Spatial transcriptomics reveals asymmetric cellular responses to injury in the regenerating spiny mouse (Acomys) ear

TY - JOUR

T1 - Spatial transcriptomics reveals asymmetric cellular responses to injury in the regenerating spiny mouse (Acomys) ear

AU - van Beijnum, Henriëtte

AU - Koopmans, Tim

AU - Tomasso, Antonio

AU - Disela, Vanessa

AU - Te Lindert, Severin

AU - Bakkers, Jeroen

AU - Alemany, Anna

AU - Berezikov, Eugene

AU - Bartscherer, Kerstin

N1 - © 2023 van Beijnum et al.; Published by Cold Spring Harbor Laboratory Press.

PY - 2023/8

Y1 - 2023/8

N2 - In contrast to other mammals, the spiny mouse (Acomys) regenerates skin and ear tissue, which includes hair follicles, glands, and cartilage, in a scar-free manner. Ear punch regeneration is asymmetric with only the proximal wound side participating in regeneration. Here, we show that cues originating from the proximal side are required for normal regeneration and use spatially resolved transcriptomics (tomo-seq) to understand the molecular and cellular events underlying this process. Analyzing gene expression across the ear and comparing expression modules between proximal and distal wound sides, we identify asymmetric gene expression patterns and pinpoint regenerative processes in space and time. Moreover, using a comparative approach with nonregenerative rodents (Mus, Meriones), we strengthen a hypothesis in which particularities in the injury-induced immune response may be one of the crucial determinants for why spiny mice regenerate whereas their relatives do not. Our data are available in SpinyMine, an easy-to-use and expandable web-based tool for exploring Acomys regeneration-associated gene expression.

AB - In contrast to other mammals, the spiny mouse (Acomys) regenerates skin and ear tissue, which includes hair follicles, glands, and cartilage, in a scar-free manner. Ear punch regeneration is asymmetric with only the proximal wound side participating in regeneration. Here, we show that cues originating from the proximal side are required for normal regeneration and use spatially resolved transcriptomics (tomo-seq) to understand the molecular and cellular events underlying this process. Analyzing gene expression across the ear and comparing expression modules between proximal and distal wound sides, we identify asymmetric gene expression patterns and pinpoint regenerative processes in space and time. Moreover, using a comparative approach with nonregenerative rodents (Mus, Meriones), we strengthen a hypothesis in which particularities in the injury-induced immune response may be one of the crucial determinants for why spiny mice regenerate whereas their relatives do not. Our data are available in SpinyMine, an easy-to-use and expandable web-based tool for exploring Acomys regeneration-associated gene expression.

KW - Animals

KW - Wound Healing/genetics

KW - Murinae/genetics

KW - Transcriptome

KW - Regeneration/genetics

KW - Skin

KW - Mammals/genetics

U2 - 10.1101/gr.277538.122

DO - 10.1101/gr.277538.122

M3 - Article

C2 - 37726147

SN - 1088-9051

VL - 33

SP - 1424

EP - 1437

JO - Genome Research

JF - Genome Research

IS - 8

ER -