Enhanced chemoimmunotherapy of breast cancer in mice by apolipoprotein A1-modified doxorubicin liposomes combined with interleukin-21

References

• Cancer.org [Internet]. Atlanta (GA): ACS; [cited 2021 Feb 4]. Available from: https://www.cancer.org/
   Google Scholar
• Cao W, Chen HD, Yu YW, et al. Changing profiles of cancer burden worldwide and in China: a secondary analysis of the global cancer statistics 2020. Chin Med J. 2021;134(7):783–791. doi: 10.1097/CM9.0000000000001474.
   PubMed Web of Science ®Google Scholar
• Lebert JM, Lester R, Powell E, et al. Advances in the systemic treatment of triple-negative breast cancer. Curr Oncol. 2018;25(Suppl 1):S142–S150. doi: 10.3747/co.25.3954.
   PubMed Web of Science ®Google Scholar
• Al-Mahmood S, Sapiezynski J, Garbuzenko OB, et al. Metastatic and triple-negative breast cancer: challenges and treatment options. Drug Deliv Transl Res. 2018;8(5):1483–1507. doi: 10.1007/s13346-018-0551-3.
   PubMed Web of Science ®Google Scholar
• Nedeljković M, Damjanović A. Mechanisms of chemotherapy resistance in triple-negative breast cancer-how we can rise to the challenge. Cells. 2019;8(9):957. doi: 10.3390/cells8090957.
   PubMed Web of Science ®Google Scholar
• Hwang SY, Park S, Kwon Y. Recent therapeutic trends and promising targets in triple negative breast cancer. Pharmacol Ther. 2019;199:30–57. doi: 10.1016/j.pharmthera.2019.02.006.
   PubMed Web of Science ®Google Scholar
• Xu Y, Xiong J, Sun X, et al. Targeted nanomedicines remodeling immunosuppressive tumor microenvironment for enhanced cancer immunotherapy. Acta Pharm Sin B. 2022;12(12):4327–4347. doi: 10.1016/j.apsb.2022.11.001.
   PubMed Web of Science ®Google Scholar
• Cochran BJ, Ong KL, Manandhar B, et al. APOA1: a protein with multiple therapeutic functions. Curr Atheroscler Rep. 2021;23(3):11. doi: 10.1007/s11883-021-00906-7.
   PubMed Web of Science ®Google Scholar
• Zhang F, Wang X, Xu X, et al. Reconstituted high density lipoprotein mediated targeted co-delivery of HZ08 and paclitaxel enhances the efficacy of paclitaxel in multidrug-resistant MCF-7 breast cancer cells. Eur J Pharm Sci. 2016;92:11–21. doi: 10.1016/j.ejps.2016.06.017.
   PubMed Web of Science ®Google Scholar
• Li J, Han M, Li J, et al. Sterically stabilized recombined HDL composed of modified apolipoprotein A-I for efficient targeting toward glioma cells. Drug Deliv. 2020;27(1):530–541. doi: 10.1080/10717544.2020.1745330.
   PubMed Web of Science ®Google Scholar
• Mooberry LK, Sabnis NA, Panchoo M, et al. Targeting the SR-B1 receptor as a gateway for cancer therapy and imaging. Front Pharmacol. 2016;7:466. doi: 10.3389/fphar.2016.00466.
   PubMed Web of Science ®Google Scholar
• Kajani S, Curley S, McGillicuddy FC. Unravelling HDL-Looking beyond the cholesterol surface to the quality Within. Int J Mol Sci. 2018;19(7):1971. doi: 10.3390/ijms19071971.
   PubMed Web of Science ®Google Scholar
• An D, Yu X, Jiang L, et al. Reversal of multidrug resistance by apolipoprotein A1-modified doxorubicin liposome for breast cancer treatment. Molecules. 2021;26(5):1280. doi: 10.3390/molecules26051280.
   PubMed Web of Science ®Google Scholar
• Singh S, Numan A, Maddiboyina B, et al. The emerging role of immune checkpoint inhibitors in the treatment of triple-negative breast cancer. Drug Discov Today. 2021;26(7):1721–1727. doi: 10.1016/j.drudis.2021.03.011.
   PubMed Web of Science ®Google Scholar
• Shi T, Ma Y, Yu L, et al. Cancer immunotherapy: a focus on the regulation of immune checkpoints. Int J Mol Sci. 2018;19(5):1389. doi: 10.3390/ijms19051389.
