Dose-dependent response of tumor vasculature to radiation therapy in combination with Sunitinib depicted by three-dimensional high-frequency power Doppler ultrasound

Angiogenesis

Volumn 16, Issue 2, 2013, Pages 443-454

  El Kaffas, Ahmed ^a,b   Giles, Anoja ^a   Czarnota, Gregory J ^a,b  

^a SUNNYBROOK RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

bFGF; SU11248; Three dimensional high frequency power Doppler ultrasound; Vascular normalization

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; SUNITINIB;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER ADJUVANT THERAPY; CANCER CHEMOTHERAPY; CANCER GROWTH; CELL DEATH; CHEMORADIOTHERAPY; CONTROLLED STUDY; DOPPLER ECHOGRAPHY; DRUG EFFECT; DRUG RESPONSE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RADIATION DOSE; RADIATION RESPONSE; THREE DIMENSIONAL ECHOCARDIOGRAPHY; TREATMENT DURATION; TUMOR VASCULARIZATION;

ANGIOGENESIS INHIBITORS; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; IMMUNOHISTOCHEMISTRY; INDOLES; MICE; NEOPLASMS, EXPERIMENTAL; PYRROLES; ULTRASONOGRAPHY, DOPPLER;

EID: 84879498361     PISSN: 09696970     EISSN: 15737209     Source Type: Journal    
DOI: 10.1007/s10456-012-9329-2     Document Type: Article

References (57)

