The secretory process of salivary glands and pancreas

  • Arthur R. Hand
Part of the Electron Microscopy in Biology and Medicine book series (EMBM, volume 6)


The study of secretory cells and the definition of the secretory process have been at the forefront of modern cell biology since the inception of this field in the early 1950s. Secretory cells, particularly the acinar cells of the exocrine pancreas, presented a unique opportunity for cell biologists, who were in the process of marrying biochemistry and morphology: Here was a cell with virtually a single-minded mission, to produce and release large amounts of digestive enzymes, whose appearance in the microscope could be correlated with reactions in the test tube and that could be induced to perform its functions by physiological manipulations or the application of readily available drugs. Since almost all cells secrete proteins, these pioneering studies found wide application, and they spawned the development of methodological approaches and technological advances too numerous to mention.


Secretory Protein Golgi Apparatus Acinar Cell Secretory Granule Secretory Process 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Palade GE: Intracellular aspects of the process of protein secretion. Science 189: 347–358, 1975.PubMedGoogle Scholar
  2. 2.
    Hand AR, Oliver C (eds): Basic Mechanisms of Cellular Secretion. Methods in Cell Biology, Vol 23. New York: Academic Press, 1981.Google Scholar
  3. 3.
    Cantin M (ed): Cell Biology of the Secretory Process. Basel: Karger, 1984.Google Scholar
  4. 4.
    Burgess TL, Kelly RB: Constitutive and regulated secretion of proteins. Ann Rev Cell Biol 3: 243–293, 1987.PubMedGoogle Scholar
  5. 5.
    Shulz I: Electrolyte and fluid secretion in the exocrine pancreas. In: Physiology of the Gastrointestinal Tract, Vol 2, 2nd ed. LR Johnson (ed), New York: Raven Press, 1147–1171, 1987.Google Scholar
  6. 6.
    Martinez JR: Ion transport and water movement. J Dent Res 66: 638–647, 1987.PubMedGoogle Scholar
  7. 7.
    Young JA, Cook DI, van Lennep EW, Roberts M: Secretion by the major salivary glands. In: Physiology of the Gastrointestinal Tract, Vol 1, 2nd ed. LR Johnson (ed), New York: Raven Press, 773–815, 1987.Google Scholar
  8. 8.
    Hand AR, Ho B: Liquid-diet-induced alterations of rat parotid acinar cells studied by electron microscopy and enzyme cytochemistry. Arch Oral Biol 26: 369–380, 1981.PubMedGoogle Scholar
  9. 9.
    Blobel G, Dobberstein B: Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane bound ribosomes of murine myeloma. J Cell Biol 67: 835–851, 1975.PubMedGoogle Scholar
  10. 10.
    Walter P, Blobel G: Purification of a membrane associated protein complex required for protein translocation across the endoplasmic reticulum. Proc Natl Acad Sci USA 77: 7112–7116, 1980.PubMedGoogle Scholar
  11. 11.
    Walter P, Blobel G: Signal recognition particle contains a 7S RNA essential for protein translocation across the endoplasmic reticulum. Nature (London) 299: 691–698, 1982.Google Scholar
  12. 12.
    Sabatini DD, Kreibich G, Morimoto T, Adesnik M: Mechanisms for the incorporation of proteins in membranes and organelles. J Cell Biol 92: 1–22, 1982.PubMedGoogle Scholar
  13. 13.
    Walter P, Lingappa VR: Mechanism of protein translocation across the endoplasmic reticulum membrane. Ann Rev Cell Biol 2: 499–516, 1986.PubMedGoogle Scholar
  14. 14.
    Perara E, Rothman RE, Lingappa VR: Uncoupling translocation from translation: Implications for transport of proteins across membranes. Science 232: 348–352, 1986.PubMedGoogle Scholar
  15. 15.
    Sly WS, Fischer HD, Gonzalez-Noriega A, Grubb JH, Natowicz M: Role of the 6-phosphomannosyl-enzyme receptor in intracellular transport and adsorptive pinocytosis of lysosomal enzymes. In: Basic Mechanisms of Cellular Secretion. Methods in Cell Biology, Vol 23. AR Hand, C Oliver (eds), New York: Academic Press, 191–214, 1981.Google Scholar
  16. 16.
    von Figura K, Hasilik A: Lysosomal enzymes and their receptors. Ann Rev Biochem 55: 167–193, 1986.Google Scholar
  17. 17.
