Drug Resistance Updates
Volume 13, Issue 1 , Pages 16-28 , February 2010

Evading tumor evasion: Current concepts and perspectives of anti-angiogenic cancer therapy

  • Amir Abdollahi

      Affiliations

    • Center of Cancer Systems Biology, Dept. of Medicine, St. Elizabeth's Medical Center, Tufts University School of Medicine, Boston, MA 02135, USA
    • Vascular Biology Program, Department of Surgery, Children's Hospital Boston and Harvard Medical School, Boston, MA 02115, USA
    • Molecular RadioOncology, Heidelberg Ion Therapy Center (HIT), Department of Radiation Oncology, University of Heidelberg Medical School and National Center for Tumor diseases (NCT), German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany
    • Corresponding Author InformationCorresponding author at: St. Elizabeth's Medical Center, 736 Cambridge Street, Boston, MA 02135, USA or Heidelberg Ion Therapy Center (HIT), INF 450, 69120 Heidelberg, Germany. Tel.: +1 617 7796569/+49 6221 5639604.
    • ,
  • Judah Folkman

      Affiliations

    • Vascular Biology Program, Department of Surgery, Children's Hospital Boston and Harvard Medical School, Boston, MA 02115, USA
    • Deceased January 14, 2008.

Received 7 December 2009 ,Revised 20 December 2009 ,Accepted 22 December 2009.

References 

  1. Abdollahi A, Gong P, Rastert R, Debus J, Hlatky L, Hahnfeldt P, et al. Genome wide expression profiling of irradiated human lung endothelial cells reveals the activation of genes involved in coagulation, inflammation and angiogenic pathways. Proc. Am. Assoc. Cancer Res. 2003;44:6155;(Abstract)
  2. Abdollahi A, Lipson KE, Han X, Krempien R, Trinh T, Weber KJ, et al. SU5416 and SU6668 attenuate the angiogenic effects of radiation-induced tumor cell growth factor production and amplify the direct anti-endothelial action of radiation in vitro. Cancer Res. 2003;63:3755–3763
  3. Abdollahi A, Lipson KE, Sckell A, Zieher H, Klenke F, Poerschke D, et al. Combined therapy with direct and indirect angiogenesis inhibition results in enhanced antiangiogenic and antitumor effects. Cancer Res. 2003;63:8890–8898
  4. Abdollahi A, Hahnfeldt P, Maercker C, Grone HJ, Debus J, Ansorge W, et al. Endostatin's antiangiogenic signaling network. Mol. Cell. 2004;13:649–663
  5. Abdollahi A, Griggs DW, Zieher H, Roth A, Lipson KE, Saffrich R, et al. Inhibition of alpha(v)beta3 integrin survival signaling enhances antiangiogenic and antitumor effects of radiotherapy. Clin. Cancer Res. 2005;11:6270–6279
  6. Abdollahi A, Hlatky L, Huber PE. Endostatin: the logic of antiangiogenic therapy. Drug Resist. Updat. 2005;8:59–74
  7. Abdollahi A, Li M, Ping G, Plathow C, Domhan S, Kiessling F, et al. Inhibition of platelet-derived growth factor signaling attenuates pulmonary fibrosis. J. Exp. Med. 2005;201:925–935
  8. Abdollahi A, Schwager C, Kleeff J, Esposito I, Domhan S, Peschke P, et al. Transcriptional network governing the angiogenic switch in human pancreatic cancer. Proc. Natl. Acad. Sci. (USA). 2007;104:12890–12895
  9. Abedini MR, Qiu Q, Yan X, Tsang BK. Possible role of FLICE-like inhibitory protein (FLIP) in chemoresistant ovarian cancer cells in vitro. Oncogene. 2004;23:6997–7004
  10. Abiatari I, DeOliveira T, Kerkadze V, Schwager C, Esposito I, Giese NA, et al. Consensus transcriptome signature of perineural invasion in pancreatic carcinoma. Mol. Cancer Ther. 2009;8:1494–1504
  11. Al-Nedawi K, Meehan B, Kerbel RS, Allison AC, Rak J. Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc. Natl. Acad. Sci. (USA). 2009;106:3794–3799
