Concomitant detection of β-amyloid peptides with N-terminal truncation and different C-terminal endings in cortical plaques from cases with Alzheimer's disease, senile monkeys and triple transgenic mice

Journal of Chemical Neuroanatomy

Volumn 40, Issue 1, 2010, Pages 82-92

  Härtig, Wolfgang ^a   Goldhammer, Simone ^a   Bauer, Ute ^a   Wegner, Florian ^a   Wirths, Oliver ^b   Bayer, Thomas A ^b   Grosche, Jens ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Alzheimer's disease; Animal model; Baboon; Digoxigenin conjugated antibody; Rhesus monkey; Triple fluorescence labelling; Triple transgenic mice

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; TAU PROTEIN;

ALZHEIMER DISEASE; AMINO ACID COMPOSITION; AMINO TERMINAL SEQUENCE; AMYLOIDOSIS; ANIMAL TISSUE; ARTICLE; BABOON; BIOCHEMISTRY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DISEASE COURSE; HISTOCHEMISTRY; HUMAN; HUMAN TISSUE; HYDROPHOBICITY; IMMUNOFLUORESCENCE; MACACA; MONKEY; MOUSE; NEUROPATHOLOGY; NONHUMAN; PATHOGENESIS; PRIMATE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; SENILE PLAQUE; SPECIES DIFFERENCE; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANTIBODIES; ANTIBODY SPECIFICITY; CEREBRAL CORTEX; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MACACA MULATTA; MICE; MICE, TRANSGENIC; MOLECULAR WEIGHT; PAPIO HAMADRYAS; PEPTIDE FRAGMENTS; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; SENILE PLAQUES; STAINING AND LABELING; TAU PROTEINS;

EID: 77952551031     PISSN: 08910618     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jchemneu.2010.03.006     Document Type: Article

References (73)

1. Akiyama H., Mori H., Sahara N., Kondo H., Ikeda K., Nishimura T., Oda T., McGeer P.L. Variable deposition of amyloid β-protein (Aβ) with the carboxy-terminus that ends at residue valine40 (Aβ40) in the cerebral cortex of patients with Alzheimer's disease: a double-labeling immunohistochemical study with antibodies specific for Aβ40 and the Aβ that ends at residues alanine42/threonine43 (Aβ4). Neurochem. Res. 1997, 22:1499-1505.
2. Bons N., Rieger F., Prudhomme D., Fisher A., Krause K.H. Microcebus murinus: a useful primate model for human cerebral aging and Alzheimer's disease?. Genes Brain Behav. 2006, 5:120-130.
3. Breyhan H., Wirths O., Duan K., Marcello A., Rettig J., Bayer T.A. APP/PS1KI bigenic mice develop early synaptic deficits and hippocampus atrophy. Acta Neuropathol. 2009, 117:677-685.
4. Casas C., Sergeant N., Itier J.-M., Blanchard V., Wirths O., van der Kolk N., Vingtdeux V., van de Steeg E., Ret G., Canton T., Drobecq H., Clark A., Bonici B., Delacourte A., Benavides J., Schmitz C., Tremp G., Bayer T.A., Benoit P., Pradier L. Massive CA1/2 neuronal loss with intraneuronal and N-terminal truncated Aβ42 accumulation in a novel Alzheimer transgenic model. Am. J. Pathol. 2004, 165:1289-1300.
5. Cynis H., Scheel E., Saido T.C., Schilling S., Demuth H.-U. Amyloidogenic processing of amyloid precursor prote: Evidence of a pivotal role of glutaminyl cyclase in generation of pyroglutamate-modified amyloid-β. Biochemistry 2008, 47:7405-7413.
6. Duyckaerts C., Potier M.-C., Delatour B. Alzheimer disease models and human neuropathology: similarities and differences. Acta Neuropathol. 2008, 115:5-38.
7. Elfenbein H.A., Rosen R.F., Stephens S.L., Switzer R.C., Smith Y., Pare J., Mehta P.D., Warzok R., Walker L.C. Cerebral β-amyloid angiopathy in aged squirrel monkeys. Histol. Histopathol. 2007, 22:155-167.
8. Frenkel D., Balass M., Solomon B. N-terminal EFRH sequence of Alzheimer's β-amyloid peptide represents the epitope of its anti-aggregating antibodies. J. Neuroimmunol. 1998, 88:85-90.
9. Gardberg A.S., Dice L.T., Ou S., Rich R.L., Helmbrecht E., Ko J., Wetzel R., Myszka D.G., Patterson P.H., Dealwis C. Molecular basis for passive immunotherapy of Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:15659-15664.
