Multi-omics Analysis Reveals Adipose-tumor Crosstalk in Patients with Colorectal Cancer
Obesity and obesity-driven cancer rates are continuing to rise worldwide. We hypothesize that adipocyte-colonocyte interactions are a key driver of obesity-associated cancers. To understand the clinical relevance of visceral adipose tissue in advancing tumor growth, we analyzed paired tumor-adjacent...
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| Published in: | Cancer prevention research (Philadelphia, Pa.) Vol. 13; no. 10; pp. 817 - 828 |
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| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
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| Language: | English |
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01-10-2020
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| Abstract | Obesity and obesity-driven cancer rates are continuing to rise worldwide. We hypothesize that adipocyte-colonocyte interactions are a key driver of obesity-associated cancers. To understand the clinical relevance of visceral adipose tissue in advancing tumor growth, we analyzed paired tumor-adjacent visceral adipose, normal mucosa, and colorectal tumor tissues as well as presurgery blood samples from patients with sporadic colorectal cancer. We report that high peroxisome proliferator-activated receptor gamma (
) visceral adipose tissue expression is associated with glycoprotein VI (GPVI) signaling-the major signaling receptor for collagen-as well as fibrosis and adipogenesis pathway signaling in colorectal tumors. These associations were supported by correlations between
visceral adipose tissue expression and circulating levels of plasma 4-hydroxyproline and serum intercellular adhesion molecule 1 (ICAM1), as well as gene set enrichment analysis and joint gene-metabolite pathway results integration that yielded significant enrichment of genes defining epithelial-to-mesenchymal transition-as in fibrosis and metastasis-and genes involved in glycolytic metabolism, confirmed this association. We also reveal that elevated prostaglandin-endoperoxide synthase 2 (
) colorectal tumor expression is associated with a fibrotic signature in adipose-tumor crosstalk via GPVI signaling and dendritic cell maturation in visceral adipose tissue. Systemic metabolite and biomarker profiling confirmed that high
expression in colorectal tumors is significantly associated with higher concentrations of serum amyloid A and glycine, and lower concentrations of sphingomyelin, in patients with colorectal cancer. This multi-omics study suggests that adipose-tumor crosstalk in patients with colorectal cancer is a critical microenvironment interaction that could be therapeutically targeted.
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| AbstractList | Obesity and obesity-driven cancer rates are continuing to rise worldwide. We hypothesize that adipocyte-colonocyte interactions are a key driver of obesity-associated cancers. To understand the clinical relevance of visceral adipose tissue in advancing tumor growth, we analyzed paired tumor-adjacent visceral adipose, normal mucosa, and colorectal tumor tissues as well as presurgery blood samples from patients with sporadic colorectal cancer. We report that high peroxisome proliferator-activated receptor gamma (
) visceral adipose tissue expression is associated with glycoprotein VI (GPVI) signaling-the major signaling receptor for collagen-as well as fibrosis and adipogenesis pathway signaling in colorectal tumors. These associations were supported by correlations between
visceral adipose tissue expression and circulating levels of plasma 4-hydroxyproline and serum intercellular adhesion molecule 1 (ICAM1), as well as gene set enrichment analysis and joint gene-metabolite pathway results integration that yielded significant enrichment of genes defining epithelial-to-mesenchymal transition-as in fibrosis and metastasis-and genes involved in glycolytic metabolism, confirmed this association. We also reveal that elevated prostaglandin-endoperoxide synthase 2 (
) colorectal tumor expression is associated with a fibrotic signature in adipose-tumor crosstalk via GPVI signaling and dendritic cell maturation in visceral adipose tissue. Systemic metabolite and biomarker profiling confirmed that high
expression in colorectal tumors is significantly associated with higher concentrations of serum amyloid A and glycine, and lower concentrations of sphingomyelin, in patients with colorectal cancer. This multi-omics study suggests that adipose-tumor crosstalk in patients with colorectal cancer is a critical microenvironment interaction that could be therapeutically targeted.
