2-deoxy-D-glucose suppresses the in vivo antitumor efficacy of erlotinib in head and neck squamous cell carcinoma cells

Oncology Research

Volumn 24, Issue 1, 2016, Pages 55-64

  Sobhakumari, Arya ^a   Orcutt, Kevin P ^b   Love Homan, Laurie ^b   Kowalski, Christopher E ^b   Parsons, Arlene D ^b   Michael Knudson, C ^b,c   Simons, Andrean L ^a,b,c  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

Author keywords

2 deoxy D glucose (2DG); Autophagy; Endoplasmic reticulum (ER) stress; Epidermal growth factor receptor (EGFR); Erlotinib; Head and neck squamous cell carcinoma (HNSCC)

Indexed keywords

ANTIOXIDANT; CHLOROQUINE; DEOXYGLUCOSE; ERLOTINIB; GLUCOSE; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; MANNOSE; PYRUVATE KINASE; PYRUVATE KINASE M2; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; CARRIER PROTEIN; DDIT3 PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; MEMBRANE PROTEIN; PROTEIN KINASE INHIBITOR; THYROID HORMONE; THYROID HORMONE-BINDING PROTEINS;

ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOPHAGY; CARCINOMA CELL; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; ENDOPLASMIC RETICULUM STRESS; FEMALE; GLUCOSE INTAKE; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR XENOGRAFT; ANIMAL; CARCINOMA, SQUAMOUS CELL; DRUG EFFECTS; DRUG SCREENING; ENDOPLASMIC RETICULUM; HEAD AND NECK NEOPLASMS; METABOLISM; NUDE MOUSE; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; AUTOPHAGY; CARCINOMA, SQUAMOUS CELL; CARRIER PROTEINS; CELL LINE, TUMOR; CHLOROQUINE; DEOXYGLUCOSE; ENDOPLASMIC RETICULUM; ERLOTINIB HYDROCHLORIDE; FEMALE; GLUCOSE; HEAD AND NECK NEOPLASMS; HUMANS; MEMBRANE PROTEINS; MICE; MICE, NUDE; PROTEIN KINASE INHIBITORS; RECEPTOR, EPIDERMAL GROWTH FACTOR; THYROID HORMONES; TRANSCRIPTION FACTOR CHOP; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84970960043     PISSN: 09650407     EISSN: 15553906     Source Type: Journal    
DOI: 10.3727/096504016X14586627440192     Document Type: Article

References (44)

