Broad HIV-1 Specific CTL Responses Reveal Extensive HLA Class I
Binding Promiscuity of HIV-Derived, Optimally Defined CTL Epitopes
Nicole Frahm1 -
Philip J.R. Goulder1
,
2 -
Christian Brander1
Together with neutralizing antibodies and virus specific T-helper
cells, HIV specific cytotoxic T lymphocytes (CTL) remain at the center
of many vaccine development efforts despite the ongoing debate
regarding their in vivo induction and function and their
potential ability to provide effective protection from infection in
vaccines. However, numerous reports support the important role that
virus specific CTL responses may have in HIV infection and that their
detailed characterization needs to continue. As in past years, we
again have compiled an updated list of all optimal HIV derived CTL
epitopes that have been described over the last 12 months. The total
number of optimal CTL epitopes has now exceeded 200 and increasingly
also includes epitopes identified in non-clade B infection and in
individuals of non-Caucasian descent. Thus, the collective information
on the specificity of these HIV directed responses is of growing
relevance for vaccine development in populations most affected by the
HIV epidemic and should facilitate further immune analyses in these
mostly non-Caucasians ethnicities.
A number of laboratories, including ours, have in the past described
the results from comprehensive CTL screening studies, in which
overlapping peptide sets spanning the entire HIV genome are used in
IFN-γ
ELISpot assays (
Novitsky2002,
Draenert2004d,
Frahm2004,
Addo2003,
Kiepiela2004,
Cao2003a,
Feeney2003,
Sabbaj2003). While several
reports show either a positive or a negative correlation between viral
loads and the breadth or magnitude of these CTL responses, none of
these recent studies have found any strong significant associations.
Importantly, studies describing correlations have often been based on
the analysis of CTL responses against a restricted number of proteins
or even single epitopes using tetramer stainings and were often
restricted to a relatively low number of subjects enrolled
(
Ogg1998,
Edwards2002,
Buseyne2002a,
Buseyne2002b,
Betts2001). The larger,
more comprehensive studies including individuals at different stages
of disease fail to see associations between CTL activity and viral
loads (
Frahm2004,
Addo2003,
Draenert2004d,
Cao2003a,
Feeney2003). Thus, it
appears that either total CTL responses are not a correlate of immune
protection, or the assays most widely applied do not reflect the
number of CTL responses that actually do mediate effective
in
vivo control of viral replication. The latter may indeed play an
important role as some of the most widely used approaches clearly have
their limitations. Overcoming them may help to obtain a more accurate
picture of the HIV specific CTL activity. For instance, recent
studies from our laboratory show that the use of autologous test
sequences yields more and stronger CTL responses to variable proteins
compared to the use of consensus sequence based peptide sets
(
Altfeld2003). Thus, most studies may underestimate the true
breadth of responses and may hide a potential association between CTL
activity, viral loads and disease progression. This limitation could
be overcome by testing an extensive number of individuals using
autologous test sequences; an undertaking that, however, will be
limited by the exuberant costs for autologous sequence peptide
synthesis.
A further concern regards the use of overlapping peptide panels that
span the entire expressed HIV genome. In most cases, these utilize
peptides that are 15-18 amino acids in length and which overlap by
either 10 or 11 amino acids. Recent studies by Draenert
(Draenert2004b) indicate that the precise location of the optimal
epitope within the overlapping peptide (OLP) significantly affects
recognition of the OLP: if the epitope is located precisely at the
C-terminal end of the OLP, it will be significantly better recognized
than if located in the middle of the OLP. Recent studies in the SIV
macaque model, where peptides can be synthesized that correspond
exactly to the autologous virus sequence, indicate that even 15-mers
overlapping by 11 amino acids fail to pick up a substantial proportion
of the responses (Watkins et al., unpublished). The ultimate
and ideal situation would be to use a panel of 11-mers overlapping by
10 amino acids, based on autologous virus sequence. The cost of such
an enterprise is prohibitive, but for a limited number of subjects
this exercise should perhaps be undertaken, as one becomes
increasingly aware of the fact that the immunodominant CTL responses
may not necessarily be the ones that are critical for immune control.
In addition, only a few different assays are currently being employed
for the detection of virus specific CTL. To our knowledge, all
optimal CTL epitopes listed in the present database have been
identified either by assessing cytotoxic activity in a
Cr51 release assay or by the induction of
IFN-γ
in Elispot or intracellular cytokine staining (ICS)
assays. While cytolytic function may be an important aspect of
effective CTL, IFN-γ
release may well be a surrogate for other
functions but not occur in all HIV-specific cells. A number of
laboratories have tackled these problems and established other assays,
such as CD107 degranulation and perforin/granzyme release assays as
alternative ways to assess CTL responses. Also, replication
inhibition assays of the type first described by Yang et al.
(Yang1997), in which CTL clones are co-cultured with HLA-matched
CD4+ T cells infected with autologous virus clones, may provide a
means to come closer to the situation in vivo. Such assays
will help to address qualitative differences in the viral replication
inhibition efficacy of CTL of different specificity and will also help
to identify processing mutations that are hard to detect in other,
non-replication based assays. The frequency of processing escape
mutations is unknown but a recent number of descriptions of mutational
processing escape mutations in HIV suggests that this is a mechanism
of escape that has been much under-recognized (Yokomaku2004,Draenert2004c,Allen2004). Overall, these assays still need further
adaptation and simplification until comprehensive responses can be
measured on a single peptide level in a larger population of HIV
infected individuals.
