Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Advertisement

British Journal of Cancer
  • View all journals
  • Search
  • My Account Login
  • Content Explore content
  • About the journal
  • Publish with us
  • Sign up for alerts
  • RSS feed
  1. nature
  2. british journal of cancer
  3. review
  4. article
Immune selection in neoplasia: towards a microevolutionary model of cancer development
Download PDF
Download PDF
  • Review
  • Open access
  • Published: 23 May 2000

Immune selection in neoplasia: towards a microevolutionary model of cancer development

  • S J Pettit1,
  • K Seymour1,
  • E O'Flaherty1 &
  • …
  • J A Kirby1 

British Journal of Cancer volume 82, pages 1900–1906 (2000)Cite this article

  • 1086 Accesses

  • 47 Citations

  • Metrics details

This article has been updated

Abstract

The dual properties of genetic instability and clonal expansion allow the development of a tumour to occur in a microevolutionary fashion. A broad range of pressures are exerted upon a tumour during neoplastic development. Such pressures are responsible for the selection of adaptations which provide a growth or survival advantage to the tumour. The nature of such selective pressures is implied in the phenotype of tumours that have undergone selection. We have reviewed a range of immunologically relevant adaptations that are frequently exhibited by common tumours. Many of these have the potential to function as mechanisms of immune response evasion by the tumour. Thus, such adaptations provide evidence for both the existence of immune surveillance, and the concept of immune selection in neoplastic development. This line of reasoning is supported by experimental evidence from murine models of immune involvement in neoplastic development. The process of immune selection has serious implications for the development of clinical immunotherapeutic strategies and our understanding of current in vivo models of tumour immunotherapy. © 2000 Cancer Research Campaign

Similar content being viewed by others

Intratumoral heterogeneity in cancer progression and response to immunotherapy

Article 11 February 2021

Mechanisms of immune activation and regulation: lessons from melanoma

Article 01 February 2022

Netie: inferring the evolution of neoantigen–T cell interactions in tumors

Article 27 October 2022

Article PDF

Change history

  • 16 November 2011

    This paper was modified 12 months after initial publication to switch to Creative Commons licence terms, as noted at publication

References

  • Ademmer K, Ebert M, Muller Ostermeyer F, Friess H, Buchler MW, Schubert W and Malfertheiner P (1998) Effector T lymphocyte subsets in human pancreatic cancer: detection of CD8(+) CD18(+) cells and CD8(+) CD103(+) cells by multi-epitope imaging. Clin Exp Immunol 112: 21–26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agrawal B, Krantz MJ, Reddish MA and Longenecker BM (1998) Cancer-associated MUC1 mucin inhibits human T-cell proliferation, which is reversible by IL-2. Nat Med 4: 43–49

    Article  CAS  PubMed  Google Scholar 

  • Aizawa K, Ueki K, Suzuki S, Yabusaki H, Kanda T, Nishimaki T, Suzuki T and Hatakeyama K (1999) Apoptosis and Bcl-2 expression in gastric carcinomas: Correlation with clinicopathological variables, p53 expression, cell proliferation and prognosis. International Journal of Oncology 14: 85–91

    CAS  PubMed  Google Scholar 

  • Alexandroff AB, Jackson AM, O’Donnell MA and James K (1999) BCG immunotherapy of bladder cancer: 20 years on. Lancet 353: 1689–1694

    Article  CAS  PubMed  Google Scholar 

  • Bennett M, O’Connell J, O’Sullivan G, Roche D, Brady C, Kelly J, Collins J and Shanahan F (1999) Expression of Fas ligand by human gastric adenocarcinomas: a potential mechanism of immune escape in stomach cancer. Gut 44: 156–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berke G (1995) The CTLs kiss of death. Cell 81: 9–12

    Article  CAS  PubMed  Google Scholar 

  • Boon T (1992) Toward a genetic analysis of tumor rejection antigens. Adv Cancer Res 58: 177–210

    Article  CAS  PubMed  Google Scholar 

  • Cai ZZ, Bettaieb A, ElMahdani N, Legres LG, Stancou R, Masliah J and Chouaib S (1997) Alteration of the sphingomyelin/ceramide pathway is associated with resistance of human breast carcinoma MCF7 cells to tumor necrosis factor-alpha-mediated cytotoxicity. J Biol Chem 272: 6918–6926

