دورية أكاديمية

Nanotechnology-augmented sonodynamic therapy and associated immune-mediated effects for the treatment of pancreatic ductal adenocarcinoma.

التفاصيل البيبلوغرافية
العنوان: Nanotechnology-augmented sonodynamic therapy and associated immune-mediated effects for the treatment of pancreatic ductal adenocarcinoma.
المؤلفون: Hadi MM; Division of Surgery and Interventional Science, Faculty of Medical Sciences, University College London, London, UK., Farrell S; Biomedical Sciences Research Institute, Ulster University, Coleraine, UK., Nesbitt H; Biomedical Sciences Research Institute, Ulster University, Coleraine, UK., Thomas K; Biomedical Sciences Research Institute, Ulster University, Coleraine, UK., Kubajewska I; Division of Surgery and Interventional Science, Faculty of Medical Sciences, University College London, London, UK.; Nanomerics Ltd, London, UK., Ng A; Division of Surgery and Interventional Science, Faculty of Medical Sciences, University College London, London, UK., Masood H; Division of Surgery and Interventional Science, Faculty of Medical Sciences, University College London, London, UK., Patel S; Division of Surgery and Interventional Science, Faculty of Medical Sciences, University College London, London, UK., Sciscione F; Division of Surgery and Interventional Science, Faculty of Medical Sciences, University College London, London, UK., Davidson B; Division of Surgery and Interventional Science, Faculty of Medical Sciences, University College London, London, UK., Callan JF; Biomedical Sciences Research Institute, Ulster University, Coleraine, UK., MacRobert AJ; Division of Surgery and Interventional Science, Faculty of Medical Sciences, University College London, London, UK., McHale AP; Biomedical Sciences Research Institute, Ulster University, Coleraine, UK., Nomikou N; Division of Surgery and Interventional Science, Faculty of Medical Sciences, University College London, London, UK. n.nomikou@ucl.ac.uk.
المصدر: Journal of cancer research and clinical oncology [J Cancer Res Clin Oncol] 2023 Jul; Vol. 149 (8), pp. 5007-5023. Date of Electronic Publication: 2022 Nov 02.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Springer-Verlag Country of Publication: Germany NLM ID: 7902060 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1432-1335 (Electronic) Linking ISSN: 01715216 NLM ISO Abbreviation: J Cancer Res Clin Oncol Subsets: MEDLINE
أسماء مطبوعة: Original Publication: Berlin ; New York : Springer-Verlag.
مواضيع طبية MeSH: Ultrasonic Therapy*/methods , Pancreatic Neoplasms*/therapy , Carcinoma, Pancreatic Ductal*/therapy, Animals ; Mice ; Cathepsin B ; Tissue Distribution ; Hematoporphyrins/pharmacology ; Nanotechnology ; Cell Line, Tumor ; Reactive Oxygen Species ; Pancreatic Neoplasms
مستخلص: Purpose: Sonodynamic therapy (SDT) is emerging as a cancer treatment alternative with significant advantages over conventional therapies, including its minimally invasive and site-specific nature, its radical antitumour efficacy with minimal side effects, and its capacity to raise an antitumour immune response. The study explores the efficacy of SDT in combination with nanotechnology against pancreatic ductal adenocarcinoma.
Methods: A nanoparticulate formulation (HPNP) based on a cathepsin B-degradable glutamate-tyrosine co-polymer that carries hematoporphyrin was used in this study for the SDT-based treatment of PDAC. Cathepsin B levels in BxPC-3 and PANC-1 cells were correlated to cellular uptake of HPNP. The HPNP efficiency to induce a sonodynamic effect at varying ultrasound parameters, and at different oxygenation and pH conditions, was investigated. The biodistribution, tumour accumulation profile, and antitumour efficacy of HPNP in SDT were examined in immunocompetent mice carrying bilateral ectopic murine pancreatic tumours. The immune response profile of excised tumour tissues was also examined.