10. Gearing M., Tigges J., Mori H., Mirra S.S. Aβ40 is a major form of β-amyloid in nonhuman primates. Neurobiol. Aging 1996, 17:903-908.
11. Geula C., Nagykery N., Wu C.K. Amyloid-β deposits in the cerebral cortex of the common marmoset (Callithrix jacchus): incidence and chemical composition. Acta Neuropathol. 2002, 103:48-58.
12. Golde T.E., Eckman C.B., Younkin S.G. Biochemical detection of Aβ isoforms: implications for pathogenesis, diagnosis, and treatment of Alzheimer's disease. Biochim. Biophys. Acta 2000, 1502:172-187.
13. Götz J., Streffer J.R., David D., Schild A., Hoerndli F., Pennanen L., Kurosinski P., Chen F. Transgenic animal models of Alzheimer's disease and related disorders: histopathology, behavior and therapy. Mol. Psychiatry 2004, 9:664-683.
14. Gravina S.A., Ho L., Eckman C.B., Long K.E., Otvos L., Younkin L.H., Suzuki N., Younkin S.G. Amyloid β protein (Aβ) in Alzheimer's disease brain. Biochemical and immunocytochemical analysis with antibodies specific for forms ending at Aβ40 or Aβ42(43). J. Biol. Chem. 1995, 270:7013-7016.
15. Gruschus J.M. Do amyloid oligomers act as traps for misfolded proteins? A hypothesis. Amyloid 2008, 15:160-165.
16. Güntert A., Döbeli H., Bohrmann B. High sensitivity analysis of amyloid-beta peptide composition in amyloid deposits from human and PS2APP mouse brain. Neuroscience 2006, 143:461-475.
17. Hardy J., Allsop D. Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol. Sci. 1991, 12:383-388.
18. Harigaya Y., Saido T.C., Eckman C.B., Prada C.-M., Shoji M., Younkin S.G. Amyloid β protein starting pyroglutamate at position 3 is a major component of the amyloid deposits in the Alzheimer's disease brain. Biochem. Biophys. Res. Commun. 2000, 276:422-427.
19. Härtig W., Hausen D., Brauer K., Arendt T., Bigl V., Brückner G. Digoxigenin-tagged anti-GFAP and multiple labelling of human glia, vessels and β-amyloid. NeuroReport 1994, 5:573-576.
20. Härtig W., Brückner G., Holzer M., Brauer K., Bigl V. Digoxigenylated primary antibodies for sensitive dual-peroxidase labelling of neuronal markers. Histochem. Cell Biol. 1995, 104:467-472.
21. Härtig W., Brückner G., Brauer K., Seeger G., Bigl V. Triple immunofluorescence labelling of parvalbumin, calbindin-D28k and calretinin in rat and monkey brain. J. Neurosci. Methods 1996, 67:89-95.
22. Härtig W., Brückner G., Schmidt C., Brauer K., Bodewitz G., Turner J.D., Bigl V. Colocalization of β-amyloid peptides, apolipoprotein E and glial markers in senile plaques in the prefrontal cortex of old rhesus monkeys. Brain Res. 1997, 751:315-322.
23. Härtig W., Kirazov L., Brückner G., Holzer M., Gärtner U., Bigl V. Blot analyses and immunocytochemistry of neural antigens with digoxigenylated primary and secondary antibodies. Brain Res. Prot. 1997, 2:35-43.
24. Härtig W., Klein C., Brauer K., Schüppel K.-F., Arendt T., Brückner G., Bigl V. Abnormally phosphorylated protein tau in the cortex of aged individuals of various mammalian orders. Acta Neuropathol. 2000, 100:305-312.
25. Härtig W., Lehmann J., Stieler J., Singer D., Grosche J., Arendt T., Hoffmann R. Simultaneous detection of tau phospho-epitopes with haptenylated antibodies. Neuroreport 2006, 17:869-874.
26. Hartmann T., Bieger S., Brühl B., Tienari P.J., Ida N., Allsop D., Roberts G.W., Masters C.L., Dotti C.G., Unsicker K., Beyreuther K. Distinct sites of intracellular production for Alzheimer's disease Aβ40/42 amyloid peptides. Nat. Med. 1997, 3:1016-1020.
27. He W., Barrow C.J. The Aβ 3-pyroglutamyl and 11-pyroglutamyl peptides found in senile plaque have greater β-sheet forming and aggregation propensities in vitro than full-length Aβ. Biochemistry 1999, 38:10871-10877.
