Skip to main content
SpringerLink
Log in

Effect of splenectomy on hepatic metastasis of colon carcinoma and natural killer activity in the liver

  • Gastrointestinal Oncology
  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

We have previously demonstrated that administration of killed streptococcal preparation (OK432), a biological response modifier, increased the number of asialo GM1-positive cells in the liver, enhanced NK activity of hepatic mononuclear cells, and reduced the number of hepatic metastases of colon 38 adenocarcinoma that were inoculated into the superior mesenteric vein of C57BL/6 strain mice. In the present study, to clarify the role of the spleen in immune surveillance of the liver, the effect of splenectomy on hepatic metastasis of colon carcinoma and on hepatic NK activity has been examined. The number of hepatic metastasis increased in the splenectomized mice, compared with that in sham-operated mice. Administration of OK432 increased the number of asialo GM1-positive cells in the liver and enhanced NK activity of hepatic mononuclear cells in both groups, but NK activity of hepatic mononuclear cells in the splenectomized mice was less than that of the sham-operated mice. An enhanced NK activity of these cells was abolished by treatment with anti-asialo-GM1 antibody plus complementin vitro. Interleukin-2 mRNA expression was increased in the spleen 2 hr after OK432 administration and persisted until 8 hr, but was scarcely noted in the liver. On the other hand, NK activity of hepatic mononuclear cells in the asialo GM1-positive cell-depleted (previous administration of antiserum against asialo GM1) mice was enhanced after OK432 administration in the sham operated and splenectomized mice, but an enhanced NK activity in these mice was only partially or not at all abolished by treatment with anti-asialo GM1 antibody plus complementin vitro, respectively. These results suggest that the spleen could play an important role in an immune surveillance of the liver. In addition, OK432 first enhanced NK activity of hepatic mononuclear cells, which are sensitive to the antibody against asialo GM1. However, when asialo GM1-positive cells were depleted, OK432 enhanced NK activity of hepatic mononuclear cells, which are resistant to anti-asialo GM1 serum.

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.

Similar content being viewed by others

References

  1. Wisse E, van't Noordende JM, van der Meulen J, Daems WT: The pit cell: Description of a new type of cell occurring in rat liver sinusoids and peripheral blood. Cell Tissue Res 173:423–435, 1976

    PubMed  Google Scholar 

  2. Dan C, Kaneda K, Wake K: A striking increased in rod-cored vesicles in pit cells (natural killer cells) and augmentation of the liver-associated natural killer activity by a streptococcal preparation (OK432). Biomed Res 6:347–351, 1985

    Google Scholar 

  3. Kaneda K, Wake K: Distribution and morphological characteristics of the pit cells in the liver of the rat. Cell Tissue Res 233:485–505, 1983

    PubMed  Google Scholar 

  4. Kaneda K, Dan C, Wake K: Pit cells as natural killer cells. Biomed Res 4:567–576, 1983

    Google Scholar 

  5. Zarcone D, Prasthofer EF, Malavasi F, Pistoia V, LoBuglio AF, Grossi CE: Ultrastructural analysis of human natural killer cell activation. Blood 69:1725–1736, 1987

    PubMed  Google Scholar 

  6. Trinchieri G, Perussia B: Human natural killer cells: Biologic and pathologic aspects. Lab Invest 50:489–513, 1984

    PubMed  Google Scholar 

  7. Reynolds CW, Timonen T, Herberman RB: Natural killer (NK) cell activity in the rat. I. Isolation and characterization of the effector cells. J Immunol 127:282–287, 1981

    PubMed  Google Scholar 

  8. Wiltrout RH, Mathieson BJ, Talmadge JE, Reynolds CW, Zhang SR, Herberman RB, Ortaldo JR: Augmentation of organ-associated natural killer activity by biological response modifiers. Isolation and characterization of large granular lymphocytes from the liver. J Exp Med 160:1431–1449, 1984

    PubMed  Google Scholar 

  9. Wiltrout RH, Herberman R, Zhang SR, Chirigos MA, Ortaldo JR, Green KM, Talmadge JE: Role of organ-associated NK cells in decreased formation of experimental metastases in lung and liver. J Immunol 134:4267–4275, 1985

    PubMed  Google Scholar 

  10. Oshimi K, Kano S, Takaku K, Okumura K: Augmentation of mouse natural killer cell activity by a streptococcal preparation, OK-432. J Natl Cancer Inst 65:1265–1269, 1980

    PubMed  Google Scholar 

  11. Sakurai Y, Tsukagoshi S, Satoh H, Akiba T, Suzuki S, Yakagaki Y: Tumor-inhibitory effect of a streptococcal preparation (NSC-B116209) Cancer Chemother Rep 56:9–17, 1972

