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Virus-Based Nanoparticles for Cancer Drug Delivery VIRUS-BASED NANOPARTICLES FOR CANCER DRUG DELIVERY By ANNA ELIZABETH CZAPAR Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy Dissertation Advisor: Dr. Nicole F. Steinmetz Department of Pathology CASE WESTERN RESERVE UNIVERSITY August 2017 CASE WESTERN RESERVE UNIVERSITY SCHOOL OF GRADUATE STUDIES We hereby approve the thesis/dissertation of Anna Elizabeth Czapar candidate for the Doctor of Philosophy degree*. (signed) George Dubyak, PhD (chair of the committee) Analisa DiFeo, PhD James Anderson, MD, PhD Clive Hamlin, PhD Nicole F. Steinmetz, PhD (date) April 21, 2017 *We also certify that written approval has been obtained for any proprietary material contained therein. i Table of Contents List of Tables…..………………………………………………….………………...…...vi List of Figures…………………………………………………......................................vii Acknowledgements………………………………………………………………............x List of Abbreviations…………………………………………………………………...xii Abstract……………………………………………………………………....................xvi Chapter 1:Introduction………………………………………….....................................1 1.1 Introduction…………………………………………..........................................................1 1.2 Drug delivery………………………………………….......................................................4 1.3 Gene therapy…………………………………………........................................................8 1.4 Immunotherapies and vaccines………………………………………….......................10 1.5 Conclusions…………………………………………........................................................14 1.6 Work cited in this chapter…………………………………………................................15 Chapter 2: Aims of thesis work………………………………………….......................21 Chapter 3: Protocols for Evaluation of Biological Fates……………………………..23 3.1 Introduction…………………………………………........................................................23 3.2 Methods presented in this chapter…………………………………………..................26 3.3 Nanomaterial target and non-target cell interactions……………………………...26 3.4 Assays to evaluate nanoparticle-blood compatibility through study of coagulation and hemolysis…………………………………………………………….....32 3.5 Pharmacokinetics and clearance………………………..………………...................34 3.6 Antibody titers, antibdoy recognition, and complement activation………….......44 iii 3.7 Summary and future prospects…………………………………………....................49 3.8 Works cited in this chapter…………………………………………..........................50 Chapter 4: Tobacco Mosaic Virus Delivery of Phenanthriplatin for Cancer Therapy………………………………………………………………………………….55 4.1 Introduction…………………………………………........................................................55 4.2 Materials and methods…………………………………………......................................56 4.3 Results and discussion………………………………………………...……...................60 4.4 Conclusions…………………………………………........................................................74 4.5 Works cited in this chapter…………………………………………...............................74 Chapter 5: Tobacco Mosaic Virus as a Nanocarrier for Ovarian Cancer Treatment………………………………………………………………………………..77 5.1 Introduction…………………………………………........................................................78 5.2 Materials and methods…………………………………………......................................80 5.3 Results and discussion…………………………………………......................................84 5.4 Conclusions and future directions…………………………………………...................98 5.5 Works cited in this chapter…………………………………………...............................99 Chapter 6: POxylation as an Alternative Stealth Coating for Biomedical Applications....................................................................................................................102 6.1 Introduction…………………………………………………………...……...................103 6.2 Materials and methods………………………………………….........…………..........107 6.3 Results and discussion…………………………………………...................………….112 6.4 Conclusions………………………………………….....…………………….................122 6.5 Works cited in this chapter…………………………………………...............……......123 iv Chapter 7: Slow-release Formulation of Cowpea Mosaic Virus In Situ Vaccine for Treatment of Ovarian Cancer………………………………………….......................128 7.1 Introduction…………………………………………..................……………………....128 7.2 Materials and methods…………………………………………............………….......130 7.3 Results and discussion…………………………………………...................………….133 7.4 Conclusions…………………………………………..................……………………....143 7.5 Works cited in this chapter…………………………………………...................……..143 Chapter 8: Conclusions and Future Directions………………………….…..............147 8.1 Scope of this work………………………………………………………......................147 8.2 Tobacco mosaic virus: a plant virus for improved platinum chemotherapy……...149 8.3 Viral-hybrid materials for delayed release of cowpea mosaic virus (CPMV) in the intraperitoneal space……………………………………………………………………….156 8.4 Future directions………………………………………………..