Inhibition of phosphatidylcholine-specific phospholipase C results in loss of mesenchymal traits in metastatic breast cancer cells

Breast Cancer Research

Volumn 14, Issue 2, 2012, Pages

  Abalsamo, Laura ^a   Spadaro, Francesca ^a   Bozzuto, Giuseppina ^a   Paris, Luisa ^a   Cecchetti, Serena ^a   Lugini, Luana ^a   Iorio, Egidio ^a   Molinari, Agnese ^a   Ramoni, Carlo ^a   Podo, Franca ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CASEIN; GALECTIN 3; LACTADHERIN; NERVE CELL ADHESION MOLECULE; PHOSPHATIDYLCHOLINE SPECIFIC PHOSPHOLIPASE C; PHOSPHOLIPASE; TRICYCLO[4.3.0.1]DECAN 9 YL XANTHOGENATE; UNCLASSIFIED DRUG; VIMENTIN; BRIDGED COMPOUND; CADHERIN; CASEIN; CDH2 PROTEIN, HUMAN; ENZYME INHIBITOR; LEUKOCYTE ANTIGEN; MEMBRANE ANTIGEN; MFGE8 PROTEIN, HUMAN; MILK PROTEIN; PHOSPHATIDYLCHOLINE-SPECIFIC PHOSPHOLIPASE C; PHOSPHOLIPASE C; PHOSPHOLIPASE D; SPHINGOMYELIN PHOSPHODIESTERASE; THIOKETONE; TRICYCLODECANE 9 YL XANTHOGENATE; TRICYCLODECANE-9-YL-XANTHOGENATE; TUMOR MARKER;

ARTICLE; BREAST CANCER; CANCER CELL; CANCER INVASION; CARCINOGENESIS; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOSOL; HUMAN; HUMAN CELL; METASTASIS; BREAST TUMOR; CELL MOTION; CYTOLOGY; CYTOPLASM; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; MESENCHYMAL STROMA CELL; MESODERM; METABOLISM; PATHOLOGY; TUMOR CELL LINE; ULTRASTRUCTURE;

ANTIGENS, CD; ANTIGENS, SURFACE; BREAST NEOPLASMS; BRIDGED COMPOUNDS; CADHERINS; CASEINS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CYTOPLASM; ENZYME INHIBITORS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GALECTIN 3; HUMANS; MESENCHYMAL STROMAL CELLS; MESODERM; MILK PROTEINS; PHOSPHOLIPASE D; SPHINGOMYELIN PHOSPHODIESTERASE; THIONES; TUMOR MARKERS, BIOLOGICAL; TYPE C PHOSPHOLIPASES; VIMENTIN;

EID: 84858327653     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr3151     Document Type: Article

References (53)

