Reduction of amyloid-beta levels in mouse eye tissues by intra-vitreally delivered neprilysin

Experimental Eye Research

Volumn 138, Issue , 2015, Pages 134-144

  Parthasarathy, Rajni ^a,b   Chow, K Martin ^c   Derafshi, Zahra ^b   Fautsch, Michael P ^d   Hetling, John R ^b   Rodgers, David W ^c   Hersh, Louis B ^c   Pepperberg, David R ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b University of Illinois at Chicago   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d MAYO CLINIC   (United States)

Author keywords

5XFAD mouse; Amyloid beta; C57BL 6J mouse; Electroretinogram; Intra vitreal injection; Neprilysin

Indexed keywords

AMYLOID BETA PROTEIN; MEMBRANE METALLOENDOPEPTIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRORETINOGRAM; ELECTRORETINOGRAPHY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; EXTRACELLULAR SPACE; EYE; HYDROLYSIS; MICROENVIRONMENT; MOLECULAR WEIGHT; MOUSE; NONHUMAN; OPTIC NERVE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN TISSUE LEVEL; RETINA DISEASE; TISSUE HOMOGENATE; TISSUE LEVEL; VITREOUS BODY; WILD TYPE; AGED; ANIMAL; C57BL MOUSE; CHOROID; DISEASE MODEL; DONOR; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; INTRAVITREAL DRUG ADMINISTRATION; LENS; METABOLISM; MIDDLE AGED; RETINA; TRANSGENIC MOUSE; VERY ELDERLY;

AGED; AGED, 80 AND OVER; AMYLOID BETA-PEPTIDES; ANIMALS; CHOROID; DISEASE MODELS, ANIMAL; ELECTRORETINOGRAPHY; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; INTRAVITREAL INJECTIONS; LENS, CRYSTALLINE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MIDDLE AGED; NEPRILYSIN; RETINA; TISSUE DONORS; VITREOUS BODY;

EID: 84938944641     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2015.06.027     Document Type: Article

References (78)

