The progression from a lower to a higher invasive stage of bladder cancer is associated with severe alterations in glucose and pyruvate metabolism

Experimental Cell Research

Volumn 335, Issue 1, 2015, Pages 91-98

  Conde, Vanessa R ^a   Oliveira, Pedro F ^a,b   Nunes, Ana R ^a   Rocha, Cátia S ^a   Ramalhosa, Elsa ^c   Pereira, José A ^c   Alves, Marco G ^a   Silva, Branca M ^a  

^a UNIVERSITY OF BEIRA INTERIOR   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c INSTITUTO POLITÉCNICO DE BRAGANÇA   (Portugal)

Author keywords

Bladder cancer; Metabolism; RT4; TCCSUP; Warburg effect

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ALANINE; ALANINE AMINOTRANSFERASE; GLUCOSE; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 3; LACTATE DEHYDROGENASE; LACTIC ACID; MONOCARBOXYLATE TRANSPORTER 4; PYRUVIC ACID; MONOCARBOXYLATE TRANSPORTER; MUSCLE PROTEIN; SLC16A4 PROTEIN, HUMAN; SLC2A1 PROTEIN, HUMAN; SLC2A3 PROTEIN, HUMAN;

AMINO ACID METABOLISM; ARTICLE; BLADDER CANCER; CANCER STAGING; GLUCOSE INTAKE; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTON NUCLEAR MAGNETIC RESONANCE; WESTERN BLOTTING; BIOSYNTHESIS; BLADDER TUMOR; DISEASE COURSE; GLYCOLYSIS; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; TUMOR INVASION;

ALANINE; ALANINE TRANSAMINASE; CELL LINE, TUMOR; DISEASE PROGRESSION; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; GLUCOSE TRANSPORTER TYPE 3; GLYCOLYSIS; HUMANS; L-LACTATE DEHYDROGENASE; LACTIC ACID; MONOCARBOXYLIC ACID TRANSPORTERS; MUSCLE PROTEINS; NEOPLASM INVASIVENESS; NEOPLASM STAGING; PHOSPHOFRUCTOKINASE-1; PYRUVIC ACID; URINARY BLADDER NEOPLASMS;

EID: 84930762528     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2015.04.007     Document Type: Article

References (53)

