BRIEF REPORT
Clinical Infectious Diseases
542 • CID 2019:69 (1 August) • BRIEF REPORT
Received 6 September 2018; editorial decision 28 November 2018; accepted 22 December
2018; published online December 24, 2018.
Correspondence: R. Loomba, NAFLD Research Center; Division of Gastroenterology and
Epidemiology, University of California, San Diego, 9500 Gilman Drive, MC 0887, La Jolla, CA
92093 (roloomba@ucsd.edu).
Clinical Infectious Diseases
®
2019;69(3):542–5
© The Author(s) 2018. Published by Oxford University Press for the Infectious Diseases Society
of America. All rights reserved. For permissions, e-mail: journals.permissions@oup.com.
DOI: 10.1093/cid/ciy1100
Discovery of Half-life of Circulating
Hepatitis B Surface Antigen in Patients
With Chronic Hepatitis B Infection
Using Heavy Water Labeling
Rohit Loomba,
1
Martin Decaris,
2
Kelvin W. Li,
2,3
Mahalakshmi Shankaran,
3
Hussein Mohammed,
2,3
Marcy Matthews,
2,3
Lisa M. Richards,
1
Phirum Nguyen,
1
Emily Rizo,
1
Barbara Andrews,
1
Robin Soto,
1
Thomas Angel,
3
Vithika Suri,
4
Kathryn M. Kitrinos,
5
Dwight Barnes,
6
Gregg Czerwieniec,
6
Kathy Brendza,
6
G. Mani Subramanian,
4
Anuj Gaggar,
4
and Marc K. Hellerstein
2,3
1
NAFLD Research Center, University of California, San Diego, La Jolla,
2
KineMed, Inc.,
Emeryville,
3
Department of Nutritional Sciences and Toxicology, University of California
Berkeley,
4
Clinical Research,
5
Biomarkers, and
6
Biology, Gilead Sciences, Inc., Foster City,
California.
In a pilot study, heavy water labeling was used to determine
hepatitis B surface antigen (HBsAg) turnover rates in chronic
hepatitis B (CHB) patients. Te mean (standard deviation)
half-life of HBsAg in blood was 6.7 (5.5) days, which refects
recent production in the liver and supports strategies aimed at
reducing HBsAg production in CHB patients.
Keywords. HBV; deuterated water; hepatitis B surface an-
tigen; half-life.
Te hepatitis B virus (HBV) releases a large quantity of viral
proteins into the infected patient’s circulation. Te most clin-
ically important of these subviral particles is the hepatitis B
surface antigen (HBsAg), as its elimination from circulation
is regarded as functional cure of chronic HBV [1]. HBsAg is
composed of 3 glycosylated proteins: small, middle, and large
proteins. Circulating levels of HBsAg can be used to monitor the
natural history of the disease and have recently been shown to be
predictive of response to treatment [2]. Currently approved an-
tiviral agents are highly efective in suppressing viral replication
and reducing liver fbrosis but have minimal efect in reducing
the levels of HBsAg and other plasma proteins [3]. In recent
years, researchers have increasingly targeted elimination of
HBsAg as an endpoint in clinical trials. However, the production
rate and the elimination rate of HBsAg have not been defnitively
quantifed. Importantly, the question of whether the persistence
of blood HBsAg refects ongoing production by the liver or
very slow clearance of the protein or a subpopulation of protein
molecules from blood remains unknown and has implications
for therapeutic attempts to eliminate HBsAg. We conducted a
small pilot study to determine the half-life of HBsAg, with the
aim of increasing our understanding of disease biology and
aiding the development of future therapeutic strategies.
Heavy water (
2
H
2
O) labeling is based on the incorporation
of tracer levels of deuterium (
2
H) into covalent C-H bonds of
amino acids, which occurs only in newly synthesized proteins,
allowing for sensitive measurements of in vivo protein synthesis
[4–6]. Te distribution of
2
H label in body water is rapid and
to all tissues following oral ingestion of
2
H
2
O and persists in
the body with a half-life of 7–10 days [6]. Elevated
2
H levels
in body water label the intracellular pool of amino acids in a
predictable manner [5, 6], thereby labeling newly synthesized
proteins. Using tandem mass spectrometric analysis of peptides
from proteins afer trypsin hydrolysis, the fraction of newly
synthesized proteins in the pool can be quantifed and protein
synthesis rates can be calculated by kinetic modeling [6]. Tis
method has several important advantages over traditional la-
beling methods, including high sensitivity of tandem mass
spectrometry for proteins, the defnitive identifcation and pu-
rity of peptides assigned to parent proteins, and the fact that
heavy water can be administered safely at low doses over days,
weeks, or months, an appropriate timeframe for the measure-
ment of proteins spanning a wide range of turnover rates. Te
half-lives (t
1/2
) of large numbers of human serum proteins as
well as individual proteins in blood have been determined using
this methodology [7–12]. Here, we describe the utilization of
heavy water labeling with tandem mass spectrometric anal-
ysis to measure the turnover of circulating HBsAg in patients
infected with HBV.
METHODS
Deuterated water (70%) was administered to all patients orally
over 21 days according to the following regimen: 50 mL 3 times
a day for 4 days (doses taken 3 or more hours apart) followed
by 50 mL twice a day for the remaining 17 days, in order to
maintain enrichment of 1.0%–2.0%
2
H in body water. Plasma
and saliva samples were drawn at 6 timepoints: baseline and
days 3, 7, 10, 14, and 21 for determination of body water en-
richment (from saliva samples) with immunoprecipitation of
HBsAg from plasma for mass spectrometric analysis of isotopic
labeling changes over time.
Briefy, HBsAg was immunoprecipitated using the HBsAg
antibody (GS-645730) with 30 μg/mg of epoxy-coated mag-
netic beads and then separated by molecular weight via sodium
dodecyl sulfate–polyacrylamide gel electrophoresis. Gel bands
containing the 3 HBsAg subtypes (small [20–25 kD], medium
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