Mitochondria as targets in angiogenesis inhibition

Molecular Aspects of Medicine

Volumn 31, Issue 1, 2010, Pages 113-131

  Park, Danielle ^a   Dilda, Pierre J ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Angiogenesis; Angiogenesis inhibitors; Mitochondria

Indexed keywords

1 (2 METHOXYETHOXY) 2 METHYL 3 (2 PYRAZINYLMETHYL)NAPHTHO[2,3 D]IMIDAZOLE 4,9 DIONE; AE 941; ALPHA TOCOPHEROL DERIVATIVE; ANGIOGENESIS INHIBITOR; ANGIOPOIETIN; APOPTOSIS INDUCING FACTOR; BEVACIZUMAB; CYTOCHROME C; EM 1241; ENDONUCLEASE G; ENDOSTATIN; ERLOTINIB; FIBROBLAST GROWTH FACTOR; GEFITINIB; GEMCITABINE; GSAO; INTEGRIN; LY 2181308; MATRIX METALLOPROTEINASE; PACLITAXEL; PROHIBITIN; PROTEIN BAX; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SILIBININ; SORAFENIB; SUNITINIB; THROMBOSPONDIN; UNCLASSIFIED DRUG; UNINDEXED DRUG; VASCULOTROPIN;

ADJUVANT THERAPY; ANTIANGIOGENIC THERAPY; APOPTOSIS; ATHEROSCLEROSIS; AUTOIMMUNE DISEASE; BREAST CANCER; CANCER INHIBITION; CANCER SURVIVAL; CELL CYCLE PROGRESSION; CLINICAL TRIAL; COLORECTAL CANCER; COLORECTAL CARCINOMA; CYTOTOXICITY; DRUG HALF LIFE; DRUG MECHANISM; DRUG SCREENING; DRUG SELECTIVITY; DRUG TARGETING; FIBROSARCOMA; GASTROINTESTINAL STROMAL TUMOR; HUMAN; KIDNEY CANCER; KIDNEY CARCINOMA; LEWIS CARCINOMA; LIVER CELL CARCINOMA; LUNG CANCER; LUNG CARCINOMA; LUNG NON SMALL CELL CANCER; LYMPHOMA; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; MITOCHONDRION; MULTIPLE MYELOMA; NONHUMAN; OVARY CANCER; PANCREAS CANCER; PANCREAS CARCINOMA; PROSTATE CARCINOMA; PROTEIN FUNCTION; RETINA MACULA DEGENERATION; REVIEW; SIGNAL TRANSDUCTION; SOLID TUMOR; TUMOR GROWTH; TUMOR VASCULARIZATION; UTERINE CERVIX CARCINOMA IN SITU;

ANGIOGENESIS INHIBITORS; ANIMALS; APOPTOSIS; DRUG DELIVERY SYSTEMS; HUMANS; MITOCHONDRIA; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC;

EID: 77649187594     PISSN: 00982997     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mam.2009.12.005     Document Type: Review

References (159)

1. Abdollahi A., Hahnfeldt P., Maercker C., Grone H.J., Debus J., Ansorge W., Folkman J., Hlatky L., and Huber P.E. Endostatin's antiangiogenic signaling network. Mol. Cell. 13 (2004) 649-663
2. Adams E., Jeter D., Cordes A.W., and Kolis J.W. Chemistry of organometalloid complexes with potential antidotes: structure of an organoarsenic(III) dithiolate ring. Inorg. Chem. 29 (1990) 1500-1503
3. Alavi A., Hood J.D., Frausto R., Stupack D.G., and Cheresh D.A. Role of Raf in vascular protection from distinct apoptotic stimuli. Science 301 (2003) 94-96
4. Altieri D.C. Survivin, cancer networks and pathway-directed drug discovery. Nat. Rev. Cancer 8 (2008) 61-70
5. Andre N., Braguer D., Brasseur G., Goncalves A., Lemesle-Meunier D., Guise S., Jordan M.A., and Briand C. Paclitaxel induces release of cytochrome c from mitochondria isolated from human neuroblastoma cells'. Cancer Res. 60 (2000) 5349-5353
6. Arbiser J.L., Moses M.A., Fernandez C.A., Ghiso N., Cao Y., Klauber N., Frank D., Brownlee M., Flynn E., Parangi S., et al. Oncogenic H-ras stimulates tumor angiogenesis by two distinct pathways. Proc. Natl. Acad. Sci. USA 94 (1997) 861-866
7. Augustin H.G., Koh G.Y., Thurston G., and Alitalo K. Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol. Cell. Biol. 10 (2009) 165-177
8. Avraamides C.J., Garmy-Susini B., and Varner J.A. Integrins in angiogenesis and lymphangiogenesis. Nat. Rev. Cancer 8 (2008) 604-617
9. Basanez G., Sharpe J.C., Galanis J., Brandt T.B., Hardwick J.M., and Zimmerberg J. Bax-type apoptotic proteins porate pure lipid bilayers through a mechanism sensitive to intrinsic monolayer curvature. J. Biol. Chem. 277 (2002) 49360-49365
10. Bates D.O., and Harper S.J. Regulation of vascular permeability by vascular endothelial growth factors. Vasc. Pharmacol. 39 (2002) 225-237
11. Bhattacharjee H., and Rosen B.P. Spatial proximity of Cys113, Cys172, and Cys422 in the metalloactivation domain of the ArsA ATPase. J. Biol. Chem. 271 (1996) 24465-24470
12. Bianco R., Troiani T., Tortora G., and Ciardiello F. Intrinsic and acquired resistance to EGFR inhibitors in human cancer therapy. Endocr Relat Cancer 12 Suppl. 1 (2005) S159-S171
