Notch modulates VEGF action in endothelial cells by inducing Matrix Metalloprotease activity

Vascular Cell

Volumn 3, Issue , 2011, Pages

  Funahashi, Yasuhiro ^a,b   Shawber, Carrie J ^b   Sharma, Anshula ^b   Kanamaru, Emi ^b   Choi, Yun K ^b   Kitajewski, Jan ^b  

^a EISAI CO LTD   (Japan)

^b Department of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE A; GELATINASE B; LIGAND; MATRIX METALLOPROTEINASE; NOTCH RECEPTOR; NOTCH1 RECEPTOR; NOTCH4 RECEPTOR; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INDUCTION; EXPRESSION VECTOR; FIBRINOLYSIS; HUMAN; HUMAN CELL; INHIBITION KINETICS; MORPHOGENESIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKIN CELL; UMBILICAL VEIN ENDOTHELIAL CELL; WESTERN BLOTTING;

MURINAE; MUS;

EID: 79955598040     PISSN: 2045824X     EISSN: None     Source Type: Journal    
DOI: 10.1186/2045-824X-3-2     Document Type: Article

References (56)

1. Influence of VEGF-R2 inhibition on MMP secretion and motility of microvascular human cerebral endothelial cells (HCEC). Wagner S Fueller T Hummel V Rieckmann P, Tonn JC, J Neurooncol 2003 62 221 231 10.1023/A:1023335732264 12777073 (Pubitemid 36591957)
2. Autocrine stimulation of VEGFR-2 activates human leukemic cell growth and migration. Dias S Hattori K, Zhu Z Heissig B, Choy M Lane W, Wu Y Chadburn A, Hyjek E Gill M, et al. J Clin Invest 2000 106 511 521 10.1172/JCI8978 10953026 (Pubitemid 30666384)
3. Impaired angiogenesis in SHR is associated with decreased KDR and MT1-MMP expression. Wang H Olszewski B, Rosebury W Wang D, Robertson A Keiser JA, Biochem Biophys Res Commun 2004 315 363 368 10.1016/j.bbrc.2004.01.059 14766216 (Pubitemid 38183115)
4. Pleiotropic roles of matrix metalloproteases in tumor angiogenesis: contrasting, overlapping and compensatory functions. Deryugina EI Quigley JP, Biochim Biophys Acta 2010 1803 103 120 10.1016/j.bbamcr.2009.09.017 19800930
5. Matrix metalloproteases: regulators of the tumor microenvironment. Kessenbrock K Plaks V Werb Z, Cell 2010 141 52 67 10.1016/j.cell.2010.03.015 20371345
6. Acute actions and novel targets of matrix metalloproteases in the heart and vasculature. Chow AK Cena J Schulz R, Br J Pharmacol 2007 152 189 205 10.1038/sj.bjp.0707344 17592511 (Pubitemid 47517601)
7. Membrane-type 1 matrix metalloprotease and cell migration. Seiki M Mori H Kajita M Uekita T, Itoh Y, Biochem Soc Symp 2003 253 262
8. Membrane-type matrix metalloproteases (MT-MMPs) in tumor metastasis. Sato H Seiki M, J Biochem 1996 119 209 215 8882706 (Pubitemid 26063238)
9. Membrane-type matrix metalloprotease 1 is a gelatinolytic enzyme and is secreted in a complex with tissue inhibitor of metalloproteases 2. Imai K Ohuchi E, Aoki T Nomura H, Fujii Y Sato H, Seiki M Okada Y, Cancer Res 1996 56 2707 2710 8665498
10. MT1-MMP-dependent neovessel formation within the confines of the three-dimensional extracellular matrix. Chun TH Sabeh F Ota I Murphy H, McDonagh KT Holmbeck K, Birkedal-Hansen H Allen ED, Weiss SJ, J Cell Biol 2004 167 757 767 10.1083/jcb.200405001 15545316 (Pubitemid 39565155)
11. Navigating ECM barriers at the invasive front: the cancer cell-stroma interface. Rowe RG Weiss SJ, Annu Rev Cell Dev Biol 2009 25 567 595 10.1146/annurev.cellbio.24.110707.175315 19575644
12. MT1-MMP- and Cdc42-dependent signaling co-regulate cell invasion and tunnel formation in 3D collagen matrices. Fisher KE Sacharidou A, Stratman AN Mayo AM, Fisher SB Mahan RD, Davis MJ Davis GE, J Cell Sci 2009 122 4558 4569 10.1242/jcs.050724 19934222
