Phospholipase Cγ activation drives increased production of autotaxin in endothelial cells and lysophosphatidic acid-dependent regression

Molecular and Cellular Biology

Volumn 30, Issue 10, 2010, Pages 2401-2410

  Im, Eunok ^a,f   Motiejunaite, Ruta ^a,d   Aranda, Jorge ^a   Park, Eun Young ^a   Federico, Lorenzo ^b   Kim, Tae Im ^c   Clair, Timothy ^e   Stracke, Mary L ^e   Smyth, Susan ^b   Kazlauskas, Andrius ^a  

^a SCHEPENS EYE RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c Yonsei University College of Medicine   (South Korea)

^d VILNIUS UNIVERSITY   (Lithuania)

^e NATIONAL CANCER INSTITUTE   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOTAXIN; LYSOPHOSPHATIDIC ACID; LYSOPHOSPHOLIPASE; LYSOPHOSPHOLIPASE D; PHOSPHOLIPASE C GAMMA; UNCLASSIFIED DRUG; CALCINEURIN; ENPP2 PROTEIN, MOUSE; INORGANIC PYROPHOSPHATASE; LYSOPHOSPHOLIPID; MULTIENZYME COMPLEX; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHODIESTERASE I; SMALL INTERFERING RNA; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL MOTILITY; CONTROLLED STUDY; DIABETIC RETINOPATHY; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ANALYSIS; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; SOLID TUMOR; ANIMAL; CATTLE; CELL CULTURE; CYTOLOGY; DRUG EFFECT; EYE; GENETICS; METABOLISM; MOUSE; PHYSIOLOGY; TRANSGENIC MOUSE; VASCULARIZATION;

MUS;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CALCINEURIN; CATTLE; CELLS, CULTURED; ENDOTHELIAL CELLS; ENZYME ACTIVATION; EYE; HUMANS; LYSOPHOSPHOLIPIDS; MICE; MICE, TRANSGENIC; MULTIENZYME COMPLEXES; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHODIESTERASE I; PHOSPHOLIPASE C GAMMA; PYROPHOSPHATASES; RNA, SMALL INTERFERING; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 77951999546     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01275-09     Document Type: Article

References (49)