1. Abramov E., Dolev I., Fogel H., Ciccotosto G.D., Ruff E., Slutsky I. Amyloid-β as a positive endogenous regulator of release probability at hippocampal synapses. Nat. Neurosci. 2009, 12:1567-1576. 10.1038/nn.2433.
2. Alexandrov P.N., Pogue A., Bhattacharjee S., Lukiw W.J. Retinal amyloid peptides and complement factor H in transgenic models of Alzheimer's disease. NeuroReport 2011, 22:623-627. 10.1097/WNR.0b013e3283497334.
3. Bates K.A., Verdile G., Li Q.X., Ames D., Hudson P., Masters C.L., Martins R.N. Clearance mechanisms of Alzheimer's amyloid-beta peptide: implications for therapeutic design and diagnostic tests. Mol. Psychiatry. 2009, 14:469-486. 10.1038/mp.2008.96.
4. Beatty S., Koh H.-H., Phil M., Henson D., Boulton M. The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv. Ophthalmol. 2000, 45:115-134. 10.1016/S0039-6257(00)00140-5.
5. Benilova I., Karran E., De Strooper B. The toxic Aβ oligomer and Alzheimer's disease: an emperor in need of clothes. Nat. Neurosci. 2012, 15:349-357. 10.1038/nn.3028.
6. Bruban J., Maoui A., Chalour N., An N., Jonet L., Feumi C., Tréton J., Sennlaub F., Behar-Cohen F., Mascarelli F., Dinet V. CCR2/CCl2-mediated inflammation protects photoreceptor cells from amyloid-β-induced apoptosis. Neurobiol. Dis. 2011, 42:55-72. 10.1016/j.nbd.2011.01.004.
7. Burdick D.1, Kosmoski J., Knauer M.F., Glabe C.G. Preferential adsorption, internalization and resistance to degradation of the major isoform of the Alzheimer's amyloid peptide, Abeta 1-42, in differentiated PC12 cells. Brain Res. 1997, 746:275-284. 10.1016/S0006-8993(96)01262-0.
8. Cano M., Thimmalappula R., Fujihara M., Nagai N., Sporn M., Wang A.L., Neufeld A.H., Biswal S., Handa J.T. Cigarette smoking, oxidative stress, and anti-oxidant response through Nrf2 signaling, and age-related macular degeneration. Vis. Res. 2010, 50:652-666. 10.1016/j.visres.2009.08.018.
9. Carson J.A., Turner A.J. β-Amyloid catabolism: roles for neprilysin (NEP) and other metallopeptidases?. J. Neurochem. 2002, 81:1-8. 10.1046/j.1471-4159.2002.00855.x.
10. Carvalho C., Katz P.S., Dutta S., Katakam P.V.G., Moreira P.I., Busija D.W. Increased susceptibility to amyloid-β toxicity in rat brain microvascular endothelial cells under hyperglycemic conditions. J. Alzheimer's Dis. 2014, 38:75-83. 10.3233/JAD-130464.
11. Dahlgren K.N., Manelli A.M., Stine W.B., Baker L.K., Kraft G.A., LaDu M.J. Oligomeric and fibrillar species of amyloid-β peptides differentially affect neuronal viability. J. Biol. Chem. 2002, 277:32046-32053. 10.1074/jbc.M201750200.
12. Dale G.E., D'Arcy B., Yuvaniyama C., Wipf B., Oefner C., D'Arcy A. Purification and crystallization of the extracellular domain of human neutral endopeptidase (neprilysin) expressed in Pichia pastoris. Acta Crystallogr. D. Biol. Crystallogr. 2000, 56:894-897. 10.1107/S0907444900004947.
13. Dasari B., Prasanthi J.R.P., Marwarha G., Singh B.B., Ghribi O. Cholesterol-enriched diet causes age-related macular degeneration-like pathology in rabbit retina. BMC Ophthalmol. 2011, 11:22. 10.1186/1471-2415-11-22.
14. Dentchev T., Milam A.H., Lee V.M., Trojanowski J.Q., Dunaief J.L. Amyloid-beta is found in drusen from some age-related macular degeneration retinas, but not in drusen from normal retinas. Mol. Vis. 2003, 9:184-190. 10.1016/S0002-9394(03)00804-3.
