Genetic characterisation of adenovirus type 8 isolated in Hiroshima city over a 15 year period.
ABSTRACT To investigate the genetic differences among the strains of adenovirus type 8 (Ad8) circulating in Hiroshima city, Japan, and to study their circulation pattern.
One hundred and twenty nine strains of adenovirus type 8 (Ad8) were isolated in Hiroshima City over a 15 year period (1983-97) from patients with keratoconjunctivitis, and analysed with six restriction enzymes-BamHI, HindIII, PstI, SacI, SalI, and SmaI-to investigate possible relations among the isolates and their genetic variability. Seven hypervariable regions of the hexon gene that carry the type specific epitope were also sequenced to investigate the variation among the genome types.
Restriction endonuclease analyses yielded three known genome types (Ad8A, 13 samples; Ad8B, seven samples; and Ad8E, 35 samples) and a novel genome type (Ad8I, 74 samples). Ad8A, Ad8B, and Ad8E were closely related, with 96% homology, whereas Ad8I had only 71% homology. Ad8A, Ad8B, and Ad8E shared 91.8% and 96.4% homology with regard to their amino acid and nucleotide sequences, respectively, with the isolate 1127 (accession no X74663). However, when compared with Ad8A, Ad8B, Ad8E, and isolate 1127, Ad8I shared only 62.7% and 69.9% homology with regard to amino acid and nucleotide sequences, respectively. Ad8A, Ad8B, and Ad8E had a unique 31 amino acid deletion in the hypervariable region 1 of the hexon gene, whereas Ad8I had a 33 residue deletion. The Ad8E strain that circulated from 1984 to 1995 was stable among the study population. Ad8I was isolated from an outbreak of epidemic keratoconjunctivitis in 1995 and was also isolated from sporadic cases until 1997.
These results confirmed that genetic variability occurs in Ad8 in the microenvironment and revealed the emergence of a new genome type (Ad8I).
- New England Journal of Medicine 01/1974; 289(25):1341-6. · 51.66 Impact Factor
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ABSTRACT: We studied the restriction endonuclease cleavage patterns of DNAs of adenovirus type 8 (Ad 8) isolated from epidemic keratoconjunctivitis cases. DNAs of 25 Ad 8 isolates collected during the period from 1975 to 1981 in Sapporo were subjected to enzymatic cleavage with PstI, BamHl , HindIII and SalI. On the basis of the cleavage patterns, the isolates were divided into two subtypes, A and B, both different from Trim strain used as the Ad 8 prototype strain. Subtype A was prevalent in the period from 1975 to 1978, while subtype B in the period from 1976 to 1981.Japanese journal of medical science & biology 01/1984; 36(6):307-13.
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ABSTRACT: Adenovirus type 8 strains were collected over a 19-year period from eye specimens from patients with keratoconjunctivitis. These strains were divided by restriction enzyme analysis with the endonucleases SalI, HindIII, SacI, KpnI, and SmaI into three genotypic subgroups. The prototype strain (Trim) was found throughout the United States from 1966 through 1985 and also in Taiwan and Greece in the early 1980s. Genotype 8C was identified in an arc from Maryland to Missouri to Alabama from 1971 through 1974. Genotype 8D was found only in an epidemic of eye disease among Vietnamese refugees being resettled in northwest Florida in 1975. Genotypes 8C and D were distinct from genotypes 8A and B described from Japan in 1975 through 1981. Hemagglutination tests with a battery of avian and mammalian erythrocytes did not distinguish between the genotypic subgroups. Similarly, the genotypes could not be differentiated by hemagglutination inhibition or serum neutralization tests with reference prototype antisera. The long-term prevalence of the Trim strain suggests that adenovirus type 8 has greater genetic stability than the other adenovirus types studied to date.Journal of Clinical Microbiology 04/1986; 23(3):469-74. · 4.07 Impact Factor
Genetic characterisation of adenovirus type 8 isolated in
Hiroshima city over a 15 year period
A K Adhikary, J Numaga, T Kaburaki, H Kawashima, M Araie, Y Ikeda,
T Ogino, E Suzuki, H Ushijima, A Mukoyama, S Matsuno, T Inada, N Okabe
J Clin Pathol 2003;56:120–125
Aims: To investigate the genetic differences among the strains of adenovirus type 8 (Ad8) circulating
in Hiroshima city, Japan, and to study their circulation pattern.
