144
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Targeting of M2 macrophages with IL-13-functionalized liposomal prednisolone inhibits melanoma angiogenesis in vivo

, , , , , , , , , , & show all
Received 31 Jul 2023, Accepted 31 Jan 2024, Published online: 20 Feb 2024

References

  • Welch HG, Mazer BL, Adamson AS. The rapid rise in cutaneous melanoma diagnoses. N Engl J Med. 2021;384(1):72–79. doi: 10.1056/nejmsb2019760.
  • Liu S, Dharanipragada P, Lomeli SH, et al. Multi-organ landscape of therapy-resistant melanoma. Nat Med. 2023;29(5):1123–1134. doi: 10.1038/s41591-023-02304-9.
  • Falcone I, Conciatori F, Bazzichetto C, et al. Tumor microenvironment: implications in melanoma resistance to targeted therapy and immunotherapy. Cancers (Basel). 2020;12(10):2870. doi: 10.3390/cancers12102870.
  • Chen J, Hu S, Wang H, et al. Integrated analysis reveals the pivotal interactions between immune cells in the melanoma tumor microenvironment. Sci Rep. 2022;12(1):10040. doi: 10.1038/s41598-022-14319-2.
  • Cerezo-Wallis D, Contreras-Alcalde M, Troulé K, et al. Midkine rewires the melanoma microenvironment toward a tolerogenic and immune-resistant state. Nat Med. 2020;26(12):1865–1877. doi: 10.1038/s41591-020-1073-3.
  • Lopes-Coelho F, Martins F, Pereira SA, et al. Anti-angiogenic therapy: current challenges and future perspectives. Int J Mol Sci. 2021;22(7):3765. doi: 10.3390/ijms22073765.
  • Zhou Q, Fang T, Wei S, et al. Macrophages in melanoma: a double-edged sword and targeted therapy strategies (review). Exp Ther Med. 2022;24(4):640. doi: 10.3892/etm.2022.11577.
  • Bardi GT, Smith MA, Hood JL. Melanoma exosomes promote mixed M1 and M2 macrophage polarization. Cytokine. 2018;105:63–72. doi: 10.1016/j.cyto.2018.02.002.
  • Banciu M, Metselaar JM, Schiffelers RM, et al. Antitumor activity of liposomal prednisolone phosphate depends on the presence of functional tumor-associated macrophages in tumor tissue. Neoplasia. 2008;10(2):108–117. doi: 10.1593/neo.07913.
  • Alupei MC, Licarete E, Patras L, et al. Liposomal simvastatin inhibits tumor growth via targeting tumor-associated macrophages-mediated oxidative stress. Cancer Lett. 2015;356(2 Pt B):946–952. doi: 10.1016/j.canlet.2014.11.010.
  • Rauca V-F, Patras L, Luput L, et al. Remodeling tumor microenvironment by liposomal codelivery of DMXAA and simvastatin inhibits malignant melanoma progression. Sci Rep. 2021;11(1):22102. doi: 10.1038/s41598-021-01284-5.
  • Patras L, Ionescu AE, Munteanu C, et al. Trojan horse treatment based on PEG-coated extracellular vesicles to deliver doxorubicin to melanoma in vitro and in vivo. Cancer Biol Ther. 2021;23(1):1–16. doi: 10.1080/15384047.2021.2003656.
  • Licarete E, Rauca VF, Luput L, et al. Overcoming intrinsic doxorubicin resistance in melanoma by anti-angiogenic and anti-metastatic effects of liposomal prednisolone phosphate on tumor microenvironment. Int J Mol Sci. 2020;21(8):2968. doi: 10.3390/ijms21082968.
  • Patras L, Sylvester B, Luput L, et al. Liposomal prednisolone phosphate potentiates the antitumor activity of liposomal 5-fluorouracil in C26 murine Colon carcinoma in vivo. Cancer Biol Ther. 2017;18(8):616–626. doi: 10.1080/15384047.2017.1345392.
  • Suk JS, Xu Q, Kim N, et al. PEGylation as a strategy for improving nanoparticle-based drug and gene delivery. Adv Drug Deliv Rev. 2016;99(Pt A):28–51. doi: 10.1016/j.addr.2015.09.012.
  • Sercombe L, Veerati T, Moheimani F, et al. Advances and challenges of liposome assisted drug delivery. Front Pharmacol. 2015;6:286. doi: 10.3389/fphar.2015.00286.
