Blood, Vol. 92 No. 12 (December 15), 1998:
pp. 4836-4843
Characterization of Seven Low Incidence Blood Group Antigens Carried
by Erythrocyte Band 3 Protein
By
P. Jarolim,
H.L. Rubin,
D. Zakova,
J. Storry, and
M.E. Reid
From the Department of Pathology, Brigham and Women's Hospital,
Harvard Medical School, Boston, MA; the Institute of Hematology and
Blood Transfusion, Prague, Czech Republic; the Department of Biomedical
Research, St. Elizabeth's Medical Center, Tufts University School of
Medicine, Boston, MA; and the Immunohematology Laboratory, New York
Blood Center, New York, NY.
 |
ABSTRACT |
Recent studies have demonstrated that band 3 carries antigens of the
Diego blood group system and have elucidated the molecular basis of
several previously unassigned low incidence and high incidence
antigens. Because the available serological data suggested that band 3 may carry additional low incidence blood group antigens, we screened
band 3 genomic DNA encoding the membrane domain of band 3 for
single-strand conformational polymorphisms. We found that the putative
first ectoplasmic loop of band 3 carries blood group antigen ELO, 432 Arg
Trp; the third putative loop harbors antigens
Vga (Van Vugt), 555 TyrHis, BOW 561 ProSer, Wu (Wulfsberg), 565 GlyAla, and
Bpa (Bishop), 569 AsnLys; and the putative fourth
ectoplasmic loop carries antigens Hga (Hughes), 656 ArgCys, and Moa (Moen), 656 ArgHis. We
studied erythrocytes from carriers of five of these blood group
antigens. We found similar levels of reticulocyte mRNA corresponding to
the two band 3 gene alleles, normal content and glycosylation of band 3 in the red blood cell membrane, and normal band 3-mediated sulfate
influx into red blood cells, suggesting that the mutations do not have
major effect on band 3 structure and function. In addition to
elucidating the molecular basis of seven low incidence blood group
antigens, these results help to create a more accurate structural model
of band 3.
© 1998 by The American Society of Hematology.
| |
INTRODUCTION |
BAND 3 (anion exchanger 1 [AE1]) is the
most abundant integral protein of the red blood cell (RBC) membrane,
being present in more than 1 million copies per RBC. It consists of two
structurally and functionally largely independent domains. The
N-terminal cytoplasmic domain of band 3 links the membrane to the
underlying spectrin-based membrane skeleton and interacts with several
glycolytic enzymes, hemoglobin, and hemichromes. The main function of
the C-terminal membrane domain is to mediate exchange of chloride and
bicarbonate anions across the plasma membrane. Current structural
models predict that the membrane domain consists of 12 to 14 transmembrane helices connected by ectoplasmic and endoplasmic
loops.1-4 The longest, fourth loop of band 3 is
N-glycosylated1,4 and the carbohydrate chain carries more
than half of the RBC ABO blood group epitopes.5
Mutations of band 3 protein have been implicated in the pathogenesis of
Southeast Asian ovalocytosis,6,7 hereditary
spherocytosis,8-11 congenital acanthocytosis,12
and, recently, distal renal tubular acidosis.13,14 An amino
acid substitution in the cytoplasmic domain of band 3 underlies the
abnormal electrophoretic mobility of a polymorphic band 3 variant known
as band 3 Memphis.15,16 Yet another variant of band 3, known as band 3 Memphis II, displays, in addition to the abnormal
electrophoretic mobility, an increased binding of the anion flux
inhibitor dihydrodiisothiocyanatodisulfonate, disodium salt
(H2DIDS).17 Spring et al18 reported
that the Memphis II variant of band 3 carries the Dia blood
group antigen.
Dia is a low incidence blood group antigen in Caucasians
that is antithetical to Dib.19 Prevalence of
Dia is much higher in American Indians, reaching up to 54%
in some groups of South American Indians.20 The underlying
polymorphism is a single amino acid substitution in position 854, with
proline of the wild-type band 3 corresponding to the Dib
antigen and leucine to the Dia antigen.21,22
Dia and Dib became the first fully
characterized antigens of the Diego blood group system assigned to the
band 3 protein.21 Subsequently, Bruce et al23
and our group24 have mapped the low incidence blood group
antigen Wra to the C-terminal end of the fourth ectoplasmic
loop. Glutamic acid 658 from the wild-type band 3 sequence underlies
the high incidence antigen, Wrb, whereas the low incidence
antigen, Wra, has lysine in the same position.
