The plasma membrane calcium pump in pancreatic cancer cells exhibiting the warburg effect relies on glycolytic ATP

Journal of Biological Chemistry

Volumn 290, Issue 41, 2015, Pages 24760-24771

  James, Andrew D ^a   Patel, Waseema ^a   Butt, Zohra ^a   Adiamah, Magretta ^a   Dakhel, Raga ^a   Latif, Ayse ^b   Uggenti, Carolina ^b   Swanton, Eileithyia ^a   Imamura, Hiromi ^c   Siriwardena, Ajith K ^d   Bruce, Jason I E ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c KYOTO UNIVERSITY   (Japan)

^d MANCHESTER ROYAL INFIRMARY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CELL MEMBRANES; CELLS;

ATP DEPLETION; PANCREATIC CANCERS; THERAPEUTIC TARGETS; WARBURG EFFECTS;

DISEASES;

2 OXOISOCAPROIC ACID; ADENOSINE TRIPHOSPHATE; GALACTOSE; PLASMA MEMBRANE CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; ALPHA-KETOISOCAPROIC ACID; CALCIUM; ENZYME INHIBITOR; IODOACETIC ACID; OXOACID;

ACIDIFICATION; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL METABOLISM; CELL PROLIFERATION; CELL TRANSPORT; CELL VIABILITY; CONTROLLED STUDY; ENZYME INHIBITION; GLYCOLYSIS; HUMAN; HUMAN CELL; METABOLIC PARAMETERS; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL RESPIRATION; OXYGEN CONSUMPTION; PANCREATIC CANCER CELL LINE; PRIORITY JOURNAL; PROTEIN FUNCTION; UPREGULATION; WARBURG EFFECT; ADENOCARCINOMA; ANTAGONISTS AND INHIBITORS; CELL MEMBRANE; CYTOSOL; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; MITOCHONDRION; PANCREAS TUMOR; PATHOLOGY; TUMOR CELL LINE;

ADENOCARCINOMA; ADENOSINE TRIPHOSPHATE; CALCIUM; CELL LINE, TUMOR; CELL MEMBRANE; CYTOSOL; ENZYME INHIBITORS; GALACTOSE; GLYCOLYSIS; HUMANS; IODOACETIC ACID; KETO ACIDS; MITOCHONDRIA; PANCREATIC NEOPLASMS; PLASMA MEMBRANE CALCIUM-TRANSPORTING ATPASES;

EID: 84943612503     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.668707     Document Type: Article

References (44)

