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Article ; Online: Imaging telomerase reverse transcriptase expression in oligodendrogliomas using hyperpolarized δ-[1-

Batsios, Georgios / Taglang, Celine / Gillespie, Anne Marie / Viswanath, Pavithra

2023 Volume 5, Issue 1, Page(s) vdad092

Abstract: Background: Telomere maintenance by telomerase reverse transcriptase (TERT) is essential for immortality in most cancers, including oligodendrogliomas. Agents that disrupt telomere maintenance such as the telomere uncapping agent 6-thio-2'- ... ...

Abstract	Background: Telomere maintenance by telomerase reverse transcriptase (TERT) is essential for immortality in most cancers, including oligodendrogliomas. Agents that disrupt telomere maintenance such as the telomere uncapping agent 6-thio-2'-deoxyguanosine (6-thio-dG) are in clinical trials. We previously showed that TERT expression in oligodendrogliomas is associated with upregulation of glucose-6-phosphate dehydrogenase (G6PD), the rate-limiting enzyme of the pentose phosphate pathway (PPP). We also showed that hyperpolarized δ-[1- Methods: We examined patient-derived oligodendroglioma cells and orthotopic tumors to assess the link between TERT and hyperpolarized δ-[1- Results: Doxycycline-inducible TERT silencing abrogated 6-PG production from hyperpolarized δ-[1- Conclusions: These results indicate that hyperpolarized δ-[1-
Language	English
Publishing date	2023-07-21
Publishing country	England
Document type	Journal Article
ZDB-ID	3009682-0
ISSN	2632-2498 ; 2632-2498
ISSN (online)	2632-2498
ISSN	2632-2498
DOI	10.1093/noajnl/vdad092
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Article: Deuterium Metabolic Imaging-Rediscovery of a Spectroscopic Tool.

Polvoy, Ilona / Qin, Hecong / Flavell, Robert R / Gordon, Jeremy / Viswanath, Pavithra / Sriram, Renuka / Ohliger, Michael A / Wilson, David M

Metabolites

2021 Volume 11, Issue 9

Abstract: The growing demand for metabolism-specific imaging techniques has rekindled interest in Deuterium ( ...

Abstract	The growing demand for metabolism-specific imaging techniques has rekindled interest in Deuterium (
Language	English
Publishing date	2021-08-25
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2662251-8
ISSN	2218-1989
ISSN	2218-1989
DOI	10.3390/metabo11090570
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Article: Metabolic reprogramming of pyruvate dehydrogenase is essential for the proliferation of glioma cells expressing mutant IDH1.

Viswanath, Pavithra / Ronen, Sabrina M

Molecular & cellular oncology

2015 Volume 3, Issue 2, Page(s) e1077922

Abstract: Mutations in isocitrate dehydrogenase 1 ( ...

Abstract	Mutations in isocitrate dehydrogenase 1 (
Language	English
Publishing date	2015-08-27
Publishing country	United States
Document type	Journal Article
ISSN	2372-3556
ISSN	2372-3556
DOI	10.1080/23723556.2015.1077922
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Article: Telomerase reverse transcriptase induces targetable alterations in glutathione and nucleotide biosynthesis in glioblastomas.

Udutha, Suresh / Taglang, Céline / Batsios, Georgios / Gillespie, Anne Marie / Tran, Meryssa / Ronen, Sabrina M / Ten Hoeve, Johanna / Graeber, Thomas G / Viswanath, Pavithra

bioRxiv : the preprint server for biology

2023

Abstract: Telomerase reverse transcriptase (TERT) is essential for glioblastoma (GBM) proliferation. Delineating metabolic vulnerabilities induced by TERT can lead to novel GBM therapies. We previously showed that TERT upregulates glutathione (GSH) pool size in ... ...

