Translational Therapeutics Research Group
Department of Neurosurgery
Marlene and Stewart Greenebaum NCI Comprehensive Cancer Center
University of Maryland School of Medicine - Baltimore, MD
2023
Carney CP*, Pandey N*, Kapur A, Saadi H, Ong HL, Chen C, Winkles JA, Woodworth GF and Kim AJ. (2023) Impact of targeting moiety type and protein corona formation on the uptake of Fn14-targeted nanoparticles by cancer cells.
ACS Nano 17, 19667-19684. *Co-first authors
Carney CP, Kapur A, Anastasiadis P, Ritzel R, Chen C, Woodworth GF, Winkles JA and Kim AJ. (2023). Fn14-directed DART nanoparticles selectively target neoplastic cells in preclinical models of triple negative breast cancer brain metastasis. Molecular Pharmaceutics 20, 314-330.
2022
Spina R, Mills I, Ahmad F, Chen C, Ames HM, Winkles JA, Woodworth GF and Bar EE. (2022). DHODH inhibition impedes glioma stem cell proliferation, induces DNA damage, and prolongs survival in orthotopic glioblastoma xenografts. Oncogene 41, 5361-5372.
Kim AJ, Winkles JA and Woodworth GF. (2022). Emerging translational approaches for brain cancer therapeutics. Advanced Drug Delivery Reviews 189, 114522.
Pandey N, Anastasiadis P, Carney CP, Kanvinde PP, Woodworth GF, Winkles JA and Kim AJ. (2022). Nanotherapeutic treatment of the invasive glioblastoma tumor microenvironment. Advanced Drug Delivery Reviews 188, 114415.
Schoen S Jr, Kilinc MS, Lee H, Guo Y, Degertekin FL, Woodworth GF and Arvanitis C. (2022). Towards controlled drug delivery in brain tumors with microbubble-enhanced focused ultrasound. Advanced Drug Delivery Reviews 180, 114043.
Kim C, Lim M, Woodworth GF and Arvanitis C. (2022). The roles of thermal and mechanical stress in focused ultrasound-mediated immunomodulation and immunotherapy for central nervous system tumors. Journal of Neuro-Oncology 157, 221.
Njonkou R, Jackson CM, Woodworth GF and Hersh DS (2022). Pediatric glioblastoma: mechanisms of immune evasion and potential therapeutic opportunities. Cancer Immunology, Immunotherapy 71, 1813-1822.
Alomari S, Kedda J, Malla AP, Pacis V, Anastasiadis P, Xu S, McFarland E, Sukhon L, Gallo B, Rincon-Torroella J, Ben-Shalom N, Ames HM, Brem H, Woodworth GF and Tyler B. (2022). Implementation of minimally invasive brain tumor resection in rodents for high viability tissue collection. Journal of Visualized Experiments 183, e64048.
Kim, N, Kwak G, Rodriguez J, Livraghi-Butrico A, Zuo X, Simon V, Han E, Shenoy SK, Pandey N, Mazur M, Birket SE, Kim AJ, Rowe SM, Boucher R, Hanes J, Suk JS. (2022) Inhaled gene therapy of preclinical muco-obstructive lung diseases by nanoparticles capable of breaching the airway mucus barrier. Thorax 77, 812
Pang S, Kapur A, Zhou K, Anastasiadis P, Ballirano N, Kim AJ, Winkles JA, Woodworth GF and Huang HC. (2022). Nanoparticle-assisted, image-guided laser interstitial thermal therapy for cancer treatment. WIREs Nanomedicine & Nanobiotechnology 14, e1826.
2021
Carney CP, Pandey N, Kapur A, Woodworth GF, Winkles JA and Kim AJ. (2021). Harnessing nanomedicine for enhanced immunotherapy for breast cancer brain metastases. Drug Delivery & Translational Research 11, 2344-2370.
Anastasiadis P, Ghandi D, Guo Y, Ahmed A-K, Bentzen SM, Arvantis C and Woodworth GF. (2021). Localized blood-brain barrier opening in infiltrating gliomas with MRI-guided acoustic emissions-controlled focused ultrasound. Proceedings of the National Academy of Sciences 118 (37), e2103280118.
