ANNUAL REVIEWS
Further
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Ann. Rev. Pharmacol. Toxicol.
Annu. Rev. Pharmacol. Toxicol. 1977.17:27-47. Downloaded from www.annualreviews.org Access provided by University of Manchester - John Rylands Library on 01/23/15. For personal use only.
Copyright ©
1977 by Annual
1977. 17.27-47
Reviews Inc. All rights reserved
COMMON MECHANISMS OF
.:-6665
HORMONE SECRETION J. M Trifaro Department of Pharmacology and Therapeutics, McGill University, Montreal, H3G Quebec, Canada
I Y6,
INTRODUCTION With the exception of the thyroid gland, which stores hormones extracellularly in the lumen of its follicles, the endocrine tissues store their hormones intracellularly (1). Two main forms of intracellular storage must be recognized: I. The steroid secreting glands which store very little amounts of hormone but large quantities of precursor. The adrenal cortex, the ovary, and the testis all belong to this category of endocrine glands in which the presence of secretory granules has not been demonstrated. However, these tissues store large amounts of esterified cholesterol in lipid droplets, and this represents a depot of hormone precursor (1, 2). 2. Endo crine tissues which store large quantities of hormones in membrane-bound or ganelles, the secretory granules. A similar way of storing secretory products may be observed in exocrine glands (3, 4) and also in nervous tissues which synthesize and release novel transmitter substances (5, 6). The main concern of this review is with the secretory events which occur in those cells storing hormones in subcellular granules. Among this type of cell are those of the adenohypophysis, the islets of Langerhans of the pancreas, the adrenal medulla, the parathyroid gland, the parafollicular cells of the thyroid, and the neurosecretory cells of the hypothalamus-neurohypophysial system. Because these tissues share the common feature of storing their hormones in granules, it is possible that the cellular and molecular mechanisms of secretion are also similar. Therefore, this article seeks to unify published observations concerning the events involved in the secretory process of these tissues. Because of space limitations, it has been necessary to make an arbitrary selection of references to discuss and illustrate the ideas presented here; in many cases there are other references of equal value which would also support these ideas. 27
28
TRIFARO
Annu. Rev. Pharmacol. Toxicol. 1977.17:27-47. Downloaded from www.annualreviews.org Access provided by University of Manchester - John Rylands Library on 01/23/15. For personal use only.
STORAGE OF HORMONES IN GRANULES Evidence for the storage of hormones in subcellular particles has come to light from results obtained through morphological and biochemical techniques. Centrifugation studies have demonstrated both that the hormone activity in the homogenates of endocrine glands can be sedimented and that the hormone-containing particles of these sediments can be further separated from other subcellular particles by density gradient centrifugation techniques (1, 7- 10). Electron microscopic analysis of the subcellular fractions containing the hormone activity has revealed the presence of membrane-bound granules similar to those observed in intact tissues (7-10). Gran ule preparations of a quite different degree of purity have been isolated from different encodrine tissues (7-11). Chromaffin granule fractions of a high degree of purity have been isolated from the adrenal medulla (7, 12, 13). The subsequent chemical analysis of these granules (14) has provided a large and valuable body of information on the mechanisms of storage (14, 15) and release of adrenal medullary hormones (14). Therefore it is important that efforts be made to obtain granule preparations of a high degree of purity from other endocrine tissues. In order to assess the importance of storage granules it is necessary to point out some of the advantages of this type of hormone storage: (a) the hormones may reach very high concentrations within the granuloisner, A. M., Douglas, W. W. 1968. A possible mechanism of release of pos terior pituitary hormones involving adenosine triphosphate and an adeno sine triphosphatase in neuro-secretory granules. Mol Pharmacal 4:53 1-40
FEBS Lett. 49:228-32
151.
