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© 2016 Itamar Livnat . © 2016 Itamar Livnat ANALYSIS OF D-AMINO ACID-CONTAINING NEUROPEPTIDES IN MOLLUSKS AND RODENTS BY ITAMAR LIVNAT DISSERTATION Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Molecular and Integrative Physiology in the Graduate College of the University of Illinois at Urbana-Champaign, 2017 Urbana, Illinois Doctoral Committee: Professor Jonathan V. Sweedler, Chair Professor Martha U. Gillette Associate Professor Lori T. Raetzman Associate Professor Justin S. Rhodes ABSTRACT Modern mass spectrometry (MS)-based neuropeptidomics continues to reveal an unprecedented level of chemical complexity in the nervous system on the peptide level, with sometimes hundreds of peptides expressed by or secreted onto specific structures. These neuropeptides have evolved for animal behaviors and regulating neuronal circuits. Neuropeptides exert their responses through GPCRs in most cases, and in order to interact with the GPCR, their structure is important. Their structures are not solely defined by their peptide sequence, but may instead depend on the myriad post-translational modifications (PTMs) they undergo. Thus, the hunt for neuropeptides must include the discovery of the exact chemical forms of the physiologically active peptides as these are required to achieve their receptor binding capability, degradation and uptake pathways, and hence bioactivity. Life, on a molecular level, has a stereoselective preference for many biochemical processes. This is especially true for protein-derived neuropeptides, which are translated by ribosomes using exclusively L-amino acids. However, D-amino acids are present in animal peptides, first evidenced by dermorphin, an analgesic skin peptide in Phyllomedusa sauvagei. Dermorphin’s existence as a D-amino acid-containing peptide (DAACP) proved not to be a singularity, but instead revealed a novel post-translational modification: peptide isomerization. Roughly 40 endogenous animal DAACPs have been found in 3 evolutionarily distinct phyla as toxins, hormones, and importantly for this work, neuropeptides. Isomerization alters the three-dimensional shape of a peptide. This change in shape has been associated with a change in bioactivity of a peptide, with the DAACP being the sole bioactive form. However, isomerization does not change the molecular weight of a peptide, making it difficult to detect using MS. Thus, bioactive peptides are likely hiding in neuropeptidomics study under the assumption that these peptides, like the majority of life, are formed solely of L-amino acids. Understanding the physiological purpose of DAACPs requires their further discovery. An approach to characterize unknown DAACPs, the DAACP discovery funnel, is presented in this work. It aims to solve this problem through a series of adapted MS-based analytical techniques capable of identifying potential DAACPs and assaying their amino acids for their chiral state. The discovery funnel is used to discover new DAACPs in the Aplysia californica nervous system and is applied, as pioneering work, to nervous system structures in rodents. ii ACKNOWLEDGMENTS My thesis work was achieved through the support of many individuals, and I cannot feel lucky enough for their help. In particular, Professor Jonathan Sweedler, my thesis advisor, has been extremely helpful and supportive through the course of this work. His insight and enthusiasm for this project has made so much of this work feasible and enjoyable to perform. Truly, it has been a privilege to work with him, and I look forward to continuing to support this project while I am in medical school. The insight and support of my committee members has been vital to the achievement of my work, as well. Professor Martha Gillette has been an extremely valuable collaborator for the pioneering work into investigating D-amino acid- containing peptides (DAACPs) in the rodent nervous system. Her insight and advice about the suprachiasmatic nucleus, as well as giving me access to her animals and lab members, is something for which I am incredibly grateful. It was only through her support that I earned not one but two graduate student fellowships during my time here. I also rotated through Martha Gillette’s laboratory, learning about the importance of circadian rhythms, which helped motivate me to take on this difficult and exciting aspect of the project. Professor Justin Rhodes has been a very inquisitive and encouraging committee member, taking such an interest in the research topic that talking to him about it always would remind me just how cutting edge this work is. Professor Lori Raetzman has provided kind support and discerning questions, and her expertise has helped guide some of the D-amino acid-containing peptide work in the pituitary. The Sweedler