Finally, assessing total CTL responses by comprehensive screening
may detect too many immunologically irrelevant responses and thus
obscure a possible association between CTL activity and viral
control. Indeed, there is compelling evidence that some single
epitope-specific responses can control viral replication as viral
escape in such epitopes is associated with increased viral loads and
acceleration of disease progression (
Draenert2004c,
Cao2003b,
Barouch2002,
Goulder1997c,
Friedrich2004,
Allen2000,
Kelleher2001,
Klenerman2002,
Leslie2004). Thus, besides single responses that appear to have
the capacity to provide strong immune surveillance, the current
assays may also detect many less efficient responses and thus hide a
possible association between CTL activity and viral load. On the
other hand, individuals with high viral loads and fast disease
progression can well maintain strong CTL responses without evidence
of affecting viral replication (
Draenert2004d). In this study,
the lack of control over viral replication could not be explained by
sequence variation in the targeted regions of the autologous virus,
indicating functional deficiencies specific to these individuals or
responses. New data from our lab and other investigators suggest
that the ability of HIV-epitope specific CTL to proliferate in
response to antigen is lost in the course of infection, and that
this defect could be associated with the loss of effective control
over viral replication (
Migueles2002) (and Lichterfeld
et
al., unpublished). Together, these studies suggest that at least
some HIV specific CTL can exert effective replication control and
that the often generalized description of ``functional deficiency of
HIV specific CTL'' is likely an over-simplification.
Regardless of possible associations between CTL activity and viral
loads, knowing the precise targets of these CTL is still a
prerequisite for many other questions to be asked, such as viral
evolution, genetic imprinting and their potential use in epitope-based
vaccines. Furthermore, the well-defined epitope landscape can be used
to address questions of antigen processing and epitope presentation.
In a recent study, we have used the optimally defined CTL epitopes to
address the degree of HLA class I binding promiscuity. Briefly, 100
HIV infected individuals of mainly non-Caucasian background were
tested for CTL responses against almost 200 described, optimal HIV
derived CTL epitopes, regardless of the individual's HLA type.
Interestingly, only about 40% of all responses were detected in
individuals who expressed the appropriate HLA class I allele. Another
20% of the responses were attributed to the presence of an allele
that fell into the same HLA-supertype as the originally described
restricting allele (for instance, an HLA-A3+ individual showing a
positive response against an HLA-A11 restricted epitope). This left
40% of all responses to be restricted by alleles that do not share
obvious similarities to the originally described allele or were, thus
far at least, not grouped into the same HLA-supertype as the original
allele. Although more detailed analyses will be required to confirm
the precise length and anchor residues for the epitopes presented on
alternative alleles, the data strongly suggest the presence of
epitopes with wide HLA-class I binding promiscuity. This is supported
by some of the epitopes included in the present update, for which
presentation and ex vivo recognition was documented for up to
four different HLA class I alleles (TL9 on B7, B42, B81 and Cw08).
Furthermore, strong support for extensive epitope binding promiscuity
is derived from the observation that CTL responses to certain regions
of the viral genome, such as Gag and Nef, show strong clustering of
responses (Frahm2004,Frahm2002a). In data now publicly available at
the Los Alamos database
(http://www.hiv.lanl.gov/content/immunology/hlatem/), we show
that 72 of 150 individuals tested reacted to the very same overlapping
18-mer peptide in Nef. Since these individuals expressed widely
diverse HLA types and the number of potential epitopes in a single
18-mer is limited, the data strongly suggest that at least some
epitopes must be presented by multiple HLA class I alleles.
Clearly, the identification of CTL epitopes that can bind multiple HLA
class I alleles will facilitate the selection of epitopes with an
increased population coverage. However, it will also be important to
assess potential functional differences between responses to the same
epitopes presented on different alleles. This may be of special
interest in cases where the epitopes are shared between HLA class I
alleles differentially associated with slow or fast HIV disease
progression. An example of this is the TL9 response restricted by
HLA-B42 and B81. HLA-B81 is associated with low viral loads in the
Durban population, whereas B42 is not (Goulder et al.,
unpublished). Sequencing of the virus indicates that escape mutations
are selected in the B81-positive subjects in the region of the virus
encoding the TL9 epitope, whereas this does not occur in the
B42-positive subjects (Leslie et al., unpublished). Other
examples include the epitope QW9, shared by HLA-B57 (slow) and HLA-B53
(fast disease progression). Using these epitopes, one may be able to
address the role that the HLA class I molecule or the presented CTL
epitope, respectively, play in determining the rate of disease
progression. Finally, cross-binding epitopes may also impact the
analyses of CTL escape patterns as allele-associated footprints may
need to take into consideration other alleles with the ability to
share CTL epitopes. Similarly, the assessment of a ``functional HLA
homozygosity'' in which alleles that frequently share CTL epitopes are
considered ``functionally homozygous'' may reveal additional insight
into the mechanism by which genetically homozygous individuals show a
faster disease progression compared to HLA heterozygous subjects
(Carrington1999).
As every year, we would like to express our gratitude to the large
number of researchers in the field who continuously contribute to this
database. The mostly unpublished data added to this years update
stemming from the AIDS Research Center at Mass. General Hospital have
been largely funded by an NIH contract (#NO1-A1-15442) supporting
HLA typing and HIV CTL epitope definition in non-Caucasian populations
and non clade B HIV infection.
We very much welcome any criticism, comments and additions to this
list since we are sure that some epitopes will unintentionally escape
our attention, despite close monitoring of the literature. Please
write or call us with any comments you may have at:
Table 1:
Best defined HIV CTL epitopes.
