Skip to main content
PMC home page
Elsevier - PMC COVID-19 Collection logoLink to Elsevier - PMC COVID-19 Collection
. 2002 Nov 12;23(1):113–128. doi: 10.1016/0165-2427(89)90114-1

Natural killer (NK) activity and interferon (IFN) production by a fraction of spleen and blood lymphocytes in swine

H Salmon 1, B Charley 2, C Labonnardiere 2, M Olivier 1, K Kelley 3, A Paraf 1
PMCID: PMC7133630  PMID: 2482570

Abstract

After carbonyl iron treatment and gradient isolation, spleen and blood pig lymphocytes exhibited NK activity and produced IFN after viral induction. Removal of plastic-adherent cells, including the majority of B cells, did not change these activities. The plastic-non-adherent cells were further separated into two subsets of roughly similar size by panning using a monoclonal, anti-T, and anti-null cell antibodies (81+cells). NK activity and IFN production were found in the 81 − cell fraction. A significantly higher proportion of null lymphocytes from blood and of splenic Fc-gamma receptor-bearing lymphocytes was also found among the 81 − cell fraction as compared to the 81 + fraction, without any change among other subsets. Similar proportions of helper (PT4+), cytotoxic (PT8+) and total T cells (MSA4+) were found among lymphocytes bound to target K562 cells and among the whole lymphocyte population. In contrast, lymphocytes that bound K562 cells demonstrated a striking increase in the proportion of Fc-gamma receptor-positive cells of high affinity. These results show that NK cells and IFN-producing cells are mainly included in the same blood and spleen fraction, and suggest that among 81 − cells only those expressing an Fc-gamma receptor of high affinity are active.