…………...................159 8.5 Works cited in this chapter……………………………..…………………...................162 Appendix I…………………………………..................................................................167 Appendix II…………………………………….............................................................178 Appendix III……………………………………...........................................................191 Appendix IV……….......................................................................................................206 Bibliography…………………………………………...................................................219 v List of Tables Table 6.1. Analytical data of azide-functionalized PMeOx. ............................................ 107 vi List of Figures Figure 1.1. Plant viruses and bacteriophages in medicine and biotechnology.. ................. 3 Figure 1.2. Schematic for loading of phenanthriplatin into TMV. ...................................... 6 Figure 1.3. Loading of RCNMV with abamectin for nematode control.. ........................... 8 Figure 1.4. CPMV as an in situ vaccine ............................................................................ 14 Figure 3.1. TMV structure and functionalization .............................................................. 24 Figure 3.2. A-PVX-PEG–cell interactions measured by flow cytometry ......................... 28 Figure 3.3. Blood biocompatibility assays ........................................................................ 34 Figure 3.4. Plasma clearance of A647-labeled, PEGylated PVX and CPMV ................... 37 Figure 3.5. Biodistribution of A647-labeled, PEGylated PVX ......................................... 40 Figure 3.6. Anti-PVX IgG titers and reactivity ................................................................. 47 Figure 4.1. Loading scheme and structures of phenanthriplatin and PhenPt-TMV. ......... 61 Figure 4.2. Synthesis and characterization of PhenPt-TMV.. ........................................... 63 Figure 4.3. Cellular uptake and efficacy of PhenPt-TMV in vitro. ................................... 65 Figure 4.4. Cellular trafficking of TMV within MDA-MB231 cells. ................................ 66 Figure 4.5. Treatment of MDA-MB231 xenografts in an athymic mouse model. ............ 68 Figure 4.6. Histology of MDA-MB231 tumor sections. ................................................... 69 Figure 4.7. Biodistribution of PhenPt-TMV in MDA-MB231 tumor bearing animals.. ... 71 vii Figure 4.8. Toxicity of PhenPt-TMV in treated animals.. ................................................. 72 Figure 5.1. Synthesis and characterization of TMV-Pt ..................................................... 86 Figure 5.2. Cellular interactions and cytotoxicity in vitro.. ............................................... 89 Figure 5.3. Efficacy and survival in high dose treatment study.. ....................................... 91 Figure 5.4. Dose escalation survival and weight ............................................................... 92 Figure 5.5. Low dose efficacy study of TMV-PhenPt and TMV-CisPt. ........................... 95 Figure 5.6. Biodistribution of TMV-PhenPt administered IP in ovarian cancer ............... 98 Figure 6.1. Schematic illustrating polymer conjugation. ................................................. 114 Figure 6.2. Characterization of surface modified TMV particles.. .................................. 116 Figure 6.3. Antibody recognition of native and stealth coated TMV.. ............................. 118 Figure 6.4. RAW 264.7 macrophage cell line uptake of stealth coated TMV as determined by flow cytometry. ................................................................................................... 120 Figure 6.5. RAW 264.7 macrophage cell line viability following 24 h of treatment with native and polymer-coated TMV particles. ............................................................. 121 Figure 6.6. Pharmacokinetics of coated TMV following intravenous injection ............. 122 Figure 7.1. DLS measurements for the assembly and disassembly of CPMV and PAMAM-G4 dendrimer ........................................................................................... 137 Figure 7.2. Topographical tapping-mode AFM images of CPMV-G4 ............................ 137 Figure 7.3. Growth of ovarian cancer cells in the intraperitoneal space ........................ 137 viii Figure 7.4. Characterization of dye-labeled CPMV and CPMV-G4 assemblies ............ 140 Figure 7.5. To Biodistribution of CPMV and CPMV-G4 in the intraperitoneal space…142 ix Acknowledgements First, I would like to thank my advisor, Dr. Nicole Steinmetz,
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