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Non-cell-autonomous mechanisms of tumor initiation and relapse by chromosomal instability

Created on 03 Nov 2025

Authors

Lafirenze, S. J. A., Kops, G. J., van Gerwen, B., Quirindongo, A. I., Janssen, A., Etemad, B., Toonen, P., Hoevenaar, W. H. M., Costermans, N., Youssef, S., de Bruin, A., Brosens, L. A. A., Jelluma, N.

Abstract

Chromosomal instability (CIN) is a hallmark of cancer, and a primary cause of genetic heterogeneity in tumors. Depending on the degree of CIN and the affected tissue, CIN can promote or suppress tumor formation, and high CIN induction has been proposed as a therapeutic strategy. How CIN achieves these effects is unclear. Here we use a conditional mouse model of graded CIN in combination with longitudinal monitoring of DMBA/TPA-initiated skin tumors to show that low CIN increases the frequency of skin tumor initiation, while higher CIN accelerates onset and growth rates. Strikingly, gene recombination analysis of the tumors reveals that upon high CIN induction the fast-growing tumors originate from rare low CIN cells, suggesting a strong non-cellautonomous effect of high CIN. Gene expression analysis and immunohistochemistry show that high CIN causes epidermal hyperplasia, immune evasion and a regenerative response that stimulates low CIN tumor growth beyond what is achieved by induction of low CIN alone. Such cell-extrinsic effects may be a common mechanism of tumor formation by CIN, as we observe it also in CIN-induced tumors of the intestine, breast and mesentery. When high CIN is induced in established skin tumors, mimicking CINbased therapy, tumors regress but relapse quickly. Relapsed tumors, too, arose from rare low CIN cells. Our findings have implications for our understanding of the contributions of CIN to cancer initiation and progression and give caution to the rationale for CIN therapies.

Preprint server: bioRxiv
The authors list and abstract were imported from bioRxiv on 03 Nov 2025.

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