Pericytes prevent regression of endothelial cell tubes by accelerating metabolism of lysophosphatidic acid

Microvascular Research

Volumn 93, Issue , 2014, Pages 62-71

  Motiejunaite, Ruta ^a,b   Aranda, Jorge ^a   Kazlauskas, Andrius ^a  

^a SCHEPENS EYE RESEARCH INSTITUTE   (United States)

^b VILNIUS UNIVERSITY   (Lithuania)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOTAXIN; LIPID PHOSPHATE PHOSPHATASE; LYSOPHOSPHATIDIC ACID; PHOSPHATASE; UNCLASSIFIED DRUG; ALKYLGLYCEROPHOSPHOETHANOLAMINE PHOSPHODIESTERASE; LYSOPHOSPHOLIPID; PHOSPHATIDATE PHOSPHATASE; PHOSPHODIESTERASE;

ANIMAL CELL; ARTICLE; BLOOD VESSEL; CATTLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DEPHOSPHORYLATION; ENDOTHELIUM CELL; ENZYME ACTIVITY; IN VITRO STUDY; LIPID METABOLISM; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; VASCULARIZATION; ANGIOGENESIS; ANIMAL; BOVINAE; CELL COMMUNICATION; COCULTURE; DOWN REGULATION; HEK293 CELL LINE; HUMAN; METABOLISM; MOUSE; PHOSPHORYLATION; TIME;

ANIMALS; CATTLE; CELL COMMUNICATION; COCULTURE TECHNIQUES; DOWN-REGULATION; ENDOTHELIAL CELLS; HEK293 CELLS; HUMANS; LYSOPHOSPHOLIPIDS; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; PERICYTES; PHOSPHATIDATE PHOSPHATASE; PHOSPHORIC DIESTER HYDROLASES; PHOSPHORYLATION; TIME FACTORS;

EID: 84901238330     PISSN: 00262862     EISSN: 10959319     Source Type: Journal    
DOI: 10.1016/j.mvr.2014.03.003     Document Type: Article

References (59)