13. Birbes H., Luberto C., Hsu Y.T., El Bawab S., Hannun Y.A., and Obeid L.M. A mitochondrial pool of sphingomyelin is involved in TNFalpha-induced Bax translocation to mitochondria. Biochem. J. 386 (2005) 445-451
14. Blanc-Brude O.P., Mesri M., Wall N.R., Plescia J., Dohi T., and Altieri D.C. Therapeutic targeting of the survivin pathway in cancer: initiation of mitochondrial apoptosis and suppression of tumor-associated angiogenesis. Clin. Cancer Res.. 9 (2003) 2683-2692
15. Boehning D., Patterson R.L., Sedaghat L., Glebova N.O., Kurosaki T., and Snyder S.H. Cytochrome c binds to inositol (1, 4, 5) trisphosphate receptors, amplifying calcium-dependent apoptosis. Nat. Cell Biol. 5 (2003) 1051-1061
16. Boehning D., Patterson R.L., and Snyder S.H. Apoptosis and calcium: new roles for cytochrome c and inositol 1, 4, 5-trisphosphate. Cell Cycle 3 (2004) 252-254
17. Boivin D., Gendron S., Beaulieu E., Gingras D., and Beliveau R. The antiangiogenic agent Neovastat (AE-941) induces endothelial cell apoptosis. Mol. Cancer Ther. 1 (2002) 795-802
18. Cao Y. Molecular mechanisms and therapeutic development of angiogenesis inhibitors. Adv Cancer Res. 100 (2008) 113-131
19. Carmeliet P. Angiogenesis in life, disease and medicine. Nature 438 (2005) 932-936
20. Carmeliet P., and Jain R.K. Angiogenesis in cancer and other diseases. Nature 407 (2000) 249-257
21. Carter B.Z., Wang R.Y., Schober W.D., Milella M., Chism D., and Andreeff M. Targeting Survivin expression induces cell proliferation defect and subsequent cell death involving mitochondrial pathway in myeloid leukemic cells. Cell Cycle 2 (2003) 488-493
22. Casanovas O., Hicklin D.J., Bergers G., and Hanahan D. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell 8 (2005) 299-309
23. Chang C.C., Heller J.D., Kuo J., and Huang R.C. Tetra-O-methyl nordihydroguaiaretic acid induces growth arrest and cellular apoptosis by inhibiting Cdc2 and survivin expression. Proc. Natl. Acad. Sci. USA 101 (2004) 13239-13244
24. Cheresh D.A., and Stupack D.G. Regulation of angiogenesis: apoptotic cues from the ECM. Oncogene 27 (2008) 6285-6298
25. Danial N.N., and Korsmeyer S.J. Cell death: critical control points. Cell 116 (2004) 205-219
26. Datta S.R., Dudek H., Tao X., Masters S., Fu H., Gotoh Y., and Greenberg M.E. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91 (1997) 231-241
27. Datta S.R., Katsov A., Hu L., Petros A., Fesik S.W., Yaffe M.B., and Greenberg M.E. 14-3-3 proteins and survival kinases cooperate to inactivate BAD by BH3 domain phosphorylation. Mol. Cell. 6 (2000) 41-51
28. Dhanabal M., Ramchandran R., Waterman M.J., Lu H., Knebelmann B., Segal M., and Sukhatme V.P. Endostatin induces endothelial cell apoptosis. J. Biol. Chem. 274 (1999) 11721-11726
29. Dilda P.J., and Hogg P.J. Arsenical-based cancer drugs. Cancer Treat. Rev. 33 (2007) 542-564
30. Dilda P.J., Decollogne S., Rossiter-Thornton M., and Hogg P.J. Para to ortho repositioning of the arsenical moiety of the angiogenesis inhibitor 4-(N-(S-glutathionylacetyl)amino)phenylarsenoxide results in a markedly increased cellular accumulation and antiproliferative activity. Cancer Res. 65 (2005) 11729-11734
31. Dilda P.J., Decollogne S., Weerakoon L., Norris M.D., Haber M., Allen J.D., and Hogg P.J. Optimization of the anti-tumor efficacy of a mitochondrial toxin by increasing the residence time in the cytosol. J. Med. Chem. 52 (2009) 6209-6216
32. Dilda P.J., Don A.S., Tanabe K.M., Higgins V.J., Allen J.D., Dawes I.W., and Hogg P.J. Mechanism of selectivity of an angiogenesis inhibitor from screening a genome-wide set of Saccharomyces cerevisiae deletion strains. J. Natl. Cancer Inst. 97 (2005) 1539-1547
33. Dilda P.J., Ramsay E.E., Corti A., Pompella A., and Hogg P.J. Metabolism of the tumor angiogenesis inhibitor 4-(N-(S-glutathionylacetyl)amino)phenylarsonous acid. J. Biol. Chem. 283 (2008) 35428-35434
34. Dohi T., Beltrami E., Wall N.R., Plescia J., and Altieri D.C. Mitochondrial survivin inhibits apoptosis and promotes tumorigenesis. J. Clin. Invest. 114 (2004) 1117-1127
35. Don A.S., and Hogg P.J. Mitochondria as cancer drug targets. Trends Mol. Med. 10 (2004) 372-378
