Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1975 Sep;12(3):687–693. doi: 10.1128/iai.12.3.687-693.1975

Characterization of monkey peripheral neutrophil granules during infection.

P G Rausch, P G Canonico
PMCID: PMC415340  PMID: 170208

Abstract

Rhesus monkey (Macaca mulatta) neutrophils were shown to contain the azurophilic granule maker enzymes myeloperoxidase and beta-glucuronidase but were deficient in the specific granule markers alkaline phosphatase (AKP) and lysozyme. Isopycnic centrifugation of leukocyte homogenates on linear sucrose gradients resulted in cosedimentation of myeloperoxidase and beta-glucuronidase with an equilibrium density of 1.18. After an intravenous inoculation of monkeys with Salmonella typhimurium AKP activity became marked, whereas that of beta-glucuronidase decreased and myeloperoxidase remained unchanged. Lysozyme was undetected throughout the course of the experiment, but was present in oil-induced peritoneal macrophages and peripheral mononuclear cells. The induced AKP exhibited partial latency and had an equilibrium density of 1.15. It is unclear, however, whether the induced AKP is associated with specific granules or cytoplasmic membranes. Hence, while these data are consistent with the presence of azurophilic granules in polymorphonuclear neutrophils from infected monkeys, the presence of specific granules in polymorphonuclear neutrophils of both uninfected and infected monkeys remains moot.