    Article  CAS  PubMed  Google Scholar 

  • Chen YT, Scanlan MJ, Sahin U, Tureci O, Gure AO, Tsang SL, Williamson B, Stockert E, Pfreundschuh M and Old LJ (1997) A testicular antigen aberrantly expressed in human cancers detected by autologous antibody screening. Proc Nat Acad Sci USA 94: 1914–1918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng JH, Zhou T, Liu CD, Shapiro JP, Brauer MJ, Kiefer MC, Barr PJ and Mountz JD (1994) Protection from Fas-mediated apoptosis by a soluble form of the Fas molecule. Science 263: 1759–1762

    Article  CAS  PubMed  Google Scholar 

  • Chouaib S, Asselin Paturel C, MamiChouaib F, Caignard A and Blay JY (1997) The host-tumor immune conflict: from immunosuppression to resistance and destruction. Immunol Today 18: 493–497

    Article  CAS  PubMed  Google Scholar 

  • Christofori G and Semb H (1999) The role of the cell-adhesion molecule E-cadherin as a tumour-suppressor gene. Trends Biochem Sci 24: 73–76

    Article  CAS  PubMed  Google Scholar 

  • Cox AL, Skipper J, Chen Y, Henderson RA, Darrow TL, Shabanowitz J, Engelhard VH, Hunt DF and Slingluff CL (1994) Identification of a peptide recognized by 5 melanoma-specific human cytotoxic T cell lines. Science 264: 716–719

    Article  CAS  PubMed  Google Scholar 

  • Cromme FV, Vanbommel PFJ, Walboomers JMM, Gallee MPW, Stern PL, Kenemans P, Helmerhorst TJM, Stukart MJ and Meijer C (1994) Differences in MHC and TAP-1 expression in cervical cancer lymph node metastases as compared with the primary tumours. Br J Cancer 69: 1176–1181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dawkins R (1988) The Blind Watchmaker Penguin: London

    Google Scholar 

  • Driscoll J, Brown MG, Finley D and Monaco JJ (1993) MHC linked LMP gene products specifically alter peptidase activities of the proteasome. Nature 365: 262–264

    Article  CAS  PubMed  Google Scholar 

  • Eder IE, Stenzl A, Hobisch A, Cronauer MV, Bartsch G and Klocker H (1997) Expression of transforming growth factors beta-1, beta 2 and beta 3 in human bladder carcinomas. Br J Cancer 75: 1753–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engel AM, Svane IM, Rygaard J and Werdelin O (1997) MCA sarcomas induced in scid mice are more immunogenic than MCA sarcomas induced in congenic, immunocompetent mice. Scand J Immunol 45: 463–470

    Article  CAS  PubMed  Google Scholar 

  • Fey MF and Tobler A (1996) Tumour heterogeneity and clonality – An old theme revisited. Ann Oncol 7: 121–128

    Article  CAS  PubMed  Google Scholar 

  • Fuchs EJ and Matzinger P (1996) Is cancer dangerous to the immune system?. Semin Immunol 8: 271–280

    Article  CAS  PubMed  Google Scholar 

  • Gallucci S, Lolkema M and Matzinger P (1999) Natural adjuvants: Endogenous activators of dendritic cells. Nat Med 5: 1249–1255

    Article  CAS  PubMed  Google Scholar 

  • Garrido F, Cabrera T, Concha A, Glew S, Ruizcabello F and Stern PL (1993) Natural history of HLA expression during tumour development. Immunol Today 14: 491–499

    Article  CAS  PubMed  Google Scholar 

  • Garrido F, Ruiz Cabello F, Cabrera T, Perez Villar JJ, Lopez Botet M, Duggan Keen M and Stern PL (1997) Implications for immunosurveillance of altered HLA class I phenotypes in human tumours. Immunol Today 18: 89–95

    Article  CAS  PubMed  Google Scholar 

  • Gastl GA, Abrams JS, Nanus DM, Oosterkamp R, Silver J, Liu F, Chen M, Albino AP and Bander NH (1993) Interleukin-10 production by human carcinoma cell lines and its relationship to interleukin-6 expression. Int J Cancer 55: 96–101

    Article  CAS  PubMed  Google Scholar 

  • Hahne M, Rimoldi D, Schroter M, Romero P, Schreier M, French LE, Schneider P, Bornand T, Fontana A, Lienard D, Cerottini JC and Tschopp J (1996) Melanoma cell expression of Fas(Apo-1/CD95) ligand: Implications for tumor immune escape. Science 274: 1363–1366

