Abstract
Many peripheral solid tumors such as sarcomas and carcinomas express tumor-specific antigens that can serve as targets for immune effector T cells. Nevertheless, overall immune surveillance against such tumors seems relatively inefficient. We studied immune surveillance against a s.c. sarcoma expressing a characterized viral tumor antigen. Surprisingly, the tumor cells were capable of inducing a protective cytotoxic T cell response if transferred as a single-cell suspension. However, if they were transplanted as small tumor pieces, tumors readily grew. Tumor growth correlated strictly with (i) failure of tumor cells to reach the draining lymph nodes and (ii) absence of primed cytotoxic T cells. Cytotoxic T cells were not tolerant or deleted because a tumor antigen-specific cytotoxic T cell response was readily induced in lymphoid tissue by immunization with virus or with tumor cells even in the presence of large tumors. Established tumors were rejected by vaccine-induced effector T cells if effector T cells were maintained by prolonged or repetitive vaccination, but not by single-dose vaccination. Thus, in addition to several other tumor-promoting parameters, some antigenic peripheral sarcomas-and probably carcinomas-may grow not because they anergize or tolerize tumor-specific T cells, but because such tumors are immunologically dealt with as if they were in a so-called immunologically privileged site and are ignored for too long.
MeSH Terms
Animals
Antigens, Neoplasm/immunology
Antigens, Viral/immunology
Bone Marrow Cells/cytology,immunology
Clonal Anergy
Dendritic Cells/immunology
Fibrosarcoma/immunology,pathology
Homeodomain Proteins/genetics,immunology
Immunologic Deficiency Syndromes/immunology
Immunologic Surveillance
Immunotherapy
Lymphocyte Depletion
Mice
Mice, Inbred C57BL
Mice, Knockout
Mice, Nude
Mice, Transgenic
T-Lymphocytes/immunology
T-Lymphocytes, Cytotoxic/immunology
Chemicals
Antigens, Neoplasm
Antigens, Viral
Homeodomain Proteins
RAG-1 protein
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Ochsenbein A F
Institute for Experimental Immunology, University Hospital, Schmelzbergstrasse 12, 8091 Zurich, Switzerland. aochsenb@pathol.unizh.ch
Klenerman P
Karrer U
Ludewig B
Pericin M
Hengartner H
Zinkernagel R M
References (31)
31 references, click to expand
-
Considerations of some current concepts in cancer research.
J Natl Cancer Inst. 1975 Oct;55(4):755-9
PMID: 1081146
-
Costimulation of T lymphocytes: the role of CD28, CTLA-4, and B7/BB1 in interleukin-2 production and immunotherapy.
Cell. 1992 Dec 24;71(7):1065-8
PMID: 1335362
-
Costimulation of antitumor immunity by the B7 counterreceptor for the T lymphocyte molecules CD28 and CTLA-4.
Cell. 1992 Dec 24;71(7):1093-102
PMID: 1335364
-
The homograft reaction.
Proc R Soc Lond B Biol Sci. 1958 Dec 4;149(935):145-66
PMID: 13614379
-
THE IMMUNOLOGICAL BASIS OF ACQUIRED CELLULAR RESISTANCE.
J Exp Med. 1964 Jul 1;120:105-20
PMID: 14194388
-
A cell culture model for T lymphocyte clonal anergy.
Science. 1990 Jun 15;248(4961):1349-56
PMID: 2113314
-
Enhanced tumor susceptibility of immunocompetent mice infected with lymphocytic choriomeningitis virus.
Cancer Immunol Immunother. 1990;32(2):117-24
PMID: 2289203
-
A new analysis of allogeneic interactions.
Aust J Exp Biol Med Sci. 1975 Feb;53(1):27-42
PMID: 238498
-
A new approach to the adoptive immunotherapy of cancer with tumor-infiltrating lymphocytes.