    PubMed  Google Scholar 

  12. Shiratori Y, Nakata R, Okano K, Komatsu Y, Shiina S, Kawase T, et al: Inhibition of hepatic metastasis of colon carcinoma by asialo GM1 positive cells in the liver. Hepatology 16:469–478, 1992

    PubMed  Google Scholar 

  13. Hood LE, Weissman IL, Wood WB: Immunology. Menlo Park; The Benjamin/Cummings Publishing Co., 1978

    Google Scholar 

  14. Kasai M, Iwamori M, Nagai Y, Okumura K, Tada T: A glycolipid on the surface of mouse natural killer cells. Eur J Immunol 10:175–180, 1980

    PubMed  Google Scholar 

  15. Habu S, Fukui H, Shimamura K, Kasai M, Nagai Y, Okumura K, Tamaoki N:In vivo effect of anti-asialo GM1. 1. Reduction of NK activity and enhancement of transplanted tumor growth in nude mice. J Immunol 127:34–38, 1981

    PubMed  Google Scholar 

  16. Corbett TH, Griswold DP, Roberts BJ, Peckham JC, Schabel FM: Tumor induction relationships in development of transplantable cancers of the colon in mice for chemotherapy assays, with a note on carcinogen structure. Cancer Res 35:2434–2439, 1975

    PubMed  Google Scholar 

  17. Freudenberg N, Schalk J, Galanos C, Katshinski T, Datz O, Pein U, Freudenberg MA: Identification and percentage frequency of isolated non-parenchymal liver cells (NPLC) in the mouse. Virchows Arch B Cell Pathol 57:109–115, 1989

    Google Scholar 

  18. Hsu SM, Raine L, Fanger H: Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques. J Histochem Cytochem 29:577–580, 1981

    PubMed  Google Scholar 

  19. Chomczynski P, Sacchi N: Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:155–159, 1987

    Google Scholar 

  20. Kashima N, Nishi-Takaoka C, Fujita T, Taki S, Yamada G, Hamuro J, Taniguchi T: Unique structure of murine interleukin-2 as deduced from cloned cDNAs. Nature 313:402–404, 1985

    PubMed  Google Scholar 

  21. Thurnherr N, Deschner EE, Stonehill EH, Lipkin M: Induction of adenocarcinoma of the colon in mice by weekly injections of 1,2-dimethylhydrazine. Cancer Res 33:940–945, 1973

    PubMed  Google Scholar 

  22. Rosenberg SA, Spiess P, Lafreniere R: A new approach to the adoptive immunotherapy of cancer with tumor-infiltrating lymphocytes. Science 233:1318–1321, 1986

    PubMed  Google Scholar 

  23. Gallinger S, Hoskin DW, Mullen JBM, Wong AHC, Roder JC: Comparison of cellular immunotherapies and anti-CD3 in the treatment of MCA-38-LD experimental hepatic metastasis in C57BL/6 mice. Cancer Res 50:2476–2480, 1990

    PubMed  Google Scholar 

  24. Sato M, Narisawa T, Sano M, Takahashi T, Goto A: Growth inhibition of transplantable murine colon adenocarcinoma 38 by indomethacin. J Cancer Res Clin Oncol 106:21–26, 1983

    Google Scholar 

  25. Plowman J, Narayanan VL, Dykes D, Szarvasi E, Briet P, Yoder OC, Paul KD: Flavone acetic acid: A novel agent with preclinical antitumor activity against colon adenocarcinoma 38 in mice. Cancer Treat Rep 70:631–635, 1986

    PubMed  Google Scholar 

  26. Thomsen LL, Ching LM, Baguley BC: Evidence for the production of nitric oxide by activated macrophages treated with the antitumor agents flavone-8-acetic acid and xanthenone-4-acetic acid. Cancer Res 50:6966–6970, 1990

    PubMed  Google Scholar 

  27. Basse P, Herberman RB, Nannmark U, Johansson BR, Hokland M, Wasserman K, Goldfarb RH: Accumulation of adoptively transferred adherent, lymphokine-activated killer cells in murine metastasis. J Exp Med 174:479–488, 1991

    PubMed  Google Scholar 

  28. Basse PH, Nannmark U, Johansson BR, Herberman RB, Goldfarb RH: Establishment of cell-to-cell contact by adoptively transferred adherent lymphokine-activated killer cells with metastatic murine melanoma cells. J Natl Cancer Inst 83:944–950, 1991

    PubMed  Google Scholar 

  29. Smithson G, Bittick TH, Chervenak R, Lee SJ, Wolcott RM: The role of NK cells in the regulation of experimental metastasis in a murine lymphoma system. J Leukocyte Biol 49:621–629, 1991

    PubMed  Google Scholar 

  30. Hart IR, Talmadge JE, Fidler IJ: Metastatic behavior of a murine reticulum cell sarcoma exhibiting organ-specific growth. Cancer Res 41:1281–1287, 1981

