Choline kinase overexpression increases invasiveness and drug resistance of human breast cancer cells

NMR in Biomedicine

Volumn 23, Issue 6, 2010, Pages 633-642

  Shah, Tariq ^a   Wildes, Flonne ^a   Penet, Marie France ^a   Winnard Jr , Paul T ^a   Glunde, Kristine ^a   Artemov, Dmitri ^a   Ackerstaff, Ellen ^a,b   Gimi, Barjor ^a,c   Kakkad, Samata ^a   Raman, Venu ^a   Bhujwalla, Zaver M ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Choline kinase; Drug resistance; Invasion; Magnetic resonance spectroscopy; MCF 7 cells

Indexed keywords

CYTOLOGY; MAGNETIC MATERIALS; MAGNETIC RESONANCE; MAGNETIC RESONANCE SPECTROSCOPY; METABOLISM; PARTICLE DETECTORS; PHOSPHOLIPIDS;

5-FLUOROURACIL; BREAST CANCER; CELL INVASION; CELL METABOLISM; CHOLINE KINASE; CHOLINE PHOSPHOLIPID METABOLISM; CONTROL-CELL; DRUG EFFLUX PUMPS; DRUG RESISTANCE; DYNAMIC TRACKING; HUMAN BREAST CANCER CELLS; INVASIVENESS; ISOFORMS; MALIGNANT CELLS; MCF-7 CELLS; NON-INVASIVE; OVER-EXPRESSION; PHOSPHOCHOLINE; PROTON MR SPECTROSCOPY; THYMIDYLATE SYNTHASE; TUMOR GRADES;

CLONE CELLS;

CHOLINE KINASE; CHOLINE KINASE ALPHA; FLUOROURACIL; PHOSPHOLIPID; PHOSPHORYLCHOLINE; RHODAMINE 123; THYMIDYLATE SYNTHASE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; ISOENZYME; TUMOR MARKER;

ARTICLE; BREAST CANCER; CANCER CELL; CELL INVASION; CELL METABOLISM; CONTROLLED STUDY; DRUG RESISTANCE; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; NUCLEAR MAGNETIC RESONANCE IMAGING; PHENOTYPE; PHOSPHOLIPID METABOLISM; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; BREAST TUMOR; FEMALE; GENETICS; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PATHOLOGY; PHYSIOLOGY; PROCEDURES; TRANSGENIC ORGANISM; TUMOR CELL LINE;

BREAST NEOPLASMS; CELL LINE, TUMOR; CHOLINE KINASE; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; ISOENZYMES; MAGNETIC RESONANCE SPECTROSCOPY; ORGANISMS, GENETICALLY MODIFIED; PHOSPHORYLCHOLINE; TUMOR MARKERS, BIOLOGICAL;

EID: 77955103532     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.1510     Document Type: Article

References (46)

