Skip to content
2000
image of 
Research Progress on the Application of Ultrasound Assistance in Tumor Immunotherapy

Abstract

Recently, ultrasound (US)-assisted tumor immunotherapy has attracted widespread attention due to its deep penetration as well as its non-invasive and non-ionizing radiation properties. In this review, we briefly elucidated the mechanisms of anti-tumor immunotherapy assisted by the US. The contents include the following: the mechanical effects, thermal effects, and cavitation effects of US, sonodynamic therapy, US combined with programmed cell death protein 1 / programmed cell death 1 ligand 1 antibodies, US-enhanced chimeric antigen receptor T cell immunotherapy, cell pyroptosis and US, US combined with radiotherapy, US combined with glycolysis inhibition, and the use of various US-modulated signaling pathways to enhance tumor immunity. This review provides a broad overview of the mechanisms and roles of US assistance in tumor immunotherapy.

Loading

Article metrics loading...

/content/journals/cmc/10.2174/0109298673337725250108091641
2025-04-18
2025-12-22
Loading full text...

Full text loading...

References

  1. Bray F. Laversanne M. Sung H. Ferlay J. Siegel R.L. Soerjomataram I. Jemal A. Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2024 74 3 229 263 10.3322/caac.21834 38572751
    [Google Scholar]
  2. Xia C. Dong X. Li H. Cao M. Sun D. He S. Yang F. Yan X. Zhang S. Li N. Chen W. Cancer statistics in China and United States, 2022: Profiles, trends, and determinants. Chin. Med. J. (Engl.) 2022 135 5 584 590 10.1097/CM9.0000000000002108 35143424
    [Google Scholar]
  3. Dagher O.K. Schwab R.D. Brookens S.K. Posey A.D. Jr. Advances in cancer immunotherapies. Cell 2023 186 8 1814 1814.e1 10.1016/j.cell.2023.02.039 37059073
    [Google Scholar]
  4. Liu Y. Cheng X. Han X. Cheng X. Jiang S. Lin Y. Zhang Z. Lu L. Qu B. Chen Y. Zhang X. Global research landscape and trends of lung cancer immunotherapy: A bibliometric analysis. Front. Immunol. 2022 13 1032747 10.3389/fimmu.2022.1032747 36532038
    [Google Scholar]
  5. Sadighi Akha A.A. Aging and the immune system: An overview. J. Immunol. Methods 2018 463 21 26 10.1016/j.jim.2018.08.005 30114401
    [Google Scholar]
  6. Liu Y. Li C. Lu Y. Liu C. Yang W. Tumor microenvironment-mediated immune tolerance in development and treatment of gastric cancer. Front. Immunol. 2022 13 1016817 10.3389/fimmu.2022.1016817 36341377
    [Google Scholar]
  7. Bergholz J.S. Wang Q. Kabraji S. Zhao J.J. Integrating immunotherapy and targeted therapy in cancer treatment: Mechanistic insights and clinical implications. Clin. Cancer Res. 2020 26 21 5557 5566 10.1158/1078‑0432.CCR‑19‑2300 32576627
    [Google Scholar]
  8. Zhao L. Shi A. Yang Y. Liu Z. Hu X.Q. Shu L.Z. Tang Y. Zhang Z. Advances in molecular and cell therapy for immunotherapy of cholangiocarcinoma. Front. Oncol. 2023 13 1140103 10.3389/fonc.2023.1140103 37064120
    [Google Scholar]
  9. Yong T. Wei Z. Gan L. Yang X. Extracellular-vesicle-based drug delivery systems for enhanced antitumor therapies through modulating the cancer-immunity cycle. Adv. Mater. 2022 34 52 2201054 10.1002/adma.202201054 35726204
    [Google Scholar]
  10. Klein C. Brinkmann U. Reichert J.M. Kontermann R.E. The present and future of bispecific antibodies for cancer therapy. Nat. Rev. Drug Discov. 2024 23 4 301 319 10.1038/s41573‑024‑00896‑6 38448606
    [Google Scholar]
  11. Davern M. Lysaght J. Cooperation between chemotherapy and immunotherapy in gastroesophageal cancers. Cancer Lett. 2020 495 89 99 10.1016/j.canlet.2020.09.014 32950619
    [Google Scholar]
  12. Bommareddy P.K. Wakimoto H. Martuza R.L. Kaufman H.L. Rabkin S.D. Saha D. Oncolytic herpes simplex virus expressing IL-2 controls glioblastoma growth and improves survival. J. Immunother. Cancer 2024 12 4 e008880 10.1136/jitc‑2024‑008880 38599661
    [Google Scholar]