1. Ang, K. K.; Berkey, B. A.; Tu, X.; Zhang, H. Z.; Katz, R.; Hammond, E. H.; Fu, K. K.; Milas, L. Impact of epidermal growth factor receptor expression on survival and pattern of relapse in patients with advanced head and neck carcinoma. Cancer Res. 62:7350-7356; 2002.
2. Grandis, J. R.; Tweardy, D. J. TGF-alpha and EGFR in head and neck cancer. J. Cell Biochem. Suppl. 17F:188-191; 1993.
3. Loeffler-Ragg, J.; Schwentner, I.; Sprinzl, G. M.; Zwierzina, H. EGFR inhibition as a therapy for head and neck squamous cell carcinoma. Expert Opin. Investig. Drugs 17:1517-1531; 2008.
4. Lynch, T. J.; Bell, D. W.; Sordella, R.; Gurubhagavatula, S.; Okimoto, R. A.; Brannigan, B. W.; Harris, P. L.; Haserlat, S. M.; Supko, J. G.; Haluska, F. G.; Louis, D. N.; Christiani, D. C.; Settleman, J.; Haber, D. A. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N. Engl. J. Med. 350:2129-2139; 2004.
5. Sequist, L. V.; Bell, D. W.; Lynch, T. J.; Haber, D. A. Molecular predictors of response to epidermal growth factor receptor antagonists in non-small-cell lung cancer. J. Clin. Oncol. 25:587-595; 2007.
6. Vermorken, J. B.; Trigo, J.; Hitt, R.; Koralewski, P.; Diaz- Rubio, E.; Rolland, F.; Knecht, R.; Amellal, N.; Schueler, A.; Baselga, J. Open-label, uncontrolled, multicenter phase II study to evaluate the efficacy and toxicity of cetuximab as a single agent in patients with recurrent and/or metastatic squamous cell carcinoma of the head and neck who failed to respond to platinum-based therapy. J. Clin. Oncol. 25:2171-2177; 2007.
7. Piperdi, B.; Perez-Soler, R. Role of erlotinib in the treatment of non-small cell lung cancer: Clinical outcomes in wild-type epidermal growth factor receptor patients. Drugs 72(Suppl. 1):11-19; 2012.
8. Sandulache, V. C.; Ow, T. J.; Pickering, C. R.; Frederick, M. J.; Zhou, G.; Fokt, I.; Davis-Malesevich, M.; Priebe, W.; Myers, J. N. Glucose, not glutamine, is the dominant energy source required for proliferation and survival of head and neck squamous carcinoma cells. Cancer 117:2926-2938; 2011.
9. Makinoshima, H.; Takita, M.; Saruwatari, K.; Umemura, S.; Obata, Y.; Ishii, G.; Matsumoto, S.; Sugiyama, E.; Ochiai, A.; Abe, R.; Goto, K.; Esumi, H.; Tsuchihara, K. Signaling through the phosphatidylinositol 3-kinase (PI3K)/mammalian target of rapamycin (mTOR) axis is responsible for aerobic glycolysis mediated by glucose transporter in epidermal growth factor receptor (EGFR)-mutated lung adenocarcinoma. J. Biol. Chem. 290:17495-17504; 2015.
10. Ren, J.; Bollu, L. R.; Su, F.; Gao, G.; Xu, L.; Huang, W. C.; Hung, M. C.; Weihua, Z. EGFR-SGLT1 interaction does not respond to EGFR modulators, but inhibition of SGLT1 sensitizes prostate cancer cells to EGFR tyrosine kinase inhibitors. Prostate 73:1453-1461; 2013.
11. Weihua, Z.; Tsan, R.; Huang, W. C.; Wu, Q.; Chiu, C. H.; Fidler, I. J.; Hung, M. C. Survival of cancer cells is maintained by EGFR independent of its kinase activity. Cancer Cell 13:385-393; 2008.
12. Camporeale, A.; Demaria, M.; Monteleone, E.; Giorgi, C.; Wieckowski, M. R.; Pinton, P.; Poli, V. STAT3 activities and energy metabolism: Dangerous liaisons. Cancers (Basel) 6:1579-1596; 2014.
13. Demaria, M.; Camporeale, A.; Poli, V. STAT3 and metabolism: How many ways to use a single molecule? Int. J. Cancer 135:1997-2003; 2014.
14. Demaria, M.; Poli, V. PKM2, STAT3 and HIF-1alpha: The Warburg's vicious circle. Jakstat 1:194-196; 2012.
15. Demaria, M.; Giorgi, C.; Lebiedzinska, M.; Esposito, G.; D'Angeli, L.; Bartoli, A.; Gough, D. J.; Turkson, J.; Levy, D. E.; Watson, C. J.; Wieckowski, M. R.; Provero, P.; Pinton, P.; Poli, V. A STAT3-mediated metabolic switch is involved in tumour transformation and STAT3 addiction. Aging (Albany NY) 2:823-842; 2010.