Methods: One hundred and twenty nine strains of adenovirus type 8 (Ad8) were isolated in Hiroshima
City over a 15 year period (1983–97) from patients with keratoconjunctivitis, and analysed with six
restriction enzymes—BamHI, HindIII, PstI, SacI, SalI, and SmaI—to investigate possible relations
among the isolates and their genetic variability. Seven hypervariable regions of the hexon gene that
carry the type specific epitope were also sequenced to investigate the variation among the genome
Results: Restriction endonuclease analyses yielded three known genome types (Ad8A, 13 samples;
Ad8B, seven samples; and Ad8E, 35 samples) and a novel genome type (Ad8I, 74 samples). Ad8A,
Ad8B, and Ad8E were closely related, with 96% homology, whereas Ad8I had only 71% homology.
Ad8A, Ad8B, and Ad8E shared 91.8% and 96.4% homology with regard to their amino acid and
nucleotide sequences, respectively, with the isolate 1127 (accession no X74663). However, when
compared with Ad8A, Ad8B, Ad8E, and isolate 1127, Ad8I shared only 62.7% and 69.9% homol-
ogy with regard to amino acid and nucleotide sequences, respectively. Ad8A, Ad8B,and Ad8E had a
unique 31 amino acid deletion in the hypervariable region 1 of the hexon gene, whereas Ad8I had a
33 residue deletion. The Ad8E strain that circulated from 1984 to 1995 was stable among the study
population. Ad8I was isolated from an outbreak of epidemic keratoconjunctivitis in 1995 and was also
isolated from sporadic cases until 1997.
Conclusions: These results confirmed that genetic variability occurs in Ad8 in the microenvironment
and revealed the emergence of a new genome type (Ad8I).
type 8 (Ad8) is the most common agent of epidemic
keratoconjunctivitis (EKC). EKC is a highly contagious ocular
infection and is often transmitted through ocular facilities,
thus causing community epidemics.3–6Type specific neutralisa-
tion, which is used for the identification of adenoviruses, can-
not distinguish genetic variation among the isolates. Ad8
genomic variants (genome types) have been classified as
Ad8A to Ad8H7–11and Ad8/D1 to Ad8/D1212–14by means of
restriction enzyme analysis of prototype and field isolates.This
genome typing has provided a powerful and practical tool for
the study of the epidemiological and clinical patterns of
adenoviruses. Although adenoviral ocular infection is com-
mon in Japan and other East Asian countries,15 16the distribu-
tion of the various genome types has not been investigated
extensively. So far, only the circulation of genome types Ad8A
and Ad8B in the north part of Japan (Sapporo) has been
he 51 serotypes of human adenovirus are classified into
six subgenera, A to F, according to their biological,
immunological,and biochemical properties.1 2Adenovirus
“Epidemic keratoconjunctivitis is a highly contagious
ocular infection and is often transmitted through ocular
facilities, thus causing community epidemics”
In our study, Ad8 strains isolated in Hiroshima city over a 15
year period were analysed with six restriction enzymes
(BamHI, HindIII, PstI, SacI, SalI, and SmaI) to investigate the
genetic differences among the isolates, and their circulation
pattern. Hypervariable regions (HVRs) of the hexon gene that
carry type specific epitopes were also sequenced to document
the degree of variation among the genome types, which may
have some relation to the disease.
MATERIALS AND METHODS
In total, 129 strains were isolated from epidemic and sporadic
cases of keratoconjunctivitis. The clinical diagnosis was
recorded as EKC, acute haemorrhagic conjunctivitis, or acute
conjunctivitis. All samples were isolated in Hep2 cells.