  13. Galluzzi L. Aryankalayil M.J. Coleman C.N. Formenti S.C. Emerging evidence for adapting radiotherapy to immunotherapy. Nat. Rev. Clin. Oncol. 2023 20 8 543 557 10.1038/s41571‑023‑00782‑x 37280366
    [Google Scholar]
  14. Qian H. Dong D. Fan P. Feng Y. Peng Y. Yao X. Wang R. Expression of KLRG1 on subpopulations of lymphocytes in the peripheral blood of patients with locally advanced nasopharyngeal carcinoma and prognostic analysis. Precis. Radiat. Oncol. 2022 6 3 199 208 10.1002/pro6.1165
    [Google Scholar]
  15. Sun W. Cheng Y. Ma X. Jin Z. Zhang Q. Wang G. Photodynamic therapy upregulates expression of HIF-1α and PD-L1 in related pathways and its clinical relevance in non-small-cell lung cancer. Eur. J. Med. Res. 2024 29 1 230 10.1186/s40001‑024‑01780‑0 38609977
    [Google Scholar]
  16. Yang J.K. Kwon H. Kim S. Recent advances in light-triggered cancer immunotherapy. J. Mater. Chem. B Mater. Biol. Med. 2024 12 11 2650 2669 10.1039/D3TB02842A 38353138
    [Google Scholar]
  17. Mušković M. Pokrajac R. Malatesti N. Combination of two photosensitisers in anticancer, antimicrobial and upconversion photodynamic therapy. Pharmaceuticals 2023 16 4 613 10.3390/ph16040613 37111370
    [Google Scholar]
  18. Iqbal M.F. Shafique M.A. Abdur Raqib M. Fadlalla Ahmad T.K. Haseeb A. Mhjoob A.M.A. Raja A. Histotripsy: An innovative approach for minimally invasive tumor and disease treatment. Ann. Med. Surg. (Lond.) 2024 86 4 2081 2087 10.1097/MS9.0000000000001897 38576932
    [Google Scholar]
  19. Qin D. Lei S. Zhang B. Liu Y. Tian J. Ji X. Yang H. Influence of interactions between bubbles on physico- chemical effects of acoustic cavitation. Ultrason. Sonochem. 2024 104 106808 10.1016/j.ultsonch.2024.106808 38377805
    [Google Scholar]
  20. Li J. Yue Z. Tang M. Wang W. Sun Y. Sun T. Chen C. Strategies to reverse hypoxic tumor microenvironment for enhanced sonodynamic therapy. Adv. Healthc. Mater. 2024 13 1 2302028 10.1002/adhm.202302028 37672732
    [Google Scholar]
  21. Hoogenboom M. Eikelenboom D. den Brok M.H. Heerschap A. Fütterer J.J. Adema G.J. Mechanical high-intensity focused ultrasound destruction of soft tissue: Working mechanisms and physiologic effects. Ultrasound Med. Biol. 2015 41 6 1500 1517 10.1016/j.ultrasmedbio.2015.02.006 25813532
    [Google Scholar]
  22. van den Bijgaart R.J.E. Eikelenboom D.C. Hoogenboom M. Fütterer J.J. den Brok M.H. Adema G.J. Thermal and mechanical high-intensity focused ultrasound: Perspectives on tumor ablation, immune effects and combination strategies. Cancer Immunol. Immunother. 2017 66 2 247 258 10.1007/s00262‑016‑1891‑9 27585790
    [Google Scholar]
  23. Wu F. Wang Z.B. Cao Y.D. Zhou Q. Zhang Y. Xu Z.L. Zhu X.Q. Expression of tumor antigens and heat-shock protein 70 in breast cancer cells after high-intensity focused ultrasound ablation. Ann. Surg. Oncol. 2007 14 3 1237 1242 10.1245/s10434‑006‑9275‑6 17187168
    [Google Scholar]
  24. Deng J. Zhang Y. Feng J. Wu F. Dendritic cells loaded with ultrasound-ablated tumour induce in vivo specific antitumour immune responses. Ultrasound Med. Biol. 2010 36 3 441 448 10.1016/j.ultrasmedbio.2009.12.004 20172447
    [Google Scholar]
  25. Lu P. Zhu X.Q. Xu Z.L. Zhou Q. Zhang J. Wu F. Increased infiltration of activated tumor-infiltrating lymphocytes after high intensity focused ultrasound ablation of human breast cancer. Surgery 2009 145 3 286 293 10.1016/j.surg.2008.10.010 19231581
    [Google Scholar]
  26. Zhang Y. Deng J. Feng J. Wu F. Enhancement of antitumor vaccine in ablated hepatocellular carcinoma by high- intensity focused ultrasound. World J. Gastroenterol. 2010 16 28 3584 3591 10.3748/wjg.v16.i28.3584 20653069
    [Google Scholar]
  27. Hu Z. Yang X.Y. Liu Y. Sankin G.N. Pua E.C. Morse M.A. Lyerly H.K. Clay T.M. Zhong P. Investigation of HIFU-induced anti-tumor immunity in a murine tumor model. J. Transl. Med. 2007 5 1 34 10.1186/1479‑5876‑5‑34 17625013
    [Google Scholar]
