The roles of ADAMTS in angiogenesis and cancer

Tumor Biology

Volumn 36, Issue 6, 2015, Pages 4039-4051

  Sun, Yi ^a   Huang, Jintuan ^a   Yang, Zuli ^a  

^a THE SIXTH AFFILIATED HOSPITAL OF SUN YAT SEN UNIVERSITY   (China)

Author keywords

ADAMTS; Angiogenesism; Tumor progression and metastasis; VEGF

Indexed keywords

ADAM PROTEIN; ADAMTS1 PROTEIN; ADAMTS10 PROTEIN; ADAMTS12 PROTEIN; ADAMTS16 PROTEIN; ADAMTS17 PROTEIN; ADAMTS18 PROTEIN; ADAMTS19 PROTEIN; ADAMTS2 PROTEIN; ADAMTS20 PROTEIN; ADAMTS6 PROTEIN; ADAMTS8 PROTEIN; ADAMTS9 PROTEIN; AGGRECANASE 1; AGGRECANASE 2; ANGIOPOIETIN 2; INTERLEUKIN 1; MITOGEN ACTIVATED PROTEIN KINASE 1; PLACENTAL GROWTH FACTOR; PLATELET DERIVED ENDOTHELIAL CELL GROWTH FACTOR; PROTEIN KINASE C; THROMBOSPONDIN 1; THROMBOSPONDIN 2; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; UNINDEXED DRUG; VASCULOTROPIN; VASCULOTROPIN 165; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2; VON WILLEBRAND FACTOR CLEAVING PROTEINASE; VEGFA PROTEIN, HUMAN;

ANGIOGENESIS; BREAST CARCINOMA; CANCER GROWTH; CELL PROLIFERATION; DOWN REGULATION; EHLERS DANLOS SYNDROME; EXTRACELLULAR MATRIX; HUMAN; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; THROMBOTIC THROMBOCYTOPENIC PURPURA; UPREGULATION; CARCINOGENESIS; CELL MOTION; CHEMISTRY; CLASSIFICATION; GENETICS; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY;

ADAM PROTEINS; CARCINOGENESIS; CELL MOVEMENT; CELL PROLIFERATION; HUMANS; NEOVASCULARIZATION, PATHOLOGIC; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84938960157     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-015-3461-8     Document Type: Review

References (112)

1. Kuno K, Kanada N, Nakashima E, Fujiki F, Ichimura F, Matsushima K. 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(1):556–62.
2. Folkman J. Angiogenesis. Annu Rev Med. 2006;57:1–18.
3. Ferrara N. VEGF as a therapeutic target in cancer. Oncology. 2005;69 Suppl 3:11–6.
4. Yoo SY, Kwon SM. Angiogenesis and its therapeutic opportunities. Mediat Inflamm. 2013;2013:127170.
5. Gimbrone Jr MA, Cotran RS, Leapman SB, Folkman J. Tumor growth and neovascularization: an experimental model using the rabbit cornea. J Natl Cancer Inst. 1974;52(2):413–27.
6. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med. 1971;285(21):1182–6.
7. Samples J, Willis M, Klauber-Demore N. Targeting angiogenesis and the tumor microenvironment. Surg Oncol Clin N Am. 2013;22(4):629–39.
8. Dvorak HF, Nagy JA, Feng D, Brown LF, Dvorak AM. Vascular permeability factor/vascular endothelial growth factor and the significance of microvascular hyperpermeability in angiogenesis. Curr Top Microbiol Immunol. 1999;237:97–132.
9. Dvorak HF, Brown LF, Detmar M, Dvorak AM. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol. 1995;146(5):1029–39.
10. Shibuya M. Structure and function of VEGF/VEGF-receptor system involved in angiogenesis. Cell Struct Funct. 2001;26(1):25–35.
11. Okada F, Rak JW, Croix BS, Lieubeau B, Kaya M, Roncari L, et al. Impact of oncogenes in tumor angiogenesis: mutant K-ras up-regulation of vascular endothelial growth factor/vascular permeability factor is necessary, but not sufficient for tumorigenicity of human colorectal carcinoma cells. Proc Natl Acad Sci U S A. 1998;95(7):3609–14.
