Crystal structure reveals conservation of amyloid-β conformation recognized by 3D6 following humanization to bapineuzumab

Alzheimer's Research and Therapy

Volumn 6, Issue 3, 2014, Pages

  Feinberg, Hadar ^b   Saldanha, José W ^e   Diep, Linnea ^a   Goel, Amita ^a   Widom, Angela ^c   Veldman, Geertruida M ^f   Weis, William I ^b   Schenk, Dale ^d   Basi, Guriqbal S ^a  

^a Elan Pharmaceuticals Inc   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c PFIZER INC   (United States)

^d Prothena Biosciences Inc   (United States)

^e NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^f ABBVIE INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3D6 IMMUNOGLOBULIN F(AB) FRAGMENT; AMYLOID BETA PROTEIN ANTIBODY; BAPINEUZUMAB; IMMUNOGLOBULIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; CRYSTAL STRUCTURE; IMMUNOTHERAPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

EID: 84903815644     PISSN: None     EISSN: 17589193     Source Type: Journal    
DOI: 10.1186/alzrt261     Document Type: Article

References (79)

1. Abeta vaccination effects on plaque pathology in the absence of encephalitis in Alzheimer disease. Masliah E, Hansen L, Adame A, Crews L, Bard F, Lee C, Seubert P, Games D, Kirby L, Schenk D, Neurology 2005 64 129 131 (Pubitemid 40082949)
2. Neuropathology of human Alzheimer disease after immunization with amyloid-beta peptide: a case report. Nicoll JA, Wilkinson D, Holmes C, Steart P, Markham H, Weller RO, Nat Med 2003 9 448 452 (Pubitemid 36460079)
3. 11C-PiB PET assessment of change in fibrillar amyloid-beta load in patients with Alzheimer's disease treated with bapineuzumab: a phase 2, double-blind, placebo-controlled, ascending-dose study. Rinne JO, Brooks DJ, Rossor MN, Fox NC, Bullock R, Klunk WE, Mathis CA, Blennow K, Barakos J, Okello AA, Rodriguez Martinez de Liano S, Liu E, Koller M, Gregg KM, Schenk D, Black R, Grundman M, Lancet Neurol 2010 9 363 372
4. Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Schenk D, Barbour R, Dunn W, Gordon G, Grajeda H, Guido T, Hu K, Huang J, Johnson-Wood K, Khan K, Kholodenko D, Lee M, Liao Z, Lieberburg I, Motter R, Mutter L, Soriano F, Shopp G, Vasquez N, Vandevert C, Walker S, Wogulis M, Yednock T, Games D, Seubert P, Nature 1999 400 173 177 (Pubitemid 29327547)
5. Neutralization of soluble, synaptotoxic amyloid beta species by antibodies is epitope specific. Zago W, Buttini M, Comery TA, Nishioka C, Gardai SJ, Seubert P, Games D, Bard F, Schenk D, Kinney GG, J Neurosci 2012 32 2696 2702
6. Immunization reverses memory deficits without reducing brain Abeta burden in Alzheimer's disease model. Dodart JC, Bales KR, Gannon KS, Greene SJ, DeMattos RB, Mathis C, DeLong CA, Wu S, Wu X, Holtzman DM, Paul SM, Nat Neurosci 2002 5 452 457 (Pubitemid 34454251)
7. A beta peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease. Janus C, Pearson J, McLaurin J, Mathews PM, Jiang Y, Schmidt SD, Chishti MA, Horne P, Heslin D, French J, Mount HT, Nixon RA, Mercken M, Bergeron C, Fraser PE, St George-Hyslop P, Westaway D, Nature 2000 408 979 982 (Pubitemid 32101644)
