Abstract
A morphological basis for transcellular potassium transport in the midgut of the mature fifth instar larvae of Hyalophora cecropia has been established through studies with the light and electron microscopes. The single-layered epithelium consists of two distinct cell types, the columnar cell and the goblet cell. No regenerative cells are present. Both columnar and goblet cells rest on a well developed basement lamina. The basal portion of the columnar cell is incompletely divided into compartments by deep infoldings of the plasma membrane, whereas the apical end consists of numerous cytoplasmic projections, each of which is covered with a fine fuzzy or filamentous material. The cytoplasm of this cell contains large amounts of rough endoplasmic reticulum, microtubules, and mitochondria. In the basal region of the cell the mitochondria are oriented parallel to the long axes of the folded plasma-lemma, but in the intermediate and apical portions they are randomly scattered within the cytoplasmic matrix. Compared to the columnar cell, the goblet cell has relatively little endoplasmic reticulum. On the other hand, the plications of the plasma membrane of the goblet cell greatly exceed those of the columnar cell. One can distinguish at least four characteristic types of folding: (a) basal podocytelike extensions, (b) lateral evaginations, (c) apical microvilli, and (d) specialized cytoplasmic projections which line the goblet chamber. Apically, the projections are large and branch to form villus-like units, whereas in the major portion of the cavity each projection appears to contain an elongate mitochondrion. Junctional complexes of similar kind and position appear between neighboring columnar cells and between adjacent columnar and goblet cells as follows: a zonula adherens is found near the luminal surface and is followed by one or more zonulae occludentes. The morphological data obtained in this study and the physiological information on ion transport through the midgut epithelium have encouraged us to suggest that the goblet cell may be the principal unit of active potassium transport from the hemolymph to the lumen of the midgut. We have postulated that ion accumulation by mitochondria in close association with plicated plasma membranes may play a role in the active movement of potassium across the midgut.
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- ANDERSON E. OOCYTE DIFFERENTIATION AND VITELLOGENESIS IN THE ROACH PERIPLANETA AMERICANA. J Cell Biol. 1964 Jan;20:131–155. doi: 10.1083/jcb.20.1.131. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ashworth L. A., Green C. Plasma membranes: phospholipid and sterol content. Science. 1966 Jan 14;151(3707):210–211. doi: 10.1126/science.151.3707.210. [DOI] [PubMed] [Google Scholar]
- BEAMS H. W., TAHMISIAN T. N., DEVINE R. L. Electron microscope studies on the cells of the malpighian tubules of the grasshopper (Orthoptera, Acrididae). J Biophys Biochem Cytol. 1955 May 25;1(3):197–202. doi: 10.1083/jcb.1.3.197. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Benedetti E. L., Emmelot P. Electron microscopic observations on negatively stained plasma membranes isolated from rat liver. J Cell Biol. 1965 Jul;26(1):299–305. doi: 10.1083/jcb.26.1.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
- CHOI J. K. The fine structure of the urinary bladder of the toad, Bufo marinus. J Cell Biol. 1963 Jan;16:53–72. doi: 10.1083/jcb.16.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