15. Ding J.-D., Lin J., Mace B.E., Herrmann R., Sullivan P., Bowes Rickman C. Targeting age-related macular degeneration with Alzheimer's disease based immunotherapies: anti-amyloid-β attenuates pathologies in an age-related macular degeneration mouse model. Vis. Res. 2008, 48:339-345. 10.1016/j.visres.2007.07.025.
16. Ding J.-D., Johnson L.V., Herrmann R., Farsiu S., Smith S.G., Groelle M., Mace B.E., Sullivan P., Jamison J.A., Kelly U., Harrabi O., Bollini S.S., Dilley J., Kobayashi D., Kuang B., Li W., Pons J., Lin J.C., Bowes Rickman C. Anti-amyloid therapy protects against retinal pigmented epithelium damage and vision loss in a model of age-related macular degeneration. Proc. Natl. Acad. Sci. USA 2011, 108:E279-E287. 10.1073/pnas.1100901108.
17. Dong Z., Li J., Sun X., Hu H., He Y., Tan Z., Ge J. Cyclic intensive light exposure induces retinal lesions similar to age-related macular degeneration in APPswe/PS1 bigenic mice. BMC Neurosci. 2012, 13:34. 10.1186/1471-2202-13-34.
18. Edwards M.M., Rodríguez J.J., Gutierrez-Lanza R., Yates J., Verkhratsky A., Lutty G.A. Retinal macroglia changes in a triple transgenic mouse model of Alzheimer's disease. Exp. Eye Res. 2014, 127:252-260. 10.1016/j.exer.2014.08.006.
19. Gu L., Guo Z. Alzheimer's Aβ42 and Aβ40 peptides form interlaced amyloid fibrils. J. Neurochem.. 2013, 126:305-311. 10.1111/jnc.12202.
20. Guo L., Salt T.E., Luong V., Wood N., Cheung W., Maass A., Ferrari G., Russo-Marie F., Sillito A.M., Cheetham M.E., Moss S.E., Fitzke F.W., Cordeiro M.F. Targeting amyloid-β in glaucoma treatment. Proc. Natl. Acad. Sci. USA 2007, 104:13444-13449. 10.1073/pnas.0703707104.
21. Guo L.Y., Alekseev O., Li Y., Song Y., Dunaief J.L. Iron increases APP translation and amyloid-beta production in the retina. Exp. Eye Res. 2014, 129:31-37. 10.1016/j.exer.2014.10.012.
22. Hersh L.B., Rodgers D.W. Neprilysin and amyloid beta peptide degradation. Curr. Alzheimer's Res. 2008, 5:225-231. 10.2174/156720508783954703.
23. Hetling J.R., Pepperberg D.R. Sensitivity and kinetics of mouse flash responses determined in vivo from paired-flash electroretinograms. J. Physiol. 1999, 516:593-609. 10.1111/j.1469-7793.1999.0593v.x.
24. Hoh Kam J., Lenassi E., Jeffery G. Viewing ageing eyes: diverse sites of amyloid beta accumulation in the ageing mouse retina and the up-regulation of macrophages. PLoS One. 2010, 5:e13127. 10.1371/journal.pone.0013127.
25. Hubin E., van Nuland N.A.J., Broersen K., Pauwels K. Transient dynamics of Aβ contribute to toxicity in Alzheimer's disease. Cell. Molec. Life Sci. 2014, 71:3507-3521. 10.1007/s00018-014-1634-z.
26. Isas J.M., Luibl V., Johnson L.V., Kayed R., Wetzel R., Glabe C.G., Langen R., Chen J. Soluble and mature amyloid fibrils in drusen deposits. Invest. Ophthalmol. Vis. Sci. 2010, 51:1304-1310. 10.1167/iovs.09-4207.
27. Itkin A., Dupres V., Dufrene Y.F., Bechinger B., Ruysschaert J.-M., Roussens V. Calcium ions promote formation of amyloid-β-peptide (1-40) oligomers causally implicated in neuronal toxicity of Alzheimer's disease. PLoS One 2011, 6:e18250. 10.1371/journal.pone.0018250.
28. Iwata N., Tsubuki S., Takaki Y., Shirotani K., Lu B., Gerard N.P., Gerard C., Hama E., Lee H.J., Saido T.C. Metabolic regulation of brain Aβ by neprilysin. Science 2001, 292:1550-1552. 10.1126/science.1059946.
29. Janciauskiene S., Westin K., Grip O., Krakau T. Detection of Alzheimer peptides and chemokines in the aqueous humor. Eur. J. Ophthalmol. 2011, 21:104-111. 10.5301/EJO.2010.2108.