8. Amyloid-beta immunotherapy for the prevention and treatment of Alzheimer disease: lessons from mice, monkeys, and humans. Lemere CA, Maier M, Jiang L, Peng Y, Seabrook TJ, Rejuvenation Res 2006 9 77 84
9. A beta peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Morgan D, Diamond DM, Gottschall PE, Ugen KE, Dickey C, Hardy J, Duff K, Jantzen P, DiCarlo G, Wilcock D, Connor K, Hatcher J, Hope C, Gordon M, Arendash GW, Nature 2000 408 982 985 (Pubitemid 32101645)
10. Phase 3 trials of Solanezumab for mild-to-moderate Alzheimer's disease. Doody RS, Thomas RG, Farlow M, Iwatsubo T, Vellas B, Joffe S, Kieburtz K, Raman R, Sun X, Aisen PS, Siemers E, Liu-Seifert H, Mohs R, New Engl J Med 2014 370 311 321
11. Two phase 3 trials of Bapineuzumab in mild-to-moderate Alzheimer's disease. Salloway S, Sperling R, Fox NC, Blennow K, Klunk W, Raskind M, Sabbagh M, Honig LS, Porsteinsson AP, Ferris S, Reichert M, Ketter N, Nejadnik B, Guenzler V, Miloslavsky M, Wang D, Lu Y, Lull J, Tudor IC, Liu E, Grundman M, Yuen E, Black R, Brashear HR, New Engl J Med 2014 370 322 333
12. An effector-reduced anti-beta-amyloid (Abeta) antibody with unique abeta binding properties promotes neuroprotection and glial engulfment of Abeta. Adolfsson O, Pihlgren M, Toni N, Varisco Y, Buccarello AL, Antoniello K, Lohmann S, Piorkowska K, Gafner V, Atwal JK, Maloney J, Chen M, Gogineni A, Weimer RM, Mortensen DL, Friesenhahn M, Ho C, Paul R, Pfeifer A, Muhs A, Watts RJ, J Neurosci 2012 32 9677 9689
13. Alzheimer's drugs take a new tack. Callaway E, Nature 2012 489 13 14
14. Alzheimer's research. Stopping Alzheimer's before it starts. Miller G, Science 2012 337 790 792
15. Mechanism of amyloid removal in patients with Alzheimer disease treated with gantenerumab. Ostrowitzki S, Deptula D, Thurfjell L, Barkhof F, Bohrmann B, Brooks DJ, Klunk WE, Ashford E, Yoo K, Xu ZX, Loetscher H, Santarelli L, Arch Neurol 2012 69 198 207
16. Epitope and isotype specificities of antibodies to beta -amyloid peptide for protection against Alzheimer's disease-like neuropathology. Bard F, Barbour R, Cannon C, Carretto R, Fox M, Games D, Guido T, Hoenow K, Hu K, Johnson-Wood K, Khan K, Kholodenko D, Lee C, Lee M, Motter R, Nguyen M, Reed A, Schenk D, Tang P, Vasquez N, Seubert P, Yednock T, Proc Natl Acad Sci U S A 2003 100 2023 2028 (Pubitemid 36254567)
17. Immunotherapy reduces vascular amyloid-beta in PDAPP mice. Schroeter S, Khan K, Barbour R, Doan M, Chen M, Guido T, Gill D, Basi G, Schenk D, Seubert P, Games D, J Neurosci 2008 28 6787 6793
18. Abeta42 immunization in Alzheimer's disease generates Abeta N-terminal antibodies. Lee M, Bard F, Johnson-Wood K, Lee C, Hu K, Griffith SG, Black RS, Schenk D, Seubert P, Ann Neurol 2005 58 430 435 (Pubitemid 41266629)
19. A beta oligomers-a decade of discovery. Walsh DM, Selkoe DJ, J Neurochem 2007 101 1172 1184