Recently, we and others have shown25,26 that three
additional low incidence antigens, Rba,27
WARR,28 and Wda,29 are associated
with different single point mutations on band 3 and therefore belong to
the Diego system. The amino acid changes associated with these three
antigens are, respectively, 548ProLeu,30,31
552ThrIle,32,33 and
557ValMet.30,31,34,35 Although only one subject
has been studied for another low incidence antigen, Tra,
the experimental evidence strongly suggests that it is also located on
the erythroid band 3 protein, with the underlying polymorphism being
551LysAsn.31
Discovery of the molecular basis of these antigens yielded the first
insight into the Diego blood group system as well as valuable
information on the position and size of the external loops of band 3. In addition, in the case of Wrb, it helped to characterize
the site of the band 3-glycophorin A interaction, because the
Wrb antigen requires the presence of both these proteins
for its expression.24,36,37 These results also suggested
band 3 might carry additional low incidence antigens. We therefore
reviewed the list of remaining low incidence antigens that had
serological characteristics consistent with the possibility of their
being carried by band 3 and that we had in liquid nitrogen storage. We
found that antigens Bpa (Bishop),38 Wu
(Wulfsberg),39 Moa (Moen),40
Vga (Van Vugt),41 Hga
(Hughes),42 BOW,43 and ELO44
fulfilled these criteria and proceeded with characterization of their
molecular basis.
| |
MATERIALS AND METHODS |
Subjects.
Samples were obtained through the Serum, Cell and Rare Fluid (SCARF)
exchange program or as gifts from numerous colleagues. Initial testing
was performed on DNA isolated from blood samples stored in liquid
nitrogen; additional testing was performed on freshly drawn blood
samples shipped on ice to Boston. The subjects were heterozygotes for
the studied blood group antigens.
DNA preparation.
DNA was isolated from blood samples (~150 µL) that had been stored
in liquid nitrogen or that had been obtained as fresh samples using the
QIAamp Blood Kit (QIAGEN Inc, Chatsworth, CA). The manufacturer's procedure for DNA isolation from whole blood was followed. The eluted
DNA was used directly for polymerase chain reaction (PCR) amplification.
Single-strand conformational polymorphism (SSCP) analysis and
sequencing of band 3 genomic DNA.
SSCP screening was performed according to Orita et al,45,46
with minor modifications. Exons encoding the membrane domain of band 3 were PCR-amplified using pairs of intronic primers flanking the exons
(Table 1; 35 cycles of 1 minute at 94°C
and 1 minute at 60°C). To each 10 µL PCR reaction, 2.5 µCi
32P-dATP (3,000 µCi/mmol; ICN, Costa Mesa, CA) was added.
The PCR products were diluted in formamide loading buffer (86%
formamide, 10% glycerol, 20 mmol/L EDTA, 0.25% bromophenol blue,
0.25% xylene cyanol), heat-denatured by boiling for 5 minutes, and
quickly cooled on ice. Samples were electrophoresed for 16 hours at
room temperature in a nondenaturing polyacrylamide mutation detection enhancement (MDE) gel (FMC BioProducts, Rockland, ME). Briefly, 25 mL
MDE gel solution was mixed with 69 mL deionized water, 6 mL 10×
TBE, 0.4 mL 10% ammonium persulfate, and 40 µL TEMED, and electrophoresis was performed at 8 W in the presence and at 4 W in the
absence of 10% glycerol. The gel was exposed to Kodak XAR-5 film
(Eastman Kodak, Rochester, NY) overnight at
80°C using intensifying screens. The band 3 gene exons
displaying the SSCP were directly sequenced using the Sequenase version
2.0 DNA Sequencing Kit (Amersham, Arlington Heights, IL). We limited
our SSCP screening to exons 11 to 20 of the band 3 gene, because these
10 exons encode the whole membrane domain of band 3 and mutations
causing altered immunogenicity of band 3 are to be expected only in
this portion of band 3.
Sequence comparisons and structural predictions.
