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Page 1: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

1

Regulation of anti-viral B cell responses

Use of virus-like particles for therapeutic vaccination

against addiction and other chronic diseases

Neue Möglichkeiten der Immuntherapie

Martin Bachmann, Immunologie Bern

Page 2: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

History of Vaccinology

live virulent live attenuated/ inactivated recombinant

Variolation (pre-1700) Vaccinia (1796)

HBV subunit (1982) Conjugate (Hib) (1987) Genetically-modified pertussis (1995)

HPV

Rabies (1885) Cholera (1896)

Allergy (1911) Tuberculosis (1921)

Diphtheria (1923) Tetanus (1926) Yellow Fever (1935) Polio (1952) Measles (1958)

Mumps (1967) Rubella (1970)

Europe: 1800 (India, China: 1000)

2000 1900

year

specificity and safety

Source: Bachmann and Dyer, Nature Reviews Drug Discovery, 3, 81 – 88 (2004), WHO

2

Page 3: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

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Risk Factors in the 21st Century   Growing Burden of Ageing Societies

Page 4: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

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•  Hypertension Ø  40%-60% Patienten non-compliant within 1 year

•  Hypercholesterinema Ø  45% non-compliant within 1 year Ø  60% non-compliant within 18 months

•  Asthma Ø  50% non-compliant within year

Sources: Am J Med 1997; 102:43-49. Am J Man Care 1997; 3:s12-17. Ann Allergy Asthma Immunol 1997;79:177-186.

  Poor compliace is a general problem

Risk Factors in the 21st Century

Page 5: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

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Drugs treating risk factors have to be:

•  Conveniant, to maximize •  Compliance

à Vaccines are conveniant since they have a long- lasting effect

  The Treatment of Risk Factors

Risk Factors in the 21st Century

Page 6: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

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ACE inhibitors

(Renin inhibitors)

AIIR blocker

  Modulate the Action of Angiotensin II

Hypertension Vaccine

Page 7: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

7

Hypertension

Remaining Problems

Sources: NHS, (2004); AJH 17: 347-335 (2004)

•  Compliance: An estimated 50-80% do not take all of the prescribed medication

•  Morning pressor surge: Pharmacokinetic profile of current inhibitors of the RAS may limit efficacy in early morning hours

Vaccine targeting angiotensin II may address these two issues, due to long-lived antibody responses

Page 8: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

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Organization: low absent high

Antibody response + - +++

- - Induction of auto-antibodies +++

Science 262, 1448-1451

Antigen Organization drives B cell responses  Repeptitivenes: a pathogen associated geometric pattern

Page 9: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

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  Why is epitope reptitiveness so important

Our immune system exploits structural features for the discrimination of self and foreign.

Viruses cannot help but have to express highly repetitive and highly ordered arrays of antigens on their surface

Viruses have small genomes and therefore consist of a small number of proteins.

Role of epitope densitiy and organisation

à Antigen Organisation is a geometric PAMP (Pathogen associated molecular pattern)

Page 10: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

 Bachmann  &  Dyer    Nat  Rev  Drug  Discov.  2004  

Active immunization: Mechanism

10

Page 11: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

 Bachmann  &  Dyer    Nat  Rev  Drug  Discov.  2004  

No IgG antibodies in the absence of T help

T help provided by the carrier is required for antibody production à Hence no boosting of the response by endogenous

cytokine

11

Page 12: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

Carrier-specific help bypasses Th cell tolerance

 Bachmann  &  Dyer    Nat  Rev  Drug  Discov.  2004  12

Page 13: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

Vaccine Design

Carrier

Linker (SMPH)

Antigen

NN

O

NO

O

O

O O

OCys

Lys

13

•  Non-replicating • Contains RNA as natural TLR7/8 ligand •  Very stable •  Economic production in bacteria •  2 g/l bacterial culture of GMP grade material

Bachmann&Jennnings Nature reviews Immunology 10:787-796

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10

100

1000

10000

Peptide Peptide Peptide- Protein Carrier

Peptide- VLP

Ant

ibod

y tit

er (

OD

50)

Adjuvants none Alum Alum none

Factor 100

Mouse

10

100

1000

10000

100000

50µg i.m.

50µg s.c.

10µg i.m.

10µg s.c.

Human

High Antibody Titers in Mice and Men

Ant

ibod

y tit

er (

End

poin

t)

J Allergy Clin Immunol.117:1470

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  Vaccine Design

Vaccine Design

CYT006-AngQb Qbeta virus-like particle

CGGDRVYIHPF

30 nm

Angiotensin II

Page 16: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

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Strong antibody responses against Angiotensin II   Efficient Antibody Induction in SHR Rats

0

10'000

20'000

30'000

40'000

d7 d14 d21 d28

CYT006-AngQb E

LIS

A tit

er (O

D50

%)

Days after immunization

J Hypertens 25:63-72

Page 17: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

17

  SHR Rats: BP Reading by Telemetry

Reduction of blood pressure in rats

*

150

160

170

180

190

0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75

Days

Sys

tolic

BP

(mm

Hg)

0

4000

8000 Anti A

ng II titer (OD

50%)

Titer CYT006-AngQb BP VLP BP CYT006-AngQb

p < 0.05

J Hypertens 25:63-72

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Indication Mild to moderate hypertension (systolic 140–179mmHg; diastolic 90–109mmHg)

Design Double-blind, randomized, placebo-controlled,

sequential two-dose comparison study in 72 patients Study period: 4 months plus 8 months safety follow-up

Endpoints Safety, tolerability, and exploratory efficacy

(change from baseline blood pressure)

Study Outline (1)   A Placebo-controlled Phase IIa Clinical Trial

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Study Outline (2)   Two Dose Levels vs. Placebo

N=24 100µg AngQb

placebo N=12

0 1 2 3 4

safety follow up

12 months

N=24 300µg AngQb

placebo N=12 safety follow up 24h ambulatory

blood pressure measurement

Injection

The Lancet, 371 (2008) 821-827

The Lancet, 371 (2008) 821-827

Page 20: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

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  Antibody Responses in Study 01