  28. Xing Y. Lu X. Pua E.C. Zhong P. The effect of high intensity focused ultrasound treatment on metastases in a murine melanoma model. Biochem. Biophys. Res. Commun. 2008 375 4 645 650 10.1016/j.bbrc.2008.08.072 18727919
    [Google Scholar]
  29. Dewhirst M.W. Lee C.T. Ashcraft K.A. The future of biology in driving the field of hyperthermia. Int. J. Hyperthermia 2016 32 1 4 13 10.3109/02656736.2015.1091093 26850697
    [Google Scholar]
  30. Cuenod C.A. Balvay D. Perfusion and vascular permeability: Basic concepts and measurement in DCE-CT and DCE-MRI. Diagn. Interv. Imaging 2013 94 12 1187 1204 10.1016/j.diii.2013.10.010 24211260
    [Google Scholar]
  31. Jackson C.M. Kochel C.M. Nirschl C.J. Durham N.M. Ruzevick J. Alme A. Francica B.J. Elias J. Daniels A. Dubensky T.W. Jr Lauer P. Brockstedt D.G. Baxi E.G. Calabresi P.A. Taube J.M. Pardo C.A. Brem H. Pardoll D.M. Lim M. Drake C.G. Systemic tolerance mediated by melanoma brain tumors is reversible by radiotherapy and vaccination. Clin. Cancer Res. 2016 22 5 1161 1172 10.1158/1078‑0432.CCR‑15‑1516 26490306
    [Google Scholar]
  32. Shin D.H. Melnick K.F. Tran D.D. Ghiaseddin A.P. In situ vaccination with laser interstitial thermal therapy augments immunotherapy in malignant gliomas. J. Neurooncol. 2021 151 1 85 92 10.1007/s11060‑020‑03557‑x 32757094
    [Google Scholar]
  33. Cirincione R. Di Maggio F.M. Forte G.I. Minafra L. Bravatà V. Castiglia L. Cavalieri V. Borasi G. Russo G. Lio D. Messa C. Gilardi M.C. Cammarata F.P. High-intensity focused ultrasound– and radiation therapy–induced immuno-modulation: Comparison and potential opportunities. Ultrasound Med. Biol. 2017 43 2 398 411 10.1016/j.ultrasmedbio.2016.09.020 27780661
    [Google Scholar]
  34. Ranjan A. Jacobs G.C. Woods D.L. Negussie A.H. Partanen A. Yarmolenko P.S. Gacchina C.E. Sharma K.V. Frenkel V. Wood B.J. Dreher M.R. Image-guided drug delivery with magnetic resonance guided high intensity focused ultrasound and temperature sensitive liposomes in a rabbit Vx2 tumor model. J. Control. Release 2012 158 3 487 494 10.1016/j.jconrel.2011.12.011 22210162
    [Google Scholar]
  35. Sheybani N.D. Witter A.R. Thim E.A. Yagita H. Bullock T.N.J. Price R.J. Combination of thermally ablative focused ultrasound with gemcitabine controls breast cancer via adaptive immunity. J. Immunother. Cancer 2020 8 2 e001008 10.1136/jitc‑2020‑001008 32819975
    [Google Scholar]
  36. Singh M. P. Sethuraman S. N. Ritchey J. Fiering S. Guha C. Malayer J. Ranjan A. In-situ vaccination using focused ultrasound heating and anti-CD-40 agonistic antibody enhances T-cell mediated local and abscopal effects in murine melanoma. Int J Hyperthermia. 2019 36 1 64 73 10.1080/02656736.2019
    [Google Scholar]
  37. Do H.D. Marie C. Bessoles S. Dhotel H. Seguin J. Larrat B. Doan B.T. Scherman D. Escriou V. Hacein-Bey-Abina S. Mignet N. Combination of thermal ablation by focused ultrasound, pFAR4-IL-12 transfection and lipidic adjuvant provide a distal immune response. Explor. Target. Antitumor Ther. 2022 3 6 398 413 [J]. 36046055
    [Google Scholar]
  38. Fite B.Z. Wang J. Kare A.J. Ilovitsh A. Chavez M. Ilovitsh T. Zhang N. Chen W. Robinson E. Zhang H. Kheirolomoom A. Silvestrini M.T. Ingham E.S. Mahakian L.M. Tam S.M. Davis R.R. Tepper C.G. Borowsky A.D. Ferrara K.W. Immune modulation resulting from MR-guided high intensity focused ultrasound in a model of murine breast cancer. Sci. Rep. 2021 11 1 927 10.1038/s41598‑020‑80135‑1 33441763
    [Google Scholar]
  39. Shen Z. Shao J. Zhang J. Qu W. Ultrasound cavitation enhanced chemotherapy: In vivo research and clinical application. Exp. Biol. Med. (Maywood) 2020 245 14 1200 1212 10.1177/1535370220936150 32567346
    [Google Scholar]
  40. Shen Z.Y. Xia G.L. Wu M.F. Ji L.Y. Li Y.J. The effects of percutaneous ethanol injection followed by 20-kHz ultrasound and microbubbles on rabbit hepatic tumors. J. Cancer Res. Clin. Oncol. 2016 142 2 373 378 10.1007/s00432‑015‑2034‑y 26306908
    [Google Scholar]
