Controlling cancer through the autotaxin-lysophosphatidic acid receptor axis

Biochemical Society Transactions

Volumn 40, Issue 1, 2012, Pages 31-36

  Gotoh, Mari ^a,b   Fujiwara, Yuko ^a   Yue, Junming ^a   Liu, Jianxiong ^a   Lee, SueChin ^a   Fells, James ^a   Uchiyama, Ayako ^b   Murakami Murofushi, Kimiko ^b   Kennel, Stephen ^c   Wall, Jonathan ^c   Patil, Renukadevi ^d   Gupte, Renuka ^d   Balazs, Louisa ^a   Miller, Duane D ^d   Tigyi, Gabor J ^a  

^a UNIVERSITY OF TENNESSEE COLLEGE OF MEDICINE   (United States)

^b OCHANOMIZU UNIVERSITY   (Japan)

^c UNIVERSITY OF TENNESSEE GRADUATE SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

4 pentadecylbenzylphosphonic acid (4 PBA); Autotaxin; Cancer; Drug discovery; Lysophosphatidic acid (LPA); Therapy

Indexed keywords

4 PENTADECYLBENZYLPHOSPHONIC ACID; ANTIMETASTATIC AGENT; AUTOTAXIN; CARBACYCLIC PHOSPHATIDIC ACID; CISPLATIN; DOXORUBICIN; LYSOPHOSPHATIDIC ACID; LYSOPHOSPHATIDIC ACID RECEPTOR; LYSOPHOSPHATIDYLCHOLINE; LYSOPHOSPHATIDYLSERINE; PACLITAXEL; UNCLASSIFIED DRUG;

ANGIOGENESIS; APOPTOSIS; BREAST CANCER; CANCER CELL; CELL INVASION; CELL MOTILITY; CELL PROLIFERATION; CELL SURVIVAL; DOWN REGULATION; DRUG TARGETING; ENDOTHELIUM CELL; GENE DOSAGE; GENE EXPRESSION; HUMAN; MALIGNANT TRANSFORMATION; MELANOMA; MELANOMA CELL; MESOTHELIUM CELL; METASTASIS; METASTASIS INHIBITION; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; PROGNOSIS; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; ANTINEOPLASTIC AGENTS; HUMANS; LYSOPHOSPHOLIPIDS; MOLECULAR TARGETED THERAPY; NEOPLASM INVASIVENESS; NEOPLASMS; PHOSPHODIESTERASE INHIBITORS; PHOSPHONIC ACIDS; PHOSPHORIC DIESTER HYDROLASES; RECEPTORS, LYSOPHOSPHATIDIC ACID; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84863011845     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20110608     Document Type: Review

References (50)