    Kornfeld R, Kornfeld S: Assembly of asparagine-linked oligosaccharides. Ann Rev Biochem 54: 631–664, 1985.PubMedGoogle Scholar
  18. 18.
    Hirschberg CB, Snider MD: Topography of glycosylation in the rough endoplasmic reticulum and Golgi apparatus. Ann Rev Biochem 56: 63–87, 1987.PubMedGoogle Scholar
  19. 19.
    Roth J: Subcellular organization of glycosylation in mammalian cells. Biochim Biophys Acta 906: 405–436, 1987.PubMedGoogle Scholar
  20. 20.
    Goldberg DE, Kornfeld S: Evidence for extensive sub- cellular organization of asparagine-linked oligosaccharide processing and lysosomal enzyme phosphorylation.J Biol Chem 258: 3159–3165, 1983.PubMedGoogle Scholar
  21. 21.
    Hand AR: Salivary glands. In: Orban’s Oral Histology and Embryology, 10th ed. SN Bhaskar (ed), St. Louis: CV Mosby, 328–360, 1985.Google Scholar
  22. 22.
    Tabas I, Kornfeld S: Biosynthetic intermediates of β-glucuronidase contain high mannose oligosaccharides with blocked phosphate residues. J Biol Chem 255: 6633–6639, 1980.PubMedGoogle Scholar
  23. 23.
    Varki A, Kornfeld S: Identification of a rat liver a-N-acetylglucosaminyl phosphodiesterase capable of removing “blocking” a-N-acetylglucosamine residues from phosphorylated high mannose oligosaccharides of lysosomal enzymes.J Biol Chem 255: 8398–8401, 1980.PubMedGoogle Scholar
  24. 24.
    Pohlmann R, Waheed A, Hasilik, A, von Figura K: Synthesis of phosphorylated recognition marker in lysosomal enzymes is located in the cis part of Golgi apparatus. J Biol Chem 257: 5323–5325, 1982.PubMedGoogle Scholar
  25. 25.
    Brown WJ, Farquhar MG: The mannose-6-phosphate receptor for lysosomal enzymes is concentrated in cis Golgi cisternae. Cell 36: 295–307, 1984.PubMedGoogle Scholar
  26. 26.
    Geuze HJ, Slot JW, Strous GJAM, Hasilik A, von Figura K: Ultrastructural localization of the mannose-6-phosphate receptor in rat liver. J Cell Biol 98: 2047–2054, 1984.PubMedGoogle Scholar
  27. 27.
    Geuze HJ, Slot JW, Strous GJAM, Hasilik A, von Figura K: Possible pathways for lysosomal enzyme delivery. J Cell Biol 101: 2253–2262, 1985.PubMedGoogle Scholar
  28. 28.
    Steiner DF, Quinn PS, Patzelt C, Chan SJ, Marsh J, Tager HS: Proteolytic cleavage in the posttranslational processing of proteins. In: Cell Biology: A Comprehensive Treatise, Vol 4. DM Prescott, L Goldstein (eds), New York: Academic Press, 175–202, 1980.Google Scholar
  29. 29.
    Gluschankof P, Cohen P: Proteolytic enzymes in the post-translational processing of polypeptide hormone precursors. Neurochem Res 12: 951–958, 1987.PubMedGoogle Scholar
  30. 30.
    Gainer H, Same Y, Brownstein MJ: Biosynthesis and axonal transport of rat neurohypophysial proteins and peptides. J Cell Biol 73: 366–381, 1977.PubMedGoogle Scholar
  31. 31.
    Orci L, Ravazzola M, Amherdt M, Madsen O, Vassalli J-D, Perrelet A: Direct identification of prohormone conversion site in insulin-secreting cells. Cell 42: 671–681, 1985.PubMedGoogle Scholar
  32. 32.
    Bing T, Poulsen K, Hackenthal E, Rix E, Taugner R: Renin in the submaxillary gland. A review. J Histochem Cytochem 28: 874–880, 1980.PubMedGoogle Scholar
  33. 33.
    Isackson PJ, Dunbar JC, Bradshaw RA, Ullrich A: The structure of murine 7S nerve growth factor: Implications for biosynthesis. Int J Neurosci 26: 95–108, 1985.PubMedGoogle Scholar
  34. 34.
