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Translational Sciences

Tissue-Specific RNA-Seq in Human Evoked Inflammation Identifies Blood and Adipose LincRNA Signatures of Cardiometabolic DiseasesSignificance

Yichuan Liu, Jane F. Ferguson, Chenyi Xue, Rachel L. Ballantyne, Ian M. Silverman, Sager J. Gosai, Jacquelyn Serfecz, Michael P. Morley, Brian D. Gregory, Mingyao Li, Muredach P. Reilly
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https://doi.org/10.1161/ATVBAHA.113.303123
Arteriosclerosis, Thrombosis, and Vascular Biology. 2014;34:902-912
Originally published March 19, 2014
Yichuan Liu
From the Departments of Biostatistics and Epidemiology and Biology, Cardiovascular Institute, Perelman School of Medicine and School of Arts and Science at the University of Pennsylvania, Philadelphia.
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Jane F. Ferguson
From the Departments of Biostatistics and Epidemiology and Biology, Cardiovascular Institute, Perelman School of Medicine and School of Arts and Science at the University of Pennsylvania, Philadelphia.
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Chenyi Xue
From the Departments of Biostatistics and Epidemiology and Biology, Cardiovascular Institute, Perelman School of Medicine and School of Arts and Science at the University of Pennsylvania, Philadelphia.
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Rachel L. Ballantyne
From the Departments of Biostatistics and Epidemiology and Biology, Cardiovascular Institute, Perelman School of Medicine and School of Arts and Science at the University of Pennsylvania, Philadelphia.
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Ian M. Silverman
From the Departments of Biostatistics and Epidemiology and Biology, Cardiovascular Institute, Perelman School of Medicine and School of Arts and Science at the University of Pennsylvania, Philadelphia.
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Sager J. Gosai
From the Departments of Biostatistics and Epidemiology and Biology, Cardiovascular Institute, Perelman School of Medicine and School of Arts and Science at the University of Pennsylvania, Philadelphia.
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Jacquelyn Serfecz
From the Departments of Biostatistics and Epidemiology and Biology, Cardiovascular Institute, Perelman School of Medicine and School of Arts and Science at the University of Pennsylvania, Philadelphia.
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Michael P. Morley
From the Departments of Biostatistics and Epidemiology and Biology, Cardiovascular Institute, Perelman School of Medicine and School of Arts and Science at the University of Pennsylvania, Philadelphia.
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Brian D. Gregory
From the Departments of Biostatistics and Epidemiology and Biology, Cardiovascular Institute, Perelman School of Medicine and School of Arts and Science at the University of Pennsylvania, Philadelphia.
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Mingyao Li
From the Departments of Biostatistics and Epidemiology and Biology, Cardiovascular Institute, Perelman School of Medicine and School of Arts and Science at the University of Pennsylvania, Philadelphia.
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Muredach P. Reilly
From the Departments of Biostatistics and Epidemiology and Biology, Cardiovascular Institute, Perelman School of Medicine and School of Arts and Science at the University of Pennsylvania, Philadelphia.
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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.

  • genomics
  • lincRNA
  • RNA sequence
  • Received September 16, 2013.
  • Accepted January 23, 2014.
  • © 2014 American Heart Association, Inc.

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    Tissue-Specific RNA-Seq in Human Evoked Inflammation Identifies Blood and Adipose LincRNA Signatures of Cardiometabolic DiseasesSignificance
    Yichuan Liu, Jane F. Ferguson, Chenyi Xue, Rachel L. Ballantyne, Ian M. Silverman, Sager J. Gosai, Jacquelyn Serfecz, Michael P. Morley, Brian D. Gregory, Mingyao Li and Muredach P. Reilly
    Arteriosclerosis, Thrombosis, and Vascular Biology. 2014;34:902-912, originally published March 19, 2014
    https://doi.org/10.1161/ATVBAHA.113.303123

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    Tissue-Specific RNA-Seq in Human Evoked Inflammation Identifies Blood and Adipose LincRNA Signatures of Cardiometabolic DiseasesSignificance
    Yichuan Liu, Jane F. Ferguson, Chenyi Xue, Rachel L. Ballantyne, Ian M. Silverman, Sager J. Gosai, Jacquelyn Serfecz, Michael P. Morley, Brian D. Gregory, Mingyao Li and Muredach P. Reilly
    Arteriosclerosis, Thrombosis, and Vascular Biology. 2014;34:902-912, originally published March 19, 2014
    https://doi.org/10.1161/ATVBAHA.113.303123
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