Timothy Eubank, PhD

Professor

Organization:

West Virginia University School of Medicine

Department:

Microbiology, Immunology & Cell Biology

Classification:

Faculty

Senior Advisor

Organization:

West Virginia University Health Sciences Center

Department:

Research & Graduate Education

Classification:

Faculty

Member

Organization:

West Virginia University WVU Cancer Institute

Department:

WVU Cancer Institute Research Programs

Classification:

Faculty

This list represents my publications over the past 5 years:

1: Pratt HG, Ma L, Dziadowicz SA, Ott S, Whalley T, Szomolay B, Eubank TD#, Hu G#, Boone BA#. Clin Transl Med. 2024 Mar;14(3):e1595. doi: 10.1002/ctm2.1595. Analysis of single nuclear chromatin accessibility reveals unique myeloid populations in human pancreatic ductal adenocarcinoma. PMID: 38426634. #Corresponding authors. 

2: Sudhakaran M, Navarrete TG, Mejía-Guerra K, Mukundi E, Eubank TD, Grotewold E, Arango D, Doseff AI. Transcriptome reprogramming through alternative splicing triggered by apigenin drives cell death in triple-negative breast cancer. Cell Death Dis. 2023 Dec 13;14(12):824. doi: 10.1038/s41419-023-06342-6. PMID: 38092740 

3: Shaw MA, Poncelet M, Viswakarma N, Vallerini GP, Hameed S, Gluth TD, Geldenhuys WJ, Hoblitzell EH, Eubank TD, Epel B, Kotecha M, Driesschaert B. SOX71, A Biocompatible Succinyl Derivative of the Triarylmethyl Radical OX071 for In Vivo Quantitative Oxygen Mapping Using Electron Paramagnetic Resonance. Mol Imaging Biol. 2023 Nov 9:10.1007/s11307-023-01869-8. doi: 10.1007/s11307-023-01869-8. PMID: 37945971 

4: Mihalik NE, Steinberger KJ, Stevens AM, Bobko AA, Hoblitzell EH, Tseytlin O, Akhter H, Dziadowicz SA, Wang L, O'Connell RC, Monaghan KL, Hu G, Mo X, Khramtsov VV, Tseytlin M, Driesschaert B, Wan ECK, Eubank TD. Dose-Specific Intratumoral GM-CSF Modulates Breast Tumor Oxygenation and Antitumor Immunity. J Immunol. 2023 Sep 27:ji2300326. doi: 10.4049/jimmunol.2300326. Epub ahead of print. PMID: 37756529.

5: Eubank TD, Bobko AA, Hoblitzell EH, Gencheva M, Driesschaert B, Khramtsov VV. In Vivo Electron Paramagnetic Resonance Molecular Profiling of Tumor Microenvironment upon Tumor Progression to Malignancy in an Animal Model of Breast Cancer. Mol Imaging Biol. 2023 Aug 23. doi: 10.1007/s11307-023-01847-0. Epub ahead of print. PMID: 37610610.

6: Rentz LE, Whetsell MA, Clayton SA, Mizener AD, Holásková I, Chapa MG, Hoblitzell EH, Eubank TD, Pistilli EE. Sexual Dimorphism of Skeletal Muscle in a Mouse Model of Breast Cancer: A Functional and Molecular Analysis. Int J Mol Sci. 2023 Jul 19;24(14):11669. doi: 10.3390/ijms241411669. PMID: 37511427; PMCID: PMC10380440.

7: Rentz LE, Whetsell M, Clayton SA, Mizener AD, Holásková I, Chapa MG, Hoblitzell EH, Eubank TD, Pistilli EE. Sexual Dimorphism of Skeletal Muscle in a Mouse Model of Breast Cancer: A Functional and Molecular Analysis. bioRxiv [Preprint]. 2023 Jun 9:2023.06.07.544049. doi: 10.1101/2023.06.07.544049. Update in: Int J Mol Sci. 2023 Jul 19;24(14): PMID: 37362158; PMCID: PMC10288531.

8: Steinberger KJ, Eubank TD. The Underexplored Landscape of Hypoxia-Inducible Factor 2 Alpha and Potential Roles in Tumor Macrophages: A Review. Oxygen (Basel). 2023 Mar;3(1):45-76. doi: 10.3390/oxygen3010005. Epub 2023 Jan 31. PMID: 37124241; PMCID: PMC10137047.