Abstract	Telomerase reverse transcriptase (TERT) is essential for glioblastoma (GBM) proliferation. Delineating metabolic vulnerabilities induced by TERT can lead to novel GBM therapies. We previously showed that TERT upregulates glutathione (GSH) pool size in GBMs. Here, we show that TERT acts via the FOXO1 transcription factor to upregulate expression of the catalytic subunit of glutamate-cysteine ligase (GCLC), the rate-limiting enzyme of Significance: Using
Language	English
Publishing date	2023-11-16
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.11.14.566937
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Article ; Online: Hyperpolarized δ-[1-

Minami, Noriaki / Hong, Donghyun / Taglang, Celine / Batsios, Georgios / Gillespie, Anne Marie / Viswanath, Pavithra / Stevers, Nicholas / Barger, Carter J / Costello, Joseph F / Ronen, Sabrina M

Scientific reports

2023 Volume 13, Issue 1, Page(s) 5190

Abstract: TERT promoter mutations are a hallmark of glioblastoma (GBM). Accordingly, TERT and GABPB1, a subunit of the upstream mutant TERT promoter transcription factor GABP, are being considered as promising therapeutic targets in GBM. We recently reported that ... ...

Abstract	TERT promoter mutations are a hallmark of glioblastoma (GBM). Accordingly, TERT and GABPB1, a subunit of the upstream mutant TERT promoter transcription factor GABP, are being considered as promising therapeutic targets in GBM. We recently reported that the expression of TERT or GABP1 modulates flux via the pentose phosphate pathway (PPP). Here, we investigated whether
MeSH term(s)	Humans ; Glioblastoma/diagnostic imaging ; Glioblastoma/drug therapy ; Glioblastoma/genetics ; Magnetic Resonance Spectroscopy/methods ; Lactones/therapeutic use ; Diagnostic Imaging ; Brain Neoplasms/diagnostic imaging ; Brain Neoplasms/drug therapy ; Brain Neoplasms/genetics ; Telomerase/genetics ; Telomerase/metabolism ; GA-Binding Protein Transcription Factor/metabolism
Chemical Substances	beta-glucono-1,5-lactone (WQ29KQ9POT) ; Lactones ; TERT protein, human (EC 2.7.7.49) ; Telomerase (EC 2.7.7.49) ; GABPB1 protein, human ; GA-Binding Protein Transcription Factor
Language	English
Publishing date	2023-03-30
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-023-32463-1
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Article ; Online: Deuterium Metabolic Imaging Reports on TERT Expression and Early Response to Therapy in Cancer.

Batsios, Georgios / Taglang, Céline / Tran, Meryssa / Stevers, Nicholas / Barger, Carter / Gillespie, Anne Marie / Ronen, Sabrina M / Costello, Joseph F / Viswanath, Pavithra

Clinical cancer research : an official journal of the American Association for Cancer Research

2022 Volume 28, Issue 16, Page(s) 3526–3536

Abstract: Purpose: Telomere maintenance is a hallmark of cancer. Most tumors maintain telomere length via reactivation of telomerase reverse transcriptase (TERT) expression. Identifying clinically translatable imaging biomarkers of TERT can enable noninvasive ... ...