28. Hosoda R., Saido T.C., Otvos L., Arai T., Mann D.M.A., Lee V.M.-Y., Trojanowski J.Q., Iwatsubo T. Quantification of modified ( peptides in Alzheimer disease and Down syndrome brains. J. Neuropathol. Exp. Neurol. 1998, 57:1089-1095.
29. Iwatsubo T., Odaka A., Suzuki N., Mizusawa H., Nukina N., Ihara Y. Visualization of Aβ42(43) and Aβ40 in senile plaques with end-specific Aβ monoclonals: Evidence that an initially deposited species is Aβ42(43). Neuron 1994, 13:45-53.
30. Iwatsubo T., Saido T.C., Mann D.M., Lee V.M., Trojanowski J.Q. Full-length amyloid β (1-42(43)) and truncated amyloid β 42(43) deposit in diffuse plaques. Am. J. Pathol. 1996, 149:1823-1830.
31. Kheterpal I., Chen M., Cook K.D., Wetzel R. Structural differences in Aβ amyloid protofibrils and fibrils mapped by hydrogen exchange-mass spectrometry with on-line proteolytic fragmentation. J. Mol. Biol. 2006, 361:785-795.
32. Kim K.S., Miller D.L., Sapienza V.J., Chen C.-M.J., Bai C., Grundke-Iqbal I., Currie J.R., Wisniewski H.M. Production and characterization of monoclonal antibodies reactive to synthetic cerebrovascular amyloid peptide. Neurosci. Res. Commun. 1988, 2:121-130.
33. Kimura N., Tanemura K., Nakamura S., Takashima S., Ono F., Sakakibara I., Ishii Y., Kyuwa S., Yoshikawa Y. Age related changes of Alzheimer's disease-associated proteins in cynomolgus monkeys. Biochem. Biophys. Res. Commun. 2003, 310:303-311.
34. Klein W.L., Krafft G.A., Finch C.E. Targeting small Aβ oligomers: the solution to an Alzheimer's disease conundrum? Trends Neurosci. 2001, 24:219-224.
35. Kumar-Singh S., Pirici D., McGowan E., Serneels S., Ceuterick C., Hardy J., Duff K., Dickson D., Van Broeckhoven C. Dense-core plaques in Tg2576 and PSAPP mouse models of Alzheimer's disease are centered on vessel walls. Am. J. Pathol. 2005, 167:527-543.
36. Kuo Y.M., Emmerling M.R., Woods A.S., Cotter R.J., Roher A.E. Isolation, chemical characterization, and quantitation of Aβ-pyroglutamyl peptide from neuritic plaques and vascular amyloid deposits. Biochem. Biophys. Res. Commun. 1997, 237:188-191.
37. Kuo Y.M., Webster S., Emmerling M.R., De Lima N., Roher A.E. Irreversible dimerization/tetramerization and post-translational modifications inhibit proteolytic degradation of Aβ peptides of Alzheimer's disease. Biochim. Biophys. Acta 1998, 1406:291-298.
38. Kuo Y.M., Kokjohn T.A., Beach T.G., Sue L.I., Brune D., Lopez J.C., Kalback W.M., Abramowski D., Sturchler-Pierrat C., Staufenbiel M., Roher A.E. Comparative analysis of amyloid-β chemical structure and amyloid plaque morphology of transgenic mouse and Alzheimer's disease brains. J. Biol. Chem. 2001, 276:12991-12998.
39. LaFerla F., Oddo S. Alzheimer's disease: Aβ, tau and synaptic dysfunction. Trends Mol. Med. 2005, 11:170-176.
40. Lemere C.A., Oh J., Stanish H.A., Peng Y., Pepivani I., Fagan A.M., Yamaguchi H., Westmoreland S.V., Mansfield K.G. Cerebral amyloid-β accumulation with aging in cotton-top tamarins. Rejuvenation Res. 2008, 11:321-332.
41. Lesné S., Koh M.T., Kotilinek L., Kayed R., Glabe C.G., Yang A., Gallagher M., Ashe K.H. A specific amyloid-β protein assembly in the brain impairs memory. Nature 2006, 440:352-357.
42. Lewczuk P., Esselmann H., Bibl M., Paul S., Svitek J., Miertschischk J., Meyrer R., Smirnov A., Maler J.M., Klein C., Otto M., Bleich S., Sperling W., Kornhuber J., Rüther E., Wiltfang J. Electrophoretic separation of amyloid β peptides in plasma. Electrophoresis 2004, 25:3336-3343.
