Neuropeptide Y fragments derived from neprilysin processing are neuroprotective in a transgenic model of Alzheimer's disease

Journal of Neuroscience

Volumn 29, Issue 4, 2009, Pages 1115-1125

  Rose, John B ^a   Crews, Leslie ^b   Rockenstein, Edward ^a   Adame, Anthony ^a   Mante, Michael ^a   Hersh, Louis B ^c   Gage, Fred H ^d   Spencer, Brian ^a   Potkar, Rewati ^a   Marr, Robert A ^e   Masliah, Eliezer ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^e ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

Alzheimer's disease; Amyloid; Cleavage; Neprilysin; Neuropeptide; Processing

Indexed keywords

AMYLOID PRECURSOR PROTEIN; GENOMIC DNA; GREEN FLUORESCENT PROTEIN; LENTIVIRUS VECTOR; MEMBRANE METALLOENDOPEPTIDASE; MESSENGER RNA; N [2 [1,2 DIHYDRO 3,5(4H) DIOXO 1,2 DIPHENYL 1,2,4 TRIAZOL 4 YL]ETHYL] N2 [[1 [2 [4 [5,11 DIHYDRO 6(6H) OXODIBENZ[B,E]AZEPIN 11 YL] 1 PIPERAZINYL] 2 OXOETHYL]CYCLOPENTYL]ACETYL]ARGININAMIDE; NALPHA (DIPHENYLACETYL) N (4 HYDROXYBENZYL) DEXTRO ARGININAMIDE; NEUROPEPTIDE Y; NEUROPEPTIDE Y [21-36]; NEUROPEPTIDE Y [31-36]; NEUROPEPTIDE Y1 RECEPTOR; NEUROPEPTIDE Y2 RECEPTOR; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DEGENERATIVE DISEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; EX VIVO STUDY; FETUS; FRONTAL CORTEX; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IN VIVO STUDY; MASS SPECTROMETRY; MOUSE; NERVE CELL CULTURE; NEUROLOGIC DISEASE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OSMOTIC MINIPUMP; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN PROCESSING; TRANSGENIC MOUSE; WESTERN BLOTTING;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ARGININE; BENZAZEPINES; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; GENETIC VECTORS; HUMANS; MICE; MICE, TRANSGENIC; NEPRILYSIN; NERVE DEGENERATION; NERVE GROWTH FACTORS; NEURONS; NEUROPEPTIDE Y; PEPTIDE FRAGMENTS; RECEPTORS, NEUROPEPTIDE Y;

EID: 59649118673     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4220-08.2009     Document Type: Article

References (67)

