Autotaxin protects MCF-7 breast cancer and MDA-MB-435 melanoma cells against Taxol-induced apoptosis

Oncogene

Volumn 28, Issue 7, 2009, Pages 1028-1039

  Samadi, N ^a   Gaetano, C ^a   Goping, I S ^a   Brindley, D N ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Ceramides; Chemoresistance; Chemotherapy; Lysophosphatidate; Lysophosphatidylcholine; Phosphatidylinositol 3 kinase

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; AUTOTAXIN; CERAMIDE; G PROTEIN COUPLED RECEPTOR; LYSOPHOSPHATIDIC ACID; LYSOPHOSPHATIDYLCHOLINE; PACLITAXEL; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN INHIBITOR; S 32826; UNCLASSIFIED DRUG; VPC 8A202;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CATALYSIS; CELL ADHESION; CELL CYCLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL INVASION; CELL MIGRATION; CELL STRAIN MCF 7; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MELANOMA; METASTASIS; MITOCHONDRIAL MEMBRANE POTENTIAL; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TUMOR GROWTH;

APOPTOSIS; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL CYCLE; CELL LINE, TUMOR; CERAMIDES; HUMANS; LYSOPHOSPHATIDYLCHOLINES; LYSOPHOSPHOLIPIDS; MELANOMA; MEMBRANE POTENTIAL, MITOCHONDRIAL; MULTIENZYME COMPLEXES; PACLITAXEL; PHOSPHODIESTERASE I; PYROPHOSPHATASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 60549083280     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2008.442     Document Type: Article

References (72)

1. Aoki J, Taira A, Takanezawa Y, Kishi Y, Hama K, Kishimoto T et al. (2002). Serum lysophosphatidic acid is produced through diverse phospholipase pathways. J Biol Chem 277:48737-48744.
2. Asakuma J, Sumitomo M, Asano T, Asano T, Hayakawa M (2003). Selective Akt inactivation and tumor necrosis actor-related apoptosis-inducing ligand sensitization of renal cancer cells by low concentrations of paclitaxel. Cancer Res 63:1365-1370.
3. Baudhuin LM, Cristina KL, Lu J, Xu Y. (2002). Akt activation induced by lysophosphatidic acid and sphingosine-1-phosphate requires both mitogen-activated protein kinase kinase and p38 mitogen-activated protein kinase and is cell-line specific. Mol Pharmacol 62:660-671.
4. Bergstralh DT, Ting JP. (2006). Microtubule stabilizing agents: their molecular signaling consequences and the potential for enhancement by drug combination. Cancer Treat Rev 32:166-179.
5. Brindley DN. (1993). Hepatic secretion of lysphosphatidylcholine: a novel transport system for polyunsaturated fatty acids and choline. J Nutr Biochem 4:442-449.
6. Brindley DN. (2004). Lipid phosphate phosphatases and related proteins: signaling functions in development, cell division, and cancer. J Cell Biochem 92:900-912.
7. Chappell J, Leitner JW, Solomon S, Golovchenko I, Goalstone ML, Draznin B. (2001). Effect of insulin on cell cycle progression in MCF-7 breast cancer cells. Direct and potentiating influence. J Biol Chem 276:38023-38028.
8. Charles AG, Han TY, Liu YY, Hansen N, Giuliano AE, Cabot MC. (2001). Taxol-induced ceramide generation and apoptosis in human breast cancer cells. Cancer Chemother Pharmacol 47:444-450.
9. Chen M, Towers LN, O'Connor KL. (2007). LPA2 (EDG4) mediates Rho-dependent chemotaxis with lower efficacy than LPA1 (EDG2) in breast carcinoma cells. Am J Physiol Cell Physiol 292:C1927-C1933.
10. Clair T, Aoki J, Koh E, Bandle RW, Nam SW, Ptaszynska MM et al. (2003). Autotaxin hydrolyzes sphingosylphosphorylcholine to produce the regulator of migration, sphingosine-1-phosphate. Cancer Res 63:5446-5453.