    Stoscheck CM, King LE Jr: Functional and structural characteristics of EGF and its receptor and their relationship to transforming proteins. J Cell Biochem 31: 135–152, 1986.PubMedGoogle Scholar
  35. 35.
    Bennick A: Salivary proline-rich proteins. Mol Cell Biochem 45: 83–99, 1982.PubMedGoogle Scholar
  36. 36.
    Mirels L, Bedi GS, Dickinson DP, Gross KW, Tabak LA: Molecular characterization of glutamic acid/glutamine-rich secretory proteins from rat submandibular glands. J Biol Chem 262: 7289–7297, 1987.PubMedGoogle Scholar
  37. 37.
    von Zastrow M, Tritton TR, Castle JD: Exocrine secretion granules contain peptide amidation activity. Proc Natl Acad Sci USA 83: 3297–3301, 1986.Google Scholar
  38. 38.
    Herzog V, Miller F: Die Lokalisation endogener Peroxydase in der Glandula parotis der Ratte. Z Zellforsch Mikrosk Anat 107: 403–420, 1970.PubMedGoogle Scholar
  39. 39.
    Hand AR, Oliver C: Relationship between the Golgi apparatus, GERL, and secretory granules in acinar cells of the rat exorbital lacrimal gland. J Cell Biol 74: 399–413, 1977.PubMedGoogle Scholar
  40. 40.
    Geuze JJ, Slot JW, Tokuyasu KT: Immunocytochemical localization of amylase and chymotrypsinogen in the exocrine pancreatic cells with special attention to the Golgi complex. J Cell Biol 82: 697–707, 1979.PubMedGoogle Scholar
  41. 41.
    Hand AR: Salivary glands. In: Oral Histology: Inheritance and Development, 2nd ed. DV Provenza, W Seibel (eds), Philadelphia: Lea and Febiger, 388–417, 1986.Google Scholar
  42. 42.
    Zeigel RF, Dalton AJ: Speculations based on the morphology of the Golgi systems in several types of protein secreting cells. J Cell Biol 15: 45–54, 1962.PubMedGoogle Scholar
  43. 43.
    Caro LG, Palade GE: Protein synthesis, storage, and discharge in the pancreatic exocrine cell. A autoradiographic study. J Cell Biol 30: 473–495, 1964.Google Scholar
  44. 44.
    Jamieson JD, Palade GE: Intracellular transport of secretory proteins in the pancreatic exocrine cell. I. Role of the peripheral elements of the Golgi complex. J Cell Biol 34: 577–596, 1967.PubMedGoogle Scholar
  45. 45.
    Jamieson JD, Palade GE: Intracellular transport of secretory proteins in the pancreatic exocrine cell. IV. Metabolic requirements. J Cell Biol 39: 589–603, 1968.PubMedGoogle Scholar
  46. 46.
    Chu LLH, MacGregor RR, Cohn DV: Energy-dependent intracellular translocation of proparathormone. J Cell Biol 72: 1–10, 1977.PubMedGoogle Scholar
  47. 47.
    Tartakoff A: Temperature and energy dependence of secretory protein transport in the exocrine pancreas. EMBOJ 5: 1477–1482, 1986.PubMedGoogle Scholar
  48. 48.
    Patzelt C, Brown D, Jeanrenaud B: Inhibitory effect of colchicine on amylase secretion by rat parotid glands. Possible localization in the Golgi area. J Cell Biol 73: 578–593, 1977.PubMedGoogle Scholar
  49. 49.
    Malaisse-Legae F, Armherdt M, Ravazzola M, Sener A, Hutton JC, Orci L, Malaisse WJ: Role of microtubules in the synthesis, conversion, and release of (pro)insulin. A biochemical and radioautographic study in rat islets. J Clin Invest 63: 1284–1296, 1979.Google Scholar
  50. 50.
    Williams JA: Effects of antimitotic agents on ultrastructure and intracellular transport of protein in pancreatic acini. In: Basic Mechanisms of Cellular Secretion. Methods in Cell Biology, Vol 23. AR Hand, C Oliver (eds), New York: Academic Press, 247–258, 1981.Google Scholar
  51. 51.
    Neutra M, Leblond CP: Synthesis of the carbohydrate of mucus in the Golgi complex as shown by electron microscope radioautography of goblet cells from rats injected with glucose-H3. J Cell Biol 30: 119–136, 1966.PubMedGoogle Scholar
  52. 52.