HLA |
Protein |
AA |
Sequence |
Reference |
A*0101 (A1) |
gp160 |
787-795 |
RRGWEVLKY |
Cao2002 |
|
|
|
|
|
A*02 (A2) |
RT |
127-135 |
YTAFTIPSV |
Draenert2004a |
|
|
|
|
|
A*0201 (A2) |
|
|
2 6 C |
Falk1991,Barouch1995 |
|
|
1°
anchor | L L |
|
|
|
|
M V |
|
|
|
2°
anchor | V |
|
A*0201 (A2) |
p17 |
77-85 |
SLYNTVATL |
Parker1994,Johnson1991,Parker1992 |
A*0201 (A2) |
p1 |
1-10 |
FLGKIWPSYK |
Yu2002b |
A*0201 (A2) |
RT |
33-41 |
ALVEICTEM |
Haas1998,Haas1999 |
A*0201 (A2) |
RT |
179-187 |
VIYQYMDDL |
Harrer1996a |
A*0201 (A2) |
RT |
309-317 |
ILKEPVHGV |
Tsomides1991,Walker1989 |
A*0201 (A2) |
Vpr |
59-67 |
AIIRILQQL |
Altfeld2001a,Altfeld2001b |
A*0201 (A2) |
gp160 |
311-320 |
RGPGRAFVTI |
Alexander-Miller1996 |
A*0201 (A2) |
gp160 |
813-822 |
SLLNATDIAV |
Dupuis1995 |
A*0201 (A2) |
Nef |
136-145 |
PLTFGWCYKL |
Maier1999,Haas1996 |
A*0201 (A2) |
Nef |
180-189 |
VLEWRFDSRL |
Maier1999,Haas1996 |
|
|
|
|
|
A*0202 (A2) |
|
|
2 C |
Barouch1995 |
|
|
|
L L |
|
|
|
|
V |
|
A*0202 (A2) |
p17 |
77-85 |
SLYNTVATL |
Goulder1999 |
|
|
|
|
|
A*0205 (A2) |
p17 |
77-85 |
SLYNTVATL |
Goulder1999 |
A*0205 (A2) |
gp41 |
335-343 |
RIRQGLERA |
Sabbaj2003 |
|
|
|
|
|
A*0207 (A2) |
p24 |
164-172 |
YVDRFYKTL |
Currier2002 |
A*0301 (A3) |
p17 |
18-26 |
KIRLRPGGK |
Harrer1996b |
A*0301 (A3) |
p17 |
20-28 |
RLRPGGKKK |
Culmann1999,Lewinsohn1999b,Goulder1997b,Wilkes1999b |
A*0301 (A3) |
p17 |
20-29 |
RLRPGGKKKY |
Goulder2000b |
A*0301 (A3) |
RT |
33-43 |
ALVEICTEMEK |
Haas1998,Haas1999 |
A*0301 (A3) |
RT |
73-82 |
KLVDFRELNK |
Yu2002a |
A*0301 (A3) |
RT |
93-101 |
GIPHPAGLK |
Yu2002a |
A*0301 (A3) |
RT |
158-166 |
AIFQSSMTK |
Threlkeld1997 |
A*0301 (A3) |
RT |
269-277 |
QIYPGIKVR |
Yu2002a |
A*0301 (A3) |
RT |
356-366 |
RMRGAHTNDVK |
Yu2002a |
A*0301 (A3) |
Integrase |
179-188 |
AVFIHNFKRK |
Yu2002a |
A*0301 (A3) |
Vif |
17-26 |
RIRTWKSLVK |
Altfeld2001a,Yu2002a |
A*0301 (A3) |
Vif |
28-36 |
HMYISKKAK |
Yu2002a |
A*0301 (A3) |
Vif |
158-168 |
KTKPPLPSVKK |
Yu2002a |
A*0301 (A3) |
Rev |
57-66 |
ERILSTYLGR |
Yu2002a,Addo2002a |
A*0301 (A3) |
gp160 |
37-46 |
TVYYGVPVWK |
Johnson1994a |
A*0301 (A3) |
gp160 |
770-780 |
RLRDLLLIVTR |
Takahashi1991 |
A*0301 (A3) |
Nef |
73-82 |
QVPLRPMTYK |
Culmann1991,Koenig1990 |
A*0301 (A3) |
Nef |
84-92 |
AVDLSHFLK |
Yu2002a |
|
|
|
|
|
A*1101 (A11) |
|
|
2 C |
Zhang1993,Rammensee1995 |
|
|
|
K |
|
|
|
|
V |
|
|
|
|
I |
|
|
|
|
F |
|
|
|
|
Y |
|
A*1101 (A11) |
p17 |
84-92 |
TLYCVHQRI |
Harrer1998 |
A*1101 (A11) |
p24 |
217-227 |
ACQGVGGPGHK |
Sipsas1997 |
A*1101 (A11) |
RT |
158-166 |
AIFQSSMTK |
Zhang1993,Threlkeld1997,Johnson1994b |
A*1101 (A11) |
RT |
341-350 |
IYQEPFKNLK |
Culmann1999 |
A*1101 (A11) |
RNase |
80-88 |
QIIEQLIKK |
Fukada1999 |
A*1101 (A11) |
Integrase |
179-188 |
AVFIHNFKRK |
Fukada1999 |
A*1101 (A11) |
gp160 |
199-207 |
SVITQACPK |
Fukada1999 |
A*1101 (A11) |
Nef |
73-82 |
QVPLRPMTYK |
Buseyne1999 |
A*1101 (A11) |
Nef |
75-82 |
PLRPMTYK |
Culmann1991 |
A*1101 (A11) |
Nef |
84-92 |
AVDLSHFLK |
Culmann1991 |
A*23 (A23) |
gp41 |
74-82 |
RYLKDQQLL |
Cao2003a |
|
|
|
|
|
A*2402 (A24) |
|
|
2 C |
Maier1994 |
|
|
|
Y I |
|
|
|
|
L |
|
|
|
|
F |
|
A*2402 (A24) |
p17 |
28-36 |
KYKLKHIVW |