  12. Almog N, Ma L, Raychowdhury R, Schwager C, Erber R, Short S, et al. Transcriptional switch of dormant tumors to fast-growing angiogenic phenotype. Cancer Res. 2009;69:836–844
  13. Amin DN, Bielenberg DR, Lifshits E, Heymach JV, Klagsbrun M. Targeting EGFR activity in blood vessels is sufficient to inhibit tumor growth and is accompanied by an increase in VEGFR-2 dependence in tumor endothelial cells. Microvasc. Res. 2008;76:15–22
  14. Amin DN, Hida K, Bielenberg DR, Klagsbrun M. Tumor endothelial cells express epidermal growth factor receptor (EGFR) but not ErbB3 and are responsive to EGF and to EGFR kinase inhibitors. Cancer Res. 2006;66:2173–2180
  15. Bedford JS, Dewey WC. Radiation Research Society. 1952–2002. Historical and current highlights in radiation biology: has anything important been learned by irradiating cells?. Radiat. Res. 2002;158:251–291
  16. Belka C, Jendrossek V, Pruschy M, Vink S, Verheij M, Budach W. Apoptosis-modulating agents in combination with radiotherapy—current status and outlook. Int. J. Radiat. Oncol. Biol. Phys. 2004;58:542–554
  17. Bergsmedh A, Szeles A, Henriksson M, Bratt A, Folkman MJ, Spetz AL, et al. Horizontal transfer of oncogenes by uptake of apoptotic bodies. Proc. Natl. Acad. Sci. (USA). 2001;98:6407–6411
  18. Bischof M, Abdollahi A, Gong P, Stoffregen C, Lipson KE, Debus JU, et al. Triple combination of irradiation, chemotherapy (pemetrexed), and VEGFR inhibition (SU5416) in human endothelial and tumor cells. Int. J. Radiat. Oncol. Biol. Phys. 2004;60:1220–1232
  19. Blagosklonny MV. Hypoxia-inducible factor: Achilles’ heel of antiangiogenic cancer therapy (review). Int. J. Oncol. 2001;19:257–262
  20. Blagosklonny MV. Antiangiogenic therapy and tumor progression. Cancer Cell. 2004;5:13–17
  21. Blanke CD. Dual-antibody therapy in advanced colorectal cancer: gather ye rosebuds while ye may. J. Clin. Oncol. 2009;27:655–658
  22. Bonner JA, Harari PM, Giralt J, Azarnia N, Shin DM, Cohen RB, et al. Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck. New Engl. J. Med. 2006;354:567–578
  23. Branford S, Rudzki Z, Walsh S, Grigg A, Arthur C, Taylor K, et al. High frequency of point mutations clustered within the adenosine triphosphate-binding region of BCR/ABL in patients with chronic myeloid leukemia or Ph-positive acute lymphoblastic leukemia who develop imatinib (STI571) resistance. Blood. 2002;99:3472–3475
  24. Braun S, Pantel K, Muller P, Janni W, Hepp F, Kentenich CR, et al. Cytokeratin-positive cells in the bone marrow and survival of patients with stage I, II, or III breast cancer. New Engl. J. Med. 2000;342:525–533
  25. Braun S, Vogl FD, Naume B, Janni W, Osborne MP, Coombes RC, et al. A pooled analysis of bone marrow micrometastasis in breast cancer. New Engl. J. Med. 2005;353:793–802
  26. Browder T, Butterfield CE, Kraling BM, Shi B, Marshall B, O’Reilly MS, et al. Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer. Cancer Res. 2000;60:1878–1886
  27. Browder T, Folkman J, Hahnfeldt P, Heymach J, Hlatky L, Kieran M, et al. Antiangiogenic therapy and p53. Science. 2002;297:471
  28. Broxterman HJ, Georgopapadakou NH. Anticancer therapeutics: a surge of new developments increasingly target tumor and stroma. Drug Resist. Updat. 2007;10:182–193
  29. Broxterman HJ, Gotink KJ, Verheul HM. Understanding the causes of multidrug resistance in cancer: a comparison of doxorubicin and sunitinib. Drug Resist. Updat. 2009;12:114–126
  30. Burstein HJ, Elias AD, Rugo HS, Cobleigh MA, Wolff AC, Eisenberg PD, et al. Phase II study of sunitinib malate, an oral multitargeted tyrosine kinase inhibitor, in patients with metastatic breast cancer previously treated with an anthracycline and a taxane. J. Clin. Oncol. 2008;26:1810–1816
