Non-invasive imaging of tumors by monitoring autotaxin activity using an enzyme-activated near-infrared fluorogenic substrate

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Madan, Damian ^a,c   Ferguson, Colin G ^a   Lee, Won Yong ^b   Prestwich, Glenn D ^b   Testa, Charles A ^a  

^a ECHELON BIOSCIENCES INC   (United States)

^b UNIVERSITY OF UTAH   (United States)

^c Intellectual Ventures   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; FEMALE; FLUORESCENT DYES; LYSOPHOSPHATIDYLCHOLINES; LYSOPHOSPHOLIPIDS; MICE; MICE, NUDE; PHOSPHORIC DIESTER HYDROLASES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84894239281     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079065     Document Type: Article

References (42)

1. Bektas M, Payne SG, Liu H, Goparaju S, Milstien S, et al. (2005) A novel acylglycerol kinase that produces lysophosphatidic acid modulates cross talk with EGFR in prostate cancer cells. J Cell Biol 169: 801-811. (Pubitemid 41002885)
2. Brindley DN, Lin FT, Tigyi GJ (2013) Role of the autotaxin- lysophosphatidate axis in cancer resistance to chemotherapy and radiotherapy. Biochim Biophys Acta 1831: 74-85.
3. Mills GB, Eder A, Fang X, Hasegawa Y, Mao M, et al. (2002) Critical role of lysophospholipids in the pathophysiology, diagnosis, and management of ovarian cancer. Cancer Treat Res 107: 259-283.
4. Parrill AL, Baker DL (2008) Autotaxin inhibition: challenges and progress toward novel anti-cancer agents. Anticancer Agents Med Chem 8: 917-923.
5. Iyer P, Lalane R 3rd, Morris C, Challa P, Vann R, et al. (2012) Autotaxin-lysophosphatidic Acid axis is a novel molecular target for lowering intraocular pressure. PLoS ONE 7: e42627.
6. Baker DL, Fujiwara Y, Pigg KR, Tsukahara R, Kobayashi S, 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.
7. Liu S, Umezu-Goto M, Murph M, Lu Y, Liu W, et al. (2009) Expression of autotaxin and lysophosphatidic acid receptors increases mammary tumorigenesis, invasion, and metastases. Cancer Cell 15: 539-550.
8. Aoki J, Taira A, Takanezawa Y, Kishi Y, Hama K, et al. (2002) Serum lysophosphatidic acid is produced through diverse phospholipase pathways. J Biol Chem 277: 48737-48744. (Pubitemid 35470839)
9. Clair T, Aoki J, Koh E, Bandle RW, Nam SW, et al. (2003) Autotaxin hydrolyzes sphingosylphosphorylcholine to produce the regulator of migration, sphingosine-1-phosphate. Cancer Res 63: 5446-5453. (Pubitemid 37139863)
10. Moolenaar WH (2002) Lysophospholipids in the limelight: autotaxin takes center stage. J Cell Biol 158: 197-199.
11. Xie Y, Meier KE (2004) Lysophospholipase D and its role in LPA production. Cell Signal 16: 975-981.
12. Nakanaga K, Hama K, Aoki J (2010) Autotaxin-an LPA producing enzyme with diverse functions. J Biochem 148: 13-24.
13. Nikitopoulou I, Oikonomou N, Karouzakis E, Sevastou I, Nikolaidou-Katsaridou N, et al. (2012) Autotaxin expression from synovial fibroblasts is essential for the pathogenesis of modeled arthritis. J Exp Med 209: 925-933.
14. Oikonomou N, Mouratis MA, Tzouvelekis A, Kaffe E, Valavanis C, et al. (2012) Pulmonary autotaxin expression contributes to the pathogenesis of pulmonary fibrosis. Am J Respir Cell Mol Biol 47: 566-574.
15. Albers HM, Ovaa H (2012) Chemical evolution of autotaxin inhibitors. Chem Rev 112: 2593-2603.
16. Gierse J, Thorarensen A, Beltey K, Bradshaw-Pierce E, Cortes-Burgos L, et al. (2010) A novel autotaxin inhibitor reduces lysophosphatidic acid levels in plasma and the site of inflammation. J Pharmacol Exp Ther 334: 310-317.
17. Bates S (2010) Progress towards personalized medicine. Drug Discov Today 15: 115-120.
18. Albers HM, Dong A, van Meeteren LA, Egan DA, Sunkara M, 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.
19. Nakamura K, Igarashi K, Ohkawa R, Yokota H, Masuda A, et al. (2012) Serum autotaxin is not a useful biomarker for ovarian cancer. Lipids 47: 927-930.