20. Amyloid-related imaging abnormalities in patients with Alzheimer's disease treated with bapineuzumab: a retrospective analysis. Sperling R, Salloway S, Brooks DJ, Tampieri D, Barakos J, Fox NC, Raskind M, Sabbagh M, Honig LS, Porsteinsson AP, Lieberburg I, Arrighi HM, Morris KA, Lu Y, Liu E, Gregg KM, Brashear HR, Kinney GG, Black R, Grundman M, Lancet Neurol 2012 11 241 249
21. Effect of immunotherapy with Bapineuzumab on cerebrospinal fluid biomarker levels in patients with mild to moderate Alzheimer disease. Blennow K, Zetterberg H, Rinne JO, Salloway S, Wei J, Black R, Grundman M, Liu E, Arch Neurol 2012 69 1002 1010
22. A phase 2 multiple ascending dose trial of bapineuzumab in mild to moderate Alzheimer disease. Salloway S, Sperling R, Gilman S, Fox NC, Blennow K, Raskind M, Sabbagh M, Honig LS, Doody R, van Dyck CH, Mulnard R, Barakos J, Gregg KM, Liu E, Lieberburg I, Schenk D, Black R, Grundman M, Neurology 2009 73 2061 2070
23. Structural correlates of antibodies associated with acute reversal of amyloid beta-related behavioral deficits in a mouse model of Alzheimer disease. Basi GS, Feinberg H, Oshidari F, Anderson J, Barbour R, Baker J, Comery TA, Diep L, Gill D, Johnson-Wood K, Goel A, Grantcharova K, Lee M, Li J, Partridge A, Griswold-Prenner I, Piot N, Walker D, Widom A, Pangalos MN, Seubert P, Jacobsen JS, Schenk D, Weis WI, J Biol Chem 2010 285 3417 3427
24. Bapineuzumab captures the N-terminus of the Alzheimer's disease amyloid-beta peptide in a helical conformation. Miles LA, Crespi GA, Doughty L, Parker MW, Sci Rep 2013 3 1302
25. Gantenerumab: a novel human anti-Abeta antibody demonstrates sustained cerebral amyloid-beta binding and elicits cell-mediated removal of human amyloid-beta. Bohrmann B, Baumann K, Benz J, Gerber F, Huber W, Knoflach F, Messer J, Oroszlan K, Rauchenberger R, Richter WF, Rothe C, Urban M, Bardroff M, Winter M, Nordstedt C, Loetscher H, J Alzheimers Dis 2012 28 49 69
26. Structures of Abeta-related peptide-monoclonal antibody complexes. Gardberg A, Dice L, Pridgen K, Ko J, Patterson P, Ou S, Wetzel R, Dealwis C, Biochemistry 2009 48 5210 5217
27. The CCP4 suite: programs for protein crystallography. Collaborative Computational Project, Number 4, Acta Crystallogr D Biol Crystallogr 1994 50 760 763
28. Combined molecular replacement. Tong L, Acta Cryst 1996 A52 782 784 (Pubitemid 126474041)
29. Coot: model-building tools for molecular graphics. Emsley P, Cowtan K, Acta Crystallogr D Biol Crystallogr 2004 60 2126 2132 (Pubitemid 41742764)
30. PHENIX: building new software for automated crystallographic structure determination. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, Read RJ, Sacchettini JC, Sauter NK, Terwilliger TC, Acta Crystallogr D Biol Crystallogr 2002 58 1948 1954 (Pubitemid 35337293)
31. Humanization of a mouse monoclonal antibody by CDR-grafting: the importance of framework residues on loop conformation. Kettleborough CA, Saldanha J, Heath VJ, Morrison CJ, Bendig MM, Protein Eng 1991 4 773 783
32. A humanized antibody that binds to the interleukin 2 receptor. Queen C, Schneider WP, Selick HE, Payne PW, Landolfi NF, Duncan JF, Avdalovic NM, Levitt M, Junghans RP, Waldmann TA, Proc Natl Acad Sci U S A 1989 86 10029 10033 (Pubitemid 20030769)
