Cell migration during development: Is it always collective and never as a single cell?

Abstract

Cell migration is a fundamental process essential for homeostasis, disease progression, and developmental biology. This review explores the mechanisms of cell migration, focusing on both single-cell and collective migration modes, and highlights their roles in early development. We examine the characteristics of amoeboid and mesenchymal migration, emphasizing their regulation and implications across various classical developmental models. By analyzing examples of single-cell migration, such as primordial germ cell migration in zebrafish and Drosophila melanogaster, and examples of collective cell migration in the lateral line of zebrafish, border cells, and testis myotubes in Drosophila, we illustrate the complexity and significance of cell-cell interactions, cell-matrix interactions, and the chemical and mechanical cues that drive migration. The review also highlights the "supracellular organization" observed in many systems where supracellular actomyosin cables are present, which allow for coordinated and cooperative movement. This cooperativity is crucial for effective positioning and function, ensuring proper tissue formation and responsive adaptation to environmental cues. This review provides insights and raises questions about the mechanisms of cell migration during development, supporting the idea that cells never migrate entirely alone. We propose that even in those cases normally described as single cell migration, some degree of collectiveness or cooperation is involved, suggesting that during development, cells always migrate in collective coordination when forming complex tissue and organ structures.