Mechanical waves identify the amputation position during wound healing in the amputated zebrafish tailfin

Leon, Marco P. de; Wen, Fu-Lai; Paylaga, Giovanni J.; Wang, Ying-Ting; Roan, Hsiao-Yuh; Wang, Chung-Han; Hsiao, Cheng‐Chieh; Lin, Keng Hui; Chen, Chen‐Hui

doi:10.1038/s41567-023-02103-6

Cited by 4 publications

(3 citation statements)

References 47 publications

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“…We present a model for the role of the fn1b + basal epidermal transient regeneration-activated cell states (TRACS) on reading and writing positional information (Figure 6A-C). In this model, basal epidermis cells adjacent to the amputation plane transition to a TRACS following loss of cell polarity by the absence of basement membrane, and mechanical distension caused by wound closure 12 . We propose that the degree of force applied to the epidermis is proportional to the thickness of the bone at the plane of amputation, along with the corresponding surface area between exposed mesenchyme and wounding epidermis, lead to a proportional number of basal epidermal cells to acquire a basal epidermis TRACS.…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, it has been suggested that positional information is encoded in the tissue within the thickness of the bone at the plane of amputation 10,11 , and that mechanical distension of the epidermis during wound closure constitutes a direct measurement of the amputation position by the wounding epidermis. A wave of mechanical distension in the basal epidermis was shown to propagate to different lengths according to the amputation position 12 . To add to the complexity of this process, it was shown that there is a 2-day time window at the beginning of regeneration when positional information is possibly reestablished de novo .…”

Section: Introductionmentioning

confidence: 99%

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Positional information modulates transient regeneration-activated cell states during vertebrate appendage regeneration

Granillo,

Zamora,

Schnittker

et al. 2024

Preprint

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Injury is a common occurrence in the life of organisms. Because the extent of damage cannot be predicted, injured organisms must determine how much tissue needs to be restored. It is known that amputation position determines the regeneration speed of amputated appendages in regeneration-competent animals. Yet, it is not clear how positional information is conveyed during regeneration. Here, we investigated tissue dynamics in regenerating caudal fins in the African killifish (Nothobranchius furzeri). We report position-specific, differential modulation of the spatial distribution, duration, and magnitude of proliferation. Regenerating fins profiled by single cell RNA sequencing identified a Transient Regeneration-Activated Cell State (TRACS) that is amplified to match a given amputation position. We located this TRACS to the basal epidermis and found them to express components and modifiers of the extracellular matrix (ECM). We propose a role for these cells in transducing positional information to the regenerating blastema by remodeling the ECM.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Positional information modulates transient regeneration-activated cell states during vertebrate appendage regeneration

Granillo,

Zamora,

Schnittker

et al. 2024

Preprint

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“…Cells interact with surrounding ECM components through various surface receptors leading to activation of downstream intracellular pathways. Following injury in regeneration-competent species such as zebrafish, mechanical waves across tissues signal the position of wounds [ 60 ] and pro-regenerative proteins such as laminin and fibronectin are upregulated whereas collagen IV, a major component of fibrotic scars, is downregulated [ 61 ]. This contrasts with non-regenerative species, including humans, that experience scarring following injury, characterized by the differentiation of fibroblasts into ECM-synthesizing myofibroblasts [ 62 ].…”

Section: Biophysical Controlsmentioning

confidence: 99%

Biophysical control of plasticity and patterning in regeneration and cancer

Murugan,

Cariba,

Abeygunawardena

et al. 2023

Cell. Mol. Life Sci.

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Cells and tissues display a remarkable range of plasticity and tissue-patterning activities that are emergent of complex signaling dynamics within their microenvironments. These properties, which when operating normally guide embryogenesis and regeneration, become highly disordered in diseases such as cancer. While morphogens and other molecular factors help determine the shapes of tissues and their patterned cellular organization, the parallel contributions of biophysical control mechanisms must be considered to accurately predict and model important processes such as growth, maturation, injury, repair, and senescence. We now know that mechanical, optical, electric, and electromagnetic signals are integral to cellular plasticity and tissue patterning. Because biophysical modalities underly interactions between cells and their extracellular matrices, including cell cycle, metabolism, migration, and differentiation, their applications as tuning dials for regenerative and anti-cancer therapies are being rapidly exploited. Despite this, the importance of cellular communication through biophysical signaling remains disproportionately underrepresented in the literature. Here, we provide a review of biophysical signaling modalities and known mechanisms that initiate, modulate, or inhibit plasticity and tissue patterning in models of regeneration and cancer. We also discuss current approaches in biomedical engineering that harness biophysical control mechanisms to model, characterize, diagnose, and treat disease states.

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Appendage-resident epithelial cells expedite wound healing response in adult zebrafish

Santoso,

De Leon,

Kao

et al. 2024

Current Biology

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Mechanical waves identify the amputation position during wound healing in the amputated zebrafish tailfin

Cited by 4 publications

References 47 publications

Positional information modulates transient regeneration-activated cell states during vertebrate appendage regeneration

Positional information modulates transient regeneration-activated cell states during vertebrate appendage regeneration

Biophysical control of plasticity and patterning in regeneration and cancer

Appendage-resident epithelial cells expedite wound healing response in adult zebrafish

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