   Web of Science ®Google Scholar
• Sathyanarayanan V, Neelapu SS. Cancer immunotherapy: strategies for personalization and combinatorial approaches. Mol Oncol. 2015;9(10):2043–2053. doi: 10.1016/j.molonc.2015.10.009.
   PubMed Web of Science ®Google Scholar
• Yu WD, Sun G, Li J, et al. Mechanisms and therapeutic potentials of cancer immunotherapy in combination with radiotherapy and/or chemotherapy. Cancer Lett. 2019;452:66–70. doi: 10.1016/j.canlet.2019.02.048.
   PubMed Web of Science ®Google Scholar
• Adams S, Diamond JR, Hamilton E, et al. Atezolizumab plus nab-paclitaxel in the treatment of metastatic triple-negative breast cancer with 2-year survival follow-up: a phase 1b clinical trial. JAMA Oncol. 2019;5(3):334–342. doi: 10.1001/jamaoncol.2018.5152.
   PubMed Web of Science ®Google Scholar
• Schmid P, Adams S, Rugo HS, et al. Atezolizumab and nab-paclitaxel in advanced triple-negative breast cancer. N Engl J Med. 2018;379(22):2108–2121. doi: 10.1056/NEJMoa1809615.
   PubMed Web of Science ®Google Scholar
• Li TF, Li K, Zhang Q, et al. Dendritic cell-mediated delivery of doxorubicin-polyglycerol-nanodiamond composites elicits enhanced anti-cancer immune response in glioblastoma. Biomaterials. 2018;181:35–52. doi: 10.1016/j.biomaterials.2018.07.035.
   PubMed Web of Science ®Google Scholar
• Mastria EM, Cai LY, Kan MJ, et al. Nanoparticle formulation improves doxorubicin efficacy by enhancing host antitumor immunity. J Control Release. 2018;269:364–373. doi: 10.1016/j.jconrel.2017.11.021.
   PubMed Web of Science ®Google Scholar
• Spolski R, Leonard WJ. Interleukin-21: a double-edged sword with therapeutic potential. Nat Rev Drug Discov. 2014;13(5):379–395. doi: 10.1038/nrd4296.
   PubMed Web of Science ®Google Scholar
• Bhatt S, Sarosiek KA, Lossos IS. Interleukin 21 - its potential role in the therapy of B-cell lymphomas. Leuk Lymphoma. 2017;58(1):17–29. doi: 10.1080/10428194.2016.1201568.
   PubMed Web of Science ®Google Scholar
• McMichael EL, Jaime-Ramirez AC, Guenterberg KD, et al. IL-21 enhances natural killer cell response to cetuximab-coated pancreatic tumor cells. Clin Cancer Res. 2017;23(2):489–502. doi: 10.1158/1078-0432.CCR-16-0004.
   PubMed Web of Science ®Google Scholar
• Zhang X, Wang S, Nan Y, et al. Inhibition of autophagy potentiated the anti-tumor effects of VEGF and CD47 bispecific therapy in glioblastoma. Appl Microbiol Biotechnol. 2018;102(15):6503–6513. doi: 10.1007/s00253-018-9069-3.
   PubMed Web of Science ®Google Scholar
• Zhang X, Fan J, Wang S, et al. Targeting CD47 and autophagy elicited enhanced antitumor effects in non-small cell lung cancer. Cancer Immunol Res. 2017;5(5):363–375. doi: 10.1158/2326-6066.CIR-16-0398.
   PubMed Web of Science ®Google Scholar
• Hacioglu C, Kar F. Capsaicin induces redox imbalance and ferroptosis through ACSL4/GPx4 signaling pathways in U87-MG and U251 glioblastoma cells. Metab Brain Dis. 2023;38(2):393–408. doi: 10.1007/s11011-022-00983-w.
   PubMed Web of Science ®Google Scholar
• Zhang X, Wang Y, Fan J, et al. Blocking CD47 efficiently potentiated therapeutic effects of anti-angiogenic therapy in non-small cell lung cancer. J Immunother Cancer. 2019;7(1):346.
   PubMed Web of Science ®Google Scholar
• Zhang X, Chen W, Fan J, et al. Disrupting CD47-SIRPα axis alone or combined with autophagy depletion for the therapy of glioblastoma. Carcinogenesis. 2018;39(5):689–699. doi: 10.1093/carcin/bgy041.
   PubMed Web of Science ®Google Scholar
• Zhang X, Luan J, Chen W, et al. Mesoporous silica nanoparticles induced hepatotoxicity via NLRP3 inflammasome activation and caspase-1-dependent pyroptosis. Nanoscale. 2018;10(19):9141–9152. doi: 10.1039/c8nr00554k.
