ADAMTS1 inhibits lymphangiogenesis by attenuating phosphorylation of the lymphatic endothelial cell-specific VEGF receptor

Experimental Cell Research

Volumn 323, Issue 2, 2014, Pages 263-275

  Inagaki, Junko ^a   Takahashi, Katsuyuki ^a   Ogawa, Hiroko ^a   Asano, Keiichi ^a   Faruk Hatipoglu, Omer ^a   Zeynel Cilek, Mehmet ^a   Obika, Masanari ^a   Ohtsuki, Takashi ^a   Hofmann, Matthias ^c   Kusachi, Shozo ^b   Ninomiya, Yoshifumi ^a   Hirohata, Satoshi ^a,b  

^a OKAYAMA UNIVERSITY   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

ADAMTS1; Lymphangiogenesis; Lymphatic endothelial cell; VEGFC; VEGFR 3

Indexed keywords

3,4 METHYLENEDIOXYAMPHETAMINE; ADAMTS1 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B; VASCULOTROPIN C; VASCULOTROPIN RECEPTOR 3;

ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO GENE TRANSFER; IN VITRO STUDY; LYMPH VESSEL ENDOTHELIUM; LYMPHANGIOGENESIS; MICROVASCULAR ENDOTHELIAL CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY;

ADAMTS1; LYMPHANGIOGENESIS; LYMPHATIC ENDOTHELIAL CELL; VEGFC; VEGFR-3;

ADAM PROTEINS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; ENDOTHELIAL CELLS; HEK293 CELLS; HUMANS; LYMPHATIC VESSELS; PHOSPHORYLATION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

EID: 84897543417     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2014.03.002     Document Type: Article

References (51)