12. Iliopoulos O, Levy AP, Jiang C, Kaelin Jr WG, Goldberg MA. Negative regulation of hypoxia-inducible genes by the von Hippel-Lindau protein. Proc Natl Acad Sci U S A. 1996;93(20):10595–9.
13. Kampen KR. The mechanisms that regulate the localization and overexpression of VEGF receptor-2 are promising therapeutic targets in cancer biology. Anticancer Drugs. 2012;23(4):347–54.
14. Brown LF, Berse B, Jackman RW, Tognazzi K, Guidi AJ, Dvorak HF, et al. Expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in breast cancer. Hum Pathol. 1995;26(1):86–91.
15. Porter S, Clark IM, Kevorkian L, Edwards DR. The ADAMTS metalloproteinases. Biochem J. 2005;386(Pt 1):15–27.
16. Hurskainen TL, Hirohata S, Seldin MF, Apte SS. ADAM-TS5, ADAM-TS6, and ADAM-TS7, novel members of a new family of zinc metalloproteases. General features and genomic distribution of the ADAM-TS family. J Biol Chem. 1999;274(36):25555–63.
17. Luque A, Carpizo DR, Iruela-Arispe ML. ADAMTS1/METH1 inhibits endothelial cell proliferation by direct binding and sequestration of VEGF165. J Biol Chem. 2003;278(26):23656–65.
18. Apte SS. A disintegrin-like and metalloprotease (reprolysin-type) with thrombospondin type 1 motif (ADAMTS) superfamily: functions and mechanisms. J Biol Chem. 2009;284(46):31493–7.
19. Clark ME, Kelner GS, Turbeville LA, Boyer A, Arden KC, Maki RA. ADAMTS9, a novel member of the ADAM-TS/metallospondin gene family. Genomics. 2000;67(3):343–50.
20. Nardi JB, Martos R, Walden KK, Lampe DJ, Robertson HM. Expression of lacunin, a large multidomain extracellular matrix protein, accompanies morphogenesis of epithelial monolayers in Manduca sexta. Insect Biochem Mol Biol. 1999;29(10):883–97.
21. Jones GC, Riley GP. ADAMTS proteinases: a multi-domain, multi-functional family with roles in extracellular matrix turnover and arthritis. Arthritis Res Ther. 2005;7(4):160–9.
22. Zheng X, Chung D, Takayama TK, Majerus EM, Sadler JE, Fujikawa K. Structure of von Willebrand factor-cleaving protease (ADAMTS13), a metalloprotease involved in thrombotic thrombocytopenic purpura. J Biol Chem. 2001;276(44):41059–63.
23. Gao G, Westling J, Thompson VP, Howell TD, Gottschall PE, Sandy JD. Activation of the proteolytic activity of ADAMTS4 (aggrecanase-1) by C-terminal truncation. J Biol Chem. 2002;277(13):11034–41.
24. Kuno K, Matsushima K. ADAMTS-1 protein anchors at the extracellular matrix through the thrombospondin type I motifs and its spacing region. J Biol Chem. 1998;273(22):13912–7.
25. Rocks N, Paulissen G, El Hour M, Quesada F, Crahay C, Gueders M, et al. Emerging roles of ADAM and ADAMTS metalloproteinases in cancer. Biochimie. 2008;90(2):369–79.
26. Stanton H, Melrose J, Little CB, Fosang AJ. Proteoglycan degradation by the ADAMTS family of proteinases. Biochim Biophys Acta. 2011;1812(12):1616–29.
27. Tang BL. ADAMTS: a novel family of extracellular matrix proteases. Int J Biochem Cell Biol. 2001;33(1):33–44.
28. Kuno K, Okada Y, Kawashima H, Nakamura H, Miyasaka M, Ohno H, et al. ADAMTS-1 cleaves a cartilage proteoglycan, aggrecan. FEBS Lett. 2000;478(3):241–5.
