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Single-Molecule Spectroscopy Studies of the Conformational Dynamics of Enzymes

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Single-Molecule Spectroscopy Studies of the Conformational Dynamics of Enzymes SINGLE-MOLECULE SPECTROSCOPY STUDIES OF THE CONFORMATIONAL DYNAMICS OF ENZYMES Maolin Lu A Dissertation Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY December 2014 Committee: H. Peter Lu, Advisor Lewis Fulcher Graduate Faculty Representative John Cable Massimo Olivucci ii ABSTRACT H. Peter Lu, Advisor Conformational motions of enzymes are highly dynamic and intrinsically stochastic. Obtaining molecular level insights into conformational dynamics of enzymes is critical for unraveling the complex intimate structure-to-function relationship. This dissertation describes the investigation of conformational dynamics of HPPK (6-hydroxymethyl-7,8-dihydropterin pyrophosphokinase) and T4 lysozyme by single-molecule FRET (Förster/fluorescence resonance energy transfer) spectroscopy and photon stamping spectroscopy. This dissertation also demonstrates the developments of corresponding single-molecule spectroscopic approaches to serve scientifically experimental demands. Multiple conformational intermediate states and multi-dimensional conformational motions of T4 lysozyme have been observed. The Markov process has successfully reproduced the experimental observations, suggesting that T4 lysozyme hinge-bending open-close conformational changes follow multiple pathways involving multiple intermediate states. The combination of lifetime and anisotropy results presents a whole picture of multi-dimensional conformational dynamics in the process of T4 lysozyme open-close hinge-bending. The non- exponential features of both lifetime and anisotropy autocorrelation functions reveal dynamic and static inhomogeneity/complexity of multi-dimensional conformational fluctuations. The investigations of probing and manipulating HPPK conformational dynamics has been described. The consistency between the decay rate of donor lifetime and rising rate of acceptor lifetime gives a direct observation of FRET dynamic process at single-molecule level. The autocorrelation analysis of donor lifetimes have revealed intermittent conformational coherence iii of multiple HPPK Loop3-active site conformational states, regulated by substrate-enzyme interactions. Mechanically manipulating a targeted dye-labeled single HPPK in pinpoint nano- scale precision and simultaneously monitoring the conformational changes during the AFM pulling event has been achieved. The observed results of different lifetime fluctuations, distinct anisotropy fluctuations and various dynamic rates have suggested the existence of function-inert and function-active scenarios of HPPK Loop 3-active site conformational dynamic motions. The developments of single-molecule spectroscopic approaches have been demonstrated, including 1) single molecule photon stamping FRET spectroscopy, on the basis of only measuring the donor’s lifetime trajectory; 2) single-molecule AFM-FRET nanoscopy, capable of effectively pinpointing and mechanically manipulating a targeted dye-labeled single protein in a large sampling area; and 3) single-molecule multi-parameter photon stamping spectroscopy system, integrating fluorescence anisotropy-FRET-lifetime and capable of observing single- molecule multi-dimensional conformational motions. iv TO THE MEMORY OF MY BELOVED GRANDPARENTS FOR THEIR UNCONDITIONAL LOVE AND SELFLESS SUPPORT v ACKNOWLEDGMENTS In the past five and half years, I have received valuable knowledge, experiences and support from many talented people. I would love to express my appreciations to them at this moment. I would love to express my deep thanks to my advisor, Dr. H. Peter Lu, for all the financial support, academic advice, professional training, and patient understanding. His professional attitude and quantitative thinking have great influence on my future career. His comprehensive interdisciplinary knowledge motivates me to expand my visions to new field and combine different knowledge together. I would like to thank my committee members: Dr. John R. Cable, Dr. Massimo Olivucci, and Dr. Lewis Fulcher for their valuable time. I am thankful to the faculty and staff working in the Center for Photochemical Sciences, particularly Dr. Alexander N. Tarnovsky, Dr. Ksenija D. Glusac and Dr. Thomas H. Kinstle for their teaching, Nora Cassidy, Alita Frater, Charles Codding, and Doug Martin for their help and coordinates. I feel delighted to thank my current and past group members for sharing their valuable experiences, especially Dr. Yuanming Wang, Dr. Yufan He, Dr. Desheng Zheng, Dr. Nipedita Pal, Dr. Dibyendu Kumar Sasmal and Dr. Vishal Govind Rao. I would love to thank my dear friends: Wendy Jenkins, Ken Jenkins, Marie Derkis, Julie George, William Bradley Burgess, Yenlin Goh, Ying-Wei Sung, Papatya C. Sevinc, Valentina Prusakova, Qian Wang, and Min Gu for their friendship, support, company and encouragement. I am very grateful to my big peasant family for their love and support, specifically my parents, my sisters, my brother, my nieces and nephews. I want to express my special thanks to Yan Han for unconditional love, persistent support, unwritten understanding, long-time waiting and company. vi TABLE OF CONTENTS Page CHAPTER 1. INTRODUCTION: SINGLE-MOLECULE SPECTROSCOPY AND SINGLE- MOLECULE ENZYMATIC DYNAMICS .................................................................................... 1 1.1. Single-Molecucle and Ensemble-Level Studies ............................................................... 1 1.2. Single-Molecule Fluorescence Spectroscopy................................................................... 4 1.2.1. Basic Requirements of Single-Molecule Fluorescence Spectroscopy ...................... 4 1.2.2. Single-Molecule Fluorescence Imaging and Detection ............................................ 5 1.3. Single-Molecule FRET Theory ...................................................................................... 12 1.3.1. FRET Fundamentals ............................................................................................... 12 1.3.2. FRET Pairs .............................................................................................................. 20 1.3.3. FRET Detection ...................................................................................................... 22 1.4. Biological Applications of Single-Molecule FRET ....................................................... 23 1.5. Single-Molecule Fluorescence Anisotropy .................................................................... 24 1.6. Single-Molecule Conformational Dynamics of Enzymes .............................................. 26 1.7. References ...................................................................................................................... 28 CHAPTER 2. EXTRACTING MULTIPLE INTERMEDIATE STATES OF SINGLE- MOLECULE T4 LYSOZYME FROM BUNCHED SUB-STEP CONFORMATIONAL MOTIONS .................................................................................................................................... 37 2.1. Introduction .................................................................................................................... 38 vii 2.1.1. Conformational Flexibility...................................................................................... 38 2.1.2. Multiple Conformational Intermediate States ......................................................... 39 2.1.3. Introduction of T4 Lysozyme ................................................................................. 40 2.2. Materials and Methods ................................................................................................... 41 2.2.1. Materials ................................................................................................................. 41 2.2.2. Single-Molecule Measurements .............................................................................. 42 2.2.3. Markov Model Analysis ......................................................................................... 43 2.3. Results and Discussion ................................................................................................... 47 2.4. Conclusions .................................................................................................................... 59 2.5. References ...................................................................................................................... 60 CHAPTER 3. MANIPULATING PROTEIN CONFORMATIONS BY SINGLE-MOLECULE AFM-FRET NANOSCOPY ......................................................................................................... 64 3.1. Introduction .................................................................................................................... 64 3.1.1 Single-Molecule Conformational Changes ............................................................. 64 3.1.2. Optical-AFM Correlated Approaches ..................................................................... 65 3.1.3. Biological Functions and Catalytic Reactions of HPPK Kinase ............................ 68 3.2. Experimental Sections .................................................................................................... 71 3.2.1 Sample Preparation ................................................................................................. 71 3.2.2. AFM-FRET Correlated Measurements................................................................... 73 3.3. Results and Discussion ..................................................................................................
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