Inhibition of autotaxin production or activity blocks lysophosphatidylcholine-induced migration of human breast cancer and melanoma cells

Molecular Carcinogenesis

Volumn 48, Issue 9, 2009, Pages 801-809

  Gaetano, Cristoforo G ^a   Samadi, Nasser ^a   Tomsig, Jose L ^b   Macdonald, Timothy L ^c   Lynch, Kevin R ^b   Brindley, David N ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF VIRGINIA   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Chemotherapy; Lysophosphatidate; Lysophosphatidylcholine; Metastasis

Indexed keywords

AUTOTAXIN; G PROTEIN COUPLED RECEPTOR; LYSOPHOSPHATIDIC ACID RECEPTOR; LYSOPHOSPHATIDYLCHOLINE; (4 (TETRADECANOYLAMINO)BENZYL)PHOSPHONIC ACID; (4-(TETRADECANOYLAMINO)BENZYL)PHOSPHONIC ACID; ANILIDE; ENPP2 PROTEIN, HUMAN; ENZYME INHIBITOR; INORGANIC PYROPHOSPHATASE; LYSOPHOSPHATIDIC ACID; LYSOPHOSPHOLIPID; MULTIENZYME COMPLEX; ORGANOPHOSPHATE; PHOSPHODIESTERASE I; PHOSPHONIC ACID DERIVATIVE; PYRIDINE DERIVATIVE; SMALL INTERFERING RNA; VPC32183;

ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CANCER GROWTH; CATALYSIS; CELL ADHESION; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; GLIOBLASTOMA; HUMAN; HUMAN CELL; KIDNEY CANCER; LUNG CANCER; MELANOMA; METASTASIS; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; RECEPTOR UPREGULATION; THYROID CANCER; BREAST TUMOR; CELL LINE; CELL MOTION; DRUG ANTAGONISM; DRUG EFFECT; GENETIC TRANSFECTION; GENETICS; KINETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR CELL LINE; WESTERN BLOTTING;

ANILIDES; BLOTTING, WESTERN; BREAST NEOPLASMS; CATALYSIS; CELL LINE; CELL LINE, TUMOR; CELL MOVEMENT; ENZYME INHIBITORS; HUMANS; KINETICS; LYSOPHOSPHATIDYLCHOLINES; LYSOPHOSPHOLIPIDS; MELANOMA; MULTIENZYME COMPLEXES; PHOSPHODIESTERASE I; PHOSPHONIC ACIDS; PHOSPHORIC ACID ESTERS; PYRIDINES; PYROPHOSPHATASES; RECEPTORS, LYSOPHOSPHATIDIC ACID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 70249149314     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.20524     Document Type: Article

References (47)

