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Biological properties associated with the enhanced lung-colonizing potential in a B16 murine melanoma line grown in a medium conditioned by syngeneic Corynebacterium parvum-elicited macrophages

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Abstract

A previous study by our laboratory showed that the peritoneal murine Corynebacterium parvum-elicited macrophages released into their growth medium an activity which enhanced the ability of B16-F10 melanoma cells to form experimental metastases in the lung of syngeneic mice. In the present study, we used a clone of B16-F10 line (F10-M3 cells) to investigate whether the increase in lung-colonizing potential due to the pro-clonogenic activity released by C. parvum-elicited macrophages was associated with biological properties characteristic of a metastatic phenotype. We have found that the pulmonary retention, growth rate in lung parenchyma, invasiveness through Matrigel, adhesiveness to IL-1-activated endothelium and MHC class I expression were increased in F10-M3 cells stimulated by the macrophage pro-clonogenic activity. By using an in vitro experimental protocol, the enhancement of lung-colonizing potential in the stimulated melanoma cells turned out to be a transient phenomenon as was the increase of invasiveness through Matrigel and the higher expression of MHC class I antigens. In conclusion, the melanoma cells stimulated by the pro-clonogenic activity released by C. parvum-elicited macrophages showed changes in biological parameters which are relevant to metastatic diffusion. These changes appeared as a temporary phenomenon which sustains the view that the metastatic phenotype represents a transient biological character influenced by host factors.

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References

  1. Nicolson GL. Tumor cell instability, diversification, and progression to the metastatic phenotype: From oncogene to oncofetal expression. Cancer Res 1987; 47: 1473–87.

    PubMed  CAS  Google Scholar 

  2. Nicolson GL. Cancer progression and growth: Relationship of paracrine and autocrine growth mechanisms to organ preference of metastasis. Exp Cell Res 1993; 204: 171–80.

    Article  PubMed  CAS  Google Scholar 

  3. Welch DR, Schissel DJ, Howrey RP et al. Tumor-elicited polymorphonuclear cells, in contrast to ‘normal’ circulating polymorphonuclear cells, stimulate invasive and metastatic potentials of rat mammary adenocarcinoma cells. Proc Natl Acad Sci USA 1989; 86: 5859–63.

    Article  PubMed  CAS  Google Scholar 

  4. Dabbous MK, North SM, Haney L et al. Macrophage and lymphocyte potentiation of syngeneic tumor cell and host fibroblast collagenolytic activity in rats. Cancer Res 1988; 48: 6832–6.

    PubMed  CAS  Google Scholar 

  5. Tanaka H, Mori Y, Ishii H et al. Enhancement of metastatic capacity of fibroblast-tumor cell interaction in mice. Cancer Res 1988; 48: 1456–9.

    PubMed  CAS  Google Scholar 

  6. Grégorie M, Liebeau B. The role of fibroblasts in tumor behavior. Cancer Metastasis Rev 1995; 14: 339–50.

    Article  Google Scholar 

  7. van Roozendaal KEP, Klijn JGM, van Ooijen B et al. Differential regulation of breast tumor cells proliferation by stromal fibroblasts of various breast tissue sources. Int J Cancer 1996; 65: 120–5.

    Article  PubMed  CAS  Google Scholar 

  8. Dabbous MK, North SM, Haney L et al. Effects of mast cellmacrophage interactions on the production of collagenolytic enzymes by metastatic tumor cells and tumor-derived and stromal fibroblasts. Clin Exp Metastasis 1995; 13: 33–41.

    Article  PubMed  CAS  Google Scholar 

  9. Alexander P. The functions of the macrophage in malignant disease. Annu Rev Med 1976; 27: 207–24.

    Article  PubMed  CAS  Google Scholar 

  10. Fidler IJ, Schroit AJ. Recognition and destruction of neoplastic cells by activated macrophages: discrimination of altered self. Biochim Biophys Acta 1998; 948: 151–73.

