Skip to main content

Advertisement

SpringerLink
Log in

Immune surveillance and natural resistance: an evaluation

  • Review
  • Published:
Cancer Immunology, Immunotherapy Aims and scope Submit manuscript

Summary

Concepts in tumour immunology are changing fundamentally.

Around 1970 tumour immunology contained the following related concepts: 1. Thousands of tumour cells arise de novo each day. 2. Tumour cells are antigenic in their host. 3. All these antigenic tumour cells are killed by a strong immune surveillance system.

A more likely set of concepts looks as follows: 1. Tumour cells do not arise frequently. 2. Tumour cells may be antigenic or not. 3. There is no need to postulate a very strong immune surveillance or natural resistance system.

In this paper I am reviewing our present knowledge of immune surveillance and natural resistance. Only scanty information appears to be available. This information suggests that virally induced tumours are usually killed by cytotoxic T lymphocytes, and natural killer cells, whereas immune surveillance and natural resistance against other tumours may be quite weak.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Bakács T, Czanik P, Kimber I et al. (1984) Enhanced K-cell activity in the peripheral blood of patients with malignant disease. Cancer Immunol Immunother 16:170

    Google Scholar 

  2. Baldwin RW (1981) Immunotherapy of cancer. Cancer Chemotherapy Annual 3:178

    Google Scholar 

  3. Baldwin RW, Byers VS (1982) Prospects for immunotherapy of cancer. In: Stoll BA (ed) Prolonged arrest of cancer. John Wiley, London, p 419–430

    Google Scholar 

  4. Baldwin RW, Price MR, Robins RA (1972) Blocking of lymphocyte-mediated cytotoxicity for rat hepatoma cells by tumor-specific antigen-antibody complexes. Nature New Biol 238:185

    Google Scholar 

  5. Bansal SC, Hargreaves R, Sjögren HO (1972) Facilitation of polyoma tumor growth in rats by blocking sera and of tumor eluate. Int J Cancer 9:97

    Google Scholar 

  6. Bernard MI, Pace RC, Unger SW, Wanebo HJ (1983) Monocyte-mediated antibody-dependent cell-mediated cytotoxicity and spontaneous cytotoxicity in normals and cancer patients as assayed by human erythrocyte lysis. Cancer Res 43:4504

    Google Scholar 

  7. Biron CA, Turgiss LR, Welsh RM (1983) Increase in NK cell number and turnover rate during acute viral infection. J Immunol 131:1539

    Google Scholar 

  8. Bolhuis RLH, Schellekens H (1981) Induction of natural killer cell activity and allocytotoxicity in human peripheral blood lymphocytes after mixed lymphocyte culture. Scand J Immunol 13:401

    Google Scholar 

  9. Brunner KT, MacDonald HT, Cerottini J-C (1981) Quantitation and clonal isolation of cytolytic T lymphocyte precursors selectively infiltrating murine sarcoma virus-induced tumors. J Exp Med 154:362

    Google Scholar 

  10. Bukowski JF, Woda BA, Habu S, Okumura K, Welsh RM (1983) Natural killer cell depletion enhances virus synthesis and virus-induced hepatitis in vivo. J Immunol 131:1531

    Google Scholar 

  11. Bukowski JF, Warner JF, Dennert G, Welsh RM (1985) Adoptive transfer studies demonstrating the antiviral effect of natural killer cells in vivo. J Exp Med 161:40

    Google Scholar 

  12. Burnett FM (1970) The concept of immunological surveillance. Prog Exp Tumor Res 13:1

    CAS  PubMed  Google Scholar 

  13. Burnett FM (1971) Immunological surveillance in neoplasia. Transplant Rev 7:3

    Google Scholar 

  14. Butterworth AE, David JR, Franks D, et al. (1977) Antibody-dependent eosinophil-mediated damage to 51Cr-labeled schistosomula of schistosoma mansoni: damage by purified eosinophils. J Exp Med 145:136