13. Endothelial cell lumen and vascular guidance tunnel formation requires MT1-MMP-dependent proteolysis in 3-dimensional collagen matrices. Stratman AN Saunders WB, Sacharidou A Koh W, Fisher KE Zawieja DC, Davis MJ Davis GE, Blood 2009 114 237 247 10.1182/blood-2008-12-196451 19339693
14. Notch function in the vasculature: insights from zebrafish, mouse and man. Shawber CJ Kitajewski J, Bioessays 2004 26 225 234 10.1002/bies.20004 14988924 (Pubitemid 38325664)
15. Notch: a membrane-bound transcription factor. Kopan R, J Cell Sci 2002 115 1095 1097 11884509 (Pubitemid 34272474)
16. The canonical Notch signaling pathway: unfolding the activation mechanism. Kopan R Ilagan MX, Cell 2009 137 216 233 10.1016/j.cell.2009.03.045 19379690
17. Vascular patterning defects associated with expression of activated Notch4 in embryonic endothelium. Uyttendaele H Ho J, Rossant J Kitajewski J, Proc Natl Acad Sci USA 2001 98 5643 5648 10.1073/pnas.091584598 11344305 (Pubitemid 32435695)
18. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Ferrara N Carver-Moore K Chen H Dowd M, Lu L O'Shea KS, Powell-Braxton L Hillan KJ, Moore MW, Nature 1996 380 439 442 10.1038/380439a0 8602242 (Pubitemid 26102720)
19. Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development. Gale NW Dominguez MG, Noguera I Pan L, Hughes V Valenzuela DM, Murphy AJ Adams NC, Lin HC Holash J, et al. Proc Natl Acad Sci USA 2004 101 15949 15954 10.1073/pnas.0407290101 15520367 (Pubitemid 39507907)
20. Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants. Krebs LT Shutter JR, Tanigaki K Honjo T, Stark KL Gridley T, Genes Dev 2004 18 2469 2473 10.1101/gad.1239204 15466160 (Pubitemid 39362888)
21. Dosage-sensitive requirement for mouse Dll4 in artery development. Duarte A Hirashima M Benedito R Trindade A, Diniz P Bekman E, Costa L Henrique D, Rossant J, Genes Dev 2004 18 2474 2478 10.1101/gad.1239004 15466159 (Pubitemid 39362889)
22. Regulation of Notch1 and Dll4 by vascular endothelial growth factor in arterial endothelial cells: implications for modulating arteriogenesis and angiogenesis. Liu ZJ Shirakawa T Li Y Soma A, Oka M Dotto GP, Fairman RM Velazquez OC, Herlyn M, Mol Cell Biol 2003 23 14 25 10.1128/MCB.23.1.14-25.2003 12482957 (Pubitemid 36008497)
23. Up-regulation of the Notch ligand Delta-like 4 inhibits VEGF-induced endothelial cell function. Williams CK Li JL Murga M Harris AL, Tosato G, Blood 2006 107 931 939 10.1182/blood-2005-03-1000 16219802 (Pubitemid 43156289)
24. Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Noguera-Troise I Daly C Papadopoulos NJ Coetzee S, Boland P Gale NW, Lin HC Yancopoulos GD, Thurston G, Nature 2006 444 1032 1037 10.1038/nature05355 17183313 (Pubitemid 46018516)
25. Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Ridgway J Zhang G, Wu Y Stawicki S, Liang WC Chanthery Y, Kowalski J Watts RJ, Callahan C Kasman I, et al. Nature 2006 444 1083 1087 10.1038/nature05313 17183323 (Pubitemid 46018529)
26. A notch1 ectodomain construct inhibits endothelial notch signaling, tumor growth, and angiogenesis. Funahashi Y Hernandez SL, Das I Ahn A, Huang J Vorontchikhina M, Sharma A Kanamaru E, Borisenko V Desilva DM, et al. Cancer Res 2008 68 4727 4735 10.1158/0008-5472.CAN-07-6499 18559519
27. Notch signaling is a direct determinant of keratinocyte growth arrest and entry into differentiation. Rangarajan A Talora C, Okuyama R Nicolas M, Mammucari C Oh H, Aster JC Krishna S, Metzger D Chambon P, et al. EMBO J 2001 20 3427 3436 10.1093/emboj/20.13.3427 11432830 (Pubitemid 32634350)
