Mechano-signalling, induced by fullerene C₆₀ nanofilms, arrests the cell cycle in the G2/M phase and decreases proliferation of liver cancer cells

References

• Schrader J, Gordon-Walker TT, Aucott RL, et al. Matrix stiffness modulates proliferation, chemotherapeutic response, and dormancy in hepatocellular carcinoma cells. Hepatology. 2011;53(4):1192–1205. doi:10.1002/hep.2410821442631
   PubMed Web of Science ®Google Scholar
• Mittal S, El-Serag HB. Epidemiology of HCC: consider the population. J Clin Gastroenterol. 2013;47:S2–S6. doi:10.1097/MCG.0b013e3182872f2923632345
   PubMed Web of Science ®Google Scholar
• Yau WL, Lam CSC, Ng L, et al. Over-expression of miR-106b promotes cell migration and metastasis in hepatocellular carcinoma by activating epithelial-mesenchymal transition process. PLoS One. 2013;8(3):e57882. doi:10.1371/journal.pone.005788223483935
   PubMed Web of Science ®Google Scholar
• Wai CT, Greenson JK, Fontana RJ, et al. A simple non-invasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C. Hepatology. 2003;38(2):518–526. doi:10.1053/jhep.2003.5034612883497
   PubMed Web of Science ®Google Scholar
• Wynn TA, Ramalingam TR. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med. 2012;18(7):1028–1040. doi:10.1038/nm.280722772564
   PubMed Web of Science ®Google Scholar
• Baiocchini A, Montaldo C, Conigliaro A, et al. Extracellular matrix molecular remodeling in human liver fibrosis evolution. PLoS One. 2016;11(3):e0151736. doi:10.1371/journal.pone.015173626998606
   PubMedGoogle Scholar
• Haase K, Pelling AE. Investigating cell mechanics with atomic force microscopy. J R Soc Interface. 2015;12(104):20140970. doi:10.1098/rsif.2014.097025589563
   PubMed Web of Science ®Google Scholar
• Gao J, Rong Y, Huang Y, et al. Cirrhotic stiffness affects the migration of hepatocellular carcinoma cells and induces sorafenib resistance through YAP. J Cell Physiol. 2018;234(3):2639–2648. doi:10.1002/jcp.2707830145835
   PubMedGoogle Scholar
• Li QS, Lee GY, Ong CN, Lim CT. AFM indentation study of breast cancer cells. Biochem Biophys Res Commun. 2008;374(4):609–613. doi:10.1016/j.bbrc.2008.07.07818656442
   PubMed Web of Science ®Google Scholar
• Lekka M, Gil D, Pogoda K, et al. Cancer cell detection in tissue sections using AFM. Arch Biochem Biophys. 2012;518(2):151–156. doi:10.1016/j.abb.2011.12.01322209753
   PubMed Web of Science ®Google Scholar
• Samani A, Zubovits J, Plewes D. Elastic moduli of normal and pathological human breast tissues: an inversion-technique-based investigation of 169 samples. Phys Med Biol. 2007;52(6):1565–1576. doi:10.1088/0031-9155/52/6/00217327649
   PubMedGoogle Scholar
• Provenzano PP, Inman DR, Eliceiri KW, et al. Collagen density promotes mammary tumor initiation and progression. BMC Med. 2008;6(1):11. doi:10.1186/1741-7015-6-1118442412
   PubMedGoogle Scholar
• Parekh A, Weaver AM. Regulation of cancer invasiveness by the physical extracellular matrix environment. Cell Adh Migr. 2009;3(3):288–292. doi:10.4161/cam.3.3.888819458499
   PubMed Web of Science ®Google Scholar
• Wu S, Zheng Q, Xing X, et al. Matrix stiffness-upregulated LOXL2 promotes fibronectin production, MMP9 and CXCL12 expression and BMDCs recruitment to assist pre-metastatic niche formation. J Exp Clin Cancer Res. 2018;37(1):99. doi:10.1186/s13046-018-0761-z29728125
   PubMedGoogle Scholar