    Slot JW, Geuze JJ, Poort C: Synthesis and intracellular transport of proteins in the exocrine pancreas of the frog (Rana esculenta). I. An ultrastructural and autoradiographic study. Cell Tissue Res 155: 135–154, 1974.PubMedGoogle Scholar
  53. 53.
    Bennett G: Role of the Golgi complex in the secretory process. In: Cell Biology of the Secretory Process. M Cantin (ed), Basel: Karger, 102–147, 1984.Google Scholar
  54. 54.
    Brown RM Jr: Observations on the relationship of the Golgi apparatus to wall formation in the marine chrysophycean alga, Pleurochrysis scherffelii Pringsheim. J Cell Biol 41: 109–123, 1969.PubMedGoogle Scholar
  55. 55.
    Marchi F, Leblond CP: Radioautographic characterization of successive compartments along the rough endoplasmic reticulum-Golgi pathway of collagen precursors in foot pad fibroblasts of [3H]proline-injected rats. J Cell Biol 98: 1705–1709, 1984.PubMedGoogle Scholar
  56. 56.
    Rambourg A, Clermont Y, Hermo L, Segretain D: Tridimensional architecture of the Golgi apparatus in mucous cells of Brunner’s glands of the mouse. Am J Anat 179: 95–107, 1987.PubMedGoogle Scholar
  57. 57.
    Meldolesi J: Dynamics of cytoplasmic membranes in guinea pig pancreatic acinar cells. I. Synthesis and turnover of membrane proteins. J Cell Biol 61: 1–13, 1974.PubMedGoogle Scholar
  58. 58.
    Meldolesi J: Membranes and membrane surfaces. Dynamics of cytoplasmic membranes in pancreatic acinar cells. Phil Trans Roy Soc Lond Ser B 268: 39–53, 1974.Google Scholar
  59. 59.
    Wallach D, Kirshner N, Schramm M: Non-parallel transport of membrane proteins and content proteins during assembly of the secretory granule in rat parotid gland. Biochim Biophys Acta 375: 87–105, 1975.PubMedGoogle Scholar
  60. 60.
    Winkler H: The biogenesis of adrenal chromaffin granules. Neuroscience 2: 657–683, 1977.PubMedGoogle Scholar
  61. 61.
    Farquhar MG: Progress in unraveling pathways of Golgi traffic. Ann Rev Cell Biol 1: 447–488, 1985.PubMedGoogle Scholar
  62. 62.
    Balch WE, Dunphy WG, Braell WA, Rothman JE: Reconstitution of the transport of protein between successive compartments of the Golgi measured by the coupled incorporation of N-acetylglucosamine. Cell 39: 405–416, 1984.PubMedGoogle Scholar
  63. 63.
    Rothman JE, Miller R, Urbani LJ: Intercompartmental transport in the Golgi complex is a dissociative process: Facile transfer of membrane protein between two Golgi populations. J Cell Biol 99: 260–271, 1984.PubMedGoogle Scholar
  64. 64.
    Fitting T, Kabat D: Evidence for a glycoprotein “signal” involved in transport between subcellular organelles. Two membrane glycoproteins encoded by murine leukemia virus reach the cell surface at different rates.J Biol Chem 257: 14011–14017, 1982.PubMedGoogle Scholar
  65. 65.
    Lodish, HF, Kong N, Snider M, Strous GJAM: Hepatoma secretory proteins migrate from the RER to Golgi at characteristic rates. Nature (London) 304: 80–83, 1983.Google Scholar
  66. 66.
    Scheele G, Tartakoff A: Exit of non-glycosylated secretory proteins from the RER is asynchronous in the exocrine pancreas. J Biol Chem 260: 926–931, 1985.PubMedGoogle Scholar
  67. 67.
    Friend DS, Farquhar MG: Functions of coated vesicles during protein absorption in the rat vas deferens. J Cell Biol 35: 357–376, 1967.PubMedGoogle Scholar
  68. 68.
    Tooze J, Tooze SA: Clathrin-coated vesicular transport of secretory proteins during the formation of ACTH-containing secretory granules in AtT20 cells. J Cell Biol 103: 839–850, 1986.PubMedGoogle Scholar
  69. 69.