16. Yang, W.; Xia, Y.; Cao, Y.; Zheng, Y.; Bu, W.; Zhang, L.; You, M. J.; Koh, M. Y.; Cote, G.; Aldape, K.; Li, Y.; Verma, I. M.; Chiao, P. J.; Lu, Z. EGFR-induced and PKCepsilon monoubiquitylation-dependent NF-kappaB activation upregulates PKM2 expression and promotes tumorigenesis. Mol. Cell 48:771-784; 2012.
17. De Rosa, V.; Iommelli, F.; Monti, M.; Fonti, R.; Votta, G.; Stoppelli, M. P.; Del Vecchio, S. Reversal of Warburg effect and reactivation of oxidative phosphorylation by differential inhibition of EGFR signaling pathways in non-small cell lung cancer. Clin. Cancer Res. 21:5110-5120; 2015.
18. Aykin-Burns, N.; Ahmad, I. M.; Zhu, Y.; Oberley, L. W.; Spitz, D. R. Increased levels of superoxide and H2O2 mediate the differential susceptibility of cancer cells versus normal cells to glucose deprivation. Biochem. J. 418:29-37; 2009.
19. Simons, A. L.; Fath, M. A.; Mattson, D. M.; Smith, B. J.; Walsh, S. A.; Graham, M. M.; Hichwa, R. D.; Buatti, J. M.; Dornfeld, K.; Spitz, D. R. Enhanced response of human head and neck cancer xenograft tumors to cisplatin combined with 2-deoxy-D-glucose correlates with increased 18FFDG uptake as determined by PET imaging. Int. J. Radiat. Oncol. Biol. Phys. 69:1222-1230; 2007.
20. Simons, A. L.; Ahmad, I. M.; Mattson, D. M.; Dornfeld, K. J.; Spitz, D. R. 2-Deoxy-D-glucose combined with cisplatin enhances cytotoxicity via metabolic oxidative stress in human head and neck cancer cells. Cancer Res. 67:3364- 3370; 2007.
21. Weichselbaum, R. R.; Dahlberg, W.; Beckett, M.; Karrison, T.; Miller, D.; Clark, J.; Ervin, T. J. Radiation-resistant and repair-proficient human tumor cells may be associated with radiotherapy failure in head- and neck-cancer patients. Proc. Natl. Acad. Sci. USA 83:2684-2688; 1986.
22. Spitz, D. R.; Malcolm, R. R.; Roberts, R. J. Cytotoxicity and metabolism of 4-hydroxy-2-nonenal and 2-nonenal in H2O2-resistant cell lines. Do aldehydic by-products of lipid peroxidation contribute to oxidative stress? Biochem. J. 267:453-459; 1990.
23. Hidalgo, M.; Siu, L. L.; Nemunaitis, J.; Rizzo, J.; Hammond, L. A.; Takimoto, C.; Eckhardt, S. G.; Tolcher, A.; Britten, C. D.; Denis, L.; Ferrante, K.; Von Hoff, D. D.; Silberman, S.; Rowinsky, E. K. Phase I and pharmacologic study of OSI- 774, an epidermal growth factor receptor tyrosine kinase inhibitor, in patients with advanced solid malignancies. J. Clin. Oncol. 19:3267-3279; 2001.
24. Sobhakumari, A.; Schickling, B. M.; Love-Homan, L.; Raeburn, A.; Fletcher, E. V.; Case, A. J.; Domann, F. E.; Miller, F. J.; Jr.; Simons, A. L. NOX4 mediates cytoprotective autophagy induced by the EGFR inhibitor erlotinib in head and neck cancer cells. Toxicol. Appl. Pharmacol. 272:736-745; 2013.
25. Mohanti, B. K.; Rath, G. K.; Anantha, N.; Kannan, V.; Das, B. S.; Chandramouli, B. A.; Banerjee, A. K.; Das, S.; Jena, A.; Ravichandran, R.; Sahi, U. P.; Kumar, R.; Kapoor, N.; Kalia, V. K.; Dwarakanath, B. S.; Jain, V. Improving cancer radiotherapy with 2-deoxy-D-glucose: Phase I/II clinical trials on human cerebral gliomas. Int. J. Radiat. Oncol. Biol. Phys. 35:103-111; 1996.
26. Xi, H.; Barredo, J. C.; Merchan, J. R.; Lampidis, T. J. Endoplasmic reticulum stress induced by 2-deoxyglucose but not glucose starvation activates AMPK through CaMKKbeta leading to autophagy. Biochem. Pharmacol. 85:1463-1477; 2013.
27. Xi, H.; Kurtoglu, M.; Liu, H.; Wangpaichitr, M.; You, M.; Liu, X.; Savaraj, N.; Lampidis, T. J. 2-Deoxy-D-glucose activates autophagy via endoplasmic reticulum stress rather than ATP depletion. Cancer Chemother. Pharmacol. 67:899-910; 2011.
28. Zagorodna, O.; Martin, S. M.; Rutkowski, D. T.; Kuwana, T.; Spitz, D. R.; Knudson, C. M. 2-Deoxyglucose-induced toxicity is regulated by Bcl-2 family members and is enhanced by antagonizing Bcl-2 in lymphoma cell lines. Oncogene 31:2738-2749; 2012.
29. Contessa, J. N.; Bhojani, M. S.; Freeze, H. H.; Rehemtulla, A.; Lawrence, T. S. Inhibition of N-linked glycosylation disrupts receptor tyrosine kinase signaling in tumor cells. Cancer Res. 68:3803-3809; 2008.