36. Don A.S., Kisker O., Dilda P., Donoghue N., Zhao X., Decollogne S., Creighton B., Flynn E., Folkman J., and Hogg P.J. A peptide trivalent arsenical inhibits tumor angiogenesis by perturbing mitochondrial function in angiogenic endothelial cells. Cancer Cell 3 (2003) 497-509
37. Dong L.F., Swettenham E., Eliasson J., Wang X.F., Gold M., Medunic Y., Stantic M., Low P., Prochazka L., Witting P.K., et al. Vitamin E analogues inhibit angiogenesis by selective induction of apoptosis in proliferating endothelial cells: the role of oxidative stress. Cancer Res. 67 (2007) 11906-11913
38. Dong L.F., Low P., Dyason J.C., Wang X.F., Prochazka L., Witting P.K., Freeman R., Swettenham E., Valis K., Liu J., et al. Alpha-tocopheryl succinate induces apoptosis by targeting ubiquinone-binding sites in mitochondrial respiratory complex II. Oncogene 27 (2008) 4324-4335
39. Donoghue N., Yam P.T., Jiang X.M., and Hogg P.J. Presence of closely spaced protein thiols on the surface of mammalian cells. Protein Sci. 9 (2000) 2436-2445
40. Duffy A., Kortmansky J., Schwartz G.K., Capanu M., Puleio S., Minsky B., Saltz L., Kelsen D.P., and O'Reilly E.M. A phase I study of erlotinib in combination with gemcitabine and radiation in locally advanced, non-operable pancreatic adenocarcinoma. Ann. Oncol. 19 (2008) 86-91
41. Dvorak H.F. Vascular permeability factor/vascular endothelial growth factor: a critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J. Clin. Oncol. 20 (2002) 4368-4380
42. Ebos J.M., Lee C.R., Cruz-Munoz W., Bjarnason G.A., Christensen J.G., and Kerbel R.S. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 15 (2009) 232-239
43. Engels I.H., Stepczynska A., Stroh C., Lauber K., Berg C., Schwenzer R., Wajant H., Janicke R.U., Porter A.G., Belka C., et al. Caspase-8/FLICE functions as an executioner caspase in anticancer drug-induced apoptosis. Oncogene 19 (2000) 4563-4573
44. Engerman R.L., Pfaffenbach D., and Davis M.D. Cell turnover of capillaries. Lab. Invest. 17 (1967) 738-743
45. Escudier B., Eisen T., Stadler W.M., Szczylik C., Oudard S., Siebels M., Negrier S., Chevreau C., Solska E., Desai A.A., et al. Sorafenib in advanced clear-cell renal-cell carcinoma. New Engl. J. Med. 356 (2007) 125-134
46. Ferrara N. Vascular endothelial growth factor as a target for anticancer therapy. Oncologist 9 Suppl. 1 (2004) 2-10
47. Folkman J. Tumor angiogenesis: therapeutic implications. New Engl. J. Med. 285 (1971) 1182-1186
48. Folkman J. Angiogenesis. Annu. Rev. Med. 57 (2006) 1-18
49. Folkman J. Antiangiogenesis in cancer therapy-endostatin and its mechanisms of action. Exp. Cell Res. 312 (2006) 594-607
50. Folkman J. Angiogenesis: an organizing principle for drug discovery?. Nat. Rev. Drug Discov. 6 (2007) 273-286
51. Folkman J., and Kalluri R. Cancer without disease. Nature 427 (2004) 787
52. Garcia-Ruiz C., Colell A., Mari M., Morales A., and Fernandez-Checa J.C. Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species. Role of mitochondrial glutathione. J. Biol. Chem. 272 (1997) 11369-11377
53. Gerber H.P., Dixit V., and Ferrara N. Vascular endothelial growth factor induces expression of the antiapoptotic proteins Bcl-2 and A1 in vascular endothelial cells. J. Biol. Chem. 273 (1998) 13313-13316
54. Gingras D., Boivin D., Deckers C., Gendron S., Barthomeuf C., and Beliveau R. Neovastat-a novel antiangiogenic drug for cancer therapy. Anticancer Drugs 14 (2003) 91-96
55. Gragoudas E.S., Adamis A.P., Cunningham Jr. E.T., Feinsod M., and Guyer D.R. Pegaptanib for neovascular age-related macular degeneration. New Engl. J. Med. 351 (2004) 2805-2816
56. Halestrap A.P., and Brennerb C. The adenine nucleotide translocase: a central component of the mitochondrial permeability transition pore and key player in cell death. Curr. Med. Chem. 10 (2003) 1507-1525
57. Halestrap A.P., Connern C.P., Griffiths E.J., and Kerr P.M. Cyclosporin A binding to mitochondrial cyclophilin inhibits the permeability transition pore and protects hearts from ischaemia/reperfusion injury. Mol. Cell. Biochem. 174 (1997) 167-172
58. Halestrap A.P., Woodfield K.Y., and Connern C.P. Oxidative stress, thiol reagents, and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide translocase. J. Biol. Chem. 272 (1997) 3346-3354