    Article  CAS  PubMed  Google Scholar 

  • Hakansson L, Adell G, Boeryd B, Sjogren F and Sjodahl R (1997) Infiltration of mononuclear inflammatory cells into primary colorectal carcinomas: An immunohistological analysis. Br J Cancer 75: 374–380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu HM, Urba WJ and Fox BA (1998) Gene-modified tumor vaccine with therapeutic potential shifts tumor-specific T cell response from a type 2 to a type 1 cytokine profile. J Immunol 161: 3033–3041

    CAS  PubMed  Google Scholar 

  • Irmler M, Thome M, Hahne M, Schneider P, Hofmann B, Steiner V, Bodmer JL, Schroter M, Burns K, Mattmann C, Rimoldi D, French LE and Tschopp J (1997) Inhibition of death receptor signals by cellular FLIP. Nature 388: 190–195

    Article  CAS  PubMed  Google Scholar 

  • Jackson AM, Alexandroff AB, Fleming D, Prescott S, Chisholm GD and James K (1994) Bacillus Calmette-Guerin (BCG) organisms directly alter the growth of bladder tumor cells. International Journal of Oncology 5: 697–703

    CAS  PubMed  Google Scholar 

  • Janeway CA, Goodnow CC and Medzhitov R (1996) Immunological tolerance – danger, pathogen on the premises. Curr Biol 6: 519–522

    Article  CAS  PubMed  Google Scholar 

  • Jodo S, Kobayashi S, Nakajima Y, Matsunaga T, Nakayama N, Ogura N, Kayagaki N, Okumura K and Koike T (1998) Elevated serum levels of soluble Fas/APO-1 (CD95) in patients with hepatocellular carcinoma. Clin Exp Immunol 112: 166–171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karecla PI, Green SJ, Bowden SJ, Coadwell J and Kilshaw PJ (1996) Identification of a binding site for integrin alpha E beta(7) in the N-terminal domain of E-cadherin. J Biol Chem 271: 30909–30915

    Article  CAS  PubMed  Google Scholar 

  • Keating PJ, Cromme FV, Duggankeen M, Snijders PJF, Walboomers JMM, Hunter RD, Dyer PA and Stern PL (1995) Frequency of downregulation of individual HLA-A and HLA-B alleles in cervical carcinomas in relation to TAP-1 expression. Br J Cancer 72: 405–411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurokohchi K, Carrington M, Mann DL, Simonis TB, Alexander Miller MA, Feinstone SM, Akatsuka T and Berzofsky JA (1996) Expression of HLA class I molecules and the transporter associated with antigen processing in hepatocellular carcinoma. Hepatology 23: 1181–1188

    Article  CAS  PubMed  Google Scholar 

  • Lanier LL (1998) NK cell receptors. Annu Rev Immunol 16: 359–393

    Article  CAS  PubMed  Google Scholar 

  • Lee PP, Yee C, Savage PA, Fong L, Brockstedt D, Weber JS, Johnson D, Swetter S, Thompson J, Greenberg PD, Roederer M and Davis MM (1999) Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients. Nat Med 5: 677–685

    Article  CAS  PubMed  Google Scholar 

  • Lehmann F, Marchand M, Hainaut P, Pouillart P, Sastre X, Ikeda H, Boon T and Coulie PG (1995) Differences in the antigens recognized by cytolytic T cells on 2 successive mctastases of a melanoma patient are consistent with immune selection. Eur J Immunol 25: 340–347

    Article  CAS  PubMed  Google Scholar 

  • Lengauer C, Kinzler KW and Vogelstein B (1998) Genetic instabilities in human cancers. Nature 396: 643–649

    Article  CAS  PubMed  Google Scholar 

  • Ljunggren HG, Stam NJ, Ohlen C, Neefjes JJ, Hoglund P, Heemels MT, Bastin J, Schumacher TNM, Townsend A, Karre K and Ploegh HL (1990) Empty MHC class I molecules come out in the cold. Nature 346: 476–480

    Article  CAS  PubMed  Google Scholar 

  • Maeda H and Shiraishi A (1996) TGF-beta contributes to the shift toward Th2-type responses through direct and IL-1O-mediated pathways in tumor-bearing mice. J Immunol 156: 73–78

    CAS  PubMed  Google Scholar 

  • Maeurer MJ, Gollin SM, Martin D, Swaney W, Bryant J, Castelli C, Robbins P, Parmiani G, Storkus WJ and Lotze MT (1996) 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 98: 1633–1641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marzo AL, Lake RA, Lo D, Sherman L, McWilliam A, Nelson D, Robinson BWS and Scott B (1999) Tumor antigens are constitutively presented in the draining lymph nodes. J Immunol 162: 5838–5845