Ikeda-Moore1998,Lewinsohn1999a |
A*2402 (A24) |
p24 |
162-172 |
RDYVDRFFKTL |
Dorrell1999,Rowland-Jones1999 |
A*2402 (A24) |
gp160 |
52-61 |
LFCASDAKAY |
Shankar1996,Lieberman1992 |
A*2402 (A24) |
gp160 |
585-593 |
RYLKDQQLL |
Dai1992 |
A*2402 (A24) |
Nef |
134-141 |
RYPLTFGW |
Ikeda-Moore1998,Goulder1997a |
|
|
|
|
|
A*2501 (A25) |
p24 |
13-23 |
QAISPRTLNAW |
Kurane1999 |
A*2501 (A25) |
p24 |
71-80 |
ETINEEAAEW |
vanBaalen1996,Klenerman1996 |
|
|
|
|
|
A*2601 (A26) |
|
|
12 6 C |
Dumrese1998 |
|
|
|
V Y |
|
|
|
|
T F |
|
|
|
|
I |
|
|
|
|
L |
|
|
|
|
F |
|
|
|
|
D I |
|
|
|
|
E L |
|
|
|
|
V |
|
A*2601 (A26) |
p24 |
35-43 |
EVIPMFSAL |
Goulder1996a |
A*2601 (A26) |
Pol |
604-612 |
ETKLGKAGY |
Sabbaj2003 |
|
|
|
|
|
A*29 (A29) |
Nef |
120-128 |
YFPDWQNYT |
Draenert2004b |
|
|
|
|
|
A*2902 (A29) |
gp160 |
209-217 |
SFEPIPIHY |
Altfeld2000a |
A*3002 (A30) |
|
|
12 C |
Rammensee1999 |
|
|
|
Y Y |
|
|
|
|
F |
|
|
|
|
L |
|
|
|
|
V |
|
|
|
|
R |
|
A*3002 (A30) |
p17 |
76-86 |
RSLYNTVATLY |
Goulder2001 |
A*3002 (A30) |
RT |
173-181 |
KQNPDIVIY |
Goulder2001 |
A*3002 (A30) |
RT |
263-271 |
KLNWASQIY |
Goulder2001 |
A*3002 (A30) |
RT |
356-365 |
RMRGAHTNDV |
Sabbaj2003 |
A*3002 (A30) |
Integrase |
219-227 |
KIQNFRVYY |
Rodriguez2004,Sabbaj2003 |
A*3002 (A30) |
gp160 |
704-712 |
IVNRNRQGY |
Goulder2001 |
A*3002 (A30) |
gp120 |
310-318 |
HIGPGRAFY |
Sabbaj2003 |
A*3002 (A30) |
gp41 |
283-291 |
KYCWNLLQY |
Goulder2001 |
A*3101 (A31) |
|
|
2 C |
Rammensee1999,Falk1994 |
|
|
|
R |
|
|
|
|
L |
|
|
|
|
V |
|
|
|
|
Y |
|
|
|
|
F |
|
A*3101 (A31) |
gp160 |
770-780 |
RLRDLLLIVTR |
Safrit1994a,Safrit1994b |
A*3201 (A32) |
RT |
392-401 |
PIQKETWETW |
Harrer1996b |
A*3201 (A32) |
gp160 |
419-427 |
RIKQIINMW |
Harrer1996b |
A*3303 (A33) |
gp41 |
187-196 |
VFAVLSIVNR |
Hossain2001 |
A*3303 (A33) |
gp41 |
320-327 |
EVAQRAYR |
Hossain2001 |
A*3303 (A33) |
Vpu |
29-37 |
EYRKILRQR |
Addo2002b |
A*3303 (A33) |
Nef |
133-141 |
TRYPLTFGW |
Cao2002 |
A*6801 (A68) |
Tat |
39-49 |
ITKGLGISYGR |
Oxenius2002 |
A*6801 (A68) |
Vpr |
52-62 |
DTWAGVEAIIR |
Sabbaj2004 |
A*6802 (A68) |
Protease |
3-11 |
ITLWQRPLV |
Rowland-Jones1999 |
A*6802 (A68) |
Protease |
30-38 |
DTVLEEWNL |
Rowland-Jones1999 |
A*6802 (A68) |
gp160 |
777-785 |
IVTRIVELL |
Wilkes1999a |
A*7401 (A19) |
Protease |
3-11 |
ITLWQRPLV |
Rowland-Jones1999 |
B*07 (B7) |
p24 |
84-92 |
HPVHAGPIA |
Yu2002a |
|
|
|
|
|
B*0702 (B7) |
|
|
123 C |
Rammensee1999,Englehard1993 |
|
|
|
P L |
|
|
|
|
A R F |
|
|
|
|
R K |
|
B*0702 (B7) |
p24 |
16-24 |
SPRTLNAWV |
Lewinsohn1999a |
B*0702 (B7) |
p24 |
48-56 |
TPQDLNTML |
Wilson1999a,Wilson1997,Jin2000,Wilkes1999c |
B*0702 (B7) |
p24 |
223-231 |
GPGHKARVL |
Goulder1999 |
B*0702 (B7) |
Vpr |
34-42 |
FPRIWLHGL |
Altfeld2001a |
B*0702 (B7) |
Vif |
48-57 |
HPRVSSEVHI |
Altfeld2001a |
B*0702 (B7) |
gp160 |
298-307 |
RPNNNTRKSI |
Safrit1994b |
B*0702 (B7) |
gp160 |
843-851 |
IPRRIRQGL |
Wilkes1999b |
B*0702 (B7) |
Nef |
68-77 |
FPVTPQVPLR |
Maier1999,Haas1996 |
B*0702 (B7) |
Nef |
68-76 |
FPVTPQVPL |
Bauer1997,Frahm2002b |
B*0702 (B7) |
Nef |
71-79 |
TPQVPLRPM |
Goulder1999 |
B*0702 (B7) |
Nef |
77-85 |
RPMTYKAAL |
Bauer1997 |
B*0702 (B7) |
Nef |
106-115 |
RQDILDLWIY |
