Cannabinoids inhibit energetic metabolism and induce AMPK-dependent autophagy in pancreatic cancer cells

Cell Death and Disease

Volumn 4, Issue 6, 2013, Pages

  Dando, I ^a   Donadelli, M ^a   Costanzo, C ^a   Dalla Pozza, E ^a   D'Alessandro, A ^b   Zolla, L ^b   Palmieri, M ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b UNIVERSITY OF TUSCIA   (Italy)

Author keywords

AMP ATP; AMPK; autophagy; cannabinoids; metabolism

Indexed keywords

1 (2,3 DICHLOROBENZOYL) 5 METHOXY 2 METHYL 3 (2 MORPHOLINOETHYL)INDOLE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; ANTINEOPLASTIC AGENT; ARACHIDONOYL CYCLOPROPYLAMIDE; CANNABINOID 1 RECEPTOR AGONIST; GLUTAMINE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MYC PROTEIN; PROTEIN KINASE B; PYRUVATE KINASE; PYRUVATE KINASE M2; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOPHAGY; CANCER CELL CULTURE; CANCER INHIBITION; CELL NUCLEUS; CITRIC ACID CYCLE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; ENERGY METABOLISM; ENZYME ACTIVATION; ENZYME LOCALIZATION; GLYCOLYSIS; HUMAN; HUMAN CELL; METABOLIC INHIBITION; METABOLOMICS; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; RESPIRATORY CHAIN;

EID: 84879666294     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.151     Document Type: Article

References (43)

