Summary
In the present study we followed with the electron microscope the changes which the lipids undergo during their transport between the blood and the fat cells in both impletion and depletion of the fat depots. Impletion was studied in tissues from mice on the first or second day after birth, when the storage of fat begins, and from newborn mice and young rats that were refed after periods of starvation. Fat depots in the state of depletion were taken from the starving animals.
During impletion the chylomicrons were found to be attached to the endothelium of the capillaries in the fat organs, where they seem to break up into smaller and less electron-dense particles. The absorption of the lipids by the capillary endothelial cells could not be observed, since no osmiophilic material was found within the capillary wall. No such material was present within the interstitial connective tissue between capillaries and fat cell. When the lipids enter the fat cell they again become observable as osmiophilic granules. These lipomicrons seem to represent the absorbed lipid material in transit between the surface of the fat cells and the fat droplets in the cells. Although dispersed throughout the cytoplasm, the lipomicrons were often accumulated at, and attached to, the surface of the growing fat droplets. They lost their identity when they were incorporated into the homogeneous material of the fat droplets.
According to these observations, several steps were distinguished during impletion and were localized at the surface of the capillaries, at the plasma membrane of the fat cells, and at the surface of the fat droplet. The findings were discussed in the light of the physiological and biochemical literature concerning the clearance of the chylomicrons from the blood.
The static pictures of the fat cells in the depleting state are very similar to those of the impleting cells. Lipomicrons are present, and they seem to emerge from the surface of the diminishing fat droplets. Also in these cells they seem to represent the lipids in transit, but in the reverse direction. At the cell border they disappear, and no osmiophilic material could be discovered within the interstitial tissue or within the capillary wall. Occasionally osmiophilic globules were found within the capillaries of the depleting fat organs, but they did not show the same relationship to the endothelium as the chylomicrons. We concluded from the similarity between the static pictures of depleting and impleting cells that the processes distinguished and localized during impletion are reversed when the cell releases fat. If this is correct, our pictures illustrate the lability of the fat organs, which respond to changing conditions by reversing the processes involved in their twofold activity of absorbing and releasing fat. The lipomicron pool in the fat cell seems to represent the lipids most immediately available either for storage or for release under ordinary nutritional conditions, where such drastic changes as in our experimental material do not occur. During both impletion and depletion the mitochondria were found to be profoundly changed. It is believed that these changes are mainly due to an infiltration of the mitochondria by lipomicrons. However, these observations do not permit us to draw conclusions as to the function of the mitochondria in the storage or release of fat.
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References
Ashworth, C. J., V. A. Stembridge and E. Sanders: Lipid absorption, transport and hepatic assimilation studied with electron microscopy. Amer. J. Physiol. 198, 1326–1328 (1960).
Becker, J.: Über Eigentümlichkeiten des Fettgewebes in der frühesten Kindheit. Z. Anat. Entwickl.-Gesch. 92, 814–839 (1930).
Bragdon, J. H., and R. Gordon jr.: Tissue distribution of C14 after the intravenous injection of labeled chylomicrons and unesterified fatty acids in the rat. J. clin. Invest. 37, 575–578 (1958).
Chase, W. H.: Fine structure of rat adipose tissue. J. Ultrastruct. Res. 2, 283–287 (1959).
Clara, M.: Bau und Entwicklung des sogenannten Fettgewebes beim Vogel. Z. mikr.-anat. Forsch. 19, 32–113 (1929).
Dabelow, A.: Die Anatomie des Fettgewebes. Regensburg. Jb. ärztl. Fortbild. 5, 437–452 (1957).
- Die Entwicklung der Fettorgane (Wassermann) im subcutanen Gewebe menschlicher Feten (nach Untersuchungen an dicken Schnitten mit Gefäßinjektionen). Anat. Anz. 104 Erg.-H. Verh. der Anat. Ges. 54. Versig in Freiburg i.Br. 1958, S. 83–96.
Dalton, S. J., and M. D. Felix: Study of Golgi substance and ergastoplasm in series of mammalian cell types. In: Fine structure of cells. Symposium, 8th Congr. of Cell Biology, Leiden 1954, p. 274.
Dole, V. P.: The fatty acid pool in adipose tissue. J. biol. Chem. 236, 3121–3124 (1961).
Gage, S. H., and P. A. Fish: Fat digestion, absorption and assimilation in man and mammals as determined by the dark field microscope, and a fat-soluble dye. Amer. J. Anat. 34, 1–77 (1924).
Gersh, I., and M. A. Still: Blood vessels in fat tissue. Relations to problems of gas exchange. J. exp. Med. 81, No 2, 219–232 (1945).
Giese, W., u. R. Hoerstenbrock: Allgemeine Pathologie des exogenen quantitativen Nahrungsmangels. In: Handbuch der allgemeinen Pathologie, ed. by F. Büchner, E. Letterer u. F. Roulet, vol. I, part 1. Berlin-Göttingen-Heidelberg: Springer 1962.
Grütz, O.: Beiträge zur Histologie und Pathogenese der Adiponecrosis (Lipodystrophia) subcutanea neonatorum. Arch. Kinderheilk. 113, 200–211 (1938).
Hausberger, F. X.: Über die nervöse Regulation des Fettstoffwechsels. Klin. Wschr. 14, 1–8 (1935).
—: Über die Natur der efferenten und den funktionellen Nachweis afferenter Nervenfasern im Fettgewebe. Dtsch. Arch. klin. Med. 180, 274–287 (1937).
—: Über die Wachstums- und Entwicklungsfähigkeit transplantierter Fettgewebs-Keimlager von Ratten. Virchows Arch. path. Anat. 302, 640–656 (1938).