1. Yang SY, Lee J, Park CG, et al. Expression of autotaxin (NPP-2) is closely linked to invasiveness of breast cancer cells. Clin Exp Metastasis 2002;19:603-608. (Pubitemid 35454570)
2. Stracke ML, Krutzsch HC, Unsworth EJ, et al. Identification, purification, and partial sequence analysis of autotaxin, a novel motility-stimulating protein. J Biol Chem 1992;267:2524-2529.
3. Kishi Y, Okudaira S, Tanaka M, et al. Autotaxin is overexpressed in glioblastoma multiforme and contributes to cell motility of glioblastoma by converting lysophosphatidylcholine to lysophosphatidic acid. J Biol Chem 2006;281:17492-17500. (Pubitemid 43909557)
4. Euer N, Schwirzke M, Evtimova V, et al. Identification of genes associated with metastasis of mammary carcinoma in metastatic versus non-metastatic cell lines. Anticancer Res 2002;22:733-740. (Pubitemid 34475222)
5. Stassar MJ, Devitt G, Brosius M, et al. Identification of human renal cell carcinoma associated genes by suppression subtractive hybridization. Br J Cancer 2001;85:1372-1382. (Pubitemid 33081935)
6. Kehlen A, Englert N, Seifert A, et al. Expression, regulation and function of autotaxin in thyroid carcinomas. Int J Cancer 2004;109:833-838. (Pubitemid 38500739)
7. Umezu-Goto M, Kishi Y, Taira A, et al. Autotaxin has lysophospholipase D activity leading to tumor cell growth and motility by lysophosphatidic acid production. J Cell Biol 2002;158:227-233.
8. So J, Wang FQ, Navari J, Schreher J, Fishman DA. LPA-induced epithelial ovarian cancer (EOC) in vitro invasion and migration are mediated by VEGF receptor-2 (VEGF-R2). Gynecol Oncol 2005;97:870-878.
9. Nam SW, Clair T, Campo CK, Lee HY, Liotta LA, Stracke ML. Autotaxin (ATX), a potent tumor motogen, augments invasive and metastatic potential of ras-transformed cells. Oncogene 2000;19:241-247. (Pubitemid 30077220)
10. Nam SW, Clair T, Kim YS, et al. Autotaxin (NPP-2), a metastasis-enhancing motogen, is an angiogenic factor. Cancer Res 2001;61:6938-6944. (Pubitemid 32896522)
11. Hama K, Aoki J, Fukaya M, et al. Lysophosphatidic acid and autotaxin stimulate cell motility of neoplastic and non-neoplastic cells through LPA1. J Biol Chem 2004;279:17634-17639. (Pubitemid 38560528)
12. Fox MA, Alexander JK, Afshari FS, Colello RJ, Fuss B. Phosphodiesterase-I alpha/autotaxin controls cytoskeletal organization and FAK phosphorylation during myelination. Mol Cell Neurosci 2004;27:140-150. (Pubitemid 39370096)
13. Dennis J, Nogaroli L, Fuss B. Phosphodiesterase-Ialpha/autotaxin (PD-Ialpha/ATX): A multifunctional protein involved in central nervous system development and disease. J Neurosci Res 2005;82(6) 737-742. (Pubitemid 41746486)
14. Tokumura A, Majima E, Kariya Y, et al. Identification of human plasma lysophospholipase D, a lysophosphatidic acid-producing enzyme, as autotaxin, a multifunctional phosphodiesterase. J Biol Chem 2002;277:39436-39442. (Pubitemid 35190918)
15. Baker DL, Fujiwara Y, Pigg KR, et al. Carba analogs of cyclic phosphatidic acid are selective inhibitors of autotaxin and cancer cell invasion and metastasis. J Biol Chem 2006;281:22786-22793. (Pubitemid 44242307)
16. Brindley DN. Hepatic secretion of lysphosphatidylcholine: A novel transport system for polyunsaturated fatty acids and choline. J Nutr Biochem 1993;4:442-449.
17. Aoki J, Taira A, Takanezawa Y, et al. Serum lysophosphatidic acid is produced through diverse phospholipase pathways. J Biol Chem 2002;77:48737-48744. (Pubitemid 35470839)
18. Radu CG, Yang LV, Riedinger M, Au M, Witte ON. T cell chemotaxis to lysophosphatidylcholine through the G2A receptor. Proc Natl Acad Sci USA 2004;101:245-250. (Pubitemid 38084235)
19. Kim KS, Ren J, Jiang Y, et al. GPR4 plays a critical role in endothelial cell function and mediates the effects of sphingosylphosphorylcholine. FASEB J 2005;9:819-821. (Pubitemid 40617395)
20. Zhu K, Baudhuin LM, Hong G, et al. Sphingosylphosphorylcholine and lysophosphatidylcholine are ligands for the G protein-coupled receptor GPR4. J Biol Chem 2001;76:41325-41335. (Pubitemid 37373292)
21. Rikitake Y, Hirata K, Yamashita T, et al. Expression of G2A, a receptor for lysophosphatidylcholine, by macrophages in murine, rabbit, and human atherosclerotic plaques. Arterioscler Thromb Vasc Biol 2002;2:2049-2053. (Pubitemid 36025213)
22. Kabarowski JH, Zhu K, Le LQ, Witte ON, Xu Y. Lysophosphatidylcholine as a ligand for the immunoregulatory receptor G2A. Science 2001;93:702-705. (Pubitemid 32728673)
