Human amyloid-b synthesis and clearance rates as
measured in cerebrospinal fluid in vivo
Randall J Bateman
1–3
, Ling Y Munsell
4
, John C Morris
1,2,5
, Robert Swarm
6
, Kevin E Yarasheski
4
&
David M Holtzman
1–3,7
Certain disease states are characterized by disturbances in
production, accumulation or clearance of protein. In Alzheimer
disease, accumulation of amyloid-b (Ab) in the brain and
disease-causing mutations in amyloid precursor protein or in
enzymes that produce Ab indicate dysregulation of production
or clearance of Ab. Whether dysregulation of Ab synthesis or
clearance causes the most common form of Alzheimer disease
(sporadic, 499% of cases), however, is not known. Here, we
describe a method to determine the production and clearance
rates of proteins within the human central nervous system
(CNS). We report the first measurements of the fractional
production and clearance rates of Ab in vivo in the human CNS
to be 7.6% per hour and 8.3% per hour, respectively. This
method may be used to search for novel biomarkers of disease,
to assess underlying differences in protein metabolism that
contribute to disease and to evaluate treatments in terms
of their pharmacodynamic effects on proposed disease-
causing pathways.
Protein production and clearance are important parameters that are
tightly regulated and reflect normal physiology as well as disease
states
1–4
. Previous studies of protein metabolism in humans have
focused on whole-body or peripheral-body proteins, but not on
proteins produced in the CNS. A technique to measure specific
protein metabolism in the CNS could provide important insights
into CNS protein physiology in health and disease. Certain disease
states are characterized by disturbances in protein production, accu-
mulation or clearance. In the CNS, disturbances in metabolism of
proteins such as the prion protein
5
, alpha-synuclein
6
, tau
7
or Ab
8
can
contribute to and, in some cases, cause neurodegenerative diseases
such as Creuzfeldt-Jakob disease, Parkinson disease, frontotemporal
dementia or Alzheimer disease, respectively.
Biochemical, genetic and animal model evidence implicates Ab as a
pathogenic peptide in Alzheimer disease. The neuropathologic and
neurochemical hallmarks of Alzheimer disease include synaptic loss
and selective neuronal death, a decrease in certain neurotransmitters
and the presence of abnormal proteinaceous deposits in neurons
(neurofibrillary tangles), in the cerebral vasculature (amyloid
angiopathy) and in the extracellular space (diffuse and neuritic
plaques). The main constituent of plaques is Ab, a peptide of 38–43
amino acids cleaved from the amyloid precursor protein (APP)
9,10
.
Throughout life, soluble Ab is secreted mostly by neurons but also
other cell types. In late-onset Alzheimer disease, the total amount of
Ab that accumulates in brain is B100–200-fold higher in homoge-
nates from Alzheimer disease brains than from control brains
11
.
Disturbance of Ab production can lead to rare forms of Alzheimer
disease in humans. Mutations in three different genes (APP, PSEN1
and PSEN2), which cause early-onset autosomal dominant Alzheimer
disease, all result in overproduction of total Ab or Ab
42
(ref. 9). In
Down syndrome, three copies of APP result in increased production of
Ab, and 100% of individuals with Down syndrome develop Alzheimer
disease pathology by age 35 (ref. 12). In late-onset Alzheimer disease
(B99% of cases), however, there is not strong evidence for over-
production of Ab. Therefore, the underlying cause of deposition of Ab
(increased production versus decreased clearance) is not known for
most cases of Alzheimer disease.
No methods were previously available to quantify protein synthesis
or clearance rates in the human CNS. Such a method would be
valuable to assess not only Ab synthesis and clearance rates in humans
but also the metabolism of a variety other proteins relevant to diseases
of the CNS. To address crucial questions about underlying pathogen-
esis of Alzheimer disease and Ab metabolism, we developed a method
for quantifying the fractional synthesis rate (FSR) and fractional
clearance rate (FCR) of Ab in vivo in the human CNS. Our results
indicate that by administering a stable isotope-labeled amino acid
(
13
C
6
-leucine), sampling cerebrospinal fluid (CSF) and using
high-resolution tandem mass spectrometry to quantify labeled
Ab, reproducible rates of Ab synthesis and clearance can be quantified
in humans.
RESULTS
In vivo labeling and quantification of Ab
To determine whether labeled Ab (Fig. 1) could be produced and
detected in vivo in a human, one individual underwent a 24-h infusion
of labeled leucine followed by a lumbar puncture to obtain CSF. We
immunoprecipitated Ab from the CSF sample with the Ab-specific
Received 2 November 2005; accepted 24 January 2006; published online 25 June 2006; doi:10.1038/nm1438
1
Departments of Neurology,
2
The Alzheimer Disease Research Center,
3
Hope Center for Neurological Disorders
4
Medicine,
5
Pathology and Immunology,
6
Anesthesiology and
7
Molecular Biology & Pharmacology, Washington University School of Medicine, 660 South Euclid Avenue, Box 8111, St. Louis, Missouri 63110,
USA. Correspondence should be addressed to R.J.B. (batemanr@neuro.wustl.edu).
856 VOLUME 12 [ NUMBER 7 [ JULY 2006 NATURE MEDICINE
TECHNICAL REPORTS
© 2006 Nature Publishing Group http://www.nature.com/naturemedicine