  41. Haskell S.C. Lu N. Stocker G.E. Xu Z. Sukovich J.R. Monitoring cavitation dynamics evolution in tissue mimicking hydrogels for repeated exposures via acoustic cavitation emissions. J. Acoust. Soc. Am. 2023 153 1 237 247 10.1121/10.0016849 36732269
    [Google Scholar]
  42. Wu H. Zheng H. Li Y. Ohl C.D. Yu H. Li D. Effects of surface tension on the dynamics of a single micro bubble near a rigid wall in an ultrasonic field. Ultrason. Sonochem. 2021 78 105735 10.1016/j.ultsonch.2021.105735 34479075
    [Google Scholar]
  43. Eichler M.J. Reul H.M. Mechanical heart valve cavitation: Valve specific parameters. Int. J. Artif. Organs 2004 27 10 855 867 10.1177/039139880402701007 15560680
    [Google Scholar]
  44. ShenZ. Y.JiangY.M.. ZhouY. F.SiH. F.WangL. High-speed photographic observation of the sonication of a rabbit carotid artery filled with microbubbles by 20-kHz low frequency ultrasound. Ultrason Sonochem. 2018 40 980 987
    [Google Scholar]
  45. Zahraie N. Haghighi H. Salehi F. Daneshvar F. Tamaddon P. Sattarahmady N. Pulsed sonodynamic therapy of melanoma cancer cells using nanoparticles of and mesoporous platinum. Ultrasound Med. Biol. 2023 49 9 2160 2168 10.1016/j.ultrasmedbio.2023.06.011 37414634
    [Google Scholar]
  46. Bismuth M. Eck M. Ilovitsh T. Nanobubble-mediated cancer cell sonoporation using low-frequency ultrasound. Nanoscale 2023 15 44 17899 17909 10.1039/D3NR03226D 37899700
    [Google Scholar]
  47. Cui L.W. Fan L.Y. Shen Z.Y. Application research progress of nanomaterial graphene and its derivative complexes in tumor diagnosis and therapy. Curr. Med. Chem. 2024 31 39 6436 6459 10.2174/0109298673251648231106112354 38299292
    [Google Scholar]
  48. Zhang Y. Fowlkes B. Liposomes-based nanoplatform enlarges ultrasound-related diagnostic and therapeutic precision. Curr. Med. Chem. 2022 29 8 1331 1341 10.2174/0929867328666210804092624 34348609
    [Google Scholar]
  49. Xu J. Solban N. Wang Y. Ferguson H. Perera S. Lin K. Cai M. Paul M. Schutt E.G. Larsen C.T. Li R. Saklatvala R. Long B.J. Ranganath S. Procopio A.T. Mittal S. Templeton A.C. Sonoporation-enhanced delivery of STING agonist induced robust immune modulation and tumor regression. Adv. Ther. (Weinh.) 2021 4 10 2100154 10.1002/adtp.202100154
    [Google Scholar]
  50. Kang S.T. Yeh C.K. Ultrasound microbubble contrast agents for diagnostic and therapeutic applications: Current status and future design. Chang Gung Med. J. 2012 35 2 125 139 [J]. 22537927
    [Google Scholar]
  51. Ho Y.J. Li J.P. Fan C.H. Liu H.L. Yeh C.K. Ultrasound in tumor immunotherapy: Current status and future developments. J. Control. Release 2020 323 12 23 10.1016/j.jconrel.2020.04.023 32302759
    [Google Scholar]
  52. Amate M. Goldgewicht J. Sellamuthu B. Stagg J. Yu F.T.H. The effect of ultrasound pulse length on microbubble cavitation induced antibody accumulation and distribution in a mouse model of breast cancer. Nanotheranostics 2020 4 4 256 269 10.7150/ntno.46892 33033688
    [Google Scholar]
  53. Li N. Tang J. Yang J. Zhu B. Wang X. Luo Y. Yang H. Jang F. Zou J. Liu Z. Wang Z. Tumor perfusion enhancement by ultrasound stimulated microbubbles potentiates PD-L1 blockade of MC38 colon cancer in mice. Cancer Lett. 2021 498 121 129 10.1016/j.canlet.2020.10.046 33129956
    [Google Scholar]
  54. Zhao P. Tian Y. Lu Y. Zhang J. Tao A. Xiang G. Liu Y. Biomimetic calcium carbonate nanoparticles delivered IL-12 mRNA for targeted glioblastoma sono-immunotherapy by ultrasound-induced necroptosis. J. Nanobiotechnology 2022 20 1 525 10.1186/s12951‑022‑01731‑z 36496387
    [Google Scholar]
  55. Dong Z. Feng L. Zhu W. Sun X. Gao M. Zhao H. Chao Y. Liu Z. CaCO3 nanoparticles as an ultra-sensitive tumor-pH-responsive nanoplatform enabling real-time drug release monitoring and cancer combination therapy. Biomaterials 2016 110 60 70 10.1016/j.biomaterials.2016.09.025 27710833
    [Google Scholar]
