Tissue-specific RNA-Seq in human evoked inflammation identifies blood and adipose LincRNA signatures of cardiometabolic diseases

Arterioscler Thromb Vasc Biol. 2014 Apr;34(4):902-12. doi: 10.1161/ATVBAHA.113.303123. Epub 2014 Feb 6.

Abstract

Objective: Inappropriate transcriptional activation of innate immunity is a pathological feature of several cardiometabolic disorders, but little is known about inflammatory modulation of long intergenic noncoding RNAs (lincRNAs) in disease-relevant human tissues.

Approach and results: We applied deep RNA sequencing (>500 million filtered reads per sample) to blood and adipose during low-dose experimental endotoxemia (lipopolysaccharide) in a healthy human, with targeted replication in separate individuals undergoing endotoxemia (n=6), to identify inflammatory lincRNAs. A subset of these lincRNAs was examined for expression in adipocytes and monocytes, modulation in adipose of obese humans, and overlap with genome-wide association study signals for inflammatory and cardiometabolic traits. Of a stringent set of 4284 lincRNAs, ≈11% to 22% were expressed with 201 and 56 lincRNAs modulated by lipopolysaccharide in blood or adipose, respectively. Tissue-specific expression of a subset of 6 lipopolysaccharide-lincRNAs was replicated with lipopolysaccharide modulation confirmed for all 3 expressed in blood and 2 of 4 expressed in adipose. The broader generalizability of findings in blood of subject A was confirmed by RNA sequencing in 7 additional subjects. We confirmed adipocytes and monocytes as potential cell-sources of selective lipopolysaccharide-regulated lincRNAs, and 2 of these, linc-DMRT2 (P=0.002) and linc-TP53I13 (P=0.01), were suppressed in adipose of obese humans. Finally, we provide examples of lipopolysaccharide-modulated lincRNAs that overlap single nucleotide polymorphisms that are associated with cardiometabolic traits.

Conclusions: Our findings provide novel insights into tissue-level, inflammatory transcriptome regulation in cardiometabolic diseases. These are complementary to more usual approaches limited to interrogation of DNA variations.

Trial registration: ClinicalTrials.gov NCT00953667.

Keywords: RNA sequence; genomics; lincRNA.

Publication types

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

MeSH terms

  • Adipocytes / metabolism
  • Adult
  • Binding Sites
  • Case-Control Studies
  • Cells, Cultured
  • Endotoxemia / blood
  • Endotoxemia / genetics*
  • Female
  • Gene Expression Profiling / methods*
  • Gene Expression Regulation
  • Genetic Markers
  • Genome-Wide Association Study
  • High-Throughput Nucleotide Sequencing*
  • Humans
  • Inflammation / blood
  • Inflammation / genetics*
  • Inflammation Mediators / blood
  • Lipopolysaccharides / pharmacology
  • Male
  • Metabolic Syndrome / blood
  • Metabolic Syndrome / genetics*
  • Monocytes / metabolism
  • Obesity / blood
  • Obesity / genetics
  • RNA, Long Noncoding / blood*
  • Reproducibility of Results
  • Sequence Analysis, RNA / methods*
  • Subcutaneous Fat / drug effects
  • Subcutaneous Fat / metabolism*
  • Transcription Factors / metabolism
  • Young Adult

Substances

  • Genetic Markers
  • Inflammation Mediators
  • Lipopolysaccharides
  • RNA, Long Noncoding
  • Transcription Factors

Associated data

  • ClinicalTrials.gov/NCT00953667