    Google Scholar 

  15. Carter RH, Drebin JA, Schatten S, Perry LL, Greene MI (1983) Regulation of the immune response to tumor antigens. IX. In vitro Lyt-1+2− cell proliferative responses to cell bound or subcellular tumor antigen. J Immunol 130:997

    Google Scholar 

  16. De Boer RJ, Hogeweg P, Dullens HFJ, De Weger RA, Den Otter W (1985) Macrophage T lymphocyte interactions in the anti-tumor immune response: A mathematical model. J Immunol 134:2748

    Google Scholar 

  17. De Jong WH, Steerenberg PA, Van de Plas MMT, Kruizinga W, Ruitenberg EJ (1985) T cell involvement in adoptive transfer of line 10 tumor immunity in strain 2 guinea pigs. J Natl Cancer Inst 75:403

    Google Scholar 

  18. Den Otter W (1985) Tumor cells do not arise frequently. Cancer Immunol Immunother 19:159

    Google Scholar 

  19. Dent PB, Fish LA, White JG, Good RA (1966) Chediak Higashi syndrome. Observations on the nature of the associated malignancy. Lab Invest 15:1634

    Google Scholar 

  20. De Weger RA (1982) Lymphocyte induced macrophage cytotoxicity. Ph D Thesis, Utrecht, The Netherlands

    Google Scholar 

  21. De Weger RA, Verbakel JMA, Oskam R, Van Den Berg HTCM, Van Basten CDH, Dullens HFJ, Den Otter W (1983) An improved method of unity gravity sedimentation separation for murine peritoneal macrophage populations. J Immunol Methods 61:117

    Google Scholar 

  22. Domzig W, Lohmann-Matthes ML (1979) Antibody-dependent cellular cytotoxicity against tumor cells. II. The promonocyte identified as effector cell. Eur J Immunol 9:267

    Google Scholar 

  23. Dullens HFJ, Den Otter W (1974) Therapy with allogeneic immune peritoneal cells. Cancer Res 34:1726

    Google Scholar 

  24. Essex M, Klein G, Snyder SP, Boyd Harrold J (1971) Correlation between humoral antibody and regression of tumors induced by feline sarcoma virus. Nature 233:195

    Google Scholar 

  25. Evans R, Lawler EM (1980) Macrophage content and immunogenicity of C57BL/6J and BALB/c ByJ methylcholanthrene-induced sarcomas. Int J Cancer 26:831

    Google Scholar 

  26. Evans R, Cox H, Alexander P (1973) Immunologically specific activation of macrophages armed with the specific macrophage arming factor (SMAF). Proc Soc Exp Biol Med 143:256

    Google Scholar 

  27. Ferry BL, Flannery GR, Robins RA, Lawry J, Baldwin RW (1984) Phenotype of cytotoxic effector cells infiltrating a transplanted chemically induced rat sarcoma. Immunology 53:243

    Google Scholar 

  28. Fidler IJ, Darnell JH, Budmen MB (1976) In vitro activation of mouse macrophages by rat lymphocyte mediators. J Immunol 117:666

    Google Scholar 

  29. Galili K, Vánky F, Rodriguez L, Klein E (1979) Activated T lymphocytes within human solid tumors. Cancer Immunol Immunother 6:129

    Google Scholar 

  30. Gallo RC, Wong-Staal F (1982) Retroviruses as etiologic agents of some animal and human leukemia and lymphomas and as tools for elucidating the molecular mechanism of leukemogenesis. Blood 60:545

    Google Scholar 

  31. Geser A, De Thé G, Lenoir G, Day NE, Williams EH (1982) Final case reporting from the Ugandan prospective study of the relationship between EBV and Burkitt's lymphoma. Int J Cancer 29:397

    Google Scholar 

  32. Gidlund M, Orn A, Wigzell H, Senik A, Gresser I (1978) Enhanced NK cell activity in mice injected with interferon and interferon inducers. Nature 273:759