    CAS  PubMed  Google Scholar 

  • Matsuda M, Salazar F, Petersson M, Masucci G, Hansson J, Pisa P, Zhang QJ, Masucci MG and Kiessling R (1994) Interleukin-10 pretreatment protects target cells from tumor-specific and allo-specific cytotoxic T cells and downregulates HLA Class I expression. J Exp Med 180: 2371–2376

    Article  CAS  PubMed  Google Scholar 

  • Medema JP, Toes REM, Scaffidi C, Zheng TS, Flavell RA, Melief CJM, Peter ME, Offringa R and Krammer PH (1997) Cleavage of FLICE (caspase-8) by granzyme B during cytotoxic T lymphocyte-induced apoptosis. Eur J Immunol 27: 3492–3498

    Article  CAS  PubMed  Google Scholar 

  • Melcher A, Todryk S, Hardwick N, Ford M, Jacobson M and Vile RG (1998) Tumor immunogenicity is determined by the mechanism of cell death via induction of heat shock protein expression. Nat Med 4: 581–587

    Article  CAS  PubMed  Google Scholar 

  • Morisaki T, Katano M, Ikubo A, Anan K, Nakamura M, Nakamura K, Sato H, Tanaka M and Torisu M (1996) Immunosuppressive cytokines (IL-10, TGF-beta) genes expression in human gastric carcinoma tissues. J Surg Oncol 63: 234–239

    Article  CAS  PubMed  Google Scholar 

  • Multhoff G, Botzler C, Wiesnet M, Muller E, Meier T, Wilmanns W and Issels RD (1995) A stress inducible 72-Kda heat shock protein (Hsp72) is expressed on the surface of human tumour cells, but not on normal cells. Int J Cancer 61: 272–279

    Article  CAS  PubMed  Google Scholar 

  • Niehans GA, Brunner T, Frizelle SP, Liston JC, Salerno CT, Knapp DJ, Green DR and Kratzke RA (1997) Human lung carcinomas express Fas ligand. Cancer Res 57: 1007–1012

    CAS  PubMed  Google Scholar 

  • Ochsenbein AF, Klenerman P, Karrer U, Ludewig B, Pericin M, Hengartner H and Zinkernagel RM (1999) Immune surveillance against a solid tumor fails because of immunological ignorance. Proc Natl Acad Sci USA 96: 2233–2238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Connell J, Bennett MW, O’Sullivan GC, Roche D, Kelly J, Collins JK and Shanahan F (1998) Fas ligand expression in primary colon adenocarcinomas: Evidence that the Fas counterattack is a prevalent mechanism of immune evasion in human colon cancer. J Pathol 186: 240–246

    Article  PubMed  Google Scholar 

  • Pena JC, Thompson CB, Recant W, Vokes EE and Rudin CM (1999) Bcl-x(L) and Bcl-2 expression in squamous cell carcinoma of the head and neck. Cancer 85: 164–170

    Article  CAS  PubMed  Google Scholar 

  • Pitti RM, Marsters SA, Lawrence DA, Roy M, Kischkel FC, Dowd P, Huang A, Donahue CJ, Sherwood SW, Baldwin DT, Godowski PJ, Wood WI, Gurney AL, Hillan KJ, Cohen RL, Goddard AD, Botstein D and Ashkenazi A (1998) Genomic amplification of a decoy receptor for Fas ligand in lung and colon cancer. Nature 396: 699–703

    Article  CAS  PubMed  Google Scholar 

  • Poppas DP, Pavlovich CP, Folkman J, Voest EE, Chen XH, Luster AD and O’Donnell MA (1998) Intravesical bacille Calmette-Guerin induces the antiangiogenic chemokine interferon-inducible protein 10. Urology 52: 268–275

    Article  CAS  PubMed  Google Scholar 

  • Restifo NP, Esquivel F, Kawakami Y, Yewdell JW, Mule JJ, Rosenberg SA and Bennink JR (1993) Identification of human cancers deficient in antigen processing. J Exp Med 177: 265–272

    Article  CAS  PubMed  Google Scholar 

  • Romero P, Dunbar PR, Valmori D, Pittet M, Ogg GS, Rimoldi D, Chen JL, Lienard D, Cerottini JC and Cerundolo V (1998) Ex vivo staining of metastatic lymph nodes by class I major histocompatibility complex tetramers reveals high numbers of antigen-experienced tumor-specific cytolytic T lymphocytes. J Exp Med 188: 1641–1650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosenberg SA (1999) A new era for cancer immunotherapy based on the genes that encode cancer antigens. Immunity 10: 281–287