59. Halestrap A.P., McStay G.P., and Clarke S.J. The permeability transition pore complex: another view. Biochimie 84 (2002) 153-166
60. Harfouche R., Hassessian H.M., Guo Y., Faivre V., Srikant C.B., Yancopoulos G.D., and Hussain S.N. Mechanisms which mediate the antiapoptotic effects of angiopoietin-1 on endothelial cells. Microvasc. Res. 64 (2002) 135-147
61. He X.W., Liu T., Xiao Y., Feng Y.L., Cheng D.J., Tingting G., Zhang L., Zhang Y., and Chen Y.X. Vascular endothelial growth factor-C siRNA delivered via calcium carbonate nanoparticle effectively inhibits lymphangiogenesis and growth of colorectal cancer in vivo. Cancer Biother. Radiopharm. 24 (2009) 249-259
62. Heinrich M., Neumeyer J., Jakob M., Hallas C., Tchikov V., Winoto-Morbach S., Wickel M., Schneider-Brachert W., Trauzold A., Hethke A., et al. Cathepsin D links TNF-induced acid sphingomyelinase to Bid-mediated caspase-9 and -3 activation. Cell Death Differ. 11 (2004) 550-563
63. Herbst R.S., and Sandler A. Bevacizumab and erlotinib: a promising new approach to the treatment of advanced NSCLC. Oncologist 13 (2008) 1166-1176
64. Hicklin D.J., and Ellis L.M. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J. Clin. Oncol. 23 (2005) 1011-1027
65. Hobson B., and Denekamp J. Endothelial proliferation in tumours and normal tissues: continuous labelling studies. Br. J. Cancer 49 (1984) 405-413
66. Holash J., Davis S., Papadopoulos N., Croll S.D., Ho L., Russell M., Boland P., Leidich R., Hylton D., Burova E., et al. VEGF-Trap: a VEGF blocker with potent antitumor effects. Proc. Natl. Acad. Sci. USA 99 (2002) 11393-11398
67. Hurwitz H., Fehrenbacher L., Novotny W., Cartwright T., Hainsworth J., Heim W., Berlin J., Baron A., Griffing S., Holmgren E., et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. New Engl. J. Med. 350 (2004) 2335-2342
68. Jain R.K., Duda D.G., Clark J.W., and Loeffler J.S. Lessons from phase III clinical trials on anti-VEGF therapy for cancer. Nat. Clin. Pract. Oncol. 3 (2006) 24-40
69. Kagan V.E., Tyurin V.A., Jiang J., Tyurina Y.Y., Ritov V.B., Amoscato A.A., Osipov A.N., Belikova N.A., Kapralov A.A., Kini V., et al. Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat. Chem. Biol. 1 (2005) 223-232
70. Kalluri R. Basement membranes: structure, assembly and role in tumour angiogenesis. Nat. Rev. Cancer 3 (2003) 422-433
71. Kerbel R.S. Tumor angiogenesis. New Engl. J. Med. 358 (2008) 2039-2049
72. Kinnally K.W., and Antonsson B. A tale of two mitochondrial channels, MAC and PTP, in apoptosis. Apoptosis 12 (2007) 857-868
73. Kroemer G., Galluzzi L., and Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 87 (2007) 99-163
74. Kuwana T., Mackey M.R., Perkins G., Ellisman M.H., Latterich M., Schneiter R., Green D.R., and Newmeyer D.D. Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111 (2002) 331-342
75. 2+ are critical targets. Mol. Cell. Biol. 28 (2008) 2304-2313
76. Lenartowicz E., Bernardi P., and Azzone G.F. Phenylarsine oxide induces the cyclosporin A-sensitive membrane permeability transition in rat liver mitochondria. J. Bioenerg. Biomembr. 23 (1991) 679-688
77. Lengauer C., Kinzler K.W., and Vogelstein B. Genetic instabilities in human cancers. Nature 396 (1998) 643-649
78. Levine A.M., Tulpule A., Quinn D.I., Gorospe III G., Smith D.L., Hornor L., Boswell W.D., Espina B.M., Groshen S.G., Masood R., et al. Phase I study of antisense oligonucleotide against vascular endothelial growth factor: decrease in plasma vascular endothelial growth factor with potential clinical efficacy. J. Clin. Oncol. 24 (2006) 1712-1719
79. Li C., Cheng X., Jiang H., and Sun X. Antiangiogenesis and damaging blood flow by antisense vascular endothelial growth factor oligodeoxynucleotides to suppress lung cancers. Tumour Biol. 27 (2006) 158-165
80. Lin Z.X., Yang L.J., Huang Q., Lin J.H., Ren J., Chen Z.B., Zhou L.Y., Zhang P.F., and Fu J. Inhibition of tumor-induced edema by antisense VEGF is mediated by suppressive vesiculo-vacuolar organelles (VVO) formation. Cancer Sci. 99 (2008) 2540-2546
81. Ling Y., Yang Y., Lu N., You Q.D., Wang S., Gao Y., Chen Y., and Guo Q.L. Endostar, a novel recombinant human endostatin, exerts antiangiogenic effect via blocking VEGF-induced tyrosine phosphorylation of KDR/Flk-1 of endothelial cells. Biochem. Biophys. Res. Commun. 361 (2007) 79-84
