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. 1996 Jul;74(2):178–186. doi: 10.1038/bjc.1996.335

A serum-mediated mechanism for concomitant resistance shared by immunogenic and non-immunogenic murine tumours.

M Franco 1, O D Bustuoabad 1, P D di Gianni 1, A Goldman 1, C D Pasqualini 1, R A Ruggiero 1
PMCID: PMC2074564  PMID: 8688319

Abstract

Resistance of tumour-bearing mice to a second tumour challenge, that is concomitant resistance, was evaluated in euthymic and nude mice using nine tumours with widely different degrees of immunogenicity. Two temporally separate peaks of concomitant resistance were detected during tumour development. The first one was exhibited only by small immunogenic tumours; it was tumour specific and mediated by classical immunological T-cell-dependent mechanisms. The second peak was shared by both immunogenic and non-immunogenic large tumours; it was non-specific, thymus independent and correlated with the activity of a serum factor (neither antibody nor complement) that inhibited the in vitro proliferation of tumour cells. This factor was eluted from a Sephadex G-15 column at fractions corresponding to a molecular weight of approximately 1000 Da and it was recovered from a high-performance liquid chromatography column in one peak presenting maximum absorption at 215 and 266 nm. The data presented in this paper suggest for the first time, to our knowledge, that in spite of the differences between immunogenic and non-immunogenic tumours, a common serum-mediated mechanism seems to underlie the concomitant resistance induced by both types of tumours at late stages of tumour development.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Akporiaye E. T., Kudalore M., Stevenson A. P., Kraemer P. M., Stewart C. C. Isolation and reactivity of host effectors associated with the manifestation of concomitant tumor immunity. Cancer Res. 1988 Mar 1;48(5):1153–1158. [PubMed] [Google Scholar]
  2. Attia M. A., Weiss D. W. Immunology of spontaneous mammary carcinomas in mice. V. Acquired tumor resistance and enhancement in strain A mice infected with mammary tumor virus. Cancer Res. 1966 Aug;26(8):1787–1800. [PubMed] [Google Scholar]
  3. Belehradek J., Jr, Barski G., Thonier M. Evolution of cell-mediated antitumor immunity in mice bearing a syngeneic chemically induced tumor. Influence of tumor growth, surgical removal and treatment with irradiated tumor cells. Int J Cancer. 1972 May 15;9(3):461–469. doi: 10.1002/ijc.2910090302. [DOI] [PubMed] [Google Scholar]
  4. Berendt M. J., North R. J., Kirstein D. P. The immunological basis of endotoxin-induced tumor regression. Requirement for a pre-existing state of concomitant anti-tumor immunity. J Exp Med. 1978 Dec 1;148(6):1560–1569. doi: 10.1084/jem.148.6.1560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beutler B., Cerami A. Cachectin and tumour necrosis factor as two sides of the same biological coin. Nature. 1986 Apr 17;320(6063):584–588. doi: 10.1038/320584a0. [DOI] [PubMed] [Google Scholar]
  6. Bonfil R. D., Ruggiero R. A., Bustuoabad O. D., Meiss R. P., Pasqualini C. D. Role of concomitant resistance in the development of murine lung metastases. Int J Cancer. 1988 Mar 15;41(3):415–422. doi: 10.1002/ijc.2910410317. [DOI] [PubMed] [Google Scholar]
  7. Brunner K. T., Mauel J., Cerottini J. C., Chapuis B. Quantitative assay of the lytic action of immune lymphoid cells on 51-Cr-labelled allogeneic target cells in vitro; inhibition by isoantibody and by drugs. Immunology. 1968 Feb;14(2):181–196. [PMC free article] [PubMed] [Google Scholar]
  8. Chandradasa K. D. The development and specific suppression of concomitant immunity in two syngeneic tumour-host systems. Int J Cancer. 1973 May;11(3):648–662. doi: 10.1002/ijc.2910110316. [DOI] [PubMed] [Google Scholar]
  9. DeWys W. D. Studies correlating the growth rate of a tumor and its metastases and providing evidence for tumor-related systemic growth-retarding factors. Cancer Res. 1972 Feb;32(2):374–379. [PubMed] [Google Scholar]
  10. Deckers P. J., Davis R. C., Parker G. A., Mannick J. A. The effect of tumor size on concomitant tumor immunity. Cancer Res. 1973 Jan;33(1):33–39. [PubMed] [Google Scholar]
  11. Finlay-Jones J. J., Bartholomaeus W. N., Fimmel P. J., Keast D., Stanley N. F. Biologic and immunologic studies on a murine model of regional lymph node metastasis. J Natl Cancer Inst. 1980 Jun;64(6):1363–1372. [PubMed] [Google Scholar]
  12. Gorelik E. Resistance of tumor-bearing mice to a second tumor challenge. Cancer Res. 1983 Jan;43(1):138–145. [PubMed] [Google Scholar]
  13. Gorelik E., Segal S., Feldman M. On the mechanism of tumor "concomitant immunity". Int J Cancer. 1981 Jun 15;27(6):847–856. doi: 10.1002/ijc.2910270618. [DOI] [PubMed] [Google Scholar]
