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Developing Carbon Nanotube Optical Sensors for in Vitro and in Vivo Detection of Biomarkers and Drugs

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Developing Carbon Nanotube Optical Sensors for in Vitro and in Vivo Detection of Biomarkers and Drugs DEVELOPING CARBON NANOTUBE OPTICAL SENSORS FOR IN VITRO AND IN VIVO DETECTION OF BIOMARKERS AND DRUGS A Dissertation Presented to the Faculty of the Weill Cornell Graduate School Of Medical Sciences In Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy By Jackson Harvey December 2017 © 2017 Jackson Harvey DEVELOPING CARBON NANOTUBE OPTICAL SENSORS FOR IN VITRO AND IN VIVO DETECTION OF BIOMARKERS AND DRUGS Jackson Harvey, Ph.D. Cornell University 2017 Diseases such as cancer can develop asymptomatically, preventing opportunities for early detection. The drive for “liquid biopsies” that can detect biomarkers in a rapid, point-of-care setting has spurred innovation in nanoparticle- based sensing schemes. One biomarker, cell-free circulating microRNA, has been a major target due to its diagnostic potential and difficulties in detecting it with standard assays. If cancer is detected, chemotherapy is often administered; unfortunately, chemotherapy can greatly decrease patient quality of life due to toxicity. Some side effects can be permanent and cumulative, as in the case of the drug doxorubicin. Sensors that can detect chemotherapy drugs in vivo would be useful as a research tool to better assess drug distribution in the organism and in cells. Clinically, an implantable cumulative sensor for doxorubicin could provide a record of lifetime exposure, minimizing chances of adverse effects. A potential nanomaterial for developing implantable sensors for biomarkers and chemotherapy drugs are single-walled carbon nanotubes. Carbon nanotubes are fluorescent in the near-infrared range, which is highly penetrant to tissue, and report their local environment via changes in their emission energy and intensity. Here, we have developed DNA-functionalized carbon nanotubes for the detection of oligonucleotide biomarkers, alkylating agents, and DNA-intercalating drugs like doxorubicin. We have discovered a method by which optical changes due to hybridization on the nanotube can be greatly enhanced, and applied it to the detection of microRNA in biofluids and in vivo. By adapting our understanding of this enhancement we were able to show directional control of nanotube solvatochromism to alkylating agents, which enabled control of sensing output signal. Mechanistic experiments allowed us to obtain new insight about the interaction of DNA-suspended nanotubes with anionic analytes, including oligonucleotides, to provide better selectivity. In detecting oligonucleotides in serum, we discovered that serum proteins can be denatured to selectively interact with nanotubes after hybridization to enhance sensing, and used this to detect viral RNA. Finally we developed a cumulative, implantable sensor for doxorubicin and other intercalating agents that enabled real- time sensing in live mice. BIOGRAPHICAL SKETCH Jackson Dean Harvey, son of Dean Harvey and Donna Harvey, was born in Fitchburg, MA and raised in Cortland, NY. He graduated from Cortland Jr. Sr. High School and attended SUNY Binghamton for his undergraduate work. While at Binghamton, he was a dual major in Biochemistry and Philosophy, and inducted into the Phi Beta Kappa society. He graduated in December 2009 earning a Bachelor of Science, Magna Cum Laude. Upon graduation he worked as a research technician at the New England Primate Research Center in the laboratory of David T. Evans, under the mentorship of Michael Alpert, studying the role of antibody-dependent cell- mediated cytotoxicity in HIV immunization. While here he attended night classes in statistics and portfolio theory at the Harvard Extension School. In 2011 he became a graduate student at Weill Cornell Graduate School of Medical Sciences. His first rotation was with David Scheinberg, where he worked with Justin Mulvey on a project covalently functionalizing carbon nanotubes for the delivery of alpha-emitting payloads to pre-targeted tumors. Captivated by this nanomaterial, he later joined the laboratory of Daniel Heller in 2012 to continue working with it. In the Heller lab, he was focused on utilizing their optical properties rather than their pharmacokinetic properties. Surrounded by an interdisciplinary team of scientists, Jackson was able to develop several collaborative projects, including a very productive relationship with Jeetain Mittal and Gül Zerze at Lehigh University. He has given oral presentations at meetings of the Electrochemical Society and presented work at the Gordon Research Conference. He is a founding member of the Weill Cornell Biotech Club and has served as the director of finance for three years. He is also a founding member of