43. Mori H., Takio K., Ogawara M., Selkoe D.J. Mass spectrometry of purified amyloid β protein in Alzheimer's disease. J. Biol. Chem. 1992, 267:17082-17086.
44. Nakamura S., Tamaoka A., Sawamura N., Shoji S., Nakayama H., Ono F., Sakakibara I., Yoshikawa Y., Mori H., Goto N., Doi K. Carboxyl end-specific monoclonal antibodies to amyloid β protein (Aβ) subtypes (Aβ40 and A β42(43) differentiate Aβ in senile plaques and amyloid angiopathy in brains of aged cynomolgus monkeys. Neurosci. Lett. 1995, 201:151-154.
45. Nakamura S., Nakayama H., Goto N., Ono F., Sakakibara I., Yoshikawa Y. Histopathological studies of senile plaques and cerebral amyloidosis in cynomolgus monkeys. J. Med. Primatol. 1998, 27:244-252.
46. Näslund J., Haroutunian V., Mohs R., Davis K.L., Davies P., Greengard P., Buxbaum J.D. Correlation between elevated levels of amyloid (-peptide in the brain and cognitive decline. JAMA 2000, 283:1571-1577.
47. Oddo S., Caccamo A., Shepherd J.D., Murphy M.P., Golde T.E., Kayed R., Metherate R., Mattson M.P., Akbari Y., LaFerla F.M. Triple-transgenic model of Alzheimer's disease: intracellular Aβ and synaptic dysfunction. Neuron 2003, 39:409-421.
48. Ohyagi Y., Tsuruta Y., Motomura K., Miyoshi K., Kikuchi H., Iwaki T., Taniwaki T., Kira J. Intraneuronal amyloid β42 enhanced by heating but counteracted by formic acid. J. Neurosci. Methods 2007, 159:134-138.
49. Oikawa N., Kimura N., Yanagisawa K. Alzheimer-type tau pathology in advanced aged nonhuman primate brains harboring substantial amyloid deposition. Brain Res. 2010, 1315:137-149.
50. Parvathy S., Davies P., Haroutunian V., Purohit D.P., Davis K.L., Mohs R.C., Park H., Moran T.M., Chan J.Y., Buxbaum J.D. Correlation between Aβx-40-Aβx-42-, and Aβx-43-containing amyloid plaques and cognitive decline. Arch. Neurol. 2001, 58:2025-2032.
51. Pitt J.C., Lindemeier J., Habbes H.-W., Veh R.W. Haptenylation of antibodies during affinity purification: a novel and convenient procedure to obtain labeled antibodies for quantification and double labeling. Histochem. Cell. Biol. 1998, 110:311-322.
52. Podlisny M.B., Tolan D.R., Selkoe D.J. Homology of the amyloid beta protein precursor in monkey and human supports a primate model for beta amyloidosis in Alzheimer's disease. Am. J. Pathol. 1991, 138:1423-1435.
53. Price D.L., Martin L.J., Sisodia S.S., Wagster M.V., Koo E.H., Walker L.C., Koliatsos V.E., Cork L.C. Aged non-human primates: an animal model of age-associated neurodegenerative disease. Brain Pathol. 1991, 1:287-296.
54. Roher A.E., Lowenson J.D., Clarke S., Woods A.S., Cotter R.J., Gowing E., Ball M.J. β-Amyloid-(1-42) is a major component of cerebrovascular amyloid deposits: implications for the pathology of Alzheimer's disease. Proc. Natl. Acad. Sci. USA 1993, 90:10836-10840.
55. Russo C., Salis S., Dolcini V., Venezia V., Song X.H., Teller J.K., Schettini G. Amino-terminal modification and tyrosine phosphorylation of carboxy-terminal fragments of the amyloid precursor protein in Alzheimer's disease and Down's syndrome brain. Neurobiol. Dis. 2001, 8:173-180. (Erratum in: Neurobiol. Dis. 2001, 8, 540).
56. Saido T.C., Iwatsubo T., Mann D.M., Shimada H., Ihara Y., Kawashima S. Dominant and differential deposition of distinct β-amyloid peptide species, AβN3(pE), in senile plaques. Neuron 1995, 14:457-466.
57. Saido T.C., Yamao-Harigaya W., Iwatsubo T., Kawashima S. Amino- and carboxyl-terminal heterogeneity of β-amyloid peptides deposited in human brain. Neurosci. Lett. 1996, 215:173-176.
58. Sani S., Traul D., Klink A., Niaraki N., Gonzalo-Ruiz A., Wu C.-K., Geula C. Distribution, progression and chemical composition of cortical amyloid-β deposits in aged rhesus monkeys: similarities to the human. Acta Neuropathol. 2003, 105:145-156.
