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Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
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Role of extrinsic physical cues in cancer progression

  • Ok-Hyeon Kim (Department of Anatomy and Cell Biology, College of Medicine, Chung-Ang University) ;
  • Tae Jin Jeon (Department of Global Innovative Drugs, Graduate School of Chung-Ang University) ;
  • Yong Kyoo Shin (Department of Pharmacology, College of Medicine, Chung-Ang University) ;
  • Hyun Jung Lee (Department of Anatomy and Cell Biology, College of Medicine, Chung-Ang University)
  • Received : 2023.02.18
  • Accepted : 2023.04.06
  • Published : 2023.05.31
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Abstract

The tumor microenvironment (TME) is a complex system composed of many cell types and an extracellular matrix (ECM). During tumorigenesis, cancer cells constantly interact with cellular components, biochemical cues, and the ECM in the TME, all of which make the environment favorable for cancer growth. Emerging evidence has revealed the importance of substrate elasticity and biomechanical forces in tumor progression and metastasis. However, the mechanisms underlying the cell response to mechanical signals-such as extrinsic mechanical forces and forces generated within the TME-are still relatively unknown. Moreover, having a deeper understanding of the mechanisms by which cancer cells sense mechanical forces and transmit signals to the cytoplasm would substantially help develop effective strategies for cancer treatment. This review provides an overview of biomechanical forces in the TME and the intracellular signaling pathways activated by mechanical cues as well as highlights the role of mechanotransductive pathways through mechanosensors that detect the altering biomechanical forces in the TME.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korean government (Grant No. 2020R1A2C2011617) and a Chung-Ang University Research Grant in 2021.

References

  1. Mansouri S, Heylmann D, Stiewe T et al (2022) Cancer genome and tumor microenvironment: reciprocal crosstalk shapes lung cancer plasticity. Elife 11, e79895
  2. Jahanban-Esfahlan R, Seidi K, Banimohamad-Shotorbani B, Jahanban-Esfahlan A and Yousefi B (2018) Combination of nanotechnology with vascular targeting agents for effective cancer therapy. J Cell Physiol 233, 2982-2992 https://doi.org/10.1002/jcp.26051
  3. Brown JM and Wilson WR (2004) Exploiting tumour hypoxia in cancer treatment. Nat Rev Cancer 4, 437-447 https://doi.org/10.1038/nrc1367
  4. Moraes C, Sun Y and Simmons CA (2011) (Micro) managing the mechanical microenvironment. Integr Biol (Camb) 3, 959-971 https://doi.org/10.1039/c1ib00056j
  5. Ladoux B and Mege RM (2017) Mechanobiology of collective cell behaviours. Nat Rev Mol Cell Biol 18, 743-757 https://doi.org/10.1038/nrm.2017.98
  6. Jain RK, Martin JD and Stylianopoulos T (2014) The role of mechanical forces in tumor growth and therapy. Annu Rev Biomed Eng 16, 321-346 https://doi.org/10.1146/annurev-bioeng-071813-105259
  7. Jang I and Beningo KA (2019) Integrins, CAFs and mechanical forces in the progression of cancer. Cancers 11, 721
  8. Henke E, Nandigama R and Ergun S (2020) Extracellular matrix in the tumor microenvironment and its impact on cancer therapy. Front Mol Biosci 6, 160
  9. Theocharis AD, Skandalis SS, Gialeli C and Karamanos NK (2016) Extracellular matrix structure. Adv Drug Deliv Rev 97, 4-27 https://doi.org/10.1016/j.addr.2015.11.001
  10. Huang J, Zhang L, Wan D et al (2021) Extracellular matrix and its therapeutic potential for cancer treatment. Signal Transduct Targeted Ther 6, 153
  11. Paszek MJ, Zahir N, Johnson KR et al (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241-254 https://doi.org/10.1016/j.ccr.2005.08.010
  12. Shieh AC (2011) Biomechanical forces shape the tumor microenvironment. Ann Biomed Eng 39, 1379-1389 https://doi.org/10.1007/s10439-011-0252-2
