Accumulation of insoluble amyloid-β in Down's syndrome is associated with increased BACE-1 and neprilysin activities

Journal of Alzheimer's Disease

Volumn 23, Issue 1, 2011, Pages 101-108

  Miners, James Scott ^a   Morris, Sean ^a   Love, Seth ^a   Kehoe, Patrick Gavin ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Alzheimer's disease; amyloid ; angiotensin converting enzyme; Down's syndrome; neprilysin; secretase

Indexed keywords

AMYLOID BETA PROTEIN; BETA SECRETASE 1; DIPEPTIDYL CARBOXYPEPTIDASE; MEMBRANE METALLOENDOPEPTIDASE;

ADULT; ALZHEIMER DISEASE; ARTICLE; AUTOPSY; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN SYNDROME; ENZYME ACTIVITY; FEMALE; FRONTAL CORTEX; HUMAN; HUMAN TISSUE; MALE; NEUROPATHOLOGY; PRIORITY JOURNAL; SOLUBILITY;

EID: 78651374915     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2010-101395     Document Type: Article

References (54)

1. Selkoe DJ (2001) Presenilin, Notch, and the genesis and treatment of Alzheimer's disease. Proc Natl Acad Sci USA 98, 11039-11041.
2. Deane R, Sagare A, Zlokovic BV (2008) The role of the cell surface LRP and soluble LRP in blood-brain barrier Abeta clearance in Alzheimer's disease. CurrPharmDes 14, 1601-1605.
3. Turner AJ, Fisk L, Nalivaeva NN (2004) Targeting amyloid-degrading enzymes as therapeutic strategies in neurodegen-eration. Ann N Y Acad Sci 1035, 1-20.
4. Weller RO, Subash M, Preston SD, Mazanti I, Carare RO (2008) Perivascular drainage of amyloid-beta peptides from the brain and its failure in cerebral amyloid angiopathy and Alzheimer's disease. Brain Pathol 18, 253-266.
5. Miners JS, Baig S, Palmer J, Palmer LE, Kehoe PG, Love S (2008) Afj-degrading enzymes in Alzheimer's disease. Brain Pathol 18, 240-252.
6. Iwatsubo T, Mann DM, Odaka A, Suzuki N, Ihara Y (1995) Amyloid fj protein (Afj) deposition: Afj 42(43) precedes Afj 40 in Down syndrome. Ann Neurol 37, 294-299.
7. Mann DM (1988) Alzheimer's disease and Down's syndrome. Histopathology 13, 125-137.
8. Lai F, Williams RS (1989) A prospective study of Alzheimer disease in Down syndrome. Arch Neurol 46, 849-853.
9. Rumble B, Retallack R, Hilbich C, Simms G, Multhaup G, Martins R, Hockey A, Montgomery P, Beyreuther K, Masters CL (1989) Amyloid A4 protein and its precursor in Down's syndrome and Alzheimer's disease. N EnglJ Med320, 1446-1452. (Pubitemid 19143709)
10. Cheon MS, Dierssen M, Kim SH, Lubec G (2008) Protein expression of BACE1, BACE2 and APP in Down syndrome brains. Amino Acids 35, 339-343.
11. Sun X, Tong Y, Qing H, Chen CH, Song W (2006) Increased BACE1 maturation contributes to the pathogenesis of Alzheimer's disease in Down syndrome. FASEB J 20, 1361-1368. (Pubitemid 44943844)
12. Mehta PD, Capone G, Jewell A, Freedland RL (2007) Increased amyloid fj protein levels in children and adolescents with Down syndrome. J Neurol Sci 254, 22-27.
13. LeverenzJB, Raskind MA (1998) Early amyloid deposition in the medial temporal lobe of young Down syndrome patients: a regional quantitative analysis. Exp Neurol 150, 296-304.
14. Wisniewski KE, Dalton AJ, McLachlan C, Wen GY, Wisniewski HM (1985) Alzheimer's disease in Down's syndrome: clinicopathologic studies. Neurology 35, 957-961.
15. Holland AJ, Hon J, Huppert FA, Stevens F, Watson P (1998) Population-based study of the prevalence and presentation of dementia in adults with Down's syndrome. Br J Psychiatry 172, 493-498.
16. Visser FE, Aldenkamp AP, van Huffelen AC, Kuilman M, Overweg J, van Wijk J (1997) Prospective study of the prevalence of Alzheimer-type dementia in institutionalized individuals with Down syndrome. Am J Ment Retard 101, 400-412.
17. Shirotani K, Tsubuki S, Iwata N, Takaki Y, Harigaya W, Maruyama K, Kiryu-Seo S, Kiyama H, Iwata H, Tomita T, Iwatsubo T, Saido TC (2001) Neprilysin degrades both amyloid p peptides 1-40 and 1-42 most rapidly and efficiently among thiorphan-and phosphoramidon-sensitive endopepti-dases. J Biol Chem 276, 21895-21901.
