Summary
The occurrence of peroxisomes, their morphogenesis during the process of sebaceous transformation and their spatial relationship to the endoplasmic reticulum and lipid droplets were investigated by light and electron microscopy after visualization of the peroxidatic activity of catalase using an alkaline diaminobenzidine medium. The morphological alterations of peroxisomes display a characteristic sequence:
-
(1)
During cellular differentiation, a remarkable proliferation of exclusively tubular, diaminobenzidine-reactive peroxisomes occurs.
-
(2)
As maturation proceeds, an extensive elongation of tubular peroxisomes is seen. Concomitantly, they are densely packed in a regular, hexagonal arrangement and both the diameter and the catalase content gradually decreases. The most conspicuous feature of mature glandular cells are numerous highly organized aggregates of tubular, almost unstained peroxisomes with a diameter of 50 nm, arranged in a hexagonal pattern. They resemble adjacent tubular profiles of smooth endoplasmic reticulum. However, membrane continuities between these two compartments were never observed.
-
(3)
During lethal disintegration peroxisomes subsequently decrease in number, probably by rapid sequestration within autophagolysosomes.
The role of tubular peroxisomes in the biosynthesis of wax esters in the mouse Meibomian gland is discussed.
Similar content being viewed by others
References
Ahlabo, I. &Barnard, I. (1971) Observations on peroxisomes in brown adipose tissue of the rat.J. Histochem. Cytochem. 19, 670–5.
Baron, C. &Blough, H. A. (1976) Composition of the neutral lipids of bovine lipid meibomian secretions.J. Lipid Res. 17, 373–6.
Bell, M. (1970) A comparative study of sebaceous gland ultrastructure in subhuman primates. I.Galago crassicaudatus, G. senegalensis, andG. demidovii.Anat. Rec. 166, 213–224.
Bell, M. (1974) A comparative study of the ultrastructure of the sebaceous glands of man and other primates.J. invest. Derm. 62, 132–43.
Bishop, J. E., Davis, P. A. &Hajra, A. K. (1979) Properties and subcellular localization of long chain alcohol synthase in developing rat brain.Fedn Proc. fedn Am. Socs exp. 38, 515.
Bishop, J. E., Hajra, A. K. (1981) Mechanism and specificity of formation of long chain alcohols by developing rat brain.J. biol. Chem. 256, 9542–50.
Bishop, J. E., Salem, M. &Hajra, A. K. (1982) Topographical distribution of lipid biosynthetic enzymes on peroxisomes (microbodies).Ann. N.Y. Acad. Sci. 386, 411–3.
Böck, P., Goldenberg, H., Hüttinger, M., Kolar, M. &Kramar, R. (1975) Preparation and characterization of catalase-positive particles (‘microperoxisomes’) from Harder's gland of the rat.Expl Cell Res. 90, 15–9.
Böck, P., Kramar, R. &Pavelka, M. (1980) Peroxisomes and related particles in animal tissues.Cell Biol. Monograph 7. Wien, New York: Springer.
Brandes, D. &Bertini, F. (1965) Role of lysosomes in cellular lytic processes. II. Cell death during holocrine secretion in sebaceous glands.Exp. mol. Path. 4, 245–65.
Downing, D. T., Strauss, J. S. (1974) Synthesis and composition of surface lipids of human skin.J. invest. Derm. 62, 228–44.
Fine, S. &Yanoff, M. (1979)Ocular Histology. A Text and Atlas 2nd edition. New York, San Francisco, London: Harper & Row.
Gorgas, K. (1982) Serial section analysis of peroxisomal shape and membrane relationships in the mouse preputial gland.Ann. N.Y. Acad. Sci. 386, 519–22.
Gorgas, K. &Völkl, A. (1983) Tubuläre Peroxisomenaggregate in der Meibomschen Drüseder Maus.Anat. Anz. 153, 273.
Gorgas, K. &Yokota, S. (1980) Peroxisomes in sebaceous glands. III. Morphological similarities of peroxisomes with smooth endoplasmic reticulum and Golgi stacks in the circumanal gland of the dog.Anat. Embryol. 169, 9–20.
Grigor, M. R. (1976) The age-related occurrence of wax esters in the mouse preputial gland tumour.Biochim. biophys. Acta. 431, 157–64.
Grigor, M. R. &Harris, E. L. (1977) Wax ester synthesis in the mouse preputial gland tumour.Biochim. biophys. Acta 488, 121–7.
