Caveolin-1-Dependent Tenascin C Inclusion in Extracellular Vesicles Is Required to Promote Breast Cancer Cell Malignancy

References

• WHO . Breast Cancer. www.who.int/news-room/fact-sheets/detail/breast-cancer
   Google Scholar
• Mehlen P , PuisieuxA. Metastasis: a question of life or death. Nat. Rev. Cancer6(6), 449–458 (2006).
   PubMed Web of Science ®Google Scholar
• Hanahan D , WeinbergRA. The hallmarks of cancer. Cell100(1), 57–70 (2000).
   PubMed Web of Science ®Google Scholar
• Hanahan D , WeinbergRA. Hallmarks of cancer: the next generation. Cell144(5), 646–674 (2011).
   PubMed Web of Science ®Google Scholar
• Núñez-Wehinger S , OrtizRJ, DíazN, DíazJ, Lobos-GonzálezL, QuestAF. Caveolin-1 in cell migration and metastasis. Curr. Mol. Med.14(2), 255–274 (2014).
   PubMedGoogle Scholar
• Díaz-Valdivia NI , DíazJ, ContrerasPet al. The non-receptor tyrosine phosphatase type 14 blocks caveolin-1-enhanced cancer cell metastasis. Oncogene39, 3693–3709 (2020).
   PubMedGoogle Scholar
• Urra H , TorresVA, OrtizRJet al. Caveolin-1-enhanced motility and focal adhesion turnover require tyrosine-14 but not accumulation to the rear in metastatic cancer cells. PLOS ONE7(4), e33085 (2012).
   PubMed Web of Science ®Google Scholar
• Campos A , Burgos-RavanalR, GonzálezMF, HuilcamanR, LobosGonzález L, QuestAFG. Cell intrinsic and extrinsic mechanisms of Caveolin-1-enhanced metastasis. Biomolecules9(8), 314 (2019).
   PubMed Web of Science ®Google Scholar
• Llorente A , de MarcoMC, AlonsoMA. Caveolin-1 and MAL are located on prostasomes secreted by the prostate cancer PC-3 cell line. J. Cell Sci.117(Pt 22), 5343–5351 (2004).
   PubMed Web of Science ®Google Scholar
• Logozzi M , DeMilito A, LuginiLet al. High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLOS ONE4(4), e5219–5229 (2009).
   PubMed Web of Science ®Google Scholar
• van Niel G , D’AngeloG, RaposoG. Shedding light on the cell biology of extracellular vesicles. Nat. Rev. Mol. Cell Biol.19(4), 213–218 (2018).
   PubMed Web of Science ®Google Scholar
• Zijlstra A , DiVizio D. Size matters in nanoscale communication. Nat. Cell Biol.20(3), 228–230 (2018).
   PubMed Web of Science ®Google Scholar
• Albacete-Albacete L , Navarro-LéridaI, LópezJAet al. ECM deposition is driven by caveolin-1-dependent regulation of exosomal biogenesis and cargo sorting. J. Cell Biol.219(11), e202006178 (2020).
   PubMedGoogle Scholar
• He M , QinH, PoonTCet al. Hepatocellular carcinoma-derived exosomes promote motility of immortalized hepatocyte through transfer of oncogenic proteins and RNAs. Carcinogenesis36(9), 1008–1018 (2015).
   PubMed Web of Science ®Google Scholar
• Campos A , SalomonC, BustosRet al. Caveolin-1-containing extracellular vesicles transport adhesion proteins and promote malignancy in breast cancer cell lines. Nanomedicine13(20), 2597–2609 (2018).
   PubMedGoogle Scholar
• Harris DA , PatelSH, GucekM, HendrixA, WestbroekW, TaraskaJW. Exosomes released from breast cancer carcinomas stimulate cell movement. PLOS ONE10(3), e0117495–e0117495 (2015).
   PubMed Web of Science ®Google Scholar
• Midwood KS , ChiquetM, TuckerRP, OrendG. Tenascin-C at a glance. J. Cell Sci.129(23), 4321–4327 (2016).
   PubMed Web of Science ®Google Scholar
• Chiquet-Ehrismann R , OrendG, ChiquetM, TuckerRP, MidwoodKS. Tenascins in stem cell niches. Matrix Biol.37, 112–123 (2014).
   PubMed Web of Science ®Google Scholar
• Midwood KS , HussenetT, LangloisB, OrendG. Advances in tenascin-C biology. Cell. Mol. Life Sci.68(19), 3175–3199 (2011).
   PubMed Web of Science ®Google Scholar
• Naik A , Al-YahyaeeA, AbdullahNet al. Neuropilin-1 promotes the oncogenic tenascin-C/integrin β3 pathway and modulates chemoresistance in breast cancer cells. BMC Cancer18(1), 533–533 (2018).
   PubMedGoogle Scholar
• Qian S , TanX, LiuX, LiuP, WuY. Exosomal Tenascin-C induces proliferation and invasion of pancreatic cancer cells by WNT signaling. Oncol. Targets Ther.12, 3197–3205 (2019).
   PubMed Web of Science ®Google Scholar
• Ji H , GreeningDW, BarnesTWet al. Proteome profiling of exosomes derived from human primary and metastatic colorectal cancer cells reveal differential expression of key metastatic factors and signal transduction components. Proteomics13(10–11), 1672–1686 (2013).
   PubMed Web of Science ®Google Scholar
• Zheng J , HernandezJM, DoussotAet al. Extracellular matrix proteins and carcinoembryonic antigen-related cell adhesion molecules characterize pancreatic duct fluid exosomes in patients with pancreatic cancer. HPB (Oxford)20(7), 597–604 (2018).
   PubMed Web of Science ®Google Scholar
• Filipe V , HaweA, JiskootW. Critical evaluation of nanoparticle tracking analysis (NTA) by NanoSight for the measurement of nanoparticles and protein aggregates. Pharmaceut. Res.27(5), 796–810 (2010).
   PubMed Web of Science ®Google Scholar
• Ros E , EncinaM, GonzálezFet al. Single cell migration profiling on a microenvironmentally tunable hydrogel microstructure device that enables stem cell potency evaluation. Lab Chip20(5), 958–972 (2020).
   PubMedGoogle Scholar
• Cooper JA . Effects of cytochalasin and phalloidin on actin. J. Cell Biol.105(4), 1473–1478 (1987).
   PubMed Web of Science ®Google Scholar
• Albacete-Albacete L , Sánchez-ÁlvarezM, DelPozo MA. Extracellular vesicles: an emerging mechanism governing the secretion and biological roles of tenascin-C. Front. Immunol.12, Doi: 10.3389/fimmu.2021.671485 (2021).
   PubMedGoogle Scholar
• Brösicke N , van LandeghemFK, SchefflerB, FaissnerA. Tenascin-C is expressed by human glioma in vivo and shows a strong association with tumor blood vessels. Cell Tissue Res.354(2), 409–430 (2013).
   PubMedGoogle Scholar
• List of top 100 proteins that are often identified in exosomes. http://exocarta.org/exosome_markers_new
   Google Scholar
• Borsi L , CarnemollaB, NicolòG, SpinaB, TanaraG, ZardiL. Expression of different tenascin isoforms in normal, hyperplastic and neoplastic human breast tissues. Int. J. Cancer52(5), 688–692 (1992).
   PubMedGoogle Scholar
• Lin C-J , YunE-J, LoUGet al. The paracrine induction of prostate cancer progression by caveolin-1. Cell Death Dis.10(11), 834–834 (2019).
   PubMedGoogle Scholar
• Kia V , MortazaviY, ParyanM, BiglariA, Mohammadi-YeganehS. Exosomal miRNAs from highly metastatic cells can induce metastasis in non-metastatic cells. Life Sci.220, 162–168 (2019).
   PubMedGoogle Scholar
• Fuentes P , SeséM, GuijarroPJet al. ITGB3-mediated uptake of small extracellular vesicles facilitates intercellular communication in breast cancer cells. Nat. Commun.11(1), 4261 (2020).
   PubMedGoogle Scholar
• Mulcahy LA , PinkRC, CarterDRF. Routes and mechanisms of extracellular vesicle uptake. J. Extracel. Vesicles3, Doi: 10.3402/jev.v3.24641 (2014).
   PubMedGoogle Scholar
• Montecalvo A , LarreginaAT, ShufeskyWJet al. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood119(3), 756–766 (2012).
   PubMed Web of Science ®Google Scholar
• Svensson KJ , ChristiansonHC, WittrupAet al. Exosome uptake depends on ERK1/2-heat shock protein 27 signaling and lipid Raft-mediated endocytosis negatively regulated by caveolin-1. J. Biol. Chem.288(24), 17713–17724 (2013).
   PubMed Web of Science ®Google Scholar
• Bonsergent E , GrisardE, BuchrieserJ, SchwartzO, ThéryC, LavieuG. Quantitative characterization of extracellular vesicle uptake and content delivery within mammalian cells. Nat. Commun.12(1), 1864 (2021).
   PubMed Web of Science ®Google Scholar
• Ramírez-Ricardo J , Leal-OrtaE, Martínez-BaezaEet al. Circulating extracellular vesicles from patients with breast cancer enhance migration and invasion via a Src-dependent pathway in MDA-MB-231 breast cancer cells. Mol. Med. Rep.22(3), 1932–1948 (2020).
   PubMed Web of Science ®Google Scholar
• Hirose H , HiraiY, SasakiM, SawaH, FutakiS. Quantitative analysis of extracellular vesicle uptake and fusion with recipient cells. Bioconjug. Chem.33(10), 1852–1859 (2022).
   PubMedGoogle Scholar
• O’Brien K , UghettoS, MahjoumS, NairAV, BreakefieldXO. Uptake, functionality, and re-release of extracellular vesicle-encapsulated cargo. Cell Rep.39(2), Doi: 10.1016/j.celrep.2022.110651 (2022).
   PubMedGoogle Scholar
• Sheen-Chen S-M , LiuY-W, SunC-Ket al. Abdominal carcinomatosis attributed to metastatic breast carcinoma. Dig. Dis. Sci.53(11), 3043–3045 (2008).
   PubMedGoogle Scholar
• Cardi M , SammartinoP, FramarinoMLet al. Treatment of peritoneal carcinomatosis from breast cancer by maximal cytoreduction and HIPEC: a preliminary report on 5 cases. Breast22(5), 845–849 (2013).
   PubMedGoogle Scholar
• Bertozzi S , LonderoAP, CedoliniCet al. Prevalence, risk factors, and prognosis of peritoneal metastasis from breast cancer. SpringerPlus4(1), 688 (2015).
   PubMedGoogle Scholar
• Stollfuss J , LandvogtN, AbensteinMet al. Non-invasive imaging of implanted peritoneal carcinomatosis in mice using PET and bioluminescence imaging. EJNMMI Res.5(1), 44 (2015).
   PubMedGoogle Scholar
• Aslakson CJ , MillerFR. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res.52(6), 1399–1405 (1992).
   PubMed Web of Science ®Google Scholar
• Taneja P , FrazierDP, KendigRDet al. MMTV mouse models and the diagnostic values of MMTV-like sequences in human breast cancer. Expert Rev. Mol. Diagn.9(5), 423–440 (2009).
   PubMed Web of Science ®Google Scholar
• Ceelen WP , LevineE ( Eds). Intraperitoneal Cancer Therapy: Principles and Practice (1st Edition).CRC Press, FL, USA (2015).
   Google Scholar
• Lundström A , HolmbomJ, LindqvistC, NordströmT. The role of alpha2 beta1 and alpha3 beta1 integrin receptors in the initial anchoring of MDA-MB-231 human breast cancer cells to cortical bone matrix. Biochem. Biophys. Res. Commun.250(3), 735–740 (1998).
   PubMedGoogle Scholar
• Lokmic Z , LämmermannT, SixtM, CardellS, HallmannR, SorokinL. The extracellular matrix of the spleen as a potential organizer of immune cell compartments. Semin. Immunol.20(1), 4–13 (2008).
   PubMedGoogle Scholar
• Nagaharu K , ZhangX, YoshidaTet al. Tenascin C induces epithelial-mesenchymal transition-like change accompanied by SRC activation and focal adhesion kinase phosphorylation in human breast cancer cells. Am. J. Pathol.178(2), 754–763 (2011).
   PubMedGoogle Scholar
• Mirzaei R , SarkarS, DzikowskiLet al. Brain tumor-initiating cells export tenascin-C associated with exosomes to suppress T cell activity. OncoImmunology7(10), e1478647 (2018).
   PubMed Web of Science ®Google Scholar
• Liu Y , CaoX. Characteristics and significance of the pre-metastatic niche. Cancer Cell30(5), 668–681 (2016).
   PubMed Web of Science ®Google Scholar
• Peinado H , ZhangH, MateiIRet al. Pre-metastatic niches: organ-specific homes for metastases. Nat. Rev. Cancer17(5), 302–317 (2017).
   PubMed Web of Science ®Google Scholar
• Doglioni G , ParikS, FendtSM. Interactions in the (pre)metastatic niche support metastasis formation. Front. Oncol.9, 219 (2019).
   PubMed Web of Science ®Google Scholar
• Dong Q , LiuX, ChengK, ShengJ, KongJ, LiuT. Pre-metastatic niche formation in different organs induced by tumor extracellular vesicles. Front. Cell Dev. Biol.9, Doi: 10.3389/fcell.2021.733627 (2021).
   Google Scholar
• Wolf T , BaierSR, ZempleniJ. The intestinal transport of bovine milk exosomes is mediated by endocytosis in human colon carcinoma Caco-2 cells and rat small intestinal IEC-6 cells. J. Nutr.145(10), 2201–2206 (2015).
   PubMed Web of Science ®Google Scholar
• Calvo A , CatenaR, NobleMSet al. Identification of VEGF-regulated genes associated with increased lung metastatic potential: functional involvement of tenascin-C in tumor growth and lung metastasis. Oncogene27(40), 5373–5384 (2008).
   PubMedGoogle Scholar
• Tanaka K , HiraiwaN, HashimotoH, YamazakiY, KusakabeM. Tenascin-C regulates angiogenesis in tumor through the regulation of vascular endothelial growth factor expression. Int. J. Cancer108(1), 31–40 (2004).
   PubMedGoogle Scholar
• Srikrishna G . S100A8 and S100A9: new insights into their roles in malignancy. J. Innate Immun.4(1), 31–40 (2012).
   PubMed Web of Science ®Google Scholar