175
Views
1
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

A Macrophages-Enriched Head and Neck Tumor Spheroid Model to Study Foslip® Behavior in Tumor Microenvironment

, , , ORCID Icon, ORCID Icon &
Pages 6545-6562 | Received 17 Jul 2023, Accepted 05 Oct 2023, Published online: 08 Nov 2023

References

  • Mhaidly N, Journe F, Najem A, et al. Macrophage profiling in head and neck cancer to improve patient prognosis and assessment of cancer cell-macrophage interactions using three-dimensional coculture models. Int J Mol Sci. 2023;24(16):12813. doi:10.3390/ijms241612813
  • Tredan O, Galmarini CM, Patel K, Tannock IF. Drug resistance and the solid tumor microenvironment. J Natl Cancer Inst. 2007;99(19):1441–1454. doi:10.1093/jnci/djm135
  • Rebelo SP, Pinto C, Martins TR, et al. 3D-3-culture: a tool to unveil macrophage plasticity in the tumour microenvironment. Biomaterials. 2018;163:185–197. doi:10.1016/j.biomaterials.2018.02.030
  • Xue Y, Song X, Fan S, Deng R. The role of tumor-associated macrophages in oral squamous cell carcinoma. Front Physiol. 2022;13:959747. doi:10.3389/fphys.2022.959747
  • Mantovani A, Allavena P. The interaction of anticancer therapies with tumor-associated macrophages. J Exp Med. 2015;212(4):435–445. doi:10.1084/jem.20150295
  • Mantovani A, Marchesi F, Malesci A, Laghi L, Allavena P. Tumour-associated macrophages as treatment targets in oncology. Nat Rev Clin Oncol. 2017;14(7):399–416. doi:10.1038/nrclinonc.2016.217
  • Evrard D, Szturz P, Tijeras-Raballand A, et al. Macrophages in the microenvironment of head and neck cancer: potential targets for cancer therapy. Oral Oncol. 2019;88:29–38. doi:10.1016/j.oraloncology.2018.10.040
  • Ruytinx P, Proost P, Van Damme J, Struyf S. Chemokine-induced macrophage polarization in inflammatory conditions. Front Immunol. 2018;9:1930. doi:10.3389/fimmu.2018.01930
  • Kuen J, Darowski D, Kluge T, Majety M. Pancreatic cancer cell/fibroblast co-culture induces M2 like macrophages that influence therapeutic response in a 3D model. Ahmad A, ed.. PLoS One. 2017;12(7):e0182039. doi:10.1371/journal.pone.0182039
  • Lee CH, Liu SY, Chou KC, et al. Tumor-associated macrophages promote oral cancer progression through activation of the axl signaling pathway. Ann Surg Oncol. 2014;21(3):1031–1037. doi:10.1245/s10434-013-3400-0
  • Alves AM, Diel LF, Lamers ML. Macrophages and prognosis of oral squamous cell carcinoma: a systematic review. J Oral Pathol Med. 2018;47(5):460–467. doi:10.1111/jop.12643
  • Curry JM, Sprandio J, Cognetti D, et al. Tumor microenvironment in head and neck squamous cell carcinoma. Semin Oncol. 2014;41(2):217–234. doi:10.1053/j.seminoncol.2014.03.003
  • Bisheshar SK, Van Der Kamp MF, De Ruiter EJ, et al. The prognostic role of tumor associated macrophages in squamous cell carcinoma of the head and neck: a systematic review and meta-analysis. Oral Oncol. 2022;135:106227. doi:10.1016/j.oraloncology.2022.106227
  • Li B, Ren M, Zhou X, Han Q, Cheng L. Targeting tumor-associated macrophages in head and neck squamous cell carcinoma. Oral Oncol. 2020;106:104723. doi:10.1016/j.oraloncology.2020.104723
  • Hagemann T, Lawrence T, McNeish I, et al. “Re-educating” tumor-associated macrophages by targeting NF-κB. J Exp Med. 2008;205(6):1261–1268. doi:10.1084/jem.20080108
  • Biswas SK, Allavena P, Mantovani A. Tumor-associated macrophages: functional diversity, clinical significance, and open questions. Semin Immunopathol. 2013;35(5):585–600. doi:10.1007/s00281-013-0367-7