29. Rodriguez-Manzaneque JC, Westling J, Thai SN, Luque A, Knauper V, Murphy G, et al. ADAMTS1 cleaves aggrecan at multiple sites and is differentially inhibited by metalloproteinase inhibitors. Biochem Biophys Res Commun. 2002;293(1):501–8.
30. Ricciardelli C, Frewin KM, Tan Ide A, Williams ED, Opeskin K, Pritchard MA, et al. The ADAMTS1 protease gene is required for mammary tumor growth and metastasis. Am J Pathol. 2011;179(6):3075–85.
31. McCulloch DR, Nelson CM, Dixon LJ, Silver DL, Wylie JD, Lindner V, et al. ADAMTS metalloproteases generate active versican fragments that regulate interdigital web regression. Dev Cell. 2009;17(5):687–98.
32. Tortorella MD, Malfait AM, Deccico C, Arner E. The role of ADAM-TS4 (aggrecanase-1) and ADAM-TS5 (aggrecanase-2) in a model of cartilage degradation. Osteoarthr Cartil. 2001;9(6):539–52.
33. Matthews RT, Gary SC, Zerillo C, Pratta M, Solomon K, Arner EC, et al. Brain-enriched hyaluronan binding (BEHAB)/brevican cleavage in a glioma cell line is mediated by a disintegrin and metalloproteinase with thrombospondin motifs (ADAMTS) family member. J Biol Chem. 2000;275(30):22695–703.
34. Sandy JD, Westling J, Kenagy RD, Iruela-Arispe ML, Verscharen C, Rodriguez-Mazaneque JC, et al. Versican V1 proteolysis in human aorta in vivo occurs at the Glu441-Ala442 bond, a site that is cleaved by recombinant ADAMTS-1 and ADAMTS-4. J Biol Chem. 2001;276(16):13372–8.
35. Nakamura M, Sone S, Takahashi I, Mizoguchi I, Echigo S, Sasano Y. Expression of versican and ADAMTS1, 4, and 5 during bone development in the rat mandible and hind limb. J Histochem Cytochem. 2005;53(12):1553–62.
36. Kuno K, Terashima Y, Matsushima K. ADAMTS-1 is an active metalloproteinase associated with the extracellular matrix. J Biol Chem. 1999;274(26):18821–6.
37. Somerville RP, Longpre JM, Jungers KA, Engle JM, Ross M, Evanko S, et al. Characterization of ADAMTS-9 and ADAMTS-20 as a distinct ADAMTS subfamily related to Caenorhabditis elegans GON-1. J Biol Chem. 2003;278(11):9503–13.
38. Collins-Racie LA, Flannery CR, Zeng W, Corcoran C, Annis-Freeman B, Agostino MJ, et al. ADAMTS-8 exhibits aggrecanase activity and is expressed in human articular cartilage. Matrix Biol. 2004;23(4):219–30.
39. Yamaji NK., Nishimura K., Abe O., Ohara T., Nagase and N. Nomura, Novel metalloprotease having aggrecanase activity. 2004, Google Patents.
40. Wang WM, Lee S, Steiglitz BM, Scott IC, Lebares CC, Allen ML, et al. Transforming growth factor-beta induces secretion of activated ADAMTS-2. A procollagen III N-proteinase. J Biol Chem. 2003;278(21):19549–57.
41. Colige A, Sieron AL, Li SW, Schwarze U, Petty E, Wertelecki W, et al. Human Ehlers-Danlos syndrome type VII C and bovine dermatosparaxis are caused by mutations in the procollagen I N-proteinase gene. Am J Hum Genet. 1999;65(2):308–17.
42. Nusgens BV, Verellen-Dumoulin C, Hermanns-Le T, De Paepe A, Nuytinck L, Pierard GE, et al. Evidence for a relationship between Ehlers-Danlos type VII C in humans and bovine dermatosparaxis. Nat Genet. 1992;1(3):214–7.
43. Li SW, Arita M, Fertala A, Bao Y, Kopen GC, Langsjo TK, et al. Transgenic mice with inactive alleles for procollagen N-proteinase (ADAMTS-2) develop fragile skin and male sterility. Biochem J. 2001;355(Pt 2):271–8.
