DLL4-notch signalling blockade synergizes combined ultrasound-stimulated microbubble and radiation therapy in human colon cancer xenografts

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  El Kaffas, Ahmed ^a,b   Nofiele, Joris ^b   Giles, Anoja ^a,b   Cho, Song ^c   Liu, Stanley K ^a,b   Czarnota, Gregory J ^a,b  

^a SUNNYBROOK RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c MEDIMMUNE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DELTA LIKE LIGAND 4 MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG; CD31 ANTIGEN; MEMBRANE PROTEIN; NOTCH RECEPTOR; PROTEIN; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; BIOPHYSICS; CANCER CONTROL; CANCER RADIOTHERAPY; CELL DEATH; COLON CANCER; CONTROLLED STUDY; DOPPLER FLOWMETRY; FEMALE; HISTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; NUDE MOUSE; SIGNAL TRANSDUCTION; THREE DIMENSIONAL POWER DOPPLER ULTRASOUND; TUMOR CELL; TUMOR GROWTH; TUMOR VASCULARIZATION; TUMOR VOLUME; TUMOR XENOGRAFT; ULTRASOUND STIMULATED MICROBUBBLE; ANIMAL; COLONIC NEOPLASMS; COLOR ULTRASOUND FLOWMETRY; DISEASE MODEL; DRUG EFFECTS; DRUG SCREENING; ECHOGRAPHY; HUMAN; METABOLISM; MICROBUBBLE; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD31; CELL DEATH; CELL LINE, TUMOR; COLONIC NEOPLASMS; DISEASE MODELS, ANIMAL; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; MICROBUBBLES; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; TUMOR BURDEN; ULTRASONOGRAPHY, DOPPLER, COLOR; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84899691019     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093888     Document Type: Article

References (34)