  • Eroglu I, Ibrahim MA. Liposome–ligand conjugates: a review on the current state of art. J Drug Targeting. 2019;28(3):225–244. doi: 10.1080/1061186x.2019.1648479.
  • Negrea G, Rauca V-F, Meszaros MS, et al. Active tumor-targeting nano-formulations containing simvastatin and doxorubicin inhibit melanoma growth and angiogenesis. Front Pharmacol. 2022;13:870347. doi: 10.3389/fphar.2022.870347.
  • Okamoto H, Yoshimatsu Y, Tomizawa T, et al. Interleukin-13 receptor α2 is a novel marker and potential therapeutic target for human melanoma. Sci Rep. 2019;9(1):1281. doi: 10.1038/s41598-019-39018-3.
  • Suzuki A, Leland P, Joshi B, et al. Targeting of IL-4 and IL-13 receptors for cancer therapy. Cytokine. 2015;75(1):79–88. doi: 10.1016/j.cyto.2015.05.026.
  • Jayasingam SD, Citartan M, Thang TH, et al. Evaluating the polarization of tumor-associated macrophages into M1 and M2 phenotypes in human cancer tissue: technicalities and challenges in routine clinical practice. Front Oncol. 2019;9:1512. doi: 10.3389/fonc.2019.01512.
  • Gupta P, Jiang ZK, Yang B, et al. Targeting and pharmacology of an anti-IL13Rα2 antibody and antibody-drug conjugate in a melanoma xenograft model. MAbs. 2021;13(1):1958662. doi: 10.1080/19420862.2021.1958662.
  • Dzhumashev D, Anton-Joseph S, Morel VJ, et al. Rapid liposomal formulation for nucleolin targeting to rhabdomyosarcoma cells. Eur J Pharm Biopharm. 2024;194:49–61. doi: 10.1016/j.ejpb.2023.11.020.
  • Tang C, Yin D, Liu T, et al. Maleimide-functionalized liposomes: prolonged retention and enhanced efficacy of doxorubicin in breast cancer with low systemic toxicity. Molecules. 2022;27(14):4632. doi: 10.3390/molecules27144632.
  • Li T, Takeoka S. A novel application of maleimide for advanced drug delivery: in vitro and in vivo evaluation of maleimide-modified pH-sensitive liposomes. Int J Nanomedicine. 2013;8:3855–3866. doi: 10.2147/ijn.s47749.
  • Metselaar JM, Wauben MHM, Wagenaar-Hilbers JPA, et al. Complete remission of experimental arthritis by joint targeting of glucocorticoids with long-circulating liposomes. Arthritis Rheum. 2003;48(7):2059–2066. doi: 10.1002/art.11140.
  • Sylvester B, Porfire A, Muntean D-M, et al. Optimization of prednisolone-loaded long-circulating liposomes via application of quality by design (QbD) approach. J Liposome Res. 2018;28(1):49–61. doi: 10.1080/08982104.2016.1254242.
  • Banciu M, Schiffelers RM, Fens MHAM, et al. Anti-angiogenic effects of liposomal prednisolone phosphate on B16 melanoma in mice. J Control Release. 2006;113(1):1–8. doi: 10.1016/j.jconrel.2006.03.019.
  • Rouser G, Fkeischer S, Yamamoto A. Two-dimensional thin layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids. 1970;5(5):494–496. doi: 10.1007/bf02531316.
  • Ying W, Cheruku PS, Bazer FW, et al. Investigation of macrophage polarization using bone marrow derived macrophages. JoVE. 2013;(76):50323. doi: 10.3791/50323.
  • Rauca V-F, Licarete E, Luput L, et al. Combination therapy of simvastatin and 5, 6-dimethylxanthenone-4-acetic acid synergistically suppresses the aggressiveness of B16.F10 melanoma cells. PLOS One. 2018;13(8):e0202827. doi: 10.1371/journal.pone.0202827.
  • Luput L, Licarete E, Drotar DM, et al. In vivo double targeting of C26 colon carcinoma cells and microenvironmental protumor processes using liposomal simvastatin. J Cancer. 2018;9(2):440–449. doi: 10.7150/jca.21560.
  • Banciu M, Schiffelers RM, Storm G. Investigation into the role of tumor-associated macrophages in the antitumor activity of doxil. Pharm Res. 2008;25(8):1948–1955. doi: 10.1007/s11095-008-9629-9.