    Google Scholar 

  33. Gillespie GY, Hansen CB, Hoskins RG, Russell SW (1978) Inflammatory cells in solid murine neoplasms. IV. Cytolytic T lymphocyte isolated from regressing or progressing Moloney sarcomas. J Immunol 119:564

    Google Scholar 

  34. Greenberg PD, Cheever MA (1984) Treatment of disseminated leukemia with cyclophosphamide and immune cells: Tumor immunity reflects long-term persistence of tumor-specific donor T cells. J Immunol 133:3401

    Google Scholar 

  35. Habu S, Akamatsu K-I, Tamaoki N, Okumura K (1984) In vivo significance of NK cells on resistance against virus (HSV-1) infection in mice. J Immunol 133:2743

    Google Scholar 

  36. Haskill JS, Fett JW (1976) Possible evidence for antibody-dependent macrophage mediated cytotoxicity directed against murine adenocarcinoma cells in vivo. J Immunol 117:1992

    Google Scholar 

  37. Hellström KE, Hellström I (1974) Lymphocyte-mediated cytotoxicity and blocking serum activity to tumor antigen. Adv Immunol 18:209

    Google Scholar 

  38. Henle W, Henle G (1982) Immunology of Epstein-Bar Virus. In: Roizman B (ed): The Herpes viruses. 1. Plenum Press, New York, p 209

    Google Scholar 

  39. Henney CS, Kuribayaski K, Kern DE, Gillis S (1981) Interleukin-2 augments natural killer cell activity. Nature 291:335

    Google Scholar 

  40. Hibbs JB, Chapman HA, Weinberg JB (1978) The macrophage as an antineoplastic surveillance cell: Biological perspectives. J Reticuloendothel Soc 24:549

    Google Scholar 

  41. Holden HT, Haskill JS, Kirchner H, Herberman RB (1976) Two functionally distinct anti-tumor effector cells isolated from primary murine sarcoma virus-induced tumors. J Immunol 117:440

    Google Scholar 

  42. Hutchinson GH, Heinemann D, Symes MO, Williamson RCN (1981) Differential immune reactivity of tumour-intrinsic and peripheral-blood lymphocytes against autoplastic colorectal carcinoma cells. Br J Cancer 44:396

    Google Scholar 

  43. Introna M, Allavena P, Biondi A, Colombo N, Villa A, Mantovani A (1983) Defective natural killer activity within human ovarian tumours: Low numbers of morphologically defined effectors present in situ. J Natl Cancer Inst 70:21

    Google Scholar 

  44. Jacobson S, Biddison WE (1984) Major histocompatibility complex molecules as virus receptors. Immunology Today 5:262

    Google Scholar 

  45. Jondal M, Svedmyr E, Klein E, Sing S (1975) Killer T cells in a Burkitt's lymphoma biopsy. Nature 225:405

    Google Scholar 

  46. Kirchner H (1984) Immunologic surveillance and human papilloma viruses. Immunology Today 5:272

    Google Scholar 

  47. Kirchner H, Chused TM, Herberman RB, Holden HT, Lavrin DH (1974) Evidence of suppressor cell activity in spleen of mice bearing primary tumors induced by Moloney Sarcoma Virus. J Exp Med 139:1473

    Article  CAS  PubMed  Google Scholar 

  48. Klein G, Sjögren HO (1960) Humoral and cellular factors in homograft and isograft immunity against sarcoma cells. Cancer Res 20:452

    Google Scholar 

  49. Klein E, Vánky F, Galili U, Vose BM, Fopp M (1980) Separation and characteristics of tumor-infiltrating lymphocytes in man. Contemp Top Immunobiol 10:79

    Google Scholar 

  50. Klein WR, Ruitenberg EJ, Steerenberg PA, De Jong WH, Kruizinga W, Misdorp W, Bier J, Tiesjema RH, Kreeftenberg JG, Teppema JS, Rapp HJ (1982) Immunotherapy by intralesional injection of BCG cell walls or live BCG in bovine ocular squamous cell carcinoma: a preliminary report. J Natl Cancer Inst 69:1095

