Publications + Abstracts

TR&D 1: Molecular Imaging Reagents for Prostate Cancer Theranostics


Noriko Mori, Jiefu Jin, Balaji,Krishnamachary, Yelena Mironchik, James Barnett and Zaver M. Bhujwalla.  FAP-α overexpression increases cancer cell migration. AACR Virtual Annual Meeting, June 22-24, 2020.


Jiefu Jin, James Barnett, Balaji Krishnamachary, Yelena Mironchik, Hisataka Kobayashi, Zaver M. Bhujwalla.  Phototheranostics of cancer associated fibroblasts by targeting fibroblast activation protein-α.  AACR Virtual Annual Meeting, June 22-24, 2020.


Jesus Pacheco-Torres, Marie-France Penet, Flonne Wildes, Yelena Mironchik, Balaji Krishnamachary, Zaver Bhujwalla.  The immune checkpoint PF-L1 alters choline kinase expression and metabolism in triple negative breast cancer cells.  AACR Virtual Annual Meeting, June 22-24, 2020.


Jesus Pacheco-Torres, Tariq Shah, W. Nathanel Brennen, Flonne Wildes, Zaver M. Bhujwalla.  Hypoxia alters normal fibroblast metabolism towards a cancer associated fibroblast phenotype.  ISMRM Virtual Annual Meeting, August 8-14, 2020.


Jesus Pacheco-Torres, Marie-France Penet, Flonne Wildes, Yelena Mironchik, Balaji Krishnamachary, and Zaver M Bhujwalla.  The immune checkpoint PD-L1 alters choline kinase expression and metabolism in triple negative breast cancer cells.  ISMRM Virtual Annual Meeting, August 8-14, 2020.


Katie M Parkins, Samata M Kakkad, Balaji Krishnamachary, Desmond Jacob, KowsalyaDevi Pavuluri, Farzad Sedaghat, Sridhar Nimmagadda, Michael T McMahon, Zaver M Bhujwalla.  The Role of Tumor Hypoxia and pHe in PD-L1 Expression.  WMIC Virtual Annual Meeting, October 7-9, 2020.

Zhihang Chen, Balaji Krishnamachary, Marie-France Penet, Sangeeta Ray, Martin Pomper, Zaver M. Bhujwalla. PSMA-targeted biodegradable dextran to delivery PD-L1 siRNA in prostate cancer. 2017 WMIC, Sept. 13-16, 2017, Philadelphia, USA.


Pacheco-Torres J, Penet MF, Mironchik Y, Krishnamachary B, Bhujwalla ZM.  The PD-L1 metabolic interactome intersects with choline metabolism and inflammation.  Cancer Metab. 2021 Feb 19;9(1):10.  doi: 10.1186/s40170-021-00245-w.  PMID: 33608051  PMCID: PMC7893974  DOI: 10.1186/s40170-021-00245-w


Pacheco-Torres J, Penet MF, Mironchik Y, Krishnamachary B, Chen Z, Bhujwalla ZM.  PD-L1 siRNA theranostics with a dextran nanoparticle highlights the importance of nanoparticle delivery for effective tumor PD-L1 downregulation.  Frontiers in Oncology (in press), 2021.


Jin J, Barnett JD, Krishnamachary B, Mironchik Y, Luo C, Kobayashi H, Bhujwalla ZM.  Targeting cancer associated fibroblasts by photoimmunotheranostics of fibroblast activation protein-α.  Mol. Cancer Therapeutics (submitted), 2021.


Krishnamachary B, Mironchik Y, Jacob D, Goggins E, Kakkad S, Ofori F, Dore-Savard L, Bharti SK, Wildes F, Penet MF, Black ME, Bhujwalla ZM. Hypoxia theranostics of a human prostate cancer xenograft and the resulting effects on the tumor microenvironment.  Neoplasia. 2020 Dec;22(12):679-688. doi: 10.1016/j.neo.2020.10.001. Epub 2020 Oct 23.


Jin J, Bhujwalla ZM. Biomimetic Nanoparticles Camouflaged in Cancer Cell Membranes and Their Applications in Cancer Theranostics.  Front Oncol. 2020 Jan 21;9:1560.


Chen Z, Krishnamachary B, Pachecho-Torres J, Penet MF, Bhujwalla ZM.  Theranostic small interfering RNA nanoparticles in cancer precision nanomedicine.  Wiley Interdiscip Rev Nanomed Nanobiotechnol. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2020 Mar;12(2):e1595.  PMID: 31642207 PMCID: PMC7360334

Hapuarachchige S, Si G, Huang C, Lesniak W, Mease R, Artemov D. Dual-modality PET-SPECT image-guided pretargeting delivery in HER2(+) breast cancer models. Bioconjugate Chemistry. In review. 2021.

