Collagen architecture in triple negative breast cancer.

This study evaluated collagen properties in TNBC samples collected from different racial groups to determine the presence of variance in matrix architecture. African American (AA) breast cancer patients have a significantly higher mortality rate and nearly a three-fold increased prevalence of triple...

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Main Authors: Zoë Dinkel, Adam Baker, Alannah Akins, Kylie L King, Matthew Harrington, Deborah Kunkel, Zhi Gao, Tong Ye, Heather Dunn
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0324655
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author Zoë Dinkel
Adam Baker
Alannah Akins
Kylie L King
Matthew Harrington
Deborah Kunkel
Zhi Gao
Tong Ye
Heather Dunn
author_facet Zoë Dinkel
Adam Baker
Alannah Akins
Kylie L King
Matthew Harrington
Deborah Kunkel
Zhi Gao
Tong Ye
Heather Dunn
author_sort Zoë Dinkel
collection DOAJ
description This study evaluated collagen properties in TNBC samples collected from different racial groups to determine the presence of variance in matrix architecture. African American (AA) breast cancer patients have a significantly higher mortality rate and nearly a three-fold increased prevalence of triple negative breast cancer (TNBC) when compared to Caucasian (C) patients. The extracellular matrix region surrounding tumors contains abundant collagen fibers, and these fibers undergo remodeling throughout cancer progression, promote metastasis, and impede treatment response. High mammographic density, commonly known as dense breast tissue, is hypothesized to be more prevalent in AA women and characterized by increased collagen deposition and associated with more aggressive cancers. The aim of this research was to investigate fibrillar collagen architecture in TNBC samples from AA and C patients using two-photon microscopy with second harmonic generation (SHG), an intrinsic optical signal produced by fibrillar collagen. Twenty tissue regions per tumor sample were randomly selected for SHG microscopy, and image processing was conducted using the Fiji macro TWOMBLI to quantify mesoscopic fibrillar morphological properties and nanoscopic fibrillar properties with the Forward-Backward SHG ratio. Compared to the images from C tumor samples, those from AA samples exhibited a significant increase in parameters including fiber area, total length, and number of endpoints and branchpoints, but had decreased lacunarity. Collagen microstructure, including fibril arrangement and packing density, did not significantly differ between the groups. These results illustrate that the TNBC samples analyzed from AA patients may have macrostructural collagen characteristics associated with aggressive phenotype tumor formation.
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spelling doaj-art-7b25ac772b984e80b07fe04f3eb92a982025-08-20T02:26:11ZengPublic Library of Science (PLoS)PLoS ONE1932-62032025-01-01205e032465510.1371/journal.pone.0324655Collagen architecture in triple negative breast cancer.Zoë DinkelAdam BakerAlannah AkinsKylie L KingMatthew HarringtonDeborah KunkelZhi GaoTong YeHeather DunnThis study evaluated collagen properties in TNBC samples collected from different racial groups to determine the presence of variance in matrix architecture. African American (AA) breast cancer patients have a significantly higher mortality rate and nearly a three-fold increased prevalence of triple negative breast cancer (TNBC) when compared to Caucasian (C) patients. The extracellular matrix region surrounding tumors contains abundant collagen fibers, and these fibers undergo remodeling throughout cancer progression, promote metastasis, and impede treatment response. High mammographic density, commonly known as dense breast tissue, is hypothesized to be more prevalent in AA women and characterized by increased collagen deposition and associated with more aggressive cancers. The aim of this research was to investigate fibrillar collagen architecture in TNBC samples from AA and C patients using two-photon microscopy with second harmonic generation (SHG), an intrinsic optical signal produced by fibrillar collagen. Twenty tissue regions per tumor sample were randomly selected for SHG microscopy, and image processing was conducted using the Fiji macro TWOMBLI to quantify mesoscopic fibrillar morphological properties and nanoscopic fibrillar properties with the Forward-Backward SHG ratio. Compared to the images from C tumor samples, those from AA samples exhibited a significant increase in parameters including fiber area, total length, and number of endpoints and branchpoints, but had decreased lacunarity. Collagen microstructure, including fibril arrangement and packing density, did not significantly differ between the groups. These results illustrate that the TNBC samples analyzed from AA patients may have macrostructural collagen characteristics associated with aggressive phenotype tumor formation.https://doi.org/10.1371/journal.pone.0324655
spellingShingle Zoë Dinkel
Adam Baker
Alannah Akins
Kylie L King
Matthew Harrington
Deborah Kunkel
Zhi Gao
Tong Ye
Heather Dunn
Collagen architecture in triple negative breast cancer.
PLoS ONE
title Collagen architecture in triple negative breast cancer.
title_full Collagen architecture in triple negative breast cancer.
title_fullStr Collagen architecture in triple negative breast cancer.
title_full_unstemmed Collagen architecture in triple negative breast cancer.
title_short Collagen architecture in triple negative breast cancer.
title_sort collagen architecture in triple negative breast cancer
url https://doi.org/10.1371/journal.pone.0324655
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AT matthewharrington collagenarchitectureintriplenegativebreastcancer
AT deborahkunkel collagenarchitectureintriplenegativebreastcancer
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