Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1974 May;71(5):1653–1657. doi: 10.1073/pnas.71.5.1653

Isozymes of Lysozyme in Leukocytes and Egg White: Evidence for the Species-Specific Control of Egg-White Lysozyme Synthesis

Alexander Hindenburg *, John Spitznagel †, Norman Arnheim *,‡
PMCID: PMC388295  PMID: 4209557

Abstract

Two structurally distinct forms of eggwhite lysozyme (EC 3.2.1.17) are known. The egg white of some species contains both of these forms, while the egg white of other species appears to contain only one or the other of them. We have immunological and electrophoretic evidence that the chicken, which has only one lysozyme type in its egg white, contains both types in its polymorphonuclear leukocytes. Experiments on Embden goose bone marrow showed that this tissue also contains both lysozymes, even though the egg white of this species contains only one of them. Our studies suggest that many avian species have the genetic loci that code for both forms of lysozyme, but that a species-specific regulatory mechanism controls whether one or the other or both of them are expressed during egg white production. The fact that two distinct lysozymes are present in chicken leukocytes may be of significance to the antibacterial mechanism of these cells, especially in light of the fact that they lack myeloperoxidase, an important leukocyte enzyme in mammals.

Keywords: leukocyte granules, bone marrow, hormones, antibacterial mechanisms, oviduct, muramidase

Full text

PDF
1653

Images in this article

1654Image
on p.1654
1654Image
on p.1654
1656Image
on p.1656

Selected References

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

  1. Arnheim N., Hindenburg A., Begg G. S., Morgan F. J. Multiple genes for lysozyme in birds. Studies on black swan egg white lysozymes. J Biol Chem. 1973 Dec 10;248(23):8036–8042. [PubMed] [Google Scholar]
  2. Arnheim N., Inouye M., Law L., Laudin A. Chemical studies on the enzymatic specificity of goose egg white lysozyme. J Biol Chem. 1973 Jan 10;248(1):233–236. [PubMed] [Google Scholar]
  3. Arnheim N., Steller R. Multiple genes for lysozyme in birds. Arch Biochem Biophys. 1970 Dec;141(2):656–661. doi: 10.1016/0003-9861(70)90185-2. [DOI] [PubMed] [Google Scholar]
  4. Brewer J. M., Ashworth R. B. Disc electrophoresis. J Chem Educ. 1969 Jan;46(1):41–45. doi: 10.1021/ed046p41. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Canfield R. E., Kammerman S., Sobel J. H., Morgan F. J. Primary structure of lysozymes from man and goose. Nat New Biol. 1971 Jul 7;232(27):16–17. doi: 10.1038/newbio232016a0. [DOI] [PubMed] [Google Scholar]
  7. Canfield R. E., McMurry S. Purification and characterization of a lysozyme from goose egg white. Biochem Biophys Res Commun. 1967 Jan 10;26(1):38–42. doi: 10.1016/0006-291x(67)90249-5. [DOI] [PubMed] [Google Scholar]
  8. Chan L., Means A. R., O'Malley B. W. Rates of induction of specific translatable messenger RNAs for ovalbumin and avidin by steroid hormones. Proc Natl Acad Sci U S A. 1973 Jun;70(6):1870–1874. doi: 10.1073/pnas.70.6.1870. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Charlemagne D., Jollès P. La spécificité de divers lysozymes vis-à-vis de substrats de faible poids moléculaire provenant de la chitine. Bull Soc Chim Biol (Paris) 1967;49(8):1103–1113. [PubMed] [Google Scholar]
  10. Dianoux A. C., Jollès P. Différences dans le comportement des lysozymes de blanc d'ceuf de poulte et d'oie vis-a-vis de Micrococcus lysodeikticus. Bull Soc Chim Biol (Paris) 1969;51(12):1559–1564. [PubMed] [Google Scholar]
  11. Dianoux A. C., Jollès P. Etude d'un lysozyme pauvre en cystine et en tryptophane: le lysozyme de blanc d'oeuf d'oie. Biochim Biophys Acta. 1967 Apr 11;133(3):472–479. [PubMed] [Google Scholar]
  12. Ghuysen J. M. Use of bacteriolytic enzymes in determination of wall structure and their role in cell metabolism. Bacteriol Rev. 1968 Dec;32(4 Pt 2):425–464. [PMC free article] [PubMed] [Google Scholar]
  13. Janoff A., Blondin J. The effect of human granulocyte elastase on bacterial suspensions. Lab Invest. 1973 Oct;29(4):454–457. [PubMed] [Google Scholar]
  14. Jollès P., Saint Blancard J., Charlemagne D., Dianoux A. C., Jollès J., Le Baron J. L. Comparative behavior of six different lysozymes in the presence of an inhibitor. Biochim Biophys Acta. 1968 Feb 5;151(2):532–534. doi: 10.1016/0005-2744(68)90123-x. [DOI] [PubMed] [Google Scholar]
  15. Means A. R., Comstock J. P., Rosenfeld G. C., O'Malley B. W. Ovalbumin messenger RNA of chick oviduct: partial characterization, estrogen dependence, and translation in vitro. Proc Natl Acad Sci U S A. 1972 May;69(5):1146–1150. doi: 10.1073/pnas.69.5.1146. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. O'Malley B. W., McGuire W. L., Kohler P. O., Korenman S. G. Studies on the mechanism of steroid hormone regulation of synthesis of specific proteins. Recent Prog Horm Res. 1969;25:105–160. doi: 10.1016/b978-0-12-571125-8.50006-5. [DOI] [PubMed] [Google Scholar]
  17. Oka T., Schimke R. T. Interaction of estrogen and progesterone in chick oviduct development. II. Effects of estrogen and progesterone on tubular gland cell function. J Cell Biol. 1969 Oct;43(1):123–137. doi: 10.1083/jcb.43.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Osborn M. J. Structure and biosynthesis of the bacterial cell wall. Annu Rev Biochem. 1969;38:501–538. doi: 10.1146/annurev.bi.38.070169.002441. [DOI] [PubMed] [Google Scholar]
  19. Osserman E. F., Klockars M., Halper J., Fischel R. E. Effects of lysozyme on normal and transformed mammalian cells. Nature. 1973 Jun 8;243(5406):331–335. doi: 10.1038/243331a0. [DOI] [PubMed] [Google Scholar]
  20. Osserman E. F., Lawlor D. P. Serum and urinary lysozyme (muramidase) in monocytic and monomyelocytic leukemia. J Exp Med. 1966 Nov 1;124(5):921–952. doi: 10.1084/jem.124.5.921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Palmiter R. D. Regulation of protein synthesis in chick oviduct. I. Independent regulation of ovalbumin, conalbumin, ovomucoid, and lysozyme induction. J Biol Chem. 1972 Oct 25;247(20):6450–6461. [PubMed] [Google Scholar]
  22. Prager E. M., Wilson A. C. Comparison of multiple duck lysozymes. Biochem Genet. 1972 Dec;7(3):269–272. doi: 10.1007/BF00484826. [DOI] [PubMed] [Google Scholar]
  23. Rhoads R. E., McKnight G. S., Schimke R. T. Quantitative measurement of ovalbumin messenger ribonucleic acid activity. Localization in polysomes, induction by estrogen, and effect of actinomycin D. J Biol Chem. 1973 Mar 25;248(6):2031–2039. [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES