Hagopian S., Johnson-wood K., Khan K., Lee M., Leibowitz P., Lieberburg I., Little S., Maslian E., Mcconlogue L., Montoya-zavala M., Mucke L., Paganini L., Penniman E., Power M., Schenk D., Seubert P., Snyder B., Soriano F., Tan H., Vitale J., Wadsworth S., Wolozin B., Zhao J. Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature 1995, 373:523-527.
18. Haass C., Selkoe D.J. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid β-peptide. Nat. Rev. Mol. Cell Biol. 2007, 8:101-112.
19. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297:353-356.
20. Hashimoto T., Serrano-Pozo A., Hori Y., Adams K.W., Takeda S., Banerji A.O., Mitani A., Joyner D., Thyssen D.H., Bacskai B.J., Frosch M.P., Spires-Jones T.L., Finn M.B., Holtzman D.M., Hyman B.T. Apolipoprotein E, especially apolipoprotein E4, increases the oligomerization of amyloid beta peptide. J. Neurosci. 2012, 32:15181-15192.
21. Hatters D.M., Peters-Libeu C.A., Weisgraber K.H. Apolipoprotein E structure: insights into function. Trends Biochem. Sci. 2006, 31:445-454.
22. Holtzman D.M., Bales K.R., Tenkova T., Fagan A.M., Parsadanian M., Sartorius L.J., Mackey B., Olney J., McKeel D., Wozniak D., Paul S.M. Apolipoprotein E isoform-dependent amyloid deposition and neuritic degeneration in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:2892-2897.
23. Holtzman D.M., Herz J., Bu G. Apolipoprotein E and apolipoprotein E receptors: normal biology and roles in Alzheimer disease. Cold Spring Harb. Perspect. Med. 2012, 2:a006312.
24. Hudry E., Dashkoff J., Roe A.D., Takeda S., Koffie R.M., Hashimoto T., Scheel M., Spires-Jones T., Arbel-Ornath M., Betensky R., Davidson B.L., Hyman B.T. Gene transfer of human Apoe isoforms results in differential modulation of amyloid deposition and neurotoxicity in mouse brain. Sci. Transl. Med. 2013, 5:212ra161.
25. Johnson-Wood K., Lee M., Motter R., Hu K., Gordon G., Barbour R., Khan K., Gordon M., Tan H., Games D., Lieberburg I., Schenk D., Seubert P., McConlogue L. Amyloid precursor protein processing and Aβ42 deposition in a transgenic mouse model of Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:1550-1555.
26. Kells A.P., Hadaczek P., Yin D., Bringas J., Varenika V., Forsayeth J., Bankiewicz K.S. Efficient gene therapy-based method for the delivery of therapeutics to primate cortex. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:2407-2411.
27. Kim J., Basak J.M., Holtzman D.M. The role of apolipoprotein E in Alzheimer's disease. Neuron 2009, 63:287-303.
28. Kim J., Jiang H., Park S., Eltorai A.E., Stewart F.R., Yoon H., Basak J.M., Finn M.B., Holtzman D.M. Haploinsufficiency of human APOE reduces amyloid deposition in a mouse model of amyloid-β amyloidosis. J. Neurosci. 2011, 31:18007-18012.