    Google Scholar 

  11. Whitworth PW, Pak CC, Esgro J et al. Macrophages and cancer. Cancer Metastasis Rev 1989/1990; 8: 319–51.

    Google Scholar 

  12. Mantovani A. Effects on in vitro tumor growth of murine macrophages isolated from sarcoma lines differing in immunogenicity and metastasizing capacity. Int J Cancer 1978; 22: 741–6.

    PubMed  CAS  Google Scholar 

  13. Evans R. Macrophage requirement for growth of a murine fibrosarcoma. Br J Cancer 1978; 37: 1086–9

    PubMed  CAS  Google Scholar 

  14. Gabizon A, Leibovich SJ, Goldman R. Contrasting effects of activated and nonactivated macrophages and macrophages from tumor-bearing mice on tumor growth in vivo. J Natl Cancer Inst 1980; 65: 913–20.

    PubMed  CAS  Google Scholar 

  15. Kadhim SA, Rees RC. Enhancement of tumor growth in mice: Evidence for the involvement of host macrophages. Cell Immunol 1984; 87: 259–69.

    Article  PubMed  CAS  Google Scholar 

  16. De Baetselier P, Kapon A, Katzav S et al. Selecting, accelerating and suppressing interactions between macrophages and tumor cells. Invasion Metastasis 1985; 5: 106–24.

    PubMed  CAS  Google Scholar 

  17. Gorelik E, Wiltrout RH, Brunda MJ et al. Augmentation of metastasis formation by thioglycollate-elicited macrophages. Int J Cancer 1982; 29: 575–81.

    PubMed  CAS  Google Scholar 

  18. Mashiba H, Matsunaga K. Inhibition and augmentation of lymphoma metastasis by adoptively transferred peritoneal macrophages in hamster. Cancer Lett 1986; 33: 11–8.

    Article  PubMed  CAS  Google Scholar 

  19. Mukai M, Shinkai K, Tateishi R et al. Macrophage potentiation of invasive capacity of rat ascites hepatoma cells. Cancer Res 1987; 47: 2167–71.

    PubMed  CAS  Google Scholar 

  20. Akedo H, Shinkai K, Mukai M et al. Potentiation and inhibition of tumor cell invasion by host cells and mediators. Invasion Metastasis 1989; 9: 134–48.

    PubMed  CAS  Google Scholar 

  21. Cecconi O, Calorini L, Mannini A et al. Enhancement of lungcolonizing potential of murine tumor cell lines co-cultivated with activated macrophages. Clin Exp Metastasis 1997; 15: 94–101.

    Article  PubMed  CAS  Google Scholar 

  22. Fidler IJ. Biological behavior of malignant melanoma cells correlated to their survival in vivo. Cancer Res 1975; 35: 218–24.

    PubMed  CAS  Google Scholar 

  23. Liotta LA, Vembu D, Saini RK et al. In vivo monitoring of the death rate of artificial murine pulmonary micrometastases. Cancer Res 1978; 38: 1231–6.

    PubMed  CAS  Google Scholar 

  24. Pauli BU, Augustin V, el Sabban ME et al. Organ-preference of metastasis. The role of endothelial cell adhesion molecules. Cancer Metastasis Rev 1990; 9: 175–89.

    Article  PubMed  CAS  Google Scholar 

  25. Zetter BR. The cellular basis of site-specific tumor metastasis. N Engl J Med 1990; 322: 605–12.

    Article  PubMed  CAS  Google Scholar 

  26. Mignatti P, Rifkin DB. Biology and biochemistry of proteinases in tumor invasion. Physiol Rev 1993; 73: 161–95.

    PubMed  CAS  Google Scholar 

  27. Liotta LA, Tryggvason K, Garbisa S et al. Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 1980; 284: 67–8.

    Article  PubMed  CAS  Google Scholar 

  28. Stetler-Stevenson WG, Aznavoorian S, Liotta LA. Tumor cell interactions with the extracellular matrix during invasion and metastasis. Ann Rev Cell Biol 1993; 9: 541-73.

