Screening and X-ray crystal structure-based optimization of autotaxin (ENPP2) inhibitors, using a newly developed fluorescence probe

ACS Chemical Biology

Volumn 8, Issue 8, 2013, Pages 1713-1721

  Kawaguchi, Mitsuyasu ^a   Okabe, Takayoshi ^a   Okudaira, Shinichi ^b   Nishimasu, Hiroshi ^a   Ishitani, Ryuichiro ^a   Kojima, Hirotatsu ^a   Nureki, Osamu ^a   Aoki, Junken ^b   Nagano, Tetsuo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; AUTOTAXIN INHIBITOR; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; DRUG INHIBITION; DRUG SCREENING; DRUG STRUCTURE; FLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR LIBRARY; MOLECULAR PROBE; PRIORITY JOURNAL; SENSITIVITY AND SPECIFICITY; X RAY;

CRYSTALLOGRAPHY, X-RAY; DRUG EVALUATION, PRECLINICAL; ENZYME ACTIVATION; ENZYME INHIBITORS; FLUORESCENT DYES; INHIBITORY CONCENTRATION 50; LIMIT OF DETECTION; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PHOSPHORIC DIESTER HYDROLASES; SMALL MOLECULE LIBRARIES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84882778016     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb400150c     Document Type: Article

References (43)

