Distinct populations of inflammatory fibroblasts and myofibroblasts in pancreatic cancer

Pancreatic stellate cells (PSCs) differentiate into cancer-associated fibroblasts (CAFs) that produce desmoplastic stroma, thereby modulating disease progression and therapeutic response in pancreatic ductal adenocarcinoma (PDA). However, it is unknown whether CAFs uniformly carry out these tasks or...

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Published in	The Journal of experimental medicine Vol. 214; no. 3; pp. 579 - 596
Main Authors	Öhlund, Daniel, Handly-Santana, Abram, Biffi, Giulia, Elyada, Ela, Almeida, Ana S., Ponz-Sarvise, Mariano, Corbo, Vincenzo, Oni, Tobiloba E., Hearn, Stephen A., Lee, Eun Jung, Chio, Iok In Christine, Hwang, Chang-Il, Tiriac, Hervé, Baker, Lindsey A., Engle, Dannielle D., Feig, Christine, Kultti, Anne, Egeblad, Mikala, Fearon, Douglas T., Crawford, James M., Clevers, Hans, Park, Youngkyu, Tuveson, David A.
Format	Journal Article
Language	English
Published	United States Rockefeller University Press 06.03.2017 The Rockefeller University Press
Subjects	Actin Actins - analysis Adenocarcinoma Animals Biology Cancer Carcinoma, Pancreatic Ductal - immunology Carcinoma, Pancreatic Ductal - metabolism Carcinoma, Pancreatic Ductal - pathology Cell culture Cells, Cultured Crosstalk Cytokines - biosynthesis Etiology Fibroblasts Fibroblasts - physiology Heterogeneity Humans Inflammation Interleukin 6 Mice Mice, Inbred C57BL Muscles Myofibroblasts - physiology Organoids Pancreatic cancer Pancreatic Neoplasms - immunology Pancreatic Neoplasms - metabolism Pancreatic Neoplasms - pathology Populations Rodents Smooth muscle STAT3 Transcription Factor - metabolism Stellate cells Stromal cells
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Abstract	Pancreatic stellate cells (PSCs) differentiate into cancer-associated fibroblasts (CAFs) that produce desmoplastic stroma, thereby modulating disease progression and therapeutic response in pancreatic ductal adenocarcinoma (PDA). However, it is unknown whether CAFs uniformly carry out these tasks or if subtypes of CAFs with distinct phenotypes in PDA exist. We identified a CAF subpopulation with elevated expression of α-smooth muscle actin (αSMA) located immediately adjacent to neoplastic cells in mouse and human PDA tissue. We recapitulated this finding in co-cultures of murine PSCs and PDA organoids, and demonstrated that organoid-activated CAFs produced desmoplastic stroma. The co-cultures showed cooperative interactions and revealed another distinct subpopulation of CAFs, located more distantly from neoplastic cells, which lacked elevated αSMA expression and instead secreted IL6 and additional inflammatory mediators. These findings were corroborated in mouse and human PDA tissue, providing direct evidence for CAF heterogeneity in PDA tumor biology with implications for disease etiology and therapeutic development.
AbstractList	Pancreatic stellate cells (PSCs) differentiate into cancer-associated fibroblasts (CAFs) that produce desmoplastic stroma, thereby modulating disease progression and therapeutic response in pancreatic ductal adenocarcinoma (PDA). However, it is unknown whether CAFs uniformly carry out these tasks or if subtypes of CAFs with distinct phenotypes in PDA exist. We identified a CAF subpopulation with elevated expression of α-smooth muscle actin (αSMA) located immediately adjacent to neoplastic cells in mouse and human PDA tissue. We recapitulated this finding in co-cultures of murine PSCs and PDA organoids, and demonstrated that organoid-activated CAFs produced desmoplastic stroma. The co-cultures showed cooperative interactions and revealed another distinct subpopulation of CAFs, located more distantly from neoplastic cells, which lacked elevated αSMA expression and instead secreted IL6 and additional inflammatory mediators. These findings were corroborated in mouse and human PDA tissue, providing direct evidence for CAF heterogeneity in PDA tumor biology with implications for disease etiology and therapeutic development. Ohlund et al. develop a three-dimensional co-culture platform of neoplastic pancreatic ductal organoids and pancreatic stellate cells (PSCs) to characterize the dynamic crosstalk between cancer cells and stromal cells, and to address stromal heterogeneity. The co-cultures reveal the co-existence of two phenotypically distinct populations of PSCs, providing insights into PDA biology and prompting a reconsideration of interventional strategies.Pancreatic stellate cells (PSCs) differentiate into cancer-associated fibroblasts (CAFs) that produce desmoplastic stroma, thereby modulating disease progression and therapeutic response in pancreatic ductal adenocarcinoma (PDA). However, it is unknown whether CAFs uniformly carry out these tasks or if subtypes of CAFs with distinct phenotypes in PDA exist. We identified a CAF subpopulation with elevated expression of α-smooth muscle actin (αSMA) located immediately