  • Licarete E, Sesarman A, Rauca VF, et al. HIF-1α acts as a molecular target for simvastatin cytotoxicity in B16.F10 melanoma cells cultured under chemically induced hypoxia. Oncol Lett. 2017;13(5):3942–3950. doi: 10.3892/ol.2017.5928.
  • Huang R-P. Detection of multiple proteins in an antibody-based protein microarray system. J Immunol Methods. 2001;255(1-2):1–13. doi: 10.1016/s0022-1759(01)00394-5.
  • Luput L, Licarete E, Sesarman A, et al. Tumor-associated macrophages favor C26 murine colon carcinoma cell proliferation in an oxidative stress-dependent manner. Oncol Rep. 2017;37(4):2472–2480. doi: 10.3892/or.2017.5466.
  • Wheeler CR, Salzman JA, Elsayed NM, et al. Automated assays for superoxide dismutase, catalase, glutathione peroxidase, and glutathione reductase activity. Anal Biochem. 1990;184(2):193–199. doi: 10.1016/0003-2697(90)90668-y.
  • Patras L, Sesarman A, Licarete E, et al. Dual role of macrophages in the response of C26 colon carcinoma cells to 5-fluorouracil administration. Oncol Lett. 2016;12(2):1183–1191. doi: 10.3892/ol.2016.4708.
  • Rauca V-F, Vlase L, Casian T, et al. Biologically active ajuga species extracts modulate supportive processes for cancer cell development. Front Pharmacol. 2019;10:334. doi: 10.3389/fphar.2019.00334.
  • Sesarman A, Tefas L, Sylvester B, et al. Anti-angiogenic and anti-inflammatory effects of long-circulating liposomes co-encapsulating curcumin and doxorubicin on C26 murine Colon cancer cells. Pharmacol Rep. 2018;70(2):331–339. doi: 10.1016/j.pharep.2017.10.004.
  • Graves PR, Siddiqui F, Anscher MS, et al. Radiation pulmonary toxicity: from mechanisms to management. Semin Radiat Oncol. 2010;20(3):201–207. doi: 10.1016/j.semradonc.2010.01.010.
  • Porfire A, Tomuta I, Muntean D, et al. Optimizing long-circulating liposomes for delivery of simvastatin to C26 colon carcinoma cells. J Liposome Res. 2015;25(4):261–269. doi: 10.3109/08982104.2014.987787.
  • D’Avanzo N, et al. LinTT1 peptide-functionalized liposomes for targeted breast cancer therapy. Int J Pharm. 2021;597:120346. doi: 10.1016/j.ijpharm.2021.120346.
  • Liu L, Ho C. 2016. A new approach to decrease the RES uptake of nanodrugs by pre-administration with Intralipid® resulting in a reduction of toxic side effects. In A. Prokop, & V. Weissig (Eds.), Intracellular Delivery III. Fundamental Biomedical Technologies. Springer, Cham. https://doi.org/10.1007/978-3-319-43525-1_5.
  • Riabov V, Gudima A, Wang N, et al. Role of tumor associated macrophages in tumor angiogenesis and lymphangiogenesis. Front Physiol. 2014;5:75. doi: 10.3389/fphys.2014.00075.
  • Guo C. The role of tumor-associated macrophages in tumor vascularization. Available at: https://vascularcell.com/public/journals/1/articles/13221-05-01-131/13221-05-20_html.html.
  • Valli F, García Vior MC, Roguin LP, et al. Crosstalk between oxidative stress-induced apoptotic and autophagic signaling pathways in Zn(II) phthalocyanine photodynamic therapy of melanoma. Free Radic Biol Med. 2020;152:743–754. doi: 10.1016/j.freeradbiomed.2020.01.018.
  • Edlich F. BCL-2 proteins and apoptosis: recent insights and unknowns. Biochem Biophys Res Commun. 2018;500(1):26–34. doi: 10.1016/j.bbrc.2017.06.190.
  • Lopez A, Reyna DE, Gitego N, et al. Co-targeting of BAX and BCL-XL proteins broadly overcomes resistance to apoptosis in cancer. Nat Commun. 2022;13(1):1199. doi: 10.1038/s41467-022-28741-7.
