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Cystic Fibrosis Transmembrane Conductance Regulator, Gulonolactone Oxidase, and P53

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Cystic Fibrosis Transmembrane Conductance Regulator, Gulonolactone Oxidase, and P53 Molecular biology of the lung and kidney of the African lungfish, Protopterus annectens, during three phases of aestivation: cystic fibrosis transmembrane conductance regulator, gulonolactone oxidase, and p53 Ching Biyun A thesis submitted to the Department of Biological Sciences National University of Singapore in fulfillment of the requirement for the degree of Doctor of Philosophy in Science 2012 Acknowledgements The completion of this project and thesis would not have been possible without the help and support of many people around me. I would first like to thank my supervisor, Prof Alex Ip Yuen Kwong for all the help and guidance he has provided. He has demonstrated time and again with his problem- solving skills and ways of handling and manouevring around situations, that nothing is impossible to manage. What seemed like impalpable illusions at first can in fact be achieved in reality, with the right approach. I would also like to thank Mrs Wong Wai Peng, Jasmine Ong Li Ying, Chng You Rong, Chen Xiu Ling, Tok Chia Yee and Hiong Kum Chew for their ideas, assistance and support in and out of the lab; and Adeline Yong Jing Hui and Samuel Wong Zheng Hao for their timely contributions. My gratitude also goes out to family members and friends who stood by me, especially Pu YuHui, who’s always around to lend a listening ear and sit through all my random gripes about insignificant things. i Table of Contents Acknowledgements………………………………………………………………….. i Table of Contents……………………………………………………………………. ii List of Tables………………………………………………………………………… xi List of Figures……………………………………………………………………….. xiii List of Abbreviations………………………………………………………………… xix Abstract……………………………………………………………………………… 1 1. Introduction…………………………………………………………………… 3 1.1. Lungfishes…………………………………………………………….. 3 1.2. Lungfish lung and air-breathing……………………………………… 4 1.3. Lungfish and aestivation……………………………………………… 5 1.4. Lungfish lung and cftr/Cftr expression in the lung of P. annectens during aestivation……………………………………………………… 7 1.5. Oxidative stress and ascorbic acid…………………………………….. 11 1.6. Ascorbic acid biosynthesis and the expression of gulo/Gulo in the kidney and other organs of P. annectens during aestivation………….. 12 1.7. Oxidative stress, apoptosis and p53…………………………………… 14 1.8. Aestivation and oxidative stress in aestivating African lungfish……… 15 1.9. Expression of p53 in P. annectens during aestivation………………… 16 1.10. Objectives and hypotheses summary………………………………….. 17 1.10.1. cftr……………………...……………………………………. 17 1.10.2 gulo……………………...…………………………………… 17 1.10.3 p53……………………...……………………………………. 18 Literature review……………………………………………………………… 20 2.1. Lungfishes…………………………………………………………….. 20 2.1.1. Six species of extant lungfishes……………………...……… 20 2.1.2. African lungfish and aestivation…………..………………… 19 2.1.3. Lung and respiration in lungfishes……………….………… 25 2.2. CFTR/CFTR…………………..………………………………………. 27 2.2.1. Functions of Cftr in lung…………………..………………… 27 ii 2.2.2. Cystic fibrosis in human and Cftr mutation/polymorphism… 29 2.3. Ascorbic acid………………….……………………………………….. 32 2.3.1. Ascorbic acid is an antioxidant……………………………… 32 2.3.2. Evolution of biochemical synthesis of ascorbic acid………... 34 2.3.3. Transport of ascorbic acid…………………………………... 37 2.3.4. Functional role of ascorbate in teleost fish………………….. 38 2.4. p53…………………………………………………………………….. 42 2.4.1. Functions of p53 in general…………………………………. 42 2.4.2. Functions of p53 in fish……………………………………... 43 3. Materials and methods…………………………………………………………. 45 3.1. Animals………………………………………………………………… 45 3.2. Experimental conditions……………………………………………….. 45 3.3. mRNA extraction and cDNA synthesis………………………………... 46 3.4. PCR…………………………………………………………………….. 46 3.5. Sequencing……………………………………………………………... 47 3.6. RACE PCR…………………………………………………………….. 47 3.7. Determination of mRNA expression by quantitative real-time PCR (qPCR)…………………………………………………………………. 47 3.8. Cftr-related experiments………………………………………………. 49 3.8.1. Primer design for PCR, RACE PCR and qPCR……………… 49 3.8.2. Cloning for cftr isoforms……………………………………... 49 3.8.2.1. cDNA synthesis by combining RNA from lungs of three fish………..…………………………………. 50 3.8.2.2. Primer design……………………………………… 50 3.8.2.3. Cloning for cftr isoforms from cDNA from lungs of three fish…………………………………………… 51 3.8.2.4. Cloning for cftr isoforms from cDNA from lungs of an individual fish………………………………….. 52 3.8.2.5. Cloning for cftr isoforms from cDNA from gills of an individual fish…………………………………... 52 3.8.3. Phylogenetic analysis………………………………………… 52 iii 3.8.4. Tissue expression………………….…………………………. 53 3.8.5. Collection and determination of Na+ concentration in airway surface liquid…………………………………………………. 