Extracellular Vesicles and Membrane Protrusions in Developmental Signaling

doi:10.3390/jdb10040039

Review

. 2022 Sep 21;10(4):39.

doi: 10.3390/jdb10040039.

Extracellular Vesicles and Membrane Protrusions in Developmental Signaling

Callie M Gustafson^{1

2}, Laura S Gammill^{1

2}

Affiliations

¹ Department of Genetics, Cell Biology and Development, University of Minnesota, 6-160 Jackson Hall, 321 Church St SE, Minneapolis, MN 55455, USA.
² Developmental Biology Center, University of Minnesota, 6-160 Jackson Hall, 321 Church St SE, Minneapolis, MN 55455, USA.

PMID: 36278544
PMCID: PMC9589955
DOI: 10.3390/jdb10040039

Review

Extracellular Vesicles and Membrane Protrusions in Developmental Signaling

Callie M Gustafson et al. J Dev Biol. 2022.

. 2022 Sep 21;10(4):39.

doi: 10.3390/jdb10040039.

Authors

Callie M Gustafson^{1

2}, Laura S Gammill^{1

2}

Affiliations

¹ Department of Genetics, Cell Biology and Development, University of Minnesota, 6-160 Jackson Hall, 321 Church St SE, Minneapolis, MN 55455, USA.
² Developmental Biology Center, University of Minnesota, 6-160 Jackson Hall, 321 Church St SE, Minneapolis, MN 55455, USA.

PMID: 36278544
PMCID: PMC9589955
DOI: 10.3390/jdb10040039

Abstract

During embryonic development, cells communicate with each other to determine cell fate, guide migration, and shape morphogenesis. While the relevant secreted factors and their downstream target genes have been characterized extensively, how these signals travel between embryonic cells is still emerging. Evidence is accumulating that extracellular vesicles (EVs), which are well defined in cell culture and cancer, offer a crucial means of communication in embryos. Moreover, the release and/or reception of EVs is often facilitated by fine cellular protrusions, which have a history of study in development. However, due in part to the complexities of identifying fragile nanometer-scale extracellular structures within the three-dimensional embryonic environment, the nomenclature of developmental EVs and protrusions can be ambiguous, confounding progress. In this review, we provide a robust guide to categorizing these structures in order to enable comparisons between developmental systems and stages. Then, we discuss existing evidence supporting a role for EVs and fine cellular protrusions throughout development.

Keywords: embryonic development; exosomes; extracellular vesicles; membrane protrusions; migrasomes.

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Conflict of interest statement

The authors declare no conflict of interest.

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References

1. Wellner K. A History of Embryology (1959), by Joseph Needham. Arizona State University; Tempe, AZ, USA: 2010.
1. Christian J.L. Morphogen gradients in development: From form to function. Wiley Interdiscip. Rev. Dev. Biol. 2012;1:3–15. doi: 10.1002/wdev.2. - DOI - PMC - PubMed
1. Takebayashi-Suzuki K., Suzuki A. Intracellular Communication among Morphogen Signaling Pathways during Vertebrate Body Plan Formation. Genes. 2020;11:341. doi: 10.3390/genes11030341. - DOI - PMC - PubMed
1. Stapornwongkul K.S., Vincent J.P. Generation of extracellular morphogen gradients: The case for diffusion. Nat. Rev. Genet. 2021;22:393–411. doi: 10.1038/s41576-021-00342-y. - DOI - PubMed
1. Thery C., Witwer K.W., Aikawa E., Alcaraz M.J., Anderson J.D., Andriantsitohaina R., Antoniou A., Arab T., Archer F., Atkin-Smith G.K., et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): A position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J. Extracell. Vesicles. 2018;7:1535750. doi: 10.1080/20013078.2018.1535750. - DOI - PMC - PubMed

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[1] Wellner K. A History of Embryology (1959), by Joseph Needham. Arizona State University; Tempe, AZ, USA: 2010.

[2] Wellner K. A History of Embryology (1959), by Joseph Needham. Arizona State University; Tempe, AZ, USA: 2010.

[3] Christian J.L. Morphogen gradients in development: From form to function. Wiley Interdiscip. Rev. Dev. Biol. 2012;1:3–15. doi: 10.1002/wdev.2. - DOI - PMC - PubMed

[4] Christian J.L. Morphogen gradients in development: From form to function. Wiley Interdiscip. Rev. Dev. Biol. 2012;1:3–15. doi: 10.1002/wdev.2. - DOI - PMC - PubMed

[5] Takebayashi-Suzuki K., Suzuki A. Intracellular Communication among Morphogen Signaling Pathways during Vertebrate Body Plan Formation. Genes. 2020;11:341. doi: 10.3390/genes11030341. - DOI - PMC - PubMed

[6] Takebayashi-Suzuki K., Suzuki A. Intracellular Communication among Morphogen Signaling Pathways during Vertebrate Body Plan Formation. Genes. 2020;11:341. doi: 10.3390/genes11030341. - DOI - PMC - PubMed

[7] Stapornwongkul K.S., Vincent J.P. Generation of extracellular morphogen gradients: The case for diffusion. Nat. Rev. Genet. 2021;22:393–411. doi: 10.1038/s41576-021-00342-y. - DOI - PubMed

[8] Stapornwongkul K.S., Vincent J.P. Generation of extracellular morphogen gradients: The case for diffusion. Nat. Rev. Genet. 2021;22:393–411. doi: 10.1038/s41576-021-00342-y. - DOI - PubMed

[9] Thery C., Witwer K.W., Aikawa E., Alcaraz M.J., Anderson J.D., Andriantsitohaina R., Antoniou A., Arab T., Archer F., Atkin-Smith G.K., et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): A position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J. Extracell. Vesicles. 2018;7:1535750. doi: 10.1080/20013078.2018.1535750. - DOI - PMC - PubMed

[10] Thery C., Witwer K.W., Aikawa E., Alcaraz M.J., Anderson J.D., Andriantsitohaina R., Antoniou A., Arab T., Archer F., Atkin-Smith G.K., et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): A position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J. Extracell. Vesicles. 2018;7:1535750. doi: 10.1080/20013078.2018.1535750. - DOI - PMC - PubMed

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Extracellular Vesicles and Membrane Protrusions in Developmental Signaling

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Extracellular Vesicles and Membrane Protrusions in Developmental Signaling

Authors

Affiliations

Abstract

Conflict of interest statement

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