Summary
The jejunal absorptive cells of the salamander Amphiuma, when examined using transmission electron microscopy, were found to possess a unique type of intracellular vacuole containing membranous tubules. These vanoles, tentatively named multitubular bodies, were located in the cytoplasm between the nucleus and the brush-border membrane, and were seen with greatest frequency in the summer and fall. The vacuoles containing multitubular bodies had an average diameter of 0.6 μm, and the membranous tubules within had an average diameter of 30 nm. The tubules differed morphologically from the vesicles in the multivesicular bodies, and from the primary lysosomes in the polylysosomal vacuoles. The tubules did not exhibit acid phosphatase activity, and were of similar diameter and membrane thickness as the Golgi saccules. In contrast to the multivesicular bodies, the multitubular bodies did not take up exogenous horseradish peroxidase. Early forms of autophagosomes resembling these vacuoles were often seen in the para-Golgi region of the cell. The multitubular bodies may represent a distinct type of autophagosome. Although the exact origin of the tubules as well as their role in cellular activity is unclear, their seasonal appearance within the multitubular bodies of the absorptive cells suggests a unique means of selective down-regulation of Golgi-like organelles.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ashford TP, Porter KR (1962) Cytoplasmic components in hepatic cell lysosomes. J Cell Biol 12: 198–202
Barka T (1963) Fat absorption and acid phosphatase activity in the intestinal epithelium of mice. JAMA 183:761–764
Behnke O (1963) Demonstration of acid phosphatase-containing granules and cytoplasmic bodies in the epithelium of fetal rat duodenum during certain stages of differentiation. J Cell Biol 18:251–265
Cardell RR, Badenhausen S, Porter KR (1967) Intestinal triglyceride absorption in the rat: An electron microscopical study. J Cell Biol 34:123–154
Cornell R, Walker WA, Isselbacher KJ (1971) Small intestinal absorption of horseradish peroxidase: A cytochemical study. Lab Invest 25:42–48
Friend DS (1969) Cytochemical staining of multivesicular body and Golgi vesicles. J Cell Biol 41:269–279
Friend DS, Murray MJ (1965) Osmium impregnation of the Golgi apparatus. Am J Anat 117:135–149
Gueze HJ, Slot JW, Strous GJAM, Lodish HF, Schwartz AL (1983) Intracellular site of asialoglycoprotein receptor-ligand uncoupling: double-label immunoelectron microscopy during receptor-mediated endocytosis. Cell 37:277–287
Harding C, Heuser J, Stahl P (1983) Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol 97:329–339
Iida H, Yamamoto T (1984) Morphological studies of the goldfish hindgut mucosa in organ culture. Cell Tissue Res 238:523–528
Iida H, Yamamoto T (1985) Intracellular transport of horseradish peroxidase in the absorptive cells of goldfish hindgut in vitro, with special reference to the cytoplasmic tubules. Cell Tissue Res 240:553–560
Iida H, Shibata Y, Yamamoto T (1986) The endosome-lysosome system in the absorptive cells of goldfish hindgut. Cell Tissue Res 243:449–452
Imon MA, White JF (1984) Association between HCO −3 absorption and K+ uptake by Amphiuma jejunum: relations among HCO −3 absorption, luminal K+ and intracellular K+ activity. Am J Physiol 246 (Gastrointest Liver Physiol 9):G732–G744
John TM, George JC (1985) Seasonal ultrastructural changes in the anterior pituitary of the migratory Canadian goose: 3. Autumn (fall) migration. Cytobios 42:99–116
Madara JL, Trier JS (1987) Functional morphology of the mucosa of the small intestine. In: Johnson LR (ed) Physiology of the Gastrointestinal Tract, 2nd Edition. Raven Press, New York, 1987, pp 1209–1249
Marzella L, Glaumann H (1987) Autophagy, microautophagy and crinophagy as mechanisms for protein degradation. In: Glaumann H, Ballard FJ (eds) Lysosomes: their role in protein breakdown. Academic Press, London, pp 319
Marzella L, Ahlberg J, Glaumann H (1981) Autophagy, heterophagy, microautophagy and crinophagy as the means for intracellular degradation. Virchows Arch [B] 36:219–234