. Abstract Obesity and obesity-driven cancer rates are continuing to rise worldwide. We hypothesize that adipocyte–colonocyte interactions are a key driver of obesity-associated cancers. To understand the clinical relevance of visceral adipose tissue in advancing tumor growth, we analyzed paired tumor-adjacent visceral adipose, normal mucosa, and colorectal tumor tissues as well as presurgery blood samples from patients with sporadic colorectal cancer. We report that high peroxisome proliferator-activated receptor gamma (PPARG) visceral adipose tissue expression is associated with glycoprotein VI (GPVI) signaling—the major signaling receptor for collagen—as well as fibrosis and adipogenesis pathway signaling in colorectal tumors. These associations were supported by correlations between PPARG visceral adipose tissue expression and circulating levels of plasma 4-hydroxyproline and serum intercellular adhesion molecule 1 (ICAM1), as well as gene set enrichment analysis and joint gene-metabolite pathway results integration that yielded significant enrichment of genes defining epithelial-to-mesenchymal transition—as in fibrosis and metastasis—and genes involved in glycolytic metabolism, confirmed this association. We also reveal that elevated prostaglandin-endoperoxide synthase 2 (PTGS2) colorectal tumor expression is associated with a fibrotic signature in adipose–tumor crosstalk via GPVI signaling and dendritic cell maturation in visceral adipose tissue. Systemic metabolite and biomarker profiling confirmed that high PTGS2 expression in colorectal tumors is significantly associated with higher concentrations of serum amyloid A and glycine, and lower concentrations of sphingomyelin, in patients with colorectal cancer. This multi-omics study suggests that adipose–tumor crosstalk in patients with colorectal cancer is a critical microenvironment interaction that could be therapeutically targeted. See related spotlight by Colacino et al., p. 803 Obesity and obesity-driven cancer rates are continuing to rise worldwide. We hypothesize that adipocyte-colonocyte interactions are a key driver of obesity-associated cancers. To understand the clinical relevance of visceral adipose tissue in advancing tumor growth, we analyzed paired tumor-adjacent visceral adipose, normal mucosa, and colorectal tumor tissues as well as presurgery blood samples from patients with sporadic colorectal cancer. We report that high peroxisome proliferator-activated receptor gamma (PPARG) visceral adipose tissue expression is associated with glycoprotein VI (GPVI) signaling-the major signaling receptor for collagen-as well as fibrosis and adipogenesis pathway signaling in colorectal tumors. These associations were supported by correlations between PPARG visceral adipose tissue expression and circulating levels of plasma 4-hydroxyproline and serum intercellular adhesion molecule 1 (ICAM1), as well as gene set enrichment analysis and joint gene-metabolite pathway results integration that yielded significant enrichment of genes defining epithelial-to-mesenchymal transition-as in fibrosis and metastasis-and genes involved in glycolytic metabolism, confirmed this association. We also reveal that elevated prostaglandin-endoperoxide synthase 2 (PTGS2) colorectal tumor expression is associated with a fibrotic signature in adipose-tumor crosstalk via GPVI signaling and dendritic cell maturation in visceral adipose tissue. Systemic metabolite and biomarker profiling confirmed that high PTGS2 expression in colorectal tumors is significantly associated with higher concentrations of serum amyloid A and glycine, and lower concentrations of sphingomyelin, in patients with colorectal cancer. This multi-omics study suggests that adipose-tumor crosstalk in patients with colorectal cancer is a critical microenvironment interaction that could be therapeutically targeted.See related spotlight by Colacino et al., p. 803.Obesity and obesity-driven cancer rates are continuing to rise worldwide. We hypothesize that adipocyte-colonocyte interactions are a key driver of obesity-associated cancers. To understand the clinical relevance of visceral adipose tissue in advancing tumor growth, we analyzed paired tumor-adjacent visceral adipose, normal mucosa, and colorectal tumor tissues as well as presurgery