1. Mills, G.B. and Moolenaar, W.H. (2003) The emerging role of lysophosphatidic acid in cancer. Nat. Rev. Cancer 3, 582-591 (Pubitemid 37328830)
2. Tigyi, G. (2010) Aiming drug discovery at lysophosphatidic acid targets. Br. J. Pharmacol. 161, 241-270
3. Stracke, M.L., Krutzsch, H.C., Unsworth, E.J., Arestad, A., Cioce, V., Schiffmann, E. and Liotta, L.A. (1992) Identification, purification, and partial sequence analysis of autotaxin, a novel motility-stimulating protein. J. Biol. Chem. 267, 2524-2529
4. Tokumura, A., Majima, E., Kariya, Y., Tominaga, K., Kogure, K., Yasuda, K. and Fukuzawa, K. (2002) Identification of human plasma lysophospholipase D, a lysophosphatidic acid-producing enzyme, as autotaxin, a multifunctional phosphodiesterase. J. Biol. Chem. 277, 39436-39442 (Pubitemid 35190918)
5. Umezu-Goto, M., Kishi, Y., Taira, A., Hama, K., Dohmae, N., Takio, K., Yamori, T., Mills, G.B., Inoue, K., Aoki, J. and Arai, H. (2002) Autotaxin has lysophospholipase D activity leading to tumor cell growth and motility by lysophosphatidic acid production. J. Cell Biol. 158, 227-233
6. van Meeteren, L.A., Ruurs, P., Stortelers, C., Bouwman, P., van Rooijen, M.A., Pradere, J.P., Pettit, T.R., Wakelam, M.J., Saulnier-Blache, J.S., Mummery, C.L. et al. (2006) Autotaxin, a secreted lysophospholipase D, is essential for blood vessel formation during development. Mol. Cell. Biol. 26, 5015-5022 (Pubitemid 43955815)
7. Tanaka, M., Okudaira, S., Kishi, Y., Ohkawa, R., Iseki, S., Ota, M., Noji, S., Yatomi, Y., Aoki, J. and Arai, H. (2006) Autotaxin stabilizes blood vessels and is required for embryonic vasculature by producing lysophosphatidic acid. J. Biol. Chem. 281, 25822-25830 (Pubitemid 44401970)
8. Baker, D.L., Morrison, P., Miller, B., Riely, C.A., Tolley, B., Westermann, A.M., Bonfrer, J.M., Bais, E., Moolenaar, W.H. and Tigyi, G. (2002) Plasma lysophosphatidic acid concentration and ovarian cancer. JAMA, J. Am. Med. Assoc. 287, 3081-3082 (Pubitemid 34633980)
9. Sutphen, R., Xu, Y., Wilbanks, G.D., Fiorica, J., Grendys, Jr, E.C., LaPolla, J.P., Arango, H., Hoffman, M.S., Martino, M., Wakeley, K. et al. (2004) Lysophospholipids are potential biomarkers of ovarian cancer. Cancer Epidemiol. Biomarkers Prev. 13, 1185-1191 (Pubitemid 38917907)
10. Nakagawa, H., Ikeda, H., Nakamura, K., Ohkawa, R., Masuzaki, R., Tateishi, R., Yoshida, H., Watanabe, N., Tejima, K., Kume, Y. et al. (2011) Autotaxin as a novel serum marker of liver fibrosis. Clin. Chim. Acta 412, 1201-1206
11. Watanabe, N., Ikeda, H., Nakamura, K., Ohkawa, R., Kume, Y., Aoki, J., Hama, K., Okudaira, S., Tanaka, M., Tomiya, T. et al. (2007) Both plasma lysophosphatidic acid and serum autotaxin levels are increased in chronic hepatitis C. J. Clin. Gastroenterol. 41, 616-623 (Pubitemid 46956520)
12. Iwasawa, Y., Fujii, T., Nagamatsu, T., Kawana, K., Okudaira, S., Miura, S., Matsumoto, J., Tomio, A., Hyodo, H., Yamashita, T. et al. (2009) Expression of autotaxin, an ectoenzyme that produces lysophosphatidic acid, in human placenta. Am. J. Reprod. Immunol. 62, 90-95
13. Kimura, T., Itoh, T., Fusazaki, T., Matsui, H., Sugawara, S., Ogino, Y., Endo, H., Kobayashi, K. and Nakamura, M. (2010) Low-density lipoprotein- cholesterol/high-density lipoprotein-cholesterol ratio predicts lipid-rich coronary plaque in patients with coronary artery disease: integrated-backscatter intravascular ultrasound study. Circ. J. 74, 1392-1398
