CAF hierarchy driven by pancreatic cancer cell p53-status creates a pro-metastatic and chemoresistant environment via perlecan
Heterogeneous subtypes of cancer-associated fibroblasts (CAFs) coexist within pancreatic cancer tissues and can both promote and restrain disease progression. Here, we interrogate how cancer cells harboring distinct alterations in p53 manipulate CAFs. We reveal the existence of a p53-driven hierarch...
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| Vydáno v: | Nature communications Ročník 10; číslo 1; s. 3637 - 22 |
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| Hlavní autoři: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
| Vydáno: |
London
Nature Publishing Group UK
12.08.2019
Nature Publishing Group Nature Portfolio |
| Témata: | |
| ISSN: | 2041-1723, 2041-1723 |
| On-line přístup: | Získat plný text |
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| Abstract | Heterogeneous subtypes of cancer-associated fibroblasts (CAFs) coexist within pancreatic cancer tissues and can both promote and restrain disease progression. Here, we interrogate how cancer cells harboring distinct alterations in p53 manipulate CAFs. We reveal the existence of a p53-driven hierarchy, where cancer cells with a gain-of-function (GOF) mutant p53 educate a dominant population of CAFs that establish a pro-metastatic environment for GOF and null p53 cancer cells alike. We also demonstrate that CAFs educated by null p53 cancer cells may be reprogrammed by either GOF mutant p53 cells or their CAFs. We identify perlecan as a key component of this pro-metastatic environment. Using intravital imaging, we observe that these dominant CAFs delay cancer cell response to chemotherapy. Lastly, we reveal that depleting perlecan in the stroma combined with chemotherapy prolongs mouse survival, supporting it as a potential target for anti-stromal therapies in pancreatic cancer.
Subtypes of cancer associated fibroblasts can both promote and suppress tumorigenesis. Here, the authors investigate how p53 status in pancreatic cancer cells affects their interaction with cancer associated fibroblasts, and report perlecan as a mediator of the pro-metastatic environment. |
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| AbstractList | Heterogeneous subtypes of cancer-associated fibroblasts (CAFs) coexist within pancreatic cancer tissues and can both promote and restrain disease progression. Here, we interrogate how cancer cells harboring distinct alterations in p53 manipulate CAFs. We reveal the existence of a p53-driven hierarchy, where cancer cells with a gain-of-function (GOF) mutant p53 educate a dominant population of CAFs that establish a pro-metastatic environment for GOF and null p53 cancer cells alike. We also demonstrate that CAFs educated by null p53 cancer cells may be reprogrammed by either GOF mutant p53 cells or their CAFs. We identify perlecan as a key component of this pro-metastatic environment. Using intravital imaging, we observe that these dominant CAFs delay cancer cell response to chemotherapy. Lastly, we reveal that depleting perlecan in the stroma combined with chemotherapy prolongs mouse survival, supporting it as a potential target for anti-stromal therapies in pancreatic cancer. Heterogeneous subtypes of cancer-associated fibroblasts (CAFs) coexist within pancreatic cancer tissues and can both promote and restrain disease progression. Here, we interrogate how cancer cells harboring distinct alterations in p53 manipulate CAFs. We reveal the existence of a p53-driven hierarchy, where cancer cells with a gain-of-function (GOF) mutant p53 educate a dominant population of CAFs that establish a pro-metastatic environment for GOF and null p53 cancer cells alike. We also demonstrate that CAFs educated by null p53 cancer cells may be reprogrammed by either GOF mutant p53 cells or their CAFs. We identify perlecan as a key component of this pro-metastatic environment. Using intravital imaging, we observe that these dominant CAFs delay cancer cell response to chemotherapy. Lastly, we reveal that depleting perlecan in the stroma combined with chemotherapy prolongs mouse survival, supporting it as a potential target for anti-stromal therapies in pancreatic cancer. Subtypes of cancer associated fibroblasts can both promote and suppress tumorigenesis. Here, the authors investigate how p53 status in pancreatic cancer cells affects