All 12 currently known amino acid sequences of human,1,4
mouse,2 rat,47 chicken,48,49 and
trout50 erythroid band 3 proteins (AE1) and of the related
anion exchangers AE2 from human,51,52 mouse,53
rat,48 and rabbit54 and AE3 from
human,55 mouse,56 and rat48 were
retrieved from Genbank and aligned using the program CLUSTAL (PCGene;
Intelligenetics, Mountain View, CA). Predictions of the number and
position of band 3 transmembrane helices were made using programs
RAOARGOS, HELIXMEM, and SOAP (PCGene) based on the reported human AE1
cDNA sequence.1,4 Based on these predictions, sequence
comparisons, and available data on band 3 modifications by enzymes and
chemicals with known cleavage and binding sites, we created a model of
band 3 with 14 transmembrane helices.
Detection of band 3 mRNA alleles in reticulocyte RNA.
Total reticulocyte RNA was isolated by ammonium chloride
lysis57 and reverse transcribed using random primers. cDNA
was PCR-amplified using primers flanking the mutations, and the PCR product was digested with the appropriate restriction endonuclease. The
digested PCR product was visualized by electrophoresis in agarose gels
stained by ethidium bromide and the amount of DNA of individual bands
was quantitated by densitometric scanning using the Eagle Eye II system
(Stratagene, La Jolla, CA) and the ONE-Dscan 1.0 program (Scanalytics,
Billerica, MA).
Sulfate fluxes and di-isothiocyano-dihydrostilbene disulphonate
(DIDS) titration curves.
Cells were washed three times at 4°C in 140 mmol/L NaCl, 10 mmol/L
Na phosphate, pH 7.4 (PBS), and three times in 84 mmol/L trisodium
citrate, 1 mmol/L EGTA, pH 6.5, and subjected to assays of
unidirectional disodium 35S-sulfate (ICN, Costa Mesa, CA)
uptake in the absence or in the presence of increasing concentrations
of the anion transport inhibitor DIDS (Molecular Probes, Eugene, OR),
as described.10 Each flux study in RBCs carrying the
studied antigens was performed in parallel using RBCs from unrelated
subjects not carrying the antigens. The dependence of the sulfate
influx on the increasing concentrations of DIDS was obtained using the
linear least squares fit.
Enzyme treatment of intact RBCs.
One volume of washed RBCs was treated with 4 vol of 
-chymotrypsin (5 mg/mL) for 1 hour at 37°C. Enzyme-treated cells were washed three
times with PBS. Both treated and untreated antigen-positive RBCs were
tested in parallel with the appropriate antisera.
Quantitation of erythrocyte membrane proteins.
Freshly drawn blood anticoagulated in acid citrate/dextrose was shipped
on ice to Boston. Within 48 hours of phlebotomy, erythrocyte ghosts
were prepared using the method of Dodge et al,58 with minor
modifications described in Jarolim et al.8 Erythrocyte membrane proteins were analyzed by sodium dodecyl
sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) followed by
densitometry as described,9 and the relative amounts of RBC
membrane proteins were expressed as ratios of integrated densitometric
peaks of individuals' proteins to the peak of band 3. The biochemical
findings were correlated with the clinical data and the results were
statistically evaluated.
| |
RESULTS |
SSCP are detected in three exons.
We detected SSCP polymorphisms in exon 12 in the carrier of the ELO
antigen; in exon 14 for Vga, BOW, Wu, and Bpa;
and in exon 16 for Hga and Moa
(Fig 1).
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| Fig 1.
Detection of seven SSCPs. SSCP screening detected
polymorphisms in exon 12 in genomic DNA from the ELO heterozygote, four
polymorphisms in exon 14, and two polymorphisms in exon 16. Two normal
bands (n) visible in wild-type (wt) homozygotes correspond to
complementary strands of PCR-amplified DNA. Heterozygosity is reflected
by the presence of an additional 1 to 2 bands.
|
|
Sequence analysis of genomic DNA shows seven amino acid
substitutions.
We PCR-amplified and directly sequenced exons containing the SSCPs. The
detected mutations are summarized in Table
2. We have verified the presence of these mutations in additional
unrelated carriers of these seven blood group antigens with the
exception of Vga, for which only related individuals were
available. All seven mutations either create or abrogate restriction
sites (Table 2). In six cases, we used PCR amplification followed by
restriction digestion with an appropriate restriction endonuclease to
confirm the presence of the mutation in additional carriers of the
blood group antigen. Because endonuclease Tth 2 is not commercially available, we directly sequenced genomic DNA from the additional Bp(a+)
subject.