Wadajkar AS, Connolly NP, Carney CP, Kanvinde PP, Winkles JA, Woodworth GF and Kimi AJ. (2021). Surface-modified nanodrug carriers for brain cancer treatment. In: “Neuromethods Book Series-Nanotherapy for Brain Tumor Drug Delivery” (Vivek Agrahari, A. Kim and Vibhuti Agrahari, eds.), Vol. 163: 127-144. Springer Nature Publishing, Basingstoke, United Kingdom.
Anastasiadis P, Winkles JA, Kim AJ and Woodworth GF. (2021). Focused ultrasound-mediated blood-brain barrier disruption for enhanced drug delivery to brain tumors. In: “Neuromethods Book Series-Nanotherapy for Brain Tumor Drug Delivery” (Vivek Agrahari, A. Kim, and Vibhuti Agrahari, eds.), Vol. 163: 205-223. Springer Nature Publishing, Basingstoke, United Kingdom.
Kanvinde PP, Malla A, Connolly NP, Szulzewsky F, Anastasiadis P, Ames HM, Kim AJ, Winkles JA, Holland EC and Woodworth GF. (2021). Leveraging the replication competent avian-like sarcoma virus/tumor virus receptor-A system for modeling human gliomas. Glia 69, 2059-2076.
Connolly NP, Galisteo R, Xu S, Bar EE, Peng S, Tran NL, Ames HM, Kim AJ, Woodworth GF, and Winkles JA. (2021). Elevated fibroblast growth factor-inducible 14 expression transforms proneural-like gliomas into more aggressive and lethal brain cancer. Glia 69, 2199-2214.
2020
Dancy JG*, Wadajkar AS*, Connolly NP, Galisteo R, Ames HM, Peng S, Tran NL, Goloubeva OG, Woodworth GF, Winkles JA, and Kim AJ. (2020) Decreased nonspecific adhesivity, receptor-targeted therapeutic nanoparticles for primary and metastatic breast cancer. Science Advances 6(3), eaax3931.
Spina R, Voss DM, Yang X, Sohn JW, Vinkler R, Schraner J, Sloan A, Welford SM, Avril N, Ames HM, Woodworth GF, and Bar EE. (2020) MCT4 regulates de novo pyrimidine biosynthesis in GBM in a lactate-independent manner. Neuro-Oncology Advances 2(1), vdz062.
Schneider CS, Woodworth GF, Vujaskovic Z, and Mishra MV. (2020). Radiosensitization of high-grade gliomas through induced hyperthermia: Review of clinical experience and the potential role of MR-guided focused ultrasound. Radiotherapy & Oncology 142, 43.
Inglut CT, Gaitan B, Najafali D, Lopez IA, Connolly NP, Orsila S, Perttilä R, Woodworth GF, Chen Y and Huang HC. (2020). Predictors and limitations of the penetration depth of photodynamic effects in the rodent brain. Photochemistry & Photobiology 96, 301.
2019
Wadajkar AS, Dancy JG, Carney CP, Hampton BS, Ames HM, Winkles JW, Woodworth GW, and Kim AJ (2019). Leveraging surface Plasmon resonance to dissect the interfacial properties of nanoparticles: Implications for tissue binding and tumor penetration. Nanomedicine: Nanotechnology, Biology, & Medicine 20, 102024.
Inglut CT, Baglo Y, Liang BJ, Cheema Y, Stabile J, Woodworth GF, and Huang HC (2019). Systematic evaluation of light-activatable biohybrids for anti-glioma photodynamic therapy. Journal of Clinical Medicine 8, 1269
Majumdar S, Wadajkar AS, Aljohani H, Reynolds MA, Kim AJ, and Chellaiah M (2019). Engineering of L-Plastin peptide-loaded biodegradable nanoparticles for sustained delivery and suppression of osteoclast function in vitro. International Journal of Cell Biology May 5, 6943986.
2018
Roberts NB, Alqazzaz A, Hwang JR, Qi X, Keegan AD, Kim AJ, Winkles JA and Woodworth GF. (2018). Oxaliplatin disrupts pathological features of glioma cells and associated macrophages independent of apoptosis induction. Journal of Neuro-Oncology 140: 497-507.