  13. Yu H, Mouw JK and Weaver VM (2011) Forcing form and function: biomechanical regulation of tumor evolution. Trends Cell Biol 21, 47-56 https://doi.org/10.1016/j.tcb.2010.08.015
  14. Levental KR, Yu H, Kass L et al (2009) Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906 https://doi.org/10.1016/j.cell.2009.10.027
  15. Hynes RO (2009) The extracellular matrix: not just pretty fibrils. Science 326, 1216-1219 https://doi.org/10.1126/science.1176009
  16. Northey JJ, Przybyla L and Weaver VM (2017) Tissue force programs cell fate and tumor aggression. Cancer Discov 7, 1224-1237 https://doi.org/10.1158/2159-8290.CD-16-0733
  17. Pang M, Teng Y, Huang J, Yuan Y, Lin F and Xiong C (2017) Substrate stiffness promotes latent TGF-beta1 activation in hepatocellular carcinoma. Biochem Biophys Res Commun 483, 553-558 https://doi.org/10.1016/j.bbrc.2016.12.107
  18. Le LT, Cazares O, Mouw JK et al (2016) Loss of miR-203 regulates cell shape and matrix adhesion through ROBO1/Rac/FAK in response to stiffness. J Cell Biol 212, 707-719 https://doi.org/10.1083/jcb.201507054
  19. Kanematsu A, Marui A, Yamamoto S et al (2004) Type I collagen can function as a reservoir of basic fibroblast growth factor. J Control Release 99, 281-292 https://doi.org/10.1016/j.jconrel.2004.07.008
  20. Noguchi S, Saito A and Nagase T (2018) YAP/TAZ signaling as a molecular link between fibrosis and cancer. Int J Mol Sci 19, 3674
  21. Scott KE, Fraley SI and Rangamani P (2021) A spatial model of YAP/TAZ signaling reveals how stiffness, dimensionality, and shape contribute to emergent outcomes. Proc Natl Acad Sci U S A 118, e2021571118
  22. Sousa-Squiavinato ACM, Rocha MR, Barcellos-de-Souza P, de Souza WF and Morgado-Diaz JA (2019) Cofilin-1 signaling mediates epithelial-mesenchymal transition by promoting actin cytoskeleton reorganization and cell-cell adhesion regulation in colorectal cancer cells. Biochim Biophys Acta Mol Cell Res 1866, 418-429 https://doi.org/10.1016/j.bbamcr.2018.10.003
  23. Huang Q, Hu X, He W et al (2018) Fluid shear stress and tumor metastasis. Am J Cancer Res 8, 763-777
  24. Tian BR, Lin WF and Zhang Y (2021) Effects of biomechanical forces on the biological behavior of cancer stem cells. J Cancer 12, 5895-5902 https://doi.org/10.7150/jca.60893
  25. Stylianopoulos T (2017) The solid mechanics of cancer and strategies for improved therapy. J Biomech Eng 139, 10.115/1.4034991
  26. Helmlinger G, Netti PA, Lichtenbeld HC, Melder RJ and Jain RK (1997) Solid stress inhibits the growth of multicellular tumor spheroids. Nat Biotechnol 15, 778-783 https://doi.org/10.1038/nbt0897-778
  27. Walsh MF, Woo RK, Gomez R and Basson MD (2004) Extracellular pressure stimulates colon cancer cell proliferation via a mechanism requiring PKC and tyrosine kinase signals. Cell Prolif 37, 427-441 https://doi.org/10.1111/j.1365-2184.2004.00324.x
  28. Kalli M, Minia A, Pliaka V, Fotis C, Alexopoulos LG and Stylianopoulos T (2019) Solid stress-induced migration is mediated by GDF15 through Akt pathway activation in pancreatic cancer cells. Sci Rep 9, 978
  29. Carmeliet P (2005) VEGF as a key mediator of angiogenesis in cancer. Oncology 69, 4-10 https://doi.org/10.1159/000088478
  30. Less JR, Posner MC, Skalak TC, Wolmark N and Jain RK (1997) Geometric resistance and microvascular network architecture of human colorectal carcinoma. Microcirculation 4, 25-33 https://doi.org/10.3109/10739689709148315
  31. Sun C, Jain RK and Munn LL (2007) Non-uniform plasma leakage affects local hematocrit and blood flow: implications for inflammation and tumor perfusion. Ann Biomed Eng 35, 2121-2129 https://doi.org/10.1007/s10439-007-9377-8
  32. Bacac M and Stamenkovic I (2008) Metastatic Cancer Cell. Ann Rev Pathol Mech 3, 221-247 https://doi.org/10.1146/annurev.pathmechdis.3.121806.151523
  33. Lee HJ, Diaz MF, Price KM et al (2017) Fluid shear stress activates YAP1 to promote cancer cell motility. Nat Commun 8, 14122