Position of the mutated amino acids in band 3.
Figure 2 schematically depicts the membrane
domain of band 3. The seven newly characterized blood group antigens
are shown in bold. Previously characterized blood group antigens
residing on band 3 are also shown. According to this scheme, six of
seven mutated amino acids are located in the putative first, third, and
fourth ectoplasmic loops of band 3, whereas asparagine 569, which is
mutated to lysine in Bp(a+) subjects, is located at the external end of
the sixth transmembrane segment. Proline 561, mutated to serine in the
BOW-positive subject, is also relatively highly conserved; however, the
degree of evolutionary conservation in the region of the third external
loop shown in Table 2 changes to some extent with variations in the
alignment parameters.
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| Fig 2.
Antigens of the Diego blood group system. Schematic
representation of the membrane domain of band 3 based on the structural
predictions described in the Materials and Methods and Results.
Positions of all antigens of the Diego blood group system are
indicated; the seven antigens described in this report are shown in
bold.
|
|
Evolutionary conservation of mutated amino acids.
We aligned the five known AE1 amino acid sequences of the erythroid
band 3 homologues as well as all 12 available sequences from the AE
gene family and evaluated the conservation of individual amino acids.
The results show (Table 2) that most of the mutated amino acids are not
conserved in evolution. The only exception again appears to be the
Bpa antigen (569 AsnLys) that is conserved in all
12 aligned amino acid sequences. Consequently, mutation of Asn 569 would be most likely to affect band 3 structure and anion exchange
function.
Effects of enzyme treatment on RBC agglutinability.
We have digested intact RBCs from the carriers of all seven studied
blood group antigens by trypsin, -chymotrypsin, pronase, and ficin.
The results of testing untreated and enzyme-treated antigen-positive
RBCs are shown in Table 3. At least two
sera containing antibodies to the seven low incidence antigens were tested on two independent experiments. Whereas the results for Vga, BOW, Wu, Hga, and Moa are
expected, the results with ELO and Bpa were not and will be
discussed later.
Similar quantities of normal and mutant mRNA alleles are detected in
reticulocyte RNA.
We isolated and reverse-transcribed total reticulocyte RNA and
amplified the cDNA as described. The PCR products were digested with
the appropriate restriction endonuclease and electrophoresed in an
ethidium bromide-stained gel. Densitometric scanning of the gel allowed
us to estimate the relative content of mRNA corresponding to the two
band 3 alleles of the heterozygous subjects. Using this
semiquantitative technique, we have not detected significant differences between the content of the two band 3 cDNA alleles, suggesting that the mutations affect neither the transcription of the
band 3 gene alleles nor the subsequent RNA processing (data not shown).
The mutations do not affect band 3 expression and function.
SDS-PAGE electrophoresis showed a normal electrophoretic pattern of
band 3 protein in the carriers of the blood group antigens, including
similar profiles of band 3 glycosylation (not shown). Subsequent
densitometric scanning detected normal content of band 3 and other RBC
membrane proteins. Because band 3 is the principal anion exchange
protein of the RBC membrane, we compared anion fluxes in erythrocytes
from carriers of the studied blood group antigens with those in normal
RBCs. We did not detect significant differences between heterozygotes
for the seven studied antigens and control subjects. Results of the
DIDS titration of sulfate influx in the cells expressing the ELO, Wu,
and Hga antigens are shown in
Fig 3.
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| Fig 3.
Band 3-mediated influx of radiolabeled sulfate. Influx of
radiolabeled sulfate into control cells and cells from carriers of the
seven low incidence blood group antigens was measured as described. No
differences between the control wild-type cells and cells expressing
the blood group polymorphisms were detected. Results are shown for the
ELO, Wu, and Hga antigens.
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| |
DISCUSSION |
As of 1995, 37 low incidence antigens were recognized as being discrete
genetic characteristics unassigned to a particular blood group
system.59 Many of the antibodies to these low incidence antigens occur together in multispecific sera.60 Often
these same sera contain antibodies to glycophorin A determinants or to
Wra, whose antithetical antigen Wrb has been
shown to result from the interaction between glycophorin A and band
3.23,24,36 Thus, we undertook a concerted effort to
identify band 3 polymorphisms recognized by these multispecific sera.