References

  1. Abb J., Abb H., Deinhardt F. Phenotype of human-interferon producing leucocytes identified by monoclonal antibodies. Clin. Exp. Immunol. 1983;52:179–184. [PMC free article] [PubMed] [Google Scholar]
  2. Binns R.M. Organization of the lymphoreticular system and lymphocyte markers in the pig. Vet. Immunol. Immunopathol. 1982;3:95–146. doi: 10.1016/0165-2427(82)90033-2. [DOI] [PubMed] [Google Scholar]
  3. Binns R.M., Licence S.T. A major subpopulation of the Fc receptor-bearing lymphocytes revealed by rosette formation in dextran media: studies with pig, sheep and rat lymphocytes. J. Immunol. Methods. 1981;43:153–162. doi: 10.1016/0022-1759(81)90018-1. [DOI] [PubMed] [Google Scholar]
  4. Cepica A., Derbyshire J.B. The effect of adoptive transfer of mononuclear leukocytes from an adult donor on spontaneous cell-mediated cytoxicity and resistance to transmissible gastro-enteritis in neonatal piglets. Can. J. Comp. Med. 1984;48:360–364. [PMC free article] [PubMed] [Google Scholar]
  5. Cepica A., Derbyshire J.B. Characterization of the effector cells in antibody dependent and spontaneous cell-mediated cytotoxicity in swine against target cells infected with transmissible gastro-enteritis virus. Res. Vet. Sci. 1986;41:70–75. [PubMed] [Google Scholar]
  6. Charley B., Petit E., Laude H., La Bonnardiere C. Myxovirus and coronavirus induced in vitro stimulation of spontaneous cell-mediated cytotoxicity by porcine blood leukocytes. Ann. Virol. (Inst. Pasteur) 1983;134E:119–126. [Google Scholar]
  7. Chung T.J., Huh N.D., Kim Y.B. Differential effects of interferon on porcine NK and K-cell activities. In: Herberman R.B., editor. NK Cells and other Natural Effector Cells. Academic Press; New York, NY: 1982. pp. 381–386. [Google Scholar]
  8. Djeu J.Y., Stocks N., Zoon K., Stanton O.J., Timonen T., Herberman R.B. Positive self regulation of cytotoxicity in human natural killer cells by production of interferon upon exposure to influenza and herpes viruses. J. Exp. Med. 1982;156:1222–1234. doi: 10.1084/jem.156.4.1222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hammerberg C., Schurig G.G. Characterization of monoclonal antibodies directed against leukocytes. Vet. Immunol. Immunopathol. 1986;11:107–121. doi: 10.1016/0165-2427(86)90092-9. [DOI] [PubMed] [Google Scholar]
  10. Ito Y., Nishiyama Y., Shimokata K., Nagata I., Takeyama H., Kunii A. The mechanism of interferon induction in mouse spleen cells stimulated with HVJ. Virology. 1978;88:128–137. doi: 10.1016/0042-6822(78)90116-2. [DOI] [PubMed] [Google Scholar]
  11. Kelley K.W., Davis W.C., Salmon H., Aynaud J.M., Olivier M. Vol. 43. 1984. Monoclonal antibodies against porcine leukocyte antigens; p. 1681. (Fed. Proc.). abstr. no. 1545. [Google Scholar]
  12. Kelley K.W., Salmon H., Davis W.C., Aynaud J.M., Paraf A. A cytotoxic murine monoclonal antibody that recognizes a porcine T-cell subset involved in lectin induced proliferation. Ann. Rech. Vet. 1988;19:141–147. [PubMed] [Google Scholar]
  13. Kim Y.B., Huh N.D., Koren H.S., Amos D.B. Natural killing (NK) and antibody dependent cellular cytotoxicity (ADCC) in specific pathogen-free (SPF) miniature swine and germ-free piglets. J. Immunol. 1980;125:755–762. [PubMed] [Google Scholar]
  14. Koren H., Amos D.B., Kim Y.B. Vol. 75. 1978. Natural killing and antibody dependent cellular cytotoxicity are independent immune functions in the Minnesota miniature swine; pp. 5127–5131. (Proc. Natl. Acad. Sci. U.S.A.). [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. La Bonnardiere C., Laude H. High interferon titer in newborn pig intestine during experimentally induced viral enteritis. Infect. Immun. 1981;32:28–31. doi: 10.1128/iai.32.1.28-31.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lesnick C.E., Derbyshire J.B. Activation of natural killer cells in newborn piglets by interferon induction. Vet. Immunol. Immunopathol. 1988;18:109–117. doi: 10.1016/0165-2427(88)90053-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lotzova E., Herberman R.B. A general overview of NK assays. In: Lotzova E., Herberman R.B., editors. vol. 1. CRC Press; Boca Raton, FL: 1986. pp. 2–20. (Immunobiology of Natural Killer Cells). [Google Scholar]
  18. Lunney J.K., Pescovitz M.D. Differentiation antigens of swine lymphoid tissues. In: Trnka Z., Miyaska M., editors. Comparative Aspects of Differentiation Antigens. Marcel Dekker; New York, NY: 1989. in press. [Google Scholar]