44. Fernandes RJ, Hirohata S, Engle JM, Colige A, Cohn DH, Eyre DR, et al. Procollagen II amino propeptide processing by ADAMTS-3. Insights on dermatosparaxis. J Biol Chem. 2001;276(34):31502–9.
45. Colige A, Vandenberghe I, Thiry M, Lambert CA, Van Beeumen J, Li SW, et al. Cloning and characterization of ADAMTS-14, a novel ADAMTS displaying high homology with ADAMTS-2 and ADAMTS-3. J Biol Chem. 2002;277(8):5756–66.
46. Somerville RP, Longpre JM, Apel ED, Lewis RM, Wang LW, Sanes JR, et al. ADAMTS7B, the full-length product of the ADAMTS7 gene, is a chondroitin sulfate proteoglycan containing a mucin domain. J Biol Chem. 2004;279(34):35159–75.
47. Dagoneau N, Benoist-Lasselin C, Huber C, Faivre L, Megarbane A, Alswaid A, et al. ADAMTS10 mutations in autosomal recessive Weill-Marchesani syndrome. Am J Hum Genet. 2004;75(5):801–6.
48. Somerville RP, Jungers KA, Apte SS. Discovery and characterization of a novel, widely expressed metalloprotease, ADAMTS10, and its proteolytic activation. J Biol Chem. 2004;279(49):51208–17.
49. Cal S, Arguelles JM, Fernandez PL, Lopez-Otin C. Identification, characterization, and intracellular processing of ADAM-TS12, a novel human disintegrin with a complex structural organization involving multiple thrombospondin-1 repeats. J Biol Chem. 2001;276(21):17932–40.
50. Porter S, Scott SD, Sassoon EM, Williams MR, Jones JL, Girling AC, et al. Dysregulated expression of adamalysin-thrombospondin genes in human breast carcinoma. Clin Cancer Res. 2004;10(7):2429–40.
51. Kevorkian L, Young DA, Darrah C, Donell ST, Shepstone L, Porter S, et al. Expression profiling of metalloproteinases and their inhibitors in cartilage. Arthritis Rheum. 2004;50(1):131–41.
52. Wagstaff L, Kelwick R, Decock J, Edwards DR. The roles of ADAMTS metalloproteinases in tumorigenesis and metastasis. Front Biosci (Landmark Ed). 2011;16:p. 1861–72.
53. Casal C, Torres-Collado AX, Plaza-Calonge Mdel C, Martino-Echarri E, Cajal Y, Ramon S, et al. ADAMTS1 contributes to the acquisition of an endothelial-like phenotype in plastic tumor cells. Cancer Res. 2010;70(11):4676–86.
54. Lee NV, Sato M, Annis DS, Loo JA, Wu L, Mosher DF, et al. ADAMTS1 mediates the release of antiangiogenic polypeptides from TSP1 and 2. EMBO J. 2006;25(22):5270–83.
55. Lawler J. The functions of thrombospondin-1 and-2. Curr Opin Cell Biol. 2000;12(5):634–40.
56. Nagy JA, Dvorak AM, Dvorak HF. VEGF-A and the induction of pathological angiogenesis. Annu Rev Pathol. 2007;2:251–75.
57. Nagy JA, Dvorak AM, Dvorak HF. Vascular hyperpermeability, angiogenesis, and stroma generation. Cold Spring Harb Perspect Med. 2012;2(2):a006544.
58. Swayne GT, Smaje LH, Bergel DH. Distensibility of single capillaries and venules in the rat and frog mesentery. Int J Microcirc Clin Exp. 1989;8(1):25–42.
59. Chang SH, Kanasaki K, Gocheva V, Blum G, Harper J, Moses MA, et al. VEGF-A induces angiogenesis by perturbing the cathepsin-cysteine protease inhibitor balance in venules, causing basement membrane degradation and mother vessel formation. Cancer Res. 2009;69(10):4537–44.
60. Liu YJ, Xu Y, Yu Q. Full-length ADAMTS-1 and the ADAMTS-1 fragments display pro- and antimetastatic activity, respectively. Oncogene. 2006;25(17):2452–67.
