3,758
Views
28
CrossRef citations to date
0
Altmetric
Articles

Enhancing the abscopal effect of radiation and immune checkpoint inhibitor therapies with magnetic nanoparticle hyperthermia in a model of metastatic breast cancer

ORCID Icon, ORCID Icon, , , , , , ORCID Icon, , ORCID Icon, ORCID Icon, , ORCID Icon & ORCID Icon show all
Pages 47-63 | Received 12 Aug 2019, Accepted 28 Aug 2019, Published online: 03 Dec 2019

References

  • Carey LA, Perou CM, Livasy CA. Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA. 2006;295(21):2492–2502.
  • Anders C, Carey LA. Understanding and treating triple-negative breast cancer. Oncology. 2008;22(11):1233–1239. discussion 1239-1240,1243.
  • Dent R, Trudeau M, Pritchard KI, et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res. 2007;13(15):4429–4434.
  • Kassam F, Enright K, Dent R, et al. Survival outcomes for patients with metastatic triple-negative breast cancer: implications for clinical practice and trial design. Clin Breast Cancer. 2009;9(1):29–33.
  • Chen MT, Sun HF, Zhao Y, et al. Comparison of patterns and prognosis among distant metastatic breast cancer patients by age groups: a SEER population-based analysis. Sci Rep. 2017;7(1):9254.
  • Tseng LM, Hsu NC, Chen SC, et al. Distant metastasis in triple-negative breast cancer. Neoplasma. 2013;60(03):290–294.
  • Willett WC. Epidemiology and nongenetic causes of breast cancer. In: Harris JR, Lippman ME, Morrow M, Osborn CK, editors. Diseases of the breast. Philadelphia, PA: Lippincott Williams & Wilkins; 2000. p. 175.
  • Refaat T, Sachdev S, Sathiaseelan V, et al. Hyperthermia and radiation therapy for locally advanced or recurrent breast cancer. Breast. 2015;24(4):418–425.
  • Oldenborg S, Van Os RM, Van Rij CM, et al. Elective re-irradiation and hyperthermia following resection of persistent locoregional recurrent breast cancer: a retrospective study. Int J Hyperthermia. 2010;26(2):136–144.
  • Linthorst M, Baaijens M, Wiggenraad R, et al. Local control rate after the combination of re-irradiation and hyperthermia for irresectable recurrent breast cancer: results in 248 patients. Radiother Oncol. 2015;117(2):217–222.
  • Bianchini G, Gianni L. The immune system and response to HER2-targeted treatment in breast cancer. Lancet Oncol. 2014;15:e45–e68.
  • Drake CG. Combination immunotherapy approaches. Ann Oncol. 2012;23(Suppl 8):viii41–viii46.
  • Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–674.
  • Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science. 2011;331(6024):1565–1570.
  • Koebel CM, Vermi W, Swann JB, et al. Adaptive immunity maintains occult cancer in an equilibrium state. Nature. 2007;450(7171):903–907.
  • Zitvogel L, Apetoh L, Ghiringhelli F, et al. The anticancer immune response: indispensable for therapeutic success? J Clin Invest. 2008;118(6):1991–2001.
  • Dewan ZM, Galloway AE, Kawashima N, et al. Fractionated but not single-dose radiotherapy induces an immune-mediated abscopal effect when combined with anti-CTLA-4 antibody. Clin Cancer Res. 2009;15(17):5379–5388.
  • Demaria S, Kawashima N, Yang AM, et al. Immune-mediated inhibition of metastases after treatment with local radiation and CTLA-4 blockade in a mouse model of breast cancer. Clin Cancer Res. 2015;11:728–734.
  • Shu CA, Rizvi NA. Into the clinic with nivolumab and pembrolizumab. Oncologist. 2016;21(5):527–528.
  • Hodi FS, O'Day SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363(8):711–723.
  • Wolchok JD, Kluger H, Callahan MK, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med. 2013;369(2):122–133.