1. Micalizzi DS, Farabaugh SM, Ford HL. Epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression. J Mammary Gland Biol Neoplasia 2010, 15:117-134. 10.1007/s10911-010-9178-9, 2886089, 20490631.
2. Podo F. Tumour phospholipid metabolism. NMR Biomed 1999, 12:413-439. 10.1002/(SICI)1099-1492(199911)12:7<413::AID-NBM587>3.0.CO;2-U, 10654290.
3. Podo F, Sardanelli F, Iorio E, Canese R, Carpinelli G, Fausto A, Canevari S. Abnormal choline phospholipid metabolism in breast and ovary cancer: molecular bases for noninvasive imaging approaches. Curr Med Imag Rev 2007, 3:123-137., http://www.ingentaconnect.com/content/ben/cmir/2007/
4. Glunde K, Artemov D, Penet MF, Jacobs MA, Bhujwalla ZM. Magnetic resonance spectroscopy in metabolic and molecular imaging and diagnosis of cancer. Chem Rev 2010, 110:3043-3059. 10.1021/cr9004007, 2877696, 20384323.
5. Janardhan S, Srivani P, Sastry GN. Choline kinase: an important target for cancer. Curr Med Chem 2006, 13:1169-1186. 10.2174/092986706776360923, 16719778.
6. Podo F, Canevari S, Canese R, Ricci A, Pisanu ME, Iorio E. MR evaluation of response to targeted treatment in cancer cells. NMR Biomed 2011, 24:648-672.
7. Beloueche-Babari M, Workman P, Leach MO. Exploiting tumor metabolism for non-invasive imaging of the therapeutic activity of molecularly targeted anticancer agents. Cell Cycle 2011, 10:2883-2893. 10.4161/cc.10.17.17192, 21857160.
8. Glunde K, Bhujwalla ZM, Ronen SM. Choline metabolism in malignant transformation. Nature Rev Cancer 2011, 11:835-848.
9. Eliyahu G, Kreizman T, Degani H. Phosphocholine as a biomarker of breast cancer: molecular and biochemical studies. Int J Cancer 2007, 120:1721-1730. 10.1002/ijc.22293, 17236204.
10. Iorio E, Mezzanzanica D, Alberti P, Spadaro F, Ramoni C, D'Ascenzo S, Millimaggi D, Pavan A, Dolo V, Canevari S, Podo F. Alterations of choline phospholipid metabolism in ovarian tumor progression. Cancer Res 2005, 65:9369-7936. 10.1158/0008-5472.CAN-05-1146, 16230400.
11. Iorio E, Ricci A, Bagnoli M, Pisanu ME, Castellano G, Di Vito M, Venturini E, Glunde K, Bhujwalla ZM, Mezzanzanica D, Canevari S, Podo F. Activation of phosphatidylcholine cycle enzymes in human epithelial ovarian cancer cells. Cancer Res 2010, 70:2126-2135. 10.1158/0008-5472.CAN-09-3833, 2831129, 20179205.
12. 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. 10.1158/0008-5472.CAN-05-1807, 16322253.
13. Ramoni C, Spadaro F, Barletta B, Dupuis ML, Podo F. Phosphatidylcholine-specific phospholipase C in mitogen-stimulated fibroblasts. Exp Cell Res 2004, 299:370-382. 10.1016/j.yexcr.2004.05.037, 15350536.
14. Liu X, Zhao Q, Araki S, Zhang S, Miao J. Contrasting effects of phosphatidylinositol- and phosphatidylcholine-specific phospholipases C on apoptosis in cultured endothelial cells. Endothelium 2006, 13:205-211. 10.1080/10623320600760423, 16840176.
15. Ramoni C, Spadaro F, Menegon M, Podo F. Cellular localization and functional role of phosphatidylcholine-specific phospholipase C in NK cells. J Immunol 2001, 167:2642-2650.
16. Spadaro F, Cecchetti S, Sanchez M, Ausiello CM, Podo F, Ramoni C. Expression and role of phosphatidylcholine-specific phospholipase C in human NK and T lymphocyte subsets. Eur J Immunol 2006, 36:3277-3287. 10.1002/eji.200635927, 17111345.
17. Cecchetti S, Spadaro F, Lugini L, Podo F, Ramoni C. Functional role of phosphatidylcholine-specific phospholipase C in regulating CD16 membrane expression in natural killer cells. Eur J Immunol 2007, 37:2912-2922. 10.1002/eji.200737266, 17899539.
18. Fantuzzi L, Spadaro F, Purificato C, Cecchetti S, Podo F, Belardelli F, Gessani S, Ramoni C. Phosphatidylcholine-specific phospholipase C activation is required for CCR5-dependent, NF-kB-driven CCL2 secretion elicited in response to HIV-1 gp120 in human primary macrophages. Blood 2008, 111:3355-3363. 10.1182/blood-2007-08-104901, 2275005, 18203956.