   PubMed Web of Science ®Google Scholar
• Revell PA, Grossman WJ, Thomas DA, et al. Granzyme B and the downstream granzymes C and/or F are important for cytotoxic lymphocyte functions. J Immunol. 2005;174(4):2124–2131. doi: 10.4049/jimmunol.174.4.2124.
   PubMed Web of Science ®Google Scholar
• Sun MH, Li XH, Xu Y, et al. Citrinin exposure disrupts organelle distribution and functions in mouse oocytes. Environ Res. 2020;185:109476. doi: 10.1016/j.envres.2020.109476.
   PubMed Web of Science ®Google Scholar
• Celis-Gutierrez J, Boyron M, Walzer T, et al. Dok1 and Dok2 proteins regulate natural killer cell development and function. Embo J. 2014;33(17):1928–1940. doi: 10.15252/embj.201387404.
   PubMed Web of Science ®Google Scholar
• Valentin-Torres A, Savarin C, Hinton DR, et al. Sustained TNF production by central nervous system infiltrating macrophages promotes progressive autoimmune encephalomyelitis. J Neuroinflammation. 2016;13(1):46. doi: 10.1186/s12974-016-0513-y.
   PubMedGoogle Scholar
• Wilson NO, Solomon W, Anderson L, et al. Pharmacologic inhibition of CXCL10 in combination with anti-malarial therapy eliminates mortality associated with murine model of cerebral malaria. PLoS One. 2013;8(4):e60898. doi: 10.1371/journal.pone.0060898.
   PubMed Web of Science ®Google Scholar
• Seo H, Kim BS, Bae EA, et al. IL21 therapy combined with PD-1 and tim-3 blockade provides enhanced NK cell antitumor activity against MHC class I-deficient tumors. Cancer Immunol Res. 2018;6(6):685–695. doi: 10.1158/2326-6066.CIR-17-0708.
   PubMed Web of Science ®Google Scholar
• Ivashkiv LB. IFNγ: signalling, epigenetics and roles in immunity, metabolism, disease and cancer immunotherapy. Nat Rev Immunol. 2018;18(9):545–558. doi: 10.1038/s41577-018-0029-z.
   PubMed Web of Science ®Google Scholar
• Prager I, Liesche C, van Ooijen H, et al. NK cells switch from granzyme B to death receptor-mediated cytotoxicity during serial killing. J Exp Med. 2019;216(9):2113–2127. doi: 10.1084/jem.20181454.
   PubMed Web of Science ®Google Scholar
• Shi Y, Moon M, Dawood S, et al. Mechanisms and management of doxorubicin cardiotoxicity. Herz. 2011;36(4):296–305. doi: 10.1007/s00059-011-3470-3.
   PubMed Web of Science ®Google Scholar
• Gonzales Carazas MM, Pinto JA, Casado FL. Biological bases of cancer immunotherapy. Expert Rev Mol Med. 2021;23:e3. doi: 10.1017/erm.2021.5.
   PubMed Web of Science ®Google Scholar
• Emens LA, Middleton G. The interplay of immunotherapy and chemotherapy: harnessing potential synergies. Cancer Immunol Res. 2015;3(5):436–443. doi: 10.1158/2326-6066.CIR-15-0064.
   PubMed Web of Science ®Google Scholar
• Coosemans A, Vankerckhoven A, Baert T, et al. Combining conventional therapy with immunotherapy: a risky business? Eur J Cancer. 2019;113:41–44. doi: 10.1016/j.ejca.2019.02.014.
   PubMed Web of Science ®Google Scholar
• Rizzo A, Ricci AD, Lanotte L, et al. Immune-based combinations for metastatic triple negative breast cancer in clinical trials: current knowledge and therapeutic prospects. Expert Opin Investig Drugs. 2022;31(6):557–565. doi: 10.1080/13543784.2022.2009456.
   PubMed Web of Science ®Google Scholar
• Schmid P, Cortes J, Pusztai L, et al. Pembrolizumab for early triple-negative breast cancer. N Engl J Med. 2020;382(9):810–821. doi: 10.1056/NEJMoa1910549.
   PubMed Web of Science ®Google Scholar
• Rizzo A, Ricci AD. Biomarkers for breast cancer immunotherapy: PD-L1, TILs, and beyond. Expert Opin Investig Drugs. 2022;31(6):549–555. doi: 10.1080/13543784.2022.2008354.
