Amoeboid Migration in Health and Disease: Immune Responses Cancer Dissemination

Overview

Journal Front Cell Dev Biol

Specialty Cell Biology

Date 2023 Jan 26

PMID 36699013

Authors

Samantha George

Joshua Alexander James Martin

Vittoria Graziani

Victoria Sanz-Moreno

Affiliations

Soon will be listed here.

Abstract

Cell migration is crucial for efficient immune responses and is aberrantly used by cancer cells during metastatic dissemination. Amoeboid migrating cells use myosin II-powered blebs to propel themselves, and change morphology and direction. Immune cells use amoeboid strategies to respond rapidly to infection or tissue damage, which require quick passage through several barriers, including blood, lymph and interstitial tissues, with complex and varied environments. Amoeboid migration is also used by metastatic cancer cells to aid their migration, dissemination and survival, whereby key mechanisms are hijacked from professionally motile immune cells. We explore important parallels observed between amoeboid immune and cancer cells. We also consider key distinctions that separate the lifespan, state and fate of these cell types as they migrate and/or fulfil their function. Finally, we reflect on unexplored areas of research that would enhance our understanding of how tumour cells use immune cell strategies during metastasis, and how to target these processes.

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References

Cantelli G, Orgaz J, Rodriguez-Hernandez I, Karagiannis P, Maiques O, Matias-Guiu X . TGF-β-Induced Transcription Sustains Amoeboid Melanoma Migration and Dissemination. Curr Biol. 2015; 25(22):2899-914. PMC: 4651903. DOI: 10.1016/j.cub.2015.09.054. View

Sharma P, Hu-Lieskovan S, Wargo J, Ribas A . Primary, Adaptive, and Acquired Resistance to Cancer Immunotherapy. Cell. 2017; 168(4):707-723. PMC: 5391692. DOI: 10.1016/j.cell.2017.01.017. View

Amini R, Bhatnagar A, Schlussler R, Mollmert S, Guck J, Norden C . Amoeboid-like migration ensures correct horizontal cell layer formation in the developing vertebrate retina. Elife. 2022; 11. PMC: 9208757. DOI: 10.7554/eLife.76408. View

Kameritsch P, Renkawitz J . Principles of Leukocyte Migration Strategies. Trends Cell Biol. 2020; 30(10):818-832. DOI: 10.1016/j.tcb.2020.06.007. View

Boland S, Bourin A, Alen J, Geraets J, Schroeders P, Castermans K . Design, synthesis, and biological evaluation of novel, highly active soft ROCK inhibitors. J Med Chem. 2015; 58(10):4309-24. DOI: 10.1021/acs.jmedchem.5b00308. View

Ruscitti P, Masedu F, Alvaro S, Airo P, Battafarano N, Cantarini L . Anti-interleukin-1 treatment in patients with rheumatoid arthritis and type 2 diabetes (TRACK): A multicentre, open-label, randomised controlled trial. PLoS Med. 2019; 16(9):e1002901. PMC: 6742232. DOI: 10.1371/journal.pmed.1002901. View

van Goethem E, Poincloux R, Gauffre F, Maridonneau-Parini I, Le Cabec V . Matrix architecture dictates three-dimensional migration modes of human macrophages: differential involvement of proteases and podosome-like structures. J Immunol. 2009; 184(2):1049-61. DOI: 10.4049/jimmunol.0902223. View

Akincilar S, Chan C, Ng Q, Fidan K, Tergaonkar V . Non-canonical roles of canonical telomere binding proteins in cancers. Cell Mol Life Sci. 2021; 78(9):4235-4257. PMC: 8164586. DOI: 10.1007/s00018-021-03783-0. View

Kai F, Drain A, Weaver V . The Extracellular Matrix Modulates the Metastatic Journey. Dev Cell. 2019; 49(3):332-346. PMC: 6527347. DOI: 10.1016/j.devcel.2019.03.026. View

10.

Muller W . Getting leukocytes to the site of inflammation. Vet Pathol. 2013; 50(1):7-22. PMC: 3628536. DOI: 10.1177/0300985812469883. View

11.

Bros M, Haas K, Moll L, Grabbe S . RhoA as a Key Regulator of Innate and Adaptive Immunity. Cells. 2019; 8(7). PMC: 6678964. DOI: 10.3390/cells8070733. View

12.

Senapati S, Mahanta A, Kumar S, Maiti P . Controlled drug delivery vehicles for cancer treatment and their performance. Signal Transduct Target Ther. 2018; 3:7. PMC: 5854578. DOI: 10.1038/s41392-017-0004-3. View

13.

Guenther C . β2-Integrins - Regulatory and Executive Bridges in the Signaling Network Controlling Leukocyte Trafficking and Migration. Front Immunol. 2022; 13:809590. PMC: 9072638. DOI: 10.3389/fimmu.2022.809590. View

14.

Mitroulis I, Alexaki V, Kourtzelis I, Ziogas A, Hajishengallis G, Chavakis T . Leukocyte integrins: role in leukocyte recruitment and as therapeutic targets in inflammatory disease. Pharmacol Ther. 2014; 147:123-135. PMC: 4324083. DOI: 10.1016/j.pharmthera.2014.11.008. View

15.

Sokeland G, Schumacher U . The functional role of integrins during intra- and extravasation within the metastatic cascade. Mol Cancer. 2019; 18(1):12. PMC: 6337777. DOI: 10.1186/s12943-018-0937-3. View

16.

Dyberg C, Fransson S, Andonova T, Sveinbjornsson B, Lannerholm-Palm J, Olsen T . Rho-associated kinase is a therapeutic target in neuroblastoma. Proc Natl Acad Sci U S A. 2017; 114(32):E6603-E6612. PMC: 5559038. DOI: 10.1073/pnas.1706011114. View

17.

Suresh S . Biomechanics and biophysics of cancer cells. Acta Biomater. 2007; 3(4):413-38. PMC: 2917191. DOI: 10.1016/j.actbio.2007.04.002. View

18.

Ali F, Ilyas A . Belumosudil with ROCK-2 inhibition: chemical and therapeutic development to FDA approval for the treatment of chronic graft-versus-host disease. Curr Res Transl Med. 2022; 70(3):103343. DOI: 10.1016/j.retram.2022.103343. View

19.

Linder S, Aepfelbacher M . Podosomes: adhesion hot-spots of invasive cells. Trends Cell Biol. 2003; 13(7):376-85. DOI: 10.1016/s0962-8924(03)00128-4. View

20.

Oudin M, Jonas O, Kosciuk T, Broye L, Guido B, Wyckoff J . Tumor Cell-Driven Extracellular Matrix Remodeling Drives Haptotaxis during Metastatic Progression. Cancer Discov. 2016; 6(5):516-31. PMC: 4854754. DOI: 10.1158/2159-8290.CD-15-1183. View