1. Amin, Z., Theis, B., Russell, R. C., House, C., Novelli, M., and Lees, W. R. (2006) Diagnosing pancreatic cancer: The role of percutaneous biopsy and CT. Clin. Radiol. 61, 996-1002.
2. Tennant, D. A., Durán, R. V., and Gottlieb, E. (2010) Targeting metabolic transformation for cancer therapy. Nat. Rev. Cancer 10, 267-277.
3. Le, A., Rajeshkumar, N. V., Maitra, A., and Dang, C. V. (2012) Conceptual framework for cutting the pancreatic cancer fuel supply. Clin. Cancer Res. 18, 4285-4290.
4. Chaika, N. V., Yu, F., Purohit, V., Mehla, K., Lazenby, A. J., DiMaio, D., Anderson, J. M., Yeh, J. J., Johnson, K. R., Hollingsworth, M. A., and Singh, P. K. (2012) Differential expression of metabolic genes in tumor and stromal components of primary and metastatic loci in pancreatic adenocarcinoma. PLoS ONE 7, e32996.
5. Zhou, W., Capello, M., Fredolini, C., Racanicchi, L., Piemonti, L., Liotta, L. A., Novelli, F., and Petricoin, E. F. (2012) Proteomic analysis reveals Warburg effect and anomalous metabolism of glutamine in pancreatic cancer cells. J. Proteome Res. 11, 554-563.
6. Cairns, R. A., Harris, I. S., and Mak, T. W. (2011) Regulation of cancer cell metabolism. Nat. Rev. Cancer 11, 85-95.
7. Guppy, M. (2002) The hypoxic core: A possible answer to the cancer paradox. Biochem. Biophys. Res. Commun. 299, 676-680.
8. Guillaumond, F., Leca, J., Olivares, O., Lavaut, M.-N., Vidal, N., Berthezène, P., Dusetti, N. J., Loncle, C., Calvo, E., Turrini, O., Iovanna, J. L., Tomasini, R., and Vasseur, S. (2013) Strengthened glycolysis under hypoxia supports tumor symbiosis and hexosamine biosynthesis in pancreatic adenocarcinoma. Proc. Natl. Acad. Sci. U.S.A. 110, 3919-3924.
9. James, A. D., Chan, A., Erice, O., Siriwardena, A. K., and Bruce, J. I. (2013) Glycolytic ATP fuels the plasma membrane calcium pump critical for pancreatic cancer cell survival. J. Biol. Chem. 288, 36007-36019.
10. Brini, M., and Carafoli, E. (2009) Calcium pumps in health and disease. Physiol. Rev. 89, 1341-1378.
11. Marroquin, L. D., Hynes, J., Dykens, J. A., Jamieson, J. D., and Will, Y. (2007) Circumventing the crabtree effect: replacing media glucose with galactose increases susceptibility of HepG2 cells to mitochondrial toxicants. Toxicol. Sci. 97, 539-547.
12. Bustamante, E., and Pedersen, P. L. (1977) High aerobic glycolysis of rat hepatoma cells in culture: role of mitochondrial hexokinase. Proc. Natl. Acad. Sci. U.S.A. 74, 3735-3739.
13. Rossignol, R., Gilkerson, R., Aggeler, R., Yamagata, K., Remington, S. J., and Capaldi, R. A. (2004) Energy substrate modulates mitochondrial structure and oxidative capacity in cancer cells. Cancer Res. 64, 985-993.
14. Lenzen, S., Schmidt, W., and Panten, U. (1985) Transamination of neutral amino acids and 2-keto acids in pancreatic B-cell mitochondria. J. Biol. Chem. 260, 12629-12634.
15. Malaisse, W. J., Sener, A., Malaisse-Legae, F., Hutton, J. C., and Christophe, J. (1981) The stimulus-secretion coupling of amino acid-induced insulin release. Metabolic interaction of L-glutamine and 2-ketoisocaproate in pancreatic islets. Biochim. Biophys. Acta 677, 39-49.
16. Noda, C., and Ichihara, A. (1974) Control of ketogenesis from amino acids. II. Ketone bodies formation from ketoisocaproate, the keto-analogue of leucine, by rat liver mitochondria. J. Biochem. 76, 1123-1130.
17. MacDonald, M. J., Fahien, L. A., Brown, L. J., Hasan, N. M., Buss, J. D., and Kendrick, M. A. (2005) Perspective: emerging evidence for signaling roles of mitochondrial anaplerotic products in insulin secretion. Am. J. Physiol. Endocrinol. Metab. 288, E1-E15.
18. Hutton, J. C., Sener, A., and Malaisse, W. J. (1979) The metabolism of 4-methyl-2-oxopentanoate in rat pancreatic islets. Biochem. J. 184, 291-301.
19. Shukla, S. K., Gebregiworgis, T., Purohit, V., Chaika, N. V., Gunda, V., Radhakrishnan, P., Mehla, K., Pipinos, I. I., Powers, R., Yu, F., and Singh, P. K. (2014) Metabolic reprogramming induced by ketone bodies diminishes pancreatic cancer cachexia. Cancer Metab. 2, 18.
20. 2+regulation of mitochondrial ATP synthesis visualized at the single cell level. ACS Chem. Biol. 6, 709-715.