0

4000

8000

0 4 8 12 16 20 24 28 32 36 40 44 48 weeks

ELI

SA

titer

300 µg AngQb 100 µg AngQb Placebo

6 14 10

Evidence for Affinity Maturation

Page 21: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

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  Mean Change of ABP: 300 µg vs. Placebo

Day-time blood pressure

Day-time Blood Pressure

-9.0 / -4.0 mm Hg p=0.015 / p=0.064

at 8am -25 / -13 mm Hg p<0.0001 / p=0.0035

The Lancet, 371 (2008) 821-827

Page 22: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

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24 Hours Measurement

placebo (SBP/DBP), n=12 300µg AngQb (SBP/DBP), n=21

70 80 90

100 110 120 130 140 150 160 170

09 10 11 12 13 14 15 16 17 18 19 20 21 22 23 00 01 02 03 04 05 06 07 08

Time (24-hour)

Am

bula

tory

blo

od p

ress

ure

(mm

Hg)

run-

in

The Lancet, 371 (2008) 821-827

Page 23: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

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Conclusion

•  Immunization against angiotensin II can significantly reduce blood-pressure in hypertensive individuals •  Regimen and dosing, however, needs optimization

Page 24: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

Regulation of anti-viral B cell responses

Use of virus-like particles for therapeutic vaccination

against addiction and other chronic diseases

Vaccination against Parkinson`s disease Martin Bachmann, Jenner Institute, University of Oxford, UK

Page 25: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

Parkinson’s Disease (PD)

  Neurodegenerative disease   Loss of dopaminergic neurons   Leading to motor control disorder   Characterised by Lewy bodies = protein aggregates in

the brain

  Mis-folded / aggregated disease-specific proteins common feature of neurodegenerative diseases

  PrP, Kreuzfeld-Jakob disease, etc   Amyloid-β (Aβ), tau - Alzheimer’s disease (AD)   α-syn – Parkinson’s disease (PD)   Huntigtons, ALS 25

Page 26: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

α-Synuclein

§  α-synuclein is expressed in various tissues and adopts a monomeric but

largely unfolded structure (J Biol Chem. 2012 May 4;287(19):15345-64.).

§  α-synuclein undergoes heavy posttranslational modification, including

phosphorylation, nitration and sometimes aggregation (Nat Rev Neurosci.

2013 Jan;14(1):38-48)

§  Mild overexpression (2-fold) but also single point mutations may cause

familial Parkinson`s disease (Lancet 364(9440):1167–1169.; Science 276:

2045)

§  Aggregated α-synuclein is thought to be central for Parkinson`s disease

development

26

Page 27: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

Parkinson’s Disease (PD)

REVIEWdoi:10.1038/nature12481

Self-propagation of pathogenic proteinaggregates in neurodegenerative diseasesMathias Jucker1,2 & Lary C. Walker3,4

For several decades scientists have speculated that the key to understanding age-related neurodegenerative disorders may befound in the unusual biology of the prion diseases. Recently, owing largely to the advent of new disease models, this hypothesishas gained experimental momentum. In a remarkable variety of diseases, specific proteins have been found to misfold andaggregate into seeds that structurally corrupt like proteins, causing them to aggregate and form pathogenic assemblies rangingfrom small oligomers to large masses of amyloid. Proteinaceous seeds can therefore serve as self-propagating agents for theinstigation and progression of disease. Alzheimer’s disease and other cerebral proteopathies seem to arise from the de novomisfolding and sustained corruption of endogenous proteins, whereas prion diseases can also be infectious in origin. However,the outcome in all cases is the functional compromise of the nervous system, because the aggregated proteins gain a toxicfunction and/or lose their normal function. As a unifying pathogenic principle, the prion paradigm suggests broadly relevanttherapeutic directions for a large class of currently intractable diseases.

P roteins are essential to cellular metabolism and communication,and they form the framework on which cells and tissues are built.To undertake these roles, most proteins fold into a specific, three-

dimensional architecture that is largely determined by their distinctivesequences of amino acids. Others have a degree of structural flexibility thatenables them to tailor their shape to the task at hand1,2. For proteins, then, asfor the rest of biology, structure governs function. Hence, it is critical for cellsto maintain an efficient quality-control system that ensures the properproduction, folding and elimination of proteins3,4. When a protein misfoldsand evades normal clearance pathways, a pathogenic process can ensue in

which the protein aggregates progressively into intracellular and/or extra-cellular deposits. The consequence is a diverse group of disorders, each ofwhich entails the aggregation of particular proteins in characteristic patternsand locations (Fig. 1)5–8. New insights into the ontogeny of these proteo-pathies are beginning to emerge from the unusual properties of the prion,arguably one of the most provocative molecules in the annals of medicine.

The prion paradigmPrions (‘proteinaceous infectious particles’) are unconventional infec-tious agents consisting of misfolded prion protein (PrP) molecules; in

1Department of Cellular Neurology, Hertie Institute for Clinical Brain Research, University of Tubingen, D-72076 Tubingen, Germany. 2DZNE, German Center for Neurodegenerative Diseases, D-72076Tubingen, Germany. 3Yerkes National Primate Research Center, Emory University, Atlanta, Georgia 30329, USA. 4Department of Neurology, Emory University, Atlanta, Georgia 30322, USA.

a

b

c

d

e

t

t

t

t

f

g

h

Figure 1 | Commonalities among age-relatedneurodegenerative diseases. The depositedproteins adopt an amyloid conformation and showprion-like self-propagation and spreading inexperimental settings, consistent with theprogressive appearance of the lesions in the humandiseases. a, Amyloid-b deposits (senile plaques) inthe neocortex of a patient with Alzheimer’s disease.b, Tau inclusion as a neurofibrillary tangle in aneocortical neuron of a patient with Alzheimer’sdisease. c, a-Synuclein inclusion (Lewy body) in aneocortical neuron from a patient with Parkinson’sdisease/Lewy body dementia. d, TDP-43 inclusionin a motoneuron of the spinal cord from a patientwith amyotrophic lateral sclerosis. Scale bars are50mm in a and 20mm in b–d. e–h, Characteristicprogression of specific proteinaceous lesions inneurodegenerative diseases over time (t, blackarrows), inferred from post-mortem analyses ofbrains. Amyloid-b deposits and tau inclusions inbrains of patients with Alzheimer’s disease (e and f),a-synuclein inclusions in brains of patients withParkinson’s disease (g), and TDP-43 inclusions inbrains of patients with amyotrophic lateral sclerosis(h). Three stages are shown for each disease, withwhite arrows indicating the putative spread of thelesions (for details see refs 5–8). Panels e and f arereproduced, with permission, from ref. 61.