Abstract	Purpose: Telomere maintenance is a hallmark of cancer. Most tumors maintain telomere length via reactivation of telomerase reverse transcriptase (TERT) expression. Identifying clinically translatable imaging biomarkers of TERT can enable noninvasive assessment of tumor proliferation and response to therapy. Experimental design: We used RNAi, doxycycline-inducible expression systems, and pharmacologic inhibitors to mechanistically delineate the association between TERT and metabolism in preclinical patient-derived tumor models. Deuterium magnetic resonance spectroscopy (2H-MRS), which is a novel, translational metabolic imaging modality, was used for imaging TERT in cells and tumor-bearing mice in vivo. Results: Our results indicate that TERT expression is associated with elevated NADH in multiple cancers, including glioblastoma, oligodendroglioma, melanoma, neuroblastoma, and hepatocellular carcinoma. Mechanistically, TERT acts via the metabolic regulator FOXO1 to upregulate nicotinamide phosphoribosyl transferase, which is the key enzyme for NAD+ biosynthesis, and the glycolytic enzyme glyceraldehyde-3-phosphate dehydrogenase, which converts NAD+ to NADH. Because NADH is essential for pyruvate flux to lactate, we show that 2H-MRS-based assessment of lactate production from [U-2H]-pyruvate reports on TERT expression in preclinical tumor models in vivo, including at clinical field strength (3T). Importantly, [U-2H]-pyruvate reports on early response to therapy in mice bearing orthotopic patient-derived gliomas at early timepoints before radiographic alterations can be visualized by MRI. Conclusions: Elevated NADH is a metabolic consequence of TERT expression in cancer. Importantly, [U-2H]-pyruvate reports on early response to therapy, prior to anatomic alterations, thereby providing clinicians with a novel tool for assessment of tumor burden and treatment response in cancer.
MeSH term(s)	Animals ; Deuterium/metabolism ; Glioblastoma ; Lactic Acid/metabolism ; Mice ; NAD/metabolism ; Pyruvic Acid/metabolism ; Telomerase/genetics ; Telomerase/metabolism
Chemical Substances	NAD (0U46U6E8UK) ; Lactic Acid (33X04XA5AT) ; Pyruvic Acid (8558G7RUTR) ; Deuterium (AR09D82C7G) ; Telomerase (EC 2.7.7.49)
Language	English
Publishing date	2022-05-25
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	1225457-5
ISSN	1557-3265 ; 1078-0432
ISSN (online)	1557-3265
ISSN	1078-0432
DOI	10.1158/1078-0432.CCR-21-4418
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Article ; Online: Hyperpolarized δ-[1- 13C]gluconolactone imaging visualizes response to TERT or GABPB1 targeting therapy for glioblastoma

Noriaki Minami / Donghyun Hong / Celine Taglang / Georgios Batsios / Anne Marie Gillespie / Pavithra Viswanath / Nicholas Stevers / Carter J. Barger / Joseph F. Costello / Sabrina M. Ronen

Scientific Reports, Vol 13, Iss 1, Pp 1-

2023 Volume 11

Abstract: Abstract TERT promoter mutations are a hallmark of glioblastoma (GBM). Accordingly, TERT and GABPB1, a subunit of the upstream mutant TERT promoter transcription factor GABP, are being considered as promising therapeutic targets in GBM. We recently ... ...

Abstract	Abstract TERT promoter mutations are a hallmark of glioblastoma (GBM). Accordingly, TERT and GABPB1, a subunit of the upstream mutant TERT promoter transcription factor GABP, are being considered as promising therapeutic targets in GBM. We recently reported that the expression of TERT or GABP1 modulates flux via the pentose phosphate pathway (PPP). Here, we investigated whether 13C magnetic resonance spectroscopy (MRS) of hyperpolarized (HP) δ- [1-13C]gluconolactone can serve to image the reduction in PPP flux following TERT or GABPB1 silencing. We investigated two different human GBM cell lines stably expressing shRNAs targeting TERT or GABPB1, as well as doxycycline-inducible shTERT or shGABPB1cells. MRS studies were performed on live cells and in vivo tumors, and dynamic sets of 13C MR spectra were acquired following injection of HP δ-[1-13C]gluconolactone. HP 6-phosphogluconolactone (6PG), the product of δ-[1-13C]gluconolactone via the PPP, was significantly reduced in TERT or GABPB1-silenced cells or tumors compared to controls in all our models. Furthermore, a positive correlation between TERT expression and 6PG levels was observed. Our data indicate that HP δ-[1-13C]gluconolactone, an imaging tool with translational potential, could serve to monitor TERT expression and its silencing with therapies that target either TERT or GABPB1 in mutant TERT promoter GBM patients.
Keywords	Medicine ; R ; Science ; Q
Subject code	570
Language	English
Publishing date	2023-03-01T00:00:00Z
Publisher	Nature Portfolio
Document type	Article ; Online
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Article ; Online: Acquisition and quantification pipeline for in vivo hyperpolarized