1. Akiyama H, Kondo H, Ikeda K, Kato M, McGeer PL (2001) Immunohistochemical localization of neprilysin in the human cerebral cortex: inverse association with vulnerability to amyloid β-protein (Aβ) deposition. Brain Res 902:277-281.
2. Albers HE, Ferris CF (1984) Neuropeptide Y: role in light-dark cycle entrainment of hamster circadian rhythms. Neurosci Lett 50:163-168.
3. Amatniek JC, Hauser WA, DelCastillo-Castaneda C, Jacobs DM, Marder K, Bell K, Albert M, Brandt J, Stern Y (2006) Incidence and predictors of seizures in patients with Alzheimer's disease. Epilepsia 47:867-872.
4. Ashford JW (2004) APOE genotype effects on Alzheimer's disease onset and epidemiology. J Mol Neurosci 23:157-165.
5. Caccamo A, Oddo S, Sugarman MC, Akbari Y, LaFerla FM (2005) Age- and region-dependent alterations in Aβ-degrading enzymes: implications for Aβ-induced disorders. Neurobiol Aging 26:645-654.
6. Cadacio CL, Milner TA, Gallagher M, Pierce JP (2003) Hilar neuropeptide Y interneuron loss in the aged rat hippocampal formation. Exp Neurol 183:147-158.
7. Carter TL, Pedrini S, Ghiso J, Ehrlich ME, Gandy S (2006) Brain neprilysin activity and susceptibility to transgene-induced Alzheimer amyloidosis. Neurosci Lett 392:235-239.
8. Cha CI, Lee YI, Lee EY, Park KH, Baik SH (1997) Age-related changes of VIP, NPY and somatostatin-immunoreactive neurons in the cerebral cortex of aged rats. Brain Res 753:235-244.
9. Chana G, Landau S, Beasley C, Everall IP, Cotter D (2003) Two-dimensional assessment of cytoarchitecture in the anterior cingulate cortex in major depressive disorder, bipolar disorder, and schizophrenia: evidence for decreased neuronal somal size and increased neuronal density. Biol Psychiatry 53:1086-1098.
10. Chan-Palay V, Lang W, Allen YS, Haesler U, Polak JM (1985) Cortical neurons immunoreactive with antisera against neuropeptide Y are altered in Alzheimer's-type dementia. J Comp Neurol 238:390-400.
11. Clarimón J, Muñoz FJ, Boada M, Tàrraga L, Sunyer J, Bertranpetit J, Comas D (2003) Possible increased risk for Alzheimer's disease associated with neprilysin gene. J Neural Transm 110:651-657.
12. Davies CA, Morroll DR, Prinja D, Mann DM, Gibbs A (1990) A quantitative assessment of somatostatin-like and neuropeptide Y-like immunostained cells in the frontal and temporal cortex of patients with Alzheimer's disease. J Neurol Sci 96:59-73.
13. Diez M, Koistinaho J, Kahn K, Games D, Hökfelt T (2000) Neuropeptides in hippocampus and cortex in transgenic mice overexpressing V717F β-amyloid precursor protein - initial observations. Neuroscience 100:259-286.
14. Diez M, Danner S, Frey P, Sommer B, Staufenbiel M, Wiederhold KH, Hökfelt T (2003) Neuropeptide alterations in the hippocampal formation and cortex of transgenic mice overexpressing β-amyloid precursor protein (APP) with the Swedish double mutation (APP23). Neurobiol Dis 14:579-594.
15. El-Amouri SS, Zhu H, Yu J, Marr R, Verma IM, Kindy MS (2008) Neprilysin: an enzyme candidate to slow the progression of Alzheimer's disease. Am J Pathol 172:1342-1354.
16. Farris W, Schütz SG, Cirrito JR, Shankar GM, Sun X, George A, Leissring MA, Walsh DM, Qiu WQ, Holtzman DM, Selkoe DJ (2007) Loss of neprilysin function promotes amyloid plaque formation and causes cerebral amyloid angiopathy. Am J Pathol 171:241-251.
17. Foti S, Haberman RP, Samulski RJ, McCown TJ (2007) Adeno-associated virus-mediated expression and constitutive secretion of NPY or NPY13-36 suppresses seizure activity in vivo. Gene Ther 14:1534-1536.
