Disruption of Glycogen Utilization Markedly Improves the Efficacy of Carboplatin against Preclinical Models of Clear Cell Ovarian Carcinoma

High stage and recurrent ovarian clear cell carcinoma (OCC) are associated with poor prognosis and resistance to chemotherapy. A distinguishing histological feature of OCC is abundant cytoplasmic stores of glucose, in the form of glycogen, that can be mobilized for cellular metabolism. Here, we repo...

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Published inCancers Vol. 12; no. 4; p. 869
Main Authors Khan, Tashbib, He, Yaowu, Kryza, Thomas, Harrington, Brittney S, Gunter, Jennifer H, Sullivan, Mitchell A, Cuda, Tahleesa, Rogers, Rebecca, Davies, Claire M, Broomfield, Amy, Gough, Madeline, Wu, Andy C, McGann, Thomas, Weroha, S John, Haluska, Paul, Forbes, Josephine M, Armes, Jane E, Barry, Sinead C, Coward, Jermaine I, Jagasia, Nisha, Chetty, Naven, Snell, Cameron E, Lourie, Rohan, Perrin, Lewis C, Hooper, John D
Format Journal Article
LanguageEnglish
Published Switzerland MDPI AG 03.04.2020
MDPI
Subjects
Acidification
Animal models
Cancer therapies
Carboplatin
Cell culture
Chemotherapy
Clinical trials
Glucose
Glycogen
Medical prognosis
Metabolism
Ovarian cancer
Ovarian carcinoma
Patients
Xenografts
2DG
clear cell ovarian cancer
glycogen
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Abstract High stage and recurrent ovarian clear cell carcinoma (OCC) are associated with poor prognosis and resistance to chemotherapy. A distinguishing histological feature of OCC is abundant cytoplasmic stores of glucose, in the form of glycogen, that can be mobilized for cellular metabolism. Here, we report the effect on preclinical models of OCC of disrupting glycogen utilization using the glucose analogue 2-deoxy-D-glucose (2DG). At concentrations significantly lower than previously reported for other cancers, 2DG markedly improves the efficacy in vitro of carboplatin chemotherapy against chemo-sensitive TOV21G and chemo-resistant OVTOKO OCC cell lines, and this is accompanied by the depletion of glycogen. Of note, 2DG doses-of more than 10-fold lower than previously reported for other cancers-significantly improve the efficacy of carboplatin against cell line and patient-derived xenograft models in mice that mimic the chemo-responsiveness of OCC. These findings are encouraging, in that 2DG doses, which are substantially lower than previously reported to cause adverse events in cancer patients, can safely and significantly improve the efficacy of carboplatin against OCC. Our results thus justify clinical trials to evaluate whether low dose 2DG improves the efficacy of carboplatin in OCC patients.
AbstractList High stage and recurrent ovarian clear cell carcinoma (OCC) are associated with poor prognosis and resistance to chemotherapy. A distinguishing histological feature of OCC is abundant cytoplasmic stores of glucose, in the form of glycogen, that can be mobilized for cellular metabolism. Here, we report the effect on preclinical models of OCC of disrupting glycogen utilization using the glucose analogue 2-deoxy-D-glucose (2DG). At concentrations significantly lower than previously reported for other cancers, 2DG markedly improves the efficacy in vitro of carboplatin chemotherapy against chemo-sensitive TOV21G and chemo-resistant OVTOKO OCC cell lines, and this is accompanied by the depletion of glycogen. Of note, 2DG doses-of more than 10-fold lower than previously reported for other cancers-significantly improve the efficacy of carboplatin against cell line and patient-derived xenograft models in mice that mimic the chemo-responsiveness of OCC. These findings are encouraging, in that 2DG doses, which are substantially lower than previously reported to cause adverse events in cancer patients, can safely and significantly improve the efficacy of carboplatin against OCC. Our results thus justify clinical trials to evaluate whether low dose 2DG improves the efficacy of carboplatin in OCC patients.