Goulder1999 |
B*0702 (B7) |
Nef |
128-137 |
TPGPGVRYPL |
Haas1996,Culmann-Penciolelli1994 |
|
|
|
|
|
B*0801 (B8) |
|
|
23 5 C |
Sutton1993,Hill1992,DiBrino1994b |
|
|
|
K K L |
|
|
|
|
R |
|
|
|
|
PR |
|
|
|
|
L |
|
B*0801 (B8) |
p17 |
24-32 |
GGKKKYKLK |
Goulder1997d,Rowland-Jones1993 |
B*0801 (B8) |
p17 |
74-82 |
ELRSLYNTV |
Goulder1997d |
B*0801 (B8) |
p24 |
128-135 |
EIYKRWII |
Sutton1993,Goulder1997d |
B*0801 (B8) |
p24 |
197-205 |
DCKTILKAL |
Sutton1993 |
B*0801 (B8) |
RT |
18-26 |
GPKVKQWPL |
Sutton1993,Walker1989 |
B*0801 (B8) |
gp160 |
2-10 |
RVKEKYQHL |
Sipsas1997 |
B*0801 (B8) |
gp160 |
586-593 |
YLKDQQLL |
Shankar1996,Johnson1992 |
B*0801 (B8) |
Nef |
13-20 |
WPTVRERM |
Goulder1997d |
B*0801 (B8) |
Nef |
90-97 |
FLKEKGGL |
Price1997,Culmann-Penciolelli1994 |
B*14 (B14) |
p15 |
42-50 |
CRAPRKKGC |
Yu2002b |
B*1402 (B14) |
|
|
23 5 C |
DiBrino1994a |
|
|
|
R R L |
|
|
|
|
K H |
|
|
|
|
L |
|
|
|
|
Y |
|
|
|
|
F |
|
B*1402 (B14) |
p24 |
166-174 |
DRFYKTLRA |
Harrer1996b |
B*1402 (B14) |
gp160 |
584-592 |
ERYLKDQQL |
Johnson1992 |
|
|
|
|
|
B*1501 (B62) |
|
|
2 C |
|
|
|
|
Q Y |
Barber1997 |
|
|
|
L F |
Barber1997 |
|
|
|
M |
Barber1997 |
B*1501 (B62) |
p24 |
137-145 |
GLNKIVRMY |
Johnson1991,Goulder1999 |
B*1501 (B62) |
RT |
260-271 |
LVGKLNWASQIY |
Johnson1999 |
B*1501 (B62) |
RT |
309-318 |
ILKEPVHGVY |
Johnson1991,Johnson1999 |
B*1501 (B62) |
Nef |
19-27 |
RMRRAEPAA |
Cao2002 |
B*1501 (B62) |
Nef |
117-127 |
TQGYFPDWQNY |
Culmann1999 |
|
|
|
|
|
B*1503 (B72) |
Integrase |
185-194 |
FKRKGGIGGY |
Honeyborne2003 |
B*1503 (B72) |
Integrase |
263-271 |
RKAKIIRDY |
Cao2003a |
B*1503 (B72) |
Tat |
38-47 |
FQTKGLGISY |
Novitsky2001 |
B*1503 (B72) |
Pol |
651-660 |
VTDSQYALGI |
Sabbaj2003 |
B*1503 (B72) |
Nef |
183-191 |
WRFDSRLAF |
Cao2002 |
|
|
|
|
|
B*1510 (B71) |
Gag p24 |
61-69 |
GHQAAMQML |
Day2003 |
B*1510 (B71) |
Vif |
79-87 |
WHLGHVSI |
Honeyborne2003 |
|
|
|
|
|
B*1516 (B63) |
|
|
2 9 |
Barber1997,Seeger1998 |
|
|
|
T Y |
|
|
|
|
S I |
|
|
|
|
V |
|
|
|
|
F |
|
B*1516 (B63) |
gp160 |
375-383 |
SFNCGGEFF |
Wilson1999a,Wilson1997 |
B*1801 (B18) |
p24 |
161-170 |
FRDYVDRFYK |
Ogg1998 |
B*1801 (B18) |
Vif |
102-111 |
LADQLIHLHY |
Altfeld2001a |
B*1801 (B18) |
Nef |
135-143 |
YPLTFGWCY |
Culmann1991,Culmann-Penciolelli1994 |
B*27 (B27) |
Vpr |
31-39 |
VRHFPRIWL |
Addo2004 |
B*2703 (B27) |
p24 |
131-140 |
RRWIQLGLQK |
Rowland-Jones1999,Rowland-Jones1998 |
B*2705 (B27) |
|
|
12 C |
Jardetzky1991,Rammensee1995 |
|
|
|
R L |
|
|
|
|
F |
|
|
|
|
K K |
|
|
|
|
R R |
|
|
|
|
G I |
|
|
|
|
A |
|
B*2705 (B27) |
p17 |
19-27 |
IRLRPGGKK |
McKinney1999,Lewinsohn1999a |
B*2705 (B27) |
p24 |
131-140 |
KRWIILGLNK |
Buseyne1993,Nixon1988,Goulder1997c |
B*2705 (B27) |
gp160 |
786-795 |
GRRGWEALKY |
Lieberman1999,Lieberman1992 |
B*2705 (B27) |
Nef |
105-114 |
RRQDILDLWI |
Goulder1997b |
B*3501 (B35) |
|
|
2 C |
Rammensee1999,Hill1992 |
|
|
|
P Y |
|
|
|
|
A F |
|
|
|
|
V M |
|
|
|
|
S L |
|
|
|
|
I |
|
B*3501 (B35) |
p17 |
36-44 |
WASRELERF |
Goulder1997a |
B*3501 (B35) |
p17 |
124-132 |
NSSKVSQNY |
Rowland-Jones1995 |
B*3501 (B35) |
p24 |
122-130 |
PPIPVGDIY |
Rowland-Jones1995 |
B*3501 (B35) |
p24 |
122-130 |