  34. Triantafillu UL, Park S, Klaassen NL, Raddatz AD and Kim Y (2017) Fluid shear stress induces cancer stem cell-like phenotype in MCF7 breast cancer cell line without inducing epithelial to mesenchymal transition. Int J Oncol 50, 993-1001 https://doi.org/10.3892/ijo.2017.3865
  35. Wang Y, Goliwas KF, Severino PE et al (2020) Mechanical strain induces phenotypic changes in breast cancer cells and promotes immunosuppression in the tumor microenvironment. Lab Invest 100, 1503-1516 https://doi.org/10.1038/s41374-020-0452-1
  36. Ross TD, Coon BG, Yun S et al (2013) Integrins in mechanotransduction. Curr Opin Cell Biol 25, 613-618 https://doi.org/10.1016/j.ceb.2013.05.006
  37. Montagner M and Dupont S (2020) Mechanical forces as determinants of disseminated metastatic cell fate. Cells 9, 250
  38. Jiang L, Zhao YD and Chen WX (2017) The function of the novel mechanical activated ion channel Piezo1 in the human osteosarcoma cells. Med Sci Monit 23, 5070-5082 https://doi.org/10.12659/MSM.906959
  39. Li X and Wang J (2020) Mechanical tumor microenvironment and transduction: cytoskeleton mediates cancer cell invasion and metastasis. Int J Biol Sci 16, 2014-2028 https://doi.org/10.7150/ijbs.44943
  40. Pang MF, Siedlik MJ, Han S, Stallings-Mann M, Radisky DC and Nelson CM (2016) Tissue stiffness and hypoxia modulate the integrin-linked kinase ILK to control breast cancer stem-like cells. Cancer Res 76, 5277-5287 https://doi.org/10.1158/0008-5472.CAN-16-0579
  41. Zhao F, Li L, Guan L, Yang H, Wu C and Liu Y (2014) Roles for GP IIb/IIIa and alphavbeta3 integrins in MDA-MB-231 cell invasion and shear flow-induced cancer cell mechanotransduction. Cancer Lett 344, 62-73 https://doi.org/10.1016/j.canlet.2013.10.019
  42. Artym VV, Swatkoski S, Matsumoto K et al (2015) Dense fibrillar collagen is a potent inducer of invadopodia via a specific signaling network. J Cell Biol 208, 331-350 https://doi.org/10.1083/jcb.201405099
  43. Le HQ, Ghatak S, Yeung CYC et al (2016) Mechanical regulation of transcription controls polycomb-mediated gene silencing during lineage commitment. Nat Cell Biol 18, 864-875 https://doi.org/10.1038/ncb3387
  44. Vangeel L and Voets T (2019) Transient receptor potential channels and calcium signaling. Cold Spring Harb Perspect Biol 11, a035048
  45. Pedersen SF, Owsianik G and Nilius B (2005) TRP channels: an overview. Cell Calcium 38, 233-252 https://doi.org/10.1016/j.ceca.2005.06.028
  46. Santoni G, Farfariello V and Amantini C (2011) TRPV channels in tumor growth and progression. Adv Exp Med Biol 704, 947-967 https://doi.org/10.1007/978-94-007-0265-3_49
  47. Yang D and Kim J (2020) Emerging role of transient receptor potential (TRP) channels in cancer progression. BMB Rep 53, 125-132 https://doi.org/10.5483/BMBRep.2020.53.3.016
  48. Nagasawa M and Kojima I (2015) Translocation of TRPV2 channel induced by focal administration of mechanical stress. Physiol Rep 3, e12296
  49. Lee WH, Choong LY, Mon NN et al (2016) TRPV4 regulates breast cancer cell extravasation, stiffness and actin cortex. Sci Rep 6, 27903
  50. Dalghi MG, Clayton DR, Ruiz WG et al (2019) Expression and distribution of PIEZO1 in the mouse urinary tract. Am J Physiol Renal Physiol 317, F303-F321 https://doi.org/10.1152/ajprenal.00214.2019
  51. Hegarty PK, Watson RW, Coffey RN, Webber MM and Fitzpatrick JM (2002) Effects of cyclic stretch on prostatic cells in culture. J Urol 168, 2291-2295 https://doi.org/10.1016/S0022-5347(05)64373-X
  52. Hoyt K, Castaneda B, Zhang M et al (2008) Tissue elasticity properties as biomarkers for prostate cancer. Cancer Biomark 4, 213-225 https://doi.org/10.3233/CBM-2008-44-505
  53. Wadhera P (2013) An introduction to acinar pressures in BPH and prostate cancer. Nat Rev Urol 10, 358-366 https://doi.org/10.1038/nrurol.2013.86
