Skip to main content
NCBI home page
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1974 May 1;139(5):1262–1282. doi: 10.1084/jem.139.5.1262

CHANGES IN CELLULAR ENZYME LEVELS AND EXTRACELLULAR RELEASE OF LYSOSOMAL ACID HYDROLASES IN MACROPHAGES EXPOSED TO GROUP A STREPTOCOCCAL CELL WALL SUBSTANCE

Philip Davies 1, Roy C Page 1, A C Allison 1
PMCID: PMC2139663  PMID: 4825245

Abstract

Mouse peritoneal macrophages exposed to type-specific polysaccharide and peptidoglycan (PPG) from group A streptococci undergo marked morphologic and biochemical changes. The cells show increases in size and an increased number of lysosomes as demonstrated by vital staining with acridine orange. There are significant elevations in the levels of both lysosomal and nonlysosomal enzymes. Higher doses of PPG cause selective release of the hydrolases into the extracellular environment with no detectable loss of cell viability. The in vitro phenomena may be relevant to understanding the role of macrophages in chronic inflammation.

Full Text

The Full Text of this article is available as a PDF (1.4 MB).

Selected References

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

  1. Abdulla E. M., Schwab J. H. Biological properties of streptococcal cell-wall particles. 3. Dermonecrotic reaction to cell-wall mucopeptides. J Bacteriol. 1966 Jan;91(1):374–383. doi: 10.1128/jb.91.1.374-383.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Allison A. C., Davies P., Page R. C. Effects of endotoxin on macrophages and other lymphoreticular cells. J Infect Dis. 1973 Jul;128(Suppl):212–219. doi: 10.1093/infdis/128.supplement_1.s212. [DOI] [PubMed] [Google Scholar]
  3. Axline S. G., Cohn Z. A. In vitro induction of lysosomal enzymes by phagocytosis. J Exp Med. 1970 Jun 1;131(6):1239–1260. doi: 10.1084/jem.131.6.1239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ayoub E. M., McCarty M. Intraphagocytic beta-N-acetylglucosaminidase. Properties of the enzyme and its activity on group A streptococcal carbohydrate in comparison with a soil bacillus enzyme. J Exp Med. 1968 Apr 1;127(4):833–851. doi: 10.1084/jem.127.4.833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ayoub E. M., Wannamaker L. W. The fate of group A streptococci following phagocytosis. In vitro phagocytic studies of isotope-labeled streptococci. J Immunol. 1967 Dec;99(6):1099–1105. [PubMed] [Google Scholar]
  6. Benassi G. Effect of sucrose on the total acid phosphatase activity and the growth of LS cells. Exp Cell Res. 1968 Apr;50(1):159–166. doi: 10.1016/0014-4827(68)90404-7. [DOI] [PubMed] [Google Scholar]
  7. COHN Z. A., BENSON B. THE DIFFERENTIATION OF MONONUCLEAR PHAGOCYTES. MORPHOLOGY, CYTOCHEMISTRY, AND BIOCHEMISTRY. J Exp Med. 1965 Jan 1;121:153–170. doi: 10.1084/jem.121.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. COHN Z. A., WIENER E. THE PARTICULATE HYDROLASES OF MACROPHAGES. II. BIOCHEMICAL AND MORPHOLOGICAL RESPONSE TO PARTICLE INGESTION. J Exp Med. 1963 Dec 1;118:1009–1020. doi: 10.1084/jem.118.6.1009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. CONCHIE J., FINDLAY J., LEVVY G. A. Mammalian glycosidases; distribution in the body. Biochem J. 1959 Feb;71(2):318–325. doi: 10.1042/bj0710318. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. CROMARTIE W. J., SCHWAB J. H., CRADDOCK J. G. The effect of a toxic cellular component of group A streptococci on connective tissue. Am J Pathol. 1960 Jul;37:79–99. [PMC free article] [PubMed] [Google Scholar]
  11. Cohn Z. A., Ehrenreich B. A. The uptake, storage, and intracellular hydrolysis of carbohydrates by macrophages. J Exp Med. 1969 Jan 1;129(1):201–225. doi: 10.1084/jem.129.1.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Coleman S. E., van de Rijn I., Bleiweis A. S. Lysis of grouped and ungrouped streptococci by lysozyme. Infect Immun. 1970 Nov;2(5):563–569. doi: 10.1128/iai.2.5.563-569.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Davies P., Allison A. C., Haswell A. D. Selective release of lysosomal hydrolases from phagocytic cells by cytochalasin B. Biochem J. 1973 May;134(1):33–41. doi: 10.1042/bj1340033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Davies P., Krakauer K., Weissmann G. Subcellular distribution of neutral protease and peptidases in rabbit polymorphonuclear leucocytes. Nature. 1970 Nov 21;228(5273):761–762. doi: 10.1038/228761a0. [DOI] [PubMed] [Google Scholar]