82. Llovet J.M., Ricci S., Mazzaferro V., Hilgard P., Gane E., Blanc J.F., de Oliveira A.C., Santoro A., Raoul J.L., Forner A., et al. Sorafenib in advanced hepatocellular carcinoma. New Engl. J. Med. 359 (2008) 378-390
83. Loges S., Mazzone M., Hohensinner P., and Carmeliet P. Silencing or fueling metastasis with VEGF inhibitors: antiangiogenesis revisited. Cancer Cell 15 (2009) 167-170
84. Maeshima Y., Sudhakar A., Lively J.C., Ueki K., Kharbanda S., Kahn C.R., Sonenberg N., Hynes R.O., and Kalluri R. Tumstatin, an endothelial cell-specific inhibitor of protein synthesis. Science 295 (2002) 140-143
85. Magnon C., Galaup A., Mullan B., Rouffiac V., Bouquet C., Bidart J.M., Griscelli F., Opolon P., and Perricaudet M. Canstatin acts on endothelial and tumor cells via mitochondrial damage initiated through interaction with alphavbeta3 and alphavbeta5 integrins. Cancer Res. 65 (2005) 4353-4361
86. Magnon C., Opolon P., Connault E., Mir L.M., Perricaudet M., and Martel-Renoir D. Canstatin gene electrotransfer combined with radiotherapy: preclinical trials for cancer treatment. Gene Ther. 15 (2008) 1436-1445
87. Manning B.D., and Cantley L.C. AKT/PKB signaling: navigating downstream. Cell 129 (2007) 1261-1274
88. Marchetti P., Decaudin D., Macho A., Zamzami N., Hirsch T., Susin S.A., and Kroemer G. Redox regulation of apoptosis: impact of thiol oxidation status on mitochondrial function. Eur. J. Immunol. 27 (1997) 289-296
89. Marusawa H., Matsuzawa S., Welsh K., Zou H., Armstrong R., Tamm I., and Reed J.C. HBXIP functions as a cofactor of survivin in apoptosis suppression. EMBO J. 22 (2003) 2729-2740
90. Marzo I., Brenner C., Zamzami N., Jurgensmeier J.M., Susin S.A., Vieira H.L., Prevost M.C., Xie Z., Matsuyama S., Reed J.C., et al. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281 (1998) 2027-2031
91. Maurer U., Charvet C., Wagman A.S., Dejardin E., and Green D.R. Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol. Cell. 21 (2006) 749-760
92. McStay G.P., Clarke S.J., and Halestrap A.P. Role of critical thiol groups on the matrix surface of the adenine nucleotide translocase in the mechanism of the mitochondrial permeability transition pore. Biochem. J. 367 (2002) 541-548
93. Meadows K.N., Bryant P., and Pumiglia K. Vascular endothelial growth factor induction of the angiogenic phenotype requires Ras activation. J. Biol. Chem. 276 (2001) 49289-49298
94. Merkwirth C., and Langer T. Prohibitin function within mitochondria: essential roles for cell proliferation and cristae morphogenesis. Biochim. Biophys. Acta 1793 (2009) 27-32
95. Miller K.D. E2100: a phase III trial of paclitaxel versus paclitaxel/bevacizumab for metastatic breast cancer. Clin. Breast Cancer 3 (2003) 421-422
96. Modjtahedi N., Giordanetto F., Madeo F., and Kroemer G. Apoptosis-inducing factor: vital and lethal. Trends Cell Biol. 16 (2006) 264-272
97. Morelli M.P., Cascone T., Troiani T., Tuccillo C., Bianco R., Normanno N., Romano M., Veneziani B.M., Fontanini G., Eckhardt S.G., et al. Anti-tumor activity of the combination of cetuximab, an anti-EGFR blocking monoclonal antibody and ZD6474, an inhibitor of VEGFR and EGFR tyrosine kinases. J. Cell. Physiol. 208 (2006) 344-353
98. Motzer R.J., Hutson T.E., Tomczak P., Michaelson M.D., Bukowski R.M., Rixe O., Oudard S., Negrier S., Szczylik C., Kim S.T., et al. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. New Engl. J. Med. 356 (2007) 115-124
99. Mukhopadhyay D., Tsiokas L., and Sukhatme V.P. Wild-type p53 and v-Src exert opposing influences on human vascular endothelial growth factor gene expression. Cancer Res. 55 (1995) 6161-6165
100. Nakahara T., Takeuchi M., Kinoyama I., Minematsu T., Shirasuna K., Matsuhisa A., Kita A., Tominaga F., Yamanaka K., Kudoh M., et al. YM155, a novel small-molecule survivin suppressant, induces regression of established human hormone-refractory prostate tumor xenografts. Cancer Res. 67 (2007) 8014-8021
101. Neuzil J., Schroder A., von Hundelshausen P., Zernecke A., Weber T., Gellert N., and Weber C. Inhibition of inflammatory endothelial responses by a pathway involving caspase activation and p65 cleavage. Biochemistry 40 (2001) 4686-4692