  56. Liao D. Huang J. Jiang C. Zhou L. Zheng M. Nezamzadeh-Ejhieh A. Qi N. Lu C. Liu J. A novel platform of MOF for sonodynamic therapy advanced therapies. Pharmaceutics 2023 15 8 2071 10.3390/pharmaceutics15082071 37631285
    [Google Scholar]
  57. Foglietta F. Canaparo R. Cossari S. Panzanelli P. Dosio F. Serpe L. Ultrasound triggers hypericin activation leading to multifaceted anticancer activity. Pharmaceutics 2022 14 5 1102 10.3390/pharmaceutics14051102 35631688
    [Google Scholar]
  58. Li M. Liu Y. Zhang Y. Yu N. Li J. Sono-activatable semiconducting polymer nanoreshapers multiply remodel tumor microenvironment for potent immunotherapy of orthotopic pancreatic cancer. Adv. Sci. (Weinh.) 2023 10 35 2305150 10.1002/advs.202305150 37870196
    [Google Scholar]
  59. Tang Q. Zhang F. Luo L. Duan Y. Zhu T. Ni Y. Wang Y. Qi H. Jiang S. Zhou J. Ma X. Zhang Y. Ultrasound-induced gold nanoparticle united with acoustic reprogramming of macrophages for enhanced cancer therapy. ACS Appl. Mater. Interfaces 2023 15 44 50926 50939 10.1021/acsami.3c12599 37877885
    [Google Scholar]
  60. Shi M. Zhang J. Wang Y. Han Y. Zhao X. Hu H. Qiao M. Chen D. Blockage of the IDO1 pathway by charge-switchable nanoparticles amplifies immunogenic cell death for enhanced cancer immunotherapy. Acta Biomater. 2022 150 353 366 10.1016/j.actbio.2022.07.022 35843594
    [Google Scholar]
  61. Yue W. Chen L. Yu L. Zhou B. Yin H. Ren W. Liu C. Guo L. Zhang Y. Sun L. Zhang K. Xu H. Chen Y. Checkpoint blockade and nanosonosensitizer-augmented noninvasive sonodynamic therapy combination reduces tumour growth and metastases in mice. Nat. Commun. 2019 10 1 2025 10.1038/s41467‑019‑09760‑3 31048681
    [Google Scholar]
  62. Nowak K.M. Schwartz M.R. Breza V.R. Price R.J. Sonodynamic therapy: Rapid progress and new opportunities for non-invasive tumor cell killing with sound. Cancer Lett. 2022 532 215592 10.1016/j.canlet.2022.215592 35151824
    [Google Scholar]
  63. Wang L. Li G. Cao L. Dong Y. Wang Y. Wang S. Li Y. Guo X. Zhang Y. Sun F. Du X. Su J. Li Q. Peng X. Shao K. Zhao W. An ultrasound-driven immune-boosting molecular machine for systemic tumor suppression. Sci. Adv. 2021 7 43 eabj4796 10.1126/sciadv.abj4796 34669472
    [Google Scholar]
  64. Wang T.W. Johmura Y. Suzuki N. Omori S. Migita T. Yamaguchi K. Hatakeyama S. Yamazaki S. Shimizu E. Imoto S. Furukawa Y. Yoshimura A. Nakanishi M. Blocking PD-L1–PD-1 improves senescence surveillance and ageing phenotypes. Nature 2022 611 7935 358 364 10.1038/s41586‑022‑05388‑4 36323784
    [Google Scholar]
  65. Dermani F.K. Samadi P. Rahmani G. Kohlan A.K. Najafi R. PD-1/PD-L1 immune checkpoint: Potential target for cancer therapy. J. Cell. Physiol. 2019 234 2 1313 1325 10.1002/jcp.27172 30191996
    [Google Scholar]
  66. Singh A. Mohan A. Dey A.B. Mitra D.K. Programmed death-1+ T cells inhibit effector T cells at the pathological site of miliary tuberculosis. Clin. Exp. Immunol. 2017 187 2 269 283 10.1111/cei.12871 27665733
    [Google Scholar]
  67. Iwai Y. Ishida M. Tanaka Y. Okazaki T. Honjo T. Minato N. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc. Natl. Acad. Sci. USA 2002 99 19 12293 12297 10.1073/pnas.192461099 12218188
    [Google Scholar]
  68. Jiang Y. Chen M. Nie H. Yuan Y. PD-1 and PD-L1 in cancer immunotherapy: Clinical implications and future considerations. Hum. Vaccin. Immunother. 2019 15 5 1111 1122 10.1080/21645515.2019.1571892 30888929
    [Google Scholar]
  69. Bie N. Yong T. Wei Z. Liang Q. Zhang X. Li S. Li X. Li J. Gan L. Yang X. Tumor-repopulating cell-derived microparticles elicit cascade amplification of chemotherapy-induced antitumor immunity to boost anti-PD-1 therapy. Signal Transduct. Target. Ther. 2023 8 1 408 10.1038/s41392‑023‑01658‑3 37875473
    [Google Scholar]
  70. Wei R. Guo L. Wang Q. Miao J. Kwok H.F. Lin Y. Targeting PD-L1 protein: Translation, modification and transport. Curr. Protein Pept. Sci. 2018 20 1 82 91 10.2174/1389203719666180928105632 30264678
    [Google Scholar]
