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Spontaneous development of functionally active long-term monocytelike cell lines from channel catfish

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Summary

During the course of studies involving the in vitro manipulation of channel catfish peripheral blood leukocytes, spontaneous proliferation was observed with unexpectedly high frequency. Propagation of these spontaneously proliferating cells has resulted in the development of long-term (>11 mo.) cell lines which stain positively for nonspecific esterase and peroxidase, are phagocytic for latex beads, and morphologically resemble mammalian monocytes or macrophages. These long-term cell lines also exhibit two important additional functional features. First, induction with lipopolysaccharide results in the secretion of relatively high levels of catfish high and low molecular weight species of interleukin-1 active on channel catfish and mouse T cells, respectively. Second, these cell lines are efficient antigen-presenting cells to autologous peripheral blood leukocytes for antigen specific in vitro proliferative and antibody responses. This antigen-presenting function is blocked by inhibitors known to prevent antigen processing and presentation by mammalian monocytes. Allogeneic mixtures of cell line (used as antigen-presenting cells) and responding peripheral blood leukocytes, however, resulted in strong mixed leukocyte reaction but not in specific antibody responses. The availability of such cell lines should facilitate further studies on accessory cell functions in fish immune responses.

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References

  1. Berzofsky, J. A.; Ozaki, S. Antibody conjugates mimic specific B-cell presentation of antigen: epitope restrictions in specific T-B interaction. In: Schook, L. B.; Tew, J. G., eds. Antigen presenting cells: diversity, differentiation and regulation. New York: Alan R. Liss Inc.; 1988:41–48.

    Google Scholar 

  2. Bird, R. C.; Nusbaum, K. E.; Screws, E. A., et al. Molecular cloning of fragments of the channel catfish virus (Herpesviridae) genome and expression of encoded mRNA during infection. Am. J. Vet. Res. 49:1850–1855; 1988.

    PubMed  CAS  Google Scholar 

  3. Blum, J. S.; Creswell, P. Role for intracellular proteases in the processing and transport of class II HLA antigens. Proc. Natl. Acad. Sci. USA 85:3975–3979; 1988.

    Article  PubMed  CAS  Google Scholar 

  4. Bly, J. E.; Miller, N. W.; Clem, L. W. A monoclonal antibody for neutrophils in normal and stressed channel catfish. Dev. Comp. Immunol. 14:211–221; 1990.

    Article  PubMed  CAS  Google Scholar 

  5. Breazile, J. E.; Mass, H. J.; Wollscheid, J., et al. A light and electron microscopic study of the leukocytes of channel catfish (Ictalurus punctatus). Zbl. Vet. Med. C. Anat. Histol. Embryol. 11:107–116; 1982.

    CAS  Google Scholar 

  6. Cannon, M. S.; Mollenhauer, H. H.; Eurell, T. E., et al. An ultrastructural study of the leukocytes of the channel catfishIctalurus punctatus. J. Morphol. 164:1–23; 1980.

    Article  Google Scholar 

  7. Clem, L. W.; Sizemore, R. C.; Ellsaesser, C. F., et al. Monocytes as accessory cells in fish immune responses. Dev. Comp. Immunol. 9:803–809; 1985.

    Article  PubMed  CAS  Google Scholar 

  8. Ellsaesser, C. F.; Miller, N. W.; Lobb, C. J., et al. A new method for the cytochemical staining of cells immobilized in agarose. Histochemistry 80:559–562; 1984.

    PubMed  CAS  Google Scholar 

  9. Ellsaesser, C. F. Isolation and characterization of channel catfish high and low molecular weight species of interleukin-1. Jackson, MS: Univ. Mississippi Medical Center; 1990. Thesis.

    Google Scholar 

  10. Ellsaesser, C. F.; Miller, N. W.; Cuchens, M. A., et al. Analysis of channel catfish peripheral blood leukocytes by brightfield microscopy and flow cytometry. Trans. Am. Fish. Soc. 114:271–277; 1985.

    Article  Google Scholar 

  11. Faulman, E.; Cuchens, M. A.; Lobb, C. J., et al. An effective culture system for studying in vitro mitogenic responses of channel catfish lymphocytes. Trans. Am. Soc. Fish. 112:673–679; 1983.

    Article  Google Scholar 

  12. Garrett, L. R.; Bost, K. L.; Buttke, T. M., et al. Changes in the DNA of lymphocytes from pristane-treated rats. Agents Actions 20:104–112; 1987.

