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Secretory Membranes and the Exocrine Storage Compartment

Richard S. Cameron, Peter Arvan, J. David Castle

10.1002/cphy.cp060307

Source: Supplement 18: Handbook of Physiology, The Gastrointestinal System, Salivary, Gastric, Pancreatic, and Hepatobiliary Secretion

Originally published: 1989

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Granule Formation and Storage
2 Granule Isolation and Preparation of Membrane Subfractions
2.1 Secretory Granules
2.2 Membrane Subfractions
3 Composition of Exocrine Granule Membranes
3.1 Membrane Lipids
3.2 Membrane Proteins
4 Storage Function and Biophysical Properties of Secretion Granules
4.1 Granule Packaging, Stability, and Osmotic Behavior
4.2 Ion Permeation of Granule Membranes
4.3 Intragranular pH and Buffering Capacity
4.4 Hydrogen‐ATPase Activity
5 Interactions With Cytoplasmic Proteins
5.1 Possible Roles of Microtubules
5.2 Microfilamentous Networks and Secretory Organelle Interactions
5.3 Other Polypeptides Binding to Secretory Membranes
5.4 Stimulus‐Enhanced Phosphorylation of Membrane and Associated Proteins
6 Exocytosis
7 Recycling, Turnover, and Sorting from Other Vesicular Traffic
7.1 Fate of Reinternalized Secretory Membrane
7.2 Secretory Membrane as a Plasmalemmal Protein Carrier
7.3 Secretory Membrane and Sorting Sites
Figure 1. Figure 1.

Low‐power electron micrograph of a rat parotid acinus consisting of functionally polarized secretory cells. Basolateral (BL) surfaces extend inward from the periphery and are separated from apical surfaces (A) by junctional complexes. Basal rough endoplasmic reticulum (ER) and centrally located extensive Golgi complexes (G) are evident. Secretory storage granules (SG; 1 μm diam) are collected near cell apices. Apical lumina are filled with discharged secretion. N, nucleus. Bar, 2 μm.
Figure 2. Figure 2.

Summary of an autoradiographic study of intracellular transport of newly synthesized secretory protein in rabbit parotid tissue. Tissue lobules were pulse labeled in vitro with [3H]leucine and subjected to chase incubation for the indicated times. Distributions of autoradiographic grains determined from electron‐macrograph autoradiograms are expressed as percent of total that were quantitated at each time point. Precursor‐product kinetic relationships between rough endoplasmic reticulum, Golgi complex, immature secretion granules, and mature secretion granules are apparent.

From Castle et al. 30
Figure 3. Figure 3.

Representative electron micrographs of a purified parotid secretion granule (A) and granule membrane fraction (B). With detailed consideration of the extent of contamination by residual mitochondria and incompletely removed secretory polypeptides as a basis, it is possible to estimate that 95% of the protein associated with the purified secretion granule membrane is bona fide granule membrane protein. Bars, 1 μm.

From Cameron and Castle 25
Figure 4. Figure 4.

