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Oncology

Endothelial-to-mesenchymal transition in tumour progression and its potential roles in tumour therapy

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Pages 1058-1069 | Received 29 Apr 2022, Accepted 08 Feb 2023, Published online: 13 Mar 2023

References

  • Maman S, Witz IP. A history of exploring cancer in context. Nat Rev Cancer. 2018;18(6):359–376.
  • DeBerardinis RJ. Tumor microenvironment, metabolism, and immunotherapy. N Engl J Med. 2020;382(9):869–871.
  • Ho WJ, Jaffee EM, Zheng L. The tumour microenvironment in pancreatic cancer - clinical challenges and opportunities. Nat Rev Clin Oncol. 2020;17(9):527–540.
  • Archetti M, Pienta KJ. Cooperation among cancer cells: applying game theory to cancer. Nat Rev Cancer. 2019;19(2):110–117.
  • Zhang Z, Karthaus WR, Lee YS, et al. Tumor microenvironment-derived NRG1 promotes antiandrogen resistance in prostate cancer. Cancer Cell. 2020;38(2):279–296.
  • Taniguchi S, Elhance A, Van Duzer A, et al. Tumor-initiating cells establish an IL-33-TGF-β niche signaling loop to promote cancer progression. Science. 2020;369(6501):269–281.
  • Hida K, Klagsbrun M. A new perspective on tumor endothelial cells: unexpected chromosome and centrosome abnormalities. Cancer Res. 2005;65(7):2507–2510.
  • Weis SM, Cheresh DA. Tumor angiogenesis: molecular pathways and therapeutic targets. Nat Med. 2011;17(11):1359–1370.
  • Shashni B, Nishikawa Y, Nagasaki Y. Management of tumor growth and angiogenesis in triple-negative breast cancer by using redox nanoparticles. Biomaterials. 2021;269:120645.
  • Li Y, Qu X, Cao B, et al. Selectively suppressing tumor angiogenesis for targeted breast cancer therapy by genetically engineered phage. Adv Mater. 2020;32(29):e2001260.
  • Piera-Velazquez S, Jimenez SA. Endothelial to mesenchymal transition: role in physiology and in the pathogenesis of human diseases. Physiol Rev. 2019;99(2):1281–1324.
  • Li Y, Lui KO, Zhou B. Reassessing endothelial-to-mesenchymal transition in cardiovascular diseases. Nat Rev Cardiol. 2018;15(8):445–456.
  • Platel V, Faure S, Corre I. Endothelial-to-mesenchymal transition (EndoMT): roles in tumorigenesis, metastatic extravasation and therapy resistance. J Oncol. 2019;2019:8361945.
  • Zeisberg EM, Tarnavski O, Zeisberg M, et al. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med. 2007;13(8):952–961.
  • Kovacic JC, Dimmeler S, Harvey RP, et al. Endothelial to mesenchymal transition in cardiovascular disease: JACC state-of-the-art review. J Am Coll Cardiol. 2019;73(2):190–209.
  • Lecce L, Xu Y, V'Gangula B, et al. Histone deacetylase 9 promotes endothelial-mesenchymal transition and an unfavorable atherosclerotic plaque phenotype. J Clin Invest. 2021;131(15):e131178.
  • Otsuki S, Saito T, Taylor S, et al. Monocyte-released HERV-K dUTPase engages TLR4 and MCAM causing endothelial mesenchymal transition. JCI Insight. 2021;6(15):e146416.
  • Wang Z, Calpe B, Zerdani J, et al. High-throughput investigation of endothelial-to-mesenchymal transformation (EndMT) with combinatorial cellular microarrays. Biotechnol Bioeng. 2016;113(7):1403–1412.
  • Mina SG, Huang P, Murray BT, et al. The role of shear stress and altered tissue properties on endothelial to mesenchymal transformation and tumor-endothelial cell interaction. Biomicrofluidics. 2017;11(4):044104.
  • Zhang ZH, Miao YY, Ke BL, et al. LY2109761, transforming growth factor β receptor type I and type II dual inhibitor, is a novel approach to suppress endothelial mesenchymal transformation in human corneal endothelial cells. Cell Physiol Biochem. 2018;50(3):963–972.
  • Balachandran K, Alford PW, Wylie-Sears J, et al. Cyclic strain induces dual-mode endothelial-mesenchymal transformation of the cardiac valve. Proc Natl Acad Sci U S A. 2011;108(50):19943–19948.
  • Akatsu Y, Takahashi N, Yoshimatsu Y, et al. Fibroblast growth factor signals regulate transforming growth factor-β-induced endothelial-to-myofibroblast transition of tumor endothelial cells via Elk1. Mol Oncol. 2019;13(8):1706–1724.
  • Liu T, Ma W, Xu H, et al. PDGF-mediated mesenchymal transformation renders endothelial resistance to anti-VEGF treatment in glioblastoma. Nat Commun. 2018;9(1):3439.