1. Ausprunk, D. H., K. Falterman, and J. Folkman. 1978. The sequence of events in the regression of corneal capillaries. Lab. Invest. 38:284-294.
2. Avery, R. L., D. J. Pieramici, M. D. Rabena, A. A. Castellarin, M. A. Nasir, and M. J. Giust. 2006. Intravitreal bevacizumab (Avastin) for neovascular age-related macular degeneration. Ophthalmology 113:363-372.
3. Benjamin, L. E., D. Golijanin, A. Itin, D. Pode, and E. Keshet. 1999. Selective ablation of immature blood vessels in established human tumors follows vascular endothelial growth factor withdrawal. J. Clin. Invest. 103:159-165.
4. Binion, D. G., G. A. West, K. Ina, N. P. Ziats, S. N. Emancipator, and C. Fiocchi. 1997. Enhanced leukocyte binding by intestinal microvascular endothelial cells in inflammatory bowel disease. Gastroenterology 112:1895-1907. (Pubitemid 27240776)
5. Carmeliet, P. 2005. Angiogenesis in life, disease and medicine. Nature 438: 932-936.
6. Chen, M., and K. L. O'Connor. 2005. Integrin alpha6beta4 promotes expression of autotaxin/ENPP2 autocrine motility factor in breast carcinoma cells. Oncogene 24:5125-5130. (Pubitemid 41129090)
7. Clair, T., J. Aoki, E. Koh, R. W. Bandle, S. W. Nam, M. M. Ptaszynska, G. B. Mills, E. Schiffmann, L. A. Liotta, and M. L. Stracke. 2003. Autotaxin hydrolyzes sphingosylphosphorylcholine to produce the regulator of migration, sphingosine-1-phosphate. Cancer Res. 63:5446-5453. (Pubitemid 37139863)
8. Clair, T., E. Koh, M. Ptaszynska, R. W. Bandle, L. A. Liotta, E. Schiffmann, and M. L. Stracke. 2005. L-Histidine inhibits production of lysophosphatidic acid by the tumor-associated cytokine, autotaxin. Lipids Health Dis. 4:5-17. (Pubitemid 40594710)
9. Eter, N., T. U. Krohne, and F. G. Holz. 2006. New pharmacologic approaches to therapy for age-related macular degeneration. BioDrugs 20:167-179. (Pubitemid 43845337)
10. Gitlin, J. D., and P. A. D'Amore. 1983. Culture of retinal capillary cells using selective growth media. Microvasc. Res. 26:74-80.
11. Gragoudas, E. S., A. P. Adamis, E. T. J. Cunningham, M. Feinsod, D. R. Guyer, and the VEGF Inhibition Study in Ocular Neovascularization Clinical Trial Group. 2004. Pegaptanib for neovascular age-related macular degeneration. N. Engl. J. Med. 351:2805-2816.
12. Hogan, P. G., L. Chen, J. Nardone, and A. Rao. 2003. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 17:2205-2232.
13. Im, E., and A. Kazlauskas. 2006. New insights regarding vessel regression. Cell Cycle 5:2057-2059. (Pubitemid 44553738)
14. Im, E., and A. Kazlauskas. 2006. Regulating angiogenesis at the level of PtdIns-4,5-P2. EMBO J. 25:2075-2082.
15. Im, E., and A. Kazlauskas. 2007. Src family kinases promote vessel stability by antagonizing the Rho/ROCK pathway. J. Biol. Chem. 282:29122-29129.
16. Im, E., A. Venkatakrishnan, and A. Kazlauskas. 2005. Cathepsin B regulates the intrinsic angiogenic threshold of endothelial cells. Mol. Biol. Cell 16: 3488-3500.
17. Ito, M., and M. Yoshioka. 1999. Regression of the hyaloid vessels and pupillary membrane of the mouse. Anat. Embryol. (Berl.) 200:403-411.
18. Kehlen, A., R. Lauterbach, A. N. Santos, K. Thiele, U. Kabisch, E. Weber, D. Riemann, and J. Langner. 2001. IL-1 beta- and IL-4-induced down-regulation of autotaxin mRNA and PC-1 in fibroblast-like synoviocytes of patients with rheumatoid arthritis (RA). Clin. Exp. Immunol. 123:147-154.
19. Kenny, P. A., T. Enver, and A. Ashworth. 2005. Receptor and secreted targets of Wnt-1/beta-catenin signalling in mouse mammary epithelial cells. BMC Cancer 5:3.