Gulyas, B. J. &Yuan, L. C. (1975) Microperoxisomes in the late pregnancy corpus luteum of Rhesus monkeys (Macaca mulatta).J. Histochem. Cytochem. 23, 359–68.
Gulyas, B. J. &Yuan, L. C. (1977) Association of microperoxisomes with the endoplasmic reticulum in the granulosa lutein cells of the Rhesus monkey (Macaca mulatta).Cell Tiss. Res. 179, 357–66.
Hajra, A. K. &Bishop, J. E. (1982) Glycerolipid biosynthesis in peroxisomes via the acyl dihydroxyacetone phosphate pathway.Ann. N.Y. Acad. Sci. 386, 170–82.
Hajra, A. K., Burke, C. L. &Jones, C. L. (1979) Subcellular localization of acyl coenzyme A: dihydroxyacetone phosphate acyltransferase in rat liver peroxisomes (microbodies).J. biol. Chem. 254, 10896–900.
Hruban, Z., Vigil, E. L. &Martan, J. (1971) Microbodies (peroxisomes) in sebaceous glands. In29th Annual Proceedings of the Electron Microscopy Society of America (edited byArceneaux, C. J.), pp. 526–7. Boston: Baton Rouge, Claitor's Publishing Division.
Hruban, Z., Vigil, E. L., Slesers, A. &Hopkins, E. (1972) Microbodies. Constituent organelles of animal cells.Lab. Invest. 279, 184–91.
Jester, J. V., Nicolaides, N. &Smith, R. E. (1981) Meibomian gland studies: histologic and ultrastructural investigations.Invest. Ophthalmol. Vis. Sci. 20, 537–47.
Karnovsky, M. J. (1971) Use of ferrocyanide-reduced osmium tetroxide in electron microscopy.J. Cell Biol. Abstract284.
Lazarow, P. B. (1978) Rat liver peroxisomes catalyze the β-oxidation of fatty acids.J. biol. Chem. 253, 1522–8.
Lazarow, P. B., De Duve, C. (1976) A fatty acyl-CoA oxidizing system in rat liver peroxisomes; enhancement by clofibrate, a hypolipidemic drug.Proc. Natn. Acad. Sci. USA 73, 2043–6.
Lazarow, P. B., Shio, H. &Robbi, M. (1980) Biogenesis of peroxisomes and the peroxisome reticulum hypothesis. In31st Moosbach Colloquim: Biological Chemistry of Organelle Formation (edited byBücher, T., Sebald, W. andWeiss, H.), pp. 187–206. New York: Springer.
Leeson, T. S. (1963) Tarsal (Meibomian) glands of the rat.Brit. J. Ophthal. 47, 222–31.
Lehir, M., Herzog, V. &Fahimi, H. D. (1979) Cytochemical detection of catalase with 3,3′-diaminobenzidine. A quantitative reinvestigation of the optimal conditions.Histochemistry 64, 51–66.
Maron, B. J. &Ferrans, V. J. (1974) Aggregates of tubules in human cardiac muscle cells.J. molec. cell Cardiol. 6, 249–64.
Moore, C. &Snyder, F. (1979) Partial characterization of acyl-CoA reductase from mouse preputial glands.Fedn Proc. Fedn Am. Socs exp. 38, 310.
Nicolaides, N. (1974) Skin lipids: Their biochemical uniqueness.Science 186, 19–26.
Nicolaides, N., Fu, H. C. &Ansari, M. N. A. (1970) Diester waxes in surface lipids of animal skin.Lipids 5, 299–307.
Nicolaides, N., Fu, H. C. &Rice, G. R. (1968) The skin surface lipids of man compared with those of eighteen species of animals.J. invest. Dermatol. 51, 83–9.
Nicolaides, N., Kaitaranta, J. K., Rawdah, T. N., Macy, J. I., Boswell, F. M. III &Smith, R. E. (1981) Meibomian gland studies: comparison of steer and human lipids.Invest. Ophthal. Vis. Sci. 20, 522–36.
Nikkari, T. (1974) Comparative chemistry of sebum.J. invest. Dermatol. 62, 257–67.
Novikoff, P. M. &Novikoff, A. B. (1972) Peroxisomes in absorptive cells of mammalian small intestine.J. Cell Biol. 53, 532–60.