59. Sevalle J., Amoyel A., Robert P., Fournié-Zaluski M.C., Roques B., Checler F. Aminopeptidase A contributes to the N-terminal truncation of amyloid β-peptide. J. Neurochem. 2009, 109:248-256.
60. Schilling S., Hoffmann T., Manhart S., Hoffmann M., Demuth H.-U. Glutaminyl cyclases unfold glutamyl cyclase activity under mild acid conditions. FEBS Lett. 2004, 563:191-196.
61. Schilling S., Appl T., Hoffmann T., Cynis H., Schulz K., Jagla W., Friedrich D., Wermann M., Buchholz M., Heiser U., von Hörsten S., und Demuth H.U. Inhibition of glutaminyl cyclase prevents pGlu-Aβ formation after intracortical/hippocampal microinjection in vivo/in situ. J. Neurochem. 2008, 106:1225-1236.
62. Schilling S., Zeitschel U., Hoffmann T., Heiser U., Francke M., Kehlen A., Holzer M., Hutter-Paier B., Prokesch M., Windisch M., Jagla W., Schlenzig D., Lindner C., Rudolph T., Reuter G., Cynis H., Montag D., Demuth H.-U., Roßner S. Glutaminyl cyclase inhibition attenuates pyroglutamate Aβ and Alzheimer's disease-like pathology. Nat. Med. 2008, 14:1106-1111.
63. Schnell S.A., Staines W.A., Wessendorf M.W. Reduction of lipofuscin-like autofluorescence in fluorescently labeled tissue. J. Histochem. Cytochem. 1999, 47:719-730.
64. Selkoe D.J. Alzheimerós disease: genes, proteins and therapy. Physiol. Rev. 2001, 81:741-766.
65. Soto C., Estrada L.D. Protein misfolding and neurodegeneration. Arch. Neurol. 2008, 65:184-189.
66. Stern E.A., Bacskai B.J., Hickey G.A., Attenello F.J., Lombardo J.A., Hyman B.T. Cortical synaptic integration in vivo is disrupted by amyloid-β plaques. J. Neurosci. 2004, 24:4535-4540.
67. Tekirian T.L., Saido T.C., Markesbery W.R., Russell M.J., Wekstein D.R., Patel E., Geddes J.W. N-terminal heterogeneity of parenchymal and cerebrovascular Aβ deposits. J. Neuropathol. Exp. Neurol. 1998, 57:76-94.
68. Uchihara T., Nakamura A., Nakayama H., Arima K., Ishizuka N., Mori H., Mizushima S. Triple immunofluorolabelling with two rabbit polyclonal antibodies and a mouse monoclonal antibody following three-dimensional analysis of cotton wool plaques in Alzheimer disease. J. Histochem. Cytochem. 2003, 51:1201-1206.
69. Walker L.C. Animal models of cerebral β-amyloid angiopathy. Brain Res. Rev. 1997, 25:70-84.
70. Walker L.C., Cork L.C. The neurobiology of aging in nonhuman primates. Alzheimer's Disease 1999, Lippincott Williams & Wilkins, Philadelphia. 2nd edition. R.D. Terry, R. Katzman, K.L. Bick, S.S. Sisodia (Eds.).
71. Wiltfang J., Esselmann H., Bibl M., Hüll M., Hampel H., Kessler H., Frölich L., Schröder J., Peters O., Jessen F., Luckhaus C., Perneczky R., Jahn H., Fiszer M., Maler J.M., Zimmermann R., Bruckmoser R., Kornhuber J., Lewczuk P. Amyloid β peptide ratio 42/40 but not Aβ correlates with phospho-tau in patients with low- and high-CSF Aβ load. J. Neurochem. 2007, 101:1053-1059.
72. Wirths O., Breyhan H., Cynis H., Schilling S., Demuth H.-U., Bayer T.A. Intraneuronal pyroglutamate-Abeta 3-42 triggers neurodegeneration and lethal neurological deficits in a transgenic mouse model. Acta Neuropathol. 2009, 118:487-496.
73. Wirths O., Bethge T., Marcello A., Harmeier A., Jawahr S., Lucassen P.J., Multhaup G., Brody D., Esparza T., Ingelsson M., Kalimo H., Lannfelt L., Bayer T.A. Pyroglutamate Abeta pathology in APP/PS1K1 mice, sporadic and familial Alzheimer's disease cases. J. Neural Transm. 2010, 117:85-96.