14. Dimova, I., Raitcheva, S., Dimitrov, R., Doganov, N. and Toncheva, D. (2006) Correlations between c-myc gene copy-number and clinicopathological parameters of ovarian tumours. Eur. J. Cancer 42, 674-679 (Pubitemid 43343691)
15. Xu, Y., Shen, Z., Wiper, D.W., Wu, M., Morton, R.E., Elson, P., Kennedy, A.W., Belinson, J., Markman, M. and Casey, G. (1998) Lysophosphatidic acid as a potential biomarker for ovarian and other gynecologic cancers. JAMA, J. Am. Med. Assoc. 719-723 (Pubitemid 28405297)
16. Masuda, A., Nakamura, K., Izutsu, K., Igarashi, K., Ohkawa, R., Jona, M., Higashi, K., Yokota, H., Okudaira, S., Kishimoto, T. et al. (2008) Serum autotaxin measurement in haematological malignancies: a promising marker for follicular lymphoma. Br. J. Haematol. 143, 60-70
17. Nakai, Y., Ikeda, H., Nakamura, K., Kume, Y., Fujishiro, M., Sasahira, N., Hirano, K., Isayama, H., Tada, M., Kawabe, T. et al. (2011) Specific increase in serum autotaxin activity in patients with pancreatic cancer. Clin. Biochem. 44, 576-581
18. Nakamura, K., Kishimoto, T., Ohkawa, R., Okubo, S., Tozuka, M., Yokota, H., Ikeda, H., Ohshima, N., Mizuno, K. and Yatomi, Y. (2007) Suppression of lysophosphatidic acid and lysophosphatidylcholine formation in the plasma in vitro: proposal of a plasma sample preparation method for laboratory testing of these lipids. Anal. Biochem. 367, 20-27 (Pubitemid 46935610)
19. Bolen, A.L., Naren, A.P., Yarlagadda, S., Beranova-Giorgianni, S., Chen, L., Norman, D., Baker, D.L., Rowland, M.M., Best, M.D., Sano, T. et al. (2011) The phospholipase A1 activity of lysophospholipase A-I links platelet activation to LPA production during blood coagulation. J. Lipid Res. 52, 958-970
20. Euer, N., Schwirzke, M., Evtimova, V., Burtscher, H., Jarsch, M., Tarin, D. and Weidle, U.H. (2002) Identification of genes associated with metastasis of mammary carcinoma in metastatic versus non-metastatic cell lines. Anticancer Res. 22, 733-740 (Pubitemid 34475222)
21. Liu, S., Umezu-Goto, M., Murph, M., Lu, Y., Liu, W., Zhang, F., Yu, S., Stephens, L.C., Cui, X., Murrow, G. et al. (2009) Expression of autotaxin and lysophosphatidic acid receptors increases mammary tumorigenesis, invasion, and metastases. Cancer Cell 15, 539-550
22. Samadi, N., Gaetano, C., Goping, I.S. and Brindley, D.N. (2009) Autotaxin protects MCF-7 breast cancer and MDA-MB-435 melanoma cells against Taxol-induced apoptosis. Oncogene 28, 1028-1039
23. E, S., Lai, Y.J., Tsukahara, R., Chen, C.S., Fujiwara, Y., Yue, J., Yu, J.H., Guo, H., Kihara, A., Tigyi, G. and Lin, F.T. (2009) Lysophosphatidic acid 2 receptor-mediated supramolecular complex formation regulates its antiapoptotic effect. J. Biol. Chem. 284, 14558-14571
24. Jazaeri, A.A., Awtrey, C.S., Chandramouli, G.V., Chuang, Y.E., Khan, J., Sotiriou, C., Aprelikova, O., Yee, C.J., Zorn, K.K., Birrer, M.J. et al. (2005) Gene expression profiles associated with response to chemotherapy in epithelial ovarian cancers. Clin. Cancer Res. 11, 6300-6310 (Pubitemid 41262961)
25. Vidot, S., Witham, J., Agarwal, R., Greenhough, S., Bamrah, H.S., Tigyi, G.J., Kaye, S.B. and Richardson, A. (2010) Autotaxin delays apoptosis induced by carboplatin in ovarian cancer cells. Cell. Signalling 22, 926-935