  15. Davies P., Rita G. A., Krakauer K., Weissmann G. Characterization of a neutral protease from lysosomes of rabbit polymorphonuclear leucocytes. Biochem J. 1971 Jul;123(4):559–569. doi: 10.1042/bj1230559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dingle J. T., Barrett A. J., Weston P. D. Cathepsin D. Characteristics of immunoinhibition and the confirmation of a role in cartilage breakdown. Biochem J. 1971 Jun;123(1):1–13. doi: 10.1042/bj1230001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dingle J. T., Fell H. B., Glauert A. M. Endocytosis of sugars in embryonic skeletal tissues in organ culture. IV. Lysosomal and other biochemical effects. General discussion. J Cell Sci. 1969 Jan;4(1):139–153. doi: 10.1242/jcs.4.1.139. [DOI] [PubMed] [Google Scholar]
  18. GILL F. A., COLE R. M. THE FATE OF A BACTERIAL ANTIGEN (STREPTOCOCCAL M PROTEIN) AFTER PHAGOCYTOSIS BY MACROPHAGES. J Immunol. 1965 Jun;94:898–915. [PubMed] [Google Scholar]
  19. GOLDBARG J. A., RUTENBURG A. M. The colorimetric determination of leucine aminopeptidase in urine and serum of normal subjects and patients with cancer and other diseases. Cancer. 1958 Mar-Apr;11(2):283–291. doi: 10.1002/1097-0142(195803/04)11:2<283::aid-cncr2820110209>3.0.co;2-8. [DOI] [PubMed] [Google Scholar]
  20. Ginsburg I. Mechanisms of cell and tissue injury induced by group A streptococci: relation to poststreptococcal sequelae. J Infect Dis. 1972 Sep;126(3):294–340. doi: 10.1093/infdis/126.3.294. [DOI] [PubMed] [Google Scholar]
  21. Glick A. D., Getnick R. A., Cole R. M. Electron microscopy of group A streptococci after phagocytosis by human monocytes. Infect Immun. 1971 Dec;4(6):772–779. doi: 10.1128/iai.4.6.772-779.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Henson P. M. Interaction of cells with immune complexes: adherence, release of constituents, and tissue injury. J Exp Med. 1971 Sep 1;134(3 Pt 2):114s–135s. [PubMed] [Google Scholar]
  23. Jones J. M., Schwab J. H. Immune response to cell wall and tissue antigens in rabbits injured with streptococcal cell wall fragments. Int Arch Allergy Appl Immunol. 1970;39(4):445–448. doi: 10.1159/000230373. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Ohanian S. H., Schwab J. H. Persistence of group a streptococcal cell walls related to chronic inflammation of rabbit dermal connective tissue. J Exp Med. 1967 Jun 1;125(6):1137–1148. doi: 10.1084/jem.125.6.1137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rickles N., Zilberstein Z., Kraus S., Arad G., Kaufstein M., Ginsburg I. Persistence of group A streptococci labeled with fluorescein isothiocyanate in inflammatory sites in the heart and muscle of mice and rabbits. Proc Soc Exp Biol Med. 1969 Jun;131(2):525–530. doi: 10.3181/00379727-131-33917. [DOI] [PubMed] [Google Scholar]
  27. SCHWAB J. H., CROMARTIE W. J., ROBERSON B. S. Identification of a toxic cellular component of group A streptococci as a complex of group-specific C polysaccharide and a protein. J Exp Med. 1959 Jan 1;109(1):43–54. doi: 10.1084/jem.109.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schwab J. H. Biological properties of streptococcal cell-wall particles. I. Determinants of the chronic nodular lesion of connective tissue. J Bacteriol. 1965 Nov;90(5):1405–1411. doi: 10.1128/jb.90.5.1405-1411.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schwab J. H. Biological properties of streptococcal cell-wall particles. II. Purification by density gradient column electrophoresis. J Bacteriol. 1965 Nov;90(5):1412–1419. doi: 10.1128/jb.90.5.1412-1419.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schwab J. H., Cromartie W. J., Ohanian S. H., Craddock J. G. Association of experimental chronic arthritis with the persistence of group A streptococcal cell walls in the articular tissue. J Bacteriol. 1967 Nov;94(5):1728–1735. doi: 10.1128/jb.94.5.1728-1735.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Temple A., Loewi G., Davies P., Howard A. Cytotoxicity of immune guinea-pig cells. II. The mechanism of macrophage cytotoxicity. Immunology. 1973 Apr;24(4):655–669. [PMC free article] [PubMed] [Google Scholar]
  32. WOOLLEN J. W., HEYWORTH R., WALKER P. G. Studies on glucosaminidase. 3. Testicular N-acetyl-beta-glucosaminidase and N-acetyl-beta-galactosaminidase. Biochem J. 1961 Jan;78:111–116. doi: 10.1042/bj0780111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Weissmann G., Dukor P., Zurier R. B. Effect of cyclic AMP on release of lysosomal enzymes from phagocytes. Nat New Biol. 1971 Jun 2;231(22):131–135. doi: 10.1038/newbio231131a0. [DOI] [PubMed] [Google Scholar]
  34. Weissmann G., Zurier R. B., Spieler P. J., Goldstein I. M. Mechanisms of lysosomal enzyme release from leukocytes exposed to immune complexes and other particles. J Exp Med. 1971 Sep 1;134(3 Pt 2):149s–165s. [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES