3,394
Views
19
CrossRef citations to date
0
Altmetric
Research Article

Exosomes released by breast cancer cells under mild hyperthermic stress possess immunogenic potential and modulate polarization in vitro in macrophages

, , , , &
Pages 696-710 | Received 24 Jan 2020, Accepted 02 Jun 2020, Published online: 22 Jun 2020

References

  • Ha PT, Le TTH, Bui TQ, et al. Doxorubicin release by magnetic inductive heating and in vivo hyperthermia-chemotherapy combined cancer treatment of multifunctional magnetic nanoparticles. New J Chem. 2019;43(14):5404–5413.
  • Jeong S. The combination of hyperthermia, radiation, and chemotherapy for tumor suppression using hollow gold nanoparticles. Int J Radiat Oncol Biol Phys. 2014;90(1):S804.
  • Phung DC, Nguyen HT, Phuong Tran TT, et al. Combined hyperthermia and chemotherapy as a synergistic anticancer treatment. J Pharm Investig. 2019;49(5):519–526.
  • Seifert G, Budach V, Keilholz U, et al. Regional hyperthermia combined with chemotherapy in paediatric, adolescent and young adult patients: current and future perspectives. Radiat Oncol. 2016;11(1):1–7.
  • Toraya-Brown S, Fiering S. Local tumour hyperthermia as immunotherapy for metastatic cancer. Int J Hyperthermia. 2014;30(8):531–539.
  • Bettaieb A, et al. 2013. Hyperthermia: cancer treatment and beyond. 257–283.
  • Shao Q, O'Flanagan S, Lam T, et al. Engineering T cell response to cancer antigens by choice of focal therapeutic conditions. Int J Hyperthermia. 2019;36(1):130–138.
  • Skitzki JJ, Repasky EA, Evans SS, et al. Hyperthermia as an immunotherapy strategy for cancer. Curr Opin Investig Drugs. 2009;10(6):550–558.
  • Yagawa Y, Tanigawa K, Kobayashi Y, et al. Cancer immunity and therapy using hyperthermia with immunotherapy, radiotherapy, chemotherapy, and surgery. JCMT. 2017;3(10):218.
  • Ley K. The second touch hypothesis: T cell activation, homing and polarization. F1000Res. 2014;3:37.
  • Pozzi L-AM, Maciaszek JW, Rock KL, et al. Both dendritic cells and macrophages can stimulate naive CD8 T cells in vivo to proliferate, develop effector function, and differentiate into memory cells. J Immunol. 2005;175(4):2071–2081.
  • Poh AR, Ernst M. Targeting macrophages in cancer: from bench to bedside. Front Oncol. 2018;8:49.
  • Siegel RL, Miller KD, Jemal A, et al. Cancer statistics, 2019. CA Cancer J Clin. 2019;69(1):7–34.
  • Gonzalez-Angulo AM, et al. Overview of resistance to systemic therapy in patients with breast cancer. Breast Cancer Chemosensitivity. 2007;608:1–22.
  • Moreno-Aspitia A, Perez EA. Treatment options for breast cancer resistant to anthracycline and taxane. Mayo Clin Proc. 2009;84(6):533–545.
  • Selli C, Sims AH. Neoadjuvant therapy for breast cancer as a model for translational research. Breast Cancer (Auckl). 2019;13:117822341982907.
  • Beninson LA, Fleshner M. Exosomes: an emerging factor in stress-induced immunomodulation. Semin Immunol. 2014;26(5):394–401.
  • Rezaie J, Ajezi S, Avci ÇB, et al. Exosomes and their application in biomedical field: difficulties and advantages. Mol Neurobiol. 2018;55(4):3372–3393.
  • Théry C, Amigorena S, Raposo G, et al. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protocols Cell Biol. 2006;30(1):3.22.1–3.22.29. 3.22.21-23.22.29.
  • Zhang Y, Liu Y, Liu H, et al. Exosomes: biogenesis, biologic function and clinical potential. Cell Biosci. 2019;9(1):19.
  • Chen T, Guo J, Yang M, et al. Chemokine-containing exosomes are released from heat-stressed tumor cells via lipid raft-dependent pathway and act as efficient tumor vaccine. J Immunol. 2011;186(4):2219–2228.
  • Ratajczak J, Wysoczynski M, Hayek F, et al. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia. 2006;20(9):1487–1495.
  • Amend SR, Valkenburg KC, Pienta KJ, et al. Murine hind limb long bone dissection and bone marrow isolation. JoVE. 2016;(110):e53936.
  • Hui WW, Hercik K, Belsare S, et al. Salmonella enterica Serovar Typhimurium alters the extracellular proteome of macrophages and leads to the production of proinflammatory exosomes. Infect Immun. 2018;86(2):e00386–17:331–334
  • Sapareto SA, Dewey WC. Thermal dose determination in cancer therapy. Int J Radiat Oncol Biol Phys. 1984;10(6):787–800.