Novikoff, A. B. &Novikoff, P. M. (1973a) Microperoxisomes.J. Histochem. Cytochem. 21, 963–6.
Novikoff, A. B., Novikoff, P. M., Davis, C. &Quintana, N. (1972) Studies on microperoxisomes. II. A cytochemical method for light and electron microscopy.J. Histochem. Cytochem. 20, 1006–23.
Novikoff, A. B., Novikoff, P. M., Davis, C. &Quintana, N. (1973b) Studies on microperoxisomes. V. Are microperoxisomes ubiquitous in mammalian cells?J. Histochem. Cytochem. 21, 737–55.
Novikoff, A. B., Novikoff, P. M., Rosen, O. M. &Rubin, Ch. S. (1980) Organelle relationships in cultured 3T3-L1 preadipocytes.J. Cell Biol. 87, 180–96.
Palay, S. L. (1958) The morphology of secretion. InFrontiers in Cytology (edited byPalay, S. L.), pp. 305–42. New Haven: Yale University Press.
Parakkal, P. F. &Matoltsy, A. G. (1964) The fine structure of the lipid droplets in the Meibomian gland of the mouse.J. Ulstrastruct. Res. 10, 417–21.
Pavelka, M., Goldenberg, H., Hüttinger, M. &Kramar, R. (1976) Enzymic and morphological studies on catalase positive particles from brown fat of cold adapted rats.Histochemistry 50, 47–55.
Potter, J. E. R., Prutkin, L. &Wheatley, V. R. (1979) Sebaceous gland differentiation. I. Separation, morphology and lipogenesis of isolated cells from the mouse preputial gland tumon.J. invest. Dermatol. 72, 120–7.
Reddy, J. &Svoboda, D. (1972) Microbodies in Leydig cell tumors of rat testis.J. Histochem. Cytochem. 20, 793–803.
Reddy, J., Svoboda, D., Azarnoff, D. &Dawar, R. (1973) Cadmium-induced Leydig cell tumors of rat testis: Morphologic and cytochemical study.J. natn Cancer Inst. 51, 891–903.
Reynolds, E. S. (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy.J. Cell Biol. 17, 208–29.
Richardson, K. C., Jarett, L. &Finke, E. H. (1960) Embedding in epoxy resins for ultrathin sectioning in electron microscopy.Stain Technol. 35, 313–25.
Robison, W. G. &Kuwabara, T. (1975) Microperoxisomes in retinal pigment epithelium.Invest. Ophthal. 14, 866–72.
Sansone, G. &Hamilton, J. G. (1969) Glyceryl ether, wax ester and triglyceride composition of the mouse preputial gland.Lipids 4, 435–40.
Snyder, F. (1972) The enzymic pathways of ether-linked lipids and their precursors. InEther Lipids: Chemistry and Biology (edited bySnyder, F.), pp. 121–56. New York: Academic Press.
Snyder, F. &Blank, M. L. (1969) Relationships of chain lengths and double bond locations inO-alkyl,O-alkyl-1-enyl, acyl, and fatty alcohol moieties in preputial glands of mice.Arch. Biochem. Biophys. 130, 101–10.
Snyder, F. &Malone, B. (1970) Enzymic interconversion of fatty alcohols and fatty acids.Biochem. Biophys. Res. Commun. 41, 1382–7.
Tiffany, J. M. (1978) Individual variations in human meibomian lipid composition.Exp. Eye Res. 27, 289–300.
Weingeist, T. A. (1972) The glands of the ocular adnexa.Int. Ophthalmol. Clin. 13, 243–61.
Wheatley, V. R. &James, A. T. (1957) Studies on sebum. 7. The composition of the sebum of some common rodents.Biochem. J. 65, 36–42.
Wheatley, V. R., Potter, J. E. R. &Lew, G. (1979) Sebaceous gland differentiation: II. The isolation, separation and characterization of cells from the mouse preputial gland.J. invest. Derm. 73, 291–6.
Author information
Authors and Affiliations
Additional information
This paper is dedicated to Professor Dr H. Leonhardt on the occasion of his 65th birthday.
Rights and permissions
About this article
Cite this article
Gorgas, K., Völkl, A. Peroxisomes in sebaceous glands. IV. Aggregates of tubular peroxisomes in the mouse Meibomian gland. Histochem J 16, 1079–1098 (1984). https://doi.org/10.1007/BF01002896
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF01002896