5 S E P T E M B E R 2 0 1 3 | V O L 5 0 1 | N A T U R E | 4 5

Macmillan Publishers Limited. All rights reserved©2013

M Jucker and LC Walker, (2013) Self-propagation of pathogenic protein aggregates in neurodegenerative diseases Nature; 501(7465):45-51

27

Page 28: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

Antibodies may stop propagation

  Small aggregates / oligomers neutralised by antibodies

  Protection of degenerative pathology

  Hope for approach to stop progression and spread of proteo-pathological disorders

28

Page 29: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

Antibodies protect against PD in mouse model

Passive Immunization Reduces Behavioral andNeuropathological Deficits in an Alpha-SynucleinTransgenic Model of Lewy Body DiseaseEliezer Masliah1,2*, Edward Rockenstein1, Michael Mante1, Leslie Crews2, Brian Spencer1, Anthony

Adame1, Christina Patrick1, Margarita Trejo1, Kiren Ubhi1, Troy T. Rohn3, Sarah Mueller-Steiner4, Peter

Seubert4, Robin Barbour4, Lisa McConlogue4, Manuel Buttini4, Dora Games4, Dale Schenk4

1 Department of Neurosciences, University of California San Diego, La Jolla, California, United States of America, 2 Department of Pathology, University of California San

Diego, La Jolla, California, United States of America, 3 Department of Biology, Boise State University, Boise, Idaho, United States of America, 4 ELAN Pharmaceuticals, South

San Francisco, California, United States of America

Abstract

Dementia with Lewy bodies (DLB) and Parkinson’s Disease (PD) are common causes of motor and cognitive deficits and areassociated with the abnormal accumulation of alpha-synuclein (a-syn). This study investigated whether passiveimmunization with a novel monoclonal a-syn antibody (9E4) against the C-terminus (CT) of a-syn was able to cross intothe CNS and ameliorate the deficits associated with a-syn accumulation. In this study we demonstrate that 9E4 was effectiveat reducing behavioral deficits in the water maze, moreover, immunization with 9E4 reduced the accumulation of calpain-cleaved a-syn in axons and synapses and the associated neurodegenerative deficits. In vivo studies demonstrated that 9E4traffics into the CNS, binds to cells that display a-syn accumulation and promotes a-syn clearance via the lysosomalpathway. These results suggest that passive immunization with monoclonal antibodies against the CT of a-syn may be oftherapeutic relevance in patients with PD and DLB.

Citation: Masliah E, Rockenstein E, Mante M, Crews L, Spencer B, et al. (2011) Passive Immunization Reduces Behavioral and Neuropathological Deficits in anAlpha-Synuclein Transgenic Model of Lewy Body Disease. PLoS ONE 6(4): e19338. doi:10.1371/journal.pone.0019338

Editor: Grainne M. McAlonan, The University of Hong Kong, Hong Kong

Received December 22, 2010; Accepted March 28, 2011; Published April 29, 2011

Copyright: ! 2011 Masliah et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permitsunrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: This work was funded by National Institutes of Health (NIH) grants AG 11385, AG 18840, AG 022074 and NS 044233 and by ELAN Pharmaceuticals. NIHhad no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Sarah Mueller-Steiner, Peter Seubert, RobinBarbour, Lisa McConlogue, Manuel Buttini, Dora Games and Dale Schenk are employed by ELAN Pharmaceuticals, who, in collaboration with the group at UCSD,were intellectually involved in the conception and execution of the in vitro and in vivo passive immunization experiments.

Competing Interests: The authors have declared the following conflict of interest: Sarah Mueller-Steiner, Peter Seubert, Robin Barbour, Lisa McConlogue,Manuel Buttini, Dora Games and Dale Schenk are employed by ELAN Pharmaceuticals. There are no patents, products in development or marketed products todeclare. This does not alter the authors’ adherence to all the PLoS ONE policies on sharing data and materials, as detailed online in the guide for authors.

* E-mail: [email protected]

Introduction

Neurodegenerative conditions with accumulation of a-synuclein(a-syn) are common causes of dementia and movement disordersin the aging population. Disorders where the clinical andpathological features of Alzheimer’s Disease (AD) and Parkinson’sDisease (PD) overlap are known as Lewy body disease (LBD) [1].a-Syn is a natively unfolded protein [2] found at the presynaptic

terminal [3] and may play a role in synaptic plasticity [4].Abnormal a-syn accumulation in synaptic terminals and axonsplays an important role in LBD [5,6,7,8]. Recent work hassuggested that a-syn oligomers rather than fibrils might be theneurotoxic species [9,10].

While in rare familial cases mutations in a-syn might contributeto oligomerization [11], it is unclear what triggers a-synaggregation in sporadic forms of LBD. Alterations in a-synsynthesis, aggregation or clearance have been proposed to impactthe formation of toxic oligomers [12,13,14]. Therefore, strategiesdirected at promoting the clearance of oligomers may be oftherapeutic value for LBD. Previous studies have used genetherapy targeting selective regions to increase a-syn clearance viaautophagy or by reducing a-syn synthesis [12,15].