NPVPVGNIY |
Rowland-Jones1995 |
B*3501 (B35) |
RT |
107-115 |
TVLDVGDAY |
Wilson1999b,Wilkes1999b |
B*3501 (B35) |
RT |
118-127 |
VPLDEDFRKY |
Shiga1996,Sipsas1997 |
B*3501 (B35) |
RT |
175-183 |
NPDIVIYQY |
Shiga1996,Sipsas1997 |
B*3501 (B35) |
RT |
175-183 |
HPDIVIYQY |
Rowland-Jones1995 |
B*3501 (B35) |
gp160 |
42-52 |
VPVWKEATTTL |
Wilkes1999b |
B*3501 (B35) |
gp160 |
78-86 |
DPNPQEVVL |
Shiga1996 |
B*3501 (B35) |
gp160 |
606-614 |
TAVPWNASW |
Johnson1994a |
B*3501 (B35) |
Nef |
74-81 |
VPLRPMTY |
Culmann1991,Culmann-Penciolelli1994 |
B*3701 (B37) |
|
|
2 C |
Falk1993 |
|
|
|
D F |
|
|
|
|
E M |
|
|
|
|
L |
|
|
|
|
I |
|
B*3701 (B37) |
Nef |
120-128 |
YFPDWQNYT |
Culmann1999,Culmann1991 |
B*3801 (B38) |
Vif |
79-87 |
WHLGQGVSI |
Sabbaj2004 |
B*3801 (B38) |
gp160 |
104-112 |
MHEDIISLW |
Cao2002 |
|
|
|
|
|
B*3901 (B39) |
|
|
2 C |
Falk1995a |
|
|
|
R L |
|
|
|
|
H |
|
B*3901 (B39) |
p24 |
61-69 |
GHQAAMQML |
Kurane1999 |
|
|
|
|
|
B*4001 (B60) |
|
|
2 C |
Falk1995b |
|
|
|
E L |
|
B*4001 (B60) |
p17 |
92-101 |
IEIKDTKEAL |
Altfeld2000b |
B*4001 (B60) |
p24 |
44-52 |
SEGATPQDL |
Altfeld2000b |
B*4001 (B60) |
p6 |
33-41 |
KELYPLTSL |
Yu2002b |
B*4001 (B60) |
RT |
5-12 |
IETVPVKL |
Draenert2004a |
B*4001 (B60) |
RT |
202-210 |
IEELRQHLL |
Altfeld2000b |
B*4001 (B60) |
gp160 |
805-814 |
QELKNSAVSL |
Altfeld2000b |
B*4001 (B60) |
Nef |
37-45 |
LEKHGAITS |
Draenert2004a |
B*4001 (B60) |
Nef |
92-100 |
KEKGGLEGL |
Altfeld2000b |
|
|
|
|
|
B*4002 (B61) |
p17 |
11-19 |
GELDRWEKI |
Sabbaj2003 |
B*4002 (B61) |
p24 |
70-78 |
KETINEEAA |
Sabbaj2003 |
B*4002 (B61) |
p24 |
78-86 |
AEWDRVHPV |
Sabbaj2003 |
B*4002 (B61) |
p15 |
64-71 |
TERQANFL |
Sabbaj2003 |
B*4002 (B61) |
Nef |
92-100 |
KEKGGLEGL |
Altfeld2000b,Sabbaj2003 |
|
|
|
|
|
B*42 (B42) |
Integrase |
260-268 |
VPRRKAKII |
Kiepiela2002 |
|
|
|
|
|
B*4201 (B42) |
p24 |
48-56 |
TPQDLNTML |
Goulder2000a |
B*4201 (B42) |
RT |
271-279 |
YPGIKVRQL |
Wilkes1999b |
B*4201 (B42) |
Nef |
128-137 |
TPGPGVRYPL |
Goulder1999 |
B*44 (B44) |
Protease |
34-42 |
EEMNLPGRW |
Rodriguez2004 |
|
|
|
|
|
B*4402 (B44) |
|
|
2 C |
Rammensee1999 |
|
|
|
E F |
|
|
|
|
Y |
|
B*4402 (B44) |
p24 |
162-172 |
RDYVDRFYKTL |
Ogg1998 |
B*4402 (B44) |
p24 |
174-184 |
AEQASQDVKNW |
Lewinsohn1999a |
B*4402 (B44) |
gp160 |
31-40 |
AENLWVTVYY |
Borrow1997 |
|
|
|
|
|
B*4415 (B12) |
p24 |
28-36 |
EEKAFSPEV |
Bird2002 |
|
|
|
|
|
B*4501 (B45) |
Gag-p2 |
1-10 |
AEAMSQVTNS |
Sabbaj2004 |
|
|
|
|
|
B*50 (B50) |
Nef |
37-45 |
LEKHGAITS |
Draenert2004a |
|
|
|
|
|
B*51 (B51) |
Vif |
57-66 |
IPLGDAKLII |
Bansal2004 |
B*51 (B51) |
Vpr |
29-37 |
EAVRHFPRI |
Cao2003a |
|
|
|
|
|
B*5101 (B51) |
|
|
2 C |
Falk1995a |
|
|
|
A F |
|
|
|
|
P I |
|
|
|
|
G |
|
B*5101 (B51) |
RT |
42-50 |
EKEGKISKI |
Haas1998,Haas1999 |
B*5101 (B51) |
RT |
128-135 |
TAFTIPSI |
Sipsas1997 |
B*5101 (B51) |
gp160 |
416-424 |
LPCRIKQII |
Tomiyama1999 |
|
|
|
|
|
B*5201 (B52) |
|
|
2 C |
Rammensee1999 |
|
|
|
I |
|
|
|
|
V |
|
|
|
|
Q |
|
B*5201 (B52) |
p24 |
143-150 |
RMYSPTSI |
Wilson1997,Wilkes1999b |
|
|
|
|
|
B*53 (B53) |
Nef |
135-143 |
YPLTFGWCF |
Kiepiela2002 |
B*5301 (B53) |
|
|
2 C |
|
|
|
|
P L |
Hill1992 |
B*5301 (B53) |
p24 |
48-56 |
