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A subset of myofibroblastic cancer-associated fibroblasts regulate collagen fiber elongation, which is prognostic in multiple cancers

A subset of myofibroblastic cancer-associated fibroblasts regulate collagen fiber elongation, which is prognostic in multiple cancers
A subset of myofibroblastic cancer-associated fibroblasts regulate collagen fiber elongation, which is prognostic in multiple cancers
Collagen structure has been shown to influence tumor cell invasion, metastasis and clinical outcome in breast cancer. However, it remains unclear how it affects other solid cancers. Here we utilized multi-photon laser scanning microscopy and Second Harmonic Generation to identify alterations to collagen fiber structure within the tumor stroma of head & neck, esophageal and colorectal cancers. Image segmentation algorithms were then applied to quantitatively characterize these morphological changes, showing that elongated collagen fibers significantly correlated with poor clinical outcome (Log Rank p < 0.05). We used TGF-? treatment to model fibroblast conversion to smooth muscle actin SMA-positive cancer associated fibroblasts (CAFs) and found that these cells induce the formation of elongated collagen fibers in vivo. However, proteomic/transcriptomic analysis of SMA-positive CAFs cultured ex-vivo showed significant heterogeneity in the expression of genes with collagen fibril organizing gene ontology. Notably, stratifying patients according to stromal SMA-positivity and collagen fiber elongation was found to provide a highly significant correlation with poor survival in all 3 cancer types (Log Rank p ? 0.003). In summary, we show that increased collagen fiber length correlates with poor patient survival in multiple tumor types and that only a sub-set of SMA-positive CAFs can mediate the formation of this collagen structure.
1949-2553
6159-6174
Hanley, Christopher J.
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Noble, Fergus
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Ward, Matthew
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Bullock, Marc
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Drifka, Cole
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Mellone, Massimiliano
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Manousopoulou, Antigoni
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Johnston, Harvey E.
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Hayden, Annette
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Thirdborough, Stephen
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Liu, Yuming
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Smith, David M.
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Mellows, Toby
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Kao, W. John
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Garbis, Spiros D.
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Mirnezami, Alexander
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Underwood, Tim J.
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Eliceiri, Kevin W
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Thomas, Gareth J.
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Hanley, Christopher J.
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Noble, Fergus
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Ward, Matthew
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Bullock, Marc
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Drifka, Cole
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Mellone, Massimiliano
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Manousopoulou, Antigoni
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Johnston, Harvey E.
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Hayden, Annette
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Thirdborough, Stephen
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Liu, Yuming
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Smith, David M.
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Mellows, Toby
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Kao, W. John
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Garbis, Spiros D.
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Mirnezami, Alexander
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Underwood, Tim J.
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Eliceiri, Kevin W
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Thomas, Gareth J.
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Hanley, Christopher J., Noble, Fergus, Ward, Matthew, Bullock, Marc, Drifka, Cole, Mellone, Massimiliano, Manousopoulou, Antigoni, Johnston, Harvey E., Hayden, Annette, Thirdborough, Stephen, Liu, Yuming, Smith, David M., Mellows, Toby, Kao, W. John, Garbis, Spiros D., Mirnezami, Alexander, Underwood, Tim J., Eliceiri, Kevin W and Thomas, Gareth J. (2016) A subset of myofibroblastic cancer-associated fibroblasts regulate collagen fiber elongation, which is prognostic in multiple cancers. Oncotarget, 7 (5), 6159-6174. (doi:10.18632/oncotarget.6740). (PMID:26716418)

Record type: Article

Abstract

Collagen structure has been shown to influence tumor cell invasion, metastasis and clinical outcome in breast cancer. However, it remains unclear how it affects other solid cancers. Here we utilized multi-photon laser scanning microscopy and Second Harmonic Generation to identify alterations to collagen fiber structure within the tumor stroma of head & neck, esophageal and colorectal cancers. Image segmentation algorithms were then applied to quantitatively characterize these morphological changes, showing that elongated collagen fibers significantly correlated with poor clinical outcome (Log Rank p < 0.05). We used TGF-? treatment to model fibroblast conversion to smooth muscle actin SMA-positive cancer associated fibroblasts (CAFs) and found that these cells induce the formation of elongated collagen fibers in vivo. However, proteomic/transcriptomic analysis of SMA-positive CAFs cultured ex-vivo showed significant heterogeneity in the expression of genes with collagen fibril organizing gene ontology. Notably, stratifying patients according to stromal SMA-positivity and collagen fiber elongation was found to provide a highly significant correlation with poor survival in all 3 cancer types (Log Rank p ? 0.003). In summary, we show that increased collagen fiber length correlates with poor patient survival in multiple tumor types and that only a sub-set of SMA-positive CAFs can mediate the formation of this collagen structure.

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Accepted/In Press date: 5 December 2015
e-pub ahead of print date: 23 December 2015
Published date: 2 February 2016
Organisations: Cancer Sciences

Identifiers

Local EPrints ID: 393539
URI: http://eprints.soton.ac.uk/id/eprint/393539
ISSN: 1949-2553
PURE UUID: 6d1fbfc4-4912-4e5d-a567-1043a631b510
ORCID for Christopher J. Hanley: ORCID iD orcid.org/0000-0003-3816-7220
ORCID for Massimiliano Mellone: ORCID iD orcid.org/0000-0002-4964-9340
ORCID for Spiros D. Garbis: ORCID iD orcid.org/0000-0002-1050-0805
ORCID for Tim J. Underwood: ORCID iD orcid.org/0000-0001-9455-2188

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Date deposited: 28 Apr 2016 13:34
Last modified: 15 Mar 2024 03:51

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Contributors

Author: Fergus Noble
Author: Matthew Ward
Author: Marc Bullock
Author: Cole Drifka
Author: Massimiliano Mellone ORCID iD
Author: Antigoni Manousopoulou
Author: Harvey E. Johnston
Author: Annette Hayden
Author: Yuming Liu
Author: David M. Smith
Author: Toby Mellows
Author: W. John Kao
Author: Spiros D. Garbis ORCID iD
Author: Kevin W Eliceiri

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