  • Callahan MK, Postow MA, Wolchok JP. CTLA-4 and PD-1 pathway blockade: combinations in the clinic. Front Oncol. 2014;4:385.
  • Hassel JC, Heinzerling L, Aberle J, et al. Combined immune checkpoint blockade (anti-PD-1/anti-CTLA-4): evaluation and management of adverse drug reactions. Cancer Treat Rev. 2017;57:36–49.
  • Mole RH. Whole body irradiation; radiobiology or medicine? BJR. 1953;26(305):234–241.
  • Verbrugge I, Hagekyriakou J, Sharp LL, et al. Radiotherapy increases the permissiveness of established mammary tumors to rejection by immunomodulatory antibodies. Cancer Res. 2012;72(13):3163–3174.
  • Postow MA, Callahan MK, Barker CA, et al. Immunologic correlates of the abscopal effect in a patient with melanoma. N Engl J Med. 2012;366(10):925–931.
  • Hodge JW, Sharp HJ, Gameiro SR. Abscopal regression of antigen disparate tumors by antigen cascade after systemic tumor vaccination in combination with local tumor radiation. Cancer Bioth Radiopharm. 2012;27:12–22.
  • Hu ZI, McArthur HL, Ho AY. The abscopal effect of radiation therapy: what is it and how can we use it in breast cancer? Curr Breast Cancer Rep. 2017;9(1):45–51.
  • Wang HY, Fu JC, Lee YC, et al. Hyperthermia stress activates heat shock protein expression via propyl isomerase 1 regulation with heat shock factor 1. Mol Cell Biol. 2013;33(24):4889–4899.
  • Basu S, Binder RJ, Suto R, et al. Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-kappa B pathway. Int Immunol. 2000;12(11):1539–1546.
  • Sauter B, Albert ML, Francisco L, et al. Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J Exp Med. 2000;191(3):423–434.
  • Repasky EA, Evans SS, Dewhirst MW. Temperature matters! And why it should matter to tumor immunologists. Cancer Immunol Res. 2013;1(4):210–216.
  • Knippertz I, Stein MF, Dorrie J, et al. Mild hyperthermia enhances human monocyte-derived dendritic cell functions and offers potential for applications in vaccination strategies. Int J Hyperthermia. 2011;27(6):591–603.
  • Frey B, Weiss EM, Rubner Y, et al. Old and new facts about hyperthermia-induced modulations of the immune system. Int J Hyperthermia. 2012;28(6):528–542.
  • Mace TA, Zhong L, Kokolus KM, et al. Effector CD8+ T-cell IFN-γ production and cytotoxicity are enhance by mild hyperthermia. Int J Hyperthermia. 2012;28(1):9–18.
  • Hatzfeld-Charbonnier AS, Lasek A, Castera L, et al. Influence of heat stress on human monocyte-derived dendritic cell functions with immunotherapeutic potential for antitumor vaccines. J Leukocyte Biol. 2007;81(5):1179–1187.
  • Higgins JP, Bernstein MB, Hodge JW. Enhancing immune responses to tumor-associated antigens. Cancer Biol Ther. 2009;8(15):1440–1449.
  • Dewhirst MW, Jones E, Samulski T. Hyperthermia. Cancer medicine. 6th ed. Hamilton: BC Decker; 2003. p. 623–636.
  • Horsman MR, Overgaard J. Hyperthermia: a potent enhancer of radiation. Clin Oncol. 2007;19(6):418–426.
  • Krawczyk PM, Eppink B, Essers J, et al. Mild hyperthermia inhibits homologous recombination, induces BRCA2 degradation, and sensitizes cancer cells to poly (ADP-ribose) polymerase-1 inhibition. Proc Natl Acad Sci. 2011;108(24):9851–9856.
  • Bergs JWJ, Krawczyk PM, Borovski T, et al. Inhibition of homologous recombination by hyperthermia shunts early double strand break repair to non-homologous end-joining. DNA Repair. 2013;12(1):38–45.
  • Tuul M, Kitao H, Iimori M, et al. Rad9, Rad17, TopBP1 and Claspin play essential roles in heat-induced activation of ATR kinase and heat tolerance. PLoS ONE. 2013;8(2):e55361.
