EPR oxygen imaging and hyperpolarized 13C MRI of pyruvate metabolism as noninvasive biomarkers of tumor treatment response to a glycolysis inhibitor 3-bromopyruvate
The hypoxic nature of tumors results in treatment resistance and poor prognosis. To spare limited oxygen for more crucial pathways, hypoxic cancerous cells suppress mitochondrial oxidative phosphorylation and promote glycolysis for energy production. Thereby, inhibition of glycolysis has the potenti...
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creator | Matsumoto, Shingo Saito, Keita Yasui, Hironobu Morris, H. Douglas Munasinghe, Jeeva P. Lizak, Martin Merkle, Hellmut Ardenkjaer-Larsen, Jan Henrik Choudhuri, Rajani Devasahayam, Nallathamby Subramanian, Sankaran Koretsky, Alan P. Mitchell, James B. Krishna, Murali C. |
description | The hypoxic nature of tumors results in treatment resistance and poor prognosis. To spare limited oxygen for more crucial pathways, hypoxic cancerous cells suppress mitochondrial oxidative phosphorylation and promote glycolysis for energy production. Thereby, inhibition of glycolysis has the potential to overcome treatment resistance of hypoxic tumors. Here, EPR imaging was used to evaluate oxygen dependent efficacy on hypoxia‐sensitive drug. The small molecule 3‐bromopyruvate blocks glycolysis pathway by inhibiting hypoxia inducible enzymes and enhanced cytotoxicity of 3‐bromopyruvate under hypoxic conditions has been reported in vitro. However, the efficacy of 3‐bromopyruvate was substantially attenuated in hypoxic tumor regions (pO2 < 10 mmHg) in vivo using squamous cell carcinoma (SCCVII)‐bearing mouse model. Metabolic MRI studies using hyperpolarized 13C‐labeled pyruvate showed that monocarboxylate transporter‐1 is the major transporter for pyruvate and the analog 3‐bromopyruvate in SCCVII tumor. The discrepant results between in vitro and in vivo data were attributed to biphasic oxygen dependent expression of monocarboxylate transporter‐1 in vivo. Expression of monocarboxylate transporter‐1 was enhanced in moderately hypoxic (8–15 mmHg) tumor regions but down regulated in severely hypoxic ( |
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Douglas ; Munasinghe, Jeeva P. ; Lizak, Martin ; Merkle, Hellmut ; Ardenkjaer-Larsen, Jan Henrik ; Choudhuri, Rajani ; Devasahayam, Nallathamby ; Subramanian, Sankaran ; Koretsky, Alan P. ; Mitchell, James B. ; Krishna, Murali C.</creator><creatorcontrib>Matsumoto, Shingo ; Saito, Keita ; Yasui, Hironobu ; Morris, H. Douglas ; Munasinghe, Jeeva P. ; Lizak, Martin ; Merkle, Hellmut ; Ardenkjaer-Larsen, Jan Henrik ; Choudhuri, Rajani ; Devasahayam, Nallathamby ; Subramanian, Sankaran ; Koretsky, Alan P. ; Mitchell, James B. ; Krishna, Murali C.</creatorcontrib><description>The hypoxic nature of tumors results in treatment resistance and poor prognosis. To spare limited oxygen for more crucial pathways, hypoxic cancerous cells suppress mitochondrial oxidative phosphorylation and promote glycolysis for energy production. Thereby, inhibition of glycolysis has the potential to overcome treatment resistance of hypoxic tumors. Here, EPR imaging was used to evaluate oxygen dependent efficacy on hypoxia‐sensitive drug. The small molecule 3‐bromopyruvate blocks glycolysis pathway by inhibiting hypoxia inducible enzymes and enhanced cytotoxicity of 3‐bromopyruvate under hypoxic conditions has been reported in vitro. However, the efficacy of 3‐bromopyruvate was substantially attenuated in hypoxic tumor regions (pO2 < 10 mmHg) in vivo using squamous cell carcinoma (SCCVII)‐bearing mouse model. Metabolic MRI studies using hyperpolarized 13C‐labeled pyruvate showed