18. Glabe CC (2005) Amyloid accumulation and pathogensis of Alzheimer's disease: significance of monomeric, oligomeric and fibrillar Aβ. Subcell Biochem 38:167-177.
19. Glabe CG, Kayed R (2006) Common structure and toxic function of amyloid oligomers implies a common mechanism of pathogenesis. Neurology 66:S74-S78.
20. Hemming ML, Patterson M, Reske-Nielsen C, Lin L, Isacson O, Selkoe DJ (2007) Reducing amyloid plaque burden via ex vivo gene delivery of an Aβ-degrading protease: a novel therapeutic approach to Alzheimer disease. PLoS Med 4:e262.
21. Hong CS, Goins WF, Goss JR, Burton EA, Glorioso JC (2006) Herpes simplex virus RNAi and neprilysin gene transfer vectors reduce accumulation of Alzheimer's disease-related amyloid-β peptide in vivo. Gene Ther 13:1068-1079.
22. Howell OW, Doyle K, Goodman JH, Scharfman HE, Herzog H, Pringle A, Beck-Sickinger AG, Gray WP (2005) Neuropeptide Y stimulates neuronal precursor proliferation in the post-natal and adult dentate gyrus. J Neurochem 93:560-570.
23. Huang SM, Mouri A, Kokubo H, Nakajima R, Suemoto T, Higuchi M, Staufenbiel M, Noda Y, Yamaguchi H, Nabeshima T, Saido TC, Iwata N (2006) Neprilysin-sensitive synapse-associated amyloid-β peptide oligomers impair neuronal plasticity and cognitive function. J Biol Chem 281:17941-17951.
24. Iijima-Ando K, Hearn SA, Granger L, Shenton C, Gatt A, Chiang HC, Hakker I, Zhong Y, Iijima K (2008) Overexpression of neprilysin reduces alzheimer amyloid-β42 (Aβ42)-induced neuron loss and intraneuronal Aβ42 deposits but causes a reduction in cAMP-responsive element-binding protein-mediated transcription, age-dependent axon pathology, and premature death in Drosophila. J Biol Chem 283:19066-19076.
25. Iwata N, Tsubuki S, Takaki Y, Watanabe K, Sekiguchi M, Hosoki E, Kawashima-Morishima M, Lee HJ, Hama E, Sekine-Aizawa Y, Saido TC (2000) Identification of the major Aβ1-42-degrading catabolic pathway in brain parenchyma: suppression leads to biochemical and pathological deposition. Nat Med 6:143-150.
26. Iwata N, Tsubuki S, Takaki Y, Shirotani K, Lu B, Gerard NP, Gerard C, Hama E, Lee HJ, Saido TC (2001) Metabolic regulation of brain Aβ by neprilysin. Science 292:1550-1552.
27. Iwata N, Mizukami H, Shirotani K, Takaki Y, Muramatsu S, Lu B, Gerard NP, Gerard C, Ozawa K, Saido TC (2004) Presynaptic localization of neprilysin contributes to efficient clearance of amyloid-β peptide in mouse brain. J Neurosci 24:991-998.
28. Jinno S, Kosaka T (2003) Patterns of expression of neuropeptides in GABAergic nonprincipal neurons in the mouse hippocampus: quantitative analysis with optical disector. J Comp Neurol 461:333-349.
29. Kaga T, Fujimiya M, Inui A (2001) Emerging functions of neuropeptide Y Y(2) receptors in the brain. Peptides 22:501-506.
30. Kawahara K, Hashimoto M, Bar-On P, Ho GJ, Crews L, Mizuno H, Rockenstein E, Imam SZ, Masliah E (2008) α-Synuclein aggregates interfere with Parkin solubility and distribution: role in the pathogenesis of Parkinson disease. J Biol Chem 283:6979-6987.
31. Leissring MA, Farris W, Chang AY, Walsh DM, Wu X, Sun X, Frosch MP, Selkoe DJ (2003) Enhanced proteolysis of β-amyloid in APP transgenic mice prevents plaque formation, secondary pathology, and premature death. Neuron 40:1087-1093.
32. Lu B, Gerard NP, Kolakowski LF Jr, Bozza M, Zurakowski D, Finco O, Carroll MC, Gerard C (1995) Neutral endopeptidase modulation of septic shock. J Exp Med 181:2271-2275.