33. Accurate prediction of the stability and activity effects of site-directed mutagenesis on a protein core. Lee C, Levitt M, Nature 1991 352 448 451 (Pubitemid 21896746)
34. Accurate modeling of protein conformation by automatic segment matching. Levitt M, J Mol Biol 1992 226 507 533
35. Humanization of recombinant antibodies. Saldanha JW, Recombinant Antibodies for Immunotherapy New York: Cambridge University Press 2009 3 19 [Little M (Series Editor)]
36. Kabat EA, Wu TT, Perry HM, Gottesman KS, Foeller C, Sequences of Proteins of Immunological Interest Bethesda, MD: U.S. Department of Health and Human Services, National Institutes for Health 5 1991
37. Molecular basis for passive immunotherapy of Alzheimer's disease. Gardberg AS, Dice LT, Ou S, Rich RL, Helmbrecht E, Ko J, Wetzel R, Myszka DG, Patterson PH, Dealwis C, Proc Natl Acad Sci U S A 2007 104 15659 15664 (Pubitemid 350035356)
38. Amyloid-beta-anti-amyloid-beta complex structure reveals an extended conformation in the immunodominant B-cell epitope. Miles LA, Wun KS, Crespi GA, Fodero-Tavoletti MT, Galatis D, Bagley CJ, Beyreuther K, Masters CL, Cappai R, McKinstry WJ, Barnham KJ, Parker MW, J Mol Biol 2008 377 181 192
39. Solution structure of the Alzheimer amyloid beta-peptide (1-42) in an apolar microenvironment. Similarity with a virus fusion domain. Crescenzi O, Tomaselli S, Guerrini R, Salvadori S, D'Ursi AM, Temussi PA, Picone D, Eur J Biochem 2002 269 5642 5648 (Pubitemid 35365553)
40. Solution structure of residues 1-28 of the amyloid b-peptide. Talafous J, Marcinowski KJ, Klopman G, Zagorski MG, Biochemistry 1994 33 7788 7796 (Pubitemid 24223797)
41. A new structural model of Abeta40 fibrils. Bertini I, Gonnelli L, Luchinat C, Mao J, Nesi A, J Am Chem Soc 2011 133 16013 16022
42. Stabilization of a beta-hairpin in monomeric Alzheimer's amyloid-beta peptide inhibits amyloid formation. Hoyer W, Gronwall C, Jonsson A, Stahl S, Hard T, Proc Natl Acad Sci U S A 2008 105 5099 5104 (Pubitemid 351738516)
43. Crystal structure of the amyloid-beta p3 fragment provides a model for oligomer formation in Alzheimer's disease. Streltsov VA, Varghese JN, Masters CL, Nuttall SD, J Neurosci 2011 31 1419 1426
44. Reshaping human antibodies for therapy. Riechmann L, Clark M, Waldmann H, Winter G, Nature 1988 332 323 327 (Pubitemid 18091075)
45. Humanized antibodies for antiviral therapy. Co MS, Deschamps M, Whitley RJ, Queen C, Proc Natl Acad Sci U S A 1991 88 2869 2873 (Pubitemid 21916521)
46. Humanized antibodies that recognize beta amyloid peptide. Basi G, Saldanha JW, US Patent 7,189,819 B2 Filed 6 December 2003. Published 13 March 2007. Assignee: Wyeth, Madison NJ, US, Neuralab Ltd
47. Replacing the complementarity-determining regions in a human antibody with those from a mouse. Jones PT, Dear PH, Foote J, Neuberger MS, Winter G, Nature 1986 321 522 525 (Pubitemid 16052256)