  • Marin-Ramos NI, Jhaveri N, Thein TZ, et al. NEO212, a conjugate of temozolomide and perillyl alcohol, blocks the endothelial-to-mesenchymal transition in tumor-associated brain endothelial cells in glioblastoma. Cancer Lett. 2019;442:170–180.
  • Zeisberg EM, Potenta S, Xie L, et al. Discovery of endothelial to mesenchymal transition as a source for carcinoma-associated fibroblasts. Cancer Res. 2007;67(21):10123–10128.
  • Gasperini P, Espigol-Frigole G, McCormick PJ, et al. Kaposi sarcoma herpesvirus promotes endothelial-to-mesenchymal transition through notch-dependent signaling. Cancer Res. 2012;72(5):1157–1169.
  • Fan CS, Chen LL, Hsu TA, et al. Endothelial-mesenchymal transition harnesses HSP90alpha-secreting M2-macrophages to exacerbate pancreatic ductal adenocarcinoma. J Hematol Oncol. 2019;12(1):138.
  • Garcia J, Sandi MJ, Cordelier P, et al. Tie1 deficiency induces endothelial-mesenchymal transition. EMBO Rep. 2012;13(5):431–439.
  • Zhu K, Pan Q, Jia LQ, et al. MiR-302c inhibits tumor growth of hepatocellular carcinoma by suppressing the endothelial-mesenchymal transition of endothelial cells. Sci Rep. 2014;4:5524.
  • Nie L, Lyros O, Medda R, et al. Endothelial-mesenchymal transition in normal human esophageal endothelial cells cocultured with esophageal adenocarcinoma cells: role of IL-1β and TGF-β2. Am J Physiol Cell Physiol. 2014;307(9):C859–C877.
  • Ghiabi P, Jiang J, Pasquier J, et al. Breast cancer cells promote a notch-dependent mesenchymal phenotype in endothelial cells participating to a pro-tumoral niche. J Transl Med. 2015;13:27.
  • Huang M, Liu T, Ma P, et al. c-Met-mediated endothelial plasticity drives aberrant vascularization and chemoresistance in glioblastoma. J Clin Invest. 2016;126(5):1801–1814.
  • Choi SH, Kim AR, Nam JK, et al. Tumour-vasculature development via endothelial-to-mesenchymal transition after radiotherapy controls CD44v6(+) cancer cell and macrophage polarization. Nat Commun. 2018;9(1):5108.
  • Fan CS, Chen WS, Chen LL, et al. Osteopontin-integrin engagement induces HIF-1alpha-TCF12-mediated endothelial-mesenchymal transition to exacerbate colorectal cancer. Oncotarget. 2018;9(4):4998–5015.
  • Zhang T, Zhang L, Gao Y, et al. Role of aneuploid circulating tumor cells and CD31(+) circulating tumor endothelial cells in predicting and monitoring anti-angiogenic therapy efficacy in advanced NSCLC. Mol Oncol. 2021;15(11):2891–2909.
  • Wang G, Yang Q, Li M, et al. Quantitative proteomic profiling of tumor-associated vascular endothelial cells in colorectal cancer. Biol Open. 2019;8(5):bio042838.
  • Wang H, Feng C, Lu M, et al. Integrative single-cell transcriptome analysis reveals a subpopulation of fibroblasts associated with favorable prognosis of liver cancer patients. Transl Oncol. 2021;14(1):100981.
  • Cai W, Sun X, Jin F, et al. PERK-eIF2α-ERK1/2 axis drives mesenchymal-endothelial transition of cancer-associated fibroblasts in pancreatic cancer. Cancer Lett. 2021;515:86–95.
  • Xiao L, Kim DJ, Davis CL, et al. Tumor endothelial cells with distinct patterns of TGFβ-driven endothelial-to-mesenchymal transition. Cancer Res. 2015;75(7):1244–1254.
  • Armingol E, Officer A, Harismendy O, et al. Deciphering cell-cell interactions and communication from gene expression. Nat Rev Genet. 2021;22(2):71–88.
  • Krizbai IA, Gasparics Á, Nagyőszi P, et al. Endothelial-mesenchymal transition of brain endothelial cells: possible role during metastatic extravasation. PLoS One. 2015;10(3):e0119655.
  • Wawro ME, Chojnacka K, Wieczorek-Szukała K, et al. Invasive colon cancer cells induce transdifferentiation of endothelium to cancer-associated fibroblasts through microtubules enriched in tubulin-β3. Int J Mol Sci. 2018;20(1):53.
  • Ciszewski WM, Sobierajska K, Wawro ME, et al. The ILK-MMP9-MRTF axis is crucial for EndMT differentiation of endothelial cells in a tumor microenvironment. Biochim Biophys Acta Mol Cell Res. 2017;1864(12):2283–2296.
  • Yoshimatsu Y, Wakabayashi I, Kimuro S, et al. TNF-α enhances TGF-β-induced endothelial-to-mesenchymal transition via TGF-β signal augmentation. Cancer Sci. 2020;111(7):2385–2399.