    Orci L, Glick BS, Rothman JE: A new type of coated vesicular carrier that appears not to contain clathrin: Its possible role in protein transport within the Golgi stack. Cell 46: 171–184, 1986.PubMedGoogle Scholar
  70. 70.
    Doxsey S, Helenius A, Blank G, Brodsky F: Inhibition of endocytosis by anti-clathrin antibodies. J Cell Biol 103: 53a, 1986.Google Scholar
  71. 71.
    Payne GS, Schekman R: A test of clathrin function in protein secretion and cell growth. Science 230: 1009–1014, 1985.PubMedGoogle Scholar
  72. 72.
    Kelly RB: Pathways of protein secretion in eukaryotes. Science 230: 25–32, 1985.PubMedGoogle Scholar
  73. 73.
    Griffiths G, Simons K: The trans Golgi network: Sorting at the exit site of the Golgi complex. Science 234: 438–443, 1986.PubMedGoogle Scholar
  74. 74.
    Tooze J, Tooze SA, Fuller SD: Sorting of progeny Coronavirus from condensed secretory proteins at the exit from the trans-Golgi network of AtT20 cells. J Cell Biol 105: 1215–1226, 1987.PubMedGoogle Scholar
  75. 75.
    Ball WD, Hand AR, Johnson AO: Secretory proteins as markers for cellular phenotypes in rat salivary glands. Dev Biol 125: 265–279, 1988.PubMedGoogle Scholar
  76. 76.
    Novikoff AB: The endoplasmic reticulum: A cytochemist’s view (a review). Proc Natl Acad Sci USA 73: 2781–2787, 1976.PubMedGoogle Scholar
  77. 77.
    Broadwell RD, Oliver C: Golgi apparatus, GERL, and secretory granule formation within neurons of the hypothalamoneurohypophysial system of control and hyperosmotically stressed mice. J Cell Biol 90: 474–484, 1982.Google Scholar
  78. 78.
    Hand AR, Oliver C: Effects of secretory stimulation on the Golgi apparatus and GERL of rat parotid acinar cells. J Histochem Cytochem 32: 403–412, 1984.PubMedGoogle Scholar
  79. 79.
    Schneider Y-J, Tulkens P, de Duve C, Trouet A: Fate of plasma membrane during endocytosis. II. Evidence of recycling (shuttle) of plasma membrane constituents. J Cell Biol 82: 466–474, 1979.PubMedGoogle Scholar
  80. 80.
    Muller WA, Steinman RM, Cohn ZA: The membrane proteins of the vacuolar system. II. Bidirectional flow between secondary lysosomes and plasma membrane. J Cell Biol 86: 304–314, 1980.PubMedGoogle Scholar
  81. 81.
    Steinman RM, Mellman IS, Muller WA, Cohn ZA: Endocytosis and the recycling of plasma membrane. J Cell Biol 96: 1–27, 1983.PubMedGoogle Scholar
  82. 82.
    Herzog V, Farquhar MG: Luminal membrane retrieved after exocytosis reaches most Golgi cisternae in secretory cells. Proc Natl Acad Sci USA 74: 5073–5077, 1977.PubMedGoogle Scholar
  83. 83.
    Farquhar MG: Recovery of surface membrane in anterior pituitary cells. Variations in traffic detected with anionic and cationic ferritin. J Cell Biol 77: R35–R42, 1978.PubMedGoogle Scholar
  84. 84.
    Ottosen PD, Courtoy PJ, Farquhar MG: Pathways followed by membrane recovered from the surface of plasma cells and myeloma cells. J Exp Med 152: 1–19, 1980.PubMedGoogle Scholar
  85. 85.
    Herzog V, Reggio H: Pathways of endocytosis from luminal plasma membrane in rat exocrine pancreas. Eur J Cell Biol 21: 141–150, 1980.PubMedGoogle Scholar
  86. 86.
    Hand AR: Morphology and cytochemistry of the Golgi apparatus of rat salivary gland acinar cells. Am J Anat 130: 141–158, 1971.PubMedGoogle Scholar
  87. 87.
    Bendayan M: Concentration of amylase along its secretory pathway in the pancreatic acinar cell as revealed by high resolution immunocytochemistry. Histochem J 16: 85–108, 1984.PubMedGoogle Scholar
  88. 88.