102. Neuzil J., Weber T., Schroder A., Lu M., Ostermann G., Gellert N., Mayne G.C., Olejnicka B., Negre-Salvayre A., Sticha M., et al. Induction of cancer cell apoptosis by alpha-tocopheryl succinate: molecular pathways and structural requirements. FASEB J. 15 (2001) 403-415
103. Neuzil J., Tomasetti M., Mellick A.S., Alleva R., Salvatore B.A., Birringer M., and Fariss M.W. Vitamin E analogues: a new class of inducers of apoptosis with selective anti-cancer effects. Curr Cancer Drug Targets 4 (2004) 355-372
104. Neuzil J., Tomasetti M., Zhao Y., Dong L.F., Birringer M., Wang X.F., Low P., Wu K., Salvatore B.A., and Ralph S.J. Vitamin E analogs, a novel group of "mitocans", as anticancer agents: the importance of being redox-silent. Mol. Pharmacol. 71 (2007) 1185-1199
105. Nissen L.J., Cao R., Hedlund E.M., Wang Z., Zhao X., Wetterskog D., Funa K., Brakenhielm E., and Cao Y. Angiogenic factors FGF2 and PDGF-BB synergistically promote murine tumor neovascularization and metastasis. J. Clin. Invest. 117 (2007) 2766-2777
106. Nury H., Dahout-Gonzalez C., Trezeguet V., Lauquin G., Brandolin G., and Pebay-Peyroula E. Structural basis for lipid-mediated interactions between mitochondrial ADP/ATP carrier monomers. FEBS Lett. 579 (2005) 6031-6036
107. O'Connor D.S., Schechner J.S., Adida C., Mesri M., Rothermel A.L., Li F., Nath A.K., Pober J.S., and Altieri D.C. Control of apoptosis during angiogenesis by survivin expression in endothelial cells. Am. J. Pathol. 156 (2000) 393-398
108. Oliveira P.J., and Wallace K.B. Depletion of adenine nucleotide translocator protein in heart mitochondria from doxorubicin-treated rats-relevance for mitochondrial dysfunction. Toxicology 220 (2006) 160-168
109. Ott M., Robertson J.D., Gogvadze V., Zhivotovsky B., and Orrenius S. Cytochrome c release from mitochondria proceeds by a two-step process. Proc. Natl. Acad. Sci. USA 99 (2002) 1259-1263
110. Paez-Ribes M., Allen E., Hudock J., Takeda T., Okuyama H., Vinals F., Inoue M., Bergers G., Hanahan D., and Casanovas O. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 15 (2009) 220-231
111. Panka D.J., and Mier J.W. Canstatin inhibits Akt activation and induces Fas-dependent apoptosis in endothelial cells. J. Biol. Chem. 278 (2003) 37632-37636
112. Papapetropoulos A., Fulton D., Mahboubi K., Kalb R.G., O'Connor D.S., Li F., Altieri D.C., and Sessa W.C. Angiopoietin-1 inhibits endothelial cell apoptosis via the Akt/survivin pathway. J. Biol. Chem. 275 (2000) 9102-9105
113. Pasquier E., Carre M., Pourroy B., Camoin L., Rebai O., Briand C., and Braguer D. Antiangiogenic activity of paclitaxel is associated with its cytostatic effect, mediated by the initiation but not completion of a mitochondrial apoptotic signaling pathway. Mol. Cancer Ther. 3 (2004) 1301-1310
114. Pastorino J.G., Tafani M., Rothman R.J., Marcinkeviciute A., Hoek J.B., and Farber J.L. Functional consequences of the sustained or transient activation by Bax of the mitochondrial permeability transition pore. J. Biol. Chem. 274 (1999) 31734-31739
115. Pebay-Peyroula E., Dahout-Gonzalez C., Kahn R., Trezeguet V., Lauquin G.J., and Brandolin G. Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426 (2003) 39-44
116. Petit A.M., Rak J., Hung M.C., Rockwell P., Goldstein N., Fendly B., and Kerbel R.S. Neutralizing antibodies against epidermal growth factor and ErbB-2/neu receptor tyrosine kinases down-regulate vascular endothelial growth factor production by tumor cells in vitro and in vivo: angiogenic implications for signal transduction therapy of solid tumors. Am. J. Pathol. 151 (1997) 1523-1530
117. Petronilli V., Costantini P., Scorrano L., Colonna R., Passamonti S., and Bernardi P. The voltage sensor of the mitochondrial permeability transition pore is tuned by the oxidation-reduction state of vicinal thiols. Increase of the gating potential by oxidants and its reversal by reducing agents. J. Biol. Chem. 269 (1994) 16638-16642
118. Presta M., Dell'Era P., Mitola S., Moroni E., Ronca R., and Rusnati M. Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev. 16 (2005) 159-178