Hong, Donghyun / Batsios, Georgios / Viswanath, Pavithra / Gillespie, Anne Marie / Vaidya, Manushka / Larson, Peder E Z / Ronen, Sabrina M

Magnetic resonance in medicine

2021 Volume 87, Issue 4, Page(s) 1673–1687

Abstract: Purpose: The goal of this study was to combine a specialized acquisition method with a new quantification pipeline to accurately and efficiently probe the metabolism of hyperpolarized : Methods: We used a multiband metabolite-specific radiofrequency ( ...

Abstract	Purpose: The goal of this study was to combine a specialized acquisition method with a new quantification pipeline to accurately and efficiently probe the metabolism of hyperpolarized Methods: We used a multiband metabolite-specific radiofrequency (RF) excitation in combination with a variable flip angle scheme to minimize substrate polarization loss and measure fast metabolic processes. We then applied spectral-temporal denoising using singular value decomposition to enhance spectral quality. This was combined with LCModel-based automatic Results: Denoising improved the metabolite signal-to-noise ratio (SNR) by approximately 5. It also improved the accuracy of metabolite quantification as evidenced by a significant reduction of the Cramer Rao lower bounds. Furthermore, the use of the automated and user-independent LCModel-based quantification approach could be performed rapidly, with the kinetic quantification of eight metabolite peaks in a 12-spectrum array achieved in less than 1 minute. Conclusion: The specialized acquisition method combined with denoising and a new quantification pipeline using LCModel for the first time for hyperpolarized
MeSH term(s)	Animals ; Brain Neoplasms/diagnostic imaging ; Carbon Isotopes ; Kinetics ; Magnetic Resonance Spectroscopy ; Pyruvic Acid/metabolism ; Rats ; Signal-To-Noise Ratio
Chemical Substances	Carbon Isotopes ; Pyruvic Acid (8558G7RUTR)
Language	English
Publishing date	2021-11-14
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	605774-3
ISSN	1522-2594 ; 0740-3194
ISSN (online)	1522-2594
ISSN	0740-3194
DOI	10.1002/mrm.29081
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Zs.A 1959: Show issues

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Article ; Online: A

Vaidya, Manushka V / Zhang, Bei / Hong, DongHyun / Brown, Ryan / Batsios, Georgios / Viswanath, Pavithra / Paska, Jan / Wulf, Gerburg / Grant, Aaron K / Ronen, Sabrina M / Larson, Peder E Z

Journal of magnetic resonance (San Diego, Calif. : 1997)

2022 Volume 343, Page(s) 107286

Abstract: Purpose: We constructed a : Methods: All experiments were carried out at 3 Tesla. The multinuclear surface coil was designed as two coplanar loops each tuned to either the : Results: When compared with single tuned surface coils, the multinuclear ... ...

Abstract	Purpose: We constructed a Methods: All experiments were carried out at 3 Tesla. The multinuclear surface coil was designed as two coplanar loops each tuned to either the Results: When compared with single tuned surface coils, the multinuclear coil performance showed a decrease in Q factor ratio, SNR, and transmit efficiency. Flip angle maps showed adequate flip angles within the phantom when the transmit voltage was set using an external phantom. Results show good detection of Conclusions: The coil enables obtaining complementary information within a scan session, thus reducing the number of trials and minimizing biological variability for studies of metabolism and bioenergetics.
MeSH term(s)	Animals ; Rats ; Magnetic Resonance Imaging ; Protons ; Rodentia/metabolism ; Bicarbonates ; Brain/diagnostic imaging ; Brain/metabolism ; Phantoms, Imaging ; Pyruvic Acid/metabolism ; Lactates ; Alanine ; Adenosine Triphosphate ; Equipment Design
Chemical Substances	Protons ; Bicarbonates ; Pyruvic Acid (8558G7RUTR) ; Lactates ; Alanine (OF5P57N2ZX) ; Adenosine Triphosphate (8L70Q75FXE)
Language	English
Publishing date	2022-08-30
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1469665-4
ISSN	1096-0856 ; 1557-8968 ; 1090-7807 ; 0022-2364
ISSN (online)	1096-0856 ; 1557-8968
ISSN	1090-7807 ; 0022-2364
DOI	10.1016/j.jmr.2022.107286
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Article ; Online: Imaging biomarkers of TERT or GABPB1 silencing in TERT-positive glioblastoma.