- CHOWDHURY T. K., SNELL F. M. A MICROELECTRODE STUDY OF ELECTRICAL POTENTIALS IN FROG SKIN AND TOAD BLADDER. Biochim Biophys Acta. 1965 Mar 29;94:461–471. doi: 10.1016/0926-6585(65)90054-3. [DOI] [PubMed] [Google Scholar]
- COPELAND E. A MITOCHONDRIAL PUMP IN THE CELLS OF THE ANAL PAPILLAE OF MOSQUITO LARVAE. J Cell Biol. 1964 Nov;23:253–263. doi: 10.1083/jcb.23.2.253. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Copeland E. Salt transport organelle in Artemia salenis (brine shrimp). Science. 1966 Jan 28;151(3709):470–471. doi: 10.1126/science.151.3709.470. [DOI] [PubMed] [Google Scholar]
- FARQUHAR M. G., PALADE G. E. Junctional complexes in various epithelia. J Cell Biol. 1963 May;17:375–412. doi: 10.1083/jcb.17.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
- FAWCETT D. W. Physiologically significant specializations of the cell surface. Circulation. 1962 Nov;26:1105–1132. doi: 10.1161/01.cir.26.5.1105. [DOI] [PubMed] [Google Scholar]
- FAWCETT D. W. SURFACE SPECIALIZATIONS OF ABSORBING CELLS. J Histochem Cytochem. 1965 Feb;13:75–91. doi: 10.1177/13.2.75. [DOI] [PubMed] [Google Scholar]
- 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]
- Gupta B. L., Berridge M. J. A coat of repeating subunits on the cytoplasmic surface of the plasma membrane in the rectal papillae of the blowfly, Calliphora erythrocephala (Meig.), studied in situ by electron microscopy. J Cell Biol. 1966 May;29(2):376–382. doi: 10.1083/jcb.29.2.376. [DOI] [PMC free article] [PubMed] [Google Scholar]
- HARVEY W. R., NEDERGAARD S. SODIUM-INDEPENDENT ACTIVE TRANSPORT OF POTASSIUM IN THE ISOLATED MIDGUT OF THE CECROPIA SILKWORM. Proc Natl Acad Sci U S A. 1964 May;51:757–765. doi: 10.1073/pnas.51.5.757. [DOI] [PMC free article] [PubMed] [Google Scholar]
- HASKELL J. A., CLEMONS R. D., HARVEY W. R. ACTIVE TRANSPORT BY THE CECROPIA MIDGUT. I. INHIBITORS, STIMULANTS, AND POTASSIUM-TRANSPORT. J Cell Physiol. 1965 Feb;65:45–55. doi: 10.1002/jcp.1030650107. [DOI] [PubMed] [Google Scholar]
- HOKIN L. E., HOKIN M. R. Studies on the carrier function of phosphatidic acid in sodium transport. I. The turnover of phosphatidic acid and phosphoinositide in the avian salt gland on stimulation of secretion. J Gen Physiol. 1960 Sep;44:61–85. doi: 10.1085/jgp.44.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
- HOKIN M. R. STUDIES ON A NA+ + K+-DEPENDENT, OUABAIN-SENSITIVE ADENOSINE TRIPHOSPHATASE IN THE AVIAN SALT GLAND. Biochim Biophys Acta. 1963 Sep 3;77:108–120. doi: 10.1016/0006-3002(63)90473-6. [DOI] [PubMed] [Google Scholar]
- ITO S., WINCHESTER R. J. The fine structure of the gastric mucosa in the bat. J Cell Biol. 1963 Mar;16:541–577. doi: 10.1083/jcb.16.3.541. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Imamura A., Takeda H., Sasaki N. The accumulation of sodium and calcium in a specific layer of frog skin. J Cell Physiol. 1965 Oct;66(2):221–225. doi: 10.1002/jcp.1030660208. [DOI] [PubMed] [Google Scholar]
- Ito S. The enteric surface coat on cat intestinal microvilli. J Cell Biol. 1965 Dec;27(3):475–491. doi: 10.1083/jcb.27.3.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
- KANNO Y., LOEWENSTEIN W. R. INTERCELLULAR DIFFUSION. Science. 1964 Feb 28;143(3609):959–960. doi: 10.1126/science.143.3609.959. [DOI] [PubMed] [Google Scholar]
- KANNO Y., LOEWENSTEIN W. R. LOW-RESISTANCE COUPLING BETWEEN GLAND CELLS. SOME OBSERVATIONS ON INTERCELLULAR CONTACT MEMBRANES AND INTERCELLULAR SPACE. Nature. 1964 Jan 11;201:194–195. doi: 10.1038/201194a0. [DOI] [PubMed] [Google Scholar]
- Kafatos F. C., Williams C. M. Enzymatic Mechanism for the Escape of Certain Moths from Their Cocoons. Science. 1964 Oct 23;146(3643):538–540. doi: 10.1126/science.146.3643.538. [DOI] [PubMed] [Google Scholar]