However, neurodegenerative processes in LBD are morewidespread than originally suspected [16] therefore there is aneed for therapeutic approaches that target toxic a-syn in multipleneuronal populations simultaneously. For this reason we began toexplore an immunotherapy approach for LBD and havepreviously shown that active immunization with recombinant a-syn ameliorates a-syn related synaptic pathology in a transgenic(tg) mouse model of PD [17]. Previous studies have shown thatintracellular antibodies (intrabodies) can inhibit a-syn aggregation[18,19] and that copolymer-1 immunotherapy reduces neurode-generation in a PD model [20].

The mechanisms through which a-syn immunotherapy mightwork are unclear given that native a-syn is cytoplasmic. However,it is possible that antibodies may recognize abnormal a-synaccumulating in the neuronal plasma membrane [10,17,21,22] orsecreted forms of a-syn. In support of this possibility, studies haveshown that oligomerized a-syn is secreted in vitro [23] and in vivo[24] via exocytosis, contributing to the propagation of thesynucleinopathy. Moreover, a-syn is present in the cerebrospinalfluid of a-syn tg mice and in patients with LBD [25,26].

This study examined whether passive immunization with anantibody against the C-terminus (CT) of a-syn (hereafter referred

PLoS ONE | www.plosone.org 1 April 2011 | Volume 6 | Issue 4 | e19338

Passive Immunization Reduces Behavioral andNeuropathological Deficits in an Alpha-SynucleinTransgenic Model of Lewy Body DiseaseEliezer Masliah1,2*, Edward Rockenstein1, Michael Mante1, Leslie Crews2, Brian Spencer1, Anthony

Adame1, Christina Patrick1, Margarita Trejo1, Kiren Ubhi1, Troy T. Rohn3, Sarah Mueller-Steiner4, Peter

Seubert4, Robin Barbour4, Lisa McConlogue4, Manuel Buttini4, Dora Games4, Dale Schenk4

1 Department of Neurosciences, University of California San Diego, La Jolla, California, United States of America, 2 Department of Pathology, University of California San

Diego, La Jolla, California, United States of America, 3 Department of Biology, Boise State University, Boise, Idaho, United States of America, 4 ELAN Pharmaceuticals, South

San Francisco, California, United States of America

Abstract

Dementia with Lewy bodies (DLB) and Parkinson’s Disease (PD) are common causes of motor and cognitive deficits and areassociated with the abnormal accumulation of alpha-synuclein (a-syn). This study investigated whether passiveimmunization with a novel monoclonal a-syn antibody (9E4) against the C-terminus (CT) of a-syn was able to cross intothe CNS and ameliorate the deficits associated with a-syn accumulation. In this study we demonstrate that 9E4 was effectiveat reducing behavioral deficits in the water maze, moreover, immunization with 9E4 reduced the accumulation of calpain-cleaved a-syn in axons and synapses and the associated neurodegenerative deficits. In vivo studies demonstrated that 9E4traffics into the CNS, binds to cells that display a-syn accumulation and promotes a-syn clearance via the lysosomalpathway. These results suggest that passive immunization with monoclonal antibodies against the CT of a-syn may be oftherapeutic relevance in patients with PD and DLB.

Citation: Masliah E, Rockenstein E, Mante M, Crews L, Spencer B, et al. (2011) Passive Immunization Reduces Behavioral and Neuropathological Deficits in anAlpha-Synuclein Transgenic Model of Lewy Body Disease. PLoS ONE 6(4): e19338. doi:10.1371/journal.pone.0019338

Editor: Grainne M. McAlonan, The University of Hong Kong, Hong Kong

Received December 22, 2010; Accepted March 28, 2011; Published April 29, 2011

Copyright: ! 2011 Masliah et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permitsunrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: This work was funded by National Institutes of Health (NIH) grants AG 11385, AG 18840, AG 022074 and NS 044233 and by ELAN Pharmaceuticals. NIHhad no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Sarah Mueller-Steiner, Peter Seubert, RobinBarbour, Lisa McConlogue, Manuel Buttini, Dora Games and Dale Schenk are employed by ELAN Pharmaceuticals, who, in collaboration with the group at UCSD,were intellectually involved in the conception and execution of the in vitro and in vivo passive immunization experiments.

Competing Interests: The authors have declared the following conflict of interest: Sarah Mueller-Steiner, Peter Seubert, Robin Barbour, Lisa McConlogue,Manuel Buttini, Dora Games and Dale Schenk are employed by ELAN Pharmaceuticals. There are no patents, products in development or marketed products todeclare. This does not alter the authors’ adherence to all the PLoS ONE policies on sharing data and materials, as detailed online in the guide for authors.

* E-mail: [email protected]

Introduction

Neurodegenerative conditions with accumulation of a-synuclein(a-syn) are common causes of dementia and movement disordersin the aging population. Disorders where the clinical andpathological features of Alzheimer’s Disease (AD) and Parkinson’sDisease (PD) overlap are known as Lewy body disease (LBD) [1].a-Syn is a natively unfolded protein [2] found at the presynaptic

terminal [3] and may play a role in synaptic plasticity [4].Abnormal a-syn accumulation in synaptic terminals and axonsplays an important role in LBD [5,6,7,8]. Recent work hassuggested that a-syn oligomers rather than fibrils might be theneurotoxic species [9,10].

While in rare familial cases mutations in a-syn might contributeto oligomerization [11], it is unclear what triggers a-synaggregation in sporadic forms of LBD. Alterations in a-synsynthesis, aggregation or clearance have been proposed to impactthe formation of toxic oligomers [12,13,14]. Therefore, strategiesdirected at promoting the clearance of oligomers may be oftherapeutic value for LBD. Previous studies have used genetherapy targeting selective regions to increase a-syn clearance viaautophagy or by reducing a-syn synthesis [12,15].