that monocarboxylate transporter‐1 is the major transporter for pyruvate and the analog 3‐bromopyruvate in SCCVII tumor. The discrepant results between in vitro and in vivo data were attributed to biphasic oxygen dependent expression of monocarboxylate transporter‐1 in vivo. Expression of monocarboxylate transporter‐1 was enhanced in moderately hypoxic (8–15 mmHg) tumor regions but down regulated in severely hypoxic (<5 mmHg) tumor regions. These results emphasize the importance of noninvasive imaging biomarkers to confirm the action of hypoxia‐activated drugs. Magn Reson Med, 2013. © 2012 Wiley Periodicals, Inc.</description><identifier>ISSN: 0740-3194</identifier><identifier>EISSN: 1522-2594</identifier><identifier>DOI: 10.1002/mrm.24355</identifier><identifier>PMID: 22692861</identifier><identifier>CODEN: MRMEEN</identifier><language>eng</language><publisher>Hoboken: Wiley Subscription Services, Inc., A Wiley Company</publisher><subject>3-bromopyruvate ; Animals ; Antineoplastic Agents - therapeutic use ; Biomarkers, Tumor - metabolism ; Carbon Radioisotopes - pharmacokinetics ; Carcinoma, Squamous Cell - diagnosis ; Carcinoma, Squamous Cell - drug therapy ; Carcinoma, Squamous Cell - metabolism ; Cell Line, Tumor ; Electron Spin Resonance Spectroscopy - methods ; EPR imaging ; Glycolysis - drug effects ; HIF-1 ; hyperpolarized 13C MRI ; Magnetic Resonance Imaging - methods ; MCT1 ; MCT1, tumor hypoxia ; Mice ; Molecular Imaging - methods ; Oxygen - metabolism ; Pyruvates - therapeutic use ; Pyruvic Acid - metabolism ; Radiopharmaceuticals - pharmacokinetics ; Reproducibility of Results ; Sensitivity and Specificity ; Treatment Outcome ; tumor hypoxia</subject><ispartof>Magnetic resonance in medicine, 2013-05, Vol.69 (5), p.1443-1450</ispartof><rights>Copyright © 2012 Wiley Periodicals, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fmrm.24355$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fmrm.24355$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22692861$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Matsumoto, Shingo</creatorcontrib><creatorcontrib>Saito, Keita</creatorcontrib><creatorcontrib>Yasui, Hironobu</creatorcontrib><creatorcontrib>Morris, H. Douglas</creatorcontrib><creatorcontrib>Munasinghe, Jeeva P.</creatorcontrib><creatorcontrib>Lizak, Martin</creatorcontrib><creatorcontrib>Merkle, Hellmut</creatorcontrib><creatorcontrib>Ardenkjaer-Larsen, Jan Henrik</creatorcontrib><creatorcontrib>Choudhuri, Rajani</creatorcontrib><creatorcontrib>Devasahayam, Nallathamby</creatorcontrib><creatorcontrib>Subramanian, Sankaran</creatorcontrib><creatorcontrib>Koretsky, Alan P.</creatorcontrib><creatorcontrib>Mitchell, James B.</creatorcontrib><creatorcontrib>Krishna, Murali C.</creatorcontrib><title>EPR oxygen imaging and hyperpolarized 13C MRI of pyruvate metabolism as noninvasive biomarkers of tumor treatment response to a glycolysis inhibitor 3-bromopyruvate</title><title>Magnetic resonance in medicine</title><addtitle>Magn Reson Med</addtitle><description>The hypoxic nature of tumors results in treatment resistance and poor prognosis. To spare limited oxygen for more crucial pathways, hypoxic cancerous cells suppress mitochondrial oxidative phosphorylation and promote glycolysis for energy production. Thereby, inhibition of glycolysis has the potential to overcome treatment resistance of hypoxic tumors. Here, EPR imaging was used to evaluate oxygen dependent efficacy on hypoxia‐sensitive drug. The small molecule 3‐bromopyruvate blocks glycolysis pathway by inhibiting hypoxia inducible enzymes and enhanced cytotoxicity of 3‐bromopyruvate under hypoxic conditions has been