26. Müller, R., Berliner, C., Leptin, J., Pörtner, D., Bialecki, W., Kleuser, B., Schumacher, U. and Milićević, N.M. (2010) Expression of sphingosine-1-phosphate receptors and lysophosphatidic acid receptors on cultured and xenografted human colon, breast, melanoma, and lung tumor cells. Tumour Biol. 31, 341-349
27. Boucharaba, A., Serre, C.M., Guglielmi, J., Bordet, J.C., Clezardin, P. and Peyruchaud, O. (2006) The type 1 lysophosphatidic acid receptor is a target for therapy in bone metastases. Proc. Natl. Acad. Sci. U.S.A. 103, 9643-9648 (Pubitemid 43955878)
28. Park, S.Y., Jeong, K.J., Panupinthu, N., Yu, S., Lee, J., Han, J.W., Kim, J.M., Lee, J.S., Kang, J., Park, C.G. et al. (2010) Lysophosphatidic acid augments human hepatocellular carcinoma cell invasion through LPA1 receptor and MMP-9 expression. Oncogene 30, 1351-1359
29. So, J., Wang, F.Q., Navari, J., Schreher, J. and Fishman, D.A. (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 (Pubitemid 40824659)
30. Ptaszynska, M.M., Pendrak, M.L., Bandle, R.W., Stracke, M.L. and Roberts, D.D. (2008) Positive feedback between vascular endothelial growth factor-A and autotaxin in ovarian cancer cells. Mol. Cancer Res. 6, 352-363 (Pubitemid 351416526)
31. Pustilnik, T.B., Estrella, V., Wiener, J.R., Mao, M., Eder, A., Watt, M.A., Bast, Jr, R.C. and Mills, G.B. (1999) Lysophosphatidic acid induces urokinase secretion by ovarian cancer cells. Clin. Cancer Res. 5, 3704-3710
32. Murthi, P., Barker, G., Nowell, C.J., Rice, G.E., Baker, M.S., Kalionis, B. and Quinn, M.A. (2004) Plasminogen fragmentation and increased production of extracellular matrix-degrading proteinases are associated with serous epithelial ovarian cancer progression. Gynecol. Oncol. 92, 80-88 (Pubitemid 38147375)
33. Lee, Z., Cheng, C.T., Zhang, H., Subler, M.A., Wu, J., Mukherjee, A., Windle, J.J., Chen, C.K. and Fang, X. (2008) Role of LPA4/p2y9/GPR23 in negative regulation of cell motility. Mol. Biol. Cell 19, 5435-5445
34. Hausmann, J., Kamtekar, S., Christodoulou, E., Day, J.E., Wu, T., Fulkerson, Z., Albers, H.M., van Meeteren, L.A., Houben, A.J., van Zeijl, L. et al. (2011) Structural basis of substrate discrimination and integrin binding by autotaxin. Nat. Struct. Mol. Biol. 18, 198-204
35. Nishimasu, H., Okudaira, S., Hama, K., Mihara, E., Dohmae, N., Inoue, A., Ishitani, R., Takagi, J., Aoki, J. and Nureki, O. (2011) Crystal structure of autotaxin and insight into GPCR activation by lipid mediators. Nat. Struct. Mol. Biol. 18, 205-212
36. Mukai, M., Nakamura, H., Tatsuta, M., Iwasaki, T., Togawa, A., Imamura, F. and Akedo, H. (2000) Hepatoma cell migration through a mesothelial cell monolayer is inhibited by cyclic AMP-elevating agents via a Rho-dependent pathway. FEBS Lett. 484, 69-73
37. Jansen, S., Andries, M., Vekemans, K., Vanbilloen, H., Verbruggen, A. and Bollen, M. (2009) Rapid clearance of the circulating metastatic factor autotaxin by the scavenger receptors of liver sinusoidal endothelial cells. Cancer Lett. 284, 216-221
38. Albers, H.M., Dong, A., van Meeteren, L.A., Egan, D.A., Sunkara, M., van Tilburg, E.W., Schuurman, K., van Tellingen, O., Morris, A.J., Smyth, S.S. et al. (2010) Boronic acid-based inhibitor of autotaxin reveals rapid turnover of LPA in the circulation. Proc. Natl. Acad. Sci. U.S.A. 107, 7257-7262