However, neurodegenerative processes in LBD are morewidespread than originally suspected [16] therefore there is aneed for therapeutic approaches that target toxic a-syn in multipleneuronal populations simultaneously. For this reason we began toexplore an immunotherapy approach for LBD and havepreviously shown that active immunization with recombinant a-syn ameliorates a-syn related synaptic pathology in a transgenic(tg) mouse model of PD [17]. Previous studies have shown thatintracellular antibodies (intrabodies) can inhibit a-syn aggregation[18,19] and that copolymer-1 immunotherapy reduces neurode-generation in a PD model [20].

The mechanisms through which a-syn immunotherapy mightwork are unclear given that native a-syn is cytoplasmic. However,it is possible that antibodies may recognize abnormal a-synaccumulating in the neuronal plasma membrane [10,17,21,22] orsecreted forms of a-syn. In support of this possibility, studies haveshown that oligomerized a-syn is secreted in vitro [23] and in vivo[24] via exocytosis, contributing to the propagation of thesynucleinopathy. Moreover, a-syn is present in the cerebrospinalfluid of a-syn tg mice and in patients with LBD [25,26].

This study examined whether passive immunization with anantibody against the C-terminus (CT) of a-syn (hereafter referred

PLoS ONE | www.plosone.org 1 April 2011 | Volume 6 | Issue 4 | e19338

29

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Active versus passive vaccination

Drug Discov Today. 2006 Nov;11(21-22):1028-33 Nat Rev Drug Discov. 2004 Jan;3(1):81-8 Vaccine. 2013 Apr 3;31(14):1777-84

•  mAb therapy is highly effective, but à cost-intensive à many patients develop anti-antibody responses which neutralize the therapeutic potential of mAbs •  Increasingly older populations pose a pharmacoeconomic threat to health- care systems resulting in downward pressure on drug-costs •  Innovative and cost-effective therapies are needed •  Vaccination addresses these issues

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Goal

1) Induction of antibodies recognizing oligomeric and

aggregated α-synuclein

2) Oligomers should be recognized preferentially over

monomeric α-synuclein (à even though native α-synuclein

is intracellular and not obviously accessible to antibodies).

3) Specific T cells should be avoided (see ELAN and their AD

vaccine) à no strong adjuvants and peptide epitopes

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Vaccine Design

Carrier

Linker (SMPH)

Antigen

NN

O

NO

O

O

O O

OCys

Lys

32

•  Non-replicating • Contains RNA as natural TLR7/8 ligand •  Very stable •  Economic production in bacteria •  2 g/l bacterial culture of GMP grade material

Bachmann&Jennnings Nature reviews Immunology 10:787-796

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Aβ1-6 DAEFRHGGC

AβQb

6

16

25

32

47 62 83

175

3 2 1

Epitopes per Qβ monomer

QβAβ1-6 Qβ

Aβ1-42 DAEFRHDSGYEVHHQKLVFFAEDVGSNKGAIIGLMVGGVVIA

CAD106: A Vaccine for Alzheimer`s now in Phase III based on the same principle

33

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-  3 peptides chosen for vaccine design: MDVFMKGL, KNEEGAPQ, EGYQDYEPEA

-  Sequence comprised between 8-10 AA à essentially no T cell epitopes

-  C-term and N-term of proteins generally accessible in aggregates

Amphipathic region Acidic tail NAC domain

1 61 95 140 N-

terminal C-

terminal

N-terminal mAb target C-terminal

Vaccine-Design: Epitope

Page 35: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

Figure 2. Peptide-specific antibody responses induced by the three vaccines and a biosimilar of CAD106 (a vaccine against Alzheimer’s disease currently developed by Novartis) (n=4 mice/group).

Good response with all peptides

35

Amphipathic region Acidic tail NAC domain

1 61 95 140 N-

terminal C-

terminal

N-terminal mAb target C-terminal

Page 36: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

IgG  from  immunised  mice  (VLP-­‐pep6de  3)  day  70

Figure 4. Immunohistochemistry on paraffin-embedded post-mortem brain tissue from a PD patient, Braak stage 4. Purified IgGs (1 mg/mL) used at 1:1000. Region sampled, substantia nigra. Scale bar, 50 µm. Lewy bodies (white arrows), Lewy neurites (black

arrows), Pale body (white arrowhead), intracellular aggregation (white dashed arrows).

Recognition of aggregated α-synuclein (human brain tissue)

36

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IgG  from  immunised  mice  (VLP-­‐pep6de  1)  day  70 IgG  from  immunised  mice  (VLP-­‐pep6de  2)  day  70

Figure 3. Immunohistochemistry on paraffin-embedded post-mortem brain tissue from a PD patient, Braak stage 4. Purified IgGs (1 mg/mL) used at 1:1000. Region sampled, substantia nigra. Scale bar, 50 µm. Lewy bodies (white arrows), intracellular aggregation

(white dashed arrows).

Recognition of aggregated α-synuclein (human brain tissue)

37

Page 38: Martin Bachmann, Immunologie Bern Use of virus-like ... · 1 Regulation of anti-viral B cell responses Use of virus-like particles for therapeutic vaccination against addiction and

Mouse Model of Parkinson`s disease progression of Parkinson's in patients. We will use this state-of-the art model to test the therapeutic efficacy of our novel vaccination approach targeting α-synuclein.

Figure 1. Characterisation of the SNCA-OVX mouse model. SNCA-OVX mice show expression of α-synuclein in TH+ve neurons of the SNc (A), have twice the level of endogenous α-synuclein expression (B), and lose 30% of SNc neurons at 18 months of age compared to the control transgenic line, expressing low levels of α-synuclein (hα−syn) (C). (D) SNCA-OVX mice exhibit reduced evoked release of dopamine from 3 months of age in the dorsal striatum. (E) At 18 months of age SNCA-OVX mice have a decreased ability to remain on the accelerating rotarod. (F) SNCA-OVX mice at 18 months of age take longer to traverse a narrow balance beam and show a greater number of foot-slips. 3) Workplan The setup of the workplan is summarized in Fig. 2.

