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Thesis Phd DEGREE of GRENOBLE UNIVERSITY Laura Amandine Thesis Submitted to obtain the PhD DEGREE OF GRENOBLE UNIVERSITY Speciality : Structural Biology and Nanobiology Ministerial decree : 7th August 2006 Presented by Laura Amandine LALLEMAND Thesis directed by Sean Mc SWEENEY and co-directed by Andrew Mc CARTHY prepared in the Structural Biology Group of ESRF (European Synchrotron Radiation Facility) in the Doctoral School of Chemistry and Life Sciences Structural and biochemical characterisation of enzymes involved in chlorogenic acid biosynthesis Nicotiana tabacum 4-coumarate CoA ligase (4CL) Coffea canephora hydroxycinnamoyl-CoA quinate/ shikimate hydroxycinnamoyltranferases (HCT, HQT) Dissertation defended on March, 21st 2011 , in front of a jury composed of : Dr. Nushin AGHAJARI Reviewer Dr. Anne IMBERTY President Pr. Catherine LAPIERRE Reviewer Dr. Andrew Mc CARTHY Thesis director Dr. James Mc CARTHY Member Dr. Sean Mc SWEENEY Thesis director THÈSE Pour obtenir le grade de DOCTEUR DE L’UNIVERSITÉ DE GRENOBLE Spécialité : Biologie structurale et nanobiologie Arrêté ministériel : 7 août 2006 Présentée par Laura Amandine LALLEMAND Thèse dirigée par Sean McSWEENEY et co-dirigée par Andrew McCARTHY préparée au sein du Groupe de Biologie Structurale de l'ESRF (Installation Européenne de Rayonnement Synchrotron) dans l'École Doctorale Chimie et Sciences du Vivant Caractérisation structurale et biochimique d'enzymes impliquées dans la biosynthèse des acides chlorogéniques Nicotiana tabacum 4-coumarate CoA ligase (4CL) Coffea canephora hydroxycinnamoyl-CoA quinate/shikimate hydroxycinnamoyltranférases (HCT, HQT) Thèse soutenue publiquement le 21 Mars 2011 , devant le jury composé de : Mme, Nushin, AGHAJARI Rapporteur Mme, Anne, IMBERTY Président du Jury Mme, Catherine, LAPIERRE Rapporteur M., Andrew, McCARTHY Directeur de thèse M., James, McCARTHY Membre M., Sean, McSWEENEY Directeur de thèse Acknowledgments This project was supported by a doctoral fellowship co-financed by Nestlé Research and the European Synchrotron Research Facility (ESRF). Most of the work was carried out in the Partnership for Structural Biology building and at the synchrotron facility in Grenoble. I am grateful to my supervisors Sean McSweeney, for accepting me as a PhD student in his group, and Andrew McCarthy, for his scientific support and guidance throughout this project. I express all my gratitude to Gordon Leonard for his valuable comments on this manuscript. I thank all the members of the ESRF Structural Biology Group and especially Virginie Carbonell, who contributed to the structural studies as a Master student. I also thank the European Molecular Biology Laboratory (EMBL)/ ESRF Joint Structural Biology Group for access and support at the synchrotron beamlines. I thank the High Throughput Crystallisation Laboratory (HTX) of the EMBL-Grenoble Outstation and the Quality Control platform of the Institut de Biologie Structurale for their technical assistance. I thank the EMBL-Heidelberg Protein Production and Purification core facility for their help concerning the pET-28M-SUMO3 vector. I gratefully acknowledge James McCarthy for his collaboration and Emilie Devienne, who contributed to the biochemical studies as an undergraduate student. I thank all the Gene Discovery and the Plant Chemistry and Functionality groups of Nestlé R&D centre in Tours, and especially Maud Lepelley, Victoria Caillet and Stéphane Michaux for their help and kindness during my visits. Finally I thank Karin Kraehenbuehl for carrying out the MS analysis and for providing the 5-FQA sample. Contents ABSTRACT ....................................................................................................................................... I RESUME ..................................................................................................................................... III ABBREVIATIONS ............................................................................................................................... V CHAPTER 1. INTRODUCTION .............................................................................................................. 7 1.1. Structure and function of plant secondary metabolites ........................................... 7 1.1.1. Generalities..................................................................................................... 7 1.1.2. Terpenes ......................................................................................................... 8 1.1.3. Alkaloids ........................................................................................................ 8 1.1.4. Phenolics ........................................................................................................ 8 1.2. Structural diversity of the phenolic compounds ...................................................... 9 1.2.1. Classification .................................................................................................. 9 1.2.2. Structure of the hydroxycinnamic acids (HCAs) ......................................... 10 1.2.3. Central role of HCAs and their corresponding CoA thioesters .................... 11 1.2.4. Structure of the chlorogenic acids (CGAs) .................................................. 11 1.2.5. Distribution of CGAs in the plant kingdom ................................................. 14 1.2.6. Related esters................................................................................................ 16 1.3. The biological role of CGAs in plants ................................................................... 16 1.3.1. Intermediates in lignin biosynthesis ............................................................. 16 1.3.2. Defence compounds ..................................................................................... 17 1.4. The impact of CGAs in humans ............................................................................ 18 1.4.1. On the food properties .................................................................................. 18 1.4.2. On health ...................................................................................................... 19 1.5. Provider pathways of CGA precursors .................................................................. 21 1.5.1. The shikimic acid pathway ........................................................................... 21 1.5.2. The general phenylpropanoid pathway ........................................................ 22 1.5.3. 4-Coumarate CoA ligase (4CL) ................................................................... 24 1.6. Genes/ enzymes of the core pathway for CGA biosynthesis ................................. 30 1.6.1. Coumaroyl ester 3-hydroxylase (C3H) ........................................................ 30 1.6.2. Hydroxycinnamoyltransferases (HCT, HQT) .............................................. 31 CHAPTER 2. MATERIALS AND METHODS ......................................................................................... 43 2.1. Cloning, over-expression and purification ............................................................ 43 2.1.1. Preliminary data ........................................................................................... 43 2.1.2. Production of recombinant 4CL2 ................................................................. 44 2.1.3. Production of recombinant HCT and HQT .................................................. 47 2.2. Biophysical characterisation .................................................................................. 60 2.2.1. Thermofluor assays ...................................................................................... 60 2.2.2. Isothermal calorimetry ................................................................................. 64 2.3. Biochemical characterisation ................................................................................. 65 2.3.1. Introduction .................................................................................................. 65 2.3.2. The high-performance liquid chromatography system ................................ 65 2.3.3. Enzymatic synthesis and purification of the CoA thioesters........................ 73 2.3.4. Comparison of the HCT and HQT-catalysed forward reactions .................. 74 2.3.5. Comparison of the HCT and HQT-catalysed reverse reactions ................... 75 2.3.6. Comparison of the activity of native and mutant HCTs............................... 76 2.4. Structural characterisation ..................................................................................... 77 2.4.1. Introduction .................................................................................................. 77 2.4.2. Tobacco 4CL2 crystallisation and structure determination.......................... 79 2.4.3. Coffee HCT crystallisation and structure determination.............................. 83 2.4.4. Homology-modelling of CcHQT ................................................................. 86 2.5. Docking calculations ............................................................................................. 86 2.5.1. Docking of hydroxycinnamic acids in 4CL2-CoA-AMP ............................ 86 2.5.2. Docking of substrates in HCT ...................................................................... 88 CHAPTER 3. RESULTS ...................................................................................................................... 91 3.1. Introduction...........................................................................................................
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