  71. Xie W. Medeiros L.J. Li S. Yin C.C. Khoury J.D. Xu J. PD-1/PD-L1 pathway and its blockade in patients with classic hodgkin lymphoma and non-hodgkin large- cell lymphomas. Curr. Hematol. Malig. Rep. 2020 15 4 372 381 10.1007/s11899‑020‑00589‑y 32394185
    [Google Scholar]
  72. Schütz F. Stefanovic S. Mayer L. von Au A. Domschke C. Sohn C. PD-1/PD-L1 pathway in breast cancer. Oncol. Res. Treat. 2017 40 5 294 297 10.1159/000464353 28346916
    [Google Scholar]
  73. Liu W.N. So W.Y. Harden S.L. Fong S.Y. Wong M.X.Y. Tan W.W.S. Tan S.Y. Ong J.K.L. Rajarethinam R. Liu M. Cheng J.Y. Suteja L. Yeong J.P.S. Iyer N.G. Lim D.W.T. Chen Q. Successful targeting of PD-1/PD-L1 with chimeric antigen receptor-natural killer cells and nivolumab in a humanized mouse cancer model. Sci. Adv. 2022 8 47 eadd1187 10.1126/sciadv.add1187 36417514
    [Google Scholar]
  74. Zhang W. Shou W.D. Xu Y.J. Bai W.K. Hu B. Low-frequency ultrasound-induced VEGF suppression and synergy with dendritic cell-mediated anti-tumor immunity in murine prostate cancer cells in vitro. Sci. Rep. 2017 7 1 5778 10.1038/s41598‑017‑06242‑8 28720900
    [Google Scholar]
  75. Wu N. Cao Y. Liu Y. Zhou Y. He H. Tang R. Wan L. Wang C. Xiong X. Zhong L. Li P. Low-intensity focused ultrasound targeted microbubble destruction reduces tumor blood supply and sensitizes anti-PD-L1 immunotherapy. Front. Bioeng. Biotechnol. 2023 11 1173381 10.3389/fbioe.2023.1173381 37139047
    [Google Scholar]
  76. Chen Y. Luo X. Liu Y. Zou Y. Yang S. Liu C. Zhao Y. Targeted nanobubbles of PD-L1 mAb combined with doxorubicin as a synergistic tumor repressor in hepatocarcinoma. Int. J. Nanomedicine 2022 17 3989 4008 10.2147/IJN.S376172 36105615
    [Google Scholar]
  77. Zhao L. Zheng R. Liu L. Chen X. Guan R. Yang N. Chen A. Yu X. Cheng H. Li S. Self-delivery oxidative stress amplifier for chemotherapy sensitized immunotherapy. Biomaterials 2021 275 120970 10.1016/j.biomaterials.2021.120970 34146889
    [Google Scholar]
  78. Liu X. Zhou J. Wu H. Chen S. Zhang L. Tang W. Duan L. Wang Y. McCabe E. Hu M. Yu Z. Liu H. Choi C.H.J. Sung J.J. Huang L. Liu R. Cheng A.S. Fibrotic immune microenvironment remodeling mediates superior anti-tumor efficacy of a nano-PD-L1 trap in hepatocellular carcinoma. Mol. Ther. 2023 31 1 119 133 10.1016/j.ymthe.2022.09.012 36146933
    [Google Scholar]
  79. Li X. Khorsandi S. Wang Y. Santelli J. Huntoon K. Nguyen N. Yang M. Lee D. Lu Y. Gao R. Kim B.Y.S. de Gracia Lux C. Mattrey R.F. Jiang W. Lux J. Cancer immunotherapy based on image-guided STING activation by nucleotide nanocomplex-decorated ultrasound microbubbles. Nat. Nanotechnol. 2022 17 8 891 899 10.1038/s41565‑022‑01134‑z 35637356
    [Google Scholar]
  80. Yang Y. Wang N. Wang Z. Han M. Yan F. Shi Z. Feng S. Ultrasound-triggered O2 Bombs: Perfluorobromooctane-loaded defect-rich metal-organic framework for enhanced sono-immunotherapy. Chem. Eng. J. 2023 474 145764 10.1016/j.cej.2023.145764
    [Google Scholar]
  81. Pérez-Larios A. Rodríguez-Barajas N. Anaya-Esparza L.M. Villagrán-de la Mora Z. Sánchez-Burgos J.A. Review of therapies using TiO2 nanomaterials for increased anticancer capability. Anticancer. Agents Med. Chem. 2022 22 12 2241 2254 10.2174/1871520622666211228112631 34963437
    [Google Scholar]
  82. Ivask A. Titma T. Visnapuu M. Vija H. Kakinen A. Sihtmae M. Pokhrel S. Madler L. Heinlaan M. Kisand V. Shimmo R. Kahru A. Toxicity of 11 metal oxide nanoparticles to three mammalian cell types in vitro. Curr. Top. Med. Chem. 2015 15 18 1914 1929 10.2174/1568026615666150506150109 25961521
    [Google Scholar]
  83. Lee H. Han J. Shin H. Han H. Na K. Kim H. Combination of chemotherapy and photodynamic therapy for cancer treatment with sonoporation effects. J. Control. Release 2018 283 190 199 10.1016/j.jconrel.2018.06.008 29885415
    [Google Scholar]
  84. Jo J. Kim J.Y. Yun J.J. Lee Y.J. Jeong Y.I.L. β-Cyclodextrin nanophotosensitizers for redox-sensitive delivery of chlorin e6. Molecules 2023 28 21 7398 10.3390/molecules28217398 37959817