laboratory has been a fantastic working environment, with great support from students, post-doctoral scholars, and staff. Dr. Lu Bai was a fantastic student mentor while she was at the University of Illinois, and she continued to support the project even after her graduation. Without her help, this project would not be as far along as it is, as she developed the ideas for the discovery funnel approach. Dr. Erik Jansson worked on this project as a post-doctoral scholar, and his help was critical for the discovery of GdYFD as a DAACP in Aplysia. Dr. James Checco has been an enthusiastic post- doctoral scholar, who has helped take this project in new directions that continues to motivate me to understanding the potential of this field. The number of projects he has taken charge of has been nothing short of impressive, including characterizing the peptide specificity of the achatin-like receptor, improving aspects of the discovery funnel that I have suggested in this work, working on new and exciting organisms for DAACP analysis, and continuing to work on the rodent nervous system. Hua-Chia Tai is a graduate student in the lab who is going to take over my project. She has proven to be a capable and enthusiastic student on the project, and her contributions have been very important. I believe that her work on other DAACPs in Aplysia, as well as discovery of the isomerase, will help advance the field iii considerably. I have great confidence in both of these current lab mates to achieve great results for this project. Dr. Elena Romanova has been a critical lab member, helping me in so many technical aspects of this project and furthering my training in mass spectrometry and data analysis techniques. Her thoughtful insights and help with dissecting Aplysia helped this project considerably. Dr. Stanislav Rubakhin has helped in many of the same ways as Dr. Elena Romanova, providing dissections, project insights, and general help on many technical and intellectual levels. I would also like to thank many of my other fellow Sweedler group members for their advice, friendship, and support: Dr. Eric Lanni, Dr. Callie Croushore, Dr. Nobutoshi Ota, Dr. Sarah Dowd, Dr. Ta-Hsuan Ong, Ning Yang, Jordan Aerts, Emily Tillmaand, Amit Patel, Sage Dunham, and Troy Comi. This research also benefited from individuals outside of the lab at the University of Illinois. Dr. Peter Yau and Dr. Brian Imai from the Roy J. Carver Proteomics Center have provided wonderful insight and support in various aspects of the discovery funnel, especially with deuterium-assisted acid hydrolysis. Dr. Lucas Li of the Roy J. carver Metabolomics Center provided experimental help and insight in the use of multiple reaction monitoring in the discovery funnel. From the Gillette laboratory, James Chu and Dr. Jennifer Mitchell provided training and help with suprachiasmatic nucleus and supraoptic nucleus dissections and insights into the rodent nervous system. I would also like to thank Dr. Wilfred Van Der Donk for his support and his efforts in the Chemistry-Biology Interface Graduate Fellowship. For the work on structural characterization on streptomonomicin, I would like to thank the Mitchell laboratory, in particular Jonathan Tietz and Professor Douglas A. Mitchell. I would also like to give a deep thanks to the wonderful collaboration we have with Professor Klaudiusz R. Weiss (Mt. Sinai), Dr. Ferdinand S. Vilim (Mt. Sinai), and Professor Jian Jing (Nanjing University). Dr. Jian Jing, in particular, has been an extremely enthusiastic supporter of my work, and I feel very fortunate to continue to work with him on the discovery funnel manuscript we are developing. I would also like to thank Professor Lingjun Li (University of Wisconsin, Madison), whose laboratory has also studied DAACPs, who has always made it a point to stop by my posters and showing such interest for the project. The support of my family and friends has been nothing short of amazing. I would especially like to thank my lovely parents for their love and support me during my entire academic career! iv TABLE OF CONTENTS Chapter 1 INTRODUCTION AND DISSERTATION OVERVIEW……………………………….. 1 Chapter 2 D-AMINO ACID-CONTAINING PEPTIDES: BIOLOGY, DISCOVERY, AND CHARACTERIZATION TECHNIQUES………………………………………………... 11 Chapter 3 RECENT AND MS-DRIVEN TECHNIQUES FOR THE DETECTION OF D- AMINO ACIDS IN PEPTIDES…………………………………………………………… 38 Chapter 4 CHARACTERIZATION OF G(D)FFD, A D-AMINO ACID-CONTAINING NEUROPEPTIDE THAT FUNCTIONS AS AN EXTRINSIC MODULATOR OF THE APLYSIA FEEDING CIRCUIT…………………………………………………….. 59 Chapter 5 OPTIMIZATION OF THE D-AMINO ACID-CONTAINING NEUROPEPTIDE DISCOVERY FUNNEL…………………………………………………………………… 103 Chapter 6 A D-AMINO ACID-CONTAINING NEUROPEPTIDE DISCOVERY FUNNEL…….. 128 Chapter 7 THE
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