Author Haluska, Paul
McGann, Thomas
Gunter, Jennifer H
Rogers, Rebecca
Chetty, Naven
Kryza, Thomas
Armes, Jane E
Forbes, Josephine M
Barry, Sinead C
Cuda, Tahleesa
Perrin, Lewis C
He, Yaowu
Broomfield, Amy
Wu, Andy C
Weroha, S John
Jagasia, Nisha
Davies, Claire M
Sullivan, Mitchell A
Harrington, Brittney S
Khan, Tashbib
Gough, Madeline
Coward, Jermaine I
Lourie, Rohan
Snell, Cameron E
Hooper, John D
AuthorAffiliation 5 Bristol-Myers Squibb, Princeton, NJ 08540, USA
3 Mater Brisbane Hospital, Mater Health Services, South Brisbane, QLD 4101, Australia; amy.broomfield@health.qld.gov.au (A.B.); Madeline.Gough@mater.org.au (M.G.); Nisha.Jagasia@mater.org.au (N.J.); Naven.Chetty@mater.org.au (N.C.)
6 ICON Cancer Care, South Brisbane, QLD 4101, Australia
4 Department of Medical Oncology, Mayo Clinic, Rochester, MN 55905, USA; weroha.saravut@mayo.edu (S.J.W.); paul.haluska@bms.com (P.H.)
1 Mater Research Institute, The University of Queensland, Translational Research Institute, Woolloongabba, QLD 4102, Australia; tashbib.khan@uq.net.au (T.K.); yaowu.he@mater.uq.edu.au (Y.H.); thomas.kryza@mater.uq.edu.au (T.K.); brittneyharr@gmail.com (B.S.H.); mitchell.sullivan@mater.uq.edu.au (M.A.S.); tahleesa.cuda@gmail.com (T.C.); rebecca.rogers@mater.uq.edu.au (R.R.); TR-ANZGOG@anzgog.org.au (C.M.D.); andy.wu@tri.edu.au (A.C.W.); thomas.p.mcgann95@gmail.com (T.M.); josephine.forbes@mater.uq.edu.au (J.M.F.); jane.armes@he
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– name: 2 Australian Prostate Cancer Research Centre-Queensland, Institute of Health and Biomedical Innovation, School of Biomedical Sciences, Faculty of Health, Queensland University of Technology, Translational Research Institute, Brisbane, QLD 4102, Australia; jennifer.gunter@qut.edu.au
– name: 1 Mater Research Institute, The University of Queensland, Translational Research Institute, Woolloongabba, QLD 4102, Australia; tashbib.khan@uq.net.au (T.K.); yaowu.he@mater.uq.edu.au (Y.H.); thomas.kryza@mater.uq.edu.au (T.K.); brittneyharr@gmail.com (B.S.H.); mitchell.sullivan@mater.uq.edu.au (M.A.S.); tahleesa.cuda@gmail.com (T.C.); rebecca.rogers@mater.uq.edu.au (R.R.); TR-ANZGOG@anzgog.org.au (C.M.D.); andy.wu@tri.edu.au (A.C.W.); thomas.p.mcgann95@gmail.com (T.M.); josephine.forbes@mater.uq.edu.au (J.M.F.); jane.armes@health.qld.gov.au (J.E.A.); sineadcbarry@gmail.com (S.C.B.); jim.coward@gmail.com (J.I.C.); Cameron.Snell@mater.org.au (C.E.S.); Rohan.Lourie@mater.org.au (R.L.); lewisperrin@mc.mater.org.au (L.C.P.)
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– name: 4 Department of Medical Oncology, Mayo Clinic, Rochester, MN 55905, USA; weroha.saravut@mayo.edu (S.J.W.); paul.haluska@bms.com (P.H.)
– name: 3 Mater Brisbane Hospital, Mater Health Services, South Brisbane, QLD 4101, Australia; amy.broomfield@health.qld.gov.au (A.B.); Madeline.Gough@mater.org.au (M.G.); Nisha.Jagasia@mater.org.au (N.J.); Naven.Chetty@mater.org.au (N.C.)
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  givenname: Andy C
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  surname: Wu
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  surname: Hooper
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  organization: Mater Research Institute, The University of Queensland, Translational Research Institute, Woolloongabba, QLD 4102, Australia
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32260077$$D View this record in MEDLINE/PubMed
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Keywords 2DG
clear cell ovarian cancer
glycogen
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Snippet High stage and recurrent ovarian clear cell carcinoma (OCC) are associated with poor prognosis and resistance to chemotherapy. A distinguishing histological...
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SubjectTerms Acidification
Animal models
Cancer therapies
Carboplatin
Cell culture
Chemotherapy
Clinical trials
Glucose
Glycogen
Medical prognosis
Metabolism
Ovarian cancer
Ovarian carcinoma
Patients
Xenografts
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Title Disruption of Glycogen Utilization Markedly Improves the Efficacy of Carboplatin against Preclinical Models of Clear Cell Ovarian Carcinoma
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Volume 12
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