Abstract
Current strategies for the immunotherapy of melanoma include augmentation of the immune response to tumor antigens represented by melanosomal proteins such as tyrosinase, gp100, and MART-1. The possibility that intentional targeting of tumor antigens representing normal proteins can result in autoimmune toxicity has been postulated but never demonstrated previously in humans. In this study, we describe a patient with metastatic melanoma who developed inflammatory lesions circumscribing pigmented areas of skin after an infusion of MART-1-specific CD8(+) T cell clones. Analysis of the infiltrating lymphocytes in skin and tumor biopsies using T cell-specific peptide-major histocompatibility complex tetramers demonstrated a localized predominance of MART-1-specific CD8(+) T cells (>28% of all CD8 T cells) that was identical to the infused clones (as confirmed by sequencing of the complementarity-determining region 3). In contrast to skin biopsies obtained from the patient before T cell infusion, postinfusion biopsies demonstrated loss of MART-1 expression, evidence of melanocyte damage, and the complete absence of melanocytes in affected regions of the skin. This study provides, for the first time, direct evidence in humans that antigen-specific immunotherapy can target not only antigen-positive tumor cells in vivo but also normal tissues expressing the shared tumor antigen.
MeSH Terms
Antigens, Neoplasm/biosynthesis,immunology
Female
Humans
Immunotherapy, Adoptive/adverse effects,methods
MART-1 Antigen
Melanocytes/cytology,immunology
Melanoma/complications,immunology,pathology,therapy
Middle Aged
Neoplasm Proteins/biosynthesis,immunology
Skin/cytology,immunology,pathology
Skin Neoplasms/complications,immunology,pathology,therapy
T-Lymphocytes, Cytotoxic/classification,immunology
Vitiligo/etiology,immunology,pathology
Chemicals
Antigens, Neoplasm
MART-1 Antigen
MLANA protein, human
Neoplasm Proteins
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Yee C
Clinical Research Division, Fred Hutchinson Cancer Research Center, Seattle, WA 98109, USA.
Thompson J A
Roche P
Byrd D R
Lee P P
Piepkorn M
Kenyon K
Davis M M
Riddell S R
Greenberg P D
References (23)
23 references, click to expand
-
Prognostic significance of hypopigmentation in malignant melanoma.
Arch Dermatol. 1987 Aug;123(8):1053-5
PMID: 3631983
-
Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients.
Nat Med. 1999 Jun;5(6):677-85
PMID: 10371507
-
Dominant positive and negative selection using a hygromycin phosphotransferase-thymidine kinase fusion gene.
Mol Cell Biol. 1991 Jun;11(6):3374-8
PMID: 1645450
-
Phase I study of cellular adoptive immunotherapy using genetically modified CD8+ HIV-specific T cells for HIV seropositive patients undergoing allogeneic bone marrow transplant. The Fred Hutchinson Cancer Research Center and the University of Washington School of Medicine, Department of Medicine, Division of Oncology.
Hum Gene Ther. 1992 Jun;3(3):319-38
PMID: 1643151
-
Eye-derived cytokines and the immunosuppressive intraocular microenvironment: a review.
Curr Eye Res. 1992;11 Suppl:41-7
PMID: 1424750
-
Cloning of the gene coding for a shared human melanoma antigen recognized by autologous T cells infiltrating into tumor.
Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3515-9
PMID: 8170938
-
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
-
Melanoma and vitiligo are associated with antibody responses to similar antigens on pigment cells.
Arch Dermatol. 1995 Mar;131(3):314-8
PMID: 7887661
-
Phenotypic analysis of antigen-specific T lymphocytes.
Science. 1996 Oct 4;274(5284):94-6
PMID: 8810254
-
Vitiligo in patients with melanoma: normal tissue antigens can be targets for cancer immunotherapy.
J Immunother Emphasis Tumor Immunol. 1996 Jan;19(1):81-4
PMID: 8859727
-
Identification of tyrosinase-related protein 2 as a tumor rejection antigen for the B16 melanoma.
J Exp Med. 1997 Feb 3;185(3):453-9
PMID: 9053445
-
Outpatient chemoimmunotherapy for the treatment of metastatic melanoma.
Semin Oncol. 1997 Feb;24(1 Suppl 4):S44-8
PMID: 9122734
-
Immunologic and therapeutic evaluation of a synthetic peptide vaccine for the treatment of patients with metastatic melanoma.
Nat Med. 1998 Mar;4(3):321-7
PMID: 9500606
-
Vaccination of melanoma patients with peptide- or tumor lysate-pulsed dendritic cells.
Nat Med. 1998 Mar;4(3):328-32
PMID: 9500607
-
Direct isolation, phenotyping and cloning of low-frequency antigen-specific cytotoxic T lymphocytes from peripheral blood.
Curr Biol. 1998 Mar 26;8(7):413-6
PMID: 9545200
-
Autologous human dendriphages pulsed with synthetic or natural tumor peptides elicit tumor-specific CTLs in vitro.
J Immunother. 1998 Mar;21(2):149-57
PMID: 9551367
-
A new look at T cells.
J Exp Med. 1998 May 4;187(9):1367-71
PMID: 9565629
-
High frequency of skin-homing melanocyte-specific cytotoxic T lymphocytes in autoimmune vitiligo.
J Exp Med. 1998 Sep 21;188(6):1203-8
PMID: 9743539
-
Immunizing patients with metastatic melanoma using recombinant adenoviruses encoding MART-1 or gp100 melanoma antigens.
J Natl Cancer Inst. 1998 Dec 16;90(24):1894-900
PMID: 9862627
-
Isolation of high avidity melanoma-reactive CTL from heterogeneous populations using peptide-MHC tetramers.
J Immunol. 1999 Feb 15;162(4):2227-34
PMID: 9973498
-
Vaccination with a recombinant vaccinia virus encoding a "self" antigen induces autoimmune vitiligo and tumor cell destruction in mice: requirement for CD4(+) T lymphocytes.
Proc Natl Acad Sci U S A. 1999 Mar 16;96(6):2982-7
PMID: 10077623
-
Quantitation of antigen-specific CD8+ T-cell responses.
Immunol Lett. 1999 Mar;66(1-3):77-80
PMID: 10203037
-
The use of anti-CD3 and anti-CD28 monoclonal antibodies to clone and expand human antigen-specific T cells.
J Immunol Methods. 1990 Apr 17;128(2):189-201
PMID: 1691237