    Article  CAS  PubMed  Google Scholar 

  • Sahin U, Tureci O, Schmitt H, Cochlovius B, Johannes T, Schmits R, Stenner F, Luo GR, Schobert I and Pfreundschuh M (1995) Human neoplasms elicit multiple specific immune responses in the autologous host. Proc Nat Acad Sci USA 92: 11810–11813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seliger B, Hohne A, Knuth A, Bernhard H, Ehring B, Tampe R and Huber C 1996 a) Reduced membrane major histocompatibility complex class I density and stability in a subset of human renal cell carcinomas with low TAP and LMP expression. Clinical Cancer Research 2: 1427–1433

    CAS  PubMed  Google Scholar 

  • Seliger B, Hohne A, Knuth A, Bernhard H, Meyer T, Tampe R, Momburg F and Huber C 1996 b) Analysis of the major histocompatibility complex class I antigen presentation machinery in normal and malignant renal cells: Evidence for deficiencies associated with transformation and progression. Cancer Res 56: 1756–1760

    CAS  PubMed  Google Scholar 

  • Seliger B, Maeurer MJ and Ferrone S (1997) TAP off – Tumors on. Immunol Today 18: 292–299

    CAS  PubMed  Google Scholar 

  • Strand S, Hofmann WJ, Hug H, Muller M, Otto G, Strand D, Mariani SM, Stremmel W, Krammer PH and Galle PR (1996) Lymphocyte apoptosis induced by CD95 (Apo-1/Fas) ligand expressing tumor cells – a mechanism of immune evasion. Nat Med 2: 1361–1366

    Article  CAS  PubMed  Google Scholar 

  • Svane IM, Engel AM, Nielsen MB, Ljunggren HG, Rygaard J and Werdelin O (1996) Chemically induced sarcomas from nude mice are more immunogenic than similar sarcomas from congenic normal mice. Eur J Immunol 26: 1844–1850

    Article  CAS  PubMed  Google Scholar 

  • Taylor Papadimitriou J and Finn OJ (1997) Biology, biochemistry and immunology of carcinoma-associated mucins. Immunol Today 18: 105–107

    Article  CAS  PubMed  Google Scholar 

  • Todryk S, Melcher AA, Hardwick N, Linardakis E, Bateman A, Colombo MP, Stoppacciaro A and Vile RG (1999) Heat shock protein 70 induced during tumor cell killing induces Th1 cytokines and targets immature dendritic cell precursors to enhance antigen uptake. J Immunol 163: 1398–1408

    CAS  PubMed  Google Scholar 

  • Torzewski M, Sarbia M, Heep H, Dutkowski P, Willers R and Gabbert HE (1998) Expression of Bcl-X-L, an antiapoptotic member of the Bcl-2 family, in esophageal squamous cell carcinoma. Clinical Cancer Research 4: 577–583

    CAS  PubMed  Google Scholar 

  • van de Welvankemenade E, Ligtenberg MJL, de Boer AJ, Buijs F, Vos HL, Melief CJM, Hilkens J and Figdor CG (1993) Episialin (MUC1) inhibits cytotoxic lymphocyte-target cell interaction. J Immunol 151: 767–776

    Google Scholar 

  • Vanky F, Nagy N, Hising C, Sjovall K, Larson B and Klein E (1997) Human ex vivo carcinoma cells produce transforming growth factor beta and thereby can inhibit lymphocyte functions in vitro. Cancer Immunol Immunother 43: 317–323

    Article  CAS  PubMed  Google Scholar 

  • Wick M, Dubey P, Koeppen H, Siegel CT, Fields PE, Chen LP, Bluestone JA and Schreiber H (1997) Antigenic cancer cells grow progressively in immune hosts without evidence for T cell exhaustion or systemic anergy. J Exp Med 186: 229–238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yannelli JR, Hyatt C, McConnell S, Hines K, Jacknin L, Parker L, Sanders M and Rosenberg SA (1996) Growth of tumor-infiltrating lymphocytes from human solid cancers: Summary of a 5-year experience. Int J Cancer 65: 413–421

    Article  CAS  PubMed  Google Scholar 

  • York IA and Rock KL (1996) Antigen processing and presentation by the class I major histocompatibility complex. Annu Rev Immunol 14: 369–396

    Article  CAS  PubMed  Google Scholar 

  • Young DC (1989) Drug resistance: the clinical problem. Drug Resistance in Cancer Therapy Ozols RF (eds, pp 1–26, Kluwer: Dordrecht

