Reduced Warburg effect in cancer cells undergoing autophagy: Steady- state 1H-MRS and real-time hyperpolarized 13C-MRS studies

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Lin, Gigin ^a,b   Andrejeva, Gabriela ^a   Wong Te Fong, Anne Christine ^a   Hill, Deborah K ^a   Orton, Matthew R ^a   Parkes, Harry G ^a   Koh, Dow Mu ^a   Robinson, Simon P ^a   Leach, Martin O ^a   Eykyn, Thomas R ^a,c   Chung, Yuen Li ^a  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b CHANG GUNG UNIVERSITY   (Taiwan)

^c ST THOMAS HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2 (4 HYDROXYPHENYL) 4 MORPHOLINOPYRIDO[3',2':4,5]FURO[3,2 D]PYRIMIDINE; LACTATE DEHYDROGENASE; LACTIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE; PROTEIN BAX; PYRUVIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; BAX PROTEIN, HUMAN; CARBON; FURAN DERIVATIVE; PYRIDINE DERIVATIVE; PYRIMIDINE DERIVATIVE;

AMINO ACID DEFICIENCY; ARTICLE; AUTOPHAGY; CANCER CELL; CARBON NUCLEAR MAGNETIC RESONANCE; CELL METABOLISM; CONTROLLED STUDY; ENZYME ACTIVITY; GLYCOLYSIS; HCT116 CELL LINE; HT 29 CELL LINE; HUMAN; HUMAN CELL; ONCOLOGICAL PARAMETERS; PROTON NUCLEAR MAGNETIC RESONANCE; REAL TIME HYPERPOLARIZED CARBON NUCLEAR MAGNETIC RESONANCE; STARVATION; STEADY STATE PROTON NUCLEAR MAGNETIC RESONANCE; WARBURG EFFECT; GENE SILENCING; GENETICS; ISOTOPE LABELING; METABOLISM; NEOPLASM; PATHOLOGY; TUMOR CELL LINE;

AUTOPHAGY; BCL-2-ASSOCIATED X PROTEIN; CARBON ISOTOPES; CELL LINE, TUMOR; FURANS; GENE KNOCKDOWN TECHNIQUES; HUMANS; ISOTOPE LABELING; L-LACTATE DEHYDROGENASE; LACTIC ACID; NAD; NEOPLASMS; PYRIDINES; PYRIMIDINES;

EID: 84899816551     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092645     Document Type: Article

References (36)