28. Construction of adenovirus vectors through Cre-lox recombination. Hardy S Kitamura M Harris-Stansil T Dai Y, Phipps ML, J Virol 1997 71 1842 1849 9032314 (Pubitemid 27078561)
29. Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. Jaffe EA Nachman RL, Becker CG Minick CR, J Clin Invest 1973 52 2745 2756 10.1172/JCI107470 4355998
30. Notch signaling in primary endothelial cells. Shawber CJ Das I, Francisco E Kitajewski J, Ann N Y Acad Sci 2003 995 162 170 10.1111/j.1749-6632.2003. tb03219.x 12814948 (Pubitemid 36706623)
31. Involvement of RBP-J in biological functions of mouse Notch1 and its derivatives. Kato H Taniguchi Y, Kurooka H Minoguchi S, Sakai T Nomura-Okazaki S, Tamura K Honjo T, Development 1997 124 4133 4141 9374409 (Pubitemid 27483338)
32. Notch oncoproteins depend on gamma-secretase/presenilin activity for processing and function. Das I Craig C, Funahashi Y Jung KM, Kim TW Byers R, Weng AP Kutok JL, Aster JC Kitajewski J, J Biol Chem 2004 279 30771 30780 10.1074/jbc.M309252200 15123653 (Pubitemid 38938010)
33. Characterization of rat aortic fragment within collagen gel as an angiogenesis model; capillary morphology may reflect the action mechanisms of angiogenesis inhibitors. Hata-Sugi N Kawase-Kageyama R Wakabayashi T, Biol Pharm Bull 2002 25 446 451 10.1248/bpb.25.446 11995922 (Pubitemid 40036733)
34. Establishment of a quantitative mouse dorsal air sac model and its application to evaluate a new angiogenesis inhibitor. Funahashi Y Wakabayashi T, Semba T Sonoda J, Kitoh K Yoshimatsu K, Oncol Res 1999 11 319 329 10757446
35. sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Lawson ND Vogel AM Weinstein BM, Dev Cell 2002 3 127 136 10.1016/S1534-5807(02)00198-3 12110173 (Pubitemid 34778401)
36. Functional replacement of the intracellular region of the Notch1 receptor by Epstein-Barr virus nuclear antigen 2. Sakai T Taniguchi Y Tamura K Minoguchi S, Fukuhara T Strobl LJ, Zimber-Strobl U Bornkamm GW, Honjo T, J Virol 1998 72 6034 6039 9621066 (Pubitemid 28283392)
37. Antiangiogenic effect by SU5416 is partly attributable to inhibition of Flt-1 receptor signaling. Itokawa T Nokihara H Nishioka Y Sone S, Iwamoto Y Yamada Y, Cherrington J McMahon G, Shibuya M Kuwano M, Ono M, Mol Cancer Ther 2002 1 295 302 12489845
38. A Foxo/Notch pathway controls myogenic differentiation and fiber type specification. Kitamura T Kitamura YI Funahashi Y Shawber CJ, Castrillon DH Kollipara R, DePinho RA Kitajewski J, Accili D, J Clin Invest 2007 117 2477 2485 10.1172/JCI32054 17717603 (Pubitemid 47494349)
39. Phorbol esters induce angiogenesis in vitro from large-vessel endothelial cells. Montesano R Orci L, J Cell Physiol 1987 130 284 291 10.1002/jcp. 1041300215 2434516 (Pubitemid 17035040)
40. Cooperative effect of TNFalpha, bFGF, and VEGF on the formation of tubular structures of human microvascular endothelial cells in a fibrin matrix. Role of urokinase activity. Koolwijk P van Erck MG de Vree WJ Vermeer MA, Weich HA Hanemaaijer R, van Hinsbergh VW, J Cell Biol 1996 132 1177 1188 10.1083/jcb.132.6.1177 8601593
41. Extracellular proteolysis and angiogenesis. Pepper MS, Thromb Haemost 2001 86 346 355 11487024 (Pubitemid 32663965)
42. Role of the matrix metalloprotease and plasminogen activator-plasmin systems in angiogenesis. Pepper MS, Arterioscler Thromb Vasc Biol 2001 21 1104 1117 10.1161/hq0701.093685 11451738 (Pubitemid 34215137)
43. Notch regulates the angiogenic response via induction of VEGFR-1. Funahashi Y Shawber CJ, Vorontchikhina M Sharma A, Outtz HH Kitajewski J, J Angiogenes Res 2010 2 3 10.1186/2040-2384-2-3 20298529