  31. Camphausen K, Moses MA, Beecken WD, Khan MK, Folkman J, O’Reilly MS. Radiation therapy to a primary tumor accelerates metastatic growth in mice. Cancer Res. 2001;61:207–2211
  32. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature. 1996;380:435–439
  33. Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature. 2000;407:249–257
  34. Casanovas O, Hicklin DJ, Bergers G, Hanahan D. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell. 2005;8:299–309
  35. Celik I, Surucu O, Dietz C, Heymach JV, Force J, Hoschele I, et al. Therapeutic efficacy of endostatin exhibits a biphasic dose-response curve. Cancer Res. 2005;65:11044–11050
  36. Cervi D, Yip TT, Bhattacharya N, Podust VN, Peterson J, Abou-Slaybi A, et al. Platelet-associated PF-4 as a biomarker of early tumor growth. Blood. 2008;111:1201–1207
  37. Chait R, Craney A, Kishony R. Antibiotic interactions that select against resistance. Nature. 2007;446:668–671
  38. Cohen MH, Li SY, Keegan P, Pazdur R. FDA drug approval summary: bevacizumab (Avastin(R)) as treatment of recurrent glioblastoma multiforme. Oncologist. 2009;14:1131–1138
  39. Combs SE, Heeger S, Haselmann R, Edler L, Debus J, Schulz-Ertner D. Treatment of primary glioblastoma multiforme with cetuximab, radiotherapy and temozolomide (GERT)—phase I/II trial: study protocol. BMC Cancer. 2006;6:133
  40. Crawford Y, Kasman I, Yu L, Zhong C, Wu X, Modrusan Z, et al. PDGF-C mediates the angiogenic and tumorigenic properties of fibroblasts associated with tumors refractory to anti-VEGF treatment. Cancer Cell. 2009;15:21–34
  41. De Luca A, Carotenuto A, Rachiglio A, Gallo M, Maiello MR, Aldinucci D, et al. The role of the EGFR signaling in tumor microenvironment. J. Cell Physiol. 2008;214:559–567
  42. Di Sano F, Fazi B, Citro G, Lovat PE, Cesareni G, Piacentini M. Glucosylceramide synthase and its functional interaction with RTN-1C regulate chemotherapeutic-induced apoptosis in neuroepithelioma cells. Cancer Res. 2003;63:3860–3865
  43. Dorrell MI, Aguilar E, Scheppke L, Barnett FH, Friedlander M. Combination angiostatic therapy completely inhibits ocular and tumor angiogenesis. Proc. Natl. Acad. Sci. (USA). 2007;104:967–972
  44. Duda DG, Jain RK, Willett CG. Antiangiogenics: the potential role of integrating this novel treatment modality with chemoradiation for solid cancers. J. Clin. Oncol. 2007;25:4033–4042
  45. Dudley AC, Khan ZA, Shih SC, Kang SY, Zwaans BM, Bischoff J, et al. Calcification of multipotent prostate tumor endothelium. Cancer Cell. 2008;14:201–211
  46. Ebos JM, Lee CR, Christensen JG, Mutsaers AJ, Kerbel RS. Multiple circulating proangiogenic factors induced by sunitinib malate are tumor-independent and correlate with antitumor efficacy. Proc. Natl. Acad. Sci. (USA). 2007;104:17069–17074
  47. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell. 2009;15:232–239
  48. Edwards E, Geng L, Tan J, Onishko H, Donnelly E, Hallahan DE. Phosphatidylinositol 3-kinase/Akt signaling in the response of vascular endothelium to ionizing radiation. Cancer Res. 2002;62:4671–4677
  49. Ehnfors J, Kost-Alimova M, Persson NL, Bergsmedh A, Castro J, Levchenko-Tegnebratt T, et al. Horizontal transfer of tumor DNA to endothelial cells in vivo. Cell Death Differ. 2009;16:749–757
  50. Eikesdal HP, Kalluri R. Drug resistance associated with antiangiogenesis therapy. Semin. Cancer Biol. 2009;19:310–317
  51. Elledge SJ, Hannon GJ. An open letter to cancer researchers. Science. 2005;310:439–441
  52. Ellis LM, Hicklin DJ. VEGF-targeted therapy: mechanisms of anti-tumour activity. Nat. Rev. Cancer. 2008;8:579–591
