Human coronary artery perivascular adipocytes overexpress genes responsible for regulating vascular morphology, inflammation, and hemostasis

Tapan K. Chatterjee, Bruce J. Aronow, Wilson S. Tong, David Manka, Yaoliang Tang, Vladimir Y. Bogdanov, Dusten Unruh, Andra L. Blomkalns, Mark G. Piegore, Daniel S. Weintraub, Steven M. Rudich, David G. Kuhel, David Y. Hui, Neal L. Weintraub

Research output: Contribution to journalArticle

59 Citations (Scopus)

Abstract

Inflammatory cross talk between perivascular adipose tissue and the blood vessel wall has been proposed to contribute to the pathogenesis of atherosclerosis. We previously reported that human perivascular (PV) adipocytes exhibit a proinflammatory phenotype and less adipogenic differentiation than do subcutaneous (SQ) adipocytes. To gain a global view of the genomic basis of biologic differences between PV and SQ adipocytes, we performed genome-wide expression analyses to identify differentially expressed genes between adipocytes derived from human SQ vs. PV adipose tissues. Although >90% of well-expressed genes were similarly regulated, we identified a signature of 307 differentially expressed genes that were highly enriched for functions associated with the regulation of angiogenesis, vascular morphology, inflammation, and blood clotting. Of the 156 PV upregulated genes, 59 associate with angiogenesis, vascular biology, or inflammation, noteworthy of which include TNFRSF11B (osteoprotegerin), PLAT, TGFB1, THBS2, HIF1A, GATA6, and SERPINE1. Of 166 PV downregulated genes, 21 associated with vascular biology and inflammation, including ANGPT1, ANGPTL1, and VEGFC. Consistent with the emergent hypothesis that PV adipocytes differentially regulate angiogenesis and inflammation, cell culture-derived adipocyteconditioned media from PV adipocytes strongly enhanced endothelial cell tubulogenesis and monocyte migration compared with media from SQ adipocytes. These findings demonstrate that PV adipocytes have the potential to significantly modulate vascular inflammatory crosstalk in the setting of atherosclerosis by their ability to signal to both endothelial and inflammatory cells.

Original languageEnglish (US)
Pages (from-to)697-709
Number of pages13
JournalPhysiological Genomics
Volume45
Issue number16
DOIs
StatePublished - Aug 15 2013

Fingerprint

Hemostasis
Adipocytes
Blood Vessels
Coronary Vessels
Inflammation
Genes
Adipose Tissue
Atherosclerosis
Endothelial Cells
Osteoprotegerin
Blood Coagulation
Monocytes
Down-Regulation
Cell Culture Techniques
Genome
Phenotype

Keywords

  • Angiogenesis
  • Atherosclerosis
  • Global gene expression pattern
  • Human perivascular fat
  • Inflammation

ASJC Scopus subject areas

  • Physiology
  • Genetics

Cite this

Human coronary artery perivascular adipocytes overexpress genes responsible for regulating vascular morphology, inflammation, and hemostasis. / Chatterjee, Tapan K.; Aronow, Bruce J.; Tong, Wilson S.; Manka, David; Tang, Yaoliang; Bogdanov, Vladimir Y.; Unruh, Dusten; Blomkalns, Andra L.; Piegore, Mark G.; Weintraub, Daniel S.; Rudich, Steven M.; Kuhel, David G.; Hui, David Y.; Weintraub, Neal L.

In: Physiological Genomics, Vol. 45, No. 16, 15.08.2013, p. 697-709.