11. Contos JJ, Fukushima N, Weiner JA, Kaushal D, Chun J. (2000). Requirement for the lpA1 lysophosphatidic acid receptor gene in normal suckling behavior. Proc Natl Acad Sci USA 97:13384-13389.
12. Croset M, Brossard N, Polette A, Lagarde M. (2000). Characterization of plasma unsaturated lysophosphatidylcholines in human and rat. Biochem J 345(Part 1):61-67.
13. Cui P, Tomsig JL, McCalmont WF, Lee S, Becker CJ, Lynch KR et al. (2007). Synthesis and biological evaluation of phosphonate derivatives as autotaxin (ATX) inhibitors. Bioorg Med Chem Lett 17:1634-1640.
14. Demidenko ZN, Kalurupalle S, Hanko C, Lim CU, Broude E, Blagosklonny MV. (2008). Mechanism of G1-like arrest by low concentrations of paclitaxel: next cell cycle p53-dependent arrest with sub G1 DNA content mediated by prolonged mitosis. Oncogene 27:4402-4410.
15. Dennis J, Nogaroli L, Fuss B. (2005). Phosphodiesterase-Ialpha/autotaxin (PD-Ialpha/ATX): a multifunctional protein involved in central nervous system development and disease. J Neurosci Res 82:737-742.
16. Dufour G, Demers MJ, Gagne D, Dydensborg AB, Teller IC, Bouchard V et al. (2004). Human intestinal epithelial cell survival and anoikis. Differentiation state-distinct regulation and roles of protein kinase B/Akt isoforms. J Biol Chem 279:44113-44122.
17. Fang X, Schummer M, Mao M, Yu S, Tabassam FH, Swaby R et al. (2002). Lysophosphatidic acid is a bioactive mediator in ovarian cancer. Biochim Biophys Acta 1582:257-264.
18. Fang X, Yu S, LaPushin R, Lu Y, Furui T, Penn LZ et al. (2000). Lysophosphatidic acid prevents apoptosis in fibroblasts via G(i)-protein- mediated activation of mitogen-activated protein kinase. Biochem J 352(Part 1):135-143.
19. Ferry G, Moulharat N, Pradere JP, Desos P, Try A, Genton A et al. (2008). S32826: a nanomolar inhibitor of autotaxin. Discovery, synthesis and applications as a pharmacological tool. J Pharmacol Exp Ther 327:809-819.
20. Fox MA, Alexander JK, Afshari FS, Colello RJ, Fuss B. (2004). Phosphodiesterase-I alpha/autotaxin controls cytoskeletal organization and FAK phosphorylation during myelination. Mol Cell Neurosci 27:140-150.
21. Frankel A, Mills GB. (1996). Peptide and lipid growth factors decrease cis-diamminedichloroplatinum-induced cell death in human ovarian cancer cells. Clin Cancer Res 2:1307-1313.
22. Furui T, LaPushin R, Mao M, Khan H, Watt SR, Watt MA et al. (1999). Overexpression of edg-2/vzg-1 induces apoptosis and anoikis in ovarian cancer cells in a lysophosphatidic acid- independent manner. Clin Cancer Res 5:4308-4318.
23. Gauthier R, Harnois C, Drolet JF, Reed JC, Vezina A, Vachon PH. (2001). Human intestinal epithelial cell survival: differentiation state-specific control mechanisms. Am J Physiol Cell Physiol 280:C1540-C1554.
24. Goetzl EJ, Dolezalova H, Kong Y, Hu YL, Jaffe RB, Kalli KR et al. (1999a). Distinctive expression and functions of the type 4 endothelial differentiation gene-encoded G protein-coupled receptor for lysophosphatidic acid in ovarian cancer. Cancer Res 59:5370-5375.