    PubMed  CAS  Google Scholar 

  29. Miller FR, Heppner GH. Cellular interactions in metastasis. Cancer Metastasis Rev 1990; 9: 21–34.

    Article  PubMed  CAS  Google Scholar 

  30. Gopas J, Rager-Zisman B, Bar-Eli M et al. The relationship between MHC antigen expression and metastasis. Adv Cancer Res 1989; 53: 89–115.

    PubMed  CAS  Google Scholar 

  31. Gattoni-Celli S, Calorini L, Simile MM et al. Modulation by MHC Class I antigens of the biology of melanoma cells. Nonimmunological mechanisms. Melanoma Res 1993; 3: 285–9.

    CAS  Google Scholar 

  32. Chen TR. In situ detection of Mycoplasma contamination in cell cultures by fluorescent Hoechst 33258 stain. Exp Cell Res 1977; 104: 255–62.

    Article  PubMed  CAS  Google Scholar 

  33. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem 1959; 37: 911–7.

    Article  PubMed  CAS  Google Scholar 

  34. Mannori G, Crottet P, Cecconi O et al. Differential colon cancer cell adhesion to E-, P-, and L-selectin: Role of mucine-type glycoproteins. Cancer Res 1995; 55: 4425–31.

    PubMed  CAS  Google Scholar 

  35. Albini A, Iwamoto Y, Kleinman, HK et al. A rapid in vitro assay for quantitating the invasive potential of tumor cells. Cancer Res 1987; 47: 3239–45.

    PubMed  CAS  Google Scholar 

  36. Nicolson GL, Dulski KM. Organ specificity of metastatic tumor colonization is related to organ-selective growth properties of malignant cells. Int J Cancer 1986; 38: 289–94.

    PubMed  CAS  Google Scholar 

  37. Rossi MC, Zetter BR. Selective stimulation of prostatic carcinoma cell proliferation by transferrin. Proc Natl Acad Sci USA 1992; 89: 6197–201.

    Article  PubMed  CAS  Google Scholar 

  38. Menter DG, Herrman JL, Nicolson GL. The role of trophic factors and autocrine/paracrine growth factors in brain metastasis. Clin Exp Metastasis 1995; 13: 67–88.

    Article  PubMed  CAS  Google Scholar 

  39. Huijzer JC, Uhlenkott CE, Meadows GG. Differences in expression of metalloproteinases and plasminogen activators in murine melanocytes and B16 melanoma variants: lack of association with in vitro invasion. Int J Cancer 1995; 63: 92–9.

    PubMed  CAS  Google Scholar 

  40. Okahara H, Yagita H, Miyake K et al. Involvement of very late activation antigen 4 (VLA-4) and vascular cell adhesion molecule 1 (VCAM-1) in Tumor Necrosis Factor ? enhancement of experimental metastasis. Cancer Res 1994; 54: 3233–6.

    PubMed  CAS  Google Scholar 

  41. Garofalo A, Chirivi RGS, Foglieni C et al. Involvement of the very late antigen 4 integrin on melanoma in interleukin 1-augmented experimental metastases. Cancer Res 1995; 55: 414–9.

    PubMed  CAS  Google Scholar 

  42. Cordon-Cardo C, Fuks Z, Drobnjak M et al. Expression of HLAA, B,C antigens on primary and metastatic tumor cell populations of human carcinomas. Cancer Res 1991; 51: 6372 80.

    PubMed  Google Scholar 

  43. Pantel K, Schlimok G, Schaller G et al. Frequent down-regulation of major histocompatibility class I antigen expression on individual micrometastatic carcinoma cells. Cancer Res 1991; 51: 4712–5.