30. Johnson L.V., Leitner W.P., Rivest A.J., Staples M.K., Radeke M.J., Anderson D.H. The Alzheimer's Aβ peptide is deposited at sites of complement activation in pathologic deposits associated with aging and age-related macular degeneration. Proc. Natl. Acad. Sci. USA 2002, 99:11830-11835. 10.1073/pnas.192203399.
31. Kummer M.P., Heneka M.T. Truncated and modified amyloid-beta species. Alzheimer's Res. Ther. 2014, 6:28. 10.1186/alzrt258.
32. LaFerla F.M., Green K.N., Oddo S. Intracellular amyloid-β in Alzheimer's disease. Nat. Rev. Neurosci. 2007, 8:499-509. 10.1038/nrn2168.
33. Lee J.H., Pidaparti R.M., Atkinson G.M., Moorthy R.S. Design of an implantable device for ocular drug delivery. J. Drug Deliv. 2012, 2012:527516. 10.1155/2012/527516.
34. Li C., Hersh L.B. Neprilysin: assay methods, purification, and characterization. Meth. Enzymol. 1995, 248:253-263. 10.1016/0076-6879(95)48018-8.
35. Liu C., Cao L., Yang S., Xu L., Liu P., Wang F., Xu D. Subretinal injection of amyloid-β peptide accelerates RPE cell senescence and retinal degeneration. Int. J. Mol. Med. 2015, 35:169-176. 10.3892/ijmm.2014.1993.
36. Liu R.T., Gao J., Cao S., Cui J.Z., Chou C.L., Fang E., Matsubara J.A. Inflammatory mediators induced by amyloid-beta in the retina and RPE in vivo: implications for inflammasome activation in age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 2013, 54:2225-2237. 10.1167/iovs.12-10849.
37. Liu Y., Guan H., Beckett T.L., Juliano M.A., Juliano L., Song E.S., Chow K.M., Murphy M.P., Hersh L.B. In vitro and in vivo degradation of Aβ peptide by peptidases coupled to erythrocytes. Peptides 2007, 28:2348-2355. 10.1016/j.peptides.2007.09.015.
38. Liu Y., Studzinski C., Beckett T., Guan H., Hersh M.A., Murphy M.P., Klein R., Hersh L.B. Expression of neprilysin in skeletal muscle reduces amyloid burden in a transgenic mouse model of Alzheimer's disease. Molec. Ther. 2009, 8:1381-1386. 10.1038/mt.2009.115.
39. Liu Y., Studzinski C., Beckett T., Murphy M.P., Klein R.L., Hersh L.B. Circulating neprilysin clears brain amyloid. Molec. Cell. Neurosci. 2010, 45:101-107. 10.1016/j.mcn.2010.05.014.
40. Luibl V., Isas J.M., Kayed R., Glabe C.G., Langen R., Chen J. Drusen deposits associated with aging and age-related macular degeneration contain nonfibrillar amyloid oligomers. J. Clin. Invest. 2006, 6:378-385. 10.1172/JCI25843.
41. Malek G., Johnson L.V., Mace B.E., Saloupis P., Schmechel D.E., Rickman D.W., Toth C.A., Sullivan P.M., Bowes Rickman C. Apolipoprotein E allele-dependent pathogenesis: a model for age-related retinal degeneration. Proc. Natl. Acad. Sci. USA 2005, 102:11900-11905. 10.1073/pnas.0503015102.
42. Manzoni C., Colombo L., Bigini P., Diana V., Cagnotto A., Messa M., Lupi M., Bonetto V., Pignataro M., Airoldi C., Sironi E., Williams A., Salmona M. The molecular assembly of amyloid Aβ controls its neurotoxicity and binding to cellular proteins. PLoS One 2011, 6:e24909. 10.1371/journal.pone.0024909.
43. Morley J.E., Farr S.A. The role of amyloid-beta in the regulation of memory. Biochem.. Pharmacol. 2014, 88:479-485. 10.1016/j.bcp.2013.12.018.
44. Nalivaeva N.N., Belyaev N.D., Zhuravin I.A., Turner A.J. The Alzheimer's amyloid-degrading peptidase, neprilysin: can we control it?. Intern. J. Alzheimer's Dis. 2012, Article ID 383796. 10.1155/2012/383796.
45. Ning A., Cui J., To E., Ashe K.H., Matsubara J. Amyloid-β deposits lead to retinal degeneration in a mouse model of Alzheimer's disease. Invest. Ophthalmol. Vis. Sci. 2008, 49:5136-5143. 10.1167/iovs.08-1849.
