High-resolution deconstruction of evolution induced by chemotherapy treatments in breast cancer xenografts

Sci Rep. 2018 Dec 18;8(1):17937. doi: 10.1038/s41598-018-36184-8.

Abstract

The processes by which tumors evolve are essential to the efficacy of treatment, but quantitative understanding of intratumoral dynamics has been limited. Although intratumoral heterogeneity is common, quantification of evolution is difficult from clinical samples because treatment replicates cannot be performed and because matched serial samples are infrequently available. To circumvent these problems we derived and assayed large sets of human triple-negative breast cancer xenografts and cell cultures from two patients, including 86 xenografts from cyclophosphamide, doxorubicin, cisplatin, docetaxel, or vehicle treatment cohorts as well as 45 related cell cultures. We assayed these samples via exome-seq and/or high-resolution droplet digital PCR, allowing us to distinguish complex therapy-induced selection and drift processes among endogenous cancer subclones with cellularity uncertainty <3%. For one patient, we discovered two predominant subclones that were granularly intermixed in all 48 co-derived xenograft samples. These two subclones exhibited differential chemotherapy sensitivity-when xenografts were treated with cisplatin for 3 weeks, the post-treatment volume change was proportional to the post-treatment ratio of subclones on a xenograft-to-xenograft basis. A subsequent cohort in which xenografts were treated with cisplatin, allowed a drug holiday, then treated a second time continued to exhibit this proportionality. In contrast, xenografts from other treatment cohorts, spatially dissected xenograft fragments, and cell cultures evolved in diverse ways but with substantial population bottlenecks. These results show that ecosystems susceptible to successive retreatment can arise spontaneously in breast cancer in spite of a background of irregular subclonal bottlenecks, and our work provides to our knowledge the first quantification of the population genetics of such a system. Intriguingly, in such an ecosystem the ratio of common subclones is predictive of the state of treatment susceptibility, showing how measurements of subclonal heterogeneity could guide treatment for some patients.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Alleles
  • Animals
  • Antineoplastic Agents / pharmacology*
  • Antineoplastic Agents / therapeutic use
  • Biomarkers, Tumor
  • Breast Neoplasms / drug therapy*
  • Breast Neoplasms / genetics
  • Breast Neoplasms / pathology
  • Cell Line, Tumor
  • Clonal Evolution / drug effects
  • Clonal Evolution / genetics
  • DNA Copy Number Variations / drug effects
  • Disease Models, Animal
  • Female
  • Gene Frequency
  • Humans
  • Mice
  • Mutation
  • Triple Negative Breast Neoplasms / drug therapy
  • Triple Negative Breast Neoplasms / genetics
  • Triple Negative Breast Neoplasms / pathology
  • Xenograft Model Antitumor Assays

Substances

  • Antineoplastic Agents
  • Biomarkers, Tumor