adjacent to neoplastic cells in mouse and human PDA tissue. We recapitulated this finding in co-cultures of murine PSCs and PDA organoids, and demonstrated that organoid-activated CAFs produced desmoplastic stroma. The co-cultures showed cooperative interactions and revealed another distinct subpopulation of CAFs, located more distantly from neoplastic cells, which lacked elevated αSMA expression and instead secreted IL6 and additional inflammatory mediators. These findings were corroborated in mouse and human PDA tissue, providing direct evidence for CAF heterogeneity in PDA tumor biology with implications for disease etiology and therapeutic development. Pancreatic stellate cells (PSCs) differentiate into cancer-associated fibroblasts (CAFs) that produce desmoplastic stroma, thereby modulating disease progression and therapeutic response in pancreatic ductal adenocarcinoma (PDA). However, it is unknown whether CAFs uniformly carry out these tasks or if subtypes of CAFs with distinct phenotypes in PDA exist. We identified a CAF subpopulation with elevated expression of a-smooth muscle actin (alpha SMA) located immediately adjacent to neoplastic cells in mouse and human PDA tissue. We recapitulated this finding in co-cultures of murine PSCs and PDA organoids, and demonstrated that organoid-activated CAFs produced desmoplastic stroma. The co-cultures showed cooperative interactions and revealed another distinct subpopulation of CAFs, located more distantly from neoplastic cells, which lacked elevated aSMA expression and instead secreted IL6 and additional inflammatory mediators. These findings were corroborated in mouse and human PDA tissue, providing direct evidence for CAF heterogeneity in PDA tumor biology with implications for disease etiology and therapeutic development. Ohlund et al. develop a three-dimensional co-culture platform of neoplastic pancreatic ductal organoids and pancreatic stellate cells (PSCs) to characterize the dynamic crosstalk between cancer cells and stromal cells, and to address stromal heterogeneity. The co-cultures reveal the co-existence of two phenotypically distinct populations of PSCs, providing insights into PDA biology and prompting a reconsideration of interventional strategies. Pancreatic stellate cells (PSCs) differentiate into cancer-associated fibroblasts (CAFs) that produce desmoplastic stroma, thereby modulating disease progression and therapeutic response in pancreatic ductal adenocarcinoma (PDA). However, it is unknown whether CAFs uniformly carry out these tasks or if subtypes of CAFs with distinct phenotypes in PDA exist. We identified a CAF subpopulation with elevated expression of alpha -smooth muscle actin ( alpha SMA) located immediately adjacent to neoplastic cells in mouse and human PDA tissue. We recapitulated this finding in co-cultures of murine PSCs and PDA organoids, and demonstrated that organoid-activated CAFs produced desmoplastic stroma. The co-cultures showed cooperative interactions and revealed another distinct subpopulation of CAFs, located more distantly from neoplastic cells, which lacked elevated alpha SMA expression and instead secreted IL6 and additional inflammatory mediators. These findings were corroborated in mouse and human PDA tissue, providing direct evidence for CAF heterogeneity in PDA tumor biology with implications for disease etiology and therapeutic development. Öhlund et al. develop a three-dimensional co-culture platform of neoplastic pancreatic ductal organoids and pancreatic stellate cells (PSCs) to characterize the dynamic crosstalk between cancer cells and stromal cells, and to address stromal heterogeneity. The co-cultures reveal the co-existence of two phenotypically distinct populations of PSCs, providing insights into PDA biology and prompting a reconsideration of interventional strategies. Pancreatic stellate cells (PSCs) differentiate into cancer-associated fibroblasts (CAFs) that produce desmoplastic stroma, thereby modulating disease progression and therapeutic response in pancreatic ductal adenocarcinoma (PDA). However, it is unknown whether CAFs uniformly carry out these tasks or if subtypes of CAFs with distinct phenotypes in PDA exist. We identified a CAF subpopulation with elevated expression of α-smooth muscle actin (αSMA) located immediately adjacent to neoplastic cells in mouse and human PDA tissue. We recapitulated this finding in co-cultures of murine PSCs and PDA organoids, and demonstrated that organoid-activated CAFs produced desmoplastic stroma. The co-cultures showed cooperative interactions and revealed another distinct subpopulation of CAFs, located more distantly from neoplastic cells, which lacked elevated αSMA expression and instead secreted IL6 and additional inflammatory mediators. These findings were corroborated in mouse and human PDA tissue, providing direct evidence for CAF heterogeneity in PDA tumor biology with implications for disease etiology and therapeutic development.
