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. 1984 Feb;43(2):561–566. doi: 10.1128/iai.43.2.561-566.1984

Polyamino acid enhancement of bacterial phagocytosis by human polymorphonuclear leukocytes and peritoneal macrophages.

P K Peterson, G Gekker, R Shapiro, M Freiberg, W F Keane
PMCID: PMC264334  PMID: 6198279

Abstract

Cationic polyamino acids are known to enhance a variety of cell-cell interactions by virtue of their ability to alter electrostatic forces of cell surfaces. In this study, the effect of polyamino acids on phagocytosis of 3H-labeled bacteria by human polymorphonuclear leukocytes (PMNs) and peritoneal macrophages was investigated. Negatively charged and neutral polyamino acids did not influence phagocytosis of unopsonized Staphylococcus epidermidis, whereas protamine, poly-L-arginine, and poly-L-lysine stimulated phagocytosis in a dose-dependent manner. At 50 micrograms/ml, greater than 30% uptake by PMNs was seen with each of these cationic polyamino acids. Although cationic polyamino acids promoted PMN and peritoneal macrophage phagocytosis of unopsonized S. epidermidis, Staphylococcus aureus M (encapsulated) and M variant (unencapsulated), and Escherichia coli J5, little effect was seen with the parent E. coli O111:B4 or a serotype O222:H16 strain. Pretreatment of bacteria and phagocytes separately demonstrated that the phagocytosis-promoting property of polyamino acids is manifest predominantly on the bacteria. Bacteria pretreated with cationic polyamino acids also elicited a PMN chemiluminescent response, and PMN-associated bacteria were killed, as determined by a fluorochrome microassay. Thus, cationic polyamino acids promote the phagocytosis and killing of many but not all bacterial strains, and in this respect polyamino acids function as opsonins.