    [Google Scholar]
  85. Fridman W.H. Remark R. Goc J. Giraldo N.A. Becht E. Hammond S.A. Damotte D. Dieu-Nosjean M.C. Sautès-Fridman C. The immune microenvironment: A major player in human cancers. Int. Arch. Allergy Immunol. 2014 164 1 13 26 10.1159/000362332 24852691
    [Google Scholar]
  86. Lin X. Huang R. Huang Y. Wang K. Li H. Bao Y. Wu C. Zhang Y. Tian X. Wang X. Nanosonosensitizer-augmented sonodynamic therapy combined with checkpoint blockade for cancer immunotherapy. Int. J. Nanomedicine 2021 16 1889 1899 10.2147/IJN.S290796 33707944
    [Google Scholar]
  87. Zhang N. Foiret J. Kheirolomoom A. Liu P. Feng Y. Tumbale S. Raie M. Wu B. Wang J. Fite B.Z. Dai Z. Ferrara K.W. Optimization of microbubble-based DNA vaccination with low-frequency ultrasound for enhanced cancer immunotherapy. Adv. Ther. (Weinh.) 2021 4 9 2100033 10.1002/adtp.202100033 34632048
    [Google Scholar]
  88. Ya Z. Guo S. Li Y. Zhu M. Zhang L. Zong Y. Wan M. Focused acoustic vortex-mediated sonochemotherapy for the amplification of immunogenic cell death combined with checkpoint blockade to potentiate cancer immunotherapy. Biomaterials 2023 301 122278 10.1016/j.biomaterials.2023.122278 37598439
    [Google Scholar]
  89. Wu P. Ya Z. Li Y. Zhu M. Zhang L. Zong Y. Guo S. Wan M. Focused acoustic vortex-regulated composite nanodroplets combined with checkpoint blockade for high-performance tumor synergistic therapy. ACS Appl. Mater. Interfaces 2022 14 27 30466 30479 10.1021/acsami.2c02137 35699948
    [Google Scholar]
  90. Johnson P.C. Abramson J.S. Engineered T. Engineered T cells: CAR T cell therapy and beyond. Curr. Oncol. Rep. 2022 24 1 23 31 10.1007/s11912‑021‑01161‑4 35059997
    [Google Scholar]
  91. Singh S. Khasbage S. Kaur R.J. Sidhu J.K. Bhandari B. Chimeric antigen receptor T cell. Indian J. Pharmacol. 2022 54 3 226 233 10.4103/ijp.ijp_531_20 35848695
    [Google Scholar]
  92. Wu Y. Liu Y. Huang Z. Wang X. Jin Z. Li J. Limsakul P. Zhu L. Allen M. Pan Y. Bussell R. Jacobson A. Liu T. Chien S. Wang Y. Control of the activity of CAR-T cells within tumours via focused ultrasound. Nat. Biomed. Eng. 2021 5 11 1336 1347 10.1038/s41551‑021‑00779‑w 34385696
    [Google Scholar]
  93. Vasudevan S.O. Behl B. Rathinam V.A. Pyroptosis-induced inflammation and tissue damage. Semin. Immunol. 2023 69 101781 10.1016/j.smim.2023.101781 37352727
    [Google Scholar]
  94. Chen B. Yan Y. Yang Y. Cao G. Wang X. Wang Y. Wan F. Yin Q. Wang Z. Li Y. Wang L. Xu B. You F. Zhang Q. Wang Y. A pyroptosis nanotuner for cancer therapy. Nat. Nanotechnol. 2022 17 7 788 798 10.1038/s41565‑022‑01125‑0 35606443
    [Google Scholar]
  95. Ding J. Wang K. Liu W. She Y. Sun Q. Shi J. Sun H. Wang D.C. Shao F. Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 2016 535 7610 111 116 10.1038/nature18590 27281216
    [Google Scholar]
  96. Slaufova M. Karakaya T. Di Filippo M. Hennig P. Beer H.D. The gasdermins: A pore-forming protein family expressed in the epidermis. Front. Immunol. 2023 14 1254150 10.3389/fimmu.2023.1254150 37771587
    [Google Scholar]
  97. Bao Y. Ge Y. Wu M. Mao Z. Ye J. Tong W. Record-high ultrasound-sensitive NO nanogenerators for cascade tumor pyroptosis and immunotherapy. Adv. Sci. (Weinh.) 2023 10 26 2302278 10.1002/advs.202302278 37400368
    [Google Scholar]
  98. Karki R. Sharma B.R. Tuladhar S. Williams E.P. Zalduondo L. Samir P. Zheng M. Sundaram B. Banoth B. Malireddi R.K.S. Schreiner P. Neale G. Vogel P. Webby R. Jonsson C.B. Kanneganti T.D. Synergism of TNF-α and IFN-γ triggers inflammatory cell death, tissue damage, and mortality in SARS-CoV-2 infection and cytokine shock syndromes. Cell 2021 184 1 149 168.e17 10.1016/j.cell.2020.11.025 33278357
    [Google Scholar]
  99. Dubyak G.R. Miller B.A. Pearlman E. Pyroptosis in neutrophils: Multimodal integration of inflammasome and regulated cell death signaling pathways. Immunol. Rev. 2023 314 1 229 249 10.1111/imr.13186 36656082