• Breuls RGM, Jiya TU, Smit TH. Scaffold stiffness influences cell behavior: opportunities for skeletal tissue engineering. Open Orthop J. 2008;2:103–109. doi:10.2174/187432500080201010319478934
   PubMedGoogle Scholar
• Mitra AK, Sawada K, Tiwari P, Mui K, Gwin K, Lengyel E. Ligand-independent activation of c-Met by fibronectin and α5β1-integrin regulates ovarian cancer invasion and metastasis. Oncogene. 2011;30(13):1566–1576. doi:10.1038/onc.2010.53221119598
   PubMed Web of Science ®Google Scholar
• Murke F, Vitorianoda CC, Giebel B, Görgens A. Concise review: asymmetric cell divisions in stem cell biology. Symmetry. 2015;7(4):2025–2037. doi:10.3390/sym7042025
   Google Scholar
• Lu P, Weaver VM, Werb Z. The extracellular matrix: a dynamic niche in cancer progression. J Cell Biol. 2012;196(4):395–406. doi:10.1083/jcb.20110214722351925
   PubMed Web of Science ®Google Scholar
• Lechler T, Fuchs E. Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature. 2005;437(7056):275–280. doi:10.1038/nature0392216094321
   PubMed Web of Science ®Google Scholar
• Lee M, Vasioukhin V. Cell polarity and cancer—cell and tissue polarity as a non-canonical tumor suppressor. J Cell Sci. 2008;121(8):1141–1150. doi:10.1242/jcs.01871318388309
   PubMed Web of Science ®Google Scholar
• Yang JD, Nakamura I, Roberts LR. The tumor microenvironment in hepatocellular carcinoma: current status and therapeutic targets. Semin Cancer Biol. 2011;21(1):35–43. doi:10.1016/j.semcancer.2010.10.00720946957
   PubMed Web of Science ®Google Scholar
• Deakin NO, Turner CE. Paxillin comes of age. J Cell Sci. 2008;121(15):2435–2444. doi:10.1242/jcs.01871318650496
   PubMed Web of Science ®Google Scholar
• Cho S, Irianto J, Discher DE. Mechanosensing by the nucleus: from pathways to scaling relationships. J Cell Biol. 2017;216(2):305–315. doi:10.1083/jcb.20161004228043971
   PubMed Web of Science ®Google Scholar
• Elosegui-Artola A, Andreu I, Beedle AEM, et al. Force triggers YAP nuclear entry by regulating transport across nuclear pores. Cell. 2017;171(6):1397–1410. doi:10.1016/j.cell.2017.10.00829107331
   PubMed Web of Science ®Google Scholar
• Geiger B, Yamada KM. Molecular architecture and function of matrix adhesions. Cold Spring Harb Perspect Biol. 2011;3(5):a005033. doi:10.1101/cshperspect.a00503321441590
   PubMedGoogle Scholar
• Tilghman RW, Cowan CR, Mih JD, et al. Matrix rigidity regulates cancer cell growth and cellular phenotype. PLoS One. 2010;5(9):e12905. doi:10.1371/journal.pone.001290520886123
   PubMed Web of Science ®Google Scholar
• Wong S, Guo WH, Wang YL. Fibroblasts probe substrate rigidity with filopodia extensions before occupying an area. Proc Natl Acad Sci USA. 2014;111(48):17176–17181. doi:10.1073/pnas.141228511125404288
   PubMedGoogle Scholar
• Yamaguchi H, Condeelis J. Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim Biophys Acta. 2007;1773(5):642–652. doi:10.1016/j.bbamcr.2006.07.00116926057
   PubMed Web of Science ®Google Scholar
• Yamaguchi H, Oikawa T. Membrane lipids in invadopodia and podosomes: key structures for cancer invasion and metastasis. Oncotarget. 2010;1(5):320–328. doi:10.18632/oncotarget.v1i521307399
   PubMedGoogle Scholar
• Abarrategi A, Gutiérrez MC, Moreno-Vicente C, et al. Multi-wall carbon nanotube scaffolds for tissue engineering purposes. Biomaterials. 2008;29(1):94–102. doi:10.1016/j.biomaterials.2007.09.02117928048
   PubMed Web of Science ®Google Scholar