29. Lambert J., Ibrahim-Verbaas C.A., Harold D., Naj A.C., Sims R., Bellenguez C., DeStafano A.L., Bis J.C., Beecham G.W., Grenier-Boley B., Russo G., Thorton-Wells T.A., Jones N., Smith A.V., Chouraki V., Thomas C., Ikram M.A., Zelenika D., Vardarajan B.N., Kamatani Y., Lin C.F., Gerrish A., Schmidt H., Kunkle B., Dunstan M.L., Ruiz A., Bihoreau M.T., Choi S.H., Reitz C., Pasquier F., Cruchaga C., Craig D., Amin N., Berr C., Lopez O.L., De Jager P.L., Deramecourt V., Johnston J.A., Evans D., Lovestone S., Letenneur L., Morón F.J., Rubinsztein D.C., Eiriksdottir G., Sleegers K., Goate A.M., Fiévet N., Huentelman M.W., Gill M., Brown K., Kamboh M.I., Keller L., Barberger-Gateau P., McGuiness B., Larson E.B., Green R., Myers A.J., Dufouil C., Todd S., Wallon D., Love S., Rogaeva E., Gallacher J., St George-Hyslop P., Clarimon J., Lleo A., Bayer A., Tsuang D.W., Yu L., Tsolaki M., Bossù P., Spalletta G., Proitsi P., Collinge J., Sorbi S., Sanchez-Garcia F., Fox N.C., Hardy J., Deniz Naranjo M.C., Bosco P., Clarke R., Brayne C., Galimberti D., Mancuso M., Matthews F., Moebus S., Mecocci P., Del Zompo M., Maier W., Hampel H., Pilotto A., Bullido M., Panza F., Caffarra P., Nacmias B., Gilbert J.R., Mayhaus M., Lannefelt L., Hakonarson H., Pichler S., Carrasquillo M.M., Ingelsson M., Beekly D., Alvarez V., Zou F., Valladares O., Younkin S.G., Coto E., Hamilton-Nelson K.L., Gu W., Razquin C., Pastor P., Mateo I., Owen M.J., Faber K.M., Jonsson P.V., Combarros O., O'Donovan M.C., Cantwell L.B., Soininen H., Blacker D., Mead S., Mosley T.H., Bennett D.A., Harris T.B., Fratiglioni L., Holmes C., de Bruijn R.F., Passmore P., Montine T.J., Bettens K., Rotter J.I., Brice A., Morgan K., Foroud T.M., Kukull W.A., Hannequin D., Powell J.F., Nalls M.A., Ritchie K., Lunetta K.L., Kauwe J.S., Boerwinkle E., Riemenschneider M., Boada M., Hiltuenen M., Martin E.R., Schmidt R., Rujescu D., Wang L.S., Dartigues J.F., Mayeux R., Tzourio C., Hofman A., Nöthen M.M., Graff C., Psaty B.M., Jones L., Haines J.L., Holmans P.A., Lathrop M., Pericak-Vance M.A., Launer L.J., Farrer L.A., van Duijn C.M., Van Broeckhoven C., Moskvina V., Seshadri S., Williams J., Schellenberg G.D., Amouyel P. Meta-analysis of 74,046 individuals identifies 11 new susceptibility loci for Alzheimer's disease. Nat. Genet. 2013, 45:1452-1458. European Alzheimer's Disease Initiative (EADI), Genetic and Environmental Risk in Alzheimer's DiseaseGenetic and Environmental Risk in Alzheimer's Disease, Alzheimer's Disease Genetic ConsortiumAlzheimer's Disease Genetic Consortium, Cohorts for Heart and Aging Research in Genomic EpidemiologyCohorts for Heart and Aging Research in Genomic Epidemiology.
30. Lemere C.A., Masliah E. Can Alzheimer disease be prevented by amyloid-β immunotherapy?. Nat. Rev. Neurol. 2010, 6:108-119.
31. Li J., Kanekiyo T., Shinohara M., Zhang Y., LaDu M.J., Xu H., Bu G. Differential regulation of amyloid-beta endocytic trafficking and lysosomal degradation by apolipoprotein E isoforms. J. Biol. Chem. 2012, 287:44593-44601.
32. Liu C., Kanekiyo T., Xu H., Bu G. Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy. Nat. Rev. Neurol. 2013, 9:106-118.
33. Manelli A.M., Stine W.B., Van Eldik L.J., LaDu M.J. ApoE and Aβ1-42 interactions. J. Mol. Neurosci. 2004, 23:235-246.
34. Morris J.C., Roe C.M., Xiong C., Fagan A.M., Goate A.M., Holtzman D.M., Mintun M.A. APOE predicts amyloid-β but not tau Alzheimer pathology in cognitively normal aging. Ann. Neurol. 2010, 67:122-131.
35. Ramanan V., Risacher S., Nho K., Kim S., Swaminathan S., Shen L., Foroud T.M., Hakonarson H., Huentelman M.J., Aisen P.S., Petersen R.C., Green R.C., Jack C.R., Koeppe R.A., Jagust W.J., Weiner M.W., Saykin A.J. APOE and BCHE as modulators of cerebral amyloid deposition: a florbetapir PET genome-wide association study. Mol. Psychiatry 2013, 19:351-357.
36. Rebeck G.W., Reiter J.S., Strickland D.K., Hyman B.T. Apolipoprotein E in sporadic Alzheimer's disease: allelic variation and receptor interactions. Neuron 1993, 11:575-580.
37. Reiman E.M., Chen K., Liu X., Bandy D., Yu M., Lee W., Ayutyanont N., Keppler J., Reeder S.A., Langbaum J.B., Alexander G.E., Klunk W.E., Mathis C.A., Price J.C., Aizenstein H.J., DeKosky S.T., Caselli R.J. Fibrillar amyloid-β burden in cognitively normal people at 3 levels of genetic risk for Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:6820-6825.