20. Kenyon, B. M., E. E. Voest, C. C. Chen, E. Flynn, J. Folkman, and R. J. D'Amato. 1996. A model of angiogenesis in the mouse cornea. Invest. Ophthalmol. Vis. Sci. 37:1625-1632.
21. Lang, R., M. Lustig, F. Francois, M. Sellinger, and H. Plesken. 1994. Apoptosis during macrophage-dependent ocular tissue remodelling. Development 120:3395-3403. (Pubitemid 24366985)
22. Lang, R. A., and J. M. Bishop. 1993. Macrophages are required for cell death and tissue remodeling in the developing mouse eye. Cell 74:453-462.
23. Liao, H. J., T. Kume, C. McKay, M. J. Xu, J. N. Ihle, and G. Carpenter. 2002. Absence of erythrogenesis and vasculogenesis in Plcg1-deficient mice. J. Biol. Chem. 277:9335-9341.
24. Liliom, K., G. Sun, M. Bunemann, T. Virag, N. Nusser, D. L. Baker, D. A. Wang, M. J. Fabian, B. Brandts, K. Bender, A. Eickel, K. U. Malik, D. D. Miller, D. M. Desiderio, G. Tigyi, and L. Pott. 2001. Sphingosylphosphocholine is a naturally occurring lipid mediator in blood plasma: a possible role in regulating cardiac function via sphingolipid receptors. Biochem. J. 355:189-197. (Pubitemid 32304249)
25. Lobov, I. B., S. Rao, T. J. Carroll, J. E. Vallance, M. Ito, J. K. Ondr, S. Kurup, D. A. Glass, M. S. Patel, W. Shu, E. E. Morrisey, A. P. McMahon, G. Karsenty, and R. A. Lang. 2005. WNT7b mediates macrophage-induced programmed cell death in patterning of the vasculature. Nature 437:417-421.
26. Long, J. S., K. Yokoyama, G. Tigyi, N. J. Pyne, and S. Pyne. 2006. Lipid phosphate phosphatase-1 regulates lysophosphatidic acid- and platelet-derived-growth-factor-induced cell migration. Biochem. J. 394:495-500.
27. Matsumoto, T., and L. Claesson-Welsh. 2001. VEGF receptor signal transduction. Sci. STKE 2001:RE21.
28. Mavria, G., Y. Vercoulen, M. Yeo, H. Paterson, M. Karasarides, R. Marais, D. Bird, and C. J. Marshall. 2006. ERK-MAPK signaling opposes Rhokinase to promote endothelial cell survival and sprouting during angiogenesis. Cancer Cell 9:33-44. (Pubitemid 43069509)
29. Mizugishi, K., T. Yamashita, A. Olivera, G. F. Miller, S. Spiegel, and R. L. Proia. 2005. Essential role for sphingosine kinases in neural and vascular development. Mol. Cell. Biol. 25:11113-11121.
30. Nam, S. W., T. Clair, Y. S. Kim, A. McMarlin, E. Schiffmann, L. A. Liotta, and M. L. Stracke. 2001. Autotaxin (NPP-2), a metastasis-enhancing motogen, is an angiogenic factor. Cancer Res. 61:6938-6944.
31. Ory, D. S., B. A. Neugeboren, and R. C. Mulligan. 1996. A stable human-derived packaging cell line for production of high titer retrovirus/vesicular stomatitis virus G pseudotypes. Proc. Natl. Acad. Sci. U. S. A. 93:11400-11406.
32. Pamuklar, Z., L. Federico, S. Liu, M. Umezu-Goto, A. Dong, M. Panchatcharam, Z. Fulerson, E. Berdyshev, V. Natarajan, X. Fang, L. A. van Meeteren, W. H. Moolenaar, G. B. Mills, A. J. Morris, and S. S. Smyth. 2009. Autotaxin/lysopholipase D and lysophosphatidic acid regulate murine hemostasis and thrombosis. J. Biol. Chem. 284:7385-7394.
33. Phng, L. K., M. Potente, J. D. Leslie, J. Babbage, D. Nyqvist, I. Lobov, J. K. Ondr, S. Rao, R. A. Lang, G. Thurston, and H. Gerhardt. 2009. Nrarp coordinates endothelial Notch and Wnt signaling to control vessel density in angiogenesis. Dev. Cell 16:70-82.
34. Ptaszynska, M. M., M. L. Pendrak, R. W. Bandle, M. L. Stracke, and D. D. Roberts. 2008. Positive feedback between vascular endothelial growth factor-A and autotaxin in ovarian cancer cells. Mol. Cancer Res. 6:352-363.
