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High-Pressure X-Ray Crystallography and Core Hydrophobicity of T4

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High-Pressure X-Ray Crystallography and Core Hydrophobicity of T4 HIGH-PRESSURE X-RAY CRYSTALLOGRAPHY AND CORE HYDROPHOBICITY OF T4 LYSOZYMES A Dissertation Presented to the Faculty of the Graduate School of Cornell University in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy by Marcus David Collins January 2006 This document is in the public domain. HIGH-PRESSURE X-RAY CRYSTALLOGRAPHY AND CORE HYDROPHOBICITY OF T4 LYSOZYMES Marcus David Collins, Ph.D. Cornell University 2006 While a great many protein structures are now known, considerably less is known experimentally about how these molecules reversibly fold and unfold into nearly unique, active structures. For more than 50 years, the central hypothesis has been that micro-scale phase separation between oil-like non-polar and charged or po- lar amino acid residues drives the formation of a “hydrophobic” protein core. A great deal of evidence supports this hypothesis, but the unfolding of proteins as a response to pressure contradicts it. A possible solution is the suggestion that pres- sure induced unfolding is a different process from thermally or chemically driven unfolding. Separately, little is known about the structural response of proteins to pressure, although pressure has clear and sometimes large effects on protein activ- ity and stability. For these reasons, we have chosen to study the cavity-containing mutant L99A of T4 Lysozyme, along with the wild-type protein, under pressures up to 2 kbar, a compression of about 0.1%. The protein is remarkably incompress- ible, and the presence of a cavity has almost no impact on the pressure response over the wild-type lysozyme. Instead, four water molecules cooperatively fill the cavity, interacting with each other and the protein roughly equally. We believe the cavity to be half full with water near 2 kbar, suggesting that despite its hydrophobic nature, the interior of a protein maintains strong electrostatic interactions. BIOGRAPHICAL SKETCH Marcus Collins and his twin brother Nathan were born in Portland, Oregon in August of 1977. Raised by an electrical engineer and a nurse, he developed an early interest in science, declaring at the age of 3 that he would like to become an “astronomical chemist”, whatever that might have meant to him. He spent a great deal of time in the woods hiking and skiing. He graduated from the University of Washington having climbed most of the Cascade volcanoes and with College and Departmental Honors in Physics. He was awarded an NSF Graduate Fellowship to study at Cornell University beginning in 1999. His present study of biological systems is a complete fluke, as he had no interest in biology in high school. At this point, his entire career appears to be some sort of cosmic coincidence, leaving him to wonder what the punchline will be. iii You have opened a new door, and I share this with you, for I have been where you are now. This world is more beautiful than I believe we can possibly comprehend. It has been a privelege to spend my days watching the tickings and tockings of an infinite universe. I dedicate this work to two people who have shared with me the equally infinite joy of watching it all. For Nathan, who will always be a physicist and more importantly my friend. and For Erin, whom I love dearly. iv ACKNOWLEDGEMENTS Words fail to describe the impact Sol Gruner has had on my life. For his con- stant patience, bizarre humor, and guidance I am eternally in his debt. Professors Neil Ashcroft, Jim Alexander, Persis Drell and Lois Pollack have shown me much compassion and care. Dr. Mark Tate has been a source of constancy and support throughout my time at Cornell. Professor (!) Peter Abbamonte has been a good friend as well. To all of them, my deepest thanks. I have greatly enjoyed my collob- oration with Dr. Michael Quillin and Professor Brian Matthews of the University of Oregon, and Gerhard Hummer of the National Institutes of Health. I would not be half the person I am were it not for the strength, inspiration, and guidance of my family: Dr. Wilfred and Mildred Gamon, Philip and Ellen Collins, and my parents, John and Kathryn Collins. Chris Mathieson, Matthew Van Sickle, and David Burdick have guided me and consoled me for many, many years. I used to enjoy talking to Raphael Kapfer about his interesting work pressurizing proteins. I dearly wish that he could share in what I have learned. Gil Toombes and Nozomi Ando have had great impact on this work and I will miss them both. The assis- tance of Paul Urayama, Marian Szebenyi, Richard Gillilan, David Schuller, and Andrew Stewart was invaluable as I began this work. The following people deserve no less mention: Gene Yore; Dr. Wai Wong; Dr. Larry Gulberg, who encouraged me in high school; Prof. David Boulware, who was my early mentor; Prof. Luke Keller, Dr. Donald Barry, Aaron Blake, Adam Kravetz, and Matthew Steven, who have all shared many a good adventure with me. Let us begin. v TABLE OF CONTENTS 1 Introduction 1 1.1 Whypressure? ............................. 