    Kraehenbuhl JP, Racine L, Jamieson JD: Immunocytochemical localization of secretory proteins in bovine pancreatic exocrine cells. J Cell Biol 72: 406–423, 1977.PubMedGoogle Scholar
  89. 89.
    Bendayan M, Roth J, Perrelet A, Orci L: Quantitative immunocytochemical localization of pancreatic secretory proteins in subcellular compartments of the rat acinar cell. J Histochem Cytochem 28: 149–160, 1980.PubMedGoogle Scholar
  90. 90.
    Jamieson JD, Palade GE: Condensing vacuole conversion and zymogen granule discharge in pancreatic exocrine cells: Metabolic studies. J Cell Biol 48: 503–522, 1971.PubMedGoogle Scholar
  91. 91.
    Castle JD, Jamieson JD, Palade GE: Radioautographic analysis of the secretory process in the parotid acinar cell of the rabbit. J Cell Biol 53: 290–311, 1972.PubMedGoogle Scholar
  92. 92.
    Wallach D, Schramm M: Calcium and the exportable protein in rat parotid gland. Parallel subcellular distribution and concomitant secretion. Eur J Biochem 21: 433–437, 1971.PubMedGoogle Scholar
  93. 93.
    Clementi F, Meldolesi J: Calcium and pancreatic secretion. I. Subcellular distribution of calcium and magnesium in the exocrine pancreas of the guinea pig. J Cell Biol 65: 88–102, 1975.Google Scholar
  94. 94.
    Verdugo P, Deyrup-Olsen I, Aitken M, Villaion M, Johnson D: Molecular mechanism of mucin secretion: I. The role of intragranular charge shielding. J Dent Res 66: 506–508, 1987.PubMedGoogle Scholar
  95. 95.
    Reggio HA, Palade GE: Sulfated compounds in the zymogen granules of the guinea pig pancreas. J Cell Biol 11: 288–314, 1978.Google Scholar
  96. 96.
    Giannattasio G, Zanini A, Rosa P, Meldolesi J, Margolis RK, Margolis RU: Molecular organization of prolactin granules. III. Intracellular transport of sulfated glycosaminoglycans and glycoproteins of the bovine prolactin granule. J Cell Biol 86: 273–279, 1980.PubMedGoogle Scholar
  97. 97.
    Mellman I, Fuchs R, Helenius A: Acidification of the endocytic and exocytic pathways. Ann Rev Biochem 55: 663–700, 1986.PubMedGoogle Scholar
  98. 98.
    Anderson RGW, Pathak RK: Vesicles and cisternae in the trans Golgi apparatus of human fibroblasts are acidic compartments. Cell 40: 634–643, 1985.Google Scholar
  99. 99.
    Arvan P, Castle JD: Osmotic properties and internal pH of isolated rat parotid secretory granules. J Biol Chem 259: 13567–13572, 1984.PubMedGoogle Scholar
  100. 100.
    Arvan P, Rudnick G, Castle JD: Relative lack of H+ translocase activity in isolated parotid secretory granules. J Biol Chem 260: 14945–14952, 1985.PubMedGoogle Scholar
  101. 101.
    Orci L, Ravazzola M, Anderson RGW: The condensing vacuole of exocrine cells is more acidic than the mature secretory vesicles. Nature (London) 326: 77–79, 1987.Google Scholar
  102. 102.
    Sherline P, Lee Y-C, Jacobs LS: Binding of microtubules to pituitary secretory granules and secretory granule membranes. J Cell Biol 72: 380–389, 1977.PubMedGoogle Scholar
  103. 103.
    Orci L, Gabbay KH, Malaisse WJ: Pancreatic beta-cell web: Its possible role in insulin secretion. Science 175: 1128–1130, 1972.PubMedGoogle Scholar
  104. 104.
    Drenckhahn D, Mannherz HG: Distribution of actin and the actin-associated proteins myosin, tropomyosin, alpha-actinin, vinculin, and villin in rat and bovine exocrine glands. Eur J Cell Biol 30: 167–176, 1983.PubMedGoogle Scholar
  105. 105.
    Bendayan M: Ultrastructural localization of actin in muscle, epithelial and secretory cells by applying the protein A-gold immunocytochemical technique. Histochem J 15: 39–58, 1983.PubMedGoogle Scholar
  106. 106.