   PubMed Web of Science ®Google Scholar
• Smyth MJ, Hayakawa Y, Cretney E, et al. IL-21 enhances tumor-specific CTL induction by anti-DR5 antibody therapy. J Immunol. 2006;176(10):6347–6355. doi: 10.4049/jimmunol.176.10.6347.
   PubMed Web of Science ®Google Scholar
• Leonard WJ, Lin JX, O’Shea JJ. The γ(c) family of cytokines: basic biology to therapeutic ramifications. Immunity. 2019;50(4):832–850. doi: 10.1016/j.immuni.2019.03.028.
   PubMed Web of Science ®Google Scholar
• Santegoets SJ, Turksma AW, Suhoski MM, et al. IL-21 promotes the expansion of CD27+ CD28+ tumor infiltrating lymphocytes with high cytotoxic potential and low collateral expansion of regulatory T cells. J Transl Med. 2013;11(1):37. doi: 10.1186/1479-5876-11-37.
   PubMedGoogle Scholar
• Zeng R, Spolski R, Finkelstein SE, et al. Synergy of IL-21 and IL-15 in regulating CD8+ T cell expansion and function. J Exp Med. 2005;201(1):139–148. doi: 10.1084/jem.20041057.
   PubMed Web of Science ®Google Scholar
• AAAS.org [Internet]. Washington (DC): AAAS; [cited 2013]. Available from: https://www.aaas.org/
   Google Scholar
• Ewens A, Luo L, Berleth E, et al. Doxorubicin plus interleukin-2 chemoimmunotherapy against breast cancer in mice. Cancer Res. 2006;66(10):5419–5426. doi: 10.1158/0008-5472.CAN-05-3963.
   PubMed Web of Science ®Google Scholar
• Whiteside TL. The tumor microenvironment and its role in promoting tumor growth. Oncogene. 2008;27(45):5904–5912. doi: 10.1038/onc.2008.271.
   PubMed Web of Science ®Google Scholar
• Hinshaw DC, Shevde LA. The tumor microenvironment innately modulates cancer progression. Cancer Res. 2019;79(18):4557–4566. doi: 10.1158/0008-5472.CAN-18-3962.
   PubMed Web of Science ®Google Scholar
• Wang M, Zhao J, Zhang L, et al. Role of tumor microenvironment in tumorigenesis. J Cancer. 2017;8(5):761–773. doi: 10.7150/jca.17648.
   PubMed Web of Science ®Google Scholar
• Hirata E, Sahai E. Tumor microenvironment and differential responses to therapy. Cold Spring Harb Perspect Med. 2017;7(7):a026781. doi: 10.1101/cshperspect.a026781.
   PubMed Web of Science ®Google Scholar
• Mestas J, Hughes CC. Of mice and not men: differences between mouse and human immunology. J Immunol. 2004;172(5):2731–2738. doi: 10.4049/jimmunol.172.5.2731.
   PubMed Web of Science ®Google Scholar
• Que H, Fu Q, Lan T, et al. Tumor-associated neutrophils and neutrophil-targeted cancer therapies. Biochim Biophys Acta Rev Cancer. 2022;1877(5):188762. doi: 10.1016/j.bbcan.2022.188762.
   PubMed Web of Science ®Google Scholar
• Takeda Y, Nara H, Araki A, et al. Human peripheral neutrophils express functional IL-21 receptors. Inflammation. 2014;37(5):1521–1532. doi: 10.1007/s10753-014-9879-0.
   PubMed Web of Science ®Google Scholar
• Dexter DL, Kowalski HM, Blazar BA, et al. Heterogeneity of tumor cells from a single mouse mammary tumor. Cancer Res. 1978;38(10):3174–3181.
   PubMed Web of Science ®Google Scholar
• Aslakson CJ, Miller FR. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res. 1992;52(6):1399–1405.
   PubMed Web of Science ®Google Scholar
• Li C, Yoshimura T, Tian M, et al. Exosomal Wnt7a from a low metastatic subclone promotes lung metastasis of a highly metastatic subclone in the murine 4t1 breast cancer. Breast Cancer Res. 2022;24(1):60. doi: 10.1186/s13058-022-01557-5.
   PubMed Web of Science ®Google Scholar
• da Rocha MCO, da Silva PB, Radicchi MA, et al. Docetaxel-loaded solid lipid nanoparticles prevent tumor growth and lung metastasis of 4T1 murine mammary carcinoma cells. J Nanobiotechnology. 2020;18(1):43. doi: 10.1186/s12951-020-00604-7.
   PubMed Web of Science ®Google Scholar