This work has led to the identification of seven new band 3 mutations.
All substitutions were studied in more than one subject and the
molecular basis of some of them was evaluated by enzyme treatment of
intact, antigen-carrying erythrocytes. Based on these results, the
International Society for Blood Transfusion (ISBT)/Working Party on
Blood Group Terminology assigned the antigens to the Diego blood group
as 010008 (ELO), 010009 (Wu), 010010 (Bpa), 010011 (Moa), 010012 (Hga), 010013 (Vga),
and 010015 (BOW).
The clinical significance of the seven characterized antigens and their
corresponding antibodies is unclear. The antigens do not represent a
major problem in blood transfusion, because the majority of donors will
lack the antigen. With the exception of ELO,61,62 they have
not been reported in association with a hemolytic disease of the
newborn.
Because it is not clear whether amino acids in the immediate vicinity
of the mutated amino acid residues are sufficient to form the epitope
of the blood group antigen or whether the epitope depends on the
conformation of other portions of band 3, we treated RBCs with enzymes
known to modify external loops of band 3. -Chymotrypsin cleaves band
3 at tyrosines 553 and 555 of the third ectoplasmic loop and, quite
predictably, -chymotrypsin treatment abrogated agglutination of the
Vga-, Wu-, and BOW-positive cells with the corresponding
antibodies. The agglutination of Hga- and
Moa-positive cells was not affected, because their epitopes
are not located in the third loop. The reactivity of both examples of anti-ELO was unaffected by trypsin or ficin treatment of
antigen-positive RBCs. However, whereas one anti-ELO was unaffected by
-chymotrypsin or pronase, the other was nonreactive with RBCs
treated with either of these enzymes. Although this has been observed
previously,63 the reason has not been determined. Perhaps
some anti-ELO antibodies recognize an epitope formed by the interaction
of loop 1 of band 3 with another membrane component that is
-chymotrypsin or pronase sensitive (such as the third loop of band
3). Unexpectedly, neither example of anti-Bpa agglutinated
antigen-positive RBCs that had been treated with any of the enzymes.
Again, it is possible that the epitope recognized by
anti-Bpa requires an interaction of the third loop of band
3 with another, enzyme-sensitive component.
Comparison of the 12 known AE1, AE2, and AE3 sequences predicts a
relatively low degree of conservation for the ectoplasmic loops
compared with the transmembrane segments. Accordingly, five mutations
occur in poorly conserved amino acids, whereas one, asparagine 569, that is mutated to Lys in the Bp(a+) subjects is conserved in all 12 AE
homologues. The high degree of evolutionary conservation of asparagine
569 and its position at the beginning of the sixth transmembrane
segment in the band 3 model (Fig 2) suggested that its substitution by
positively charged lysine may have major structural and functional
consequences. However, we have observed neither morphological
abnormalities of the Bp(a+) RBCs nor differences between DIDS titration
of sulfate influx in the Bp(a+) and control RBCs. Proline 561, mutated
in BOW, is conserved in AE1 and AE2; however, only 3 of 5 AE1 sequences
contain proline in the corresponding position. With the exception of
BOW, we have studied DIDS-inhibitable sulfate influx in fresh
erythrocytes from carriers of the other band 3 mutations and found no
effect on sulfate influx. Based on these results, we propose that the first, third, and fourth ectoplasmic loops are not involved in the
regulation of band 3-mediated anion exchange.
The main contributions of this work, besides clarifying the molecular
basis of seven blood group antigens, are twofold. First, the results
strongly support extracellular localization of the mutated amino acids.
Because available serological data suggest that additional low
incidence blood group antigens may be carried by band 3, ongoing
characterization of such antigens may further improve the structural
model of band 3.