18. Eckman EA, Adams SK, Troendle FJ, Stodola BA, Kahn MA, Fauq AH, Xiao HD, Bernstein KE, Eckman CB (2006) Regulation of steady-state fj-amyloid levels in the brain by neprilysin and endothelin-converting enzyme but not angiotensin-converting enzyme. J Biol Chem 281, 30471-30478.
19. 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-fj peptide in mouse brain. J Neurosci 24, 991-998.
20. 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 Afj by neprilysin. Science 292,1550-1552.
21. 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 Afj-degrading protease: a novel therapeutic approach to Alzheimer disease. PLoS Med 4, e262.
22. Leissring MA, Farris W, Chang AY, Walsh DM, Wu X, Sun X, Frosch MP, Selkoe DJ (2003) Enhanced proteolysis of fj-amyloid in APP transgenic mice prevents plaque formation, secondary pathology, and premature death. Neuron 40, 1087-1093.
23. 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.
24. Hemming ML, Selkoe DJ, Farris W (2007) Effects of prolonged angiotensin-converting enzyme inhibitor treatment on amyloid fj-protein metabolism in mouse models of Alzheimer disease. Neurobiol Dis 26, 273-281.
25. Hu J, Igarashi A, Kamata M, Nakagawa H (2001) Angiotensin-converting enzyme degrades Alzheimer amyloid fS-peptide (Afj); retards Afj aggregation, deposition, fibril formation; and inhibits cytotoxicity. J Biol Chem 276, 47863-47868.
26. Oba R, Igarashi A, Kamata M, Nagata K, Takano S, Nakagawa H (2005) The N-terminal active centre of human angiotensin-converting enzyme degrades Alzheimer amyloid fj-peptide. Eur J Neurosci 21, 733-740.
27. Toropygin IY, Kugaevskaya EV, Mirgorodskaya OA, Elisseeva YE, Kozmin YP, Popov IA, Nikolaev EN, Makarov AA, Kozin SA (2008) The N-domain of angiotensin-converting enzyme specifically hydrolyzes the Arg-5-His-6 bond of Alzheimer's Afj-(1-16) peptide and its isoAsp-7 analogue with different efficiency as evidenced by quantitative matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 22, 231-239.
28. Wang J, Ho L, Chen L, Zhao Z, Zhao W, Qian X, Humala N, Seror I, Bartholomew S, Rosendorff C, Pasinetti GM (2007)Valsartan lowers brain fj-amyloid protein levels and improves spatial learning in a mouse model of Alzheimer disease. J Clin Invest 117, 3393-3402.
29. Zou K, Yamaguchi H, Akatsu H, Sakamoto T, Ko M, Mizoguchi K, Gong JS, Yu W, Yamamoto T, Kosaka K, Yanagisawa K, Michikawa M (2007) Angiotensin-converting enzyme converts amyloid fj-protein 1-42 (Afj(1-42)) to Afj(1-40), and its inhibition enhances brain Afj deposition. J Neurosci 27, 8628-8635.
30. Miners JS, Baig S, Tayler H, Kehoe PG, Love S (2009) Neprilysin and insulin-degrading enzyme levels are increased in Alzheimer disease in relation to disease severity. J Neu-ropathol Exp Neurol 68, 902-914.
31. Miners JS, van Helmond Z, Kehoe PG, Love S (2010) Changes with age in the activities of fj-secretase and the Afj-degrading enzymes neprilysin, insulin-degrading enzyme and angiotensin-converting enzyme. Brain Pathol 20, 794-802.
32. Fukumoto H, Cheung BS, Hyman BT, Irizarry MC (2002) fj-secretase protein and activity are increased in the neocortex in Alzheimer disease. Arch Neurol 59, 1381-1389.
33. Tyler SJ, Dawbarn D, Wilcock GK, Allen SJ (2002) a-and fj-secretase: profound changes in Alzheimer's disease. Biochem Biophys Res Commun 299, 373-376.
34. Fukumoto H, Rosene DL, Moss MB, Raju S, Hyman BT, Irizarry MC (2004) fj-secretase activity increases with aging in human, monkey, and mouse brain. Am J Pathol 164, 719-725.
35. Li R, Lindholm K, Yang LB, Yue X, Citron M, Yan R, Beach T, Sue L, Sabbagh M, Cai H, Wong P, Price D, Shen Y (2004) Amyloid fjpeptide load is correlated with increased fj-secretase activity in sporadic Alzheimer's disease patients. Proc Natl Acad Sci USA 101, 3632-3637.
36. van Helmond Z, Miners JS, Kehoe PG, Love S (2010) Oligomeric Afj in Alzheimer's disease: relationship to plaque and tangle pathology, APOE genotype and cerebral amyloid angiopathy. Brain Pathol 20, 468-480.
37. Miners JS, Ashby E, Van Helmond Z, Chalmers KA, Palmer LE, Love S, Kehoe PG (2008) Angiotensin-converting enzyme (ACE) levels and activity in Alzheimer's disease, and relationship of perivascular ACE-1 to cerebral amyloid angiopathy. Neuropathol Appl Neurobiol 34, 181-193.
