PTEN deficiency and mutant p53 confer glucose-addiction to thyroid cancer cells: Impact of glucose depletion on cell proliferation, cell survival, autophagy and cell migration

Genes and Cancer

Volumn 5, Issue 7-8, 2014, Pages 226-239

  Morani, Federica ^a   Phadngam, Suratchanee ^a   Follo, Carlo ^a   Titone, Rossella ^a   Thongrakard, Visa ^a,b   Galetto, Alessandra ^a   Alabiso, Oscar ^a   Isidoro, Ciro ^a  

^a UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^b CHULALONGKORN UNIVERSITY   (Thailand)

Author keywords

Autophagy; Glucose; Metabolic stress; P53; PTEN; Warburg effect

Indexed keywords

GLUCOSE TRANSPORTER 1; MUTANT PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P53;

ARTICLE; AUTOPHAGY; CELL CYCLE ASSAY; CELL DEATH; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOFLUOROMETRY; DENSITOMETRY; GENE SILENCING; GENETIC TRANSFECTION; GLUCOSE TRANSPORT; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; PLASMID; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; RNA INTERFERENCE; STARVATION; THYROID CANCER; WESTERN BLOTTING; WOUND HEALING;

EID: 84921350759     PISSN: 19476019     EISSN: 19476027     Source Type: Journal    
DOI: None     Document Type: Article

References (55)

1. Koppenol WH, Bounds PL, Dang CV. Otto Warburg's contributions to current concepts of cancer metabolism. Nature Reviews Cancer. 2011;11:325-37.
2. Newsholme EA, Crabtree B, Ardawi MS. The role of high rates of glycolysis and glutamine utilization in rapidly dividing cells. Bioscience Reports. 1985;5:393-400.
3. Ostergaard L, Tietze A, Nielsen T, et al. The Relationship between Tumor Blood Flow, Angiogenesis, Tumor Hypoxia, and Aerobic Glycolysis. Cancer Research. 2013;73:5618-24.
4. Lock R, Roy S, Kenific CM, et al. Autophagy facilitates glycolysis during Ras-mediated oncogenic transformation. Mol Biol Cell. 2011;22:165-78.
5. Fung C, Lock R, Gao S, Salas E, Debnath J. Induction of autophagy during extracellular matrix detachment promotes cell survival. Mol Biol Cell. 2008;19:797-806.
6. Akalay I, Janji B, Hasmim M, et al. Epithelial-to-mesenchymal transition and autophagy induction in breast carcinoma promote escape from T-cell-mediated lysis. Cancer Res. 2013;73:2418-27.
7. Dong C, Yuan T, Wu Y, et al. Loss of FBP1 by Snail- mediated repression provides metabolic advantages in basal-like breast cancer. Cancer Cell. 2013;23:316-31.
8. Garcia-Cao I, Song MS, Hobbs RM, et al. Systemic elevation of PTEN induces a tumor-suppressive metabolic state. Cell. 2012;149:49-62.
9. Liu J, Zhang C, Hu W, Feng Z. Tumor suppressor p53 and its mutants in cancer metabolism. Cancer Lett. 2013. pii: S0304-3835(13)00863-X. doi: 10.1016/j.canlet.2013.12.025.
10. Berkers CR, Maddocks OD, Cheung EC, Mor I, Vousden KH. Metabolic regulation by p53 family members. Cell Metab. 2013;18:617-33.
11. Maiuri MC, Galluzzi L, Morselli E, Kepp O, Malik SA, Kroemer G. Autophagy regulation by p53. Curr Opin Cell Biol. 2010;22:181-5.
12. Muller PA, Caswell PT, Doyle B, et al. Mutant p53 drives invasion by promoting integrin recycling. Cell. 2009;139:1327-41.
13. Morton JP, Timpson P, Karim SA, et al. Mutant p53 drives metastasis and overcomes growth arrest/senescence in pancreatic cancer. Proc Natl Acad Sci U S A. 2010;107:246-51.
14. Saiselet M, Floor S, Tarabichi M, et al. Thyroid cancer cell lines: an overview. Frontiers in Endocrinology (Lausanne). 2012;3:133.
15. Weng LP, Gimm O, Kum JB, et al. Transient ectopic expression of PTEN in thyroid cancer cell lines induces cell cycle arrest and cell type-dependent cell death. Human molecular genetics. 2001;10:251-8.
16. Kroemer G, Marino G, Levine B. Autophagy and the integrated stress response. Mol Cell. 2010;40:280-93.
17. Morani F, Titone R, Pagano L, et al. Autophagy and thyroid carcinogenesis: genetic and epigenetic links. Endocr Relat Cancer. 2013;21:R13-29.
18. Klionsky DJ, Abdalla FC, Abeliovich H, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2012; 8:445-544.
19. Wu YT, Tan HL, Shui G, et al. Dual role of 3-methyladenine in modulation of autophagy via different temporal patterns of inhibition on class I and III phosphoinositide 3-kinase. J Biol Chem. 2010;285:10850-61.
20. Liang CC, Park AY, Guan JL. In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc. 2007;2:329-333
21. O'Neil RG, Wu L, Mullani N. Uptake of a fluorescent deoxyglucose analog (2-NBDG) in tumor cells. Mol Imaging Biol. 2005;7:388-92.
22. Szablewski L. Expression of glucose transporters in cancers. Biochimica et Biophysica Acta. 2013;1835:164-9.
23. Matsuzu K, Segade F, Wong M, Clark OH, Perrier ND, Bowden DW. Glucose transporters in the thyroid. Thyroid. 2005;15:545-50.
24. Samih N, Hovsepian S, Aouani A, Lombardo D, Fayet G. Glut-1 translocation in FRTL-5 thyroid cells: role of phosphatidylinositol 3-kinase and N-glycosylation. Endocrinology. 2000;141:4146-55.
25. Hosaka Y, Tawata M, Kurihara A, Ohtaka M, Endo T, Onaya T. The regulation of two distinct glucose transporter (GLUT1 and GLUT4) gene expressions in cultured rat thyroid cells by thyrotropin. Endocrinology. 1992;131:159-65.
26. Semenza GL. Hypoxia-inducible factors in physiology and medicine. Cell. 2012;148:399-408.
27. Burrows N, Resch J, Cowen RL, et al. Expression of hypoxia-inducible factor 1 alpha in thyroid carcinomas. Endocr Relat Cancer. 2010;17:61-72.
28. Burrows N, Babur M, Resch J, et al. GDC-0941 inhibits metastatic characteristics of thyroid carcinomas by targeting both the phosphoinositide-3 kinase (PI3K) and hypoxia-inducible factor-1a (HIF-1a) pathways. J Clin Endocrinol Metab. 2011;96:E1934-43.
