Plasticity of cancer invasion and energy metabolism. Issue 5 (May 2023)

• Record Type: Journal Article
• Authors: Parlani, Maria; Jorgez, Carolina; Friedl, Peter
• Is Part Of: Trends in cell biology. Volume 33:Issue 5(2023)
• Page Start: 388
• Page End: 402
• Publication Date: 2023-05
• Subjects: cellular bioenergetics -- migration plasticity -- metabolic stress -- amoeboid migration; Cytology -- Periodicals; Cytology -- Research -- Periodicals; 571.6
• DOI: 10.1016/j.tcb.2022.09.009
• Languages: English
• ISSNs: 0962-8924

Abstract

Abstract: Energy deprivation is a frequent adverse event in tumors that is caused by mutations, malperfusion, hypoxia, and nutrition deficit. The resulting bioenergetic stress leads to signaling and metabolic adaptation responses in tumor cells, secures survival, and adjusts migration activity. The kinetic responses of cancer cells to energy deficit were recently identified, including a switch of invasive cancer cells to energy-conservative amoeboid migration and an enhanced capability for distant metastasis. We review the energy programs employed by different cancer invasion modes including collective, mesenchymal, and amoeboid migration, as well as their interconversion in response to energy deprivation, and we discuss the consequences for metastatic escape. Understanding the energy requirements of amoeboid and other dissemination strategies offers rationales for improving therapeutic targeting of metastatic cancer progression. Highlights: Mechanochemical strategies deployed by cancer cells to invade tissues depend upon different amounts of energy production and consumption. Whereas collective and mesenchymal migration is bioenergetically demanding, amoeboid migration is energetically favorable. Under conditions of energy deprivation, invading cancer cells adapt both their cytoskeletal activity and metabolism to save energy and secure migration. Recently identified transitions in response to oxygen and energy deprivation include collective-to-amoeboid and mesenchymal-to-amoeboid transitions. Understanding the crosstalk between bioenergetic and cell migration pathways will aid the identification of intervention points to interfere with tumor cell dissemination and metastasis.