23. Lin P, Ye RD. The lysophospholipid receptor G2A activates a specific combination of G proteins and promotes apoptosis. J Biol Chem 2003;78:14379-14386. (Pubitemid 36799989)
24. Mills GB, Moolenaar WH. The emerging role of lysophosphatidic acid in cancer. Nat Rev Cancer 2003;3:582-591. (Pubitemid 37328830)
25. Brindley DN. Lipid phosphate phosphatases and related proteins: signaling functions in development, cell division, and cancer. J Cell Biochem 2004;92:900-912.
26. Lynch KR. Lysophospholipid receptor nomenclature. Biochim Biophys Acta 2002;1582:70-71.
27. Lee CW, Rivera R, Gardell S, Dubin AE, Chun J. GPR92 as a new G12/13- and Gq-coupled lysophosphatidic acid receptor that increases camp, LPA5. J Biol Chem 2006;281:23589-23597.
28. Pasternack SM, von Kugelgen I, Aboud KA, et al. G protein-coupled receptor P2Y5 and its ligand LPA are involved in maintenance of human hair growth. Nat Genet 2008;40:329-334.
29. Xu Y, Fang XJ, Casey G, Mills GB. Lysophospholipids activate ovarian and breast cancer cells. Biochem J 1995;309:933-940.
30. Xu Y, Gaudette DC, Boynton JD, et al. Characterization of an ovarian cancer activating factor in ascites from ovarian cancer patients. Clin Cancer Res 1995;1:1223-1232.
31. Van Leeuwen FN, Olivo C, Grivell S, Giepmans BN, Collard JG, Moolenaar WH. Rac activation by lysophosphatidic acid LPA1 receptors through the guanine nucleotide exchange factor Tiam1. J Biol Chem 2003;278:400-406. (Pubitemid 36043589)
32. Shida D, Kitayama J, Yamaguchi H, et al. Lysophosphatidic acid (LPA) enhances the metastatic potential of human colon carcinoma DLD1 cells through LPA1. Cancer Res 2003;63:1706-1711. (Pubitemid 36373664)
33. Yamada T, Sato K, Komachi M, et al. Lysophosphatidic acid (LPA) in malignant ascites stimulates motility of human pancreatic cancer cells through LPA1. J Biol Chem 2004;279:6595-6605. (Pubitemid 38248796)
34. Sun B, Nishihira J, Suzuki M, et al. Induction of macrophage migration inhibitory factor by lysophosphatidic acid: Relevance to tumor growth and angiogenesis. Int J Mol Med 2003;12:633-641.
35. Murph MM, Hurst-Kennedy J, Newton V, Brindley DN, Radhakrishna H. Lysophosphatidic acid decreases the nuclear localization and cellular abundance of the p53 tumor suppressor in A549 lung carcinoma cells. Mol Cancer Res 2007;5:1201-1211. (Pubitemid 350137115)
36. Xie Y, Meier KE. Lysophospholipase D and its role in LPA production. Cell Signal 2004;16:975-981.
37. Fourcade O, Simon MF, Viode C, et al. Secretory phospholipase A2 generates the novel lipid mediator lysophosphatidic acid in membrane microvesicles shed from activated cells. Cell 1995;80:919-927.
38. Rae JM, Creighton CJ, Meck JM, Haddad BR, Johnson MD. MDA-MB-435 cells are derived from M14 melanoma cells - A loss for breast cancer, but a boon for melanoma research. Breast Cancer Res Treat 2007;104:13-19.
39. Cui P, Tomsig JL, McCalmont WF, et al. Synthesis and biological evaluation of phosphonate derivatives as autotaxin (ATX) inhibitors. Bioorg Med Chem Lett 2007;17:1634-1640. (Pubitemid 46274360)
40. Ferry G, Moulharat N, Pradère J-P, et al. S32826: A nonomolar inhibitor of autotaxin. Discovery, synthesis and applications as a pharmacological tool. J Pharmacol Expt Therap 2008; 327:809-819.
41. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680-685.
42. Ferguson CG, Bigman CS, Richardson RD, van Meeteren LA, Moolenaar WH, Prestwich GD. Fluorogenic phospholipid substrate to detect lysophospholipase D/autotaxin activity. Org Lett 2006;8:2023-2026.
43. Lee S, Lynch KR. Brown recluse spider (Loxosceles reclusa) venom phospholipase D (PLD) generates lysophosphatidic acid (LPA). Biochem J 2005;391:317-323.
44. Seuwen K, Ludwig MG, Wolf RM. Receptors for protons or lipid messengers or both? J Recept Signal Transduct Res 2006;26:599-610.
45. Murakami N, Yokomizo T, Okuno T, Shimizu T. G2A is a proton-sensing G-protein-coupled receptor antagonized by lysophosphatidylcholine. J Biol Chem 2004;279:42484-42491. (Pubitemid 39372132)
46. Saunders LP, Ouellette A, Bandle R, et al. Identification of small-molecule inhibitors of autotaxin that inhibit melanoma cell migration and invasion. Mol Cancer Ther 2008;7:3352-3362.
47. Samadi N, Gaetano C, Goping IS, Brindley DN. Autotaxin protects MCF-7 breast cancer and MDA-MB-435 melanoma cells against Taxol-induced apoptosis. Oncogene 2008;[Epub ahead of print].