Histotripsy induces apoptosis and reduces hypoxia in a neuroblastoma xenograft model

References

• Bagatell R, Beck-Popovic M, London WB, et al. Significance of MYCN amplification in international neuroblastoma staging system stage 1 and 2 neuroblastoma: a report from the international neuroblastoma risk group database. J Clin Oncol. 2009;27(3):365–370. doi:10.1200/JCO.2008.17.9184
   PubMed Web of Science ®Google Scholar
• Monclair T, Brodeur GM, Ambros PF, et al. The international neuroblastoma risk group (INRG) staging system: an INRG task force report. J Clin Oncol. 2009;27(2):298–303. doi:10.1200/JCO.2008.16.6876
   PubMed Web of Science ®Google Scholar
• Irwin MS, Naranjo A, Zhang FF, et al. Revised neuroblastoma risk classification system: a report from the children’s oncology group. J Clin Oncol. 2021;39(29):3229–3241. doi:10.1200/JCO.21.00278
   PubMed Web of Science ®Google Scholar
• Pinto NR, Applebaum MA, Volchenboum SL, et al. Advances in risk classification and treatment strategies for neuroblastoma. J Clin Oncol. 2015;33(27):3008–3017. doi:10.1200/JCO.2014.59.4648
   PubMed Web of Science ®Google Scholar
• Barr EK, Applebaum MA. Genetic predisposition to neuroblastoma. Children , 2018;5(9):119. doi:10.3390/children5090119
   PubMedGoogle Scholar
• Park JR, Kreissman SG, London WB, et al. Effect of tandem autologous stem cell transplant vs single transplant on event-free survival in patients with high-risk neuroblastoma: a randomized clinical trial. Jama. 2019;322(8):746–755. doi:10.1001/jama.2019.11642
   PubMed Web of Science ®Google Scholar
• Sharma R, Mer J, Lion A, et al. Clinical presentation, evaluation, and management of neuroblastoma. Pediatr Rev. 2018;39(4):194–203. doi:10.1542/pir.2017-0087
   PubMed Web of Science ®Google Scholar
• Herd F, Basta NO, McNally RJQ, et al. A systematic review of re-induction chemotherapy for children with relapsed high-risk neuroblastoma. Eur J Cancer. 2019;111:50–58. doi:10.1016/j.ejca.2018.12.032
   PubMed Web of Science ®Google Scholar
• Friedman DN, Henderson TO. Late effects and survivorship issues in patients with neuroblastoma. Children , 2018;5(8):107. doi:10.3390/children5080107
   PubMedGoogle Scholar
• Huertas-Castaño C, Gómez-Muñoz MA, Pardal R, Vega FM. Hypoxia in the initiation and progression of neuroblastoma tumours. Int J Mol Sci. 2019;21(1):39. doi:10.3390/ijms21010039
   PubMed Web of Science ®Google Scholar
• Jögi A, Øra I, Nilsson H, et al. Hypoxia alters gene expression in human neuroblastoma cells toward an immature and neural crest-like phenotype. Proc Natl Acad Sci U S A. 2002;99(10):7021–7026. doi:10.1073/pnas.102660199
   PubMed Web of Science ®Google Scholar
• Hockel M, Vaupel P. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. JNCI. 2001;93(4):266–276. doi:10.1093/jnci/93.4.266
   PubMedGoogle Scholar
• Zaghloul N. Vascular endothelial growth factor blockade rapidly elicits alternative proangiogenic pathways in neuroblastoma. Int J Oncol. 2009;34(2):401–407.