Author	Elyada, Ela Tiriac, Hervé Kultti, Anne Clevers, Hans Feig, Christine Crawford, James M. Handly-Santana, Abram Almeida, Ana S. Oni, Tobiloba E. Hwang, Chang-Il Lee, Eun Jung Engle, Dannielle D. Tuveson, David A. Öhlund, Daniel Fearon, Douglas T. Baker, Lindsey A. Park, Youngkyu Ponz-Sarvise, Mariano Egeblad, Mikala Hearn, Stephen A. Chio, Iok In Christine Biffi, Giulia Corbo, Vincenzo
AuthorAffiliation	7 Department of Diagnostic and Public Health, University and Hospital Trust of Verona, 37134 Verona, Italy 8 Graduate Program in Molecular and Cellular Biology, Stony Brook University, Stony Brook, NY 11794 5 Department of Oncology, Clinica Universidad de Navarra, CIMA, IDISNA, Pamplona 31008, Spain 6 ARC-Net centre for applied research on cancer, University and Hospital Trust of Verona, 37134 Verona, Italy 9 University of Cambridge, Cancer Research UK, Cambridge Institute, Cambridge, UK 1 Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724 10 Hofstra Northwell School of Medicine, Hempstead, NY 11550 3 Department of Surgical and Perioperative Sciences, Surgery, Umeå University, 901 85 Umeå, Sweden 2 Lustgarten Foundation Pancreatic Cancer Research Laboratory, Cold Spring Harbor, NY 11724 4 APC Microbiome Institute and School of Microbiology, University College Cork, Cork, Ireland 11 Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences (KNAW), University Medical Centre Utrec
AuthorAffiliation_xml	– name: 4 APC Microbiome Institute and School of Microbiology, University College Cork, Cork, Ireland – name: 2 Lustgarten Foundation Pancreatic Cancer Research Laboratory, Cold Spring Harbor, NY 11724 – name: 11 Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences (KNAW), University Medical Centre Utrecht and CancerGenomics.nl, 3584 CT Utrecht, Netherlands – name: 1 Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724 – name: 5 Department of Oncology, Clinica Universidad de Navarra, CIMA, IDISNA, Pamplona 31008, Spain – name: 9 University of Cambridge, Cancer Research UK, Cambridge Institute, Cambridge, UK – name: 3 Department of Surgical and Perioperative Sciences, Surgery, Umeå University, 901 85 Umeå, Sweden – name: 6 ARC-Net centre for applied research on cancer, University and Hospital Trust of Verona, 37134 Verona, Italy – name: 8 Graduate Program in Molecular and Cellular Biology, Stony Brook University, Stony Brook, NY 11794 – name: 7 Department of Diagnostic and Public Health, University and Hospital Trust of Verona, 37134 Verona, Italy – name: 10 Hofstra Northwell School of Medicine, Hempstead, NY 11550
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BackLink	https://www.ncbi.nlm.nih.gov/pubmed/28232471$$D View this record in MEDLINE/PubMed https://urn.kb.se/resolve?urn=urn:nbn:se:umu:diva-132073$$DView record from Swedish Publication Index
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Snippet	Pancreatic stellate cells (PSCs) differentiate into cancer-associated fibroblasts (CAFs) that produce desmoplastic stroma, thereby modulating disease... Ohlund et al. develop a three-dimensional co-culture platform of neoplastic pancreatic ductal organoids and pancreatic stellate cells (PSCs) to characterize... Öhlund et al. develop a three-dimensional co-culture platform of neoplastic pancreatic ductal organoids and pancreatic stellate cells (PSCs) to characterize...
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SubjectTerms	Actin Actins - analysis Adenocarcinoma Animals Biology Cancer Carcinoma, Pancreatic Ductal - immunology Carcinoma, Pancreatic Ductal - metabolism Carcinoma, Pancreatic Ductal - pathology Cell culture Cells, Cultured Crosstalk Cytokines - biosynthesis Etiology Fibroblasts Fibroblasts - physiology Heterogeneity Humans Inflammation Interleukin 6 Mice Mice, Inbred C57BL Muscles Myofibroblasts - physiology Organoids Pancreatic cancer Pancreatic Neoplasms - immunology Pancreatic Neoplasms - metabolism Pancreatic Neoplasms - pathology Populations Rodents Smooth muscle STAT3 Transcription Factor - metabolism Stellate cells Stromal cells
Title	Distinct populations of inflammatory fibroblasts and myofibroblasts in pancreatic cancer
URI	https://www.ncbi.nlm.nih.gov/pubmed/28232471 https://www.proquest.com/docview/1983437325 https://www.proquest.com/docview/1872581353 https://www.proquest.com/docview/1877847643 https://pubmed.ncbi.nlm.nih.gov/PMC5339682 https://urn.kb.se/resolve?urn=urn:nbn:se:umu:diva-132073
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