48. A plaque-specific antibody clears existing beta-amyloid plaques in Alzheimer's disease mice. Demattos RB, Lu J, Tang Y, Racke MM, Delong CA, Tzaferis JA, Hole JT, Forster BM, McDonnell PC, Liu F, Kinley RD, Jordan WH, Hutton ML, Neuron 2012 76 908 920
49. Reshaping human antibodies: grafting an antilysozyme activity. Verhoeyen M, Milstein C, Winter G, Science 1988 239 1534 1536
50. Modeling antibody hypervariable loops: a combined algorithm. Martin AC, Cheetham JC, Rees AR, Proc Natl Acad Sci U S A 1989 86 9268 9272 (Pubitemid 20010406)
51. Antibody modeling: implications for engineering and design. Morea V, Lesk AM, Tramontano A, Methods 2000 20 267 279 (Pubitemid 32905162)
52. Assembly of combinatorial antibody libraries on phage surfaces: the gene III site. Barbas CF 3rd, Kang AS, Lerner RA, Benkovic SJ, Proc Natl Acad Sci U S A 1991 88 7978 7982 (Pubitemid 21915278)
53. Making antibody fragments using phage display libraries. Clackson T, Hoogenboom HR, Griffiths AD, Winter G, Nature 1991 352 624 628 (Pubitemid 21912394)
54. Generation of a large combinatorial library of the immunoglobulin repertoire in phage lambda. Huse WD, Sastry L, Iverson SA, Kang AS, Alting-Mees M, Burton DR, Benkovic SJ, Lerner RA, Science 1989 246 1275 1281 (Pubitemid 20066710)
55. Linkage of recognition and replication functions by assembling combinatorial antibody Fab libraries along phage surfaces. Kang AS, Barbas CF, Janda KD, Benkovic SJ, Lerner RA, Proc Natl Acad Sci U S A 1991 88 4363 4366 (Pubitemid 21914540)
56. By-passing immunization. Human antibodies from V-gene libraries displayed on phage. Marks JD, Hoogenboom HR, Bonnert TP, McCafferty J, Griffiths AD, Winter G, J Mol Biol 1991 222 581 597
57. Antigen-specific human monoclonal antibodies from mice engineered with human Ig heavy and light chain YACs. Green LL, Hardy MC, Maynard-Currie CE, Tsuda H, Louie DM, Mendez MJ, Abderrahim H, Noguchi M, Smith DH, Zeng Y, David NE, Sasai H, Garza D, Brenner DG, Hales JF, McGuinness RP, Capon DJ, Klapholz S, Jakobovits A, Nat Genet 1994 7 13 21 (Pubitemid 24232374)
58. YAC vectors. Humanizing the mouse genome. Jakobovits A, Curr Biol 1994 4 761 763
59. Antigen-specific human antibodies from mice comprising four distinct genetic modifications. Lonberg N, Taylor LD, Harding FA, Trounstine M, Higgins KM, Schramm SR, Kuo CC, Mashayekh R, Wymore K, McCabe JG, Nature 1994 368 856 859 (Pubitemid 24137750)
60. Potent antibody therapeutics by design. Carter PJ, Nat Rev Immunol 2006 6 343 357
61. Engineered antibody fragments and the rise of single domains. Holliger P, Hudson PJ, Nat Biotechnol 2005 23 1126 1136 (Pubitemid 41486394)
62. When binding is enough: nonactivating antibody formats. Labrijn AF, Aalberse RC, Schuurman J, Curr Opin Immunol 2008 20 479 485
63. Polynucleotides encoding improved humanized immunoglobulins. Queen CL, Schneider WP, Selick HE, US patent 5,693,761 Filed 1995 Published Dec 2, 1997. Assignee: Protein Design Labs, Inc., Mountain View, Calif.
64. Humanized Immunoglobulins. Queen CL, Selick HE, US patent 5,530,101. Filed 1990 Published June 25, 1996. Assignee: Protein Design Labs, Inc., Mountain View, Calif.