their interaction with cancer associated fibroblasts, and report perlecan as a mediator of the pro-metastatic environment. Subtypes of cancer associated fibroblasts can both promote and suppress tumorigenesis. Here, the authors investigate how p53 status in pancreatic cancer cells affects their interaction with cancer associated fibroblasts, and report perlecan as a mediator of the pro-metastatic environment. Heterogeneous subtypes of cancer-associated fibroblasts (CAFs) coexist within pancreatic cancer tissues and can both promote and restrain disease progression. Here, we interrogate how cancer cells harboring distinct alterations in p53 manipulate CAFs. We reveal the existence of a p53-driven hierarchy, where cancer cells with a gain-of-function (GOF) mutant p53 educate a dominant population of CAFs that establish a pro-metastatic environment for GOF and null p53 cancer cells alike. We also demonstrate that CAFs educated by null p53 cancer cells may be reprogrammed by either GOF mutant p53 cells or their CAFs. We identify perlecan as a key component of this pro-metastatic environment. Using intravital imaging, we observe that these dominant CAFs delay cancer cell response to chemotherapy. Lastly, we reveal that depleting perlecan in the stroma combined with chemotherapy prolongs mouse survival, supporting it as a potential target for anti-stromal therapies in pancreatic cancer.Heterogeneous subtypes of cancer-associated fibroblasts (CAFs) coexist within pancreatic cancer tissues and can both promote and restrain disease progression. Here, we interrogate how cancer cells harboring distinct alterations in p53 manipulate CAFs. We reveal the existence of a p53-driven hierarchy, where cancer cells with a gain-of-function (GOF) mutant p53 educate a dominant population of CAFs that establish a pro-metastatic environment for GOF and null p53 cancer cells alike. We also demonstrate that CAFs educated by null p53 cancer cells may be reprogrammed by either GOF mutant p53 cells or their CAFs. We identify perlecan as a key component of this pro-metastatic environment. Using intravital imaging, we observe that these dominant CAFs delay cancer cell response to chemotherapy. Lastly, we reveal that depleting perlecan in the stroma combined with chemotherapy prolongs mouse survival, supporting it as a potential target for anti-stromal therapies in pancreatic cancer. Heterogeneous subtypes of cancer-associated fibroblasts (CAFs) coexist within pancreatic cancer tissues and can both promote and restrain disease progression. Here, we interrogate how cancer cells harboring distinct alterations in p53 manipulate CAFs. We reveal the existence of a p53-driven hierarchy, where cancer cells with a gain-of-function (GOF) mutant p53 educate a dominant population of CAFs that establish a pro-metastatic environment for GOF and null p53 cancer cells alike. We also demonstrate that CAFs educated by null p53 cancer cells may be reprogrammed by either GOF mutant p53 cells or their CAFs. We identify perlecan as a key component of this pro-metastatic environment. Using intravital imaging, we observe that these dominant CAFs delay cancer cell response to chemotherapy. Lastly, we reveal that depleting perlecan in the stroma combined with chemotherapy prolongs mouse survival, supporting it as a potential target for anti-stromal therapies in pancreatic cancer. Subtypes of cancer associated fibroblasts can both promote and suppress tumorigenesis. Here, the authors investigate how p53 status in pancreatic cancer cells affects their interaction with cancer associated fibroblasts, and report perlecan as a mediator of the pro-metastatic environment. |
| ArticleNumber | 3637 |
| Author | Nobis, Max Zaratzian, Anaiis Da Silva, Andrew Wang, Yingxiao Kalna, Gabriella Roden, Daniel Mathivanan, Suresh Rouet, Romain Warren, Sean C. Grey, Shane T. Vennin, Claire Lucas, Morghan C. Mélénec, Pauline Samuel, Monisha Pajic, Marina Cox, Thomas R. Benda, Ales Elgundi, Zehra Pinese, Mark Leung, Wilfred Reed, Daniel A. Timpson, Paul Murphy, Kendelle J. Morton, Jennifer P. Braithwaite, Anthony W. Herrmann, David Christ, Daniel Croucher, David R. Sansom, Owen J. Cazet, Aurélie S. Phillips, Phoebe A. Gill, Anthony J. Parker, Benjamin L. Whitelock, John M. Parkin, Ashleigh |