1. Lum JJ, Bauer DE, Kong M, Harris MH, Li C, et al. (2005) Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120:237-248. (Pubitemid 40174766)
2. Amaravadi RK, Thompson CB (2007) The roles of therapy-induced autophagy and necrosis in cancer treatment. Clin Cancer Res 13:7271-7279.
3. Mathew R, Karantza-Wadsworth V, White E (2007) Role of autophagy in cancer. Nat Rev Cancer 7:961-967. (Pubitemid 350165856)
4. Rosenfeldt MT, Ryan KM (2009) The role of autophagy in tumour development and cancer therapy. Expert Rev Mol Med 11:e36.
5. Nishida K, Kyoi S, Yamaguchi O, Sadoshima J, Otsu K (2009) The role of autophagy in the heart. Cell Death Differ 16:31-38.
6. Nedelsky NB, Todd PK, Taylor JP (2008) Autophagy and the ubiquitin-proteasome system: collaborators in neuroprotection. Biochim Biophys Acta 1782:691-699.
7. Raynaud FI, Eccles S, Clarke PA, Hayes A, Nutley B, et al. (2007) Pharmacologic characterization of a potent inhibitor of class I phosphatidylinositide 3-kinases. Cancer Res 67:5840-5850. (Pubitemid 46985018)
8. Fan QW, Cheng C, Hackett C, Feldman M, Houseman BT, et al. (2010) Akt and autophagy cooperate to promote survival of drug-resistant glioma. Sci Signal 3:ra81.
9. Kirkegaard K, Taylor MP, Jackson WT (2004) Cellular autophagy: surrender, avoidance and subversion by microorganisms. Nat Rev Microbiol 2:301-314. (Pubitemid 39490100)
10. Hanahan D,Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646-674.
11. Levine B, Klionsky DJ (2004) Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 6:463-477. (Pubitemid 38456176)
12. Jung CH, Ro SH, Cao J, Otto NM, Kim DH (2010) mTOR regulation of autophagy. FEBS Lett 584:1287-1295.
13. Kwock L, Smith JK, Castillo M, Ewend MG, Collichio F, et al. (2006) Clinical role of proton magnetic resonance spectroscopy in oncology: brain, breast, and prostate cancer. Lancet Oncol 7:859-868. (Pubitemid 44464079)
14. Day SE, Kettunen MI, Gallagher FA, Hu DE, Lerche M, et al. (2007) Detecting tumor response to treatment using hyperpolarized 13C magnetic resonance imaging and spectroscopy. Nat Med 13:1382-1387. (Pubitemid 350073590)
15. Golman K, Zandt RI, Lerche M, Pehrson R, Ardenkjaer-Larsen JH (2006) Metabolic imaging by hyperpolarized 13C magnetic resonance imaging for in vivo tumor diagnosis. Cancer Res 66:10855-10860. (Pubitemid 44876982)
16. Day SE, Kettunen MI, Cherukuri MK, Mitchell JB, Lizak MJ, et al. (2011) Detecting response of rat C6 glioma tumors to radiotherapy using hyperpolarized [1-13C]pyruvate and 13C magnetic resonance spectroscopic imaging. Magn Reson Med 65:557-563.
17. Park I, Bok R, Ozawa T, Phillips JJ, James CD, et al. (2011) Detection of early response to temozolomide treatment in brain tumors using hyperpolarized 13C MR metabolic imaging. J Magn Reson Imaging 33:1284-1290.
18. Lodi A, Woods SM, Ronen SM (2013) Treatment with the MEK inhibitor U0126 induces decreased hyperpolarized pyruvate to lactate conversion in breast, but not prostate, cancer cells. NMR Biomed 26:299-306.
19. Ward CS, Venkatesh HS, Chaumeil MM, Brandes AH, Vancriekinge M, et al. (2010) Noninvasive detection of target modulation following phosphatidylinositol 3-kinase inhibition using hyperpolarized 13C magnetic resonance spectroscopy. Cancer Res 70:1296-1305.
20. Bohndiek SE, Kettunen MI, Hu DE, Witley TH, Kennedy BW, et al. (2010) Detection of tumor response to a vascular disrupting agent by hyperpolarized 13C magnetic resonance spectroscopy. Mol Cancer Ther 9:3278-3288.
21. Rabinowitz JD, White E (2010) Autophagy and metabolism. Science 330:1344-1348.
22. Han J, Hou W, Goldstein LA, Lu C, Stolz DB, et al. (2008) Involvement of protective autophagy in TRAIL resistance of apoptosis-defective tumor cells. J Biol Chem 283:19665-19677.
23. Zhang L, Yu J, Park BH, Kinzler KW, Vogelstein B (2000) Role of BAX in the apoptotic response to anticancer agents. Science 290:989-992.
24. Board M, Humm S, Newsholme EA (1990) Maximum activities of key enzymes of glycolysis, glutaminolysis, pentose phosphate pathway and tricarboxylic acid cycle in normal, neoplastic and suppressed cells. Biochem J 265:503-509. (Pubitemid 20041995)
25. Hill DK, Jamin Y, Orton MR, Tardif N, Parkes HG, et al. (2013) (1)H NMR and hyperpolarized (1)(3)C NMR assays of pyruvate-lactate: a comparative study. NMR Biomed 26:1321-1325.
26. Tyagi RK, Azrad A, Degani H, Salomon Y (1996) Simultaneous extraction of cellular lipids and water-soluble metabolites: evaluation by NMR spectroscopy. Magn Reson Med 35:194-200. (Pubitemid 26044386)
27. Sitter B, Sonnewald U, Spraul M, Fjosne HE, Gribbestad IS (2002) High-resolution magic angle spinning MRS of breast cancer tissue. NMR Biomed 15:327-337. (Pubitemid 34960100)
28. O'Donovan TR, O'Sullivan GC, McKenna SL (2011) Induction of autophagy by drug-resistant esophageal cancer cells promotes their survival and recovery following treatment with chemotherapeutics. Autophagy 7:509-524.
29. Crowley LC, Elzinga BM, O'Sullivan GC, McKenna SL (2011) Autophagy induction by Bcr-Abl-expressing cells facilitates their recovery from a targeted or nontargeted treatment. Am J Hematol 86:38-4730.
30. Harris T, Eliyahu G, Frydman L, Degani H (2009) Kinetics of hyperpolarized 13C1-pyruvate transport and metabolism in living human breast cancer cells. Proc Natl Acad Sci U S A 106:18131-18136.
31. Christensen CE, Karlsson M, Winther JR, Jensen PR, Lerche MH (2013) Non-invasive in-cell determination of free cytosolic [NAD+]/[NADH] ratios using hyperpolarized glucose show large variations in metabolic phenotypes. J Biol Chem. 10.1074/jbc.M113.498626.
32. Santidrian AF, Matsuno-Yagi A, Ritland M, Seo BB, Le Boeuf SE, et al. (2013) Mitochondrial complex I activity and NAD+/NADH balance regulate breast cancer progression. J Clin Invest 123:1068-1081.
33. Williamson DH, Lund P, Krebs HA (1967) The redox state of free nicotinamide-adenine dinucleotide in the cytoplasm and mitochondria of rat liver. Biochem J 103:514-527.
34. Witney TH, Kettunen MI, Brindle KM (2011) Kinetic modeling of hyperpolarized 13C label exchange between pyruvate and lactate in tumor cells. J Biol Chem 286:24572-24580.
35. Hill DK, Orton MR, Mariotti E, Boult JK, Panek R, et al. (2013) Model free approach to kinetic analysis of real-time hyperpolarized 13C magnetic resonance spectroscopy data. PLoS ONE 8:e71996.
36. Houri JJ, Ogier-Denis E, De Stefanis D, Bauvg C, Baccino FM, et al. (1995) Differentiation-dependent autophagy controls the fate of newly synthesized N-linked glycoproteins in the colon adenocarcinoma HT-29 cell line. Biochem J 309(Pt 2):521-527.