  53. Ellis LM, Hicklin DJ. Resistance to targeted therapies: refining anticancer therapy in the era of molecular oncology. Clin. Cancer Res. 2009;15:7471–7478
  54. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, et al. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature. 1996;380:439–442
  55. Fertil B, Malaise EP. Intrinsic radiosensitivity of human cell lines is correlated with radioresponsiveness of human tumors: analysis of 101 published survival curves. Int. J. Radiat. Oncol. Biol. Phys. 1985;11:1699–1707
  56. Fokt RM, Templeton A, Gillessen S, Ohlschlegel C, Schmid HP. Prostatic metastasis of renal cell carcinoma successfully treated with sunitinib. Urol. Int. 2009;83:122–124
  57. Folkman J. Tumor angiogenesis: therapeutic implications. New Engl. J. Med. 1971;285:1182–1186
  58. Folkman J. Seminars in Medicine of the Beth Israel Hospital, Boston. Clinical applications of research on angiogenesis. New Engl. J. Med. 1995;333:1757–1763
  59. Folkman J. Angiogenesis: an organizing principle for drug discovery?. Nat. Rev. Drug Discov. 2007;6:273–286
  60. Folkman J, Camphausen K. Cancer. What does radiotherapy do to endothelial cells?. Science. 2001;293:227–228
  61. Folkman J, Hahnfeldt P, Hlatky L. Cancer: looking outside the genome. Nat. Rev. Mol. Cell Biol. 2000;1:76–79
  62. Francia G, Emmenegger U, Kerbel RS. Tumor-associated fibroblasts as “Trojan Horse” mediators of resistance to anti-VEGF therapy. Cancer Cell. 2009;15:3–5
  63. Gao D, Nolan DJ, Mellick AS, Bambino K, McDonnell K, Mittal V. Endothelial progenitor cells control the angiogenic switch in mouse lung metastasis. Science. 2008;319:195–198
  64. Garcia-Barros M, Paris F, Cordon-Cardo C, Lyden D, Rafii S, Haimovitz-Friedman A, et al. Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science. 2003;300:1155–1159
  65. Geng L, Donnelly E, McMahon G, Lin PC, Sierra-Rivera E, Oshinka H, et al. Inhibition of vascular endothelial growth factor receptor signaling leads to reversal of tumor resistance to radiotherapy. Cancer Res. 2001;61:2413–2419
  66. Gerdes HH, Carvalho RN. Intercellular transfer mediated by tunneling nanotubes. Curr. Opin. Cell Biol. 2008;20:470–475
  67. Gorre ME, Mohammed M, Ellwood K, Hsu N, Paquette R, Rao PN, et al. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science. 2001;293:876–880
  68. Gorski DH, Beckett MA, Jaskowiak NT, Calvin DP, Mauceri HJ, Salloum RM, et al. Blockage of the vascular endothelial growth factor stress response increases the antitumor effects of ionizing radiation. Cancer Res. 1999;59:3374–3378
  69. Gupta VK, Jaskowiak NT, Beckett MA, Mauceri HJ, Grunstein J, Johnson RS, et al. Vascular endothelial growth factor enhances endothelial cell survival and tumor radioresistance. Cancer J. 2002;8:47–54
  70. Hahnfeldt P, Folkman J, Hlatky L. Minimizing long-term tumor burden: the logic for metronomic chemotherapeutic dosing and its antiangiogenic basis. J. Theor. Biol. 2003;220:545–554
  71. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100:57–70
  72. Hecht JR, Mitchell E, Chidiac T, Scroggin C, Hagenstad C, Spigel D, et al. A randomized phase IIIB trial of chemotherapy, bevacizumab, and panitumumab compared with chemotherapy and bevacizumab alone for metastatic colorectal cancer. J. Clin. Oncol. 2009;27:672–680
  73. Hida K, Hida Y, Amin DN, Flint AF, Panigrahy D, Morton CC, et al. Tumor-associated endothelial cells with cytogenetic abnormalities. Cancer Res. 2004;64:8249–8255
  74. Hida K, Klagsbrun M. A new perspective on tumor endothelial cells: unexpected chromosome and centrosome abnormalities. Cancer Res. 2005;65:2507–2510