1. Ramanathan A., Wang C., Schreiber S.L. Perturbational profiling of a cell-line model of tumorigenesis by using metabolic measurements. Proc. Natl. Acad. Sci. 2005, 102(17):5992-5997.
2. Lopez-Lazaro M. A new view of carcinogenesis and an alternative approach to cancer therapy. Mol. Med. 2010, 16(3):144-153.
3. Warburg O., Wind F., Negelein E. The metabolism of tumors in the body. J. Gen. Physiol. 1927, 8(6):519-530.
4. Warburg O. On the origin of cancer cells. Science 1956, 123(3191):309-314.
5. Vaz C.V., Alves M.G., Marques R., Moreira P.I., Oliveira P.F., Maia C.J., Socorro S. Androgen-responsive and nonresponsive prostate cancer cells present a distinct glycolytic metabolism profile. Int. J. Biochem. Cell Biol. 2012, 44(11):2077-2084.
6. Oliveira P.F., Martins A.D., Moreira A.C., Cheng C.Y., Alves M.G. The Warburg effect revisited-lesson from the sertoli cell. Med. Res. Rev. 2015, 35(1):126-151.
7. Zhao W., Chang C., Cui Y., Zhao X., Yang J., Shen L., Zhou J., Hou Z., Zhang Z., Ye C., Hasenmayer D., Perkins R., Huang X., Yao X., Yu L., Huang R., Zhang D., Guo H., Yan J. Steroid receptor coactivator-3 regulates glucose metabolism in bladder cancer cells through coactivation of hypoxia inducible factor 1alpha. J. Biol. Chem. 2014, 289(16):11219-11229.
8. Reis H., Tschirdewahn S., Szarvas T., Rubben H., Schmid K.W., Grabellus F. Expression of GLUT1 is associated with increasing grade of malignancy in non-invasive and invasive urothelial carcinomas of the bladder. Oncol. Lett. 2011, 2(6):1149-1153.
9. Osthus R.C., Shim H., Kim S., Li Q., Reddy R., Mukherjee M., Xu Y., Wonsey D., Lee L.A., Dang C.V. Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J. Biol. Chem. 2000, 275(29):21797-21800.
10. Ros S., Schulze A. Balancing glycolytic flux: the role of 6-phosphofructo-2-kinase/fructose 2, 6-bisphosphatases in cancer metabolism. Cancer Metab. 2013, 1(1):8.
11. Liang W., Hao Z., Han J.L., Zhu D.J., Jin Z.F., Xie W.L. CAV-1 contributes to bladder cancer progression by inducing epithelial-to-mesenchymal transition. Urol. Oncol. 2014, 32(6):855-863.
12. Mitra A.P., Datar R.H., Cote R.J. Molecular pathways in invasive bladder cancer: new insights into mechanisms, progression, and target identification. J. Clin. Oncol. 2006, 24(35):5552-5564.
13. Ferlay J., Soerjomataram I., Ervik M. Cancer Incidence and Mortality Worldwide: IARC CancerBase. GLOBOCAN 2012 v1.0 2013, International Agency for Research on Cancer, Lyon, France.
14. Oosterlinck W., Lobel B., Jakse G., Malmstrom P.U., Stockle M., Sternberg C. Guidelines on bladder cancer. Eur. Urol. 2002, 41(2):105-112.
15. Vaidya S., Lakhey M., Kc S., Hirachand S. Urothelial tumours of the urinary bladder: a histopathological study of cystoscopic biopsies. J. Nepal Med. Assoc. 2013, 52(191):475-478.
16. Shin K., Lim A., Odegaard J.I., Honeycutt J.D., Kawano S., Hsieh M.H., Beachy P.A. Cellular origin of bladder neoplasia and tissue dynamics of its progression to invasive carcinoma. Nat. Cell Biol. 2014, 16(5):469-478.
17. Kashif Khan M., Ahmed I., Raza S.J. Factors effecting recurrence and progression of high grade non invasive bladder cancer treated by intravesical BCG. Pak. J. Med. Sci. 2014, 30(2):326-330.
18. Porru S., Pavanello S., Carta A., Arici C., Simeone C., Izzotti A., Mastrangelo G. Complex relationships between occupation, environment, DNA adducts, genetic polymorphisms and bladder cancer in a case-control study using a structural equation modeling. PloS One 2014, 9(4):e94566.
19. Wu Y., Yang Y. Complex association between ERCC2 gene polymorphisms, gender, smoking and the susceptibility to bladder cancer: a meta-analysis. Tumour Biol. 2014, 35(6):5245-5257.