DNA was extracted from the infected cells by a modified Hirt’s
procedure. Briefly, confluent monolayers of Hep2 cells in
25 cm2flasks were inoculated with virus stock and incubated
dislodged with a cell scraper and pelleted by low speed
centrifugation. Cells were washed twice with phosphate buff-
ered saline and resuspended in 1 ml of lysis buffer (10mM
Tris/HCl (pH 7.4), 10mM EDTA, 1% sodium dodecyl sulfate
(SDS)) for 15 minutes at room temperature. The suspension
was incubated with 200 µg/ml of proteinase K (Sigma Chemi-
cal, St Louis, Missouri, USA) at 37°C for one hour. After incu-
bation,5M NaCl was added to a final concentration of 1M,and
further incubated at 4°C overnight to precipitate cellular DNA.
Abbreviations: Ad8, adenovirus type 8; EKC, epidemic
keratoconjunctivitis; HVR, hypervariable region; PCR, polymerase chain
reaction; PCRF, pairwise comigrating restriction fragments; SDS, sodium
dodecyl sulfate; TE buffer, Tris/EDTA buffer
See end of article for
Dr Numaga, Department of
School of Medicine, The
University of Tokyo,
Kita-ku, Tokyo 114-0024,
Japan; jnumaga @
Accepted for publication
19 September 2002
The suspension was then centrifuged at 15 000 ×g for 30 min-
utes. The supernatant was incubated with 30 µg of RNase A
(Sigma Chemical) for one hour and extracted twice in phenol/
chloroform. Next, the supernatant was precipitated in two
volumes of 100% ethanol. After drying, the DNA was
suspended in 50 µl of Tris/EDTA buffer (10mM Tris/HCl
(pH 7.4),10mM EDTA) and measured spectrophotometrically.
DNA restriction enzyme analysis
Restriction enzyme analyses were performed with BamHI,
HindIII, PstI, SacI, SalI, and SmaI (Boehringer Mannheim,
Mannheim, Germany). Briefly, a 2 µg aliquot of DNA was
incubated with 10 units of restriction endonucleases in 20 µl
of reaction mixture at an appropriate temperature (that
recommended for each restriction endonuclease) for three
hours. After digestion, all products were electrophoresed on a
1.2% horizontal submerged agarose gel at 90 V for three hours
in 50 mM Tris acetate EDTA buffer (pH 8.0). The gel was
stained with ethidium bromide (1 µg/ml) and photographed
under ultraviolet light with a polaroid camera (Funakoshi,
Tokyo, Japan). HindIII digests of λ DNA (Boehringer
Mannheim) were used as molecular weight markers.Genomic
homology between the two strains was calculated using the
percentage of pairwise comigrating restriction fragments
(PCRF) of a pair divided by the total number of bands in the
pair.Genome type identifications were conducted by compari-
son of the resulting patterns with the published restriction
patterns of the prototype and genome types.7 8 12
PCR, cycle sequencing, and sequence analysis
HVRs were sequenced by generating overlapping polymerase
chain reaction (PCR) products and direct cycle sequencing. A
set of six primers (forward primers: AdHD1N, 5′-TGG ACC
CCA TGC TAT GGC TC-3′ (439 to 459); and AdHD3F, 5′-TGG
TCG ACT TGC AAG ACA G-3′ (824–842); reverse primers:
AdHD2R, 5′-TAG GTT GAC CAT CTT CAG TGG T-3′ (526–505);
AdHD3R, 5′-CTG TCC ACC GCA GAG TTC CA-3′ (929–911);
and AdHd4,5′-GCC ACG TTC GAG TAC AGA AAA C-3′ (1187–
1166)) were selected based on the alignment of hexon gene
sequences available from GeneBank (Ad8 (X74663), Ad19
(X74666)) from human adenovirus serotypes Ad8, Ad19,
Ad37, Ad9, and Ad15, respectively. All products were
sequenced in both directions with internal and template
primers. Full length adenoviral DNA, extracted by Hirt’s
method, was used as a template for PCR. The PCR amplifica-
tion was carried out in 50 µl reaction mixtures containing 1 µl
aliquots of DNA, 5 µl of 10× concentrated buffer, 0.5 µM each
of the primer pair, 200 µM of each dNTP, and 1.25 U of Taq
polymerase (Boehringer Mannheim). The assays were per-
formed in a programmable heat block (model 9600-R; Perkin
Elmer,Foster City,California,USA).Thermal cycling consisted
of preliminary denaturation for three minutes at 94°C,
Ad9 (X74664),and Ad15
followed by 35 cycles of denaturation at 94°C for one minute,
annealing at 47°C for one minute and at 72°C for two minutes,
and a final extension at 72°C for seven minutes. The amplifi-
cation products were analysed on a 1.5% agarose gel.Next,the
Hiroshima. The open boxes indicate cleavage patterns identical to
those of Ad8B. The various shaded boxes indicate cleavage patterns
different from those of Ad8B and also distinct from each other.