Huang CT, Guo X, Bařinka C, Lupold SE, Pomper MG, Gabrielson K, Raman V, Artemov D, Hapuarachchige S. Development of 5D3-DM1: A novel anti-prostate-specific membrane antigen antibody-drug conjugate for PSMA-positive prostate cancer therapy. Mol Pharm. 2020 Sep 8;17(9):3392-3402. doi: 10.1021/acs.molpharmaceut.0c00457. Epub 2020 Aug 17. PMID: 32803984

Hapuarachchige S, Huang CT, Donnelly MC, Bařinka C, Lupold SE, Pomper MG, Artemov D. Cellular delivery of bioorthogonal pretargeting therapeutics in PSMA-positive prostate cancer. Mol Pharm. 2020 Jan 6;17(1):98-108. doi: 10.1021/acs.molpharmaceut.9b00788. Epub 2019 Dec 16. PMID: 31840521

Chen Z, Krishnamachary B, Penet MF, Bhujwalla ZM. Acid-degradable Dextran as an Image Guided siRNA Carrier for COX-2 Downregulation. Theranostics. 2018 Jan 1;8(1):1-12. doi: 10.7150/thno.21052. eCollection 2018.

TR&D 2: Optimizing and Humanizing a Reporter Gene for Imaging in Deep Tissue


Meier S, Gilad AA, Brandon JA, Qian C, Gao E, Abisambra JE, Vandsburger M. Non-invasive detection of adeno-associated viral gene tgransfer using a genetically encoded CEST-MRI reporter gene in the murine heart. Sci Rep. 2018 Mar 15;8(1):4638. doi: 10.1038/s41598-018-22993-4.

A. Bar-Shir, L. Alon, M. Korrer, H.S. Lim, N.N. Yadav, Y. Kato, A.P. Pathak, J.W.M. Bulte, A.A. Gilad. Quantification and tracking of genetically engineered dendritic cells for studying immunotherapy. Magn. Reson. Med. 79, 1010-1019 (2018).


M.T. McMahon, J.W.M. Bulte. Two decades of dendrimers as versatile MRI agents: A tale with and without metals. WIREs Nanomed. Nanobiotech. 10, 1-17 (2018).


L. Alon, D.L. Kraitchman, M. Schär, A. Cortez, N.N. Yadav, J. Cook, P. Johnston, R. Krimins, M.T. McMahon, P.C.M. van Zijl, S. Nimmagadda, M.G. Pomper, J.W.M. Bulte, A.A. Gilad. Molecular imaging of CXCL12 promoter-driven HSV1-TK reporter gene expression.  Biotech. Bioproc. Eng., 23, 208-217 (2018).


J.W.M. Bulte, H.E Daldrup-Link. Clinical tracking of cell transfer and cell transplantation: Trials and tribulations. Radiology 289, 604-615 (2018).


W. Zhu, C. Chu, S. Kuddannaya, Y. Yuan, P. Walczak, A. Singh, X. Song, J.W.M. Bulte. In vivo imaging of composite hydrogel scaffold degradation using CEST MRI and two-color NIR imaging. Adv. Funct. Mater. 29, 1903753 (2019).


Y. Yuan, J. Zhang, X. Qi, S. Li, G. Liu, S. Siddhanta, I. Barman, X. Song, M.T. McMahon, J.W.M. Bulte. Furin-mediated intracellular self-assembly of olsalazine nanoparticles for enhanced MR imaging and tumor therapy. Nat. Mater. 18, 1376-1383 (2019).


Y. Yuan, Z. Wei, C. Chu, J. Zhang, X. Song, P. Walczak, J.W.M. Bulte. Developing zinc-specific iCEST MRI as imaging biomarker for prostate cancer. Angew. Chem. Int. Ed., 58, 15512-15517 (2019).


A.M. Thomas, J. Xu, P.A. Calabresi, P.C.M. van Zijl, J.W.M. Bulte. Monitoring diffuse injury during disease progression in experimental autoimmune encephalomyelitis with on resonance variable delay multiple pulse (onVDMP) CEST MRI. NeuroImage Jan 1;204:116245 (2020).