Science. 1986 Sep 19;233(4770):1318-21
PMID: 3489291
-
A theory of self-nonself discrimination.
Science. 1970 Sep 11;169(3950):1042-9
PMID: 4194660
-
Failure of immunosurveillance against chemically induced in situ tumors in mice.
J Natl Cancer Inst. 1974 Mar;52(3):729-32
PMID: 4826561
-
Immunological surveillance in neoplasia.
Transplant Rev. 1971;7:3-25
PMID: 5146537
-
Tumor rejection after direct costimulation of CD8+ T cells by B7-transfected melanoma cells.
Science. 1993 Jan 15;259(5093):368-70
PMID: 7678351
-
Fibroblasts as efficient antigen-presenting cells in lymphoid organs.
Science. 1995 Jun 2;268(5215):1343-7
PMID: 7761853
-
Tumor antigens recognized by T lymphocytes.
Annu Rev Immunol. 1994;12:337-65
PMID: 8011285
-
Tolerance, danger, and the extended family.
Annu Rev Immunol. 1994;12:991-1045
PMID: 8011301
-
Induction of diabetes is influenced by the infectious virus and local expression of MHC class I and tumor necrosis factor-alpha.
J Immunol. 1993 Jun 1;150(11):5185-94
PMID: 8496610
-
Manipulation of costimulatory signals to enhance antitumor T-cell responses.
Curr Opin Immunol. 1995 Oct;7(5):682-6
PMID: 8573312
-
Visualization, characterization, and turnover of CD8+ memory T cells in virus-infected hosts.
J Exp Med. 1996 Apr 1;183(4):1367-75
PMID: 8666895
-
Analysis of cytotoxic T cell responses to dominant and subdominant epitopes during acute and chronic lymphocytic choriomeningitis virus infection.
J Immunol. 1996 Dec 15;157(12):5543-54
PMID: 8955205
-
On the key role of secondary lymphoid organs in antiviral immune responses studied in alymphoplastic (aly/aly) and spleenless (Hox11(-)/-) mutant mice.
J Exp Med. 1997 Jun 16;185(12):2157-70
PMID: 9182687
-
Antigenic cancer cells grow progressively in immune hosts without evidence for T cell exhaustion or systemic anergy.
J Exp Med. 1997 Jul 21;186(2):229-38
PMID: 9221752
-
Self antigens expressed by solid tumors Do not efficiently stimulate naive or activated T cells: implications for immunotherapy.
J Exp Med. 1997 Aug 29;186(5):645-53
PMID: 9271580
-
A simple method for evaluating the rejection of grafted spleen cells by flow cytometry and tracing adoptively transferred cells by light microscopy.
J Immunol Methods. 1997 Aug 22;207(1):33-42
PMID: 9328584
-
A non-retroviral RNA virus persists in DNA form.
Nature. 1997 Nov 20;390(6657):298-301
PMID: 9384383
-
Virus-specific MHC-class II-restricted TCR-transgenic mice: effects on humoral and cellular immune responses after viral infection.
Eur J Immunol. 1998 Jan;28(1):390-400
PMID: 9485218
-
Dendritic cells efficiently induce protective antiviral immunity.
J Virol. 1998 May;72(5):3812-8
PMID: 9557664
-
Cancer vaccines.
Nat Med. 1998 May;4(5 Suppl):525-31
PMID: 9585204
-
Cross-presentation: a general mechanism for CTL immunity and tolerance.
Immunol Today. 1998 Aug;19(8):368-73
PMID: 9709505
-
Tumor-infiltrating lymphocytes exhibiting high ex vivo cytolytic activity fail to prevent murine melanoma tumor growth in vivo.
J Immunol. 1998 Sep 1;161(5):2187-94
PMID: 9725210
-
Liver transplant recipients are not at increased risk for nonlymphoid solid organ tumors.
Cancer. 1998 Sep 15;83(6):1237-43
PMID: 9740091