Identification of adenovirus type 8 (Ad8) genome types in
electrophoresed on a 1.2% agarose gel with a HindIII digest of λ
DNA (lane m) as molecular weight standard. Lanes A, B, E, and I
contain genome types Ad8A (isolates from 1983), Ad8B (from 1984),
Ad8E (from 1994), and Ad8I (from 1995), respectively. Ad8 digested
with (A) SalI and PstI; (B) SmaI and BamHI; (C) HindIII and SacI.
Restriction fragments of adenovirus type 8 (Ad8) were
Genome typing of adenovirus type 8121
PCR products were purified using a DNA fragment purifica-
tion kit (Mag Extractor-PCR and Gel Cleanup; Toyobo, Osaka,
Japan) according to the manufacturer’s instructions.The cycle
sequence reaction was carried out with an ABI prism dye ter-
minator cycle sequencing ready reaction kit (Applied Biosys-
tems, Chiba, Japan). The sequences were determined by a
genetic analyser 310 (Applied Biosystems). The nucleotide
sequences of four genome types (Ad8A, Ad8B, Ad8E, and
Ad8I) were compared with the available sequence of the Ad8
isolate, 1127 (accession number, X74663). DNASIS software
(Hitachi Software Ltd, Tokyo, Japan) was used for sequence
alignment and analysis.
Nucleotide sequence accession numbers
Sequence data from this article have been deposited in
GeneBank/DDBJ under the accession numbers: hexon gene
Ad8A (AB090341),Ad8B (AB090342),Ad8E (AB090343),and
Ad8I (AB090344). The amino acid sequences of the residues
Prevalence among the age groups
Patients were divided into three age groups: 0–9 years, 10–19
years,and > 20 years.Thirty two (24.8%) of the stains isolated
came from the 0–9 year old group,whereas only 9 (6.9%) were
in the 10–19 year old group. Most isolates (88 (68.2%)) came
from the > 20 years old group.
Cleavage patterns with the restriction endonucleases
Restriction endonuclease cleavage patterns with SacI, PstI,
and SmaI divided the isolates into two groups, whereas
HindIII and SalI divided them into three groups (fig 1).
Cleavage pattern with HindIII
Upon digestion with HindIII, 20 isolates showed identical
restriction patterns shared by Ad8A and Ad8B. Thirty five iso-
lates, classified as Ad8E, showed a distinct restriction pattern.
However, 74 isolates showed a different restriction pattern.
These isolates are a novel genome type, designated Ad8I (fig
Cleavage pattern with SalI
Upon digestion with SalI, 48 isolates showed a similar restric-
tion pattern to that of Ad8A and Ad8E. The pattern of seven
isolates was identical to that of Ad8B. However, 74 isolates
showed a new restriction pattern (fig 2A).
Cleavage pattern with PstI, SmaI, and SacI
Fifty five isolates showed restriction patterns that correspond
with Ad8A, Ad8B, and Ad8E. However, 23 isolates showed a
new restriction pattern (fig 2A–C).
Cleavage pattern with BamHI
BamHI was not useful for distinguishing between the
different isolates because they all showed an identical restric-
tion pattern (fig 2B).
