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Structure-Function Relationships of the Cytoplasmic Domains of the Cystic Fibrosis Transmembrane Conductance Regulator

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Structure-Function Relationships of the Cytoplasmic Domains of the Cystic Fibrosis Transmembrane Conductance Regulator Structure-Function Relationships of the Cytoplasmic Domains of the Cystic Fibrosis Transmembrane Conductance Regulator Fabian S. Seibert A thesis submitted in confonnity with the requirements for the degree of Doctor of Philosophy, Graduate Department of Eiochemistry, University of Toronto. @Copyright by Fabian S. Seibert 1997 National iibrary Bibliothèque nationale du Canada Acquisitions and Acquisitions et Bibliogaphic Services services bibliographiques 395 WeIlington Sbeet 395. rue Wellington Ottawa ON K1A ON4 OttawaON K1AON4 Canada Canada The author has granted a non- L'auteur a accordé une licence non exclusive licence allowing the exclusive permetbat à la National Library of Canada to Bibliothèque nationale du Canada de reproduce, loan, distribute or sell reproduire, prêter, distribuer ou copies of this thesis in microfom, vendre des copies de cette thèse sous paper or electronic formats. la forme de microfichelnlm, de reproduction sur papier ou sur format électronique. The author retains ownership of the L'auteur conserve la propriété du copyright in this thesis. Neither the droit d'auteur qui protège cette thèse. thesis nor substantial extracts fiom it Ni la thèse ni des extraits substantiels may be printed or otherwise de celle-ci ne doivent être imprimés reproduced without the author' s ou autrement reproduits sans son permission. autorisation. The cystic fibrosis transrnembrane conductance regulator (Cm)is a chloride chamel, located in the apical membrane of wet epithelia. Mutations in the gene coding for CFTR result in cystic fibrosis (CF) either by disruptiag the biosynthetic processing of the protein or through the production of a functionally irnpaired channel. When studying CFTR. the molecule traditionally has been dissected into three functional units: (i) the dodeca- helical transrnembrane pore that fomthe ion conductive pathway, (ii) two cytoplasrnically located nucleotide binding folds which hydrolyze ATP to open as well as to close the channel. and (iii) a cytoplasmically located R-domain, the phosphorylation of which is required to put CFTR into an activation competent fom. The major base phosphorylating CFTR is the CAMP-dependent protein kinase (PKA). Upon hormonal induction, PKA phosphorylates several sites within the R-domain, thereby allowing a graded response to various levels of stimulation. Thus far, only the importance of perfect dibasic consensus sites for potential interactions with PKA ha been investigated in this mechanism. The present study demonsmtes that PU-mediated phosphorylation under lirniting conditions also occurs on monobasic consensus sites and contributes to CFTR activation. Additional phosphorylation is shown to be accepted by sites that lack a positively charged residue in close physical proximity. To obtain an initial idea of associations between the three functional uni& of CFTR, this thesis also addresses the importance of the previously uninvestigated cytoplasmic loops (CLs) that connect the transrnembrane helixes on the cytoplasrnically exposed side of the pore-forming unit. Reconstruction of CF-associated point mutations in al1 four CLs illustrates that many of the amino acid substitutions inhibit maturation of Cmsuggesting that correct foiding of the loops may be critical for achievernent of the correct overall conformation of the protein. In addition, the CLs contribute to CFTR function since mutations in both CL1 and CL3 significantly alter the open probability of the chloride channel. However, the loops are functionaily distinct since CL1 mutations modify the mean closed tirne of the cbannel, whereas CL3 aiterations mainly affect the mean open time. The fact that mutations in the loops influence the gating of CFTR, rather than its conductance, may suggest that despite their proximity to the pore entrante, the importance of the CLs lies in relaying regdatory stimuli to the pore as opposed to an involvement in actual ion movement. Fabian S. Seibert Department of Biochernistry University of Toronto 1997 Thesis Title: Structure-Function Relationships of the Cytoplasrnic Domains of the Cystic Fibrosis Trammembrane Conductance Regulator 'Jeder Tag ist ein neuer Anfang, ein Morgen voiler Waerme.' Br. lmmanuel Jakobs 'Each day brings a new dawn.' ACKNOWLEDGMENTS Bavaria and Austria are linked by a graceful mountain named Untersberg. Should you ever visit Untersberg, you may climb one side of the mountain, cross a long plateau with beautiful alpine fauna and flora, and then descend on the opposite side through a steep, wet cave. This is the most întimidating part of the tour, but once greeted by the sunlight, you are rewarded with a rnagnificent view of the Northem Alps. When my father and 1 took this trip, we stopped on the plateau and talked about life. Maybe 1 have reached that sarne point in my studies, so 1 would Iike to sit dom and Say thank you to everybody who has made this possible. 