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Selected References

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  1. Allen R. C., Loose L. D. Phagocytic activation of a luminol-dependent chemiluminescence in rabbit alveolar and peritoneal macrophages. Biochem Biophys Res Commun. 1976 Mar 8;69(1):245–252. doi: 10.1016/s0006-291x(76)80299-9. [DOI] [PubMed] [Google Scholar]
  2. DE VRIES A., SALGO J., MATOTH Y., NEVO A., KATCHALSKI E. Effect of basic polyamino acids on phagocytosis in vitro. Arch Int Pharmacodyn Ther. 1955 Nov 1;104(1):1–10. [PubMed] [Google Scholar]
  3. Deierkauf F. A., Beukers H., Deierkauf M., Riemersma J. C. Phygocytosis by rabbit polymorphonuclear leukocytes: the effect of albumin and polyamino acids on latex uptake. J Cell Physiol. 1977 Aug;92(2):169–175. doi: 10.1002/jcp.1040920205. [DOI] [PubMed] [Google Scholar]
  4. Fearon D. T. Identification of the membrane glycoprotein that is the C3b receptor of the human erythrocyte, polymorphonuclear leukocyte, B lymphocyte, and monocyte. J Exp Med. 1980 Jul 1;152(1):20–30. doi: 10.1084/jem.152.1.20. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Fischetti V. A. Requirements for the opsonic activity of human IgG directed to type 6 group A streptococci: net basic charge and intact Fc region. J Immunol. 1983 Feb;130(2):896–902. [PubMed] [Google Scholar]
  6. Gallin J. I. Degranulating stimuli decrease the neagative surface charge and increase the adhesiveness of human neutrophils. J Clin Invest. 1980 Feb;65(2):298–306. doi: 10.1172/JCI109672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gallin J. I., Durocher J. R., Kaplan A. P. Interaction of leukocyte chemotactic factors with the cell surface. I. Chemotactic factor-induced changes in human granulocyte surface charge. J Clin Invest. 1975 May;55(5):967–974. doi: 10.1172/JCI108026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ginsburg I., Lahav M., Ne'eman N., Duchan Z., Chanes S., Sela M. N. The interaction of leukocytes and their hydrolases with bacteria in vitro and in vivo: the modification of the bactericidal and bacteriolytic reactions by cationic and anionic macromolecular substances and by anti-inflammatory agents. Agents Actions. 1976 Feb;6(1-3):292–305. doi: 10.1007/BF01972246. [DOI] [PubMed] [Google Scholar]
  9. Ginsburg I., Sela M. N., Morag A., Ravid Z., Duchan Z., Ferne M., Rabinowitz-Bergner S., Thomas P. P., Davies P., Niccols J. Role of leukocyte factors and cationic polyelectrolytes in phagocytosis of group A streptococci and Candida albicans by neutrophils, macrophages, fibroblasts and epithelial cells: modulation by anionic polyelectrolytes in relation to pathogenesis of chronic inflammation. Inflammation. 1981 Dec;5(4):289–312. doi: 10.1007/BF00911094. [DOI] [PubMed] [Google Scholar]
  10. Horwitz M. A. Phagocytosis of microorganisms. Rev Infect Dis. 1982 Jan-Feb;4(1):104–123. doi: 10.1093/clinids/4.1.104. [DOI] [PubMed] [Google Scholar]
  11. Kozel T. R. Dissociation of a hydrophobic surface from phagocytosis of encapsulated and non-encapsulated cryptococcus neoformans. Infect Immun. 1983 Mar;39(3):1214–1219. doi: 10.1128/iai.39.3.1214-1219.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kulczycki A., Jr, Solanki L., Cohen L. Isolation and partial characterization of Fc gamma-binding proteins of human leukocytes. J Clin Invest. 1981 Dec;68(6):1558–1565. doi: 10.1172/JCI110410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. MacGowan A. P., Peterson P. K., Keane W., Quie P. G. Human peritoneal macrophage phagocytic, killing, and chemiluminescent responses to opsonized Listeria monocytogenes. Infect Immun. 1983 Apr;40(1):440–443. doi: 10.1128/iai.40.1.440-443.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Nagura H., Asai J., Katsumata Y., Kojima K. Role of electric surface charge of cell membrane in phagocytosis. Acta Pathol Jpn. 1973 May;23(2):279–290. doi: 10.1111/j.1440-1827.1973.tb00792.x. [DOI] [PubMed] [Google Scholar]
  15. Ohman L., Hed J., Stendahl O. Interaction between human polymorphonuclear leukocytes and two different strains of type 1 fimbriae-bearing Escherichia coli. J Infect Dis. 1982 Dec;146(6):751–757. doi: 10.1093/infdis/146.6.751. [DOI] [PubMed] [Google Scholar]
  16. Pantazis C. G., Kniker W. T. Assessment of blood leukocyte microbial killing by using a new fluorochrome microassay. J Reticuloendothel Soc. 1979 Aug;26(2):155–170. [PubMed] [Google Scholar]
  17. Peterson P. K., Verhoef J., Schmeling D., Quie P. G. Kinetics of phagocytosis and bacterial killing by human polymorphonuclear leukocytes and monocytes. J Infect Dis. 1977 Oct;136(4):502–509. doi: 10.1093/infdis/136.4.502. [DOI] [PubMed] [Google Scholar]
  18. Peterson P. K., Wilkinson B. J., Kim Y., Schmeling D., Quie P. G. Influence of encapsulation on staphylococcal opsonization and phagocytosis by human polymorphonuclear leukocytes. Infect Immun. 1978 Mar;19(3):943–949. doi: 10.1128/iai.19.3.943-949.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Smith D. L., Rommel F. A rapid micro method for the simultaneous determination of phagocytic-microbiocidal activity of human peripheral blood leukocytes in vitro. J Immunol Methods. 1977;17(3-4):241–247. doi: 10.1016/0022-1759(77)90106-5. [DOI] [PubMed] [Google Scholar]
  20. Verbrugh H. A., Hoidal J. R., Nguyen B. Y., Verhoef J., Quie P. G., Peterson P. K. Human alveolar macrophage cytophilic immunoglobulin G-mediated phagocytosis of protein A-positive staphylococci. J Clin Invest. 1982 Jan;69(1):63–74. doi: 10.1172/JCI110442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Verbrugh H. A., Keane W. F., Hoidal J. R., Freiberg M. R., Elliott G. R., Peterson P. K. Peritoneal macrophages and opsonins: antibacterial defense in patients undergoing chronic peritoneal dialysis. J Infect Dis. 1983 Jun;147(6):1018–1029. doi: 10.1093/infdis/147.6.1018. [DOI] [PubMed] [Google Scholar]
  22. Verhoef J., Peterson P. K., Quie P. G. Human polymorphonuclear leucocyte receptors for staphylococcal opsonins. Immunology. 1977 Aug;33(2):231–239. [PMC free article] [PubMed] [Google Scholar]
  23. Verhoef J., Peterson P. K., Quie P. G. Kinetics of staphylococcal opsonization, attachment, ingestion and killing by human polymorphonuclear leukocytes: a quantitative assay using [3H]thymidine labeled bacteria. J Immunol Methods. 1977;14(3-4):303–311. doi: 10.1016/0022-1759(77)90141-7. [DOI] [PubMed] [Google Scholar]
  24. Weiss J., Victor M., Elsbach P. Role of charge and hydrophobic interactions in the action of the bactericidal/permeability-increasing protein of neutrophils on gram-negative bacteria. J Clin Invest. 1983 Mar;71(3):540–549. doi: 10.1172/JCI110798. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wilkinson B. J., Sisson S. P., Kim Y., Peterson P. K. Localization of the third component of complement on the cell wall of encapsulated Staphylococcus aureus M: implications for the mechanism of resistance to phagocytosis. Infect Immun. 1979 Dec;26(3):1159–1163. doi: 10.1128/iai.26.3.1159-1163.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. van Oss C. J. Phagocytosis as a surface phenomenon. Annu Rev Microbiol. 1978;32:19–39. doi: 10.1146/annurev.mi.32.100178.000315. [DOI] [PubMed] [Google Scholar]

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