  54. Kim OH, Choi YW, Park JH et al (2022) Fluid shear stress facilitates prostate cancer metastasis through Piezo1-Src-YAP axis. Life Sci 308, 120936
  55. Luo M, Cai G, Ho KKY et al (2022) Compression enhances invasive phenotype and matrix degradation of breast cancer cells via Piezo1 activation. BMC Mol Cell Biol 23, 1
  56. De Felice D and Alaimo A (2020) Mechanosensitive piezo channels in cancer: focus on altered calcium signaling in cancer cells and in tumor progression. Cancers (Basel) 12, 1780
  57. Pardo-Pastor C, Rubio-Moscardo F, Vogel-Gonzalez M et al (2018) Piezo2 channel regulates RhoA and actin cytoskeleton to promote cell mechanobiological responses. Proc Natl Acad Sci U S A 115, 1925-1930 https://doi.org/10.1073/pnas.1718177115
  58. Chen X, Wanggou S, Bodalia A et al (2018) A feedforward mechanism mediated by mechanosensitive ion channel piezo1 and tissue mechanics promotes glioma aggression. Neuron 100, 799-815 https://doi.org/10.1016/j.neuron.2018.09.046
  59. Chaudhary PK and Kim S (2021) An insight into GPCR and G-proteins as cancer drivers. Cells 10, 3288
  60. Rosenbaum DM, Rasmussen SG and Kobilka BK (2009) The structure and function of G-protein-coupled receptors. Nature 459, 356-363 https://doi.org/10.1038/nature08144
  61. Venkatakrishnan AJ, Deupi X, Lebon G, Tate CG, Schertler GF and Babu MM (2013) Molecular signatures of G-protein-coupled receptors. Nature 494, 185-194 https://doi.org/10.1038/nature11896
  62. O'Hayre M, Degese MS and Gutkind JS (2014) Novel insights into G protein and G protein-coupled receptor signaling in cancer. Curr Opin Cell Biol 27, 126-135 https://doi.org/10.1016/j.ceb.2014.01.005
  63. Balkwill F (2004) Cancer and the chemokine network. Nat Rev Cancer 4, 540-550 https://doi.org/10.1038/nrc1388
  64. Xu J, Mathur J, Vessieres E et al (2018) GPR68 senses flow and is essential for vascular physiology. Cell 173, 762-775 e716
  65. Wei WC, Bianchi F, Wang YK, Tang MJ, Ye H and Glitsch MD (2018) Coincidence detection of membrane stretch and extracellular pH by the proton-sensing receptor OGR1 (GPR68). Curr Biology 28, 3815-3823 https://doi.org/10.1016/j.cub.2018.10.046
  66. Yang N, Chen T, Wang L et al (2020) CXCR4 mediates matrix stiffness-induced downregulation of UBTD1 driving hepatocellular carcinoma progression via YAP signaling pathway. Theranostics 10, 5790-5801 https://doi.org/10.7150/thno.44789
  67. Lamaze C and Torrino S (2015) Caveolae and cancer: a new mechanical perspective. Biomed J 38, 367-379 https://doi.org/10.4103/2319-4170.164229
  68. Thomsen P, Roepstorff K, Stahlhut M and van Deurs B (2002) Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking. Mol Biol Cell 13, 238-250 https://doi.org/10.1091/mbc.01-06-0317
  69. Boucrot E, Howes MT, Kirchhausen T and Parton RG (2011) Redistribution of caveolae during mitosis. J Cell Sci 124, 1965-1972 https://doi.org/10.1242/jcs.076570
  70. Buwa N, Mazumdar D and Balasubramanian N (2020) Caveolin1 tyrosine-14 phosphorylation: role in cellular responsiveness to mechanical cues. J Membr Biol 253, 509-534 https://doi.org/10.1007/s00232-020-00143-0
  71. Wang Z, Wang N, Liu P et al (2015) Caveolin-1, a stress-related oncotarget, in drug resistance. Oncotarget 6, 37135-37150 https://doi.org/10.18632/oncotarget.5789
  72. Pu W, Qiu J, Nassar ZD et al (2020) A role for caveolaforming proteins caveolin-1 and CAVIN1 in the pro-invasive response of glioblastoma to osmotic and hydrostatic pressure. J Cell Mol Med 24, 3724-3738 https://doi.org/10.1111/jcmm.15076
  73. Yang H, Guan L, Li S et al (2016) Mechanosensitive caveolin-1 activation-induced PI3K/Akt/mTOR signaling pathway promotes breast cancer motility, invadopodia formation and metastasis in vivo. Oncotarget 7, 16227-16247 https://doi.org/10.18632/oncotarget.7583
  74. Avvisato CL, Yang, X, Shah S et al (2007) Mechanical force modulates global gene expression and beta-catenin signaling in colon cancer cells. J Cell Sci 120, 2672-2682 https://doi.org/10.1242/jcs.03476