61. Kumar S, Sharghi-Namini S, Rao N, Ge R. ADAMTS5 functions as an anti-angiogenic and anti-tumorigenic protein independent of its proteoglycanase activity. Am J Pathol. 2012;181(3):1056–68.
62. Rodriguez-Manzaneque JC, Milchanowski AB, Dufour EK, Leduc R, Iruela-Arispe ML. Characterization of METH-1/ADAMTS1 processing reveals two distinct active forms. J Biol Chem. 2000;275(43):33471–9.
63. Fu Y, Nagy JA, Brown LF, Shih SC, Johnson PY, Chan CK, et al. Proteolytic cleavage of versican and involvement of ADAMTS-1 in VEGF-A/VPF-induced pathological angiogenesis. J Histochem Cytochem. 2011;59(5):463–73.
64. Nicosia RF, Tuszynski GP. Matrix-bound thrombospondin promotes angiogenesis in vitro. J Cell Biol. 1994;124(1-2):183–93.
65. Tolsma SS, Volpert OV, Good DJ, Frazier WA, Polverini PJ, Bouck N. Peptides derived from two separate domains of the matrix protein thrombospondin-1 have anti-angiogenic activity. J Cell Biol. 1993;122(2):497–511.
66. Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N. Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med. 2000;6(1):41–8.
67. Streit M, Riccardi L, Velasco P, Brown LF, Hawighorst T, Bornstein P, et al. Thrombospondin-2: a potent endogenous inhibitor of tumor growth and angiogenesis. Proc Natl Acad Sci U S A. 1999;96(26):14888–93.
68. Lawler J, Detmar M. Tumor progression: the effects of thrombospondin-1 and -2. Int J Biochem Cell Biol. 2004;36(6):1038–45.
69. Gustavsson H, Tesan T, Jennbacken K, Kuno K, Damber JE, Welen K. ADAMTS1 alters blood vessel morphology and TSP1 levels in LNCaP and LNCaP-19 prostate tumors. BMC Cancer. 2010;10:288.
70. Yee KO, Connolly CM, Duquette M, Kazerounian S, Washington R, Lawler J. The effect of thrombospondin-1 on breast cancer metastasis. Breast Cancer Res Treat. 2009;114(1):85–96.
71. Lee YJ, Koch M, Karl D, Torres-Collado AX, Fernando NT, Rothrock C, et al. Variable inhibition of thrombospondin 1 against liver and lung metastases through differential activation of metalloproteinase ADAMTS1. Cancer Res. 2010;70(3):948–56.
72. Vazquez F, Hastings G, Ortega MA, Lane TF, Oikemus S, Lombardo M, 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(33):23349–57.
73. Park JE, Keller GA, Ferrara N. The vascular endothelial growth factor (VEGF) isoforms: differential deposition into the subepithelial extracellular matrix and bioactivity of extracellular matrix-bound VEGF. Mol Biol Cell. 1993;4(12):1317–26.
74. Iruela-Arispe ML, Carpizo D, Luque A. ADAMTS1: a matrix metalloprotease with angioinhibitory properties. Ann N Y Acad Sci. 2003;995:183–90.
75. Gupta K, Gupta P, Wild R, Ramakrishnan S, Hebbel RP. Binding and displacement of vascular endothelial growth factor (VEGF) by thrombospondin: effect on human microvascular endothelial cell proliferation and angiogenesis. Angiogenesis. 1999;3(2):147–58.
76. Gengrinovitch S, Berman B, David G, Witte L, Neufeld G, Ron D. Glypican-1 is a VEGF165 binding proteoglycan that acts as an extracellular chaperone for VEGF165. J Biol Chem. 1999;274(16):10816–22.
77. Chen J, Zhi Y, Chang X, Zhang S, Dai D. Expression of ADAMTS1 and its correlation with angiogenesis in primary gastric cancer and lymph node metastasis. Dig Dis Sci. 2013;58(2):405–13.
78. Xu Z, Yu Y, Duh EJ. Vascular endothelial growth factor upregulates expression of ADAMTS1 in endothelial cells through protein kinase C signaling. Invest Ophthalmol Vis Sci. 2006;47(9):4059–66.