1. 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., Ovaa H. Boronic acid-based inhibitor of autotaxin reveals rapid turnover of LPA in the circulation. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:7257-7562.
2. Aranda J., MotiejunaitE R., Im E., Kazlauskas A. Diabetes disrupts the response of retinal endothelial cells to the angiomodulator lysophosphatidic acid. Diabetes 2012, 61:1225-1233.
3. Armulik A., Genové G., Betsholtz C. Pericytes: developmental, physiological and pathological perspectives, problems and promises. Dev. Cell 2011, 21:193-215.
4. Benjamin L.E., Hemo I., Keshet E. A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development 1998, 125:1591-1598.
5. Benjamin L.E., Golijanin D., Itin A., Pode D., Keshet E. Selective ablation of immature blood vessels in established human tumors follows vascular endothelial growth factor withdrawal. J. Clin. Invest. 1999, 103:159-165.
6. Bréart B., Ramos-Perez W.D., Mendoza A., Salous A.K., Gobert M., Huang Y., Adams R.H., Lafaille J.J., Escalante-Alcalde D., Morris A.J., Schwab S.R. Lipid phosphate phosphatase 3 enables efficient thymic egress. J. Exp. Med. 2011, 208:1267-1278.
7. Carmeliet P., Jain R. Molecular mechanisms and clinical applications of angiogenesis. Nature 2011, 473:298-307.
8. Dang L.T., Lawson N.D., Fish J.E. MicroRNA control of vascular endothelial growth factor signaling output during vascular development. Arterioscler. Thromb. Vasc. Biol. 2013, 33:193-200.
9. Darland D.C., Massingham L.J., Smith S.R., Piek E., Saint-Geniez M., D'Amore P.A. Pericyte production of cell-associated VEGF is differentiation-dependent and is associated with endothelial survival. Dev. Biol. 2003, 264:275-288.
10. Enge M., Bjarnegård M., Gerhardt H., Gustafsson E., Kalén M., Asker N., Hammes H.P., Shani M., Fässler R., Betsholtz C. Endothelium-specific platelet-derived growth factor-B ablation mimics diabetic retinopathy. EMBO J. 2002, 21:4307-4316.
11. Escalante-Alcalde D., Hernandez L., Le Stunff H., Maeda R., Lee H.S., Jr-Gang-Cheng Sciorra, V.A., Daar, I., Spiegel, S., Morris, A.J., Stewart, C.L. The lipid phosphatase LPP3 regulates extra-embryonic vasculogenesis and axis patterning. Development 2003, 130:4623-4637.
12. Evensen L., Micklem D.R., Blois A., Berge S.V., Aarsaether N., Littlewood-Evans A., Wood J., Lorens J.B. Mural cell associated VEGF is required for organotypic vessel formation. PLoS One 2009, 4:e5798.
13. Franco M., Roswall P., Cortez E., Hanahan D., Pietras K. Pericytes promote endothelial cell survival through induction of autocrine VEGF-A signaling and Bcl-w expression. Blood 2011, 118:2906-2917.
14. Gaengel K., Genové G., Armulik A., Betsholtz C. Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler. Thromb. Vasc. Biol. 2009, 29:630-638.
15. Hamzah J., Jugold M., Kiessling F., Rigby P., Manzur M., Marti H.H., Rabie T., Kaden S., Gröne H.J., Hämmerling G.J., Arnold B., Ganss R. Vascular normalization in Rgs5-deficient tumours promotes immune destruction. Nature 2008, 453:410-414.
16. Hasegawa Y., Erickson J.R., Goddard G.J., Yu S., Liu S., Cheng K.W., Eder A., Bandoh K., Aoki J., Jarosz R., Schrier A.D., Lynch K.R., Mills G.B., Fang X. Identification of a phosphothionate analogue of lysophosphatidic acid (LPA) as a selective agonist of the LPA3 receptor. J. Biol. Chem. 2003, 278:11962-11969.
17. Helfrich I., Scheffrahn I., Bartling S., Weis J., von Felbert V., Middleton M., Kato M., Ergün S., Schadendorf D. Resistance to antiangiogenic therapy is directed by vascular phenotype, vessel stabilization, and maturation of malignant melanoma. J. Exp. Med. 2010, 207:491-503.
18. Hellström M., Gerhardt H., Kalen M., Li X., Eriksson U., Wolburg H., Betsholtz C. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J. Cell Biol. 2001, 153:543-553.
19. Hirschi K.K., Rohovsky S.A., D'Amore P.A. PDGF, TGF-beta, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J. Cell Biol. 1998, 141:805-814.
20. Humtsoe J.O., Feng S., Thakker G.D., Yang J., Hong J., Wary K.K. Regulation of cell-cell interactions by phosphatidic acid phosphatase 2b/VCIP. EMBO J. 2003, 22:1539-1554.
21. Im E., Kazlauskas A. New insights regarding vessel regression. Cell Cycle 2006, 5:2057-2059.