  • Wiehe A, Senge MO. The Photosensitizer Temoporfin (m THPC) – chemical, Pre‐clinical and Clinical Developments in the Last Decade † ‡. Photochem Photobiology. 2023;99(2):356–419. doi:10.1111/php.13730
  • Peng Q, Nesland JM. Effects of photodynamic therapy on tumor stroma. Ultrastruct Pathol. 2004;28(5–6):333–340. doi:10.1080/01913120490515586
  • Korbelik M, Hamblin MR. The impact of macrophage-cancer cell interaction on the efficacy of photodynamic therapy. Photochem Photobiol Sci. 2015;14(8):1403–1409. doi:10.1039/c4pp00451e
  • Rumie Vittar NB, Lamberti MJ, Pansa MF, et al. Ecological photodynamic therapy: new trend to disrupt the intricate networks within tumor ecosystem. Biochim Biophys Acta Rev Cancer. 2013;1835(1):86–99. doi:10.1016/j.bbcan.2012.10.004
  • Zhu Z, Scalfi-Happ C, Ryabova A, et al. Photodynamic activity of Temoporfin nanoparticles induces a shift to the M1-like phenotype in M2-polarized macrophages. J Photochem Photobiol B. 2018;185:215–222. doi:10.1016/j.jphotobiol.2018.06.015
  • Lassalle HP, Dumas D, Gräfe S, D’Hallewin MA, Guillemin F, Bezdetnaya L. Correlation between in vivo pharmacokinetics, intratumoral distribution and photodynamic efficiency of liposomal mTHPC. J Control Release. 2009;134(2):118–124. doi:10.1016/j.jconrel.2008.11.016
  • Reshetov V, Lassalle HP, François A, et al. Photodynamic therapy with conventional and PEGylated liposomal formulations of mTHPC (temoporfin): comparison of treatment efficacy and distribution characteristics in vivo. Int J Nanomedicine. 2013:3817. doi:10.2147/IJN.S51002
  • Millard M, Yakavets I, Zorin V, Kulmukhamedova A, Marchal S, Bezdetnaya L. Drug delivery to solid tumors: the predictive value of the multicellular tumor spheroid model for nanomedicine screening. Int J Nanomedicine. 2017;12:7993–8007. doi:10.2147/IJN.S146927
  • Costa EC, De Melo-Diogo D, Moreira AF, Carvalho MP, Correia IJ. Spheroids formation on non-adhesive surfaces by liquid overlay technique: considerations and practical approaches. Biotechnol J. 2018;13(1):1700417. doi:10.1002/biot.201700417
  • Langhans SA. Three-dimensional in vitro cell culture models in drug discovery and drug repositioning. Front Pharmacol. 2018;9:6. doi:10.3389/fphar.2018.00006
  • Di Modugno F, Colosi C, Trono P, Antonacci G, Ruocco G, Nisticò P. 3D models in the new era of immune oncology: focus on T cells, CAF and ECM. J Exp Clin Cancer Res. 2019;38(1):117. doi:10.1186/s13046-019-1086-2
  • Yakavets I, Jenard S, Francois A, et al. Stroma-rich co-culture multicellular tumor spheroids as a tool for photoactive drugs screening. J Clin Med. 2019;8(10):1686. doi:10.3390/jcm8101686
  • Yakavets I, Francois A, Guiot M, et al. NIR imaging of the integrin-rich head and neck squamous cell carcinoma using ternary copper indium selenide/zinc sulfide-based quantum dots. Cancers. 2020;12(12):3727. doi:10.3390/cancers12123727
  • Yakavets I, Francois A, Lamy L, et al. Effect of stroma on the behavior of temoporfin-loaded lipid nanovesicles inside the stroma-rich head and neck carcinoma spheroids. J Nanobiotechnol. 2021;19(1):3. doi:10.1186/s12951-020-00743-x
  • Lamy L, François M, Bezdetnaya L, Yakavets I. Phototoxicity of temoporfin-loaded cyclodextrin nanosponges in stroma-rich three-dimensional models of head and neck cancer. Eur J Pharm Biopharm. 2023;184:1–6. doi:10.1016/j.ejpb.2023.01.010