1. Stracke, M. L., Krutzsch, H. C., Unsworth, E. J., Arestad, A., Cioce, V., Schiffmann, E., and Liotta, L. A. (1992) Autotaxin is an exoenzyme possessing 5′-nucleotide phosphodiesterase/ATP pyrophosphatase and ATPase activities J. Biol. Chem. 267, 2524-2529
2. 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
3. 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
4. Aoki, J., Inoue, A., and Okudaira, S. (2008) Two pathways for lysophosphatidic acid production Biochim. Biophys. Acta 1781, 513-518
5. 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
6. van Meeteren, L. A., Ruurs, P., Stortelers, C., Bouwman, P., van Rooijen, M. A., PradeÌre, J. P., Pettit, T. R., Wakelam, M. J., Saulnier-Blache, J. S., Mummery, C. L., Moolenaar, W. H., and Jonkers, J. (2006) Autotaxin, a secreted lysophospholipase D, is essential for blood vessel formation during development Mol. Cell. Biol. 26, 5015-5022
7. 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
8. Koike, S., Keino-Masu, K., Ohto, T., Sugiyama, F., Takahashi, S., and Masu, M. (2009) Autotaxin/lysophospholipase D-mediated lysophosphatidic acid signaling is required to form distinctive large lysosomes in the visceral endoderm cells of the mouse yolk sac J. Biol. Chem. 284, 33561-33570
9. Inoue, M., Rashid, M. H., Fujita, R., Contos, J. J., Chun, J., and Ueda, H. (2004) Initiation of neuropathic pain requires lysophosphatidic acid receptor signaling Nat. Med. 10, 712-718
10. Yang, S. Y., Lee, J., Park, C. G., Kim, S., Hong, S., Chung, H. C., Min, S. K., Han, J. W., Lee, H. W., and Lee, H. Y. (2002) Expression of autotaxin (NPP-2) is closely linked to invasiveness of breast cancer cells Clin. Exp. Metastasis 19, 603-608
11. Kishi, Y., Okudaira, S., Tanaka, M., Hama, K., Shida, D., Kitayama, J., Yamori, T., Aoki, J., Fujimaki, T., and Arai, H. (2006) Autotaxin is overexpressed in glioblastoma multiforme and contributes to cell motility of glioblastoma by converting lysophosphatidylcholine to lysophosphatidic acid J. Biol. Chem. 281, 17492-17500
12. Mills, G. B. and Moolenaar, W. H. (2003) The emerging role of lysophosphatidic acid in cancer Nat. Rev. Cancer 3, 582-591
13. van Meeteren, L. A. and Moolenaar, W. H. (2007) Regulation and biological activities of the autotaxin-LPA axis Prog. Lipid Res. 46, 145-160
14. Tania, M., Khan, M. A., Zhang, H., Li, J., and Song, Y. (2010) Autotaxin: a protein with two faces Biochem. Biophys. Res. Commun. 401, 493-497
15. Pamuklar, Z., Federico, L., Liu, S., Umezu-Goto, M., Dong, A., Panchatcharam, M., Fulkerson, Z., Berdyshev, E., Natarajan, V., Fang, X., van Meeteren, L. A., Moolenaar, W. H., Mills, G. B., Morris, A. J., and Smyth, S. S. (2009) Autotaxin/lysopholipase D and lysophosphatidic acid regulate murine hemostasis and thrombosis J. Biol. Chem. 284, 7385-7394
16. Hama, K., Aoki, J., Fukaya, M., Kishi, Y., Sakai, T., Suzuki, R., Ohta, H., Yamori, T., Watanabe, M., Chun, J., and Arai, H. (2004) Lysophosphatidic acid and autotaxin stimulate cell motility of neoplastic and non-neoplastic cells through LPA1 J. Biol. Chem. 279, 17634-17639
17. van Corven, E. J., Groenink, A., Jalink, K., Eichholtz, T., and Moolenaar, W. H. (1989) Lysophosphatidate-induced cell proliferation: identification and dissection of signaling pathways mediated by G proteins Cell 59, 45-54
18. Noguchi, K., Herr, D., Mutoh, T., and Chun, J. (2009) Lysophosphatidic acid (LPA) and its receptors Curr. Opin. Pharmacol. 9, 15-23
19. Liu, S., Umezu-Goto, M., Murph, M., Lu, Y., Liu, W., Zhang, F., Yu, S., Stephens, L. C., Cui, X., Murrow, G., Coombes, K., Muller, W., Hung, M. -C., Perou, C. M., Lee, A. V., Fang, X., and Mills, G. B. (2009) Expression of autotaxin and lysophosphatidic acid receptors increases mammary tumorigenesis, invasion, and metastases Cancer Cell 15, 539-550
20. Zhou, Z., Subramanian, P., Sevilmis, G., Globke, B., Soehnlein, O., Karshovska, E., Megens, R., Heyll, K., Chun, J., Saulnier-Blache, J. S., Reinholz, M., van Zandvoort, M., Weber, C., and Schober, A. (2011) Lipoprotein-derived lysophosphatidic acid promotes atherosclerosis by releasing CXCL1 from the endothelium Cell Metab. 13, 592-600
21. Tager, A. M., LaCamera, P., Shea, B. S., Campanella, G. S., Selman, M., Zhao, Z., Polosukhin, V., Wain, J., Karimi-Shah, B. A., Kim, N. D., Hart, W. K., Pardo, A., Blackwell, T. S., Xu, Y., Chun, J., and Luster, A. D. (2008) The lysophosphatidic acid receptor LPA1 links pulmonary fibrosis to lung injury by mediating fibroblast recruitment and vascular leak Nat. Med. 14, 45-54