  • Pankhurst QA, Thanh NKT, Jones SK, et al. Progress in applications of magnetic nanoparticles in biomedicine. J Phys D Appl Phys. 2009;42(22):224001–224016.
  • Ivkov R. Magnetic nanoparticle hyperthermia: a new frontier in biology and medicine? Int J Hyperthermia. 2013;29(8):703–705.
  • Dennis CL, Ivkov R. Physics of heat generation using magnetic nanoparticles for hyperthermia. Int J Hyperthermia. 2013;29(8):715–729.
  • Johannsen M, Gneveckow U, Eckelt L, et al. Clinical hyperthermia of prostate cancer using magnetic nanoparticles: presentation of a new interstitial technique. Int J Hyperthermia. 2005;21(7):637–647.
  • Maier-Hauff K, Ulrich F, Nestler D, et al. Efficacy and safety of intratumoral thermotherapy using magnetic iron-oxide nanoparticles combined with external beam radiotherapy on patients with recurrent glioblastoma multiforme. J Neurooncol. 2011;103(2):317–324.
  • Dennis CL, Jackson AJ, Borchers JA, et al. Nearly complete regression of tumors via collective behavior of magnetic nanoparticles in hyperthermia. Nanotechnology. 2009;20(39):395103.
  • Zadnik P, Molina C, Sarabia-Estrada R, et al. Characterization of intra-tumor magnetic nanoparticle distribution and heating in a rat model of metastatic spine disease. J Neurosurg Spine. 2014;20(6):740–750.
  • Guistini AJ, Ivkov R, Hoopes PJ. Magnetic nanoparticle biodistribution following intratumoral administration. Nanotechnology. 2001;22:345101.
  • DeNardo SJ, DeNardo GL, Miers LA, et al. Development of tumor targeting bioprobes (111In-chimeric L6 monoclonal antibody nanoparticles) for alternating magnetic field cancer therapy. Clin Cancer Res. 2005;11(19):7087s–7092s.
  • DeNardo SJ, DeNardo GL, Natarajan A, et al. Thermal dosimetry predictive of efficacy of 111In-Ch L6 nanoparticle AMF induced therapy for human breast cancer in mice. J Nucl Med. 2007;48(3):437–444.
  • Attaluri A, Kandala SK, Zhou H, et al. Magnetic nanoparticle hyperthermia enhances radiation therapy: a study in mouse models of human prostate cancer. Int J Hyperthermia. 2015;31(4):359–374.
  • Yang S, Zhang JJ, Huang XY. Mouse models for tumor metastasis. Methods Mol Biol. 2012;928:221–228.
  • Gruettner C, Mueller K, Teller J, et al. Synthesis and antibody conjugation of magnetic nanoparticles with improved specific power absorption rates for alternating magnetic field cancer therapy. J Magn Magn Mater. 2007;311:181–186.
  • Natarajan A, Gruettner C, Ivkov R, et al. NanoFerrite particle based radioimmunonanoparticles: binding affinity and in vivo pharmacokinetics. Bioconjugate Chem. 2008;19(6):1211–1218.
  • Sharma A, Cornejo Mihalic J, et al. Physical characterization and in vivo organ distribution of coated iron oxide nanoparticles. Sci Rep. 2018;20:4916.
  • Dennis CL, Krycka KL, Borchers JA, et al. Internal magnetic structure of nanoparticles dominates time-dependent relaxation processes in a magnetic field. Adv Funct Mater. 2015;25(27):4300–4311.
  • Bordelon DE, Cornejo C, Grüttner C, et al. Magnetic nanoparticle heating efficiency reveals magneto-structural differences when characterized with wide ranging and high amplitude alternating magnetic fields. J Appl Phys. 2011;109(12):124904.
  • Bordelon DE, Goldstein RC, Nemkov VS, et al. Modified solenoid coil that efficiently produces high amplitude AC magnetic fields with enhanced uniformity for biomedical applications. IEEE Trans Magn. 2012;48(1):47–52.