46. Normando E.M., Coxon K.M., Guo L., Cordeiro M.F. Focus on: amyloid β. Exper. Eye Res. 2009, 89:446-447. 10.1016/j.exer.2009.05.004.
47. Oakley H., Cole S.L., Logan S., Maus E., Shao P., Craft J., Guillozet-Bongaarts A., Ohno M., Disterhoft J., Van Eldik L., Berry R., Vassar R. Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J. Neurosci. 2006, 26:10129-10140. 10.1523/JNEUROSCI.1202-06.2006.
48. Oddo S., Caccamo A., Smith I.F., Green K.N., LaFerla F.M. A dynamic relationship between intracellular and extracellular pools of Aβ. Amer. J. Pathol. 2006, 169:184-194. 10.2353/ajpath.2006.050593.
49. Organisciak D.T., Vaughan D.K. Retinal light damage: mechanisms and protection. Progr. Retin. Eye Res. 2010, 29:113-134. 10.1016/j.preteyeres.2009.11.004.
50. Park S.W., Kim J.H., Mook-Jung I., Kim K.W., Park W.J., Park K.H., Kim J.H. Intracellular amyloid beta alters the tight junction of retinal pigment epithelium in 5XFAD mice. Neurobiol. Aging. 2014, 35:2013-2020. 10.1016/j.neurobiolaging.2014.03.008.
51. Parthasarathy R., Fautsch M.P., Pepperberg D.R. Quantification of amyloid-beta in mouse and human eye tissues 2014, IOVS 2014;35: ARVO E-Abstract 1317.
52. Pauwels K., Williams T.L., Morris K.L., Jonckheere W., Vandersteen A., Kelly G., Schymkowitz J., Rousseau F., Pastore A., Serpell L.C., Broersen K. Structural basis for increased toxicity of pathological Aβ42:Aβ40 ratios in Alzheimer's disease. J. Biol. Chem. 2012, 287:5650-5660. 10.1074/jbc.M111.264473.
53. Pikuleva I.A., Curcio C.A. Cholesterol in the retina: the best is yet to come. Progr. Ret. Eye Res. 2014, 41:64-89. 10.1016/j.preteyeres.2014.03.002.
54. Prakasam A., Muthuswamy A., Ablonczy Z., Greig N.H., Fauq A., Rao K.J., Pappolla M.A., Sambamurti K. Differential accumulation of secreted AβPP metabolites in ocular fluids. J. Alzheimer's Dis. 2010, 20:1243-1253. 10.3233/JAD-2010-100210.
55. Pryor N.E., Moss M.A., Hestekin C.N. Unraveling the early events of amyloid-β protein (Aβ) aggregation: techniques for the determination of Aβ aggregate size. Int. J. Mol. Sci. 2012, 13:3038-3072. 10.3390/ijms13033038.
56. Puzzo D., Privitera L., Laznik E., Fà M., Staniszewski A., Palmeri A., Arancio O. Picomolar amyloid-β positively modulates synaptic plasticity and memory in hippocampus. J. Neurosci. 2008, 28:14537-14545. 10.1523/JNEUROSCI.2692-08.2008.
57. Puzzo D., Arancio O. Amyloid-β peptide: Dr. Jekyll or Mr. Hyde?. J. Alzheimer's Dis. 2013, 33:S111-S120. 10.3233/JAD-2012-129033.
58. Querfurth H.W., LaFerla F.M. Alzheimer's disease. New. Engl. J. Med. 2010, 362:329-344. 10.1056/NEJMra0909142.
59. Ripoli C., Cocco S., Li Puma D.D., Piacentini R., Mastrodonato A., Scala F., Puzzo D., D'Ascenzo M., Grassi C. Intracellular accumulation of amyloid-β (Aβ) protein plays a major role in Aβ-induced alterations of glutamatergic synaptic transmission and plasticity. J. Neurosci. 2014, 34:12893-12903. 10.1523/JNEUROSCI.1201-14.2014.
60. Roques B.P., Noble F., Dauge V., Fournié-Zaluski M.C., Beaumont A. Neutral endopeptidase 24.11: structure, inhibition, and experimental and clinical pharmacology. Pharmacol. Rev. 1993, 45:87-146.
61. Saido T., Leissring M.A. Proteolytic degradation of amyloid β-protein. Cold Spring Harb. Perspect. Med. 2012, 2:a006379. 10.1101/cshperspect.a006379.