33. Marr RA, Rockenstein E, Mukherjee A, Kindy MS, Hersh LB, Gage FH, Verma IM, Masliah E (2003) Neprilysin gene transfer reduces human amyloid pathology in transgenic mice. J Neurosci 23:1992-1996.
34. Masliah E, Rockenstein E, Veinbergs I, Mallory M, Hashimoto M, Takeda A, Sagara Y, Sisk A, Mucke L (2000) Dopaminergic loss and inclusion body formation in alpha-synuclein mice: implications for neurodegenerative disorders. Science 287:1265-1269.
35. Medeiros MS, Turner AJ (1994) Post-secretory processing of regulatory peptides: the pancreatic polypeptide family as a model example. Biochimie 76:283-287.
36. Medeiros Mdos S, Turner AJ (1996) Metabolism and functions of neuropeptide Y. Neurochem Res 21:1125-1132.
37. Minthon L, Edvinsson L, Ekman R, Gustafson L (1990) Neuropeptide levels in Alzheimer's disease and dementia with frontotemporal degeneration. J Neural Transm Suppl 30:57-67.
38. Mohajeri MH, Kuehnle K, Li H, Poirier R, Tracy J, Nitsch RM (2004) Antiamyloid activity of neprilysin in plaque-bearing mouse models of Alzheimer's disease. FEBS Lett 562:16-21.
39. Mucke L, Abraham CR, Ruppe MD, Rockenstein EM, Toggas SM, Mallory M, Alford M, Masliah E (1995) Protection against HIV-1 gp120-induced brain damage by neuronal overexpression of human amyloid precursor protein (hAPP). J Exp Med 181:1551-1556.
40. Naveilhan P, Hassani H, Canals JM, Ekstrand AJ, Larefalk A, Chhajlani V, Arenas E, Gedda K, Svensson L, Thoren P, Ernfors P (1999) Normal feeding behavior, body weight and leptin response require the neuropeptide Y Y2 receptor. Nat Med 5:1188-1193.
41. Nilsson CL, Brinkmalm A, Minthon L, Blennow K, Ekman R (2001) Processing of neuropeptide Y, galanin, and somatostatin in the cerebrospinal fluid of patients with Alzheimer's disease and frontotemporal dementia. Peptides 22:2105-2112.
42. Oda M, Morino H, Maruyama H, Terasawa H, Izumi Y, Torii T, Sasaki K, Nakamura S, Kawakami H (2002) Dinucleotide repeat polymorphisms in the neprilysin gene are not associated with sporadic Alzheimer's disease. Neurosci Lett 320:105-107.
43. Palop JJ, Chin J, Roberson ED, Wang J, Thwin MT, Bien-Ly N, Yoo J, Ho KO, Yu GQ, Kreitzer A, Finkbeiner S, Noebels JL, Mucke L (2007) Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 55:697-711.
44. Ramos B, Baglietto-Vargas D, del Rio JC, Moreno-Gonzalez I, Santa-Maria C, Jimenez S, Caballero C, Lopez-Tellez JF, Khan ZU, Ruano D, Gutierrez A, Vitorica J (2006) Early neuropathology of somatostatin/NPY GABAergic cells in the hippocampus of a PS1xAPP transgenic model of Alzheimer's disease. Neurobiol Aging 27:1658-1672.
45. Redrobe JP, Dumont Y, St-Pierre JA, Quirion R (1999) Multiple receptors for neuropeptide Y in the hippocampus: putative roles in seizures and cognition. Brain Res 848:153-166.
46. Redrobe JP, Dumont Y, Herzog H, Quirion R (2004) Characterization of neuropeptide Y, Y(2) receptor knockout mice in two animal models of learning and memory processing. J Mol Neurosci 22:159-166.
47. Reilly CE (2001) Neprilysin content is reduced in Alzheimer brain areas. J Neurol 248:159-160.
48. Rockenstein E, Mallory M, Mante M, Sisk A, Masliaha E (2001) Early formation of mature amyloid-b proteins deposits in a mutant APP transgenic model depends on levels of Aβ1-42. J Neurosci Res 66:573-582.
49. Rockenstein E, Mallory M, Mante M, Alford M, Windisch M, Moessler H, Masliah E (2002a) Effects of Cerebrolysin on amyloid-β deposition in a transgenic model of Alzheimer's disease. J Neural Transm Suppl 2002:327-336.