53 3.9. Gulo-related experiments……………………………………………… 53 3.9.1. Primer design for PCR, RACE PCR and qPCR……………… 53 3.9.2. Phylogenetic analysis………………………………………… 54 3.9.3. Tissue expression………………….…………………………. 54 3.9.4. Western blot…………………………………………………... 54 3.9.5. Determination of concentrations of ascorbic acid and dehydroascorbic acid…………………………………………. 55 3.10. p53-related experiments……………………………………………….. 56 3.10.1. Primer design for PCR, RACE PCR and qPCR……………. 56 3.10.2. Phylogenetic analysis………………………………………. 56 3.11. Statistical analysis……………………………….…………………….. 56 4. CHAPTER 1—Cystic fibrosis transmembrane conductance regulator...……… 66 4.1. Results…………………………………………………………………. 66 4.1.1. Nucleotide and deduced amino acid sequence of the predominant form of cftr/Cftr from the lung………….……… 66 4.1.2. Phylogenetic relationship of the deduced predominant form of Cftr from the lung……………………..……………………… 66 4.1.3. Isoforms of cftr from the lungs combined from three fish……………………………………………………………. 66 4.1.3.1. Control in freshwater……………………………… 67 4.1.3.2. Fish after 6 months of aestivation in air…………… 67 4.1.3.3. Fish after 1 day of arousal from 6 months of aestivation in air…………………………………… 68 4.1.4. Isoforms of cftr from the lungs of an individual fish in freshwater…………………………………………………….. 68 4.1.5. Tissue expression of the predominant form of cftr…………… 68 4.1.6. Isoforms of cftr from the gills of an individual fish in freshwater…………………………………………………….. 69 iv 4.1.7. Changes in mRNA expression of various cftr isoforms in the lung during three phases of aestivation……………….……… 69 4.1.8. Na+ concentrations in airway surface liquids from the lungs of control fish or fish after 6 months of aestivation in air, or 1 d arousal from 6 months of aestivation in air…………………... 70 4.2. Discussion……………………………………………………………… 112 4.2.1. cftr from the lungs and gills of P. annectens……………….. 112 4.2.2. Molecular characterization of the predominant form of cftr/Cftr from the lung of P. annectens……………………... 113 4.2.2.1. A sequence analysis of Cftr/CFTR from P. annectens, elasmobranchs, teleosts and tetrapods 114 4.2.2.2. Transmembrane domains and transmembrane region M6………………………………………. 115 4.2.2.3. First extracellular loop…………………………. 118 4.2.2.4. Nucleotide binding domains……………………. 121 4.2.2.5. Walker A motif…………………………………. 121 4.2.2.6. Walker B motif…………………………………. 123 4.2.2.7. Regulatory Domain…………………………….. 125 4.2.2.8. Predicted phosphorylation sites………………… 130 4.2.2.9. Interactions with other molecules………………. 130 4.2.2.10. PDZ motif………………………………………. 132 4.2.2.11. Phylogenetic analysis…………………………... 134 4.2.3. Cftr isoforms and polymorphism in the lung of P. annectens—possible relationships between respiration in air, desiccation and aestivation?.................................................... 134 4.2.4. Cftr mutation and cystic fibrosis in human…………………. 137 4.2.5. ‘Cystic fibrosis’ in lungs of P. annectens—a strategy to reduce airway surface evaporative water loss during aestivation?.............................................................................. 140 4.2.6. The evolutionary origins of CFTR mutation/polymorphism and cystic fibrosis in human?.................................................. 146 v 4.2.7. Accessory breathing organs and swim bladders—future comparative studies?............................................................... 149 4.2.8. Tissue expression of cftr in P. annectens…………………… 151 4.2.9. Expression of cftr/Cftr in fish gills and the function of Cftr in osmoregulation in teleosts………………………………... 152 4.2.10. Expression of multiple cftr/Cftr isoforms in the gills of P. annectens in freshwater…………………………………….. 154 4.2.11. Cftr isoforms and polymorphism in lungs and gills of P. annectens—a clue to the huge genome of lungfishes?........... 156 5. CHAPTER 2—Gulonolactone oxidase...……………………………………… 159 5.1. Results………………………………………………………………….. 159 5.1.1. Nucleotide and deduced amino acid sequence of gulo/Gulo from the kidneys of P. annectens and 5 other extant lungfishes……………………………………………………... 159 5.1.2. Phylogenetic relationship of the deduced Gulo from the kidneys of P. annectens and 5 other extant lungfishes……...... 159 5.1.3. Tissue expression of gulo…………………………………….. 160 5.1.4. Changes in mRNA expression of gulo in the kidney during three phases of aestivation…………………………………… 160 5.1.5. Changes in protein expression of Gulo in the kidney during three phases of aestivation…………………………………… 160 5.1.6. Changes in mRNA expression of gulo in the brain during three phases of aestivation…………………………………… 160 5.1.7. Changes in protein expression of Gulo in the brain during three phases of aestivation…………………………………… 161 5.1.8. Changes in protein expression of Gulo in the lung during three phases of aestivation…………………………………… 161 5.1.9. Ascorbic acid concentrations in the kidney, brain and lung during three phases of aestivation……………………………. 161 5.2. Discussion……………………………………………………………… 180 5.2.1. gulo
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