119. Quillet-Mary A., Jaffrezou J.P., Mansat V., Bordier C., Naval J., and Laurent G. Implication of mitochondrial hydrogen peroxide generation in ceramide-induced apoptosis. J. Biol. Chem. 272 (1997) 21388-21395
120. Raffetto J.D., and Khalil R.A. Matrix metalloproteinases and their inhibitors in vascular remodeling and vascular disease. Biochem. Pharmacol. 75 (2008) 346-359
121. Rak J., Mitsuhashi Y., Bayko L., Filmus J., Shirasawa S., Sasazuki T., and Kerbel R.S. Mutant ras oncogenes upregulate VEGF/VPF expression: implications for induction and inhibition of tumor angiogenesis. Cancer Res. 55 (1995) 4575-4580
122. Reck M. Gefitinib in the treatment of advanced non-small-cell lung cancer. Expert Rev. Anticancer Ther. 9 (2009) 401-412
123. Rundhaug J.E. Matrix metalloproteinases and angiogenesis. J. Cell. Mol. Med. 9 (2005) 267-285
124. Safran M., and Kaelin Jr. W.G. HIF hydroxylation and the mammalian oxygen-sensing pathway. J. Clin. Invest. 111 (2003) 779-783
125. Scaffidi C., Fulda S., Srinivasan A., Friesen C., Li F., Tomaselli K.J., Debatin K.M., Krammer P.H., and Peter M.E. Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17 (1998) 1675-1687
126. Schleicher M., Shepherd B.R., Suarez Y., Fernandez-Hernando C., Yu J., Pan Y., Acevedo L.M., Shadel G.S., and Sessa W.C. Prohibitin-1 maintains the angiogenic capacity of endothelial cells by regulating mitochondrial function and senescence. J. Cell. Biol. 180 (2008) 101-112
127. Schurmann A., Mooney A.F., Sanders L.C., Sells M.A., Wang H.G., Reed J.C., and Bokoch G.M. P21-activated kinase 1 phosphorylates the death agonist bad and protects cells from apoptosis. Mol. Cell. Biol. 20 (2000) 453-461
128. Scorrano L., and Korsmeyer S.J. Mechanisms of cytochrome c release by proapoptotic BCL-2 family members. Biochem. Biophys. Res. Commun. 304 (2003) 437-444
129. Shiau C.W., Huang J.W., Wang D.S., Weng J.R., Yang C.C., Lin C.H., Li C., and Chen C.S. Alpha-Tocopheryl succinate induces apoptosis in prostate cancer cells in part through inhibition of Bcl-xL/Bcl-2 function. J. Biol. Chem. 281 (2006) 11819-11825
130. Shimizu S., Narita M., and Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399 (1999) 483-487
131. Sieber O.M., Heinimann K., and Tomlinson I.P. Genomic instability-the engine of tumorigenesis?. Nat. Rev. Cancer 3 (2003) 701-708
132. Singh R.P., Dhanalakshmi S., Tyagi A.K., Chan D.C., Agarwal C., and Agarwal R. Dietary feeding of silibinin inhibits advance human prostate carcinoma growth in athymic nude mice and increases plasma insulin-like growth factor-binding protein-3 levels. Cancer Res. 62 (2002) 3063-3069
133. Singh R.P., Dhanalakshmi S., Agarwal C., and Agarwal R. Silibinin strongly inhibits growth and survival of human endothelial cells via cell cycle arrest and downregulation of survivin, Akt and NF-kappaB: implications for angioprevention and antiangiogenic therapy. Oncogene 24 (2005) 1188-1202
134. Singh R.P., Gu M., and Agarwal R. Silibinin inhibits colorectal cancer growth by inhibiting tumor cell proliferation and angiogenesis. Cancer Res. 68 (2008) 2043-2050
135. Siskind L.J., Kolesnick R.N., and Colombini M. Ceramide channels increase the permeability of the mitochondrial outer membrane to small proteins. J. Biol. Chem. 277 (2002) 26796-26803
136. Song Z., Yao X., and Wu M. Direct interaction between survivin and Smac/DIABLO is essential for the anti-apoptotic activity of survivin during taxol-induced apoptosis. J. Biol. Chem. 278 (2003) 23130-23140
137. Sun C., Nettesheim D., Liu Z., and Olejniczak E.T. Solution structure of human survivin and its binding interface with Smac/Diablo. Biochemistry 44 (2005) 11-17
138. Taylor R.C., Cullen S.P., and Martin S.J. Apoptosis: controlled demolition at the cellular level. Nat Rev Mol. Cell. Biol. 9 (2008) 231-241
139. Tolcher A.W., Mita A., Lewis L.D., Garrett C.R., Till E., Daud A.I., Patnaik A., Papadopoulos K., Takimoto C., Bartels P., et al. Phase I and pharmacokinetic study of YM155, a small-molecule inhibitor of survivin. J. Clin. Oncol. 26 (2008) 5198-5203
140. Tran J., Rak J., Sheehan C., Saibil S.D., LaCasse E., Korneluk R.G., and Kerbel R.S. Marked induction of the IAP family antiapoptotic proteins survivin and XIAP by VEGF in vascular endothelial cells. Biochem. Biophys. Res. Commun. 264 (1999) 781-788