A.M. Thomas, S. Li, C. Chu, I. Shats, J. Xu, P.A. Calabresi, P.C.M. van Zijl, P. Walczak, J.W.M. Bulte. Evaluation of cell transplant-mediated attenuation of diffuse injury in experimental autoimmune encephalomyelitis using onVDMP CEST MRI. Exp. Neurol., 10.1016/j.expneurol.2020.113316 (2020).


J.W.M. Bulte. Chimeric antigen receptor T cell immunotherapy induces transient tumor hyperoxia instead of hypoxia. Radiology: Imaging Cancer, 3:e200135 (2021).


K. Saha, E.J. Sontheimer, P.J. Brooks, M.R. Dwinell, C.A. Gersbach, D.R. Liu, S.A. Murray, S.Q. Tsai, R.C. Wilson, D.G. Anderson, A.Asokan, J. Banfield, K.S. Bankiewicz, G. Bao, J.W.M. Bulte, N. Bursac, J. Campbell, D.F. Carlson, E. Chaikoff, Z-Y. Chen, R. H. Cheng, K.J. Clark, D.T. Curiel, J. Dahlman, B.E. Deverman, M.E. Dickinson, J.A. Doudna, S.C. Ekker, M. Emborg, G.Feng, B.S. Freedman, D.M. Gamm, G. Gao, I.C. Ghiran, P.M. Glazer, S. Gong, J.D. Heaney, J.D. Hennebold, J.T. Hinson, A. Khvorova, S. Kiani, W.R. Lagor, K.S. Lam, K.W. Leong, J.E. Levine, J.A. Lewis, C.M. Lutz, D.H. Ly, S. Maragh, P.B. McCray, T.C. McDevitt, O. Mirochnitchenko, R. Morizane, N. Murthy, R.S. Prather, J.A. Ronald, S. Roy, S. Roy, V. Sabbisetty, W.M. Saltzman, P.J. Santangelo, D.J. Segal, M. Shimoyama, M.C. Skala, A.F. Tarantal, J.C. Tilton, G.A. Truskey, M. Vandsburger, J.K. Watts, K.D. Wells, S.A. Wolfe, Q. Xu, W. Xue, G. Yi, J. Zhou and the SCGE Consortium. The NIH somatic cell genome editing consortium. Nature, in press.


Y. Yuan, P. Raj, J. Zhang, S. Siddhanta, I. Barman, J.W.M. Bulte. Furin-mediated self-assembly of olsalazine nanoparticles for targeted Raman imaging of tumors. Angew. Chem. Int. Ed., doi: 10.1002/anie.202014839 (2021). Front cover


J.W.M. Bulte, A. Shakeri-Zadeh. Sightseeing cells: Insights obtained with MRI cell tracking. Cell and Gene Therapy Insights, in press.


Y. Yuan, C. Wang, S. Kuddannaya, D. Arifin, J. Zhang, Z. Han, P. Walczak, G. Liu, J.W.M. Bulte. High-mannose expression enables in vivo tracking of unlabeled mesenchymal stem cells. Nat. Biomed. Eng., in revision.

TR&D 3: Imaging Agents for Inflammatory Components of Malignancy


R. Naik, V. Misheneva, I. Minn, T. Melnikova, W. Mathews, R.F. Dannals, M.G. Pomper, A. Savonenko, M. Pletnikov, A.G. Horti. PET tracer for imaging of macrophage colony stimulating factor receptor (CSF1R). Society of Nuclear Medicine and Molecular Imaging, Philadelphia, PA 2018.

Dhiraj Kumar, Ala Lisok, Samit Chatterjee, Bryan Wharram, Ronnie Mease, Martin Pomper and Sridhar Nimmagadda. A highly specific hydrophilic peptide for PET imaging of PD-L1 expression in tumors. Society of Nuclear Medicine and Molecular Imaging, Philadelphia, PA 2018.

Katherine Zukotynski, Steven P. Rowe, John Valliant, Chun K. Kim, Martin G. Pomper and Steve Y. Cho. 18F-DCFPyL PET/CT in Castration-Resistant Prostate Cancer (CRPC): Imaging results prior to and following abiraterone or enzalutemide therapy. Society of Nuclear Medicine and Molecular Imaging, Philadelphia, PA 2018.