20. Xu X, Yang G, Zhang H, Prestwich GD (2009) Evaluating dual activity LPA receptor pan-antagonist/autotaxin inhibitors as anti-cancer agents in vivo using engineered human tumors. Prostaglandins Other Lipid Mediat 89: 140-146.
21. Ntziachristos V, Weissleder R (2001) Experimental three-dimensional fluorescence reconstruction of diffuse media by use of a normalized Born approximation. Opt Lett 26: 893-895. (Pubitemid 33693607)
22. Sevick-Muraca EM (2012) Translation of near-infrared fluorescence imaging technologies: emerging clinical applications. Annual review of medicine 63: 217-231.
23. Gong H, Kovar JL, Baker B, Zhang A, Cheung L, et al. (2012) Near-infrared fluorescence imaging of mammalian cells and xenograft tumors with SNAP-tag. PLoS ONE 7: e34003.
24. Kovar JL, Volcheck W, Sevick-Muraca E, Simpson MA, Olive DM (2009) Characterization and performance of a near-infrared 2-deoxyglucose optical imaging agent for mouse cancer models. Anal Biochem 384: 254-262.
25. Marshall MV, Draney D, Sevick-Muraca EM, Olive DM (2010) Single-dose intravenous toxicity study of IRDye 800CW in Sprague-Dawley rats. Mol Imaging Biol 12: 583-594.
26. Ferguson CG, Bigman CS, Richardson RD, van Meeteren LA, Moolenaar WH, et al. (2006) Fluorogenic phospholipid substrate to detect lysophospholipase D/autotaxin activity. Org Lett 8: 2023-2026. (Pubitemid 43823601)
27. Hoeglund AB, Bostic HE, Howard AL, Wanjala IW, Best MD, et al. (2010) Optimization of a pipemidic acid autotaxin inhibitor. J Med Chem 53: 1056-1066.
28. Parrill AL, Echols U, Nguyen T, Pham TC, Hoeglund A, et al. (2008) Virtual screening approaches for the identification of non-lipid autotaxin inhibitors. Bioorg Med Chem 16: 1784-1795. (Pubitemid 351226589)
29. Moolenaar WH, Perrakis A (2011) Insights into autotaxin: how to produce and present a lipid mediator. Nat Rev Mol Cell Biol 12: 674-679.
30. Nishimasu H, Ishitani R, Aoki J, Nureki O (2012) A 3D view of autotaxin. Trends Pharmacol Sci 33: 138-145.
31. Nishimasu H, Okudaira S, Hama K, Mihara E, Dohmae N, et al. (2011) Crystal structure of autotaxin and insight into GPCR activation by lipid mediators. Nat Struct Mol Biol 18: 205-212.
32. Hausmann J, Kamtekar S, Christodoulou E, Day JE, Wu T, et al. (2011) Structural basis of substrate discrimination and integrin binding by autotaxin. Nat Struct Mol Biol 18: 198-204.
33. Nishimasu H, Ishitani R, Aoki J, Nureki O (2012) A 3D view of autotaxin. Trends Pharmacol Sci.
34. Saunders LP, Cao W, Chang WC, Albright RA, Braddock DT, et al. (2011) Kinetic analysis of autotaxin reveals substrate-specific catalytic pathways and a mechanism for lysophosphatidic acid distribution. J Biol Chem 286: 30130-30141.
35. Gaetano CG, Samadi N, Tomsig JL, Macdonald TL, Lynch KR, et al. (2009) Inhibition of autotaxin production or activity blocks lysophosphatidylcholine- induced migration of human breast cancer and melanoma cells. Mol Carcinog 48: 801-809.
36. Samadi N, Gaetano C, Goping IS, Brindley DN (2009) Autotaxin protects MCF-7 breast cancer and MDA-MB-435 melanoma cells against Taxol-induced apoptosis. Oncogene 28: 1028-1039.
37. Kishi Y, Okudaira S, Tanaka M, Hama K, Shida D, et al. (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.
38. Zhang H, Xu X, Gajewiak J, Tsukahara R, Fujiwara Y, et al. (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.
39. Chapman ME, Hu L, Plato CF, Kohan DE (2010) Bioimpedance spectroscopy for the estimation of body fluid volumes in mice. Am J Physiol Renal Physiol 299: F280-283.
40. Liu Y, Kati W, Chen CM, Tripathi R, Molla A, et al. (1999) Use of a fluorescence plate reader for measuring kinetic parameters with inner filter effect correction. Anal Biochem 267: 331-335. (Pubitemid 29095880)
41. Liu XW, Sok DE, Yook HS, Sohn CB, Chung YJ, et al. (2007) Inhibition of lysophospholipase D activity by unsaturated lysophosphatidic acids or seed extracts containing 1-linoleoyl and 1-oleoyl lysophosphatidic acid. J Agric Food Chem 55: 8717-8722. (Pubitemid 350013118)
42. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.