Harder BG, Blomquist MR, Wang J, Kim AJ, Woodworth GF, Winkles JA, Loftus JC and Tran NL. (2018). Developments in blood-brain barrier penetrance and drug repurposing for improved treatment of glioblastoma. Frontiers in Oncology 8, 462.
Hersh DS, Harder BJ, Roos A, Peng S, Heath JE, Legesse T, Kim AJ, Woodworth GF, Tran NL and Winkles JA. (2018). The TNF receptor family member Fn14 is highly expressed in recurrent glioblastoma (GBM) and in GBM patient-derived xenografts with acquired temozolomide resistance. Neuro-Oncology 20:1321-1330.
Roos A, Dhruv HD, Peng S, Inge LJ, Tuncali S, Pineda M, Millard N, Mayo Z, Eschbacher JM, Loftus JC, Winkles JA and Tran NL. (2018). EGFRvIII-Stat5 signaling enhances glioblastoma cell migration and survival. Molecular Cancer Research 16,1185-1195.
Hersh DS, Peng S, Dancy JG, Galisteo R, Eschbacher JM, Castellani RJ, Heath JE, Legesse T, Kim AJ, Woodworth GF, Tran NL, Winkles JA. (2018) Differential expression of the TWEAK receptor Fn14 in IDH1 wild-type and mutant gliomas. Journal of Neuro-Oncology 138(2), 241-250.
Hersh DS, Anastasiadis P, Mohammadabadi A, Nguyen BA, Guo S, Winkles JA, Kim AJ, Gullapalli R, Keller A, Frenkel V and Woodworth GF. (2018) MR-guided transcranial focused ultrasound safely enhances interstitial dispersion of large polymeric nanoparticles in the living brain. PLoS One 13, e0192240.
Connolly NP, Shetty AC, Stokum JA, Hoeschele I, Siegel MB, Miller CR, Kim AJ, Ho C, Davila E, Simard JM, Devine SE, Rossmeisl JH, Holland EC, Winkles JA and Woodworth GF. (2018) Cross-species transcriptional analysis reveals conserved and host-specific neoplastic processes in mammalian glioma. Scientific Reports 8, 1180.
2017
Wadajkar AS, Dancy JG, Roberts NR, Connolly NP, Strickland DK, Winkles JA, Woodworth GF, Kim AJ. (2017) Decreased non-specific adhesivity, receptor targeted (DART) nanoparticles exhibit improved dispersion, cellular uptake, and tumor retention in invasive gliomas. Journal of Controlled Release 267, 144-153.
Connolly NP, Stokum JA, Schneider CS, Ozawa T, Xu S, Galisteo R, Castellani RJ, Kim AJ, Simard M, Winkles JA, Holland EC, Woodworth GF. (2017) Genetically engineered rat gliomas: PDGF-driven tumor initiation and progression in tv-a transgenic rats recreate key features of human brain cancer. PLoS ONE 12, e0174557.
Roos A, Dhruv HD, Mathews IT, Inge LJ, Tuncali S, Hartman LK, Chow D, Millard N, Yin HH, Kloss J, Loftus JC, Winkles JA, Berens ME, Tran NL. (2017) Identification of aurintricarboxylic acid as a selective inhibitor of the TWEAK-Fn14 signaling pathway in glioblastoma cells. Oncotarget 8, 12234-12246.
Wadajkar AS, Dancy JG, Hersh DS, Anastasiadis P, Tran NL, Woodworth GF, Winkles JA, Kim AJ. (2017) Tumor-targeted nanotherapeutics: Overcoming treatment barriers for glioblastoma. WIREs Nanomedicine & Nanobiotechnology, 9:e1439. Highlighted in Advanced Science News website (www.advancedsciencenews.com).
2016
Armstrong CA, Galisteo R, Brown SAN, Winkles JA. (2017) TWEAK activation of the non-canonical NF-kB signaling pathway differentially regulates melanoma and prostate cancer cell invasion. Oncotarget 7, 81474-81492.
Roberts NB*, Wadajkar AS*, Winkles JA, Davila E, Kim AJ, Woodworth GF. (2016) Repurposing platinum-based chemotherapies for multi-modal treatment of glioblastoma. OncoImmunology 5, e1208876.