Genome type circulation
The analysis of 129 isolates from Hiroshima using six restric-
tion enzymes (Bam HI, HindIII, PstI, SacI, SalI, and SmaI)
yielded three known genome types, namely: Ad8A (13
isolates), Ad8B (seven isolates), and Ad8E (35 isolates) and a
new genome type, designated Ad8I (74 isolates) (fig 2). Ad8A
and Ad8B circulated between 1983 and 1988, and Ad8E
between 1984 and 1995.Ad8I was first isolated from epidemic
cases in 1995, and then from sporadic cases of EKC until 1997
Homology among the genome types
DNA homology studies of serotype 8 are often difficult, owing
to its growth properties. Some strains grow well but others
replicate slowly in the laboratory,as reported previously.12 14In
our study,there was not enough DNA for the analysis of small
fragments with low molecular weight.
in Hiroshima. The distribution of Ad8 genome types in Hiroshima on
a yearly basis. Ad8A (A) and Ad8B (B) were co-circulating from
1983 to 1988. Ad8E (E) was co-circulating with Ad8A and Ad8B
from 1984 to 1988 and circulated as a single genome type from
1989 to 1995. A new genome type Ad8I (I) was isolated from the
outbreak of epidemic keratoconjunctivitis in 1995. All 66 cases from
the outbreak were Ad8I. Ad8I was subsequently recovered from
sporadic cases in 1996 and 1997.
Annual trends of adenovirus type 8 (Ad8) genome types
restriction endonuclease cleavage fragments from the
DNA of Ad8 genome type
Pairwise comparison of comigrating
Number of comigrating fragments
Ad8AAd8B Ad8E Ad81
Ad8, adenovirus type 8.
122Adhikary, Numaga, Kaburaki, et al
Pairwise comparison of PCRF showed that Ad8A has a total
of 48 fragments for the six restriction enzymes. Ad8B and
Ad8E shared 46 (96%) fragments with Ad8A, whereas Ad8I
shared 34 (71%) fragments with Ad8A (table 1).
Nucleotide sequence analysis
Ad8A, Ad8B, and Ad8E share 91.8% and 96.4% homology in
their amino acid and nucleotide sequences, respectively, with
the isolate 1127 (accession number, X74663) at the HVRs of
the hexon gene. However, when compared with Ad8A, Ad8B,
Ad8E, and isolate 1127, Ad8I shared only 62.7%. and 69.9%
homology in amino acid and nucleotide sequences, respec-
tively. Ad8A, Ad8B, and Ad8E showed a unique deletion of 31
amino acids in HVR 1, whereas Ad8I showed a 33 residue
deletion (fig 4).
Ad8 has a much higher tropism for conjunctival cells and pro-
duces more severe clinical manifestations and pathological
8 (Ad8). The sequences of loop 1 (L1) and loop 2 (L2) have been aligned to obtain maximal homology. Deduced amino acid sequences of the
Ad8 isolate, 1127, was obtained from Gene Bank (accession number, X74663). Ad8 (x) indicates isolate 1127.
Comparison of predicted amino acid sequences of seven hypervariable regions (HVRs) among the genome types of adenovirus type
Genome typing of adenovirus type 8123
alterations in EKC than do the Ad19 and Ad37 types. Thus,
Ad8 has been the target of extensive studies, including those
at the molecular level. This serotype persists in the population
and causes sporadic epidemics, whereas Ad19 and Ad37
seemed to pass through the population in individual waves.9
Ad8 also has more genomic variants than Ad19 and
Ad37.7 8 12 15Genome typing by restriction endonucleases had
been used successfully to establish separate identities at the
molecular level of otherwise serologically identical strains.
This typing offers a chance to follow the epidemiological dis-
tribution of the virus in different geographical regions and
time periods. Ad8 is currently endemic in Japan and other
East Asian countries.7 8 15Ad8 isolates from the Asian Pacific
and the USA are classified into genome types Ad8A to Ad8H
(table 2). The interdomestic circulation of some genome types
(for example, Ad8E in Taiwan, Korea, and Japan; Ad8D in Tai-
wan and the USA) has been documented.In Japan,molecular
studies of Ad8 were conducted only in the northern part of the
country (Sapporo) and only two genome types, Ad8A and
Ad8B, were reported between 1975 and 1986.
