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. 1966 Feb 1;28(2):277–301. doi: 10.1083/jcb.28.2.277

ORIGIN OF GRANULES IN POLYMORPHONUCLEAR LEUKOCYTES

Two Types Derived from Opposite Faces of the Golgi Complex in Developing Granulocytes

Dorothy Ford Bainton 1, Marilyn G Farquhar 1
PMCID: PMC2106917  PMID: 5914694

Abstract

The origin, nature, and distribution of polymorphonuclear leukocyte (PMN) granules were investigated by examining developing granulocytes from normal rabbit bone marrow which had been fixed in glutaraldehyde and postfixed in OsO4. Two distinct types of granules, azurophil and specific, were distinguished on the basis of their differences in size, density, and time and mode of origin. Both types are produced by the Golgi complex, but they are formed at different stages of maturation and originate from different faces of the Golgi complex. Azurophil granules are larger (∼800 mµ) and more dense. They are formed only during the progranulocyte stage and arise from the proximal or concave face of the Golgi complex by budding and subsequent aggregation of vacuoles with a dense core. Smaller (∼500 mµ), less dense specific granules are formed during the myelocyte stage; they arise from the distal or convex face of the Golgi complex by pinching-off and confluence of vesicles which have a finely granular content. Only azurophil granules are found in progranulocytes, but in mature PMN relatively few (10 to 20%) azurophils are seen and most (80 to 90%) of the granules present are of the specific type. The results indicate that inversion of the azurophil/specific granule ratio occurs during the myelocyte stage and is due to: (a) reduction of azurophil granules by multiple mitoses; (b) lack of new azurophil granule formation after the progranulocyte stage; and (c) continuing specific granule production. The findings demonstrate the existence of two distinct granule types in normal rabbit PMN and their separate origins from the Golgi complex. The implications of the observations are discussed in relationship to previous morphological and cytochemical studies on PMN granules and to such questions as the source of primary lysosomes and the concept of polarity within the Golgi complex.