  • Fares J, Fares MY, Khachfe HH, et al. Molecular principles of metastasis: a hallmark of cancer revisited. Sig Transduct Target Ther. 2020;5(1):28. doi: 10.1038/s41392-020-0134-x.
  • Sonju JJ, Dahal A, Singh SS, et al. Peptide-functionalized liposomes as therapeutic and diagnostic tools for cancer treatment. J Control Release. 2021;329:624–644. doi: 10.1016/j.jconrel.2020.09.055.
  • Mantovani A, Marchesi F, Jaillon S, et al. Tumor-associated myeloid cells: diversity and therapeutic targeting. Cell Mol Immunol. 2021;18(3):566–578. doi: 10.1038/s41423-020-00613-4.
  • Christofides A, Strauss L, Yeo A, et al. The complex role of tumor-infiltrating macrophages. Nat Immunol. 2022;23(8):1148–1156. doi: 10.1038/s41590-022-01267-2.
  • Dhakal M, Hardaway JC, Guloglu FB, et al. IL-13Rα1 is a surface marker for M2 macrophages influencing their differentiation and function. Eur J Immunol. 2014;44(3):842–855. doi: 10.1002/eji.201343755.
  • Ge Z, Ding S. The crosstalk between tumor-associated macrophages (TAMs) and tumor cells and the corresponding targeted therapy. Front Oncol. 2020;10:590941. doi: 10.3389/fonc.2020.590941.
  • Tariq M, Zhang J-Q, Liang G-K, et al. Gefitinib inhibits M2-like polarization of tumor-associated macrophages in lewis lung cancer by targeting the STAT6 signaling pathway. Acta Pharmacol Sin. 2017;38(11):1501–1511. doi: 10.1038/aps.2017.124.
  • Yao Z, Zhang J, Zhang B, et al. Imatinib prevents lung cancer metastasis by inhibiting M2-like polarization of macrophages. Pharmacol Res. 2018;133:121–131. doi: 10.1016/j.phrs.2018.05.002.
  • Gao H, Zhang S, Yang Z, et al. In vitro and in vivo intracellular distribution and anti-glioblastoma effects of docetaxel-loaded nanoparticles functioned with IL-13 peptide. Int J Pharm. 2014;466(1-2):8–17. doi: 10.1016/j.ijpharm.2014.03.012.
  • Haibe Y, Kreidieh M, El Hajj H, et al. Resistance mechanisms to anti-angiogenic therapies in cancer. Front Oncol. 2020;10:221. doi: 10.3389/fonc.2020.00221.
  • Ma X. TNF-α and IL-12:a balancing act in macrophage functioning. Microbes Infect. 2001;3(2):121–129. doi: 10.1016/s1286-4579(00)01359-9.
  • Huang Y, Nan G. Oxidative stress-induced angiogenesis. J Clin Neurosci. 2019;63:13–16. doi: 10.1016/j.jocn.2019.02.019.
  • Mantovani A, Marchesi F, Malesci A, et al. Tumour-associated macrophages as treatment targets in oncology. Nat Rev Clin Oncol. 2017;14(7):399–416. doi: 10.1038/nrclinonc.2016.217.
  • Valacca C, Tassone E, Mignatti P. TIMP-2 interaction with MT1-MMP activates the AKT pathway and protects tumor cells from apoptosis. PLOS One. 2015;10(9):e0136797. doi: 10.1371/journal.pone.0136797.
  • Cern A, Golbraikh A, Sedykh A, et al. Quantitative structure - property relationship modeling of remote liposome loading of drugs. J Control Release. 2012;160(2):147–157. doi: 10.1016/j.jconrel.2011.11.029.
  • Kim M, Lee JS, Kim W, et al. Aptamer-conjugated nano-liposome for immunogenic chemotherapy with reversal of immunosuppression. J Control Release. 2022;348:893–910. doi: 10.1016/j.jconrel.2022.06.039.
  • Moiseev RV, Kaldybekov DB, Filippov SK, et al. Maleimide-Decorated PEGylated mucoadhesive liposomes for ocular drug delivery. Langmuir. 2022;38(45):13870–13879. ' doi: 10.1021/acs.langmuir.2c02086.
  • Banciu M, Fens MHAM, Storm G, et al. Antitumor activity and tumor localization of liposomal glucocorticoids in B16 melanoma-bearing mice. J Control Release. 2008;127(2):131–136. doi: 10.1016/j.jconrel.2008.01.008.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.