39. Kanda, H., Newton, R., Klein, R., Morita, Y., Gunn, M.D. and Rosen, S.D. (2008) Autotaxin, an ectoenzyme that produces lysophosphatidic acid, promotes the entry of lymphocytes into secondary lymphoid organs. Nat. Immunol. 9, 415-423 (Pubitemid 351405111)
40. Matsuzaki, S., Ishizuka, T., Hisada, T., Aoki, H., Komachi, M., Ichimonji, I., Utsugi, M., Ono, A., Koga, Y., Dobashi, K. et al. (2010) Lysophosphatidic acid inhibits CC chemokine ligand 5/RANTES production by blocking IRF-1-mediated gene transcription in human bronchial epithelial cells. J. Immunol. 185, 4863-4872
41. Im, E., Motiejunaite, R., Aranda, J., Park, E.Y., Federico, L., Kim, T.I., Clair, T., Stracke, M.L., Smyth, S. and Kazlauskas, A. (2010) Phospholipase Cγactivation drives increased production of autotaxin in endothelial cells and lysophosphatidic acid-dependent regression. Mol. Cell. Biol. 30, 2401-2410
42. Inoue, M., Ma, L., Aoki, J., Chun, J. and Ueda, H. (2008) Autotaxin, a synthetic enzyme of lysophosphatidic acid (LPA), mediates the induction of nerve-injured neuropathic pain. Mol. Pain. 4, 6
43. Gupte, R., Patil, R., Liu, J., Wang, Y., Lee, S.C., Fujiwara, Y., Fells, J., Bolen, A.L., Emmons-Thompson, K., Yates, C.R. et al. (2011) Benzyl and naphthalene methylphosphonic acid inhibitors of autotaxin with anti-invasive and anti-metastatic activity. ChemMedChem 6, 922-935
44. David, M., Wannecq, E., Descotes, F., Jansen, S., Deux, B., Ribeiro, J., Serre, C.M., Gres, S., Bendriss-Vermare, N., Bollen, M. et al. (2010) Cancer cell expression of autotaxin controls bone metastasis formation in mouse through lysophosphatidic acid-dependent activation of osteoclasts. PLoS ONE 5, e9741
45. van Meeteren, L.A., Ruurs, P., Christodoulou, E., Goding, J.W., Takakusa, H., Kikuchi, K., Perrakis, A., Nagano, T. and Moolenaar, W.H. (2005) Inhibition of autotaxin by lysophosphatidic acid and sphingosine 1-phosphate. J. Biol. Chem. 280, 21155-21161 (Pubitemid 40805676)
46. Baker, D.L., Fujiwara, Y., Pigg, K.R., Tsukahara, R., Kobayashi, S., Murofushi, H., Uchiyama, A., Murakami-Murofushi, K., Koh, E., Bandle, R.W. et al. (2006) Carba analogs of cyclic phosphatidic acid are selective inhibitors of autotaxin and cancer cell invasion and metastasis. J. Biol. Chem. 281, 22786-22793
47. Uchiyama, A., Mukai, M., Fujiwara, Y., Kobayashi, S., Kawai, N., Murofushi, H., Inoue, M., Enoki, S., Tanaka, Y., Niki, T. et al. (2007) Inhibition of transcellular tumor cell migration and metastasis by novel carba-derivatives of cyclic phosphatidic acid. Biochim. Biophys. Acta 1771, 103-112 (Pubitemid 46073879)
48. Gupte, R., Siddam, A., Lu, Y., Li, W., Fujiwara, Y., Panupinthu, N., Pham, T.C., Baker, D.L., Parrill, A.L., Gotoh, M. et al. (2010) Synthesis and pharmacological evaluation of the stereoisomers of 3-carba cyclic-phosphatidic acid. Bioorg. Med. Chem. Lett. 20, 7525-7528
49. Zhang, H., Xu, X., Gajewiak, J., Tsukahara, R., Fujiwara, Y., Liu, J., Fells, J.I., Perygin, D., Parrill, A.L., Tigyi, G. and Prestwich, G.D. (2009) Dual activity lysophosphatidic acid receptor pan-antagonist/autotaxin inhibitor reduces breast cancer cell migration in vitro and causes tumor regression in vivo. Cancer Res. 69, 5441-5449
50. Xu, X. and Prestwich, G.D. (2010) Inhibition of tumor growth and angiogenesis by a lysophosphatidic acid antagonist in an engineered three-dimensional lung cancer xenograft model. Cancer 116, 1739-1750