   PubMed Web of Science ®Google Scholar
• Chen S, Zhang M, Xing L, et al. HIF-1alpha contributes to proliferation and invasiveness of neuroblastoma cells via SHH signaling. PLOS One. 2015;10(3):e0121115. doi:10.1371/journal.pone.0121115
   PubMed Web of Science ®Google Scholar
• Herrmann A, Rice M, Lévy R, et al. Cellular memory of hypoxia elicits neuroblastoma metastasis and enables invasion by non-aggressive neighbouring cells. Oncogenesis. 2015;4(2):e138-e138. doi:10.1038/oncsis.2014.52
   Web of Science ®Google Scholar
• Zhao Y, Cao J, Melamed A, et al. Losartan treatment enhances chemotherapy efficacy and reduces ascites in ovarian cancer models by normalizing the tumor stroma. Proc Natl Acad Sci U S A. 2019;116(6):2210–2219. doi:10.1073/pnas.1818357116
   PubMed Web of Science ®Google Scholar
• Bellary A, Villarreal A, Eslami R, et al. Perfusion-guided sonopermeation of neuroblastoma: a novel strategy for monitoring and predicting liposomal doxorubicin uptake in vivo. Theranostics. 2020;10(18):8143–8161. doi:10.7150/thno.45903
   PubMed Web of Science ®Google Scholar
• de Senneville BD, Moonen C, Ries M. MRI-guided HIFU methods for the ablation of liver and renal cancers. Adv Exp Med Biol. 2016;880:43–63.
   PubMed Web of Science ®Google Scholar
• Xu Z, Hall TL, Vlaisavljevich E, et al. Histotripsy: the first noninvasive, non-ionizing, non-thermal ablation technique based on ultrasound. Int J Hyperthermia. 2021;38(1):561–575. doi:10.1080/02656736.2021.1905189
   PubMed Web of Science ®Google Scholar
• Vidal-Jove J, Serres X, Vlaisavljevich E, et al. First-in-man histotripsy of hepatic tumors: the THERESA trial, a feasibility study. Int J Hyperthermia. 2022;39(1):1115–1123. doi:10.1080/02656736.2022.2112309
   PubMed Web of Science ®Google Scholar
• Cleveland RO, McAteer JA. Physics of shock-wave lithotripsy. Smith AD, Badlani GH, Preminger GM, Kavoussi LR, editors. Smith’s textbook of endourology. Blackwell Publishing Ltd.; 2012. p. 527–558.
   Google Scholar
• Bader KB, Vlaisavljevich E, Maxwell AD. For whom the bubble grows: physical principles of bubble nucleation and dynamics in histotripsy ultrasound therapy. Ultrasound Med Biol. 2019;45(5):1056–1080. doi:10.1016/j.ultrasmedbio.2018.10.035
   PubMed Web of Science ®Google Scholar
• Vlaisavljevich E, Owens G, Lundt J, et al. Non-invasive liver ablation using histotripsy: preclinical safety study in an in vivo porcine model. Ultrasound Med Biol. 2017;43(6):1237–1251. doi:10.1016/j.ultrasmedbio.2017.01.016
   PubMed Web of Science ®Google Scholar
• Hendricks-Wenger A, Hutchison R, Vlaisavljevich E, et al. Immunological effects of histotripsy for cancer therapy. Front Oncol. 2021;11:681629. doi:10.3389/fonc.2021.681629
   PubMed Web of Science ®Google Scholar
• Worlikar T, Mendiratta-Lala M, Vlaisavljevich E, et al. Effects of histotripsy on local tumor progression in an in vivo orthotopic rodent liver tumor model. BME Front. 2020;2020:9830304. doi:10.34133/2020/9830304
   PubMedGoogle Scholar
• Bader KB, Wallach EL, Shekhar H, et al. Estimating the mechanical energy of histotripsy bubble clouds with high frame rate imaging. Phys Med Biol. 2021;66(16):165004. doi:10.1088/1361-6560/ac155d
   Web of Science ®Google Scholar
• Bollen V, Hendley SA, Paul JD, et al. In vitro thrombolytic efficacy of single- and five-cycle histotripsy pulses and rt-PA. Ultrasound Med Biol. 2020;46(2):336–349. doi:10.1016/j.ultrasmedbio.2019.10.009
   PubMed Web of Science ®Google Scholar