1. Hermanson DJ, Cannabinoids Marnett LJ. endocannabinoids, and cancer. Cancer Metastasis Rev 2011; 30: 599-612.
2. Pisanti S, Bifulco M. Endocannabinoid system modulation in cancer biology and therapy. Pharmacol Res 2009; 60: 107-116.
3. Pisanti S, Malfitano AM, Grimaldi C, Santoro A, Gazzerro P, Laezza C et al. Use of cannabinoid receptor agonists in cancer therapy as palliative and curative agents. Best Pract Res Clin Endocrinol Metab 2009; 23: 117-131.
4. Velasco G, Carracedo A, Blazquez C, Lorente M, Aguado T, Haro A et al. Cannabinoids and gliomas. Mol Neurobiol 2007; 36: 60-67.
5. Qamri Z, Preet A, Nasser MW, Bass CE, Leone G, Barsky SH et al. Synthetic cannabinoid receptor agonists inhibit tumor growth and metastasis of breast cancer. Mol Cancer Ther 2009; 8: 3117-3129.
6. Sarfaraz S, Afaq F, Adhami VM, Mukhtar H. Cannabinoid receptor as a novel target for the treatment of prostate cancer. Cancer Res 2005; 65: 1635-1641.
7. Proto MC, Gazzerro P, Di Croce L, Santoro A, Malfitano AM, Pisanti S et al. Interaction of endocannabinoid system and steroid hormones in the control of colon cancer cell growth. J Cell Physiol 2012; 227: 250-258.
8. Guindon J, Hohmann AG. The endocannabinoid system and cancer: therapeutic implication. Br J Pharmacol 2011; 163: 1447-1463.
9. De Petrocellis L, Melck D, Palmisano A, Bisogno T, Laezza C, Bifulco M et al. The endogenous cannabinoid anandamide inhibits human breast cancer cell proliferation. Proc Natl Acad Sci USA 1998; 95: 8375-8380.
10. Donadelli M, Dando I, Zaniboni T, Costanzo C, Dalla Pozza E, Scupoli MT et al. Gemcitabine/cannabinoid combination triggers autophagy in pancreatic cancer cells through a ROS-mediated mechanism. Cell Death Dis 2011; 2: e152.
11. Salazar M, Carracedo A, Salanueva IJ, Hernandez-Tiedra S, Lorente M, Egia A et al. Cannabinoid action induces autophagy-mediated cell death through stimulation of ER stress in human glioma cells. J Clin Invest 2009; 119: 1359-1372.
12. Yu L, McPhee CK, Zheng L, Mardones GA, Rong Y, Peng J et al. Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature 2010; 465: 942-946.
13. Levine B. Cell biology: autophagy and cancer. Nature 2007; 446: 745-747.
14. Vara D, Salazar M, Olea-Herrero N, Guzman M, Velasco G, Diaz-Laviada I. Anti-tumoral action of cannabinoids on hepatocellular carcinoma: role of AMPK-dependent activation of autophagy. Cell Death Differ 2011; 18: 1099-1111.
15. Hardie DG. AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev 2011; 25: 1895-1908.
16. Hawley SA, Boudeau J, Reid JL, Mustard KJ, Udd L, Makela TP et al. Complexes between the LKB1 tumor suppressor, STRAD alpha/beta and MO25 alpha/beta are upstream kinases in the AMP-activated protein kinase cascade. J Biol 2003; 2: 28.
17. Shaw RJ, Kosmatka M, Bardeesy N, Hurley RL, Witters LA, DePinho RA et al. The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc Natl Acad Sci USA 2004; 101: 3329-3335.
18. Woods A, Johnstone SR, Dickerson K, Leiper FC, Fryer LG, Neumann D et al. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol 2003; 13: 2004-2008.
19. Sakamoto K, Goransson O, Hardie DG, Alessi DR. Activity of LKB1 and AMPK-related kinases in skeletal muscle: effects of contraction, phenformin, and AICAR. Am J Physiol Endocrinol Metab 2004; 287: E310-E317.
20. Hawley SA, Pan DA, Mustard KJ, Ross L, Bain J, Edelman AM et al. Calmodulindependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab 2005; 2: 9-19.
21. Hurley RL, Anderson KA, Franzone JM, Kemp BE, Means AR, Witters LA. The Ca2\+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases. J Biol Chem 2005; 280: 29060-29066.
22. Woods A, Dickerson K, Heath R, Hong SP, Momcilovic M, Johnstone SR et al. Ca2\+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab 2005; 2: 21-33.
23. Fogarty S, Hawley SA, Green KA, Saner N, Mustard KJ, Hardie DG. Calmodulindependent protein kinase kinase-beta activates AMPK without forming a stable complex: synergistic effects of Ca2\+ and AMP. Biochem J 2010; 426: 109-118.
24. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J et al. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 2001; 108: 1167-1174.
25. Colell A, Ricci JE, Tait S, Milasta S, Maurer U, Bouchier-Hayes L et al. GAPDH and autophagy preserve survival after apoptotic cytochrome c release in the absence of caspase activation. Cell 2007; 129: 983-997.
26. Kroemer G, Pouyssegur J. Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell 2008; 13: 472-482.
27. Wise DR, DeBerardinis RJ, Mancuso A, Sayed N, Zhang XY, Pfeiffer HK et al. Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc Natl Acad Sci USA 2008; 105: 18782-18787.
28. Castellino RC, Durden DL. Mechanisms of disease: the PI3K-Akt-PTEN signaling node-an intercept point for the control of angiogenesis in brain tumors. Nat Clin Pract Neurol 2007; 3: 682-693.
29. Fleming A, Noda T, Yoshimori T, Rubinsztein DC. Chemical modulators of autophagy as biological probes and potential therapeutics. Nat Chem Biol 2011; 7: 9-17.
30. Wang S, Song P, Zou MH. AMP-activated protein kinase, stress responses and cardiovascular diseases. Clin Sci (Lond) 2012; 122: 555-573.
31. Lamberts RR, Onderwater G, Hamdani N, Vreden MJ, Steenhuisen J, Eringa EC et al. Reactive oxygen species-induced stimulation of 5'AMP-activated protein kinase mediates sevoflurane-induced cardioprotection. Circulation 2009; 120: S10-S15.
32. Shrivastava A, Kuzontkoski PM, Groopman JE, Prasad A. Cannabidiol induces programmed cell death in breast cancer cells by coordinating the cross-talk between apoptosis and autophagy. Mol Cancer Ther 2011; 10: 1161-1172.
33. Murray J, Taylor SW, Zhang B, Ghosh SS, Capaldi RA. Oxidative damage to mitochondrial complex I due to peroxynitrite: identification of reactive tyrosines by mass spectrometry. J Biol Chem 2003; 278: 37223-37230.
34. Colell A, Green DR, Ricci JE. Novel roles for GAPDH in cell death and carcinogenesis. Cell Death Differ 2009; 16: 1573-1581.
35. Dando I, Fiorini C, Pozza ED, Padroni C, Costanzo C, Palmieri M et al. UCP2 inhibition triggers ROS-dependent nuclear translocation of GAPDH and autophagic cell death in pancreatic adenocarcinoma cells. Biochim Biophys Acta 2013; 1833: 672-679.
36. Kwon HJ, Rhim JH, Jang IS, Kim GE, Park SC, Yeo EJ. Activation of AMP-activated protein kinase stimulates the nuclear localization of glyceraldehyde 3-phosphate dehydrogenase in human diploid fibroblasts. Exp Mol Med 2010; 42: 254-269.
37. Cairns RA, Harris IS, Mak TW. Regulation of cancer cell metabolism. Nat Rev Cancer 2011; 11: 85-95.
38. Hitosugi T, Kang S, Vander Heiden MG, Chung TW, Elf S, Lythgoe K et al. Tyrosine phosphorylation inhibits PKM2 to promote the Warburg effect and tumor growth. Sci Signal 2009; 2: ra73.
39. David CJ, Chen M, Assanah M, Canoll P, Manley JL. HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer. Nature 2010; 463: 364-368.
40. Aquila S, Guido C, Santoro A, Perrotta I, Laezza C, Bifulco M et al. Human sperm anatomy: ultrastructural localization of the cannabinoid1 receptor and a potential role of anandamide in sperm survival and acrosome reaction. Anat Rec (Hoboken) 2010; 293: 298-309.
41. D'Alessandro A, Gevi F, Zolla L. A robust high resolution reversed-phase HPLC strategy to investigate various metabolic species in different biological models. Mol Biosyst 2011; 7: 1024-1032.
42. Sana TR, Waddell K, Fischer SM. A sample extraction and chromatographic strategy for increasing LC/MS detection coverage of the erythrocyte metabolome. J Chromatogr B Analyt Technol Biomed Life Sci 2008; 871: 314-321.
43. Christofk HR, Vander Heiden MG, Wu N, Asara JM, Cantley LC. Pyruvate kinase M2 is a phosphotyrosine-binding protein. Nature 2008; 452: 181-186.