50. Rockenstein E, Mallory M, Hashimoto M, Song D, Shults CW, Lang I, Masliah E (2002b) Differential neuropathological alterations in transgenic mice expressing alpha-synuclein from the platelet-derived growth factor and Thy-1 promoters. J Neurosci Res 68:568-578.
51. Rockenstein E, Schwach G, Ingolic E, Adame A, Crews L, Mante M, Pfragner R, Schreiner E, Windisch M, Masliah E (2005a) Lysosomal pathology associated with alpha-synuclein accumulation in transgenic models using an eGFP fusion protein. J Neurosci Res 80:247-259.
52. Rockenstein E, Mante M, Alford M, Adame A, Crews L, Hashimoto M, Esposito L, Mucke L, Masliah E (2005b) High β-secretase activity elicits neurodegeneration in transgenic mice despite reductions in amyloid-β levels: implications for the treatment of Alzheimer disease. J Biol Chem 280:32957-32967.
53. Selkoe DJ (1994a) Cell biology of the amyloid β-protein precursor and the mechanisms of Alzheimer's disease. Annu Rev Cell Biol 10:373-403.
54. Selkoe DJ (1994b) Alzheimer's disease: a central role for amyloid. J Neuropathol Exp Neurol 53:438-447.
55. Silva AP, Pinheiro PS, Carvalho AP, Carvalho CM, Jakobsen B, Zimmer J, Malva JO (2003) Activation of neuropeptide Y receptors is neuroprotective against excitotoxicity in organotypic hippocampal slice cultures. FASEB J 17:1118-1120.
56. Silva AP, Xapelli S, Grouzmann E, Cavadas C (2005) The putative neuroprotective role of neuropeptide Y in the central nervous system. Curr Drug Targets CNS Neurol Disord 4:331-347.
57. Singer O, Marr RA, Rockenstein E, Crews L, Coufal NG, Gage FH, Verma IM, Masliah E (2005) Targeting BACE1 with siRNAs ameliorates Alzheimer disease neuropathology in a transgenic model. Nat Neurosci 8:1343-1349.
58. Skidgel RA, Erdös EG (2004) Angiotensin converting enzyme (ACE) and neprilysin hydrolyze neuropeptides: a brief history, the beginning and follow-ups to early studies. Peptides 25:521-525.
59. Sodeyama N, Mizusawa H, Yamada M, Itoh Y, Otomo E, Matsushita M (2001) Lack of association of neprilysin polymorphism with Alzheimer's disease and Alzheimer's disease-type neuropathological changes. J Neurol Neurosurg Psychiatry 71:817-818.
60. Sokolowski MB (2003) NPY and the regulation of behavioral development. Neuron 39:6-8.
61. Toggas SM, Masliah E, Rockenstein EM, Rall GF, Abraham CR, Mucke L (1994) Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature 367:188-193.
62. Veinbergs I, Van Uden E, Mallory M, Alford M, McGiffert C, DeTeresa R, Orlando R, Masliah E (2001) Role of apolipoprotein E receptors in regulating the differential in vivo neurotrophic effects of apolipoprotein E. Exp Neurol 170:15-26.
63. Vezzani A, Sperk G, Colmers WF (1999) Neuropeptide Y: emerging evidence for a functional role in seizure modulation. Trends Neurosci 22:25-30.
64. Walsh DM, Selkoe DJ (2004) Oligomers on the brain: the emerging role of soluble protein aggregates in neurodegeneration. Protein Pept Lett 11:213-228.
65. Wood LS, Pickering EH, McHale D, Dechairo BM (2007) Association between neprilysin polymorphisms and sporadic Alzheimer's disease. Neurosci Lett 427:103-106.
66. Yasojima K, Akiyama H, McGeer EG, McGeer PL (2001a) Reduced neprilysin in high plaque areas of Alzheimer brain: a possible relationship to deficient degradation of β-amyloid peptide. Neurosci Lett 297:97-100.
67. Yasojima K, McGeer EG, McGeer PL (2001b) Relationship between β amyloid peptide generating molecules and neprilysin in Alzheimer disease and normal brain. Brain Res 919:115-121.