Among four genome types detected in Hiroshima, Ad8A
and Ad8B circulated for a short period of time, from 1983 to
1988. However. Ad8E was genetically stable among the popu-
lation of Hiroshima for a longer period of time, from 1984 to
early 1995. In comparison, Ad8E circulated in Taiwan
(Kaoshiung) and Korea (Pushan) in 1981–1987 and in 1983,
“The isolation of a new genome type is medically and
epidemiologically important because the appearance of
new genome types can result in more severe attacks of
The novel genome type Ad8I, which replaced Ad8E, circulated
for a short period of time from 1995 to 1997.Ad8I was isolated
from an outbreak of EKC in 1995, which affected mainly the
older age group. The same genome type was isolated from
sporadic cases until 1997. It is unclear whether this new
genome type was imported from elsewhere or evolved
indigenously.A large number of tourists visit Hiroshima every
year.There is a strong possibility that some travellers may have
unwittingly imported the new strain. This type of situation
occurred in a Vietnamese refugee camp in Florida, USA in
1975, where Vietnamese children suffered from EKC as a
result of Ad8D infection after they were transferred from
Thailand to Florida. It is unlikely that Ad8I evolved from
indigenous Ad8A, Ad8B, or Ad8E strains because Ad8B and
Ad8E share 96% PCRF with Ad8A, whereas Ad8I shares only
71% restriction fragments. Therefore Ad8I is genetically
distant from Ad8A, Ad8B, or Ad8E.
Ad8A,Ad8B,and Ad8E share 91.8% and 96.4% homology in
their amino acid and nucleotide sequences, respectively, with
the isolate 1127 (accession no,X74663).When compared with
Ad8A, Ad8B, Ad8E, and isolate 1127, Ad8I shared only 62.7%.
and 69.9% homology in amino acid and nucleotide sequences,
respectively.Ad8A,Ad8B,and Ad8E all had a unique 31 amino
acid deletion in HVR 1, whereas Ad8I had a 33 residue
deletion. Changes in the hypervariable regions of the Ad8I
strain provided it with its type specificity, as detected by the
neutralisation assay and haemoagglutination inhibition test.
Sequence variation in the hexon gene ofAd8Imay have played
an important role in the outbreak of EKC.17 18An association
genome type (Ad8I),reminiscent of the isolation of a new Ad7
genotype in the Netherlands from epidemic cases.19
Ad8 did not circulate as a single genome type in Hiroshima,
but displayed a series of genetic changes, although the
presence of Ad8E in Hiroshima over a 12 year period indicated
that this genome type was very stable. The isolation of a new
genome type is medically and epidemiologically important
because the appearance of new genome types can result in
more severe attacks of conjunctivitis.14Continued investiga-
tions into the genome types of adenoviruses will help to define
the unique evolutionary tendencies of these viruses.
Supported in part by grant in aid for Scientific Research (C) number
10470175 from the Ministry of Education,Science and Culture,Japan.
A K Adhikary, A Mukoyama, S Matsuno, T Inada, N Okabe,
Infectious Diseases Surveillance Centre, National Institute of Infectious
Diseases, Tokyo 162-8640, Japan
J Numaga, T Kaburaki, H Kawashima, M Araie, Department of
Ophthalmology, Graduate School of Medicine, The University of Tokyo,
Tokyo 114-0024, Japan
Y Ikeda, T Ogino, Hiroshima City Institute of Public Health, Hiroshima
E Suzuki, H Ushijima , Department of Developmental Medical Sciences,
Graduate School of Medicine, The University of Tokyo, Tokyo 113-0033,
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Distribution of Ad8 genome types in
Date CountryGenome type
Ad8A, Ad8B, Ad8E, Ad8I
Ad8C, Ad8D, Ad8E, Ad8F, Ad8G, Ad8H
Ad8A–Ad8I, genome types; Ad8P, prototype strain (Trim).
Take home messages
• Three known adenovirus type 8 (Ad8) genome types
(Ad8A, Ad8B, and Ad8E) and a novel genome type (Ad8I)
were detected in Hiroshima between 1983 and 1997
• Ad8A, Ad8B, and Ad8E were closely related, with 96%
homology, whereas Ad8I had only 71% homology
• Ad8A, Ad8B, and Ad8E were closely related to the isolate
1127 (accession no X74663), whereas Ad8I was more
• Ad8I was isolatedfrom
keratoconjunctivitis in 1995 and was also isolated from
sporadic cases until 1997
• The Ad8E strain that circulated from 1984 to 1995 was
stable among the study population
124 Adhikary, Numaga, Kaburaki, et al
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Genome typing of adenovirus type 8125
Arun Kumar Adhikary