143. Yoshida, H., Miki, N., Ishida, H., Yamamoto, T. 1968. Release of amylase from zymogen granules by ATP and a low concentration of CaH. Biochem. Biophys. Acta 1 5 8 :489-90
Hellman, B., Tiiljedal, I. B. 1970. Solu bilizing effect of nucleotides on isolated insulin secretory granules. J. Cell Bioi.
148.
141.
144.
Howell, S. L., Young, D. A., Lacy, P. E. 1969. Isolation and properties of secre tory granules from rat islets of Langer hans. Ill. Studies of the stability of iso lated Beta granules. J. Cell Bioi. 4 1 : 1 67-76
147.
Biochem. J J O I : 1 8C-20C
1 37. Vilhardt, H., J�rgensen, T. 1972. Free Row electrophoresis of isolated seen: tory granules from bovine neurohypo physes. Experientia 28:852-53 1 38. Woodin, A. M., French, J. E., Mar chesi, V. T. 1963. Morphological changes associated with the extrusion of protein induced in the polymorphonu clear leucocyte by staphy lococca1 leucocidin. Biachem. J 87:567-7 1 1 39. Abood, L. G. 1966. Interrelationships between phosphates and calcium in bioelectric phenomena. In t. Rev.
45
Diabetes 22: 1 6--24
1 57. 1 5 8.
Randle, P. J., Hales, C. N. 1972. See Ref. 1 2 1 , pp. 2 1 9-35 Pipeleers, D. G., Pipeleers-Marichal, M. A., Kipnis, D. M. 1976. Mi crotubule assembly and intracellular transport of secretory granules in pan creatic islets. Science 1 9 1 :88-90
46
TRIFARO
1 59.
Lacy, P. E., Walker, M. M., Fink, J. 1 972. Perifusion of isolated rat islets in
1 60.
Weisenberg, R. C. 1972. Microtubule formation in vitro in solutions contain ing low calcium concentrations. Science
vitro. Diabetes 2 1 :987-98
Annu. Rev. Pharmacol. Toxicol. 1977.17:27-47. Downloaded from www.annualreviews.org Access provided by University of Manchester - John Rylands Library on 01/23/15. For personal use only.
161.
1 64.
Shelanski, M. L. 1 973. Chemistry of the filaments and tubules of brain. J. His to
induced by high K+ and by hypo thalamus-stalk-median eminence ex tract. Endocrinology 89:408- 1 2 Douglas, W . W . , Sorimachi, M. 1972. Effects of cytochalasin B and colchicine on secretion of posterior pituitary and adrenal medullary hormones. Br. J. Pharmacol. Chemother. 45 : 1 43-44
Sundberg, D. K., Krulich, L., Fawcett, C. P., Illner, P., McCann, S. M. 1 973. The effect of colchicine on the release of rat anterior pituitary hormones in vitro. Proc. Soc. Exp. Bioi. Med. 1 1 00
1 75.
Temple, R., Williams, J. A., Wilber, J. F., Wolff, J. 1972. Colchicine and hor mone secretion. Biochem. Biophys. Res.
1 66.
Jamieson,J. D. 1 972. Transport and dis charge of exportable proteins in pan creatic exocrine cells: In vitro studies.
1 67.
Stadler, J., Franke, W. W. 1 974. Char acterization of the colchicine binding of membrane fractions from rat and mouse liver. J. Cell Bioi. 60:297-303 Mizel, S. B., Wilson, L. 1 972. Nucleo side transport in mammalian cells. Inhi bition by colchicine. Biochemistry
del, B., Orci, L. 1 974. Actin in pan creatic islet cells. E ndocrinology 95:
1 77.
1 78.
1 79.
Trifar6, 1. M., Collier, B., Lastowecka, A., Stern, D. 1 972. Inhibition by colchi cine and by vinblastine of acetylcholine induced catecholamine release from the adrenal gland: an anticholinergic ac tion, not an effect upon microtubules. Mol. Pharmacol. 8:264-67
Douglas, W. W., Sorimachi, M. 1 972. Colchicine inhibits adrenal medullary secretion evoked by acetylcholine with out affecting that evoked by potassium.