    Google Scholar 

  51. Koneval T, Applebaum E, Popovic D, Gill L, Sisson G, Wood GW, Anderson B (1977) Demonstration of immunoglobulin in tumor and marginal tissues of squamous cell carcinomas of the head and neck. J Natl Cancer Inst 59:1089

    Google Scholar 

  52. Koren HS, Herberman RB (1983) Natural killing-present and future (Summary of workshop on natural killer cells). J Natl Cancer Inst 70:785

    Google Scholar 

  53. Levy PC, Shaw GM, LoBuglio AF (1979) Human monocyte, lymphocyte, and granulocyte antibody-dependent cell-mediated cytotoxicity toward tumor cells. J Immunol 123:594

    Google Scholar 

  54. Lewis MG, McCloy E, Blake J (1973) The significance of humoral antibodies in the localization of human malignant melanoma. Br J Surg 60:443

    Google Scholar 

  55. Lewis MG, Phillips TM, Rowden G (1978) Beneficial and detrimental effects of humoral immunity in malignancy. Pathobiol Annu 8:217

    Google Scholar 

  56. McKhann CF (1981) Tumor immunology. Past, present and future. Accomplishments in Cancer Res 125

  57. Minato M, Bloom BR, Jones C, Holland J, Reid LM (1979) Mechanism of rejection of virus persistently infected cells by athymic nude mice. J Exp Med 149:1117

    Google Scholar 

  58. Miyakoshi H, Koide H, Aoki T (1984) In vitro antibody-dependent cellular cytotoxicity against human T-cell leukemia/lymphoma virus (HTLV)-producing cells. Int J Cancer 33:287

    Google Scholar 

  59. Moore M, Vose BM (1981) Extravascular natural cytotoxicity in man — anti-K562 activity of lymph node and tumour-infiltrating lymphocytes. Int J Cancer 27:265

    Google Scholar 

  60. Mulé JJ, Forstrom JW, George E, et al. (1981) Production of T-cell lines with inhibitory or stimulatory activity against syngeneic tumors in vivo. A preliminary report. Int J Cancer 28:611

    Google Scholar 

  61. Murray JL, Lee LT (1984) Decreased monocyte antibody-dependent cell-mediated toxicity in stage I–II malignant melanoma. Augmentation by subcutaneous Corynebacterium parvum. Cancer Immunol Immunother 17:66

    Google Scholar 

  62. Nehlsen SL (1971) Prolonged administration of antithymocyte serum in mice. I. Observations on cellular and humoral immunity. Clin Exp Immunol 9:63

    Google Scholar 

  63. Nelson M, Nelson DS, Hopper KE (1981) Inflammation and tumor growth. I. Tumor growth in mice with depressed capacity to mount inflammatory responses: Possible role of macrophages. Am J Pathol 104:114

    Google Scholar 

  64. Nepom GT, Hellström H, Hellström KE (1983) Suppressor mechanisms in tumour immunity. Experientia 39:235

    Google Scholar 

  65. Paluch E, Ioachim LM (1978) Lung carcinoma-reactive antibodies isolated from tumor tissues and pleural effusions of lung cancer patients. J Natl Cancer Inst 61:319

    Google Scholar 

  66. Pearson GR, Neel HB, Weiland LH et al. (1984) Antibody-dependent cellular cytotoxicity and disease course in North American patients with nasopharyngeal carcinoma: a prospective study. Int J Cancer 33:777

    Google Scholar 

  67. Pels E, Den Otter W (1979) Natural cytotoxic macrophages in the peritoneal cavity of mice. Br J Cancer 40:856

    Google Scholar 

  68. Pels E, De Weger RA, Den Otter W (1984) Lymphocyte-induced macrophage cytotoxicity. Production of Specific Macrophage Arming Factor by sensitized Lyt 1+2+ T-lymphocytes. Int Arch Allergy Appl Immunol 74:140