22. Im E., Kazlauskas A. Regulating angiogenesis at the level of PtdIns-4,5-P2. EMBO J. 2006, 25:2075-2082.
23. Im E., Venkatakrishnan A., Kazlauskas A. Cathepsin B regulates the intrinsic angiogenic threshold of endothelial cells. Mol. Biol. Cell 2005, 16:3488-3500.
24. Im E., MotiejunaitE R., Aranda J., Park E.Y., Federico L., Kim T.I., Clair T., Stracke M.L., Smyth S.S., Kazlauskas A. Phospholipase Cgamma activation drives increased production of autotaxin in endothelial cells and lysophosphatidic acid-dependent regression. Mol. Cell. Biol. 2010, 30:2401-2410.
25. Jeansson M., Gawlik A., Anderson G., Li C., Kerjaschki D., Henkelman M., Quaggin S.E. Angiopoietin-1 is essential in mouse vasculature during development and in response to injury. J. Clin. Invest. 2011, 121:2278-2289.
26. Koike N., Fukumura D., Gralla O., Au P., Schechner J.S., Jain R.K. Tissue engineering: creation of long-lasting blood vessels. Nature 2004, 428:138-139.
27. Kume K., Shimizu T. cDNA cloning and expression of murine 1-acyl-sn-glycerol-3-phosphate acyltransferase. Biochem. Biophys. Res. Commun. 1997, 237:663-666.
28. Mandarino L.J., Sundarraj N., Finlayson J., Hassell H.R. Regulation of fibronectin and laminin synthesis by retinal capillary endothelial cells and pericytes in vitro. Exp. Eye Res. 1993, 57:609-621.
29. Mazzone M., Dettori D., Leite de Oliveira R., Loges S., Schmidt T., Jonckx B., Tian Y.M., Lanahan A.A., Pollard P., Ruiz de Almodovar C., De Smet F., Vinckier S., Aragonés J., Debackere K., Luttun A., Wyns S., Jordan B., Pisacane A., Gallez B., Lampugnani M.G., Dejana E., Simons M., Ratcliffe P., Maxwell P., Carmeliet P. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell 2009, 136:839-851.
30. McDermott M.I., Sigal Y.J., Crump J.S., Morris A.J. Enzymatic analysis of lipid phosphate phosphatases. Methods 2006, 39:169-179.
31. Moolenaar W.H., van Meeteren L.A., Giepmans B.N.G. The ins and outs of lysophosphatidic acid signaling. BioEssays 2004, 26:870-881.
32. Morris A.J., Panchatcharam M., Cheng H.Y., Federico L., Fulkerson Z., Selim S., Escalante-Acalde D., Smyth S.S. Regulation of vascular cell function by bioactive lysophospholipids. J. Thromb. Haemost. 2009, 7(Suppl. 1):38-43.
33. Morris A.J., Selim S., Salous A., Smyth S.S. Blood relatives: dynamic regulation of bioactive lysophosphatidic acid and sphingosine-1-phosphate metabolism in the circulation. Trends Cardiovasc. Med. 2009, 19:135-140.
34. Nakasaki T., Tanaka T., Okudaira S., Hirosawa M., Umemoto E., Otani K., Jin S., Bai Z., Hayasaka H., Fukui Y., Aozasa K., Fujita N., Tsuruo T., Ozono K., Aoki J., Miyasaka M. Involvement of the lysophosphatidic acid-generating enzyme autotaxin in lymphocyte-endothelial cell interactions. Am. J. Pathol. 2008, 173:1566-1576.
35. Nam S.W., Clair T., Kim Y.S., McMarlin A., Schiffmann E., Liotta L.A., Stracke M.L. Autotaxin (NPP-2), a metastasis-enhancing motogen, is an angiogenic factor. Cancer Res. 2001, 61:6938-6944.
36. Panchatcharam M., Miriyala S., Salous A., Wheeler J., Dong A., Mueller P., Sunkara M., Escalante-Alcalde D., Morris A.J., Smyth S.S. Lipid phosphate phosphatase 3 negatively regulates smooth muscle cell phenotypic modulation to limit intimal hyperplasia. Arterioscler. Thromb. Vasc. Biol. 2013, 33:52-59.
37. Potente M., Gerhardt H., Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell 2011, 146:873-887.
38. 3 receptor-selective agonist activity. J. Med. Chem. 2003, 46:5575-5578.
39. Ren H., Panchatcharam M., Mueller P., Escalante-Alcalde D., Morris A.J., Smyth S.S. Lipid phosphate phosphatase (LPP3) and vascular development. Biochim. Biophys. Acta 2013, 1831:126-132.
40. Roberts R., Sciorra V.A., Morris A.J. Human type 2 phosphatidic acid phosphohydrolases. Substrate specificity of the type 2a, 2b, and 2c enzymes and cell surface activity of the 2a isoform. J. Biol. Chem. 1998, 273:22059-22067.
41. Salous A.K., Panchatcharam M., Sunkara M., Mueller P., Dong A., Wang Y., Graf G.A., Smyth S.S., Morris A.J. Mechanism of rapid elimination of lysophosphatidic acid and related lipids from the circulation of mice. J. Lipid Res. 2013, 54:2775-2784.
