Functional consequences of somatic polyploidy in development

Gabriella S. Darmasaputra; Lotte M. van Rijnberk; Matilde Galli

doi:10.1242/dev.202392

journal article Open Access Feb 28, 2024

Functional consequences of somatic polyploidy in development

Gabriella S. Darmasaputra Lotte M. van Rijnberk

Matilde Galli

Development Vol. 151 No. 5 · The Company of Biologists

View at Publisher Save 10.1242/dev.202392

Abstract

ABSTRACT
Polyploid cells contain multiple genome copies and arise in many animal tissues as a regulated part of development. However, polyploid cells can also arise due to cell division failure, DNA damage or tissue damage. Although polyploidization is crucial for the integrity and function of many tissues, the cellular and tissue-wide consequences of polyploidy can be very diverse. Nonetheless, many polyploid cell types and tissues share a remarkable similarity in function, providing important information about the possible contribution of polyploidy to cell and tissue function. Here, we review studies on polyploid cells in development, underlining parallel functions between different polyploid cell types, as well as differences between developmentally-programmed and stress-induced polyploidy.

Topics

No keywords indexed for this article. Browse by subject →

References

191

[1]

Abmayr "Myoblast fusion: lessons from flies and mice" Development (2012) 10.1242/dev.068353

[2]

Almeida "Polyploidy in development and tumor models in Drosophila" Semin. Cancer Biol. (2022) 10.1016/j.semcancer.2021.09.011

[3]

Amodeo "Cell-Size Control" Cold Spring Harb. Perspect. Biol. (2016) 10.1101/cshperspect.a019083

[4]

Andalis "Defects arising from whole-genome duplications in Saccharomyces cerevisiae" Genetics (2004) 10.1534/genetics.104.029256

[5]

Andrulis "High-resolution localization of Drosophila Spt5 and Spt6 at heat shock genes in vivo: roles in promoter proximal pausing and transcription elongation" Genes Dev. (2000) 10.1101/gad.844200

[6]

Anisimov "Endopolyploidy as a morphogenetic factor of development" Cell Biol. Int. (2005) 10.1016/j.cellbi.2005.10.013

[7]

Arrese "Insect fat body: energy, metabolism, and regulation" Annu. Rev. Entomol. (2010) 10.1146/annurev-ento-112408-085356

[8]

Azar "RNA-Seq identifies genes whose proteins are transformative in the differentiation of cytotrophoblast to syncytiotrophoblast, in human primary villous and BeWo trophoblasts" Sci. Rep. (2018) 10.1038/s41598-018-23379-2

[9]

Bursty Gene Expression in the Intact Mammalian Liver

Keren Bahar Halpern, Sivan Tanami, Shanie Landen et al.

Molecular Cell 2015 10.1016/j.molcel.2015.01.027

[10]

Barlow "Cytological studies on the organization of DNA in giant trophoblast nuclei of the mouse and the rat" Chromosoma (1974) 10.1007/bf00331800

[11]

Bastock "Drosophila oogenesis" Curr. Biol. (2008) 10.1016/j.cub.2008.09.011

[12]

Belyaeva "Su(UR)ES: a gene suppressing DNA underreplication in intercalary and pericentric heterochromatin of Drosophila melanogaster polytene chromosomes" Proc. Natl. Acad. Sci. USA (1998) 10.1073/pnas.95.13.7532

[13]

Bielski "Genome doubling shapes the evolution and prognosis of advanced cancers" Nat. Genet. (2018) 10.1038/s41588-018-0165-1

[14]

Bischoff "Cell rearrangements, cell divisions and cell death in a migrating epithelial sheet in the abdomen of Drosophila" Development (2009) 10.1242/dev.035410

[15]

Blanpain "Plasticity of epithelial stem cells in tissue regeneration" Science (1979) (2014) 10.1126/science.1242281

[16]

Boisnard-Lorig "Dynamic analyses of the expression of the histone::YFP fusion protein in Arabidopsis show that syncytial endosperm is divided in mitotic domains" Plant Cell (2001) 10.1105/tpc.13.3.495

[17]

Bourdon (2010)

[18]

Bourdon "Evidence for karyoplasmic homeostasis during endoreduplication and a ploidy-dependent increase in gene transcription during tomato fruit growth" Development (2012) 10.1242/dev.084053

[19]

Boveri (1905)

[20]

Breuer "Behavior of polytene chromosomes of rhynchosciara angelae at different stages of larval development" Chromosoma (1955) 10.1007/bf00329733

[21]

Buntrock "Organ growth without cell division: somatic polyploidy in a moth, Ephestia kuehniella" Genome (2012) 10.1139/g2012-060

[22]

Campbell "Targeting protein function: the expanding toolkit for conditional disruption" Biochem. J (2016) 10.1042/bcj20160240

[23]

Cao "Tension creates an endoreplication wavefront that leads regeneration of epicardial tissue" Dev. Cell (2017) 10.1016/j.devcel.2017.08.024

[24]

Carvalho "The yolk syncytial layer in early zebrafish development" Trends Cell Biol. (2010) 10.1016/j.tcb.2010.06.009

[25]

Chakraborty "Conserved chamber-specific polyploidy maintains heart function in Drosophila" Development (2023) 10.1242/dev.201896

[26]

Chell "Nutrition-responsive glia control exit of neural stem cells from quiescence" Cell (2010) 10.1016/j.cell.2010.12.007

[27]

Chen "Canonical and atypical E2Fs regulate the mammalian endocycle" Nat. Cell Biol. (2012) 10.1038/ncb2595