• Kumar R, Raza K. C60 fullerenes as drug delivery carriers for anticancer agents: promises and hurdles. Pharm Nanotechnol. 2017;5(3):169–179.29361902
   PubMedGoogle Scholar
• Kolosnjaj J, Szwarc H, Moussa F. Toxicity studies of fullerenes and derivatives. Adv Exp Med Biol. 2007;620:168–180.18217343
   PubMed Web of Science ®Google Scholar
• Sun C, Wang L, Gao D, et al. C60(OH)22: a potential histone deacetylase inhibitor with anti-angiogenic activity. Nanoscale. 2016;8(36):16332–16339. doi:10.1039/c6nr04875g27714131
   PubMedGoogle Scholar
• Prylutska S, Politenkova S, Afanasieva K, et al. A nanocomplex of C60 fullerene with cisplatin: design, characterization, and toxicity. Beilstein J Nanotechnol. 2017;8(1):1494–1501. doi:10.3762/bjnano.8.14928900603
   PubMedGoogle Scholar
• Prylutska S, Grynyuk I, Matyshevska O, et al. C60 fullerene as synergistic agent in tumor-inhibitory doxorubicin treatment. Drugs R D. 2014;14(4):333–340. doi:10.1007/s40268-014-0074-425504158
   PubMedGoogle Scholar
• Mori TT, Takada H, Ito S, Matsubayashi K, Miwa N, Sawaguchi T. Preclinical studies on safety of fullerene upon acute oral administration and evaluation for no mutagenesis. Toxicology. 2006;225(1):48–54. doi:10.1016/j.tox.2006.05.00116782258
   PubMedGoogle Scholar
• Hendrickson OD, Zherdev AV, Gmoshinskii IV, Dzantiev BB. Fullerenes: in vivo studies of biodistribution, toxicity, and biological action. Nanotechnol Russ. 2014;9(11–12):601–617. doi:10.1134/S199507801406010X
   Google Scholar
• Injac R, Perse M, Obermajer N, et al. Potential hepatoprotective effects of fullerenol C60(OH)24 in doxorubicin-induced hepatotoxicity in rats with mammary carcinomas. Biomaterials. 2008;29(24–25):3451–3460. doi:10.1016/j.biomaterials.2008.04.04818501960
   PubMed Web of Science ®Google Scholar
• Tolkachov M, Sokolova V, Loza K, et al. Study of biocompatibility effect of nanocarbon particles on various cell types in vitro. Mat-Wiss U Werkstofftech. 2016;47(2–3):216–221. doi:10.1002/mawe.201600486
   Web of Science ®Google Scholar
• Baati T, Bourasset F, Gharbi N, et al. The prolongation of the lifespan of rats by repeated oral administration of [60]fullerene. Biomaterials. 2012;33(19):4936–4946. doi:10.1016/j.biomaterials.2012.03.03622498298
   PubMed Web of Science ®Google Scholar
• Harhaji L, Isakovic A, Reicevic N, et al. Multiple mechanisms underlying the anticancer action of nanocrystalline fullerene. Eur J Pharmacol. 2007;568(1–3):89–98. doi:10.1016/j.ejphar.2007.04.04117560995
   PubMedGoogle Scholar
• Franskevych D, Palyvoda K, Petukhov D, et al. Fullerene C60 penetration into leukemic cells and its photoinduced cytotoxic effects. Nanoscale Res Lett. 2017;12(1):40. doi:10.1186/s11671-016-1819-528091953
   PubMedGoogle Scholar
• Raoof M, Mackeyev Y, Cheney MA, Wilson LJ, Curley SA. Internalization of C60 fullerenes into cancer cells with accumulation in the nucleus via the nuclear pore complex. Biomaterials. 2012;33(10):2952–2960. doi:10.1016/j.biomaterials.2011.12.04322245558
   PubMed Web of Science ®Google Scholar
• Salonen E, Lin S, Reid ML, et al. Real‐time translocation of fullerene reveals cell contraction. Small. 2008;4(11):1986–1992. doi:10.1002/smll.20070127918949789
   PubMedGoogle Scholar
• Sawosz E, Chwalibog A, Szeliga J, et al. Visualization of gold and platinum nanoparticles interacting with Salmonella Enteritidis and Listeria monocytogenes. Int J Nanomed. 2010;5:631–637.