Immunocytochemical demonstration of antigen distribution with heterologous antiserum to parotid secretory granule membranes. A, B: bars, 10 μm. Indirect immunofluorescent staining of 0.5‐μm‐thick frozen sections of parotid (A) and exocrine pancreas (B). Immunoreactivity is concentrated over secretion granule membrane profiles that are identified on the basis of their apical cytoplasmic location, size, and frequency. Staining is not detected in the basal cytoplasm, which contains abundant rough endoplasmic reticulum and mitochondria. C1–3: bar, 0.1 μm. Indirect immunolabeling with ferritin conjugates on isolated, aldehyde‐fixed parotid secretion granules. C2, ferritin decoration reveals that the granule membrane antiserum recognizes determinants on the cytosolic aspect of the granule membrane. No ferritin decorates secretory granules when preimmune serum (C1) or antiserum specific for content polypeptides (proline‐rich polypeptides (C3) is substituted for the membrane antiserum (C2). D‐F: bar, 10 μm. Indirect immunofluorescent staining of endocrine (epithelial and nonepithelial) and neural tissues with parotid granule membrane antibodies selected by adsorption for determinants on the cytoplasmic surface. For recovery of antibodies bound to intact parotid granules, granule suspensions were treated in 200 mM glycine (pH 2.8), and desorbed antibodies were recovered in supernate after sedimentation of granules through 0.75 M sucrose. Soluble IgG fractions served subsequently as the primary antiserum. D: 6‐μm‐thick frozen section of the CA3 region of rat hippocampus. SR, stratum radiatum; PL, pyramidal cell layer; SO, stratum oriens. Immunolabeling observed throughout the neuropile is particularly prominent adjacent to the pyramidal cell layer. Cell bodies and dendrites are unstained. E: 2‐μm‐thick frozen section of rat adrenal medulla. Chromaffin cells show a diffuse (or in some cases punctate) fluorescent pattern in the cytoplasm that is assumed to mark chromaffin granules. F: 4‐μm‐thick frozen section of rat liver. Label is associated with the bile canalicular surface and associated pericanalicular cellular organelles.

A and B from Cameron et al. 24
Figure 5. Figure 5.

Comparative two‐dimensional sodium dodecyl sulfate‐polyacrylamide gel electrophoretic analyses of purified exocrine secretory granule membrane polypeptides. Autoradiographic patterns obtained by parallel electrophoresis of radioiodinated (chloramine T) parotid and pancreas secretory granule membrane polypeptides. A: parotid pattern; 3 groups of polypeptides distinguished in the text on the basis of molecular weight are indicated by brackets (I‐III). B: solid arrow, position of pancreatic zymogen granule membrane protein GP‐2. Horizontal values, pH values; vertical values, molecular weight X 10−3.

From Cameron et al. 24
Figure 6. Figure 6.

Two‐dimensional electrophoretic analysis of rat liver Golgi secretory vesicle membranes. Autoradiogram of radioiodinated (chloramine T) membrane polypeptides from a sodium carbonate‐treated Golgi fraction 1 (GF1) fraction (A). Analogous polypeptides, especially 30,000‐Mr polypeptides, have similar (but not identical) mobilities. Even though this group of polypeptides are prominent radiolabeled species, they may not be such major constituents of the Golgi vesicle membrane as signified by their minor contributions to a Coomassie blue‐stained polypeptide profile (B). Horizontal values, pH values; vertical values, molecular weight X 10−3.

A from Ehrenreich et al. 55.


Figure 1.

Low‐power electron micrograph of a rat parotid acinus consisting of functionally polarized secretory cells. Basolateral (BL) surfaces extend inward from the periphery and are separated from apical surfaces (A) by junctional complexes. Basal rough endoplasmic reticulum (ER) and centrally located extensive Golgi complexes (G) are evident. Secretory storage granules (SG; 1 μm diam) are collected near cell apices. Apical lumina are filled with discharged secretion. N, nucleus. Bar, 2 μm.



Figure 2.

Summary of an autoradiographic study of intracellular transport of newly synthesized secretory protein in rabbit parotid tissue. Tissue lobules were pulse labeled in vitro with [3H]leucine and subjected to chase incubation for the indicated times. Distributions of autoradiographic grains determined from electron‐macrograph autoradiograms are expressed as percent of total that were quantitated at each time point. Precursor‐product kinetic relationships between rough endoplasmic reticulum, Golgi complex, immature secretion granules, and mature secretion granules are apparent.

From Castle et al. 30


Figure 3.

Representative electron micrographs of a purified parotid secretion granule (A) and granule membrane fraction (B). With detailed consideration of the extent of contamination by residual mitochondria and incompletely removed secretory polypeptides as a basis, it is possible to estimate that 95% of the protein associated with the purified secretion granule membrane is bona fide granule membrane protein. Bars, 1 μm.

From Cameron and Castle 25


Figure 4.