  14. Howell S. B., Dean J. H., Law L. W. Defects in cell-mediated immunity during growth of a syngeneic simian virus-induced tumor. Int J Cancer. 1975 Jan 15;15(1):152–169. doi: 10.1002/ijc.2910150118. [DOI] [PubMed] [Google Scholar]
  15. Kearney R., Nelson D. S. Concomitant immunity to syngeneic methylcholanthrene-induced tumours in mice. Occurrence and specificity of concomitant immunity. Aust J Exp Biol Med Sci. 1973 Dec;51(6):723–735. doi: 10.1038/icb.1973.70. [DOI] [PubMed] [Google Scholar]
  16. Keski-Oja J., Postlethwaite A. E., Moses H. L. Transforming growth factors in the regulation of malignant cell growth and invasion. Cancer Invest. 1988;6(6):705–724. doi: 10.3109/07357908809078038. [DOI] [PubMed] [Google Scholar]
  17. Kordon E., Lanari C., Molinolo A. A., Elizalde P. V., Charreau E. H., Dosne Pasqualini C. Estrogen inhibition of MPA-induced mouse mammary tumor transplants. Int J Cancer. 1991 Dec 2;49(6):900–905. doi: 10.1002/ijc.2910490617. [DOI] [PubMed] [Google Scholar]
  18. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  19. Leveson S. H., Howell J. H., Paolini N. S., Tan M. H., Holyoke E. D., Goldrosen M. H. Correlations between the leukocyte adherence inhibition microassay and in vivo tests of transplantation resistance. Cancer Res. 1979 Feb;39(2 Pt 2):582–586. [PubMed] [Google Scholar]
  20. Meiss R. P., Bonfil R. D., Ruggiero R. A., Pasqualini C. D. Histologic aspects of concomitant resistance induced by nonimmunogenic murine tumors. J Natl Cancer Inst. 1986 Jun;76(6):1163–1175. [PubMed] [Google Scholar]
  21. Nomi S., Naito K., Kahan B. D., Pellis N. R. Effects of concomitant and sinecomitant immunity on postsurgical metastasis in mice. Cancer Res. 1986 Dec;46(12 Pt 1):6111–6115. [PubMed] [Google Scholar]
  22. North R. J. The murine antitumor immune response and its therapeutic manipulation. Adv Immunol. 1984;35:89–155. doi: 10.1016/s0065-2776(08)60575-1. [DOI] [PubMed] [Google Scholar]
  23. O'Reilly M. S., Holmgren L., Shing Y., Chen C., Rosenthal R. A., Moses M., Lane W. S., Cao Y., Sage E. H., Folkman J. Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell. 1994 Oct 21;79(2):315–328. doi: 10.1016/0092-8674(94)90200-3. [DOI] [PubMed] [Google Scholar]
  24. Pasqualini C. D., Colmerauer M. E. Immunological enhancement of a murine allogeneic lymphoma. Medicina (B Aires) 1976 May-Jun;36(3):189–192. [PubMed] [Google Scholar]
  25. Pazos P., Lanari C., Meiss R., Charreau E. H., Pasqualini C. D. Mammary carcinogenesis induced by N-methyl-N-nitrosourea (MNU) and medroxyprogesterone acetate (MPA) in BALB/c mice. Breast Cancer Res Treat. 1992 Jan;20(2):133–138. doi: 10.1007/BF01834643. [DOI] [PubMed] [Google Scholar]
  26. Prehn R. T. Two competing influences that may explain concomitant tumor resistance. Cancer Res. 1993 Jul 15;53(14):3266–3269. [PubMed] [Google Scholar]
  27. Rao V. S., Bonavida B. Specific enhancement of tumor growth and depression of cell-mediated immunity following sensitization to soluble tumor antigens. Cancer Res. 1976 Apr;36(4):1384–1391. [PubMed] [Google Scholar]
  28. Rao V. S., Bonavida B., Zighelboim J., Fahey J. L. Preferential induction of serum blocking activity and enhancement of skin allograft by soluble alloantigen. Transplantation. 1974 Jun;17(6):568–575. doi: 10.1097/00007890-197406000-00004. [DOI] [PubMed] [Google Scholar]
  29. Ruggiero R. A., Bustuoabad O. D., Bonfil R. D., Meiss R. P., Pasqualini C. D. "Concomitant immunity" in murine tumours of non-detectable immunogenicity. Br J Cancer. 1985 Jan;51(1):37–48. doi: 10.1038/bjc.1985.6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ruggiero R. A., Bustuoabad O. D., Cramer P., Bonfil R. D., Pasqualini C. D. Correlation between seric antitumor activity and concomitant resistance in mice bearing nonimmunogenic tumors. Cancer Res. 1990 Nov 15;50(22):7159–7165. [PubMed] [Google Scholar]
  31. Tuttle R. L., Knick V. C., Stopford C. R., Wolberg G. In vivo and in vitro antitumor activity expressed by cells of concomitantly immune mice. Cancer Res. 1983 Jun;43(6):2600–2605. [PubMed] [Google Scholar]
  32. Vaage J. Influence of tumor antigen on maintenance versus depression of tumor-specific immunity. Cancer Res. 1973 Mar;33(3):493–503. [PubMed] [Google Scholar]
  33. WINN H. J. Immune mechanisms in homotransplantation. II. Quantitative assay of the immunologic activity of lymphoid cells stimulated by tumor homografts. J Immunol. 1961 Feb;86:228–239. [PubMed] [Google Scholar]
  34. Zahalka M. A., Okon E., Naor D. Blocking lymphoma invasiveness with a monoclonal antibody directed against the beta-chain of the leukocyte adhesion molecule (CD18). J Immunol. 1993 May 15;150(10):4466–4477. [PubMed] [Google Scholar]

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