25. Goetzl EJ, Kong Y, Mei B. (1999b). Lysophosphatidic acid and sphingosine 1-phosphate protection of T cells from apoptosis in association with suppression of Bax. J Immunol 162:2049-2056.
26. Hama K, Aoki J, Fukaya M, Kishi Y, Sakai T, Suzuki R et al. (2004). Lysophosphatidic acid and autotaxin stimulate cell motility of neoplastic and non-neoplastic cells through LPA1. J Biol Chem 279:17634-17639.
27. Harnois C, Demers MJ, Bouchard V, Vallee K, Gagne D, Fujita N et al. (2004). Human intestinal epithelial crypt cell survival and death: complex modulations of Bcl-2 homologs by Fak, PI3-K/Akt-1, MEK/Erk, and p38 signaling pathways. J Cell Physiol 198:209-222.
28. Hu X, Haney N, Kropp D, Kabore AF, Johnston JB, Gibson SB. (2005). Lysophosphatidic acid (LPA) protects primary chronic lymphocytic leukemia cells from apoptosis through LPA receptor activation of the anti-apoptotic protein AKT/PKB. J Biol Chem 280:9498-9508.
29. Inoue CN, Nagano I, Ichinohasama R, Asato N, Kondo Y, Iinuma K. (2001). Bimodal effects of platelet-derived growth factor on rat mesangial cell proliferation and death, and the role of lysophosphatidic acid in cell survival. Clin Sci (Lond) 101:11-19.
30. Jasinska R, Zhang QX, Pilquil C, Singh I, Xu J, Dewald J et al. (1999). Lipid phosphate phosphohydrolase-1 degrades exogenous glycerolipid and sphingolipid phosphate esters. Biochem J 340(Part 3):677-686.
31. Jemal A, Siegel R, Ward E, Murray T, Xu J, Smigal C et al. (2006). Cancer statistics, 2006. CA Cancer J Clin 56:106-130.
32. Kabarowski JH, Zhu K, Le LQ, Witte ON, Xu Y. (2001). Lysophosphatidylcholine as a ligand for the immunoregulatory receptor G2A. Science 293:702-705.
33. Kim KS, Ren J, Jiang Y, Ebrahem Q, Tipps R, Cristina K et al. (2005). GPR4 plays a critical role in endothelial cell function and mediates the effects of sphingosylphosphorylcholine. FASEB J 19:819-821.
34. Koh JS, Lieberthal W, Heydrick S, Levine JS. (1998). Lysophosphatidic acid is a major serum noncytokine survival factor for murine macrophages which acts via the phosphatidylinositol 3-kinase signaling pathway. J Clin Invest 102:716-727.
35. Krajewski S, Krajewska M, Turner BC, Pratt C, Howard B, Zapata JM et al. (1999). Prognostic significance of apoptosis regulators in breast cancer. Endocr Relat Cancer 6:29-40.
36. Lee CW, Rivera R, Gardell S, Dubin AE, Chun J. (2006). GPR92 as a new G12/13- and Gq-coupled lysophosphatidic acid receptor that increases cAMP, LPA5. J Biol Chem 281:23589-23597.
37. Levine JS, Koh JS, Triaca V, Lieberthal W. (1997). Lysophosphatidic acid: a novel growth and survival factor for renal proximal tubular cells. Am J Physiol 273:F575-F585.
38. Lin P, Ye RD. (2003). The lysophospholipid receptor G2A activates a specific combination of G proteins and promotes apoptosis. J Biol Chem 278:14379-14386.
39. Marchetti P, Urien S, Cappellini GA, Ronzino G, Ficorella C. (2002). Weekly administration of paclitaxel: theoretical and clinical basis. Crit Rev Oncol Hematol 44(Suppl):S3-S13.
40. Martin A, Duffy PA, Liossis C, Gomez-Munoz A, O'Brien L, Stone JC et al. (1997). Increased concentrations of phosphatidate, diacylglycerol and ceramide in ras- and tyrosine kinase (fps)-transformed fibroblasts. Oncogene 14:1571-1580.