9: Gluth TD, Poncelet M, Gencheva M, Hoblitzell EH, Khramtsov VV, Eubank TD, Driesschaert B. Biocompatible Monophosphonated Trityl Spin Probe, HOPE71, for In Vivo Measurement of pO2, pH, and [Pi] by Electron Paramagnetic Resonance Spectroscopy. Anal Chem. 2023 Jan 17;95(2):946-954. doi: 10.1021/acs.analchem.2c03476. Epub 2022 Dec 20. PMID: 36537829; PMCID: PMC9852220.

10: Ye Q, Hickey J, Summers K, Falatovich B, Gencheva M, Eubank TD, Ivanov AV, Guo NL. Multi-Omics Immune Interaction Networks in Lung Cancer Tumorigenesis, Proliferation, and Survival. Int J Mol Sci. 2022 Nov 29;23(23):14978. doi: 10.3390/ijms232314978. PMID: 36499305; PMCID: PMC9738413.

11: Poncelet M, Ngendahimana T, Gluth TD, Hoblitzell EH, Eubank TD, Eaton GR, Eaton SS, Driesschaert B. Synthesis and characterization of a biocompatible 13C1 isotopologue of trityl radical OX071 for in vivo EPR viscometry. Analyst. 2022 Dec 5;147(24):5643-5648. doi: 10.1039/d2an01527g. PMID: 36373434; PMCID: PMC9729415.

12: O'Connell RC, Tseytlin O, Bobko AA, Eubank TD, Tseytlin M. Rapid scan EPR: Automated digital resonator control for low-latency data acquisition. J Magn Reson. 2022 Dec;345:107308. doi: 10.1016/j.jmr.2022.107308. Epub 2022 Oct 21. PMID: 36356489; PMCID: PMC10266206.

13: Ye Q, Falatovich B, Singh S, Ivanov AV, Eubank TD, Guo NL. A Multi-Omics Network of a Seven-Gene Prognostic Signature for Non-Small Cell Lung Cancer. Int J Mol Sci. 2021 Dec 25;23(1):219. doi: 10.3390/ijms23010219. PMID: 35008645; PMCID: PMC8745553.

14: Pratt HG, Steinberger KJ, Mihalik NE, Ott S, Whalley T, Szomolay B, Boone BA, Eubank TD. Macrophage and Neutrophil Interactions in the Pancreatic Tumor Microenvironment Drive the Pathogenesis of Pancreatic Cancer. Cancers (Basel). 2021 Dec 31;14(1):194. doi: 10.3390/cancers14010194. PMID: 35008355; PMCID: PMC8750413.

15: Gluth TD, Poncelet M, DeVience S, Gencheva M, Hoblitzell EH, Khramtsov VV, Eubank TD, Driesschaert B. Large-scale synthesis of a monophosphonated tetrathiatriarylmethyl spin probe for concurrent in vivo measurement of pO2, pH and inorganic phosphate by EPR. RSC Adv. 2021 Jul 27;11(42):25951-25954. doi: 10.1039/d1ra04551b. PMID: 34354828; PMCID: PMC8314523.

16: Ahmad RS, Eubank TD, Lukomski S, Boone BA. Immune Cell Modulation of the Extracellular Matrix Contributes to the Pathogenesis of Pancreatic Cancer. Biomolecules. 2021 Jun 17;11(6):901. doi: 10.3390/biom11060901. PMID: 34204306; PMCID: PMC8234537.

17: Mihalik NE, Wen S, Driesschaert B, Eubank TD. Formulation and In Vitro Characterization of PLGA/PLGA-PEG Nanoparticles Loaded with Murine Granulocyte- Macrophage Colony-Stimulating Factor. AAPS PharmSciTech. 2021 Jun 24;22(5):191. doi: 10.1208/s12249-021-02049-z. PMID: 34169366; PMCID: PMC8361900.

18: Velayutham M, Poncelet M, Eubank TD, Driesschaert B, Khramtsov VV. Biological Applications of Electron Paramagnetic Resonance Viscometry Using a 13C-Labeled Trityl Spin Probe. Molecules. 2021 May 8;26(9):2781. doi: 10.3390/molecules26092781. PMID: 34066858; PMCID: PMC8125944.

19: Ye Q, Mohamed R, Dakhlallah D, Gencheva M, Hu G, Pearce MC, Kolluri SK, Marsh CB, Eubank TD, Ivanov AV, Guo NL. Molecular Analysis of ZNF71 KRAB in Non-Small-Cell Lung Cancer. Int J Mol Sci. 2021 Apr 4;22(7):3752. doi: 10.3390/ijms22073752. PMID: 33916522; PMCID: PMC8038441.

