Intermittent F-actin Perturbations by Magnetic Fields Inhibit Breast Cancer Metastasis
Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články
PubMed
36939445
PubMed Central
PMC10017101
DOI
10.34133/research.0080
PII: 0080
Knihovny.cz E-zdroje
- Publikační typ
- časopisecké články MeSH
F-actin (filamentous actin) has been shown to be sensitive to mechanical stimuli and play critical roles in cell attachment, migration, and cancer metastasis, but there are very limited ways to perturb F-actin dynamics with low cell toxicity. Magnetic field is a noninvasive and reversible physical tool that can easily penetrate cells and human bodies. Here, we show that 0.1/0.4-T 4.2-Hz moderate-intensity low-frequency rotating magnetic field-induced electric field could directly decrease F-actin formation in vitro and in vivo, which results in decreased breast cancer cell migration, invasion, and attachment. Moreover, low-frequency rotating magnetic fields generated significantly different effects on F-actin in breast cancer vs. noncancerous cells, including F-actin number and their recovery after magnetic field retrieval. Using an intermittent treatment modality, low-frequency rotating magnetic fields could significantly reduce mouse breast cancer metastasis, prolong mouse survival by 31.5 to 46.0% (P < 0.0001), and improve their overall physical condition. Therefore, our work demonstrates that low-frequency rotating magnetic fields not only can be used as a research tool to perturb F-actin but also can inhibit breast cancer metastasis through F-actin modulation while having minimum effects on normal cells, which reveals their potential to be developed as temporal-controlled, noninvasive, and high-penetration physical treatments for metastatic cancer.
Institute of Physics of the Czech Academy of Sciences Prague Czech Republic
International Magnetobiology Frontier Research Center Science Island Hefei 230031 P R China
Zobrazit více v PubMed
Nurnberg A, Kitzing T, Grosse R. Nucleating actin for invasion. Nat Rev Cancer. 2011;11(3):177–187. PubMed
Shan DD, Chen L, Njardarson JT, Gaul C, Ma X, Danishefsky SJ, Huang XY. Synthetic analogues of migrastatin that inhibit mammary tumor metastasis in mice. Proc Natl Acad Sci USA. 2005;102(10):3772–3776. PubMed PMC
Chen L, Yang SY, Jakoncic J, Zhang JJL, Huang X-Y. Migrastatin analogues target fascin to block tumour metastasis. Nature. 2010;476(7291):1062–1066. PubMed PMC
Kirson ED, Gurvich Z, Schneiderman R, Dekel E, Itzhaki A, Wasserman Y, Schatzberger R, Palti Y. Disruption of cancer cell replication by alternating electric fields. Cancer Res. 2004;64(9):3288–3295. PubMed
Pless M, Weinberg U. Tumor treating fields: Concept, evidence and future. Expert Opin Investig Drugs. 2011;20(8):1099–1106. PubMed
Davies AM, Weinberg U, Palti Y. Tumor treating fields: A new frontier in cancer therapy. Ann N Y Acad Sci. 2013;1291:86–95. PubMed
Van Huizen AV, Morton JM, Kinsey LJ, Von Kannon DG, Saad MA, Birkholz TR, Czajka JM, Cyrus J, Barnes FS, Beane WS. Weak magnetic fields alter stem cell-mediated growth. Sci Adv. 2019;5(1): Article eaau7201. PubMed PMC
Carter CS, Huang SC, Searby CC, Cassaidy B, Miller MJ, Grzesik WJ, Piorczynski TB, Pak TK, Walsh SA, Acevedo M, et al. Exposure to static magnetic and electric fields treats type 2 diabetes. Cell Metab. 2020;32(4):561–574.e7. PubMed PMC
Yu B, Liu J, Cheng J, Zhang L, Song C, Tian X, Fan Y, Lv Y, Zhang X. A static magnetic field improves iron metabolism and prevents high-fat-diet/streptozocin-induced diabetes. Innovation (Camb). 2021;2(1): Article 100077. PubMed PMC
Torbet J, Dickens MJ. Orientation of skeletal muscle actin in strong magnetic fields. FEBS Lett. 1984;173(2):403–406. PubMed