  75. Hirota K, Semenza GL. Regulation of angiogenesis by hypoxia-inducible factor 1. Crit. Rev. Oncol. Hematol. 2006;59:15–26
  76. Holmgren L, O’Reilly MS, Folkman J. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat. Med. 1995;1:149–153
  77. Huber PE, Bischof M, Jenne J, Heiland S, Peschke P, Saffrich R, et al. Trimodal cancer treatment: beneficial effects of combined antiangiogenesis, radiation, and chemotherapy. Cancer Res. 2005;65:3643–3655
  78. Hurwitz H, Fehrenbacher L, Novotny W, Cartwright T, Hainsworth J, Heim W, et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. New Engl. J. Med. 2004;350:2335–2342
  79. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell. 2002;110:673–687
  80. Inoue M, Hager JH, Ferrara N, Gerber HP, Hanahan D. VEGF-A has a critical, nonredundant role in angiogenic switching and pancreatic beta cell carcinogenesis. Cancer Cell. 2002;1:193–202
  81. Iwamoto FM, Abrey LE, Beal K, Gutin PH, Rosenblum MK, Reuter VE, et al. Patterns of relapse and prognosis after bevacizumab failure in recurrent glioblastoma. Neurology. 2009;73:1200–1206
  82. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science. 2005;307:58–62
  83. Jain RK. Lessons from multidisciplinary translational trials on anti-angiogenic therapy of cancer. Nat. Rev. Cancer. 2008;8:309–316
  84. Jensen AD, Munter MW, Bischoff H, Haselmann R, Timke C, Krempien R, et al. Treatment of non-small cell lung cancer with intensity-modulated radiation therapy in combination with cetuximab: the NEAR protocol (NCT00115518). BMC Cancer. 2006;6:122
  85. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science. 2008;321:1801–1806
  86. Kaiser J. Genomics. Billion-dollar cancer mapping project steps forward. Science. 2008;321:26–27
  87. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat. Rev. Cancer. 2006;6:392–401
  88. Kerbel R, Folkman J. Clinical translation of angiogenesis inhibitors. Nat. Rev. Cancer. 2002;2:727–739
  89. Kerbel RS. Inhibition of tumor angiogenesis as a strategy to circumvent acquired resistance to anti-cancer therapeutic agents. Bioessays. 1991;13:31–36
  90. Kerbel RS, Kamen BA. The anti-angiogenic basis of metronomic chemotherapy. Nat. Rev. Cancer. 2004;4:423–436
  91. Kienast Y, von Baumgarten L, Fuhrmann M, Klinkert WE, Goldbrunner R, Herms J, et al. Real-time imaging reveals the single steps of brain metastasis formation. Nat. Med. 2009 Dec 20;[doi:10.1038/nm.2072]
  92. Kieran MW, Folkman J, Heymach J. Angiogenesis inhibitors and hypoxia. Nat. Med. 2003;9:1104–1105
  93. Kim TJ, Landen CN, Lin YG, Mangala LS, Lu C, Nick AM, et al. Combined anti-angiogenic therapy against VEGF and integrin alpha (ν)beta(3) in an orthotopic model of ovarian cancer. Cancer Biol. Ther. 2009;Epub ahead of print
  94. Kim Y, Suh N, Sporn M, Reed JC. An inducible pathway for degradation of FLIP protein sensitizes tumor cells to TRAIL-induced apoptosis. J. Biol. Chem. 2002;277:22320–22329
  95. Klein CA. Parallel progression of primary tumours and metastases. Nat. Rev. Cancer. 2009;9:302–312
  96. Klement G, Baruchel S, Rak J, Man S, Clark K, Hicklin DJ, et al. Continuous low-dose therapy with vinblastine and VEGF receptor-2 antibody induces sustained tumor regression without overt toxicity. J. Clin. Invest. 2000;105:R15–R24
  97. Koutras AK, Krikelis D, Alexandrou N, Starakis I, Kalofonos HP. Brain metastasis in renal cell cancer responding to sunitinib. Anticancer Res. 2007;27:4255–4257
  98. Krempien R, Muenter MW, Huber PE, Nill S, Friess H, Timke C, et al. Randomized phase II—study evaluating EGFR targeting therapy with cetuximab in combination with radiotherapy and chemotherapy for patients with locally advanced pancreatic cancer–PARC: study protocol [ISRCTN56652283]. BMC Cancer. 2005;5:131