    Cameron RS, Cameron PL, Castle JD: A common spectrum of polypeptides occurs in secretion granule membranes of different exocrine glands. J Cell Biol 103: 1299–1313, 1986.PubMedGoogle Scholar
  107. 107.
    Amsterdam A, Ohad I, Schramm M: Dynamic changes in the ultrastructure of the acinar cell of the rat parotid gland during the secretory cycle. J Cell Biol 41: 753–773, 1969.PubMedGoogle Scholar
  108. 108.
    Hand AR: The fine structure of von Ebner’s gland of the rat. J Cell Biol 44: 340–353, 1970.PubMedGoogle Scholar
  109. 109.
    Orci L, Perrelet A, Friend DS: Freeze-fracture of membrane fusion during exocytosis in pancreatic B-cells. J Cell Biol 75: 23–30, 1977.PubMedGoogle Scholar
  110. 110.
    Tanaka Y, De Camilli P, Meldolesi J: Membrane interactions between secretion granules and plasmalemma in three exocrine glands. J Cell Biol 84: 438–453, 1980.PubMedGoogle Scholar
  111. 111.
    Chandler DE, Heuser JE: Arrest of membrane fusion events in mast cells by quick-freezing. J Cell Biol 86: 666–674, 1980.PubMedGoogle Scholar
  112. 112.
    Ornberg RL, Reese TS: Beginning of exocytosis captured by rapid-freezing of Limulus amebocytes. J Cell Biol 90:40–54, 1981.PubMedGoogle Scholar
  113. 113.
    Curran MJ, Brodwick MS: Direct visualization of exocytosis in mast cells. Biophys J 45: 170a, 1984.Google Scholar
  114. 114.
    Zimmerberg J, Sardet C, Epel D: Exocytosis of sea urchin egg cortical vesicles in vitro is retarded by hyperosmotic sucrose: Kinetics of fusion monitored by quantitative light-scattering microscopy. J Cell Biol 101: 2398–2410, 1985.PubMedGoogle Scholar
  115. 115.
    Holz RW: The role of osmotic forces in exocytosis from adrenal chromaffin cells. Ann Rev Physiol 48: 175–189, 1986.Google Scholar
  116. 116.
    Zimmerberg J, Curran M, Cohen FS, Brodwick M: Simultaneous electrical and optical measurements show that membrane fusion precedes secretory granule swelling during exocytosis of beige mouse mast cells. Proc Natl Acad Sci USA 84: 1585–1589, 1987.PubMedGoogle Scholar
  117. 117.
    Oliver C, Hand AR: Uptake and fate of luminally administered horseradish peroxidase in resting and isoproterenol stimulated rat parotid acinar cells. J Cell Biol 76: 207–220, 1978.PubMedGoogle Scholar
  118. 118.
    Patzak A, Winkler H: Exocytotic exposure and recycling of membrane antigens of chromaffin granules: Ultrastructural evaluation after immunolabeling. J Cell Biol 102: 510–515, 1986.PubMedGoogle Scholar
  119. 119.
    Butcher FR, Putney JW Jr: Regulation of parotid gland function by cyclic nucleotides and calcium. Adv Cyclic Nucleotide Res 13: 215–249, 1980.PubMedGoogle Scholar
  120. 120.
    Williams JA: Regulatory mechanisms in pancreas and salivary acini. Ann Rev Physiol 46: 361–375, 1984.Google Scholar
  121. 121.
    Putney JW Jr: Identification of cellular activation mechanisms associated with salivary secretion. Ann Rev Physiol 48: 75–88, 1986.Google Scholar
  122. 122.
    Baum BJ: Regulation of salivary secretion. In: The Salivary System. LM Sreebny (ed), Boca Raton, FL: CRC Press, 123–134, 1987.Google Scholar
  123. 123.
    Solomon TE: Control of exocrine pancreatic secretion. In: Physiology of the Gastrointestinal Tract, 2nd ed. LR Johnson (ed), New York: Raven Press, 1173–1207, 1987.Google Scholar
  124. 124.
    Gardner JD, Jensen RT: Secretagogue receptors on pancreatic acinar cells. In: Physiology of the Gastrointestinal Tract, 2nd ed. LR Johnson (ed), New York: Raven Press, 1109–1127, 1987.Google Scholar
  125. 125.
    Stryer L, Bourne HR: G proteins: A family of signal transducers. Ann Rev Cell Biol 2: 391–419, 1986.PubMedGoogle Scholar
  126. 126.