20: Mattes MD, Eubank TD, Almubarak M, Wen S, Marano GD, Jacobson GM, Ma PC. A Prospective Trial Evaluating the Safety and Systemic Response From the Concurrent Use of Radiation Therapy with Checkpoint Inhibitor Immunotherapy in Metastatic Non-Small Cell Lung Cancer. Clin Lung Cancer. 2021 Jul;22(4):268-273. doi: 10.1016/j.cllc.2021.01.012. Epub 2021 Jan 25. PMID: 33608212; PMCID: PMC8310528.

21: Madan E, Peixoto ML, Dimitrion P, Eubank TD, Yekelchyk M, Talukdar S, Fisher PB, Mi QS, Moreno E, Gogna R. Cell Competition Boosts Clonal Evolution and Hypoxic Selection in Cancer. Trends Cell Biol. 2020 Dec;30(12):967-978. doi: 10.1016/j.tcb.2020.10.002. Epub 2020 Nov 4. PMID: 33160818.

22: Steinberger KJ, Forget MA, Bobko AA, Mihalik NE, Gencheva M, Roda JM, Cole SL, Mo X, Hoblitzell EH, Evans R, Gross AC, Moldovan L, Marsh CB, Khramtsov VV, Eubank TD. Correction: Hypoxia-Inducible Factor α Subunits Regulate Tie2-Expressing Macrophages That Influence Tumor Oxygen and Perfusion in Murine Breast Cancer. J Immunol. 2020 Dec 1;205(11):3231. doi: 10.4049/jimmunol.2001134. Epub 2020 Oct 28. Erratum for: J Immunol. 2020 Oct 15;205(8):2301-2311. PMID: 33115855; PMCID: PMC7853301.

23: Kofina V, Demirer M, Erdal BS, Eubank TD, Yildiz VO, Tatakis DN, Leblebicioglu B. Bone grafting history affects soft tissue healing following implant placement. J Periodontol. 2021 Feb;92(2):234-243. doi: 10.1002/JPER.19-0709. Epub 2020 Aug 19. PMID: 32779206.

24: Sanzhaeva U, Poncelet M, Tseytlin O, Tseytlin M, Gencheva M, Eubank TD, Khramtsov VV, Driesschaert B. Synthesis, Characterization, and Application of a Highly Hydrophilic Triarylmethyl Radical for Biomedical EPR. J Org Chem. 2020 Aug 21;85(16):10388-10398. doi: 10.1021/acs.joc.0c00557. Epub 2020 Aug 6. PMID: 32698583; PMCID: PMC7814971.

25: Steinberger KJ, Bailey MT, Gross AC, Sumner LA, Voorhees JL, Crouser N, Curry JM, Wang Y, DeVries AC, Marsh CB, Glaser R, Yang EV, Eubank TD. Stress- induced Norepinephrine Downregulates CCL2 in Macrophages to Suppress Tumor Growth in a Model of Malignant Melanoma. Cancer Prev Res (Phila). 2020 Sep;13(9):747-760. doi: 10.1158/1940-6207.CAPR-19-0370. Epub 2020 Jun 9. PMID: 32518084; PMCID: PMC7607650.

26: Poblete JMS, Ballinger MN, Bao S, Alghothani M, Nevado JB Jr, Eubank TD, Christman JW, Magalang UJ. Macrophage HIF-1α mediates obesity-related adipose tissue dysfunction via interleukin-1 receptor-associated kinase M. Am J Physiol Endocrinol Metab. 2020 May 1;318(5):E689-E700. doi: 10.1152/ajpendo.00174.2019. Epub 2020 Mar 10. PMID: 32154744; PMCID: PMC7717118.

27: Leblebicioglu B, Alssum L, Eubank TD, Yildiz VO, Tatakis DN. Wound Fluid Cytokine Profile Following Bone Regeneration Procedures. J Oral Implantol. 2020 Apr 1;46(2):107-113. doi: 10.1563/aaid-joi-D-19-00061. PMID: 31909694.

28: Dakhlallah D, Wang Y, Bobo TA, Ellis E, Mo X, Piper MG, Eubank TD, Marsh CB. Constitutive AKT Activity Predisposes Lung Fibrosis by Regulating Macrophage, Myofibroblast and Fibrocyte Recruitment and Changes in Autophagy. Adv Biosci Biotechnol. 2019 Oct;10(10):346-373. doi: 10.4236/abb.2019.1010027. Epub 2019 Oct 30. PMID: 31750010; PMCID: PMC6866236.

