Chromatin remodeling underlies the senescence-associated secretory phenotype of tumor stromal fibroblasts that supports cancer progression

Cancer Res. 2012 May 1;72(9):2251-61. doi: 10.1158/0008-5472.CAN-11-3386. Epub 2012 Mar 15.

Abstract

Age is a major risk factor for the development of cancer. Senescent fibroblasts, which accumulate with age, secrete protumorigenic factors collectively referred to as the senescence-associated secretory phenotype (SASP). Here, we examined the molecular mechanisms that control SASP activation, focusing on the known SASP factor osteopontin (OPN). We found that expression of the canonical SASP members interleukin (IL)-6 and IL-8, but not OPN, were dependent upon a persistent DNA damage response (DDR) as evidenced by ATM and NF-κB activation. Treatment with several histone deacetylase (HDAC) inhibitors robustly activated SASP in the absence of DNA breaks, suggesting that DDR-dependent SASP activation occurs in response to chromatin remodeling rather than physical breaks in DNA. In the setting of HDAC inhibition, IL-6 and IL-8 expression remained dependent upon ATM and NF-κB, while OPN expression remained independent of these factors. Further analysis revealed that HDAC1 inhibition was sufficient to induce OPN expression, which is interesting given that loss of HDAC1 expression correlates with increased OPN expression within the stromal compartment of invasive breast cancers. Importantly, fibroblasts treated with HDAC inhibitors promoted tumor growth in vivo. Our findings therefore indicate that HDAC modulation plays an important role in stromal cell activation, with important implications for the use of HDAC inhibitors in the treatment of cancer.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Breast Neoplasms / genetics
  • Breast Neoplasms / metabolism*
  • Breast Neoplasms / pathology*
  • Cellular Senescence / physiology
  • Chromatin / metabolism*
  • DNA Damage
  • Disease Progression
  • Female
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Fibroblasts / pathology
  • Histone Deacetylase 1 / antagonists & inhibitors
  • Histone Deacetylase 1 / metabolism
  • Histone Deacetylase Inhibitors / pharmacology
  • Humans
  • Interleukin-6 / biosynthesis*
  • Interleukin-6 / genetics
  • Interleukin-8 / biosynthesis*
  • Interleukin-8 / genetics
  • Mice
  • Mice, Inbred NOD
  • Mice, SCID
  • Osteopontin / biosynthesis*
  • Osteopontin / genetics
  • Phenotype
  • RNA, Messenger / biosynthesis
  • RNA, Messenger / genetics
  • Stromal Cells / drug effects
  • Stromal Cells / metabolism
  • Stromal Cells / pathology

Substances

  • CXCL8 protein, human
  • Chromatin
  • Histone Deacetylase Inhibitors
  • IL6 protein, human
  • Interleukin-6
  • Interleukin-8
  • RNA, Messenger
  • Osteopontin
  • Histone Deacetylase 1