TPYDINQML |
Gotch1993 |
B*5301 (B53) |
p24 |
176-184 |
QASQEVKNW |
Buseyne1999,Buseyne1996,Buseyne1997 |
B*5301 (B53) |
Tat |
2-11 |
EPVDPRLEPW |
Addo2001 |
B*5301 (B53) |
Nef |
135-143 |
YPLTFGWCY |
Sabbaj2003 |
|
|
|
|
|
B*5501 (B55) |
|
|
2 C |
Barber1995 |
|
|
|
P |
|
|
|
|
A |
|
B*5501 (B55) |
gp160 |
42-51 |
VPVWKEATTT |
Shankar1996,Lieberman1999 |
|
|
|
|
|
B*57 (B57) |
Integrase |
123-132 |
STTVKAACWW |
Rodriguez2004,Addo2004 |
B*57 (B57) |
Nef |
116-124 |
HTQGYFPDW |
Draenert2002 |
|
|
|
|
|
B*5701 (B57) |
|
|
12 C |
Barber1997 |
|
|
|
A F |
|
|
|
|
T W |
|
|
|
|
S |
|
|
|
|
K Y |
|
B*5701 (B57) |
p24 |
15-23 |
ISPRTLNAW |
Johnson1991,Goulder1996b |
B*5701 (B57) |
p24 |
30-40 |
KAFSPEVIPMF |
Goulder1996b |
B*5701 (B57) |
p24 |
108-118 |
TSTLQEQIGWF |
Goulder1996b |
B*5701 (B57) |
p24 |
176-184 |
QASQEVKNW |
Goulder1996b |
B*5701 (B57) |
RT |
244-252 |
IVLPEKDSW |
vanderBurg1997,Hay1999 |
B*5701 (B57) |
Integrase |
173-181 |
KTAVQMAVF |
Goulder1996b,Hay1999 |
B*5701 (B57) |
Vpr |
30-38 |
AVRHFPRIW |
Altfeld2001a |
B*5701 (B57) |
Vif |
31-39 |
ISKKAKGWF |
Altfeld2001a |
B*5701 (B57) |
Rev |
14-23 |
KAVRLIKFLY |
Addo2001 |
B*5701 (B57) |
Nef |
116-125 |
HTQGYFPDWQ |
Culmann1991 |
B*5701 (B57) |
Nef |
120-128 |
YFPDWQNYT |
Culmann1991 |
|
|
|
|
|
B57 (B57) |
Nef |
116-124 |
HTQGYFPDW |
Draenert2002 |
|
|
|
|
|
B*5703 (B57) |
p24 |
30-37 |
KAFSPEVI |
Goulder2000b |
B*5703 (B57) |
p24 |
30-40 |
KAFSPEVIPMF |
Goulder2000b |
B*5801 (B58) |
|
|
12 C |
Falk1995b,Barber1997 |
|
|
|
A F |
|
|
|
|
T W |
|
|
|
|
S |
|
|
|
|
K |
|
|
|
|
V |
|
|
|
|
I |
|
B*5801 (B58) |
p24 |
108-117 |
TSTVEEQQIW |
Bertoletti1998 |
B*5801 (B58) |
p24 |
108-117 |
TSTLQEQIGW |
Goulder1996b |
B*5801 (B58) |
RT |
375-383 |
IAMESIVIW |
Kiepiela2002 |
B*5801 (B58) |
Rev |
14-23 |
KAVRLIKFLY |
Addo2001 |
B*81 (B81) |
Pol |
715-723 |
LFLDGIDKA |
Addo2002a |
B*8101 (B81) |
p24 |
48-56 |
TPQDLNTML |
Goulder2000a |
B*8101 (B81) |
Vpr |
34-42 |
FPRIWLHGL |
Altfeld2001a |
Cw*0102 (Cw1) |
|
|
23 C |
Barber1997 |
|
|
|
A L |
|
|
|
|
L |
|
|
|
|
P |
|
Cw*0102 (Cw1) |
p24 |
36-43 |
VIPMFSAL |
Goulder1997a |
Cw*03 (Cw03) |
Nef |
83-91 |
AALDLSHFL |
Draenert2004a |
Cw*0303 (Cw9) |
Gag p24 |
164-172 |
YVDRFFKTL |
Honeyborne2003 |
Cw*0304 (Cw10) |
Gag p24 |
164-172 |
YVDRFFKTL |
Honeyborne2003 |
Cw*0304 (Cw10) |
gp41 |
46-54 |
RAIEAQQHL |
Trocha2002,Currier2002 |
Cw*0401 (Cw4) |
|
|
2 6 C |
Falk1994 |
|
|
|
Y L |
|
|
|
|
P F |
|
|
|
|
F M |
|
|
|
|
V |
|
|
|
|
I |
|
|
|
|
L |
|
Cw*0401 (Cw4) |
gp160 |
375-383 |
SFNCGGEFF |
Johnson1993,Wilson1997 |
Cw*05 (Cw05) |
Gag p24 |
174-185 |
AEQASQEVKNWM |
Draenert2004a |
|
|
|
|
|
Cw*07 (Cw7) |
Nef |
105-115 |
KRQEILDLWVY |
Kiepiela2002 |
Cw*07 (Cw7) |
Nef |
105-115 |
RRQDILDLWIY |
Yu2002a |
|
|
|
|
|
Cw*0802 (Cw8) |
p24 |
48-56 |
TPQDLNTML |
Goulder2000a |
Cw*0802 (Cw8) |
Nef |
83-91 |
AAVDLSHFL |
Cao2003a |
|
|
|
|
|
Cw*12 (Cw12) |
Tat |
30-37 |
CCFHCQVC |
Nixon1999,Cao2003a |
|
|
|
|
|
Cw*15 (Cw15) |
gp41 |
46-54 |
RAIEAQQHL |
Trocha2002 |
- Addo2001
-
M. M. Addo, M. Altfeld, E. S. Rosenberg, R. L. Eldridge, M. N. Philips,
K. Habeeb, A. Khatri, C. Brander, G. K. Robbins, G. P. Mazzara, P. J.
Goulder, & B. D. Walker.