  • Kumar A, Attaluri A, Mallipudi R, et al. Method to reduce non-specific heating of small animals in solenoid coils. Int J Hyperthermia. 2013;29(2):106–120.
  • Wong J, Armour E, Kazanzides P, et al. High-resolution, small animal radiation research platform with X-ray tomographic guidance capabilities. Int J Radiat Oncol. 2008;71(5):1591–1599.
  • Gilchrist RK, Medal R, Shorey WD, et al. Selective inductive heating of lymph nodes. Ann Surgery. 1957;146(4):596–606.
  • Kandala SK, Liapi E, Whitcomb LL, et al. Temperature-controlled power modulation compensates for heterogeneous nanoparticle distributions: a computational optimization analysis for magnetic hyperthermia. Int J Hyperthermia. 2019;36(1):115–129.
  • Kim K, Skora AD, Li Z, et al. Eradication of metastatic mouse cancers resistant to immune checkpoint blockade by suppression of myeloid-derived cells. Proc Natl Acad Sci. 2014;111(32):11774–11779.
  • Prosnitz LR, Maguire P, Anderson JM, et al. The treatment of high-grade soft tissue sarcomas with preoperative thermoradiotherapy. Int J Radiat Oncol Biol Phys. 1999;45(4):941–949.
  • Lewis JJ, Leung D, Heslin M, et al. Association of local recurrence with subsequent survival in extremity soft tissue sarcoma. JCO. 1997;15(2):646–652.
  • Gustafson P, Rooser B, Rydholm A. Is local recurrence of minor importance for metastases in soft tissue sarcoma? Cancer. 1991;67(8):2083–2086.
  • Hill SA, Denekamp J. Does local tumour heating in mice influence metastatic spread? BJR. 1982;55(654):444–451.
  • Oda M, Koga S, Maeta M. Effects of total-body hyperthermia on metastases from experimental mouse tumors. Cancer Res. 1985;45:1532–1535.
  • Urano J, Rice L, Epstein R, et al. Effect of whole-body hyperthermia on cell survival, metastasis frequency and host immunity in moderately and weakly immunogenic murine tumors. Cancer Res. 1983;43(3):1039–1043.
  • Yerushalmi A. Influence on metastatic spread of whole-body or local tumor hyperthermia. Eur J Cancer. 1976;12(6):455–463.
  • Thrall DE, Prescott DM, Samulski TV, et al. Radiation plus local hyperthermia versus radiation plus the combination of local and whole-body hyperthermia in canine sarcomas. Int J Radiat Oncol Biol Phys. 1996;34(5):1087–1096.
  • Vasanthan A, Mitsumori M, Park JH, et al. Regional hyperthermia combined with radiotherapy for uterine cervical cancers: a multi-institutional prospective randomized trial of the international atomic energy agency. Int J Radiat Oncol Biol Phys. 2005;61(1):145–153.
  • Franckena M, Stalpers LJ, Koper PC, et al. Long-term improvement in the treatment outcome after radiotherapy and hyperthermia in locoregionally advanced cervix cancer: an update of the Dutch Deep Hyperthermia Trial. Int J Radiat Oncol Biol Phys. 2008;70(4):1176–1182.
  • Toraya-Brown S, Sheen MR, Zhang P, et al. Local hyperthermia treatment of tumors induces CD8+ T cell-mediated resistance against distal and secondary tumors. Nanomedicine. 2014;10(6):1273–1285.
  • Hoopes PJ, Wagner RJ, Song A, et al. The effect of hypofractionated radiation and magnetic nanoparticle hyperthermia on tumor immunogenicity and overall treatment response. Proc SPIE Int Soc Opt Eng. 2017;10066:100660D1–100660D22.
  • Wang H, Zhang L, Shi Y, et al. Abscopal antitumor immune effects of magnet-mediated hyperthermia at a high therapeutic temperature on Walker-256 carcinosarcomas in rats. Oncol Lett. 2014;7(3):764–770.