reported in vitro. However, the efficacy of 3‐bromopyruvate was substantially attenuated in hypoxic tumor regions (pO2 < 10 mmHg) in vivo using squamous cell carcinoma (SCCVII)‐bearing mouse model. Metabolic MRI studies using hyperpolarized 13C‐labeled pyruvate showed that monocarboxylate transporter‐1 is the major transporter for pyruvate and the analog 3‐bromopyruvate in SCCVII tumor. The discrepant results between in vitro and in vivo data were attributed to biphasic oxygen dependent expression of monocarboxylate transporter‐1 in vivo. Expression of monocarboxylate transporter‐1 was enhanced in moderately hypoxic (8–15 mmHg) tumor regions but down regulated in severely hypoxic (<5 mmHg) tumor regions. These results emphasize the importance of noninvasive imaging biomarkers to confirm the action of hypoxia‐activated drugs. Magn Reson Med, 2013. © 2012 Wiley Periodicals, Inc.</description><subject>3-bromopyruvate</subject><subject>Animals</subject><subject>Antineoplastic Agents - therapeutic use</subject><subject>Biomarkers, Tumor - metabolism</subject><subject>Carbon Radioisotopes - pharmacokinetics</subject><subject>Carcinoma, Squamous Cell - diagnosis</subject><subject>Carcinoma, Squamous Cell - drug therapy</subject><subject>Carcinoma, Squamous Cell - metabolism</subject><subject>Cell Line, Tumor</subject><subject>Electron Spin Resonance Spectroscopy - methods</subject><subject>EPR imaging</subject><subject>Glycolysis - drug effects</subject><subject>HIF-1</subject><subject>hyperpolarized 13C MRI</subject><subject>Magnetic Resonance Imaging - methods</subject><subject>MCT1</subject><subject>MCT1, tumor hypoxia</subject><subject>Mice</subject><subject>Molecular Imaging - methods</subject><subject>Oxygen - metabolism</subject><subject>Pyruvates - therapeutic use</subject><subject>Pyruvic Acid - metabolism</subject><subject>Radiopharmaceuticals - pharmacokinetics</subject><subject>Reproducibility of Results</subject><subject>Sensitivity and Specificity</subject><subject>Treatment Outcome</subject><subject>tumor hypoxia</subject><issn>0740-3194</issn><issn>1522-2594</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNo9kd1u1DAQhS0EokvhghdAlrhO6_8kl2hVSqUuoOXv0rITZ-sS26ntLA3Pw4PidtvejMea78xI5wDwFqMTjBA5ddGdEEY5fwZWmBNSEd6y52CFaoYqilt2BF6ldI0QatuavQRHhIiWNAKvwL-zr1sYbped8dA6tbN-B5Xv4dUymTiFUUX71_QQ0zXcbC9gGOC0xHmvsoHOZKXDaJODKkEfvPV7lezeQG2DU_G3ielOkGcXIszRqOyMzzCaNAWfDMwBKrgbly6MS7IJWn9ltc0FppWOwYXHU6_Bi0GNybx5eI_Bj49n39efqssv5xfrD5eVpazhlelqItAwND3uG82aTg2m08WKQeCaa0FLFUhpzkTP2DBwXv4dE6wMGKWcHoP3h71TDDezSVlehzn6clJiShqMW96QQr17oGbtTC-nWIyLi3w0tQCnB-CPHc3yNMdI3qUlS1ryPi252W7um6KoDgqbsrl9UhQPpahpzeWvz-dyQ9ei_vltKyn9D2eHmM4</recordid><startdate>201305</startdate><enddate>201305</enddate><creator>Matsumoto, Shingo</creator><creator>Saito, Keita</creator><creator>Yasui, Hironobu</creator><creator>Morris, H. Douglas</creator><creator>Munasinghe, Jeeva P.</creator><creator>Lizak, Martin</creator><creator>Merkle, Hellmut</creator><creator>Ardenkjaer-Larsen, Jan Henrik</creator><creator>Choudhuri, Rajani</creator><creator>Devasahayam, Nallathamby</creator><creator>Subramanian, Sankaran</creator><creator>Koretsky, Alan P.</creator><creator>Mitchell, James B.</creator><creator>Krishna, Murali C.</creator><general>Wiley Subscription Services, Inc., A Wiley Company</general><general>Wiley Subscription Services, Inc</general><scope>BSCLL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>M7Z</scope><scope>P64</scope></search><sort><creationdate>201305</creationdate><title>EPR oxygen imaging and hyperpolarized 13C MRI of pyruvate metabolism as noninvasive biomarkers of tumor treatment response to a glycolysis inhibitor 3-bromopyruvate</title><author>Matsumoto, Shingo ; Saito, Keita ; Yasui, Hironobu ; Morris, H. 