Second, some of the antigens are located in the regions that have been
implicated in the adhesion of modified RBCs to vascular endothelium.64-71 Band 3 was hypothesized to function as a
receptor during invasion of human erythrocytes by Plasmodium
falciparum.64 Naturally occurring anti-band 3 autoantibodies were found to recognize modified band 3 protein on the
surface of Plasmodium falciparum-infected erythrocytes.65 Cytoadherence-related neoantigens on
Plasmodium falciparum-infected human erythrocytes, resulting
from the exposure of normally cryptic regions of the band 3 protein,66 were placed into the third ectoplasmic loop of
band 3.67,68 The antibodies in sera of individuals living
in a malaria-endemic region recognize peptide motifs from the
extracellular loops of band 3,69 and the immune response to
these band 3 neoantigens is associated with low parasite
density.70 Monoclonal antibodies that react with human band
3 residues 542-555 from the third external loop recognize different
band 3 conformations in uninfected and Plasmodium falciparum-infected erythrocytes.71 The cytoadherence
of Plasmodium falciparum could be blocked both with synthetic
peptides corresponding to motifs from the third ectoplasmic loop of
band 3.67 Erythrocytes from carriers of low incidence blood
group antigens in ectoplasmic loops of band 3 may serve as a model for
evaluation of the sequence requirements for adhesion of Plasmodium
falciparum-infected erythrocytes to the vascular endothelium.
Kay72 assigned the senescent RBC antigen to the third
ectoplasmic loop, specifically amino acids 538-554. Erythrocytes
carrying polymorphisms in the external loops of band 3 will again be
useful for evaluation of the role of band 3 in erythrocyte cell aging. It is interesting to note that multiple antibodies to these low prevalence antigens are often found concomitantly in sera that contain
autoreactive erythrocyte antibodies as well as in sera from individuals
who have not received any prior RBC stimulus.
Finally, in a recent communication, Thevenin et al73
reported that synthetic peptides derived from the second and third ectoplasmic regions of band 3 completely inhibited adherence of sickle
cells to an endothelial monolayer in a static assay. These results
again suggested that the third external loop of band 3 plays a role in
the sequence-specific adhesion of modified RBCs to the vascular
endothelium.
The majority of the data on the adhesion of parasitized and sickled
erythrocytes have been obtained from in vitro studies using antibodies
and synthetic peptides. Both these experimental approaches are prone to
artifacts. Large antibody molecules may interfere with numerous
interactions upon binding to the RBC surface. Inhibition of
interactions by synthetic peptides is also frequently nonspecific, and
the peptides may mimic other yet unknown antigens with similar or
identical amino acid sequences. Erythrocytes from donors with
substitutions in the ectoplasmic loops of band 3 represent therefore a
valuable system for testing of the role of this portion of band 3 in
erythrocyte aging, in cytoadherence of malarial parasites, or in
adhesion of parasitized and sickled RBCs to the endothelium.
| |
ACKNOWLEDGMENT |
The authors thank the many colleagues who, over many years, sent us
samples of RBCs expressing low incidence antigens. We also thank the
following people who recently responded to requests for blood samples
from selected donors: Ranjan Malde from the National Blood Service
(London and the South East), London, UK; Graham Rowe from the National
Blood Service (Wales), Cardiff, Wales; Judy Martin from the American
Red Cross (Badger Region), Madison, WI; and Marilyn Moulds from Gamma
Biologicals, Inc (Houston, TX). We thank Dr Jiri Zavadil.
Milena Pohlova from the Institute of Hematology and Blood Transfusion
(Prague, Czech Republic) for help with DNA sequencing and for
preparation of the figures.
| |
FOOTNOTES |
Submitted May 26, 1998;
accepted August 11, 1998.
Supported in part by a grant from the National Blood Foundation (P.J.),
by Grant No. 4118-3 from the Grant Agency of the Ministry of Health,
Czech Republic (P.J.), and by a National Institutes of Health
Specialized Center of Research (SCOR) grant in Transfusion and Medicine
(HL 54459; M.E.R.).
The publication costs of this
article were defrayed in part by
page charge payment. This article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. section
1734 solely to indicate this fact.
Presented in part at the 49th Annual Meeting of the American
Association of Blood Banks, Orlando, FL, October 6-10, 1996.
Address reprint requests to P. Jarolim, MD, PhD, Department of
Pathology, Brigham and Women's Hospital, Harvard Medical School, 75 Francis St, Boston, MA 02111; e-mail: pjarolim{at}rics.bwh.harvard.edu.
| |
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Abstract
Introduction
