Cell-in-cell phenomena across the tree of life.

Journal

Scientific reports

ISSN: 2045-2322

Titre abrégé: Sci Rep

Pays: England

ID NLM: 101563288

Informations de publication

Date de publication:
29 Mar 2024

Historique:

received: 02 11 2023

accepted: 19 03 2024

medline: 30 3 2024

pubmed: 30 3 2024

entrez: 30 3 2024

Statut: epublish

Résumé

Cells in obligately multicellular organisms by definition have aligned fitness interests, minimum conflict, and cannot reproduce independently. However, some cells eat other cells within the same body, sometimes called cell cannibalism. Such cell-in-cell events have not been thoroughly discussed in the framework of major transitions to multicellularity. We performed a systematic screening of 508 articles, from which we chose 115 relevant articles in a search for cell-in-cell events across the tree of life, the age of cell-in-cell-related genes, and whether cell-in-cell events are associated with normal multicellular development or cancer. Cell-in-cell events are found across the tree of life, from some unicellular to many multicellular organisms, including non-neoplastic and neoplastic tissue. Additionally, out of the 38 cell-in-cell-related genes found in the literature, 14 genes were over 2.2 billion years old, i.e., older than the common ancestor of some facultatively multicellular taxa. All of this suggests that cell-in-cell events may have originated before the origins of obligate multicellularity. Thus, our results show that cell-in-cell events exist in obligate multicellular organisms, but are not a defining feature of them. The idea of eradicating cell-in-cell events from obligate multicellular organisms as a way of treating cancer, without considering that cell-in-cell events are also part of normal development, should be abandoned.

Identifiants

DOI: 10.1038/s41598-024-57528-7 PMID: 38553457

pubmed: 38553457

doi: 10.1038/s41598-024-57528-7

pii: 10.1038/s41598-024-57528-7

doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

Pagination

7535

Subventions

Organisme : NIH HHS

ID : U54 CA217376

Pays : United States

Informations de copyright

Références

Kapsetaki, S. E. et al. Is chimerism associated with cancer across the tree of life?. PLoS ONE 18, e0287901 (2023).

pubmed: 37384647 pmcid: 10309991 doi: 10.1371/journal.pone.0287901

Sharma, N. & Dey, P. Cell cannibalism and cancer. Diagn. Cytopathol. 39, 229–233 (2011).

pubmed: 21319327 doi: 10.1002/dc.21402

Fais, S. & Overholtzer, M. Cell-in-cell phenomena in cancer. Nat. Rev. Cancer 18, 758–766 (2018).

pubmed: 30420767 doi: 10.1038/s41568-018-0073-9

Qian, Y. & Shi, Y. Natural killer cells go inside: Entosis versus cannibalism. Cell Res. 19, 1320–1321 (2009).

pubmed: 19956185 doi: 10.1038/cr.2009.134

Florey, O., Kim, S. E. & Overholtzer, M. Entosis: Cell-in-cell formation that kills through entotic cell death. Curr. Mol. Med. 15, 861–866 (2015).

pubmed: 26511711 doi: 10.2174/1566524015666151026100042

Siquara da Rocha, L. de O., Souza, B. S. de F., Lambert, D. W. & Gurgel Rocha, C. de A. Cell-in-cell events in oral squamous cell carcinoma. Front. Oncol. 12, 931092 (2022).

White, E. Entosis: It’s a cell-eat-cell world. Cell 131, 840–842 (2007).

pubmed: 18045529 pmcid: 2857714 doi: 10.1016/j.cell.2007.11.015

Xia, P., Wang, S., Guo, Z. & Yao, X. Emperipolesis, entosis and beyond: Dance with fate. Cell Res. 18, 705–707 (2008).

pubmed: 18521104 doi: 10.1038/cr.2008.64

Fais, S. Cannibalism: A way to feed on metastatic tumors. Cancer Lett. 258, 155–164 (2007).

pubmed: 17977647 doi: 10.1016/j.canlet.2007.09.014

Fais, S. & Overholtzer, M. Cell-in-cell phenomena, cannibalism, and autophagy: Is there a relationship?. Cell Death Dis. 9, 95 (2018).

pubmed: 29367622 pmcid: 5833709 doi: 10.1038/s41419-017-0111-7

Borensztejn, K. et al. Classification of cell-in-cell structures: Different phenomena with similar appearance. Cells 10 (2021).

Uribe-Querol, E. & Rosales, C. The multiple roles of trogocytosis in immunity, the nervous system, and development. Biomed. Res. Int. 2021, 1601565 (2021).

pubmed: 34604381 pmcid: 8483919 doi: 10.1155/2021/1601565

Elgar, M. A. Cannibalism. Ecology and evolution among diverse taxa (1992).