Marzella L, Yu QC, Mergner WJ, Trump BF (1984) Unbuffered osmium staining of cell organelles: alterations induced by cell injury. Virchows Arch [B] 45:273–288
McDowell EM (1974) Unbuffered osmium staining in pars recta of the proximal tubules from rat kidney studies by thin and semithin section cytochemistry. Histochemistry 39:335–344
Moe H, Behnke O (1962) Cytoplasmic bodies containing mitochondria, ribosomes, and rough surfaced endoplasmic membranes in the epithelium of the small intestine of newborn rats. J Cell Biol 13:168–171
Mortimore GE (1982) Mechanisms of cellular protein catabolism. Nutr Rev 40:1–12
Mortimore GE, Hutson NJ, Surmacz CA (1983) Quantitative correlation between proteolysis and macro- and microautophagy in mouse hepatocytes during starvation and refeeding. Proc Natl Acad Sci USA 80:2179–2183
Ogawa K, Masutani K, Shinonaga Y (1962) Electron histochemical demonstration of acid phosphatase in the normal rat jejunum. J Histochem Cytochem 10:228–229
Pfeifer U (1973) Cellular autophagy and cell atrophy in the rat liver during long-term starvation: a quantitative morphological study with regard to diurnal variations. Virchows Arch [B] 12:195
Resau JH, Marzella L, Trump BF, Jones RT (1984) Degradation of zymogen granules by lysosomes in cultured pancreatic explants. Am J Pathol 115:134–150
Robinson JM, Karnovsky MJ (1983) Ultrastructural localization of several phosphatases with cerium. J Histochem Cytochem 31:1197–1208
Schnell AH, Borg LAH (1985) Lysosomes and pancreatic islet function: glucose-dependent alterations of lysosomal morphology. Cell Tissue Res 239:537–545
Smith RE, Farquhar MG (1966) Lysosome function in the regulation of the secretory process in cells of the anterior pituitary gland. J Cell Biol 31:319–347
Thyberg J, Blombren K, Hellgren D, Hedin U (1982) Lysosomophagy in cultured macrophages treated with the anti-microtubular drug nocodazole. Eur J Cell Biol 27:279–288
Trier JS, Rubin CE (1965) Electron microscopy of the small intestine: A review. Gastroenterology 49:574–603
Trier JS, Phelps PC, Eidelman S, Rubin CE (1965) Wipple's disease: Light and electron microscopic correlation of jejunal mucosal histology with antibiotic treatment and clinical status. Gastroenterology 48:684–707
Walker WA, Cornell R, Davenport LM, Isselbacher KJ (1972) Macromolecular absorption: Mechanism of horseradish peroxidase uptake and transport in adult and neonatal rat intestine. J Cell Biol 54:195–205
Weibel ER (1979) Stereologic methods. Vol I, Practical methods for biological morphometry. Academic Press, London
Weibel ER, Staubli W, Gnagi HR, Hess FA (1969) Correlated morphometric and biochemical studies on the liver cell. I. Morphometric model, stereologic methods, and normal morphometric data for rat liver. J Cell Biol 42:68–91
White JF, Britanisky R (1986) Adrenergic agents stimulate and cholinergic agents inhibit H+ secretion by amphibian jejunum. Am J Physiol 251:G405-G412
White JF, Hinton CF (1988) Norepinephrine induces Na+-H+ and Cl−-HCO −3 exchange in Amphiuma intestine: locus and responses to amiloride. Am J Physiol 255:G18-G26
Yamashiro DJ, Tycko B, Fluss SR, Maxfield FR (1984) Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway. Cell 37:789–800
Yu QC, Marzella L (1986) Modification of lysosomal protein degradation in mouse liver with taxol. Am J Pathol 122:553–561
Yu QC, Marzella L (1988a) Response of autophagic protein degradation to physiologic and pathologic stimuli in rat hepatocyte monolayer cultures. Lab Invest 58:643–652
Yu QC, Marzella L (1990) Pathobiology of lysosomes. In: Mergner WJ, Jones RT, Trump BF (eds) Cell death: mechanisms and Propagation, vol. 1, Feld & Wood, Philadelphia (in press)
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Yu, QC., White, J.F. Multitubular bodies in intestinal cells of Amphiuma means/tridactylum (Urodela): ultrastructural characterization. Cell Tissue Res 261, 163–171 (1990). https://doi.org/10.1007/BF00329449
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00329449