22. PradeÌre, J. P., Klein, J., GreÌs, S., Guigné, C., Neau, E., Valet, P., Calise, D., Chun, J., Bascands, J. L., Saulnier-Blache, J. S., and Schanstra, J. P. (2007) LPA1 receptor activation promotes renal interstitial fibrosis J. Am. Soc. Nephrol. 18, 3110-3118
23. Houben, A. J. and Moolenaar, W. H. (2011) Autotaxin and LPA receptor signaling in cancer Cancer Metastasis Rev. 30, 557-565
24. Liu, S., Murph, M., Panupinthu, N., and Mills, G. B. (2009) ATX-LPA receptor axis in inflammation and cancer Cell Cycle 8, 3695-3701
25. Nakanaga, K., Hama, K., and Aoki, J. (2010) Autotaxin-An LPA producing enzyme with diverse functions J. Biochem. 148, 13-24
26. Ferry, G., Moulharat, N., PradeÌre, J. P., Desos, P., Try, A., Genton, A., Giganti, A., Beucher-Gaudin, M., Lonchampt, M., Bertrand, M., Saulnier-Blache, J. S., Tucker, G. C., Cordi, A., and Boutin, J. A. (2008) S32826, a nanomolar inhibitor of autotaxin: discovery, synthesis and applications as a pharmacological tool J. Pharmacol. Exp. Ther. 327, 809-819
27. 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
28. Baker, D. L., Fujiwara, Y., Pigg, K. R., Tsukahara, R., Kobayashi, S., Murofushi, H., Uchiyama, A., Murakami-Murofushi, K., Koh, E., Bandle, R. W., Byun, H. S., Bittman, R., Fan, D., Murph, M., Mills, G. B., and Tigyi, G. (2006) Carba analogs of cyclic phosphatidic acid are selective inhibitors of autotaxin and cancer cell invasion and metastasis J. Biol. Chem. 281, 22786-22793
29. 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., Moolenaar, W. H., and Ovaa, H. (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
30. Albers, H. M., van Meeteren, L. A., Egan, D. A., van Tilburg, E. W., Moolenaar, W. H., and Ovaa, H. (2010) Discovery and optimization of boronic acid based inhibitors of autotaxin J. Med. Chem. 53, 4958-4967
31. Gierse, J., Thorarensen, A., Beltey, K., Bradshaw-Pierce, E., Cortes-Burgos, L., Hall, T., Johnston, A., Murphy, M., Nemirovskiy, O., Ogawa, S., Pegg, L., Pelc, M., Prinsen, M., Schnute, M., Wendling, J., Wene, S., Weinberg, R., Wittwer, A., Zweifel, B., and Masferrer, J. (2010) A novel autotaxin inhibitor reduces lysophosphatidic acid levels in plasma and the site of inflammation J. Pharmacol. Exp. Ther. 334, 310-317
32. 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
33. 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., Jansen, S., Andries, M., Hall, T., Pegg, L. E., Benson, T. E., Kasiem, M., Harlos, K., Kooi, C. W., Smyth, S. S., Ovaa, H., Bollen, M., Morris, A. J., Moolenaar, W. H., and Perrakis, A. (2011) Structural basis of substrate discrimination and integrin binding by autotaxin Nat. Struct. Mol. Biol. 18, 198-204
34. Ferguson, C. G., Bigman, C. S., Richardson, R. D., van Meeteren, L. A., Moolenaar, W. H., and Prestwich, G. D. (2006) Fluorogenic phospholipid substrate to detect lysophospholipase D/autotaxin activity Org. Lett. 8, 2023-2026
35. 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
36. Kawaguchi, M., Okabe, T., Okudaira, S., Hanaoka, K., Fujikawa, Y., Terai, T., Komatsu, T., Kojima, H., Aoki, J., and Nagano, T. (2011) Fluorescence probe for lysophospholipase C/NPP6 activity and a potent NPP6 inhibitor J. Am. Chem. Soc. 133, 12021-12030
37. Bollen, M., Gijsbers, R., Ceulemans, H., Stalmans, W., and Stefan, C. (2000) Nucleotide pyrophosphatases/phosphodiesterases on the move Crit. Rev. Biochem. Mol. Biol. 35, 393-432
38. Yukiura, H., Hama, K., Nakanaga, K., Tanaka, M., Asaoka, Y., Okudaira, S., Arima, N., Inoue, A., Hashimoto, T., Arai, H., Kawahara, A., Nishina, H., and Aoki, J. (2011) Autotaxin regulates vascular development via multiple lysophosphatidic acid (LPA) receptors in zebrafish J. Biol. Chem. 286, 43972-43983
39. Nishimasu, H., Ishitani, R., Aoki, J., and Nureki, O. (2012) A 3D view of autotaxin Trends Pharmacol. Sci. 33, 138-145
40. Stefan, C., Jansen, S., and Bollen, M. (2005) NPP-type ectophosphodiesterases: Unity in diversity Trends Biochem. Sci. 30, 542-550
41. North, E. J., Howard, A., Wanjala, I., Pham, T., Baker, D., and Parrill, A. (2010) Pharmacophore development and application toward the identification of novel, small-molecule autotaxin inhibitors J. Med. Chem. 53, 3095-3105
42. 2+ coordination in the alkaline phosphatase superfamily by EXAFS and X-ray crystallography J. Mol. Biol. 415, 102-117
43. Choi, J. W., Herr, D. R., Noguchi, K., Yung, Y. C., Lee, C. W., Mutoh, T., Lin, M. E., Teo, S. T., Park, K. E., Mosley, A. N., and Chun, J. (2010) LPA receptors: Subtypes and biological actions Annu. Rev. Pharmacol. Toxicol. 50, 157-186