1. Aoyama C, Liao H, Ishidate K. Structure and function of choline kinase isoforms in mammalian cells. Prog. Lipid. Res. 2004; 43: 266-281.
2. Kent C. Regulation of phosphatidylcholine biosynthesis. Prog. Lipid. Res. 1990; 29: 87-105.
3. Ramirez de Molina A, Rodriguez-Gonzalez A, Gutierrez R, Martinez-Pineiro L, Sanchez J, Bonilla F, Rosell R, Lacal J. Overexpression of choline kinase is a frequent feature in human tumor-derived cell lines and in lung, prostate, and colorectal human cancers. Biochem. Biophys. Res. Commun. 2002; 296: 580-583.
4. Warden CH, Friedkin M. Regulation of choline kinase activity and phosphatidylcholine biosynthesis by mitogenic growth factors in 3T3 fibroblasts. J. Biol. Chem. 1985; 260: 6006-6011.
5. Uchida T. Stimulation of phospholipid synthesis in HeLa cells by epidermal growth factor and insulin: activation of choline kinase and glycerophosphate acyltransferase. Biochim. Biophys. Acta. 1996; 1304: 89-104.
6. Pelech SL, Vance DE. Regulation of phosphatidylcholine biosynthesis. Biochim. Biophys. Acta. 1984; 779: 217-251.
7. Vigo C, Vance DE. Effect of diethylstilboestrol on phosphatidylcholine biosynthesis and choline metabolism in the liver of roosters. Biochem. J. 1981; 200: 321-326. (Pubitemid 12218255)
8. Jimenez B, del Peso L, Montaner S, Esteve P, Lacal JC. Generation of phosphorylcholine as an essential event in the activation of Raf-1 and MAP-kinases in growth factors-induced mitogenic stimulation. J. Cell Biochem. 1995; 57: 141-149.
9. Chung T, Huang JS, Mukherjee JJ, Crilly KS, Kiss Z. Expression of human choline kinase in NIH 3T3 fibroblasts increases the mitogenic potential of insulin and insulin-like growth factor I. Cell Signal. 2000; 12: 279-288.
10. Glunde K, Shah T, Winnard PT Jr, Raman V, Takagi T, Vesuna F, Artemov D, Bhujwalla ZM. Hypoxia regulates choline kinase expression through hypoxia-inducible factor-1 alpha signaling in a human prostate cancer model. Cancer Res. 2008; 68: 172-180.
11. Aboagye EO, Bhujwalla ZM. Malignant transformation alters membrane choline phospholipid metabolism of human mammary epithelial cells. Cancer Res. 1999; 59: 80-84.
12. Ramirez de Molina A, Gutierrez R, Ramos MA, Silva JM, Silva J, Bonilla F, Sanchez JJ, Lacal JC. Increased choline kinase activity in human breast carcinomas: clinical evidence for a potential novel antitumor strategy. Oncogene. 2002; 21: 4317-4322.
13. Hourani R, Horska A, Albayram S, Brant LJ, Melhem E, Cohen KJ, Burger PC, Weingart JD, Carson B, Wharam MD, Barker PB. Proton magnetic resonance spectroscopic imaging to differentiate between nonneoplastic lesions and brain tumors in children. J. Magn. Reson. Imaging. 2006; 23: 99-107.
14. Casciani E, Polettini E, Bertini L, Emiliozzi P, Amini M, Pansadoro V, Gualdi GF. Prostate cancer: evaluation with endorectal MR imaging and three-dimensional proton MR spectroscopic imaging. Radiol. Med. (Torino). 2004; 108: 530-541.
15. Kim JK, Park SH, Lee HM, Lee YH, Sung NK, Chung DS, Kim OD. In vivo 1H-MRS evaluation of malignant and benign breast diseases. Breast. 2003; 12: 179-182.
16. Bhakoo KK, Williams SR, Florian CL, Land H, Noble MD. Immortalization and transformation are associated with specific alterations in choline metabolism. Cancer Res. 1996; 56: 4630-4635. (Pubitemid 26338062)
17. Glunde K, Ackerstaff E, Mori N, Jacobs MA, Bhujwalla ZM. Choline phospholipid metabolism in cancer: consequences for molecular pharmaceutical interventions. Mol. Pharm. 2006; 3: 496-506.
18. Banez-Coronel M, de Molina AR, Rodriguez-Gonzalez A, Sarmentero J, Ramos MA, Garcia-Cabezas MA, Garcia-Oroz L, Lacal JC. Choline kinase alpha depletion selectively kills tumoral cells. Curr. Cancer Drug. Targets. 2008; 8: 709-719.
19. Ramirez deMolina, Sarmentero-Estrada A, Belda-Iniesta J, Taron C, Ramirez M, de Molina V, Cejas P, Skrzypski M, Gallego-Ortega D, de Castro J, Casado E, Garcia-Cabezas MA, Sanchez JJ, Nistal M, Rosell R, Gonzalez-Baron M, Lacal JC. Expression of choline kinase alpha to predict outcome in patients with early-stage non-small-cell lung cancer: a retrospective study. Lancet. Oncol. 2007; 8: 889-897.
20. Eliyahu G, Kreizman T, Degani H. Phosphocholine as a biomarker of breast cancer: molecular and biochemical studies. Int. J. Cancer. 2007; 120: 1721-1730.
21. Glunde K, Raman V, Mori N, Bhujwalla ZM. RNA interference-mediated choline kinase suppression in breast cancer cells induces differentiation and reduces proliferation. Cancer Res. 2005; 65: 11034-11043.
22. Mori N, Glunde K, Takagi T, Raman V, Bhujwalla ZM. Choline kinase down-regulation increases the effect of 5-fluorouracil in breast cancer cells. Cancer Res. 2007; 67: 11284-11290.
23. Hosaka K, Tanaka S, Nikawa J, Yamashita S. Cloning of a human choline kinase cDNA by complementation of the yeast cki mutation. FEBS Lett. 1992; 304: 229-232.