• Banerjee D, Hernandez SL, Garcia A, et al. Notch suppresses angiogenesis and progression of hepatic metastases. Cancer Res. 2015;75(8):1592–1602. doi:10.1158/0008-5472.CAN-14-1493
   PubMed Web of Science ®Google Scholar
• Montfort A, Colacios C, Levade T, et al. The TNF paradox in cancer progression and immunotherapy. Front Immunol. 2019;10:1818. doi:10.3389/fimmu.2019.01818
   PubMed Web of Science ®Google Scholar
• Forsythe JA, Jiang BH, Iyer NV, et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol. 1996;16(9):4604–4613. doi:10.1128/MCB.16.9.4604
   PubMed Web of Science ®Google Scholar
• Kim KJ, Li B, Winer J, et al. Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature. 1993;362(6423):841–844. doi:10.1038/362841a0
   PubMed Web of Science ®Google Scholar
• Carmeliet P. VEGF as a key mediator of angiogenesis in cancer. Oncology. 2005;69(Suppl 3):4–10. doi:10.1159/000088478
   PubMed Web of Science ®Google Scholar
• Kano MR, Morishita Y, Iwata C, et al. VEGF-A and FGF-2 synergistically promote neoangiogenesis through enhancement of endogenous PDGF-B-PDGFRbeta signaling. J Cell Sci. 2005;118(Pt 16):3759–3768. doi:10.1242/jcs.02483
   PubMed Web of Science ®Google Scholar
• Rosenbaum SR, Wilski NA, Aplin AE. Fueling the fire: inflammatory forms of cell death and implications for cancer immunotherapy. Cancer Discov. 2021;11(2):266–281. doi:10.1158/2159-8290.CD-20-0805
   PubMed Web of Science ®Google Scholar
• Boutilier AJ, Elsawa SF. Macrophage polarization states in the tumor microenvironment. Int J Mol Sci. 2021;22(13):6995.
   PubMed Web of Science ®Google Scholar
• Ley K. M1 means kill; M2 means heal. J Immunol. 2017;199(7):2191–2193. doi:10.4049/jimmunol.1701135
   PubMed Web of Science ®Google Scholar
• Palano MT, Gallazzi M, Cucchiara M, et al. Neutrophil and natural killer cell interactions in cancers: dangerous liaisons instructing immunosuppression and angiogenesis. Vaccines. 2021;9(12):1488. doi:10.3390/vaccines9121488
   Web of Science ®Google Scholar
• Qu S, Worlikar T, Felsted AE, et al. Non-thermal histotripsy tumor ablation promotes abscopal immune responses that enhance cancer immunotherapy. J Immunother Cancer. 2020;8(1):e000200. doi:10.1136/jitc-2019-000200
   PubMed Web of Science ®Google Scholar
• Vidal-Jove J, Serres-Creixams X, Ziemlewicz TJ, et al. Liver histotripsy mediated abscopal effect-case report. IEEE Trans Ultrason Ferroelectr Freq Control. 2021;68(9):3001–3005. doi:10.1109/TUFFC.2021.3100267
   PubMed Web of Science ®Google Scholar
• Stark K, Eckart A, Haidari S, et al. Capillary and arteriolar pericytes attract innate leukocytes exiting through venules and 'instruct’ them with pattern-recognition and motility programs. Nat Immunol. 2013;14(1):41–51. doi:10.1038/ni.2477
   PubMed Web of Science ®Google Scholar
• Hall TL, Kieran K, Ives K, et al. Histotripsy of rabbit renal tissue in vivo: temporal histologic trends. J Endourol. 2007;21(10):1159–1166. doi:10.1089/end.2007.9915
   PubMed Web of Science ®Google Scholar
• Winterroth F, Xu Z, Wang T-Y, et al. Examining and analyzing subcellular morphology of renal tissue treated by histotripsy. Ultrasound Med Biol. 2011;37(1):78–86. doi:10.1016/j.ultrasmedbio.2010.10.002
   PubMed Web of Science ®Google Scholar
• Dewhirst MW, Secomb TW. Transport of drugs from blood vessels to tumour tissue. Nat Rev Cancer. 2017;17(12):738–750. doi:10.1038/nrc.2017.93
   PubMed Web of Science ®Google Scholar
• Secomb TW, Hsu R, Ong ET, et al. Analysis of the effects of oxygen supply and demand on hypoxic fraction in tumors. Acta Oncol. 1995;34(3):313–316. doi:10.3109/02841869509093981
   PubMed Web of Science ®Google Scholar