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Selected References

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  1. BAHR G. F. Osmium tetroxide and ruthenium tetroxide and their reactions with biologically important substances. Electron stains. III. Exp Cell Res. 1954 Nov;7(2):457–479. doi: 10.1016/s0014-4827(54)80091-7. [DOI] [PubMed] [Google Scholar]
  2. CAPONE R. J., WEINREB L., CHAPMAN G. B. ELECTRON MICROSCOPE STUDIES ON NORMAL HUMAN MYELOID ELEMENTS. Blood. 1964 Mar;23:300–320. [PubMed] [Google Scholar]
  3. DANIELS E. W. ORIGIN OF THE GOLGI SYSTEM IN AMOEBAE. Z Zellforsch Mikrosk Anat. 1964 Sep 17;64:38–51. doi: 10.1007/BF00339184. [DOI] [PubMed] [Google Scholar]
  4. DROCHMANS P. [Morphology of glycogen. Electron microscopic study of the negative stains of particulate glycogen]. J Ultrastruct Res. 1962 Apr;6:141–163. doi: 10.1016/s0022-5320(62)90050-3. [DOI] [PubMed] [Google Scholar]
  5. ELSBACH P., RIZACK M. A. ACID LIPASE AND PHOSPHOLIPASE ACTIVITY IN HOMOGENATES OF RABBIT POLYMORPHONUCLEAR LEUKOCYTES. Am J Physiol. 1963 Dec;205:1154–1158. doi: 10.1152/ajplegacy.1963.205.6.1154. [DOI] [PubMed] [Google Scholar]
  6. FARQUHAR M. G. Origin and fate of secretory granules in cells of the anterior pituitary gland. Trans N Y Acad Sci. 1961 Feb;23:346–351. doi: 10.1111/j.2164-0947.1961.tb01361.x. [DOI] [PubMed] [Google Scholar]
  7. FEDORKO M. E., MORSE S. I. ISOLATION, CHARACTERIZATION, AND DISTRIBUTION OF ACID MUCOPOLYSACCHARIDES IN RABBIT LEUCOCYTES. J Exp Med. 1965 Jan 1;121:39–48. doi: 10.1084/jem.121.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. FLOREY H. W., GRANT L. H. Leucocyte migration from small blood vessels stimulated with ultraviolet light: an electron-microscope study. J Pathol Bacteriol. 1961 Jul;82:13–17. doi: 10.1002/path.1700820103. [DOI] [PubMed] [Google Scholar]
  9. FRIEND D. S., MURRAY M. J. OSMIUM IMPREGNATION OF THE GOLGI APPARATUS. Am J Anat. 1965 Jul;117:135–149. doi: 10.1002/aja.1001170109. [DOI] [PubMed] [Google Scholar]
  10. Farquhar M. G., Palade G. E. Cell junctions in amphibian skin. J Cell Biol. 1965 Jul;26(1):263–291. doi: 10.1083/jcb.26.1.263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. GOODMAN J. R., REILLY E. B., MOORE R. E. Electron microscopy of formed elements of normal human blood. Blood. 1957 May;12(5):428–442. [PubMed] [Google Scholar]
  12. HIRSCH J. G., COHN Z. A. DIGESTIVE AND AUTOLYTIC FUNCTIONS OF LYSOSOMES IN PHAGOCYTIC CELLS. Fed Proc. 1964 Sep-Oct;23:1023–1025. [PubMed] [Google Scholar]
  13. HIRSCH J. G. Cinemicrophotographic observations on granule lysis in polymorphonuclear leucocytes during phagocytosis. J Exp Med. 1962 Dec 1;116:827–834. doi: 10.1084/jem.116.6.827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. HORN R. G., SPICER S. S., WETZEL B. K. PHAGOCYTOSIS OF BACTERIA BY HETEROPHIL LEUKOCYTES: ACID AND ALKALINE PHOSPHATASE CYTOCHEMISTRY. Am J Pathol. 1964 Aug;45:327–335. [PMC free article] [PubMed] [Google Scholar]
  15. JAMIESON J. D., PALADE G. E. SPECIFIC GRANULES IN ATRIAL MUSCLE CELLS. J Cell Biol. 1964 Oct;23:151–172. doi: 10.1083/jcb.23.1.151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. KARNOVSKY M. J. Simple methods for "staining with lead" at high pH in electron microscopy. J Biophys Biochem Cytol. 1961 Dec;11:729–732. doi: 10.1083/jcb.11.3.729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. KILLMANN S. A., CRONKITE E. P., FLIEDNER T. M., BOND V. P. Mitotic indices of human bone marrow cells. I. Number and cytologic distribution of mitoses. Blood. 1962 Jun;19:743–750. [PubMed] [Google Scholar]
  18. LOCKWOOD W. R., ALLISON F. ELECTRON MICROGRAPHIC STUDIES OF PHAGOCYTIC CELLS. I. MORPHOLOGICAL CHANGES OF THE CYTOPLASM AND GRANULES OF RABBIT GRANULOCYTES ASSOCIATED WITH INGESTION OF ROUGH PNEUMOCOCCUS. Br J Exp Pathol. 1963 Dec;44:593–600. [PMC free article] [PubMed] [Google Scholar]
  19. MOLLENHAUER H. H., WHALEY W. G. An observation on the functioning of the Golgi apparatus. J Cell Biol. 1963 Apr;17:222–225. doi: 10.1083/jcb.17.1.222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. PALAY S. L. The fine structure of secretory neurons in the preoptic nucleus of the goldish (Carassius auratus). Anat Rec. 1960 Dec;138:417–443. doi: 10.1002/ar.1091380404. [DOI] [PubMed] [Google Scholar]
  21. PAPPAS G. D., PURPURA D. P. Fine structure of dendrites in the superficial neocortical neuropil. Exp Neurol. 1961 Dec;4:507–530. doi: 10.1016/0014-4886(61)90049-8. [DOI] [PubMed] [Google Scholar]
  22. PARSONS D. F. A simple method for obtaining increased contrast in araldite sections by using postfixation staining of tissues with potassium permanganate. J Biophys Biochem Cytol. 1961 Nov;11:492–497. doi: 10.1083/jcb.11.2.492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. PEASE D. C. An electron microscopic study of red bone marrow. Blood. 1956 Jun;11(6):501–526. [PubMed] [Google Scholar]
  24. RICHARDSON K. C., JARETT L., FINKE E. H. Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol. 1960 Nov;35:313–323. doi: 10.3109/10520296009114754. [DOI] [PubMed] [Google Scholar]
  25. RINEHART J. F. Electron microscopic studies of sectioned white blood cells and platelets; with observations on the derivation of specific granules from mitochondria. Am J Clin Pathol. 1955 Jun;25(6):605–619. doi: 10.1093/ajcp/25.6.605. [DOI] [PubMed] [Google Scholar]
  26. ROSENBLUTH J., WISSIG S. L. THE DISTRIBUTION OF EXOGENOUS FERRITIN IN TOAD SPINAL GANGLIA AND THE MECHANISM OF ITS UPTAKE BY NEURONS. J Cell Biol. 1964 Nov;23:307–325. doi: 10.1083/jcb.23.2.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. SABATINI D. D., BENSCH K., BARRNETT R. J. Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J Cell Biol. 1963 Apr;17:19–58. doi: 10.1083/jcb.17.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. SCHARRER E., BROWN S. Neurosecretion. XII. The formation of neurosecretory granules in the earthworm, Lumbricus terrestris L. Z Zellforsch Mikrosk Anat. 1961;54:530–540. doi: 10.1007/BF00340453. [DOI] [PubMed] [Google Scholar]
  29. WATSON M. L. Staining of tissue sections for electron microscopy with heavy metals. J Biophys Biochem Cytol. 1958 Jul 25;4(4):475–478. doi: 10.1083/jcb.4.4.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. WELLINGS S. R., PHILP J. R. THE FUNCTION OF THE GOLGI APPARATUS IN LACTATING CELLS OF THE BALB/CCRGL MOUSE. AN ELECTRON MICROSCOPIC AND AUTORADIOGRAPHIC STUDY. Z Zellforsch Mikrosk Anat. 1964 Jan 31;61:871–882. doi: 10.1007/BF00340040. [DOI] [PubMed] [Google Scholar]
  31. ZUCKER-FRANKLIN D., HIRSCH J. G. ELECTRON MICROSCOPE STUDIES ON THE DEGRANULATION OF RABBIT PERITONEAL LEUKOCYTES DURING PHAGOCYTOSIS. J Exp Med. 1964 Oct 1;120:569–576. doi: 10.1084/jem.120.4.569. [DOI] [PMC free article] [PubMed] [Google Scholar]

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