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Biochemical and Genetic Investigations on Patients with Congenital Disorders of Glycosylation

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Biochemical and Genetic Investigations on Patients with Congenital Disorders of Glycosylation Biochemical and Genetic Investigations on Patients with Congenital Disorders of Glycosylation. by Faiqa Imtiaz A thesis submitted for the degree of Doctor of Philosophy (Ph.D.) in the Faculty of Life Sciences of the University of London Biochemistry, Endocrinology and Metabolism Unit Institute of Child Health University College London March 2002 ProQuest Number: U643421 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 complete 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 U643421 Published by ProQuest LLC(2016). Copyright of the Dissertation is held by the Author. All rights reserved. This work is protected against unauthorized copying under Title 17, United States Code. Microform Edition © ProQuest LLC. ProQuest LLC 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106-1346 ABSTRACT This study presents an overall review of the Congenital Disorders of Glycosylation (CDG) and describes genetic and enzymological investigations employed to identify and confirm the basic defect in 21 patients that were diagnosed as CDG-I on the basis of their clinical features and abnormal isoelectric focusing (lEF) pattern of serum transferrin. Fifteen patients from thirteen families were found to have CDG-Ia on the basis of markedly reduced phosphomannomutase (PMM) activity in fibroblasts in culture. Mutation analysis of the PMM2 gene demonstrated the presence of 8 missense mutations. All the patients were compound heterozygotes for these mutations. No correlation could be established between genotype and clinical/enzymological phenotypes in the CDG-Ia patients. Human PMM is encoded by two gene^ PMMl (22ql3) and PMM2 (16pl3), which are expressed in a tissue-specific manner. Patients with severe and milder forms of CDG-Ia were analysed for any possible mutations in PMMl. No mutations were detected. Detailed enzyme kinetics experiments were performed to investigate the inhibition of PMM using synthetic analogues. One patient had reduced phosphomannose isomerase (PMI) activity in fibroblasts and genetic analysis of the MPI gene, encoding PMI showed a homozygous mutation, D131N, which confirmed the patient suffered from CDG-Ib. Another patient who had normal PMM and PMI activities in fibroblasts was found to have missense mutations in the hALG6 gene encoding al,3 glucosyltransferase and was classified as CDG-Ic. Four patients, classified as CDG-Ix, who had normal PMM and PMI activities but defective protein iV-glycosylation as indicated by abnormal IFF patterns of serum transferrin, were investigated for plausible defects in the enzymes involved in the synthesis of precursor glucosyl donors for lipid-linked oligosaccharides, namely, GDP- mannose pyrophosphorylase, dolichol phosphate mannose synthase, and glutamine: fructose-6-phosphate amidotransferase, in fibroblasts. No significant difference was discernible in specific activities of these enzymes between control and patients’ fibroblasts. These four patients were also tested for a-glucosidase I activity in fibroblasts (a marker for CDG-IIb), but showed no significant difference compared with controls. 11 Preface Part of the work presented in this thesis has been published Papers 1. Martin A, Watterson M, Brown A, Imtiaz F, Winchester B. G, Watkin D J and Fleet G.WJ. (1999) 6R- and 6S-6C-Methylmannose and D-mannuronolactone. Inhibition of phosphoglucomutase: agents for the study of the primary metabolism of mannose. Tetrahedron Asymmetry 10: 355-366. 2. Imtiaz F, Worthington V, Champion M, Beesley C, Charlwood J, Clayton P, Keir G, Mian N, Winchester B. (2000) Genotypes and Phenotypes of patients in the UK with carbohydrate-deficient glycoprotein syndrome type I. J Inherit Metab Dis 23:162-174. 3. Schollen E, Borland L, de Koning T.J, Van Diggelen O P, Huijmans J.G.M, Marquardt T, Babovic-Vuksanovic D, Patterson M, Imtiaz F, Winchester B, Adamowicz M, Pronicka E, Freeze H and Matthijs G. (2000) Genomic Organization of the Human Phosphomannose Isomerase (MPI) Gene and Mutation Analysis in Patients with Congenital Disorders of Glycosylation Type Ib (CDG-Ib). Human Mutation 16: 247-252. 4. Matthijs G, Schollen E, Bjursell C, Erlandson A, Freeze H, Imtiaz F, Kjaergaard S, Martinsson T, Schwartz M, Seta N, Vuillaumier-Barrot S, Westphal V and Winchester B. (2000) Mutations in PMM2 That Cause Congenital Disorders of Glycosylation, Type la {CDG-\d).Human Mutation 16: 386-394. 