    [Google Scholar]
  100. Chen Z. Liu W. Yang Z. Luo Y. Qiao C. Xie A. Jia Q. Yang P. Wang Z. Zhang R. Sonodynamic-immunomodulatory nanostimulators activate pyroptosis and remodel tumor microenvironment for enhanced tumor immunotherapy. Theranostics 2023 13 5 1571 1583 10.7150/thno.79945 37056565
    [Google Scholar]
  101. Meng K. Lu H. Clinical application of high-LET radiotherapy combined with immunotherapy in malignant tumors. Precis. Radiat. Oncol. 2024 8 1 42 46 10.1002/pro6.1225
    [Google Scholar]
  102. Yao Y. Yao N. Qin Z. Ma J. Lu J. Cui L. Qu W. Yuan S. Tong S. Li N. Li H. Extensive-stage small cell lung cancer: Is prophylactic cranial irradiation necessary in the era of immunotherapy with MRI surveillance? Precis. Radiat. Oncol. 2023 7 2 111 117 10.1002/pro6.1200
    [Google Scholar]
  103. Bandyopadhyay S. Quinn T.J. Scandiuzzi L. Basu I. Partanen A. Tomé W.A. Macian F. Guha C. Low-intensity focused ultrasound induces reversal of tumor-induced T cell tolerance and prevents immune escape. J. Immunol. 2016 196 4 1964 1976 10.4049/jimmunol.1500541 26755821
    [Google Scholar]
  104. Qiao K. Luo C. Huang R. Xiang J. Pan Y. Zhang S. Jiang C. Ding S. Yang H. Huang Y. Ning S. Ultrasound triggered tumor metabolism suppressor induces tumor starvation for enhanced sonodynamic immunotherapy of breast cancer. Int. J. Nanomedicine 2023 18 3801 3811 10.2147/IJN.S413543 37457803
    [Google Scholar]
  105. Sha M. Li H. Liu Y. Tang C. Bai X. Wang Y. Yuan B. Liu K. Gao X. Yan J. Wei S. Chang J. Kang J. Mn-CaCO3-based nanosystem for augmented sonodynamic-chemodynamic immunotherapy via PI3K/Akt signaling pathway. Chem. Eng. J. 2024 484 149450 10.1016/j.cej.2024.149450
    [Google Scholar]
  106. Li Y. Li M. Zheng J. Ma Z. Yu T. Zhu Y. Li P. Nie F. Ultrasound-responsive nanocarriers delivering siRNA and Fe3O4 nanoparticles reprogram macrophages and inhibit M2 polarization for enhanced NSCLC immunotherapy. ACS Appl. Mater. Interfaces 2024 16 42 56634 56652 10.1021/acsami.4c10036 39378273
    [Google Scholar]
  107. Wang C. Zhang R. He J. Yu L. Li X. Zhang J. Li S. Zhang C. Kagan J.C. Karp J.M. Kuai R. Ultrasound-responsive low-dose doxorubicin liposomes trigger mitochondrial DNA release and activate cGAS-STING-mediated antitumour immunity. Nat. Commun. 2023 14 1 3877 10.1038/s41467‑023‑39607‑x 37391428
    [Google Scholar]
  108. Tan Y. Yang S. Ma Y. Li J. Xie Q. Liu C. Zhao Y. Nanobubbles containing sPD-1 and Ce6 mediate combination immunotherapy and suppress hepatocellular carcinoma in mice. Int. J. Nanomedicine 2021 16 3241 3254 10.2147/IJN.S305857 34007176
    [Google Scholar]
  109. Doroshow D.B. Bhalla S. Beasley M.B. Sholl L.M. Kerr K.M. Gnjatic S. Wistuba I.I. Rimm D.L. Tsao M.S. Hirsch F.R. PD-L1 as a biomarker of response to immune-checkpoint inhibitors. Nat. Rev. Clin. Oncol. 2021 18 6 345 362 10.1038/s41571‑021‑00473‑5 33580222
    [Google Scholar]
  110. To K.K.W. Cho W.C. Drug repurposing to circumvent immune checkpoint inhibitor resistance in cancer immunotherapy. Pharmaceutics 2023 15 8 2166 10.3390/pharmaceutics15082166 37631380
    [Google Scholar]
  111. Liu Y.T. Sun Z.J. Turning cold tumors into hot tumors by improving T-cell infiltration. Theranostics 2021 11 11 5365 5386 10.7150/thno.58390 33859752
    [Google Scholar]
  112. Wei C. Ma Y. Wang F. Liao Y. Chen Y. Zhao B. Zhao Q. Wang D. Tang D. Igniting hope for tumor immunotherapy: Promoting the “Hot and Cold” tumor transition. Clin. Med. Insights Oncol. 2022 16 11795549221120708 10.1177/11795549221120708 36147198
    [Google Scholar]
/content/journals/cmc/10.2174/0109298673337725250108091641
Loading
/content/journals/cmc/10.2174/0109298673337725250108091641
Loading

Data & Media loading...


  • Article Type:
    Review Article
Keywords: immunity ; tumor ; chimeric antigen receptor ; PD-1 ; sonodynamic therapy ; Ultrasound
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error
Please enter a valid_number test