24. Pilatus U, Aboagye E, Artemov D, Mori N, Ackerstaff E, Bhujwalla ZM. Real-time measurements of cellular oxygen consumption, pH, and energy metabolism using nuclear magnetic resonance spectroscopy. Magn. Reson. Med. 2001; 45: 749-755.
25. Ackerstaff E, Gimi B, Artemov D, Bhujwalla ZM. Anti-inflammatory agent indomethacin reduces invasion and alters metabolism in a human breast cancer cell line. Neoplasia. 2007; 9: 222-235.
26. Hetherington HP, Avison MJ, Shulman RG. 1H homonuclear editing of rat brain using semiselective pulses. Proc. Natl. Acad. Sci. USA. 1985; 82: 3115-3118.
27. Hetherington HP HJ, Pan JW, Rothman DL, Shulman RG. A fully localized 1H homonuclear editing sequence to observe lactate in human skeletal muscle after exercise. J. Magn. Reson. 1989; 82: 86-96.
28. Pilatus U, Ackerstaff E, Artemov D, Mori N, Gillies RJ, Bhujwalla ZM. Imaging prostate cancer invasion with multi-nuclear magnetic resonance methods: the Metabolic Boyden Chamber. Neoplasia. 2000; 2: 273-279. (Pubitemid 30346083)
29. Tyagi RK, Azrad A, Degani H, Salomon Y. Simultaneous extraction of cellular lipids and water-soluble metabolites: evaluation by NMR spectroscopy. Magn. Reson. Med. 1996; 35: 194-200.
30. Glunde K, Guggino SE, Solaiyappan M, Pathak AP, Ichikawa Y, Bhujwalla ZM. Extracellular acidification alters lysosomal trafficking in human breast cancer cells. Neoplasia. 2003; 5: 533-545.
31. Aiken NR, Gillies RJ. Phosphomonoester metabolism as a function of cell proliferative status and exogenous precursors. Anticancer Res. 1996; 16: 1393-1397.
32. Jagannathan NR, Kumar M, Seenu V, Coshic O, Dwivedi SN, Julka PK, Srivastava A, Rath GK. Evaluation of total choline from in-vivo volume localized proton MR spectroscopy and its response to neoadjuvant chemotherapy in locally advanced breast cancer. Br. J. Cancer. 2001; 84: 1016-1022.
33. Ramirez de Molina A, Gallego-Ortega D, Sarmentero J, Banez-Coronel M, Martin-Cantalejo Y, Lacal JC. Choline kinase is a novel oncogene that potentiates RhoA-induced carcinogenesis. Cancer Res. 2005; 65: 5647-5653.
34. Ackerstaff E, Pflug BR, Nelson JB, Bhujwalla ZM. Detection of increased choline compounds with proton nuclear magnetic resonance spectroscopy subsequent to malignant transformation of human prostatic epithelial cells. Cancer Res. 2001; 61: 3599-3603. (Pubitemid 32694969)
35. Glunde K, Jie C, Bhujwalla ZM. Molecular causes of the aberrant choline phospholipid metabolism in breast cancer. Cancer Res. 2004; 64: 4270-4276.
36. Morse DL, Carroll D, Day S, Gray H, Sadarangani P, Murthi S, Job C, Baggett B, Raghunand N, Gillies RJ. Characterization of breast cancers and therapy response by MRS and quantitative gene expression profiling in the choline pathway. NMR Biomed. 2009; 22: 114-127.
37. Tugnoli V, Tosi MR, Barbarella G, Bertoluzza A, Ricci R, Trevisan C. In vivo 1H MRS and in vitro multinuclear MR study of human brain tumors. Anticancer Res. 1996; 16: 2891-2899.
38. Calabrese C, Pisi A, Di Febo G, Liguori G, Filippini G, Cervellera M, Righi V, Lucchi P, Mucci A, Schenetti L, Tonini V, Tosi MR, Tugnoli V. Biochemical alterations from normal mucosa to gastric cancer by ex vivo magnetic resonance spectroscopy. Cancer Epidemiol. Biomarkers Prev. 2008; 17: 1386-1395.
39. Ackerstaff E, Artemov D, Gillies RJ, Bhujwalla ZM. Hypoxia and the presence of human vascular endothelial cells affect prostate cancer cell invasion and metabolism. Neoplasia. 2007; 9: 1138-1151.
40. Pestalozzi BC, Peterson HF, Gelber RD, Goldhirsch A, Gusterson BA, Trihia H, Lindtner J, Cortes-Funes H, Simmoncini E, Byrne MJ, Golouh R, Rudenstam CM, Castiglione-Gertsch M, Allegra CJ, Johnston PG. Prognostic importance of thymidylate synthase expression in early breast cancer. J. Clin. Oncol. 1997; 15: 1923-1931 .
41. Schinkel AH, Jonker JW. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv. Drug Deliv. Rev. 2003; 55: 3-29.
42. Johnson LV, Walsh ML, Bockus BJ, Chen LB. Monitoring of relative mitochondrial membrane potential in living cells by fluorescence microscopy. J. Cell Biol. 1981; 88: 526-535.
43. Neyfakh AA. Use of fluorescent dyes as molecular probes for the study of multidrug resistance. Exp. Cell Res. 1988; 174: 168-176.
44. Tapiero H, Munck JN, Fourcade A, Lampidis TJ. Cross-resistance to rhodamine 123 in Adriamycin- and daunorubicin-resistant Friend leukemia cell variants. Cancer Res. 1984; 44: 5544-5549.
45. Comerford KM, Wallace TJ, Karhausen J, Louis NA, Montalto MC, Colgan SP. Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene. Cancer Res. 2002; 62: 3387-3394. (Pubitemid 34651384)
46. Krishnamurthy P, Ross DD, Nakanishi T, Bailey-Dell K, Zhou S, Mercer KE, Sarkadi B, Sorrentino BP, Schuetz JD. The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J. Biol.Chem. 2004; 279: 24218-24225.