    Google Scholar 

  69. Penn I, Halgrimson CG, Starzl TE (1971) De novo malignant tumors in organ transplant recipients. Transplant Proc 3:773

    Google Scholar 

  70. Piessens WF, Churchill W, Sharma SD (1981) On the killing of syngenic tumor cells by guinea pig macrophages activated in vitro with lymphocyte mediators. Lymphokines 3:293

    Google Scholar 

  71. Plata F, Sordat B (1977) Murine sarcoma virus (MSV)-induced tumors in mice. I. Distribution of MSV-immune cytolytic T lymphocytes in vivo. Int J Cancer 19:205

    Google Scholar 

  72. Puccetti P, Holden HT (1979) Cytolytic and cytostatic anti-tumor activities of macrophages from mice injected with murine sarcoma virus. Int J Cancer 23:123

    Google Scholar 

  73. Ran M, Witz IP (1972) Tumor-associated immunoglobulins. Enhancement of syngeneic tumors by IgG2-containing tumor eluates. Int J Cancer 9:242

    Google Scholar 

  74. Ran M, Landes E, Brenner HJ et al. (1974) Tumor-bound immunoglobulins: immunoglobulin coating human cancer cells. Correlation with pathological grading. Isr J Med Sci 10:642

    Google Scholar 

  75. Roder JC, Haliotis T (1980) Do NK cells play a role in anti-tumor surveillance? Immunology Today 1:96

    Google Scholar 

  76. Roder JC, Laing L, Haliotis T (1982) NK cells: fundamental aspects and role in cancer. In: Herberman RB (ed) Human cancer immunology vol 6. North Holland, Amsterdam

    Google Scholar 

  77. Rosenberg SA (1984) Immunotherapy of cancer by systemic administration of lymphoid cells plus interleukin-2. J Biol Response Mod 3:501

    Google Scholar 

  78. Rosenstein Y, Theelen M, Sánchez I, Celis E (1985) Isolation, purification, and characterization of a mouse plasmacytoma cell surface glycoprotein involved in the resistance of the tumor cells to immune destruction. J Natl Cancer Inst 74:609

    Google Scholar 

  79. Russell SW, Gillespie GY, Pace JL (1980) Evidence for mononuclear phagocytes in solid neoplasms and appraisal of their nonspecific cytotoxic capabilities. Contemp Top Immunobiol 10:143

    Google Scholar 

  80. Sanford BH, Hohn HI, Daly JJ, Soo SF (1973) Long-term spontaneous tumor incidence in neonatally thymectomized mice. J Immunol 110:1437

    Google Scholar 

  81. Schmidt JA, Mizel SB, Cohen D, Green I (1982) Interleukin-1, a potential regulator of fibroblast proliferation. J Immunol 128:2177

    Google Scholar 

  82. Shimizu K, Shen F-W (1979) Role of different T cell sets in the rejection of syngeneic chemically induced tumors. J Immunol 122:1162

    Google Scholar 

  83. Shu S, Steerenberg PA, Hunter JF, et al. (1981) Adoptive immunity to the guinea pig line-10 hepatoma and the nature of in vitro lymphoid-tumor cell interactions. Cancer Res 41:3499

    Google Scholar 

  84. Sjögren HO, Bansal SC (1971) Antigen in virally induced tumors. Prog Immunol 1:92

    Google Scholar 

  85. Sjögren HO, Hellström I, Bansal SC, et al. (1971) Suggestive evidence that the “blocking antibodies” of tumor bearing individuals may be antigen-antibody complexes. Proc Natl Acad Sci USA 68:1372

    Google Scholar 

  86. Stjernswärd J, Vánky F (1972) Stimulation of lymphocytes by autochthonous cancer. Nat Cancer Inst Monogr 35:237

    Google Scholar 

  87. Sullivan JL, Byron KS, Brewster FE, Purtilo DT (1980) Deficient natural killer cell activity in X-linked lymphoproliferative syndrome. Science 210:543