141. Tyagi A., Singh R.P., Ramasamy K., Raina K., Redente E.F., Dwyer-Nield L.D., Radcliffe R.A., Malkinson A.M., and Agarwal R. Growth inhibition and regression of lung tumors by silibinin: modulation of angiogenesis by macrophage-associated cytokines and nuclear factor-kappaB and signal transducers and activators of transcription 3. Cancer Prev. Res. (Phila Pa) 2 (2009) 74-83
142. Vahsen N., Cande C., Briere J.J., Benit P., Joza N., Larochette N., Mastroberardino P.G., Pequignot M.O., Casares N., Lazar V., et al. AIF deficiency compromises oxidative phosphorylation. EMBO J. 23 (2004) 4679-4689
143. Valle V.G., Fagian M.M., Parentoni L.S., Meinicke A.R., and Vercesi A.E. The participation of reactive oxygen species and protein thiols in the mechanism of mitochondrial inner membrane permeabilization by calcium plus prooxidants. Arch. Biochem. Biophys. 307 (1993) 1-7
144. Vaux D.L., and Silke J. Mammalian mitochondrial IAP binding proteins. Biochem. Biophys. Res. Commun. 304 (2003) 499-504
145. Vieira H.L., Belzacq A.S., Haouzi D., Bernassola F., Cohen I., Jacotot E., Ferri K.F., El Hamel C., Bartle L.M., Melino G., et al. The adenine nucleotide translocator: a target of nitric oxide, peroxynitrite, and 4-hydroxynonenal. Oncogene 20 (2001) 4305-4316
146. Viloria-Petit A.M., and Kerbel R.S. Acquired resistance to EGFR inhibitors: mechanisms and prevention strategies. Int. J. Radiat. Oncol. Biol. Phys. 58 (2004) 914-926
147. Vogel C., Hager C., and Bastians H. Mechanisms of mitotic cell death induced by chemotherapy-mediated G2 checkpoint abrogation. Cancer Res. 67 (2007) 339-345
148. Wang H.W., Sharp T.V., Koumi A., Koentges G., and Boshoff C. Characterization of an anti-apoptotic glycoprotein encoded by Kaposi's sarcoma-associated herpesvirus which resembles a spliced variant of human survivin. EMBO J. 21 (2002) 2602-2615
149. Wang J., Shi Y.Q., Yi J., Ye S., Wang L.M., Xu Y.P., He M., and Kong X.M. Suppression of growth of pancreatic cancer cell and expression of vascular endothelial growth factor by gene silencing with RNA interference. J. Dig. Dis. 9 (2008) 228-237
150. Weber T., Dalen H., Andera L., Negre-Salvayre A., Auge N., Sticha M., Lloret A., Terman A., Witting P.K., Higuchi M., et al. Mitochondria play a central role in apoptosis induced by alpha-tocopheryl succinate, an agent with antineoplastic activity: comparison with receptor-mediated pro-apoptotic signaling. Biochemistry 42 (2003) 4277-4291
151. Wu Y., Li Z.Y., Zhao X., Kan B., and Wei Y.Q. Inhibition of ovarian tumor growth by gene therapy with recombinant soluble vascular endothelial growth factor receptor 2. Hum. Gene Ther. 17 (2006) 941-948
152. Wudarczyk J., Debska G., and Lenartowicz E. Relation between the activities reducing disulfides and the protection against membrane permeability transition in rat liver mitochondria. Arch. Biochem. Biophys. 327 (1996) 215-221
153. Xiang R., Mizutani N., Luo Y., Chiodoni C., Zhou H., Mizutani M., Ba Y., Becker J.C., and Reisfeld R.A. A DNA vaccine targeting survivin combines apoptosis with suppression of angiogenesis in lung tumor eradication. Cancer Res. 65 (2005) 553-561
154. Yamamoto S., Tamai H., Ishisaka R., Kanno T., Arita K., Kobuchi H., and Utsumi K. Mechanism of alpha-tocopheryl succinate-induced apoptosis of promyelocytic leukemia cells. Free Radic. Res. 33 (2000) 407-418
155. Yasui H., Hideshima T., Richardson P.G., and Anderson K.C. Recent advances in the treatment of Multiple Myeloma. Curr. Pharm. Biotechnol. 7 (2006) 381-393
156. Yu J.L., Rak J.W., Coomber B.L., Hicklin D.J., and Kerbel R.S. Effect of p53 status on tumor response to antiangiogenic therapy. Science 295 (2002) 1526-1528
157. Yuan S., Fu Y., Wang X., Shi H., Huang Y., Song X., Li L., Song N., and Luo Y. Voltage-dependent anion channel 1 is involved in endostatin-induced endothelial cell apoptosis. FASEB J. 22 (2008) 2809-2820
158. Zhang X., and Lawler J. Thrombospondin-based antiangiogenic therapy. Microvasc. Res. 74 (2007) 90-99
159. Zhao Y., Neuzil J., and Wu K. Vitamin E analogues as mitochondria-targeting compounds: from the bench to the bedside?. Mol. Nutr. Food Res. 53 (2009) 129-139