   PubMed Web of Science ®Google Scholar
• Sawosz E, Grodzik M, Hotowy A, et al. Warsaw University of Life Sciences. The method of multilateral assessment of biocompatibility of materials. Poland patent 423414. 2017 11 10.
   Google Scholar
• Wierzbicki M, Jaworski S, Kutwin M, et al. Diamond, graphite, and graphene oxide nanoparticles decrease migration and invasiveness in glioblastoma cell lines by impairing extracellular adhesion. Int J Nanomed. 2017;12:7241–7254. doi:10.2147/IJN.S146193
   PubMed Web of Science ®Google Scholar
• Zgłobicka I, Chlanda A, Woźniak M, et al. Microstructure and nanomechanical properties of single stalks from diatom Didymosphenia geminata and their change due to adsorption of selected metal ions. J Phycol. 2017;53(4):880–888. doi:10.1111/jpy.1254828523651
   PubMedGoogle Scholar
• Dulińska M, Targosz W, Strojny W, et al. Stiffness of normal and pathological erythrocytes studied by means of atomic force microscopy. J. Biochem Biophys Methods. 2006;66(1–3):1–11. doi:10.1016/j.jbbm.2005.11.00316443279
   PubMedGoogle Scholar
• https://medschool.ucsd.edu, UC San Diego, Health Sciences, California, USA. Cell cycle analysis by DNA content (propidium iodide). Available from: https://healthsciences.ucsd.edu/research/moores/shared-resources/flow-cytometry/protocols/Pages/cell-cycle-with-pi.aspx. Accessed 717, 2018
   Google Scholar
• Saeedfar K, Heng LY, Ling TL, Rezayi M. Potentiometric urea biosensor based on an immobilized fullerene–urease bio-conjugate. Ah S Sens. 2013;13(12):16851–16866. doi:10.3390/s131216851
   PubMed Web of Science ®Google Scholar
• Chen B, Kumar G, Co CC, Ho CC. Geometric control of cell migration. Sci Rep. 2013;3:2827. doi:10.1038/srep0282724089214
   PubMedGoogle Scholar
• Jaworski S, Sawosz E, Grodzik M, et al. In vitro evaluation of the effects of graphene platelets on glioblastoma multiforme cells. Int J Nanomed. 2013;8:413–420.
   PubMed Web of Science ®Google Scholar
• Lee JH, Kim DH, Lee HH, Kim HW. Role of nuclear mechanosensitivity in determining cellular responses to forces and biomaterials. Biomaterials. 2019;197:60–71. doi:10.1016/j.biomaterials.2019.01.01030641265
   PubMedGoogle Scholar
• Lunova M, Zablotskii V, Dempsey NM, et al. Modulation of collective cell behaviour by geometrical constraints. Integr Biol. 2016;8(11):1099–1110. doi:10.1039/C6IB00125D
   Google Scholar
• Theocharis AD, Skandalis SS, Gialeli C, Karamanos NK. Extracellular matrix structure. Adv Drug Deliv Rev. 2016;97:4–27. doi:10.1016/j.addr.2015.11.00126562801
   PubMed Web of Science ®Google Scholar
• Tatur S, Maccarini M, Barker RD, Nelson A, Fragneto G. Effect of functionalized gold nanoparticles on floating lipid bilayers. Langmuir. 2013;29(22):6606–6614. doi:10.1021/la401074y23638939
   PubMedGoogle Scholar
• Yadav BC, Kumar R. Structure, properties, and applications of fullerenes. Int J Nanotechnol APP. 2008;2(1):15–24.