35. Rao, S., I. B. Lobov, J. E. Vallance, K. Tsujikawa, I. Shiojima, S. Akunuru, K. Walsh, L. E. Benjamin, and R. A. Lang. 2007. Obligatory participation of macrophages in an angiopoietin 2-mediated cell death switch. Development 134:4449-4458.
36. Rogers, M. S., R. M. Rohan, A. E. Birsner, and R. J. D'Amato. 2004. Genetic loci that control the angiogenic response to basic fibroblast growth factor. FASEB J. 18:1050-1059.
37. Sakurai, Y., K. Ohgimoto, Y. Kataoka, N. Yoshida, and M. Shibuya. 2005. Essential role of Flk-1 (VEGF receptor 2) tyrosine residue 1173 in vasculogenesis in mice. Proc. Natl. Acad. Sci. U. S. A. 102:1076-1081.
38. Saunders, W. B., B. L. Bohnsack, J. B. Faske, N. J. Anthis, K. J. Bayless, K. K. Hirschi, and G. E. Davis. 2006. Coregulation of vascular tube stabilization by endothelial cell TIMP-2 and pericyte TIMP-3. J. Cell Biol. 175: 179-191.
39. Sciorra, V. A., and A. J. Morris. 2002. Roles for lipid phosphate phosphatases in regulation of cellular signaling. Biochim. Biophys. Acta 1582:45-51.
40. Takahashi, T., S. Yamaguchi, K. Chida, and M. Shibuya. 2001. A single autophosphorylation site on KDR/Flk-1 is essential for VEGF-A-dependent activation of PLC-gamma and DNA synthesis in vascular endothelial cells. EMBO J. 20:2768-2778. (Pubitemid 32938560)
41. Tanaka, M., S. Okudaira, Y. Kishi, R. Ohkawa, S. Iseki, M. Ota, S. Noji, Y. Yatomi, J. Aoki, and H. Arai. 2006. Autotaxin stabilizes blood vessels and is required for embryonic vasculature by producing lysophosphatidic acid. J. Biol. Chem. 281:25822-25830.
42. Tice, D. A., W. Szeto, I. Soloviev, B. Rubinfeld, S. E. Fong, D. L. Dugger, J. Winer, P. M. Williams, D. Wieand, V. Smith, R. H. Schwall, D. Pennica, and P. Polakis. 2002. Synergistic induction of tumor antigens by Wnt-1 signaling and retinoic acid revealed by gene expression profiling. J. Biol. Chem. 277: 14329-14335.
43. Tokumura, A., E. Majima, Y. Kariya, K. Tominaga, K. Kogure, K. Yasuda, and K. Fukuzawa. 2002. Identification of human plasma lysophospholipase D, a lysophosphatidic acid-producing enzyme, as autotaxin, a multifunctional phosphodiesterase. J. Biol. Chem. 277:39436-39442.
44. Umezu-Goto, M., Y. Kishi, A. Taira, K. Hama, N. Dohmae, K. Takio, T. Yamori, G. B. Mills, K. Inoue, J. Aoki, and H. Arai. 2002. Autotaxin has lysophospholipase D activity leading to tumor cell growth and motility by lysophosphatidic acid production. J. Cell Biol. 158:227-233.
45. Valius, M., C. Bazenet, and A. Kazlauskas. 1993. Tyrosines 1021 and 1009 are phosphorylation sites in the carboxy terminus of the platelet-derived growth factor receptor beta subunit and are required for binding of phospholipase C gamma and a 64-kilodalton protein, respectively. Mol. Cell. Biol. 13:133-143.
46. Valius, M., and A. Kazlauskas. 1993. Phospholipase C-gamma 1 and phosphatidylinositol 3 kinase are the downstream mediators of the PDGF receptor's mitogenic signal. Cell 73:321-334. (Pubitemid 23123310)
47. van Meeteren, L. A., and W. H. Moolenaar. 2007. Regulation and biological activities of the autotaxin-LPA axis. Prog. Lipid Res. 46:145-160.
48. van Meeteren, L. A., P. Ruurs, C. Stortelers, P. Bouwman, M. A. van Rooijen, J. P. Pradère, T. R. Pettit, M. J. Wakelam, J. S. Saulnier-Blache, C. L. Mummery, W. H. Moolenaar, and J. Jonkers. 2006. Autotaxin, a secreted lysophospholipase D, is essential for blood vessel formation during development. Mol. Cell. Biol. 26:5015-5022.
49. Zirn, B., B. Samans, S. Wittmann, T. Pietsch, I. Leuschner, N. Graf, and M. Gessler. 2006. Target genes of the WNT/beta-catenin pathway in Wilms tumors. Genes Chromosomes Cancer 45:565-574. (Pubitemid 43727163)