blood samples from patients with sporadic colorectal cancer. We report that high peroxisome proliferator-activated receptor gamma (PPARG) visceral adipose tissue expression is associated with glycoprotein VI (GPVI) signaling-the major signaling receptor for collagen-as well as fibrosis and adipogenesis pathway signaling in colorectal tumors. These associations were supported by correlations between PPARG visceral adipose tissue expression and circulating levels of plasma 4-hydroxyproline and serum intercellular adhesion molecule 1 (ICAM1), as well as gene set enrichment analysis and joint gene-metabolite pathway results integration that yielded significant enrichment of genes defining epithelial-to-mesenchymal transition-as in fibrosis and metastasis-and genes involved in glycolytic metabolism, confirmed this association. We also reveal that elevated prostaglandin-endoperoxide synthase 2 (PTGS2) colorectal tumor expression is associated with a fibrotic signature in adipose-tumor crosstalk via GPVI signaling and dendritic cell maturation in visceral adipose tissue. Systemic metabolite and biomarker profiling confirmed that high PTGS2 expression in colorectal tumors is significantly associated with higher concentrations of serum amyloid A and glycine, and lower concentrations of sphingomyelin, in patients with colorectal cancer. This multi-omics study suggests that adipose-tumor crosstalk in patients with colorectal cancer is a critical microenvironment interaction that could be therapeutically targeted.See related spotlight by Colacino et al., p. 803. |
| Author | Schrotz-King, Petra Holowatyj, Andreana N Hursting, Stephen D Bowers, Laura W Achaintre, David Keski-Rahkonen, Pekka Haffa, Mariam Scherer, Dominique Habermann, Nina Abbenhardt-Martin, Clare Simon, Thomas Viskochil, Richard Warby, Christy A Weijenberg, Matty P Himbert, Caroline Ulrich, Alexis Boehm, Juergen Boucher, Kenneth M Schneider, Martin Lin, Tengda Nattenmüller, Johanna Gicquiau, Audrey Kauczor, Hans-Ulrich von Knebel-Doeberitz, Magnus Kok, Dieuwertje E Ueland, Per M Scalbert, Augustin Gsur, Andrea Ulrich, Cornelia M Herpel, Esther Kloor, Matthias Schirmacher, Peter Gigic, Biljana Ose, Jennifer |
| Author_xml | – sequence: 1 givenname: Andreana N orcidid: 0000-0001-8001-8793 surname: Holowatyj fullname: Holowatyj, Andreana N email: andreana.holowatyj@vumc.org, neli.ulrich@hci.utah.edu organization: Vanderbilt-Ingram Cancer Center, Nashville, Tennessee – sequence: 2 givenname: Mariam orcidid: 0000-0003-0156-7749 surname: Haffa fullname: Haffa, Mariam organization: National Center for Tumor Diseases (NCT), Heidelberg, Germany – sequence: 3 givenname: Tengda surname: Lin fullname: Lin, Tengda organization: University of Utah, Salt Lake City, Utah – sequence: 4 givenname: Dominique orcidid: 0000-0003-4430-296X surname: Scherer fullname: Scherer, Dominique organization: University of Heidelberg, Heidelberg, Germany – sequence: 5 givenname: Biljana orcidid: 0000-0002-8085-2072 surname: Gigic fullname: Gigic, Biljana organization: University of Heidelberg, Heidelberg, Germany – sequence: 6 givenname: Jennifer orcidid: 0000-0002-2030-9676 surname: Ose fullname: Ose, Jennifer organization: University of Utah, Salt Lake City, Utah – sequence: 7 givenname: Christy A surname: Warby fullname: Warby, Christy A organization: University of Utah, Salt Lake City, Utah – sequence: 8 givenname: Caroline orcidid: 0000-0003-4084-8340 surname: Himbert fullname: Himbert, Caroline organization: University of Utah, Salt Lake City, Utah – sequence: 9 givenname: Clare surname: Abbenhardt-Martin fullname: Abbenhardt-Martin, Clare organization: National Center for Tumor Diseases (NCT), Heidelberg, Germany – sequence: 10 givenname: David surname: Achaintre fullname: Achaintre, David organization: International Agency for Research on Cancer (IARC), Lyon, France – sequence: 11 givenname: Juergen surname: Boehm fullname: Boehm, Juergen organization: University of Utah, Salt Lake City, Utah – sequence: 12 givenname: Kenneth M orcidid: 0000-0003-2833-0127 surname: Boucher fullname: Boucher, Kenneth M organization: Huntsman Cancer Institute, Salt Lake City, Utah – sequence: 13 givenname: Audrey surname: Gicquiau fullname: Gicquiau, Audrey organization: International Agency for Research on Cancer (IARC), Lyon, France – sequence: 14 givenname: Andrea orcidid: 0000-0002-9795-1528 surname: Gsur fullname: Gsur, Andrea organization: Institute of Cancer Research, Medical University of Vienna, Vienna, Austria – sequence: 15 givenname: Nina surname: Habermann fullname: Habermann, Nina organization: European Molecular Biology Laboratory (EMBL), Heidelberg, Germany – sequence: 16 givenname: Esther surname: Herpel fullname: Herpel, Esther organization: University Hospital, Heidelberg, Germany – sequence: 17 givenname: Hans-Ulrich surname: Kauczor fullname: Kauczor, Hans-Ulrich organization: University of Heidelberg, Heidelberg, Germany – sequence: 18 givenname: Pekka surname: Keski-Rahkonen fullname: Keski-Rahkonen, Pekka organization: International Agency for Research on Cancer (IARC), Lyon, France – sequence: 19 givenname: Matthias surname: Kloor fullname: Kloor, Matthias organization: European Molecular Biology Laboratory (EMBL), Heidelberg, Germany – sequence: 20 givenname: Magnus orcidid: 0000-0002-0498-6781 surname: von Knebel-Doeberitz fullname: von Knebel-Doeberitz, Magnus organization: European Molecular Biology Laboratory (EMBL), Heidelberg, Germany – sequence: 21 givenname: Dieuwertje E orcidid: 0000-0001-7154-8207 surname: Kok fullname: Kok, Dieuwertje E organization: Wageningen University and Research, Wageningen, The Netherlands – sequence: 22 givenname: Johanna orcidid: 0000-0003-4032-378X surname: Nattenmüller fullname: Nattenmüller, Johanna organization: University of Heidelberg, Heidelberg, Germany – sequence: 23 givenname: Peter orcidid: 0000-0003-4339-3492 surname: Schirmacher fullname: Schirmacher, Peter organization: European Molecular Biology Laboratory (EMBL), Heidelberg, Germany – sequence: 24 givenname: Martin surname: Schneider fullname: Schneider, Martin organization: University of Heidelberg, Heidelberg, Germany – sequence: 25 givenname: Petra surname: Schrotz-King fullname: Schrotz-King, Petra organization: National Center for Tumor Diseases (NCT), Heidelberg, Germany – sequence: 26 givenname: Thomas surname: Simon fullname: Simon, Thomas organization: GRN-Clinic, Weinheim, Germany – sequence: 27 givenname: Per M orcidid: 0000-0002-1903-0571 surname: Ueland fullname: Ueland, Per M organization: Maastricht University, Maastricht, the Netherlands – sequence: 28 givenname: Richard surname: Viskochil fullname: Viskochil, Richard organization: University of Utah, Salt Lake City, Utah – sequence: 29 givenname: Matty P orcidid: 0000-0003-1695-4768 surname: Weijenberg fullname: Weijenberg, Matty P organization: BEVITAL, Bergen, Norway – sequence: 30 givenname: Augustin orcidid: 0000-0001-6651-6710 surname: Scalbert fullname: Scalbert, Augustin organization: International Agency for Research on Cancer (IARC), Lyon, France – sequence: 31 givenname: Alexis orcidid: 0000-0003-1469-2186 surname: Ulrich fullname: Ulrich, Alexis organization: University of Heidelberg, Heidelberg, Germany – sequence: 32 givenname: Laura W surname: Bowers fullname: Bowers, Laura W organization: Lineberger Comprehensive Cancer Center, Chapel Hill, North Carolina – sequence: 33 givenname: Stephen D surname: Hursting fullname: Hursting, Stephen D organization: Lineberger Comprehensive Cancer Center, Chapel Hill, North Carolina – sequence: 34 givenname: Cornelia M orcidid: 0000-0003-1469-2186 surname: Ulrich fullname: Ulrich, Cornelia M email: andreana.holowatyj@vumc.org, neli.ulrich@hci.utah.edu organization: University of Utah, Salt Lake City, Utah |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32655010$$D View this record in MEDLINE/PubMed |
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| Snippet | Obesity and obesity-driven cancer rates are continuing to rise worldwide. We hypothesize that adipocyte-colonocyte interactions are a key driver of... Abstract Obesity and obesity-driven cancer rates are continuing to rise worldwide. We hypothesize that adipocyte–colonocyte interactions are a key driver of... |
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| SubjectTerms | Adipose Tissue Carcinogenesis Colorectal Neoplasms Humans Intra-Abdominal Fat Obesity Tumor Microenvironment |
| Title | Multi-omics Analysis Reveals Adipose-tumor Crosstalk in Patients with Colorectal Cancer |
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