    Dowd FJ, Watson EL, Horio B, Lau Y-S, Park K: Phosphorylation of rabbit parotid microsomal protein occurs only with β-adrenergic stimulation. Biochem Biophys Res Commun 101: 281–288, 1981.PubMedGoogle Scholar
  127. 127.
    Baum BJ, Freiberg JM, Ito, H, Roth GS, Filburn CR: β-adrenergic regulation of protein phosphorylation and its relationship to exocrine secretion in dispersed rat parotid gland acinar cells. J Biol Chem 256: 9731–9736, 1981.PubMedGoogle Scholar
  128. 128.
    Freedman SD, Jamieson JD: Hormone-induced protein phosphorylation. II. Localization to the ribosomal fraction from rat exocrine pancreas and parotid of a 29,000-dalton protein phosphorylated in situ in response to secretagogues. J Cell Biol 95: 909–917, 1982.PubMedGoogle Scholar
  129. 129.
    Quissell DO, Deisher LM, Barzen KA: The rate-determining step in cAMP-mediated exocytosis in the rat parotid and submandibular glands appears to involve analogous 26-kDa integral membrane phosphoproteins. Proc Natl Acad Sci USA 82: 3237–3241, 1985.PubMedGoogle Scholar
  130. 130.
    Marino CR, Gorelick FS, Castle JD: Isoproterenol induced phosphorylation of granule membrane proteins in the rat parotid gland. J Cell Biol 105: 57a, 1987.Google Scholar
  131. 131.
    Mednieks MI, Jungmann RA, Hand AR: Ultrastructural immunocytochemical localization of cyclic AMP-dependent protein kinase regulatory subunits in rat parotid acinar cells. Eur J Cell Biol 44: 308–317, 1987.PubMedGoogle Scholar
  132. 132.
    Mednieks MI, Hand AR: Cyclic AMP-dependent protein kinase in stimulated rat parotid gland cells: Compartmental shifts after in vitro treatment with isoproterenol. Eur J Cell Biol 28: 264–271, 1982.Google Scholar
  133. 133.
    Schwoch G: Selective regulation of the amount of the catalytic subunit of cyclic AMP-dependent protein kin- ases during isoprenaline-induced growth of the rat parotid gland. Biochem J 248: 243–250, 1987.PubMedGoogle Scholar
  134. 134.
    Volpe P, Krause K-H, Hashimoto S, Zorzato F, Pozzan T, Meldolesi J, Lew PD: “Calciosome,” a cytoplasmic organelle: The inositol 1,4,5-trisphosphate-sensitive Ca2+ store of non-muscle cells? Proc Natl Acad Sci USA 85: 1091–1095, 1988.PubMedGoogle Scholar
  135. 135.
    Putney JW Jr: A model for receptor-regulated calcium entry. Cell Calcium 7: 1–12, 1986.PubMedGoogle Scholar
  136. 136.
    Foskett JK, Gunter-Smith PJ, Melvin JE, Turner RJ: Physiological localization of an agonist-sensitive pool of Ca2+ in parotid acinar cells. Proc Natl Acad Sci USA 86:167–171, 1989.PubMedGoogle Scholar
  137. 137.
    Kikkawa U, Nishizuka Y: The role of protein kinase C in transmembrane signalling. Ann Rev Cell Biol 2: 149–178, 1986.PubMedGoogle Scholar
  138. 138.
    Burnham DB, Williams JA: Effects of carbachol, cholecystokinin, and insulin on protein phosphorylation in isolated pancreatic acini. J Biol Chem 257: 10523–10528, 1982.PubMedGoogle Scholar
  139. 139.
    Wrenn RW: Phosphorylation of a pancreatic zymogen granule membrane protein by endogenous calcium/phospholipid-dependent protein kinase. Biochim Biophys Acta 775: 1–6, 1984.PubMedGoogle Scholar
  140. 140.
    Dowd F, Watson EL, Lau Y-S, Justin J, Pasieniuk J, Jacobson KL: Calcium-dependent protein kinase reactions associated with parotid gland secretory granule membranes. J Dent Res 66: 557–563, 1987.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1990

Authors and Affiliations

  • Arthur R. Hand
    • 1
  1. 1.NIDR, NIHBethesdaUSA

Personalised recommendations