Nimmagadda S. Quantifying PD-L1 expression to monitor immune checkpoint therapy: Opportunities and challenges. Cancers (Basel). 2020 Oct 29;12(11):3173. doi: 10.3390/cancers12113173. PMID: 33137949

Nimmagadda S, Penet MF. Ovarian cancer targeted theranostics. Front Oncol. 2020 Jan 21;9:1537. doi: 10.3389/fonc.2019.01537. PMID: 32039018

Lesniak WG, Mease RC, Chatterjee S, Kumar D, Lisok A, Wharram B, Kalagadda VR, Emens LA, Pomper MG, Nimmagadda S. Development of [18F]FPy-WL12 as a PD-L1 specific PET imaging peptide. Mol Imaging. 2019 Jan-Dec;18:1536012119852189. doi: 10.1177/1536012119852189. PMID: 31187691

Horti AG, Naik R, Foss CA, Minn I, Misheneva V, Du Y, Wang Y, Mathews WB, Wu Y, Hall A, LaCourse C, Ahn HH, Nam H, Lesniak WG, Valentine H, Pletnikova O, Troncoso JC, Smith MD, Calabresi PA, Savonenko A, Dannals RF, Pletnikov MV, Pomper MG. PET imaging of microglia by targeting macrophage colony-stimulating factor 1 receptor (CSF1R). Proc Natl Acad Sci U S A. 2019 Jan 29;116(5):1686-169, PMID: 30635412. PMCID: PMC6358677

De Silva RA, Kumar D, Lisok A, Chatterjee S, Wharram B, Venkateswara Rao K, Mease R, Dannals RF, Pomper MG, Nimmagadda S. Peptide-based 68Ga-PET radiotracer for imaging PD-L1 expression in cancer. Mol Pharm. 2018 Sep 4;15(9):3946-3952. doi: 10.1021/acs.molpharmaceut.8b00399. 

TR&D 4: CEST MRI Agents for Receptor Imaging


S. Ray Banerjee, X. Song, X. Yang, I. Minn, A. Lisok, Y. Chen, A. Bui, S. Chatterjee, J. Chen, P.C.M. van Zijl, M.T. McMahon, M. G. Pomper, “Salicylic Acid-Based Polymeric Contrast Agents for Targeted Molecular Magnetic Resonance Imaging of Prostate Cancer”, J Nucl Med May 1, 2017 vol. 58 no. supplement 1 732

Heo HY, Jiang S, van Zijl PCM, Zhou J. A Novel MR Fingerprinting (MRF) Approach for fast quantitative Chemical Exchange Saturation Transfer MRI analysis by Subgrouping Proton Exchange Models (CESTSPEM). Intl. Soc. Mag. Reson. Med. 2018. Power Pitch.


Liu G, Ray Banerjee S, Yang X, Yadav N, Lisok A, Jablonska A, Xu J, Li Y, Pomper MG, van Zijl P. A dextran-based probe for the targeted magnetic resonance imaging of tumours expressing prostate-specific membrane antigen. Nat Biomed Eng. 2017;1:977-982. doi: 10.1038/s41551-017-0168-8. Epub 2017 Dec 12. PMID: 29456877; PMCID: PMC5810963.

Han Z, Zhang S, Fujiwara K, Zhang J, Li Y, Liu J, van Zijl PCM, Lu ZR, Zheng L, Liu G. An extradomain-B fibronectin-targeted dextran-based CEST MRI probe for detecting pancreatic cancer. Bioconjug Chem. 2019 Apr 2. doi:10.1021/acs.bioconjchem.9b00161. [Epub ahead of print] PubMed PMID: 30938983.

Xu X, Xu J, Knutsson L, Liu J, Liu H, Li Y, Lal B, Laterra J, Artemov D, Liu G, van Zijl PCM, Chan KWY. The effect of the mTOR inhibitor rapamycin on glucoCEST signal in a preclinical model of glioblastoma. Magn Reson Med. 2019 Jun;81(6):3798-3807. doi: 10.1002/mrm.27683. Epub 2019 Feb 22. PubMed PMID: 30793789.

Zhou J, Heo HY, Knutsson L, van Zijl PCM, Jiang S. APT-weighted MRI: Techniques, current neuro applications, and challenging issues. J Magn Reason Imaging. 2019 Jan 20. doi: 10.1002/jmri.26645. [Epub ahead of print] Review. PubMed PMID: 30663162.

Heo HY, Han Z, Jiang S, Schär M, van Zijl PCM, Zhou J. Quantifying amide proton exchange rate and concentration in chemical exchange saturation transfer imaging of the human brain. Neuroimage. 2019 Apr 1;189:202-213. doi: 10.1016/j.neuroimage.2019.01.034. Epub 2019 Jan 14. PubMed PMID: 30654175; PubMed Central PMCID: PMC6422734.