Immunocytochemical demonstration of antigen distribution with heterologous antiserum to parotid secretory granule membranes. A, B: bars, 10 μm. Indirect immunofluorescent staining of 0.5‐μm‐thick frozen sections of parotid (A) and exocrine pancreas (B). Immunoreactivity is concentrated over secretion granule membrane profiles that are identified on the basis of their apical cytoplasmic location, size, and frequency. Staining is not detected in the basal cytoplasm, which contains abundant rough endoplasmic reticulum and mitochondria. C1–3: bar, 0.1 μm. Indirect immunolabeling with ferritin conjugates on isolated, aldehyde‐fixed parotid secretion granules. C2, ferritin decoration reveals that the granule membrane antiserum recognizes determinants on the cytosolic aspect of the granule membrane. No ferritin decorates secretory granules when preimmune serum (C1) or antiserum specific for content polypeptides (proline‐rich polypeptides (C3) is substituted for the membrane antiserum (C2). D‐F: bar, 10 μm. Indirect immunofluorescent staining of endocrine (epithelial and nonepithelial) and neural tissues with parotid granule membrane antibodies selected by adsorption for determinants on the cytoplasmic surface. For recovery of antibodies bound to intact parotid granules, granule suspensions were treated in 200 mM glycine (pH 2.8), and desorbed antibodies were recovered in supernate after sedimentation of granules through 0.75 M sucrose. Soluble IgG fractions served subsequently as the primary antiserum. D: 6‐μm‐thick frozen section of the CA3 region of rat hippocampus. SR, stratum radiatum; PL, pyramidal cell layer; SO, stratum oriens. Immunolabeling observed throughout the neuropile is particularly prominent adjacent to the pyramidal cell layer. Cell bodies and dendrites are unstained. E: 2‐μm‐thick frozen section of rat adrenal medulla. Chromaffin cells show a diffuse (or in some cases punctate) fluorescent pattern in the cytoplasm that is assumed to mark chromaffin granules. F: 4‐μm‐thick frozen section of rat liver. Label is associated with the bile canalicular surface and associated pericanalicular cellular organelles.

A and B from Cameron et al. 24


Figure 5.

Comparative two‐dimensional sodium dodecyl sulfate‐polyacrylamide gel electrophoretic analyses of purified exocrine secretory granule membrane polypeptides. Autoradiographic patterns obtained by parallel electrophoresis of radioiodinated (chloramine T) parotid and pancreas secretory granule membrane polypeptides. A: parotid pattern; 3 groups of polypeptides distinguished in the text on the basis of molecular weight are indicated by brackets (I‐III). B: solid arrow, position of pancreatic zymogen granule membrane protein GP‐2. Horizontal values, pH values; vertical values, molecular weight X 10−3.

From Cameron et al. 24


Figure 6.

Two‐dimensional electrophoretic analysis of rat liver Golgi secretory vesicle membranes. Autoradiogram of radioiodinated (chloramine T) membrane polypeptides from a sodium carbonate‐treated Golgi fraction 1 (GF1) fraction (A). Analogous polypeptides, especially 30,000‐Mr polypeptides, have similar (but not identical) mobilities. Even though this group of polypeptides are prominent radiolabeled species, they may not be such major constituents of the Golgi vesicle membrane as signified by their minor contributions to a Coomassie blue‐stained polypeptide profile (B). Horizontal values, pH values; vertical values, molecular weight X 10−3.

A from Ehrenreich et al. 55.
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Article Title: Secretory Membranes and the Exocrine Storage Compartment
 

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Richard S. Cameron, Peter Arvan, J. David Castle. Secretory Membranes and the Exocrine Storage Compartment. Compr Physiol 2011, Supplement 18: Handbook of Physiology, The Gastrointestinal System, Salivary, Gastric, Pancreatic, and Hepatobiliary Secretion: 107-126. First published in print 1989. doi: 10.1002/cphy.cp060307