CDKN2A/p16 Loss Implicates CDK4 as a Therapeutic Target in Imatinib-Resistant Dermatofibrosarcoma Protuberans

Mol Cancer Ther. 2015 Jun;14(6):1346-53. doi: 10.1158/1535-7163.MCT-14-0793. Epub 2015 Apr 7.

Abstract

Dermatofibrosarcoma protuberans (DFSP) is an aggressive PDGFB-dependent cutaneous sarcoma characterized by infiltrative growth and frequent local recurrences. Some DFSP progress to a higher-grade fibrosarcomatous form, with rapid growth and increased risk of metastasis. Imatinib provides clinical benefit in approximately 50% of patients with unresectable or metastatic DFSP. However, efficacious medical therapies have not been developed for imatinib-resistant DFSP. We established a model of imatinib-resistant DFSP and evaluated CDK4/6 inhibition as a genomically credentialed targeted therapy. DFSP105, an imatinib-resistant human cell line, was established from a fibrosarcomatous DFSP (FS-DFSP), and was studied by SNP arrays and sequencing to identify targetable genomic alterations. Findings were validated in vitro and in vivo, and confirmed in a series including 12 DFSP and 6 FS-DFSP. SNP analysis of DFSP105 revealed a homozygous deletion encompassing CDKN2A and CDKN2B. The resultant p16 loss implicated CDK4/6 as a potential therapeutic target in DFSP. We further demonstrated CDKN2A homozygous deletion in 1 of 12 conventional DFSP and 2 of 6 FS-DFSP, whereas p16 expression was lost in 4 of 18 DFSP. In vitro treatment of DFSP105 with two structurally distinct selective CDK4/6 inhibitors, PD-0332991 and LEE011, led to inhibition of RB1 phosphorylation and inhibition of proliferation (GI50 160 nmol/L and 276 nmol/L, respectively). In vivo treatment of DFSP105 with PD-0332991 (150 mg/kg) inhibited xenograft growth in mice, in comparison with imatinib-treated or -untreated tumors. In conclusion, CDKN2A deletion can contribute to DFSP progression. CDK4/6 inhibition is a preclinically effective treatment against p16-negative, imatinib-resistant FS-DFSP, and should be evaluated as a therapeutic strategy in patients with unresectable or metastatic imatinib-resistant DFSP.

Publication types

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

MeSH terms

  • Adult
  • Aged
  • Aminopyridines / pharmacology
  • Animals
  • Blotting, Western
  • Cell Line, Tumor
  • Collagen Type I / genetics
  • Collagen Type I, alpha 1 Chain
  • Cyclin-Dependent Kinase 4 / antagonists & inhibitors
  • Cyclin-Dependent Kinase 4 / genetics*
  • Cyclin-Dependent Kinase 4 / metabolism
  • Cyclin-Dependent Kinase Inhibitor p16 / genetics*
  • Cyclin-Dependent Kinase Inhibitor p16 / metabolism
  • Dermatofibrosarcoma / drug therapy
  • Dermatofibrosarcoma / genetics*
  • Dermatofibrosarcoma / pathology
  • Drug Resistance, Neoplasm / drug effects
  • Drug Resistance, Neoplasm / genetics*
  • Gene Deletion
  • Gene Fusion
  • Humans
  • Imatinib Mesylate / pharmacology*
  • Mice
  • Middle Aged
  • Phosphorylation / genetics
  • Piperazines / pharmacology
  • Polymorphism, Single Nucleotide
  • Proto-Oncogene Proteins c-sis / genetics
  • Purines / pharmacology
  • Pyridines / pharmacology
  • RNA Interference
  • Retinoblastoma Protein / metabolism
  • Xenograft Model Antitumor Assays
  • Young Adult

Substances

  • Aminopyridines
  • Collagen Type I
  • Collagen Type I, alpha 1 Chain
  • Cyclin-Dependent Kinase Inhibitor p16
  • Piperazines
  • Proto-Oncogene Proteins c-sis
  • Purines
  • Pyridines
  • Retinoblastoma Protein
  • Imatinib Mesylate
  • Cyclin-Dependent Kinase 4
  • palbociclib
  • ribociclib