38. Saunders A.M., Strittmatter W.J., Schmechel D., George-Hyslop P.H., Pericak-Vance M.A., Joo S.H., Rosi B.L., Gusella J.F., Crapper-MacLachlan D.R., Alberts M.J. Association of apolipoprotein E allele epsilon 4 with late-onset familial and sporadic Alzheimer's disease. Neurology 1993, 43:1467-1472.
39. Schmechel D.E., Saunders A.M., Strittmatter W.J., Crain B.J., Hulette C.M., Joo S.H., Pericak-Vance M.A., Goldgaber D., Roses A.D. Increased amyloid β-peptide deposition in cerebral cortex as a consequence of apolipoprotein E genotype in late-onset Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:9649-9653.
40. Sondhi D., Hackett N.R., Peterson D.A., Stratton J., Baad M., Travis K.M., Wilson J.M., Crystal R.G. Enhanced survival of the LINCL mouse following CLN2 gene transfer using the rh.10 rhesus macaque-derived adeno-associated virus vector. Mol. Ther. 2007, 15:481-491.
41. Sondhi D., Johnson L., Purpura K., Monette S., Souweidane M.M., Kaplitt M.G., Kosofsky B., Yohay K., Ballon D., Dyke J., Kaminksy S.M., Hackett N.R., Crystal R.G. Long-term expression and safety of administration of AAVrh.10hCLN2 to the brain of rats and nonhuman primates for the treatment of late infantile neuronal ceroid lipofuscinosis. Hum. Gene Ther. Method 2012, 23:324-335.
42. Strittmatter W.J., Saunders A.M., Schmechel D., Pericak-Vance M., Enghild J., Salvesen G.S., Roses A.D. Apolipoprotein E: high-avidity binding to β-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:1977-1981.
43. Sullivan P., Han B., Liu F., Mace B., Ervin J., Wu S., Koger D., Paul S., Bales K.R. Reduced levels of human apoE4 protein in an animal model of cognitive impairment. Neurobiol. Aging 2011, 32:791-801.
44. Sullivan P.M., Mezdour H., Aratani Y., Knouff C., Najib J., Reddick R.L., Quarfordt S.H., Maeda N. Targeted replacement of the mouse apolipoprotein E gene with the common human APOE3 allele enhances diet-induced hypercholesterolemia and atherosclerosis. J. Biol. Chem. 1997, 272:17972-17980.
45. Suri S., Heise V., Trachtenberg A.J., Mackay C.E. The forgotten APOE allele: a review of the evidence and suggested mechanisms for the protective effect of APOE e2. Neurosci. Biobehav. Rev. 2013, 37:2878-2886.
46. Talbot C., Lendon C., Craddock N., Shears S., Morris J., Goate A. Protection against Alzheimer's disease with apoE epsilon 2. Lancet 1994, 343:1432-1433.
47. Walker L., Pahnke J., Madauss M., Vogelgesang S., Pahnke A., Herbst E., Stausske D., Walther R., Kessler C., Warzok R.W. Apolipoprotein E4 promotes the early deposition of Aβ42 and then Aβ40 in the elderly. Acta Neuropathol. 2000, 100:36-42.
48. Youmans K.L., Tai L.M., Nwabuisi-Heath E., Jungbauer L., Kanekiyo T., Gan M., Kim J., Eimer W.A., Estus S., Rebeck G.W., Weeber E.J., Bu G., Yu C., Ladu M.J. APOE4-specific changes in Abeta accumulation in a new transgenic mouse model of Alzheimer disease. J. Biol. Chem. 2012, 287:41774-41786.
49. Yu J., Tan L., Hardy J. Apolipoprotein E in Alzheimer's disease: an update. Annu. Rev. Neurosci. 2014, 37:79-100.
50. Zhao L., Lin S., Bales K.R., Gelfanova V., Koger D., Delong C., Hale J., Liu F., Hunter J.M., Paul S.M. Macrophage-mediated degradation of β-amyloid via an apolipoprotein E isoform-dependent mechanism. J. Neurosci. 2009, 29:3603-3612.
51. Zolotukhin S., Potter M., Zolotukhin I., Sakai Y., Loiler S., Fraites T.J., Chiodo V.A., Phillipsberg T., Muzyczka N., Hauswirth W.W., Flotte T.R., Byrne B.J., Snyder R.O. Production and purification of serotype 1, 2, and 5 recombinant adeno-associated viral vectors. Methods 2002, 28:158-167.