Results: The HPNP formulation significantly improved cellular uptake of hematoporphyrin for both BxPC-3 and PANC-1 cells, while increase of cellular uptake was positively correlated in PANC-1 cells. There was a clear SDT-induced cytotoxicity at the ultrasound conditions tested, and the treatment impaired the capacity of both BxPC-3 and PANC-1 cells to form colonies. The overall acoustic energy and pulse length, rather than the power density, were key in eliciting the effects observed in vitro. The SDT treatment in combination with HPNP resulted in 21% and 27% reduction of the target and off-target tumour volumes, respectively, within 24 h. A single SDT treatment elicited an antitumour effect that was characterized by an SDT-induced decrease in immunosuppressive T cell phenotypes.
Conclusion: SDT has significant potential to serve as a monotherapy or adjunctive treatment for inoperable or borderline resectable PDAC.
(© 2022. The Author(s).)
التعليقات: Erratum in: J Cancer Res Clin Oncol. 2023 Mar 22;:. (PMID: 36947238)
References: Blando J, Sharma A, Higa MG (2019) Comparison of immune infiltrates in melanoma and pancreatic cancer highlights vista as a potential target in pancreatic cancer. Proc Natl Acad Sci USA 116:1692–1697. (PMID: 10.1073/pnas.1811067116306354256358697)
Cavallo-Medved D, Dosescu J, Linebaugh BE, Sameni M, Rudy D, Sloane BF (2003) Mutant K-ras regulates cathepsin B localization on the surface of human colorectal carcinoma cells. Neoplasia 5:507–519. (PMID: 10.1016/S1476-5586(03)80035-0149654441502576)
Churlaud G, Pitoiset F, Jebbawi F, Lorenzon R, Bellier B, Rosenzwajg M, Klatzmann D (2015) Human and mouse CD8(+)CD25(+)FOXP3(+) regulatory T cells at steady state and during interleukin-2 therapy. Front Immunol 6:171. (PMID: 10.3389/fimmu.2015.00171259268354397865)
Civale J, Bamber J, Rivens I, ter Haar G (2006) Optimising HIFU lesion formation with backscatter attenuation estimation (BAE). AIP Conf Proc 829:176. (PMID: 10.1063/1.2205461)
Dai Z, Zhang S, Xie Q, Wu S, Su J, Li S, Xu Y, Li XC (2014) Natural CD8 + CD122 + T cells are more potent in suppression of allograft rejection than CD4 + CD25 + regulatory T cells. Am J Transpl 14:39–48. (PMID: 10.1111/ajt.12515)
Das M, Shen L, Liu Q, Goodwin TJ, Huang L (2019) Nanoparticle delivery of RIG-I agonist enables effective and safe adjuvant therapy in pancreatic cancer. Mol Ther 27:507–517. (PMID: 10.1016/j.ymthe.2018.11.01230545600)
Du YX, Liu ZW, You L, Wu WM, Zhao YP (2016) Advances in understanding the molecular mechanism of pancreatic cancer metastasis. Hepatobil Pancreat Dis Int 15:361–370. (PMID: 10.1016/S1499-3872(15)60033-9)
Facciabene A, Motz GT, Coukos G (2012) T-regulatory cells: key players in tumor immune escape and angiogenesis. Cancer Res 72:2162–2171. (PMID: 10.1158/0008-5472.CAN-11-3687225499463342842)
Gao Z, Zheng J, Yang B (2013) Sonodynamic therapy inhibits angiogenesis and tumor growth in a xenograft mouse model. Cancer Lett 335:93–99. (PMID: 10.1016/j.canlet.2013.02.00623402818)
Gardner A, Ruffell B (2016) Dendritic cells and cancer immunity. Trends Immunol 37:855–865. (PMID: 10.1016/j.it.2016.09.006277935695135568)
Giovannetti E, van der Borden CL, Frampton AE, Ali A, Firuzi O, Peters GJ (2017) Never let it go: stopping key mechanisms underlying metastasis to fight pancreatic cancer. Semin Cancer Biol 44:43–59. (PMID: 10.1016/j.semcancer.2017.04.00628438662)
Göbl R, Virga S, Rackerseder J, Frisch B, Navab N, Hennersperger C (2017) Acoustic window planning for ultrasound acquisition. Int J Comput Assist Radiol Surg 12:993–1001. (PMID: 10.1007/s11548-017-1551-3282853395447334)
Guillaumond F, Leca J, Olivares O, Lavaut MN, Vidal N, Berthezene P, Dusetti NJ, Loncle C, Calvo E, Turrini O, Iovanna JL, Tomasini R, Vasseur S (2013) Strengthened glycolysis under hypoxia supports tumor symbiosis and hexosamine biosynthesis in pancreatic adenocarcinoma. PNAS 110:3919–3924. (PMID: 10.1073/pnas.1219555110234071653593894)
Guo C, Zhao Y (2021) Autophagy in pancreatic cancer. J Mol Cell Biol 13:786–790. (PMID: 10.1093/jmcb/mjab0538782586)
Hadi MM, Nesbitt H, Masood H, Sciscione F, Patel S, Ramesh BS, Emberton M, Callan JF, MacRobert A, McHale AP, Nomikou N (2021) Investigating the performance of a novel pH and cathepsin B sensitive, stimulus-responsive nanoparticle for optimised sonodynamic therapy in prostate cancer. J Control Rel 329:76–86. (PMID: 10.1016/j.jconrel.2020.11.040)
Inui T, Makita K, Miura H, Matsuda A, Kuchiike D, Kubo K, Mette M, Uto Y, Nishikata T, Hori H, Sakamoto N (2014) Case report: a breast cancer patient treated with GcMAF, sonodynamic therapy and hormone therapy. Anticancer Res 34:4589–4593. (PMID: 25075104)
Lakens D (2013) Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t-tests and ANOVAs. Front Psychol 4:863. (PMID: 10.3389/fpsyg.2013.00863243244493840331)
Liu Y, Zheng P (2020) Preserving the CTLA-4 checkpoint for safer and more effective cancer immunotherapy. Trends Pharmacol Sci 41:4–12. (PMID: 10.1016/j.tips.2019.11.00331836191)
McHale AP, Callan JF, Nomikou N, Fowley C, Callan B (2016) Sonodynamic therapy: concept, mechanism and application to cancer treatment. Adv Exp Med Biol 880:429–450. (PMID: 10.1007/978-3-319-22536-4_2226486350)
Nesbitt H, Logan K, Thomas K, Callan B, Gao J, McKaig T, Taylor M, Love M, Stride E, McHale AP, Callan JF (2021) Sonodynamic therapy complements PD-L1 immune checkpoint inhibition in a murine model of pancreatic cancer. Cancer Lett 517:88–95. (PMID: 10.1016/j.canlet.2021.06.00334119606)
Nicholas D, Nesbitt H, Farrell S, Logan K, McMullin E, Gillan T, Kelly P, O’Rourke D, Porter S, Thomas K, O’Hagan BMG, Nomikou N, Callan B, Callan JF, McHale AP (2021) Exploiting a rose bengal-bearing, oxygen-producing nanoparticle for SDT and associated immune-mediated therapeutic effects in the treatment of pancreatic cancer. Eur J Pharm Biopharm 163:49–59. (PMID: 10.1016/j.ejpb.2021.03.00533798727)
Niknafs N, Zhong Y, Moral JA, Zhang L, Shao MX, Lo A, Makohon-Moore A, Lacobuzio-Donahue CA, Karchin R (2019) Characterization of genetic subclonal evolution in pancreatic cancer mouse models. Nat Commun 10:5435. (PMID: 10.1038/s41467-019-13100-w317807496882784)
Nomikou N, Curtis K, McEwan C, O’Hagan BMG, Callan B, Callan JF, McHale AP (2017) A versatile, stimulus-responsive nanoparticle-based platform for use in both sonodynamic and photodynamic cancer therapy. Acta Biomater 49:414–421. (PMID: 10.1016/j.actbio.2016.11.03127856283)
Ohue Y, Nishikawa H (2019) Regulatory T (Treg) cells in cancer: can Treg cells be a new therapeutic target? Cancer Sci 110:2080–2089. (PMID: 10.1111/cas.14069311024286609813)
Peng Y, Jia L, Wang S, Cao W, Zheng J (2018) Sonodynamic therapy improves antitumor immune effect by increasing the infiltration of CD8 + T cells and altering tumor blood vessels in murine B16F10 melanoma xenograft. Oncol Rep 40:2163–2170. (PMID: 30106435)
