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Carbohydrate and Bacterial Binding Specificity of Human Intelectin-1

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Carbohydrate and Bacterial Binding Specificity of Human Intelectin-1 Carbohydrate and Bacterial Binding Specificity of Human Intelectin-1 By Christine R. Isabella M.S. Biochemistry University of Wisconsin – Madison, 2017 B.S. Molecular and Cellular Biology University of Puget Sound, 2012 SUBMITTED TO THE DEPARTMENT OF CHEMISTRY IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY IN CHEMISTRY AT THE MASSACHUSETTS INSTITUTE OF TECHNOLOGY February 2021 Ó 2021 Massachusetts Institute of Technology. All Rights Reserved. Signature of Author: _____________________________________________________________ Department of Chemistry January 11, 2021 Certified By: ___________________________________________________________________ Laura L. Kiessling Novartis Professor of Chemistry Thesis Supervisor Accepted By: ___________________________________________________________________ Adam P. Willard Associate Professor of Chemistry Chair, Department Committee on Graduate Students 1 This doctoral thesis has been examined by a committee of professors from the Department of Chemistry as follows: Barbara Imperiali _______________________________________________________________ Thesis Committee Chair Class of 1922 Professor of Biology and Chemistry Laura L. Kiessling _______________________________________________________________ Thesis Supervisor Novartis Professor of Chemistry Ronald T. Raines ________________________________________________________________ Thesis Committee Member Roger and Georges Firmenich Professor of Natural Products Chemistry Eric J. Alm ____________________________________________________________________ Thesis Committee Member Professor of Biological Engineering 2 Carbohydrate and Bacterial Binding Specificity of Human Intelectin-1 By Christine R. Isabella Submitted to the Department of Chemistry on January 15, 2021 in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in Chemistry ABSTRACT The mucosal surfaces of the human body exist in close contact with complex communities of resident microorganisms termed the microbiome. The microbiome is crucial for host health, and therefore the host must discern betWeen which microbes colonize and which must be cleared. Human soluble lectins are secreted carbohydrate-binding proteins that bind microbes by specific recognition of cell surface glycans. Many soluble lectins are important mucosal innate immune factors, as lectins binding to microbes can result in their clearance from the host. However, the glycan and microbial binding specificities of lectins are poorly defined. In this thesis, I aim to address this gap with a focus on human intelectin-1 (hItln-1). In Chapter 1, I revieW the recently identified class of lectins, the X-type lectins. The X-type lectins, or intelectins, are found throughout chordates and share highly conserved sequences but their biological roles are not well understood. However, their expression patterns and microbial binding specificity suggest a role in regulation of the microbiome. In Chapter 2, I build on previous work to further define hItln-1 carbohydrate specificity. These studies reveal that carbohydrate conformation is stabilized by stereoelectronic effects, and that carbohydrates are bound by hItln-1 in their stabilized conformation. In Chapter 3, I turn to bacterial cell recognition by hItln-1 and determine that hItln-1 displays competitive binding to bacterial strains in a mixture. These studies reveal the need to assay lectin-bacteria recognition against diverse microbial communities to understand their binding specificity in a biological context. In Chapter 4, I develop lectin-sequencing (lectin- SEQ) as a method for identifying bacterial targets of lectins in native communities. Using the human stool microbiome, I assess binding to stool bacteria by hItln-1, and surfactant protein-D (SP-D). Lectin-SEQ reveals that hItln-1 recognizes health-promoting commensal bacteria, while SP-D recognizes pathogenic bacteria. These results indicate a novel role for hItln-1 in promoting colonization of commensal bacteria. Thesis Supervisor: Laura L. Kiessling Title: Novartis Professor of Chemistry 3 Acknowledgements It turns out that a Ph.D. is true type II fun. There were countless times when I thought I Wouldn’t do it, and for all of those times there were people there who supported and encouraged me, and those who ensured that, in the end, it all looked like fun. To all of you, I owe a debt of gratitude. First, I must thank Laura. You have alWays encouraged me and believed in my abilities more than I believed in myself. I will alWays be grateful for your push to dive deep into lectin- SEQ and your interest and excitement in seeing it through to the finish line. I appreciate, too, the