Fig 2 Workflow of the program As done previously for a vaccine against Alzheimer`s disease, the PI (MFB) will design vaccines based on selected α-synuclein-derived peptides and one protein-based vaccine. Normal and α-synuclein-transgenic mice will be immunized and the induced antibodies will

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0.5 s

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0.5 s

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0.5 s

*** ** ***

A B C

Figure 3

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20

40

60

80

100

120

140

Regio(

[DA] (% of Snca­/­)

CPu NAc0

20

40

60

80

100

120

140

Regio(

CPu NAc0

20

40

60

80

100

120

140

Regio(

CPu NAc0

20

40

60

80

100

120

140

Regio(

CPu NAc0

20

40

60

80

100

120

140

Regio(

**

[DA] (% of Snca­/­)

[DA] (% of Snca­/­)

[DA] (% of Snca­/­)

[DA] (% of Snca­/­)

G H I

J K

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Stim

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Figure 1

B

D

α‐syn 

hα‐syn SNCA‐OVX Snca‐/‐  C57Bl6 

A

C

E

3 m

on

ths

hα-syn SNCA-OVX Snca-/-

18 m

on

ths

hα-syn SNCA-OVX Snca-/-

F

G H

‐ PK  + PK LB509 

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SNCA‐OVX 

CA3 sg

sp

SNpc

SNpr

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

80m 80m 80m

A' C'

3­4 mth 12 mth 18 mth

Snca (­/­)

SNCA OVX

0.5 !"

0.5 s

Snca (­/­)

SNCA OVX

0.5 !"

0.5 s

0.5 !"

0.5 s

*** ** ***

A B C

Figure 3

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#$%&'(

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18 mth

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D

CPu

NAc

0.5 s

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**

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SNCA OVX

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0.5 s

CPu NAc0

20

40

60

80

100

120

140

Regio(

[DA] (% of Snca­/­)

CPu NAc0

20

40

60

80

100

120

140

Regio(

CPu NAc0

20

40

60

80

100

120

140

Regio(

CPu NAc0

20

40

60

80

100

120

140

Regio(

CPu NAc0

20

40

60

80

100

120

140

Regio(

**

[DA] (% of Snca­/­)

[DA] (% of Snca­/­)

[DA] (% of Snca­/­)

[DA] (% of Snca­/­)

G H I

J K

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Stim

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A

C D

E

Figure 2

F

B

Figure 1

B

D

α‐syn 

hα‐syn SNCA‐OVX Snca‐/‐  C57Bl6 

A

C

E

3 m

on

ths

hα-syn SNCA-OVX Snca-/-

18 m

on

ths

hα-syn SNCA-OVX Snca-/-

F

G H

‐ PK  + PK LB509 

Syn‐1 

Snca‐/‐ 

SNCA‐OVX 

CA3 sg

sp

SNpc

SNpr

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

80m 80m 80m

Figure 1

B

D

α‐syn 

hα‐syn SNCA‐OVX Snca‐/‐  C57Bl6 

A

C

E

3 m

on

ths

hα-syn SNCA-OVX Snca-/-

18 m

on

ths

hα-syn SNCA-OVX Snca-/-

F

G H

‐ PK  + PK LB509 

Syn‐1 

Snca‐/‐ 

SNCA‐OVX 

CA3 sg

sp

SNpc

SNpr

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

80m 80m 80m

Figure 1

B

D

α‐syn 

hα‐syn SNCA‐OVX Snca‐/‐  C57Bl6 

A

C

E

3 m

on

ths

hα-syn SNCA-OVX Snca-/-

18 m

on

ths

hα-syn SNCA-OVX Snca-/-

F

G H

‐ PK  + PK LB509 

Syn‐1 

Snca‐/‐ 

SNCA‐OVX 

CA3 sg

sp

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SNpr

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

80m 80m 80m

Figure 1

B

D

α‐syn 

hα‐syn SNCA‐OVX Snca‐/‐  C57Bl6 

A

C

E

3 m

on

ths

hα-syn SNCA-OVX Snca-/-

18 m

on

ths

hα-syn SNCA-OVX Snca-/-

F

G H

‐ PK  + PK LB509 

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CA3 sg

sp

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α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

80m 80m 80m

Figure 1

B

D

α‐syn 

hα‐syn SNCA‐OVX Snca‐/‐  C57Bl6 

A

C

E

3 m

on

ths

hα-syn SNCA-OVX Snca-/-

18 m

on

ths

hα-syn SNCA-OVX Snca-/-

F

G H

‐ PK  + PK LB509 

Syn‐1 

Snca‐/‐ 

SNCA‐OVX 

CA3 sg

sp

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α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

80m 80m 80m

B'

Figure 1

B

D

α‐syn 

hα‐syn SNCA‐OVX Snca‐/‐  C57Bl6 

A

C

E

3 m

on

ths

hα-syn SNCA-OVX Snca-/-

18 m

on

ths

hα-syn SNCA-OVX Snca-/-

F

G H

‐ PK  + PK LB509 

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 Snca‐/‐ 

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α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn

 Snca‐/‐ 

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80m 80m 80m

Figure 1

B

D

α‐syn 

hα‐syn SNCA‐OVX Snca‐/‐  C57Bl6 

A

C

E

3 m

on

ths

hα-syn SNCA-OVX Snca-/-

18 m

on

ths

hα-syn SNCA-OVX Snca-/-

F

G H

‐ PK  + PK LB509 

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sp

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hα‐syn

 Snca‐/‐ 

SNCA‐OVX 

α‐synuclein  TH  α‐synuclein/ TH 

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 Snca‐/‐ 

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80m 80m 80m

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A

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Figure 2

F

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A

C D

E

Figure 2

F

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18'months'

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A

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E

Figure 2

F

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A

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A

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Figure 2

F

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A

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F

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F

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A

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F

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Vaccine'(Design(

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Tes$ng'in'murine'model'

Early'process'development'

progression of Parkinson's in patients. We will use this state-of-the art model to test the therapeutic efficacy of our novel vaccination approach targeting α-synuclein.