79. Kumar S, Rao N, Ge R. Emerging roles of ADAMTSs in angiogenesis and cancer. Cancers (Basel). 2012;4(4):1252–99.
80. Obika M, Ogawa H, Takahashi K, Li J, Hatipoglu OF, Cilek MZ, et al. Tumor growth inhibitory effect of ADAMTS1 is accompanied by the inhibition of tumor angiogenesis. Cancer Sci. 2012;103(10):1889–97.
81. Gustavsson H, Wang W, Jennbacken K, Welen K, Damber JE. ADAMTS1, a putative anti-angiogenic factor, is decreased in human prostate cancer. BJU Int. 2009;104(11):1786–90.
82. Gustavsson H, Jennbacken K, Welen K, Damber JE. Altered expression of genes regulating angiogenesis in experimental androgen-independent prostate cancer. Prostate. 2008;68(2):161–70.
83. Porter S, Span PN, Sweep FC, Tjan-Heijnen VC, Pennington CJ, Pedersen TX, et al. ADAMTS8 and ADAMTS15 expression predicts survival in human breast carcinoma. Int J Cancer. 2006;118(5):1241–7.
84. Masui T, Hosotani R, Tsuji S, Miyamoto Y, Yasuda S, Ida J, et al. Expression of METH-1 and METH-2 in pancreatic cancer. Clin Cancer Res. 2001;7(11):3437–43.
85. Gendron C, Kashiwagi M, Lim NH, Enghild JJ, Thogersen IB, Hughes C, et al. Proteolytic activities of human ADAMTS-5: comparative studies with ADAMTS-4. J Biol Chem. 2007;282(25):18294–306.
86. Sharghi-Namini S, Fan H, Sulochana KN, Potturi P, Xiang W, Chong YS, et al. The first but not the second thrombospondin type 1 repeat of ADAMTS5 functions as an angiogenesis inhibitor. Biochem Biophys Res Commun. 2008;371(2):215–9.
87. El Hour M, Moncada-Pazos A, Blacher S, Masset A, Cal S, Berndt S, et al. Higher sensitivity of Adamts12-deficient mice to tumor growth and angiogenesis. Oncogene. 2010;29(20):3025–32.
88. Llamazares M, Obaya AJ, Moncada-Pazos A, Heljasvaara R, Espada J, Lopez-Otin C, et al. The ADAMTS12 metalloproteinase exhibits anti-tumorigenic properties through modulation of the Ras-dependent ERK signalling pathway. J Cell Sci. 2007;120(Pt 20):3544–52.
89. Ren B, Yee KO, Lawler J, Khosravi-Far R. Regulation of tumor angiogenesis by thrombospondin-1. Biochim Biophys Acta. 2006;1765(2):178–88.
90. Colige A, Ruggiero F, Vandenberghe I, Dubail J, Kesteloot F, Van Beeumen J, et al. Domains and maturation processes that regulate the activity of ADAMTS-2, a metalloproteinase cleaving the aminopropeptide of fibrillar procollagens types I-III and V. J Biol Chem. 2005;280(41):34397–408.
91. Dubail J, Kesteloot F, Deroanne C, Motte P, Lambert V, Rakic JM, et al. ADAMTS-2 functions as anti-angiogenic and anti-tumoral molecule independently of its catalytic activity. Cell Mol Life Sci. 2010;67(24):4213–32.
92. Sadler JE. Biochemistry and genetics of von Willebrand factor. Annu Rev Biochem. 1998;67:395–424.
93. Ruggeri ZM. The role of von Willebrand factor in thrombus formation. Thromb Res. 2007;120 Suppl 1:S5–9.
94. Levy GG, Nichols WC, Lian EC, Foroud T, McClintick JN, McGee BM, et al. Mutations in a member of the ADAMTS gene family cause thrombotic thrombocytopenic purpura. Nature. 2001;413(6855):488–94.
95. Starke RD, Ferraro F, Paschalaki KE, Dryden NH, McKinnon TA, Sutton RE, et al. Endothelial von Willebrand factor regulates angiogenesis. Blood. 2011;117(3):1071–80.