1. Kerbel RS (2000) Tumor angiogenesis: past, present and the near future. Carcinogenesis 21: 505-515. (Pubitemid 30137936)
2. El Kaffas A, Tran W, Czarnota GJ (2012) Vascular Strategies for Enhancing Tumour Response to Radiation Therapy. TCRT 11: 421-432.
3. Franses JW, Edelman ER (2011) The evolution of endothelial regulatory paradigms in cancer biology and vascular repair. Cancer Research 71: 7339- 7344. doi:10.1158/0008-5472.CAN-11-1718.
4. Hida K, Akiyama K, Ohga N, Maishi N, Hida Y, et al. (2013) Tumor endothelial cells acquire drug resistance in a tumor microenvironment. Journal of Biochemistry 153: 243-249.
5. Bergers G, Hanahan D (2008) Modes of resistance to anti-angiogenic therapy. Nature Reviews Cancer 8: 592-603. doi:10.1038/nrc2442.
6. Senan S, Smit EF (2007) Design of clinical trials of radiation combined with antiangiogenic therapy. The Oncologist 12: 465-477. doi:10.1634/ theoncologist. 12-4-465. (Pubitemid 46698724)
7. Lobov IB, Renard RA, Papadopoulos N, Gale NW, Thurston G, et al. (2006) Delta-like ligand 4 (Dll4 ) is induced by VEGF as a negative regulator of angiogenic sprouting. Proceedings of the National Academy of Sciences 104: 3219-3224. (Pubitemid 46364140)
8. Patel NS, Li J-L, Generali D, Poulsom R, Cranston DW, et al. (2005) Upregulation of delta-like 4 ligand in human tumor vasculature and the role of basal expression in endothelial cell function. Cancer Research 65: 8690-8697. doi:10.1158/0008-5472.CAN-05-1208. (Pubitemid 41377356)
9. Sainson RC, Harris AL (2007) Anti-Dll4 therapy: can we block tumour growth by increasing angiogenesis? Trends in molecular medicine 13: 389-395. doi:10.1016/j.molmed.2007.07.002. (Pubitemid 47385383)
10. Kuhnert F, Kirshner JR, Thurston G (2011) Dll4-Notch signaling as a therapeutic target in tumor angiogenesis. Vascular cell 3: 20. doi:10.1186/2045-824X-3-20.
11. Noguera-Troise I, Daly C, Papadopoulos NJ, Coetzee S, Boland P, et al. (2006) Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 444: 1032-1037. doi:10.1038/nature05355. (Pubitemid 46018516)
12. Ridgway J, Zhang G, Wu Y, Stawicki S, Liang W-C, et al. (2006) Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 444: 1083-1087. doi:10.1038/nature05313. (Pubitemid 46018529)
13. Kleibeuker E, Griffioen AW, Verheul HM, Slotman BJ, Thijssen VL (2012) Combining angiogenesis inhibition and radiotherapy: A double-edged sword. Drug Resistance Updates 15: 173-182. doi:10.1016/j.drup.2012.04.002.
14. Mriouah J, Boura C, Thomassin M (2012) Tumor vascular responses to antivascular and antiangiogenic strategies: looking for suitable models. Trends in Biotechnology 30: 649-658. doi:10.1016/j.tibtech.2012.08.006.
15. Liu SK, Bham S a S, Fokas E, Beech J, Im J, et al. (2011) Delta-like ligand 4- notch blockade and tumor radiation response. Journal of the National Cancer Institute 103: 1778-1798. doi:10.1093/jnci/djr419.
16. Goertz DE, Todorova M, Mortazavi O, Agache V, Chen B, et al. (2012) Antitumor effects of combining docetaxel (taxotere) with the antivascular action of ultrasound stimulated microbubbles. PloS one 7: e52307. doi:10.1371/journal. pone.0052307.
17. Ngwa W, Makrigiorgos GM, Berbeco RI (2012) Gold nanoparticle-aided brachytherapy with vascular dose painting: Estimation of dose enhancement to the tumor endothelial cell nucleus. Medical physics 39: 392. doi:10.1118/1.3671905.
18. Berbeco RI, Ngwa W, Makrigiorgos GM (2011) Localized dose enhancement to tumor blood vessel endothelial cells via megavoltage X-rays and targeted gold nanoparticles: new potential for external beam radiotherapy. International journal of radiation oncology, biology, physics 81: 270-276. doi:10.1016/j.ijrobp.2010.10.022.
19. Czarnota GJ, Karshafian R, Burns PN, Wong S, Al Mahrouki A, et al. (2012) Tumor radiation response enhancement by acoustical stimulation of the vasculature. Proceedings of the National Academy of Sciences of the United States of America 109: E2033-41. doi:10.1073/pnas.1200053109.
20. Tran WT, Iradji S, Sofroni E, Giles A, Eddy D, et al. (2012) Microbubble and ultrasound radioenhancement of bladder cancer. British journal of cancer 107: 469-476. doi:10.1038/bjc.2012.279.
21. Kim HC, Al-Mahrouki A, Gorjizadeh A, Karshafian R, Czarnota GJ (2013) Effects of Biophysical Parameters in Enhancing Radiation Responses of Prostate Tumors with Ultrasound-Stimulated Microbubbles. Ultrasound in medicine & biology: 1-12. doi:10.1016/j.ultrasmedbio.2013.01.012.
22. Al-Mahrouki A a, Karshafian R, Giles A, Czarnota GJ (2012) Bioeffects of ultrasound-stimulated microbubbles on endothelial cells: gene expression changes associated with radiation enhancement in vitro. Ultrasound in medicine & biology 38: 1958-1969. doi:10.1016/j.ultrasmedbio.2012.07.009.
23. Kwok SJJ, El Kaffas A, Lai P, Al Mahrouki A, Lee J, et al. (2013) Ultrasound- Mediated Microbubble Enhancement of Radiation Therapy Studied Using Three-Dimensional High-Frequency Power Doppler Ultrasound. Ultrasound In Medecine and Biology in press.
24. García-Barros M, Thin TH, Maj J, Cordon-Cardo C, Haimovitz-Friedman A, et al. (2010) Impact of stromal sensitivity on radiation response of tumors implanted in SCID hosts revisited. Cancer Research 70: 8179-8186. doi:10.1158/0008-5472.CAN-10-1871.
25. Fuks Z, Kolesnick R (2005) Engaging the vascular component of the tumor response. Cancer Cell 8: 89-91. doi:10.1016/j.ccr.2005.07.014. (Pubitemid 41132735)
26. El Kaffas A, Giles A, Czarnota GJ (2013) Dose-dependent response of tumor vasculature to radiation therapy in combination with Sunitinib depicted by three-dimensional high-frequency power Doppler ultrasound. Angiogenesis 16: 443-454. doi:10.1007/s10456-012-9329-2.
27. 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 Research 62: 6371-6375. (Pubitemid 35364088)
28. Foster F (2000) Advances in ultrasound biomicroscopy. Ultrasound in Medecine and Biology 26: 1-27. doi:10.1016/S0301-5629(99)00096-4. (Pubitemid 30045518)
29. Haimovitz-Friedman A, Kan CC, Ehleiter D, Persaud RS, McLoughlin M, et al. (1994) Ionizing radiation acts on cellular membranes to generate ceramide and initiate apoptosis. The Journal of Experimental Medicine 180: 525.
30. Rotolo J, Zhang J, Donepudi M, Lee H, Fuks Z, et al. (2005) Caspase-dependent and -independent activation of acid sphingomyelinase signaling. The Journal of biological chemistry 280: 26425-26434. doi:10.1074/jbc.M414569200. (Pubitemid 41022239)
31. Sofia Vala I, Martins LR, Imaizumi N, Nunes RJ, Rino J, et al. (2010) Low doses of ionizing radiation promote tumor growth and metastasis by enhancing angiogenesis. PloS one 5: e11222. doi:10.1371/journal.pone.0011222.
32. Sofia Vala I, Martins LR, Imaizumi N, Nunes RJ, Rino J, et al. (2010) Low doses of ionizing radiation promote tumor growth and metastasis by enhancing angiogenesis. PloS one 5: e11222. doi:10.1371/journal.pone.0011222.
33. Thanik V, Chang C (2010) Cutaneous low-dose radiation increases tissue vascularity through upregulation of angiogenic and vasculogenic pathways. Journal of Vascular Research 47: 472-480. doi:10.1159/000313875.
34. Goel S, Wong AH, Jain RK (2012) Vascular Normalization as a Therapeutic Strategy. Cold Spring Harbor Perspectives in Medecine 2: 1-24. doi:10.1101/cshperspect.a006486.