Minami, Noriaki / Hong, Donghyun / Stevers, Nicholas / Barger, Carter J / Radoul, Marina / Hong, Chibo / Chen, Lee / Kim, Yaewon / Batsios, Georgios / Gillespie, Anne Marie / Pieper, Russel O / Costello, Joseph F / Viswanath, Pavithra / Ronen, Sabrina M

Neuro-oncology

2022 Volume 24, Issue 11, Page(s) 1898–1910

Abstract: Background: TERT promoter mutations are observed in 80% of wild-type IDH glioblastoma (GBM). Moreover, the upstream TERT transcription factor GABPB1 was recently identified as a cancer-specific therapeutic target for tumors harboring a TERT promoter ... ...

Abstract	Background: TERT promoter mutations are observed in 80% of wild-type IDH glioblastoma (GBM). Moreover, the upstream TERT transcription factor GABPB1 was recently identified as a cancer-specific therapeutic target for tumors harboring a TERT promoter mutation. In that context, noninvasive imaging biomarkers are needed for the detection of TERT modulation. Methods: Multiple GBM models were investigated as cells and in vivo tumors and the impact of TERT silencing, either directly or by targeting GABPB1, was determined using 1H and hyperpolarized 13C magnetic resonance spectroscopy (MRS). Changes in associated metabolic enzymes were also investigated. Results: 1H-MRS revealed that lactate and glutathione (GSH) were the most significantly altered metabolites when either TERT or GABPB1 was silenced, and lactate and GSH levels were correlated with cellular TERT expression. Consistent with the drop in lactate, 13C-MRS showed that hyperpolarized [1-13C]lactate production from [1-13C]pyruvate was also reduced when TERT was silenced. Mechanistically, the reduction in GSH was associated with a reduction in pentose phosphate pathway flux, reduced activity of glucose-6-phosphate dehydrogenase, and reduced NADPH. The drop in lactate and hyperpolarized lactate were associated with reductions in glycolytic flux, NADH, and expression/activity of GLUT1, monocarboxylate transporters, and lactate dehydrogenase A. Conclusions: Our study indicates that MRS-detectable GSH, lactate, and lactate production could serve as metabolic biomarkers of response to emerging TERT-targeted therapies for GBM with activating TERT promoter mutations. Importantly these biomarkers are readily translatable to the clinic, and thus could ultimately improve GBM patient management.
MeSH term(s)	Humans ; Glioblastoma/drug therapy ; Carbon Isotopes/metabolism ; Carbon Isotopes/therapeutic use ; Lactic Acid/metabolism ; Biomarkers ; Telomerase/metabolism ; GA-Binding Protein Transcription Factor/metabolism
Chemical Substances	Carbon-13 (FDJ0A8596D) ; Carbon Isotopes ; Lactic Acid (33X04XA5AT) ; Biomarkers ; TERT protein, human (EC 2.7.7.49) ; Telomerase (EC 2.7.7.49) ; GABPB1 protein, human ; GA-Binding Protein Transcription Factor
Language	English
Publishing date	2022-04-25
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2028601-6
ISSN	1523-5866 ; 1522-8517
ISSN (online)	1523-5866
ISSN	1522-8517
DOI	10.1093/neuonc/noac112
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