Dancy JG, Wadajkar AS, Schneider CS, Mauban JRH, Woodworth GF, Winkles JA, Kim AJ. (2016) Non-specific binding and steric hindrance thresholds for penetration of particulate drug carriers within tumor tissue. Journal of Controlled Release 238, 139.
Hersh DS, Nguyen BA, Dancy JG, Adapa AR, Winkles JA, Woodworth GF, Kim AJ, Frenkel V. (2016) Pulsed ultrasound non-destructively expands the extracellular and perivascular spaces of the brain. Brain Research 1646, 543.
Hersh DS, Kim AJ, Winkles JA, Eisenberg HE, Woodworth GF, Frenkel V. (2016) Emerging applications of therapeutic ultrasound in neuro-oncology: Moving beyond tumor ablation. Neurosurgery 79, 643-654.
Perez JG, Tran NL, Rosenblum MG, Schneider CS, Connolly NP, Kim AJ, Woodworth GF, Winkles JA (2016). The TWEAK receptor Fn14 is a potential cell surface portal for targeted delivery of glioblastoma therapeutics. Oncogene 35, 2145.
Hersh DS*, Wadajkar AS*, Roberts NB, Perez JG, Connolly NP, Frenkel V, Winkles JA, Woodworth GF, Kim AJ (2016). Evolving drug delivery strategies to overcome the blood brain barrier. Current Pharmaceutical Design (Invited Review) 22, 1177.
2015
Schneider CS, Perez JG, Cheng E, Zhang C, Panagiotis M, Hanes J, Winkles JA, Woodworth GF*, and Kim AJ* (2015). Minimizing the non-specific binding of nanoparticles to the brain enables active targeting of Fn14-positive glioblastoma cells. Biomaterials 42, 42.
Schneider CS, Bhargav AG, Perez JG, Wadajkar AS, Winkles JA, Woodworth GF*, Kim AJ* (2015). Surface plasmon resonance as a high throughput method to evaluate specific and non-specific binding of nanotherapeutics. Journal of Controlled Release 219, 331.
Cheng E, Whitsett TG, Tran NL, Winkles JA (2015). The TWEAK receptor Fn14 is an Src-inducible protein and a positive regulator of Src-driven cell invasion. Molecular Cancer Research 13, 575.
Mastorakos P, Zhang C, Berry S, Oh Y, Lee S, Eberhart CG, Woodworth GF, Suk JS, Hanes J (2015). Highly PEGylated DNA nanoparticles provide uniform and widespread gene transfer in the brain. Advanced Healthcare Materials 4, 1023.
2014
Kim AJ, Woodworth GF, Boylan NJ, Suk JS, Hanes J (2014). Highly compacted pH-responsive DNA nanoparticles mediate transgene silencing in experimental glioma. Journal of Materials Chemistry B 2, 8165.
Dhruv, HD, Whitsett, TG, Jameson, NM, Patel, F, Winkles, JA, Berens, ME, Tran, NL (2014). Tumor necrosis factor-like weak inducer of apoptosis (TWEAK) promotes glioblastoma cell chemotaxis via Lyn activation. Carcinogenesis 35, 218.
Nance E, Timbie K, Miller GW, Song J, Louttit C, Klibanov AL, Shih TY, Swaminathan G, Tamargo RJ,Woodworth GF, Hanes J, Price RJ (2014). Non-invasive delivery of stealth, brain-penetrating nanoparticles across the blood-brain barrier using MRI-guided focused ultrasound. Journal of Controlled Release 189, 123.
Zhou H, Mohamedali KA, Gonzalez-Angulo AM, Cao Y, Migliorini M, Cheung LH, LoBello J, Lei X, Qi Y, Hittelman WN, Winkles JA, Tran NL, Rosenblum MG (2014). Development of human serine protease-based therapeutics targeting Fn14 and identification of Fn14 as a new target overexpressed in TNBC. Molecular Cancer Therapeutics 13, 2688.
Pan-in P, Wanichwecharungruang S, Hanes J, Kim AJ (2014). Cellular trafficking and anticancer activity of Garcinia mangostana extract-encapsulated polymeric nanoparticles. International Journal of Nanomedicine 9, 3677.
