Focused ultrasound delivers targeted immune cells to metastatic brain tumors

Cancer Research

Volumn 73, Issue 6, 2013, Pages 1892-1899

  Alkins, Ryan ^a,b   Burgess, Alison ^a   Ganguly, Milan ^a   Francia, Giulio ^a   Kerbel, Robert ^a,b   Wels, Winfried S ^c   Hynynen, Kullervo ^a,b  

^a Sunnybrook Health Sciences Centre   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c INSTITUTE FOR TUMOR BIOLOGY AND EXPERIMENTAL THERAPY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN TUMOR; CANCER IMMUNOTHERAPY; COMPUTER ASSISTED THERAPY; CONTRAST ENHANCEMENT; CONTROLLED STUDY; ECHOGRAPHY; FEASIBILITY STUDY; FOCUSED ULTRASOUND; GENE DISRUPTION; GENETIC TRANSFECTION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCOMPETENT CELL; MALE; METASTASIS POTENTIAL; MICROBUBBLE; MOLECULARLY TARGETED THERAPY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RAT; REPRODUCIBILITY; TUMOR LOCALIZATION; TUMOR VASCULARIZATION; ULTRASOUND;

ANIMALS; BRAIN NEOPLASMS; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; GENES, ERBB-2; HUMANS; MALE; NEOPLASM TRANSPLANTATION; RATS; RATS, NUDE; ULTRASONIC THERAPY;

EID: 84875423207     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-2609     Document Type: Article

References (45)