20. Dinney C.P., McConkey D.J., Millikan R.E., Wu X., Bar-Eli M., Adam L., Kamat A.M., Siefker-Radtke A.O., Tuziak T., Sabichi A.L., Grossman H.B., Benedict W.F., Czerniak B. Focus on bladder cancer. Cancer Cell 2004, 6(2):111-116.
21. McConkey D.J., Lee S., Choi W., Tran M., Majewski T., Lee S., Siefker-Radtke A., Dinney C., Czerniak B. Molecular genetics of bladder cancer: emerging mechanisms of tumor initiation and progression. Urol. Oncol. 2010, 4:429-440.
22. Jin X., Yun S.J., Jeong P., Kim I.Y., Kim W.J., Park S. Diagnosis of bladder cancer and prediction of survival by urinary metabolomics. Oncotarget 2014, 5(6):1635-1645.
23. Langbein S., Zerilli M., Zur Hausen A., Staiger W., Rensch-Boschert K., Lukan N., Popa J., Ternullo M.P., Steidler A., Weiss C., Grobholz R., Willeke F., Alken P., Stassi G., Schubert P., Coy J.F. Expression of transketolase TKTL1 predicts colon and urothelial cancer patient survival: warburg effect reinterpreted. Br. J. Cancer 2006, 94(4):578-585. 10.1038/sj.bjc.6602962.
24. Rigby C.C., Franks L.M. A human tissue culture cell line from a transitional cell tumour of the urinary bladder: growth, chromosone pattern and ultrastructure. Br. J. Cancer 1970, 24(4):746-754.
25. Nayak S.K., O]Toole C., Price Z.H. A cell line from an anaplastic transitional cell carcinoma of human urinary bladder. Br. J. Cancer 1977, 35(2):142-151.
26. Alves M.G., Oliveira P.J., Carvalho R.A. Substrate selection in hearts subjected to ischemia/reperfusion: role of cardioplegic solutions and gender. NMR Biomed. 2011, 24(9):1029-1037.
27. Rato L., Alves M.G., Socorro S., Carvalho R.A., Cavaco J.E., Oliveira P.F. Metabolic modulation induced by oestradiol and DHT in immature rat sertoli cells cultured in vitro. Biosci. Rep. 2012, 32(1):61-69.
28. Dias T.R., Alves M.G., Tomás G.D., Socorro S., Silva B.M., Oliveira P.F. White tea as a promising antioxidant medium additive for sperm storage at room temperature: a comparative study with green tea. J. Agric. Food Chem. 2014, 62(3):608-617.
29. Alves M.G., Machado N.G., Sardao V.A., Carvalho R.A., Oliveira P.J. Anti-apoptotic protection afforded by cardioplegic celsior and histidine buffer solutions to hearts subjected to ischemia and ischemia/reperfusion. J. Cell. Biochem. 2011, 112(12):3872-3881.
30. Underwood A.H., Newsholme E. Properties of phosphofructokinase from rat liver and their relation to the control of glycolysis and gluconeogenesis. Biochem. J. 1965, 95:868-875.
31. Xiong Y., Lei Q.Y., Zhao S., Guan K.L. Regulation of glycolysis and gluconeogenesis by acetylation of PKM and PEPCK. Cold Spring Harb. Symp. Quant. Biol. 2011, 76:285-289.
32. Feron O. Pyruvate into lactate and back: from the Warburg effect to symbiotic energy fuel exchange in cancer cells. Radiother. Oncol. 2009, 92(3):329-333.
33. Williamson D., Lund P., Krebs H. The redox state of free nicotinamide-adenine dinucleotide in the cytoplasm and mitochondria of rat liver. Biochem. J. 1967, 103:514-527.
34. Galluzzi L., Kepp O., Vander Heiden M.G., Kroemer G. Metabolic targets for cancer therapy. Nat. Rev. Drug Discov. 2013, 12(11):829-846.
35. DeBerardinis R.J., Mancuso A., Daikhin E., Nissim I., Yudkoff M., Wehrli S., Thompson C.B. Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc. Natl. Acad. Sci. 2007, 104(49):19345-19350.
36. Elstrom R.L., Bauer D.E., Buzzai M., Karnauskas R., Harris M.H., Plas D.R., Zhuang H., Cinalli R.M., Alavi A., Rudin C.M. Akt stimulates aerobic glycolysis in cancer cells. Cancer Res. 2004, 64(11):3892-3899.