[28]

Cheniclet "Cell expansion and endoreduplication show a large genetic variability in pericarp and contribute strongly to tomato fruit growth" Plant Physiol. (2005) 10.1104/pp.105.068767

[29]

Chevalier "Elucidating the functional role of endoreduplication in tomato fruit development" Ann. Bot. (2011) 10.1093/aob/mcq257

[30]

Chinzei "Nucleic acid changes in the whole body and several organs of the silkworm, Bombyx mori, during metamorphosis" J. Insect Physiol. (1972) 10.1016/0022-1910(72)90098-4

[31]

Choudry "Transcriptional characterization of human megakaryocyte polyploidization and lineage commitment" J. Thromb. Haemost. (2021) 10.1111/jth.15271

[32]

Cohen "Fizzy-related dictates a cell cycle switch during organ repair and tissue growth responses in the drosophila hindgut" eLife (2018) 10.7554/elife.38327

[33]

The Causes and Consequences of Polyploidy in Normal Development and Cancer

Teresa Davoli, Titia de Lange

Annual Review of Cell and Developmental Biology 2011 10.1146/annurev-cellbio-092910-154234

[34]

De Almeida Engler "Nematode-induced endoreduplication in plant host cells: why and how?" Mol. Plant-Microbe Interact. (2013) 10.1094/mpmi-05-12-0128-cr

[35]

De Almeida Engler "Molecular markers and cell cycle inhibitors show the importance of cell cycle progression in nematode-induced galls and syncytia" Plant Cell (1999) 10.1105/tpc.11.5.793

[36]

De Chiara "Tubular cell polyploidy protects from lethal acute kidney injury but promotes consequent chronic kidney disease" Nat. Commun. (2022) 10.1038/s41467-022-33110-5

[37]

De Renty "Cytoplasmic localization of p21 protects trophoblast giant cells from DNA damage induced apoptosis" PLoS One (2014) 10.1371/journal.pone.0097434

[38]

Dej "The endocycle controls nurse cell polytene chromosome structure during Drosophila oogenesis" Development (1999) 10.1242/dev.126.2.293

[39]

Demontis "Integration of Insulin receptor/Foxo signaling and dMyc activity during muscle growth regulates body size in Drosophila" Development (2009) 10.1242/dev.027466

[40]

Dittmann "Ploidy levels and DNA synthesis in fat body cells of the adult mosquito, Aedes aegypti: the role of juvenile hormone" Arch. Insect Biochem. Physiol. (1989) 10.1002/arch.940120302

[41]

Doerflinger "The Drosophila anterior-posterior axis is polarized by asymmetric myosin activation" Curr. Biol. (2022) 10.1016/j.cub.2021.11.024

[42]

Donne "Polyploidy in liver development, homeostasis and disease" Nat. Rev. Gastroenterol. Hepatol. (2020) 10.1038/s41575-020-0284-x

[43]

Single-nucleus RNA-seq and FISH identify coordinated transcriptional activity in mammalian myofibers

Matthieu Dos Santos, Stéphanie Backer, Benjamin Saintpierre et al.

Nature Communications 2020 10.1038/s41467-020-18789-8

[44]

The ploidy conveyor of mature hepatocytes as a source of genetic variation

Andrew W. Duncan, Matthew H. Taylor, Raymond D. Hickey et al.

Nature 2010 10.1038/nature09414

[45]

Ebert "Nuclear DNA of myocardial cells in the periphery of infarctions and scars" Virchows Arch. B Cell Pathol. (1977) 10.1007/bf02889280

[46]

Edgar "Endocycles: a recurrent evolutionary innovation for post-mitotic cell growth" Nat. Rev. Mol. Cell Biol. (2014) 10.1038/nrm3756

[47]

Editorial "Giant-cells in syphilomata" Edinb. Med. J. (1877)

[48]

Editorial "The nature of giant-cells in tubercle" Br. Med. J. (1878)

[49]

Epstein "Cell size, nuclear content, and the development of polyploidy in the mammalian liver" Proc. Natl. Acad. Sci. USA (1967) 10.1073/pnas.57.2.327

[50]

Increased insulin-like growth factor 1 production by polyploid adipose stem cells promotes growth of breast cancer cells

Roberta Fajka-Boja, Annamária Marton, Anna Tóth et al.

BMC Cancer 2018 10.1186/s12885-018-4781-z

Showing 50 of 191 references

Metrics

24

Citations

191

References

Details

Published: Feb 28, 2024
Vol/Issue: 151(5)
License: View

Authors

G

Gabriella S. Darmasaputra

Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences and University Medical Center Utrecht , Uppsalalaan 8, 3584 CT, Utrecht , the Netherlands

L

Lotte M. van Rijnberk

Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences and University Medical Center Utrecht , Uppsalalaan 8, 3584 CT, Utrecht , the Netherlands

M

Matilde Galli

Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences and University Medical Center Utrecht , Uppsalalaan 8, 3584 CT, Utrecht , the Netherlands

Funding

European Research Council Award: 101040020 DevCycle

Nederlandse Organisatie voor Wetenschappelijk Onderzoek Award: OCENW.KLEIN.258

Cancer Genomics Center

Cite This Article

Gabriella S. Darmasaputra, Lotte M. van Rijnberk, Matilde Galli (2024). Functional consequences of somatic polyploidy in development. Development, 151(5). https://doi.org/10.1242/dev.202392

Functional consequences of somatic polyploidy in development

You May Also Like