96. Hodivala-Dilke K. alphavbeta3 integrin and angiogenesis: a moody integrin in a changing environment. Curr Opin Cell Biol. 2008;20(5):p. 514–9.
97. Hodivala-Dilke KM, Reynolds AR, Reynolds LE. Integrins in angiogenesis: multitalented molecules in a balancing act. Cell Tissue Res. 2003;314(1):131–44.
98. Dalton SL, Scharf E, Briesewitz R, Marcantonio EE, Assoian RK. Cell adhesion to extracellular matrix regulates the life cycle of integrins. Mol Biol Cell. 1995;6(12):1781–91.
99. Yu Q, Stamenkovic I. Angiopoietin-2 is implicated in the regulation of tumor angiogenesis. Am J Pathol. 2001;158(2):563–70.
100. Hashizume H, Falcon BL, Kuroda T, Baluk P, Coxon A, Yu D, et al. Complementary actions of inhibitors of angiopoietin-2 and VEGF on tumor angiogenesis and growth. Cancer Res. 2010;70(6):2213–23.
101. Thomas M, Felcht M, Kruse K, Kretschmer S, Deppermann C, Biesdorf A, et al. Angiopoietin-2 stimulation of endothelial cells induces alphavbeta3 integrin internalization and degradation. J Biol Chem. 2010;285(31):23842–9.
102. Lee M, Rodansky ES, Smith JK, Rodgers GM. ADAMTS13 promotes angiogenesis and modulates VEGF-induced angiogenesis. Microvasc Res. 2012;84(2):109–15.
103. Koo BH, Coe DM, Dixon LJ, Somerville RP, Nelson CM, Wang LW, et al. ADAMTS9 is a cell-autonomously acting, anti-angiogenic metalloprotease expressed by microvascular endothelial cells. Am J Pathol. 2010;176(3):1494–504.
104. Kelwick R, Wagstaff L, Decock J, Roghi C, Cooley LS, Robinson SD, et al. Metalloproteinase-dependent and -independent processes contribute to inhibition of breast cancer cell migration, angiogenesis and liver metastasis by a disintegrin and metalloproteinase with thrombospondin motifs-15. Int J Cancer. 2015;136(4):E14–26.
105. Nissinen L, Kahari VM. ADAMTS5: a new player in the vascular field. Am J Pathol. 2012;181(3):743–5.
106. Saharinen P, Eklund L, Pulkki K, Bono P, Alitalo K. VEGF and angiopoietin signaling in tumor angiogenesis and metastasis. Trends Mol Med. 2011;17(7):347–62.
107. Rao N, Ke Z, Liu H, Ho CJ, Kumar S, Xiang W, et al. ADAMTS4 and its proteolytic fragments differentially affect melanoma growth and angiogenesis in mice. Int J Cancer. 2013;133(2):294–306.
108. Keightley M, Sales K, Jabbour H. PGF2alpha-F-prostanoid receptor signalling via ADAMTS1 modulates epithelial cell invasion and endothelial cell function in endometrial cancer. BMC Cancer. 2010;10(1):488.
109. Hsu YP, Staton CA, Cross N, Buttle DJ. Anti-angiogenic properties of ADAMTS-4 in vitro. Int J Exp Pathol. 2012;93(1):70–7.
110. Karagiannis ED, Popel AS. Anti-angiogenic peptides identified in thrombospondin type I domains. Biochem Biophys Res Commun. 2007;359(1):63–9.
111. Lo PHY, Lung HL, Cheung AKL, Apte SS, Chan KW, Kwong FM, et al. Extracellular protease ADAMTS9 Suppresses esophageal and nasopharyngeal carcinoma tumor formation by inhibiting angiogenesis. Cancer Res. 2010;70(13):5567–76.
112. Kuno K, Bannai K, Hakozaki M, Matsushima K, Hirose K. The carboxyl-terminal half region of ADAMTS-1 suppresses both tumorigenicity and experimental tumor metastatic potential. Biochem Biophys Res Commun. 2004;319(4):1327–33.