Br. J. Pharmacal. 45: 129-32 1 72. Lagunoff, D., Chi, E. Y. 1 975.
Effect of colchicine on mast cell secretion stimu-
Ulpian, C., Trifar6, J. M. 1 976. Isola tion of myosin from the adrenal medulla. Can. Fed. Bioi. Soc. Meet., p. 178 (Abstr.) Burridge, K., Slater, 1. H. 1 975. Asso ciation of actin and myosin with secre tory granule membranes. Nature 254: 526-29
181.
LeBeux, Y J., Willemot, J. 1 975. An ultrastructural study of the microfila ments in rat brain by means of E-PTA staining and heavy� meromyosin label ing. II. The Synapses. Cell Tissue Res.
1 82.
Wessels, N. K., Spooner, B. S., Ash, J. F., Bradley, M. 0., Luduena, M. A., Taylor, E. L., Wrenn, J. T., Yamada, K. M. 1 97 1 . Microfilaments in cellular and developmental processes. Science 1 7 1 :
1 83 .
Mizel, S. B., Wilson, L. 1972. Inhibition of the transport of several hexoses in mammalian cells by cytochalasin B. J.
Pharm. Sci. 54:779-80
171.
327-3 1
Brooks, J. c., Siegel, F. L. 1973. Purifi cation of a calcium-binding phospho protein from beef adrenal medulla. J.
1 1 :2573-78
1 70.
1 630-35
Phillips, J. H., Slater, A. 1975. Actin in the adrenal medulla. FEBS Lett. 56:
1 80.
C urro Top. Membr. Transp. 3:273-338
Spoor, R. P., Ferguson, F. C. 1965. Col chicine. IV. Neuromuscular transmis sion in isolated frog and rat tissues. J.
Berl, S., Puszkin, S., Nicklas, W. J. 1 973. Actomyosin-like protein in brain.
Science 1 79:441-46
Commun. 46: 1 454-6 1
1 69.
202
176. Gabbiani, G., Malaisse-Lagae, F., Blon
142: 1 097-
1 65.
1 68.
1 74.
1 77: 1 1 04-5
chem. Cytochem. 2 1 :529-39 1 62. Kraicer, J., Milligan, J. W. 1 9 7 1 . Effect of colchicine on in vitro ACTH release
1 63.
1 73.
lated by polymyxin B and A23 1 87. 1. Cell Bioi. 67:230a (Abstr.) Poisner, A. M. 1 970. Actomyosin-like protein from the adrenal medulla. Fed. Proc. 29:545 (Abstr.) Trifar6, J. M., Ulpian, C. 1 975. Ac tomyosin-like protein isolated from the adrenal medulla. FEBS Lett. 57: 1 98-
BioI. Chem. 248:41 89-93
1 60:37-68
1 3 5-43
Bioi. Chem. 247:4 1 02-5
1 84.
Nakazato, Y, Douglas, W. W. 1 973. Cytochalasin blocks sympathetic gan glionic transmission: a presynaptic effect antagonized by pyruvate. Proc.
1 85.
Sanger, 1. W., Sanger, 1. M. 1 975. States of actin and cytochalasin-B. J. Cell BioI. 67:3 8 1 a (Abstr.) Pollard, T. D., Weihing, R. R. 1 974. Actin and myosin and cell movement.
1 86.
Natl. Acad. Sci. USA 70: 1 730-33
C R C Crit. Rev. Biochem. 2: 1-65
1 87. Lazarides, E., Weber, K. 1974. Actin
antibody: The specific visualization of actin filaments in non-muscle cells.
COMMON MECHANISMS OF HORMONE SECRETION
Proc. Natl. A cad. Sci. USA 7 1 :2268-72 1 88.
Sanger, I. W. 1 975. Changing patterns of actin localization during cell division.
Proc. Nat!. Acad. Sci. USA 72: 1 9 1 3- 1 6
1 89. Douglas, W. W . , Poisner, A . M . , Trifaro, J . M. 1 966. Lysolecithin and other phospholipids in the adrenal medulla of various species. Life Sci.
Annu. Rev. Pharmacol. Toxicol. 1977.17:27-47. Downloaded from www.annualreviews.org Access provided by University of Manchester - John Rylands Library on 01/23/15. For personal use only.
5 : 809- 1 5
1 90.
191.
1 92.
Blaschko, H . , Firemark, H . , Smith, A . D., Winkler, H. 1 967. Lipids o f the adrenal medulla: lysolecithin, a charac teristic constituent of chromaffin gran ules. Biochem. J. 104:545-49 Trifaro, J. M. 1 969. Phospholipid me tabolism and adrenal medullary activ ity. I. The effect of acetylcholine on tis sue uptake and incorporation of ortho phosphate-J2p into nucleotides and phospholipids of bovine adrenal medulla. Mol. Pharmacal. 5:3 82-93 Trifaro, J. M . 1 969. The effect of Ca2+
47
omission in the secretion of catechola mines and the incorporation of ortho phosphate-llP into nucleotides and phospholipids of bovine adrenal medulla during acetylcholine stimula tion. Mol. Pharmacal. 5:420-3 1 1 93 . Lucy, J. A. 1 970. The fusion of biologi cal membranes. Nature 227:8 1 5- 1 7 1 94. Koening, H. 1 974. See Ref. 4 , pp. 273301
1 95.
Dean, P. M. 1 975. Exocytosis model ling: An electrostatic function for cal cium in stimulus-secretion coupling. J.
1 96.
Dean, P. M., Matthews, E. K. 1 975. The London-Van der Waals attraction constant of secretory granules and its significance. J. Thear. BioI. 54: 309-2 1 Poste, G. 1 97 1 . Membrane fusion reac tion: A theory. J. Theor. BioI. 32:
Theor. Bioi. 54:289-308
1 97.
1 65-84
Further
Quick links to online content
Ann. Rev. Pharmacol. Toxicol.
Annu. Rev. Pharmacol. Toxicol. 1977.17:27-47. Downloaded from www.annualreviews.org Access provided by University of Manchester - John Rylands Library on 01/23/15. For personal use only.
Copyright ©
1977 by Annual
1977. 17.27-47
Reviews Inc. All rights reserved
COMMON MECHANISMS OF
.:-6665
HORMONE SECRETION J. M Trifaro Department of Pharmacology and Therapeutics, McGill University, Montreal, H3G Quebec, Canada
I Y6,
INTRODUCTION With the exception of the thyroid gland, which stores hormones extracellularly in the lumen of its follicles, the endocrine tissues store their hormones intracellularly (1). Two main forms of intracellular storage must be recognized: I. The steroid secreting glands which store very little amounts of hormone but large quantities of precursor. The adrenal cortex, the ovary, and the testis all belong to this category of endocrine glands in which the presence of secretory granules has not been demonstrated. However, these tissues store large amounts of esterified cholesterol in lipid droplets, and this represents a depot of hormone precursor (1, 2). 2. Endo crine tissues which store large quantities of hormones in membrane-bound or ganelles, the secretory granules. A similar way of storing secretory products may be observed in exocrine glands (3, 4) and also in nervous tissues which synthesize and release novel transmitter substances (5, 6). The main concern of this review is with the secretory events which occur in those cells storing hormones in subcellular granules. Among this type of cell are those of the adenohypophysis, the islets of Langerhans of the pancreas, the adrenal medulla, the parathyroid gland, the parafollicular cells of the thyroid, and the neurosecretory cells of the hypothalamus-neurohypophysial system. Because these tissues share the common feature of storing their hormones in granules, it is possible that the cellular and molecular mechanisms of secretion are also similar. Therefore, this article seeks to unify published observations concerning the events involved in the secretory process of these tissues. Because of space limitations, it has been necessary to make an arbitrary selection of references to discuss and illustrate the ideas presented here; in many cases there are other references of equal value which would also support these ideas. 27
28
TRIFARO
Annu. Rev. Pharmacol. Toxicol. 1977.17:27-47. Downloaded from www.annualreviews.org Access provided by University of Manchester - John Rylands Library on 01/23/15. For personal use only.
STORAGE OF HORMONES IN GRANULES Evidence for the storage of hormones in subcellular particles has come to light from results obtained through morphological and biochemical techniques. Centrifugation studies have demonstrated both that the hormone activity in the homogenates of endocrine glands can be sedimented and that the hormone-containing particles of these sediments can be further separated from other subcellular particles by density gradient centrifugation techniques (1, 7- 10). Electron microscopic analysis of the subcellular fractions containing the hormone activity has revealed the presence of membrane-bound granules similar to those observed in intact tissues (7-10). Gran ule preparations of a quite different degree of purity have been isolated from different encodrine tissues (7-11). Chromaffin granule fractions of a high degree of purity have been isolated from the adrenal medulla (7, 12, 13). The subsequent chemical analysis of these granules (14) has provided a large and valuable body of information on the mechanisms of storage (14, 15) and release of adrenal medullary hormones (14). Therefore it is important that efforts be made to obtain granule preparations of a high degree of purity from other endocrine tissues. In order to assess the importance of storage granules it is necessary to point out some of the advantages of this type of hormone storage: (a) the hormones may reach very high concentrations within the granuloisner, A. M., Douglas, W. W. 1968. A possible mechanism of release of pos terior pituitary hormones involving adenosine triphosphate and an adeno sine triphosphatase in neuro-secretory granules. Mol Pharmacal 4:53 1-40
FEBS Lett. 49:228-32
151.
143. Yoshida, H., Miki, N., Ishida, H., Yamamoto, T. 1968. Release of amylase from zymogen granules by ATP and a low concentration of CaH. Biochem. Biophys. Acta 1 5 8 :489-90
Hellman, B., Tiiljedal, I. B. 1970. Solu bilizing effect of nucleotides on isolated insulin secretory granules. J. Cell Bioi.
148.
141.
144.
Howell, S. L., Young, D. A., Lacy, P. E. 1969. Isolation and properties of secre tory granules from rat islets of Langer hans. Ill. Studies of the stability of iso lated Beta granules. J. Cell Bioi. 4 1 : 1 67-76
147.
Biochem. J J O I : 1 8C-20C
1 37. Vilhardt, H., J�rgensen, T. 1972. Free Row electrophoresis of isolated seen: tory granules from bovine neurohypo physes. Experientia 28:852-53 1 38. Woodin, A. M., French, J. E., Mar chesi, V. T. 1963. Morphological changes associated with the extrusion of protein induced in the polymorphonu clear leucocyte by staphy lococca1 leucocidin. Biachem. J 87:567-7 1 1 39. Abood, L. G. 1966. Interrelationships between phosphates and calcium in bioelectric phenomena. In t. Rev.
45
Diabetes 22: 1 6--24
1 57. 1 5 8.
Randle, P. J., Hales, C. N. 1972. See Ref. 1 2 1 , pp. 2 1 9-35 Pipeleers, D. G., Pipeleers-Marichal, M. A., Kipnis, D. M. 1976. Mi crotubule assembly and intracellular transport of secretory granules in pan creatic islets. Science 1 9 1 :88-90
46
TRIFARO
1 59.
Lacy, P. E., Walker, M. M., Fink, J. 1 972. Perifusion of isolated rat islets in
1 60.
Weisenberg, R. C. 1972. Microtubule formation in vitro in solutions contain ing low calcium concentrations. Science
vitro. Diabetes 2 1 :987-98
Annu. Rev. Pharmacol. Toxicol. 1977.17:27-47. Downloaded from www.annualreviews.org Access provided by University of Manchester - John Rylands Library on 01/23/15. For personal use only.