65. Recombinant altered antibodies and methods of making altered antibodies. Winter GP, US patent 5,255,539. Filed Oct. 25, 1991 Published July 6, 1993. Assignee: Medical Research Council, London, England
66. Antibodies with altered effector function. Winter GP, Duncan AR, Burton DR, US patent 5,624,821 Filed Jun. 7, 1995 Published Apr. 29, 1997. Assignee: Scotgen Biopharmaceuticals Incorporated, Menlo Park, Calif.
67. 'Knobs-into-holes' engineering of antibody CH3 domains for heavy chain heterodimerization. Ridgway JB, Presta LG, Carter P, Protein Eng 1996 9 617 621 (Pubitemid 26241639)
68. Immunoglobulin domain crossover as a generic approach for the production of bispecific IgG antibodies. Schaefer W, Regula JT, Bahner M, Schanzer J, Croasdale R, Durr H, Gassner C, Georges G, Kettenberger H, Imhof-Jung S, Schwaiger M, Stubenrauch KG, Sustmann C, Thomas M, Scheuer W, Klein C, Proc Natl Acad Sci U S A 2011 108 11187 11192
69. Simultaneous targeting of multiple disease mediators by a dual-variable-domain immunoglobulin. Wu C, Ying H, Grinnell C, Bryant S, Miller R, Clabbers A, Bose S, McCarthy D, Zhu RR, Santora L, Davis-Taber R, Kunes Y, Fung E, Schwartz A, Sakorafas P, Gu J, Tarcsa E, Murtaza A, Ghayur T, Nat Biotechnol 2007 25 1290 1297 (Pubitemid 350076510)
70. Anti-tau antibodies that block tau aggregate seeding in vitro markedly decrease pathology and improve cognition in vivo. Yanamandra K, Kfoury N, Jiang H, Mahan TE, Ma S, Maloney SE, Wozniak DF, Diamond MI, Holtzman DM, Neuron 2013 80 402 414
71. Anti-abeta therapeutics in Alzheimer's disease: the need for a paradigm shift. Golde TE, Schneider LS, Koo EH, Neuron 2011 69 203 213
72. Alzheimer mechanisms and therapeutic strategies. Huang Y, Mucke L, Cell 2012 148 1204 1222
73. Alzheimer's disease, a multifactorial disorder seeking multitherapies. Iqbal K, Grundke-Iqbal I, Alzheimers Dement 2010 6 420 424
74. Preventing Alzheimer's disease. Selkoe DJ, Science 2012 337 1488 1492
75. Safety and biomarker effects of solanezumab in patients with Alzheimer's disease. Farlow M, Arnold SE, van Dyck CH, Aisen PS, Snider BJ, Porsteinsson AP, Friedrich S, Dean RA, Gonzales C, Sethuraman G, Demattos RB, Mohs R, Paul SM, Siemers ER, Alzheimers Dement 2012 8 261 271
76. Directed selection of a conformational antibody domain that prevents mature amyloid fibril formation by stabilizing Abeta protofibrils. Habicht G, Haupt C, Friedrich RP, Hortschansky P, Sachse C, Meinhardt J, Wieligmann K, Gellermann GP, Brodhun M, Gotz J, Halbhuber KJ, Rocken C, Horn U, Fandrich M, Proc Natl Acad Sci U S A 2007 104 19232 19237
77. Single-domain antibodies recognize selectively small oligomeric forms of amyloid beta, prevent Abeta-induced neurotoxicity and inhibit fibril formation. Lafaye P, Achour I, England P, Duyckaerts C, Rougeon F, Mol Immunol 2009 46 695 704
78. Anti-oligomeric Abeta single-chain variable domain antibody blocks Abeta-induced toxicity against human neuroblastoma cells. Zameer A, Kasturirangan S, Emadi S, Nimmagadda SV, Sierks MR, J Mol Biol 2008 384 917 928
79. Molecular structure of beta-amyloid fibrils in Alzheimer's disease brain tissue. Lu JX, Qiang W, Yau WM, Schwieters CD, Meredith SC, Tycko R, Cell 2013 154 1257 1268