  99. Kunkel P, Ulbricht U, Bohlen P, Brockmann MA, Fillbrandt R, Stavrou D, et al. Inhibition of glioma angiogenesis and growth in vivo by systemic treatment with a monoclonal antibody against vascular endothelial growth factor receptor-2. Cancer Res. 2001;61:6624–6628
  100. Lamszus K, Brockmann MA, Eckerich C, Bohlen P, May C, Mangold U, et al. Inhibition of glioblastoma angiogenesis and invasion by combined treatments directed against vascular endothelial growth factor receptor-2, epidermal growth factor receptor, and vascular endothelial-cadherin. Clin. Cancer Res. 2005;11:4934–4940
  101. Lee SL, Rouhi P, Dahl JL, Zhang D, Ji H, Hauptmann G, et al. Hypoxia-induced pathological angiogenesis mediates tumor cell dissemination, invasion, and metastasis in a zebrafish tumor model. Proc. Natl. Acad. Sci. (USA). 2009;106:19485–19490
  102. Lee TY, Muschal S, Pravda EA, Folkman J, Abdollahi A, Javaherian K. Angiostatin regulates the expression of antiangiogenic and pro-apoptotic pathways via targeted inhibition of mitochondrial proteins. Blood. 2009;114:1987–1998
  103. Longley DB, Wilson TR, McEwan M, Allen WL, McDermott U, Galligan L, et al. c-FLIP inhibits chemotherapy-induced colorectal cancer cell death. Oncogene. 2006;25:838–848
  104. Mauceri HJ, Hanna NN, Beckett MA, Gorski DH, Staba MJ, Stellato KA, et al. Combined effects of angiostatin and ionizing radiation in antitumour therapy. Nature. 1998;394:287–291
  105. Medioni J, Choueiri TK, Zinzindohoue F, Cho D, Fournier L, Oudard S. Response of renal cell carcinoma pancreatic metastasis to sunitinib treatment: a retrospective analysis. J. Urol. 2009;181:2470–2475
  106. Michel JB, Yeh PJ, Chait R, Moellering RC, Kishony R. Drug interactions modulate the potential for evolution of resistance. Proc. Natl. Acad. Sci. (USA). 2008;105:14918–14923
  107. Motzer RJ, Hutson TE, Tomczak P, Michaelson MD, Bukowski RM, Oudard S, et al. Overall survival and updated results for sunitinib compared with interferon alfa in patients with metastatic renal cell carcinoma. J. Clin. Oncol. 2009;27:3584–3590
  108. Motzer RJ, Hutson TE, Tomczak P, Michaelson MD, Bukowski RM, Rixe O, et al. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. New Engl. J. Med. 2007;356:115–124
  109. Murray LJ, Abrams TJ, Long KR, Ngai TJ, Olson LM, Hong W, et al. SU11248 inhibits tumor growth and CSF-1R-dependent osteolysis in an experimental breast cancer bone metastasis model. Clin. Exp. Metastasis. 2003;20:757–766
  110. Muschal S, Lee TY, Korn B, Folkman J, Huber PE, Javaherian K, et al. Identification of novel angiostatin binding partners using a protein array (27K) based high-throughput protein–protein interaction screen. Proc. Am. Assoc. Cancer Res. 2008;378:(Abstract)
  111. Nakagawa T, Tohyama O, Yamaguchi A, et al. E7050: a dual c-Met and VEGFR2 tyrosine kinase inhibitor promotes tumor regression and prolongs survival in Mouse xenograft models. Cancer Sci. 2009 September;Epub ahead of print
  112. Ng QS, Goh V, Milner J, Padhani AR, Saunders MI, Hoskin PJ. Acute tumor vascular effects following fractionated radiotherapy in human lung cancer: In vivo whole tumor assessment using volumetric perfusion computed tomography. Int. J. Radiat. Oncol. Biol. Phys. 2007;67:417–424
  113. Nyberg P, Xie L, Kalluri R. Endogenous inhibitors of angiogenesis. Cancer Res. 2005;65:3967–3979
  114. O’Reilly MS, Holmgren L, Shing Y, Chen C, Rosenthal RA, Moses M, et al. Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell. 1994;79:315–328