   Google Scholar
• Kopova I, Bacakova L, Lavrentiev V, Vacik J. Growth and potential damage of human bone-derived cells on fresh and aged fullerene C60 films. Int J Mol Sci. 2013;14(5):9182–9204. doi:10.3390/ijms1405918223624607
   PubMedGoogle Scholar
• Gatoo MA, Naseem S, Arfat MY, Mahmood Dar A, Qasim K, Zubair S. Physicochemical properties of nanomaterials: implication in associated toxic manifestations. Biomed Res Int. 2014;2014:498420.25165707
   PubMedGoogle Scholar
• Haeger A, Krause M, Wolf K, Friedl P. Cell jamming: collective invasion of mesenchymal tumor cells imposed by tissue confinement. Biochim Biophys Acta. 2014;1840(8):2386–2395. doi:10.1016/j.bbagen.2014.03.02024721714
   PubMedGoogle Scholar
• Marchesan S, Melchionna M, Prato M. Carbon nanostructures for nanomedicine: opportunities and challenges. Fuller Nanotub Car N. 2014;22(1–3):190–195. doi:10.1080/1536383X.2013.798726
   Web of Science ®Google Scholar
• Nguyen VH, Meghani NM, Amin HH, et al. Modulation of serum albumin protein corona for exploring cellular behaviors of fattigation-platform nanoparticles. Colloid Surface B. 2018;170:179–186. doi:10.1016/j.colsurfb.2018.05.060
   PubMed Web of Science ®Google Scholar
• Liu Y, Wang Z, Wang X. AFM-based study of fullerenol (C60(OH)24)-induced changes of elasticity in living SMCC-7721 cells. J Mech Behav Biomed. 2015;45:65–74. doi:10.1016/j.jmbbm.2014.12.011
   PubMed Web of Science ®Google Scholar
• Dong Y, Xie X, Wang Z, et al. Increasing matrix stiffness upregulates vascular endothelial growth factor expression in hepatocellular carcinoma cells mediated by integrin β1. Biochem Bioph Res Commun. 2014;444(3):427–432. doi:10.1016/j.bbrc.2014.01.079
   PubMed Web of Science ®Google Scholar
• Morozevich G, Kozlova N, Cheglakov I, Ushakova N, Integrin BA. α5β1 controls invasion of human breast carcinoma cells by direct and indirect modulation of MMP-2 collagenase activity. Cell Cycle. 2009;8(14):2219–2225. doi:10.4161/cc.8.14.898019617714
   PubMed Web of Science ®Google Scholar
• Wu Y, Qiao X, Qiao S, Yu L. Targeting integrins in hepatocellular carcinoma. Expert Opin Ther Targets. 2011;15(4):421–437. doi:10.1517/14728222.2011.55540221332366
   PubMed Web of Science ®Google Scholar
• Fu Y, Fang Z, Liang Y, et al. Overexpression of integrin β1 inhibits proliferation of hepatocellular carcinoma cell SMMC-7721 through preventing Skp2-dependent degradation of p27 via PI3K pathway. J Cell Biochem. 2007;102(3):704–718. doi:10.1002/jcb.2132317407140
   PubMedGoogle Scholar
• Reed NI, Chen C, Tsujino K, Arnold TD, DeGrado WF, Sheppard D. The αvβ1 integrin plays a critical in vivo role in tissue fibrosis. Sci Transl Med. 2015;7(288):288ra79–288ra79. doi:10.1126/scitranslmed.aaa5094
   PubMed Web of Science ®Google Scholar
• Yeh YC, Ling JY, Chen WC, Lin HH, Tang MJ. Mechanotransduction of matrix stiffness in regulation of focal adhesion size and number: reciprocal regulation of caveolin-1 and β1 integrin. Sci Rep. 2017;7(1):15008. doi:10.1038/s41598-017-14932-629118431
   PubMedGoogle Scholar