| Author_xml | – sequence: 1 givenname: Claire surname: Vennin fullname: Vennin, Claire organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney, Molecular Pathology department, the Netherlands Cancer Institute – sequence: 2 givenname: Pauline surname: Mélénec fullname: Mélénec, Pauline organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney – sequence: 3 givenname: Romain orcidid: 0000-0003-4210-9613 surname: Rouet fullname: Rouet, Romain organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney – sequence: 4 givenname: Max surname: Nobis fullname: Nobis, Max organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney – sequence: 5 givenname: Aurélie S. orcidid: 0000-0001-7075-8448 surname: Cazet fullname: Cazet, Aurélie S. organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney – sequence: 6 givenname: Kendelle J. surname: Murphy fullname: Murphy, Kendelle J. organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney – sequence: 7 givenname: David orcidid: 0000-0002-9514-7501 surname: Herrmann fullname: Herrmann, David organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney – sequence: 8 givenname: Daniel A. orcidid: 0000-0002-3736-7725 surname: Reed fullname: Reed, Daniel A. organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney – sequence: 9 givenname: Morghan C. surname: Lucas fullname: Lucas, Morghan C. organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney – sequence: 10 givenname: Sean C. orcidid: 0000-0002-5253-7147 surname: Warren fullname: Warren, Sean C. organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney – sequence: 11 givenname: Zehra surname: Elgundi fullname: Elgundi, Zehra organization: Graduate school of Biomedical Engineering, University of New South Wales Sydney – sequence: 12 givenname: Mark orcidid: 0000-0001-5078-6687 surname: Pinese fullname: Pinese, Mark organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney – sequence: 13 givenname: Gabriella surname: Kalna fullname: Kalna, Gabriella organization: Cancer Research UK Beatson Institute – sequence: 14 givenname: Daniel surname: Roden fullname: Roden, Daniel organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney – sequence: 15 givenname: Monisha surname: Samuel fullname: Samuel, Monisha organization: Department of Physiology, Anatomy and Microbiology, School of Life Sciences, La Trobe University – sequence: 16 givenname: Anaiis surname: Zaratzian fullname: Zaratzian, Anaiis organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre – sequence: 17 givenname: Shane T. orcidid: 0000-0003-2160-1625 surname: Grey fullname: Grey, Shane T. organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney – sequence: 18 givenname: Andrew surname: Da Silva fullname: Da Silva, Andrew organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre – sequence: 19 givenname: Wilfred surname: Leung fullname: Leung, Wilfred organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney, Department of Biomedical Sciences, College of Veterinary Medicine, Cornell University – sequence: 21 givenname: Suresh surname: Mathivanan fullname: Mathivanan, Suresh organization: Department of Physiology, Anatomy and Microbiology, School of Life Sciences, La Trobe University – sequence: 22 givenname: Yingxiao orcidid: 0000-0003-0265-326X surname: Wang fullname: Wang, Yingxiao organization: Department of Bioengineering, Institute of Engineering in Medicine, University of California – sequence: 23 givenname: Anthony W. surname: Braithwaite fullname: Braithwaite, Anthony W. organization: Children’s Medical Research Institute, University of Sydney, Department of Pathology, Dunedin School of Medicine, University of Otago, Maurice Wilkins Centre, University of Otago – sequence: 24 givenname: Daniel orcidid: 0000-0002-7313-3977 surname: Christ fullname: Christ, Daniel organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney – sequence: 25 givenname: Ales surname: Benda fullname: Benda, Ales organization: Biomedical imaging facility, Lowy Cancer Research Centre, University of New South Wales – sequence: 26 givenname: Ashleigh surname: Parkin fullname: Parkin, Ashleigh organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney – sequence: 27 givenname: Phoebe A. surname: Phillips fullname: Phillips, Phoebe A. organization: Pancreatic Cancer Translational Research Group, Lowy Cancer Research Centre, School of Medical Sciences, University of New South Wales, Australian Centre for Nanomedicine, University of New South Wales – sequence: 28 givenname: John M. surname: Whitelock