    PubMed  Google Scholar 

  31. Cohen SA, Salazar D, von Muenchhausen W, Werner-Wasik M, Nolan JP: Natural antitumor defense system of the murine liver. Leukocyte Biol 37:559–569, 1985

    Google Scholar 

  32. Bouwens L, Wisse E: Tissue localization and kinetics of pit cells or large granular lymphocytes in the liver of rats treated with biological response modifiers. Hepatology 8:46–52, 1988

    PubMed  Google Scholar 

  33. Reynolds CW, Denn AC III, Barlozzari T, Wiltrout RH, Reichardt DA, Herberman RB: Natural killer activity in the rat. IV. distribution of large granular lymphocytes (LGL) following intravenous and intraperitoneal transfer. Cell Immunol 86:371–380, 1984

    PubMed  Google Scholar 

  34. Rolstad B, Herberman RB, Reynolds CW: Natural killer activity in the rat. V. The circulation patterns and tissue localization of peripheral blood large granular lymphocytes (LGL). J Immunol 136:2800–2808, 1986

    PubMed  Google Scholar 

  35. Bouwens L, Remels L, Baekeland M, van Bossuyt H, Wisse E: Large granular lymphocytes or “pit cells” from rat liver: Isolation, ultrastructural characterization and natural killer activity. Eur J Immunol 17:37–42, 1987

    PubMed  Google Scholar 

  36. Bouwens L, Wisse E: Immune-electron microscopic characterization of large granular lymphocytes (natural killer cells) from rat liver. Eur J Immunol 17:1423–1428, 1987

    PubMed  Google Scholar 

  37. Vanderkerken K, Bouwens L, Wisse E: Heterogeneity and differentiation of pit cells or large granular lymphocytes of the rats.In Cells of the Hepatic Sinusoid, Vol 2. E Wisse, DL Knook, K Decker (eds). Rijweijk; Kupffer Cell Foundation, 1989; pp 456–461

    Google Scholar 

  38. Leung KH, Salazar D, Ip MM, Cohen SA: Characterization of natural cytotoxic effector cells isolated from rat liver. Nat Immun Cell Growth Regul 6:150–160, 1987

    PubMed  Google Scholar 

  39. Lukomska B, Olszewski WL, Engeset A: Rat liver contains a distinct blood-borne population of NK cells resistent to antiasialo-GM1 antiserum. Immunol Lett 6:277–281, 1983

    PubMed  Google Scholar 

  40. Saito M, Ichimura O, Kataoka M, Moriya Y, Ueno K, Sugawara Y, Nanjo M, Ishida N: Pronounced antitumor effect of LAK-like cells induced in the peritoneal cavity of mice after intraperitoneal injection of OK432, a killed streptococcal preparation. Cancer Immunol Immunother 22:161–168, 1986

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Gastroenterology, Institute of Adult Disease, Asahi Life Foundation, 1-9-14 Nishi-Shin' juku, Shinjuku-ku, Tokyo, Japan

    Yasushi Shiratori MD, Tateo Kawase, Ryo Nakata, Mitsugu Tanaka, Yohko Hikiba, Ken 'Ichi Okano, Masayuki Matsumura, Yasuro Niwa, Yutaka Komatsu, Shuichiro Shiina & Masao Omato

  2. Department of Pathology, Jikei University School of Medicine, 3-25-8 Nishi-Shinbashi, Minato-ku, Tokyo, Japan

    Yasushi Shiratori MD, Tateo Kawase, Ryo Nakata, Mitsugu Tanaka, Yohko Hikiba, Ken 'Ichi Okano, Masayuki Matsumura, Yasuro Niwa, Yutaka Komatsu, Shuichiro Shiina & Masao Omato

  3. 2nd Department of Internal Medicine, Faculty of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, 113, Tokyo, Japan

    Yasushi Shiratori MD, Tateo Kawase, Ryo Nakata, Mitsugu Tanaka, Yohko Hikiba, Ken 'Ichi Okano, Masayuki Matsumura, Yasuro Niwa, Yutaka Komatsu, Shuichiro Shiina & Masao Omato

Authors
  1. Yasushi Shiratori MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tateo Kawase
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ryo Nakata
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mitsugu Tanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yohko Hikiba
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ken 'Ichi Okano
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Masayuki Matsumura
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yasuro Niwa
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yutaka Komatsu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Shuichiro Shiina
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Masao Omato
    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

Shiratori, Y., Kawase, T., Nakata, R. et al. Effect of splenectomy on hepatic metastasis of colon carcinoma and natural killer activity in the liver. Digest Dis Sci 40, 2398–2406 (1995). https://doi.org/10.1007/BF02063244

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02063244

Key words

Search

Navigation