1. Kuno K., Kanada N., Nakashima E., et al. Molecular cloning of a gene encoding a new type of metalloproteinase-disintegrin family protein with thrombospondin motifs as an inflammation associated gene. J. Biol. Chem. 1997, 272:556-562.
2. Tang B.L. ADAMTS: a novel family of extracellular matrix proteases. Int. J. Biochem. Cell Biol. 2001, 33:33-44.
3. Porter S., Clark I.M., Kevorkian L., et al. The ADAMTS metalloproteinases. Biochem. J. 2005, 386:15-27.
4. Apte S.S. A disintegrin-like and metalloprotease (reprolysin-type) with thrombospondin type 1 motif (ADAMTS) superfamily: functions and mechanisms. J. Biol. Chem. 2009, 284:31493-31497.
5. Stanton H., Melrose J., Little C.B., et al. Proteoglycan degradation by the ADAMTS family of proteinases. Biochim. Biophys. Acta 2011, 1812:1616-1629.
6. Thai S.N., Iruela-Arispe M.L. Expression of ADAMTS1 during murine development. Mech. Dev. 2002, 115:181-185.
7. Krampert M., Kuenzle S., Thai S.N., et al. ADAMTS1 proteinase is up-regulated in wounded skin and regulates migration of fibroblasts and endothelial cells. J. Biol. Chem. 2005, 280:23844-23852.
8. Malfait A.M., Liu R.Q., Ijiri K., et al. Inhibition of ADAM-TS4 and ADAM-TS5 prevents aggrecan degradation in osteoarthritic cartilage. J. Biol. Chem. 2002, 277:22201-22208.
9. Diamantis I., Luthi M., Hosli M., et al. Cloning of the rat ADAMTS-1 gene and its down regulation in endothelial cells in cirrhotic rats. Liver 2000, 20:165-172.
10. Rosenberg G.A. Matrix metalloproteinases in neuroinflammation. Glia 2002, 39:279-291.
11. Espey L.L., Yoshioka S., Russell D.L., et al. Ovarian expression of a disintegrin and metalloproteinase with thrombospondin motifs during ovulation in the gonadotropin-primed immature rat. Biol. Reprod. 2000, 62:1090-1095.
12. Robker R.L., Russell D.L., Espey L.L., et al. Progesterone-regulated genes in the ovulation process: ADAMTS-1 and cathepsin L proteases. Proc. Nat. Acad. Sci. U.S.A. 2000, 97:4689-4694.
13. Vankemmelbeke M.N., Holen I., Wilson A.G., et al. Expression and activity of ADAMTS-5 in synovium. Eur. J. Biochem. 2001, 268:1259-1268.
14. DeClerck Y.A. Interactions between tumour cells and stromal cells and proteolytic modification of the extracellular matrix by metalloproteinases in cancer. Eur. J. Cancer 2000, 36:1258-1268.
15. Masui T., Hosotani R., Tsuji S., et al. Expression of METH-1 and METH-2 in pancreatic cancer. Clin. Cancer Res.: An Official Journal of the American Association for Cancer Research 2001, 7:3437-3443.
16. Shindo T., Kurihara H., Kuno K., et al. ADAMTS-1: a metalloproteinase-disintegrin essential for normal growth, fertility, and organ morphology and function. J. Clin. Invest. 2000, 105:1345-1352.
17. Mittaz L., Russell D.L., Wilson T., et al. Adamts-1 is essential for the development and function of the urogenital system. Biol. Reprod. 2004, 70:1096-1105.
18. Gunther W., Skaftnesmo K.O., Arnold H., et al. Distribution patterns of the anti-angiogenic protein ADAMTS-1 during rat development. Acta Histochem. 2005, 107:121-131.
19. Brown H.M., Dunning K.R., Robker R.L., et al. Requirement for ADAMTS-1 in extracellular matrix remodeling during ovarian folliculogenesis and lymphangiogenesis. Dev. Biol. 2006, 300:699-709.
20. Russell D.L., Doyle K.M., Ochsner S.A., et al. Processing and localization of ADAMTS-1 and proteolytic cleavage of versican during cumulus matrix expansion and ovulation. J. Biol. Chem. 2003, 278:42330-42339.
21. Brown H.M., Dunning K.R., Robker R.L., et al. ADAMTS1 cleavage of versican mediates essential structural remodeling of the ovarian follicle and cumulus-oocyte matrix during ovulation in mice. Biol. Reprod. 2010, 83:549-557.
22. Brown H.M., Robker R.L., Russell D.L. Development and hormonal regulation of the ovarian lymphatic vasculature. Endocrinology 2010, 151:5446-5455.
23. Oveland E., Karlsen T.V., Haslene-Hox H., et al. Proteomic evaluation of inflammatory proteins in rat spleen interstitial fluid and lymph during LPS-induced systemic inflammation reveals increased levels of ADAMST1. J. Proteome Res. 2012, 11:5338-5349.
24. Abdulnour-Nakhoul S.M., Al-Tawil Y., Gyftopoulos A.A., et al. Alterations in junctional proteins, inflammatory mediators and extracellular matrix molecules in eosinophilic esophagitis. Clin. Immunol. 2013, 148:265-278.
25. Iruela-Arispe M.L., Carpizo D., Luque.A. ADAMTS1: a matrix metalloprotease with angioinhibitory properties. Ann. N. Y. Acad. Sci. 2003, 995:183-190.
26. Luque A., Carpizo D.R., Iruela-Arispe.M.L. ADAMTS1/METH1 inhibits endothelial cell proliferation by direct binding and sequestration of VEGF165. J. Biol. Chem. 2003, 278:23656-23665.