37. DeBerardinis R.J., Lum J.J., Hatzivassiliou G., Thompson C.B. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab. 2008, 7(1):11-20.
38. Flier J.S., Mueckler M.M., Usher P., Lodish H.F. Elevated levels of glucose transport and transporter messenger RNA are induced by ras or src oncogenes. Science 1987, 235(4795):1492-1495.
39. Hoskin P.J., Sibtain A., Daley F.M., Wilson G.D. GLUT1 and CAIX as intrinsic markers of hypoxia in bladder cancer: relationship with vascularity and proliferation as predictors of outcome of ARCON. Br. J. Cancer 2003, 89(7):1290-1297.
40. Cheng L., Davison D.D., Adams J., Lopez-Beltran A., Wang L., Montironi R., Zhang S. Biomarkers in bladder cancer: translational and clinical implications. Crit. Rev. Oncol./Hematol. 2014, 89(1):73-111.
41. Pradelli L., Villa E., Zunino B., Marchetti S., Ricci J. Glucose metabolism is inhibited by caspases upon the induction of apoptosis. Cell Death Dis. 2014, 5(9):e1406.
42. Hasawi N.A., Khandari M.A., Luqmani Y.A. Phosphofructokinase: a mediator of glycolytic flux in cancer progression. Crit. Rev. Oncol./Hematol. 2014, 92(3):312-321.
43. Chehtane M., Khaled A.R. Interleukin-7 mediates glucose utilization in lymphocytes through transcriptional regulation of the hexokinase II gene. Am. J. Physiol. Cell Phys. 2010, 298(6):C1560-C1571.
44. Gray L.R., Tompkins S.C., Taylor E.B. Regulation of pyruvate metabolism and human disease. Cell. Mol. Life Sci. 2014, 14:2577-2604.
45. Kim J-w Tchernyshyov I, Semenza G.L., Dang C.V. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 2006, 3(3):177-185.
46. Fan J., Kang H.-B., Shan C., Elf S., Lin R., Xie J., Gu T.-L., Aguiar M., Lonning S., Chung T.-W. Tyr-301 phosphorylation inhibits pyruvate dehydrogenase by blocking substrate binding, and promotes the Warburg effect. J. Biol. Chem. 2014, 289:26533-26541.
47. Sonveaux P., Végran F., Schroeder T., Wergin M.C., Verrax J., Rabbani Z.N., De Saedeleer C.J., Kennedy K.M., Diepart C., Jordan B.F. Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J. Clin. Investig. 2008, 118(12):3930-3942.
48. Pelicano H., Carney D., Huang P. ROS stress in cancer cells and therapeutic implications. Drug Resist. Update 2004, 7(2):97-110.
49. Pavlides S., Vera I., Gandara R., Sneddon S., Pestell R.G., Mercier I., Martinez-Outschoorn U.E., Whitaker-Menezes D., Howell A., Sotgia F. Warburg meets autophagy: cancer-associated fibroblasts accelerate tumor growth and metastasis via oxidative stress, mitophagy, and aerobic glycolysis. Antioxid. Redox Signal. 2012, 16(11):1264-1284.
50. Ye C., Shu X.O., Wen W., Pierce L., Courtney R., Gao Y.T., Zheng W., Cai Q. Quantitative analysis of mitochondrial DNA 4977-bp deletion in sporadic breast cancer and benign breast diseases. Breast Cancer Res. Treat. 2008, 108(3):427-434.
51. Futyma K., Putowski L., Cybulski M., Miotla P., Rechberger T., Semczuk A. The prevalence of mtDNA4977 deletion in primary human endometrial carcinomas and matched control samples. Oncol. Rep. 2008, 20(3):683-688.
52. Wada T., Tanji N., Ozawa A., Wang J., Shimamoto K., Sakayama K., Yokoyama A.M. Mitochondrial DNA mutations and 8-hydroxy-2'-deoxyguanosine Content in Japanese patients with urinary bladder and renal cancers. Anticancer Res. 2006, 26(5A):3403-3408.
53. Shakhssalim N., Houshmand M., Kamalidehghan B., Faraji A., Sarhangnejad R., Dadgar S., Mobaraki M., Rosli R., Sanat M.H. The mitochondrial C16069T polymorphism, not mitochondrial D310 (D-loop) mononucleotide sequence variations, is associated with bladder cancer. Cancer Cell Int. 2013, 13:120-129.