    Article  PubMed  CAS  Google Scholar 

  13. Gillis, S.; Scheid, M.; Watson, J. Biochemical and biologic characterization of lymphocyte regulatory molecules. III. The isolation and phenotypic characterization of interleukin-2 producing T cell lymphomas. J. Immunol. 125:2570–2578; 1980.

    PubMed  CAS  Google Scholar 

  14. Gillis, S.; Ferou, M. M.; You, W., et al. T cell growth factor: parameters of production and a quantitative microassay for activity. J. Immunol. 120:2027–2032; 1978.

    PubMed  CAS  Google Scholar 

  15. Gillis, S.; Mizel, S. B. T-cell lymphoma model for the analysis of interleukin-1 mediated T-cell activation. Proc. Natl. Acad. Sci. USA 78:1133–1137; 1981.

    Article  PubMed  CAS  Google Scholar 

  16. Glimcher, L. H.; Kim, K. J.; Green, I., et al. Ia antigen-bearing B cell tumor lines can present protein antigen and alloantigen in a major histocompatibility complex-restricted fashion to antigen-reactive T cells. J. Exp. Med. 155:445–459; 1982.

    Article  PubMed  CAS  Google Scholar 

  17. Gronowicz, E. S.; Doss, C. A.; Howard, F. D., et al. An in vitro line of B cell tumor BCL1 can be activated by LPS to secrete IgM. J. Immunol. 125:976–980; 1980.

    PubMed  CAS  Google Scholar 

  18. Hayhoe, F. G. H.; Flemans, R. J. Color atlas of hematological cytology, 2nd ed. New York: John Wiley & Sons; 1982.

    Google Scholar 

  19. Hoffman, R. A.; Kung, P. C.; Hansen, W. P., et al. Simple and rapid measurement of human T lymphocytes and their subclasses in the peripheral blood. Proc. Natl. Acad. Sci. USA 77:4914–4917; 1980.

    Article  PubMed  CAS  Google Scholar 

  20. Horibata, K.; Harris, A. W. Mouse myelomas and lymphomas in culture. Exp. Cell Res. 60:61–77; 1970.

    Article  PubMed  CAS  Google Scholar 

  21. Kohler, G.; Milstein, C. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 256:495–497; 1971.

    Article  Google Scholar 

  22. Koren, H. S.; Handwerger, B. S.; Wunderlich, J. R. Identification of macrophage-like characteristics in a cultured murine tumor line. J. Immunol. 114:894–897; 1975.

    PubMed  CAS  Google Scholar 

  23. Kripke, M. L.; Weiss, D. W. Studies on the immune responses of BALB/c mice during tumor induction by mineral oil. Int. J. Cancer 6:422–430; 1970.

    Article  PubMed  CAS  Google Scholar 

  24. Lechler, R. I.; Lombardi, G.; Batchelor, J. R., et al. The molecular basis of alloreactivity. Immunol. Today 11:83–88; 1990.

    Article  PubMed  CAS  Google Scholar 

  25. Lepe-Zuniga, J. L.; Zigler, J. S.; Zimmerman, M. L., et al. Differences between intra- and extracellular interleukin-1. Mol. Immunol. 221:1387–1392; 1985.

    Article  Google Scholar 

  26. Machamer, C. E.; Creswell, P. Monensin prevents terminal glycosylation ofN- andO-linked oligosaccharides of the HLA-DR associated invariant chain and inhibits its dissociation from theα-β chain complex. Proc. Natl. Acad. Sci. USA 81:1287–1291; 1984.

    Article  PubMed  CAS  Google Scholar 

  27. Mahajan, C. L.; Dheer, J. M. S. An autoradiographic and cytochemical study of erythropoeisis inChanna punctatus. J. Fish Biol. 17:641–648; 1980.

    Article  CAS  Google Scholar 

  28. Miller, N. W.; Sizemore, R. C.; Clem, L. W. Phylogeny of lymphocyte heterogeneity: the cellular requirements for in vitro antibody responses of channel catfish leukocytes. J. Immunol. 134:2884–2888; 1985.

    PubMed  CAS  Google Scholar 

  29. Miller, N. W.; Bly, J. E.; van Ginkel, F., et al. Phylogeny of lymphocyte heterogeneity: Identification and separation of functionally distinct subpopulations of channel catfish lymphocytes with monoclonal antibodies. Dev. Comp. Immunol. 11:739–747; 1987.