    Google Scholar 

  88. Talmadge JE, Meyers KM, Prieur DJ, Starkey JR (1980) Role of NK cells in tumor growth and metastasis in beige mice. Nature 284:622

    Google Scholar 

  89. Thunold S, Tønder O, Larsen O (1973) Immunoglobulins in eluates of malignant human tumors. Acta Pathol Microbiol Immunol Scand (A Suppl) 236:97

    Google Scholar 

  90. Timonen T, Ranki A, Saksela E, Häyry P (1979) Human natural cell-mediated cytotoxicity against fetal fibroblasts. Cell Immunol 48:121

    Google Scholar 

  91. Timonen T, Ortaldo JR, Herberman RB (1981) Characteristics of human large granular lymphocytes and relationship to natural killer and K-cells. J Exp Med 153:569

    Google Scholar 

  92. Trinchieri G, Matsumoto-Kobayashi M, Clark SC, Sechra J, London L, Perussia B (1984) Response of resting human peripheral blood natural killer cells to interleukin 2. J Exp Med 160:1147

    Google Scholar 

  93. Trowbridge IS (1983) Therapeutic potential of monoclonal antibodies that block biological function. In: Boss BD, Langman R, Trowbridge I, Dulbecco R (eds) Monoclonal Antibodies and Cancer. Academic Press, San Diego, p 53

    Google Scholar 

  94. Tsunawaki S, Oshima H, Mizuno D, Yamazaki M (1983) Induction of polymorphonuclear leukocyte-mediated cytolysis by wheat germ agglutinin and antitumor antibody. Gann 74:258

    Google Scholar 

  95. Vadas MA, Nicola NA, Metcalf D (1983) Activation of antibody-dependent cell-mediated cytotoxicity of human neutrophils and eosinophils by separate coloney stimulating factors. J Immunol 130:795

    Google Scholar 

  96. Vánky F, Trempe G, Klein E, Stjernswärd J (1975) Human tumor-lymphocyte interaction in vitro: blastogenesis correlated to detectable immunoglobulin in the biopsy. Int J Cancer 15:640

    Google Scholar 

  97. Van Loveren H, Den Otter W (1974) Macrophages in solid tumors. I. Immunologically specific effector cells. J Natl Cancer Inst 53:1057

    Google Scholar 

  98. Van Loveren H, Snoek M, Den Otter W (1982) Host macrophages are involved in systemic adoptive immunity against tumors. Experientia 38:488

    Google Scholar 

  99. Von Kleist S, Troupel S, King M, Burtin P (1977) A clinical comparison between non-specific cross-reacting antigen and CEA in patients' sera. Br J Cancer 35:875

    Google Scholar 

  100. Von Kleist S, King M, Huet C (1980) Evidence for membrane-bound antibodies directed against antigens expressed on tumors. Contemp Top Immunobiol 10:177

    Google Scholar 

  101. Vose BM, Vánky F, Argov S, Klein E (1977) Natural cytotoxicity in man: Activity of lymph node and tumor infiltrating lymphocytes. Eur J Immunol 7:753

    Google Scholar 

  102. Welsh RM (1978) Cytotoxic cells induced during lymphocyte choriomeningitis virus infection in mice. I. Characterization of natural killer cell induction. J Exp Med 148:163

    Google Scholar 

  103. Witz IP. (1973) The biological significance of tumour-bound immunoglobulins. Curr Top Microbiol Immunol 61:151

    Google Scholar 

  104. Zbar B, Bernstein I, Tanaka T (1970) Tumor immunity produced by the intradermal inoculation of living tumor cells and living Mycobacterium bovis (strain BCG). Science 170:1217

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Pathologisch Instituut, Pasteurstraat 2, 3511 HX, Utrecht, The Netherlands

    Willem Den Otter

Authors
  1. Willem Den Otter
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Den Otter, W. Immune surveillance and natural resistance: an evaluation. Cancer Immunol Immunother 21, 85–92 (1986). https://doi.org/10.1007/BF00199854

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00199854

Keywords

Search

Navigation