    Google Scholar 

  • Zhang K, Sikut R and Hansson GC (1997) A MUC1 mucin secreted from a colon carcinoma cell line inhibits target cell lysis by natural killer cells. Cell Immunol 176: 158–165

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Surgery, Surgical Immunobiology Group, University of Newcastle upon Tyne, NE2 4HH, UK

    S J Pettit, K Seymour, E O'Flaherty & J A Kirby

Authors
  1. S J Pettit
    View author publications

    Search author on:PubMed Google Scholar

  2. K Seymour
    View author publications

    Search author on:PubMed Google Scholar

  3. E O'Flaherty
    View author publications

    Search author on:PubMed Google Scholar

  4. J A Kirby
    View author publications

    Search author on:PubMed Google Scholar

Rights and permissions

From twelve months after its original publication, this work is licensed under the Creative Commons Attribution-NonCommercial-Share Alike 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/

Reprints and permissions

About this article

Cite this article

Pettit, S., Seymour, K., O'Flaherty, E. et al. Immune selection in neoplasia: towards a microevolutionary model of cancer development. Br J Cancer 82, 1900–1906 (2000). https://doi.org/10.1054/bjoc.2000.1206

Download citation

  • Received: 13 April 1999

  • Revised: 01 February 2000

  • Accepted: 17 February 2000

  • Published: 23 May 2000

  • Issue date: 01 June 2000

  • DOI: https://doi.org/10.1054/bjoc.2000.1206

Share this article

Anyone you share the following link with will be able to read this content:

Sorry, a shareable link is not currently available for this article.

Provided by the Springer Nature SharedIt content-sharing initiative

Keywords

  • immune selection
  • evolution
  • tumour
  • immune escape

This article is cited by

  • Beeinflussung maligner Tumoren durch Anästhesieverfahren

    • K. Fukui
    • C. Werner
    • G. Pestel

    Der Anaesthesist (2012)

  • Generation of MHC class I ligands in the secretory and vesicular pathways

    • Margarita Del Val
    • Salvador Iborra
    • Silvia Lázaro

    Cellular and Molecular Life Sciences (2011)

  • Intracellular esterase activity in living cells may distinguish between metastatic and tumor-free lymph nodes

    • Elena Afrimzon
    • Assaf Deutsch
    • Mordechai Deutsch

    Clinical & Experimental Metastasis (2008)

  • Chemokines: novel targets for breast cancer metastasis

    • Simi Ali
    • Gwendal Lazennec

    Cancer and Metastasis Reviews (2007)

  • Designing antibodies for oncology

    • Jerome E. Tanner

    Cancer and Metastasis Reviews (2005)

Download PDF

Advertisement

Explore content

  • Research articles
  • Reviews & Analysis
  • News & Comment
  • Current issue
  • Collections
  • Follow us on Twitter
  • Sign up for alerts
  • RSS feed

About the journal

  • Journal Information
  • Open access publishing
  • About the Editors
  • Contact
  • Special Issues
  • For Advertisers
  • Subscribe

Publish with us

  • For Authors & Referees
  • Language editing services
  • Submit manuscript

Search

Advanced search

Quick links

  • Explore articles by subject
  • Find a job
  • Guide to authors
  • Editorial policies

British Journal of Cancer (Br J Cancer)

ISSN 1532-1827 (online)

ISSN 0007-0920 (print)

nature.com sitemap

About Nature Portfolio

  • About us
  • Press releases
  • Press office
  • Contact us

Discover content

  • Journals A-Z
  • Articles by subject
  • protocols.io
  • Nature Index

Publishing policies

  • Nature portfolio policies
  • Open access

Author & Researcher services

  • Reprints & permissions
  • Research data
  • Language editing
  • Scientific editing
  • Nature Masterclasses
  • Research Solutions

Libraries & institutions

  • Librarian service & tools
  • Librarian portal
  • Open research
  • Recommend to library

Advertising & partnerships

  • Advertising
  • Partnerships & Services
  • Media kits
  • Branded content

Professional development

  • Nature Awards
  • Nature Careers
  • Nature Conferences

Regional websites

  • Nature Africa
  • Nature China
  • Nature India
  • Nature Japan
  • Nature Middle East
  • Privacy Policy
  • Use of cookies
  • Legal notice
  • Accessibility statement
  • Terms & Conditions
  • Your US state privacy rights
Springer Nature

© 2025 Springer Nature Limited