    Article  PubMed  CAS  Google Scholar 

  30. Miller, N. W.; Deuter, A.; Clem, L. W. Phylogeny of lymphocyte heterogeneity: the cellular requirement for the mixed leucocyte reaction with channel catfish. Immunology 59:123–128; 1986.

    PubMed  CAS  Google Scholar 

  31. Miller, N. W.; Clem, L. W. Microsystem for in vitro primary and secondary immunization of channel catfish (Ictalurus punctatus) leucocytes with hapten-carrier conjugates. J. Immunol. Methods 72:367–379; 1984.

    Article  PubMed  CAS  Google Scholar 

  32. Miller, N. W.; Clem, L. W. A culture system for mitogen-induced proliferation of channel catfish (Ictalurus punctatus) peripheral blood lymphocytes. J. Tissue Cult. Methods 11:69–73; 1988.

    Article  Google Scholar 

  33. Mizel, S. B.; Rosenstreich, D. L. Regulation of lymphocyte activating factor (LAF) production and secretion in P388D1 cells. Identification of high molecular weight precursors of LAF. J. Immunol. 122:2173–2179; 1979.

    PubMed  CAS  Google Scholar 

  34. Nusbaum, K. E.; Grizzle, J. M. Uptake of channel catfish virus from water by channel catfish and bluegills. Am. J. Vet. Res. 48:375–377; 1987.

    PubMed  CAS  Google Scholar 

  35. Papadimitriou, J. M.; Ashman, R. B. Macrophages: current views on their differentiation, structure and function. Ultrastruct. Pathol. 13:343–372; 1989.

    PubMed  CAS  Google Scholar 

  36. Ryser, J. E.; Robson MacDonald, H. Limiting dilution analysis of alloantigen-reactive T lymphocytes. I. Comparison of precursor frequencies for proliferative and cytolytic responses. J. Immunol. 122:1691–1696; 1979.

    PubMed  CAS  Google Scholar 

  37. Sanders, S. K.; Alexander, E. L.; Braylan, R. C. A high yield technique for preparing cells fixed in suspension for scanning electron microscopy. J. Cell Biol. 67:476–480; 1975.

    Article  PubMed  CAS  Google Scholar 

  38. Sizemore, R. C.; Miller, N. W.; Cuchens, M. A., et al. Phylogeny of lymphocyte heterogeneity: the cellular requirement for the in vitro mitogenic responses of channel catfish leucocytes. J. Immunol. 133:2920–2924; 1984.

    PubMed  CAS  Google Scholar 

  39. Skinner, M. A.; Malbrook, J. An estimation of the frequency of precursor cells which generate cytotoxic lymphocytes. J. Exp. Med. 143:1562–1567; 1976.

    Article  PubMed  CAS  Google Scholar 

  40. Sun, T.; Li, C. Y.; Yam, L. T. Atlas of cytochemistry and immunocytochemistry of hematologic neoplasms. Chicago: American Society of Clinical Pathology Press; 1985.

    Google Scholar 

  41. Vallejo, A. N.; Miller, N. W.; Jorgensen, T., et al. Phylogeny of immune recognition: antigen processing/presentation in channel catfish immune responses to hemocyanins. Cell. Immunol. 130:364–377; 1990.

    Article  PubMed  CAS  Google Scholar 

  42. Wise, J. A.; Harrell, S. F.; Busch, R. L., et al. Vertical transmission of channel catfish virus. Am. J. Vet. Res. 49:1506–1509; 1988.

    PubMed  CAS  Google Scholar 

  43. Ziegler, H. K.; Unanue, E. R. Decrease in macrophage antigen catabolism caused by ammonia and chloroquine is associated with inhibition of antigen presentation to T cells. Proc. Natl. Acad. Sci. USA 79:175–178; 1982.

    Article  PubMed  CAS  Google Scholar 

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This work was supported in part by grant 5-R37-AI-19530 from the National Institutes of Health, Bethesda, MD.

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Vallejo, A.N., Ellsaesser, C.F., Miller, N.W. et al. Spontaneous development of functionally active long-term monocytelike cell lines from channel catfish. In Vitro Cell Dev Biol - Animal 27, 279–286 (1991). https://doi.org/10.1007/BF02630904

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