Abstract
The human Melan-A/MART-1 gene encodes an HLA-A2-restricted peptide epitope recognized by melanoma-reactive CD8(+) cytotoxic T lymphocytes. Here we report that this gene also encodes at least one HLA-DR4-presented peptide recognized by CD4(+) T cells. The Melan-A/MART-1(51-73) peptide was able to induce the in vitro expansion of specific CD4(+) T cells derived from normal DR4(+) donors or from DR4(+) patients with melanoma when pulsed onto autologous dendritic cells. CD4(+) responder T cells specifically produced IFN-gamma in response to, and also lysed, T2.DR4 cells pulsed with the Melan-A/MART-1(51-73) peptide and DR4(+) melanoma target cells naturally expressing the Melan-A/MART-1 gene product. Interestingly, CD4(+) T cell immunoreactivity against the Melan-A/MART-1(51-73) peptide typically coexisted with a high frequency of anti-Melan-A/MART-1(27-35) reactive CD8(+) T cells in freshly isolated blood harvested from HLA-A2(+)/DR4(+) patients with melanoma. Taken together, these data support the use of this Melan-A/MART-1 DR4-restricted melanoma epitope in future immunotherapeutic trials designed to generate, augment, and quantitate specific CD4(+) T cell responses against melanoma in vivo.
MeSH Terms
Amino Acid Sequence
Antigens, Neoplasm/immunology
CD4-Positive T-Lymphocytes/immunology
Cancer Vaccines/immunology,therapeutic use
Epitopes
HLA-DR4 Antigen/immunology
Humans
Interferon-gamma/analysis
MART-1 Antigen
Melanoma/immunology
Molecular Sequence Data
Neoplasm Proteins/immunology
Peptide Fragments/chemical synthesis,immunology,therapeutic use
Tumor Cells, Cultured
Chemicals
Antigens, Neoplasm
Cancer Vaccines
Epitopes
HLA-DR4 Antigen
MART-1 Antigen
MLANA protein, human
Neoplasm Proteins
Peptide Fragments
Interferon-gamma
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Zarour H M
Department of Medicine, University of Pittsburgh Cancer Institute, Pittsburgh, PA 15213, USA. zarourhm@msx.upmc.edu
Kirkwood J M
Kierstead L S
Herr W
Brusic V
Slingluff C L
Sidney J
Sette A
Storkus W J
References (27)
27 references, click to expand
-
A new gene coding for a differentiation antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas.
J Exp Med. 1994 Jul 1;180(1):35-42
PMID: 8006593
-
Cloning genes encoding MHC class II-restricted antigens: mutated CDC27 as a tumor antigen.
Science. 1999 May 21;284(5418):1351-4
PMID: 10334988
-
CD4 T cells kill melanoma cells by mechanisms that are independent of Fas (CD95).
Int J Cancer. 1998 Jan 30;75(3):384-90
PMID: 9455798
-
CD4 T cells and their role in antitumor immune responses.
J Exp Med. 1999 Mar 1;189(5):753-6
PMID: 10049938
-
Melanoma cells present a MAGE-3 epitope to CD4(+) cytotoxic T cells in association with histocompatibility leukocyte antigen DR11.
J Exp Med. 1999 Mar 1;189(5):871-6
PMID: 10049951
-
Production of stable cytolytic T-cell clones directed against autologous human melanoma.
Int J Cancer. 1987 Mar 15;39(3):390-6
PMID: 3493226
-
The use of computer-assisted video image analysis for the quantification of CD8+ T lymphocytes producing tumor necrosis factor alpha spots in response to peptide antigens.
J Immunol Methods. 1997 Apr 25;203(2):141-52
PMID: 9149807
-
HLA DR4w4-binding motifs illustrate the biochemical basis of degeneracy and specificity in peptide-DR interactions.
J Immunol. 1993 Sep 15;151(6):3163-70
PMID: 7690794
-
Peptide binding specificity of HLA-DR4 molecules: correlation with rheumatoid arthritis association.
J Exp Med. 1995 May 1;181(5):1847-55
PMID: 7722459
-
Identification of naturally processed and HLA-presented Epstein-Barr virus peptides recognized by CD4(+) or CD8(+) T lymphocytes from human blood.
Proc Natl Acad Sci U S A. 1999 Oct 12;96(21):12033-8
PMID: 10518571
-
Identification of MAGE-3 epitopes presented by HLA-DR molecules to CD4(+) T lymphocytes.
J Exp Med. 1999 Mar 1;189(5):767-78
PMID: 10049940
-
Isolation of novel HLA-DR restricted potential tumor-associated antigens from the melanoma cell line FM3.
Cancer Res. 1997 Aug 1;57(15):3238-44
PMID: 9242455
-
Neural network-based prediction of candidate T-cell epitopes.
Nat Biotechnol. 1998 Oct;16(10):966-9
PMID: 9788355
-
Biochemical identification of a mutated human melanoma antigen recognized by CD4(+) T cells.
J Exp Med. 1999 Mar 1;189(5):757-66
PMID: 10049939
-
Binding specificity of a class II-restricted hepatitis B epitope by DR molecules from responder and nonresponder vaccine recipients.
Hum Immunol. 1998 Dec;59(12):783-93
PMID: 9831134
-
Melanoma-specific CD4+ T cells recognize nonmutated HLA-DR-restricted tyrosinase epitopes.
J Exp Med. 1996 May 1;183(5):1965-71
PMID: 8642306
-
Human CD4+ T cells specifically recognize a shared melanoma-associated antigen encoded by the tyrosinase gene.
Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9461-5
PMID: 7937789
-
Isolation of tyrosinase-specific CD8+ and CD4+ T cell clones from the peripheral blood of melanoma patients following in vitro stimulation with recombinant vaccinia virus.
J Immunol. 1996 Nov 1;157(9):4079-86
PMID: 8892642
-
Natural ligand motifs of closely related HLA-DR4 molecules predict features of rheumatoid arthritis associated peptides.
Biochim Biophys Acta. 1996 Jun 7;1316(2):85-101
PMID: 8672555
-
Several common HLA-DR types share largely overlapping peptide binding repertoires.
J Immunol. 1998 Apr 1;160(7):3363-73
PMID: 9531296
-
The role of CD4+ T cell responses in antitumor immunity.
Curr Opin Immunol. 1998 Oct;10(5):588-94
PMID: 9794842
-
Identification of the immunodominant peptides of the MART-1 human melanoma antigen recognized by the majority of HLA-A2-restricted tumor infiltrating lymphocytes.
J Exp Med. 1994 Jul 1;180(1):347-52
PMID: 7516411
-
Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions.
Eur J Immunol. 1997 Dec;27(12):3135-42
PMID: 9464798
-
Prediction of MHC class II-binding peptides using an evolutionary algorithm and artificial neural network.
Bioinformatics. 1998;14(2):121-30
PMID: 9545443
-
Reactivity of autologous CD4+ T lymphocytes against human melanoma. Evidence for a shared melanoma antigen presented by HLA-DR15.
J Immunol. 1995 Jan 15;154(2):772-9
PMID: 7814883
-
Generation of tumor-specific CTLs from melanoma patients by using peripheral blood stimulated with allogeneic melanoma tumor cell lines. Fine specificity and MART-1 melanoma antigen recognition.
J Immunol. 1995 Jan 15;154(2):762-71
PMID: 7814882
-
Identification of a novel major histocompatibility complex class II-restricted tumor antigen resulting from a chromosomal rearrangement recognized by CD4(+) T cells.
J Exp Med. 1999 May 17;189(10):1659-68
PMID: 10330445