  • Daigneault M, Preston JA, Marriott HM, Whyte MKB, Dockrell DH. the identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. Doherty TM, ed.. PLoS One. 2010;5(1):e8668. doi:10.1371/journal.pone.0008668
  • Bertani FR, Mozetic P, Fioramonti M, et al. Classification of M1/M2-polarized human macrophages by label-free hyperspectral reflectance confocal microscopy and multivariate analysis. Sci Rep. 2017;7(1):8965. doi:10.1038/s41598-017-08121-8
  • Wang J, Li D, Cang H, Guo B. Crosstalk between cancer and immune cells: role of tumor‐associated macrophages in the tumor microenvironment. Cancer Med. 2019;8(10):4709–4721. doi:10.1002/cam4.2327
  • Galli SJ, Borregaard N, Wynn TA. Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nat Immunol. 2011;12(11):1035–1044. doi:10.1038/ni.2109
  • Nascimento CR, Rodrigues Fernandes NA, Gonzalez Maldonado LA, Rossa Junior C. Comparison of monocytic cell lines U937 and THP-1 as macrophage models for in vitro studies. Biochem Biophys Rep. 2022;32:101383. doi:10.1016/j.bbrep.2022.101383
  • Harris PE, Ralph P, Litcofsky P, Moore MA. Distinct activities of interferon-gamma, lymphokine and cytokine differentiation-inducing factors acting on the human monoblastic leukemia cell line U937. Cancer Res. 1985;45(1):9–13.
  • Coutier S, Bezdetnaya L, Marchal S, et al. Foscan® (mTHPC) photosensitized macrophage activation: enhancement of phagocytosis, nitric oxide release and tumour necrosis factor-α-mediated cytolytic activity. Br J Cancer. 1999;81(1):37–42. doi:10.1038/sj.bjc.6690648
  • Reinhard A, Bressenot A, Dassonneville R, et al. Photodynamic therapy relieves colitis and prevents colitis-associated carcinogenesis in mice. Inflamm Bowel Dis. 2015;21(5):985–995. doi:10.1097/MIB.0000000000000354
  • Taniguchi K, Hikiji H, Okinaga T, et al. Essential role of lysophosphatidylcholine acyltransferase 3 in the induction of macrophage polarization in PMA-treated U937 cells. J Cell Biochem. 2015;116(12):2840–2848. doi:10.1002/jcb.25230
  • Benner B, Scarberry L, Suarez-Kelly LP, et al. Generation of monocyte-derived tumor-associated macrophages using tumor-conditioned media provides a novel method to study tumor-associated macrophages in vitro. J Immunother Cancer. 2019;7(1):140. doi:10.1186/s40425-019-0622-0
  • Sawa-Wejksza K, Dudek A, Lemieszek M, Kaławaj K, Kandefer-Szerszeń M. Colon cancer–derived conditioned medium induces differentiation of THP-1 monocytes into a mixed population of M1/M2 cells. Tumour Biol. 2018;40(9):101042831879788. doi:10.1177/1010428318797880
  • Sánchez-Reyes K, Pedraza-Brindis EJ, Hernández-Flores G, et al. The supernatant of cervical carcinoma cells lines induces a decrease in phosphorylation of STAT-1 and NF-κB transcription factors associated with changes in profiles of cytokines and growth factors in macrophages derived from U937 cells. Innate Immun. 2019;25(6):344–355. doi:10.1177/1753425919848841
  • Hu G, Guo M, Xu J, et al. Nanoparticles targeting macrophages as potential clinical therapeutic agents against cancer and inflammation. Front Immunol. 2019;10:1998. doi:10.3389/fimmu.2019.01998
  • Siegler EL, Kim YJ, Wang P. Nanomedicine targeting the tumor microenvironment: therapeutic strategies to inhibit angiogenesis, remodel matrix, and modulate immune responses. J Cell Immunother. 2016;2(2):69–78. doi:10.1016/j.jocit.2016.08.002
  • Ye J, Yang Y, Dong W, et al. Drug-free mannosylated liposomes inhibit tumor growth by promoting the polarization of tumor-associated macrophages. Int J Nanomed. 2019;14:3203–3220. doi:10.2147/IJN.S207589