moments aWay from the science when you took the time to support me. I feel very lucky to have an advisor who truly cares about me as a person and a scientist. The Kiessling Group has been an incredible place to learn and live and grow over the past five years. I was draWn to the lab in large part because of the people, and I still feel lucky to spend my days with you all. I have to thank Darryl, for recruiting me, for teaching me all of the hIntL secrets, for believing in my abilities, and for passing down such an aWesome project. I learned so much from you in the first months of my time in the lab that set the stage for my time in the Kiessling lab, and to this day, I hear your voice in my head talking about all of the cool hIntL projects we could do. Heather, I will never forget the first time you talked to me. You offered me a pour-over coffee and I felt like I was welcomed into a club. I admire you so much as a scientist and a person, and I learned so much from you, including but not limited to how to most efficiently order Jimmy John’s to the lab. Alex—We really went through it all together. You have been a source of encouragement to me day after day throughout the years and I am appreciative of you alWays making the time to troubleshoot experiments, chat, and snack. I hope one day we can return to Bull Shoals and live our best lives. Sayaka, thank you for alWays sharing your snacks with me and reminding me to eat when I am hangry. Thank you for alWays taking the time to help me think through experiments and results. And thank you for just being the most kind and sincere and caring person, and for running TWO half marathons with me that I Was undertrained for. Finally, I owe so much to LectinLand for embodying the “all hands on deck” motto. I am grateful for having such a wonderful team with so much engagement and excitement about all of our various projects. Thank you all for teaching me, working with me, spending hours sorting bacteria with me, and just generally being the best subgroup. I want to next thank those who made UW – Madison feel like home. To my IPiB family—moving to a neW institution made me realize how special the people and the relationships built at UW truly are. To Delia, my soul tWin and little sister, thank you for everything. To Dylan (Dylz), our QQ and Dominoes study sessions got me through so much, and have been greatly missed the last three years. And I’m guessing you really need a haircut. To Dana, I am yet to meet a comparable cooking partner. To Mark, my bike has been lonely, and I haven’t fallen off of it recently. To Karl, I hope my life legacy is the flong cape, and I am so glad that I get to still see you in Boston. To Anji, you have been an inspiration to me since the day I met you and I can’t wait to see what you do next. Ian and Sue, I’m so glad that we were all Discertators together, and that it led to so many adventures in Wisconsin and Boston. From bike camping to Friday Fish Fry to candlepin bowling, you guys have been incredible friends. I am 4 also grateful that I got to collaborate with Ian and had the opportunity to learn so much about protein crystallography from him. When the Kiessling Group moved to MIT, I was lucky to meet incredible people who have made my experience in Cambridge unforgettable. Lisa, you were my first MIT friend and you have alWays made me feel welcome here. I am grateful to have you as a source of encouragement and inspiration, for teaching me everything about job hunting, and for countless runs…and pastries. Smrithi, thank you for alWays showing up to lab with a smile and ready to make lectins in cells that were basically dead. You brought much needed light to my days and real perseverance to our project and I will alWays be sad that a pandemic cut your time in the lab short. I have had so much fun working with you and watching you grow over the years, and I am excited to see what you do next. Katherine, thank you for being a great friend, only sometimes being distracting, and for alWays being passionate. I am grateful for the time we spent as co- presidents of WIC, for ceramics (RIP), and for alWays having you to talk to and knowing that you will go to bat for me and/or probably literally fight people if I need you to. Victoria, you are Wise beyond your years. Thank you for alWays keeping the perspective that life is full of pain and that you can’t ruin a project with one experiment. Janet, we might not have a snack shelf, but We have many snack adventures. I am grateful for our quarantine walks and for your listening ear and constant encouragement. I don’t know if I would have made it through the last feW months if it weren’t for both of you, Sugo Sunday, Caturday, and boba. I believe you will truly move with motion one day. There are a feW very special people who I wouldn’t have made it through without.
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