  • Wu DM, Liu T, Deng SH, et al. Alpha-1 antitrypsin induces epithelial-to-mesenchymal transition, endothelial-to-mesenchymal transition, and drug resistance in lung cancer cells. Onco Targets Ther. 2020;13:3751–3763.
  • Kalluri R, LeBleu VS. The biology, function, and biomedical applications of exosomes. Science. 2020;367(6478):eaau6977.
  • Yeon JH, Jeong HE, Seo H, et al. Cancer-derived exosomes trigger endothelial to mesenchymal transition followed by the induction of cancer-associated fibroblasts. Acta Biomater. 2018;76:146–153.
  • Yamada NO, Heishima K, Akao Y, et al. Extracellular vesicles containing microRNA-92a-3p facilitate partial endothelial-mesenchymal transition and angiogenesis in endothelial cells. Int J Mol Sci. 2019;20(18):4406.
  • Kim J, Lee C, Kim I, et al. Three-dimensional human liver-chip emulating premetastatic niche formation by breast cancer-derived extracellular vesicles. ACS Nano. 2020;14(11):14971–14988.
  • Omori K, Morikawa T, Kunita A, et al. Lipocalin-type prostaglandin D synthase-derived PGD(2) attenuates malignant properties of tumor endothelial cells. J Pathol. 2018;244(1):84–96.
  • Wawro ME, Sobierajska K, Ciszewski WM, et al. Nonsteroidal anti-inflammatory drugs prevent vincristine-dependent cancer-associated fibroblasts formation. Int J Mol Sci. 2019;20(8):1941.
  • Jiao K, Zhen J, Wu M, et al. 27-Hydroxycholesterol-induced EndMT acts via STAT3 signaling to promote breast cancer cell migration by altering the tumor microenvironment. Cancer Biol Med. 2020;17(1):88–100.
  • Banerjee D, Barton SM, Grabham PW, et al. High-dose radiation increases Notch1 in tumor vasculature. Int J Radiat Oncol Biol Phys. 2020;106(4):857–866.
  • Yin Z, Dong C, Jiang K, et al. Heterogeneity of cancer-associated fibroblasts and roles in the progression, prognosis, and therapy of hepatocellular carcinoma. J Hematol Oncol. 2019;12(1):101.
  • Sahai E, Astsaturov I, Cukierman E, et al. A framework for advancing our understanding of cancer-associated fibroblasts. Nat Rev Cancer. 2020;20(3):174–186.
  • Kobayashi H, Enomoto A, Woods SL, et al. Cancer-associated fibroblasts in gastrointestinal cancer. Nat Rev Gastroenterol Hepatol. 2019;16(5):282–295.
  • Ishii G, Ochiai A, Neri S. Phenotypic and functional heterogeneity of cancer-associated fibroblast within the tumor microenvironment. Adv Drug Deliv Rev. 2016;99(Pt B):186–196.
  • Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–674.
  • Li Z, Di C, Li S, et al. Smart nanotherapeutic targeting of tumor vasculature. Acc Chem Res. 2019;52(9):2703–2712.
  • Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell. 2011;147(2):275–292.
  • Yang J, Antin P, Berx G, et al. Guidelines and definitions for research on epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 2020;21(6):341–352.
  • Smeda M, Kieronska A, Adamski MG, et al. Nitric oxide deficiency and endothelial-mesenchymal transition of pulmonary endothelium in the progression of 4T1 metastatic breast cancer in mice. Breast Cancer Res. 2018;20(1):86.
  • Krizbai IA, Gasparics A, Nagyoszi P, et al. Endothelial-mesenchymal transition of brain endothelial cells: possible role during metastatic extravasation. PLoS One. 2015;10(3):e0123845.
  • Ribas A. Adaptive immune resistance: how cancer protects from immune attack. Cancer Discov. 2015;5(9):915–919.
  • Liu X, Hoft DF, Peng G. Tumor microenvironment metabolites directing T cell differentiation and function. Trends Immunol. 2022;43(2):132–147.
  • Riegler J, Gill H, Ogasawara A, et al. VCAM-1 density and tumor perfusion predict T-cell infiltration and treatment response in preclinical models. Neoplasia. 2019;21(10):1036–1050.
  • Mao X, Xu J, Wang W, et al. Crosstalk between cancer-associated fibroblasts and immune cells in the tumor microenvironment: new findings and future perspectives. Mol Cancer. 2021;20(1):131.
  • Lin PP. Aneuploid circulating tumor-derived endothelial cell (CTEC): a novel versatile player in tumor neovascularization and cancer metastasis. Cells. 2020;9(6):1539.
  • Chua KV, Fan CS, Chen CC, et al. Octyl gallate induces pancreatic ductal adenocarcinoma cell apoptosis and suppresses endothelial-mesenchymal transition-promoted M2-macrophages, HSP90α secretion, and tumor growth. Cells. 2019;9(1):91.