29: Dakhlallah DA, Wisler J, Gencheva M, Brown CM, Leatherman ER, Singh K, Brundage K, Karsies T, Dakhlallah A, Witwer KW, Sen CK, Eubank TD, Marsh CB. Circulating extracellular vesicle content reveals de novo DNA methyltransferase expression as a molecular method to predict septic shock. J Extracell Vesicles. 2019 Sep 28;8(1):1669881. doi: 10.1080/20013078.2019.1669881. PMID: 31632618; PMCID: PMC6781191.

30: Gorodetskii AA, Eubank TD, Driesschaert B, Poncelet M, Ellis E, Khramtsov VV, Bobko AA. Development of multifunctional Overhauser-enhanced magnetic resonance imaging for concurrent in vivo mapping of tumor interstitial oxygenation, acidosis and inorganic phosphate concentration. Sci Rep. 2019 Aug 20;9(1):12093. doi: 10.1038/s41598-019-48524-3. PMID: 31431629; PMCID: PMC6702349.

31: Tseytlin O, Guggilapu P, Bobko AA, AlAhmad H, Xu X, Epel B, O'Connell R, Hoblitzell EH, Eubank TD, Khramtsov VV, Driesschaert B, Kazkaz E, Tseytlin M. Modular imaging system: Rapid scan EPR at 800 MHz. J Magn Reson. 2019 Aug;305:94-103. doi: 10.1016/j.jmr.2019.06.003. Epub 2019 Jun 8. PMID: 31238278; PMCID: PMC6656609.

32: Poncelet M, Driesschaert B, Tseytlin O, Tseytlin M, Eubank TD, Khramtsov VV. Dextran-conjugated tetrathiatriarylmethyl radicals as biocompatible spin probes for EPR spectroscopy and imaging. Bioorg Med Chem Lett. 2019 Jul 15;29(14):1756-1760. doi: 10.1016/j.bmcl.2019.05.017. Epub 2019 May 13. PMID: 31129052; PMCID: PMC6557268.

Dr. Eubank’s research program focus is on the role of myeloid cells/mononuclear phagocytes in tumor growth and angiogenesis as well as monocyte and macrophage HIF (hypoxia inducible factor) biology. His group reported that monocytes and macrophages can be “re-educated” in solid tumors to become anti-angiogenic and were the first to report that GM-CSF stimulates tumor macrophages to overexpress the soluble form of VEGFR-1, which sequesters tumor-produced VEGF from bioactivity, and become more “M1”-like depending on local tumor microenvironment (TME). Further, they were the first to report the disparate functions of HIF-1α and HIF-2α in tumor-associated macrophages and that a hypoxia inducible factor (HIF-2α) can be anti-angiogenic. In more recent and current work, they are focused on understanding the macrophage subsets and functions responsible for generating and perpetuating the hypoxic and immunosuppressive TME in both breast and pancreatic cancers. They are also investigating methods to alleviate hypoxia and immunosuppression by directing macrophage functions. Dr. Eubank has numerous publications in Immunity, Blood, Cancer Research, and J of Immunology pertaining to this focus. Further, he received the K99/R00 Pathway to Independence Award from the NCI for his work with macrophage regulation of breast cancer growth and angiogenesis. His expertise in macrophage HIF biology has led to several patent applications using a novel small molecule compound to stabilize HIF-2α to regulate dysfunctional and unproductive angiogenesis that perpetuates hypoxia.

In vivo Multifunctional Magnetic Resonance

Dr. Eubank’s current interests include the continuous investigation into the role of novel macrophage subtypes which augment tumor progression and unproductive angiogenesis that perpetuate tumor hypoxia, as determined by particulate and soluble oxygen-sensing EPR probes (in collaboration with Dr. Andrey Bobko, Dept of Biochemistry, Dr. Valery Khramtsov, Dept of Biochemistry, Dr. Benoit Driesschaert, Dept of Pharmaceutical Sciences, WVU) and EPR imaging (in collaboration with Dr. Mark Tseytlin, Dept of Biochemistry) and immunohistochemistry/micro-CT techniques. He is also interested in how the different macrophage HIFs regulate degree of success of chemotherapy compounds in mouse models of breast cancer. Finally, he is collaborating with Dr. Ray Raylman, Dept of Radiology, Dr. Valery Khramtsov and Dr. Mark Tsyetlin on elucidating the origin and role of macrophages that initiate and maintain treatment resistance in breast and pancreatic cancers (in collaboration with Dr. Brian Boone, surgical oncologist).