Full text

PDF
687

Images in this article

689Image
on p.689

Selected References

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

  1. Baggiolini M., De Duve C., Masson P. L., Heremans J. F. Association of lactoferrin with specific granules in rabbit heterophil leukocytes. J Exp Med. 1970 Mar 1;131(3):559–570. doi: 10.1084/jem.131.3.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baggiolini M., Hirsch J. G., De Duve C. Further biochemical and morphological studies of granule fractions from rabbit heterophil leukocytes. J Cell Biol. 1970 Jun;45(3):586–597. doi: 10.1083/jcb.45.3.586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baggiolini M. The enzymes of the granules of polymorphonuclear leukocytes and their functions. Enzyme. 1972;13(1):132–160. doi: 10.1159/000459653. [DOI] [PubMed] [Google Scholar]
  4. Bainton D. F., Farquhar M. G. Origin of granules in polymorphonuclear leukocytes. Two types derived from opposite faces of the Golgi complex in developing granulocytes. J Cell Biol. 1966 Feb;28(2):277–301. doi: 10.1083/jcb.28.2.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bainton D. F. Sequential degranulation of the two types of polymorphonuclear leukocyte granules during phagocytosis of microorganisms. J Cell Biol. 1973 Aug;58(2):249–264. doi: 10.1083/jcb.58.2.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bainton D. F., Ullyot J. L., Farquhar M. G. The development of neutrophilic polymorphonuclear leukocytes in human bone marrow. J Exp Med. 1971 Oct 1;134(4):907–934. doi: 10.1084/jem.134.4.907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bretz U., Baggiolini M. Biochemical and morphological characterization of azurophil and specific granules of human neutrophilic polymorphonuclear leukocytes. J Cell Biol. 1974 Oct;63(1):251–269. doi: 10.1083/jcb.63.1.251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brune K., Spitznagel J. K. Peroxidaseless chicken leukocytes: isolation and characterization of antibacterial granules. J Infect Dis. 1973 Jan;127(1):84–94. doi: 10.1093/infdis/127.1.84. [DOI] [PubMed] [Google Scholar]
  9. Böyum A. Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand J Clin Lab Invest Suppl. 1968;97:77–89. [PubMed] [Google Scholar]
  10. Canonico P. G., Bird J. W. Lysosomes in skeletal muscle tissue. Zonal centrifugation evidence for multiple cellular sources. J Cell Biol. 1970 May;45(2):321–333. doi: 10.1083/jcb.45.2.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. DE DUVE C., PRESSMAN B. C., GIANETTO R., WATTIAUX R., APPELMANS F. Tissue fractionation studies. 6. Intracellular distribution patterns of enzymes in rat-liver tissue. Biochem J. 1955 Aug;60(4):604–617. doi: 10.1042/bj0600604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. DeChatelet L. R., Cooper M. R. A modified procedure for the determination of leukocyte alkaline phosphatase. Biochem Med. 1970 Aug;4(1):61–68. doi: 10.1016/0006-2944(70)90103-1. [DOI] [PubMed] [Google Scholar]
  13. DeChatelet L. R., Volk J. V., McCall C. E., Cooper M. R. Studies on leukocyte phosphatases. II. Inhibition of leukocyte alkaline phosphatase by amino acids and its reversal by zinc. Clin Chem. 1971 Mar;17(3):210–213. [PubMed] [Google Scholar]
  14. Dingle J. T., Barrett A. J. Uptake of biologically active substances by lysosomes. Proc R Soc Lond B Biol Sci. 1969 Apr 15;173(1030):85–93. doi: 10.1098/rspb.1969.0040. [DOI] [PubMed] [Google Scholar]
  15. Farquhar M. G., Bainton D. F., Baggiolini M., de Duve C. Cytochemical localization of acid phosphatase activity in granule fractions from rabbit polymorphonuclear leukocytes. J Cell Biol. 1972 Jul;54(1):141–156. doi: 10.1083/jcb.54.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Folds J. D., Welsh I. R., Spitznagel J. K. Neutral proteases confined to one class of lysosomes of human polymorphonuclear leukocytes. Proc Soc Exp Biol Med. 1972 Feb;139(2):461–463. doi: 10.3181/00379727-139-36164. [DOI] [PubMed] [Google Scholar]
  17. Jain N. C. Alkaline phosphatase activity in leukocytes of some animal species. Acta Haematol. 1968;39(1):51–59. doi: 10.1159/000208941. [DOI] [PubMed] [Google Scholar]
  18. KAPLOW L. S. A histochemical procedure for localizing and evaluating leukocyte alkaline phosphatase activity in smears of blood and marrow. Blood. 1955 Oct;10(10):1023–1029. [PubMed] [Google Scholar]
  19. KAPLOW L. S. SIMPLIFIED MYELOPEROXIDASE STAIN USING BENZIDINE DIHYDROCHLORIDE. Blood. 1965 Aug;26:215–219. [PubMed] [Google Scholar]
  20. 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]
  21. Leffell M. S., Spitznagel J. K. Association of lactoferrin with lysozyme in granules of human polymorphonuclear leukocytes. Infect Immun. 1972 Nov;6(5):761–765. doi: 10.1128/iai.6.5.761-765.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. McCall C. E., Katayama I., Cotran R. S., Finland M. Lysosomal and ultrastructural changes in human "toxic" neutrophils during bacterial infection. J Exp Med. 1969 Feb 1;129(2):267–293. doi: 10.1084/jem.129.2.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Padgett G. A., Hirsch J. G. Lysozyme: its absence in tears and leukocytes of cattle. Aust J Exp Biol Med Sci. 1967 Oct;45(5):569–570. doi: 10.1038/icb.1967.56. [DOI] [PubMed] [Google Scholar]
  24. Paul B. B., Strauss R. R., Jacobs A. A., Sbarra A. J. Function of h(2)o(2), myeloperoxidase, and hexose monophosphate shunt enzymes in phagocytizing cells from different species. Infect Immun. 1970 Apr;1(4):338–344. doi: 10.1128/iai.1.4.338-344.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Prieur D. J., Olson H. M., Young D. M. Lysozyme deficiency-an inherited disorder of rabbits. Am J Pathol. 1974 Nov;77(2):283–298. [PMC free article] [PubMed] [Google Scholar]
  26. Proctor R. A., White J. D., Ayala E., Canonico P. G. Phagocytosis of Francisella tularensis by Rhesus monkey peripheral leukocytes. Infect Immun. 1975 Jan;11(1):146–151. doi: 10.1128/iai.11.1.146-151.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rayfield E. J., George D. T., Beisel W. R. Altered growth hormone homeostasis during acute bacterial sepsis in the rhesus monkey. J Clin Endocrinol Metab. 1974 May;38(5):746–754. doi: 10.1210/jcem-38-5-746. [DOI] [PubMed] [Google Scholar]
  28. Robertson P. B., Ryel R. B., Taylor R. E., Shyu K. W., Fullmer H. M. Collagenase: localization in polymorphonuclear leukocyte granules in the rabbit. Science. 1972 Jul 7;177(4043):64–65. doi: 10.1126/science.177.4043.64. [DOI] [PubMed] [Google Scholar]
  29. SKOOG W. A., BECK W. S. Studies on the fibrinogen, dextran and phytohemagglutinin methods of isolating leukocytes. Blood. 1956 May;11(5):436–454. [PubMed] [Google Scholar]
  30. Spitznagel J. K., Dalldorf F. G., Leffell M. S., Folds J. D., Welsh I. R., Cooney M. H., Martin L. E. Character of azurophil and specific granules purified from human polymorphonuclear leukocytes. Lab Invest. 1974 Jun;30(6):774–785. [PubMed] [Google Scholar]
  31. TRUBOWITZ S., MOSCHIDES E., FELDMAN D. Alkaline phosphatase activity of the polymorphonuclear leukocyte in rapidly induced leukopenia and leukocytosis. J Lab Clin Med. 1961 May;57:747–754. [PubMed] [Google Scholar]
  32. Zeya H. I., Spitznagel J. K. Isolation of polymorphonuclear leukocyte granules from rabbit bone marrow. Lab Invest. 1971 Mar;24(3):237–245. [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES