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Proteases in the Atlantic Salmon, Salmo Salar L. Physiological And

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Proteases in the Atlantic Salmon, Salmo Salar L. Physiological And Proteases in the Atlantic salmon,Salmo salar L. Physiological and biological aspects. Sigfus Einarsson A thesis presented for the degree of Doctor of Philosophy in the University of Glasgow, Faculty of Science, Department of Zoology. December, 1993. ©Sigfus Einarsson 1993 i ProQuest Number: 11007772 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a com plete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. uest ProQuest 11007772 Published by ProQuest LLC(2018). Copyright of the Dissertation is held by the Author. All rights reserved. This work is protected against unauthorized copying under Title 17, United States C ode Microform Edition © ProQuest LLC. ProQuest LLC. 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106- 1346 CrtloQ GLASGOW UNIVERSITY LIBRARY DECLARATION. I declare that this thesis represents, except where note is made to the contrary, work carried out by myself. The text was composed by myself. S. Einarsson December, 1993. ACKNOWLEDGEMENTS. First I want to thank my mother, Margret K. Petursdottir and my wife, Retno Henryati Susanti for their invaluable aid and support during this work. I will be forever indepted to them. The beginning of this work was carried out at the Freshwater Fisheries Laboratories, Pitlochry. The major part was carried out at the University of Glasgow, Department of Zoology, and at the Almond Bank rearing station, Perth. I thank all respective persons for providing research facilities. The work was funded by Lanasjo5ur Islenskra Namsmanna, Reykjavik. Island. Many thanks to Dr. P. S. Davies and Dr. C. Talbot who supervised the project. Special thanks to Mike Miles, Kate Orr, Cathy McLagan, June Freel, Liz Denton, Margaret Mullin, Peter Rickus and last but not least Dr. A. Taylor. Thanks to Dr. Turner and Dr. Kennedy and to all those who have aided and helped me in this work. Thanks to various members of staff in the Statistics Department for their advice on statistical problems, and to Dr. N. Metcalfe for invaluable advice in the same field. CONTENTS Page numbers Abstract. x Chapter I. General introduction. 1 1. The biology of the Atlantic salmon. 1 2. Feeding of salmon in the wild, in culture and in relation to digestive enzymes 4 3. The digestive enzymes pepsin, trypsin and chymotrypsin. 8 3.1. Endopeptidases of the stomach. 8 3.2. Endopeptidases of the intestine. 10 4. Digestive physiology of teleostei. 12 4.1. Digestive physiology of the stomach. 12 4.2 Digestive physiology of the pancreas. 15 5. Workplan. 17 Chapter II. Morphology and ultrastructure of the digestive tract. 20 1. Introduction. 20 2. Materials and methods. 21 2.1. The fish. 21 2.2. Light microscopic studies. 22 2.3. Transmission electron microscopic studies. 24 2.4. Scanning electron microscopic studies. 26 3. Results. 27 3.1. The cardiac and the transitional area of the stomach. 27 3.2. The pyloric area. 28 3.3. The intestine. 28 3.4. Pancreatic tissue. 29 4. Discussion. 30 4.1. The cardiac and the transitional area of the stomach. 30 4.2. The pyloric area. 32 4.3. The intestine. 33 4.4. Pancreatic tissue. 34 Chapter III. Assay procedures for digestive enzymes. 36 1. Introduction. 36 2. Materials and methods. 38 2.1 The kinetics of pepsin, trypsin and chymotrypsin activity. 38 2.2. pH profiles of pepsin, trypsin and chymotrypsin. 41 2.3. Specificity of DL'BApNA and SAAPPpNA towards trypsin and chymotrypsin, respectively. 43 2.4. The effect of trypsin on the chymotrypsin assay. 43 3. Results. 44 3.1. Characteristics of pepsin. 44 3.1.1. Kinetics of pepsin activity. 44 3.1.2. pH-profiles of pepsin. 45 3.2. Characteristics of trypsin. 45 3.2.1. Kinetics of trypsin activity. 45 3.2.2. Trypsin activity as a function of pH. 45 3.3. Characteristics of chymotrypsin. 46 3.3.1. Kinetics of chymotrypsin activity. 46 3.3.2. Chymotrypsin activity as a function of pH. 46 3.4. Specificity of DL’BApNA and SAAPPpNA, towards trypsin and chymotrypsin, respectively. 47 3.5. The effect of trypsin on the chymotrypsin assay. 47 4. Discussion. 47 4.1. Pepsin. 47 4.2. Trypsin. 49 4.3. Chymotrypsin. 51 4.4. Specificity of BApNA, SAAPP/jNA, towards trypsin and chymotrypsin, respectively. 53 4.5. The effect of trypsin on the chymotrypsin assay. 53 Chapter IV. Control of secretion of trypsin and chymotrypsin from the pancreas. 55 1. Introduction. 55 2. Materials and methods. 58 2.1. Cholecystokinin In vivo. 58 v 2.2. Cholecystokinin, in vitro. 61 2.3. Acetylcholine and carbamylcholine, in vitro. 62 3. Results. 63 3.1. The in vivo effect of cholecystokinin. 63 3.2. The in vitro effect of cholecystokinin. 65 3.3. The in vitro effect of acetylcholine and carbamylcholine. 65 4. Discussion. 66 Chapter V. Localisation of pepsinogen, trypsinogen and chymotrypsinogen. 71 1. Introduction. 71 2. Materials and methods. 73 2.1. Localisation of pepsinogen. 73 2.1.1. Light microscopy and immunolocalisation of pepsinogen. 73 2.1.2. Assay of pepsin activity in the stomach. 75 2.2. Localisation of trypsinogen and chymotrypsinogen. 78 3. Results. 80 3.1. Localisation of pepsinogen. 80 3.1.1. Immunolocalisation of pepsinogen. 80 3.1.2. Pepsin activity in the stomach. 81 3.2. Localisation of trypsinogen and chymotrypsinogen. 82 3.2.1. Mobilisation of pancreatic granules by CCK. 82 3.2.2. Trypsin and chymotrypsin in the pancreas, pyloric caeca and intestine. 82 4. Discussion. 83 Chapter VI. Effect of feeding on the secretion of pepsin, trypsin and chymotrypsin. 86 1. Introduction. 86 2. Materials and methods. 89 2.1. The effect of starvation on pepsin, trypsin and chymotrypsin, and the gallbladder. 89 2.2. The effect of food on pepsin. 91 2.3. The effect of food on trypsin and chymotrypsin vi and the gallbladder. 93 3. Results. 95 3.1. The effect of starvation on pepsin, trypsin and chymotrypsin, and the gallbladder. 95 3.2. The effect of food on pepsin. 97 3.3. The effect of food on trypsin and chymotrypsin and on the gallbladder. 98 3.3.1. Digesta. 98 3.3.2. Discharge of the gallbladder and secretion of trypsin and chymotrypsin. 99 3.3.3. Trypsin and chymotrypsin activities in the intestinal digesta. 100 4. Discussion. 101 4.1. The effect of starvation on pepsin, trypsin and chymotrypsin, and the gallbladder. 101 4.2. The effect of food on pepsin. 102 4.3. The effect of food on trypsin and chymotrypsin and the gallbladder. 104 Chapter VII. Differences in digestive enzyme activity in upper and lower modal group salmon. 112 1. Introduction. 112 2. Materials and methods. 114 2.1. Lower and upper modal group salmon in their first year. 114 2.2. The effect of starvation, CCK and feeding. 117 3. Results. 119 3.1. Lower and upper modal salmon in their first year. 119 3.1.1. Changes with time in body weight and gut digesta. 119 3.1.2. Changes with time in the digestive enzyme activity. 120 3.2. The effect of starvation, cholecystokinin and feeding. 123 4. Discussion. 125 4.1. Lower and upper modal salmon in their first year. 125 4.2. The effect of starvation, CCK and feeding. 132 vii Chapter VIII. Conclusion and prospects. 134 IX. References. 140 X. Appendices 182 List of figures After page Figure 1 ( a ) An overall view of the gut and its related components 27 ( b ) Schematic map explaining the terminology of the gut 27 Figure 2 ( a ) Transverse section from the whole upper cardiac area 27 ( b ) Transverse section from the whole lower cardiac area 27 ( c ) Section showing the stomach glands of the cardiac area 27 ( d ) Section from the transitional area of the stomach 27 Figure 3 T.E.M. section from the cardiac area of the stomach, showing gastric cells 27 Figure 4 ( a ) Transverse section through the whole pyloric area 28 ( b ) Section from the mucosa of the pyloric area 28 Figure 5 ( a ) Section from the pancreatic tissue and the pyloric caeca 28 ( b ) Section from the ascending intestinal wall 28 ( c ) T.E.M. section from the epithelium of the pyloric caecal region 28 ( d ) Section from the epithelium of the rectum 28 Figure 6 ( a ) Endocrine cells in the pyloric caecal region, top 29 ( b ) Endocrine cells in the pyloric caecal region, bottom 29 Figure 7 ( a ) Duct openings on the surface of the primary viii fold of a pyloric caeca 30 ( b ) Duct opening on the surface of the intestinal wall in the pyloric caecal area 30 ( a ) Endocrine pancreas: Islet of Langerhans ( Brockmann bodies ) 30 ( b ) Pancreatic duct 30 ( a ) Exocrine pancreatic cells on T.E.M. sections 30 ( b ) Endocrine pancreatic cells ( Islet of Langerhans ) on T.E.M. sections 30 ( a ) Substrate saturation of pepsin activity 44 ( b ) Lineweaver-Burk plot of data from ( a ). 44 Pepsin activty as a function of pH 45 ( a ) Substrate saturation of trypsin activity 45 ( b ) Lineweaver-Burk plot of data from ( a ). 45 Trypsin activity as a function of pH 45 ( a ) Substrate saturation of chymotrypsin activity 46 ( b ) Lineweaver-Burk plot of data from ( a ). 46 Chymotrypsin activity as a function of pH 46 Breakdown of the trypsin substrate, DL'BA/?NA and the 47 chymotrypsin substrate, SAAPPpNA, by trypsin and chymotrypsin 47 The effect of TLCK on chymotrypsin activity 47 In vivo stimulation by CCK of trypsin ( a ) ix and chymptrypsin ( b ) secretion at 4.6 °C 63 Figure 19 In vivo stimulation by CCK of trypsin ( a ) and chymptrypsin ( b ) secretion at 8.0 °C 64 Figure 20 In vitro stimulation of trypsin secretion, a time profile for 1 fish ( a ), and for 6 fish ( b ) 65 Figure 21 In vitro stimulation of chymotrypsin secretion, a time profile for 1 fish ( a ), and for 6 fish ( b ) 65 Figure 22 ( a ) Immunostaining of pepsinogen in the anterior cardiac area 81 ( b ) Immunostaining of pepsinogen in the posterior cardiac area 81 Figure 23 Pepsin activity in the posterior oesophagus, anterior cardiac area, posterior cardiac area and the pyloric area 81 Figure 24 Fraction of granule to acinar tissue point counts in the pancreas on T.E.M.
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