- Kaye G. I., Cole J. D., Donn A. Electron microscopy: sodium localization in normal and ouabain-treated transporting cells. Science. 1965 Nov 26;150(3700):1167–1168. doi: 10.1126/science.150.3700.1167. [DOI] [PubMed] [Google Scholar]
- LAUFER H. Forms of enzymes in insect development. Ann N Y Acad Sci. 1961 Nov 2;94:825–835. doi: 10.1111/j.1749-6632.1961.tb35576.x. [DOI] [PubMed] [Google Scholar]
- LINNANE A. W., VITOLS E., NOWLAND P. G. Studies on the origin of yeast mitochondria. J Cell Biol. 1962 May;13:345–350. doi: 10.1083/jcb.13.2.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LOEWENSTEIN W. R., KANNO Y. STUDIES ON AN EPITHELIAL (GLAND) CELL JUNCTION. I. MODIFICATIONS OF SURFACE MEMBRANE PERMEABILITY. J Cell Biol. 1964 Sep;22:565–586. doi: 10.1083/jcb.22.3.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LUFT J. H. Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol. 1961 Feb;9:409–414. doi: 10.1083/jcb.9.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Loewenstein W. R., Socolar S. J., Higashino S., Kanno Y., Davidson N. Intercellular Communication: Renal, Urinary Bladder, Sensory, and Salivary Gland Cells. Science. 1965 Jul 16;149(3681):295–298. doi: 10.1126/science.149.3681.295. [DOI] [PubMed] [Google Scholar]
- PEACHEY L. D. ELECTRON MICROSCOPIC OBSERVATIONS ON THE ACCUMULATION OF DIVALENT CATIONS IN INTRAMITOCHONDRIAL GRANULES. J Cell Biol. 1964 Jan;20:95–111. doi: 10.1083/jcb.20.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
- PEACHEY L. D., RASMUSSEN H. Structure of the toad's urinary bladder as related to its physiology. J Biophys Biochem Cytol. 1961 Aug;10:529–553. doi: 10.1083/jcb.10.4.529. [DOI] [PMC free article] [PubMed] [Google Scholar]
- PEASE D. C. Fine structures of the kidney seen by electron microscopy. J Histochem Cytochem. 1955 Jul;3(4):295–308. doi: 10.1177/3.4.295. [DOI] [PubMed] [Google Scholar]
- PEASE D. C. Infolded basal plasma membranes found in epithelia noted for their water transport. J Biophys Biochem Cytol. 1956 Jul 25;2(4 Suppl):203–208. doi: 10.1083/jcb.2.4.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
- PHILPOTT C. W., COPELAND D. E. FINE STRUCTURE OF CHLORIDE CELLS FROM THREE SPECIES OF FUNDULUS. J Cell Biol. 1963 Aug;18:389–404. doi: 10.1083/jcb.18.2.389. [DOI] [PMC free article] [PubMed] [Google Scholar]
- ROSSI C. S., LEHNINGER A. L. STOICHIOMETRIC RELATIONSHIPS BETWEEN ACCUMULATION OF IONS BY MITOCHONDRIA AND THE ENERGY-COUPLING SITES IN THE RESPIRATORY CHAIN. Biochem Z. 1963;338:698–713. [PubMed] [Google Scholar]
- ROTH T. F., PORTER K. R. YOLK PROTEIN UPTAKE IN THE OOCYTE OF THE MOSQUITO AEDES AEGYPTI. L. J Cell Biol. 1964 Feb;20:313–332. doi: 10.1083/jcb.20.2.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- SKOU J. C. ENZYMATIC BASIS FOR ACTIVE TRANSPORT OF NA+ AND K+ ACROSS CELL MEMBRANE. Physiol Rev. 1965 Jul;45:596–617. doi: 10.1152/physrev.1965.45.3.596. [DOI] [PubMed] [Google Scholar]
- Sharp G. W., Leaf A. Metabolic requirements for active sodium transport stimulated by aldosterone. J Biol Chem. 1965 Dec;240(12):4816–4821. [PubMed] [Google Scholar]
- VENABLE J. H., COGGESHALL R. A SIMPLIFIED LEAD CITRATE STAIN FOR USE IN ELECTRON MICROSCOPY. J Cell Biol. 1965 May;25:407–408. doi: 10.1083/jcb.25.2.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
- VOUTE C. L. AN ELECTRON MICROSCOPIC STUDY OF THE SKIN OF THE FROG (RANA PIPIENS). J Ultrastruct Res. 1963 Dec;52:497–510. doi: 10.1016/s0022-5320(63)80081-7. [DOI] [PubMed] [Google Scholar]