1. Fuks Z, Kolesnick R (2005) Engaging the vascular component of the tumor response. Cancer Cell 8:89-91 (Pubitemid 41132735)
2. García-Barros M, Thin TH, Maj J, Cordon-Cardo C, Haimovitz-Friedman A, Fuks Z et al (2010) Impact of stromal sensitivity on radiation response of tumors implanted in SCID hosts revisited. Cancer Res 70:8179-8186
3. Garcia-Barros M, Paris F, Cordon-Cardo C, Lyden D, Rafii S, Haimovitz-Friedman A et al (2003) Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science 300:1155-1159 (Pubitemid 36583102)
4. Paris F, Fuks Z, Kang A, Capodieci P, Juan G, Ehleiter D et al (2001) Endothelial apoptosis as the primary lesion initiating intestinal radiation damage in mice. Science 293:293 (Pubitemid 32694744)
5. Moeller BJ, Dreher MR, Rabbani ZN, Schroeder T, Cao Y, Li CY et al (2005) Pleiotropic effects of HIF-1 blockade on tumor radiosensitivity. Cancer Cell 8:99-110 (Pubitemid 41132739)
6. Moeller BJ, Cao Y, Li CY, Dewhirst MW (2004) Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell 5:429-441 (Pubitemid 38610245)
7. Moeller BJ, Dewhirst MW (2006) HIF-1 and tumour radiosensitivity. Br J Cancer 95:1-5 (Pubitemid 43980546)
8. Lehnert S (2007) Biomolecular action of ionizing radiation. Taylor & Francis, New York
9. Prise KM, Schettino G, Folkard M, Held KD (2005) New insights on cell death from radiation exposure. Lancet Oncol 6:520-528 (Pubitemid 40903633)
10. Truman J, Hambardzumyan D, Garcia-Barros M, Chan R, Fuks Z, Haimovitz-Friedman A (2006) Basic fibroblast growth factor inhibits radiation-induced apoptosis of endothelial cells by inhibiting acid sphingomyelinase activity. Radiother Oncol 78:S74
11. Vit J-P, Rosselli F (2003) Role of the ceramide-signaling pathways in ionizing radiation-induced apoptosis. Oncogene 22:8645-8652 (Pubitemid 38010487)
12. Kolesnick R, Fuks Z (2003) Radiation and ceramide-induced apoptosis. Oncogene 22:5897-5906 (Pubitemid 37176710)
13. Gupta N, Nodzenski E, Khodarev NN, Yu J, Khorasani L, Beckett MA et al (2001) Angiostatin effects on endothelial cells mediated by ceramide and RhoA. EMBO Rep 2:536-540 (Pubitemid 32611352)
14. Haimovitz-Friedman A, Kan CC, Ehleiter D, Persaud RS, McLoughlin M, Fuks Z et al (1994) Ionizing radiation acts on cellular membranes to generate ceramide and initiate apoptosis. J Exp Med 180:525 (Pubitemid 24224129)
15. Peña LA, Fuks Z, Kolesnick RN (2000) Radiation-induced apoptosis of endothelial cells in the murine central nervous system: protection by fibroblast growth factor and sphingomyelinase deficiency. Cancer Res 60:321-327 (Pubitemid 30070758)
16. Fuks Z, Persaud RS, Alfieri A, Mcloughlin M, Ehleiter D, Schwartz JL et al (1994) Basic fibroblast growth factor protects endothelial cells against radiation induced programmed cell death in vitro and in vivo. Cancer Res 54:2582-2590 (Pubitemid 24173742)
17. Fuks Z, Vlodavsky I, Andreeff M, McLoughlin M, Haimovitz-Friedman A (1992) Effects of extracellular matrix on the response of endothelial cells to radiation in vitro. Eur J Cancer 28:725-731
18. Gu Q, Wang D, Wang X, Peng R, Liu J, Jiang T et al (2004) Basic fibroblast growth factor inhibits radiation-induced apoptosis of HUVECs. I. The PI3K/AKT pathway and induction of phosphorylation of BAD. Radiat Res 161:692-702 (Pubitemid 39149578)
19. Truman J-P, García-Barros M, Kaag M, Hambardzumyan D, Stancevic B, Chan M et al (2010) Endothelial membrane remodeling is obligate for anti-angiogenic radiosensitization during tumor radiosurgery. PLoS ONE 5:e12310
20. Barcellos-Hoff MH, Park C, Wright EG (2005) Radiation and the microenvironment - tumorigenesis and therapy. Nat Rev Cancer 5:867-875 (Pubitemid 41746031)
21. Park HJ, Griffin RJ, Hui S, Levitt H, Song CW (2012) Radiation-induced vascular damage in tumors: implications of vascular damage in ablative hypofractionated radiotherapy (SBRT and SRS). Vascular 327:311-327
22. Cuneo KC, Geng L, Fu A, Orton D, Hallahan DE, Chakravarthy AB (2008) SU11248 (sunitinib) sensitizes pancreatic cancer to the cytotoxic effects of ionizing radiation. Int J Radiat Oncol Biol Phys 71:873-879 (Pubitemid 351749533)
23. Schueneman AJ, Himmelfarb E, Geng L, Tan J, Donnelly E, Mendel D et al (2003) SU11248 maintenance therapy prevents tumor regrowth after fractionated irradiation of murine tumor models. Cancer Res 63:4009-4016 (Pubitemid 36917920)
24. Mendel DB, Laird AD, Xin X, Louie SG, Christensen JG, Li G et al (2003) In vivo antitumor activity of SU11248, a novel tyrosine kinase inhibitor targeting vascular endothelial growth factor and platelet-derived growth factor receptors: determination of a pharmacokinetic/pharmacodynamic relationship. Clin Cancer Res 9:327-337 (Pubitemid 36109749)
25. Osusky KL, Hallahan DE, Fu A, Ye F, Shyr Y, Geng L (2004) The receptor tyrosine kinase inhibitor SU11248 impedes endothelial cell migration, tubule formation, and blood vessel formation in vivo, but has little effect on existing tumor vessels. Angiogenesis 7:225-233
26. Faivre S, Demetri G, Sargent W, Raymond E (2007) Molecular basis for sunitinib efficacy and future clinical development. Nat Rev Drug Discov 6:734-745 (Pubitemid 47338181)
27. Senan S, Smit EF (2007) Design of clinical trials of radiation combined with antiangiogenic therapy. Oncologist 12:465-477 (Pubitemid 46698724)
28. Zwolak P, Jasinski P, Terai K, Gallus NJ, Ericson ME, Clohisy DR et al (2008) 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 44:2506-2517