  • van Rhoon GC, Samaras T, Yarmolenko PS, et al. CEM43 °C thermal dose thresholds: a potential guide for magnetic resonance radiofrequency exposure levels? Eur Radiol. 2013;23(8):2215–2227.
  • Han C, Zhou J, Liang C, et al. Human umbilical cord mesenchymal stem cell derived exosomes encapsulated in functional peptide hydrogels promote cardiac repair. Biomater Sci. 2019;7(7):2920–2933.
  • Zheng Y, He R, Wang P, et al. Exosomes from LPS-stimulated macrophages induce neuroprotection and functional improvement after ischemic stroke by modulating microglial polarization. Biomater Sci. 2019;7(5):2037–2049.
  • Sen K, Banerjee S, Mandal M, et al. Dual drug loaded liposome bearing apigenin and 5-Fluorouracil for synergistic therapeutic efficacy in colorectal cancer. Colloids Surf B Biointerf. 2019;180:9–22.
  • Sheppe AEF, Kummari E, Walker A, et al. PGE2 augments inflammasome activation and M1 polarization in macrophages infected with Salmonella typhimurium and Yersinia enterocolitica. Front Microbiol. 2018;9:2447.
  • Zhou X, Jiao Z, Ji J, et al. Characterization of mouse serum exosomal small RNA content: the origins and their roles in modulating inflammatory response. Oncotarget. 2017;8(26):42712–42727.
  • van Rhoon GC. Is CEM43 still a relevant thermal dose parameter for hyperthermia treatment monitoring? Int J Hyperthermia. 2016;32(1):50–62.
  • Zhang H, Freitas D, Kim HS, et al. Identification of distinct nanoparticles and subsets of extracellular vesicles by asymmetric flow field-flow fractionation. Nat Cell Biol. 2018;20(3):332–343.
  • Sharma S, LeClaire M, Gimzewski JK, et al. Ascent of atomic force microscopy as a nanoanalytical tool for exosomes and other extracellular vesicles. Nanotechnology. 2018;29(13):132001.
  • Krakhmal NV, Zavyalova MV, Denisov EV, et al. Cancer invasion: patterns and mechanisms. Acta Naturae. 2015;7(2):17–28.
  • Mummidi S, et al. Macrophage migration and invasion is regulated by MMP10 expression. PLoS One. 2013;8(5):e63555.
  • De Toro J, Herschlik L, Waldner C, et al. Emerging roles of exosomes in normal and pathological conditions: new insights for diagnosis and therapeutic applications. Front Immunol. 2015;6:6.
  • Mathieu M, Martin-Jaular L, Lavieu G, et al. Specificities of secretion and uptake of exosomes and other extracellular vesicles for cell-to-cell communication. Nat Cell Biol. 2019;21(1):9–17.
  • de Jong OG, Verhaar MC, Chen Y, et al. Cellular stress conditions are reflected in the protein and RNA content of endothelial cell-derived exosomes. J Extracell Vesicles. 2012;1(1):18396.
  • Vulpis E, Soriani A, Cerboni C, et al. Cancer exosomes as conveyors of stress-induced molecules: new players in the modulation of NK cell response. IJMS. 2019;20(3):611.
  • Williams EC, Coimbra R, Chan TW, et al. Precious cargo: modulation of the mesenteric lymph exosome payload after hemorrhagic shock. J Trauma Acute Care Surg. 2019;86(1):52–61.
  • Wu J, Li M, Liu L, et al. Nitric oxide and interleukins are involved in cell proliferation of RAW264.7 macrophages activated by viili exopolysaccharides. Inflammation. 2013;36(4):954–961.
  • Ghazaei C. Role and mechanism of the Hsp70 molecular chaperone machines in bacterial pathogens. J Med Microbiol. 2017;66(3):259–265.
  • Ito A, Shinkai M, Honda H, et al. Augmentation of MHC class I antigen presentation via heat shock protein expression by hyperthermia. Cancer Immunol Immunother. 2001;50(10):515–522.
  • Ito A, Matsuoka F, Honda H, et al. Heat shock protein 70 gene therapy combined with hyperthermia using magnetic nanoparticles. Cancer Gene Ther. 2003;10(12):918–925.
  • Guo D, Chen Y, Wang S, et al. Exosomes from heat-stressed tumour cells inhibit tumour growth by converting regulatory T cells to Th17 cells via IL-6. Immunology. 2018;154(1):132–143.
  • Arango Duque G, Descoteaux A. Macrophage cytokines: involvement in immunity and infectious diseases. Front Immunol. 2014;5:5.
  • Lillard JW, Boyaka PN, Taub DD, et al. RANTES potentiates antigen-specific mucosal immune responses. J Immunol. 2001;166(1):162–169.
  • Neyrolles O, et al. Exosomal Hsp70 induces a pro-inflammatory response to foreign particles including mycobacteria. PLoS One. 2010;5(4):e10136.
  • Kelleher RJ, Balu-Iyer S, Loyall J, et al. Extracellular vesicles present in human ovarian tumor microenvironments induce a phosphatidylserine-dependent arrest in the T-cell signaling cascade. Cancer Immunol Res. 2015;3(11):1269–1278.
  • Shenoy GN, Loyall J, Maguire O, et al. Exosomes associated with human ovarian tumors harbor a reversible checkpoint of T-cell responses. Cancer Immunol Res. 2018;6(2):236–247.
  • Panjwani NN, Popova L, Srivastava PK, et al. Heat shock proteins gp96 and hsp70 activate the release of nitric oxide by APCs. J Immunol. 2002;168(6):2997–3003.
  • Song S, Zhou F, Chen WR, et al. PDT-induced HSP70 externalization up-regulates NO production via TLR2 signal pathway in macrophages. FEBS Lett. 2013;587(2):128–135.
  • Ley K. M1 means kill; M2 means heal. J Immunol. 2017;199(7):2191–2193.
  • Orecchioni M, et al. Macrophage polarization: different gene signatures in M1(LPS+) vs. classically and M2(LPS–) vs. alternatively activated macrophages. Front Immunol. 2019;10:1084.
  • Bardi GT, Smith MA, Hood JL, et al. Melanoma exosomes promote mixed M1 and M2 macrophage polarization. Cytokine. 2018;105:63–72.
  • Zhang W, Zhang Y, He Y, et al. Lipopolysaccharide mediates time-dependent macrophage M1/M2 polarization through the Tim-3/Galectin-9 signalling pathway. Exp Cell Res. 2019;376(2):124–132.
  • Adkins I, Sadilkova L, Hradilova N, et al. Severe, but not mild heat-shock treatment induces immunogenic cell death in cancer cells. OncoImmunology. 2017;6(5):e1311433.
  • Ouzounova M, Lee E, Piranlioglu R, et al. Monocytic and granulocytic myeloid derived suppressor cells differentially regulate spatiotemporal tumour plasticity during metastatic cascade. Nat Commun. 2017;8(1):1–13.
  • Kanemoto S, Nitani R, Murakami T, et al. Multivesicular body formation enhancement and exosome release during endoplasmic reticulum stress. Biochem Biophys Res Commun. 2016;480(2):166–172.
  • Lehmann BD, Paine MS, Brooks AM, et al. Senescence-associated exosome release from human prostate cancer cells. Cancer Res. 2008;68(19):7864–7871.
  • O’Neill C, Gilligan K, Dwyer R, et al. Role of extracellular vesicles (EVs) in cell stress response and resistance to cancer therapy. Cancers. 2019;11(2):136.
  • Zhang H-C, Liu X-B, Huang S, et al. Microvesicles derived from human umbilical cord mesenchymal stem cells stimulated by hypoxia promote angiogenesis both in vitro and in vivo. Stem Cells Dev. 2012;21(18):3289–3297.
  • Heppner G, Miller F, Malathy Shekhar PV, et al. Nontransgenic models of breast cancer. Breast Cancer Res. 2000;2(5).
  • Simões RV, Serganova IS, Kruchevsky N, et al. Metabolic plasticity of metastatic breast cancer cells: adaptation to changes in the microenvironment. Neoplasia. 2015;17(8):671–684.
  • Tao K, Fang M, Alroy J, et al. Imagable 4T1 model for the study of late stage breast cancer. BMC Cancer. 2008;8(1):1–20.
  • Adachi S, Kokura S, Okayama T, et al. Effect of hyperthermia combined with gemcitabine on apoptotic cell death in cultured human pancreatic cancer cell lines. Int J Hyperthermia. 2009;25(3):210–219.
  • Cesna V, Sukovas A, Jasukaitiene A, et al. Narrow line between benefit and harm: additivity of hyperthermia to cisplatin cytotoxicity in different gastrointestinal cancer cells. World J Gastroenterol. 2018;24(10):1072–1083.
  • Kirui DK, Celia C, Molinaro R, et al. Mild hyperthermia enhances transport of liposomal gemcitabine and improves in vivo therapeutic response. Adv Healthc Mater. 2015;4(7):1092–1103.
  • Okayama T, Kokura S, Ishikawa T, et al. Antitumor effect of pretreatment for colon cancer cells with hyperthermia plus geranylgeranylacetone in experimental metastasis models and a subcutaneous tumor model of colon cancer in mice. Int J Hyperthermia. 2009;25(2):141–149.
  • Vertrees RA, Das GC, Popov VL, et al. Synergistic interaction of hyperthermia and gemcitabine in lung cancer. Cancer Biol Ther. 2005;4(10):1144–1153.