1 1.1.1 Pressureeffectsonproteins . 2 1.1.2 Pressure as a thermodynamic variable . 3 1.1.3 Volumepropertiesofproteins . 6 1.2 Selecting probes for high pressure experiments . ..... 7 1.3 T4lysozymes .............................. 11 1.3.1 Structural and thermodynamic studies . 13 1.3.2 T4 lysozyme under pressure . 15 1.4 Hydrophobic models and protein folding . 17 1.4.1 Hydrophobicsolutesinwater . 18 1.4.2 Hydrophobicinteractions. 23 1.4.3 Hydrophobicity in proteins . 25 1.4.4 Unresolvedproblems . 26 1.5 GoalsandOrganization . 34 2 High Pressure Equipment 37 2.1 High-pressurebasics . .. .. 37 2.1.1 Pressurerange ......................... 38 2.1.2 Materials ............................ 38 2.1.3 Highpressureseals . 39 2.1.4 Pressure generation and measurement . 40 2.2 CrystallographicCell . 46 2.3 Othercellsandmethods . 49 3 Experimental Methods: Crystallographic Data Collection 52 3.1 Crystalgrowth ............................. 52 3.1.1 Basictechniques ........................ 52 3.1.2 PhageT4lysozyme . .. .. 54 3.2 Preparing crystals for diffraction experiments . ..... 57 3.2.1 Generalconsiderations . 57 3.2.2 Loading the Beryllium pressure cell . 58 3.3 Datacollection ............................. 62 3.3.1 F1stationequipment. 62 3.3.2 Choosing collection parameters . 64 3.3.3 Alignment of the crystal in the pressure cell . 66 3.3.4 Other beryllium cell issues . 68 3.4 Datacollected.............................. 68 vi 4 Refinement of Crystallographic X-ray data 72 4.1 Basicdiffractiontheory. 72 4.1.1 Quantummechanicalbasis . 72 4.1.2 Scatteringfactors . 79 4.1.3 The reciprocal lattice and symmetry . 80 4.1.4 Temperaturefactors . 84 4.2 Datareduction,refinement,anderror . 85 4.2.1 Reduction and observational uncertainties . .. 85 4.2.2 Thephaseproblem . .. .. 87 4.2.3 Maximum likelihood and error formalism . 89 4.2.4 Thelikelihoodfunction. 91 4.2.5 Errorformalism......................... 93 4.3 Practical aspects of model refinement . 97 4.3.1 Theatomicmodel........................ 97 4.3.2 Practical refinement indicators . 98 4.3.3 Ramachandranplots . 102 4.3.4 Electrondensitymaps . 102 4.4 Refinementprotocolandresults . 104 4.4.1 Procedures............................ 104 4.4.2 Robustmodelquantities . 106 4.4.3 Refinement statistics and review . 108 4.5 Summary ................................110 5 Structure of T4 lysozymes at high pressure 113 5.1 T4 lysozyme at ambient pressure . 113 5.1.1 Staticstructure . 113 5.1.2 Known modes of structural change in T4 lysozymes . 114 5.2 Methodsofstructurecomparison . 116 5.2.1 Orienting molecules for comparison . 117 5.2.2 Orientationofhelices . 121 5.2.3 Volumecalculation . 121 5.2.4 Detectionlimits. 124 5.2.5 Anoteonisotropicscaling . 125 5.3 Observed changes in the structure of T4 lysozyme at high pressure . 126 5.3.1 Overall changes in unit cell and molecular volume . 126 5.3.2 Changes in cavity volume . 127 5.3.3 Radiiofgyration . 128 5.3.4 Differencesintemperaturefactors . 131 5.3.5 Empiricaluncertainties . 133 5.3.6 Observed displacements at pressure . 135 5.3.7 Domainrealignment . 139 5.3.8 ChangesintheC-helix . 142 5.3.9 ChangesintheC-terminaldomain . 143 vii 5.4 Remarks.................................148 6 Observation and simulation of water in cavities at high pressure 150 6.1 Construction of experimental electron density maps . ...... 150 6.1.1 Review..............................150 6.1.2 Observed difference electron density maps . 151 6.1.3 Integrating electron density in the cavity . 153 6.1.4 Including water in the atomic model . 154 6.1.5 Waterorsomethingelse?. 155 6.2 Molecular dynamics simulation . 156 6.2.1 Principles of molecular dynamics . 157 6.2.2 TheAMBERforcefield . 158 6.2.3 Thermodynamics and implementation . 160 6.3 Observedwaterinthecavity. 163 6.3.1 ElectronDensityMaps . 163 6.3.2 Atomicmodel.......................... 166 6.4 MolecularDynamicsresults . 167 6.5 Othercavities ..............................171 6.5.1 WT*Lysozyme ......................... 171 6.5.2 OthercavitiesinL99ALysozyme . 172 6.6 Remarks.................................172 7 Strongly Interacting Protein Interiors 175 7.1 New thoughts on protein structure and folding . 175 7.1.1 Unfolding under pressure . 175 7.1.2 Buriedwaterandproteinfunction. 181 7.1.3 Side chain flexibility . 189 7.2 TheJanusfaceofwater . 195 7.3 Futuredirections .. .. .. 198 A Refinement scripts 200 A.1 Masterrefinementscript . 200 A.2 Callingscripts.............................. 212 B Structure analysis scripts 213 B.1 pdbtools.pm...............................213 B.2 linear.pm ................................234
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