Abstract
Metastasis is identified as the main cause of cancer-related deaths. Migration of cancer cells to other organs (metastasis) can happen through multiple types of migration modalities. Collective migration of cancerous cells is termed as epithelial mode, whereas single-cell migration is named either mesenchymal or amoeboid. The modality of migration is primarily controlled by the cancer cells and the tumor environment. As one of the major biochemical factors within the tumor microenvironment, oxidative stress is generated as a result of the imbalance between the reactive oxygen species and antioxidant species. It plays a major role in cancer development and dissemination by affecting signaling pathways and enhancing migration and tissue invasion. In order to tackle the oxidative stress, tumor cells tend to migrate away from the source by adopting different modes of migration. Tumor cells subjected to oxidative stress conditions instigate the single-cell migration from the collective one and undergo EMT (epithelial to mesenchymal transition) which has been explained elsewhere. However, few studies have initiated the process to recognize the connection between oxidative stress and amoeboid migration. This chapter is designed to identify the role of oxidative stress on the amoeboid mode of migration. Understanding the relationship between oxidative stress and amoeboid migration is crucial because it is being identified as one of the major reasons behind the tumor dissemination. Additionally, identification of oxidative stress-mediated factors that influence amoeboid migration might help in the detection of potential targets for therapeutic purposes.
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Reference
Boekhorst Vt, Jiang L, Mahlen M, Meerlo M, Dunkel G, Durst FC, Yang Y, Levine H, Burgering BM.T, Friedl P 2020 Calpain-2 regulates hypoxia/HIF-induced amoeboid reprogramming and metastasis. bioRxiv preprint. https://doi.org/10.1101/2020.01.06.892497
Bracalente C, Salguero N, Notcovich C, Müller CB, da Motta LL, Klamt F, Ibañez IL, Durán H (2016) Reprogramming human A375 amelanotic melanoma cells by catalase overexpression: reversion or promotion of malignancy by inducing melanogenesis or metastasis. Oncotarget 7:41142–41153. https://doi.org/10.18632/oncotarget.9220
Bronsert P, Enderle-Ammour K, Bader M, Timme S, Kuehs M, Csanadi A, Kayser G, Kohler I, Bausch D, Hoeppner J, Hopt UT, Keck T, Stickeler E, Passlick B, Schilling O, Reiss CP, Vashist Y, Brabletz T, Berger J, Lotz J, Olesch J, Werner M, Wellner UF (2014) Cancer cell invasion and EMT marker expression: a three-dimensional study of the human cancer-host interface. J Pathol 234:410–422. https://doi.org/10.1002/path.4416
Buricchi F, Giannoni E, Grimaldi G, Parri M, Raugei G, Ramponi G, Chiarugi P (2007) Redox regulation of ephrin/integrin cross-talk. Cell Adhes Migr 1:33–42
Calvo F, Sanz-Moreno V, Agudo-Ibáñez L, Wallberg F, Sahai E, Marshall CJ, Crespo P (2011) RasGRF suppresses Cdc42-mediated tumor cell movement, cytoskeletal dynamics and transformation. Nat Cell Biol 13:819–826. https://doi.org/10.1038/ncb2271
Cantelli G, Orgaz JL, Rodriguez-Hernandez I, Karagiannis P, Maiques O, Matias-Guiu X, Nestle FO, Marti RM, Karagiannis SN, Sanz-Moreno V (2015) TGF-β-induced transcription sustains amoeboid melanoma migration and dissemination. Curr Biol 25:2899–2914. https://doi.org/10.1016/j.cub.2015.09.054
Carragher NO, Walker SM, Scott Carragher LA, Harris F, Sawyer TK, Brunton VG, Ozanne BW, Frame MC (2006) Calpain 2 and Src dependence distinguishes mesenchymal and amoeboid modes of tumor cell invasion: a link to integrin function. Oncogene 25:5726–5740. https://doi.org/10.1038/sj.onc.1209582
Cartier-Michaud A, Malo M, Charrière-Bertrand C, Gadea G, Anguille C, Supiramaniam A, Lesne A, Delaplace F, Hutzler G, Roux P, Lawrence DA, Barlovatz-Meimon G (2012) Matrix-bound PAI-1 supports cell Blebbing via RhoA/ROCK1 signaling. PLoS One 7:e32204. https://doi.org/10.1371/journal.pone.0032204
Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, Schumacker PT (1998) Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci U S A 95:11715–11720. https://doi.org/10.1073/pnas.95.20.11715
Charras G, Paluch E (2008) Blebs lead the way: how to migrate without lamellipodia. Nat Rev Mol Cell Biol 9:730–736. https://doi.org/10.1038/nrm2453
Crosas-Molist E, Bertran E, Rodriguez-Hernandez I, Herraiz C, Cantelli G, Fabra À, Sanz-Moreno V, Fabregat I (2017) The NADPH oxidase NOX4 represses epithelial to amoeboid transition and efficient tumor dissemination. Oncogene 36:3002–3014. https://doi.org/10.1038/onc.2016.454
Ferraro D, Corso S, Fasano E, Panieri E, Santangelo R, Borrello S, Giordano S, Pani G, Galeotti T (2006) Pro-metastatic signaling by c-met through RAC-1 and reactive oxygen species (ROS). Oncogene 25:3689–3698. https://doi.org/10.1038/sj.onc.1209409
Friedl P, Alexander S (2011) Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 147:992–1009. https://doi.org/10.1016/j.cell.2011.11.016
Friedl P, Wolf K (2003) Tumor-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 3:362–374. https://doi.org/10.1038/nrc1075
Friedl P, Borgmann S, Bröcker EB (2001) Amoeboid leukocyte crawling through extracellular matrix: lessons from the Dictyostelium paradigm of cell movement. J Leukoc Biol 70:491–509. https://doi.org/10.1189/jlb.70.4.491
Friedl P, Hegerfeldt Y, Tusch M (2004) Collective cell migration in morphogenesis and cancer. Int J Dev Biol 48:441–449. https://doi.org/10.1387/ijdb.041821pf
Friedl P, Locker J, Sahai E, Segall JE (2012) Classifying collective cancer cell invasion. Nat Cell Biol 14:777–783. https://doi.org/10.1038/ncb2548
Grigore A, Jolly M, Jia D, Farach-Carson MC, Levine H (2016) Tumor budding: the name is EMT. Partial EMT J Clin Med 5:51. https://doi.org/10.3390/jcm5050051
Hegerfeldt Y, Tusch M, Bröcker E-B, Friedl P (2002) Collective cell movement in primary melanoma explants: plasticity of cell-cell interaction, beta1-integrin function, and migration strategies. Cancer Res 62:2125–2130
Herraiz C, Calvo F, Pandya P, Cantelli G, Rodriguez-Hernandez I, Orgaz JL, Kang N, Chu T, Sahai E, Sanz-Moreno V (2016) Reactivation of p53 by a cytoskeletal sensor to control the balance between DNA damage and tumor dissemination. J Natl Cancer Inst 108:djv289. https://doi.org/10.1093/jnci/djv289
Jabs T (1999) Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem Pharmacol 57:231–245. https://doi.org/10.1016/s0006-2952(98)00227-5
Killich T, Plath PJ, Wei X, Bultmann H, Rensing L, Vicker MG (1993) The locomotion, shape and pseudopodial dynamics of unstimulated Dictyostelium cells are not random. J Cell Sci 106. (Pt 4:1005–13)
Kim MH, Yoo HS, Kim MY, Jang HJ, Baek MK, Kim HR, Kim KK, Shin BA, Ahn BW, Jung YD (2007) Helicobacter pylori stimulates urokinase plasminogen activator receptor expression and cell invasiveness through reactive oxygen species and NF-kappaB signaling in human gastric carcinoma cells. Int J Mol Med 19:689–697
Lee K, Kim S, Kim J-R (2009) Reactive oxygen species regulate urokinase plasminogen activator expression and cell invasion via mitogen-activated protein kinase pathways after treatment with hepatocyte growth factor in stomach cancer cells. J Exp Clin Cancer Res 28:73. https://doi.org/10.1186/1756-9966-28-73
Lehmann S, te Boekhorst V, Odenthal J, Bianchi R, van Helvert S, Ikenberg K, Ilina O, Stoma S, Xandry J, Jiang L, Grenman R, Rudin M, Friedl P (2017) Hypoxia induces a HIF-1-dependent transition from collective-to-amoeboid dissemination in epithelial Cancer cells. Curr Biol 27:392–400. https://doi.org/10.1016/j.cub.2016.11.057
Margheri F, Luciani C, Taddei ML, Giannoni E, Laurenzana A, Biagioni A, Chillà A, Chiarugi P, Fibbi G, Del Rosso M (2014) The receptor for urokinase-plasminogen activator (uPAR) controls plasticity of cancer cell movement in mesenchymal and amoeboid migration style. Oncotarget 5:1538–1553. https://doi.org/10.18632/oncotarget.1754
Marnett LJ (2000) Oxyradicals and DNA damage. Carcinogenesis 21:361–370. https://doi.org/10.1093/carcin/21.3.361