    PubMed  CAS  Google Scholar 

  44. Garrido F, Cabrera T, Lopez-Nevot AM et al. HLA class I antigens in human tumors. Adv Cancer Res 1995; 67: 155–95.

    Article  PubMed  CAS  Google Scholar 

  45. De Baetselier P, Katzav S, Gorelik E et al. Differential expression of H-2 gene products in tumour cells is associated with their metastatogenic properties. Nature 1980; 288: 179–81.

    Article  PubMed  CAS  Google Scholar 

  46. Katzav S, Segal S, Feldman M. Immuno-selection in vivo of H-2D phenotypic variants from a metastatic clone of sarcoma cells results in cell lines of altered metastatic competence. Int J Cancer 1984; 33: 407–15

    PubMed  CAS  Google Scholar 

  47. Taniguchi K, Karre K, Klein G. Lung colonization and metastasis by disseminated B16 melanoma cells: H-2 associated control at the level of the host and the tumor cell. Int J Cancer 1985; 36: 503–10.

    PubMed  CAS  Google Scholar 

  48. Kawano Y-I, Taniguchi K, Toshitani A et al. Synergistic defense system by cooperative natural effectors against metastasis of B16 melanoma cells in H-2-associated control: different behavior of H-2+ and H-2¯ cells in metastatic process. J Immunol 1986; 136: 4729–34.

    PubMed  CAS  Google Scholar 

  49. Piontek G, Taniguchi K, Ljunggren H et al. YAC-1 MHC class I variants reveal association between decreased NK sensitivity and increased H-2 expression after interferon treatment or in vivo passage. J Immunol 1985; 135: 4281–8.

    PubMed  CAS  Google Scholar 

  50. Storkus WJ, Alexander J, Payne JA et al. Reversal of natural killing susceptibility in target cells expressing transfected class I HLA genes. Proc Natl Acad Sci USA 1989; 86: 2361–4.

    Article  PubMed  CAS  Google Scholar 

  51. Hanna N, Fidler IJ. Role of natural killer cells in the destruction of circulating tumor emboli. J Natl Cancer Inst 1980; 65: 801–9.

    PubMed  CAS  Google Scholar 

  52. Hanna N, Burton RC. Definitive evidence that natural killer (NK) cells inhibit experimental tumor metastasis in vivo. J Immunol 1981; 127: 1754–8.

    PubMed  CAS  Google Scholar 

  53. Gorelik E, Wiltrout RH, Okumura K et al. Role of NK cells in the control of metastatic spread and growth of tumor cells in mice. Int J Cancer 1982; 30: 107–12.

    PubMed  CAS  Google Scholar 

  54. Wiltrout RH, Herberman RB, Zhang S-R et al. Role of organassociated NK cells in decreased formation of experimental metastases in lung and liver. J Immunol 1985; 134: 4267–75.

    PubMed  CAS  Google Scholar 

  55. McMillan TJ, Rao J, Everett CA et al. Interferon-induced alterations in metastatic capacity, class-1 antigen expression and natural killer cell sensitivity of melanoma cells. Int J Cancer 1987; 40: 659–63.

    PubMed  CAS  Google Scholar 

  56. Zoller M, Strubel A, Hammerling G et al. Interferon-gamma treatment of B16 melanoma cells: Opposing effects for non-adaptive and adaptive immune defense and its reflection by metastatic spread. Int J Cancer 1988; 41: 256–66.

    PubMed  CAS  Google Scholar 

  57. Lollini PL, De Giovanni C, Nicoletti G et al. Enhancement of experimental metastatic ability by tumor necrosis factor-alpha alone or in combination with interferon-gamma. Clin Exp Metastasis 1990; 8: 215–24

    Article  PubMed  CAS  Google Scholar 

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Calorini, L., Mannini, A., Bianchini, F. et al. Biological properties associated with the enhanced lung-colonizing potential in a B16 murine melanoma line grown in a medium conditioned by syngeneic Corynebacterium parvum-elicited macrophages. Clin Exp Metastasis 17, 889–895 (1999). https://doi.org/10.1023/A:1006783431599

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