19. Wang N, Sun C, Huo S, Zhang Y, Zhao J, Zhang S, Miao J. Cooperation of phosphatidylcholine-specific phospholipase C and basic fibroblast growth factor in the neural differentiation of mesenchymal stem cells in vitro. Int J Biochem Cell Biol 2008, 40:294-306. 10.1016/j.biocel.2007.08.003, 17890138.
20. Spadaro F, Ramoni C, Mezzanzanica D, Miotti S, Alberti P, Cecchetti S, Iorio E, Dolo V, Canevari S, Podo F. Phosphatidylcholine-specific phospholipase C activation in epithelial ovarian cancer cells. Cancer Res 2008, 68:6541-6549. 10.1158/0008-5472.CAN-07-6763, 18701477.
21. Paris L, Cecchetti S, Spadaro F, Abalsamo L, Lugini L, Pisanu ME, Iorio E, Natali PG, Ramoni C, Podo F. Inhibition of phosphatidylcholine-specific phospholipase C downregulates HER2 overexpression on plasma membrane of breast cancer cells. Breast Cancer Res 2010, 12:R27. 10.1186/bcr2575, 2917016, 20462431.
22. Amtmann E. The antiviral, antitumoral xanthate D609 is a competitive inhibitor of phosphatidylcholine-specific phospholipase C. Drug Exp Clin Res 1996, 22:287-294.
23. Chan SYV, Hilchie AL, Brown MG, Anderson R, Hoskin DW. Apoptosis induced by intracellular ceramide accumulation in MDA-MB-435 breast carcinoma cells is dependent on the generation of reactive oxygen species. Exp Mol Pathol 2007, 82:1-11. 10.1016/j.yexmp.2006.03.001, 16624283.
24. Podo F, Ferretti A, Knijn A, Zhang P, Ramoni C, Barletta B, Pini C, Baccarini S, Pulciani S. Detection of phosphatidylcholine-specific phospholipase C in NIH-3T3 fibroblasts and their H-ras transformants: NMR and immunochemical studies. Anticancer Res 1996, 16:1399-1412.
25. Clark MA, Shorr RG, Bomalaski JS. Antibodies prepared to Bacillus cereus phospholipase C crossreact with a phosphatidylcholine preferring phospholipase C in mammalian cells. Biochem Biophys Res Commun 1986, 140:114-119. 10.1016/0006-291X(86)91065-X, 3096314.
26. Meng A, Luberto C, Meier P, Bai A, Yang X, Hannun YA, Zhou D. Sphingomyelin synthase as a potential target for D609-induced apoptosis in U937 human monocytic leukemia cells. Exp Cell Res 2004, 292:385-392. 10.1016/j.yexcr.2003.10.001, 14697345.
27. Iorio E, Di Vito M, Spadaro F, Ramoni C, Lococo E, Carnevale R, Lenti L, Strom R, Podo F. Triacsin C inhibits the formation of 1H NMR-visible mobile lipids and lipid bodies in HuT 78 apoptotic cells. Biochim Biophys Acta 2003, 1634:1-14.
28. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipids from animal tissue. J Biol Chem 1957, 226:497-509.
29. Albini A, Iwamoto Y, Kleinman HK, Martin GR, Aaronson SA, Kozlowski JM, McEwan RN. A rapid in vitro assay for quantitating the invasive potential of tumor cells. Cancer Res 1987, 47:3239-3245.
30. Colone M, Calcabrini A, Toccacieli L, Bozzuto G, Stringaro A, Gentile M, Cianfriglia M, Ciervo A, Caragia M, Budillon A, Meo G, Arancia G, Molinari A. The multidrug transporter P-glycoprotein: a mediator of melanoma invasion?. J Invest Dermatol 2008, 128:957-971. 10.1038/sj.jid.5701082, 17943188.
31. Mateos MV, Salvador GA, Giusto NM. Selective localization of phosphatidylcholine-derived signaling in detergent-resistant membranes from synaptic endings. Biochim Biophys Acta 2010, 1798:624-636. 10.1016/j.bbamem.2009.12.008, 20026046.
32. Drabsch Y, Ramsay RG, Gonda TJ. MYB suppresses differentiation and apoptosis of human breast cancer cells. Breast Cancer Res 2010, 12:R55. 10.1186/bcr2614, 2949644, 20659323.
33. Gocze PM, Freeman DA. Factors underlying the variability of lipid droplet fluorescence in MA-10 Leydig tumor cells. Cytometry 1994, 17:151-158. 10.1002/cyto.990170207, 7835165.
34. Münster PN, Srethapakdi M, Moasser MM, Rosen N. Inhibition of heat shock protein 90 function by ansamycins causes the morphological and functional differentiation of breast cancer cells. Cancer Res 2001, 61:2945-2952.
35. Kokkinos MI, Wong MK, Newgreen DF, Thompson EW, Waltham M. Vimentin and epithelial-mesenchymal transition in human breast cancer - observations in vitro and in vivo. Cells Tissues Organs 2007, 185:191-203. 10.1159/000101320, 17587825.
36. Honjo Y, Nangia-Makker P, Inohara H, Raz A. Downregulation of galectin-3 suppresses tumorigenicity of human breast carcinoma cells. Clin Cancer Res 2001, 7:661-668.