44. Inhibition of membrane-type 1 matrix metalloprotease by hydroxamate inhibitors: an examination of the subsite pocket. Yamamoto M Tsujishita H Hori N Ohishi Y, Inoue S Ikeda S, Okada Y, J Med Chem 1998 41 1209 1217 10.1021/jm970404a 9548812 (Pubitemid 28208176)
45. Matrix metalloproteases and tumor metastasis. Deryugina EI Quigley JP, Cancer Metastasis Rev 2006 25 9 34 10.1007/s10555-006-7886-9 16680569
46. Tumstatin, the NC1 domain of alpha3 chain of type IV collagen, is an endogenous inhibitor of pathological angiogenesis and suppresses tumor growth. Hamano Y Kalluri R, Biochem Biophys Res Commun 2005 333 292 298 10.1016/j.bbrc.2005.05.130 15979458 (Pubitemid 40848291)
47. Matrix metalloprotease-9 triggers the angiogenic switch during carcinogenesis. Bergers G Brekken R McMahon G Vu TH, Itoh T Tamaki K, Tanzawa K Thorpe P, Itohara S Werb Z, Hanahan D, Nat Cell Biol 2000 2 737 744 10.1038/35036374 11025665
48. Roles of pericellular proteolysis by membrane type-1 matrix metalloprotease in cancer invasion and angiogenesis. Seiki M Yana I, Cancer Sci 2003 94 569 574 10.1111/j.1349-7006.2003.tb01484.x 12841863 (Pubitemid 36975009)
49. Dissecting the role of matrix metalloproteases (MMP) and integrin alpha(v)beta3 in angiogenesis in vitro: absence of hemopexin C domain bioactivity, but membrane-Type 1-MMP and alpha(v)beta3 are critical. Nisato RE Hosseini G Sirrenberg C Butler GS, Crabbe T Docherty AJ, Wiesner M Murphy G, Overall CM Goodman SL, Pepper MS, Cancer Res 2005 65 9377 9387 10.1158/0008-5472.CAN-05-1512 16230401 (Pubitemid 41508006)
50. Notch activation during endothelial cell network formation in vitro targets the basic HLH transcription factor HESR-1 and downregulates VEGFR-2/KDR expression. Taylor KL Henderson AM Hughes CC, Microvasc Res 2002 64 372 383 10.1006/mvre.2002.2443 12453432 (Pubitemid 35370739)
51. The role of the vascular endothelial growth factor-Delta-like 4 ligand/Notch4-ephrin B2 cascade in tumor vessel remodeling and endothelial cell functions. Hainaud P Contreres JO Villemain A Liu LX, Plouet J Tobelem G, Dupuy E, Cancer Res 2006 66 8501 8510 10.1158/0008-5472.CAN-05-4226 16951162 (Pubitemid 44449163)
52. Angiogenesis: a team effort coordinated by notch. Phng LK Gerhardt H, Dev Cell 2009 16 196 208 10.1016/j.devcel.2009.01.015 19217422
53. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Hiratsuka S Nakamura K Iwai S Murakami M, Itoh T Kijima H, Shipley JM Senior RM, Shibuya M, Cancer Cell 2002 2 289 300 10.1016/S1535-6108(02)00153-8 12398893 (Pubitemid 41043963)
54. Regulation of multiple angiogenic pathways by Dll4 and Notch in human umbilical vein endothelial cells. Harrington LS Sainson RC Williams CK Taylor JM, Shi W Li JL, Harris AL, Microvasc Res 2008 75 144 154 10.1016/j.mvr.2007.06. 006 17692341 (Pubitemid 351249857)
55. Down-regulation of notch-1 inhibits invasion by inactivation of nuclear factor-kappaB, vascular endothelial growth factor, and matrix metalloprotease-9 in pancreatic cancer cells. Wang Z Banerjee S, Li Y Rahman KM, Zhang Y Sarkar FH, Cancer Res 2006 66 2778 2784 10.1158/0008-5472.CAN-05-4281 16510599
56. Down-regulation of Notch-1 and Jagged-1 inhibits prostate cancer cell growth, migration and invasion, and induces apoptosis via inactivation of Akt, mTOR, and NF-kappaB signaling pathways. Wang Z Li Y, Banerjee S Kong D, Ahmad A Nogueira V, Hay N Sarkar FH, J Cell Biochem 2010 109 726 736 20052673