Stem cell migration drives lung repair in living mice

Maurizio Chioccioli; Shuyu Liu; Sumner Magruder; Aleksandra Tata; Lucia Borriello; John E. McDonough; Arvind Konkimalla; Sang Hun Kim; Jessica Nouws; David G. Gonzalez; Brian Traub; Xianjun Ye; Tao Yang; David R. Entenberg; Smita Krishnaswamy; Caroline E. Hendry; Naftali Kaminski; Purushothama Rao Tata; Maor Sauler

doi:10.1016/j.devcel.2024.02.003

Stem cell migration drives lung repair in living mice

Maurizio Chioccioli, Shuyu Liu, Sumner Magruder, Aleksandra Tata, Lucia Borriello, John E. McDonough, Arvind Konkimalla, Sang Hun Kim, Jessica Nouws, David G. Gonzalez, Brian Traub, Xianjun Ye, Tao Yang, David R. Entenberg, Smita Krishnaswamy, Caroline E. Hendry, Naftali Kaminski, Purushothama Rao Tata, Maor Sauler

Pathology

Research output: Contribution to journal › Article › peer-review

Abstract

Tissue repair requires a highly coordinated cellular response to injury. In the lung, alveolar type 2 cells (AT2s) act as stem cells to replenish both themselves and alveolar type 1 cells (AT1s); however, the complex orchestration of stem cell activity after injury is poorly understood. Here, we establish longitudinal imaging of AT2s in murine intact tissues ex vivo and in vivo in order to track their dynamic behavior over time. We discover that a large fraction of AT2s become motile following injury and provide direct evidence for their migration between alveolar units. High-resolution morphokinetic mapping of AT2s further uncovers the emergence of distinct motile phenotypes. Inhibition of AT2 migration via genetic depletion of ArpC3 leads to impaired regeneration of AT2s and AT1s in vivo. Together, our results establish a requirement for stem cell migration between alveolar units and identify properties of stem cell motility at high cellular resolution.

Original language	English (US)
Pages (from-to)	830-840.e4
Journal	Developmental cell
Volume	59
Issue number	7
DOIs	https://doi.org/10.1016/j.devcel.2024.02.003
State	Published - Apr 8 2024

ASJC Scopus subject areas

Molecular Biology
General Biochemistry, Genetics and Molecular Biology
Developmental Biology
Cell Biology

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Chioccioli, M., Liu, S., Magruder, S., Tata, A., Borriello, L., McDonough, J. E., Konkimalla, A., Kim, S. H., Nouws, J., Gonzalez, D. G., Traub, B., Ye, X., Yang, T., Entenberg, D. R., Krishnaswamy, S., Hendry, C. E., Kaminski, N., Tata, P. R., & Sauler, M. (2024). Stem cell migration drives lung repair in living mice. Developmental cell, 59(7), 830-840.e4. https://doi.org/10.1016/j.devcel.2024.02.003

Chioccioli, M, Liu, S, Magruder, S, Tata, A, Borriello, L, McDonough, JE, Konkimalla, A, Kim, SH, Nouws, J, Gonzalez, DG, Traub, B, Ye, X, Yang, T, Entenberg, DR, Krishnaswamy, S, Hendry, CE, Kaminski, N, Tata, PR & Sauler, M 2024, 'Stem cell migration drives lung repair in living mice', Developmental cell, vol. 59, no. 7, pp. 830-840.e4. https://doi.org/10.1016/j.devcel.2024.02.003

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abstract = "Tissue repair requires a highly coordinated cellular response to injury. In the lung, alveolar type 2 cells (AT2s) act as stem cells to replenish both themselves and alveolar type 1 cells (AT1s); however, the complex orchestration of stem cell activity after injury is poorly understood. Here, we establish longitudinal imaging of AT2s in murine intact tissues ex vivo and in vivo in order to track their dynamic behavior over time. We discover that a large fraction of AT2s become motile following injury and provide direct evidence for their migration between alveolar units. High-resolution morphokinetic mapping of AT2s further uncovers the emergence of distinct motile phenotypes. Inhibition of AT2 migration via genetic depletion of ArpC3 leads to impaired regeneration of AT2s and AT1s in vivo. Together, our results establish a requirement for stem cell migration between alveolar units and identify properties of stem cell motility at high cellular resolution.",

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AU - Chioccioli, Maurizio

AU - Liu, Shuyu

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AU - Tata, Aleksandra

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AU - McDonough, John E.

AU - Konkimalla, Arvind

AU - Kim, Sang Hun

AU - Nouws, Jessica

AU - Gonzalez, David G.

AU - Traub, Brian

AU - Ye, Xianjun

AU - Yang, Tao

AU - Entenberg, David R.

AU - Krishnaswamy, Smita

AU - Hendry, Caroline E.

AU - Kaminski, Naftali

AU - Tata, Purushothama Rao

AU - Sauler, Maor

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AB - Tissue repair requires a highly coordinated cellular response to injury. In the lung, alveolar type 2 cells (AT2s) act as stem cells to replenish both themselves and alveolar type 1 cells (AT1s); however, the complex orchestration of stem cell activity after injury is poorly understood. Here, we establish longitudinal imaging of AT2s in murine intact tissues ex vivo and in vivo in order to track their dynamic behavior over time. We discover that a large fraction of AT2s become motile following injury and provide direct evidence for their migration between alveolar units. High-resolution morphokinetic mapping of AT2s further uncovers the emergence of distinct motile phenotypes. Inhibition of AT2 migration via genetic depletion of ArpC3 leads to impaired regeneration of AT2s and AT1s in vivo. Together, our results establish a requirement for stem cell migration between alveolar units and identify properties of stem cell motility at high cellular resolution.

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Stem cell migration drives lung repair in living mice

Abstract

ASJC Scopus subject areas

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