Mo WC, Zhang Z-J, Wang D-L, Liu Y, Bartlett PF, He R-Q. Shielding of the geomagnetic field alters actin assembly and inhibits cell motility in human neuroblastoma cells. Sci Rep. 2016;6: Article 22624. PubMed PMC
Gartzke J, Lange K. Cellular target of weak magnetic fields: Ionic conduction along actin filaments of microvilli. Am J Physiol Cell Physiol. 2002;283(5):C1333–C1346. PubMed
Coletti D, Teodori L, Albertini MC, Rocchi M, Pristerà A, Fini M, Molinaro M, Adamo S. Static magnetic fields enhance skeletal muscle differentiation in vitro by improving myoblast alignment. Cytometry A. 2007;71(10):846–856. PubMed
Dini L, Dwikat M, Panzarini E, Vergallo C, Tenuzzo B. Morphofunctional study of 12- PubMed
Gioia L, Saponaro I, Bernabò N, Tettamanti E, Mattioli M, Barboni B. Chronic exposure to a 2 mT static magnetic field affects the morphology, the metabolism and the function of in vitro cultured swine granulosa cells. Electromagn Biol Med. 2013;32(4):536–550. PubMed
Valiron O, Peris L, Rikken G, Schweitzer A, Saoudi Y, Remy C, Job D. Cellular disorders induced by high magnetic fields. J Magn Reson Imaging. 2005;22(3):334–340. PubMed
Qian AR, Hu LF, Gao X, Zhang W, di SM, Tian ZC, Yang PF, Yin DC, Weng YY, Shang P. Large gradient high magnetic field affects the association of MACF1 with actin and microtubule cytoskeleton. Bioelectromagnetics. 2009;30(7):545–555. PubMed
Zhang J, Meng X, Ding C, Xie L, Yang P, Shang P. Regulation of osteoclast differentiation by static magnetic fields. Electromagn Biol Med. 2017;36(1):8–19. PubMed
Wang Z, Hao F, Ding C, Yang Z, Shang P. Effects of static magnetic field on cell biomechanical property and membrane ultrastructure. Bioelectromagnetics. 2014;35(4):251–261. PubMed
Wosik J, Chen W, Qin K, Ghobrial RM, Kubiak JZ, Kloc M. Magnetic field changes macrophage phenotype. Biophys J. 2018;114(8):2001–2013. PubMed PMC
Zablotskii V, Lunov O, Novotná B, Churpita O, Trošan P, Holáň V, Syková E, Dejneka A, Kubinová Š. Down-regulation of adipogenesis of mesenchymal stem cells by oscillating high-gradient magnetic fields and mechanical vibration. Appl Phys Lett. 2014;105(10): Article 103702.
Harris AR, Jreij P, Fletcher DA. Mechanotransduction by the actin cytoskeleton: converting mechanical stimuli into biochemical signals. Annu Rev Biophys. 2018;47:617–631.
Roy NH, Burkhardt JK. The actin cytoskeleton: A mechanical intermediate for signal integration at the immunological synapse. Front Cell Dev Biol. 2018;6: Article 116. PubMed PMC
Gouget CLM, Hwang YY, Barakat AI. Model of cellular mechanotransduction via actin stress fibers. Biomech Model Mechanobiol. 2016;15(2):331–344. PubMed
Wang N. Review of cellular mechanotransduction. J Phys D Appl Phys. 2017;50(23): Article 233002. PubMed PMC
Makrodouli E, Oikonomou E, Koc M, Andera L, Sasazuki T, Shirasawa S, Pintzas A. BRAF and RAS oncogenes regulate Rho GTPase pathways to mediate migration and invasion properties in human colon cancer cells: A comparative study. Mol Cancer. 2011;10:118. PubMed PMC
Friedl P, Wolf K, Zegers MM. Rho-directed forces in collective migration. Nat Cell Biol. 2014;16:208–210. PubMed
Nobes CD, Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell. 1995;81(1):53–62. PubMed
Lee H, Eskin SG, Ono S, Zhu C, McIntire LV. Force-history dependence and cyclic mechanical reinforcement of actin filaments at the single molecular level. J Cell Sci. 2019;132(4): Article jcs216911. PubMed PMC
Unlu A. Computational prediction of actin–actin interaction. Mol Biol Rep. 2014;41(1):355–364. PubMed PMC
Pauling L. Diamagnetic anisotropy of the peptide group. Proc Natl Acad Sci USA. 1979;76(5):2293–2294. PubMed PMC