27. Lee N.V., Sato M., Annis D.S., et al. ADAMTS1 mediates the release of antiangiogenic polypeptides from TSP1 and 2. Embo J. 2006, 25:5270-5283.
28. Liu Y.J., Xu Y., Yu.Q. Full-length ADAMTS-1 and the ADAMTS-1 fragments display pro- and antimetastatic activity, respectively. Oncogene 2006, 25:2452-2467.
29. Lu X., Wang Q., Hu G., et al. ADAMTS1 and MMP1 proteolytically engage EGF-like ligands in an osteolytic signaling cascade for bone metastasis. Genes Dev. 2009, 23:1882-1894.
30. Tyan S.W., Hsu C.H., Peng K.L., et al. Breast cancer cells induce stromal fibroblasts to secrete ADAMTS1 for cancer invasion through an epigenetic change. PLoS One 2012, 7:e35128.
31. Freitas V.M., do Amaral J.B., Silva T.A., et al. Decreased expression of ADAMTS-1 in human breast tumors stimulates migration and invasion. Mol. Cancer 2013, 12:2.
32. Rocks N., Paulissen G., Quesada-Calvo F., et al. ADAMTS-1 metalloproteinase promotes tumor development through the induction of a stromal reaction in vivo. Cancer Res. 2008, 68:9541-9550.
33. Vazquez F., Hastings G., Ortega M.A., et al. METH-1, a human ortholog of ADAMTS-1, and METH-2 are members of a new family of proteins with angio-inhibitory activity. J. Biol. Chem. 1999, 274:23349-23357.
34. Obika M., Ogawa H., Takahashi K., et al. The tumor growth inhibitory effect of ADAMTS1 is accompanied by the inhibition of tumor angiogenesis. Cancer Sci. 2012.
35. Cilek M.Z., Hirohata S., Hatipoglu O.Faruk, et al. AHR, a novel acute hypoxia-response sequence, drives reporter gene expression under hypoxia in vitro and in vivo. Cell Biol. Int. 2011, 35:1-8.
36. Miyoshi T., Hirohata S., Ogawa H., et al. Tumor-specific expression of the RGD-alpha3(IV)NC1 domain suppresses endothelial tube formation and tumor growth in mice. Faseb J. 2006, 20:1904-1906.
37. Sezer S., Simsek N., Celik H.T., et al. Association of collagen type I alpha 1 gene polymorphism with inguinal hernia. Hernia 2013.
38. Takemoto S., Murakami T., Kusachi S., et al. Increased expression of dermatopontin mRNA in the infarct zone of experimentally induced myocardial infarction in rats: comparison with decorin and type I collagen mRNAs. Basic Res. Cardiol. 2002, 97:461-468.
39. Yaykasli K.O., Oohashi T., Hirohata S., et al. ADAMTS9 activation by interleukin 1 beta via NFATc1 in OUMS-27 chondrosarcoma cells and in human chondrocytes. Mol. Cell Biochem. 2009, 323:69-79.
40. Demircan K., Yonezawa T., Takigawa T., et al. ADAMTS1, ADAMTS5, ADAMTS9 and aggrecanase-generated proteoglycan fragments are induced following spinal cord injury in mouse. Neurosci. Lett. 2013, 544:25-30.
41. Sezaki S., Hirohata S., Iwabu A., et al. Thrombospondin-1 is induced in rat myocardial infarction and its induction is accelerated by ischemia/reperfusion. Exp. Biol. Med. (Maywood) 2005, 230:621-630.
42. Iwamoto M., Hirohata S., Ogawa H., et al. Connective tissue growth factor induction in a pressure-overloaded heart ameliorated by the angiotensin II type 1 receptor blocker olmesartan. Hypertens. Res. 2010, 33:1305-1311.
43. Rodriguez-Manzaneque J.C., Milchanowski A.B., Dufour E.K., et al. Characterization of METH-1/ADAMTS1 processing reveals two distinct active forms. J. Biol. Chem. 2000, 275:33471-33479.
44. Alitalo K., Tammela T., Petrova.T.V. Lymphangiogenesis in development and human disease. Nature 2005, 438:946-953.
45. Wissmann C., Detmar M. Pathways targeting tumor lymphangiogenesis. Clin. Cancer Res.: An Official Journal of the American Association for Cancer Research 2006, 12:6865-6868.
46. Feng Y., Hu J., Ma J., et al. RNAi-mediated silencing of VEGF-C inhibits non-small cell lung cancer progression by simultaneously down-regulating the CXCR4, CCR7, VEGFR-2 and VEGFR-3-dependent axes-induced ERK, p38 and AKT signalling pathways. Eur. J. Cancer 2011, 47:2353-2363.
47. Zhu C., Qi X., Chen Y., et al. PI3K/Akt and MAPK/ERK1/2 signaling pathways are involved in IGF-1-induced VEGF-C upregulation in breast cancer. J. Cancer Res. Clin. Oncol. 2011, 137:1587-1594.
48. Cursiefen C., Maruyama K., Bock F., et al. Thrombospondin 1 inhibits inflammatory lymphangiogenesis by CD36 ligation on monocytes. J. Exp. Med. 2011, 208:1083-1092.
49. Gustavsson H., Tesan T., Jennbacken K., et al. ADAMTS1 alters blood vessel morphology and TSP1 levels in LNCaP and LNCaP-19 prostate tumors. BMC Cancer 2010, 10:288.
50. Chen J., Zhi Y., Chang X., et al. Expression of ADAMTS1 and its correlation with angiogenesis in primary gastric cancer and lymph node metastasis. Dig. Dis. Sci. 2013, 58:405-413.
51. Lee Y.J., Koch M., Karl D., et al. Variable inhibition of thrombospondin 1 against liver and lung metastases through differential activation of metalloproteinase ADAMTS1. Cancer Res. 2010, 70:948-956.