29. Yoon SS, Stangenberg L, Lee Y-J, Rothrock C, Dreyfuss JM, Baek K-H et al (2009) Efficacy of sunitinib and radiotherapy in genetically engineered mouse model of soft-tissue sarcoma. Int J Radiat Oncol Biol Phys 74:1207-1216
30. O'Reilly MS (2006) Radiation combined with antiangiogenic and antivascular agents. Semin Radiat Oncol 16:45-50 (Pubitemid 41832315)
31. Heath VL, Bicknell R (2009) Anticancer strategies involving the vasculature. Nat Rev Clin Oncol 6:395-404
32. Gordon MS, Mendelson DS, Kato G (2010) Tumor angiogenesis and novel antiangiogenic strategies. Int J Cancer 126:1777-1787
33. Li J, Huang S, Armstrong EA, Fowler JF, Harari PM (2005) Angiogenesis and radiation response modulation after vascular endothelial growth factor receptor-2 (VEGFR2) blockade. Int J Radiat Oncol Biol Phys 62:1477-1485 (Pubitemid 40982073)
34. Timke C, Zieher H, Roth A, Hauser K, Lipson KE, Weber KJ et al (2008) Combination of vascular endothelial growth factor receptor/platelet-derived growth factor receptor inhibition markedly improves radiation tumor therapy. Clin Cancer Res 14:2210-2219 (Pubitemid 351551134)
35. Foster FS, Burns PN, Simpson DH, Wilson SR, Christopher DA, Goertz DE (2000) Ultrasound for the visualization and quantification of tumor microcirculation. Cancer Metastasis Rev 19:131-138 (Pubitemid 32004702)
36. Foster F (2000) Advances in ultrasound biomicroscopy. Ultrasound Med Biol 26:1-27 (Pubitemid 30045518)
37. Goertz DE, Yu JL, Kerbel RS, Burns PN, Foster FS (2002) High-frequency Doppler ultrasound monitors the effects of antivascular therapy on tumor blood flow. Cancer Res 62:6371-6375 (Pubitemid 35364088)
38. Pinter SZ, Lacefield JC (2009) Understanding quantification of microvascularity with high-frequency power Doppler ultrasound. Proc SPIE 7265:72650U-72650U-9
39. Donnelly EF, Geng L, Wojcicki WE, Fleischer AC, Hallahan DE (2001) Quantified power Doppler US of tumor blood flow correlates with microscopic quantification of tumor blood vessels. Radiology 219:166-170 (Pubitemid 32234069)
40. Chen J-J, Chen J-JJ, Chiang C-S, Hong J-H, Yeh C-K (2011) Assessment of tumor vasculature for diagnostic and therapeutic applications in a mouse model in vivo using 25-MHz power Doppler imaging. Ultrasonics 51:925-931
41. Palmowski M, Huppert J, Hauff P, Reinhardt M, Schreiner K, Socher MA et al (2008) Vessel fractions in tumor xenografts depicted by flow- or contrast-sensitive three-dimensional high-frequency Doppler ultrasound respond differently to antiangiogenic treatment. Cancer Res 68:7042-7049
42. Xuan JW, Bygrave M, Jiang H, Valiyeva F, Dunmore-Buyze J, Holdsworth DW et al (2007) Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound. Cancer Res 67:2830-2839 (Pubitemid 46548973)
43. Ohishi H, Hirai T, Yamada R, Hirohashi S, Uchida H, Hashimoto H et al (1998) Three-dimensional power Doppler sonography of tumor vascularity. Ultrasound Med 17:619-622 (Pubitemid 28447354)
44. Su J-M, Huang Y-F, Chen HHW, Cheng Y-M, Chou C-Y (2006) Three-dimensional power Doppler ultrasound is useful to monitor the response to treatment in a patient with primary papillary serous carcinoma of the peritoneum. Ultrasound Med Biol 32:623-626
45. Galván R, Mercé L, Jurado M, Mínguez JA, López-García G, Alcázar JL (2010) Three-dimensional power Doppler angiography in endometrial cancer: correlation with tumor characteristics. Ultrasound Obstet Gynecol 35:723-729
46. Niermann KJ, Fleischer AC, Donnelly EF, Schueneman AJ, Geng L, Hallahan DE (2005) Sonographic depiction of changes of tumor vascularity in response to various therapies. Ultrasound Q 21:61-67 (quiz 149, 153-154) (Pubitemid 40734817)
47. Ebos JML, Lee CR, Christensen JG, Mutsaers AJ, Kerbel RS (2007) Multiple circulating proangiogenic factors induced by sunitinib malate are tumor-independent and correlate with antitumor efficacy. Proc Natl Acad Sci USA 104:17069-17074 (Pubitemid 350210993)
48. Griffioen AW, Mans LA, de Graaf AMA, Nowak-Sliwinska P, de Hoog CLMM, de Jong TAM et al (2012) Rapid angiogenesis onset after discontinuation of sunitinib treatment of renal cell carcinoma patients. Clin Cancer Res 18:3961-3971
49. Jain RK (2005) Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307:58-62 (Pubitemid 40093472)
50. Vakoc BJ, Lanning RM, Tyrrell JA, Padera TP, Bartlett LA, Stylianopoulos T et al (2009) Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging. Nat Med 15:1219-1223
51. Baker DG, Krochak RJ (1989) The response of the microvascular system to radiation: a review. Cancer Investig 7:287-294 (Pubitemid 19271682)
52. Denekamp J (1984) Vascular endothelium as the vulnerable element in tumours. Acta Radiol Oncol 23:217-225 (Pubitemid 15072794)
53. Nguyen V, Gaber MW, Sontag MR, Kiani MF (2000) Late effects of ionizing radiation on the microvascular networks in normal tissue. Radiat Res 154:531-536
54. Roth NM, Sontag MR, Kiani MF (1999) Early effects of ionizing radiation on the microvascular networks in normal tissue. Radiat Res 151:270-277 (Pubitemid 29109137)
55. Ogawa K, Boucher Y, Kashiwagi S, Fukumura D, Chen D, Gerweck LE (2007) Influence of tumor cell and stroma sensitivity on tumor response to radiation. Cancer Res 67:4016-4021 (Pubitemid 46815045)
56. Gerweck LE, Vijayappa S, Kurimasa A, Ogawa K, Chen DJ (2006) Tumor cell radiosensitivity is a major determinant of tumor response to radiation. Cancer Res 66:8352-8355 (Pubitemid 44449143)
57. El Kaffas A, Tran W, Czarnota GJ (2012) Vascular strategies for enhancing tumour response to radiation therapy. Technol Cancer Res Treatment 11:421-432