—: Quantitative studies on the development of autotransplants of immature adipose tissue of rats. Anat. Rec. 122, 507–516 (1955).
—, u. O. Gujot: Über die Veränderungen des Gehaltes an Fett-, Wasser-, Glykogen- und Trockensubstanz im wachsenden Fettgewebe junger Ratten. Naunyn-Schmiedeberg's Arch. exp. Path. Pharmak. 187, 647–654 (1937).
Havel, R. J., and D. T. Fredericksen: The metabolism of chylomicra. I. The removal of palmitic acid-1-C14 labeled chylomicra from dog plasma. J. clin. Invest. 35, 1025–1032 (1956).
—, and A. Goldfien: The role of the liver and of extrahepatic tissue in the transport and metabolism of fatty acids and triglycerides in the dog. J. Lipid Res. 2, 389–395 (1961).
Hayes, T. L., F. T. Lindgren and J. C. Schooley: Electron microscopy of chylomicrons. Semiannual Report Biology and Medicine, Donner Laboratory, Berkeley. UCRL-9897, pp. 91–95 (1961).
Hoffman, A.: Die Entwicklung des Fettgewebes beim Menschen. Z. mikr.-anat. Forsch. 56, 415–449 (1950).
Jeanrenaud, B.: Dynamic aspects of adipose tissue metabolism. Metabolism 10, 535–581 (1960).
Korn, E. D.: Clearing factor, a heparin-activated lipoprotein lipase. I. Isolation and characterization of the enzyme from normal rat heart. J. biol. Chem. 215, 1–14 (1955).
—: Clearing factor, a heparin-activated lipoprotein lipase. II. Substrate specificity and activation of coconut oil. J. biol. Chem. 215, 15–26 (1955).
Lever, J. D.: The fine structure of brown adipose tissue in the rat with observations on the cytological changes following starvation and adrenalectomy. Anat. Rec. 128, 361–372 (1957).
Liebelt, R. A.: Postnatal development of two types of fat depots in the NH and CBA inbred strains of mice. Amer. J. Anat. 105, 197–218 (1959).
Luft, J.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961).
Metzner, R.: Über die Beziehung der Granula zum Fettansatz. Arch. Anat. Physiol., Anat. Abt. 82–96 (1890).
Miller, J. E., and H. L. Eastlick: Studies on transplanted embryonic limbs. IV. The cytology of the “adipose tissue”. Trans. Amer. microscop. Soc. 71, 1–19 (1952).
Olson, R. E., and J. W. Vester: Nutrition-endocrine interrelationship in the control of fat transport in man. Physiol. Rev. 40, 677–733 (1960).
Paley, S. L., and L. D. Karlin: An electron microscopic study of the intestinal villus I. J. biophys. biochem. Cytol. 5, 363–372 (1959).
Rampone, A. J.: Rate of fat uptake by intestinal lymphatics. Proc. Soc. exp. Biol. (N.Y.) 108, 278–281 (1961).
Rodbell, M.: The removal and metabolism of chylomicrons by adipose tissue in vitro. J. biol. Chem. 235, 1613–1620 (1960).
Rosano, H. L., P. Duby and I. H. Schulman: Mechanism of the selective flux of salts and water migration through non-aqueous liquid membranes. J. physiol. Chem. 65, 1704–1708 (1960).
Schoenheimer, B., and D. Rittenberg: Deuterium as an indicator in the study of intermediary metabolism. III. The role of the fat tissues. J. biol. Chem. 111, 175–181 (1935).
—: VI. Synthesis and destruction of fatty acids in the organism. J. biol. Chem. 114, 381–390 (1936).
Shapiro, B.: Progress in the chemistry of fat, p. 178. London: Pergamon Press 1957.
—: Lipid dynamics in adipose tissue. In: Progress in the chemistry of fats and other lipids, vol. 4, p. 177–197. New York: Pergamon Press 1957.
—, L. Chowers and G. Rose: Fatty acids uptake and esterification in adipose tissue. Biochim. biophys. Acta (Amst.) 23, 115–120 (1957).
Swank, R. L., and L. W. Levy: Chylomicron dissolution. Dosage and site of heparin. Amer. J. Physiol. 171, 208–217 (1952).
Wassermann, F.: Die Fettorgane des Menschen. Entwicklung, Bau und systematische Stellung des sogenannten Fettgewebes. Z. Zellforsch. 3, 235–329 (1926).
—: Über die Bildung der Appendices epiploicae beim Menschen, besonders über die Entwicklung der Fettorgane in denselben. Verh. anat. Ges. (Jena) 36, 155–165 (1927).
—: Über Speicherung, Entspeicherung und Wiederspeicherung der Fettorgane. Anat. Anz., Erg.-Bd. 67, 181–194 (1929).
—: Die histologischen Grundlagen der Fettspeicherung. Z. Kreisl.-Forsch. 23, 665–687 (1931).
- Fettorgane und lymphatisches System. Sitzgsber. Ges. für Morphologie u. Physiologie, München, 42. Jahrg. 1933.
—, and T. F. McDonald: Electron microscopic investigation of the surface membrane structures of the fat-cell and of their changes during depletion of the cell. Z. Zellforsch. 52, 778–800 (1960).
—, and Thomas F. McDonald: Electron microscopic study concerning the pathway and metabolism of lipids between the blood and the fat cell. Anat. Rec. 139, 284 (1961).
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Work performed under the auspices of the U.S. Atomic Energy Commission.
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Wassermann, F., McDonald, T.F. Electron microscopic study of adipose tissue (fat organs) with special reference to the transport of lipids between blood and fat cells. Zeitschrift für Zellforschung 59, 326–357 (1963). https://doi.org/10.1007/BF00339791
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DOI: https://doi.org/10.1007/BF00339791