Vassilev PM, Dronzine RT, Vassileva MP, Georgiev GA. Parallel arrays of microtubules formed in electric and magnetic fields. Biosci Rep. 1982;2(12):1025–1029. PubMed
Bras W, Diakun GP, Díaz JF, Maret G, Kramer H, Bordas J, Medrano FJ. The susceptibility of pure tubulin to high magnetic fields: A magnetic birefringence and x-ray fiber diffraction study. Biophys J. 1998;74(3):1509–1521. PubMed PMC
Denegre JM, Valles JM Jr, Lin K, Jordan WB, Mowry KL. Cleavage planes in frog eggs are altered by strong magnetic fields. Proc Natl Acad Sci USA. 1998;95(25):14729–14732. PubMed PMC
Valles JM. Model of magnetic field-induced mitotic apparatus reorientation in frog eggs. Biophys J. 2002;82(3):1260–1265. PubMed PMC
Valles JM, Wasserman SRRM, Schweidenback C, Edwardson J, Denegre JM, Mowry KL. Processes that occur before second cleavage determine third cleavage orientation in PubMed
Zhang L, Hou Y, Li Z, Ji X, Wang Z, Wang H, Tian X, Yu F, Yang Z, Pi L, et al. 27 T ultra-high static magnetic field changes orientation and morphology of mitotic spindles in human cells. eLife. 2017;6: Article e22911. PubMed PMC
Luo Y, Ji X, Liu J, Li Z, Wang W, Chen W, Wang J, Liu Q, Zhang X. Moderate intensity static magnetic fields affect mitotic spindles and increase the antitumor efficacy of 5-FU and Taxol. Bioelectrochemistry. 2016;109:31–40. PubMed
Mo WC, Liu Y, Cooper HM, He RQ. Altered development of PubMed
Mershin A, Kolomenski AA, Schuessler HA, Nanopoulos DV. Tubulin dipole moment, dielectric constant and quantum behavior: Computer simulations, experimental results and suggestions. Biosystems. 2004;77(1–3):73–85. PubMed
Bras W, Torbet J, Diakun GP, Rikken GL, Diaz JF. The diamagnetic susceptibility of the tubulin dimer. J Biophys. 2014;2014: Article 985082. PubMed PMC
Glade N, Tabony J. Brief exposure to high magnetic fields determines microtubule self-organisation by reaction-diffusion processes. Biophys Chem. 2005;115(1):29–35. PubMed
Liu Y, Guo Y, Valles JM Jr, Tang JX. Microtubule bundling and nested buckling drive stripe formation in polymerizing tubulin solutions. Proc Natl Acad Sci USA. 2006;103(28):10654–10659. PubMed PMC
Guo Y, Liu Y, Oldenbourg R, Tang JX, Valles JM Jr. Effects of osmotic force and torque on microtubule bundling and pattern formation. Phys Rev E Stat Nonlinear Soft Matter Phys. 2008;78(4 Pt 1): Article 041910. PubMed
Wang DL, Wang XS, Xiao R, Liu Y, He RQ. Tubulin assembly is disordered in a hypogeomagnetic field. Biochem Biophys Res Commun. 2008;376(2):363–368. PubMed
Eguchi Y, Ueno S. Stress fiber contributes to rat Schwann cell orientation under magnetic field. IEEE T Magn. 2005;41(10):4146–4148.
Brangwynne CP, Koenderink GH, MacKintosh FC, Weitz DA. Nonequilibrium microtubule fluctuations in a model cytoskeleton. Phys Rev Lett. 2008;100(11): Article 118104. PubMed
Westendorf C, Negrete J Jr, Bae AJ, Sandmann R, Bodenschatz E, Beta C. Actin cytoskeleton of chemotactic amoebae operates close to the onset of oscillations. Proc Natl Acad Sci USA. 2013;110(10):3853–3858. PubMed PMC
Ren J, Ding L, Xu Q, Shi G, Li X, Li X, Ji J, Zhang D, Wang Y, Wang T, et al. LF-MF inhibits iron metabolism and suppresses lung cancer through activation of P53-miR-34a-E2F1/E2F3 pathway. Sci Rep. 2017;7: Article 749. PubMed PMC
Nie YZ, Du L, Mou Y, Xu Z, Weng L, Du Y, Zhu Y, Hou Y, Wang T. Effect of low frequency magnetic fields on melanoma: tumor inhibition and immune modulation. BMC Cancer. 2013;13:582. PubMed PMC
Nie YZ, Chen Y, Mou Y, Weng L, Xu Z, Du Y, Wang W, Hou Y, Wang T. Low frequency magnetic fields enhance antitumor immune response against mouse H22 hepatocellular carcinoma. PLOS ONE. 2013;8(11): Article e72411. PubMed PMC