1 am especially grateful to my supervisors, Dr. David Clarke and Dr. Jack Riordan, for their excellent guidance, continued support, and much patience. With his balanced, calm, but determined approach to life, Dr. Clarke never failed to disperse rny oh-so-fiequent womes. I especially know to appreciate that Dr. Clarke always looked out for me and ensured that things happened in such a way that they were beneficial to me and to my future. Dr. Riordan first introduced me to this tield of research, for which he radiates great enthusiasm. Dr. Riordan's excitement about rny data was highly rewarding and helped to push on. Both supervisors gave me much fieedom in my approach to the addressed problems, but at the same time, they were always willing to provide superb advice on theory and techniques. 1 was very fortunate to be allowed to see two quite different approaches to science and hope to be able to build on both. Thank you, David, thank you, Jack, for everything! An invaluable element towards the completion of this work was Dr. Tip Loo. 1 would Iike to thank Dr. Loo for many helpful discussions and for patiently giving expert advice. In molecular biology problems anse fiequently, but have no fear, there is Dr. Loo. Also. I now believe that the 'just do it' approach really works. Over the years 1 had many colleagues whose humor and advice were a tremendous help. Cheryl Ho was a wonderful lab-mate who trîed to make sure that 1 kept life in perspective and who was always willing to assist. Dr. Xiu-Bao Chang showed me how to cut a plasmid, Dr. Zbysko Gnelczak taught me the G-A-T-C's of CFTR,and Tim Jensen first htroduced me to phosphorylation experiments. Dr. Gergely Lukasc, Dr. Abdalla Mohammed, and Tom Singer gave me the illusion that 1 was something like a real scientist by fiequently discussing their hdings with me and Dr. Gretchen Kiser is the most cheerful penon there is in the CF field. Many thanks also to Noa Alon, Dr. Richard Callaghan, Dr. Am Duhanty, Barbara Greis, Yue-Xian Hou, Dr. Norbert Kartner, Dr. Mohabir Ramjeesingh, Monique Sapiano, Rose Templeton, Dr. Iris Ziegler, and our lab- neighbors. I want to express my gratitude to Dr. John Hanrahan for allowing me to visit his laboratory and to Dr. Yanlin Jia, Dr. Paul Linsdell, Dr. Ceri Mathews, and Joe Tabcharani for giving me the very basic feel that 1 have for the patch-clarnping technique and for showing me what Montreal is al1 about. Thank you ver-much, also, to my cornittee members, Dr. Reinhart Reithmeier and Dr. David Williams, for al1 their advice and especially for improving this thesis by critically and thoroughly reviewing it. Finally, 1 want to Say a very special thank you to my parents and to my brother Peter. My family was the one consistent point of reference over the last few years. They were always there for me to share the ups and to buffer the downs. 1 defmitely lucked out to be part of this family. WelI, it's time to head for the cave! TABLE OF CONTENTS ABSTRACT TABLE OF CONTENTS LIST OF FTGURES LIST OF TABLES LIST OF AIBBREVIATIONS XIV Short-forms xiv Legend of Phosphorylation Mutants xv CHAPTTER 1: INTRODUCTION Cystic Fibrosk (CF) Symptoms of the Disease Ainvays Pancreas Other Organs Treatments CF - a Disease of Altered Fluid Transport Physiology of the Sweat Gland Physiology of the Ainvays Search for the Biochemical Defect in CF The CF Gene and its Gene Product Identification of the Gene Affected in CF The Gene Product - CFTR Predictions of Topology ABC-superfamily of Proteins Function of the Gene Product Conductance Properties of CFTR Expression of CFTR Regdafion 4 CFTR Regulation by Phosphorylation CAMP-dependentprotein kinase (PU) Protein Kinase C (PKC) Additiond Kinases Phosphatases The R-domain Regulation by ATP Nucleotide Binding Folds Biochemical and Functional Findings Models of Regdation by ATP Evidence to Support ATP Models Reconciling Two Modes of Regulation Targeting and Processing of CFTR The Phe 508 Deletion Mutation Inefficient Processing of CFTR Processing Characteristics Chaperones Degradation of CFTR Rescue of Misprocessed Molecules Synthesis of the CFTR Protein Apical Processes in CFTR Expression Apical Targeting Recycling and Recniitment Additional Functions of the CFTR Molecule Classes of CF-causing Mutations Regulation of Sodium Conductance Regulation of the Ou~dRectifier History Activation of the Outward Rectifier Is CFTR an ATP Channel? Role in Mucin Secretion Additional Proposals CHAITER 2: MATERIALS AND METHODS Construction of Vectors and Mutants Expression of Mutants Temperature Shift and Glycerol Exposure Protein Detection Endoglycosidase H Digestion Phosphorylation of CFTR Cyanogen
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