Figure 1. Characterisation of the SNCA-OVX mouse model. SNCA-OVX mice show expression of α-synuclein in TH+ve neurons of the SNc (A), have twice the level of endogenous α-synuclein expression (B), and lose 30% of SNc neurons at 18 months of age compared to the control transgenic line, expressing low levels of α-synuclein (hα−syn) (C). (D) SNCA-OVX mice exhibit reduced evoked release of dopamine from 3 months of age in the dorsal striatum. (E) At 18 months of age SNCA-OVX mice have a decreased ability to remain on the accelerating rotarod. (F) SNCA-OVX mice at 18 months of age take longer to traverse a narrow balance beam and show a greater number of foot-slips. 3) Workplan The setup of the workplan is summarized in Fig. 2.

Fig 2 Workflow of the program As done previously for a vaccine against Alzheimer`s disease, the PI (MFB) will design vaccines based on selected α-synuclein-derived peptides and one protein-based vaccine. Normal and α-synuclein-transgenic mice will be immunized and the induced antibodies will

F'3­4 mth 12 mth 18 mth

Snca (­/­)

SNCA OVX

0.5 !"

0.5 s

Snca (­/­)

SNCA OVX

0.5 !"

0.5 s

0.5 !"

0.5 s

*** ** ***

A B C

Figure 3

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0.5 s

)*+,!"

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18 mth

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D

CPu

NAc

0.5 s

)*+,!"

**

*

*

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SNCA OVX

)*+,!"

0.5 s

CPu NAc0

20

40

60

80

100

120

140

Regio(

[DA] (% of Snca­/­)

CPu NAc0

20

40

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80

100

120

140

Regio(

CPu NAc0

20

40

60

80

100

120

140

Regio(

CPu NAc0

20

40

60

80

100

120

140

Regio(

CPu NAc0

20

40

60

80

100

120

140

Regio(

**

[DA] (% of Snca­/­)

[DA] (% of Snca­/­)

[DA] (% of Snca­/­)

[DA] (% of Snca­/­)

G H I

J K

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CPu NAc

Stim

Stim

Figure 1

B

D

α‐syn 

hα‐syn SNCA‐OVX Snca‐/‐  C57Bl6 

A

C

E

3 m

on

ths

hα-syn SNCA-OVX Snca-/-

18 m

on

ths

hα-syn SNCA-OVX Snca-/-

F

G H

‐ PK  + PK LB509 

Syn‐1 

Snca‐/‐ 

SNCA‐OVX 

CA3 sg

sp

SNpc

SNpr

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

80m 80m 80m

A' C'

3­4 mth 12 mth 18 mth

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SNCA OVX

0.5 !"

0.5 s

Snca (­/­)

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Figure 3

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CPu

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0.5 s

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CPu NAc0

20

40

60

80

100

120

140

Regio(

[DA] (% of Snca­/­)

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20

40

60

80

100

120

140

Regio(

CPu NAc0

20

40

60

80

100

120

140

Regio(

CPu NAc0

20

40

60

80

100

120

140

Regio(

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20

40

60

80

100

120

140

Regio(

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[DA] (% of Snca­/­)

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Stim

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A

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Figure 2

F

B

Figure 1

B

D

α‐syn 

hα‐syn SNCA‐OVX Snca‐/‐  C57Bl6 

A

C

E

3 m

on

ths

hα-syn SNCA-OVX Snca-/-

18 m

on

ths

hα-syn SNCA-OVX Snca-/-

F

G H

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Syn‐1 

Snca‐/‐ 

SNCA‐OVX 

CA3 sg

sp

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SNpr

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

80m 80m 80m

Figure 1

B

D

α‐syn 

hα‐syn SNCA‐OVX Snca‐/‐  C57Bl6 

A

C

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on

ths

hα-syn SNCA-OVX Snca-/-

18 m

on

ths

hα-syn SNCA-OVX Snca-/-

F

G H

‐ PK  + PK LB509 

Syn‐1 

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SNCA‐OVX 

CA3 sg

sp

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α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

80m 80m 80m

Figure 1

B

D

α‐syn 

hα‐syn SNCA‐OVX Snca‐/‐  C57Bl6 

A

C

E

3 m

on

ths

hα-syn SNCA-OVX Snca-/-

18 m

on

ths

hα-syn SNCA-OVX Snca-/-

F

G H

‐ PK  + PK LB509 

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sp

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hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

80m 80m 80m

Figure 1

B

D

α‐syn 

hα‐syn SNCA‐OVX Snca‐/‐  C57Bl6 

A

C

E

3 m

on

ths

hα-syn SNCA-OVX Snca-/-

18 m

on

ths

hα-syn SNCA-OVX Snca-/-

F

G H

‐ PK  + PK LB509 

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hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

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80m 80m 80m

Figure 1

B

D

α‐syn 

hα‐syn SNCA‐OVX Snca‐/‐  C57Bl6 

A

C

E

3 m

on

ths

hα-syn SNCA-OVX Snca-/-

18 m

on

ths

hα-syn SNCA-OVX Snca-/-

F

G H

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SNCA‐OVX 

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sp

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hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn 

Snca‐/‐ 

SNCA‐OVX 

80m 80m 80m

B'

Figure 1

B

D

α‐syn 

hα‐syn SNCA‐OVX Snca‐/‐  C57Bl6 

A

C

E

3 m

on

ths

hα-syn SNCA-OVX Snca-/-

18 m

on

ths

hα-syn SNCA-OVX Snca-/-

F

G H

‐ PK  + PK LB509 

Syn‐1 

Snca‐/‐ 

SNCA‐OVX 

CA3 sg

sp

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α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn

 Snca‐/‐ 

SNCA‐OVX 

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn

 Snca‐/‐ 

SNCA‐OVX 

80m 80m 80m

Figure 1

B

D

α‐syn 

hα‐syn SNCA‐OVX Snca‐/‐  C57Bl6 

A

C

E

3 m

on

ths

hα-syn SNCA-OVX Snca-/-

18 m

on

ths

hα-syn SNCA-OVX Snca-/-

F

G H

‐ PK  + PK LB509 

Syn‐1 

Snca‐/‐ 

SNCA‐OVX 

CA3 sg

sp

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α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn

 Snca‐/‐ 

SNCA‐OVX 

α‐synuclein  TH  α‐synuclein/ TH 

hα‐syn

 Snca‐/‐ 

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80m 80m 80m

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Vaccine'(Design(

An-body'specificity(Tes-ng(

Tes$ng'in'murine'model'

Early'process'development'

Janezic et al., PNAS, 2013 38

111-kb wild-type human SNCA locus (Fig. S1A). Two mouse lineswere generated: SNCA-OVX, which overexpresses human α-synto levels that model those associated with SNCA multiplications(10), and hα-syn, which expresses human α-syn at a low/moderatelevel as a control for expression of human α-syn. Both lines were

bred to a mouse α-syn-null (Snca−/−) pure C57/Bl6 background(11) to preclude confounding interactions with endogenous α-syn.Complete transgene integration was confirmed by exon PCRamplification of all six human SNCA exons (Fig. S1B). ForSNCA-OVX mice, a single site of integration was identified by

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Fig. 1. Characterization of α-syn transgenic mice. (A and B) Double immunofluorescence labeling for α-syn and TH confirms human α-syn transgene ex-pression in TH-immunoreactive dopamine neurons of the (A) SNc and (B) VTA in 3-mo-old SNCA-OVX and hα-syn animals. (Scale bars, 200 μm.) (C) Quanti-tative Western analysis of striatal α-syn expression in 3-mo-old SNCA-OVX, hα-syn, Snca−/−, and C57/Bl6 animals reveals that SNCA-OVX animals express thehuman wild-type SNCA transgene at 1.9-fold higher levels compared with endogenous mouse α-syn protein in C57/Bl6 animals. No α-syn expression wasobserved in Snca−/− control animals. One-way ANOVA with Bonferroni post hoc analysis; ****P < 0.0001, ***P < 0.001, n = 2–3. (D) Immunohistochemicalanalysis revealed somatic cytoplasmic α-syn immunostaining in cells of the SNc in 18-mo-old SNCA-OVX mice using the Syn-1 antibody with formic acid (FA)pretreatment. Similar structures were weakly labeled in 18-mo-old SNCA-OVX mice using the LB509 antibody autoclaved (AC) in citric buffer. This staining wasabolished when proteinase K (PK) antigen retrieval was applied instead. All of these immunohistochemical stainings were carried out together with controltissue (entorhinal cortex from a PD patient with dementia that shows prominent Lewy body and neuritic pathology). No “amyloid” pathology was detectedwith thioflavine S in either 18-mo-old SNCA-OVX or Snca−/−, whereas several Lewy bodies and dystrophic neurites were detected in the positive PD control.(Scale bars, 20 μm; magnification: all pictures, 400×.) (E and G) At 3 mo of age, stereological cell counting revealed no differences in the number of TH-immunoreactive neurons in the SNc of SNCA-OVX mice compared with hα-syn and Snca−/− mice. One-way ANOVA: no main effect of genotype: F < 1, P > 0.05,n = 5 per genotype. Data are expressed as the mean ± SEM. Representative images of TH-immunoreactivity in the SNc are shown. (Scale bar, 200 μm.) (F and H)Analysis of 18-mo-old animals revealed a 30% loss of TH-immunoreactive neurons in the SNc of SNCA-OVX mice compared with hα-syn mice. One-way ANOVAwith Bonferroni post hoc analysis: main effect of genotype: F(2,12) = 6.3, *P < 0.05, n = 5 per genotype. Data are expressed as the mean ± SEM. Representativeimages of TH immunoreactivity in the SNc are shown. (Scale bar, 200 μm.)

Janezic et al. PNAS | Published online September 30, 2013 | E4017

NEU

ROSC

IENCE

PNASPL

US

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α-syn is recognized in tg-mouse model

39

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40

Goal

1) Induction of antibodies recognizing oligomeric and

aggregated α-synuclein

2) Oligomers should be recognized preferentially over

monomeric α-synuclein (à even though native α-synuclein

is intracellular and not obviously accessible to antibodies).

3) Specific T cells should be avoided (see ELAN and their AD

vaccine) à no strong adjuvants and peptide epitopes

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41

Soluble proteins versus aggregates

à Low affinity antibodies recognize aggregates but not soluble proteins

Bivalent Binding à „avidity“ Monovalent Binding à „affinity“

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α-synuclein specific Abs have low affinity

Peptide 1 200 nM 190 nM Peptide 3 30 nM 35 nM

Day 14

42

Day 70

Affinity of immune sera

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2. a. Dopamine neurotransmission (FCV)

2. b. Behavioural studies

Study 2

VLP-peptide (20 μg),  s.c.  administra0on  (every  2  weeks  for  1  month,  then  monthly)

0 21 Experimental day (month)

28 (1)

(2) 7 14

Age of animal 10 wks

(3) (4) (5) (6)

14 wks (3.5 mo.)

6 wks

(12) (18)

12 mo.

18 mo.

1. Biochemistry: assess α-synuclein protein burden (ELISA, WB) Study 1

Vaccination of young mice (6 week-old)

Controls: -  SNCA-OVX mice: administration of non-coupled VLPs

Efficacy Experiment Ongoing

43

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Acknowledgements

Cytos Biotechnology, Zürich Gunther Spohn Patrik Maurer Gary Jennings

Hypertension Robert Sabat, Berlin Frank Wagner, Berlin Jürg Nussberger, Lausanne

44

University of Oxford Aadil El-Turabi Marika Doucet Richard Wade-Martins

University Hospital Zürich Franziska Zabel Antonia Fettelschoss Thomas Kündig

BRSC Riga Paul Pumpens Andris Zeltins Andris Dishlers