37. Markowska AI, Liu FT, Panjvani N. Galectin-3 is an important mediator of VEGF- and bFGF-mediated angiogenic response. J Exp Med 2010, 207:1981-1993. 10.1084/jem.20090121, 2931172, 20713592.
38. Neutzner M, Lopez T, Feng X, Bergmann-Leitner ES, Leitner WW, Udey MC. MFG-E8/lactadherin promotes tumor growth in an angiogenesis-dependent transgenic mouse model of multistage carcinogenesis. Cancer Res 2007, 67:6777-6785. 10.1158/0008-5472.CAN-07-0165, 17638889.
39. Yang C, Hayashida T, Forster N, Li C, Shen D, Maheswaran S, Chen L, Anderson KS, Ellisen LW, Sgroi D, Schmidt EV. The integrin αvβ3-5 ligand MFG-E8 is a p63/p73 target gene in triple negative breast cancers but exhibits suppressive functions in ER+ and erbB2+ breast cancers. Cancer Res 2011, 71:937-945. 10.1158/0008-5472.CAN-10-1471, 3074111, 21127199.
40. Charras G, Paluch E. Blebs lead the way: how to migrate without lamellipodia. NatRev Mol Cell Biol 2008, 9:730-736.
41. Singh ATK, Radeff JM, Kunnel JG, Stern PH. Phosphatidylcholine-specific phospholipase C inhibitor, tricyclodecan-9-yl xanthogenate (D609), increases phospholipase D-mediated phosphatidylcholine hydrolysis in UMR-106 osteoblastic osteosarcoma cells. Biochim Biophys Acta 2000, 1487:201-208.
42. Kang Y, Massagué J. Epithelial-mesenchymal transitions: twist in development and metastasis. Cell 2004, 118:277-279. 10.1016/j.cell.2004.07.011, 15294153.
43. Larue L, Bellacosa A. Epithelial-mesenchymal transition in development and cancer: role of phosphatidylinositol 3' kinase/AKT pathways. Oncogene 2005, 24:7443-7454. 10.1038/sj.onc.1209091, 16288291.
44. Yan W, Cao QJ, Arenas RB, Bentley B, Shao R. GATA3 inhibits breast cancer metastasis through the reversal of epithelial-mesenchymal transition. J Biol Chem 2010, 285:14042-14051. 10.1074/jbc.M110.105262, 2859565, 20189993.
45. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbel LL, Polyak K, Brisken C, Yang J, Weinberg RA. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715. 10.1016/j.cell.2008.03.027, 2728032, 18485877.
46. Glinsky VV, Kiriakova G, Glinskii OV, Mossine VV, Mawhinney TP, Turk JR, Glinskii AB, Huxley VH, Price JE, Glinsky GV. Synthetic galectin-3 inhibitor increases metastatic cancer cell sensitivity to taxol-induced apoptosis in vitro and in vivo. Neoplasia 2009, 11:901-909. 2735801, 19724684.
47. Guarino M, Rubino B, Ballabio G. The role of epithelial-mesenchymal transition in cancer pathology. Pathology 2007, 39:305-318. 10.1080/00313020701329914, 17558857.
48. Zhou H, Huang S. mTOR signaling in cancer cell motility and tumor metastasis. Crit Rev Eukaryot Gene Expr 2010, 10:1-16.
49. Platet N, Prévostel C, Derocq D, Joubert D, Rochefort H, Garcia M. Breast cancer cell invasiveness: correlation with protein kinase C activity and differential regulation by phorbol ester in estrogen receptor-positive and -negative cells. Int J Cancer 1998, 75:750-756. 10.1002/(SICI)1097-0215(19980302)75:5<750::AID-IJC14>3.0.CO;2-A, 9495244.
50. Beloueche-Babari M, Peak JC, Jackson LE, Tiet MY, Leach MO, Eccles SA. Changes in choline metabolism as potential biomarkers of phospholipase Cγ-1 inhibition in human prostate cancer cells. Mol Cancer Ther 2009, 8:1305-1311. 10.1158/1535-7163.MCT-09-0039, 19417158.
51. Rizzo MA, Shome K, Watkins SC, Romero G. The recruitment of raf-1 to membranes is mediated by direct interaction with phosphatidic acid and is independent of association with Ras. J Biol Chem 2000, 275:23911-23918. 10.1074/jbc.M001553200, 10801816.
52. Zhao C, Du G, Skowronek K, Frohamn MA, Bar-Sagi D. Phospholipase D2-generated phosphatidic acid couples EGFR stimulation to Ras activation by SoS. Nat Cell Biol 2007, 9:706-712.
53. Mérida I, Avila-Flores A, Garcia J, Merino E, Almena M, Torres-Ayuso P. Diacylglycerol kinase alpha, from negative modulation of T cell activation to control of cancer progression. Adv Enzyme Regul 2009, 49:174-188. 10.1016/j.advenzreg.2009.01.003, 19534031.