29. Andrade BM, Cazarin J, Zancan P, Carvalho DP. AMP-activated protein kinase upregulates glucose uptake in thyroid PCCL3 cells independent of thyrotropin. Thyroid. 2012;22:1063-8.
30. Gao X, Neufeld TP, Pan D. Drosophila PTEN regulates cell growth and proliferation through PI3K-dependent and -independent pathways. Dev Biol. 2000;221:404-18.
31. Schwartzenberg-Bar-Yoseph F, Armoni M, Karnieli E. The tumor suppressor p53 down-regulates glucose transporters GLUT1 and GLUT4 gene expression. Cancer Res. 2004;64:2627-33.
32. Bensaad K, Tsuruta A, Selak MA, et al. TIGAR, a p53- inducible regulator of glycolysis and apoptosis. Cell. 2006;126:107-20.
33. Waldman T, Kinzler KW, Vogelstein B. p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res 1995;55:5187-5190.
34. Miyashita T, Krajewski S, Krajewska M, et al. Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 1994;9:1799-1805.
35. Kubbutat MH, Jones SN, Vousden KH. Regulation of p53 stability by Mdm2. Nature. 1997;387: 299-303.
36. Vakifahmetoglu-Norberg H, Kim M, Xia HG, et al. Chaperone-mediated autophagy degrades mutant p53. Genes Dev. 2013;27:1718-1730.
37. Thongrakard V, Titone R, Follo C, et al. Turmeric Toxicity in A431 Epidermoid Cancer Cells Associates with Autophagy Degradation of Anti-apoptotic and Anti-autophagic p53 Mutant. Phytother. Res. 2014; DOI: 10.1002/ptr.5196
38. Wong RP, Tsang WP, Chau PY, et al. p53-R273H gains new function in induction of drug resistance through down-regulation of procaspase-3. Mol Cancer Ther.2007;6:1054-61.
39. Morselli E, Tasdemir E, Maiuri MC, et al. Mutant p53 protein localized in the cytoplasm inhibits autophagy. Cell Cycle. 2008;7:3056-61.
40. Muller PA, Trinidad AG, Timpson P, et al. Mutant p53 enhances MET trafficking and signalling to drive cell scattering and invasion. Oncogene. 2013;32:1252-65.
41. Tennant DA, Duran RV, Gottlieb E. Targeting metabolic transformation for cancer therapy. Nat Rev Cancer. 2010;10:267-77.
42. Jang M, Kim SS, Lee J. Cancer cell metabolism: implications for therapeutic targets. Exp Mol Med. 2013 Oct 4;45:e45.
43. Zhao Y, Butler EB, Tan M. Targeting cellular metabolism to improve cancer therapeutics. Cell Death Dis. 2013;4:e532. doi: 10.1038/cddis.2013.60.
44. Duan W, Shen X, Lei J, et al. Hyperglycemia, a neglected factor during cancer progression. Biomed Res Int. 2014;2014:461-917. doi: 10.1155/2014/461917.
45. Beckner ME, Stracke ML, Liotta LA, Schiffmann E. Glycolysis as primary energy source in tumor cell chemotaxis. J Natl Cancer Inst. 1990;82:1836-40.
46. Elf SE, Chen J. Targeting glucose metabolism in patients with cancer. Cancer. 2014;120:774-80.
47. Cao X, Fang L, Gibbs S, et al. Glucose uptake inhibitor sensitizes cancer cells to daunorubicin and overcomes drug resistance in hypoxia. Cancer Chemother Pharmacol. 2007;59:495-505.
48. Dwarakanath B, Jain V. Targeting glucose metabolism with 2-deoxy-D-glucose for improving cancer therapy. Future Oncol. 2009;5:581-5.
49. Sandulache VC, Skinner HD, Wang Y, et al. Glycolytic inhibition alters anaplastic thyroid carcinoma tumor metabolism and improves response to conventional chemotherapy and radiation. Mol Cancer Ther. 2012;11:1373-80.
50. Meyerhardt JA, Sato K, Niedzwiecki D, et al. Dietary glycemic load and cancer recurrence and survival in patients with stage III colon cancer: findings from CALGB 89803. J Natl Cancer Inst. 2012;104:1702-11.
51. Castino R, Bellio N, Follo C, Murphy D, Isidoro C. Inhibition of PI3k class III-dependent autophagy prevents apoptosis and necrosis by oxidative stress in dopaminergic neuroblastoma cells. Toxicol Sci. 2010;117:152-62.
52. Castino R, Fiorentino I, Cagnin M, Giovia A, Isidoro C. Chelation of lysosomal iron protects dopaminergic SH-SY5Y neuroblastoma cells from hydrogen peroxide toxicity by precluding autophagy and Akt dephosphorylation. Toxicol Sci. 2011a;123:523-41.
53. Castino R, Pucer A, Veneroni R, et al. Resveratrol reduces the invasive growth and promotes the acquisition of a long-lasting differentiated phenotype in human glioblastoma cells. J Agric Food Chem. 2011b;59:4264-72.
54. Castino R, Bellio N, Nicotra G, Follo C, Trincheri NF, Isidoro C. Cathepsin D-Bax death pathway in oxidative stressed neuroblastoma cells. Free Radical Biology and Medicine. 2007;42:1305-16.
55. Trincheri NF, Follo C, Nicotra G, Peracchio C, Castino R, Isidoro C. Resveratrol-induced apoptosis depends on the lipid kinase activity of Vps34 and on the formation of autophagolysosomes. Carcinogenesis. 2008;29:381-9.