Abstract
Adoptive T cell therapy, involving the ex vivo selection and expansion of antigen-specific T cell clones, provides a means of augmenting antigen-specific immunity without the in vivo constraints that can accompany vaccine-based strategies. A phase I study was performed to evaluate the safety, in vivo persistence, and efficacy of adoptively transferred CD8+ T cell clones targeting the tumor-associated antigens, MART1MelanA and gp100 for the treatment of patients with metastatic melanoma. Four infusions of autologous T cell clones were administered, the first without IL-2 and subsequent infusions with low-dose IL-2 (at 0.25, 0.50, and 1.0 x 10(6) unitsm(2) twice daily for the second, third, and fourth infusions, respectively). Forty-three infusions of MART1MelanA-specific or gp100-specific CD8+ T cell clones were administered to 10 patients. No serious toxicity was observed. We demonstrate that the adoptively transferred T cell clones persist in vivo in response to low-dose IL-2, preferentially localize to tumor sites and mediate an antigen-specific immune response characterized by the elimination of antigen-positive tumor cells, regression of individual metastases, and minor, mixed or stable responses in 8 of 10 patients with refractory, metastatic disease for up to 21 mo.
MeSH Terms
Adult
Antigens, Neoplasm/immunology
CD8-Positive T-Lymphocytes/immunology,transplantation
Cell Movement
Clone Cells/immunology,transplantation
Female
Graft Survival
Humans
Immunotherapy, Adoptive
Interleukin-2/therapeutic use
MART-1 Antigen
Male
Melanoma/immunology,secondary,therapy
Membrane Glycoproteins/immunology
Middle Aged
Monophenol Monooxygenase/immunology
Neoplasm Proteins/immunology
Recurrence
Safety
T-Lymphocyte Subsets/immunology,transplantation
Treatment Outcome
gp100 Melanoma Antigen
Chemicals
Antigens, Neoplasm
Interleukin-2
MART-1 Antigen
MLANA protein, human
Membrane Glycoproteins
Neoplasm Proteins
PMEL protein, human
gp100 Melanoma Antigen
Monophenol Monooxygenase
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Yee C
Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue North, D3-100, Seattle, WA 98109, USA. cyee@fhcrc.org
Thompson J A
Byrd D
Riddell S R
Roche P
Celis E
Greenberg P D
References (29)
29 references, click to expand
-
Two subsets of memory T lymphocytes with distinct homing potentials and effector functions.
Nature. 1999 Oct 14;401(6754):708-12
PMID: 10537110
-
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
-
Vaccination with mage-3A1 peptide-pulsed mature, monocyte-derived dendritic cells expands specific cytotoxic T cells and induces regression of some metastases in advanced stage IV melanoma.
J Exp Med. 1999 Dec 6;190(11):1669-78
PMID: 10587357
-
Induction of primary NY-ESO-1 immunity: CD8+ T lymphocyte and antibody responses in peptide-vaccinated patients with NY-ESO-1+ cancers.
Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):12198-203
PMID: 11027314
-
Identification of a human melanoma antigen recognized by tumor-infiltrating lymphocytes associated with in vivo tumor rejection.
Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6458-62
PMID: 8022805
-
Phenotypic analysis of antigen-specific T lymphocytes.
Science. 1996 Oct 4;274(5284):94-6
PMID: 8810254
-
Tumor escape from immune recognition: lethal recurrent melanoma in a patient associated with downregulation of the peptide transporter protein TAP-1 and loss of expression of the immunodominant MART-1/Melan-A antigen.
J Clin Invest. 1996 Oct 1;98(7):1633-41
PMID: 8833913
-
Identification of subdominant CTL epitopes of the GP100 melanoma-associated tumor antigen by primary in vitro immunization with peptide-pulsed dendritic cells.
J Immunol. 1997 Feb 15;158(4):1796-802
PMID: 9029118
-
Immunoselection in vivo: independent loss of MHC class I and melanocyte differentiation antigen expression in metastatic melanoma.
Int J Cancer. 1997 Apr 10;71(2):142-7
PMID: 9139833
-
T cell defined tumor antigens.
Curr Opin Immunol. 1997 Oct;9(5):684-93
PMID: 9368778
-
Prospects for adoptive T cell therapy.
Curr Opin Immunol. 1997 Oct;9(5):702-8
PMID: 9368780
-
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
-
HLA-peptide tetrameric complexes.
Curr Opin Immunol. 1998 Aug;10(4):393-6
PMID: 9722914
-
HLA-independent heterogeneity of CD8+ T cell responses to MAGE-3, Melan-A/MART-1, gp100, tyrosinase, MC1R, and TRP-2 in vaccine-treated melanoma patients.
J Immunol. 1998 Dec 15;161(12):6970-6
PMID: 9862732
-
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
-
Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients.
Nat Med. 1999 Jun;5(6):677-85
PMID: 10371507
-
Melanocyte destruction after antigen-specific immunotherapy of melanoma: direct evidence of t cell-mediated vitiligo.
J Exp Med. 2000 Dec 4;192(11):1637-44
PMID: 11104805
-
Immunity against cancer: lessons learned from melanoma.
Curr Opin Immunol. 2001 Apr;13(2):134-40
PMID: 11228404
-
Clinical trial designs for the early clinical development of therapeutic cancer vaccines.
J Clin Oncol. 2001 Mar 15;19(6):1848-54
PMID: 11251017
-
Preferential localization of effector memory cells in nonlymphoid tissue.
Science. 2001 Mar 23;291(5512):2413-7
PMID: 11264538
-
Adoptive transfer of cloned melanoma-reactive T lymphocytes for the treatment of patients with metastatic melanoma.
J Immunother. 2001 Jul-Aug;24(4):363-73
PMID: 11565838
-
Ex vivo expansion of polyclonal and antigen-specific cytotoxic T lymphocytes by artificial APCs expressing ligands for the T-cell receptor, CD28 and 4-1BB.
Nat Biotechnol. 2002 Feb;20(2):143-8
PMID: 11821859
-
Phase I trial of adoptive immunotherapy with cytolytic T lymphocytes immunized against a tyrosinase epitope.
J Clin Oncol. 2002 Feb 15;20(4):1075-86
PMID: 11844833
-
Observations on the systemic administration of autologous lymphokine-activated killer cells and recombinant interleukin-2 to patients with metastatic cancer.
N Engl J Med. 1985 Dec 5;313(23):1485-92
PMID: 3903508
-
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
-
Low-dose subcutaneous recombinant interleukin-2 in advanced human malignancy: a phase II outpatient study.
Mol Biother. 1990 Mar;2(1):18-26
PMID: 2334534
-
Adoptive T cell therapy of tumors: mechanisms operative in the recognition and elimination of tumor cells.
Adv Immunol. 1991;49:281-355
PMID: 1853786
-
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
-
Phase II study of intermittent continuous infusion of low-dose recombinant interleukin-2 in advanced melanoma and renal cell cancer.
Ann Oncol. 1994 Feb;5(2):179-81
PMID: 8186163