41. McGrogan BT, Gilmartin B, Carney DN, McCann A. (2008). Taxanes, microtubules and chemoresistant breast cancer. Biochim Biophys Acta 1785:96-132.
42. Melet A, Song K, Bucur O, Jagani Z, Grassian AR, Khosravi-Far R. (2008). Apoptotic pathways in tumor progression and therapy. Adv Exp Med Biol 615:47-79.
43. Mills GB, Moolenaar WH. (2003). The emerging role of lysophosphatidic acid in cancer. Nat Rev Cancer 3:582-591.
44. Moolenaar WH, van Meeteren LA, Giepmans BN. (2004). The ins and outs of lysophosphatidic acid signaling. Bioessays 26:870-881.
45. Murph MM, Hurst-Kennedy J, Newton V, Brindley DN, Radhakrishna H. (2007). Lysophosphatidic acid decreases the nuclear localization and cellular abundance of the p53 tumor suppressor in A549 lung carcinoma cells. Mol Cancer Res 5:1201-1211.
46. Nam SW, Clair T, Campo CK, Lee HY, Liotta LA, Stracke ML. (2000). Autotaxin (ATX), a potent tumor motogen, augments invasive and metastatic potential of ras-transformed cells. Oncogene 19:241-247.
47. Nam SW, Clair T, Kim YS, McMarlin A, Schiffmann E, Liotta LA et al. (2001). Autotaxin (NPP-2), a metastasis-enhancing motogen, is an angiogenic factor. Cancer Res 61:6938-6944.
48. Pasternack SM, von Kugelgen I, Aboud KA, Lee YA, Ruschendorf F, Voss K et al. (2008). G protein-coupled receptor P2Y5 and its ligand LPA are involved in maintenance of human hair growth. Nat Genet 40:329-334.
49. Pilquil C, Dewald J, Cherney A, Gorshkova I, Tigyi G, English D et al. (2006). Lipid phosphate phosphatase-1 regulates lysophosphatidate- induced fibroblast migration by controlling phospholipase D2-dependent phosphatidate generation. J Biol Chem 281:38418-38429.
50. Radeff-Huang J, Seasholtz TM, Matteo RG, Brown JH. (2004). G protein mediated signaling pathways in lysophospholipid induced cell proliferation and survival. J Cell Biochem 92:949-966.
51. Radu CG, Yang LV, Riedinger M, Au M, Witte ON. (2004). T cell chemotaxis to lysophosphatidylcholine through the G2A receptor. Proc Natl Acad Sci USA 101:245-250.
52. Ramjaun AR, Tomlinson S, Eddaoudi A, Downward J. (2007). Upregulation of two BH3-only proteins, Bmf and Bim, during TGF beta-induced apoptosis. Oncogene 26:970-981.
53. Rikitake Y, Hirata K, Yamashita T, Iwai K, Kobayashi S, Itoh H et al. (2002). Expression of G2A, a receptor for lysophosphatidylcholine, by macrophages in murine, rabbit, and human atherosclerotic plaques. Arterioscler Thromb Vasc Biol 22:2049-2053.
54. Rusovici R, Ghaleb A, Shim H, Yang VW, Yun CC. (2007). Lysophosphatidic acid prevents apoptosis of Caco-2 colon cancer cells via activation of mitogen-activated protein kinase and phosphorylation of Bad. Biochim Biophys Acta 1770:1194-1203.
55. Sakashita F, Osada S, Takemura M, Imai H, Tomita H, Nonaka K et al. (2007). The effect of p53 gene expression on the inhibition of cell proliferation by paclitaxel. Cancer Chemother Pharmacol 62:379-385.
56. Saunders DE, Lawrence WD, Christensen C, Wappler NL, Ruan H, Deppe G. (1997). Paclitaxel-induced apoptosis in MCF-7 breast-cancer cells. Int J Cancer 70:214-220.