  115. Paez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Vinals F, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell. 2009;15:220–231
  116. Paris F, Fuks Z, Kang A, Capodieci P, Juan G, Ehleiter D, et al. Endothelial apoptosis as the primary lesion initiating intestinal radiation damage in mice. Science. 2001;293:293–297
  117. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, et al. An integrated genomic analysis of human glioblastoma multiforme. Science. 2008;321:1807–1812
  118. Pennacchietti S, Michieli P, Galluzzo M, Mazzone M, Giordano S, Comoglio PM. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell. 2003;3:347–361
  119. Pezzolo A, Parodi F, Corrias MV, Cinti R, Gambini C, Pistoia V. Tumor origin of endothelial cells in human neuroblastoma. J. Clin. Oncol. 2007;25:376–383
  120. Rak J, Yu JL. Oncogenes and tumor angiogenesis: the question of vascular “supply” and vascular “demand”. Semin. Cancer Biol. 2004;14:93–104
  121. Rapisarda A, Melillo G. Role of the hypoxic tumor microenvironment in the resistance to anti-angiogenic therapies. Drug Resist. Updat. 2009;12:74–80
  122. Relf M, LeJeune S, Scott PA, Fox S, Smith K, Leek R, et al. Expression of the angiogenic factors vascular endothelial cell growth factor, acidic and basic fibroblast growth factor, tumor growth factor beta-1, platelet-derived endothelial cell growth factor, placenta growth factor, and pleiotrophin in human primary breast cancer and its relation to angiogenesis. Cancer Res. 1997;57:963–969
  123. Reynolds LE, Wyder L, Lively JC, Taverna D, Robinson SD, Huang X, et al. Enhanced pathological angiogenesis in mice lacking beta3 integrin or beta3 and beta5 integrins. Nat. Med. 2002;8:27–34
  124. Ruoslahti E. Specialization of tumour vasculature. Nat. Rev. Cancer. 2002;2:83–90
  125. Rustom A, Saffrich R, Markovic I, Walther P, Gerdes HH. Nanotubular highways for intercellular organelle transport. Science. 2004;303:1007–1010
  126. Schueneman AJ, Himmelfarb E, Geng L, Tan J, Donnelly E, Mendel D, et al. SU11248 maintenance therapy prevents tumor regrowth after fractionated irradiation of murine tumor models. Cancer Res. 2003;63:4009–4016
  127. Semenza GL. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer. 2003;3:721–732
  128. Shah NP, Nicoll JM, Nagar B, Gorre ME, Paquette RL, Kuriyan J, et al. Multiple BCR-ABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (STI571) in chronic phase and blast crisis chronic myeloid leukemia. Cancer Cell. 2002;2:117–125
  129. Shinohara ET, Cao C, Niermann K, Mu Y, Zeng F, Hallahan DE, et al. Enhanced radiation damage of tumor vasculature by mTOR inhibitors. Oncogene. 2005;24:5414–5422
  130. Shojaei F, Ferrara N. Role of the microenvironment in tumor growth and in refractoriness/resistance to anti-angiogenic therapies. Drug Resist. Updat. 2008;11:219–230
  131. Shojaei F, Wu X, Malik AK, Zhong C, Baldwin ME, Schanz S, et al. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+myeloid cells. Nat. Biotechnol. 2007;25:911–920
  132. Shojaei F, Wu X, Qu X, Kowanetz M, Yu L, Tan M, et al. G-CSF-initiated myeloid cell mobilization and angiogenesis mediate tumor refractoriness to anti-VEGF therapy in mouse models. Proc. Natl. Acad. Sci. (USA). 2009;106:6742–6747
  133. Shojaei F, Wu X, Zhong C, Yu L, Liang XH, Yao J, et al. Bv8 regulates myeloid-cell-dependent tumour angiogenesis. Nature. 2007;450:825–831
  134. Sjoblom T, Jones S, Wood LD, Parsons DW, Lin J, Barber TD, et al. The consensus coding sequences of human breast and colorectal cancers. Science. 2006;314:268–274