• Levi N, Hantgan RR, Lively MO, Caroll DL, Prasad GL. C60 fullerenes: detection of intracellular photoluminescence and lack of cytotoxic effects. J Nanobiotechnol. 2006;4(1):1–11. doi:10.1186/1477-3155-4-14
   PubMedGoogle Scholar
• Sun H, Tang H, Xie D, et al. Krüppel-like factor 4 blocks hepatocellular carcinoma dedifferentiation and progression through activation of hepatocyte nuclear factor-6. Clin Cancer Res. 2016;22(2):502–512. doi:10.1158/1078-0432.CCR-16-019026338995
   PubMedGoogle Scholar
• Su JM, Gui L, Zhou YP, Zha XL. Expression of focal adhesion kinase and α5 and β1 integrins in carcinomas and its clinical significance. World J Gastroenterol. 2002;8(4):613–618. doi:10.3748/wjg.v8.i4.61312174366
   PubMedGoogle Scholar
• Wu Y, Zuo J, Ji G, et al. Proapoptotic function of integrin β3 in human hepatocellular carcinoma cells. Clin Cancer Res. 2009;15(1):60–69. doi:10.1158/1078-0432.CCR-09-054719118033
   PubMedGoogle Scholar
• Kim SH, Turnbull J, Guimond S. Extracellular matrix and cell signaling: the dynamic cooperation of integrin, proteoglycan, and growth factor receptor. J Endocrinol. 2011;209(2):139–151. doi:10.1530/JOE-10-037721307119
   PubMed Web of Science ®Google Scholar
• Nowakowska A, Tarasiuk J. Procesy inwazji I przerzutowania komórek nowotworowych opornych na chemioterapię. Postepy Hig Med Dosw. 2017;71:380–397.
   Google Scholar
• Wang W, Wen Q, Luo J, et al. Suppression of β-catenin nuclear translocation by CGP57380 decelerates poor progression and potentiates radiation-induced apoptosis in nasopharyngeal carcinoma. Theranostics. 2017;7(7):2134–2149. doi:10.7150/thno.1766528656063
   PubMed Web of Science ®Google Scholar
• Khalaf AM, Fuentes D, Morshid AI, et al. Role of Wnt/β-catenin signaling in hepatocellular carcinoma, pathogenesis, and clinical significance. J Hepatocell Carcinoma. 2018;5:61. doi:10.2147/JHC.S15670129984212
   PubMed Web of Science ®Google Scholar
• Huang DL, Bax NA, Buckley CD, Weis WI, Dunn AR. Vinculin forms a directionally asymmetric catch bond with F-actin. Science. 2017;357(6352):703–706. doi:10.1126/science.aan255628818948
   PubMedGoogle Scholar
• Ling X, Kamangar S, Boytim ML, et al. Proliferating cell nuclear antigen as the cell cycle sensor for an HLA-derived peptide blocking T cell proliferation. J Immunol. 2000;164(12):6188–6192. doi:10.4049/jimmunol.164.12.618810843669
   PubMedGoogle Scholar
• Liang YL, Lei TW, Wu H, et al. S-phase delay in human hepatocellular carcinoma cells induced by overexpression of integrin β1. World J Gastroenterol. 2003;9(8):1689–1696. doi:10.3748/wjg.v9.i8.168912918102
   PubMedGoogle Scholar
• Provenzano PP, Keely PJ. Mechanical signaling through the cytoskeleton regulates cell proliferation by coordinated focal adhesion and Rho GTPase signaling. J Cell Sci. 2011;124(8):1195–1205. doi:10.1242/jcs.06700921444750
   PubMed Web of Science ®Google Scholar
• Shi J, Ye G, Zhao G, et al. Coordinative control of G2/M phase of the cell cycle by non-coding RNAs in hepatocellular carcinoma. PeerJ. 2018;6:e5787. doi:10.7717/peerj.578730364632
   PubMed Web of Science ®Google Scholar