Pham TND, Shields MA, Spaulding C, Principe DR, Li B, Underwood PW, Trevino JG, Bentrem DJ, Munshi HG (2021) Preclinical models of pancreatic ductal adenocarcinoma and their utility in immunotherapy studies. Cancers 13:440. (PMID: 10.3390/cancers13030440335038327865443)
Seth A, Heo MB, Sung MH, Lim YT (2015) Infection-mimicking poly(γ-glutamic acid) as adjuvant material for effective anti-tumor immune response. Int J Biol Macromol 75:495–504. (PMID: 10.1016/j.ijbiomac.2015.02.01325709015)
Soltani M, Souri M, Kashkooli MF (2021) Effects of hypoxia and nanocarrier size on pH-responsive nano-delivery system to solid tumors. Sci Rep 11:19350. (PMID: 10.1038/s41598-021-98638-w345885048481507)
Tao J, Yang G, Zhou W, Qui J, Chen G, Luo W, Zhao F, You L, Zheng L, Zhang T, Zhao Y (2021) Targeting hypoxic tumor microenvironment in pancreatic cancer. J Hematol Oncol 14:14. (PMID: 10.1186/s13045-020-01030-w334360447805044)
Thomas RG, Surendran SP, Jeong YY (2020) Tumor microenvironment-stimuli responsive nanoparticles for anticancer therapy. Front Mol Biosci 7:610533. (PMID: 10.3389/fmolb.2020.610533333922647775573)
Vieyra-Lobato MR, Vela-Ojeda J, Montiel-Cervantes L, Lopez-Santiago R, Moreno-Lafont MC (2018) Description of CD8( + ) regulatory T lymphocytes and their specific intervention in graft-versus-host and infectious diseases, autoimmunity, and cancer. J Immunol Res 2018:3758713. (PMID: 10.1155/2018/3758713301554936098849)
Wang X, Zhang W, Xu Z, Luo Y, Mitchell D, Moss RW (2009) Sonodynamic and photodynamic therapy in advanced breast carcinoma: a report of 3 cases. Integr Cancer Ther 8:283–287. (PMID: 10.1177/153473540934369319815599)
Weber JS (2008) Tumor evasion may occur via expression of regulatory molecules: a case for CTLA-4 in melanoma. J Invest Dermatol 128:2750–2752. (PMID: 10.1038/jid.2008.34118997841)
Yu Y, Ma X, Gong R, Zhu J, Wei L, Yao J (2018) Recent advances in CD8( + ) regulatory T cell research. Oncol Lett 15:8187–8194. (PMID: 298055535950136)
Yue W, Chen L, Yu L, Zhou B, Yin H, Ren W, Liu C, Guo L, Zhang Y, Sun L, Zhang K, Huixiong X, Chen Y (2019) Checkpoint blockade and nanosonosensitizer-augmented noninvasive sonodynamic therapy combination reduces tumour growth and metastases in mice. Nat Commun 10:2025. (PMID: 10.1038/s41467-019-09760-3310486816497709)
Zhang Z, Ji S, Zhang B, Liu J, Qin Y, Xu J, Yu X (2018) Role of angiogenesis in pancreatic cancer biology and therapy. Biomed Pharmacother 108:1135–1140. (PMID: 10.1016/j.biopha.2018.09.13630372814)
Zhang Q, Bao C, Cai X, Jin L, Sun L, Lang Y, Li L (2018) Sonodynamic therapy-assisted immunotherapy: A novel modality for cancer treatment. Cancer Sci 109:1330–1345. (PMID: 10.1111/cas.13578295752975980136)
معلومات مُعتمدة: United Kingdom WT_ Wellcome Trust; MC_PC_17180 United Kingdom MRC_ Medical Research Council
فهرسة مساهمة: Keywords: Anticancer immune response; Cathepsin B; Hematoporphyrin; Nanoparticles; Pancreatic cancer; Sonodynamic therapy
المشرفين على المادة: EC 3.4.22.1 (Cathepsin B)
0 (Hematoporphyrins)
0 (Reactive Oxygen Species)
تواريخ الأحداث: Date Created: 20221102 Date Completed: 20230719 Latest Revision: 20231213
رمز التحديث: 20240628
مُعرف محوري في PubMed: PMC10349707
DOI: 10.1007/s00432-022-04418-y
PMID: 36319895
قاعدة البيانات: MEDLINE