  19. Mage M.G., McHugh L.L., Rothstein T.L. Mouse lymphocytes with and without surface immunoglobulin: preparative scale separation in polystyrene tissue culture dishes coated with specifically purified anti-immunoglobulin. J. Immunol. Methods. 1977;15:47–56. doi: 10.1016/0022-1759(77)90016-3. [DOI] [PubMed] [Google Scholar]
  20. Minato N., Reid L., Canlor H., Lengyel P., Bloom P.R. Mode of regulation of natural killer cell activity by interferon. J. Exp. Med. 1980;152:124–137. doi: 10.1084/jem.152.1.124. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Norley S.J., Wardley R.C. Investigation of porcine natural killer cell activity with reference to African swine fever virus infection. Immunology. 1983;49:593–597. [PMC free article] [PubMed] [Google Scholar]
  22. Pescovitz M.D., Lunney J.K., Sachs D.H. Preparation and characterization of monoclonal antibodies reactive with porcine PBL. J. Immunol. 1984;133:368–375. [PubMed] [Google Scholar]
  23. Peter H.J., Dalligge H., Zawatzky R., Euler S., Leibold W., Kirchner H. Human peripheral null lymphocytes. II. Producers of type 1 interferon upon stimulation with tumor cells, herpes simplex virus and Corynebacterium parvum. Eur. J. Immunol. 1980;10:547–555. doi: 10.1002/eji.1830100712. [DOI] [PubMed] [Google Scholar]
  24. Reynolds C.W., Ortaldo J.R. Natural killer activity: the definition of a function rather than a cell type. Immunol. Today. 1987;8:172–174. doi: 10.1016/0167-5699(87)90032-6. [DOI] [PubMed] [Google Scholar]
  25. Salmon H. Surface markers of porcine lymphocytes and distribution in various organs. Int. Arch. Allergy Appl. Immunol. 1979;60:262–274. doi: 10.1159/000232351. [DOI] [PubMed] [Google Scholar]
  26. Salmon H. Rosette-formation of pig thymic lymphocytes with sheep and pig erythrocytes. II. Markers for cortical and medullary thymocytes. Thymus. 1983;5:105–113. [PubMed] [Google Scholar]
  27. Salmon H. Surface markers of swine lymphocytes: application to the study of local immune system of mammary gland and transplanted gut. In: Tumbleson M.E., editor. Vol. 3. Plenum; New York, NY: 1986. pp. 1855–1864. (Swine in Biomedical Research). [Google Scholar]
  28. Salmon H., Licence S.T., Binns R.M. Staining of pig lymphocyte subpopulations with acid α-naphthyl acetate esterase. Vet. Immunol. Immunopathol. 1987;14:173–179. doi: 10.1016/0165-2427(87)90051-1. [DOI] [PubMed] [Google Scholar]
  29. Savary A., Lotzova E. Phylogeny and ontogeny of NK cells. In: Lotzova E., Herberman R.B., editors. vol. 1. CRC Press; Boca Raton, FL: 1986. pp. 45–61. (Immunobiology of Natural Killer Cells). [Google Scholar]
  30. Takamatsu H., Koide F. Augmentation of porcine spontaneous cell-mediated cytotoxicity in vitro. Jpn. J. Vet. Sci. 1985;47(5):749–759. doi: 10.1292/jvms1939.47.749. [DOI] [PubMed] [Google Scholar]
  31. Tedder T.F., Fearon D.T., Gartland G.L., Cooper M.D. Expression of C3b receptors on human B cells and myelomonocytic cells but not natural killer. J. Immunol. 1983;130:1668–1673. [PubMed] [Google Scholar]
  32. Timonen T., Saksela E., Virtanen I.E., Cantell K. Natural killer cells are responsible for the interferon production induced in human lymphocytes by tumor cell contact. Eur. J. Immunol. 1980;10:422–427. [Google Scholar]
  33. Timonen T., Ortaldo J.R., Herberman R.B. Characteristics of human large granular lymphocytes and relationship to natural killer and K cells. J. Exp. Med. 1981;153:569–582. doi: 10.1084/jem.153.3.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Trinchieri G., Santoli D., Dee R.R., Knowles B.B. Anti-viral activity induced by culturing lymphocytes with tumor-derived or virus-transformed cells. J. Exp. Med. 1978;147:1299–1313. doi: 10.1084/jem.147.5.1299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Welsh R.M. Mouse natural killer cells: induction, specificity and function. J. Immunol. 1978;121:1631–1635. [PubMed] [Google Scholar]
  36. Welsh R.M. Natural killer cells and interferon. CRC Crit. Rev. Immunol. 1984;5:55–93. [PubMed] [Google Scholar]
  37. Yang W.C., Schultz R.D. Ontogeny of natural killer activity and antibody dependent cell mediated cytotoxicity in pigs. Dev. Comp. Immunol. 1986;10:405–418. doi: 10.1016/0145-305x(86)90030-3. [DOI] [PubMed] [Google Scholar]
  38. Yang W.C., Schultz R.D., Spano J.S. Isolation and characterization of porcine natural killer (NK) cells. Vet. Immunol. Immunopathol. 1987;14:345–356. doi: 10.1016/0165-2427(87)90037-7. [DOI] [PubMed] [Google Scholar]

Articles from Veterinary Immunology and Immunopathology are provided here courtesy of Elsevier

RESOURCES