42. Samuel R., Daheron L., Liao S., Vardam T., Kamoun W.S., Batista A., Buecker C., Schäfer R., Han X., Au P., Scadden D.T., Duda D.G., Fukumura D., Jain R.K. Generation of functionally competent and durable engineered blood vessels from human induced pluripotent stem cells. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:12774-12779.
43. Saulnier-Blache J.S., Girard A., Simon M.F., Lafontan M., Valet P. A simple and highly sensitive radioenzymatic assay for lysophosphatidic acid quantification. J. Lipid Res. 2000, 41:1947-1951.
44. Saunders W.B., Bohnsack B.L., Faske J.B., Anthis N.J., Bayless K.J., Hirschi K.K., Davis G.E. Coregulation of vascular tube stabilization by endothelial cell TIMP-2 and pericyte TIMP-3. J. Cell Biol. 2006, 175:179-191.
45. Schrimpf C., Xin C., Campanholle G., Gill S.E., Stallcup W., Lin S.L., Davis G.E., Gharib S.A., Humphreys B.D., Duffield J.S. Pericyte TIMP3 and ADAMTS1 modulate vascular stability after kidney injury. J. Am. Soc. Nephrol. 2012, 23:868-883.
46. Simon M.F., Rey A., Castan-Laurel I., Grés S., Sibrac D., Valet P., Saulnier-Blache J.S. Expression of ectolipid phosphate phosphohydrolases in 3T3F442A preadipocytes and adipocytes. Involvement in the control of lysophosphatidic acid production. J. Biol. Chem. 2002, 277:23131-23136.
47. Simons M. An inside view: VEGF receptor trafficking and signaling. Physiology (Bethesda) 2012, 27:213-222.
48. Smyth S.S., Cheng H.Y., Miriyala S., Panchatcharam M., Morris A.J. Roles of lysophosphatidic acid in cardiovascular physiology and disease. Biochim. Biophys. Acta 2008, 1781:563-570.
49. Stratman A.N., Malotte K.M., Mahan R.D., Davis M.J., Davis G.E. Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood 2009, 114:5091-5101.
50. Stratman A.N., Schwindt A.E., Malotte K.M., Davis G.E. Endothelial-derived PDGF-BB and HB-EGF coordinately regulate pericyte recruitment during vasculogenic tube assembly and stabilization. Blood 2010, 116:4720-4730.
51. Tachikawa M., Tsuji K., Ikeda S., Hosoya K. Lysophospholipids enhance taurine release from rat retinal vascular endothelial cells under hypoosmotic stress. Microvasc. Res. 2009, 78:332-337.
52. Tanaka M., Okudaira S., Kishi Y., Ohkawa R., Iseki S., Ota M., Noji S., Yatomi Y., Aoki J., Arai H. Autotaxin stabilizes blood vessels and is required for embryonic vasculature by producing lysophosphatidic acid. J. Biol. Chem. 2006, 281:25822-25830.
53. Tomsig J.L., Snyder A.H., Berdyshev E.V., Skobeleva A., Mataya C., Natarajan V., Brindley D.N., Lynch K.R. Lipid phosphate phosphohydrolase type 1 (LPP1) degrades extracellular lysophosphatidic acid in vivo. Biochem. J. 2009, 419:611-618.
54. Uemura A., Ogawa M., Hirashima M., Fujiwara T., Koyama S., Takagi H., Honda Y., Wiegand S.J., Yancopoulos G.D., Nishikawa S. Recombinant angiopoietin-1 restores higher-order architecture of growing blood vessels in mice in the absence of mural cells. J. Clin. Invest. 2002, 110:1619-1628.
55. van Meeteren L.A., Ruurs P., Stortelers C., Bouwman P., van Rooijen M.A., Pradère J.P., Pettit T.R., Wakelam M.J., Saulnier-Blache J.S., Mummery C.L., Moolenaar W.H., Jonkers J. Autotaxin, a secreted lysophospholipase D, is essential for blood vessel formation during development. Mol. Cell. Biol. 2006, 26:5015-5022.
56. Wu W.T., Chen C.N., Lin C.I., Chen J.H., Lee H. Lysophospholipids enhance matrix metalloproteinase-2 expression in human endothelial cells. Endocrinology 2005, 146:3387-3400.
57. Ye J., Coulouris G., Zaretskaya I., Cutcutache I., Rozen S., Madden T.L. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinforma. 2012, 13:134.
58. Yukiura H., Hama K., Nakanaga K., Tanaka M., Asaoka Y., Okudaira S., Arima N., Inoue A., Hashimoto T., Arai H., Kawahara A., Nishina H., Aoki J. Autotaxin regulates vascular development via multiple lysophosphatidic acid (LPA) receptors in zebrafish. J. Biol. Chem. 2011, 286:43972-43983.
59. Zhao Y., Kalari S.K., Usatyuk P.V., Gorshkova I., He D., Watkins T., Brindley D.N., Sun C., Bittman R., Garcia J.G., Berdyshev E.V., Natarajan V. Intracellular generation of sphingosine 1-phosphate in human lung endothelial cells: role of lipid phosphate phosphatase-1 and sphingosine kinase 1. J. Biol. Chem. 2007, 282:14165-14177.