Gudipaty, S. A., Conner, C. M., Rosenblatt, J. & Montell, D. J. Unconventional ways to live and die: Cell death and survival in development, homeostasis, and disease. Annu. Rev. Cell Dev. Biol. 34, 311–332 (2018).

pubmed: 30089222 pmcid: 6791364 doi: 10.1146/annurev-cellbio-100616-060748

Sierro, F. et al. Suicidal emperipolesis: A process leading to cell-in-cell structures, T cell clearance and immune homeostasis. Curr. Mol. Med. 15, 819–827 (2015).

pubmed: 26511707 doi: 10.2174/1566524015666151026102143

Durgan, J. & Florey, O. Cancer cell cannibalism: Multiple triggers emerge for entosis. Biochim. Biophys. Acta Mol. Cell Res. 1865, 831–841 (2018).

pubmed: 29548938 doi: 10.1016/j.bbamcr.2018.03.004

Bourke, A. F. G. Principles of Social Evolution (Oxford University Press, 2011).

doi: 10.1093/acprof:oso/9780199231157.001.0001

West, S. A., Fisher, R. M., Gardner, A. & Kiers, E. T. Major evolutionary transitions in individuality. Proc. Natl. Acad. Sci. U. S. A. 112, 10112–10119 (2015).

pubmed: 25964342 pmcid: 4547252 doi: 10.1073/pnas.1421402112

Aktipis, C. A. et al. Cancer across the tree of life: Cooperation and cheating in multicellularity. Philos. Trans. R. Soc. Lond. B Biol. Sci. 370, 20140219–20140219 (2015).

pubmed: 26056363 pmcid: 4581024 doi: 10.1098/rstb.2014.0219

Fisher, R. M., Cornwallis, C. K. & West, S. A. Group formation, relatedness, and the evolution of multicellularity. Curr. Biol. 23, 1120–1125 (2013).

pubmed: 23746639 doi: 10.1016/j.cub.2013.05.004

Probst, A. J. et al. Coupling genetic and chemical microbiome profiling reveals heterogeneity of archaeome and bacteriome in subsurface biofilms that are dominated by the same archaeal species. PLoS One 9, e99801 (2014).

pubmed: 24971452 pmcid: 4074051 doi: 10.1371/journal.pone.0099801

CommonTree. NCBI https://www.ncbi.nlm.nih.gov/Taxonomy/CommonTree/wwwcmt.cgi .

Letunic, I. & Bork, P. Interactive tree of life (iTOL) v5: An online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 49, W293–W296 (2021).

pubmed: 33885785 pmcid: 8265157 doi: 10.1093/nar/gkab301

Cosson, P. & Lima, W. C. Intracellular killing of bacteria: Is Dictyostelium a model macrophage or an alien?. Cell. Microbiol. 16, 816–823 (2014).

pubmed: 24628900 pmcid: 4291096 doi: 10.1111/cmi.12291

Sarode, S. C., Sarode, G. S. & Patil, S. Hunger for survival in cancer cells. J. Int. Oral Health 8, I (2016).

Krajcovic, M. et al. A non-genetic route to aneuploidy in human cancers. Nat. Cell Biol. 13, 324–330 (2011).

pubmed: 21336303 pmcid: 3576821 doi: 10.1038/ncb2174

Overholtzer, M. & Brugge, J. S. The cell biology of cell-in-cell structures. Nat. Rev. Mol. Cell Biol. 9, 796–809 (2008).

pubmed: 18784728 doi: 10.1038/nrm2504

Ahmed Wani, F. & Bhardwaj, S. Cytological evaluation and significance of cell cannibalism in effusions and urine cytology. Malays. J. Pathol. 37, 265–270 (2015).

pubmed: 26712673

Gupta, K. & Dey, P. Cell cannibalism: Diagnostic marker of malignancy. Diagn. Cytopathol. 28, 86–87 (2003).

pubmed: 12561027 doi: 10.1002/dc.10234

Lugini, L. et al. Cannibalism of live lymphocytes by human metastatic but not primary melanoma cells. Cancer Res. 66, 3629–3638 (2006).

pubmed: 16585188 doi: 10.1158/0008-5472.CAN-05-3204

Sarode, S. C. & Sarode, G. S. Cellular cannibalism in central and peripheral giant cell granuloma of the oral cavity can predict biological behavior of the lesion. J. Oral Pathol. Med. 43, 459–463 (2014).

pubmed: 24112367 doi: 10.1111/jop.12119

Hattori, M. et al. Cell cannibalism and nucleus-fragmented cells in voided urine: Useful parameters for cytologic diagnosis of low-grade urothelial carcinoma. Acta Cytol. 51, 547–551 (2007).

pubmed: 17718119 doi: 10.1159/000325792

Kinjyo, M., Soejima, T., Watanabe, S. & Hamano, K. A cytological and clinical significance of ’ “pair cells”’in urine cytology. J. Jpn. Soc. Clin. Cytol. (1999).