  135. Sonpavde G, Periman PO, Bernold D, Weckstein D, Fleming MT, Galsky MD, et al. Sunitinib malate for metastatic castration-resistant prostate cancer following docetaxel-based chemotherapy. Ann. Oncol. 2009;
  136. Steeg PS. Angiogenesis inhibitors: motivators of metastasis?. Nat. Med. 2003;9:822–823
  137. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. New Engl. J. Med. 2005;352:987–996
  138. Szmit S, Zagrodzka M, Kurzyna M, Opolski G, Szczylik C. Sunitinib malate, a receptor tyrosine kinase inhibitor, is effective in the treatment of restrictive heart failure due to heart metastases from renal cell carcinoma. Cardiology. 2009;114:67–71
  139. Tan J, Hallahan DE. Growth factor-independent activation of protein kinase B contributes to the inherent resistance of vascular endothelium to radiation-induced apoptotic response. Cancer Res. 2003;63:7663–7667
  140. TCGA . Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature. 2008;455:1061–1068
  141. Teicher BA, Holden SA, Dupuis NP, Kakeji Y, Ikebe M, Emi Y, et al. Potentiation of cytotoxic therapies by TNP-470 and minocycline in mice bearing EMT-6 mammary carcinoma. Breast Cancer Res. Treat. 1995;36:227–236
  142. Timke C, Zieher H, Roth A, Hauser K, Lipson KE, Weber KJ, et al. Combination of vascular endothelial growth factor receptor/platelet-derived growth factor receptor inhibition markedly improves radiation tumor therapy. Clin. Cancer Res. 2008;14:2210–2219
  143. Tjin Tham Sjin RM, Naspinski J, Birsner AE, Li C, Chan R, Lo KM, et al. Endostatin therapy reveals a U-shaped curve for antitumor activity. Cancer Gene Ther. 2006;13:619–627
  144. Turzanski J, Grundy M, Shang S, Russell N, Pallis M. P-glycoprotein is implicated in the inhibition of ceramide-induced apoptosis in TF-1 acute myeloid leukemia cells by modulation of the glucosylceramide synthase pathway. Exp. Hematol. 2005;33:62–72
  145. Vroling L, van der Veldt AA, de Haas RR, Haanen JB, Schuurhuis GJ, Kuik DJ, et al Increased numbers of small circulating endothelial cells in renal cell cancer patients treated with sunitinib. Angiogenesis. 2009;12:69–79
  146. Waldren CA. Classical radiation biology dogma, bystander effects and paradigm shifts. Hum. Exp. Toxicol. 2004;23:95–100
  147. Wild-Bode C, Weller M, Rimner A, Dichgans J, Wick W. Sublethal irradiation promotes migration and invasiveness of glioma cells: implications for radiotherapy of human glioblastoma. Cancer Res. 2001;61:2744–2750
  148. Willett CG, Duda DG, di Tomaso E, Boucher Y, Czito BG, Vujaskovic Z, et al. Complete pathological response to bevacizumab and chemoradiation in advanced rectal cancer. Nat. Clin. Pract. Oncol. 2007;4:316–321
  149. Willett CG, Duda DG, di TE, Boucher Y, Ancukiewicz M, Sahani DV, et al. Efficacy, safety, and biomarkers of neoadjuvant bevacizumab, radiation therapy, and fluorouracil in rectal cancer: a multidisciplinary phase II study. J. Clin. Oncol. 2009;27:3020–3026
  150. Yeh P, Tschumi AI, Kishony R. Functional classification of drugs by properties of their pairwise interactions. Nat. Genet. 2006;38:489–494
  151. Yu JL, Rak JW, Coomber BL, Hicklin DJ, Kerbel RS. Effect of p53 status on tumor response to antiangiogenic therapy. Science. 2002;295:1526–1528
  152. Zwolak P, Jasinski P, Terai K, Gallus NJ, Ericson ME, Clohisy DR, et al. Addition of receptor tyrosine kinase inhibitor to radiation increases tumour control in an orthotopic murine model of breast cancer metastasis in bone. Eur. J. Cancer. 2008;44:2506–2517

PII: S1368-7646(09)00077-6

doi: 10.1016/j.drup.2009.12.001

Drug Resistance Updates
Volume 13, Issue 1 , Pages 16-28 , February 2010

Article Tools

* Image Usage & Resolution