The HIV-1 regulatory proteins Tat and Rev are frequently
targeted by cytotoxic T lymphocytes derived from HIV-1-infected
individuals.
Proc Natl Acad Sci U S A 98(4):1781-1786, 2001.
- Addo2002a
-
M. Addo.
Personal communication, 2002.
- Addo2002b
-
M. M. Addo, M. Altfeld, A. Rathod, M. Yu, X. G. Yu, P. J. R. Goulder, E. S.
Rosenberg, & B. D. Walker.
HIV-1 Vpu represents a minor target for cytotoxic T lymphocytes
in HIV-1-infection.
AIDS 16(7):1071-1073, 2002.
- Addo2003
-
M. M. Addo, X. G. Yu, A. Rathod, D. Cohen, R. L. Eldridge, D. Strick, M. N.
Johnston, C. Corcoran, A. G. Wurcel, C. A. Fitzpatrick, M. E. Feeney, W. R.
Rodriguez, N. Basgoz, R. Draenert, D. R. Stone, C. Brander, P. J. R. Goulder,
E. S. Rosenberg, M. Altfeld, & B. D. Walker.
Comprehensive epitope analysis of human immunodeficiency virus type 1
(HIV-1)-specific T-cell responses directed against the entire expressed
HIV-1 genome demonstrate broadly directed responses, but no correlation to
viral load.
J Virol 77(3):2081-2092, 2003.
- Addo2004
-
M. M. Addo & A. Rathod.
Personal communication, 2004.
- Alexander-Miller1996
-
M. A. Alexander-Miller, K. C. Parker, T. Tsukui, C. D. Pendleton, J. E.
Coligan, & J. A. Berzofsky.
Molecular analysis of presentation by HLA-A2.1 of a promiscuously
binding V3 loop peptide from the HIV-1 Envelope protein to human
cytotoxic T lymphocytes.
Int Immunol 8(5):641-649, 1996.
- Allen2000
-
T. M. Allen, D. H. O'Connor, P. Jing, J. L. Dzuris, B. R. Mothe, T. U. Vogel,
E. Dunphy, M. E. Liebl, C. Emerson, N. Wilson, K. J. Kunstman, X. Wang, D. B.
Allison, A. L. Hughes, R. C. Desrosiers, J. D. Altman, S. M. Wolinsky,
A. Sette, & D. I. Watkins.
Tat-specific cytotoxic T lymphocytes select for SIV escape
variants during resolution of primary viraemia.
Nature 407(6802):386-390, 2000.
- Allen2004
-
T. M. Allen et al.
Selection, transmission and reversion of an antigen processing CTL
escape mutation in HIV-1 infection.
J of Virol in press, 2004.
- Altfeld2000a
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M. A. Altfeld.
Personal communication, 2000.
- Altfeld2000b
-
M. A. Altfeld, A. Trocha, R. L. Eldridge, E. S. Rosenberg, M. N. Phillips,
M. M. Addo, R. P. Sekaly, S. A. Kalams, S. A. Burchett, K. McIntosh, B. D.
Walker, & P. J. Goulder.
Identification of dominant optimal HLA-B60- and
HLA-B61-restricted cytotoxic T-lymphocyte (CTL) epitopes: Rapid
characterization of CTL responses by enzyme-linked immunospot assay.
J Virol 74(18):8541-8549, 2000.
- Altfeld2001a
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M. Altfeld, M. M. Addo, R. L. Eldridge, X. G. Yu, S. Thomas, A. Khatri,
D. Strick, M. N. Phillips, G. B. Cohen, S. A. Islam, S. A. Kalams,
C. Brander, P. J. Goulder, E. S. Rosenberg, & B. D. Walker.
Vpr is preferentially targeted by CTL during HIV-1 infection.
J Immunol 167(5):2743-2752, 2001.
- Altfeld2001b
-
M. A. Altfeld, B. Livingston, N. Reshamwala, P. T. Nguyen, M. M. Addo, A. Shea,
M. Newman, J. Fikes, J. Sidney, P. Wentworth, R. Chesnut, R. L. Eldridge,
E. S. Rosenberg, G. K. Robbins, C. Brander, P. E. Sax, S. Boswell, T. Flynn,
S. Buchbinder, P. J. Goulder, B. D. Walker, A. Sette, & S. A. Kalams.
Identification of novel HLA-A2-restricted human immunodeficiency
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HLA-A2 supertype peptide-binding motif.
J Virol 75(3):1301-1311, 2001.
- Altfeld2003
-
M. Altfeld, M. M. Addo, R. Shankarappa, P. K. Lee, T. M. Allen, X. G. Yu,
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Mullins, E. S. Rosenberg, C. Brander, B. Korber, & B. D. Walker.
Enhanced detection of human immunodeficiency virus type 1-specific
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autologous virus sequences.
J Virol 77(13):7330-7340, 2003.
- Bansal2004
-
A. Bansal, P. Goepfert, et al.
Personal communication, 2004.
- Barber1995
-
L. D. Barber, B. Gillece-Castro, L. Percival, X. Li, C. Clayberger, &
P. Parham.
Overlap in the repertoires of peptides bound in vivo by a group of
related class I HLA-B allotypes.
Curr Biol 5:179-190, 1995.
- Barber1997
-
L. D. Barber, L. Percival, K. L. Arnett, J. E. Gumperz, L. Chen, & P. Parham.
Polymorphism in the α1
helix of the HLA-B heavy chain can
have an overriding influence on peptide-binding specificity.
J Immunol 158:1660-1669, 1997.
- Barouch1995
-
D. Barouch, T. Friede, S. Stevanovic, L. Tussey, K. Smith, S. Rowland-Jones,
V. Braud, A. McMichael, & H. G. Rammensee.
HLA-A2 subtypes are functionally distinct in peptide binding and
presentation.
J Exp Med 182:1847-1856, 1995.
- Barouch2002
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2005-02-27