Alok, M., Singh, S. & Swarn, K. Cell cannibalism as an indicator of anaplasia and tumor aggressiveness in carcinoma breast. J. Adv. Res. Biol. Sci. (2013).

Kojima, S., Sekine, H., Fukui, I. & Ohshima, H. Clinical significance of “cannibalism” in urinary cytology of bladder cancer. Acta Cytol. 42, 1365–1369 (1998).

pubmed: 9850644 doi: 10.1159/000332169

Overholtzer, M. et al. A nonapoptotic cell death process, entosis, that occurs by cell-in-cell invasion. Cell 131, 966–979 (2007).

pubmed: 18045538 doi: 10.1016/j.cell.2007.10.040

Bartosh, T. J., Ullah, M., Zeitouni, S., Beaver, J. & Prockop, D. J. Cancer cells enter dormancy after cannibalizing mesenchymal stem/stromal cells (MSCs). Proc. Natl. Acad. Sci. U. S. A. 113, E6447–E6456 (2016).

pubmed: 27698134 pmcid: 5081643 doi: 10.1073/pnas.1612290113

Sockett, R. E. & Lambert, C. Bdellovibrio as therapeutic agents: A predatory renaissance?. Nat. Rev. Microbiol. 2, 669–675 (2004).

pubmed: 15263901 doi: 10.1038/nrmicro959

Li, Y., Sun, X. & Dey, S. K. Entosis allows timely elimination of the luminal epithelial barrier for embryo implantation. Cell Rep. 11, 358–365 (2015).

pubmed: 25865893 pmcid: 5089169 doi: 10.1016/j.celrep.2015.03.035

Abdu, Y., Maniscalco, C., Heddleston, J. M., Chew, T.-L. & Nance, J. Developmentally programmed germ cell remodelling by endodermal cell cannibalism. Nat. Cell Biol. 18, 1302–1310 (2016).

pubmed: 27842058 pmcid: 5129868 doi: 10.1038/ncb3439

Wen, J. W. & Winklbauer, R. Ingression-type cell migration drives vegetal endoderm internalisation in the Xenopus gastrula. Elife 6 (2017).

Gaitanos, T. N., Koerner, J. & Klein, R. Tiam–Rac signaling mediates trans-endocytosis of ephrin receptor EphB2 and is important for cell repulsion. J. Cell Biol. (2016).

Abmayr, S. M. & Pavlath, G. K. Myoblast fusion: Lessons from flies and mice. Development 139, 641–656 (2012).

pubmed: 22274696 pmcid: 3265056 doi: 10.1242/dev.068353

Landemaine, A., Rescan, P.-Y. & Gabillard, J.-C. Myomaker mediates fusion of fast myocytes in zebrafish embryos. Biochem. Biophys. Res. Commun. 451, 480–484 (2014).

pubmed: 25078621 doi: 10.1016/j.bbrc.2014.07.093

Moore, C. A., Parkin, C. A., Bidet, Y. & Ingham, P. W. A role for the Myoblast city homologues Dock1 and Dock5 and the adaptor proteins Crk and Crk-like in zebrafish myoblast fusion. Development 134, 3145–3153 (2007).

pubmed: 17670792 doi: 10.1242/dev.001214

Kim, J. H., Jin, P., Duan, R. & Chen, E. H. Mechanisms of myoblast fusion during muscle development. Curr. Opin. Genet. Dev. 32, 162–170 (2015).

pubmed: 25989064 pmcid: 4508005 doi: 10.1016/j.gde.2015.03.006

Lizier, M. et al. Cell fusion in the liver, revisited. World J. Hepatol. 10, 213–221 (2018).

pubmed: 29527257 pmcid: 5838440 doi: 10.4254/wjh.v10.i2.213

Gene. Bethesda (MD): National library of medicine (US), National center for biotechnology information. Accession No. TM9SF4 transmembrane 9 superfamily member 4 [Homo sapiens (human)]. https://www.ncbi.nlm.nih.gov/gene/9777 (2004).