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Douglas</au><au>Munasinghe, Jeeva P.</au><au>Lizak, Martin</au><au>Merkle, Hellmut</au><au>Ardenkjaer-Larsen, Jan Henrik</au><au>Choudhuri, Rajani</au><au>Devasahayam, Nallathamby</au><au>Subramanian, Sankaran</au><au>Koretsky, Alan P.</au><au>Mitchell, James B.</au><au>Krishna, Murali C.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>EPR oxygen imaging and hyperpolarized 13C MRI of pyruvate metabolism as noninvasive biomarkers of tumor treatment response to a glycolysis inhibitor 3-bromopyruvate</atitle><jtitle>Magnetic resonance in medicine</jtitle><addtitle>Magn Reson Med</addtitle><date>2013-05</date><risdate>2013</risdate><volume>69</volume><issue>5</issue><spage>1443</spage><epage>1450</epage><pages>1443-1450</pages><issn>0740-3194</issn><eissn>1522-2594</eissn><coden>MRMEEN</coden><abstract>The hypoxic nature of tumors results in treatment resistance and poor prognosis. To spare limited oxygen for more crucial pathways, hypoxic cancerous cells suppress mitochondrial oxidative phosphorylation and promote glycolysis for energy production. Thereby, inhibition of glycolysis has the potential to overcome treatment resistance of hypoxic tumors. Here, EPR imaging was used to evaluate oxygen dependent efficacy on hypoxia‐sensitive drug. The small molecule 3‐bromopyruvate blocks glycolysis pathway by inhibiting hypoxia inducible enzymes and enhanced cytotoxicity of 3‐bromopyruvate under hypoxic conditions has been reported in vitro. However, the efficacy of 3‐bromopyruvate was substantially attenuated in hypoxic tumor regions (pO2 < 10 mmHg) in vivo using squamous cell carcinoma (SCCVII)‐bearing mouse model. Metabolic MRI studies using hyperpolarized 13C‐labeled pyruvate showed that monocarboxylate transporter‐1 is the major transporter for pyruvate and the analog 3‐bromopyruvate in SCCVII tumor. The discrepant results between in vitro and in vivo data were attributed to biphasic oxygen dependent expression of monocarboxylate transporter‐1 in vivo. Expression of monocarboxylate transporter‐1 was enhanced in moderately hypoxic (8–15 mmHg) tumor regions but down regulated in severely hypoxic (<5 mmHg) tumor regions. These results emphasize the importance of noninvasive imaging biomarkers to confirm the action of hypoxia‐activated drugs. Magn Reson Med, 2013. © 2012 Wiley Periodicals, Inc.</abstract><cop>Hoboken</cop><pub>Wiley Subscription Services, Inc., A Wiley Company</pub><pmid>22692861</pmid><doi>10.1002/mrm.24355</doi><tpages>8</tpages><oa>free_for_read</oa></addata></record> |
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subjects | 3-bromopyruvate Animals Antineoplastic Agents - therapeutic use Biomarkers, Tumor - metabolism Carbon Radioisotopes - pharmacokinetics Carcinoma, Squamous Cell - diagnosis Carcinoma, Squamous Cell - drug therapy Carcinoma, Squamous Cell - metabolism Cell Line, Tumor Electron Spin Resonance Spectroscopy - methods EPR imaging Glycolysis - drug effects HIF-1 hyperpolarized 13C MRI Magnetic Resonance Imaging - methods MCT1 MCT1, tumor hypoxia Mice Molecular Imaging - methods Oxygen - metabolism Pyruvates - therapeutic use Pyruvic Acid - metabolism Radiopharmaceuticals - pharmacokinetics Reproducibility of Results Sensitivity and Specificity Treatment Outcome tumor hypoxia |
title | EPR oxygen imaging and hyperpolarized 13C MRI of pyruvate metabolism as noninvasive biomarkers of tumor treatment response to a glycolysis inhibitor 3-bromopyruvate |
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