161.
1 64.
Shelanski, M. L. 1 973. Chemistry of the filaments and tubules of brain. J. His to
induced by high K+ and by hypo thalamus-stalk-median eminence ex tract. Endocrinology 89:408- 1 2 Douglas, W . W . , Sorimachi, M. 1972. Effects of cytochalasin B and colchicine on secretion of posterior pituitary and adrenal medullary hormones. Br. J. Pharmacol. Chemother. 45 : 1 43-44
Sundberg, D. K., Krulich, L., Fawcett, C. P., Illner, P., McCann, S. M. 1 973. The effect of colchicine on the release of rat anterior pituitary hormones in vitro. Proc. Soc. Exp. Bioi. Med. 1 1 00
1 75.
Temple, R., Williams, J. A., Wilber, J. F., Wolff, J. 1972. Colchicine and hor mone secretion. Biochem. Biophys. Res.
1 66.
Jamieson,J. D. 1 972. Transport and dis charge of exportable proteins in pan creatic exocrine cells: In vitro studies.
1 67.
Stadler, J., Franke, W. W. 1 974. Char acterization of the colchicine binding of membrane fractions from rat and mouse liver. J. Cell Bioi. 60:297-303 Mizel, S. B., Wilson, L. 1 972. Nucleo side transport in mammalian cells. Inhi bition by colchicine. Biochemistry
del, B., Orci, L. 1 974. Actin in pan creatic islet cells. E ndocrinology 95:
1 77.
1 78.
1 79.
Trifar6, 1. M., Collier, B., Lastowecka, A., Stern, D. 1 972. Inhibition by colchi cine and by vinblastine of acetylcholine induced catecholamine release from the adrenal gland: an anticholinergic ac tion, not an effect upon microtubules. Mol. Pharmacol. 8:264-67
Douglas, W. W., Sorimachi, M. 1 972. Colchicine inhibits adrenal medullary secretion evoked by acetylcholine with out affecting that evoked by potassium.
Br. J. Pharmacal. 45: 129-32 1 72. Lagunoff, D., Chi, E. Y. 1 975.
Effect of colchicine on mast cell secretion stimu-
Ulpian, C., Trifar6, J. M. 1 976. Isola tion of myosin from the adrenal medulla. Can. Fed. Bioi. Soc. Meet., p. 178 (Abstr.) Burridge, K., Slater, 1. H. 1 975. Asso ciation of actin and myosin with secre tory granule membranes. Nature 254: 526-29
181.
LeBeux, Y J., Willemot, J. 1 975. An ultrastructural study of the microfila ments in rat brain by means of E-PTA staining and heavy� meromyosin label ing. II. The Synapses. Cell Tissue Res.
1 82.
Wessels, N. K., Spooner, B. S., Ash, J. F., Bradley, M. 0., Luduena, M. A., Taylor, E. L., Wrenn, J. T., Yamada, K. M. 1 97 1 . Microfilaments in cellular and developmental processes. Science 1 7 1 :
1 83 .
Mizel, S. B., Wilson, L. 1972. Inhibition of the transport of several hexoses in mammalian cells by cytochalasin B. J.
Pharm. Sci. 54:779-80
171.
327-3 1
Brooks, J. c., Siegel, F. L. 1973. Purifi cation of a calcium-binding phospho protein from beef adrenal medulla. J.
1 1 :2573-78
1 70.
1 630-35
Phillips, J. H., Slater, A. 1975. Actin in the adrenal medulla. FEBS Lett. 56:
1 80.
C urro Top. Membr. Transp. 3:273-338
Spoor, R. P., Ferguson, F. C. 1965. Col chicine. IV. Neuromuscular transmis sion in isolated frog and rat tissues. J.
Berl, S., Puszkin, S., Nicklas, W. J. 1 973. Actomyosin-like protein in brain.
Science 1 79:441-46
Commun. 46: 1 454-6 1
1 69.