Lozupone, F. et al. The human homologue of Dictyostelium discoideum phg1A is expressed by human metastatic melanoma cells. EMBO Rep. 10, 1348–1354 (2009).

pubmed: 19893578 pmcid: 2799214 doi: 10.1038/embor.2009.236

Lozupone, F. & Fais, S. Cancer cell cannibalism: A primeval option to survive. Curr. Mol. Med. 15, 836–841 (2015).

pubmed: 26511709 doi: 10.2174/1566524015666151026100916

Dujon, A. M. et al. The effect of placentation type, litter size, lactation and gestation length on cancer risk in mammals. Proc. Biol. Sci. 290, 20230940 (2023).

pubmed: 37357861

Hedges, S. B., Dudley, J. & Kumar, S. TimeTree: A public knowledge-base of divergence times among organisms. Bioinformatics 22, 2971–2972 (2006).

pubmed: 17021158 doi: 10.1093/bioinformatics/btl505

Kumar, S. et al. TimeTree 5: An expanded resource for species divergence times. Mol. Biol. Evol. 39, msac174 (2022).

pubmed: 35932227 pmcid: 9400175 doi: 10.1093/molbev/msac174

Keeling, P. J. & Burki, F. Progress towards the tree of eukaryotes. Curr. Biol. 29, R808–R817 (2019).

pubmed: 31430481 doi: 10.1016/j.cub.2019.07.031

Burki, F., Roger, A. J., Brown, M. W. & Simpson, A. G. B. The new tree of eukaryotes. Trends Ecol. Evol. 35, 43–55 (2020).

pubmed: 31606140 doi: 10.1016/j.tree.2019.08.008

Adl, S. M. et al. Revisions to the classification, nomenclature, and diversity of eukaryotes. J. Eukaryot. Microbiol. 66, 4–119 (2019).

pubmed: 30257078 pmcid: 6492006 doi: 10.1111/jeu.12691

Schoch, C. L. et al. NCBI taxonomy: A comprehensive update on curation, resources and tools. Database (Oxford) 2020 (2020).

O’Flanagan, C. H., Smith, L. A., McDonell, S. B. & Hursting, S. D. When less may be more: Calorie restriction and response to cancer therapy. BMC Med. 15, 106 (2017).

pubmed: 28539118 pmcid: 5442682 doi: 10.1186/s12916-017-0873-x

Vidoni, C. et al. Calorie restriction for cancer prevention and therapy: Mechanisms, expectations, and efficacy. J. Cancer Prev. 26, 224–236 (2021).

pubmed: 35047448 pmcid: 8749320 doi: 10.15430/JCP.2021.26.4.224

Wang, X. et al. Cell-in-cell phenomenon and its relationship with tumor microenvironment and tumor progression: A review. Front. Cell Dev. Biol. 7, 311 (2019).

pubmed: 31850347 pmcid: 6901391 doi: 10.3389/fcell.2019.00311

Hu, J. L. et al. CAFs secreted exosomes promote metastasis and chemotherapy resistance by enhancing cell stemness and epithelial-mesenchymal transition in colorectal cancer. Mol. Cancer 18, 91 (2019).

pubmed: 31064356 pmcid: 6503554 doi: 10.1186/s12943-019-1019-x

Tian, T. et al. Exosome uptake through clathrin-mediated endocytosis and macropinocytosis and mediating miR-21 delivery. J. Biol. Chem. 289, 22258–22267 (2014).

pubmed: 24951588 pmcid: 4139237 doi: 10.1074/jbc.M114.588046

Feng, D. et al. Cellular internalization of exosomes occurs through phagocytosis. Traffic 11, 675–687 (2010).

pubmed: 20136776 doi: 10.1111/j.1600-0854.2010.01041.x

Conner, C. M. To the Edge of Apoptotic Cell Death and Back (University of California, 2021).

Schutt, B. Cannibalism: A Perfectly Natural History (Algonquin Books, 2018).

Greenhalgh, T. & Peacock, R. Effectiveness and efficiency of search methods in systematic reviews of complex evidence: Audit of primary sources. BMJ 331, 1064–1065 (2005).

pubmed: 16230312 pmcid: 1283190 doi: 10.1136/bmj.38636.593461.68

Knoll, A. H. The multiple origins of complex multicellularity. Annu. Rev. Earth Planet. Sci. 39, 217–239 (2011).

doi: 10.1146/annurev.earth.031208.100209

Cisneros, L. et al. Ancient genes establish stress-induced mutation as a hallmark of cancer. PLoS One 12, e0176258 (2017).

pubmed: 28441401 pmcid: 5404761 doi: 10.1371/journal.pone.0176258

Ertesvåg, H. Alginate-modifying enzymes: Biological roles and biotechnological uses. Front. Microbiol. 6, 523 (2015).

pubmed: 26074905 pmcid: 4444821

Gabbert, A. D. et al. The missing pieces: The role of secretion systems in Campylobacter jejuni virulence. Biomolecules 13 (2023).

Salmond, G. P. C. & Reeves, P. J. Membrance traffic wardens and protein secretion in Gram-negative bacteria. Trends Biochem. Sci. 18, 7–12 (1993).

pubmed: 8438237 doi: 10.1016/0968-0004(93)90080-7