Gurunathan S, Winkles JA, Ghosh S, Hayden MS (2014). Regulation of fibroblast growth factor-inducible 14 (Fn14) expression levels via ligand-independent lysosomal degradation. Journal of Biological Chemistry 289, 12976.
Schuster BS, Kim AJ, Kays JC, Kanzawa MM, Suk JS, Hanes J (2014). The cystic fibrosis sputum barrier to adeno-associated virus gene therapy. Molecular Therapy 22, 1484.
Pease M, Oglesby EN, Cone-Kimball E, Jefferys JL, Steinhart MR, Kim AJ, Hanes J, Quigley HS (2014). Scleral permeability varies by mouse strain and Is decreased by chronic experimental glaucoma. Investigative Ophthalmology & Visual Science. 55, 2564.
Suk JS, Kim AJ, Trehan K, Schneider CS, Cebotaru L, Woodward OM, Boylan NJ, Boyle MP, Lai SK, Guggino WB, Hanes J (2014). Lung gene therapy with highly compacted DNA nanoparticles that overcome the mucus barrier. Journal of Controlled Release. 178, 8.
Woodworth GF, Dunn GP, Nance EA, Hanes J, Brem H (2014). Emerging insights into barriers to effective brain tumor therapeutics. Frontiers in Oncology. 4, 126.
Other Relevant Articles
Cheng, E, Armstrong, CL, Galisteo, R, and Winkles, JA (2013). TWEAK/Fn14 axis-targeted therapeutics: Moving basic science discoveries to the clinic. Frontiers in Immunology. 4, 473.
Zhou H, Hittelman WN, Yagita H, Cheung LH, Martin SS, Winkles JA, Rosenblum MG (2013). Antitumor activity of a humanized, bivalent immunotoxin targeting fn14-positive solid tumors. Cancer Research. 73, 4439.
Zhou, H, Ekmekcioglu, S, Marks, JW, Mohamedali, KA, Asrani, K, Phillips, KK, Brown, SAN, Cheng, E, Weiss, MB, Hittelman, WN, Tran, NL, Yagita, H, Winkles, JA, and Rosenblum, MG (2013). The TWEAK receptor Fn14 is a therapeutic target in melanoma: Immunotoxins targeting Fn14 receptor for malignant melanoma treatment. Journal of Investigative Dermatology. 133, 1052.
Kim AJ, Boylan NJ, Suk JS, Hwangbo M, Yu T, Schuster BS, Cebotaru L, Lesniak, WG, Oh JS, Adstamongkonkul P, Choi AY, Kannan RM, Hanes J (2013). Use of single-site functional PEG-dendrons to prepare gene vectors that penetrate human mucus barriers. Angewandte Chemie Int Ed. 52, 3985.
Schuster BS, Suk JS, Woodworth GF, Hanes J (2013). Nanoparticle diffusion in respiratory mucus from humans without lung disease. Biomaterials. 34, 3439.
Brown, SAN, Cheng, E, Williams, MS, and Winkles, JA (2013). TWEAK-independent Fn14 self-association and NF-kB activation is mediated by the C-terminal region of the Fn14 cytoplasmic domain. PloS ONE. 8, e65248.
Kim AJ and Hanes J (2012). The emergence of multiple particle tracking in intracellular trafficking of nanomedicines. Biophysical Reviews. 4, 83.
Nance EA, Woodworth GF, Sailor KA, Shih TY, Xu Q, Swaminathan G, Xiang D, Eberhart C, HanesJ (2012). A dense poly(ethylene glycol) coating improves penetration of large polymeric nanoparticles within brain tissue. Science Translational Medicine. 4, 149ra119.
Fortin, SP, Ennis, MJ, Schumacher, CA, Zylstra-Diegel, CR, Williams, BO, Ross, JTD., Winkles, JA, Loftus, JC, Symons, MH, and Tran, NL (2012). Cdc42 and the guanine nucleotide exchange factors Ect2 and Trio mediate Fn14-induced migration and invasion of glioblastoma cells. Molecular Cancer Research. 10, 958.