38. Miners JS, Verbeek MM, Rikkert MO, Kehoe PG, Love S (2008)Immunocapture- based fluorometric assay for the mea surement of neprilysin-specific enzyme activity in brain tissue homogenates and cerebrospinal fluid. J Neurosci Methods 167, 229-236.
39. Alves MF, Araujo MC, Juliano MA, Oliveira EM, Krieger JE, Casarini DE, Juliano L, Carmona AK (2005) A continuous fluorescent assay for the determination of plasma and tissue angiotensin I-converting enzyme activity. Braz J Med Biol Res 38, 861-868.
40. Sabatini RA, Guimaraes PB, Fernandes L, Reis FC, Bersanetti PA, Mori MA, Navarro A, Hilzendeger AM, Santos EL, Andrade MC, Chagas JR, Pesquero JL, Casarini DE, Bader M, Carmona AK, Pesquero JB (2008) ACE activity is modulated by kinin B2 receptor. Hypertension 51, 689-695.
41. Hemming ML, Selkoe DJ (2005) Amyloid fj-protein is degraded by cellular angiotensin-converting enzyme (ACE) and elevated by an ACE inhibitor. J Biol Chem 280, 37644-37650.
42. van HelmondZ, Miners JS, Kehoe PG, Love S (2010) Higher soluble amyloid fj concentration in frontal cortex of young adults than in normal elderly or Alzheimer's Disease. Brain Pathol 20, 787-793.
43. Barbiero L, Benussi L, Ghidoni R, Alberici A, Russo C, Schettini G, Pagano SF, Parati EA, Mazzoli F, Nicosia F, Signorini S, Feudatari E, Binetti G (2003) BACE-2 is over-expressed in Down's syndrome. Exp Neurol 182, 335-345.
44. Holsinger RM, McLean CA, Beyreuther K, Masters CL, Evin G (2002) Increased expression of the amyloid precursor fj-secretase in Alzheimer's disease. Ann Neurol 51, 783-786.
45. Zhao J, Fu Y, Yasvoina M, Shao P, Hitt B, O'Connor T, Logan S, Maus E, Citron M, Berry R, Binder L, Vassar R (2007) fj-site amyloid precursor protein cleaving enzyme 1 levels become elevated in neurons around amyloid plaques: implications for Alzheimer's disease pathogenesis. J Neurosci 27, 3639-3649.
46. Apelt J, Ach K, Schliebs R (2003) Aging-related down-regulation of neprilysin, a putative fj-amyloid-degrading enzyme, in transgenic Tg2576 Alzheimer-like mouse brain is accompanied by an astroglial upregulation in the vicinity of fj-amyloid plaques. Neurosci Lett 339, 183-186.
47. Leal MC, Dorfman VB, Gamba AF, Frangione B, Wisniewski T, Castano EM, Sigurdsson EM, Morelli L (2006) Plaque-associated overexpression of insulin-degrading enzyme in the cerebral cortex of aged transgenic tg2576 mice with Alzheimer pathology. J Neuropathol Exp Neurol 65, 976-987.
48. Vepsalainen S, Hiltunen M, Helisalmi S, Wang J, van Groen T, Tanila H, Soininen H (2008) Increased expression of Afj degrading enzyme IDE in the cortex of transgenic mice with Alzheimer's disease-like neuropathology. Neurosci Lett 438, 216-220.
49. Wang R, Wang S, Malter JS, Wang DS (2009) Effects of HNE-modification induced by Afj on neprilysin expression and activity in SH-SY5Y cells. J Neurochem 108, 1072-1082.
50. Miners S, Ashby E, Baig S, Harrison R, Tayler H, Speedy E, Prince JA, Love S, Kehoe PG (2009) Angiotensin-converting enzyme levels and activity in Alzheimer's disease: differences in brain and CSF ACE and association with ACE1 genotypes. Am J Transl Res 1, 163-177.
51. Jung SS, Zhang W, Van Nostrand WE (2003) Pathogenic Afj induces the expression and activation of matrix metal-loproteinase-2 in human cerebrovascular smooth muscle cells. J Neurochem 85, 1208-1215.
52. Lee JM, Yin KJ, Hsin I, Chen S, Fryer JD, Holtzman DM, Hsu CY, Xu J (2003) Matrix metalloproteinase-9 and spontaneous hemorrhage in an animal model of cerebral amyloid angiopathy. Ann Neurol 54, 379-382.
53. Belyaev ND, Nalivaeva NN, Makova NZ, Turner AJ (2009) Neprilysin gene expression requires binding of the amyloid precursor protein intracellular domain to its promoter: implications for Alzheimer disease. EMBO Rep 10, 94-100.
54. von Rotz RC, Kohli BM, Bosset J, Meier M, Suzuki T, Nitsch RM, Konietzko U (2004) The APP intracellular domain forms nuclear multiprotein complexes and regulates the transcription of its own precursor. J Cell Sci 117, 4435-4448.