62. Selkoe D.J. Preventing Alzheimer's disease. Science. 2012, 337:1488-1492. 10.1126/science.1228541.
63. Sharma K., Sharma N.K., Anand A. Why AMD is a disease of ageing and not of development: mechanisms and insights. Front. Aging Neurosci. 2014, 6. (Article 151). 10.3389/fnagi.2014.00151.
64. Shirotani K., Tsubuki S., Iwata N., Takaki Y., Harigaya W., Maruyama K., Kiryu-Seo S., Kiyama H., Iwata H., Tomita T., Iwatsubo T., Saido T.C. Neprilysin degrades both amyloid β peptides 1-40 and 1-42 most rapidly and efficiently among thiorphan- and phosphoramidon-sensitive endopeptidases. J. Biol. Chem. 2001, 276:21895-21901. 10.1074/jbc.M008511200.
65. Solomonov I., Korkotian E., Born B., Feldman Y., Bitler A., Rahimi F., Li H., Bitan G., Sagi I. Zn2+-Aβ40 complexes form metastable quasi-spherical oligomers that are cytotoxic to cultured hippocampal neurons. J. Biol. Chem. 2012, 287:20555-20564. 10.1074/jbc.M112.344036.
66. Soscia S.J., Kirby J.E., Washicosky K.J., Tucker S.M., Ingelsson M., Hyman B., Burton M.A., Goldstein L.E., Duong S., Tanzi R.E., Moir R.D. The Alzheimer's disease-associated amyloid-β-protein is an antimicrobial peptide. PLoS One 2010, 3:e9505. 10.1371/journal.pone.0009505.
67. Tanzi R.E., Moir R.D., Wagner S.L. Clearance of Alzheimer's Aβ peptide: the many roads to perdition. Neuron 2004, 43:605-608. 10.1016/j.neuron.2004.08.024.
68. Tao W. Application of encapsulated cell technology for retinal degenerative diseases. Expert Opin. Biol. Ther. 2006, 6:717-726. 10.1517/14712598.6.7.717.
69. Turner A.J., Isaac R.E., Coates D. The neprilysin (NEP) family of zinc metalloendopeptidases: genomics and function. Bioessays 2001, 23:261-269.
70. Walsh D.M., Selkoe D.J. Aβ oligomers - a decade of discovery. J. Neurochem. 2007, 101:1172-1184. 10.1111/j.1471-4159.2006.04426.x.
71. Wang J., Zhu C., Xu Y., Liu B., Wang M., Wu K. Development and expression of amyloid-β peptide 42 in retinal ganglion cells in rats. Anat. Rec. 2011, 294:1401-1405. 10.1002/ar.21438.
72. Wang J., Ohno-Matsui K., Morita I. Elevated amyloid β production in senescent retinal pigment epithelium, a possible mechanism of subretinal deposition of amyloid-β in age-related macular degeneration. Biochem. Biophys. Res. Commun. 2012, 423:73-78. 10.1016/j.bbrc.2012.05.085.
73. Warmlander S., Tiiman A., Abelein A., Luo J., Jarvet J., Soderberg K.L., Danielsson J., Graslund A. Biophysical studies of the amyloid β-peptide: interactions with metal ions and small molecules. Chembiochem. 2013, 14:1692-1704. 10.1002/cbic.201300262.
74. Wildsmith K.R., Holley M., Savage J.C., Skerrett R., Landreth G.E. Evidence for impaired amyloid β clearance in Alzheimer's disease. Alzheimer's Res. Ther. 2013, 5:33. 10.1186/alzrt187.
75. Woodell A., Rohrer B. A mechanistic review of cigarette smoke and age-related macular degeneration. Adv. Exper. Med. Biol. 2014, 801:301-307. 10.1007/978-1-4614-3209-8_38.
76. Yankner B.A., Lu T. Amyloid-β-protein toxicity and the pathogenesis of Alzheimer disease. J. Biol. Chem. 2009, 284:4755-4759. 10.1074/jbc.R800018200.
77. Yoneda S., Hara H., Hirata A., Fukushima M., Inomata Y., Tanihara H. Vitreous fluid levels of β-amyloid(1-42) and tau in patients with retinal diseases. Jpn. J. Ophthalmol. 2005, 49:106-108. 10.1007/s10384-004-0156-x.
78. Yoon S.S., Jo S.A. Mechanisms of amyloid-β peptide clearance: potential therapeutic targets for Alzheimer's disease. Biomol. Ther. Seoul. 2012, 20:245-255. 10.4062/biomolther.2012.20.3.245.