Research output: Contribution to journalArticle

Chatterjee, TK, Aronow, BJ, Tong, WS, Manka, D, Tang, Y, Bogdanov, VY, Unruh, D, Blomkalns, AL, Piegore, MG, Weintraub, DS, Rudich, SM, Kuhel, DG, Hui, DY & Weintraub, NL 2013, 'Human coronary artery perivascular adipocytes overexpress genes responsible for regulating vascular morphology, inflammation, and hemostasis', Physiological Genomics, vol. 45, no. 16, pp. 697-709. https://doi.org/10.1152/physiolgenomics.00042.2013
Chatterjee, Tapan K. ; Aronow, Bruce J. ; Tong, Wilson S. ; Manka, David ; Tang, Yaoliang ; Bogdanov, Vladimir Y. ; Unruh, Dusten ; Blomkalns, Andra L. ; Piegore, Mark G. ; Weintraub, Daniel S. ; Rudich, Steven M. ; Kuhel, David G. ; Hui, David Y. ; Weintraub, Neal L. / Human coronary artery perivascular adipocytes overexpress genes responsible for regulating vascular morphology, inflammation, and hemostasis. In: Physiological Genomics. 2013 ; Vol. 45, No. 16. pp. 697-709.
@article{f2d57474141a4f40bf916fbfc81f6599,
title = "Human coronary artery perivascular adipocytes overexpress genes responsible for regulating vascular morphology, inflammation, and hemostasis",
abstract = "Inflammatory cross talk between perivascular adipose tissue and the blood vessel wall has been proposed to contribute to the pathogenesis of atherosclerosis. We previously reported that human perivascular (PV) adipocytes exhibit a proinflammatory phenotype and less adipogenic differentiation than do subcutaneous (SQ) adipocytes. To gain a global view of the genomic basis of biologic differences between PV and SQ adipocytes, we performed genome-wide expression analyses to identify differentially expressed genes between adipocytes derived from human SQ vs. PV adipose tissues. Although >90{\%} of well-expressed genes were similarly regulated, we identified a signature of 307 differentially expressed genes that were highly enriched for functions associated with the regulation of angiogenesis, vascular morphology, inflammation, and blood clotting. Of the 156 PV upregulated genes, 59 associate with angiogenesis, vascular biology, or inflammation, noteworthy of which include TNFRSF11B (osteoprotegerin), PLAT, TGFB1, THBS2, HIF1A, GATA6, and SERPINE1. Of 166 PV downregulated genes, 21 associated with vascular biology and inflammation, including ANGPT1, ANGPTL1, and VEGFC. Consistent with the emergent hypothesis that PV adipocytes differentially regulate angiogenesis and inflammation, cell culture-derived adipocyteconditioned media from PV adipocytes strongly enhanced endothelial cell tubulogenesis and monocyte migration compared with media from SQ adipocytes. These findings demonstrate that PV adipocytes have the potential to significantly modulate vascular inflammatory crosstalk in the setting of atherosclerosis by their ability to signal to both endothelial and inflammatory cells.",
keywords = "Angiogenesis, Atherosclerosis, Global gene expression pattern, Human perivascular fat, Inflammation",
author = "Chatterjee, {Tapan K.} and Aronow, {Bruce J.} and Tong, {Wilson S.} and David Manka and Yaoliang Tang and Bogdanov, {Vladimir Y.} and Dusten Unruh and Blomkalns, {Andra L.} and Piegore, {Mark G.} and Weintraub, {Daniel S.} and Rudich, {Steven M.} and Kuhel, {David G.} and Hui, {David Y.} and Weintraub, {Neal L.}",
year = "2013",
month = "8",
day = "15",
doi = "10.1152/physiolgenomics.00042.2013",
language = "English (US)",
volume = "45",
pages = "697--709",
journal = "Physiological Genomics",
issn = "1094-8341",
publisher = "American Physiological Society",
number = "16",

}

TY - JOUR

T1 - Human coronary artery perivascular adipocytes overexpress genes responsible for regulating vascular morphology, inflammation, and hemostasis

AU - Chatterjee, Tapan K.

AU - Aronow, Bruce J.

AU - Tong, Wilson S.

AU - Manka, David

AU - Tang, Yaoliang

AU - Bogdanov, Vladimir Y.

AU - Unruh, Dusten

AU - Blomkalns, Andra L.

AU - Piegore, Mark G.

AU - Weintraub, Daniel S.