202
176. Gabbiani, G., Malaisse-Lagae, F., Blon
142: 1 097-
1 65.
1 68.
1 74.
1 77: 1 1 04-5
chem. Cytochem. 2 1 :529-39 1 62. Kraicer, J., Milligan, J. W. 1 9 7 1 . Effect of colchicine on in vitro ACTH release
1 63.
1 73.
lated by polymyxin B and A23 1 87. 1. Cell Bioi. 67:230a (Abstr.) Poisner, A. M. 1 970. Actomyosin-like protein from the adrenal medulla. Fed. Proc. 29:545 (Abstr.) Trifar6, J. M., Ulpian, C. 1 975. Ac tomyosin-like protein isolated from the adrenal medulla. FEBS Lett. 57: 1 98-
BioI. Chem. 248:41 89-93
1 60:37-68
1 3 5-43
Bioi. Chem. 247:4 1 02-5
1 84.
Nakazato, Y, Douglas, W. W. 1 973. Cytochalasin blocks sympathetic gan glionic transmission: a presynaptic effect antagonized by pyruvate. Proc.
1 85.
Sanger, 1. W., Sanger, 1. M. 1 975. States of actin and cytochalasin-B. J. Cell BioI. 67:3 8 1 a (Abstr.) Pollard, T. D., Weihing, R. R. 1 974. Actin and myosin and cell movement.
1 86.
Natl. Acad. Sci. USA 70: 1 730-33
C R C Crit. Rev. Biochem. 2: 1-65
1 87. Lazarides, E., Weber, K. 1974. Actin
antibody: The specific visualization of actin filaments in non-muscle cells.
COMMON MECHANISMS OF HORMONE SECRETION
Proc. Natl. A cad. Sci. USA 7 1 :2268-72 1 88.
Sanger, I. W. 1 975. Changing patterns of actin localization during cell division.
Proc. Nat!. Acad. Sci. USA 72: 1 9 1 3- 1 6
1 89. Douglas, W. W . , Poisner, A . M . , Trifaro, J . M. 1 966. Lysolecithin and other phospholipids in the adrenal medulla of various species. Life Sci.
Annu. Rev. Pharmacol. Toxicol. 1977.17:27-47. Downloaded from www.annualreviews.org Access provided by University of Manchester - John Rylands Library on 01/23/15. For personal use only.
5 : 809- 1 5
1 90.
191.
1 92.
Blaschko, H . , Firemark, H . , Smith, A . D., Winkler, H. 1 967. Lipids o f the adrenal medulla: lysolecithin, a charac teristic constituent of chromaffin gran ules. Biochem. J. 104:545-49 Trifaro, J. M. 1 969. Phospholipid me tabolism and adrenal medullary activ ity. I. The effect of acetylcholine on tis sue uptake and incorporation of ortho phosphate-J2p into nucleotides and phospholipids of bovine adrenal medulla. Mol. Pharmacal. 5:3 82-93 Trifaro, J. M . 1 969. The effect of Ca2+
47
omission in the secretion of catechola mines and the incorporation of ortho phosphate-llP into nucleotides and phospholipids of bovine adrenal medulla during acetylcholine stimula tion. Mol. Pharmacal. 5:420-3 1 1 93 . Lucy, J. A. 1 970. The fusion of biologi cal membranes. Nature 227:8 1 5- 1 7 1 94. Koening, H. 1 974. See Ref. 4 , pp. 273301
1 95.
Dean, P. M. 1 975. Exocytosis model ling: An electrostatic function for cal cium in stimulus-secretion coupling. J.
1 96.
Dean, P. M., Matthews, E. K. 1 975. The London-Van der Waals attraction constant of secretory granules and its significance. J. Thear. BioI. 54: 309-2 1 Poste, G. 1 97 1 . Membrane fusion reac tion: A theory. J. Theor. BioI. 32:
Theor. Bioi. 54:289-308
1 97.
1 65-84