Knutsson L, Seidemo A, Rydhög Scherman A, Markenroth Bloch K, Kalyani RR, Andersen M, Sundgren PC, Wirestam R, Helms G, van Zijl PCM, Xu X. Arterial Input Functions and Tissue Response Curves in Dynamic Glucose-Enhanced (DGE) Imaging: Comparison Between glucoCEST and Blood Glucose Sampling in Humans. Tomography. 2018 Dec;4(4):164-171. doi: 10.18383/j.tom.2018.00025. PubMed PMID: 30588502; PubMed Central PMCID: PMC6299743.

Chen L, Wei Z, Chan KWY, Cai S, Liu G, Lu H, Wong PC, van Zijl PCM, Li T, Xu J. Protein aggregation linked to Alzheimer's disease revealed by saturation transfer MRI. Neuroimage. 2019 Mar;188:380-390. doi: 10.1016/j.neuroimage.2018.12.018. Epub 2018 Dec 13. PubMed PMID: 30553917; PubMed Central PMCID: PMC6401270.

Chen L, Barker PB, Weiss RG, van Zijl PCM, Xu J. Creatine and phosphocreatine mapping of mouse skeletal muscle by a polynomial and Lorentzian line-shape fitting CEST method. Magn Reson Med. 2019 Jan;81(1):69-78. doi: 10.1002/mrm.27514. Epub 2018 Sep 23. PubMed PMID: 30246265; PubMed Central PMCID: PMC6258268.

Sehgal AA, Li Y, Lal B, Yadav NN, Xu X, Xu J, Laterra J, van Zijl PCM. CEST MRI of 3-O-methyl-D-glucose uptake and accumulation in brain tumors. Magn Reason Med. 2019 Mar;81(3):1993-2000. doi: 10.1002/mrm.27489. Epub 2018 Sep 11. PubMed PMID: 30206994; PubMed Central PMCID: PMC6347504.

Xu X, Xu J, Chan KWY, Liu J, Liu H, Li Y, Chen L, Liu G, van Zijl PCM. GlucoCEST imaging with on-resonance variable delay multiple pulse (onVDMP) MRI. Magn Reson Med. 2019 Jan;81(1):47-56. doi: 10.1002/mrm.27364. Epub 2018 Jul 29. PubMed PMID: 30058240; PubMed Central PMCID: PMC6258333.

Liu J, Han Z, Chen G, Li Y, Zhang J, Xu J, van Zijl PCM, Zhang S, Liu G. CEST MRI of sepsis-induced acute kidney injury. NMR Biomed. 2018 Aug;31(8):e3942. doi: 10.1002/nbm.3942. Epub 2018 Jun 13. PubMed PMID: 29897643.

Knutsson L, Xu J, Ahlgren A, van Zijl PCM. CEST, ASL, and magnetization transfer contrast: How similar pulse sequences detect different phenomena. Magn Reson Med. 2018 Oct;80(4):1320-1340. doi: 10.1002/mrm.27341. Epub 2018 May 30. Review. PubMed PMID: 29845640; PubMed Central PMCID: PMC6097930.

Liu J, Bai R, Li Y, Staedtke V, Zhang S, van Zijl PCM, Liu G. MRI detection of bacterial brain abscesses and monitoring of antibiotic treatment using bacCEST. Magn Reson Med. 2018 Aug;80(2):662-671. doi: 10.1002/mrm.27180. Epub 2018 Mar 25. PubMed PMID: 29577382; PubMed Central PMCID: PMC5910221.

Banerjee SR, Song X, Yang X, Minn I, Lisok A, Chen Y, Bui A, Chatterjee S, Chen J, van Zijl PCM, McMahon MT, Pomper MG. Salicylic Acid-Based Polymeric Contrast Agents for Molecular Magnetic Resonance Imaging of Prostate Cancer. Chemistry. 2018 May 17;24(28):7235-7242. doi: 10.1002/chem.201800882. Epub 2018 Apr 26. PubMed PMID: 29508450; PubMed Central PMCID: PMC5980787.

Chen L, Xu X, Zeng H, Chan KWY, Yadav N, Cai S, Schunke KJ, Faraday N, van Zijl PCM, Xu J. Separating fast and slow exchange transfer and magnetization transfer using off-resonance variable-delay multiple-pulse (VDMP) MRI. Magn Reason Med. 2018 Oct;80(4):1568-1576. doi: 10.1002/mrm.27111. Epub 2018  Feb 5. PubMed PMID: 29405374; PubMed Central PMCID: PMC6077103.