Burke CW, Suk JS, Kim AJ, Hsiang YJ, Klibanov AL, Hanes J, Price RJ (2012). Markedly enhanced skeletal muscle transfection achieved by the delivery of non-viral gene nanocarriers with small microbubbles and pulsed 1 MHz ultrasound. Journal of Controlled Release. 162, 414.
Boylan NJ, Kim AJ, Suk JS, Adstamongkonkul P, Simons BW, Lai SK, Cooper MJ, Hanes J (2012). Enhancement of airway gene transfer by DNA nanoparticles using a pH-responsive block copolymer of polyethylene glycol and poly-L-lysine. Biomaterials. 33, 2361.
Kim AJ, Boylan NJ, Suk JS, Lai SK, Hanes J (2012). Non-degradative intracellular trafficking of highly compacted polymeric DNA nanoparticles. Journal of Controlled Release. 158, 102.
Zhou, H, Marks, JW, Hittelman, WN, Yagita, H, Rosenblum, MG, and Winkles, JA (2011). Development and characterization of a potent immunotoxin targeting the Fn14 receptor on solid tumor cells. Molecular Cancer Therapeutics. 10, 1276.
Percec V, Wilson DA, Leowanawat P, Wilson CJ, Hughes AD, Kaucher MS, Hammer DA, Levine DH, Kim AJ, Bates FS, Davis KP, Lodge TP, Klein ML, DeVane RH, Aqad E, Rosen BM, Argintaru AO, Sienkowska MJ, Rissanen K, Nummelin S, Ropponen J (2010). Self-Assembly of janus-dendrimers into monodisperse dendrosomes and other complex architectures. Science. 328, 1009.
Kim AJ, Kaucher MS, Davis KP, Peterca M, Iman MR, Christian NA, Levine DH, Bates FS, Percec V, Hammer DA (2009). Proton transport through dendritic helical pore incorporated polymersomes. Advanced Functional Materials. 19, 2930.
Fortin, SP, Ennis, MJ, Savitch, BA, Carpentieri, D, McDonough, WS, Winkles, JA, Loftus, JC, Kingsley, C, Hostetter, G, and Tran, NL (2009). Tumor necrosis factor-like weak inducer of apoptosis (TWEAK) stimulation of glioma cell survival is dependent on Akt2 function. Molecular Cancer Research. 7, 1871.
Winkles JA (2008). The TWEAK-Fn14 cytokine-receptor axis: discovery, biology and therapeutic targeting. Nature Reviews Drug Discovery. 7, 411.
Moon JH, Kim AJ, Crocker JC, Yang S (2007). High-throughput synthesis of anisotropic colloids via holographic lithography. Advanced Materials. 19, 2508.
Tran, NL, McDonough, WS, Savitch, BA, Fortin, SP, Winkles, JA, Symons, M, Nakada, M, Cunliffe, HE, Hostetter, G, Hoelzinger, DB, Rennert, JL, Michaelson, JS, Burkly, LC, Lipinski, CA, Loftus, JC, Mariani, L, and Berens, ME (2006). Increased Fn14 expression levels promote glioma cell invasion via Rac1 and NF-kB and correlate with poor patient outcome. Cancer Research. 66, 9535.
Kim AJ, Manoharan VN, Crocker JC (2005). Swelling-based method for preparing stable, functionalized polymer colloids. Journal of the American Chemical Society. 127, 1592.
Tran, NL, McDonough, WS, Savitch, BA, Sawyer, TF, Winkles, JA, and Berens, ME (2005). The tumor necrosis factor-like weak inducer of apoptosis (TWEAK)-fibroblast growth factor-inducible 14 (Fn14) signaling system regulates glioma cell survival via NF-kB pathway activation and Bcl-xL/Bcl-w expression. Journal of Biological Chemistry. 280, 3483.
Tran, NL, McDonough, WS, Donohue, PJ, Winkles, JA, Berens, TJ, Ross, KR, Hoelzinger, DB, Beaudry, C, Coons, SW and Berens, ME (2003). The human Fn14 receptor gene is up-regulated in migrating glioma cells in vitro and overexpressed in advanced glial tumors. American Journal of Pathology. 162, 1313.