30. Yoon, S. J.; Nakayama, K.; Hikita, T.; Handa, K.; Hakomori, S. I. Epidermal growth factor receptor tyrosine kinase is modulated by GM3 interaction with N-linked GlcNAc termini of the receptor. Proc. Natl. Acad. Sci. USA 103:18987-18991; 2006.
31. Schiavi, A.; Maglioni, S.; Palikaras, K.; Shaik, A.; Strappazzon, F.; Brinkmann, V.; Torgovnick, A.; Castelein, N.; De Henau, S.; Braeckman, B. P.; Cecconi, F.; Tavernarakis, N.; Ventura, N. Iron-starvation-induced mitophagy mediates lifespan extension upon mitochondrial stress in C. elegans. Curr. Biol. 25:1810-1822; 2015.
32. Guan, X.; Qian, Y.; Shen, Y.; Zhang, L.; Du, Y.; Dai, H.; Qian, J.; Yan, Y. Autophagy protects renal tubular cells against ischemia/reperfusion injury in a time-dependent manner. Cell. Physiol. Biochem. 36:285-298; 2015.
33. Shen, Y.; Yang, J.; Zhao, J.; Xiao, C.; Xu, C.; Xiang, Y. The switch from ER stress-induced apoptosis to autophagy via ROS-mediated JNK/p62 signals: A survival mechanism in methotrexate-resistant choriocarcinoma cells. Exp. Cell Res. 334:207-218; 2015.
34. Jeon, J. Y.; Kim, S. W.; Park, K. C.; Yun, M. The bifunctional autophagic flux by 2-deoxyglucose to control survival or growth of prostate cancer cells. BMC Cancer 15:623; 2015.
35. Kim, S. E.; Park, H. J.; Jeong, H. K.; Kim, M. J.; Kim, M.; Bae, O. N.; Baek, S. H. Autophagy sustains the survival of human pancreatic cancer PANC-1 cells under extreme nutrient deprivation conditions. Biochem. Biophys. Res. Commun. 463:205-210; 2015.
36. Suzuki, M.; O'Dea, J. D.; Suzuki, T.; Agar, N. S. 2-Deoxyglucose as a substrate for glutathione regeneration in human and ruminant red blood cells. Comp. Biochem. Physiol. B 75:195-197; 1983.
37. Ahmad, I. M.; Aykin-Burns, N.; Sim, J. E.; Walsh, S. A.; Higashikubo, R.; Buettner, G. R.; Venkataraman, S.; Mackey, M. A.; Flanagan, S. W.; Oberley, L. W.; Spitz, D. R. Mitochondrial O2.- and H2O2 mediate glucose deprivation- induced stress in human cancer cells. J. Biol. Chem. 280:4254-4263; 2005.
38. Coleman, M. C.; Asbury, C. R.; Daniels, D.; Du, J.; Aykin- Burns, N.; Smith, B. J.; Li, L.; Spitz, D. R.; Cullen, J. J. 2-Deoxy-D-glucose causes cytotoxicity, oxidative stress, and radiosensitization in pancreatic cancer. Free Radic. Biol. Med. 44:322-331; 2008.
39. Hadzic, T.; Aykin-Burns, N.; Zhu, Y.; Coleman, M. C.; Leick, K.; Jacobson, G. M.; Spitz, D. R. Paclitaxel combined with inhibitors of glucose and hydroperoxide metabolism enhances breast cancer cell killing via H2O2-mediated oxidative stress. Free Radic. Biol. Med. 48:1024-1033; 2010.
40. Fath, M. A.; Diers, A. R.; Aykin-Burns, N.; Simons, A. L.; Hua, L.; Spitz, D. R. Mitochondrial electron transport chain blockers enhance 2-deoxy-D-glucose induced oxidative stress and cell killing in human colon carcinoma cells. Cancer Biol. Ther. 8:1228-1236; 2009.
41. Rutkowski, D. T.; Kaufman, R. J. A trip to the ER: Coping with stress. Trends Cell Biol. 14:20-28; 2004.
42. Ling, Y. H.; Li, T.; Perez-Soler, R.; Haigentz, M.; Jr. Activation of ER stress and inhibition of EGFR N-glycosylation by tunicamycin enhances susceptibility of human non-small cell lung cancer cells to erlotinib. Cancer Chemother. Pharmacol. 64:539-548; 2009.
43. Fernandes, H.; Cohen, S.; Bishayee, S. Glycosylation-induced conformational modification positively regulates receptorreceptor association: A study with an aberrant epidermal growth factor receptor (EGFRvIII/DeltaEGFR) expressed in cancer cells. J. Biol. Chem. 276:5375-5383; 2001.
44. Kim, S. M.; Yun, M. R.; Hong, Y. K.; Solca, F.; Kim, J. H.; Kim, H. J.; Cho, B. C. Glycolysis inhibition sensitizes nonsmall cell lung cancer with T790M mutation to irreversible EGFR inhibitors via translational suppression of Mcl-1 by AMPK activation. Mol. Cancer Ther. 12:2145-2156; 2013.