57. Sietsma H, Dijkhuis AJ, Kamps W, Kok JW. (2002). Sphingolipids in neuroblastoma: their role in drug resistance mechanisms. Neurochem Res 27:665-674.
58. Snyder JP, Nettles JH, Cornett B, Downing KH, Nogales E. (2001). The binding conformation of Taxol in beta-tubulin: a model based on electron crystallographic density. Proc Natl Acad Sci USA 98:5312-5316.
59. So J, Wang FQ, Navari J, Schreher J, Fishman DA. (2005). LPA-induced epithelial ovarian cancer (EOC) in vitro invasion and migration are mediated by VEGF receptor-2 (VEGF- R2). Gynecol Oncol 97:870-878.
60. Spankuch B, Kurunci-Csacsko E, Kaufmann M, Strebhardt K. (2007). Rational combinations of siRNAs targeting Plk1 with breast cancer drugs. Oncogene 26:5793-5807.
61. Stracke ML, Krutzsch HC, Unsworth EJ, Arestad A, Cioce V, Schiffmann E et al. (1992). Identification, purification, and partial sequence analysis of autotaxin, a novel motility-stimulating protein. J Biol Chem 267:2524-2529.
62. Sun B, Nishihira J, Suzuki M, Fukushima N, Ishibashi T, Kondo M et al. (2003). Induction of macrophage migration inhibitory factor by lysophosphatidic acid: relevance to tumor growth and angiogenesis. Int J Mol Med 12:633-641.
63. Swanton C, Marani M, Pardo O, Warne PH, Kelly G, Sahai E et al. (2007). Regulators of mitotic arrest and ceramide metabolism are determinants of sensitivity to paclitaxel and other chemotherapeutic drugs. Cancer Cell 11:498-512.
64. Tigyi G, Parrill AL. (2003). Molecular mechanisms of lysophosphatidic acid action. Prog Lipid Res 42:498-526.
65. Tomura H, Mogi C, Sato K, Okajima F. (2005). Proton-sensing and lysolipid-sensitive G- protein-coupled receptors: a novel type of multi-functional receptors. Cell Signal 17:1466-1476.
66. Umezu-Goto M, Kishi Y, Taira A, Hama K, Dohmae N, Takio K et al. (2002). Autotaxin has lysophospholipase D activity leading to tumor cell growth and motility by lysophosphatidic acid production. J Cell Biol 158:227-233.
67. Weiner JA, Chun J. (1999). Schwann cell survival mediated by the signaling phospholipid lysophosphatidic acid. Proc Natl Acad Sci USA 96:5233-5238.
68. Xu Y, Shen Z, Wiper DW, Wu M, Morton RE, Elson P et al. (1998). Lysophosphatidic acid as a potential biomarker for ovarian and other gynecologic cancers. Jama 280:719-723.
69. Yang SY, Lee J, Park CG, Kim S, Hong S, Chung HC et al. (2002). Expression of autotaxin (NPP-2) is closely linked to invasiveness of breast cancer cells. Clin Exp Metastasis 19:603-608.
70. Ye X, Ishii I, Kingsbury MA, Chun J. (2002). Lysophosphatidic acid as a novel cell survival/apoptotic factor. Biochim Biophys Acta 1585:108-113.
71. Yue J, Yokoyama K, Balazs L, Baker DL, Smalley D, Pilquil C et al. (2004). Mice with transgenic overexpression of lipid phosphate phosphatase-1 display multiple organotypic deficits without alteration in circulating lysophosphatidate level. Cell Signal 16:385-399.
72. Zhu K, Baudhuin LM, Hong G, Williams FS, Cristina KL, Kabarowski JH et al. (2001). Sphingosylphosphorylcholine and lysophosphatidylcholine are ligands for the G protein- coupled receptor GPR4. J Biol Chem 276:41325-41335.