5. Hendriksz CJ, McClean P, Henderson M J, Keir, Worthington V C, Imtiaz F, Schollen E, Matthijs G, Winchester B G. (2001) Successful treatment of carbohydrate deficient glycoprotein syndrome type lb with oral mannose.Arc/z Dis Child S5: 339-340 Abstracts 1. Imtiaz F, Worthington V, Champion M, Beesley C, Charlwood J, Clayton P, Keir G, Mian N, Winchester B. (1999) Genotypes and Phenotypes of patients in the UK with carbohydrate-deficient glycoprotein syndrome type I. J Inherit Metab Dis Supplement, Volume 22: July; Abstract. Ill Poster Presentations 1. Title: Biochemical and genetic analysis of British CDGS type I patients Presented at: SSIEM 37* Annual Symposium, September 1999, Genoa, Italy Imtiaz F, Worthington V, Champion M, Beesley C, Charlwood J, Clayton P, Keir G, Winchester B. 2. Title: Successful treatment of carbohydrate deficient glycoprotein syndrome type lb with oral mannose Presented at: Society for Glycobiology, November 2000, Boston, USA Imtiaz F, Hendriksz CJ, McClean P, Henderson M J, Keir, Worthington V C, Winchester B. IV Acknowledgements I am extremely grateful to my principal supervisor Professor Bryan Winchester for his continued support, guidance and concern. I would like to thank Dr. Nasi Mian for his endless assistance, ideas and suggestions throughout this PhD. I would also like to thank Professor Peter Clayton, Dr. Geoff Keir and especially Dr. Clare Beesley for her role as a supervisor and friend. I am indebted to The Enzyme Laboratory and would like to give a special thanks to Elizabeth Young, Viki Worthington and Derek Burke for their assistance. I would also like to thank the clinicians who referred the patients and their families who allowed the further investigation of defects in their children. I would really like to thank all my friends at the Institute of Child Health, especially Philippa, Kevin, Tammy, Anna, Wendy, Hugh, Paulett, George and Simon for making the past four years so much fun. I would like to give special thanks to Professor Pinar Ozand, King Faisal Specialist Hospital, for taking me under his wing and introducing me to this field of science and to Dr. Mohammed, Saudi Arabian Cultural Bureau, for looking after me for the past eight years. Finally, I am eternally grateful to my wonderful parents for their unconditional love and support, my brothers and to my husband Shehzad for his unceasing patience, support and love. Table of Contents Table of Contents Abstract ii Preface iii Acknowledgements v Table of Contents vi List of Figures xiii List of Tables xvii List of Abbreviations xix Chapter 1: Introduction 1 1.1 Preface 1 1.2 Protein Glycosylation 2 1.2.1 Protein 0-linked Glycosylation 3 1.2.1.1 0-P-GalNAc-linked glycosylation 3 1.2.1.2 0-P-GlcNAc-linked glycosylation 4 1.3 A-linked Glycosylation 4 1.3.1 Assembly of the lipid-linked oligosaccharide 5 1.3.1.1 Dolichol and dolichol phosphate 7 1.3.1.2 The synthesis of glycosyl substrates for the 9 assembly of the LLO 1.3.1.3 Biochemistry and enzymology of the synthesis 9 of nucleotide-activated sugars 1.3.1.4 Synthesis of dolichol phosphate mannose and 10 dolichol phosphate glucose 1.3.1.5 Glycosyltransferases involved in LLO assembly 12 1.3.1.5.1 Topography of the synthesis of the LLO 15 1.3.1.6 Self-regulatory aspects of LLO assembly 16 1.3.1.7 Bypass or salvage routes involved in LLO synthesis 17 under non-physiological conditions 1.3.2 The Oligosaccharyltransferase (OST) complex 18 1.3.2.1 Requirements and constraints of the oligosaccharyl- 20 transferase reaction with respect to the polypeptide as a substrate 1.3.2.1.1 Co-translational translocation of polypeptides 20 to the ER lumen 1.3.2.1.2 Influence of the nature of the JV-glycosylation 21 sequon and other polypeptide-structure based constraints on the ^-glycosylation reaction VI Table of Contents 1.3.2.2 Effects of truncation of LLO on its transfer to the polypeptide 23 by OST and post-transfer processing in the ER 1.3.2.2.1 Influence of structural aspects of the LLO donor on 24 OST reaction efficiency 1.3.3 Processing of protein-bound oligosaccharides in the ER 25 1.3.4 Processing of protein N-linked oligosaccharides in Golgi apparatus 28 1.4 Congenital Disorders of Glycosylation 30 1.5 CDG-I syndromes 30 1.5.1 Protein Æ-glycosylation defect in serum transferrin in CDG-Ia 33 1.5.1.1 Genetic defect in CDG-Ia 34 1.5.2 Biochemical defect in CDG-Ib 34 1.5.2.1 Genetic defect in CDG-Ib 36 1.5.2.2 Mannose therapy as treatment for CDG-Ib 36 1.5.3 Biochemical defect in CDG-Ic 37 1.5.3.1 Genetic defect in CDG-Ic 39 1.5.4 CDG-Id 41 1.5.4.1 Biochemical defect in CDG-Id 41 1.5.4.2 Genetic defect in CDG-Id 42 1.5.5 Biochemical defect in CDG-Ie 42 1.5.5.1 Genetic defect in CDG-Ie 43 1.5.6 CDG-If 43 1.6 CDG-II syndromes 46 1.6.1 CDG-IIa-iV-acetylglucosaminyltransferase II deficiency 47 1.6.2 CDG-IIb-a-Glucosidase I deficiency 48 1.6.3 CDG-IIc-GDP-fucose deficiency 50 1.7 Other disorders of protein glycosylation 52 1.8 Aims of the thesis 53
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