fullname: Whitelock, John M. organization: Graduate school of Biomedical Engineering, University of New South Wales Sydney – sequence: 29 givenname: Anthony J. surname: Gill fullname: Gill, Anthony J. organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, Sydney Medical School, University of Sydney, NSW Health Pathology, Department of Anatomical Pathology, Royal North Shore Hospital, St Leonards, Cancer Diagnosis and Pathology Research Group, Kolling Institute of Medical Research – sequence: 30 givenname: Owen J. orcidid: 0000-0001-9540-3010 surname: Sansom fullname: Sansom, Owen J. organization: Cancer Research UK Beatson Institute – sequence: 31 givenname: David R. surname: Croucher fullname: Croucher, David R. organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney – sequence: 32 givenname: Benjamin L. surname: Parker fullname: Parker, Benjamin L. organization: Schools of Life and Environmental Sciences, the Charles Perkin Centre, the University of Sydney – sequence: 33 givenname: Marina surname: Pajic fullname: Pajic, Marina organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney – sequence: 34 givenname: Jennifer P. orcidid: 0000-0001-5766-9141 surname: Morton fullname: Morton, Jennifer P. organization: Cancer Research UK Beatson Institute – sequence: 35 givenname: Thomas R. orcidid: 0000-0001-9294-1745 surname: Cox fullname: Cox, Thomas R. email: t.cox@garvan.org.au organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney – sequence: 36 givenname: Paul surname: Timpson fullname: Timpson, Paul email: p.timpson@garvan.org.au organization: The Garvan Institute of Medical Research & The Kinghorn Cancer Centre, St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales Sydney |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31406163$$D View this record in MEDLINE/PubMed |
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| Contributor | Leonard, Conrad Kazakoff, Stephen Christ, Angelika Holmes, Oliver Beilin, Maria Papangelis, Virginia Chambers, Cecilia R Epari, Krishna P Bassi, Claudio Fletcher, David R Chou, Angela Pavlakis, Nick Arshi, Mehreen Nguyen, Nan Q Grimmond, Sean M Nones, Katia Mukhedkar, Sanjay Eshleman, James R O'Connnor, Chelsie Worthley, Chris Biankin, Andrew V Samra, Jaswinder S Barbour, Andrew P O'Rourke, Thomas J Kench, James G Dwarte, Tanya Merrett, Neil D Nikfarjam, Mehrdad Brooke-Smith, Mark E Lam, Vincent W Andrews, Lesley Kirk, Judy Pearson, John V Ritchie, Shona Hofmann, Oliver McLeod, Duncan Bruxner, Tim Sandroussi, Charbel Asghari, Ray Hodgkinson, Peter Zeps, Nikolajs Chen, John Ballal, Mo Fawcett, Jonathan W Das, Amitabha Jamieson, Nigel B Tucker, Katherine High, Hilda A Dixon, Judith Mead, R Scott Clouston, Andrew D Chang, David K Johns, Amber L Hruban, Ralph H Beghelli, Stefania Waddell, Nicola Texler, Michael Ismail, Kasim Pereira, Brooke Addala, Venkateswar Scardoni, Maria Froio, Danielle Ruszkiewicz, Andrew R Forest, Cindy Slater, Kellee Spigellman, |
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| Snippet | Heterogeneous subtypes of cancer-associated fibroblasts (CAFs) coexist within pancreatic cancer tissues and can both promote and restrain disease progression.... Subtypes of cancer associated fibroblasts can both promote and suppress tumorigenesis. Here, the authors investigate how p53 status in pancreatic cancer cells... |
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| SubjectTerms | 13 13/106 14/3 14/33 14/5 14/69 38/61 59/5 631/67 631/67/327 631/80 64/60 82/58 Animals Cancer Cancer-Associated Fibroblasts - pathology Cell Line, Tumor Cell Movement Cell Proliferation Chemotherapy Drug Resistance, Neoplasm - genetics Fibroblasts Gene Expression Regulation, Neoplastic - genetics Heparan Sulfate Proteoglycans - metabolism Humanities and Social Sciences Metastases Metastasis Mice Mice, Inbred BALB C multidisciplinary Neoplasm Invasiveness - pathology p53 Protein Pancreas - pathology Pancreatic cancer Pancreatic Neoplasms - genetics Pancreatic Neoplasms - pathology Perlecan Science Science (multidisciplinary) Signal Transduction - physiology Stroma Tumor Suppressor Protein p53 - genetics Tumor Suppressor Protein p53 - metabolism |
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| Title | CAF hierarchy driven by pancreatic cancer cell p53-status creates a pro-metastatic and chemoresistant environment via perlecan |
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