Endothelial cell surface ATP synthase-triggered caspase-apoptotic pathway is essential for K1-5-induced antiangiogenesis

Cancer Research

Volumn 64, Issue 10, 2004, Pages 3679-3686

  Veitonmäki, Niina ^a   Cao, Renhai ^a   Wu, Lin Hua ^c   Moser, Tammy L ^d   Li, Bo ^d   Pizzo, Salvatore V ^d   Zhivotovsky, Boris ^b   Cao, Yihai ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; CASPASE; CASPASE 3; CASPASE 8; CASPASE 9; NEUTRALIZING ANTIBODY; PLASMINOGEN; PLASMINOGEN KRINGLE DOMAIN 1-5; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; UNCLASSIFIED DRUG;

ALPHA CHAIN; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BETA CHAIN; CANCER; CELL SURFACE; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; DRUG RESEARCH; DRUG SCREENING; ENDOTHELIUM CELL; ENZYME ACTIVATION; KRINGLE DOMAIN; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION;

ANGIOGENESIS INHIBITORS; ANIMALS; APOPTOSIS; ATP SYNTHETASE COMPLEXES; CASPASES; CHICK EMBRYO; CORNEA; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; FIBROSARCOMA; HUMANS; ISOENZYMES; KRINGLES; MALE; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; PLASMINOGEN;

EID: 2442691834     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-03-1754     Document Type: Article

References (42)

1. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996;86:353-64.
2. O'Reilly MS, Holmgren L, Shing Y, Chen C, Rosenthal RA, Moses M, Lane WS, Cao Y, Sage EH, Folkman J. Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 1994;79:315-28.
3. O'Reilly MS, Boehm T, Shing Y, et al. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 1997;88:277-85.
4. Maeshima Y, Sudhakar A, Lively JC, et al. Tumstatin, an endothelial cell-specific inhibitor of protein synthesis. Science 2002;295:140-3.
5. O'Reilly MS, Pirie-Shepherd S, Lane WS, Folkman J. Antiangiogenic activity of the cleaved conformation of the serpin antithrombin. Science 1999;285:1926-8.
6. Volpert OV, Lawler J, Bouck NP. A human fibrosarcoma inhibits systemic angiogenesis and the growth of experimental metastases via thrombospondin-1. Proc Natl Acad Sci USA 1998;95:6343-8.
7. Dong Z, Kumar R, Yang X, Fidler IJ. Macrophage-derived metalloelastase is responsible for the generation of angiostatin in Lewis lung carcinoma. Cell 1997;88:801-10.
8. Holmgren L, O'Reilly MS, Folkman J. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat Med 1995;1:149-53.
9. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1995;1:27-31.
10. Ferrara, N. Vascular endothelial growth factor and the regulation of angiogenesis. Recent Prog Horm Res 2000;55:15-35; discussion: 16-35.
11. Dvorak HF. VPF/VEGF and the angiogenic response. Semin Perinatol 2000;24:75-8.
12. Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature 2000;407: 249-57.
13. Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J. Vascular-specific growth factors and blood vessel formation. Nature 2000;407:242-8.
14. Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 1998;92:735-45.
15. Cao Y, Ji RW, Davidson D, et al. Kringle domains of human angiostatin. Characterization of the anti-proliferative activity on endothelial cells. J Biol Chem 1996; 271:29461-7.
16. Cao Y, Chen A, An SS, Ji RW, Davidson D, Llinas M. Kringle 5 of plasminogen is a novel inhibitor of endothelial cell growth. J Biol Chem 1997;272:22924-8.
17. Cao R, Wu HL, Veitonmaki N, Linden P, Farnebo J, Shi GY, Cao Y. Suppression of angiogenesis and tumor growth by the inhibitor K1-5 generated by plasmin-mediated proteolysis. Proc Natl Acad Sci USA 1999;96:5728-33.
18. Lucas R, Holmgren L, Garcia I, et al. Multiple forms of angiostatin induce apoptosis in endothelial cells. Blood 1998;92:4730-41.
19. Claesson-Welsh L, Welsh M, Ito N, et al. Angiostatin induces endothelial cell apoptosis and activation of focal adhesion kinase independently of the integrin-binding motif RGD. Proc Natl Acad Sci USA 1998;95:5579-83.
20. 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;6:41-8.
21. Dixelius J, Larsson H, Sasaki T, et al. Endostatin-induced tyrosine kinase signaling through the Shb adaptor protein regulates endothelial cell apoptosis. Blood 2000;95: 3403-11.
22. Dhanabal M, Ramchandran R, Waterman MJ, et al. Endostatin induces endothelial cell apoptosis. J Biol Chem 1999;274:11721-6.
23. Maeshima Y, Colorado PC, Torre A, et al. Distinct antitumor properties of a type IV collagen domain derived from basement membrane. J Biol Chem 2000;275:21340-8.
24. Volpert OV, Zaichuk T, Zhou W, et al. Inducer-stimulated Fas targets activated endothelium for destruction by anti-angiogenic thrombospondin-1 and pigment epithelium-derived factor. Nat Med 2002;8:349-57.
25. Nor JE, Mitra RS, Sutorik MM, Mooney DJ, Castle VP, Polverini PJ. Thrombospondin-1 induces endothelial cell apoptosis and inhibits angiogenesis by activating the caspase death pathway. J Vasc Res 2000;37:209-18.
26. Moser TL, Stack MS, Asplin I, et al. Angiostatin binds ATP synthase on the surface of human endothelial cells. Proc Natl Acad Sci USA 1999;96:2811-6.
27. Moser TL, Kenan DJ, Ashley TA, et al. Endothelial cell surface F1-F0 ATP synthase is active in ATP synthesis and is inhibited by angiostatin. Proc Natl Acad Sci USA 2001;98:6656-61.
28. Kohler C, Orrenius S, Zhivotovsky B. Evaluation of caspase activity in apoptotic cells. J Immunol Methods 2002;265:97-110.
29. Zheng J, Ramirez VD. Piceatannol, a stilbene phytochemical, inhibits mitochondrial F0F1-ATPase activity by targeting the Fl complex. Biochem Biophys Res Commun 1999;261:499-503.
30. Jain RK, Schlenger K, Hockel M, Yuan F. Quantitative angiogenesis assays: progress and problems. Nat Med 1997;3:1203-8.
31. Bedner E, Smolewski P, Amstad P, Darzynkiewicz Z. Activation of caspases measured in situ by binding of fluorochrome-labeled inhibitors of caspases (FLICA): correlation with DNA fragmentation. Exp Cell Res 2000;259:308-13.
32. Smolewski P, Bedner E, Du L, et al. Detection of caspases activation by fluorochrome-labeled inhibitors: multiparameter analysis by laser scanning cytometry. Cytometry 2001;44:73-82.
33. Grabarek J, Amstad P, Darzynkiewicz Z. Use of fluorescently labeled caspase inhibitors as affinity labels to detect activated caspases. Hum Cell 2002;15:1-12.
34. Darzynkiewicz Z, Bedner E, Smolewski P, Lee BW, Johnson GL. Detection of caspases activation in situ by fluorochrome-labeled inhibitors of caspases (FLICA). Methods Mol Biol 2002;203:289-99.
35. Nunez G, Benedict MA, Hu Y, Inohara N. Caspases: the proteases of the apoptotic pathway. Oncogene 1998;17:3237-45.
36. Estrov Z, Manna SK, Harris D, et al, Phenylarsine oxide blocks interleukin-1β-induced activation of the nuclear transcription factor NF-κB, inhibits proliferation, and induces apoptosis of acute myelogenous leukemia cells. Blood 1999; 94:2844-53.
37. Gastman BR, Johnson DE, Whiteside TL, Rabinowich H. Tumor-induced apoptosis of T lymphocytes: elucidation of intracellular apoptotic events. Blood 2000;95: 2015-23.
38. Tarui T, Miles LA, Takada Y. Specific interaction of angiostatin with integrin α(v)β(3) in endothelial cells. J Biol Chem 2001;276:39562-8.
39. Troyanovsky B, Levchenko T, Mansson G, Matvijenko O, Holmgren L. Angiomotin: an angiostatin binding protein that regulates endothelial cell migration and tube formation. J Cell Biol 2001;152:1247-54.
40. O'Reilly MS, Brem H, Folkman J. Treatment of murine hemangioendotheliomas with the angiogenesis inhibitor AGM-1470. J Pediatr Surg 1995;30:325-9; discussion: 329-30.
41. Bergers G, Javaherian K, Lo KM, Folkman J, Hanahan D, Effects of angiogenesis inhibitors on multistage carcinogenesis in mice. Science 1999;284:808-12.
42. Boehm T, Folkman J, Browder T, O'Reilly MS. Antiangiogenic therapy of experimental cancer does not induce acquired drug resistance. Nature 1997;390:404-7.