Migratory responses in enucleated cells: The forces driving the locomotion movement of unicellular organisms

Locomotion movements are a fundamental characteristic of a variety of species, including prokaryotic and eukaryotic, that has a high impact on essential physiological and pathological processes. For decades, many different authors have focused on studying specific individual processes and their corresponding biomolecular components involved in cellular locomotion movements. Recently, we have shown that locomotion movements are regulated by integrative self-organized molecular processes operating at the systemic level. Here, to verify that said systemic behavior also exists in extreme critical physiological conditions such as those corresponding to enucleated cells, we carried out an extensive study with 200 enucleated cells (cytoplasts) belonging to the <i>Amoeba proteus</i> species. The migratory movements of both enucleated and nonenucleated cells (400 in total) have been individually studied in four different scenarios: in the absence of stimuli, under a galvanotactic field, in a chemotactic gradient, and under complex conditions such as simultaneous galvanotactic and chemotactic stimuli. All the experimental trajectories were analyzed using nonlinear quantitative metrics for individual cell trajectories. The results show that both nonenucleated amoebas and cytoplasts display the same type of dynamic migratory patterns. The locomotion displacements of enucleated cells are a consequence of complex self-organized molecular dynamics, modulated at a systemic-cytoplasmic level. We have also quantitatively detected that enucleation clearly affects the correlation times and the intensity of the migratory responses of cytoplasts. The fact that cytoplasts preserved the dynamic properties of their migratory trajectories when compared with nonenucleated cells suggests that nuclear activity has a minor role in regulating the locomotion displacements of cells.

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Journal
PNAS Nexus
Published
2025-07-25
DOI
https://doi.org/10.1093/pnasnexus/pgaf232
Primary Topic
Protist diversity and phylogeny
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article
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article

Migratory responses in enucleated cells: The forces driving the locomotion movement of unicellular organisms

Alberto Pérez-Samartı́n, Luis Martínez Sáez, José I. López, Marı́a Fedetz et al.
PNAS Nexus
Protist diversity and phylogeny
article

Migratory responses in enucleated cells: The forces driving the locomotion movement of unicellular organisms

Alberto Pérez-Samartı́n, Luis Martínez Sáez, José I. López, Marı́a Fedetz, Jesús M. Cortés, Carlos Bringas Roldan, Iker Malaina, Jose Carrasco-Pujante, Ildefonso M. De la Fuente, Gorka Pérez‐Yarza
article en

Abstract

Locomotion movements are a fundamental characteristic of a variety of species, including prokaryotic and eukaryotic, that has a high impact on essential physiological and pathological processes. For decades, many different authors have focused on studying specific individual processes and their corresponding biomolecular components involved in cellular locomotion movements. Recently, we have shown that locomotion movements are regulated by integrative self-organized molecular processes operating at the systemic level. Here, to verify that said systemic behavior also exists in extreme critical physiological conditions such as those corresponding to enucleated cells, we carried out an extensive study with 200 enucleated cells (cytoplasts) belonging to the <i>Amoeba proteus</i> species. The migratory movements of both enucleated and nonenucleated cells (400 in total) have been individually studied in four different scenarios: in the absence of stimuli, under a galvanotactic field, in a chemotactic gradient, and under complex conditions such as simultaneous galvanotactic and chemotactic stimuli. All the experimental trajectories were analyzed using nonlinear quantitative metrics for individual cell trajectories. The results show that both nonenucleated amoebas and cytoplasts display the same type of dynamic migratory patterns. The locomotion displacements of enucleated cells are a consequence of complex self-organized molecular dynamics, modulated at a systemic-cytoplasmic level. We have also quantitatively detected that enucleation clearly affects the correlation times and the intensity of the migratory responses of cytoplasts. The fact that cytoplasts preserved the dynamic properties of their migratory trajectories when compared with nonenucleated cells suggests that nuclear activity has a minor role in regulating the locomotion displacements of cells.

PNAS NexusVol. 4(8)
Ikerbasque (ES), University of the Basque Country (ES), BioCruces Health research Institute (ES), Achucarro Basque Center for Neuroscience (ES), Centro de Edafología y Biología Aplicada del Segura (ES), Instituto de Parasitología y Biomedicina "López - Neyra" (ES)
Openalex Percentile: Top 83%
Protist diversity and phylogeny
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