1. Lee Y-T. Breast carcinoma: pattern of metastasis at autopsy. J Surg Oncol 1983;23:175-80.
2. Lin NU, Bellon JR, Winer EP. CNS metastases in breast cancer. J Clin Oncol 2004;22:3608-17.
3. Abbott NJ,Rönnbäck L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006;7:41-53.
4. Lockman PR, Mittapalli RK, Taskar KS, Rudraraju V, Gril B, Bohn KA, et al. Heterogeneous blood-tumor barrier permeability determines drug efficacy in experimental brain metastases of breast cancer. Clin Cancer Res 2010;16:5664-78.
5. Linn SC, Giaccone G, van Diest PJ, Blokhuis WM, van Der Valk P, van Kalken CK, et al. Prognostic relevance of p-glycoprotein expression in breast cancer. Ann Oncol 1995;6:679-85.
6. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. Human breast cancer: correlation of relapse and survival with amplification of the HER2/neu oncogene. Science 1987;235:177-82.
7. Slamon DJ, Leyland-Jones B, Shak S, Fuchs H, Paton V, Bajamonde A, et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med 2001;344:783-92.
8. Geyer CE, Forster J, Lindquist D, Chan S, Romieu CG, Pienkowski T, et al. Lapatinib plus capecitabine for HER2-positive advanced breast cancer. N Engl J Med 2006;355:2733-43.
9. Smyth MJ, Hayakawa Y, Takeda K, Yagita H. New aspects of naturalkiller-cell surveillance and therapy of cancer. Nat Rev Cancer 2002; 2:850-61.
10. Uherek C, Tonn T, Uherek B, Becker S, Schnierle B, Klingemann H-G, et al. Retargeting of NK-cell cytolytic activity to ErbB2 expressing tumor cells results in efficient and selective tumor cell destruction. Blood 2002;100:1265-73.
11. Daldrup-Link HE, Meier R, Rudelius M, Piontek G, Piert M, et al. In vivo tracking of genetically engineered anti-Her2/neu directed natural killer cells to Her2/neu positive mammary tumors with magnetic resonance imaging. Eur Radiol 2005;15:4-13.
12. Meier R, Piert M, Piontek G, Rudelius M, Oostendorp RA, Senekowitsch-Schmidtke R, et al. Tracking of [18F]FDG-labeled natural killer cells to HER2/neu-positive tumors. Nucl Med Biol 2008;35:579-88.
13. Pestalozzi BC, Brignoli S. Trastuzumab in CSF. J Clin Oncol 2000; 18:2350-1.
14. Stemmler HJ, Schmitt M, Willems A, Bernhard H, Harbeck N, Heinemann V. Ratio of trastuzumab levels in serum and cerebrospinal fluid is altered in HER2-positive breast cancer patients with brain metastases and impairment of blood-brain barrier. Anticancer Drugs 2007;18: 23-8.
15. Polli JW, Humphreys JE, Harmon KA, Castellino S, O'Mara MJ, Olson KL, et al. The role of efflux and uptake transporters in [N-{3-chloro-4-[(3- fluorobenzyl)oxy]phenyl}-6-[5-({[2-(methylsulfonyl)ethyl]amino} methyl)-2-furyl]-4-quinazolinamine (GW572016, lapatinib) disposition and drug interactions. Drug Metab Dispos 2008;36:695-701.
16. Hynynen K, McDannold N, Vykhodtseva N, Jolesz FA. NoninvasiveMR imaging-guided focal opening of the blood-brain barrier in rabbits. Radiology 2001;220:640-6.
17. McDannold N, Vykhodtseva N, Hynynen K. Use of ultrasound pulses combined with Definity® for targeted blood-brain barrier disruption: a feasibility study. Ultrasound Med Biol 2007;33:584-90.
18. Sheikov N, McDannold N, Vykhodtseva N, Jolesz F, Hynynen K. Cellular mechanisms of the blood-brain barrier opening induced by ultrasound in presence of microbubbles. Ultrasound Med Biol 2004;30:979-89.
19. Sheikov N, Mcdannold N, Sharma S, Hynynen K. Effect of focused ultrasound applied with an ultrasound contrast agent on the tight junctional integrity of the brain microvascular endothelium. Ultrasound Med Biol 2008;34:1093-104.
20. Kinoshita M, McDannold N, Jolesz FA, Hynynen K. Noninvasive localized delivery of Herceptin to the mouse brain by MRI-guided focused ultrasound-induced blood-brain barrier disruption. Proc Natl Acad Sci 2006;103:11719-23.
21. Liu HL, Hua MY, Chen PY, Chu PC, Pan CH, Yang HW, et al. Bloodbrain barrier disruption with focused ultrasound enhances delivery of chemotherapeutic drugs for glioblastoma treatment. Radiology 2010;255:415-25.
22. Burgess A, Ayala-Grosso CA, Ganguly M, Jordão JF, Aubert I, Hynynen K. Targeted delivery of neural stem cells to the brain using MRI-guided focused ultrasound to disrupt the blood-brain barrier. PLoS One 2011;6:e27877.
23. McDannold N, Arvanitis CD, Vykhodtseva N, Livingstone MS. Temporary disruption of the blood-brain barrier by use of ultrasound and microbubbles: safety and efficacy evaluation in rhesus macaques. Cancer Res 2012;72:3652-63.
24. Francia G, Man S, Lee CJ, Xu P, Mossoba ME, Emmenegger U, et al. Comparative impact of trastuzumab and cyclophosphamide on HER-2-postive human breast cancer xenografts. Clin Cancer Res 2009;15: 6358-66.
25. Kobayashi N, Allen N, Clendenon NR, Ko LW. An improved rat braintumor model. J Neurosurg 1980;53:808-15.
26. Chopra R, Curiel L, Staruch R, Morrison L, Hynynen K. An MRI-compatible system for focused ultrasound experiments in small animal models. Med Phys 2009;36:1867-74.
27. O'Reilly MA, Hynynen K. Blood-brain barrier: real-time feedback-controlled focused ultrasound disruption by using an acoustic emissions-based controller. Radiology 2012;263:96-106.
28. O'Reilly MA, Muller A, Hynynen K. Ultrasound insertion loss of rat parietal bone appears to be proportional to animal mass at submegahertz frequencies. Ultrasound Med Biol 2011;37:1930-7.
29. Tonn T, Becker S, Esser R, Schwabe D, Seifried E. Cellular immunotherapy of malignancies using the clonal natural killer cell line NK-92. J Hematother Stem Cell Res 2001;10:535-44.
30. Arai S, Meagher R, Swearingen M, Myint H, Rich E, Martinson J, et al. Infusion of the allogeneic cell line NK-92 in patients with advanced renal cell cancer or melanoma: a phase I trial. Cytotherapy 2008; 10:625-32.
31. Ahmed N, Ratnayake M, Savoldo B, Perlaky L, Dotti G, Wels WS, et al. Regression of experimental medulloblastoma following transfer of HER2-specific T cells. Cancer Res 2007;67:5957-64.
32. Ahmed N, Salsman VS, Kew Y, Shaffer D, Powell S, Zhang YJ, et al. HER2-specific T cells target primary glioblastoma stem cells and induce regression of autologous experimental tumors. Clin Cancer Res 2010;16:474-85.
33. Altland OD, Dalecki D, Suchkova VN, Francis CW. Low-intensity ultrasound increases endothelial cell nitric oxide synthase activity and nitric oxide synthesis. J Thromb Haemost 2004;2:637-43.
34. Hsu S, Huang T. Bioeffect of ultrasound on endothelial cells in vitro. Biomol Eng 2004;21:99-104.
35. Deng J, Huang Q, Wang F, Liu Y, Wang Z, Wang Z, et al. The role of caveolin-1 in blood-brain barrier disruption induced by focused ultrasound combined with microbubbles. J Mol Neurosci 2012; 46:677-87.
36. Ward M, Wu J, Chiu JF. Ultrasound-induced cell lysis and sonoporation enhanced by contrast agents. J Acoust Soc Am 1999;5:2951-7.
37. Wu J. Shear stress in cells generated by ultrasound. Prog Biophys Mol Biol 2007 93:363-73.
38. VanBavel E. Effects of shear stress on endothelial cells: possible relevance for ultrasound applications. Prog Biophys Mol Biol 2007; 93:374-83.
39. Dewitz TS, Hung TC, Martin RR, McIntire LV. Mechanical trauma in leukocytes. J Lab Clin Med 1977;90:728-36.
40. Okuyama M., Kambayashi J, Sakon M, Monden M. LFA-1/ICAM-3 mediates neutrophil homotypic aggregation under fluid shear stress. J Cell Biochem 1996;60:550-9.
41. Moazzam F, DeLano FA, Zweifach BW, Schmid-Schönbein GW. The leukocyte response to fluid stress. Proc Natl Acad Sci 1997;94: 5338-43.
42. Kitayama J, Hidemura A, Saito H, Nagawa H. Shear stress affects migration behavior of polymorphonuclear cells arrested on endothelium. Cell Immunol 2000;203:39-46.
43. Cinamon G, Shinder V, Alon R. Shear forces promote lymphocyte migration across vascular endothelium bearing apical chemokines. Nat Immunol 2001;2:515-22.
44. Marty B, Larrat B, Van Landeghem M, Robic C, Robert P, Port M, et al. Dynamic study of blood-brain barrier closure after its disruption using ultrasound: a quantitative analysis. J Cereb Blood Flow Metab 2012;32:1948-58.
45. Yedgar S, Koshkaryev A, Barshtein G. The red blood cell in vascular occlusion. Pathophysiol Haemost Thromb 2002;32:263-8.