AU - Rudich, Steven M.

AU - Kuhel, David G.

AU - Hui, David Y.

AU - Weintraub, Neal L.

PY - 2013/8/15

Y1 - 2013/8/15

N2 - Inflammatory cross talk between perivascular adipose tissue and the blood vessel wall has been proposed to contribute to the pathogenesis of atherosclerosis. We previously reported that human perivascular (PV) adipocytes exhibit a proinflammatory phenotype and less adipogenic differentiation than do subcutaneous (SQ) adipocytes. To gain a global view of the genomic basis of biologic differences between PV and SQ adipocytes, we performed genome-wide expression analyses to identify differentially expressed genes between adipocytes derived from human SQ vs. PV adipose tissues. Although >90% of well-expressed genes were similarly regulated, we identified a signature of 307 differentially expressed genes that were highly enriched for functions associated with the regulation of angiogenesis, vascular morphology, inflammation, and blood clotting. Of the 156 PV upregulated genes, 59 associate with angiogenesis, vascular biology, or inflammation, noteworthy of which include TNFRSF11B (osteoprotegerin), PLAT, TGFB1, THBS2, HIF1A, GATA6, and SERPINE1. Of 166 PV downregulated genes, 21 associated with vascular biology and inflammation, including ANGPT1, ANGPTL1, and VEGFC. Consistent with the emergent hypothesis that PV adipocytes differentially regulate angiogenesis and inflammation, cell culture-derived adipocyteconditioned media from PV adipocytes strongly enhanced endothelial cell tubulogenesis and monocyte migration compared with media from SQ adipocytes. These findings demonstrate that PV adipocytes have the potential to significantly modulate vascular inflammatory crosstalk in the setting of atherosclerosis by their ability to signal to both endothelial and inflammatory cells.

AB - Inflammatory cross talk between perivascular adipose tissue and the blood vessel wall has been proposed to contribute to the pathogenesis of atherosclerosis. We previously reported that human perivascular (PV) adipocytes exhibit a proinflammatory phenotype and less adipogenic differentiation than do subcutaneous (SQ) adipocytes. To gain a global view of the genomic basis of biologic differences between PV and SQ adipocytes, we performed genome-wide expression analyses to identify differentially expressed genes between adipocytes derived from human SQ vs. PV adipose tissues. Although >90% of well-expressed genes were similarly regulated, we identified a signature of 307 differentially expressed genes that were highly enriched for functions associated with the regulation of angiogenesis, vascular morphology, inflammation, and blood clotting. Of the 156 PV upregulated genes, 59 associate with angiogenesis, vascular biology, or inflammation, noteworthy of which include TNFRSF11B (osteoprotegerin), PLAT, TGFB1, THBS2, HIF1A, GATA6, and SERPINE1. Of 166 PV downregulated genes, 21 associated with vascular biology and inflammation, including ANGPT1, ANGPTL1, and VEGFC. Consistent with the emergent hypothesis that PV adipocytes differentially regulate angiogenesis and inflammation, cell culture-derived adipocyteconditioned media from PV adipocytes strongly enhanced endothelial cell tubulogenesis and monocyte migration compared with media from SQ adipocytes. These findings demonstrate that PV adipocytes have the potential to significantly modulate vascular inflammatory crosstalk in the setting of atherosclerosis by their ability to signal to both endothelial and inflammatory cells.

KW - Angiogenesis

KW - Atherosclerosis

KW - Global gene expression pattern

KW - Human perivascular fat

KW - Inflammation

UR - http://www.scopus.com/inward/record.url?scp=84882686511&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84882686511&partnerID=8YFLogxK

U2 - 10.1152/physiolgenomics.00042.2013

DO - 10.1152/physiolgenomics.00042.2013

M3 - Article

C2 - 23737535

AN - SCOPUS:84882686511

VL - 45

SP - 697

EP - 709

JO - Physiological Genomics

JF - Physiological Genomics

SN - 1094-8341

IS - 16

ER -