GRO-Biotech, a coalition of industry-minded graduate students around New York City. iii DEDICATION This work is dedicated to: My parents, Dean and Donna Harvey. My grandparents, Lawrence and Eleanor Harvey. My wife, Soyeon Kate Kim. And the rest of my wonderful family. My mentor and advisor, Daniel Heller. With sincerest thanks to the leadership of the pharmacology program: David Scheinberg, Lorraine Gudas, and Yueming Li. And to my students: Lexi Sun, Xinghuo Li, Hanan Baker, Corrin Pimentel, Deeksha Deep, and Kathryn Tully. Docendo discimus. iv ACKNOWLEDGMENTS This work was completed with the assistance and support of excellent collaborators, including Jeetain Mittal and Gül Zerze at Lehigh University, Andrea Ventura and Joana Vidigal at Memorial Sloan Kettering, and Oliver Zivanovic at Memorial Sloan Kettering. I also thank the Molecular Cytology Core Facility at Memorial Sloan Kettering Cancer Center and Navid Paknejad for atomic force microscopy measurements. This work also relied heavily, in one way or another, on the diverse expertise of the Heller Lab. The excellent discussions and helpful input made for a rewarding experience in completing this work. And finally my mentor and advisor, Daniel Heller, whose support in all facets of my graduate student career made this possible. Your scientific guidance, enthusiasm, and leadership has been essential to successful completion of this work. I must also make a special acknowledgement to the Heller Lab Research Fund and its generous donors, who have been unwavering in their support of the Heller Lab’s mission. Resources from this fund were used well. Other support for this work came from the NIH Director’s New Innovator Award (DP2-HD075698), NIH/NCI Cancer Center Support Grant (P30-CA008748), the Center for Molecular Imaging and Nanotechnology, the Louis V. Gerstner Jr. Young Investigator’s Fund, the Experimental Therapeutics Center, the Alan and Sandra Gerry Metastasis Research Initiative, Cycle for Survival, the Frank A. Howard Scholars Program, the Honorable Tina Brozman Foundation for Ovarian Cancer Research, the v Byrne Research Fund, the Anna Fuller Fund, Mr. William H. Goodwin and Mrs. Alice Goodwin the Commonwealth Foundation for Cancer Research, and the Imaging and Radiation Sciences Program at Memorial Sloan Kettering Cancer Center. Molecular simulation work was performed at the Lehigh University and is supported by the U.S. Department of Energy (DOE) Office of Science, Basic Energy Sciences (BES), and Division of Material Sciences and Engineering, under Award DE-SC0013979. Use of the high-performance computing capabilities of the Extreme Science and Engineering Discovery Environment (XSEDE) was supported by the National Science Foundation (NSF) under grant number TG-MCB-120014. This research also used resources of the National Energy Research Scientific Computing Center, a DOE Office of Science User Facility supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. P.V.J was supported by the National Cancer Institute (NCI) Grant NIH T32 Training Grant 2T32CA062948-21. H.A.B. was supported by a Medical Scientist Training Program grant from the National Institute of General Medical Sciences of the National Institutes of Health under award number T32GM007739 to the Weill Cornell/Rockefeller/Sloan-Kettering Tri- Institutional MD-PhD Program. RMW was supported by the Ovarian Cancer Research Fund Alliance [Anna Schreiber Mentored Investigator Award 370463]. D.R. was supported by an American Cancer Society 2013 Roaring Fork Valley Research Fellowship. vi TABLE OF CONTENTS BIOGRAPHICAL SKETCH ......................................................................................... iii DEDICATION .............................................................................................................. iv ACKNOWLEDGMENTS .............................................................................................. v CHAPTER 1: UNDERSTANDING CARBON NANOTUBE OPTICAL SENSORS FOR APPLICATIONS IN BIOLOGY ........................................................................... 1 1.1 Abstract ................................................................................................................. 1 1.2 Carbon and carbon nanotubes ............................................................................... 2 1.3 The origin and naming of carbon nanotubes......................................................... 4 1.4 Electronic properties of carbon nanotubes: the basics .......................................... 6 1.4.1 From wave functions to density of states ....................................................... 7 1.4.2 Electronic properties: summary ................................................................... 14 1.5 Optical properties of carbon nanotubes .............................................................. 15 1.6 Carbon
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