21. Bellance, N., Benard, G., Furt, F., Begueret, H., Smolková, K., Passerieux, E., Delage, J. P., Baste, J. M., Moreau, P., and Rossignol, R. (2009) Bioenergetics of lung tumors: Alteration of mitochondrial biogenesis and respiratory capacity. Int. J. Biochem. Cell Biol. 41, 2566-2577.
22. Warburg, O. (1956) Injuring of respiration the origin of cancer cells. Science 123, 309-314.
23. Frezza, C., and Gottlieb, E. (2009) Mitochondria in cancer: not just innocent bystanders. Semin. Cancer Biol. 19, 4-11.
24. Martin, M., Beauvoit, B., Voisin, P. J., Canioni, P., Guérin, B., and Rigoulet, M. (1998) Energetic and morphological plasticity of C6 glioma cells grown on 3-D support; effect of transient glutamine deprivation. J. Bioenerg. Biomembr. 30, 565-578.
25. Rodríguez-Enríquez, S., Gallardo-Pérez, J. C., Avilés-Salas, A., Marín- Hernández, A., Carreño-Fuentes, L., Maldonado-Lagunas, V., and Moreno-Sánchez, R. (2008) Energy metabolism transition in multi-cellular human tumor spheroids. J. Cell Physiol. 216, 189-197.
26. Zu, X. L., and Guppy, M. (2004) Cancer metabolism: facts, fantasy, and fiction. Biochem. Biophys. Res. Commun. 313, 459-465.
27. Busk, M., Horsman, M. R., Kristjansen, P. E., van der Kogel, A. J., Bussink, J., and Overgaard, J. (2008) Aerobic glycolysis in cancers: implications for the usability of oxygen-responsive genes and fluorodeoxyglucose-PET as markers of tissue hypoxia. Int. J. Cancer 122, 2726-2734.
28. Nakashima, R. A., Paggi, M. G., and Pedersen, P. L. (1984) Contributions of glycolysis and oxidative phosphorylation to adenosine 5α-triphosphate production in AS-30D hepatoma cells. Cancer Res. 44, 5702-5706.
29. Xu, R.-H., Pelicano, H., Zhang, H., Giles, F. J., Keating, M. J., and Huang, P. (2005) Synergistic effect of targeting mTOR by rapamycin and depleting ATP by inhibition of glycolysis in lymphoma and leukemia cells. Leukemia 19, 2153-2158.
30. Semenza, G. L. (2008) Tumor metabolism: cancer cells give and take lactate. J. Clin. Invest. 118, 3835-3837.
31. 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., Kelley, M. J., Gallez, B., Wahl, M. L., Feron, O., and Dewhirst, M. W. (2008) Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J. Clin. Invest. 118, 3930-3942.
32. Gatenby, R. A., and Gillies, R. J. (2004) Why do cancers have high aerobic glycolysis? Nat. Rev. Cancer 4, 891-899.
33. Chen, Z., Zhang, H., Lu, W., and Huang, P. (2009) Role of mitochondriaassociated hexokinase II in cancer cell death induced by 3-bromopyruvate. Biochim. Biophys. Acta 1787, 553-560.
34. Ihrlund, L. S., Hernlund, E., Khan, O., and Shoshan, M. C. (2008) 3-Bromopyruvate as inhibitor of tumour cell energy metabolism and chemopotentiator of platinum drugs. Mol. Oncol. 2, 94-101.
35. 2+ATPase in pancreatic acinar cells: role of the mitochondria. Am. J. Physiol. Cell Physiol. 295, C1247-C1260.
36. Kim, J. S., Ahn, K. J., Kim, J. A., Kim, H. M., Lee, J. D., Lee, J. M., Kim, S. J., and Park, J. H. (2008) Role of reactive oxygen species-mediated mitochondrial dysregulation in 3-bromopyruvate induced cell death in hepatoma cells: ROS-mediated cell death by 3-BrPA. J. Bioenerg. Biomembr. 40, 607- 618.
37. Rodríguez-Enríquez, S., Vital-González, P. A., Flores-Rodríguez, F. L., Marín-Hernández, A., Ruiz-Azuara, L., and Moreno-Sánchez, R. (2006) Control of cellular proliferation by modulation of oxidative phosphorylation in human and rodent fast-growing tumor cells. Toxicol. Appl. Pharmacol. 215, 208-217.
38. Echarte, M. M., Rossi, R. C., and Rossi, J. P. (2007) Phosphorylation of the plasma membrane calcium pump at high ATP concentration. On the mechanism of ATP hydrolysis. Biochemistry 46, 1034-1041.
39. 2+ATPase in ECV304. Cell Calcium 45, 177-184.
40. 2+ATPase from red cell membranes by ATP. Biochim. Biophys. Acta 996, 153-159.
41. Puchulu-Campanella, E., Chu, H., Anstee, D. J., Galan, J. A., Tao, W. A., and Low, P. S. (2013) Identification of the components of a glycolytic enzyme metabolon on the human red blood cell membrane. J. Biol. Chem. 288, 848-858.
42. Campanella, M. E., Chu, H., and Low, P. S. (2005) Assembly and regulation of a glycolytic enzyme complex on the human erythrocyte membrane. Proc. Natl. Acad. Sci. U.S.A. 102, 2402-2407.
43. 2+uptake in smooth muscle plasma membrane vesicles by an endogenous glycolytic cascade. FASEB J. 3, 2298-2301.
44. 2+uptake in smooth muscle plasma membrane vesicles. J. Gen. Physiol. 99, 21-40.