Mishra K (2018) Intracellular reactive oxygen species determine cancer stem cell radiosensitivity related to predictive biomarker for radiotherapy. J Radiat Cancer Res 9:147. https://doi.org/10.4103/jrcr.jrcr_1_19
Nimnual AS, Taylor LJ, Bar-Sagi D (2003) Redox- dependent down regulation of rho by Rac. Nat Cell Biol 5:236–241. https://doi.org/10.1038/ncb938
Oppel F, Müller N, Schackert G, Hendruschk S, Martin D, Geiger KD, Temme A (2011) SOX2-RNAi attenuates S-phase entry and induces RhoA-dependent switch to protease-independent amoeboid migration in human glioma cells. Mol Cancer 10:137. https://doi.org/10.1186/1476-4598-10-137
Pandya P, Orgaz JL, Sanz-Moreno V (2017) Modes of invasion during tumor dissemination. Mol Oncol 11:5–27. https://doi.org/10.1002/1878-0261.12019
Pani G, Galeotti T, Chiarugi P (2010) Metastasis: cancer cell’s escape from oxidative stress. Cancer Metastasis Rev 29:351–378. https://doi.org/10.1007/s10555-010-9225-4
Parri M, Taddei ML, Bianchini F, Calorini L, Chiarugi P (2009) EphA2 Reexpression prompts invasion of melanoma cells shifting from mesenchymal to amoeboid-like motility style. Cancer Res 69:2072–2081. https://doi.org/10.1158/0008-5472.CAN-08-1845
Pinner S, Sahai E (2008) PDK1 regulates cancer cell motility by antagonising inhibition of ROCK1 by RhoE. Nat Cell Biol 10:127–137. https://doi.org/10.1038/ncb1675
Radisky DC, Levy DD, Littlepage LE, Liu H, Nelson CM, Fata JE, Leake D, Godden EL, Albertson DG, Nieto MA, Werb Z, Bissell MJ (2005) Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 436:123–127. https://doi.org/10.1038/nature03688
Ridley AJ (2003) Cell migration: integrating signals from front to Back. Science 302(80):1704–1709. https://doi.org/10.1126/science.1092053
Sadok A, Pierres A, Dahan L, Prévôt C, Lehmann M, Kovacic H (2009) NADPH oxidase 1 controls the persistence of directed cell migration by a rho-dependent switch of 2/3 Integrins. Mol Cell Biol 29:3915–3928. https://doi.org/10.1128/MCB.01199-08
Sahai E, Marshall CJ (2003) Differing modes of tumor cell invasion have distinct requirements for rho/ROCK signalling and extracellular proteolysis. Nat Cell Biol 5:711–719. https://doi.org/10.1038/ncb1019
Simic MG, Bergtold DS, Karam LR (1989) Generation of oxy radicals in biosystems. Mutat Res Mol Mech Mutagen 214:3–12. https://doi.org/10.1016/0027-5107(89)90192-9
Sosa V, Moliné T, Somoza R, Paciucci R, Kondoh H, LLeonart ME (2013) Oxidative stress and cancer: an overview. Ageing Res Rev 12:376–390. https://doi.org/10.1016/j.arr.2012.10.004
Wang Y, Bibi M, Min P, Deng W, Zhang Y, Du J (2019) SOX2 promotes hypoxia-induced breast cancer cell migration by inducing NEDD9 expression and subsequent activation of Rac1/HIF-1α signaling. Cell Mol Biol Lett 24:55. https://doi.org/10.1186/s11658-019-0180-y
Wildenberg GA, Dohn MR, Carnahan RH, Davis MA, Lobdell NA, Settleman J, Reynolds AB (2006) p120-catenin and p190RhoGAP regulate cell-cell adhesion by coordinating antagonism between Rac and rho. Cell 127:1027–1039. https://doi.org/10.1016/j.cell.2006.09.046
Wolf K, Mazo I, Leung H, Engelke K, von Andrian UH, Deryugina EI, Strongin AY, Bröcker EB, Friedl P (2003a) Compensation mechanism in tumor cell migration. J Cell Biol 160:267–277. https://doi.org/10.1083/jcb.200209006
Wolf K, Müller R, Borgmann S, Bröcker EB, Friedl P (2003b) Blood 102:3262–3269. https://doi.org/10.1182/blood-2002-12-3791
Wyckoff JB, Pinner SE, Gschmeissner S, Condeelis JS, Sahai E (2006) ROCK- and myosin-dependent matrix deformation enables protease-independent tumor-cell invasion in vivo. Curr Biol 16:1515–1523. https://doi.org/10.1016/j.cub.2006.05.065
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Gayan, S., Ghuge, P.S., Chitnis, M.S., Dey, T. (2021). Oxidative Stress in Cancer and Its Influence on Amoeboidal Migration. In: Chakraborti, S., Ray, B.K., Roychowdhury, S. (eds) Handbook of Oxidative Stress in Cancer: Mechanistic Aspects. Springer, Singapore. https://doi.org/10.1007/978-981-15-4501-6_79-1
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